Biota Neotropica 22(4): e20221416, 2022
www.scielo.br/bn
ISSN 1676-0611 (online edition)
Article
Ants associated with fronds of the tropical bracken fern Pteridium esculentum subsp.
arachnoideum
Isabella Rodrigues Lancellotti1
, Antônio José Mayhé-Nunes2, Rodrigo Machado Feitosa3
,
Anderson dos Santos Portugal1 & Marcelo Guerra Santos1*
1
Universidade do Estado do Rio de Janeiro, Faculdade de Formação de Professores, Departamento de
Ciências, Laboratório de Biodiversidade, São Gonçalo, RJ, Brasil.
2
Universidade Federal Rural do Rio de Janeiro, Instituto de Ciências Biológicas e da Saúde, Departamento de
Biologia Animal, Seropédica, RJ, Brasil.
3
Universidade Federal do Paraná, Departamento de Zoologia, Laboratório de Sistemática e Biologia de
Formigas, Curitiba, PR, Brasil.
*Corresponding author: marceloguerrasantos@gmail.com
LANCELLOTTI, I.R., MAYHÉ-NUNES, A.J., FEITOSA, R.M., PORTUGAL, A.S., SANTOS, M.G.
Ants associated with fronds of the tropical bracken fern Pteridium esculentum subsp. arachnoideum.
Biota Neotropica 22(4): e20221416. https://doi.org/10.1590/1676-0611-BN-2022-1416
Abstract: Pteridium is a cosmopolitan genus of ferns that possess nectaries on its fronds (fern leaves), thereby
attracting ants. Foliar (or extrafloral) nectaries are nectar-producing glands that are not related to pollination, but
rather attract ants and other arthropods. Foliar nectaries are found in 101 fern species, belonging to 11 genera
and six families. The aim of the study is to characterize the community of ants that visit the fronds of Pteridium
esculentum subsp. arachnoideum, as well as daily and seasonal ant abundance in different frond development
stages. The study was conducted in the Atlantic Forest of Rio de Janeiro state, Brazil. Bimonthly collections were
established, where 30 expanding fronds and 30 fully expanded fronds were randomly marked. In each 1-hour
shift starting at 8:30 am and ending at 5:30 pm, the fronds were observed for the presence of ants. Thirty three ant
species were recorded on the Pteridium esculentum subsp. arachnoideum fronds, distributed into six subfamilies
and 13 genera. The most abundant species were Solenopsis sp.1 and Ectatomma tuberculatum. Eight ant species
were observed foraging the nectaries of tropical bracken fern fronds. Ectatomma tuberculatum has been observed
feeding on the nectaries and patrolling the fronds. Ant activity peak was on mid-day during the rainy season. The
tropical bracken fern Pteridium esculentum subsp. arachnoideum has a rich (the highest recorded until now on
Pteridium species) and diverse ant community on its fronds, mainly on the expanding fronds. The presence of
generalist predatory ants (Ectatomma tuberculatum and Solenopsis sp.1) during the entire study period suggests
a positive interaction between ants and Pteridium esculentum subsp. arachnoideum.
Keywords: ant-plant interactions; Atlantic Forest; behavioral ecology; foliar nectaries; pteridophytes.
Formigas associadas às frondes da samambaia Pteridium esculentum subsp.
arachnoideum
Resumo: Pteridium é um gênero cosmopolita de samambaias que possui nectários em suas frondes (folhas de
samambaias), atraindo formigas. Nectários foliares (ou extraflorais) são glândulas produtoras de néctar que não
estão relacionadas com a polinização, mas podem atrair formigas e outros artrópodes. Nectários foliares já foram
registrados em 101 espécies de samambaias, pertencentes a 11 gêneros e seis famílias. O objetivo do estudo é
caracterizar a comunidade de formigas que visitam as frondes de Pteridium esculentum subsp. arachnoideum,
bem como a abundância diária e sazonal das formigas em diferentes estágios foliares. O estudo foi realizado na
Mata Atlântica do estado do Rio de Janeiro, Brasil. Foram estabelecidas coletas bimestrais, onde foram marcadas
aleatoriamente 30 frondes em expansão e 30 frondes totalmente expandidas. Em cada turno de 1 hora com início
às 8h30 e término às 17h30, as frondes marcadas foram observadas quanto à presença de formigas. Trinta e três
espécies de formigas foram registradas nas frondes do Pteridium esculentum subsp. arachnoideum, distribuídas em
seis subfamílias e 13 gêneros. As espécies mais abundantes foram Solenopsis sp.1 e Ectatomma tuberculatum. Foram
registradas oito espécies de formigas forrageando os nectários foliares da samambaia. Ectatomma tuberculatum
foi observada se alimentando nos nectários e patrulhando as frondes. As formigas tiveram o pico de atividade
https://doi.org/10.1590/1676-0611-BN-2022-1416
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Biota Neotrop., 22(4): e20221416, 2022
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Lancellotti, I.R. et al.
ao meio-dia e na estação chuvosa. A samambaia tropical Pteridium esculentum subsp. arachnoideum tem uma
elevada riqueza (a maior já registrada até o momento para espécies de Pteridium) e diversidade de formigas em
suas frondes, com maior frequência nas frondes não totalmente expandidas. A presença de formigas predadoras
generalistas (Ectatomma tuberculatum e Solenopsis sp.1) durante todo o período de estudo sugere uma interação
positiva entre as formigas e Pteridium esculentum subsp. arachnoideum.
Palavras-chave: interações formiga-planta; Mata Atlântica; ecologia comportamental; nectários foliares; pteridófitas.
Introduction
Pteridium (bracken fern) is a fern genus distributed world-wide.
The circumscription of species is widely discussed in the literature,
about 20 morphotypes have been recognized, and several infra-specific
ranks have been adopted (PPG I 2016, Thomson 2016, Schwartsburd
et al. 2018). While some authors recognize only two species: Pteridium
aquilinum (L.) Kuhn and P. esculentum (G. Forst.) Cockayne along
their infraspecies (Thomson 2016). All the species of the genus have
nectaries on their fronds (fern leaves) (Tryon & Tryon 1982), and the
oldest record of nectaries in ferns was reported by Francis Darwin in
1877 for Pteridium aquilinum (L.) Kuhn (Lloyd 1901).
Foliar (or extrafloral) nectaries are nectar-producing glands that are
not related to pollination, but rather attract ants and other arthropods
(Koptur et al. 2013). Fern nectars contain a variety of amino acids and
a large amount of sugar, particularly sucrose, fructose and glucose
(Koptur 1992, Mehltreter et al. 2022). Foliar nectaries are found in
101 fern species, belonging to 11 genera and six families (Lloyd 1901,
Koptur et al. 1982, White & Turner 2012, Mehltreter et al. 2022). Some
authors believe that the nectaries promote interactions between ferns
and ants (Koptur et al. 1982, 1998, Page 1982).
There are many records of ants and bees associated with the bracken
fern nectaries (Page 1982, Tempel 1983, Heads & Lawton 1984, 1985,
Olesen 1988; Rashbrook et al. 1992, White & Turner 2012), though
some authors reported no ants on the Pteridium nectaries for some
bracken populations (Rumpf et al. 1994). The function of nectaries
remains controversial (Cooper-Driver 1990); some studies reported
no benefits from ants that visited the foliar nectaries for Pteridium
species (Tempel 1983, Heads & Lawton 1984, Rashbrook et al. 1992),
while others related benefits for ants and plants (Heads 1986, Jones
& Paine 2012). The highest density and frequency rates of ants have
been observed on young fronds of Pteridium species in the rainy season
(Tempel 1983, Rashbrook et al. 1992).
Many studies have characterized arthropod fauna associated with
Pteridium spp. fronds (Lawton 1976, Balick et al. 1978, Hendrix 1980,
Winterbourn 1987), while others have reported ants visiting their
nectaries (Lawton 1976, Balick et al. 1978, Page 1982) and assessed
the interactions between these two organisms (Page 1982, Tempel 1983,
Heads & Lawton 1984, 1985, Rashbrook et al. 1992). However, few of
these characterized the entire ant community present on the fronds of this
fern (Douglas 1983, Tempel 1983, Heads & Lawton 1984, 1985). These
studies evaluated Pteridium species of USA, England, Scotland, South
Africa, and New Zealand. For the Neotropical Region, Ávila & Otero
(2013) recorded five ant species visiting the nectaries of the croziers of
Pteridium caudatum from Venezuela [Brachymyrmex sp., Camponotus
rufipes (Fabricius, 1775), Linepithema sp. Pheidole sp., and Solenopsis
geminata (Fabricius, 1804)]. Martins et al. (1995) recorded one species
(Atta sexdens rubropilosa Forel, 1908) cutting pinnae and rachis of the
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bracken fern fronds. Santos and Mayhé-Nunes (2007) reported a single
ant species [Dolichoderus attelaboides (Fabricius, 1775)] associated
with the nectaries of P. arachnoideum [Pteridium esculentum subsp.
arachnoideum (Kaulf.) Thomson].
Pteridium esculentum subsp. arachnoideum (Kaulf.) Thomson
is a tropical bracken species widely distributed in South and Central
America. Despite being a native species in these regions, it has a high
invasive potential and can cause several environmental problems in
natural and anthropic areas (Schwartsburd et al. 2017, Oliveira et al.
2018). The present study aims to characterize the ant community on
fronds of Pteridium esculentum subsp. arachnoideum (tropical bracken
fern), a Neotropical fern species, as well as daily and seasonal ant
abundance in different frond development stages.
Materials and Methods
1. Study area
The study was conducted in a population of Pteridium esculentum
subsp. arachnoideum located in the Restinga (coastal sandy plain)
of the Maricá Environmental Protection Area, in the municipality of
Maricá, Rio de Janeiro state, Southeastern Brazil (22° 57’ 41.05”S,
42° 53’ 20.22” W). Restinga is a type of vegetation associated with
the Atlantic Forest. Nimer (1972) classified Maricá’s climate as
hot tropical and super humid, with short dry periods. Studies that
characterized Maricá’s climate between 1989 and 2000 indicate that
the minimum temperature is lower in winter (8.6 °C to 15.2 °C), with
July as the coldest month (always below 15 °C), while the highest
temperatures are recorded in summer, with means between 29.2 °C
and 37.3 °C, and February being the hottest month (temperatures
always above 33 °C, reaching 37.7 °C) (Pereira et al. 2001). In the
study area there are only two seasons. According to Barbieri (2005),
the rainy season in Southeastern Brazil occurs between October and
March and the dry season between April and September.
2. Collection and laboratory procedures
Tempel (1983) divided the frond development of Pteridium into
6 stages. In this study, the fronds in stages 1 to 5 were considered
expanding fronds, and those in stage 6 fully expanded fronds (Figure 1).
Since P. arachnoideum has subterraneous rhizomes, the fronds were
used as a sampling unit. Thirty expanding fronds and thirty fully
expanded fronds were randomly marked with red ribbon, at least 2m
apart to each other. Throughout the day (8:30 am–5:30 pm), the fronds
were inspected during each 1-hour shift and all ants on bracken fronds
collected with an entomological aspirator, to obtain the abundance of
each species. The ants which were feeding on the bracken fern nectaries
were recorded. Collections were carried out every two months for one
year, one day (without rain) per month, between February 2009 and
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Biota Neotrop., 22(4): e20221416, 2022
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Ants on fronds of the tropical bracken fern
Figure 1. Frond stages of Pteridium esculentum subsp. arachnoideum. A: Fully
expanded frond. B-C: Expanding frond. All photos: Marcelo Guerra Santos.
February 2010. The ants were preserved in 70% alcohol, mounted
in entomological boxes (Lattke 2003), and identified by Dr. Antônio
Mayhé-Nunes and Dr. Rodrigo M. Feitosa. Vouchers were deposited
in the herbarium of the Faculdade de Formação de Professores da
Universidade do Estado do Rio de Janeiro (RFFP 20.281) and the Padre
Jesus Santiago Moure Entomological Collection, Universidade Federal
do Paraná, Department of Zoology (DZUP).
3. Statistical analyses
To detect differences in ant frequencies (number of observations)
between expanding and fully expanded fronds (categorical variables),
we performed a Pearson’s chi-squared test (Gotelli and Ellison 2011).
The expected richness of ants on bracken fronds was calculated using
the estimator Chao 2. It provides a minimum estimate of richness in
homogeneous samples using presence and absence (incidence) data, in just
one or two samples (Magurran 2013). The statistical tests were conducted
in PAST (PAleontological STatistics), version 3.10 (Hammer et al. 2001).
Circular statistics were used to estimate the month of highest
incidence of the ant species, time of intensity peak on fern fronds.
Furthermore, the mean angle, Rayleigh test (p), and length of mean
vector (r) were calculated. The program Oriana was used for the
calculations of circular statistics (Kovach 2009).
Results
A total of 599 ants were observed on the fronds of Pteridium
esculentum subsp. arachnoideum. Of this total, we managed to collect
only 529 ants, and all were identified at least to the generic level. We
recorded 33 ant species on the tropical bracken fern fronds, distributed
among six subfamilies and 13 genera (Table 1). The observed richness
was similar to the richness estimated by Chao 2 = 33.8 ± 6.0. Eight ant
species were observed foraging the nectaries of tropical bracken fern
fronds, Brachymyrmex sp.1 (Figure 2F), Camponotus crassus Mayr,
https://doi.org/10.1590/1676-0611-BN-2022-1416
Figure 2. Ants on frond nectaries of Pteridium esculentum subsp. arachnoideum.
A: Ectatomma tuberculatum feeding on the nectary. It’s possible to see a nectar
droplet in their open jaws. B: Camponotus crassus. C: Wasmannia auropunctata.
D: Ectatomma brunneum. E: Pheidole sp. F: Brachymyrmex sp. (arrow).
*Nectaries. Photo A: Isabella Rodrigues Lancellotti. Photos B, C, E, F: Marcelo
Guerra Santos. Photo D: Camille Santos Carraco.
1862 (Figure 2B), Camponotus sp.1, Ectatomma tuberculatum (Olivier,
1792) (Figure 2A), Ectatomma brunneum (Fr. Smith, 1858) (Figure 2D),
Pheidole sp.1 (Figure 2E), Solenopsis sp.1, and Wasmannia auropunctata
(Roger, 1863) (Figure 2C). Ectatomma tuberculatum has also been
observed patrolling the fronds.
The subfamilies with the highest ant richness were Formicinae and
Myrmicinae (both with nine species). The species with the greatest
abundance were Solenopsis sp.1 (165 individuals) and Ectatomma
tuberculatum (151 individuals) (Figure 2A), and those with intermediate
abundance were Brachymyrmex sp.1 (65 individuals), Camponotus sp.1
(26 individuals), and Wasmannia auropunctata (21 individuals). All other
28 ant species had an abundance of less than 10 individuals (Table 1).
The chi-squared test (X2) demonstrated a significant difference for
ant abundance between the analyzed months (X2 = 397.17, DF = 6,
P < 0.000001), with the higher abundance in October (100 individuals)
and December (226 individuals), both in the beginning of the rainy
season (Table 1). October and December are the months most likely
to find 25 of the 33 species recorded, among them the species with
the highest abundance, Ectatomma tuberculatum and Solenopsis sp.1
(October and December respectively). April, June, and August (dry
season), and February (end of the rainy season) are the months with the
lowest probability of finding ant species on Pteridium esculentum subsp.
arachnoideum (Table 1).
There was a significant difference in the frequency of ants (number
of observations) visiting the expanding and fully expanded fronds of
Pteridium esculentum subsp. arachnoideum in all the months observed,
with ants showing a preference for the former (Table 2). Most ants (19
species) have their highest visitation intensity peak between 10:30
am and 1:30 pm, including the species with the highest abundance,
Solenopsis sp.1 and Ectatomma tuberculatum (Table 3).
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Lancellotti, I.R. et al.
Table 1. Abundance and circular statistical tests (month of highest incidence of the species and Rayleigh test (p) of ant species collected on the fronds of Pteridium
esculentum subsp. arachnoideum, between February 2009 and February 2010, in the Restinga of Maricá, Rio de Janeiro state, Brazil. Rainy season (between October
and March) and dry season (between April and September) (Barbieri 2005).
Subfamily
Ant species
Feb 9 Apr 9 Jun 9 Aug 9 Oct 9 Dec 9
Dolichoderinae
Ectatomminae
Formicinae
Myrmicinae
Abundance
Month of
highest
incidence
Rayleigh
test (p)
Dorymyrmex brunneus
(Forel, 1908)
1
0
0
0
2
0
1
4
0,76
December
0,137
Dorymyrmex sp.
2
0
0
0
1
0
0
3
0,57
Janaury
0,137
Linepithema iniquum
(Mayr, 1870)
0
0
0
1
0
0
0
1
0,19
February
< 1E-12
Linepithema sp.
0
0
0
3
0
0
2
5
0,95
August
0,137
Tapinoma atriceps
Emery, 1888
0
0
0
1
1
1
0
3
0,57
October
0,512
Tapinoma
melanocephalum
(Fabricius, 1793)
0
1
1
4
4
0
0
10
2,08
October
0,512
Tapinoma sp.1
0
0
0
1
0
0
0
1
0,19
August
0,512
Tapinoma sp.2
0
0
0
0
2
1
0
3
0,57
October
0,137
Ectatomma brunneum
(Fr. Smith, 1858)
0
0
0
0
8
0
0
8
1,51
October
< 1E-12
Ectatomma tuberculatum
(Olivier, 1792)
33
9
28
4
40
32
5
151
28,54
December
< 1E-12
Brachymyrmex sp.1
0
4
4
14
13
11
19
65
12,29
December
0,895
Brachymyrmex sp.2
0
0
0
1
1
3
0
5
0,95
October
0,512
Camponotus crassus
Mayr, 1862
1
0
0
1
1
0
1
4
0,76
August
0,512
Camponotus leydigi
Forel, 1886
0
1
0
0
1
0
0
2
0,38
October
0,512
Camponotus sexguttatus
(Fabricius, 1793)
0
0
0
1
0
0
0
1
0,19
August
0,512
Camponotus sp.1
–
5
–
5
10
4
2
26
4,91
October
0,137
Camponotus sp.2
0
0
0
0
8
0
0
8
1,51
October
< 1E-12
Camponotus sp.3
0
1
0
0
0
0
0
1
0,19
April
0,512
Camponotus sp.4
0
0
1
0
2
1
0
4
0,76
November
0,512
0
0
0
0
0
1
0
1
0,19
December
0,512
0
0
0
0
1
9
0
10
1,89
December
0,512
0
0
1
0
1
1
0
0
0
0
0
0
0
4
0
0
2
1
0
0
0
0
0
0
0
8
0
15
0
0
0
0
1
0
2
1
2
2
2
154
2
0
0
0
0
0
1
0
0
1
2
5
3
165
3
21
0,19
0,38
0,95
0,57
31,19
0,57
3,97
December
October
February
December
December
December
August
0,512
0,137
0,512
0,512
< 1E-12
0,137
0,137
0
0
2
0
0
0
0
2
0,38
August
0,137
0
1
0
0
1
0
0
2
0,38
June
0,512
1
0
0
0
0
0
0
1
0,19
February
0,512
3
3
47
0
0
26
0
1
40
0
0
59
0
1
100
0
0
226
0
0
31
3
5
529
0,57
0,95
February
February
0,033
0,512
Cephalotes minutus
(Fabricius, 1804)
Cephalotes pusillus
(Klug, 1824)
Cephalotes sp.1
Nylanderia sp.
Pheidole sp.1
Pheidole sp.2
Solenopsis sp.1
Solenopsis sp.2
Wasmannia auropunctata
(Roger, 1863)
Ponerinae
Neoponera villosa
(Fabricius, 1804)
Pseudomyrmecinae Pseudomyrmex gracilis
(Fabricius, 1804)
Pseudomyrmex pallidus
(Fr. Smith, 1855)
Pseudomyrmex sp.1
Pseudomyrmex sp.2
Abundance
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Feb 10
Relative
abundance
(%)
Month
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Ants on fronds of the tropical bracken fern
Table 2. Ant frequency (number of observations) on Pteridium esculentum
subsp. arachnoideum fronds at different stages of development in the Restinga
of Maricá, Rio de Janeiro state, Brazil.
Month/year
Expanding
fronds
Fully
expanded
fronds
Chi-squared test
February 2009
37
20
5,07, P = 0,024
April 2009
53
18
17,25 P = 3,27E-05
June 2009
42
20
7,80 P = 0,005
August 2009
35
18
5,45 P = 0,019
October 2009
82
58
4,11 P = 0,042
December 2009
139
20
89,06 P < 1,0E-06
February 2010
45
12
19,10 P = 1,2E-05
N
433
166
Discussion
The record of 33 ant species belonging to 13 genera is the highest
ant richness recorded on Pteridium fronds until now, of this total, eight
were observed foraging the nectaries. Tempel (1983) listed 18 nectar
feeding ants, distributed on 12 genera on Pteridium aquilinum, in USA.
This author also found Myrmicinae as the richest subfamily (9 spp.).
Douglas (1983) reported nine ant species associated with the nectaries
of P. aquilinum in USA. Ávila and Otero (2013) recorded five ant
species visiting the nectaries of the croziers of Pteridium caudatum, in
Venezuela. Heads and Lawton (1984, 1985) reported three ant species
on nectaries of P. aquilinum in England. In Brazil, Martins et al. (1995)
reported a single ant species [Atta sexdens (Linnaeus, 1758)] cutting
pinnae and rachis of the Pteridium fronds. Santos and Mayhé-Nunes
(2007) recorded Dolichoderus attelaboides (Fabricius 1775) as the
only ant species associated with the foliar nectaries of P. arachnoideum
[Pteridium esculentum subsp. arachnoideum] in the Atlantic Forest of
Rio de Janeiro state.
Vargas et al. (2010) recorded 52 ant species in the litter of the
Restinga of Maricá (restinga vegetation). So, the richness found on
the P. esculentum subsp. arachnoideum fronds represents 63.5% of
the ants registered for this region until now. For angiosperms species
with foliar nectaries in Cerrado (Brazilian savanna), 34 ant species
were found on Caryocar brasiliense Cambess. (Caryocaraceae), 24 on
Ouratea hexasperma (A.St.-Hil.) Baill. (Ochnaceae), and 12 on Qualea
grandiflora Mart. (Vochysiaceae) (Oliveira & Pie 1998). In mangrove
vegetation, Talipariti pernambucense (Arruda) Bovini (Malvaceae) was
visited by 19 ant species (Cogni & Freitas, 2002).
The ant visitation on Pteridium esculentum subsp. arachnoideum
fronds was greater in October and December (both in the beginning
of the rainy season). Tempel (1983) conducted a study in New Jersey
(EUA) and found that nectar secretion by Pteridium aquilinum and
ant visitation were more frequent from May to August, that is, in
summer, with high rates of precipitation. In South Africa, the period
in which ants have the greatest impact on Pteridium herbivores occurs
between November and December, corresponding to the rainy season
in this region (Rashbrook et al. 1992). These data indicate that the
change in ant visitation of bracken fronds is highly associated with
the summer season.
https://doi.org/10.1590/1676-0611-BN-2022-1416
The most abundant ant species (Brachymyrmex sp.1, Camponotus
sp.1, Ectatomma tuberculatum, Solenopsis sp.1, and Wasmannia
auropunctata) on tropical bracken fern have their highest visitation
intensity peak near to mid-day, between 12:00 and 2:00 pm. According
to Kaspari (2003), temperature is an important factor that regulates
the activities of ant populations. Increased visitation may be attributed
to the natural rise in the daily activities of ants as a function of their
ectothermy and exudation of foliar nectaries. Ectatomma tuberculatum
was one of the ant species with highest abundance, and visited the fronds
of Pteridium esculentum during 9:30 am to 4:30 pm with the intensity
peak at 1:07 pm. (Table 3). This ant species presents high activity at
night, with massive exiting of workers at end of the day (sunset) and
massive entry in the nest at beginning of the morning (sunrise), or high
foraging activity in the morning and no mass exit at sunset (Wheeler
1986). According to Valenzuela-González et al. (1995), E. tuberculatum
foraging was mainly nocturnal during the dry season and diurnal in the
rainy season. Page (1982) reported that the foliar nectaries of Pteridium
aquilinum were more active in the morning. Mehltreter et al. (2022),
analyzing 16 fern species (Aglaomorpha and Campyloneurum genera),
observed that nectar secretion occurred mainly during the night and
early morning, but could continue until the afternoon, depending on air
humidity conditions. In fact, in Restinga of Maricá it was possible to
observe a few tropical bracken ferns secreting nectar during the period
close to noon (Figure 2A). But we did not measure local climatic data in
these days. The nighttime period was not assessed here and probably a
different ant community may be visiting the foliar nectaries of Pteridium
esculentum subsp. arachnoideum at this period. However, Tempel
(1983) evaluated populations of Pteridium aquilinum Kuhn in New
Jersey (USA) at night and found no evidence of nocturnal ant activity.
Ectatomma tuberculatum and Solenopsis sp.1, both generalist
predator ants (Wheeler 1986, Valenzuela-González et al. 1995, Wojcik
et al. 2001, see also comments by Tolofo 2011 on other Ectatomma
species), were present during the entire period of observations, and
were the most abundant species on the fronds of Pteridium esculentum
subsp. arachnoideum. E. tuberculatum has been observed feeding
on the nectaries, and patrolling the fronds, whereas Solenopsis sp.1
was only feeding on nectaries. However, other generalist predator
ants were also present in lower abundance, as follows: Dorymyrmex
brunneus (Forel, 1908), Dorymyrmex sp., Ectatomma brunneum,
Neoponera villosa (Fabricius, 1804), Pheidole sp.1, Pheidole sp.2,
Pseudomyrmex sp.1 and Pseudomyrmex sp.2 (Table 4). Douglas (1983)
observed that Camponotus pennsylvanicus (De Geer, 1773), Formica
obscuriventris (Mayr, 1870), and Formica subsericea (Say, 1836)
defend the nectaries of the developing croziers, while other smaller
species such as Tapinoma sessile (Say, 1836), Temnothorax rugatulus
(Emery, 1895), Leptothorax muscorum (Nylander, 1846), and Lasius
alienus (Foerster, 1850) (not predatory ant species) only utilize
nectar and do not seem to defend the fern croziers. The establishing
mutualistic relationship between ants and foliar nectaries seems to
depend on the occurrence and abundance of large or aggressive ants
visiting the plants (Koptur 1984, Heads 1986).
The frequency of ants (number of observations) was greater on
expanding fronds than on fully expanded fronds of P. esculentum
subsp. arachnoideum. Marquis (2012) reports that phenology is vital
in determining herbivore attack intensity, since the plant life cycle
can allow plants to evade attack or be exposed in its most vulnerable
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Biota Neotrop., 22(4): e20221416, 2022
6
Lancellotti, I.R. et al.
Table 3. Ant species abundance per hour of visitation on Pteridium esculentum subsp. arachnoideum fronds and circular statistical tests (mean time, mean angle,
and length of mean vector), between February 2009 and February 2010 (seven collections), in the Restinga of Maricá, Rio de Janeiro state, Brazil. (n = 529 ants).
Ant species
Time
Time of
intensity
peak
Length
of mean
vector
(r)
8:30
AM
9:30
AM
10:30
AM
11:30
AM
12:30
PM
1:30
PM
2:30
PM
3:30
PM
4:30
PM
5:30
PM
Brachymyrmex sp.1
2
3
4
11
14
6
7
14
5
0
12:52
(193,095°)
0,859
Brachymyrmex sp.2
0
0
0
0
1
1
1
0
2
0
02:42
(220,525°)
0,914
Camponotus
crassus
0
0
0
0
0
0
1
3
0
0
03:15
(228,766°)
0,994
Camponotus
leydigi
0
0
0
0
2
0
0
0
0
0
12:30
(187,5°)
0,697
Camponotus
sexguttatus
0
0
1
0
0
0
0
0
0
0
10:30
(157,5°)
1
Camponotus sp.1
0
0
3
4
4
6
7
2
0
0
01:37
(204,485°)
0,931
Camponotus sp.2
0
0
3
3
1
0
0
1
0
0
11:40
(175,209°)
0,921
Camponotus sp.3
0
0
0
0
0
0
0
0
1
0
04:30
(247,5°)
1
Camponotus sp.4
0
1
1
0
1
0
1
0
0
0
01:30
(202,5°)
1
Cephalotes pusillus
0
1
1
1
0
0
0
1
6
0
03:30
(232,5°)
0,377
Cephalotes minutus
0
0
0
0
1
0
0
0
0
0
12:30
(187,5°)
1
Cephalotes sp.1
0
0
0
0
0
0
0
0
1
0
01:30
(202,5°)
1
Dorymyrmex
brunneus
0
0
0
1
0
1
1
1
0
0
04:30
(247,5°)
0,394
Dorymyrmex sp.
0
0
0
0
0
2
0
0
1
0
04:30
(247,5°)
0,369
Ectatomma
brunneum
0
0
2
1
1
0
3
1
0
0
01:00
(195,211°)
0,883
Ectatomma
tuberculatum
0
21
21
22
14
15
21
24
13
0
01:07
(196,868°)
0,438
Linepithema
iniquum
0
0
0
0
1
0
0
0
0
0
08:30
(127,5°)
0,513
Linepithema sp.
0
0
0
1
2
0
1
1
0
0
02:53
(223,266°)
0,565
Nylanderia sp.
0
0
0
0
0
0
0
2
0
0
02:30
(217,5°)
1
Neoponera villosa
0
0
0
1
0
1
0
0
0
0
02:30
(217,5°)
0,72
Pheidole sp.1
0
1
3
0
0
1
0
0
0
0
09:30
(142,5°)
0,531
Pheidole sp.2
0
1
2
0
0
0
0
0
0
0
10:30
(157,5°)
0,596
Pseudomyrmex
gracillis
0
0
1
1
0
0
0
0
0
0
10:30
(157,5°)
0,494
Continue...
http://www.scielo.br/bn
https://doi.org/10.1590/1676-0611-BN-2022-1416
Biota Neotrop., 22(4): e20221416, 2022
7
Ants on fronds of the tropical bracken fern
...Continuation
Ant species
Time
Time of
intensity
peak
Length
of mean
vector
(r)
8:30
AM
9:30
AM
10:30
AM
11:30
AM
12:30
PM
1:30
PM
2:30
PM
3:30
PM
4:30
PM
5:30
PM
Pseudomyrmex
pallidus
0
0
0
1
0
0
0
0
0
0
11:30
(172,5°)
0,398
Pseudomyrmex sp.1
0
0
1
2
0
0
0
0
0
0
11:10
(167,513°)
0,992
Pseudomyrmex sp.2
0
1
0
2
0
0
0
1
0
0
01:02
(195,653°)
0,381
Solenopsis sp.1
0
0
0
0
0
2
1
4
3
0
12:28
(187,177°)
0,374
Solenopsis sp.2
0
1
1
0
0
0
0
1
0
0
10:00
(150°)
0,991
Tapinoma atriceps
0
0
1
0
1
0
0
0
0
0
12:30
(187,5°)
0,476
Tapinoma
melanocephalum
0
0
3
2
2
0
0
0
1
0
11:30
(172,5°)
0,707
Tapinoma sp.1
0
0
0
0
0
0
1
0
0
0
02:30
(217,5°)
1
Tapinoma sp.2
0
0
1
0
2
0
0
0
0
0
01:30
(202,5°)
0,319
Wasmannia
auropunctata
0
0
4
7
1
4
0
3
2
0
01:30
(202,5°)
0,638
Table 4. Genera of ants found on Pteridium esculentum subsp. arachnoideum in the Restinga of Maricá, Rio de Janeiro state and their respective feeding habits.
Genus
Feeding habit
Brachymyrmex Most species are omnivorous, and some exploit the sugary
solutions of extrafloral nectaries or trophobiont insects.
Reference
Baccaro et al. (2015); Quirán (2005)
Camponotus
Omnivorous.
Cephalotes
Omnivorous, feed on sugary secretions produced by membracids
and extrafloral nectaries, and have a preference for pollen grains.
Dorymyrmex
Hunt live insects, including alates (flying ants). Some species
collect honeydew from sap-sucking insects.
Ectatomma
Omnivorous. Prey on annelids, gastropods and a number of
arthropods, including ants, wasps, bee pupae, lizards and termites.
Also frequently seen collecting sugary liquids secreted by
hemipterans, extrafloral nectaries and flower and fruit exudates.
Baccaro et al. (2015); Lattke (2003); Tolofo (2011)
Linepithema
Generalists. Feed on sugary solutions from extrafloral nectaries and
honeydew from hemipterans, but may be opportunist predators.
Baccaro et al. (2015)
Nylanderia
Generalists, frequently visit extrafloral nectaries.
Neoponera
Omnivorous, generalist predators or specialists. Occasionally feed
on the arillus of fallen seeds on the forest floor.
Baccaro et al. (2015); Lattke (2003)
Pheidole
Omnivorous, predators and necrophagous.
Baccaro et al. (2015); Wilson (2003)
Pseudomyrmex Omnivorous and very aggressive. Many species are associated with
plants that have extrafloral nectaries.
Solenopsis
Predators and necrophagous. They may explore extrafloral
nectaries.
Tapinoma
Some species feed on sugary solutions produced by aphids and
coccids.
Wasmannia
Omnivorous.
https://doi.org/10.1590/1676-0611-BN-2022-1416
Fernández (2003)
Baccaro et al. (2015); Moretti & Ribeiro (2006)
Baccaro et al. (2015)
Baccaro et al. (2015); LaPolla et al. (2011)
Baccaro et al. (2015); Whitcomb et. al (1972)
Baccaro et al. (2015); Wojcik et al. (2001)
Baccaro et al. (2015)
Baccaro et al. (2015); Fisher & Cover (2007)
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Biota Neotrop., 22(4): e20221416, 2022
8
Lancellotti, I.R. et al.
phase, when not fully mature. Tempel (1983) found that nectar
secretion is significantly higher in the first developmental stages of
Pteridium aquilinum, and becomes practically inactive in the final
stages. As such, the activity pattern of ants is correlated to foliar
nectar exudation. Rashbrook et al. (1992) observed a larger number
of ants on young fronds, which have more active nectaries (greater
nectar exudation). Thus, it can be inferred that in the most vulnerable
stage (juvenile), higher nectar production acts as a lure for ants, which
sometimes protect individuals that supply nectar. In the Restinga of
Maricá we observed very few full expanded fronds of the tropical
bracken fern secreting nectar during the day (Figure 2A). However,
almost all observed fronds (expanding and full expanded) were not
secreting nectar. Even though, the ants still remained scraping the
nectaries (Figures 2B–F).
According to Tempel (1993), most of the significant damage to
Pteridium aquilinum occurs before maturity, demonstrating no need
for the additional protection provided by ants in the final stage of
development, and in turn, the low nectar production. Furthermore,
studies conducted by Santos et al. (2005) found cyanogenesis in
all young Pteridium arachnoideum fronds but in only 9.1% of the
mature fronds. Cyanogenesis is a defensive process in which the plant
releases hydrocyanic acid when injured by herbivores (Vetter 2000).
The levels of phenolic substances, which may also act defensively,
increase significantly during the maturation of P. esculentum subsp.
arachnoideum fronds (unpublished data). Furthermore, the fronds
exhibit a norsesquiterpene denominated ptaquiloside, which is
responsible for toxic, mutagenic and cancerigenous action in Pteridium
species (Yamada et al. 2007).
The tropical bracken fern Pteridium esculentum subsp.
arachnoideum has a remarkedly rich (the highest recorded until now
on Pteridium species) and diverse ant community on its fronds, mainly
on the expanding fronds, which peaks at the mid of the day in the
rainy season. The presence of generalist predatory ants (Ectatomma
tuberculatum and Solenopsis sp.1) during the entire study period
suggests that there may be a positive interaction between ants and
Pteridium esculentum subsp. arachnoideum. Future studies are needed
to understand the relationship between these ants and the tropical
bracken fern, especially those that interact with leaf nectaries.
Acknowledgments
We are indebted to Bianca da Silva (in memoriam), Rafael Pontes,
André Siqueira, and Luiz José Soares Pinto for their help in collecting
and screening the material. Thanks to Márcio Mendes Bento da
Silva for his help with the illustrations. MGS and RMF thank CNPq
(Conselho Nacional de Desenvolvimento Científico e Tecnológico;
grants 308045/2017-3 and 301495/2019-0, respectively), FAPERJ
(Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro grant
E-26/203.236/2017), and PROCIÊNCIA (Programa de Incentivo à
Produção Científica, Técnica e Artística) of UERJ (Universidade do
Estado do Rio de Janeiro) for financial support.
Associate Editor
José Mermudes
http://www.scielo.br/bn
Author Contributions
Isabella Rodrigues Lancellotti: Substantial contribution in the
concept and design of the study; data collection; data analysis and
interpretation; manuscript preparation; critical revision, adding
intellectual content.
Marcelo Guerra Santos: Substantial contribution in the concept and
design of the study; data collection; data analysis and interpretation;
manuscript preparation; critical revision, adding intellectual content.
Anderson dos Santos Portugal: Data analysis and interpretation;
critical revision, adding intellectual content.
Antônio José Mayhé-Nunes: Species identification, data analysis
and interpretation; manuscript preparation critical revision, adding
intellectual content.
Rodrigo Machado Feitosa: Species identification, data analysis
and interpretation; manuscript preparation critical revision, adding
intellectual content.
Conflicts of Interest
The authors declare that they have no conflict of interest related to
the publication of this manuscript.
Data Availability
Supporting data are available at <https://doi.org/10.48331/scielodata.
XB751P> and <https://data.scielo.org/dataset.xhtml?persistentId =
doi:10.48331/scielodata.XB751P>.
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Received: 31/08/2022
Accepted: 21/12/2022
Published online: 23/01/2023
https://doi.org/10.1590/1676-0611-BN-2022-1416