24
CABI WORKING PAPER
The Asian Citrus Greening
Disease (Huanglongbing):
Evidence Note on Invasiveness and
Potential Economic Impacts for East Africa
June 2021
Authors
Djamila Djeddour
Corin Pratt
Kate Constantine
Ivan Rwomushana
Roger Day
KNOWLEDGE FOR LIFE
The copyright holder of this work is CAB International (trading as CABI). It is made available under a
Creative Commons Attribution-Non-commercial Licence (CC BY-NC). For further details please refer to
http://creativecommons.org/license.
This paper was prepared as part of the Action on Invasives and Plantwise Plus programmes. Action on
Invasives is supported by the UK Foreign, Commonwealth and Development Office (FCDO) and the
Netherlands Directorate General for International Cooperation (DGIS). Plantwise Plus, in addition to
FCDO and DGIS, is also funded by European Commission Directorate-General for International
Cooperation and Development (DEVCO) and Swiss Agency for Development and Cooperation (SDC).
We thank the survey respondents, including those whose partial responses have been quoted with
their permission.
CABI is an international intergovernmental organization, and we gratefully acknowledge the core
financial support from our member countries (and lead agencies) including the United Kingdom
(Foreign, Commonwealth and Development Office), China (Chinese Ministry of Agriculture and Rural
Affairs), Australia (Australian Centre for International Agricultural Research), Canada (Agriculture and
Agri-Food Canada), the Netherlands (Directorate-General for International Cooperation) and
Switzerland (Swiss Agency for Development and Cooperation). See http://www.cabi.org/aboutcabi/who-we-work-with/key-donors/ for full details.
This CABI Working Paper was internally peer-reviewed. It may be referred to as:
Djeddour, D., Pratt, C., Constantine, K., Rwomushana, I. and Day, R. (2021) The Asian citrus greening
disease (huanglongbing): Evidence note on invasiveness and potential economic impacts for East
Africa. CABI Working Paper 24, 94 pp. DOI: https://dx.doi.org/10.1079/CABICOMM-62-8158
Djamila Djeddour, CABI UK, Bakeham Lane, Egham, Surrey, TW20 9TY.
Email: d.djeddour@cabi.org; ORCID: https://orcid.org/0000-0002-1421-4101
Corin Pratt, CABI UK, Bakeham Lane, Egham, Surrey, TW20 9TY.
Email: c.pratt@cabi.org; ORCID: https://orcid.org/0000-0001-8070-7302
Kate Constantine, CABI UK, Bakeham Lane, Egham, Surrey, TW20 9TY.
Email: k.constantine@cabi.org; ORCID: https://orcid.org/0000-0001-9053-3537
Ivan Rwomushana, CABI, Canary Bird, 673 Limuru Road, Muthaiga, PO Box 633-00621,
Nairobi, Kenya.
Email: I.Rwomushana@cabi.org; ORCID: https://orcid.org/0000-0001-5840-8058
Roger Day, CABI, Canary Bird, 673 Limuru Road, Muthaiga, PO Box 633-00621, Nairobi, Kenya.
Email: r.day@cabi.org; ORCID: https://orcid.org/0000-0002-4854-7609
Cover photo: Citrus tree with severe dieback, a typical symptom of citrus greening disease, Kwale
County, Kenya. Credit: Ivan Rwomushana, CABI.
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Table of contents
Table of contents .................................................................................................................................... 3
Abstract ................................................................................................................................................... 4
Executive summary ................................................................................................................................. 5
Acronyms .............................................................................................................................................. 10
Introduction .......................................................................................................................................... 11
1 Citrus production and the citrus greening problem .......................................................................... 11
1.1 Commodity context .................................................................................................................... 11
1.2 History of citrus production and trends in East Africa ................................................................ 13
1.3 Understanding African and Asian citrus greening and their vectors .......................................... 16
1.4 Differentiating symptoms of African and Asian greening in East Africa ..................................... 19
1.5 Huanglongbing symptoms and crop damage ............................................................................. 20
1.6 Current spread and distribution of HLB in Africa ........................................................................ 23
1.7 Modelling environmental suitability and potential distribution of HLB and its vector .............. 24
2 Impacts of HLB on citrus and other socio-economic variables .......................................................... 28
2.1 Documented impacts of Huanglongbing in other regions .......................................................... 28
2.2 Documented impacts of Huanglongbing in East Africa .............................................................. 30
2.3 Potential yield loss to Huanglongbing in East Africa................................................................... 31
2.4 Estimates of economic loss due to Huanglongbing in East Africa .............................................. 33
2.5 Huanglongbing and trade ........................................................................................................... 38
3 Huanglongbing management............................................................................................................. 40
3.1 Chemical control ......................................................................................................................... 42
3.2 Antimicrobial control .................................................................................................................. 44
3.3 Botanicals and organic management.......................................................................................... 45
3.4 Resistant varieties ....................................................................................................................... 47
3.5 Biological control ........................................................................................................................ 48
3.6 Good Agricultural Practice .......................................................................................................... 51
3.7 IPM .............................................................................................................................................. 53
4 Advice, information and communication .......................................................................................... 66
4.1 Sources of information on HLB control....................................................................................... 66
4.2 Criteria for control advice ........................................................................................................... 66
4.3 Information resources and tools................................................................................................. 67
5 Recommendations ............................................................................................................................. 67
Acknowledgements............................................................................................................................... 69
References ............................................................................................................................................ 70
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Abstract
Huanglongbing (HLB), also known as citrus greening disease, is one of the most devastating pathogens
of citrus worldwide and is caused by closely-related species of systemic Candidatus bacteria. Vectored
by the Asian citrus psyllid (ACP), Diaphorina citri, the heat-tolerant, Asian form of the disease,
Candidatus Liberibacter asiaticus (CLas) is the most serious and widespread. In East Africa, the heatsensitive form of the disease is vectored by the African citrus triozid (ACT) Trioza erytreae and remains
the most prevalent disease, particularly in the cooler, mid to high altitude areas. Since 2010 however,
CLas which can also be transmitted by T. erytreae, has been spreading in the African continent and
significantly, the Asian HLB vector has also been detected in Tanzania and Kenya. There is now a clear
and present threat of HLB to the citrus industry in Africa, including the previously sustainable warmer
citrus producing regions of East Africa. Modelling of environmental suitability suggests that without
preventative measures CLas could establish widely in Africa, with potential hotspots in Central and
South-eastern Africa, incurring substantial economic losses. The following evidence note reviews the
global literature on the HLB pathogen-vector complex, highlighting potential risks and estimating
economic impact for Africa. A synthesis of recommendations for biosecurity preparedness,
surveillance and management options is outlined to inform decision makers and growers.
4
Executive summary
Background
Asian citrus greening disease or huanglongbing (HLB), caused by the bacterium Candidatus
Liberibacter asiaticus (CLas), is a devastating disease of citrus trees which has spread globally via trade
from its origins in Asia, posing a huge threat and economic burden to nearly all citrus producing regions
of the world. Global interventions to prevent the spread of HLB and reduce its impact have been, for
the most part, ineffective. The primary vector for this disease, Diaphorina citri (Asian citrus psyllid, or
ACP) is present in East Africa and the recent detection of HLB in Kenya and Tanzania brings into sharp
focus the need for coordinated action to contain and/or eradicate the disease before it spreads and
becomes ubiquitous in the region. This evidence note therefore provides information on the key facts
about HLB, including the losses currently experienced and estimations of potential further losses if
HLB continues to spread and becomes endemic throughout citrus-growing regions of Africa. A
summary of the research and development on control measures is provided, as well as a synthesis of
recommendations for management of HLB and its vectors. This information will be useful for a wide
range of stakeholders, including researchers, policy makers, donors and other high-level decision
makers.
Strategic importance of citrus
From an economic point of view, citrus fruits rank first in terms of world fruit production and
international trade value. The world production of citrus for 2018 was estimated at 139 million tonnes
(cultivated in over 140 countries around the world), the major producers being China, Brazil, the USA
and countries bordering the Mediterranean. Average citrus production for all of Eastern Africa was 1.2
million tonnes in 2018. Citrus is an important domestic crop throughout East Africa, where production
is mainly by smallholders. The yields of smallholder farmers in East Africa often do not exceed 4–10
t/ha, while the crop has the potential of producing up to 50–70 t/ha in countries practicing integrated
pest management (IPM). In East Africa, Tanzania has overtaken Kenya as the largest citrus producer
after Kenya was severely impacted by the African form of the greening disease (African citrus greening
disease, AfCGD) transmitted by the African citrus psyllid (ACT).
Understanding African and Asian citrus greening (Huanglongbing) and their vectors
Citrus greening disease is associated with three Gram-negative bacteria: Candidatus Liberibacter
asiaticus (CLas), Candidatus Liberibacter africanus (CLaf), and Candidatus Liberibacter americanus
(CLam). The liberibacters are native to particular geographical zones but in modern times have spread,
along with their psyllid vectors, to new areas in association with the development and extension of
susceptible crops. CLas, vectored by the temperature tolerant Asian citrus psyllid, D. citri, is associated
with Asian HLB and both it and its vector are the most prevalent and devastating pathosystem, having
spread worldwide from China. The African form CLaf, which shows symptoms under somewhat moist
and cool conditions and at higher elevations, is transmitted by the African citrus psyllid, Trioza erytreae
and causes AfCGD. Whilst it is considered less debilitating than CLas-associated HLB, it is a widespread
and persistent problem in Africa, where a number of new lineages of the species have been reported.
Huanglongbing symptoms and crop damage
The HLB bacteria can infect most citrus cultivars, species, and hybrids, as well as some citrus relatives.
The first symptom of HLB is usually the appearance of a yellow flush of growth on an infected tree,
5
hence the name “huanglongbing” which translates from the Chinese as “yellow dragon” or “yellow
shoot disease”. Progressive yellowing and thinning of the entire canopy follows, leaves turn
paleyellow and display characteristic blotchy mottling or vein yellowing, point upwards and are
reduced in size. In the early stages of infection, diagnosis can be difficult as trees remain symptomless,
however chronically infected trees become sparsely foliated and show extensive twig dieback and
eventually, premature death, which can occur several months to years after infection. The fruits,
which are abnormally bitter in taste, are often small, lopsided with aborted dark seeds, and remain
green in part (hence the origin of the name greening) and drop prematurely reducing yields. Severe
symptoms in trees have been observed one to five years after onset of the first symptoms, depending
on the age of the tree at the time of infection, but also on the number of infections per tree, which
are often multiple. The disease’s rapid progress, combined with the impact on yield and quality of
fruits means that affected orchards can lose their economic viability within seven to ten years of
planting.
Current spread and distribution of Huanglongbing in East Africa
Huanglongbing was first detected in Ethiopia in 2010 and continues to spread within the country
including to regions distant from the first detections and at high altitudes. Assays of T. erytreae (ACT)
collected in the field have confirmed infection with CLas raising the prospect of HLB proliferation aided
by a novel additional vector. Recent reports have now also confirmed the presence of the primary HLB
vector, D. citri in Ethiopia including at relatively high altitudes, with imminent spread predicted. D. citri
has also been reported from sites across the south of Kenya to the coast and in the north-east of
Tanzania, an important citrus-producing region, with spread ongoing. The recent discovery of CLas in
the coastal region of Kenya close to the border with Tanzania, particularly in the presence of its
increasingly widespread primary vector is understandably a cause of great concern for citrus
producers in the area. HLB and its vector are yet to be confirmed in Uganda, but it is clear that citrus
production across Eastern Africa is under severe threat from this destructive disease. The recent
arrival of D. citri in Nigeria, a major producer of citrus, raises the prospect of HLB proliferation in West
Africa, a region predicted to be highly suitable to the disease and its primary vector.
Economic impacts of Huanglongbing in East Africa
The yield losses to Asian citrus greening, once widely established, can be expected to be significant
and a potential threat to ongoing citrus production for resource-poor growers. At this early stage of
invasion, however, production losses in citrus due to HLB in Eastern Africa are likely to be limited and
have received minimal analysis in the literature. As infected plants age and symptoms are increasingly
expressed, and the disease spreads via its vector(s) to infect citrus more extensively across the region,
as is probable, the losses to citriculture could be very significant. Producers in hotter lowland areas
who are currently spared losses to the less heat-tolerant African citrus greening disease could now
face major impacts from the more damaging and heat-tolerant Asian citrus greening. The majority of
citrus in the region is now at potential risk from one or both of these diseases. Extrapolating HLB
production losses equivalent to those reported for Florida, the estimated annual value of lost
production in four East African countries (Ethiopia, Kenya, Tanzania and Uganda) ranges from US$ 21.3
to 63.8 million within five to ten years. Over a longer timeframe (ten to fifteen years), estimated
annual production losses range from US$ 63.8 to 127.6 for these countries. Economic losses could be
greater still for major sub-Saharan African citrus producers such as Nigeria and South Africa should
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HLB arrive, underlining the pressing need for rigorous and practicable action plans for vulnerable
citrus-producing regions.
Huanglongbing and trade
HLB is primarily a vector-borne disease but the risk of local and regional spread is further increased by
movement of frequently traded plant products from infected areas. Trade of infected host citrus
material (budwood, grafted trees, rootstock seedlings) and alternative hosts such Murraya koenigii in
the Rutaceae family, are recognized pathways for HLB introduction and can also carry Asian citrus
psyllid eggs and/or nymphs over long distances. Increasing regional trade, reservoir host plants and
similar climatic patterns are likely to contribute to spread of the disease. The arrival of D. citri in
mainland Africa presents a serious threat to African citriculture since citrus production at all altitudes
would be at risk, potentially resulting in the industry becoming economically non-viable within a few
years. Due to the severity of HLB, EPPO recommends the prohibition of importation of citrus plants
for planting and cut branches or buds of citrus from areas or countries where HLB or either of its
vectors are present. Both T. erytreae and D. citri are recommended for regulation as quarantine pests
in the European Union, whereby exporting countries may be required to apply mandatory
phytosanitary procedures, which results in extra cost to exporters and the National Plant Protection
Organizations. At present, none of the bacteria associated with HLB have been found in the EPPO
region, although one of its vectors, T. erytreae, is present in Spain and Portugal. In South Africa, the
National Plant Protection Organization is developing an early warning system in collaboration with the
citrus industry as part of the South African Emergency Plant Pest Response Plan and has alerted the
agricultural community, importers, researchers and smallholders to the risks of HLB to the entire
continent.
Management of Huanglongbing
To date, there has been a decline in all commercial citrus industries that have faced this disease and
with adequate control still lacking, most of the citrus-producing countries remain under threat.
Disease management is complicated by long incubation periods and difficulties of diagnosis. The first
line of defence for HLB has always been quarantine measures to ensure the bacteria is prevented from
entry but once introduced, psyllid management is critical to slow establishment and spread, and this
invariably involves a persistent spray regime to maintain low vector populations. In the absence of
sustainable curative treatments or resistant citrus lines, countries not yet severely affected by HLB
have demonstrated some benefit by adopting rigorous and coordinated approaches to management.
The “3-pronged” preventive measures revolve around the use of disease-free nursery stock (produced
in insect-proof nurseries), area-wide suppression of the vector, D. citri, and eradication of
symptomatic trees to reduce or eliminate inoculum sources. However, these efforts are often
undermined by the ubiquitous presence of disease reservoirs from citrus trees across the region, in
commercial orchards and household gardens, as well as alternative hosts such as ornamental Murraya
species, where subtle symptoms may go undetected. Whilst the use of insecticides can form an
important and cost-effective component of HLB management, their application needs to be judicious
and well timed since overapplication of pesticides not only increases costs but also leads to resistance
development and has negative environmental and human health implications. Many alternatives to
chemical control such as thermotherapy, shoot-tip grafting, antibiotic treatment, nutritional sprays
and pruning have provided some short-term relief but proved impractical options long term.
Furthermore, these can even undermine the effectiveness of broader mitigation measures, by
7
allowing sources of inoculum to persist. Classical biocontrol using parasitoid wasps has been successful
in small, non-continental land masses but is unlikely to reduce CLas transmission sufficiently to
mitigate against HLB. Substantial research investments are made worldwide into HLB, its vector and
citrus breeding, and the advances of modern biology and chemistry provide some hope that new
research directions may offer ways to combat this devastating disease.
Huanglongbing advice and information
HuangIongbing is still a new disease in Kenya, and consequently not much information is being
disseminated on the proper identification of the disease and how to differentiate it from African citrus
greening disease, as well as its vector. ICIPE has recently completed a project on citrus pests and
diseases and one of the next steps suggested was to compile and document all the available
information on the efficacy of different management options of HLB and its vector, learning from
experiences in the USA, China and South Africa. Consequently, awareness-raising among the farming
communities, extension and quarantine personnel is required. This could be through mass media, ICT,
training and communication materials in local languages, amongst other methods. In terms of control,
HLB does not lend itself to many of the common methods employed for most pests as the disease is
often detected late when the citrus tree starts showing symptoms. Therefore, any recommendations
communicated to the farmer would need to be efficacious, safe, sustainable, practical, available and
affordable.
Recommendations
The following key recommendations are provided for the sustainable management of HLB in Africa.
High-level policy makers:
•
Recognise the magnitude of the HLB threat (present and potential) and make policy decisions,
backed by available economic estimates and science-based evidence
•
Lobby for budgetary allocation to facilitate an immediate, official national response backed
by policy and legislation to enable coordinated (potentially mandatory) contingency action to
curb the spread of the disease at the earliest opportunity
•
Aim to create preparedness action plans across the East African Community and harmonize
with established steering committees across the continent (e.g. South Africa’s Emergency
Plant Pest Response strategy and HLB action plan) to mitigate and contain the disease
Regulators:
•
Strengthen the content and enforcement of phytosanitary regulations on movement of citrus
plants and alternate hosts
•
Fast-track the process of testing, validating and registering products for the control of the HLB
vector
Researchers:
•
Carry out surveys to identify local natural enemies that can be used in augmentative and
conservation biocontrol
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•
Test locally-available biopesticides and other natural materials and produce formulations that
can maximise the toxic effects on ACP whilst limiting the side effects on beneficials
Advisory services:
•
Expand extension efforts to facilitate and coordinate judicious control of the psyllid vector if
detected, promoting IPM and low-risk options for management, as well as rapid removal of
infected trees in commercial, smallholder and abandoned citrus groves
•
Develop an array of cost-effective, clear and harmonized monitoring and impact assessment
protocols to be followed for HLB studies
Smallholder farmers:
•
Engage in early warning surveillance, with ACP scouting and trapping as part of routine insect
pest scouting programmes
•
Treatment and removal of infected trees as a priority and replacement with healthy trees,
with added protection from psyllid ingress in hotspot areas
Commercial farmers:
•
Citrus nurseries are encouraged to proceed with changing over to citrus tree production in
insect secure structures
•
Commercial growers need compliance agreements to ensure production of certified diseasefree material and implementation of phytosanitary protocols for movement and elimination
of inoculum
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Acronyms
ACP
Asian citrus psyllid
ACT
African citrus triozid
AfCGD
African citrus greening disease
ACGD
Asian citrus greening disease
AEZ
Agro-ecological zone
CABI
CAB International (Centre for Agriculture & Biosciences International)
CHMA
Citrus Health Management Areas
CLaf
Candidatus Liberibacter africanus
CLam
Candidatus Liberibacter americanus
CLas
Candidatus Liberibacter asiaticus
CRI
Citrus Research Institute
CRDF
Citrus Research and Development Fund
DALRRD
Department of Agriculture, Agrarian Reform and Rural Development
EIL
Economic injury level
EPPO
European Plant Protection Organisation
ETL
Economic threshold level
FAOSTAT
Food and Agriculture Organisation Statistical Database
HLB
Huanglongbing
HMO
Horticultural mineral oil
ICIPE
International Centre of Insect Physiology and Ecology
IGR
Insect growth regulator
IPM
Integrated pest management
NPPOZA
The National Plant Protection Organization of South Africa
PMDG
Pest Management Decision Guide
PPE
Personal protective equipment
SADC
Southern African developing countries
USDA
United States Department of Agriculture
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Introduction
Citrus is one of the world’s major fruit crops, recognized for contributing to food and nutritional
security, and ranks first in the global fruit trade. Indeed, citrus has remained the most sought-after
global fruit during the Covid-19 crisis, as people seek to boost their immune system by increasing
vitamin C intake. However, several biotic and abiotic factors are responsible for decreasing yields and
substantial economic losses worldwide. Among these, the insect-transmitted, phloem limited
bacterial disease, Huanglongbing (HLB), also known as citrus greening disease, is one of the most
ravaging pathogens of all commercial citrus varieties, for which an effective cure remains elusive.
Three closely-related species of Liberibacter are known to cause the symptoms of greening
disease: Candidatus Liberibacter asiaticus (CLas), Candidatus Liberibacter americanus (CLam),
and Candidatus Liberibacter africanus (CLaf). The heat-tolerant, Asian form of the disease, transmitted
by the Asian citrus psyllid (ACP), Diaphorina citri Kuwayama (Hemiptera: Liviidae) is the most
devastating and widespread. In East Africa, the heat-sensitive form of the disease caused by CLaf
(African citrus greening didease (AfCGD) is vectored by Trioza erytreae (Hemiptera: Triozidae), also
known as the African citrus triozid (ACT) (Aubert, 1987) and remains the most prevalent disease,
particularly in the cooler, mid to high altitude areas, causing yield losses of 25–100% in Kenya and
Tanzania (Richard et al., 2018).
In the last decade, CLas and its heat-tolerant insect vector have been spreading to the African
mainland and there is now a clear and present threat of HLB to the citrus industry in Africa, including
the previously sustainable warmer citrus-producing regions of East Africa.
In view of the threat posed by this pest complex, this evidence note aims to review the comprehensive
literature on HLB and its management from global experiences, and consolidate the relevant research
to provide recommendations for decision makers in Africa responsible for the response to the insect
vector and disease, as well as for external organizations seeking to assist in management. This
information will be useful for decision makers to prioritize investment and interventions in responding
to the growing threat. This evidence note is structured into five sections as follows:
•
Section 1 reviews citrus production trends, the citrus greening problem, current distribution
of the pest and vector and its environmental suitability.
•
Section 2 reviews the impacts of citrus greening in other affected regions and make informed
predictions on citrus yield losses and impact on trade in East Africa.
•
Section 3 provides information on ongoing and recent research on control methods,
highlighting the range of options using other countries as examples.
•
Sections 4 and 5 conclude with some sources of information and final recommendations for
key stakeholder groups in Kenya (with relevance to neighbouring African countries).
1 Citrus production and the citrus greening problem
1.1 Commodity context
The various species of citrus (Rutaceae) are all believed to be native to the subtropical and tropical
regions of Asia and the Malay Archipelago, and to have spread from there to all other continents
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where they have been cultivated throughout the ages. As many as 300 species have been described,
though the group presents taxonomic challenges due to the marked sexual compatibility between the
different species, which has generated hundreds of varieties. The term citrus fruits includes different
types of fruits and products. Although oranges are the major fruit in the citrus fruits group, accounting
for about 70% of citrus output, the group also includes small citrus fruits such as tangerines, mandarins,
clementines and satsumas, as well as lemons, limes and grapefruits. Today, an exceptional array of
varieties of citrus trees have evolved and been developed through natural evolution and artificial
selection. Wu et al. (2018) suggest citrus diversified during the late Miocene epoch through a rapid
Southeast Asian radiation that correlates with a marked weakening of the monsoons.
From an economic point of view, citrus fruits rank first in terms of world fruit production and
international trade value. The world production of citrus for 2018 was estimated at 139 million tonnes
(cultivated in over 140 countries around the world), the major producers being China, Brazil, the USA
and countries bordering the Mediterranean (Fig. 1). Nigeria is the largest citrus producer in Africa,
producing around 4 million tonnes (FAOSTAT, 2019), with acreage and production having dramatically
increased thanks to suitable ecological and climatic conditions for production (Oke et al., 2020).
Eastern Africa accounts for around 137,000 tonnes (FAOSTAT, 2019).
Fig. 1. World production of citrus fruits in tons (© Actualitix.com CC BY-NC-SA 4.0).
As a source of vitamin C and numerous other vitamins and minerals, citrus is marketed throughout
the world as a beneficial healthy fruit. Because of their nutritional and organoleptic qualities, citrus
fruits contribute to nutritional balance for both Northern and Southern populations. In Africa, citrus
fruits are an important source of income to farmers with scarce resources. There are two clearly
differentiated markets in the citrus sector: the fresh citrus fruits market (largely oranges) and the
processed citrus products market, orange juice being the most widely consumed fruit juice in the
world. Over the last two decades, small, easy peel and seedless citrus fruits (tangerines, clementines,
mandarins and satsumas) have seen a consumer-driven rise in trade, at the expense of fresh oranges.
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Consumption of citrus fruit juices has also increased, thanks to product convenience and healthiness,
quality improvements, price competitiveness, promotional activity and technological advances in
processing, storage and packaging. Among the major citrus varieties, only grapefruit has a level of
processed utilization comparable to oranges (Lacirignola and D'Onghia, 2009).
1.2 History of citrus production and trends in East Africa
Citrus fruits, grown by commercial and smallholder farmers worldwide, are one of the most
economically important fruit crops, creating employment in rural areas, income for resource-poor
farmers and providing human nourishment (Kilalo et al., 2009; Yesuf, 2013). Nigeria and South Africa
are the largest citrus producers in Africa (Oke et al., 2020) and in East Africa, Tanzania has become the
largest citrus producer after Kenya’s higher elevation growers faced severe impacts from greening
disease (Makorere, 2014). Citrus is grown within a broad band of approximately ±40◦ latitude of the
equator in tropical and subtropical climates with ideal temperatures ranging from 20 to 34 degrees
Celsius (Ackerman, 1938). Citrus is an important crop throughout East Africa, where production is
mainly by smallholders, however yield is in decline due to pests and diseases (Ouma, 2008; Otieno,
2015). The yields of smallholder farmers in Africa often do not exceed 4–10 t/ha, while the crop has
the potential of producing up to 50–70 t/ha in suitable countries practicing integrated pest
management (IPM) programmes (Kilalo et al., 2009).
Information (where available) is provided in Table 1 on the average area harvested, yield and
production of citrus in countries typically included within the definition of East Africa.
Table 1. Average area harvested, yield and production of citrus in East Africa (average 2016–2018).
Area harvested
(ha) (average
2016–2018)
Yield (hg/ha)
(average 2016–
2018)
Production (tonnes)
(average 2016–
2018)
United Republic of Tanzania
50,190
206,387
443,219
Kenya
23,475
483,652
195,343
Ethiopia
77,72
247,911
42,699
Somalia
3,858
184,024
24,020
South Sudan
1,969
980,91
19,316
Rwanda
3,130
63,983
9,598
Djibouti
no data
no data
2,624
Country
FAOSTAT (2019). Note: Data not available for Eritrea, Uganda or Burundi.
Kenya
Despite the decline in citrus fruit yields since the 1970s in Kenya, this remains a very important
domestic commodity, ranked as the most extensively cultivated fruit crop in the country (Ajene et al.,
2020a). The majority of the fruits produced in Kenya are consumed locally as a fresh product, and a
smaller quantity is processed into juices, jam and marmalades (MMA, 2008).
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The most common species of citrus planted are sweet oranges, lemons, limes, tangerines, grapefruits
and pummelos. In 2014, total citrus production was estimated at 140,292 mt, valued at US$ 31.1
million (HCDA, 2014). These levels of production are insufficient to meet domestic demand and the
country has moved from self-sufficiency to relying on imports of up to 44,000 tonnes (from Egypt,
South Africa and Tanzania) to satisfy increasing popularity (Ouma, 2008; Makorere, 2014; Gitahi, 2016;
TradeMap, 2019).
Low citrus yields and stagnation in production have been attributed to a range of factors including
severe shortages of land, pest and diseases, declining government support, increasing competition
from imports and lack of credit/investment capital (Ouma, 2008). Pests and disease infestation have
resulted in reduced quality and quantity of outputs, as such the country’s horticultural industry has
encountered huge losses on domestic trade, and on potential export earnings whilst undermining the
domestic systems competitiveness (Tschirley et al., 2004; Gitahi et al., 2016). The highest citrus
production is in the coastal, eastern and Rift Valley regions, although most smallholder farmers in
North Rift abandoned citrus orchards due to low yields caused by diseases and insect pests (Mulaa et
al., 2009). As far as fruit production is concerned, smallholder horticulture accounts for 40% of its
production, with the market share of fruits accounting for 99% of the domestic market (Ouma, 2008)
and prices are consequently determined by demand and supply forces. The production of citrus fruits
contributes a modest 13% of the total fruit production area and has been suffering from low yields,
with citrus greening being a prime constraint. In Tanzania by contrast, citrus fruits are widely grown
over some 41,642.91 hectares of land to produce around 100.18 tonnes per hectare per year
(Makorere, 2014). One study in the Kenyan counties of Makueni and Machakos highlight that for both
small and medium scale farmers, citrus production is a major source of income - the majority of
growers interviewed (89%) producing oranges on their farms with clementine the next most popular
citrus fruit (23%), followed by lemon (13%), while a few produced tangerines (4%), grapefruit (1%),
lime (%) and peach (1%). Similar trends were observed in both the surveyed counties, with a smaller
percentage of orange producers in Makueni (Gitahi et al., 2019).
Losses due to pests and diseases are compounded by the use of non-budding planting materials, low
fertilizer use and lack of irrigation, inadequate use of chemical pesticides and planting of unimproved
cultivars of scions and root stocks (Tschirley et al., 2004; Ouma, 2008; Kongai et al., 2018). This is
exacerbated further by the use of infected planting materials, whose casual and uncertified
distribution is recognized as a key transmission route for bacteria in particular. African citrus greening
disease alone has significantly constrained Kenya’s citrus fruit prospects. The disease was first
observed in South Africa in the late 1920s (Oberholzer et al., 1963) subsequently spreading to a
number of other African countries (Bové, 2014a). Furthermore, in East Africa much citrus production
is on smallholder farms which are characterized by intensive cultivation on available land close to
other farms which is likely to contribute to the spread of both the vector and disease, especially when
there is a lack of a coordinated management response (Ouma, 2008; Parsa et al., 2014).
Tanzania
Oranges were first introduced to Tanzania (Muheza District) in the early 1900s and by the late 1970s
were of major economic importance (Ebony Consulting International, 2003). Today citrus fruits are
one of Tanzania’s most important horticultural cash crops, exceeding that of its neighbours Kenya and
Uganda. It is grown in most regions in Tanzania with highest production in the Tanga region which is
well-known for the variety of its citrus fruits, followed by the coastal region and Morogoro (22.41,
14
18.31, 10.9 t/ha citrus productivity, respectively) (Nyambo and Verschoor, 2005; Makorere, 2014).
Out of an average 160,000 tons of citrus fruits produced per year in Tanzania, more than 85,000 tons
are sold in the Kenyan markets (Makorere, 2014). Tanzania exports primarily oranges (mostly
Washington Navel) to Kenya (accounting for 44% of imported oranges) with very limited export to
other East African countries (and negligible exports outside of Africa) for local consumption but also
for re-export to other regional markets (MMA, 2008). Indeed, exports from Tanga region in Tanzania
to Kenya are estimated to account for 60% of oranges produced (MMA, 2008). Tanzanian oranges are
delivered to Nairobi, Mombasa and Nakuru; during the peak season on a daily basis an average of
421,200,000 oranges (421,000 bags) arrive in Kenya (MMA, 2008). Tanzania also imports citrus from
other countries such as South Africa. The Tanzanian domestic market includes primarily rural and
urban consumption through informal markets, formal retail channels and institutional consumption,
and the market of processed products which is not yet well developed (MMA, 2008). However, the
citrus industry in Tanzania is not well developed, constrained by lack of irrigation and farmers’ limited
skills (Makorere, 2014). The most common varieties of oranges produced include Msasa, Nairobi,
Valencia, as well as Pamba, Jaffa, Washington and Zanzibar. Yield is approximately 8.5 t/ha (MMA,
2008).
Ethiopia
In Ethiopia, citrus is one of the most economically-important fruit crops grown by smallholder and
commercial farmers and includes sweet orange (82% of total citrus grown), mandarin, lime, lemon,
grapefruit, citrus hybrids, sour orange and citron (Dagnew et al., 2014). The main varieties of sweet
orange grown include Valencia (61.1% of locations considered), an unknown variety (58.3%),
Washington Navel (47.2%), Hamlin (44.4%), Pineapple (38.9%) and Jaffa (16.7%), with the most
commonly-used rootstocks being Sour orange, Volkameriana and Troyer Citrange (Dagnew et al.,
2014). Approximately 70% of the industry is represented by the major citrus production areas of Afar,
Somali, Oromia and Amhara Regional States (Bekele, 2007). Citrus farming occurs as part of mixed
agriculture with other crops, vegetables and non-citrus trees. The majority of fruit produced (98%) is
supplied to local markets such as Addis Ababa, Nazareth, Methahara, Diredawa and Harar, with fruits
from the north central farms marketed at Dessie, Woldva and Mekele towns, with only a very small
proportion (2%) from central east areas exported to neighbouring countries i.e. Djibouti and Somalia
(Bekele, 2007). The industry is threatened by various diseases (Dagnew et al., 2014).
Somalia
Grapefruit is the major citrus variety grown in the Mogadishu region of Somalia. Plantations were
established in the 1970s with cultivars consisting of both old and new varieties such as Marsh seedless,
Ruby and Redblush with sour orange and rough lemon rootstocks. In addition to grapefruit, smallfruited acid lime is the second most important citrus variety grown.
Eritrea
Citrus is one of the leading agricultural products in Eritrea (Lansford, 2017). Within the country the
western escarpment and south-western lowland zone are particularly suitable for citrus production
under irrigation by smallholders and medium scale irrigated plantations for internal market and export.
Citrus is also produced in the north-western lowland zone under a hot arid climate and the greenbelt
zone on the eastern escarpment of the central highland zone in the lower areas where the climate is
suitable (Ministry of Agriculture, 1995). Citrus production activities are reported to have begun
15
seriously from 1952 and by 1958 the De Nadai citrus farm in Elaberd was exporting over 3,500 tons to
the Arabian Peninsula and Europe. By the late 1960s it is reported that the 1200-hectare plantations
of De Nadai were the most productive in Eritrea (Negash, 1997). The Ministry of Agriculture reported
the total cultivated land in Eritrea to be 410 ha (373 ha orange, 33 ha lemon, and 4 ha mandarin) and
production 4,450 tonnes in 2003 with the average yield per ha for all citrus approximately 10.0 tonnes
per ha and as such much below the international averages (Naqvi et al., 2016).
Uganda
In Uganda, commercial citrus production (common sweet oranges, lemons and tangerines) began in
the 1960s with over a decade of successful production followed by declining productivity and an
eventual re-establishment of the industry in the 1990s (Njoroge et al., 2009; Kongai et al., 2018).
Common varieties include Sweet Valencia, Washington Navel, Hamlin and the local orange (Kongai et
al., 2018). Kongai et al. (2018) report that in eastern Uganda citrus farming is a smallholder enterprise
whereby farmers produce citrus using traditional technologies with limited chemicals and irrigation
and use of informally-distributed plant materials. Fruits are commonly sold fresh as value addition by
processing is not established with a lack of coordination in the value chain. However, citrus is a
profitable venture that can lead to improved farm income for smallholders as well as local
employment opportunities (Kongai et al., 2018). The total area under citrus fruit cultivation is
approximately 10,000 ha with a total annual production of 10,000 tonnes (Njoroge et al., 2009).
Rwanda
In Rwanda the production of common sweet oranges mainly occurs in the south-west Cyangugu
province with fruits consumed fresh locally and some processing into juice taking place (Njoroge et al.,
2009). Citrus production in Djibouti has grown at an average annual rate of 2.41% from 1,704 tonnes
in 1999 to 2,676 tonnes in 2018 (Knoema, 2020a).
South Sudan
Depending on the agro-ecological zone, a wide range of food and cash crops are grown in South Sudan,
including citrus. Here, citrus production has increased at an average annual rate of 7.08% from 13,000
tonnes in 2012 to 19,480 tonnes in 2018 (Knoema, 2020b). However, most activity in the rural sector
is low-output subsistence agriculture. There is a lack of information on citrus production and it is
therefore assumed that the citrus grown here would be similar to that of Sudan where the most
important citrus fruit trees include sweet orange, grapefruit and lime with other citrus grown but on
a much smaller scale including mandarin, lemon and pummelo (NBSAP, 2000).
Burundi
Limited information is available on citrus production in Burundi, however the Poverty Reduction
Strategy Paper states that in order to improve economic growth, promotion of agricultural inputs was
to be intensified which would include the introduction of rootstocks of citrus trees (IMF, 2009).
1.3 Understanding African and Asian citrus greening and their vectors
Citrus greening has been known, from its first description in the early 1900s in China, as huanglongbing
(HLB, translated as “yellow shoot disease”), referring to the characteristic yellow colour of the new
flush of growth on infected trees. The same disease is called mottle leaf in the Philippines, dieback in
India, phloem necrosis and vein phloem degeneration in Indonesia, and citrus destruction in Thailand.
16
Practically all commercial citrus species and cultivars are sensitive, regardless of rootstocks; with
grapefruit, sweet oranges, some tangelos and mandarins being the most susceptible, and limes,
lemons, sour oranges and trifoliate oranges the least (Abdullah et al., 2009). By the 1970s, HLB had
devastated many citrus-growing regions in Asia and Africa (National Academies of Sciences,
Engineering, and Medicine, 2018) but for twenty years, during the 1970s and 1980s, the only way to
confirm infection by HLB in trees showing symptoms was by Transmission Electron Microscopy (TEM)
(Garnier and Bové, 1996). Characterization of the causal organism as a bacterium was eventually
achieved by cytology coupled with electron microscopy (Garnier et al., 1984a,b). Specific detection
and identification of the African and the Asian HLB bacteria as Gram-negative organisms, belonging to
a new genus of alpha division of Proteobacteria: “Liberibacter”, or more precisely, “Candidatus
Liberibacter” was subsequently made on the basis of their 16SrDNA sequences (Villechanoux et al.,
1992). The term Candidatus indicated that the taxonomical identification of the bacterium could not
be carried out with cultured organisms but involved molecular characterization. Within the
“Candidatus Liberibacter” genus, the African bacterium and the bacterium from the Asian diseases
represented two distinct species, which were named Candidatus Liberibacter africanus (CLaf) and
Candidatus Liberibacter asiaticus (CLas) respectively (Jagoueix et al., 1994, 1997; Gottwald, 2010). The
subsequent evolution of PCR techniques allowed CLaf and/or CLas to be detected and identified
appropriately (Jagoueix et al., 1996; Hocquellet et al., 1999). The disease spread to Oceania, South
and North America and the name huanglongbing was officially adopted for all forms of the disease in
1995 (Bové, 2014b) following research demonstrating its infectious nature and transmissibility by graft
inoculation (Lin, 1956), and by two citrus psyllids.
A third Liberibacter, Candidatus Liberibacter americanus (CLam), was discovered in Brazil in 2004. The
nomenclature adopted for the naming was on the basis of the continent from where each Liberibacter
species had evolved. Later in 2005, the Asian HLB was reported for the first time in the Americas,
namely in Florida and Sao Paulo, and by 2013, the disease was widespread in North, Central and South
America. Subsequently, HLB is now widely used to describe the African, American and Asian forms of
the disease wherever they occur, and is provided together with the specific causative agent to
differentiate the strains (Fig. 2).
CLaf, which causes African citrus greening disease (AfCGD) is widespread in Africa. CLaf is historically
known to be the most prevalent Liberibacter species on citrus on the continent and was first observed
in South African citrus orchards in the late 1920s (Oberholzer et al., 1963). The disease associated with
CLaf in South Africa is locally known as African greening (Oberholzer et al., 1963). Since its initial
discovery, CLaf has been associated with citrus in 15 other African countries and the Mascarene islands
(Graça, 1991; Garnier and Bové, 1996; Bové, 2014a; Roberts et al., 2017). In some areas in Kenya,
whole orchards were lost due to HLB, while mild infestations caused up to 25% yield loss (Kilalo et al.,
2009). Following the discovery of HLB in Kenya at Thika, Kamiti and Kitale in the 1970s (Schwartz,
1975), application of systemic and contact insecticides was recommended combined with removal of
HLB-infected trees, planting disease-free nursery stock and abandonment of citrus production in areas
above 800 m.a.s.l. that were known to be prone to colonization by the psyllid vector (Beige et al.,
1984). Within the East African region, HLB was first reported in Tanzania (Schimwela, 2016); Rwanda
(Aubert, 1987), Burundi (Bové, 2006) and Angola (Fourie et al., 2020), with CLaf as causal organism
and T. erytreae as vector.
17
Fig. 2. Distribution of Candidatus Liberibacter asiaticus [green], Candidatus Liberibacter africanus
[blue] and Candidatus Liberibacter americanus [orange] (CABI ISC data, August 2020).
A number of new lineages of the Candidatus species have also been reported including five subspecies
of CLaf identified from indigenous rutaceous trees in South Africa i.e. CL africanus subsp. capensis
(CLafC) (Garnier et al., 2000), CL africanus subsp. clausenae (CLafCl), CL africanus subsp. vepridis
(CLafV), CL africanus subsp. zanthoxyli (CLafZ) (Roberts et al., 2015) and CL tecleae (CLafT) (Roberts
and Pietersen, 2016). Currently, little is known about these ‘CL africanus’ subspecies regarding their
host range, transmission and disease-causing potential to citrus, although CLafCl has been reported
from citrus in Ethiopia, Kenya and Tanzania (Shimwela et al., 2016; Roberts et al., 2017; Ajene et al.,
2020b).
Although the liberibacters remained native to the particular zones where they were discovered, in
modern times they have spread, along with their psyllid vectors, to new areas, along with their
susceptible crops (aidoo). CLaf is transmitted by the African citrus triozid T. erytreae (del Guercio)
(Triozidae), also known as the African citrus triozid (ACT) (Aidoo, 2020b). By contrast, CLas is
transmitted by the Asian citrus psyllid (ACP) D. citri Kuwayama (Liviidae) (Graça & Korsten, 2004) (Figs.
3 and 4). However, both ACT and ACP have been shown to be capable of transmitting both forms of
the disease experimentally (Lallemand et al., 1986).
ACP infests species in at least 10 genera in the family Rutaceae (which contains about 160 genera
including Citrus) with variable suitability for oviposition, development and reproduction. This insect
requires 2 to 7 weeks to develop from egg to adult, adults live several months, and there are 9 or 10
generations per year. Adults fly 25 to 50 m regularly, but have been found to fly up to 100 m towards
new leaf flushes over a 3-day period (Boina et al., 2009). In laboratory conditions, D. citri are capable
of flying continuously for up to 2.4 km without wind assistance (Martini et al., 2014; Lewis–Rosenblum
et al., 2015) and further long-range dispersal of psyllids might be facilitated by wind (Gottwald et al.,
2007). It is interesting to note that psyllids have been collected in dogue nets towed behind light
aircraft flying at a height of 300m (White, 1970). ACT can disperse up to 1.52 km within 7 days in the
absence of host plants (Berg and Deacon, 1988). Trapping data from Florida indicate no consistent
ACP seasonal movement patterns, which means continuous monitoring is required. Multimodal
sensory inputs contribute to host finding; ACP orient to leaf flush via volatile signals and assess plant
18
suitability using gustatory and visual cues. Ovipositing females prefer the plant species on which they
developed, but preferences can shift after exposure to an alternative host.
Adults are attracted to colours within the reflectance spectra of rutaceous plants. This has formed the
basis for monitoring of ACP and ACT with traps. A survey in Kenya compared eight differently coloured
double-sided sticky traps to evaluate which colour was most effective for detecting ACT and ACP,
particularly at low densities. Yellow and green traps captured more ACTs and ACPs than any other trap
type (Aidoo et al., 2020b). Infected plants are more attractive to ACP due to HLB-induced volatiles.
However, infected trees are less suitable for ACP development, and psyllids leave infected plants
shortly after pathogen acquisition, promoting pathogen spread.
T. erytreae is the only Trioza species to feed and develop on Rutaceae plants, not only citrus, but also
citrus relatives, including Vepris lanceolata (Lam.) {= Vepris undulata (Thumb.), = Toddalia lanceolata
(Lam.)} and Clausena anisata (Willd.), two preferred, native hosts of the African citrus psyllid. Fagara
capensis (Thumb.) {= Zanthoxylum capense (Thumb.)} is also an adequate indigenous host for T.
erytreae development (Moran, 1968). In Kenya, a recent study also found this insect feeding on Ficus
thonningii (Blume), Ficus sycomorus L. (both Moraceae), Stephania abyssinica (Quart, Dill & A. Rich)
Walp. (Menispermaceae), Murraya koenigii (L.), Teclea nobilis (Del.), Calodendrum capense (L.f.)
Thunb. and Vepris bilocularis (Wright & Arn.) Engl. (Rutaceae) (Aidoo et al., 2019). Thus, before citrus
and its hybrids (which are not indigenous to Africa) were introduced into Africa, T. erytreae had at
least two native rutaceous hosts to complete its development: V. lanceolata and C. anisata. These two
plants are among the original host plants of T. erytreae (Moran, 1968). V. lanceolata is not only a
preferred host of ACT, it has also been reported as a host to the HLB bacterium, CLaf (Korsten et al.,
1996). T erytreae also develops well on Citrus limon and must have been well pre-adapted to this host
at the time of the introduction of citrus to Africa. For this pre-adaptation purpose, F. capensis was
almost as suitable as C. limon for the development of T. erytreae (Moran, 1968).
The African continent remained free from CLas until 2010, when detection of this bacterium was
reported from citrus trees in northern Ethiopia (Saponari et al., 2010). CLas has recently been reported
from Kenya (Ajene et al., 2020a), while the HLB vector D. citri is reported from Ethiopa, Tanzania,
Kenya and Nigeria (Rwomushana et al., 2017; Ajene et al., 2020c; Oke et al., 2020). Secondary
transmission is also possible by grafting and colonization by parasitic dodder plants (Cuscuta spp.)
(Zhou et al., 2007; Graça, 2008).
1.4 Differentiating symptoms of African and Asian greening in East Africa
The African form of the disease (CLaf) and its associated psyllid vector, ACT, are both heat-sensitive,
occurring in regions of cool, moist climate, often on highlands, with temperatures below ~30°C (Bové,
2014a). The Asian form of HLB (CLas) and its Asian psyllid vector, ACP are both heat-tolerant, occurring
at temperatures above 27°C (Batool et al., 2007), although they are more sensitive to high rainfall and
humidity (Moran and Blowers, 1967; Catling, 1972; Aubert, 1987; Graça, 1991).
Symptoms of HLB are influenced by temperatures at which affected trees grow. The two Candidatus
species, CLas and CLaf both cause the characteristic symptoms of chlorosis that resemble zinc
deficiency and mottling on leaves, as well as the poorly developed root systems and decay from the
rootlets (Graça, 1991; Batool et al., 2007). The blotchy mottle pattern on one side of the leaf midrib is
not symmetrical to that on the other side and this asymmetry distinguishes blotchy mottle from
nutrient deficiency. In early stages of infection, blotchy mottle might be the only leaf pattern to be
19
seen. Twig dieback, fruit drop, irregularly-shaped (lopsided) fruit, reduced fruit size and lower internal
fruit quality with bitter taste are other typical symptoms (Fig. 6). However, the Asian form of greening
causes more extensive dieback and tree death. In the case of African greening, fruits remain immature
and green, and seeds are aborted and stained (Batool et al., 2007). Usually the actual causative agent
will be identified using molecular tools. Typically, the nymphs of T. erytreae live in individual
depressions on the undersides of host plants (Fig. 5), whereas nymphs of D. citri tend to colonize the
stems of new growth and never produce individual pits on the leaves (Halbert and Manjunath, 2004).
3
4
Fig. 3. Adults and nymphs of D. citri on citrus plant (credit: I. Rwomushana, CABI); Fig. 4. Adult D. citri
on citrus flush (credit: D. Hall, USDA-Agricultural Research Service).
5
Fig. 5. Nymphs of Trioza erytreae (African citrus triozid) on leaf (credit: Peter Stephen, CRI).
1.5 Huanglongbing symptoms and crop damage
Greening-affected trees generally exhibit open growth, stunting, twig dieback, sparse yellow foliage
or severe fruit drop (Batool et al., 2007). After inoculation of the phloem sieve tubes in the citrus host
20
during feeding of the psyllid vector, Ca. Liberibacters exploit phloem cellular processes for nutrient
acquisition. CLas levels increase rapidly, however infected trees remain asymptomatic through the
early disease phase. Indeed, these multiple asymptomatic infections, incomplete systemic distribution
within trees and prolonged incubation period can make detection of HLB difficult. Sometimes a citrus
plant will express with typical HLB infection such as yellow shoots and blotchy, mottled, narrow leaves,
sometimes with vein yellowing, on one branch while other parts of the tree remain symptomless. As
the bacterial colonization progresses systemically, the canopy also becomes thin and chlorotic, tree
growth slows, leaves remain reduced in size and leaf tips become necrotic (Halbert and Manjunath,
2004; Bové, 2006; Gottwald et al., 2007). Mathematical models based on HLB epidemiology have
shown that once detectable infections occur in 5% of trees within an orchard, it is likely that 90% of
the orchard is infected (Craig et al., 2018), even in the presence of control.
6
Fig. 6. Fruit of HLB-infected citrus tree showing colour inversion (credit: USDA-Animal and Plant Health
Inspection Service (APHIS)).
In the early stages of the disease, a clear diagnosis may be difficult to achieve because of mildness of
symptoms and resemblance to other conditions. McCollum and Baldwin (2017) found that HLB
symptoms were more pronounced during cooler seasons than in warmer months. Leaves can thicken
and veins enlarge and appear corky. Later, yellow blotches appear between veins that remain green,
similar to zinc deficiency or other nutritional deficiencies and leaves may drop as twig ends become
necrotic (Gottwald et al., 2007). The root systems are poorly developed, showing very few fibrous
roots, likely due to nutrient starvation (Graça, 1991; Batool et al., 2007). In some cases, green colour
develops on fruit at the peduncular rather than the stylar end, causing inverted colouration. Fruit from
diseased trees are marked by their bitter taste, they are reduced in size, may be asymmetrical and
contain small, brownish/black aborted seeds. As the disease progresses, fruit yield and quality decline
(Timmer et al., 2000; Halbert and Manjunath, 2004; Bové, 2006).
Ca. Liberibacter spp. multiply in the sieve tubes of infected plant hosts, squeezing from sieve cell to
cell through sieve pores. As a host response to the spread of the bacterium in the vascular system, an
21
increase in callose deposition occurs and as the bacteria multiply, the flow of phloem sap between
cells is impeded, disrupting the movement of sugars (Koh et al., 2012). CLas also suppresses the
immune response of the tree allowing for a long incubation period. One of the predominant
biochemical responses to HLB is the excessive accumulation of starch in the aerial plant parts, due to
the upregulation of glucose-phosphate transport, which is involved with the increased entrance of
glucose into this pathway (Martinelli and Dandekar, 2017). It is this imbalance in sugar transport and
metabolism and persistence of starch in leaves that results in root starvation, severe health decline
and eventual death (Etxeberria et al., 2009; Fan et al., 2010; Zheng et al., 2018). Changes in the
secondary metabolite profiles of citrus and suppression of defence responses have also been found in
CLas-affected citrus (Nwugo et al., 2013).
CLas must first be ingested and then translocated into the insect’s gut tissues. Subsequently the
bacteria can replicate and systemically infect the insect, moving to the salivary tissues from which they
can infect other host plants (Ammar et al., 2011). Most vectored plant pathogens can be acquired by
their vectors at or just prior to the onset of symptoms. Until then, the plant might be infected, but it
is not spread to other plants. The time between infection and the time when vectors can acquire the
pathogens is the latent period, whilst the incubation period refers to the time between infection and
appearance of symptoms (National Academies of Sciences, Engineering, and Medicine, 2018). With
HLB, the latent period is equal to one generation of psyllid vectors (Lee et al., 2015), and the incubation
period is long and variable, up to at least 6 years (Shen et al., 2013). Lee et al. (2015) reported on the
phenomenon of infective colonization events - in other words, HLB is passed on from adults to their
progeny as the nymphs acquire CLas from their feeding site, previously infected by their parents (Lee
et al., 2015).
The two main factors regulating psyllid populations are availability of young growing shoots for
oviposition and temperature and depending on these, the latent period can occur in 2–3 weeks. A
single female psyllid is capable of producing 800 to 1,000 eggs over her lifespan (Tsai and Liu, 2000).
The increase in numbers of infected psyllids can be enormous, especially if abundant new colonization
sites are available for emerging infected adults. Late nymphs and adults have a propensity to acquire
CLas on young flush tissue and are attracted to the yellow-green colour of HLB-infected trees (Graça,
1991), which explains their attraction to yellow/green sticky traps (Sétamou et al., 2016). CLas
infection of the citrus tree further induces the release of methyl salicylate, a plant host volatile, which
renders infected plants more attractive than uninfected plants. However, infected trees are less
suitable than uninfected plants as hosts for development of ACP, and the tendency of psyllids to leave
infected plants shortly after pathogen acquisition may promote the spread of the pathogen (National
Academies of Sciences, Engineering, and Medicine, 2018). As acquisition time increases, so does the
percentage of psyllids becoming infected with CLas (Brlansky and Rogers, 2007). Additionally, adult
psyllids have been shown to be capable of acquiring CLas from citrus that is infected with the pathogen
yet not showing symptoms but due to the uneven distribution of the pathogen within a plant, not all
parts of the tree will serve as an inoculum source at any given time (Brlansky and Rogers, 2007). The
disease tolerance of different citrus varieties varies significantly and some have been found to
accumulate a greatly reduced pathogen load compared with susceptible varieties (Albrecht and
Bowman, 2012) and show less severe symptoms (Fan et al., 2012).
HLB impact is dependent on several other variables including age of tree at first infection, levels of
tolerance and environmental factors. These variables may allow some trees to maintain the same or
similar levels of productivity several years post-infection, while others may decline rapidly. HLB causes
22
fruits to drop prematurely, resulting in a 30–100% yield reduction. HLB-infected trees become
unproductive within 2 to 4 years after the onset of the disease and young infected trees typically do
not reach productive age.
Tree mortality can occur several months to years after infection (McClean and Schwarz, 1970; Graça,
1991; Bové, 2006; Batool et al., 2007; Bassanezi et al., 2011; Liao and Burns, 2012). Huanglongbing
can infect all commercial citrus cultivars and causes substantial economic losses by shortening the
production life span of infected trees (Bové, 2006). Without any control, in younger orchards, tree
death can result in 50% of plantings within 5 years, and may take longer in older groves (Gottwald,
2010). In China, without any control, it took only about 5 years for an orchard to reach 100% infection.
In Reunion, the time needed to reach 100% infection was estimated to be 13 years while the average
time worldwide is reported as 8 years (Bové, 2006).
1.6 Current spread and distribution of HLB in Africa
Saponari et al. (2010) reported the presence of CLas in samples from symptomatic sweet orange
budwood trees and orchard plants collected in April 2009 from Tigray and North Wollo in northern
Ethiopia. These were the first records of CLas for the country and for the African continent. The
authors at the time recommended prompt eradication of symptomatic trees and further surveys to
determine the full distribution of the disease and its vectors, however, Bové reported failure in
encouragement of Ethiopian authorities to do this in 2012 and 2013. A survey in November 2017 of
the African citrus greening vector T. erytreae was carried out in the Amhara Region (central to northwestern Ethiopia) by Ajene et al. (2019). Screening of T. erytreae samples collected from sweet orange,
lemon and tangerine trees revealed them to be carrying CLas, the first time this had been reported in
field populations of the psyllid. Previous research has demonstrated the capacity of T. erytreae to
transmit CLas (Massonie et al., 1976) and this development has brought additional concerns of T.
erytreae as an alternate route of HLB proliferation in the absence of, or in addition to the primary CLas
vector, D. citri. In 2020, following reports of presence of the primary HLB vector from Tanzania and
Kenya, Ajene et al. (2020b) surveyed citrus-growing regions in Ethiopia for the psyllid and found it to
be present in five locations in North and South Wollo in the north of the country, at altitudes between
1,619 and 2,112 m.a.s.l – higher than is typical for the psyllid in its native range. The source of D. citri
was not clear, but the psyllid may have arrived on imported plant materials. Vector management was
recommended, but the spread of D. citri southward is expected to be imminent (Ajene et al., 2020a).
In addition, a recent study has shown that CLas is increasingly widespread in Ethiopia, present in
regions of the country distant from previously surveyed areas and thriving at higher altitudes with
cooler temperatures (Ajene et al., 2020b).
The first detection of D. citri in Eastern Africa was reported from 2014 and 2015 surveys in Tanzania
by Shimwela et al. (2016) at altitudes of 300–600 m.a.s.l. around Morogoro in the east of the country.
Rwomushana et al. (2017) conducted further surveys for the psyllid from 2015 to 2016 in Kenya,
Tanzania and Zanzibar. D. citri was found to be present in Kenya at six sites: four in Kwale county in
the south-east near to the coast and the Tanzania border; one in Nairobi county; and one in Kericho
county in the west, at altitudes ranging from 20–1,666 m.a.s.l. In Tanzania, D. citri was most prevalent
in the Morogoro region from which it was first reported but was also present to the east to Dar es
Salaam and Zanzibar and south to Kibiti, at altitudes ranging from 19–668 m.a.s.l. It was apparent from
this study that the distribution of D. citri in these countries was expanding (Rwomushana et al., 2017).
Between 2016 and 2018, Rasowo et al. (2019) surveyed citrus in Kenya and Tanzania for greening
23
symptoms and vectors and concurred that D. citri is spreading fast in the region and adapting to new
geographic areas and ecologies. Of great significance to both Kenya and Tanzania in the immediate
term is the recent detection of CLas at sites in the warm coastal region of Kenya, close to the border
with Tanzania (Ajene et al., 2020a). With D. citri also present in this area, there is a high risk of HLB
proliferation in the region.
Kalyebi et al. (2016) reported presence of CLas in T. erytreae specimens from Washington Navel and
rough lemon at two sites in eastern Uganda - a first record of the disease in the country - however,
subsequent research has suggested that this was a misidentification of Candidatus Liberibacter
africanus subsp. clausenae (CLafCl) (Roberts et al., 2017; Ajene et al., 2020a) and to date it is not
apparent that CLas or D. citri are present in the country.
The current distribution and ongoing spread of both CLas and its primary vector D. citri in multiple
countries, compounded by T. erytreae’s potential to vector HLB including at higher altitudes is cause
for huge concern. Furthermore, the predicted suitability of many important citrus-growing regions in
East Africa to the disease and its main vector (as described in Section 1.7), warrants urgent action to
contain and limit the impacts of HLB in the region.
Of great significance to Nigeria – a major citrus producer – and its neighbours in West Africa is the
recent arrival of D. citri (Oke et al., 2020). The psyllid was collected from sites in Oyo State in the southwest of the country in October 2019. The psyllids were assayed for presence of CLaf, CLam and CLas,
but fortunately none tested positive for any of these liberibacters. The tropical climate prevailing in
citrus-producing areas of Nigeria and other West African countries may favour the rapid spread of this
psyllid and are also expected to be ideal for HLB should the disease arrive in the region (NaroueiKhandan et al., 2016; Ajene et al., 2020d; Oke et al., 2020). For this reason, a rapid response to control
D. citri and the development of rigorous plans to manage HLB in the region, should it arrive, would be
valuable.
1.7 Modelling environmental suitability and potential distribution of HLB and
its vector
A challenge to the African citrus industry is the current lack of knowledge on the habitat suitability for
Liberibacter infection across the continent (Ajene et al., 2020d). In order to make effective risk
assessments of potential bio-security threats, prediction models are extremely useful and help to
inform management strategies to minimise future losses, in addition to estimating the potential
impacts of climate change on species distributions (Graça and Korsten, 2004; Ajene et al., 2020d).
Although insect vector transmission is one of the major contributors to disease spread and previous
studies have focused on this, it is also important to consider the environmental requirements of the
pathogen (Gottwald, 2010). Here, consensus modelling for the vector and pathogen provides a more
robust view of potential disease distribution (Ajene et al., 2020b). Narouei-Khandan et al. (2016)
conducted the first study assessing the potential global risk of HLB (CLas) and ACP establishment in
citrus-growing areas using two types of correlative modelling approaches to assess climate suitability:
(i) Maximum Entrophy (MaxEnt) as a presence-only or a presence-background model (Phillips et al.,
2006) and (ii) Multi-Model Framework (Worner et al., 2010) whereby from nine models the Support
Vector Machine (SVM) achieved the highest performance rank.
24
Predictions for potential HLB (CLas) distribution for both models were that central and eastern parts
of Africa would be environmentally suitable for the Asian form of HLB. Highly suitable areas predicted
for ACP establishment were the lowlands in Central and Eastern Africa, in addition, large areas in
Central and West Africa, and coastal areas in Northern Africa were predicted as climatically highly
suitable for the psyllid. Thus, without preventative measures these predictions suggest CLas could
establish widely in Africa with potential hotspots in Central and South-eastern Africa (Fig. 7) (NaroueiKhandan et al., 2016).
7
Fig. 7. Consensus model showing the hotspot areas where one or two models (MaxEnt and SVM) agree
on the probability of both citrus huanglongbing (HLB) caused by CLas and the Asian citrus psyllid (ACP)
occurrence (from Narouei-Khandan et al., 2016).
MaxEnt and Multi-Model (SVM) predictions by Shimwela et al. (2016) predict suitability for D. citri
establishment in the majority of citrus-growing areas in Africa. They conclude that establishment of D.
citri and CLas is highly likely in East Africa, part of South-central Africa, and some areas of West Africa,
where climatic conditions would be suitable (Shimwela et al., 2016). Ajene et al. (2020a) using a threemodel consensus (MaxEnt, BIOCLIM and Boosted Regression Trees) again predict potential
distribution of CLas in large areas of Central, Eastern and Southern Africa and some parts of Western
Africa where marginal to optimal habitat suitability is demonstrated for HLB establishment (Fig. 8).
Predictions under climate change scenarios indicate in a moderate scenario, hotspots were
predominantly in Southern Africa, whereas in the extreme scenario, hotspots were predominantly in
Western, Central and Eastern Africa.
A further consensus model considering the environmental requirements for both the vector and
pathogen indicate large areas of optimum habitat suitability for the pathogen in coastal and western
Kenya where citrus production is high with increased risk of spread into central Kenya.
Large areas of optimum habitat in citrus-producing areas were also identified in Ethiopia including
Nura-Hera, Awasa, Jimma and Dire Dawa. In Tanzania large areas were found to be marginal for the
optimal suitability for the pathogen, but the island of Zanzibar showed high suitability. In eastern
Uganda, for the major citrus-producing region of the country, the model showed marginal suitability
for CLas (Fig. 9) (Ajene et al., 2020b).
25
Fig. 8. Potential distribution of Huanglongbing in Africa, as predicted by three-model consensus
(BIOCLIM, MaxEnt and Boosted Regression Trees) (from Ajene et al., 2020a).
9
Fig. 9. Potential distribution of Huanglongbing associated with Candidatus Liberibacter asiaticus in
Eastern Africa, as predicted from the current occurrence locations using global 50-year climate data
with MaxEnt (from Ajene et al., 2020b).
Thermal niche maps produced by Taylor et al. (2019) support the model findings. Here, climatepredictive mapping (where transmission can occur between 16°C and 30–33°C with peak transmission
26
at approximately 25°C) highlights highly suitable areas for HLB establishment including large citrusproducing regions near the equator in many African countries that are highlighted as not only
permissive, but highly suitable for HLB for 12 months of the year (Figs. 10 and 11).
Fig. 10. The number of months per year that locations have permissive temperatures according to
Taylor et al.’s H11 S(T) model (from Taylor et al., 2019).
Fig. 11. The number of months per year that locations have highly suitable temperatures according to
Taylor et al.’s H11 S(T) model (from Taylor et al., 2019).
In summary, environmental modelling allows the prediction of the potential distribution of HLB
associated with Candidatus Liberibacter asiaticus. The findings from the studies presented here
suggest that both the psyllid vector and pathogen have high probability of wide establishment in
important citrus-producing areas of Africa and that their distribution would be further facilitated by
changing climatic conditions.
27
2 Impacts of HLB on citrus and other socio-economic
variables
2.1 Documented impacts of Huanglongbing in other regions
Asian citrus psyllid poses a major threat to citrus everywhere and is the prime focus of citrus pest
management wherever it is present, with a large portion of economic losses in citrus production on
the Asian and American continents attributed to Huanglongbing (Bové, 2006).
Globally, citrus producers are facing serious problems with the emergence of the HLB disease (Teixeira
et al., 2008; Bassanezi et al., 2011). The United States is a major global citrus producer with the 2018–
2019 crop valued at $3.35 billion. HLB was responsible for the decrease in the production of oranges
for processing in the United States from around 8 to 2 billion tons from 2007–2008 to 2017–2018, a
drop of more than 70% since HLB was detected in 2005 (Hodges and Spreen, 2015). The fresh fruit
market also decreased by 21% during the same time interval. This market was less impacted than the
rest of the citrus industry because, in the United States, around 90% of the oranges produced in Florida,
the state with the largest prevalence of HLB, are processed for juice, while California supplies oranges
for the fresh market (USDA-NASS, 2018). Detection of HLB in Florida in 2005 impacted the entire
Florida citrus industry, with its citriculture practices changing overnight. The result was intensive
pesticide applications, aggressive removal of citrus greening-positive trees, and the complete switch
from outdoor to indoor citrus nursery operations (Hall et al., 2012). Singerman and Useche
(2016) reported a threefold increase in the price of a box of oranges since HLB had been detected in
the United States. Economic loss from systemic infection is generally considered as a function of
disease incidence (Qureshi and Stansly, 2020). A vector such as D. citri is a pest in its own right and its
damage potential is increased in proportion to the number capable of transmitting disease. For a
perennial crop such as citrus, there is the additional challenge for vector management in that disease
incidence is cumulative rather than reset every cycle, as in annual crops. A preventive approach is
therefore more favourable for citrus, especially early on, as the biological and economic impact of
disease is greatest on young plants.
Eradication of HLB-infected and nearby trees in Florida eliminated one-tenth of citrus production
capacity by 2008 and in Florida alone, HLB has caused a cumulative loss of $2.994 billion in grower
revenues over the 2006–2007 to 2013–2014 period, an average of $374 million per year (Hodges et
al., 2014), whilst a 2016 economic impact analysis reported losses of more than $4.6 billion and over
30,000 jobs. Growers in other orange-growing states such as California, Texas and Arizona are also
becoming increasingly affected by HLB. In California, economic losses amounting to $2.7 billion due to
Asian greening have been reported (Lopez and Durborow, 2015). In the past decade in the US, HLB
has caused around a 21% decrease in the fresh citrus fruit market and about a 72% decline in the
production of oranges used for juice and other products (Dala-Paula et al., 2019). Several unsuccessful
attempts have been made to cure or reduce HLB symptoms in Florida, where most citrus growers have
chosen to live with diseased trees rather than eliminate them and this has proved the Achilles heel in
the fight against HLB.
In China, where the disease originated, top-producing Jiangxi Province had lost 25% of its groves as of
the end of 2018, with the destruction of a hundred million commercially grown citrus trees reported
in Asia (Zhang et al., 2010).
28
In 2004, the first discovery of the disease in the Western Hemisphere was in São Paulo, Brazil. Since
then, the disease has eliminated 52.6 million sweet orange trees, a 31% reduction in area. The psyllid
vector was reported in São Paulo and Florida as early as 1942 and 1998, respectively (Bové,
2006; Tansey et al., 2017) however. CLam was the most prevalent bacteria species in Brazil in 2005,
which initially affected more than 90% of the infected trees, decreasing to 60% in 2007. During this
period, there was an increase in CLas infection, from 5 to 35% of the infected trees, while a combined
infection remained practically the same at 5% (Coletta-Filho et al., 2010; Gasparoto et al., 2012). The
detrimental effect of HLB on citrus was further evidenced by the loss of a million CLas-infected citrus
trees in São Paulo within 3 years (Gottwald et al., 2007). The Brazilian industry responded rapidly
however, with sensitive molecular tools for diagnosis (PCR) in place within months of the first reports
and in less than a year the Brazilian Government enacted legislation to enforce eradication, mitigation
and prevention measures. As a result, the incidence of greening within all the major citrus-growing
estates has massively declined but the disease took its toll nonetheless and the number of citrus farms
declined from 14.6 thousand in 2007 to 9.5 thousand in 2018 with the greatest impact on small and
medium-sized citrus growers that were unable to control and cope with the damage caused by HLB
(Bassanezzi et al., 2020).
In South Africa, severe losses from African citrus greening were experienced (30–100% in some areas)
in the 1930s, 40s and 50s (Graça, 1991). Subsequently, control strategies have helped maintain HLB
incidence at economically-acceptable levels despite heavy losses up until the late 1970s (Schwarz,
1967; Buitendag and von Broembsen, 1993). This is in part due to the temperature sensitivity of CLaf
(Schwarz and Green, 1972) and its natural vector, T. erytreae, limiting the occurrence of HLB to cooler
production areas (McClean and Oberholzer, 1965), combined with the effective control of T. erytreae.
In Saudi Arabia, all sweet oranges and mandarin trees had been lost by 1986 leaving only limes (Aubert,
1994). In Indonesia alone, HLB has resulted in the destruction of 3 million trees (Tirtawadja, 1980).
In the Philippines, citrus culture has been drastically limited by HLB. Between 1961 and 1970, the area
planted to citrus was reduced by over 60%, and in 1971 over one million trees were destroyed in one
province alone due to HLB (Graça, 1991). Similarly, in certain areas of Indonesia, the incidence of the
disease is high. For instance, Tirtawadja (1980) reports the destruction of 30 million trees (Graça and
Korsten, 2004). In northern Bali, almost 100% of mandarin trees planted in 1990–1991 were severely
affected in 1996. In India, the disease is widespread (Bové et al., 1993; Varma et al., 1993) with
reported catastrophic losses (Graça, 1991). India revealed that 83–95% of the 25% yield losses in citrus
were associated with D. citri through direct damage or sooty mould fungus (Khan et al., 2014). In the
Pokhara Valley of Nepal, a major mandarin-growing area, trees show HLB symptoms before they are
10 years old. The trees are replaced and the disease reoccurs on new trees. This cycle of replanting
has occurred several times since the disease was introduced from India in the 1960s (Regmi et al.,
1996). In Thailand, HLB has caused severe destruction of citrus since its arrival in the 1960s, with
typical yields low and groves commonly entering decline and becoming unprofitable as early as 5–8
years after planting. The north of the country has been very badly affected and many citrus areas have
gone out of production (Roistacher, 1996).
Losses due to HLB have been more extensively documented in Asia than Africa, however it is estimated
that by the early 1990s more than 60 million trees had been destroyed by the disease globally (Graça
and Korsten, 2004).
29
2.2 Documented impacts of Huanglongbing in East Africa
In East Africa, African citrus greening has caused major yield losses of 25–100% in citrus production,
especially for small-scale producers (Ekesi, 2015; Rasowo et al., 2019). Indeed, citrus greening has
been a persistent constraint to citrus production in Kenya, which has resulted in stagnation in
production and low yields, and allowed imports from other countries such as South Africa and
Tanzania to meet growing domestic demand (Tschirley et al., 2004). For example, in Central province
of Kenya, T. erytreae ranked highest among the foliar pests, causing 65.1% infestation in young and
50.2% infestation in old orchards (Ekesi, 2015).
Accurate estimation of yield losses due to insect pests and diseases in a perennial crop is difficult.
However, HLB disease of citrus in Kenya has been identified as a major limitation (Ministry of
Agriculture, 1982). Indeed, citrus losses in Kenyan orchards due to HLB were reported to be over 75%
in 2012 (Gitahi et al., 2016). Disease management for citrus greening or HLB involves the continual
removal of infected trees since there is no cure or resistance. Affected trees provide considerably
reduced yields due to continuous fruit drop, tree stunting and dieback, in addition to infected fruits
being poor quality and inedible (Bové, 2006; Rasowo et al., 2019). Production costs are also increased
due to fertilizer costs and more frequent insecticide applications, as well as the cost for removing trees
and replanting (Farnsworth et al., 2014). Although chemical control has been recommended in
response to the insect pest problems on citrus (Beige et al., 1984), small-scale farmers often face
financial and other socio-economic constraints to uptake (Kilalo et al., 2009). However, overdependence on chemical pesticides can result in pesticide resistance and is ultimately not
economically feasible, sustainable or environmentally appropriate (Gitahi et al., 2016). Furthermore,
psyllids are persistent vectors of HLB and are throughout their lifetime carriers because of the
transovarial transmission of HLB (Kilalo et al., 2009).
Unfortunately, the significant costs in tackling HLB render commercial citrus production unprofitable,
resulting in curtailed production or in some cases abandoning citrus production altogether (in Kenya)
(Ekesi, 2015; Rwomushana et al., 2017). It has been reported that whole orchards have been lost due
to HLB disease (Kenya Agricultural Research Institute, 1991 - in Kilalo et al., 2009). Indeed, pests and
diseases, including ACT, false codling moth and HLB, have put the smallholder citrus industry in Kenya
in jeopardy, resulting in unemployment and consequently lower living standards and welfare (Gitahi
et al., 2016).
A phased replacement of infected orchards at low altitudes where citrus greening (CLaf) and its vector
(T. erytreae) do not thrive has been recommended (Tschirley et al., 2004). However, the detection of
D. citri in Kenya, Nigeria and Tanzania has serious implications for citrus production in sub-Saharan
Africa (Shimwela et al., 2016; Ajene et al., 2020c; Oke, 2020) and is cause for concern as the psyllid
can spread fast and rapidly adapt to new geographical areas and ecologies (Shimwela et al., 2016;
Rasowo et al., 2019). Although CLaf has caused significant decline and stagnation in citriculture in
Africa the restriction of its vector T. erytreae to high elevations and low temperatures has allowed
some degree of management especially in comparison to CLas- associated HLB (Aubert, 1987; Graça
et al., 2016). The arrival of the vector D. citri, globally considered to be the more damaging due to its
superior ability to vector HLB, in combination with the presence of CLas in Ethiopia and Kenya presents
a serious threat to the future of citrus production and subsequently smallholder livelihoods in East
Africa.
30
2.3 Potential yield loss to Huanglongbing in East Africa
The development of disease within an individual HLB-infected citrus tree, in relation to tree age and
disease load, and the associated impact on yield, fruit quality and long-term tree health is described
in Section 1.5 – “Huanglongbing symptoms and crop damage”. In addition, Section 2.1 gives an
overview of the impacts HLB has had on citrus production worldwide, covering lost production, tree
mortality, tree destruction and associated economic costs. Yield losses in trees infected with HLB can
be variable, influenced by tree age and disease severity and increasing over time. The international
literature can provide insights into HLB-associated citrus yield losses experimentally and at scale, and
of what could be expected with widespread establishment of HLB in Eastern Africa.
In São Paulo, Brazil, Bassanezi et al. (2011) assessed yield loss to HLB for several sweet orange cultivars
in relation to disease severity. It is difficult to establish a quantitative relationship between disease
severity and yield for citrus which displays alternate bearing, with trees tending to bear heavy fruit
crops one year and little or no crop the following year making forecasting difficult, and with
neighbouring plants behaving differently in the same year. Nonetheless, Bassanezi et al. (2011) were
able to demonstrate that a negative exponential model satisfactorily described the relationship
between yield and HLB severity for all varieties of 4–6-year-old trees surveyed in the study. Yield
reduction was observed even at low levels of disease severity, contrary to some earlier studies and a
high correlation between relative yield and number of fruits indicated that most of the reduction in
yield caused by HLB was likely due to early fruit drop or lack of new fruit on diseased branches, rather
than only reduction in fruit weight. In trees with 100% symptomatic canopy a relative yield of 14% to
19% was expected. All cultivars appeared to have a similar tolerance to HLB and a single equation was
proposed to describe the relative yield–HLB severity relationship for the cultivars assessed:
y = exp(- 1.85x) which could be used to predict the economic life of HLB-affected groves in Brazil.
A survey-based study by Singerman and Useche (2016) assessed Florida citrus producers’ estimates of
HLB infection levels and impact on citrus operations. At this time (approximately 10 years after the
arrival of HLB in Florida), the average percentages of HLB-infected acres and HLB-infected trees in a
citrus operation were 90% and 80% respectively. Compared to pre-HLB levels, the average percentage
of yield loss attributed to HLB was 41%. Central Florida was estimated to experience a 12% greater
yield loss than south-west Florida. The study was conducted against a reported backdrop of Florida
citrus acreage and yield reductions of 26% and 42% respectively and a production decrease from 242
million to 104.6 million boxes by 2014. In the words of the authors at the time of reporting there was
“neither a cure nor an economically viable option for managing HLB-infected trees”.
A modelling study by Bassanezi and Bassanezi (2008) assessed the impact of HLB on citrus yield in
relation to tree age when infected (Fig. 12). The model estimated yield impacts of HLB in the absence
of control, accounting for disease incidence progress, disease severity progress and disease severity–
fruit yield relationship according to the age of trees at first symptom onset. Disease incidence and
disease severity progression were assumed to be faster in younger trees than older ones due to more
frequent and intensive flushes in younger trees attracting a higher population of D. citri vectoring HLB
allowing higher infection rates, and a smaller canopy size leading to higher relative severity of initial
symptoms and faster distribution of the pathogen throughout the tree. Using this approach, the
authors estimated that without HLB control measures, São Paulo citrus blocks infected up to 5 years
old would suffer a major reduction in yield within 2 to 4 years after the onset of first symptomatic
31
trees. Older citrus blocks would not suffer major yield reduction for 5 to 10 years after the appearance
of the first symptomatic trees.
A
B
Fig. 12. A) Estimated HLB severity curves (proportion of symptomatic canopy area) as function of tree
age at first symptom onset in trees without any control measures; B) Expected yield curves for healthy
citrus groves in São Paulo compared with HLB-infected groves without any disease control, with first
HLB symptomatic trees detected at 1, 4, 8 and 10 years old (Bassanezi and Bassanezi, 2008).
These results underline the challenge in convincing growers with older infected trees to destroy them
(a matter discussed further below), but also that without HLB control measures it would be extremely
challenging to grow economically sustainable new citrus groves using young trees. An innovative
strategy implemented in China is to retain citrus in nurseries for 2–3 years before planting out in the
field to reduce the attractiveness of the trees to D. citri. Bassanezi and Bassanezi (2008) suggest that
with additional modification informed by improved knowledge of the disease, this model could be
used to generate increasingly accurate and valuable simulations.
The measures implemented to limit citrus yield losses to HLB in Brazil for the benefit of the industry
as a whole have brought about challenging societal issues. The coordinated and enforced preventative
measures against various citrus diseases in Brazil, which included the frequent elimination of trees
and was supported by research institutions and plant protection agencies, facilitated grower
acceptance in the early years of the strict recommendations to control HLB (Bové, 2006). As the
disease spread, growers’ voluntary adherence to and acceptance of the eradication programme and
law enforcement diminished and the elimination of trees became voluntary. In orchards with older,
fruit- bearing trees exhibiting symptoms but which were still productive, their elimination represented
an immediate revenue loss with a consequent faster exit from the business and this caused a
resurgence in the disease. In general, from the first appearance of HLB symptoms in 8- to 12-year-old
orange trees, it can take 4 to 5 years for the yield to decrease by approximately 60%, compared with
non-symptomatic trees (Bassanezi, 2018). Over time, it was evident that elimination, when adopted
alone by a grower located in a region with a high HLB incidence, and/or whose orchard was relatively
small, had little effect on reducing disease progression within an orchard (Bassanezi et al., 2013a,b).
From 2010–2014, Monzo and Stansly (2017) conducted a large-scale experimental study in orange
groves in the south-west Florida citrus-growing area, investigating economic injury levels for D. citri
control in process oranges from mature trees with high HLB incidence. Trees under the most intensive
32
insecticide application regimes harboured fewest D. citri and produced greatest yields, however the
more intensive the application regime, the higher the management costs. The authors were able to
develop treatment thresholds during the growing season as a function of application costs, juice
market prices and D. citri densities. The use of conservative thresholds for mature trees with high HLB
incidence was expected to help maintain economic viability by reducing excessive insecticide
application, leaving room for non-aggressive management approaches such as biological control. For
application at a large scale, with citrus of all ages and varying HLB incidence, however, this thresholdbased management approach would likely have to integrate effective additional measures for younger
trees (Monzo and Stansly, 2017).
The various considerations described above including effective vector management, citrus grove age
profile, encouraged/enforced removal and destruction of diseased plants and associated societal
challenges must all be considered in HLB action plans and in the immediate response to this damaging
disease if yield losses to citrus in Eastern Africa are to be limited.
2.4 Estimates of economic loss due to Huanglongbing in East Africa
The discovery of CLas in Ethiopia and Kenya (Saponari et al., 2010; Ajene et al., 2020a), particularly in
the presence of its increasingly widespread primary vector, D. citri, (Shimwela et al., 2016;
Rwomushana et al. 2017; Rasowo et al., 2019; Ajene, 2020c) is understandably a cause of great
concern for citrus producers in the region; producers already facing significant pest and disease
burdens (Rasowo et al., 2019; Wangithi, 2019). The yield losses to Asian citrus greening once widely
established can be expected to be significant and a potential threat to ongoing citrus production for
resource-poor growers. At this early stage of invasion, however, production losses in citrus due to CLas
in Eastern Africa are likely to be limited and have received minimal analysis in the literature to date.
As infected plants age and symptoms are increasingly expressed, and the disease spreads via its
vector(s) to infect citrus more extensively across the region as is probable, the losses to citriculture
could be hugely damaging. Producers in higher temperature, lowland areas currently spared losses to
the less heat-tolerant African citrus greening disease could now face major losses to the more
damaging and heat-tolerant Asian citrus greening, with the majority of citrus in the region now at
potential risk from one or both of these diseases (Rwomushana et al., 2017; Rasowo et al., 2019).
Reporting from regions of the world with a longer history of CLas invasion such as Asia, South America
and the USA (summarized in Section 2.1) describes a typical sequence of disease progression and
impact, namely rapid disease spread via its primary vector, D. citri, followed by rising yield losses over
time as infected trees become increasingly symptomatic and eventually die, with many trees
intentionally destroyed to prevent further spread. In addition to lost production, costs of vector and
disease management, replanting and production inputs also increase, while fruit quality is reduced.
One country that has broadly avoided this outcome to date is Brazil, the world’s largest citrus producer,
where a “three-pronged system” was rapidly implemented following detection of HLB in São Paulo
State in 2004 (Bové, 2014b). This system involves actively monitoring for HLB, testing and removing
infected trees as mandated by the government (Miranda et al., 2012); replacing removed trees with
healthy trees from nurseries legally required to be covered and insect-proof; and controlling D. citri
through insecticide treatment of all farmed citrus trees (Bové, 2014b). Management is successful
when the percentage of HLB-infected trees on a farm is kept below 1%, therefore, management of
HLB must be implemented as quickly as possible following detection of the disease (Bové, 2014b). This
has not been the case in Eastern Africa. HLB was first detected in Ethiopia in 2009 (Saponari et al.,
33
2010) and has since become more widespread (Ajene et al., 2020d) and is now accompanied by its
primary vector D. citri (Ajene et al., 2020b), making accelerated spread and increased incidence of
citrus infection in the country highly likely. The disease is also now present in Kenya (Ajene et al.,
2020a) close to the border with Tanzania, with the key vector D. citri present and spreading in both
countries (Rwomushana et al., 2017). With an immediate and coordinated response across the region
of the type demonstrated in Brazil, with buy-in from all citrus growers both smallholder and
commercial, there may be a possibility of significantly limiting the spread and impact of HLB in Eastern
Africa over the coming years, however, given the response to date and the presence of the disease
and primary vector in various agroecological settings in multiple countries, a medium-term outcome
closer to that seen in Florida may be more likely and would still require a rapid and extensive response.
In Florida, programmes designed to limit the spread and impact of HLB similar to those used in Brazil
were rolled out, however, not all growers implemented the suggested measures, which were
voluntary and potentially expensive (e.g. destruction of infected citrus trees and coordinated
application of specific insecticides) (Singerman and Rogers, 2020). Further measures that have been
implemented to manage the disease in Florida include the release of biocontrol agents against D. citri
and the establishment of Citrus Health Management Areas (CHMA) to provide regional coordination
of insecticide sprays targeting the psyllid (Alvarez et al., 2016). Analysis of the impacts of HLB in Florida
has been ongoing since the disease was first detected and recognised as a threat to the entire citrus
industry. Citrus production in the state, a major grower of oranges for juice, is frequently reported in
recent literature to have decreased by two thirds or more since 2005 (i.e. ~11–15 years), primarily due
to HLB (Monzo and Stansly, 2017; Singerman et al., 2018; Trejo-Pech et al., 2018; Singerman and
Rogers 2020), following production decreases of around 23% over the first five years with the disease
(Monzo and Stansly, 2017) up to 49% in a decade (HLB plus other factors) (Alvarez et al., 2016). Long
term prospects for Florida citrus based on historical yield trends and without significant innovation
such as resistant (GM) citrus offer a highly pessimistic outlook (Spreen and Zansler, 2016).
Citrus production systems differ between regions, however, to better understand the scale of risk to
Eastern Africa from HLB, it is possible to extrapolate representative levels of loss from other regions
suffering the impacts of this disease. Assuming a fairly rigorous response to the disease in Eastern
Africa, with vector monitoring and management implemented, removal of infected trees and
replanting with certified disease-free stock, but with limitations to coordination and buy-in from
diverse growers including many smallholders, the scale of impacts seen in Florida could be realistic
with ongoing spread of HLB; possibly more so than those under the highly coordinated and rapid
response observed in Brazil, underpinned by legal mandate. Whilst yield losses can vary widely
depending on management at the farm scale and the actions of surrounding citrus growers in addition
to biotic and abiotic factors, regional production losses over a number of years of coexistence with
the disease can give an impression of the potential large-scale, longer-term impacts of HLB to
citriculture and factor in various elements in addition to direct yield loss, such as increased disease
management costs, greater input requirements, lost trade, tree mortality/destruction and
abandonment of production. Additional to lost production will be other important factors such as
increased costs to the consumer, lost employment within the sector, and reduced food security of an
important source of nutrition. In Table 2, production losses of the scale reported in Florida are
extrapolated to Eastern Africa, with near term (5–10 year) and medium-term (10–15 year) annual loss
projections.
34
For Kenya, given the presence of both D. citri and now HLB, without rapid containment measures it
seems likely that citrus will suffer increasing infection and losses in the coming years to this disease,
as has been seen in other parts of the world. Citrus is grown across the country in areas from tropical
to subtropical with key production across a band covering parts of coastal, eastern, central and
western regions of Kenya over a range of altitudes (Richards et al., 2018). Citrus is typically grown in
small orchards and backyards by small scale producers with only a few large plantations in Kenya
(Richards et al., 2018). As a result of ACGD, much of the commercial citrus growing above 800 m.a.s.l.
was abandoned in the 1970s, with active production continuing in the lowlands which remain free of
the disease (Rwomushana et al., 2017). Modelling of environmental suitability for HLB by Ajene et al.
(2020d) which focuses in detail on Eastern Africa and includes recent records of the disease in the
region suggests that the productive western and coastal regions of Kenya show optimum suitability
for the disease, and with D. citri also present in these areas there is a high risk of spread of HLB to
citrus production areas across the central region (HLB and D. citri distribution models are discussed
further in Section 1.7). Additionally, HLB was detected in citrus trees surveyed by Ajene et al. (2020a)
close to sea level on the warm Kenyan coast and thriving in higher altitude, cooler regions of Ethiopia
more than 2,100 m.a.s.l. The primary vector, D. citri was also detected at low altitude sites along the
Kenyan coast and has since been detected at altitudes greater than 2,100 m.a.s.l. in Ethiopia
(Rwomushana et al., 2017; Ajene et al., 2020a). Given the apparent ability of HLB to thrive at a range
of altitudes, along with its primary host D. citri and with potential assisted spread at mid to higher
altitudes by the alternate vector T. erytreae (Ajene et al., 2019; Ajene et al., 2020a), and with
abandonment of commercial citriculture in many high-altitude areas, 90% of production in Kenya is
estimated to be at risk of disease for the purpose of calculating potential citrus production losses to
HLB.
In Ethiopia, HLB was first recorded just over a decade ago, but recent studies have found the pathogen
to be more widespread and affecting citrus in regions distant from the first detections (Saponari et al.,
2010; Ajene et al., 2020a). Modelling by Ajene et al. (2020a) suggests that the majority of citrus
production across key districts in the South Nations, Nationalities and People (SNNP) region, Oromia,
Amhara and Dire Dawa (Dagnew et al., 2014) falls within the area of optimum potential distribution
of HLB. Given the recent detection of D. citri in the country which is expected to accelerate the
proliferation of the disease (Ajene et al., 2020a), the broad potential altitudinal and temperature
tolerances of the bacterium and its primary vector and the potential role of T. erytreae as an additional
vector at higher altitudes, it is expected that citrus production across the country faces a significant
threat from HLB. As for Kenya, 90% of Ethiopian citrus production is estimated to be at risk from HLB
for the purpose of loss calculations.
In Tanzania, D. citri was first reported in 2016 from Morogoro (Shimwela et al., 2016), with subsequent
monitoring revealing an even greater distribution of the psyllid across the key citrus production zones
of east to north-east Tanzania including Morogoro, across the coast region to Dar es Salaam and north
to Tanga and the Kenyan border (Rwomushana et al., 2017). These regions host Tanzania’s commercial
citrus orchards, mostly at altitudes below 600 m.a.s.l., with backyard citrus trees grown throughout
the country at various altitudes (Shimwela et al., 2016). Modelling by Ajene et al. (2020a) suggests
that this important region of citrus production in Tanzania has habitat suitability for HLB ranging from
marginal to optimal, with regions in the north, south and west also suitable to varying degrees. Given
the presence of the vector D. citri throughout the key citrus production areas and the presence of HLB
and D. citri across the border in Kenya, it is highly likely that HLB will soon reach Tanzania and once
35
present has a high chance of spreading quickly, with subsequent impacts on production. As for Kenya
and Ethiopia and given the modelled suitability of key production areas and altitudinal and
temperature tolerance observed in HLB and its primary vector, with further risk of spread through T.
erytreae, 90% of citrus production is estimated to be at risk from HLB for loss calculations.
In Table 2, representative production losses are estimated for a scenario in which HLB is spread via its
primary vector D. citri amongst the Eastern African countries currently at high risk, with both the
vector and disease present (Kenya and Ethiopia) or the vector present and a high risk of the disease
arriving imminently (Tanzania). Potential losses are expressed as annual value of lost production based
on a scale of production loss comparable (although conservative) to that observed in Florida. Upper
and lower bounds of loss are provided for the near-term (5–10 years) and medium term (10–15 years)
at 10–30% and 30–60% of current (recent 5-year average) production levels accordingly. Recent
producer prices (average 2014–2018 where available, otherwise most recent available average from
that range) are used for crop value calculation – citrus prices will likely rise as production decreases
and production costs increase, but the benefit of increased prices to the producer will be a deficit to
the buyer; in addition, the future citrus price is challenging to predict. Citrus production values by
category provided by FAOSTAT vary by country, with some providing a breakdown (e.g. oranges,
lemons and limes etc) but others providing grand totals. Therefore, total citrus production values are
used and producer price of the primary citrus type (typically oranges) is used for calculation. Where
producer price is not available for a country, average price of provided values for other countries
assessed is used.
Time lags before significant loss is expected relate to the potentially asymptomatic latent disease
period typical of HLB. The increased scale of production loss over time relates to increased tree
infection incidence, tree mortality and citrus abandonment, as has been observed in other parts of
the world, particularly in Florida and parts of Asia. Production losses over time are significant, but
lower than multiple reports for Florida described above; this is in an effort to be realistic in loss scale,
but conservative, with rate of disease spread across each country potentially slower than in the highdensity citrus production system in Florida, but with management systems potentially less
coordinated and proactive in mitigating HLB impacts e.g. due to extensive independent smallholder
production with minimal pest control measures applied (Ajene et al., 2020b). Key production regions
with higher density, high quality and possible commercial citrus are likely to be at risk of rapid spread
of HLB via D. citri, with smallholder backyard citrus production a potential ongoing source of disease
even in the case of proactive insecticide use by commercial growers. Climatic variability may also affect
the rate of disease spread and severity, with warm, wet regions at greatest risk (Bové 2014a; Ajene et
al., 2020b).
For Uganda, neither D. citri nor HLB appear yet to be present in the country, despite an earlier report
of HLB presence by Kalyebi et al. (2015) (see Roberts et al., 2017). Significant citrus production is
undertaken in the east of the country (Ajene et al., 2020a), particularly in Teso region, Busoga region
and parts of the central region (Kongai et al., 2018). This mid-altitude (~1,000–1,400 m.a.s.l.) area is
expected to be somewhere between marginal to highly suitable for HLB according to modelling by
Ajene et al. (2020a). Shimwela et al. (2016) suggest only the south-east (primarily Lake Victoria) would
be highly suitable for the primary vector D. citri, however modelling by Narouei-Khandan et al. (2016)
predicts that much of Uganda including the primary citrus growing areas would be suitable for both
D. citri and HLB. In addition, T. erytreae which is present in Uganda could be a potential additional
vector of HLB in the mid to higher-altitude citrus-growing regions should the disease arrive. 90% of
36
citrus production is estimated to be at risk for loss calculations. Citrus production data for Uganda are
scarce and highly variable, with no records on FAOSTAT.
Annual citrus production estimates range widely, for example from 10,000 tonnes nationally (Njoroge
et al., 2009) to 600,000 tonnes in Teso region alone (Dennis, 2013). Kongai et al. (2018) report citrus
production of 200,000 tonnes in 2009, projected to rise to 360,000 by 2011. In 2015, citrus output in
the region was estimated at 769,177 tonnes (Kongai et al., 2018). Unfortunately, the primary
references for these figures could not be sourced, so the lower of these figures (200,000 tonnes) is
used as an estimate for calculating potential losses to Uganda. As neither the primary vector nor
disease are yet present in Uganda, HLB losses may not be apparent for some time (if at all if strict
quarantine and phytosanitary measures can be implemented), however figures are provided to give
an impression of the potential scale of loss to HLB should it arrive, particularly given the presence of
HLB and D. citri in neighbouring Kenya.
The economic value of potential production losses over time to HLB for the East African countries
discussed are detailed in Table 2.
Table 2 – Economic value of potential citrus production losses to HLB under a scenario of extensive
establishment, widespread but poorly coordinated vector management and partial removal of
infected citrus disease reservoir.
Country
Proportion of
national
production at
risk
National
production (tonnes)
(5-year average
2014 to 2018)
Crop value
($/tonne) (average
2014 to 2018
where available)
Lost annual
production value
(1000 $)
Lost annual
production value
(1000 $)
[5–10 years]
[10–15 years]
Lower
Upper
Lower
Upper
Ethiopia
0.9
46,082
298
1,236
3,707
3,707
7,414
Kenya
0.9
216,252
250
4,873
14,618
14,618
29,237
Tanzania
0.9
418,695
272
10,258
30,774
30,774
61,547
Uganda
0.9
200,000
272
4,900
14,700
14,700
29,400
Potential citrus production losses to HLB could be substantial in Eastern Africa, particularly for
Tanzania, with significant additional impacts on employment, trade and nutrition; increased costs of
production and pest management for growers and elevated citrus prices for consumers likely. The loss
scenario described would also rely on a level of response to HLB across its current distribution that
would include imminent action to remove infected citrus and proactively manage its key vector(s),
address the risk of alternative host plants as a disease reservoir and maintain these activities at a
significant level in perpetuity until a silver bullet or very effective IPM approach can be established.
Without immediate, strong actions as outlined in the recommendations section (Section 5, p67),
production losses could be higher still. Immediate, coordinated action, based on a rigorous regional
action plan and informed by the activities carried out in areas of the world that continue to manage
HLB effectively, as in Brazil, could keep production losses to a minimum. This would require a high
level of coordination and buy-in from many stakeholders including countless smallholder producers,
37
with government level oversight and the availability of funds and resources to support the necessary
HLB management activities.
Without sustained high level management or development of novel, highly effective and available
treatment(s), citrus losses to HLB could be expected to grow further beyond the timeframe in the
scenario above, potentially threatening the long-term viability of citriculture in these countries. In
addition, climate change may exacerbate losses to HLB, as detailed by Ajene et al. (2020a).
For each affected country listed above the losses to HLB would be highly significant, with citrus a
growing and valuable commodity in Eastern Africa (Kongai et al., 2018). Losses to major citrus
producers in sub-Saharan Africa could be greater still, given the recent discovery of D. citri in Nigeria
(Oke et al., 2020) and with South Africa also vulnerable, particularly to movement of the psyllid south
from Tanzania through Mozambique. Key citrus production areas of Nigeria appear highly suitable for
HLB, with D. citri also expected to thrive here (Narouei-Khandan et al., 2016; Shimwela et al., 2016;
Ajene et al., 2020a). Important production areas of South Africa are thought to be suitable for HLB
(Narouei-Khandan et al., 2016; Ajene et al., 2020a), with Shimwela et al. (2016) also predicting
suitability of much of this area for D. citri. Narouei-Khandan et al. (2016) suggest some limitation of
westward spread of D. citri in South Africa under their MaxEnt model, but significant overlap with key
production in their SVM model. South Africa has long been preparing for HLB, with extensive direct
experience of African citrus greening and close observation of HLB impacts and management in Asia
and the Americas informing action plans for the country. Preparedness for HLB in Nigeria is less
apparent from the literature, however, the recent arrival of D. citri will no doubt prompt accelerated
planning to protect the citrus industry. Both countries have the opportunity to mitigate losses to HLB
should it arrive and South Africa in particular looks ready to implement measures equivalent to those
seen working effectively in Brazil. To demonstrate the potential impact of HLB if high level control
were not achieved, the production loss scenario described above for Eastern African countries was
applied to South Africa and Nigeria, giving the following production loss estimates:
South Africa (with an estimated 70% of production at risk)
5–10 year lost annual production of $48.7–$146.1 million
10–15 year lost annual production of $146.1–$292.3 million
Nigeria (with an estimated 95% of production at risk)
5–10 year lost annual production of $102.5–$ 307.6 million
10–15 year lost annual production of $307.6–$615.3 million
These figures demonstrate the huge potential impacts of HLB to major citrus producers in sub-Saharan
Africa even under an active management programme and the importance of rigorous, rapid mitigation
measures against HLB and its primary vector as implemented by countries that have successfully
tackled this damaging disease to date. High phytosanitary standards and exclusion measures to
prevent establishment of HLB in each of these countries (and their neighbours) for as long as is feasible
will be of significant importance in limiting impacts on citrus.
2.5 Huanglongbing and trade
The main means of movement and dispersal of the disease is by vector transmission by the African
citrus psyllid, T. erytreae and the Asian citrus psyllid, D. citri. In terms of trade, the risk of spread is
greatest via frequently-traded plant products such as citrus material (budwood, grafted trees,
38
rootstock seedlings) from infected areas which can carry eggs and/or nymphs over longer distances.
Indeed, 5th or 6th-instar nymphs, as well as adults born from these nymphs are capable of transmitting
the greening/HLB agent to citrus. Murraya paniculata, in the Rutaceae family, frequently used as an
ornamental bush or hedge, is one of the best hosts of D. citri and can carry eggs or nymphs of the
vector facilitating its introduction to new regions, and Indian curry leaf tree, Murraya koeniggii, is also
readily exchanged with Asia and can carry eggs and nymphs to unaffected areas (Rwomushana et al.,
2017). However, entry on citrus fruit is extremely unlikely for both species (Batool et al., 2007). Natural
dispersal for both psyllids is likely to be limited to local spread, although Rwomushana et al. (2017)
suggest D. citri can spread considerably from areas in which it is detected (adults can disperse at least
2 km within 12 days and are capable of long distance spread from 90 up to 470 km).
In coastal Kenya there are a wide range of suitable host plants on which CLas can successfully multiply
and be transmissible (Rwomushana et al., 2017). Indeed, increasing regional trade, reservoir host
plants and similar climatic patterns could mean CLas is more widespread than currently documented
in East Africa (Ajene et al., 2020d).
A first point of entry for the vectors likely includes border areas, for instance Rwomushana et al. (2017)
reported D. citri in high numbers in locations bordering Kenya and Tanzania, with a reduction in insects
collected moving inland into Kenya. Much of the long-distance movement of vectors and pathogens
can be accounted for by movement of infected and infested plants (Shimwela et al., 2016). There is a
high phytosanitary risk of introducing Liberibacter-infected citrus into regions where the disease may
not be present but the vector occurs i.e. via infected citrus budwood or trees (Bassanezi et al., 2020).
Regulation of citrus planting materials is urgently needed, for example, in Tanzania, farmers source
orange seedlings/trees from their own backyard nurseries or buy them from other farmers with small
home nurseries; a potential route for disease spread.
Due to the severity of HLB, EPPO recommended the prohibition of importation of citrus plants for
planting and cut branches of citrus from countries where either citrus greening bacterium or either of
its vectors occur (EPPO, 2020). T. erytreae and D. citri are both recommended for regulation as
quarantine pests in the European Union, whereby exporting countries may be required to apply
mandatory phytosanitary procedures, which results in extra cost to exporters and the National Plant
Protection Organizations. At present, none of the bacteria associated with HLB has been found in the
EPPO region, although one of its vectors, T. erytreae, is present in Spain and Portugal (Siverio et al.,
2017; EPPO, 2019).
In the Republic of South Africa, where the citrus export market contributes enormously to job creation
and economic growth, the Department of Agriculture, Agrarian Reform and Rural Development
(DALRRD) has alerted the agricultural community, importers, international travellers, academic
institutions and all citizens about the potential risk facing the country, Southern African developing
countries (SADC) and the entire continent as regards CLas and HLB. The National Plant Protection
Organization of South Africa (NPPOZA), within DALRRD, is already developing an early warning system
and Steering Committee for this pest in collaboration with the citrus industry. This is in line with the
South African Emergency Plant Pest Response Plan. More actors will be addressed in the development
of this strategic plan to ensure that all relevant state bodies are included, as well as research
organizations, commercial, small-scale and subsistence producers (Larkin, 2021).
39
3 Huanglongbing management
Since its emergence in China nearly 100 years ago, a number of management strategies have been
employed in an attempt to mitigate the extensive economic damage caused by HLB worldwide, with
the level of reaction largely a function of the disease’s status on the invasion continuum. The disease
remains widespread in the majority of citrus-producing regions however, and a safe, specific, effective
and sustainable treatment for CLas has yet to be found. Strategies for control have included
insecticides, biocontrol, antimicrobials, cultural techniques and thermotherapy. The lack of
breakthroughs in HLB management, despite the significant investments in research, can be attributed
to the complexities of the system; notably the host’s perennial nature, the lack of resistance in any
citrus relative, the difficulty of breeding to produce HLB-resistant cultivars, the pathogen itself, which
was only recently successfully cultured in pure form (Ha et al., 2019), the complexity of the
vector/bacterium/host interactions and the lack of a good model system have all proved challenging
aspects to a sustainable and effective management strategy.
The disease is not easy to recognize in the field and the symptoms can be confused with other diseases
or with nutrient deficiencies (Huang et al., 1980). A yellowing tree canopy, blotchy mottled leaves and
small irregular fruits with aborted seeds provide the best indications of huanglongbing infection
however accurate diagnosis is key. A diagnostic protocol for CLaf, CLam and CLas and for their
detection in their psyllid vectors D. citri and T. erytreae has been published by EPPO (2014). The
protocol involves detection based on the disease symptoms and molecular tests (PCR) and it is
recognised that sensitive, cost-effective detection of CLas infections in citrus and its psyllid vector form
a vital part of a vigorous HLB management programme. Currently quantitative polymerase chain
reaction (qPCR), along with conventional PCR and DNA sequencing, is used by accredited laboratories
for verifying infection. Diagnostic sampling is a challenge however and this is due to the uneven CLas
spatial and temporal distribution in hosts and vectors, together with the long lag time between
inoculation and bacterial detectability (National Academies of Sciences, Engineering, and Medicine,
2018). The early detection of the bacterium in the vector is also essential and can be done considerably
before the tree exhibits symptoms, since this can take months to years (Lee et al., 2015). Plant
inspectorate agencies are advised to adopt regular use of PCR indexing of samples for HLB, to ensure
citrus germplasm propagation and shipment of clean citrus planting material (Magomere et al., 2009;
Shimwela et al., 2016).
In the US, substantial financial investment has been given to HLB research for over a decade, in hopes
of finding short-, medium-, and long-term solutions; CHMA have been established in Florida, one of
the worst hit areas of production, to promote regional coordination of insecticide applications, but
their effectiveness is hampered, both by intermittent grower participation and by persistence of
vector and pathogen reservoirs in abandoned groves and backyard trees. In these situations, the most
effective control strategy has been to remove infected trees in an area and then replant with CLasfree trees (Abdullah et al., 2009).
Current recommendations are that control of the psyllid vector should be done as soon as its presence
is noticed in citrus groves, even in regions free of HLB (McCollum and Baldwin, 2017). In areas where
HLB incidence is low, mitigation consists of judicious removal of symptomatic trees, intensive
monitoring, chemical and biological control of the insect vector. In Florida, a novel rapid and easy tool
has been developed for early detection of citrus greening disease, which can detect and quantify the
biomolecule limonin, where elevated content is responsible for the bitter taste in citrus fruits (Saraf
40
et al., 2019). Deployment of trained canine teams for detection of CLas in commercial and research
orchards has also been utilised in California, with dogs detecting infections with great accuracy and
discrimination from other pathogens (Gottwald et al., 2020).
With a multi-million-dollar project portfolio, the not-for-profit Citrus Research and Development
Foundation (CRDF) was created to supervise HLB research and development efforts in Florida. This
included a number of strategies such as interrupting the breeding/feeding of psyllids, vector
management, breeding for disease-resistant plants traditionally or through genetic engineering,
control of the HLB inoculum and improvement of the host response. Between 2010 and 2017, CRDF
invested $124 million in 398 citrus projects, 90% of which were focused on HLB. Support for HLB
research has also been provided by the US Department of Agriculture (USDA) and the USDA
Agricultural Research Service (ARS), with more than $450 million directed at citrus disease research
since 2009 (USDA, 2017). The HLB Multi-Agency Coordination Group was established in 2013 to
promote further coordination across federal and state agencies and help provide short term solutions
for citrus growers and this too has awarded some $30 million towards HLB research.
The search for a biotechnological answer to control D. citri has gone beyond transgenic citrus; for
instance, RNA interference has been used to silence genes in D. citri, that can alter wing development
(El-Shesheny et al., 2013; Killiny and Kishk, 2017), increase susceptibility to insecticides (Killiny et al.,
2014; Kishk et al., 2017b), and disrupt sucrose metabolism (Kishk et al., 2017a; Santos-Ortega and
Killiny, 2018). Biotechnological solutions are considered more environmentally friendly than chemical
methods, but some growers and consumers have concerns about transgenic crops. Additionally, many
of these experimental approaches are still primarily confined to laboratory and greenhouse settings.
Prevention measures play a pivotal role, particularly in areas where the disease has not yet wreaked
widespread havoc. Citrus growers in China have pioneered this strategy and are successfully managing
HLB incidence to below 5% over multiple growing seasons, with a three-pronged approach, or “three
axes”, involving the use of disease-free saplings, removal of infested trees and monitoring/control of
vectors. In Brazil, the strategy is much the same, with judicious management of trees and pests
allowing growers to stabilize incidence and effectively halt the disease’s alarming progression.
Whilst the research in the US and other countries has expanded knowledge of every aspect of HLB, a
failsafe management strategy remains elusive. Fighting the epidemic should involve a combination of
approaches rather than reliance on a silver bullet. Ultimately, integrating these approaches into
coordinated, official, national, regional and area-wide action plans and control strategies, involving
growers and citrus/ornamental nurseries and extension workers, should be prioritized before it’s too
late. Action plans aiming to do this have been developed in countries where eradication and/or
containment is still a possibility e.g. in California (Albrecht et al., 2020) and Texas in the US, the
Caribbean and South Africa (CRI).
In East Africa, the need for area-wide action plans has been recognized and a multi-partnered project
“Strengthening Citrus production systems through the introduction of IPM measures for pests and
diseases in Kenya and Tanzania (SCIPM)”, was implemented and culminated in some key broad,
recommendations which will be considered in the final section (S. Faris, ICIPE, pers. comm., 2020).
41
3.1 Chemical control
Worldwide, insecticides have formed a key component of ACP management and when both disease
and vector are present, the use of pesticides has often been favoured (Graça and Korsten, 2004).
Chemical control is invariably costly however and Boina and Bloomquist (2015) estimated annual costs
per hectare of ACP management in citrus to be in the range of $240 to >$1000, depending on the type
of insecticide used, application frequency and method of application.
The following section provides a summary of the historical literature on chemical control of HLB
vectors and many pesticides are either no longer recommended or indeed no longer in use.
Nearly every pesticide available for insect control has been tested against citrus psyllids in Florida
(reviewed in Grafton-Cardwell et al., 2013; Qureshi et al., 2014; Boina and Bloomquist, 2015) and
largely consisted of foliar applications of broad-spectrum insecticides and reduced-risk insecticides, as
well as soil or trunk applications of systemic insecticides. Psyllid behaviour, population size and life
stage at the time of acquisition influence pesticide effectiveness (Pelz-Stelinski et al., 2010) and
psyllids infected with CLas were found to be more susceptible to at least five commonly-applied
pesticides than those that were not infected (Tiwari et al., 2011).
However, by virtue of its high fecundity and short generation times, D. citri can respond rapidly to
selection pressures and consequently growers’ reliance on the most effective pesticides, applied more
frequently and at higher rate, has selected for resistance (Qureshi et al., 2014). Some degree of
resistance to key insecticides (organophosphates, carbamates and neonicotinoids) has already been
documented in ACP populations in Florida (Tiwari et al., 2011; Tiwari et al., 2012) and so judicious and
rotational application (with different modes of action) was recommended, contingent on actual pest
populations and individual or regional assessment of all factors.
As for many cropping systems, there is no universal spray regime to fit every grower. As well as
restriction to nationally-registered pesticides, overall cost, efficacy, conservation of beneficial insects
and resistance management will all serve to influence the spraying programme. Timing of applications
has also been found to be critical for population reduction. New flushes of foliage regulate the
dynamics of several citrus pests requiring soft tissues for oviposition and development including D.
citri and because young trees flush more frequently than mature trees, these need more protection
(Qureshi et al., 2014).
Insecticide applications (foliar or soil-applied) in newly-planted or well-established groves was found
to significantly delay or lower the incidence and spread of HLB compared with untreated groves.
Moreover, a significant reduction in disease spread was observed when the applications were made
with an effective insecticide, at a frequency of ≥2 applications per year soon after the incidence of the
disease (Chiyaka et al., 2012).
In Florida, systemic neonicotinoid insecticides, such as thiamethoxam (WHO Class II), imidacloprid
(WHO Class II), clothianidin (WHO Class II) and chlorantraniliprole (WHO Class U) were used in citrus
but their use as soil applications to young trees was rate restricted (Qureshi et al., 2011). Sprays of
broad-spectrum insecticides prior to flushing were proven an effective strategy for reducing
populations of ACP in Florida, particularly when overwintering adults were targeted (Qureshi and
Stansly, 2010). Qureshi et al. (2014) investigated 23 products including cyantraniliprole (WHO U),
flupyradifurone (WHO II) and sulfoxaflor (WHO II) and found that they provided more than 90%
reduction in psyllid populations. With a few exceptions, most foliar sprays were found to suppress
42
adults longer than nymphs and direct effects on nymphs are measurable for only the 2–3 weeks it
takes for new shoots to harden and for nymphs to mature to adulthood (Qureshi et al., 2014). Most
young nymphs are protected inside the newly-developing unfolded leaves where ACPs oviposit,
therefore some avoid contact with insecticide sprays. Consequently, insecticides that leave persistent
residues are needed to control nymphs as they emerge from eggs tucked within foliage and to protect
trees from incursions of ACP adults. Residual control by foliar insecticides was found to be longer
lasting with pyrethroids and thiamethoxam (WHO II) and shortest for insecticides approved for organic
production (Qureshi and Stansly, 2020).
These residual populations along with surviving adults are usually enough to initiate a new generation
and consequently required follow up treatment (Qureshi et al., 2014). Monitoring the onset and
duration of flush periods, together with visual inspection of the flush and trapping to monitor for
nymphs and adults, is thought to facilitate timely intervention with insecticide applications and
reduction of ACP populations (Boina and Bloomquist, 2015).
Historically in Asia, a range of insecticides, mostly organophosphates and pyrethroids, have been used
in very intensive spray programmes to kill nymphs and eggs of the HLB vector on flush growth. In
Southeast Asia, control has not been achieved with as many as 35–52 applications of synthetic
pesticides a year. These sprays often comprised four or more active ingredients (many of which were
highly toxic and illegal). In China, an estimated 10–13 sprays per year were required during flush
periods to rehabilitate citrus production in an HLB-infected area (Roistacher, 1996). D. citri was
controlled at the time using systemic insecticides like dimethoate (WHO II) and other highly toxic
pesticides which are banned or heavily restricted by international agreement today (Graça, 1991). In
Jiangxi Province in China, protecting the city’s $1.5 billion navel orange industry relies on helicopters
spraying broad-spectrum insecticides to keep the psyllids in check.
Synchronization of application with or prior to flushing plays an important role, as does the use of
sticky cards to monitor D. citri in order to time control action (Aubert and Hua, 1990). The timely and
appropriate use of insecticides achieved good control of T. erytreae in South Africa (Graça, 1991). In
Florida, young trees were found to be best protected with soil drenches and trunk injections with
neonicotinoids and cyantraniliprole (WHO U) in rotation (Stansly et al., 2012) and thus served as a
rotation partner to slow the evolution of insecticide resistance in ACP. However, these soil applications
were generally supplemented with foliar applications of broad-spectrum insecticides (Boina and
Bloomquist, 2015).
In Brazil’s commercial orchards, to prevent secondary infections from diseased trees within an orchard,
and primary infections by psyllids from outside the orchard, psyllid control was conducted at biweekly
intervals (shorter than the egg-to-adult lifecycle of ACP). Additionally, more frequent insecticide
sprays were advocated from bud development to leaf maturity (Cifuentes-Arenas et al., 2018) in
flushing young trees, freshly pruned or irrigated trees with induced flushing (Hall et al., 2016;
Cifuentes-Arenas et al., 2018). Ultimately, in Brazilian commercial orchards, psyllid control is
contingent on tree age, vegetative stage and block position. For nursery trees, drench application of
systemic insecticides 1 to 5 days before planting has been recommended. For young trees (up to three
years old), three to four applications per year of systemic insecticides by drench or trunk was
recommended during the shooting period, plus foliar applications at intervals of 7 to 14 days. For
mature trees (> 3 years old), foliar applications at intervals of 7 to 28 days were recommended (more
frequently during the shooting period and in blocks at the edge of the farm) (Miranda et al., 2017).
43
Reduced-risk insecticides with novel chemistries and modes of action could be a promising rotational
tool in insecticide resistance management programmes for ACP (Boina and Bloomquist, 2015). Lab
studies have shown that the IGRs, pyriproxyfen (juvenile hormone mimic) (WHO Class U) and the
slightly hazardous buprofezin (WHO Class III) and diflubenzuron (WHO Class III) (both chitin synthesis
inhibitors), have promising ovicidal and nymphicidal activities against ACP, as well as adverse effects
on reproduction (both fecundity and egg viability) and morphology of adults emerging from treated
older nymphs. Controlling nymphs is as important as controlling adults, because pathogen
transmission efficiency of infected adults was found to be greater when they acquire the pathogen as
nymphs rather than as adults (Tiwari et al., 2012).
Qureshi et al. (2014) found that the application of insecticides with horticultural mineral oil (HMO) as
adjuvant generally improved their efficacy against ACP in Florida.
A baseline survey of farmers in major citrus-producing counties of Kenya by Gitahi et al. (2019)
highlighted the lack of knowledge on alternative pest management practices other than pesticides. A
study by Constantine et al. (2020) also confirmed the low use of biopesticide products in Kenya,
alongside high use of conventional chemical pesticides. In Africa, most farmers depend solely on the
use of synthetic pesticides to minimize damage and output losses due to the citrus greening pest
complex. In the absence of alternative pest management strategies, farmers resort to widespread and
unguided use of pesticides, spraying frequently and mixing various pesticide brands in an attempt to
make them more effective (Muriithi et al., 2016) which is not only expensive, but also often highly
toxic with serious negative effects on people and environment. The majority of citrus growers in
Machakos and Makueni reported use of synthetic pesticides (91%) (Gitahi et al., 2019). Some of the
pesticides used are listed as persistent organic pollutants (POPs), leading to rejection of produce in
any export markets. In addition, fruit quality is negatively impacted by heavy use of pesticides and the
associated depletion of enemies can result in serious outbreaks of minor pests such as citrus red mite,
Panonychus citri. Furthermore, many farmers base their application of pesticide on the observable
damage caused by pests and in the case of HLB, this means the disease can take hold.
In Uganda, dimethoate (Rogor, Perfekthion, Roxion) (WHO Class II) had been recommended for use in
citrus (NAADS, 2020). In Kenya, fully registered products for use in citrus include buprofezin (WHO III),
bifenthrin (WHO II), imidacloprid (WHO II), carbaryl (WHO II) and diazinon (WHO II) (PCPB, 2018).
While insecticidal control of HLB pests has been shown to significantly increase production, the
collateral impact on environmental and public health, side-effects to beneficial arthropod fauna of
citrus agroecosystems, risks of resistance and relative costs of insecticide applications compared to
the value of the crop make it important to seek and integrate other optimal management options
(Monzo and Stansly, 2017). Farmers rely heavily on advice about what products to use, therefore
raising awareness and knowledge of those providing advice is essential, as well as understanding
farmer’s perceptions of alternative controls.
3.2 Antimicrobial control
The search for a novel treatment for citrus greening has, to date, relied heavily on modern molecular
techniques with a limited number of new chemicals being tested in commercial groves. A number of
publications described the use of different compounds against citrus greening disease, including
classic antibiotics that are frequently used to treat bacterial infections in animals and humans (Zhang
et al., 2014; Hu et al., 2017). Antibiotics have long been used in several agricultural practices and in
44
citrus, the use of trunk-injected or budwood/root-soaked antibiotics has received considerable
interest, although it is highly labour intensive. Both methods offered temporary relief of HLB
symptoms (1–1.5 years) and in Taiwan, China, Reunion, the Philippines, South Africa and India, trunk
injections provided the best results (Graça and Korsten, 2004). Injection of tetracycline into the trunk
of affected sweet orange trees in South Africa has resulted in at least partial recovery of the trees. In
2016, the antibiotics streptomycin sulfate, oxytetracycline hydrochloride and oxytetracycline calcium
complex were approved for emergency field use in foliar sprays to treat HLB in Florida but after two
years the results were inconclusive (Blaustein et al., 2017). Populations of residual bacteria that
survived the treatment have also been reported to regrow over time (Hu and Wang, 2016). Thus, longterm use of antibiotics may be needed to control HLB, which leads to problems with operational costs
and potential adverse environmental effects (Blaustein et al., 2017). Phytotoxicity is also well
documented in the literature, when tetracycline and oxytetracycline are applied at the concentrations
needed for efficacy against CLas. In Indonesia, a nation-wide, large-scale tetracycline injection
programme failed to give control. Additionally, most antibiotics are temperature sensitive and their
efficiency is largely reduced in hot weather. Overall, public concerns about emergence of antibioticresistant bacteria and potential side effects on humans are curtailing the use of antibiotics in
agriculture and the environment, although all the low- to middle-income WHO regions of the world
continue to recommend their use on crop plants (with the exception of Africa) (Taylor and Reeder,
2020).
The race to find a non-antibiotic chemical compound against CLas bacterium, which have little to no
negative effects on humans is ongoing. Several effective and partially effective non-antibiotic
antimicrobial compounds including metals and natural products have been identified and the
developments in pure culturing of CLas are opening the door to the use of genetics-based methods to
understand and mitigate the spread of HLB. A recent discovery of a novel class of heat-stable
antimicrobial peptides (SAMPs) which effectively kills the HLB-causing bacterium has been developed
from greening-tolerant Australian finger lime and other wild citrus relatives (Huang et al., 2021). This
natural plant product is reportedly safe to humans, systemic and long lasting and will be further
enhanced with proprietary injection technology. Innovative research such as this is needed if an
effective, environmentally-friendly treatment is to be found to help with the fight against D. citri and
HLB.
3.3 Botanicals and organic management
The persistent use of broad spectrum, synthetic pesticides in HLB management has led to resistance
in citrus psyllids (Tiwari et al., 2011) and increased the need for judicious and reduced use of hard
chemistry insecticides. Alternative, less environmentally-toxic products such as botanicals have been
found to be less harmful to some beneficial insects, including coccinellids and spiders (Walter, 1999;
Tang et al., 2002) and may have potential for IPM, particularly in habitats where conventional
insecticides are not allowed or appropriate such as organic citrus and urban areas.
Petroleum-derived spray oils have been used to control susceptible phytophagous pests and diseases
of plants for over a century (Agnello, 2002). These highly refined products are classified as horticultural
mineral oils (HMOs) and agricultural mineral oils (AMOs) (Kuhlmann and Jacques, 2002) and are able
to kill the insect pests by disturbing their respiratory systems (Liu and Stansly, 1995). These mineral
oils offer an economically-attractive and environmentally-safe pest management option which can, in
many cases, be accepted for organic production (Stansly and Conner, 2004). Oils have the additional
45
effect of repelling adults from new flush, thereby reducing oviposition and deposits of emulsified HMO
on foliage also reduce landing rates, feeding and reproduction on citrus (Ouyang et al., 2013). Studies
have indicated that effectivity of HMOs is enhanced when combined with improved canopy
management (pruning) (Khalid et al., 2012) and should coincide with critical stages in order to ensure
efficient suppression of insect population (Rae et al., 1997). Importantly, these HMOs were found to
have no phytotoxicity if used in low enough concentrations (Rae et al., 1997) although use of heavy
mineral oils was more likely to have deleterious impacts on trees. Growers in organic groves rely
mostly on spray oils and botanicals derived from neem and pyrethrum, surfactants, insecticidal soaps
and kaolin spray (Qureshi and Stansly, 2020).
Other groups of reduced-risk insecticides that hold potential are botanical insecticides such as neembased formulations, sucrose octanoate and organosilicone spray adjuvants (Boina and Bloomquist,
2015). All these are effective against nymphs. Insecticides approved for use in organic orchards such
as the mineral oils and even bacterial culture or extracts such as Chromobacterium subtsugae
(Grandevo) (Qureshi et al., 2013), whilst capable of comparable levels of suppression to their synthetic
alternatives, tend to be short lived. Nonetheless, these are thought to have some use in rotation
applications, to reduce selection for insecticide resistance in psyllids, conserve natural enemies, and
for application on blooming citrus for which few synthetic products are allowed, and in organic groves
that prohibit synthetic products (Qureshi et al., 2013). Frequent applications of such insecticides
during the growing season have been suggested as being compatible with biological control.
Another promising natural management opportunity could come from the use of volatile chemicals
released by plants which not only repel herbivores (Pickett et al., 1992; Agrawal and Karban, 1999)
but potentially deter their feeding (Jackson et al., 1996; Dugravot et al., 2003). Interplanting guava,
Psidium guajava L. with citrus has been reported to reduce populations of D. citri and this has been
linked to the repellent properties of guava volatiles containing toxic metabolites (Beattie et al., 2006;
Hall et al., 2008; Zaka et al., 2010). Guava leaves are known to lower attraction of D. citri to orange
leaf volatiles (Zaka et al., 2010) Additionally, the sulphur compound, dimethyl disulphide (DMDS),
produced by guava in response to mechanical foliar injury (Rouseff et al., 2008) has been found to
confer protection to citrus foliage by impacting on behavioural activity. Application of DMDS in
formulation (Qureshi and Stansly, 2020) appeared to cause existing D. citri populations to disperse
from treated trees and delay ingress into plots. Citrus host plants of D. citri did not produce this
compound even after mechanical wounding (Rouseff et al., 2008). Balandrin et al. (1988) found a
range of sulphur compounds including di-n-propyl disulphide in neem seeds (Azadirachta indica). The
Azadirachtin based biopesticide (Azamax™ EC) was also found to be effective against D. citri nymphs
(Silva Santos et al., 2015).
Terpenes found in guava but not citrus also have been reported to have repellent properties (Qureshi
and Stansly, 2020) and Alquézar et al. (2017) hint at encouraging genetic engineering approaches to
modify citrus to emit these naturally repellent chemicals, as was achieved with Arabidopsis plants
(Brassicaceae).
Other botanicals and essential oils identified as repellent include crushed garlic chive oil/leaves/plants
(Allium tuberosum) (Mann et al., 2011), as well as tea tree, thyme, rose and lavender oils, with some
also reducing attraction to citrus leaves (Mann et al., 2012). Fir oil has also exhibited promise for
reducing D. citri in small field plots (Kuhns et al., 2016). The plant volatile, methyl salicylate, has also
been shown to disrupt or confuse D. citri (Martini et al., 2016) but has potential to also disrupt
46
parasitoid cues for host detection and therefore use in moderation is suggested (Rodriguez-Saona et
al., 2011). The use of lures using host plant volatiles may hold promise if they can be optimized to
enhance visual surveillance or be integrated in an attract-and-kill strategy whilst drawing psyllids away
from target hosts (Qureshi and Stansly, 2020).
In Florida, HLB management strategies also focus on actions to support and prolong tree health and
fruit production in infected trees (National Research Council, 2010). Peer-reviewed literature on these
practices is scant, but they are based on the premise that stressed trees are more vulnerable to HLB.
Through Enhanced Foliar Nutritional Programs, mixtures of readily absorbable foliar nutrients and
phytohormones are applied as sprays and aim to compensate for nutrient losses caused by the
blockage of conducting tissues in diseased trees. Anecdotal reports of increased yields and improved
health of trees have been reported by growers (Muraro, 2012) but researchers have raised concerns
that reducing or ceasing efforts to control the ACP in favour of nurturing infected trees places the two
management approaches in conflict with one another (Gottwald et al., 2012) and critically could
potentially lead to the proliferation of the disease as the inoculum remains in the trees. Ultimately
and despite the potential for short-term tree health improvement and reduced HLB impacts on fruit
yield, these costly approaches are not curative nor sustainable (Rouse et al., 2017).
As well as enhanced nutrition by foliar sprays, regulation of soil pH to enhance nutrient uptake, and
precision irrigation based on soil moisture sensing and needs of HLB-affected trees approaches have
also been adopted in sophisticated, multifaceted approaches to water and nutrient supplementation
in high-intensity production systems (Roka et al., 2009; Zheng et al., 2018).
Compounds perceived to activate systemic acquired resistance pathways in plants (such as salicylic
acid) to increase tree defence responses have also been used (Masuoka et al., 2011; Baldwin et al.,
2012). Plant growth regulators have also been tested, unsuccessfully, to reduce HLB-associated fruit
drop (Albrigo and Stover, 2015).
Tomaseto et al. (2019) also reported that the use of trap crops on the border of citrus orchards, such
as orange jasmine (Murraya paniculata), treated with insecticides to attract and kill D. citri before
settling, could prove an effective strategy if implemented close to citrus tree planting. Further
integration with other tactics (e.g. kaolin), as a push-and-pull strategy, could further decrease
infestation rates inside citrus orchards.
Gitahi et al. (2019) found citrus farmers from Machakos and Makueni counties in Kenya used
intercropping (1.2%), plant-based pesticides (6%) and irrigation (4%) practices to manage citrus pests.
Other methods to prevent psyllids from settling or feeding on leaves have also been investigated.
Products formulated with kaolin clay have been shown to reduce adult and psyllid numbers on flush,
disrupting plant-finding ability and dispersal (Miranda et al., 2018).
3.4 Resistant varieties
HLB’s intractability is in part due to the lack of natural resistance in any citrus relative and the difficulty
of breeding to produce HLB-resistant cultivars (Bové, 2006; Graça et al., 2016; Miles et al., 2017). It is
also thought that the association between Citrus and liberibacters is a recent one and as such, too
short for the trees to have built up resistance to the bacterium (National Research Council, 2010). R&D
efforts in the US have focused on conventional resistance breeding programmes of new rootstock and
scion varieties to provide resistance/tolerance to CLas, whilst also funding projects into genetically
47
engineered (GE) resistance (National Academies of Sciences, Engineering, and Medicine, 2018). The
genetic complexity of the Citrus genus results in high levels of heterozygosity, and consequently many
generations of breeding and selection are required to develop new cultivars which possess the
combinations of genes required for the commercial fresh or processing markets (e.g. fruit and juice
quality, productivity, biotic and abiotic stress resistance traits) (National Academies of Sciences,
Engineering, and Medicine, 2018). Furthermore, seed-borne breeding programmes are challenged by
the 3–7 years of tree juvenility, along with the large areas of land required to grow and evaluate trees.
While a great deal of breeding has been carried out in the United States and other major citrusgrowing areas, most of the commercial cultivars currently grown were selected in the 19th century
(National Academies of Sciences, Engineering, and Medicine, 2018). Genetic improvement through
engineering allows some of these challenges to be bypassed, targeting improvement of existing
cultivars, avoiding random assortment of genes and the loss of existing genetic integrity from the
desired cultivar. Traditionally, citrus cultivars are propagated vegetatively by grafting to maintain the
integrity of the desired cultivar. Rootstocks are selected for disease and nematode resistance, soil
adaptation, resistance to flooding and drought, cold hardiness, and effects on tree size (Castle et al.,
2016).
Whilst there are currently no commercial citrus cultivars, varieties or scion-rootstock grafting
combinations with innate resistance to CLas infection (Graça et al., 2016) some commercial varieties
such as lemon [C. limon (L.) Burm. F.] and Persian lime (Citrus latifolia), along with US-897 rootstock
(Citrus reticulata Blanco × Poncirus trifoliata L. Raf.) and the “LB8-9” Sugar Belle® mandarin hybrid (SB;
“Clementine” mandarin × “Minneola” tangelo) (Gmitter et al., 2010) show apparent HLB tolerance
under natural HLB-endemic conditions in Florida (Deng et al., 2019), whilst SB mandarin and “Bearss”
lemon trees also maintain vigorous growth and fruit yield compared to many sensitive sibling
mandarin cultivars; HLB-tolerant citrus relatives also include Australian finger lime (Microcitrus
australasica), Australian desert lime (Eremocitrus glauca), Hawaiian mock orange (M. paniculata) and
Khasi papeda (Citrus latipes) (Huang et al., 2021). Orange, mandarin and lemon represent three
different kinds of citrus from the taxonomic point of view (Wu et al., 2014). Despite representing
genetically diverse citrus species, Deng et al. (2019) report evidence of shared anatomical responses
underlying HLB-tolerance in “Bearss” lemon and LB8-9 Sugar Belle® mandarin; decreased phloem
destruction and increased replacement phloem generation was found in field grown trees naturally
exposed to HLB and this anatomical insight provides some potential for incorporation into breeding
programmes to bridge production as well as develop new approaches to combat HLB in the future.
Genetic engineering can potentially circumvent some of the challenges inherent in citrus breeding
programmes and research into gene editing and silencing of bacterial proteins and insect salivary
effectors, which contribute to the disease spread may hold valuable potential. Complete control of
HLB may not be feasible until plants expressing high levels of resistance to the vector and/or disease
are available or can be bred or engineered.
3.5 Biological control
Indigenous generalist predators have always been an important component of citrus insect pest
management (McCoy, 1985). In Florida and California, ladybirds (Coleoptera: Coccinellidae), syrphid
flies (Diptera: Syrphidae), lacewings (Neuroptera: Chrysopidae), and predatory mites (Acari) (Michaud,
2004; Michaud and Olsen, 2004; Qureshi and Stansly, 2007; Juan-Blasco et al., 2012; Kistner et al.,
48
2016b) are all common predators of citrus psyllids and have been found to play a vital role in regulating
populations of D. citri (Berg et al., 1992; Qureshi and Stansly, 2009). The extent of control provided by
each individual taxon remains largely unknown, though coccinellids seem to provide the most ACP
control in Florida (Michaud, 2004; Qureshi and Stansly, 2007), whereas in California, syrphid
(Allograpta species) and lacewing (Chrysoperla species) larvae feeding on ACP nymphs have a
collective predation rate inflicting 86% mortality (Kistner et al., 2016b). Work from Pakistan indicates
spiders are not important ACP predators in unsprayed citrus orchards (Vetter et al., 2013).
In their native range, among the most effective natural enemies of HLB vectors are Hymenopteran
parasitoids from the genus Tamarixia (Hoddle and Pandey, 2014). The complex of parasitoids was
comprehensively studied in the 1960s–1970s in South Africa and Swaziland and subsequently in
Cameroon some 30 years later (Tamesse and Messi, 2002; Pérez-Rodríguez et al., 2019). In areas
where insecticides are not sprayed in South Africa, such as abandoned or experimental orchards and
gardens, parasitoids were found to be important biotic regulators of T. erytreae. The two main primary
parasitoids of T. erytreae in South Africa are the ectoparasitoid Tamarixia dryi (Waterston)
(Hymenoptera: Eulophidae) and the endoparasitoid Psyllaephagus pulvinatus (Waterston)
(Hymenoptera: Encyrtidae) (Pérez-Rodríguez et al., 2019). Both are solitary koinobiont parasitoids (in
other words they parasitize earlier host stages and allow host activity to continue feeding and growing
during parasitism). A third, new parasitoid species from the genus Tamarixia was also recorded by
Pérez-Rodríguez et al. (2019) in South Africa. These primary parasitoids are themselves frequently
attacked by a complex of hyperparasitoids which significantly reduce their impact (Berg and Greenland,
2000). Aphidencyrtus cassatus is considered the most abundant (Aubert, 1987). Growers in Florida
have released the convergent ladybird Hippodamia convergens Guérin-Méneville from California;
however, it is still not common there in citrus (Qureshi and Stansly, 2011).
The parasitoid T. dryi was successfully used as a classical biological agent against T. erytreae in the
islands of La Réunion and Mauritius (Etienne and Aubert, 1980; Aubert and Quilici, 1988). In these
islands, both HLB psyllid vectors T. erytreae and D. citri coexisted, as well as CLas and Claf but only the
control of T. erytreae by T. dryi was successful (Pérez-Rodríguez et al., 2019). Almost complete
elimination of HLB was achieved in Réunion through a combination of biocontrol (taking care not to
introduce hyperparasites in the process), removal of infected trees and replanting with bacteria-free
material. The lack of success controlling D. citri is linked to a number of factors, including size of
population, availability of alternate host plant for D. citri and host psyllid for T. dryi, as well as climate
suitability (Halbert and Manjunath, 2004).
Two parasitoids from the Indian subcontinent, the endoparasitoid Diaphorencyrtis aligarhensis
(Shafee, Alam and Agaral) (Encyrtidae) and the ectoparasitoid Tamarixia radiata (Waterston)
(Eulophidae) have also been used for classical biocontrol of D. citri. Both kill their hosts through a
combination of parasitism and host feeding (Rohrig et al., 2011). D. aligarhensis attacks second
through fourth ACP instars (Skelley and Hoy, 2004; Rohrig et al., 2011) and a single female can kill up
to 280 nymphs in her lifetime (Chien et al., 1995). T. radiata is an efficient idiobiont (lives outside the
host whilst preventing development) of ACP nymphs, inflicting mortality of >90% of presented nymphs
(Skelley and Hoy, 2004) and a single female can kill up to 500 nymphs in her lifetime (Chien et al.,
1995).
These two parasitoids have been released in Mauritius, Réunion Island, and Florida and California (US)
(Michaud, 2002; Hoddle, 2012). T. radiata was also released in Taiwan and Guadeloupe. Dramatic
49
success was achieved by T. radiata in Réunion Island and Guadeloupe (Hall, 2008). In Florida, T. radiata
established successfully but control was variable, with reduction in psyllid populations ranging from 4
to 70% and impact limited by local predators (Michaud, 2004) or significant levels of parasitism (20–
56%) (Qureshi et al., 2009). In California, T. radiata established (Hoddle, 2012), and, acting with local
generalist predators, it reduced the net reproductive rate of D. citri by 55–95% (Kistner et al., 2016a).
D. aligarhensis has been recovered in California (as of 2017) in the majority of release sites, with
parasitism ranging from 0.2–34.5% but it failed to establish in Florida. More time is needed to evaluate
the impact of the parasitoid on pest populations in California. T. radiata and its psyllid host have also
been inadvertently introduced into Texas, Puerto Rico, Venezuela, and possibly other areas, most
likely through the movement of infested host plant material from where they were previously
associated.
In Florida, generalist predators such as coccinellids can cause >95% mortality of ACP parasitized by T.
radiata (Michaud, 2004) and this can cause parasitism estimates in the field to be underestimated
(Michaud, 2004; Qureshi and Stansly, 2009). In California, invasive ants such as Linepithema humile
(Mayr) (Hymenoptera: Formicidae) which form mutualisms with honeydew producing Hemiptera such
as ACP, provide active defence from predators and parasitoids, and can considerably reduce the
efficacy of biological control agents in citrus orchards (Vega and Rust, 2001). Whilst undeniably useful
in minimizing immigration into commercial orchards from urban trees (backyard citrus) and
abandoned groves, the level of control offered by indigenous and imported natural enemies is not
adequate as a stand-alone practice in commercial orchards because of ingress of psyllids from
abandoned orchards (Lewis-Rosenblum et al., 2015). Although the combined effects of these natural
enemies have failed to curb the spread of HLB in Florida, conservation of these and other beneficial
arthropods is essential for effective citrus pest management in other parts of the US and elsewhere.
Diniz et al. (2020) reported that the release of parasitoids in areas outside the managed groves, such
as abandoned orchards or residential trees, has the potential to maximize actions for D. citri control,
contributing to the reduction of psyllid ingress into commercial areas.
The rotational pesticide application patterns of many commercial citrus groves, while critical to
mitigate against resistance development by the psyllid, will be detrimental to any potential benefits
biocontrol agents confer. Additionally, the parasitoid T. radiata attacks nymphs (Skelley and Hoy,
2004), but trees can become infected by adult feeding well before any subsequent nymphs develop
to an acceptable stage for parasitoid oviposition. As a result, the primary long-term benefit of psyllid
suppression by T. radiata in commercial orchards would be to reduce the production of infected adults
developing from nymphs; whilst this has benefits, a reduced adult population would not eliminate the
loss of the infected trees or the eventual spread of the pathogen. Garcia et al. (2019) have developed
an adaptable computational index to identify suitable areas for biocontrol and successfully tested the
D. citri – T. radiata system using Brazil as an example. Field data indicated that this index is reliable for
mapping “suitable” regions that can potentially support biological control programmes.
Entomopathogenic fungi used as biopesticides may also play an important role for regulation of ACP
and provide an eco-friendly management strategy for the integrated management of D. citri but the
use of insect pathogenic fungal sprays to control psyllids has not been reported (Hall, 2008). The
entomopathogenic fungi Cladosporium sp. nr. oxysporum and Capnodium citri have been considered
important mortality factors for D. citri in Réunion Island (Aubert, 1987). Nymphal mortality rates of
60–70% occurred where minimum daily relative humidity exceeded about 88% (Aubert, 1987). The
fungus Hirsutella citriformis was reported to be common in Guadeloupe during periods when humidity
50
was greater than 80% (Étienne et al., 2001). In Florida, dead D. citri adults infected by H. citriformis
(Meyer et al., 2007) have been observed from mid-summer through winter, mainly in larger trees (Hall
et al., 2008) whose microhabitat the fungus may favour. The fungus Isaria fumosorosea (Hypocreales:
Cordycipitaceae) has been reported to kill D. citri in Florida (Meyer et al., 2008).
Virulent fungal strains of Cordyceps fumosorosea (syn. Isaria fumosorosea), Beauveria bassiana and
Metarhizium anisopliae have been assessed in laboratory and field conditions (Majeed et al., 2017;
Saldarriaga et al., 2017), the first two achieving high adult mortality, particularly with high relative
humidity and rainfall. Ibarra-Cortes et al. (2018) ascertained the fatality rate of C. fumosorosea, B.
bassiana and M. anisopliae to be 28%, 55%, and 43%, respectively, to D. citri adults, and 47%, 69%,
and 100%, respectively, to the nymphs when applying spore suspensions of the individual fungi under
laboratory conditions. A study by Avery et al. (2011) documented that adult psyllids infected by I.
fumosorosea have reduced feeding, which could potentially reduce the spread of huanglongbing.
Glasshouse experiments with a new strain of entomopathogenic fungus, Cordyceps javanica have also
shown potential to have high infection rates (Ou, 2018).
Bacterial-based biocontrol is another eco-friendly control method generally compatible with organic
production. Citrus-inhabiting bacteria with antimicrobial properties have been assessed (Riera et al.,
2017) and found to slow the disease progression but only if applications were made during very early
infection. Beneficial microbes may suppress infection and slow symptom development by triggering
host plant defence responses (Wang et al., 2017). Because biocontrol efforts can be hampered by low
microbial survival, several candidate beneficial bacteria are being analysed for antimicrobial
compounds that could be extracted for concentrated application (Wang et al., 2017).
The potential efficacy of entomopathogens will include ambient air temperatures and relative
humidity within the citrus grove, air circulation within the canopy, accurate spray equipment and
thorough coverage of the foliage during spray applications. High levels of rainfall and UV-exposure are
expected to limit the persistence of fungi (Ignoffo, 1992). Sprays should be timed early against
developing populations and repeated or integrated with other control methods. Avery et al. (2011)
showed that infected psyllids mostly stop feeding within 24 h of infection, suggesting they might not
actually transmit disease during this time which might mitigate against slower kill rates compared to
insecticides.
In Machakos and Machueni counties in Kenya, 8.6% of citrus farmers reportedly use biocontrol against
pests and diseases in their farms (Gitahi et al., 2019).
In summary, biological control holds a great deal of potential and has proven itself to be an important
tool for reducing the incidence of the disease on commercial farms; in particular, reducing the
production of infected adults developing from nymphs in peripheral reservoirs to limit ingress outside
the managed groves, such as abandoned orchards or residential trees has its benefits. However,
reduced adult populations would not eliminate the loss of infected trees nor the eventual spread of
the pathogen and so biocontrol needs to be integrated with other management tools for control to
be successful.
3.6 Good Agricultural Practice
Good agricultural practices for citrus include appropriate site selection, adequate plant population
(110 trees per acre), use of clean planting and grafting stock (obtained either from disease-indexed
51
nursery stock, or from disease-free areas), irrigation, the application of organic and inorganic fertilizers,
regular pruning of overcrowded canopies (best done with mechanical pruning saws or secateurs as
citrus is a hardwood), regular weed control, judicious and timely use of pesticides, good farm
sanitation (removal of infested trees ideally when psyllid populations are low to prevent disturbance
and spread (Buitendag and von Broembsen, 1993) and harvesting with care to help maximise yield.
According to Ghana’s Ministry of Food and Agriculture (MoFA) and GIZ, the German Development
Agency, citrus producers in Ghana (where citrus is planted over a larger area than any other
horticultural crop) can expect to double their yields, when following these guidelines (GIZ, 2015).
Monitoring and surveillance of ACP in citrus groves and rutaceous trees elsewhere is vital for psyllid
prevention. Visual inspection of eggs and nymphs on flush shoots (Sétamou et al., 2008), monitoring
of adult populations using yellow or lime-green sticky traps (Hall and Hentz, 2010), stem tap sampling
(Stansly et al., 2010), vacuum sampling (Thomas, 2012), and/or sweep nets (Stansly et al., 2010) can
all be employed. To improve trapping efficiency, scientists have tested mating disruptors (Mankin et
al., 2016), odorants released by citrus plants that attract ACP (Coutinho-Abreu et al., 2014), and sex
pheromones (Zanardi et al., 2018). In addition, a reported strong edge effect in D. citri distribution in
groves, has informed the efficient setup of traps to monitor ACP (Gottwald, 2010). Significant progress
has also been made toward reducing psyllid access to young citrus by planting seedlings on beds
covered with metalized polyethylene mulch. The mulch should be at least 3 mm thick, with a clear,
UV-stabilized coating to protect the reflective surface (Croxton and Stansly, 2014).
The benefits reaped from following recommended practices can be all too easily offset however, by
the increased costs entailed and this may prohibit adoption by many small-scale farmers. Despite a
paucity of peer-reviewed literature to validate these approaches, it is thought that vulnerability to HLB
can be somewhat mitigated by enhancing tree health, be it through good husbandry, orchard
sanitation, use of reflective mulch to repel ACP and/or manipulation of nutrition and irrigation.
In the US and China where HLB has had devastating impacts, some of the innovative strategies used
to support the management of Asian psyllid infestations have been: (i) the use of wind breaks (natural
or artificial) on the windward edges of groves to reduce incursion; (ii) replacement (reset) planting of
young trees within mixed, mature groves (since large block plantings create the perfect microclimate
for the vector); (iii) delayed transplanting of seedlings into fields until they are 2–3 years old to counter
the increased susceptibility and rapid decline of young trees following HLB infection (Stansly and
Rogers, 2006); and (iv) orientation of newly-planted citrus rows along the north–south axis (Martini et
al., 2015). Individual protective tree covers, particularly for young trees, have also been effective by
physically excluding psyllids from trees as well as the use of screened greenhouses (530 x 530-micron
mesh) (Stansly and Rogers, 2006) or greenhouses with positive pressure ventilation systems.
Almost every country facing the threat of citrus disease has adopted a certification programme to
rebuild or preserve its citrus industry (Vapnek, 2009). Underpinned by quarantine, clean stock and
track and trace distribution, these programmes, when mandatory, create precise requirements and
obligations to prevent introduction and spread and facilitate detection and control. In Kenya and
Tanzania, there is no citrus certification scheme and therefore no assurance that nursery-sourced
planting material is greening disease-free. In Tanzania, young trees used for replacing old or diseased
trees as well as trees required for expanding orchards are either produced by farmers themselves
(66.7%) or purchased from other farmers that have small home nurseries (23.3%) or obtained through
wild rootstock (10%) (Izamuhaye, 2008) and there is no certified source of plant material. This is also
52
the case in Kenya, meaning there is no assurance that material derived from nurseries will be diseasefree (Kyalo et al., 2018).
Rasowo et al. (2019) reported that around 59% of the 105 farms visited in Kenya and Tanzania had
unhealthy citrus trees, with disease-free citrus only recorded in farms where intensive management
practices were employed. Most farmers (85%) grew grafted citrus seedlings obtained from nurseries
along the roadsides. Half the farmers occasionally treated their citrus plants with pesticides if and
when they saw pests, but only 14% of the farmers used fertilizers. Farmers tended to rely on their own
experience (47%) or advice from agricultural commercial retailers (40%), with just a few (13%) taking
advice from government extension officers. Over 90% of farmers could not recognize HLB/ACG
symptoms or the psyllid vector.
Indigenous Technical Knowledge in Kenya relies on availability of local materials and human resources;
some the practices include use of wood ash, kerosene, table salt, lime, cow urine and cow dung but
according to Kilalo et al. (2009), insect pest management practices by citrus farmers in Kenya are
inadequate to deal with the pest and diseases situations within farms with use of synthetic pesticides
remaining the most prevalent among citrus fruits farmers. Very few surveyed farmers in Kenya’s
Machakos and Machueni counties knew that they could remove affected plant parts and plant disease
free materials to control ACT and greening disease for instance (Gitahi et al., 2019).
In summary, improving the orchard environment through good management and vigilance plays a
very big role in mitigating HLB. The layout and design should ensure good ventilation and exposure to
sunlight, good soil management including efficient fertilization programmes, inoculum removal and
good quality and disease-free planting material. While these practices may not keep the trees free of
greening and virus diseases indefinitely, they will prolong their useful lifespan and keep the trees
productive for some years even after they have been infected (FFTC, 2003).
3.7 IPM
The rationalization of pesticide use is a cornerstone of IPM and its economic and environmental
advantages in citrus groves, over a purely chemical approach, have been demonstrated (Hattingh,
1994). The citrus agro-system lends itself well to IPM since citrus trees are long-lived and not disrupted
by frequent ploughing or planting. Studies in South Africa, California and Australia have all reported
cost savings linked to reduced input costs and higher prices for pesticide-free fruit (Urquhart, 1999).
Economic thresholds based on economic injury levels are key to integrated pest management systems,
but these are hard to employ when the pest is a disease vector, because of uncertainty as to the
proportion of potential vectors capable of transmitting the pathogen. Furthermore, the damage
potential of the disease is to some extent a function of the age of the plant when infected (Stansly and
Qureshi, 2020). Nonetheless, to implement IPM of D. citri, it is necessary to monitor adult and nymphal
populations since information collected can be used to make decisions about spray applications.
Effectiveness of ACP spray programmes can also be evaluated by monitoring population trends using
visual inspections as well as methods such as tap-sampling (hitting a branch with a blunt object to
dislodge adults), sticky traps and sweep-net sampling, which have all been found to have similar
sensitivity per sampling effort (Monzo and Stansly, 2020). Stem taps have the advantage of rapid data
processing time and less sampling effort required to attain similar precision levels at all but the lowest
ACP densities and are thus recommended for large-scale ACP monitoring plans (Monzo and Stansly,
2020), whilst sticky traps are advisable for early ACP detection and to monitor young plantations
53
where stem tapping is not efficient. Adult visual sampling also provides a cheap alternative to stem
tapping in cases of low ACP infestation levels and can record nymphs on expanding flush shoots (Flores
et al., 2009; Hall et al., 2010) as well as adults although data consistency may be compromised by
scouting ability and expertise so adequate training is essential. However, because symptoms are
irregularly distributed and CLas has been found in higher concentrations away from the trunk, visual
surveys need to view the aerial parts of the canopy (Teixeira et al., 2008).
Due to the fact that ACP exhibits strong border effect in its niche occupation in groves,
recommendations are made to monitor its populations on trees along grove borders (Sétamou and
Bartels, 2015). Moreira et al. (2019) also observed lower cumulative HLB incidence in citrus plots with
higher tree densities.
The challenges of adoption of IPM, such as increased labour and monitoring costs and reduced
production during transition periods, can be considerable. Fenemore and Norton (1985) found that
high pesticide use was more likely in high value fruit crops to manage the risk of producing low quality
product and due to economies of scale achieved by mixing groups of pesticides (e.g. fungicides and
insecticides) when no viable alternatives to a single disease problem existed. Gitahi et al. (2019) found
IPM was only practiced on small scale by farmers but that there was high demand and willingness to
pay for an IPM package as a substitute to conventional pesticide use. To encourage the adoption of
IPM technologies by farmers, government should consider providing some form of support for the
transition period. In order to ensure benefits arising from IPM are distributed more equitably,
particular attention should be paid to providing extension support, as well as management and
technical training, for emerging farmers, including women to promote awareness of the possible cost
effectiveness of an IPM approach, as well as health and safety benefits (Urquhart, 1999).
In South Africa, CLaf was responsible for causing severe losses up until the late 1970s (Buitendag and
von Broembsen, 1993), however the incidence of HLB is now maintained at economically acceptable
levels through integrated management strategies involving inoculum removal and vector control
(Pretorius and van Vuuren, 2006). Furthermore, the HLB management experiences in Brazil
demonstrates that the CLas disease can also be managed if the preventive management practices of
inoculum reduction and vector control are applied at a regional scale (Bassanezi et al., 2020).
Whilst both biological and chemical control strategies are important components of an IPM
programme for ACP, biocontrol agents are slow to suppress populations compared to insecticides and
may not be effective in preventing HLB spread. Therefore, once the HLB disease is detected and/or
becomes widespread in an area, the chemical control option has advantages, mitigating vector and
disease spread, with barriers, repellents and sanitary measures used to further reduce psyllids to very
low levels. Reduced-risk insecticides with systemic action (applied to the soil) have been used as
alternatives to broad-spectrum insecticides in IPM for ACP in the US (Boina and Bloomquist, 2015) to
try to preserve the diversity of biological control agents and maintain ecological stability. Research has
shown that 96% of adult psyllids fly at heights less than 7 ft, and >99% of ACP fly at less than 9 ft.
Fencing with ACP-impermeable mesh on the perimeters of an orchard, which extends above these
heights, has been shown to substantially reduce psyllid introduction into orchards (Sétamou et al.,
2018). Live windbreaks at borders, while potentially not as effective as fencing, have also been shown
to reduce psyllid numbers in orchards (Martini et al., 2015).
The rapid movement of the bacterium to the roots (Raiol Júnior et al., 2017) is the main cause for the
failure of methods such as pruning and thermotherapy. Foliar nutritional sprays, resistance inducers,
54
phytohormones and antibiotic treatments have limited effects on HLB bacteria titres, maintenance of
tree health, yield and fruit quality. Foliar nutritional sprays only correct mineral deficiencies in the
healthy parts of diseased trees but do not reduce HLB symptoms of leaf mottle and lopsided fruit
(Vashisth and Livingston, 2019; Bassanezi et al., 2020). Finding the best combinations of control
strategies suited to different environmental and growing conditions, vector and pathogen pressure,
tree cultivars and tree health would benefit growers where HLB is not yet a chronic problem but soon
could be, especially if HLB infection is not detected quickly and if there is reluctance to remove
inoculum sources. Effective quarantine measures are essential to prevent the introduction of the HLB
organism or the vector, bearing in mind the possibility that the HLB-carrying D. citri vector could be
introduced 'naturally' or through alternative hosts such as Murraya spp. (Graça and Korsten, 2004).
Summary and recommendations on control methods
It is widely acknowledged that the best strategy against HLB is to prevent the introduction and
establishment rather than to cure the HLB disease. Su et al. (1986) were the first to define the threepart management strategy that is now recommended around the world. Their programme included
production of clean plants (insect proof nurseries and production and trade of clean citrus material),
comprehensive psyllid control and elimination of known inoculum. Where the disease has not yet
been detected, the recommendations include quarantine measures against both vector and disease
to mitigate human movement of infected citrus material (grafted trees, seedlings, budwood) and
rutaceous hosts which can undermine any management efforts if neglected, as well as early detection
and diagnosis of HLB and its vectors, removal of inoculum, and scouting for and eradication of citrus
psyllids, once identified, using focused and appropriate control methods. In areas where ACP is still
absent or scattered, prevention policies to avoid its establishment are called for.
Systematic, delimiting surveys across the region are required to establish the exact distribution of HLB
in the East African region and bordering southern areas and to validate occurrence reports.
Furthermore, data quantifying the range and number of host plants and the extent to which they have
been infected (hot and low spot areas), as well as the prevalence of ACP and the proportion of the
population that is infected is needed. This would involve sending samples to taxonomists and research
labs for taxonomic/PCR confirmation, which in turn would need to be underpinned with surveillance
monitoring/trapping training). Infected psyllids can provide early warning of the presence of CLas,
prior to symptom development. Track and trace system for trees is also needed to qualify the
potentially wider distribution of infected material and to evaluate the prospects for eradication and/or
containment for the region given the localization of HLB-positive sites identified by Ajene et al. (2020a)
in Kenya (Gebeyehu et al., 2020).
Awareness raising should also form a crucial aspect of any action plan, with mass campaigns (media,
stakeholder workshops including policy makers, citrus industry, regulators, farmers, extensionists,
quarantine personnel etc), training opportunities to build capacity and plant health rallies to
disseminate information in local languages. Table 3 provides a synthesis of recommendations on
surveillance and management for African countries.
There is a closing window of opportunity to eradicate/contain the disease in East Africa. Much
research has been conducted into HLB and its vector around the world and lessons can be learned
from the action plans and management programmes which have been or are being implemented in
many countries. Whilst it is acknowledged that the best management options may be difficult to
implement in different countries and will be influenced by the technology available and existing
55
resources, a multifaceted, integrated management programme, with clearly defined roles and
responsibilities between sectors, is essential and coordination within the East African region must be
promoted in order to maximise and share experience and resources for the management of HLB. It is
important to acknowledge that grower choices and behaviours are fully intertwined with many
different issues and outcomes. Individual grower needs and scale of production, and also that of their
neighbours, all influence disease spread, vector population dynamics and areawide adoption of
proposed scientific solutions. Singerman and Useche (2019) proposed replacing the voluntary
character of the area-wide pest management programme with a mandatory component along with a
self-enforcing feature to guarantee participation as key policy changes to make the programme
successful. This top-down regulation could then serve to generate a bottom-up collective action,
provided growers were given appropriate incentives and support.
The growing biosecurity threat to the Southern African citrus production areas has prompted the
development of HLB and ACP Action Plans in South Africa and regional efforts in East Africa should
ideally be tied in to these response actions, from citrus farmers on the ground, right up to national
legislation to enforce restrictions on plant movement and controls at provincial and country
boundaries. In Southern African countries, early warning surveillance has been initiated in Eswatini,
Zimbabwe, Namibia, Angola, Zambia and Mozambique, with no CLas or ACP detection in these
countries so far (Gebeyehu et al., 2020). In South Africa, a suite of biosecurity preparedness actions
has been developed; these include capacity building, awareness raising, detection and monitoring
surveys in commercial orchards, farms, non-residential areas and border posts/entry points, all
informed by a dedicated HLB and ACP Action Plan adopted by an HLB steering committee.
56
Table 3. Recommendations on surveillance and management for African countries.
Method
Availability in Africa
Chemical control Many are recommended
however the lower risk products
may be unavailable or costly.
Recommendations for smallholders Recommendations for commercial Recommendations for government
farms
•
•
•
•
Only use pesticides
recommended by the
government. Select
lower risk pesticides or
selective insecticides if
available/affordable to
protect natural enemies.
Rotate insecticides with
different modes of
action and follow all
safety and operating
advice.
Buy from registered
dealers. Use proper PPE
and observe the reentry/pre-harvest
intervals of the product.
Check for leaves that
look yellowed or
mottled with green
midribs, and take
collective action to
control the disease
vectors, if the disease is
present.
57
•
•
•
•
Use proper PPE and
observe the reentry/pre-harvest
intervals of the product.
Spray regime should be
informed by effective
monitoring of the psyllid
using yellow sticky traps
and visual inspections,
ideally coordinated
across commercial
orchards in the region,
to determine critical
time for simultaneous
pesticide application and
prevention of spread.
Edges and blocks on the
farm periphery should
be heavily monitored
and prioritized for
treatment.
Elimination of inoculum
sources should also be
conducted outside
commercial orchards, in
•
•
•
Publish and make public
the list of recommended
chemicals for control of
ACP which have low
impact on beneficials.
Sensitize regulatory
authorities for initiating
necessary actions aimed
at fast-tracking the
process of testing,
validating and
registering products for
control with new active
ingredients and
adjuvants which may
provide more effective
and more
environmentally-friendly
ACP suppression.
Preparedness for
Areawide ACP
Treatment Programme
to allow for informed,
coordinated insecticide
treatment among
Method
Availability in Africa
Recommendations for smallholders Recommendations for commercial Recommendations for government
farms
•
•
•
•
Applications should be
informed by monitoring
and aim to minimize
impact on natural
enemies. Scouting and
coordination amongst
neighbouring
smallholders is critical.
Onset and duration of
flushes should be
monitored and young
trees with multiple
flushes prioritized for
control.
Soil drenches are best
applied when the tree is
flushing and during dry
periods. Foliar sprays
with different types of
materials, including oil
can be used during the
rainy season.
Broad spectrum foliar
insecticides may be
more suitable for
mature trees (not when
58
•
•
rural and urban areas,
and abandoned or
poorly managed
orchards to prevent
secondary infection.
Use pesticides
recommended by
government, especially
those with low impact
on beneficial organisms.
Rotate insecticides with
different modes of
action or consider IGR
products.
Consider low-volume
spraying to allow
application over wider
areas.
neighbouring orchards
to maximise control,
should the disease and
vector be found more
widely.
Method
Availability in Africa
Recommendations for smallholders Recommendations for commercial Recommendations for government
farms
flowering) but control is
challenged by
asynchronous flushing
and shorter residual
effects.
Botanicals
Commercial neem products are
available in some countries (e.g.
Nimbecidine). Some essential oils
tested in Africa (e.g. Ocimum sp.)
•
•
Use recommended
neem products, organic
and "soft" foliar
insecticides such as oils
and soaps (horticultural
spray oil, neem oil,
kaolin clay, insecticidal
soap) but applications
may need to be made
frequently when psyllids
are observed (every 7 to
14 days) since these lack
persistent effect.
Interplanting with guava
may help repel psyllids.
Consider using
homemade neem
products to repel
psyllids.
59
•
Assess efficacy of natural
products such as neem
and interplanting with
guava and adopt for use.
•
•
Accept supporting data
from other countries for
registration of novel
botanicals (e.g. antimicrobial peptides).
Work with international
agencies to test locally
manufactured botanical
pesticides, essential oils
which maximise toxic
effect or repellence of
ACP/ACT and reduce
side effects on beneficial
arthropods.
Method
Availability in Africa
Biological
control
Native parasitoids present in
South Africa for T. erytreae but
hyperparasitoids can reduce
effectiveness.
Recommendations for smallholders Recommendations for commercial Recommendations for government
farms
•
•
Host
plant No resistant citrus seedling trees
resistance
or scion-rootstock combinations
have as yet been identified.
•
Adapt specific cultural
practices that conserve
native natural enemies
such as coccinellids and
syrphids (e.g. use only
low-risk, species-specific
pest control products).
Maintain crop diversity
and flower strips
comprising suitable wild
plants to allow natural
enemies to persist in the
environment when
psyllid numbers are low.
•
Choose varieties which
are naturally more
tolerant e.g. Tangelo
nova, Tangerine Dancy
and Tangerine Sugar
Bell.
•
60
Adapt cultural practices
to augment naturally
occurring arthropods
(spiders, ladybirds,
syrphids) to help
suppress populations of
psyllids.
•
Choose varieties which
are naturally more
tolerant e.g. Tangelo
nova, Tangerine Dancy
and Tangerine Sugar
Bell.
•
•
•
Work with international
agencies to test
candidate biological
control agents for ACP
following the IPPC
guidelines.
Explore the possibility of
classical biological
control through the
introduction of specific
parasitoids from
Asia/countries where
previously implemented
(e.g. La Réunion).
Facilitate multiplication
of any current varieties
showing more tolerance
to HLB.
Maintain international
dialogue to help
incorporate latest
research into breeding
programmes and new
tools emerging from
biotechnology,
Method
Availability in Africa
Recommendations for smallholders Recommendations for commercial Recommendations for government
farms
molecular genetics and
genomics research.
IPM
Many options but may be
ineffective when just one
method used, especially if psyllid
becomes more ubiquitous. Need
for greater grower information
resources and sensitization to
merits of IPM in citrus, for all
pests and diseases.
•
•
Check for the presence
of psyllids in young
flushes and carry out
effective monitoring (biweekly) using branch tap
method and/or sticky
traps to inform
management options.
Use non-chemical
methods wherever
possible.
Trees should be given
adequate irrigation and
nutrients to maintain
optimal health and
productivity but
management practices
which promote new
flush such as hedging
and topping and
fertilization should be
used judiciously.
61
•
•
•
•
Check for the presence
of psyllids in young
flushes and carry out
effective monitoring (biweekly) using tap
method and/or sticky
traps to inform
management options.
Maintain good records
of agronomy,
monitoring,
interventions, yield etc
and review regularly.
Use scion-rootstock
variety combinations
with higher productive
efficiency.
Provide adequate
fertilization and
irrigation, higher
planting density.
•
•
•
Implementation of
National Action Plan to
include Area Wide
Integrated Management
Strategies to
eliminate/contain the
disease and mitigate
further spread.
Launch awareness
campaign as part of a
Regional Information
Communication Strategy
to highlight HLB threat
(including
grower/exporter
information package,
training materials on
alert early warning,
symptoms, seasonality
and management).
Facilitate cooperative
approach for integrated
management across the
region (through
Method
Availability in Africa
Recommendations for smallholders Recommendations for commercial Recommendations for government
farms
•
•
•
Surveillance/
monitoring
•
stakeholder workshops,
capacity building for
detection and diagnosis,
subsidized training in
management and
surveillance networks
etc), including more
focused, rapid action
plans for hotspot areas.
Infected trees should be
removed and replaced
with disease free stock.
Remove abandoned and
unproductive citrus
trees that may act as
refugia.
Use live windbreaks on
the borders of orchards
(>9ft tall) and keep trees
relatively short for
better visual inspection.
Tree taps method used
to monitor adults as well
as sticky traps placed in
the northern, southern
and middle rows of
citrus orchards and
increased scouting of
edges.
62
•
•
Regular scouting of
border trees is
recommended: every 2–
4 weeks, depending on
the season and age of
the tree.
Scout young trees as
often as once a week,
mature trees once a
month. Every 2 weeks is
suggested as the normal
protocol during periods
of flushing.
•
Mobilize resources
and/or develop capacity
for information network
to communicate and
share early warning
systems, contingency
plans, as well as highquality monitoring data
from known geographic
locations/ incursion
detection surveys with
rapid sample analysis
and reporting.
Method
Availability in Africa
Recommendations for smallholders Recommendations for commercial Recommendations for government
farms
•
•
Good
Agricultural
Practice
No citrus certification scheme in
Kenya and Tanzania. Lack of
knowledge regarding HLB and
vectors, poor grove
management, local trade in
infected material.
•
•
Use disease-free
planting material from
certified sources.
Proactive scouting for
the vectors and rapid
and safe removal
/disposal of infected
trees with symptoms of
greening.
63
•
•
One central row should
also be sampled, to
determine if psyllid
movement farther into
the orchard has
occurred. Sample a
single flush from each of
10 trees along each
border.
Treatment is
recommended before
psyllids reach 0.5
nymphs per flush, or 2 of
10 flushes are infested.
•
Ensure citrus material
has phytosanitary
accreditation and track
and trace system for
provenance and
distribution.
Active and regular
scouting and
management to mitigate
introduction of diseased
material and subsequent
spread.
National regulation and
compliance scheme for
citrus nurseries and
suppliers to ensure
certification and traceability
scheme for clean planting
material and appropriate
quarantine measures to
mitigate introduction and
spread.
•
Quarantine and official
orders for border control
of plant/fruit movement.
Review early detection
tools such as caninebased detection, altered
metabolic, volatile
organic compounds for
potential to support PCR
based HLB diagnosis.
Method
Availability in Africa
Recommendations for smallholders Recommendations for commercial Recommendations for government
farms
•
•
Keeping trees short for
ease of monitoring and
management.
Good horticultural
practices involving the
application of optimal
nutrition and irrigation
to reduce tree stress and
vulnerability.
•
•
•
Tree pruning
Pruning of infected parts of the
plant is a common practice in
many parts of East Africa. The
severe pruning results in
maximum stimulation and the
strongest regrowth. Severe root
dieback occurs with HLB, and it
is not known whether an
affected tree can withstand the
severe pruning to re-establish a
canopy and produce an
•
There is a rapid
regrowth response of
the pruned trees which
may indicate that a
pruning approach could
be effective at
rejuvenating the HLBaffected trees, and an
alternative to tree
removal and replanting
in the short term but
64
•
•
Establishment of screen
houses and insect-proof
nurseries/covers for
susceptible young
plantings and wind
barriers at orchard
edges.
Training of nursery
operators and
technicians in all aspects
of management,
sanitation and
movement protocols.
Removal (rogueing) of
infected trees.
Fruit yields from pruned
trees never surpass the
yields from non-pruned
trees possibly due to the
severe pruning
treatment.
The effectiveness could
be combined with
enhanced foliar nutrition
treatments, although
Method
Availability in Africa
acceptable fruit yield. Severe
pruning is unlikely to be cost
effective in the longer term.
Recommendations for smallholders Recommendations for commercial Recommendations for government
farms
new flushes induced by
pruning are attractive to
psyllids so only light
pruning is recommended
in areas where disease is
not endemic
65
the benefits only accrue
in the early years.
4 Advice, information and communication
4.1 Sources of information on HLB control
HuangIongbing is still a new disease in Kenya, and consequently not much information is being disseminated on
the proper identification of the disease and how to differentiate it from ACGD, as well as its vector. ICIPE has
recently completed a project of citrus pests and diseases and one of the next steps suggested was to compile and
document all the available information on the efficacy of different management options of HLB and its vector,
learning from experiences in the USA, China and South Africa. Consequently, this would mean creating awareness
among the farming communities, extension and quarantine personnel about this new disease and its vector
(through mass media, ICT, training and communication materials in local languages). In terms of control, HLB
does not lend itself to some of the common methods employed for most pests as the disease is often detected
late when the citrus tree starts showing symptoms. Therefore, any recommendations communicated to the
farmer should be efficacious, safe, sustainable, practical, available and affordable.
4.2 Criteria for control advice
We recommend the following criteria for control advice:
•
Efficacy This is often assumed to be the most important criterion, even if this is not stated explicitly. If
a practice is to be recommended there should be some evidence that it will be effective in at least some
situations. Where a product has to be registered, this generally includes demonstration of efficacy, but
many IPM practices do not involve a registered product. Results from controlled trials in an appropriate
context are desirable, though not always available.
•
Safety Even registered products can be hazardous to human health without precautions. Safety should
thus be considered based on a consideration of how the product is likely to be used rather than whether
recommended safety precautions are adequate. Some practices not requiring registration can also be
hazardous, such as some plant extracts.
•
Sustainability Possible effects on non-target organisms, such as pollinators, natural enemies and other
organisms, should be considered. A control method may also have potential to create new problems,
such as resurgence of other pests or pesticide resistance.
•
Practicality Some methods may be impractical for some farmers, particularly those requiring elaborate
safety precautions. Others may be only practical at a small scale.
•
Availability Availability of regulated products is initially determined by their registration status, but even
registered products may not be widely stocked if distribution is expensive and/or the perceived market
is small. Unregulated inputs for some control methods may not be easily available, such as seeds of
companion plants.
•
Cost-effectiveness At the simplest level the cost of control must be less than the value of crop loss
avoided, for it to be worthwhile. Opportunity and other costs may need to be considered.
66
4.3 Information resources and tools
Citrus Pest & Disease Prevention Program (CPDPP): Best practices in response to huanglongbing in California
citrus.
https://citrusinsider.org/wp-content/uploads/2019/06/Voluntary-Actions-Best-Practices-COMPLETEFINAL.pdf (accessed 21 July 2020)
California Department of Food & Agriculture Action Plan for Asian Citrus Psyllid and Huanglongbing (Citrus
Greening) in California. https://www.cdfa.ca.gov/citruscommittee/docs/ActionPlan.pdf (accessed 2 March 2021)
Animal and Plant Health Inspection Service, US Department of Agriculture: Citrus greening programme
information including links to multi-agency response measures.
https://www.aphis.usda.gov/aphis/ourfocus/planthealth/plant-pest-and-disease-programs/pests-anddiseases/citrus/citrus-greening (accessed 2 March 2021)
Summary action plan and procedure for early detection and response to HLB and the Asian citrus psyllid entering
South Africa. http://sana.co.za/wp-content/uploads/2013/01/DAFF-citrus-greening-action-plan-1.pdf (accessed
21 July 2020)
Invasive Species Compendium: This is a free encyclopaedic resource that brings together a wide range of different
types of science-based information to support decision making in invasive species management worldwide.
www.cabi.org/isc
Crop Protection Compendium: This is an encyclopaedic resource that brings together a wide range of different
types of science-based information on all aspects of crop protection. It comprises detailed datasheets on pests,
diseases, weeds, host crops and natural enemies. https://www.cabi.org/cpc
5 Recommendations
HLB presents a serious and rapidly-growing threat to citrus-growing regions across the whole of Africa. A
successful response will require acceptance of the urgency of the situation, willingness to cooperate and
persevere with management plans in the near- and mid-term, but above all, it will need an unprecedented degree
of cooperation across many sectors. As demonstrated around the world, only through a coordinated effort by
government officials, regulatory agencies, plant protection agencies, citrus growers, research institutions,
extension workers and society can the wider introduction and spread of HLB be prevented and the vector
contained to protect this valuable crop in the East African Region.
High-level policy makers:
•
Recognize the magnitude of the HLB threat (present and potential) and make policy decisions, backed
by available economic estimates and science-based evidence
•
Lobby for budgetary allocation to facilitate an immediate, official national response backed by policy
and legislation, to enable coordinated (potentially mandatory) contingency action to curb the spread
of the disease at the earliest opportunity
•
Aim to create preparedness action plans across the East African Community and harmonize with
established steering committees across the continent (e.g. South Africa’s Emergency Plant Pest
67
Response strategy and HLB action plan) to mitigate and contain the disease. Consider use of incentives
for replanting certified disease-free material, including HLB Safe Citrus Tree Production Systems
•
Provide support for capacity building and knowledge exchange/dissemination across the entire citrus
value chain to include early warning surveillance (track and trace), awareness raising, development of
standard monitoring and diagnostic protocols and integrated management
Regulators:
•
Strengthen the letter and enforcement of phytosanitary regulations on movement of citrus plants and
alternate hosts
•
Develop an HLB alert brochure followed by a comprehensive brochure on all aspects of management
•
Regulate and implement protection of nursery stock in ACP-proof structures
•
Plan and implement inspection of commercial and garden citrus and alternate hosts of ACP and HLB
•
Prepare to impose strict quarantine and containment measures in hotspots, at country boundaries and
at provincial boundaries with only nurseries certificated HLB-free permitted to move citrus trees
•
Encourage track and trace system for movement control
•
Fast-track the process of testing, validating and registration of products for the control of the HLB vector
Researchers:
•
Undertake coordinated monitoring at the regional scale to create a dynamic picture of ACP demography,
density and impact across the citrus-growing areas of Africa and share valuable data for vector
management plans
•
Carry out surveys to identify local natural enemies that can be used in augmentative and conservation
biocontrol
•
Test locally-available biopesticides and essentials oils and produce formulations that can maximise the
toxic effect on ACP and reduce side effects on beneficials
•
Timely and systematic communication of research outcomes and integration into national action plans
•
Establish and support international research networking links to stay abreast of HLB research progress
Advisory services:
•
Create a communications plan to raise awareness within the citrus production community/value chain,
and public at large regarding dangers and risks associated with ACP and HLB
•
Expand extension efforts to facilitate and coordinate judicious control of the psyllid vector if detected,
promoting IPM and low-risk options for management, as well as rapid removal of infected trees in
commercial, smallholder and abandoned citrus groves
•
Creation of Citrus Health Management Areas to promote coordinated and integrated management
68
•
Develop an array of cost-effective, clear and harmonized monitoring and impact assessment protocols
to be followed for HLB studies
Smallholder farmers:
•
Engage in good agricultural practice to maximise tree health, including good irrigation and fertilization
(e.g. mulching, use of organic manure)
•
Practice good preventative action by selecting healthy budwood and protect seedlings and flushing
plants as a priority, with additional focus on grove edges
•
Engage in early warning surveillance, with ACP scouting and trapping as a routine
•
Treatment and removal of infected trees as a priority and replacement with healthy trees, with added
protection from psyllid ingress in hotspot areas
Commercial farmers:
•
Citrus nurseries are encouraged to proceed with changing over to citrus tree production in insectsecure structures
•
Commercial growers need compliance agreements to ensure production of certified disease-free
material and implementation of phytosanitary protocols regarding movement and elimination of
inoculum
•
Commercial nurseries should work towards an effective disease/vector management contingency
programme
•
Commercial farmers should engage in training on HLB/ACP scouting, diagnosis, monitoring and
contingency management
Acknowledgements
This paper was prepared as part of the Action on Invasives and Plantwise Plus programmes. Action on Invasives
is supported by the UK Foreign, Commonwealth and Development Office (FCDO) and the Netherlands Directorate
General for International Cooperation (DGIS). Plantwise Plus, in addition to FCDO and DGIS, is also funded by
European Commission Directorate-General for International Cooperation and Development (DEVCO) and Swiss
Agency for Development and Cooperation (SDC).
CABI is an international intergovernmental organization, and we gratefully acknowledge the core financial
support from our member countries (and lead agencies) including the UK (FCDO), China (Chinese Ministry of
Agriculture and Rural Affairs), Australia (Australian Centre for International Agricultural Research), Canada
(Agriculture and Agri-Food Canada), the Netherlands (DGIS) and Switzerland (Swiss Agency for Development and
Cooperation). See http://www.cabi.org/about-cabi/who-we-work-with/key-donors/ for full details.
The authors acknowledge the contribution of Samira Faris Mohamed, icipe (International Centre of Insect
Physiology and Ecology) for sharing outcomes of the Citrus International Stakeholder Meeting. We thank Dr
Richard Shaw (CABI) for his valuable inputs when serving as internal peer reviewer for this paper.
69
References
Abdullah, T.L., Shokrollah, H., Sijam, K. and Abdullah, S.N.A. (2009) Control of huanglongbing (HLB) disease with
reference to its occurrence in Malaysia. African Journal of Biotechnology 8, 4007–4015.
Ackerman, E. (1938) Influences of climate on the cultivation of citrus fruits. Geographical Review 28(2), 289–302.
https://do.org/10.2307/210476
Agnello, A. (2002) Petroleum-derived spray oils: chemistry, history, refining, and formulation. In: Beattie, G.A.C.,
Watson, D.M., Stevens, M.L., Rae, D.J. and Spooner-Hart, R.N. (eds) Spray Oils Beyond 2000: Sustainable
Pest and Disease Management. University of Western Sydney, Sydney, Australia, pp. 2–18.
Agrawal, A.A. and Karban, R. (1999) Why induced defenses may be favored over constitutive strategies in plants.
In: Tollrian, R. and Harvell, C.D. (eds) The Ecology and Evolution of Inducible Defenses. Princeton
University Press, Princeton, NJ, USA, pp. 45–61.
Aidoo, O.F., Tanga, C.M., Khamis, F.M., Rasowo, B.A., Mohamed, S.A., Badii, B.K., Salifu, D., Sétamou, M., Ekesi,
S. and Borgemeister, C. (2019) Host suitability and feeding preference of the African citrus triozid Trioza
erytreae Del Guercio (Hemiptera: Triozidae), natural vector of “Candidatus Liberibacter africanus.”
Journal of Applied Entomology 143, 262–270.
Aidoo, O.F., Tanga, C.M., Mohamed, S.A, Khamis, F.M., Opisa, S., Rasowo, B.A., Kimemia, J.W., Ambajao, J.,
Sétamou, M., Ekesi, S. and Borgemeister, C. (2020a) The African citrus triozid Trioza erytreae Del Guercio
(Hemiptera: Triozidae): temporal dynamics and susceptibility to entomopathogenic fungi in East Africa.
International Journal of Tropical Insect Science 41, 563–573. https://doi.org/10.1007/s42690-020-002415
Aidoo, O.F., Tanga, C.M., Mohamed, S.A., Khamis, F.M., Baleba, S.B.S., Rasowo, B.A., Ambajo, J., Sétamou, M.,
Ekesi, S. and Borgemeister, C. (2020b) Detection and monitoring of ‘Candidatus’ Liberibacter spp.
vectors: African citrus triozid Trioza erytreae Del Guercio (Hemiptera: Triozidae) and Asian citrus psyllid
Diaphorina citri Kuwayama (Hemiptera: Liviidae) in citrus groves in East Africa. Agricultural and Forest
Entomology 22(4), 401–409. https://doi.org/10.1111/afe.12395
Ajene, I.J., Khamis, F., Mohammed, S., Rasowo, B., Ombura, F.L., Pietersen, G., van Asch, B. and Ekesi, S. (2019)
First report of field population of Trioza erytreae carrying the Huanglongbing- associated pathogen,
‘Candidatus Liberibacter asiaticus’, in Ethiopia. Plant Disease 103(7). https://doi.org/10.1094/PDIS-0119-0238-PDN
Ajene, I.J., Khamis, F.M., van Asch, B., Pietersen, G., Seid, N., Rwomushana, I., Ombura, F.L.O., Momanyi, G.,
Finyange, P., Rasowo, B.A., Tanga, C.M., Mohammed, S. and Ekesi, S. (2020a) Distribution of Candidatus
Liberibacter species in Eastern Africa, and the first report of Candidatus Liberibacter asiaticus in Kenya.
Scientific Reports 10(3919). https://doi.org/10.1038/s41598-020-60712-0
Ajene, I.J., Khamis, F., Ballo, S., Pietersen, G., van Asch, B., Seid, N., Azerefegne, F., Ekesi, S. and Mohamed, S.
(2020b) Detection of Asian citrus psyllid (Hemiptera: Psyllidae) in Ethiopia: a new haplotype and its
implication to the proliferation of Huanglongbing. Journal of Economic Entomology 113(4), 1640–1647.
https://doi.org/10.1093/jee/toaa113
70
Ajene, I.J., Khamis, F.M., Mohammed, S., Adediji, A.O., Atiri, G.I., Kazeem, S.A. and Ekesi, S. (2020c) First report
of ‘Candidatus Liberibacter africanus' associated with citrus greening disease in Nigeria. Plant Disease
Notes 104(5), 1535. https://doi.org/10.1094/PDIS-11-19-2380-PDN
Ajene, I.J., Khamis, F., van Asch, B., Pietersen, G., Rasowo, B.A., Ekesi, S. and Mohamed, S. (2020d) Habitat
suitability and distribution potential of Liberibacter species “Candidatus Liberibacter asiaticus” and
“Candidatus Liberibacter africanus” associated with citrus greening disease. Diversity and Distributions
26, 575–588. https://doi.org/10.1111/ddi.13051
Albrecht, C., Hicks, A., Hornbaker, V., Khalid, S., Kumagai, L., Morgan, D. and Okasaki, K. (2020) Action plan for
Asian Citrus Psyllid and Huanglongbing (citrus greening) in California. Journal of Citrus Pathology 7(1), 56.
Available at: https://escholarship.org/uc/item/5zh6m715 accessed 8 June 2021.
Albrecht, U. and Bowman, K. D. (2012) Tolerance of trifoliate citrus rootstock hybrids to Candidatus Liberibacter
asiaticus. Scientia Horticulturae 147(Supplement C), 71–80.
Albrigo, L.G. and Stover, E.W. (2015) Effect of plant growth regulators and fungicides on Huanglongbing-related
preharvest
fruit
drop
of
citrus.
HortTechnology
25(6),
785–790.
https://doi.org/10.21273/HORTTECH.25.6.785
Alquézar, B., Volpe, H.X.L., Magnani, R.F., de Miranda, M.P., Santos, M.A., Wulff, N.A., Bento, J.M.S., Bento, J.R.P.,
Bouwmeester, H. and Peña, L. (2017) β-caryophyllene emitted from a transgenic Arabidopsis or chemical
dispenser repels Diaphorina citri, vector of Candidatus Liberibacters. Scientific Reports 7(1), 5639.
Alvarez, S., Rohrig, E., Solís, D. and Thomas, M.H. (2016) Citrus greening disease (Huanglongbing) in Florida:
Economic impact, management and the potential for biological control. Agricultural Research 5, 109–
118. https://doi.org/10.1007/s40003-016-0204-z
Ammar, E.D., Shatters Jr, R.G., Lynch, C. and Hall, D. (2011) Detection and relative titer of Candidatus Liberibacter
asiaticus in the salivary glands and alimentary canal of Diaphorina citri (Hemiptera: Psyllidae) vector of
citrus huanglongbing disease. Annals of the Entomological Society of America 104(3), 526–533.
Aubert, B. (1987) Trioza erytreae del Guercio and Diaphorina citri Kuwayama (Homoptera: Psylloidea), the two
vectors of citrus greening disease: Biological aspects and possible control strategies. Fruits 42, 149–162.
Aubert, B. (1994) Citrus greening disease, a serious limiting factor for citriculture in Asia and Africa. In:
Proceedings of the International Society of Citriculture: VII International Citrus Congress, March 8–13,
1992, Acireale, Italy. Volume 2. International Society of Citriculture, Catania, Italy, pp. 817–820.
Aubert, B. and Hua, X.Y. (1990) Monitoring flight activity of Diaphorina citri on citrus and Murraya canopies. In:
Aubert, B., Tontyaporn, S. and Buangsuwon, D. (eds) Rehabilitation of citrus industry in the Asia Pacific
Region. Proceedings of the 4th International Asia Pacific Conference on Citrus Rehabilitation, 4–10
February 1990, Chiang Mai, Thailand. Food and Agriculture Organization / United Nations Development
Programme, Rome, Italy, pp. 181–187.
Aubert, B. and Quilici, S. (1988) Monitoring adult psyllas on yellow traps in Reunion Island. International
Organization of Citrus Virologists Conference Proceedings 10, 249–254. Available at:
https://escholarship.org/uc/item/4mn0b3tj accessed 5 May 2021.
71
Avery, P.B., Wekesa, V.W., Hunter, W.B., Hall, D.G., Mckenzie, C.L., Osborne, L.S., Powell, C.A. and Rogers, M.E.
(2011) Effects of the Isaria fumosorosea (Hypocreales: Cordycipitaceae) on reduced feeding and
mortality of the Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae). Biocontrol Science and
Technology 21(9), 1065–1078.
Balandrin, M.F., Lee, S.M. and Klocke, J.A. (1988) Biologically active volatile organosulfur compounds from seeds
of the neem tree, Azadirachta indica (Meliaceae). Journal of Agricultural and Food Chemistry 36(5),
1048–1054. https://doi.org/10.1021/jf00083a035
Baldwin, E., Bai, J., Plotto, A., Manthey, J., Narciso, J., Dea, S. and Irey, M. (2012) Effect of nutritional spray regimes
on orange juice flavor quality and juice Liberibacter (CLas) DNA detection. Proceedings of the Florida
State Horticultural Society 125, 239–242.
Bassanezi, R.B. (2018) Evolución de la severidad y el daño de huanglongbing en plantaciones de naranjo dulce y
sus implicaciones para el manejo de la enfermedad. Cítricos en las Américas 1, 31–44.
Bassanezi, R.B. and Bassanezi, R.C. (2008) An approach to model the impact of Huangdongbing on citrus yield.
In: Gottwald, T.R. and Graham, J.H. (eds) Proceedings of the Meeting, International Research Conference
on Huanglongbing, Orlando Florida, December 2008. Plant Management Network, pp. 301–304.
Available at: https://swfrec.ifas.ufl.edu/hlb/database/pdf/22_IRCHLB_08.pdf accessed 5 May 2021.
Bassanezi, R.B., Montesino, L.H., Gasparoto, M.C.G., Filho, A.B. and Amorim, L. (2011) Yield loss caused by
huanglongbing in different sweet orange cultivars in São Paulo, Brazil. European Journal of Plant
Pathology 130, 577–586. https://doi.org/10.1007/s10658-011-9779-1
Bassanezi, R.B., Belasque Jr, J. and Montesino, L.H. (2013a) Frequency of symptomatic trees removal in small
citrus
blocks on citrus
huanglongbing epidemics. Crop Protection 52, 72–77.
https://doi.org/10.1016/j.cropro.2013.05.012
Bassanezi, R.B., Montesino, L.H., Gimenes-Fernandes, N., Yamamoto, P.T., Gottwald, T.R., Amorim, L. and Filho,
A.B. (2013b) Efficacy of area-wide inoculum reduction and vector control on temporal progress of
huanglongbing in young sweet orange plantings. Plant Disease 97(6), 789–796.
https://doi.org/10.1094/PDIS-03-12-0314-RE
Bassanezi, R.B., Lopes, S.A., Miranda, M.P., Wulff, N.A., Volpe, H.X.L. and Ayres, A. (2020) Overview of citrus
huanglongbing spread and management strategies in Brazil. Tropical Plant Pathology 45, 251–264.
https://doi.org/10.1007/s40858-020-00343-y
Batool, A., Iftikhar, Y., Mughal, S.M., Khan, M.M., Jaskani, M.J., Abbas, M. and Khan, I.A. (2007) Citrus Greening
Disease – A major cause of citrus decline in the world: A review. Horticultural Science (Prague) 34, 159–
166. https://doi.org/10.17221/1897-HORTSCI
Beattie, G.A.C., Holford, P., Mabberley, D.J., Haigh, A.M., Bayer, R. and Broadbent, P. (2006) Aspects and insights
of Australia–Asia collaborative research on huanglongbing. In: Proceedings of the International
Workshop for the Prevention of Citrus Greening Disease in Severely Infected Areas. International
Research Division, Tokyo, Japan, pp. 47–64.
Beige, C., Kanyagia, S., Muriuki, S., Otieno, S., Seif, A. and Whittle, A. (1984) Horticultural Crops Protection
Handbook. Ministry of Agriculture and Livestock Development, National Horticultural Research Station,
Thika, Kenya, 165 pp.
72
Bekele, S.M. (2007) Identification of citrus (Citrus sinensis) postharvest pathogens from Ethiopia and their control.
PhD Thesis, University of Pretoria, South Africa, 181 pp.
Berg, M.A van den, Dippenaar-Schoeman, A.S., Deacon, V.E. and Anderson, S.H. (1992) Interactions between
citrus psylla, Trioza erytreae (Hem. Triozidae),and spiders in an unsprayed citrus orchard in the
transvaal lowveld. Entomophaga 37, 599–608. https://doi.org/10.1007/BF02372330
Berg, M.A. van den and Deacon, V.E. (1988) Dispersal of the citrus psylla, Trioza erytreae, in the absence of its
host plants. Phytophylactica 20, 361–368.
Berg, M.A. van den and Greenland, J. (2000) Tamarixia dryi, parasitoid of the citrus psylla, Trioza erytreae: a
review. African Plant Protection 6, 25–28.
Besigye, B.D. (2013) Financial cost benefit analysis of drip irrigation system for production of citrus fruits in the
cattle corridor of uganda: a case of odina irrigation scheme - Soroti District. First level master degree in
irrigation problems in developing countries. Uuniversità Degli Studi di Firenze, pp. 71. Available at:
http://www.pienocampo.it/solinas/FINANCIAL%20COST%20BENEFIT%20ANALYSIS%20OF%20DRIP%20I
RRIGATION%20SYSTEM%20FOR%20PRODUCTION%20OF%20CITRUS%20FRUITS%20IN%20THE%20CATT
LE%20CORRIDOR%20OF%20UGANDA%20A%20CASE%20OF%20ODINA%20IRRIGATION%20SCHEME%2
0-%20SOROTI%20DISTRICT.pdf accessed 4 July 2020.
Blaustein, R., Lorca, G. and Teplitski, M. (2017) Challenges for managing Candidatus Liberibacter spp.
(huanglongbing disease pathogen): Current control measures and future directions. Phytopathology
108(4). https://doi.org/10.1094/PHYTO-07-17-0260-RVW
Boina, D.R. and Bloomquist, J. (2015) Chemical control of the asian citrus psyllid and of huanglongbing disease in
citrus. Pest Management Science 71(6), 808–823. https://doi.org/10.1002/ps.3957
Boina, D.R., Meyer, W.L., Onagbola, E.O. and Stelinski, L.L. (2009) Quantifying dispersal of Diaphorina citri
(Hemiptera: Psyllidae) by immunomarking and potential impact of unmanaged groves on commercial
citrus management. Environmental Entomology 38, 1250–1258.
Bové, J.M. (2006) Huanglongbing: A destructive, newly-emerging, century-old disease of citrus. Journal of Plant
Pathology 88, 7–37. https://doi.org/10.4454/jpp.v88i1.828
Bové, J.M. (2014a) Heat-tolerant Asian HLB meets heat-sensitive African HLB in the Arabian Peninsula! Why?
Journal of Citrus Pathology 1(1), 1–78.
Bové, J.M. (2014b) Huanglongbing or yellow shoot, a disease of Gondwanan origin: Will it destroy citrus
worldwide? Phytoparasitica 42, 579–583. https://doi.org/10.1007/s12600-014-0415-4
Bové, J.M., Garnier, M., Ahlawat, Y.S., Chakraborty, N.K. and Varma, A. (1993) Detection of the Asian strains of
thegreening BLO by DNA-DNA hybridisation in Indianorchard trees and Malaysian Diaphorina citri psyllids.
International Organization of Citrus Virologists Conference Proceedings 12, 258–263. Available at:
https://escholarship.org/uc/item/0ng306x8 accessed 5 May 2021.
Brlansky, R.H. and Rogers, M.E. (2007) Citrus huanglongbing: understanding the vector-pathogen interaction for
disease
management.
Online.
APSnet
Features.
Available
at:
https://www.apsnet.org/edcenter/apsnetfeatures/Pages/Huanglongbing.aspx accessed 8 June 2021.
73
Buitendag, C.H. and von Broembsen, L.A. (1993) Living with citrus greening in South Africa. International
Organization of Citrus Virologists Conference Proceedings 12, 269–273. Available at:
https://escholarship.org/uc/item/8wq051rr accessed 5 May 2021.
Castle, W.S., Bowman, K.D., Grosser, J.W., Futch, S.H. and Graham, J.H. (2016) Florida Citrus Rootstock Selection
Guide. 3rd Edn., UF/IFAS Extension Service, University of Florida, pp: 3.
Catling, H.D. (1972) Factors regulating populations of psyllid vectors of greening. International Organization of
Citrus
Virologists
Conference
Proceedings
5,
51–57.
Available
at:
https://escholarship.org/uc/item/6w3265wb accessed 5 May 2021.
Chien, C.C., Chu, Y.I. and Ku, S.C. (1995) Influences of host densities on the population increase of the eulophid
wasp, Tamarixia radiata, and its host-killing ability. Plant Protection Bulletin Taipei 37, 81–96.
Chiyaka, C., Singer, B., Halbert, S., Morris, J. and van Bruggen, A. (2012) Modeling huanglongbing transmission
within a citrus tree. Proceedings of the National Academy of Sciences of the United States of America 109,
12213–12218. https://doi.org/10.1073/pnas.1208326109
Cifuentes-Arenas, J.C., de Goes, A., de Miranda, M.P., Beattie, G.A.C. and Lopes, S.A. (2018) Citrus flush shoot
ontogeny modulates biotic potential of Diaphorina citri. PLoS One 13(1), e0190563.
https://doi.org/10.1371/journal.pone.0190563
Coletta-Filho, H.D., Carlos, E.F., Lotto, L.L., Luciane, F.C., Alves, K.C.S., Pereira, M.A.R. and Machado, M.A. (2010)
Prevalence of Candidatus Liberibacter spp. in HLB-diseased citrus plants in São Paulo State, Brazil.
International Organization of Citrus Virologists Conference Proceedings 17, 110–115. Available at:
https://escholarship.org/uc/item/7zg8d1v4 accessed 5 May 2021.
Constantine, K., Kansiime, M., Idah, M., Nunda, W., Chacha, D., Rware, H., Makale, F., Mulema, J., Godwin, J.,
Williams, F., Edgington, S. and Day, R. (2020) Why don't smallholder farmers in Kenya use more
biopesticides? Pest Management Science 76(11), 3615–3625. https://doi.org/10.1002/ps.5896
Coutinho-Abreu, I., Forster, L., Guda, T. and Ray, A. (2014) Odorants for surveillance and control of the Asian
Citrus Psyllid (Diaphorina citri). PLoS ONE 9, e109236. https://doi.org/10.1371/journal.pone.0109236
Craig, A., Cunniffe, N., Parry, M., Laranjeira, F. and Gilligan, C. (2018) Grower and regulator conflict in
management of the citrus disease huanglongbing in Brazil: A modelling study. Journal of Applied
Entomology 55(4), 1956–1965.
Croxton, S.D. and Stansly, P.A. (2014) Metalized polyethylene mulch to repel Asian citrus psyllid, slow spread of
huanglongbing and improve growth of new citrus plantings. Pest ManagementScience 70(2), 318–323.
https://doi.org/10.1002/ps.3566
Dagnew, A., Belew, D., Admassu, B. and Yesuf, M. (2014) Citrus production, constraints and management
practices in Ethiopia: The case of Pseudocercospora leaf and fruit spot disease. Science, Technology and
Arts Research Journal 3(2), 4–18. http://dx.doi.org/10.4314/star.v3i2.2
Dala-Paula, B.M., Plotto, A., Bai, J., Manthey, J.A., Baldwin, E.A., Ferrarezi, R.S., Gloria, M.B.A. et al. (2019) Effect
of huanglongbing or greening disease on orange juice quality, a review. Frontiers in Plant Science 9, 1976.
https://doi.org/10.3389/fpls.2018.01976
74
Deng, H., Achor, D., Exteberria, E., Yu, Q., Du, D., Stanton, D., Liang, G. and Gmitter Jr., F.G. (2019) Phloem
regeneration is a mechanism for huanglongbing-tolerance of “Bearss” lemon and “LB8-9” Sugar Belle®
Mandarin. Frontiers in Plant Science 10, 277. https://doi.org/10.3389/fpls.2019.00277
Diniz, A.J.F., Garcia, A.G., Alves, G.R., Reigada, C., Vieira, J.M. and Parra, J.R.P. (2020) The enemy is outside:
Releasing the parasitoid Tamarixia radiata (Hymenoptera: Eulophidae) in external sources of HLB inocula
to control the Asian citrus psyllid Diaphorina citri (Hemiptera: Liviidae). Neotropical Entomology 49(2),
250–257. https://doi.org/10.1007/s13744-019-00736-y
D'Onghia, A.M. and Lacirignola, C. (2009) The Mediterranean citriculture: productions and perspectives. In:
D'Onghia A.M., Djelouah, K. and Roistacher, C.N. (eds) Citrus tristeza virus and Toxoptera citricidus: a
serious threat to the Mediterranean citrus industry. Options Méditerranéennes: Série B. Etudes et
Recherches, 65. CIHEAM, Bari, Italy, pp. 13–17.
Dugravot, S., Grolleau, F., Macherel, D., Rochetaing, A., Hue, B., Stankiewicz, M., Huignard, J. and Lapied, B. (2003)
Dimethyl disulfide exerts insecticidal neurotoxicitythrough mitochondrial dysfunction and activation of
insect KATP channels. Journal of Neurophysiology 90, 259–270.
Ebony Consulting International (2003) Rice sub-sector study, Development Alternatives Inc.– private enterprise
support activities project – Tanzania. Final report April 2003. Maple Place North Momentum Park 145
Western Service Road Woodmead, South Africa. Prepared under USAID Contract No. PCE-I-00-9900002-00. Available at:
http://www.value- chains.org/dyn/bds/docs/410/DAI%20pesa%20Rice%20Subsector%20Study%20Apri
l%202003.pdf accessed 12 July 2020.
Ekesi, S. (2015) Arthropod pest composition and abundance on Citrus sinensis in the lowland and highland
production
locales
of
Kenya.
Acta
Horticulturae
1065,
1019–102.
https://doi.org/10.17660/ActaHortic.2015.1065.140
El-Shesheny, I., Hajeri, S., El-Hawary, I., Gowda, S. and Killiny, N. (2013) Silencing abnormal wing disc gene of the
asian citrus psyllid, Diaphorina citri disrupts adult wing development and increases nymph mortality.
PLoS One 8(5), e65392. https://doi.org/10.1371/journal.pone.0065392
EPPO (2014) PM 9/18 (1) Decision-Support Scheme for prioritizing action during outbreaks. EPPO Bulletin 44(3),
443–456. https://doi.org/10.1111/epp.12164
EPPO (2019) EPPO Global Database. https://gd.eppo.int/ accessed 1 July 2020.
EPPO (2020) PM 9/27 (1) ‘Candidatus Liberibacter’ species that are causal agents of huanglongbing disease of
citrus and their vectors: procedures for official control. EPPO Bulletin 50(1), 122–141.
https://doi.org/10.1111/epp.12619
Etienne, J. and Aubert, B. (1980) Biological control of psyllid vectors of greening disease on Reunion Island.
International Organization of Citrus Virologists Conference Proceedings 8(8), 118–121.
Étienne, J., Quilici, S., Marival, D. and Franck, A. (2001) Biological control of Diaphorina citri (Hemiptera: Psyllidae)
in Guadeloupe by imported Tamarixia radiata (Hymenoptera: Eulophidae). Fruits 56(5), 307–315.
https://doi.org/10.1051/fruits:2001131
75
Etxeberria, E., Gonzalez, P., Achor, D. and Albrigo, G. (2009) Anatomical distribution of abnormally high levels
of starch in HLB-affected Valencia orange trees. Physiological and Molecular Plant Pathology 74(1), 76–
83. https://doi.org/10.1016/j.pmpp.2009.09.004
Fan, J., Chen, C., Blansky, R.H., Gmitter, F.G. and Li, Z.-G. (2010) Changes in
carbohydrate metabolism in
Citrus sinensis infected with ‘Candidatus Liberibacter asiaticus'. Plant Pathology 59, 1037–1043.
https://doi.org/10.1111/j.1365-3059.2010.02328.x
Fan, J., Chen, C., Yu, Q., Khalaf, A., Achor, D.S., Brlansky, R.H., Moore, G.A., Li, Z.G. and Gmitter, F.G. (2012)
Comparative transcriptional and anatomical analyses of tolerant rough lemon and susceptible sweet
orange in response to “Candidatus Liberibacter asiaticus”
infection.
Molecular
Plant-Microbe
Interactions 25(11), 1396–1407.
Farnsworth, D., Grogan, K., van Bruggen, A. and Moss, C. (2014) The potential economic cost and response to
greening in Florida citrus. Choices 29, 1–6.
FAOSTAT (2019) Food and agriculture data. http://faostat.fao.org accessed 4 May 2021.
Fenemore, P.G. and Norton, G.A. (1985) Problems of implementing improvements in pest control: a case study
of apples in the UK. Crop Protection 4(1), 51–70.
FFTC (2003) Citrus Greening and Virus Diseases. Food & Fertilizer Technology Center for the Asian and Pacific
Region. Available at: https://www.fftc.org.tw/en/publications/main/177 accessed 4 May 2021.
Flores, D., Hall, D.G., Jenkins, D.A. and Sétamou, M. (2009) Abundance of Asian citrus psyllid on yellow sticky
traps in Florida, Puerto Rico, and Texas citrus groves. Southwest Entomologist 34, 1–11.
Fourie, P., Kirkman. W., Cook, G., Steyn, C., de Bruyn, R., Bester, R., Roberts, R., Bassimba, D.D., José, C.M., Maree,
H.J. (2020) First report of 'Candidatus Liberibacter africanus' associated with African Greening of Citrus
in Angola. Plant Disease 105, 486. https://doi.org/10.1094/PDIS-06-20-1392-PDN.
Garcia, A.G., Diniz, A.J.F. and Parra, J.R.P. (2019) A fuzzy-based index to identify suitable areas for host-parasitoid
interactions: Case study of the Asian citrus psyllid Diaphorina citri and its natural enemy Tamarixia
radiata. Biological Control 135, 135–140. https://doi.org/10.1016/j.biocontrol.2019.05.001
Gardner, C.L., da Silva, D.R., Pagliai, F.A., Pan, L., Padgett-Pagliai, K.A., Blaustein, R.A., Merli, M.L., Zhang, D.,
Pereira, C., Teplitski, M., Chaparro, J.X., Folimonova, S.Y., Conesa, A., Gezan, S., Lorca, G.L. and Gonzalez,
C.F. (2020) Assessment of unconventional antimicrobial compounds for the control of ‘Candidatus
Liberibacter asiaticus’, the causative agent of citrus greening disease. Scientific Reports 10, 5395.
https://doi.org/10.1038/s41598-020-62246-x
Garnier, M. and Bové, J.M. (1996) Distribution of the huanglongbing (greening) liberobacter species in fifteen
African and Asian countries. International Organization of Citrus Virologists Conference Proceedings 13,
388–391. Available at: https://escholarship.org/uc/item/8v467619 accessed 5 May 2021.
Garnier, M., Danel, N. and Bové, J.M. (1984a) Aetiology of citrus greening disease. Annales de l'Institut
Pasteur/Microbiologie 135(1), 169–179.
Garnier, M., Danel, N. and Bové, J.M. (1984b) The greening organism is a gram-negative bacterium. International
Organization of Citrus Virologists Conference Proceedings 9, 115–124. Available at:
https://escholarship.org/uc/item/9277j4jm accessed 5 May 2021.
76
Garnier, M., Jagoueix-Eveillard, S., Cronje, P.R., Le Roux, H.F. and Bove, J.M. (2000) Genomic characterization of
a liberibacter present in an ornamental rutaceous tree, Calodendrum capense, in the Western Cape
province of South Africa. Proposal of ‘Candidatus Liberibacter africanus subsp. capensis’. International
Journal
of
Systematic
and
Evolutionary
Microbiology
50(6),
2119–2125.
https://doi.org/10.1099/00207713-50-6-2119
Gasparoto, M.C.G., Coletta-Filho, H.D., Bassanezi, R.B., Lopes, S.A., Lourenço, S.A. and Amorim, S.A. (2012)
Influence of temperature on infection and establishment of ‘Candidatus Liberibacter americanus' and
‘Candidatus Liberibacter asiaticus' in citrus plants. Plant Pathology 61, 658–664.
https://doi.org/10.1111/j.1365-3059.2011.02569.x
Gebeyehu, S., Grout, T., Fourie P. and and Hattingh, V. (2020) HLB now in Kenya: Preparations to mitigate its
impact on the southern African citrus industry. CRI (Citrus Research International) Cutting edge, securing
the future of citrus through science. CRI no. 296, May 2020, p7. Available at:
https://www.crw.org.za/home/document-home/extension/cri-the-cutting-edge/cri-the-cutting-edge220-286/6549-cri-cutting-edge-296-2020-hlb-now-in-kenya/file accessed accessed 23 June 2020.
Gitahi, D.W. (2016) Evaluation of Knowledge and Practices of Managing Citrus Pests and Diseases and the
Willingness to pay for an Integrated Pest Management Strategy in Selected Counties in Kenya. MSC
Thesis,
Egerton
University,
Kenya,
55
pp.
Available
from:
http://34.250.91.188:8080/xmlui/handle/123456789/965 accessed 16 June 2021.
Gitahi, R., Kasili, R. Kyallo, M. and Kehlenbeck, K. (2016) Diversity of threatened local mango landraces on
smallholder farms in Eastern Kenya. Forests, Trees and Livelihoods 25(4), 239–254.
https://doi.org/10.1080/14728028.2016.1201436
Gitahi, D.W., Muriithi, B.W., Owuor, G., Diiro, G. and Mohamed, S. (2019) Willingness to pay for an integrated
pest management strategy for suppression of citrus infesting false codling moth, African citrus Trioza and
greening disease among citrus producers in Kenya. Journal of Economics and Sustainable Development
10(2), 44–53.
GIZ (Deutsche Gesellschaft für Internationale Zusammenarbeit) (2015) Citrus growers in Ghana improve their
yields. Available at: https://www.giz.de/en/mediacenter/31804.html accessed 5 December 2020.
Gmitter, F.G., Castle, W.S. and Grosser, J.W. (2010) Mandarin tree named ‘LB8-9’. Florida Foundation Seed
Producers, Inc., Assignee. U.S. Patent No PP 21356.
Gottwald, T.R. (2010) Current epidemiological understanding of citrus huanglongbing. Annual Review of
Phytopathology 48, 119–139. https://doi.org/10.1146/annurev-phyto-073009-114418
Gottwald, T., Graça, J.V.D. and Bassanezi, R.B. (2007) Citrus huanglongbing: The pathogen and its impact. Plant
Health Progress 8(1), 1–36. https://doi.org/10.1094/PHP-2007-0906-01-RV
Gottwald, T.R., Graham, J.H., Irey, M.S., McCollum, T.G. and Wood, B.W. (2012) Inconsequential effect of
nutritional treatments on huanglongbing control, fruit quality, bacterial titer and disease progress. Crop
Protection 36, 73–82.
Gottwald, T., Poole, G., McCollum, T., Hall, D., Hartung, J.B., Luo, W., Posny, D., Duan, Y.P., Taylor, E., da Graça,
J., Polek, M., Louws, F. and Schneider, W. (2020) Canine olfactory detection of a vectored phytobacterial
77
pathogen, Liberibacter asiaticus, and integration with disease control. Proceedings of the National
Academy of Sciences 117(7), 3492–3501. https://doi.org/10.1073/pnas.1914296117
Graça, J.V. (1991) Citrus greening disease. Annual Review of Phytopathology 29, 109–136.
Graça, J.V. (2008) Biology, history and world status of huanglongbing. In: Taller Internacional sobre
Huanglongbing de los cítricos (Candidatus Liberibacter spp.) y el psílido asiático de los cítricos (Diaphorina
citri), 7–9 May 2008, Hermosilla, Sonora, Mexico. Concitver, Martinez de la Torrre, Veracruz, Mexico, 7
pp. Available at: http://www.concitver.com/huanglongbingYPsilidoAsiatico/Indice.html accessed 8 June
2021.
Graça J.V. and Korsten, L. (2004) Citrus huanglongbing: Review, present status and future strategies. In: Naqvi,
S.A.M.H. (ed.) Diseases of Fruits and Vegetables. Volume I Diagnosis and Management. Springer,
Netherlands, pp. 229–245. https://doi.org/10.1007/1-4020-2606-4
Graça, J.V., Douhan, G.W., Halbert, S.E., Keremane, M.J., Lee, R.F., Vidalakis, G., Zhao, H. (2016) Huanglongbing:
An overview of a complex pathosystem ravaging the world’s citrus: Citrus huanglongbing. Journal of
Integrative Plant Biology 58(4), 373–387. https://doi.org/10.1111/jipb.12437
Grafton-Cardwell, E.E., Stelinski, L.L. and Stansly, P.A. (2013) Biology and management of Asian citrus psyllid,
vector of the huanglongbing pathogens. Annual Review of Entomology 58, 413–432.
https://doi.org/10.1146/annurev-ento-120811-153542
Ha, P.T., He, R., Killiny, N., Brown, J.K., Omsland, A., Gang, D.R. and Beyenal, H. (2019) Host-free biofilm culture
of “Candidatus Liberibacter asiaticus,” the bacterium associated with huanglongbing. Biofilm 1, 100005.
https://doi.org/10.1016/j.bioflm.2019.100005
Halbert, S.E. and Manjunath, K.L. (2004) Asian citrus psyllids (Steronrryncha: Psyllidae) and greening disease of
citrus: a literature review and assessment of risk in Florida. Florida Entomologist 87, 330–353.
Hall, D.G. (2008) Biological control of Diaphorina citri. In: I Taller Internacional sobre Huanglongbing de los cítricos
(Candidatus Liberibacter spp.) y el psílido asiático de los cítricos (Diaphorina citri), 7–9 May 2008,
Hermosilla, Sonora, Mexico. Concitver, Martinez de la Torrre, Veracruz, Mexico, 7 pp. Available at:
https://www.ars.usda.gov/ARSUserFiles/35403/Hallpsyllidbiocontrol2008.pdf accessed 5 May 2021.
Hall, D.G. and Hentz, M.G. (2010) Sticky traps and stem-tap sampling protocols for the Asian citrus psyllid
(Hemiptera: Psyllidae). Journal of Economic Entomology 103, 541–549.
Hall, D.G., Gottwald, T.R., Chau, N.M., Ichinose, K., Dien, L.Q. and Beattie, G.A.C. (2008) Greenhouse
investigations on the effect of guava on infestations of Asian citrus psyllid in citrus. Proceedings of the
Florida State Horticultural Society 121, 104–109.
Hall, D.G., Sétamou, M. and Mizell, R.F. III (2010) A comparison of sticky traps for monitoring Asian citrus psyllid
(Diaphorina citri Kuwayama). Crop Protection 29, 1341–1346.
Hall, D., Richardson, M., El-Desouky, A. and Halbert, S. (2012) Asian citrus psyllid, Diaphorina citri, vector of citrus
huanglongbing disease. Entomologia Experimentalis et Applicata 146, 207–222.
Hall, D.G., Albrecht, U. and Bowman, K.D. (2016) Transmission rates of ‘Ca. Liberibacter asiaticus’ by Asian citrus
psyllid are enhanced by the presence and developmental stage of citrus flush. Journal of Economic
Entomology 109, 558–563.
78
Hattingh, V. (1994) IPM on citrus in southern Africa. Citrus Journal 4(3), 21–24.
HCDA (2014) Horticulture validated report. Horticultural Crops Directorate of Agriculture Food Authority,
Kenya, pp.68. Available at: https://vdocuments.mx/horticulture-validated-report-afa-agriculture-andfood-horticulture.html accessed 14 July 2020.
Hocquellet, A., Toorawa, P., Bové, J.M. and Garnier, M. (1999) Detection and identification of the two
“Candidatus Liberobacter sp.” associated with citrus huanglongbing by PCR amplification of ribosomal
protein genes of the beta operon. Molecular and Cellular Probes 13, 373–379.
https://doi.org/10.1006/mcpr.1999.0263
Hoddle, M.S. (2012) Foreign exploration for natural enemies of Asian citrus psyllid, Diaphorina citri (Hemiptera:
Psyllidae), in the Punjab of Pakistan for use in a classical biological control program in California USA.
Pakistan Entomologist 34(1), 1–5.
Hoddle, M.S. and Pandey, R. (2014) Host range testing of Tamarixia radiata (Hymenoptera: Eulophidae) sourced
from the Punjab of Pakistan for classical biological control of Diaphorina citri (Hemiptera: Liviidae:
Euphyllurinae: Diaphorinini) in California. Journal of Economic Entomology 107, 125–136.
https://doi.org/10.1603/EC13318
Hodges, A.W., Rahmani, M., Stevens, T.J. and Spreen, T.H. (2014) Economic Impacts of the Florida Citrus
Industry in 2012-2013. Final sponsored project to the Florida Department of Citrus. Food and Resource
Economics Department, Gainesville, FL. Available at: http://www.fred.ifas.ufl.edu/pdf/economicimpact-analysis/Economic_Impacts_Florida_Citrus_Industry_2012-13.pdf accessed 12 June 2020.
Hodges, A.W. and Spreen, T.H. (2015) Economic impacts of citrus greening (HLB) in Florida, 2006/07–2010/11.
EDIS document FE903. Institute of Food and Agricultural Sciences, University of Florida, Gainesville, FL,
USA, 6 pp.
Hu, J. and Wang, N. (2016) Evaluation of the spatiotemporal dynamics of oxytetracycline and its control effect
against citrus huanglongbing via trunk injection. Phytopathology 106, 1495–1503.
Hu, J., Jiang, J. and Wang, N. (2017) Control of citrus huanglongbing via trunk injection of plant defense activators
and antibiotics. Phytopathology 108(2), 186–195. https://doi.org/10.1094/PHYTO-05-17-0175-R
Huang, C., Chen, M. and Chiu, R. (1980) Separation of a mycoplasma like organism from the likubin complex in
citrus. Plant Disease 64, 564–566.
Huang, C., Araujo, K., Niño Sánchez, J., Kund, G., Trumble, J., Roper, C., Elvin K. and Hailing-Jin, G. (2021) A stable
antimicrobial peptide with dual functions of treating and preventing citrus huanglongbing. Proceedings
of the National Academy of Sciences 118(6), e2019628118. https://doi.org/10.1073/pnas.2019628118
Ibarra-Cortés, K.H., Guzmán-Franco, A.W., González-Hernández, H., Ortega-Arenas, L.D., Villanueva-Jiménez, J.A.
and Robles-Bermúdez, A. (2018) Susceptibility of Diaphorina citri (Hemiptera: Liviidae) and its parasitoid
Tamarixia radiata (Hymenoptera: Eulophidae) to entomopathogenic fungi under laboratory conditions.
Neotropical Entomology 47, 131–138. https://doi.org/10.1007/s13744-017-0539-6
Ignoffo, C. (1992) Environmental factors affecting persistence of entomopathogens. Florida Entomologist 75(4),
516–525. https://doi.org/10.2307/3496133
79
IMF (International Monetary Fund) (2009) Burundi: Poverty Reduction Strategy Paper—Annual Progress Report—
Joint Staff Advisory Note Country Report No. 09/91. Publication Services 700 19th Street, N.W.
Washington, D.C. 20431 10 pp. Available at: Burundi: Poverty Reduction Strategy Paper—Annual
Progress Report— Joint Staff Advisory Note; IMF Country Report 09/91; January 6, 2009 accessed 30 July
2020.
Inoue, H., Ohnishi, J., Ito, T., Tomimura, K., Miyata, S., Iwanami, T. and Ashihara, W. (2009) Enhanced proliferation
and efficient transmission of Candidatus Liberibacter asiaticus by adult Diaphorina citri after acquisition
feeding in the nymphal stage. Annals of Applied Biology 155(1), 29–36. https://doi.org/10.1111/j.17447348.2009.00317.x
Irey, M.S., Gast, T. and Snively, J. (2008) Economic impact of managing huanglongbing in groves at southern
gardens citrus. In: I Taller Internacional sobre Huanglongbing de los cítricos (Candidatus Liberibacter spp.)
y el psílido asiático de los cítricos (Diaphorina citri), 7–9 May 2008, Hermosilla, Sonora, Mexico. Concitver,
Martinez
de
la
Torrre,
Veracruz,
Mexico,
7
pp.
Available
at:
http://www.concitver.com/huanglongbingYPsilidoAsiatico/Memor%C3%83%C2%ADa-12%20Irey.pdf
accessed 5 May 2021.
Izamuhaye, J.C. (2008) Explorative Study on Citrus Farming systems A Case of Tanga Region. Master in Agricultural
Production Chain Management thesis. Wageningen UR, Netherlands, 69 pp.
Jackson, D.L., Jarosik, V. and Dixon, A.F.G. (1996) Resource partitioning and tolerance of monoterpenes in four
species of spruce aphid. Physiological Entomology 21, 242–246.
Jagoueix, S., Bové, J.M. and Garnier, M. (1994) The phloem-limited bacterium of greening disease of citrus is a
member of the α subdivision of the Proteobacteria. International Journal of Systematic Bacteriology 44,
379–386.
Jagoueix, S., Bové, J.M. and Garnier, M. (1996) PCR detection of the two ‘Candidatus’ liberobacter species
associated with greening disease of citrus. Molecular and Cellular Probes 10, 43–50.
https://doi.org/10.1006/mcpr.1996.0006
Jagoueix, S., Bové, J.M. and Garnier, M. (1997) Comparison of the 16S/23S ribosomalintergenic regions of
“Candidatus Liberobacter asiaticum” and “Candidatus Liberobacter africanum”, the two species
associated with citrus huanglongbing (greening) disease. International Journal of Systematic Bacteriology
47, 224–227.
Jones, M.N., Stansly, P.A. and Russo, J. (2013) Extension model to improve Asian citrus psyllid control in citrus
health management areas (CHMAs). Proceedings of the Florida State Horticultural Society 126, 1–4.
Available at: https://swfrec.ifas.ufl.edu/hlb/database/pdf/5_Jones_13.pdf accessed 16 June 2021.
Juan-Blasco, M., Qureshi, J.A., Urbaneja, A. and Stansly, P.A. (2012) Predatory mite, Amblyseius swirskii (Acari:
Phytoseiidae), for biological control of Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae). Florida
Entomologist 95, 543–551.
Kalyebi, A., Aisu, G., Ramathani, I., Ogwang, J., McOwen, N. and Russell, P. (2016) Detection and identification of
etiological agents (Liberibacter spp.) associated with citrus greening disease in Uganda. Uganda Journal
of Agricultural Sciences 16, 43–54. https://doi.org/10.4314/ujas.v16i1.4
80
Khalid, M.S., Malik, A.U., Saleem, B.A., Khan A.S. and Javed, N. (2012) Horticultural mineral oil application and
tree canopy management improve cosmetic fruit quality of Kinnow mandarin. African Journal of
Agricultural Research 7(23), 3464–3472.
Khan, A.A., Afzal, M., Qureshi, J.A., Khan, A.M. and Raza, A.M. (2014) Botanicals, selective insecticides, and
predators to control Diaphorina citri (Hemiptera: Liviidae) in citrus orchards. Insect Science 21(6), 717–
726. https://doi.org/10.1111/1744-7917.12173
Kilalo, D., Olubayo, F., Obukosia, S. and Shibairo, S.I. (2009) Farmer management practices of citrus insect pests
in Kenya. African Journal of Horticultural Science 2, 168–176.
Killiny, N. and Kishk, A. (2017) Delivery of dsRNA through topical feeding for RNA interference in the citrus sap
piercing-sucking hemipteran, Diaphorina citri. Archives of Insect Biochemistry and Physiology 95(2),
e21394. https://doi.org/10.1002/arch.21394
Killiny, N., Hajeri, S., Tiwari, S., Gowda, S. and Stelinski, L.L. (2014) Double-stranded RNA uptake through topical
application, mediates silencing of five CYP4 genes and suppresses insecticide resistance in Diaphorina
citri. PLoS One 9(10), e110536. https://doi.org/10.1371/journal.pone.0110536
Kishk, A., Anber, H.A.I., AbdEl-Raof, T.K., El-Sherbeni, A.E.H.D., Hamed, S., Gowda, S. and Killiny, N. (2017a) RNA
interference of carboxyesterases causes nymph mortality in the Asian citrus psyllid, Diaphorina citri.
Archives of Insect Biochemistry and Physiology 94, e21377. https://doi.org/10.1002/arch.21394
Kishk, A., Hijaz, F., Anber, H.A., AbdEl-Raof, T.K., El-Sherbeni, A-H.D., Hamed, S., Killiny, N. 2017b RNA interference
of acetylcholinesterase in the Asian citrus psyllid, Diaphorina citri, increases its susceptibility to
carbamate and organophosphate insecticides. Pesticide Biochemistry Physiology 143, 81–89.
Kistner, E.J., Amrich, R., Castillo, M., Strode, V. and Hoddle, M.S. (2016a) Phenology of Asian citrus psyllid
(Hemiptera: Liviidae), with special reference to biological control by Tamarixia radiata, in the residential
landscape of Southern California. Journal of Economic Entomology 109(3), 1047–1057.
https://doi.org/10.1093/jee/tow021
Kistner, E.J., Melhem, N., Carpenter, E., Castillo, M. and Hoddle, M.S. (2016b) Abiotic and biotic mortality factors
affecting Asian citrus psyllid (Hemiptera: Liviidae) demographics in Southern California. Annals of the
Entomological Society of America 109(6), 860–871.
Knoema (2020a) Djibouti - Citrus fruit production quantity 2008-2019 - knoema.com. [online] Available at:
https://knoema.com/atlas/Djibouti/topics/Agriculture/Crops-Production-Quantity-tonnes/Citrus-fruitproduction accessed 30 July 2020.
Knoema (2020b) South Sudan - Citrus fruit production quantity 2012-2019 – knoema.com. [online] Available at:
https://knoema.com/atlas/South-Sudan/topics/Agriculture/Crops-Production-Quantity-tonnes/Citrusfruit-production accessed 30 July 2020.
Koh, E.J., Zhou, L., Williams, D.S., Park, J., Ding, N., Duan, Y.P. and Kang, B.H. (2012) Callose deposition in the
phloem plasmodesmata and inhibition of phloem transport in citrus leaves infected with “Candidatus
Liberibacter asiaticus”. Protoplasma 249, 687–697.
Kongai, H., Mangisoni, J., Elepu, G., Chilembwe, E. and Makoka, D. (2018) Analysis of citrus value chain in eastern
Uganda. African Crop Science Journal 26, 417–431. https://doi.org/10.4314/acsj.v26i3.7
81
Korsten, L., Jagoueix, S., Bové, J. and Garnier, M. (1996) Huanglongbing (greening) detection in South Africa.
International Organization of Citrus Virologists Conference Proceedings 13, 395–398. Available from
https://escholarship.org/uc/item/83922200 accessed 16 June 2021.
Kuhlmann, B. and Jacques, D.F. (2002) Classifications, standards and nomenclature ⎯ mineral oils, agricultural
mineral oils and horticultural mineral oils. In: Beattie, G.A.C., Watson, D.M., Stevens, M.L., Rae, D.J. and
Spooner-Hart, R.N. (eds) Spray Oils Beyond 2000: Sustainable Pest and Disease Management. University
of Western Sydney, Sydney, Australia, pp. 29–38.
Kuhns, E.H., Martini, X., Hoyte, A. and Stelinski, L.L. (2016) Repellent activity of botanical oils against Asian citrus
psyllid, Diaphorina citri (Hemiptera: Liviidae). Insects 7(3), 35. https://doi.org/10.3390/insects7030035
Kyalo, R., Abdel-Rahman, E.M., Mohamed, S.A., Ekesi, S., Borgemeister, C. and Landmann, T. (2018) Importance
of remotely-sensed vegetation variables for predicting the spatial distribution of African citrus triozid
(Trioza
erytreae)
in
Kenya.
International
Journal
of
Geo-Information
7,
429.
https://doi.org/10.3390/ijgi7110429
Lacirignola, C. and D’Onghia, A.M. (2009) The Mediterranean citriculture: productions and perspectives. In:
D’Onghia, A.M., Djelouah, K. and Roistacher, C.N. (eds.) Citrus tristeza virus and Toxoptera citricidus: a
serious threat to the Mediterranean citrus industry. Options Méditerranéennes: Série B. Etudes et
Recherches. 65. Le Centre International de Hautes Etudes Agronomiques Mediterraneennes (CIHEAM),
Bari, Italy, pp. 13–17. Available from: http://om.ciheam.org/om/pdf/b65/b65.pdf accessed 16 June
2021.
Lallemand, J., Fos, A. and Bove, J.M. (1986) Transmission de la bacterie associee al a forme africaine de la maladie
du “greening” par le psylla asiatique Diaphorina citri Kuwayama. Fruits 41, 341–343.
Lansford, T. (2017) Political Handbook of the World 2016–2017. University of Southern Mississippi, CQ Press,
Mississippi, USA, 976 pp.
Larkin, P. (2021) Farmers on high alert as Asian Citrus Green disease spreads. Independent Online, (IOL).
Available at: https://www.iol.co.za/business-report/economy/farmers-on-high-alert-as-asian-citrusgreen-disease-spreads-4ac0c8cc-5936-437a-90be-2b2c919a26a8 accessed 12 March 2021.
Lee, J.A., Halbert, S.E., Dawson, W.O., Robertson, C.J., Keesling, J.E. and Singer, B.H. (2015) Asymptomatic spread
of huanglongbing and implications for disease control. Proceedings of the National Academy of Sciences
of the United States of America 112(24), 7605–7610.
Lewis-Rosenblum, H., Martini, X., Tiwari, S. and Stelinski, L.L. (2015) Seasonal movement patterns and long-range
dispersal of Asian citrus psyllid in Florida citrus. Journal of Economic Entomology 108, 3–10.
Lezama-Gutiérrez, R., Molina-Ochoa, J., Chávez-Flores, O., Ángel-Sahagún, C.A., Skoda, S.R., Reyes-Martínez, G.,
Barba-Reynoso, M., Rebolledo-Domínguez, O., Ruíz-Aguilar, G.M.L. and Foster, J.E. (2012) Use of the
entomopathogenic fungi Metarhizium anisopliae, Cordyceps bassiana and Isaria fumosorosea to control
Diaphorina citri (Hemiptera: Psyllidae) in Persian lime under field conditions. International Journal of
Tropical Insect Science 32(1), 39–44.
Liao, H.K. and Burns, J. (2012) Gene expression in Citrus sinensis fruit tissues harvested from huanglongbinginfected trees: comparison with girdled fruit. Journal of Experimental Botany 63, 3307–3319.
https://doi.org/10.1093/jxb/ers070
82
Lin, K.H. (1956) Yellow shoot disease (huanglongbing) of citrus (in Chinese). Preliminary observations on the
disease. Investigations on the cause of the disease. Natural transmission and spread of the disease. Acta
Phytopathologica Sinica 2, 1–11 and 14–38.
Liu, T.X. and Stansly, P.A. (1995) Toxicity and repellency of some biorational insecticides to Bemisia argentifolii
on tomato plants. Entomologia Experimentalis et Applicata 74, 137–143.
Lopez, J.A. and Durborow, S.L. (2015) Huanglongbing and the California citrus industry: A cost comparison of do
nothing vs. do something management practices. Texas Journal of Agriculture and Natural Resources 27,
51–68.
Magomere, T.O., Obukosia, S., Mutitu, E., Ngichabe C., Olubayo, F. and Shibairo, S. (2009) PCR detection and
distribution of huanglongbing disease and psyllid vectors on citrus varieties with changes in elevation in
Kenya. Journal of Biological Sciences 9(7), 697–709. https://doi.org/10.3923/jbs.2009.697.709
Majeed, M.Z., Fiaz, M., Ma, C.-S. and Afzal, M. (2017) Entomopathogenicity of three muscardine fungi, Beauveria
bassiana, Isaria fumosorosea and Metarhizium anisopliae, against the Asian citrus psyllid, Diaphorina citri
Kuwayama (Hemiptera: Psyllidae). Egyptian Journal of Biological Pest Control 27(2), 211–215.
Makorere, R. (2014) An exploration of factors affecting development of citrus industry in Tanzania: Empirical
evidence from Muheza District, Tanga Region. International Journal of Food and Agricultural Economics
2, 135–154.
Mankin R.W., Rohde, B.B. and McNeill, S.A. (2016) Vibrational duetting mimics to trap and disrupt mating of the
devastating Asian citrus psyllid insect pest. Proceedings of Meetings on Acoustics 25(1), 010006.
https://doi.org/10.1121/2.0000185
Mann, R.S., Rouseff, R.L., Smoot, J.M., Castle, W.S. and Stelinski, L.L. (2011) Sulfur volatiles from Allium spp. affect
Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae), response to citrus volatiles.
Bulletin of Entomological Research 101, 89–97.
Mann, R.S., Ali, J.G., Hermann, S.L., Tiwari, S., Pelz-Stelinski, K.S., Alborn, H.T. and Stelinski, L.L. (2012) Induced
release of a plant-defense volatile ‘deceptively’ attracts insect vectors to plants infected with a bacterial
pathogen. PLoS Pathogens 8, e1002610. https://doi.org/10.1371/journal.ppat.1002610
Martinelli, F. and Dandekar, A.M. (2017) Genetic mechanisms of the devious intruder Candidatus Liberibacter in
citrus. Frontiers of Plant Science 8, 904. https://doi.org/10.3389/fpls.2017.00904
Martini, X., Addison, T., Fleming, B., Jackson, I., Pelz-Stelinski, K. and Stelinski, L.L. (2013) Occurrence of
Diaphorina citri (Hemiptera: Liviidae) in an unexpected ecosystem: The Lake Kissimmee State Park Forest,
Florida. Florida Entomologist 96, 658–660.
Martini X., Hoyte, A. and Stelinski, L.L. (2014) Abdominal color of the Asian citrus psyllid (Hemiptera: Liviidae) is
associated with flight capabilities. Annals of the Entomological Society of America 107, 842–847.
Martini X., Pelz-Stelinski, K.S. and Stelinski L.L. (2015) Absence of windbreaks and replanting citrus in solid sets
increase density of Asian citrus psyllid populations. Agriculture, Ecosystems and Environment 212, 168–
174.
83
Martini, X., Willett, D.S., Kuhns, E.H. and Stelinski, L.L. (2016) Disruption of vector host preference with plant
volatiles may reduce spread of insect-transmitted plant pathogens. Journal of Chemical Ecology 42, 357–
367. https://doi.org/10.1007/s10886-016-0695-x
Massonie, G., Garnier, M. and Bové, J.M. (1976) Transmission of Indian citrus decline by Trioza erytreae (Del
Guercio), the vector of South African greening. In: Calavan, E.C. (ed.) Proceedings, International
Organization of Citrus Virologists Conference. University of California, Riverside, CA, USA, pp. 18–20.
Masuoka, Y., Pustika, A., Subandiyah, S., Okada, A., Hanundin, E., Purwanto, B., Okuda, M., Okada, Y., Saito, A.,
Holford, P., Beattie, A. and Iwanami, T. (2011) Lower concentrations of microelements in leaves of citrus
infected with ‘Candidatus Liberibacter asiaticus'. Japan Agricultural Research Quarterly: JARQ 45, 269–
275. https://doi.org/10.6090/jarq.45.269
McClean, A.P.D. and Oberholzer, P.C.J. (1965) Citrus psylla, a vector of the greening disease of sweet orange.
South African Journal of Agricultural Science 8, 297–298.
McClean, A.P.D. and Schwarz, R.E. (1970) Greening or blotchy-mottle disease of citrus. Phytophylactica 2, 177–
194.
McCollum, G. and Baldwin, E. (2017) Huanglongbing: devastating disease of citrus. In Janick, J. (ed.) Horticultural
Reviews
44.
John
Wiley
and
Sons,
Hoboken,
NJ,
USA,
pp.
315–361.
https://doi.org/10.1002/9781119281269.ch7
McCoy, C.W. (1985) Citrus: current status of biological control in Florida. In: Hoy, M.A. and Herzog, D.C. (eds)
Biological Control in Agricultural IPM System. Academic Press, Orlando, FL, USA, pp. 481–499.
McDaniel, J.R. and Moran, V.C. (1972) The parasitoid complex of the citrus psylla Trioza erytreae (Del Guercio)
[Homoptera: Psyllidae]. Entomophaga 17, 297–317.
McKenna, M. (2019) Antibiotics set to flood Florida’s troubled orange orchards. Nature 567, 302–303.
https://doi.org/10.1038/d41586-019-00878-4
Meyer, J.M., Hoy, M.A. and Boucias, D.G. (2007) Morphological and molecular characterization of a Hirsutella
species infecting the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae), in Florida.
Journal of Invertebrate Pathology 95(2), 101–109.
Meyer, J.M., Hoy, M.A. and Boucias, D.G. (2008) Isolation and characterization of an Isaria fumosorosea isolate
infecting the Asian citrus psyllid in Florida. Journal of Invertebrate Pathology 99, 96–102.
Michaud, J.P. (2002) Biological control of Asian citrus psyllid, Diaphorina citri in Florida – a preliminary report.
Entomological News 113, 216–222.
Michaud, J.P. (2004) Natural mortality of Asian citrus psyllid (Homoptera: Psyllidae) in Central Florida. Biological
Control 29, 260–269. https://doi.org/10.1016/S1049-9644(03)00161-0
Michaud, J.P. and Olsen, L. (2004) Suitability of Asian citrus psyllid, Diaphorina citri (Homoptera: Psyllidae) as
prey for lady beetles (Coleoptera: Coccinellidae). BioControl 49, 417–431.
Miles, G.P., Stover, E. Ramadugu, C., Manjunath, Keremane M.L. and Lee R.F. (2017) Apparent tolerance to
huanglongbing
in
Citrus
and
Citrus-related
germplasm.
HortScience
52,
31–39.
https://doi.org/10.21273/HORTSCI11374-16
84
Milosavljević, I., Schall, K., Hoddle, C., Morgan, D.P. and Hoddle, M. (2017) Biocontrol program targets Asian citrus
psyllid
in
California’s
urban
areas.
California
Agriculture
71,
169–177.
https://doi.org/10.3733/ca.2017a0027
Ministry of Agriculture (1995) Eritrea: country report to the FAO international technical conference on plant
genetic resources (Leipzig, 1996). Prepared by Ministry of Agriculture Asmara, August 1995 pp. 25
Available at:
http://www.fao.org/fileadmin/templates/agphome/documents/PGR/SoW1/africa/ERITREA.pdf
accessed 22 June 2020.
Miranda, M.P., Volpe, H.X.L., Veiga, A.C., Zanardi, O.Z., Bassanezi, R.B., Andrade, D.J. and Sousa, M.C. (2017)
Manejo de insetos e ácaros vetores de fitopatógenos nos citros. Informe Agropecuário 38, 83–93.
Miranda, M., Zanardi, O., Tomaseto, A., Volpe, H., Garcia, R. and Prado, E. (2018) Processed kaolin affects the
probing and settling behavior of Diaphorina citri (Hemiptera: Lividae). Pest Management Science 74(8),
1964–1972.
Miranda, S.H.G., Adami, A.C.O. and Bassanezi, R.B. (2012) Economic impacts of huanglongbing disease in Sao
Paulo State. International Association of Agricultural Economists (IAAE) Triennial Conference, Foz do
Iguaçu,
Brazil,
18–24
August,
2012.
Available
at:
https://swfrec.ifas.ufl.edu/hlb/database/pdf/00002960.pdf accessed 4 May 2021.
MMA (Match Maker Associates Limited) (2008) Citrus for local and regional markets sub sector quick scan
Tanzania. Match Maker Associates Limited, Arusha, Tanzania, 22 pp. Available at:
http://www.tzdpg.or.tz/fileadmin/_migrated/content_uploads/Citrus_for_local_and_regional_markets
_-_Quick_scan_-_Final_draft.pdf accessed 4 May 2021.
Monzo, C. and Stansly, P.A. (2017) Economic injury levels for Asian citrus psyllid control in process oranges from
mature trees with high incidence of huanglongbing. PLoS ONE 12, e0175333.
https://doi.org/10.1371/journal.pone.0175333
Monzo, C. and Stansly, P.A. (2020) Economic value of conservation biological control for management of the
Asian citrus psyllid, vector of citrus huanglongbing disease. Pest Management Science 76, 1691–1698.
https://doi.org/10.1002/ps.5691
Moran, V.C. (1968) Preliminary observations on the choice of host plants by adults of citrus psylla, Trioza erytreae
(Del Guercio) (Homoptera: Psyllidae). Journal of the Entomological Society of South Africa 31, 403–410.
Moran, V.C. and Blowers, J.R. (1967) On the biology of the South African citrus psylla, Trioza erytreae (Del
Guercio) (Homoptera: Psyllidae). Journal of the Entomological Society of South Africa 30, 96–106.
Moreira, A.S., Stuchi, E.S., Silva, P.R.B., Bassanezi, R.B., Girardi, E.A. and Laranjeira, F.F. (2019) Could tree density
play a role in managing Citrus huanglongbing epidemics? Tropical Plant Pathology 44, 268–274.
Mulaa, M., Cherunya, A., Wanyama, J. and Mugita, A. (2009) Screening citrus rootstock/scion combinations for
tolerance to major pests and diseases in North Rift Kenya. Acta Horticulturae 911, 223–226.
https://doi.org/10.17660/ActaHortic.2011.911.22
Muraro, R.P. (2012) Evolution of citrus disease management programs and their economic implications: The case
of Florida’s citrus industry. Proceedings of the Florida State Horticulture Society 125, 126–129.
85
Muriithi, B., Affognon, H., Diiro, G., Kingori, S., Tanga, C., Nderitu, P., Mohamed, S. and Ekesi, S. (2016) Impact
assessment of Integrated Pest Management (IPM) strategy for suppression of mango-infesting fruit flies
in Kenya. Crop Protection 81, 20–29. https://doi.org/10.1016/j.cropro.2015.11.014
Narouei-Khandan, H.A., Halbert, S.E., Worner, S.P. and van Bruggen, A.H.C. (2016) Global climate suitability of
citrus huanglongbing and its vector, the Asian citrus psyllid, using two correlative species distribution
modeling approaches, with emphasis on the USA. European Journal of Plant Pathology 144, 655–670.
https://doi.org/10.1007/S10658-015-0804-7
Naqvi, S.D.Y., Rao, G.S., Kiflemariam, W.B. and Guesh, D. (2016) A survey on incidence and severity of citrus
gummosis caused by Phytophthora species in Zoba Anseba. Eritrea Journal of Eco-friendly Agriculture
11(2), 158–163.
National Academies of Sciences, Engineering, and Medicine (2018) A Review of the Citrus Greening Research and
Development Efforts Supported by the Citrus Research and Development Foundation: Fighting a Ravaging
Disease. The National Academies Press, Washington, DC, USA, 288 pp. https://doi.org/10.17226/25026
National Agriculture Advisory Services (NAADS) (2018) Pest and diseases in oranges. Available at:
https://naads.or.ug/pests-and-diseases-in-oranges/ accessed 30 July 2020.
National Biodiversity Strategy and Action Plan (Sudan) (NBSAP) (2000) Part 2. [online] Available
at: https://www.cbd.int/doc/world/sd/sd-nbsap-01-p2-en.pdf). 71 pp. accessed 30 July 2020.
National Research Council (2010) Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening
Disease. The National Academies Press, Washington, DC, USA, pp. 328 https://doi.org/10.17226/12880
Negash, T. (1997) Eritrea and Ethiopia: The Federal Experience. Routledge, London, UK, 225 pp.
Njoroge, S.M., Lan Phi, N.T. and Sawamura, M. (2009) Chemical composition of peel essential oils of sweet
oranges (Citrus sinensis) from Uganda and Rwanda. Journal of Essential Oil-Bearing Plants 12(1), 26–33.
Nwugo, C.C., Duan, Y. and Lin, H. (2013) Study on citrus response to huanglongbing highlights a down-regulation
of defense-related proteins in lemon plants upon “Ca. Liberibacter asiaticus” infection. PLoS One 8,
e67442. https://doi.org/10.1371/journal.pone.0067442
Nyambo, B. and Verschoor, R. (2005) Partnership for market access; towards a sustainable market-oriented
horticultural sector in Tanzania. Wageningen UR Position Paper, 42 pp. Available at:
https://research.wur.nl/en/publications/partnership-for-market-access-towards-a-sustainable-marketorient-5 accessed 5 May 2021.
Oberholzer, P.C.J., von Staden, D.F.A. and Basson, W.J. (1963) Greening disease of sweet orange in South Africa.
International Organization of Citrus Virologists Conference Proceedings 3, 213–219. Available at:
https://escholarship.org/uc/item/2jb2v3kb accessed 5 May 2021.
Oke, A.O., Oladigbolu, A.A., Kunta, M., Alabi, O.J. and Sétamou, M. (2020) First report of the occurrence of Asian
citrus psyllid Diaphorina citri (Hemiptera: Liviidae), an invasive species in Nigeria, West Africa. Scientific
Reports 10, 9418. https://doi.org/10.1038/s41598-020-66380-4
Ou, D., Zhang, L.H., Guo, C.F., Chen, X.S., Ali, S. and Qiu, B.L. (2018) Identification of a new Cordyceps javanica
fungus isolate and its toxicity evaluation against Asian citrus psyllid. MicrobiologyOpen 8(6), e00760.
https://doi.org/10.1002/mbo3.760
86
Otieno, J. (2015) Citrus fruit growers in Kenya, Tanzania get $1.34m for pest and disease project. The EastAfrican.
Published 9 May 2015. Available at: Citrus fruit growers in Kenya, Tanzania get $1.34m for pest and
disease project - Kenya | ReliefWeb accessed 1 June 2020.
Ouma, G. (2008) Challenges and approaches to sustainable citrus production in Kenya. The African Journal of
Plant Science and Biotechnology 2(2), 49–51.
Ouyang, G., Fang, X., Lu, H., Zhou, X., Meng, X., Yu, S., Guo, M. and Xia, Y. (2013) Repellency of five mineral oils
against Diaphorina citri (Hemiptera: Liviidae). Florida Entomologist 96, 974–982.
https://doi.org/10.1653/024.096.0335
Pest Control Products Board (PCPB) (2018) Pest control Products Registered for Use in Kenya [online] pp. 562
Available at: http://cacafrica.com/Public/Home/xiazai/PCPB%20List%20of%20Registered%20Products
%20Version%201_2019.pdf accessed 25 February 2021.
Parsa, S., Morse, S., Bonifacio, A., Chancellor, T., Condori, B., Crespo-Pérez, V., Hobbs, S., Kroschel, J., Ba, M.,
Rebaudo, F., Sherwood, S., Vanek, S., Faye, E., Herrera, M. and Dangles, O. (2014) Obstacles to integrated
pest management adoption in developing countries. Proceedings of the National Academy of Sciences of
the United States of America 111(10), 3889–3894. https://doi.org/10.1073/pnas.1312693111
Pelz-Stelinski, K.S., Brlansky, R.H., Ebert, T.A. and Rogers, M.E. (2010) Transmission parameters for Candidatus
Liberibacter asiaticus by Asian citrus psyllid (Hemiptera: Psyllidae). Journal of Economic Entomology
103(5), 1531–1541.
Pérez-Rodríguez, J., Krüger, K., Pérez-Hedo, M., Ruíz-Rivero, O., Urbaneja, A. and Ten, A. (2019) Classical biological
control of the African citrus psyllid Trioza erytreae, a major threat to the European citrus industry.
Scientific Reports 9, 9440. https://doi.org/10.1038/s41598-019-45294-w
Phillips, S.J., Anderson, R.P. and Schapire, R.E. (2006) Maximum entropy modelling of species geographic
distributions. Ecological Modelling 190, 231–259.
Pickett, J.A., Wadhams, L.J., Woodcock, C.M. and Hardie, J. (1992) The chemical ecology of aphids. Annual Review
of Entomology 37, 67–90.
Pretorius, M.C. and van Vuuren, S.P. (2006) Managing huanglongbing (citrus greening disease) in the Western
Cape. South African Fruit Journal 5(4), 59–62.
Qureshi, J.A. and Stansly, P.A. (2007) Integrated approaches for managing Asian citrus psyllid Diaphorina citri
(Homoptera: Psyllidae) in Florida. Proceedings of the Florida State Horticultural Society 120, 110–115.
Qureshi, J.A. and Stansly, P. (2009) Exclusion techniques reveal significant biotic mortality suffered by Asian citrus
psyllid Diaphorina citri (Hemiptera: Psyllidae) populations in Florida citrus. Biological Control 50, 129–
136.
Qureshi, J.A. and Stansly, P.A. (2010) Dormant season foliar sprays of broad-spectrum insecticides: An effective
component of integrated management for Diaphorina citri (Hemiptera: Psyllidae) in citrus orchards. Crop
Protection 29, 860–866.
Qureshi, J.A. and Stansly, P.A. (2011) Three homopteran pests of citrus as prey for the convergent lady beetle:
Suitability
and
preference.
Environmental
Entomology
40(6),
1503–1510.
https://doi.org/10.1603/EN11171
87
Qureshi, J.A. and Stansly, P.A (2020) Asian citrus psyllid: Biology, ecology and management of the huanglongbing
vector. CABI, Wallingford, UK, 305 pp.
Qureshi, J.A., Kostyk, B.C. and Stansly, P.A. (2011) Effectiveness of selective insecticides to control Asian citrus
psyllid and citrus leafminer during leaf flushing. Proceedings of the Florida State Horticultural Society 124,
85–89.
Qureshi, J., Khan, A., Jones, M. and Stansly, P. (2013) Management of Asian citrus psyllid in organic citrus groves.
Citrus Industry 94(2), 6–10.
Qureshi, J.A., Kostyk, B.C. and Stansly, P.A. (2014) Insecticidal suppression of Asian citrus psyllid Diaphorina citri
(Hemiptera: Liviidae), vector of huanglongbing pathogens. PLoS ONE 9(12), e112331.
https://doi.org/10.1371/journal.pone.0112331
Rae, D.J., Liang, W.G., Watson, D.M., Beattie, G.A.C. and Huang, M.D. (1997) Evaluation of petroleum spray oils
for control of the Asian citrus psylla, Diaphorina citri (Kuwayama) (Hemiptera: Psyllidae) in China.
International Journal of Pest Management 43, 71–75.
Raiol Jr., L.L., Cifuentes-Arenas, J.C. and Lopes, S.A. (2017) Speed of Candidatus Liberibacter asiaticus movement
in citrus plants. Journal of Citrus Pathology 4, 34–35.
Rasowo, B.A., Khamis, F.M., Mohamed, S.A., Ajene, I.J., Aidoo, O.F., Ombura, L., Sétamou, M., Ekesi, S. and
Borgemeister, C. (2019) African citrus greening disease in East Africa: Incidence, severity, and distribution
patterns. Journal of Economic Entomology 112, 2389–2397. https://doi.org/10.1093/jee/toz167
Razi, M.F., Keremane, M.L., Ramadugu, C., Roose, M., Khan, I.A. and Lee, R.F. (2014) Detection of Citrus
huanglongbing-associated ‘Candidatus Liberibacter asiaticus’ in Citrus and Diaphorina citri in Pakistan,
seasonal variability, and implications for disease management. Phytopathology 104, 257–268.
https://doi.org/10.1094/PHYTO-08-13-0224-R
Regmi, C., Garnier, M. and Bové, J.M. (1996) Detection of the Asian huanglongbing (greening) Liberobacter in
Nepal by DNA-DNA hybridization. International Organization of Citrus Virologists Conference Proceedings
13, 267–270. Available at: https://escholarship.org/uc/item/8bf35665 accessed 5 May 2021.
Richard, K., Abdel-Rahman, E.M., Mohamed, S.A., Ekesi, S., Borgemeister, C. and Landmann, T. (2018) Importance
of remotely-sensed vegetation variables for predicting the spatial distribution of African citrus triozid
(Trioza erytreae) in Kenya. ISPRS International Journal of Geo-Information 7(11), 429.
https://doi.org/10.3390/ijgi7110429
Riera, N., Handique, U., Zhang, Y., Dewdney, M. and Wang, N. (2017) Characterization of antimicrobial-producing
beneficial bacteria isolated from huanglongbing escape citrus trees. Frontiers in Microbiology 8, 2415.
https://doi.org/10.3389/fmicb.2017.02415
Roberts, R. and Pietersen, G. (2016) A novel subspecies of ‘Candidatus Liberibacter africanus’ found on native
Teclea gerrardii (Family: Rutaceae) from South Africa. Antonie van Leeuwenhoek 110, 437–444.
Roberts, R., Steenkamp, E.T. and Pietersen, G. (2015) Three novel lineages of ‘Candidatus Liberibacter africanus’
associated with native rutaceous hosts of Trioza erytreae in South Africa. International Journal of
Systematic and Evolutionary Microbiology 65(2), 723–731. https://doi.org/10.1099/ijs.0.069864-0
88
Roberts, R., Cook, G., Grout, T., Khamis, F., Rwomushana, I., Nderitu, P., Seguni, Z., Materu, C., Steyn, C., Pietersen,
G., Ekesi, S. and Roux, H. (2017) Resolution of the identity of ‘Candidatus Liberibacter’ species from
huanglongbing-affected citrus in East Africa. Plant Disease 101(8), 1481–1488.
Rodriguez-Saona, C., Kaplan, I., Braasch, J., Chinnasamy, D. and Williams, L. (2011) Field responses of predaceous
arthropods to methyl salicylate: a meta-analysis and case study in cranberries. Biological Control 59, 294–
303.
Rohrig, E., Shirk, P.D., Hall, D.G. and Stansly, P.A. (2011) Larval development of Diaphorencyrtus aligarhensis
(Hymenoptera: Encyrtidae), an endoparasitoid of Diaphorina citri (Hemiptera: Psyllidae). Annals of the
Entomological Society of America 104, 50–58.
Roistacher, C.N. (1996) The economics of living with citrus diseases: Huanglongbing (Greening) in Thailand.
International Organization of Citrus Virologists Conference Proceedings 13, 279–285. Available from
https://escholarship.org/uc/item/3kg8m6jr accessed 16 June 2021.
Roka, F., Muraro, R., Morris, R.A., Spyke, P., Morgan, K., Schumann, A., Castle, W. and Stover, E. (2009) Citrus
production systems to survive greening: Economic thresholds. Proceedings of the Florida State
Horticulture Society 122, 122–126.
Rouse, R.E., Ozores-Hampton, M., Roka, F.M. and Roberts, P. (2017) Rehabilitation of huanglongbing-affected
Citrus trees using severe pruning and enhanced foliar nutritional treatments. HortScience 52(7), 972–978.
Rouseff, R.L., Onagbola, E.O., Smoot, J.M. and Stelinski, L.L. (2008) Sulfur volatiles in guava (Psidium guajava L.)
leaves: possible defense mechanism. Journal of Agricultural Food Chemistry 56, 8905–8910.
https://doi.org/10.1021/jf801735v
Rwomushana, I., Khamis, F., Grout, T., Mohamed, S., Sétamou, M., Borgemeister, C., Heya, H., Tanga, C., Nderitu,
P., Seguni, Z., Materu, C. and Ekesi, S. (2017) Detection of Diaphorina citri Kuwayama (Hemiptera:
Liviidae) in Kenya and potential implication for the spread of huanglongbing disease in East Africa.
Biological Invasions 19(10), 2777–2787. https://doi.org/10.1007/s10530-017-1502-5
Saldarriaga, A.J.J., D’Alessandro, C.P., Conceschi, M.R., Mascarin, G.M. and Delalibera Jr, I. (2017) Efficacy of
entomopathogenic fungi against adult Diaphorina citri from laboratory to field applications. Journal of
Pest Science 90, 947–960. https://doi.org/10.1007/s10340-017-0846-z
Santos-Ortega, Y. and Killiny, N. (2018) Silencing of sucrose hydrolase causes nymph mortality and disturbs adult
osmotic homeostasis in Diaphorina citri (Hemiptera: Liviidae). Insect Biochemistry and Molecular Biology
101, 131–143. https://doi.org/10.1016/j.ibmb.2018.09.003
Saponari, M., De Bac, G., Breithaupt, J., Loconsole, G., Yokomi, R.K. and Catalano, L. (2010) First report of
‘Candidatus Liberibacter asiaticus’ associated with huanglongbing in sweet orange in Ethiopia. Plant
Disease 94, 482.
Saraf, N., Barkam, S., Peppler, M., Metke, A., Vázquez-Guardado, A., Singh, S., Emile, C., Bico, A., Rodas, C. and
Seal, S. (2019) Microsensor for limonin detection: An indicator of citrus greening disease. Sensors and
Actuators B: Chemical 283, 724–730. https://doi.org/10.1016/j.snb.2018.12.067
Schwarz, R.E. (1967) Results of a greening survey on sweet orange in the major citrus-growing areas of the
republic of South Africa. South African Journal of Agricultural Science 10, 471–476.
89
Schwartz, R.E. (1975) Technical report on citrus greening in Kenya. KEN 71/528. UNDP Horticultural Crops
Development Project, FAO, Rome, Italy, 14 pp.
Schwarz, R.E. and Green, G.C. (1972) Heat requirements for symptom suppression and inactivation of the
greening pathogen. International Organization of Citrus Virologists Conference Proceedings 5, 44–51.
Available at: https://escholarship.org/uc/item/8x3493ft accessed 5 May 2021.
Sechler, A., Schuenzel, E.L., Cooke, P., Donnua, S., Thaveechai, N., Postnikova, E., Stone, A.L., Schneider, W.L.,
Damsteegt, V.D. and Schaad, N.W. (2009) Cultivation of ‘Candidatus Liberibacter asiaticus’, ‘Ca. L.
africanus’, and ‘Ca. L. americanus’ associated with huanglongbing. Phytopathology 99, 480–486.
Sétamou, M. and Bartels, D.W. (2015) Living on the edges: spatial niche occupation of Asian citrus psyllid,
Diaphorina citri Kuwayama (Hemiptera: Liviidae), in citrus groves. PLoS ONE, 10: e0131917.
https://doi.org/10.1371/journal.pone.0131917
Sétamou, M., Flores, D., French, J.V. and Hall, D.G. (2008) Dispersion patterns and sampling plans for Diaphorina
citri (Hemiptera: Psyllidae) in citrus. Journal of Economic Entomology 101, 1478–1487.
Sétamou, M., Simpson, C.R., Alabi, O.J., Nelson, S.D., Telagamsetty, S. and Jifon, J.L. (2016) Quality matters:
Influences of citrus flush physicochemical characteristics on population dynamics of the Asian citrus
psyllid (Hemiptera: Liviidae). PLoS ONE 11(12), e0168997.
https://doi.org/10.1371/journal.pone.0168997
Sétamou, M., Alabi, O.J. Tofangsazi, N. and Grafton-Cardwell, E. (2018) COPF: Citrus orchard perimeter fencing
as a strategy for reducing Asian citrus psyllid. Journal of Applied Entomology 142(10), 959–966.
https://doi.org/10.1111/jen.12535
Shen, W., Cevallos-Cevallos, J.M., Da Rocha, U.N., Arevalo, H.A., Stansly, P.A., Roberts, P.D. and van Bruggen, A.H.
(2013) Relation between plant nutrition, hormones, insecticide applications, bacterial endophytes, and
Candidatus Liberibacter Ct values in citrus trees infected with huanglongbing. European Journal of Plant
Pathology 137, 727–742. https://doi.org/10.1007/s10658-013-0283-7
Shimwela, M.M., Narouei-Khandan, H.A., Halbert, S.E., Keremane, M.L., Minsavage, G.V., Timilsina, S., Massawe,
D.P., Jones, J.B. and van Bruggen, A.H. (2016) First occurrence of Diaphorina citri in East Africa,
characterization of the Ca. Liberibacter species causing huanglongbing (HLB) in Tanzania, and potential
further spread of D. citri and HLB in Africa and Europe. European Journal of Plant Pathology 146, 349–
368. https://doi.org/10.1007/s10658-016-0921-y
Silva Santos, M., Zanardi, O.Z., Pauli, K.S., Forim, M.R., Yamamoto, P.T. and Vendramin, J.D. (2015) Toxicity of an
azadirachtin-based biopesticide on Diaphorina citri Kuwayama (Hemiptera: Liviidae) and its
ectoparasitoid Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae). Crop Protection 74, 116–123.
Singerman, A. and Useche, P. (2016) Impact of citrus greening on citrus operations in Florida. IFAS Extension
FE983. University of Florida, FL, USA, 4 pp. Available at: http://edis.ifas.ufl.edu/pdffiles/FE/FE98300.pdf
accessed 5 May 2021.
Singerman, A. and Useche, P. (2019) The role of strategic uncertainty in area-wide pest management decisions
of Florida citrus growers. American Journal of Agricultural Economics 101(4), 991–1011.
90
Singerman, A. and Rogers, M.E. (2020) The economic challenges of dealing with citrus greening: the case of
Florida. Journal of Integrated Pest Management 11, 3. https://doi.org/10.1093/jipm/pmz037
Singerman, A., Burani-Arouca, M. and Futch, S.H. (2018) The profitability of new citrus plantings in Florida in the
era of huanglongbing. HortScience 53, 1655–1663. https://doi.org/10.21273/HORTSCI13410-18
Siverio, F., Marco-Noales, E., Bertolini, E., Teresani, G., Peñalver, J., Mansilla, P., Aguín, O., Pérez-Otero, R.,
Abelleira, A., Guerra-García, A., Hernández, E., Cambra, M. and López, M. (2017) Survey of huanglongbing
associated with 'Candidatus Liberibacter' species in Spain: Analyses of citrus plants and Trioza erytreae.
Phytopathologia Mediterranea 56, 98–110. https://doi.org/10.14601/Phytopathol_Mediterr-18679
Skelley, L.H. and Hoy, M.A. (2004) A synchronous rearing method for the Asian citrus psyllid and its parasitoids
in quarantine. Biological Control 29, 14–23.
Spreen, T. and Zansler, M. (2016) Economic Analysis of Incentives to Plant Citrus Trees in Florida. HortTechnology
26, 720-726. https://doi.org/10.21273/HORTTECH03424-16.
Stansly, P.A. and Conner, J.M. (2004) Control of silverleaf whitefly in pepper with horticultural mineral oil and
other insecticides. Arthropod Management Tests 30(1). https://doi.org/10.1093/amt/30.1.E56
Stansly, P. and Rogers, M.E. (2006) Managing Asian citrus psyllid populations. Citrus Industry 87, 17–19.
Stansly, P.A., Arevalo, H.A. and Qureshi, J.A. (2010) Monitoring methods for Asian citrus psyllid. Citrus Industry
Magazine April 2010, 20–22.
Stansly, P.A., Qureshi, J.A. and Kostyk, B.C. (2012) Foliar applications of sulfoxaflor, BYI02960, and some
commonly used insecticides for control of Asian citrus psyllid and citrus leafminer in oranges: Summer,
2011. Arthropod Management Tests 37, 1–2. https://doi.org/10.4182/amt.2012.D7
Stauderman, K., Avery, P., Aristizábal, L. and Arthurs, S. (2012) Evaluation of Isaria fumosorosea (Hypocreales:
Cordycipitaceae) for control of the Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae). Biocontrol
Science and Technology 22, 747–761. https://doi.org/10.1080/09583157.2012.686599
Su, H.J., Cheon, J.U. and Tsai, M.J. (1986) Citrus greening (Likubin) and some viruses and their control trials. In:
Plant Virus Diseases of Horticultural Crops in the Tropics and Subtropics. FFTC Book Series No. 33. Food
and Fertilizer Technology Center for the Asian and Pacific Region, Taiwan, pp. 143–147.
Tamesse J.L., Messi J., Silatsa Soufo E., Kambou J., Tiagho A.B., Ondoua Ndongo A. and Dzokou V.J. (2002)
Complexe des parasitoïdes de Trioza erytreae (Del Guercio) (Homoptera: Triozidae), psylle des agrumes
au Cameroun. Fruits 57, 19–28.
Tang, Y.Q., Weathersbee, A.A. III and Mayer, R.T. (2002) Effect of neem seed extract on the brown citrus aphid
(Homoptera: Aphididae) and its parasitoid Lysiphlebus testaceipes (Hymenoptera: Aphidiidae).
Environmental Entomology 31, 172–176.
Tansey, A.J., Vanaclocha, P., Monzo, C., Jones, M. and Stansly, P. (2017) Costs and benefits of insecticide and
foliar nutrient applications to huanglongbing-infected citrus trees. Pest Management Science 73, 904–
916. doi: https://doi.org/10.1002/ps.436
Taylor, P. and Reeder, R. (2020) Antibiotic use on crops in low and middle-income countries based on
recommendations made by agricultural advisors. CABI Agriculture and Bioscience 1(1).
https://doi.org/10.1186/s43170-020-00001-y
91
Taylor, R.A., Ryan, S.J., Lippi, C.A., Hall, D.G., Narouei-Khandan, H.A., Rohr, J.R. and Johnson, L.R. (2019) Predicting
the fundamental thermal niche of crop pests and diseases in a changing world: A case study on citrus
greening. Journal of Applied Ecology 56(8), 2057–2068. https://doi.org/10.1111/1365-2664.13455
Teixeira, D.C., Ayres, J., Kitajima, E.W., Danet, L., Jagoueix-Eveillard, S., Saillard, C. and Bové, J.M. (2005) First
report of a huanglongbing-like disease of citrus in São Paulo state, Brazil and association of a new
liberibacter species, ‘Candidatus Liberibacter americanus’, with the disease. Plant Disease 89, 107.
https://doi.org/10.1094/PD-89-0107A
Teixeira, D.C., Saillard, C., Couture, C., Martins, E.C., Wulff, N.A., Eveillard-Jagoueix, S., Yamamoto, P.T., Ayres,
A.J. and Bove, J.M. (2008) Distribution and quantification of Candidatus Liberibacter americanus, agent
of huanglongbing disease of citrus in São Paulo State, Brazil, in leaves of an affected sweet orange tree
as
determined
by
PCR.
Molecular
and
Cellular
Probes
22,
139–150.
https://doi.org/10.1016/j.mcp.2007.12.006
Thomas, D.B. (2012) Comparison of insect vacuums for sampling Asian citrus psyllid (Homoptera: Psyllidae) on
citrus trees. Southwestern Entomologist 37, 55–60. https://doi.org/10.3958/059.037.0107
Timmer, L.M., Garnsey, S.M. and Graham, J.H. (2000) Compendium of Citrus Diseases, 2nd edition. APS Press, St.
Paul, MN, USA, 92 pp. https://doi.org/10.1094/9780890545850
Timmer, L.W., Bové, J.M., Ayres, A.J., Bassanezi, R.B., Belasque Jr, J., Chamberlain, H.K., Dawson, W.O., Dewdney,
M.M., Graham, J.H. and Irey, M. (2011) HLB: it's not too late – yet. Citrus Industry 92, 6–7.
Tirtawadja, S. (1980) Citrus virus research in Indonesia. International Organization of Citrus Virologists
Conference Proceedings 8, 129–132. Available at: https://escholarship.org/uc/item/95r3t5jx accessed 5
May 2021.
Tiwari, S., Pelz-Stelinski, K. and Stelinski, L.L. (2011) Effect of Candidatus Liberibacter asiaticus infection on
susceptibility of Asian citrus psyllid, Diaphorina citri, to selected insecticides. Pest Management Science
67(1), 94–99.
Tiwari, S., Stelinski, L.L. and Rogers, M.E. (2012) Biochemical basis of organophosphate and carbamate resistance
in Asian citrus psyllid. Journal of Economic Entomology 105(2), 540–548.
Tomaseto, A.F., Marques, R.N., Fereres, A., Zanardi, O.Z., Volpe, H.X., Alquezar, B., Pena, L. and Miranda, M.P.
(2019) Orange jasmine as a trap crop to control Diaphorina citri. Scientific Reports 9(1).
https://doi.org/10.1038/s41598-019-38597-5
TradeMap (2019) Retrieved from www.trademap.org (accessed 23 July 2020).
Trejo-Pech, C., Spreen, T. and Zansler, M. (2018) Is growing oranges in Florida a good investment? American
Journal of Agricultural Economics 100, 625–639. https://doi.org/10.1093/ajae/aax107
Tsai, J.H. and Liu, Y.H. (2000) Biology of Diaphorina citri (Homoptera: Psyllidae) on four host plants. Journal of
Economic Entomology 93, 1721–1725.
Tschirley, D.L., Muendo, K.M. and Webber, M.T. (2004) Improving Kenya's domestic horticultural production and
marketing system: Current competitiveness, forces of change, and challenges for the future. Horticultural
Research and Seed Sector. Volume 2 Horticultural Marketing. Working Paper No. 08B/2004. Egerton
University, Nairobi, Kenya, 48 pp. https://doi.org/10.22004/ag.econ.55156
92
Urbaneja-Bernat, P., Pérez-Rodríguez, J., Krüger, K., Catalán, J., Rizza, R., Hernández-Suárez, E., Urbaneja, A. and
Tena, A. (2019) Host range testing of Tamarixia dryi (Hymenoptera: Eulophidae) sourced from South
Africa for classical biological control of Trioza erytreae (Hemiptera: Psyllidae) in Europe. Biological Control
135, 110–116. https://doi.org/10.1016/j.biocontrol.2019.04.018
Urquhart, P. (1999) IPM and the citrus industry in South Africa. International Institute for Environment and
Development, Gatekeeper Series 86, 20 pp. Available at: https://pubs.iied.org/6338iied accessed 5 May
2021.
USDA (2017) USDA Invests $13.6 Million in Citrus Greening Research. Press Release No. 0010.17 Available at:
https://www.usda.gov/media/press-releases/2017/01/19/usda-invests-136-million-citrus-greeningresearch accessed 23 July 2020.
USDA-NASS (United states Department of Agriculture-National Agricultural Statistics Service Information) (2018)
Citrus
Fruits
2018
Summary,
34
pp.
Available
at:
https://usda.library.cornell.edu/concern/publications/j9602060k accessed 5 May 2021.
Vapnek, J. (2009) Legislatively establishing a health certification programme for citrus. FAO Legal Papers Online
# 81 November 2009. Pp. 18. Available at:
http://www.ipcinfo.org/fileadmin/user_upload/legal/docs/lpo81.pdf accessed 27 July 2020.
Varma, A., Ahlawat, Y.S., Chakraborty, N.K., Garnier, M. and Bové, J.M. (1993) Detection of greening BLO by
electron microscopy, DNA hybridization in citrus leaves with and without mottle from various regions in
India. International Organization of Citrus Virologists Conference Proceedings 12, 280–285. Available at:
https://escholarship.org/uc/item/5ts7z3wp accessed 5 May 2021.
Vashisth, T. and Livingston, T. (2019) Assessment of pruning and controlled-release fertilizer to rejuvenate
huanglongbing-affected
sweet
orange.
HortTechnology
29,
1–8.
https://doi.org/10.21273/HORTTECH04382-19
Vega, S.J. and Rust, M.K. (2001) Argentine ant: a significant invasive species in agricultural, urban and natural
environments. Sociobiology 37, 3–25.
Vetter, R.S., Khan, S.Z., Arif, M.J., Hoddle, C.D. and Hoddle, M.S. (2013) Spiders (Araneae) surveyed from unsprayed citrus orchards in Faisalabad, Pakistan and their potential as biological control agents of
Diaphorina citri (Hemiptera: Liviidae). Pakistan Entomologist 35, 61–69.
Villechanoux, S., Garnier, M., Renaudin, J. and Bové, J.M. (1992) Detection of several strains of the bacteriumlike organism of citrus greening disease by DNA probes. Current Microbiology 24, 89–95.
Walter, A.J., Hall, D.G. and Duan, Y.P. (2012) Low incidence of ‘Candidatus Liberibacter asiaticus’ in Murraya
paniculata and associated Diaphorina citri. Plant Disease 96, 827–832. https://doi.org/10.1094/PDIS-0811-0668
Walter, J.F. (1999) Commercial experience with neem products. In: Hall, F.R. and Menn, J.J. (eds) Biopesticides:
Use and Delivery. Humana Press, Totowa, NJ, USA, pp. 155–170.
Wang, N., Stelinski, L.L., Pelz-Stelinski, K.S., Graham, J.S. and Zhang, Y. (2017) Tale of the huanglongbing disease
pyramid in the context of the citrus microbiome. Phytopathology 107(4), 380–387.
93
Wangithi, C.M. (2019) Evaluation of the magnitude of citrus yield losses due to African citrus triozid, false codling
moth, the greening disease and other pests of economic importance in Kenya. Journal of Economics and
Sustainable Development 10(20), 87–97. https://doi.org/10.7176/JESD/10-20-11
White, T.C.R. (1970) Airborne arthropods collected in South Australia with a drogue-net towed by a light aircraft.
Pacific Insects 12(2), 251–259.
Worner, S.P., Ikeda, T., Leday, G. and Joy, M. (2010) Surveillance tools for freshwater invertebrates. Biosecurity
Technical Paper 2010/21. Ministry of Agriculture and Forestry, New Zealand, 112 pp.
Wu, G.A. Prochnik, S., Jenkins, J., Salse, J., Hellsten, U. et al. (2014) Sequencing of diverse mandarin, pummelo
and orange genomes reveals complex history of admixture during citrus domestication. Nature
Biotechnology 32(7), 656–662. https://doi.org/10.1038/nbt.2906
Wu, G.A., Terol, J., Ibanez, V., López-García, A., Pérez-Román, E., Borredá, C., Domingo, C., Tadeo, F.R., CarbonellCaballero, J., Alonso, R. and Curk, F. (2018) Genomics of the origin and evolution of Citrus. Nature
554(7692), 311–316.
Yesuf, M. (2013) Pseudocercospora leaf and fruit spot disease of citrus: Achievements and challenges in the citrus
industry: A review. Agricultural Sciences 4(7), 324–328.
Zaka, S.M., Zeng, Z-N., Holford, P. and Beattie, G.A.C. (2010) Repellent effect of guava leaf volatiles on settlement
of adults of citrus psylla, Diaphorina citri Kuwayama, on citrus. Insect Science 17, 39–45.
Zanardi, O.Z., Volpe, H.X.L., Favaris, A.P., Silva, W.D., Luvizotto, R.A., Magnani, R.F., Esperança, V., Delfino, J.Y.,
de Freitas, R., Miranda, M.P. and Parra, J.R.P. (2018) Putative sex pheromone of the Asian citrus psyllid,
Diaphorina citri, breaks down into an attractant. Scientific Reports 8, 455.
https://doi.org/10.1038/s41598-017-18986-4
Zhang, M., Duan, Y., Zhou, L., Turecheck, W.W., Stover, E. and Powell, C.A. (2010) Screening molecules for control
of citrus huanglongbing using an optimized regeneration system for ‘Candidatus Liberibacter asiaticus’infected periwinkle (Catharanthus roseus) cuttings. Phytopathology 100, 239–245.
https://doi.org/10.1094/PHYTO-100-3-0239
Zhang, M., Guo, Y., Powell, C.A., Doud, M.S., Yang, C. and Duan, Y. (2014) Effective antibiotics against 'Candidatus
Liberibacter asiaticus' in HLB-affected citrus plants identified via the graft-based evaluation. PLoS ONE 9,
e111032. https://doi.org/10.1371/journal.pone.0111032
Zhang, M., Yang, C., Powell, C.A., Avery, P.B., Wang, J., Huang, Y. and Duan, Y. (2019) Field evaluation of
integrated management for mitigating citrus huanglongbing in Florida. Frontiers in Plant Science 9, 1890.
https://doi.org/10.3389/fpls.2018.01890
Zheng, Y.M., Kumar, N., Gonzalez, P. and Etxeberria, E. (2018) Strigolactones restore vegetative and reproductive
developments in huanglongbing (HLB) affected, greenhouse-grown citrus trees by modulating
carbohydrate
distribution.
Scientia
Horticulturae
237,
89–95.
https://doi.org/10.1016/j.scienta.2018.04.017
Zhou, L.J., Gabriel, D.W., Duan, Y.P., Halbert, S.E. and Dixon, W.N. (2007) First report of dodder transmission of
huanglongbing from naturally infected Murraya paniculata to Citrus. Plant Disease 91, 227–227.
94
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CABI, Nosworthy Way
Wallingford, Oxfordshire, OX10 8DE, UK
T: +44 (0)1491 832111
E: corporate@cabi.org
CABI, Bakeham Lane
Egham, Surrey, TW20 9TY, UK
T: +44 (0)1491 829080
E: cabieurope-uk@cabi.org
E: microbialservices@cabi.org
KNOWLEDGE FOR LIFE