Reproductive Condition of Some Bat Species in MT Makiling
Reproductive Condition of Some Bat Species in MT Makiling
Reproductive Condition of Some Bat Species in MT Makiling
Section G-2L
27 May 2015
____________________
1
A special problem submitted in partial fulfillment of the requirements in ZOO 148 - Mammalogy laboratory
under Prof. Phillip A. Alviola, 2nd semester, 2014-2015.
ABSTRACT
ii
TABLE OF CONTENTS
ABSTRACT
INTRODUCTION
METHODOLOGY
10
20
RECOMMENDATIONS
21
LITERATURE CITED
22
APPENDICES
24
INTRODUCTION
Background of the Study
Mammals are considered as a successful group of animals flourishing in and adapting to a
wide range of habitat (Gonzales, Afuang, Alviola, Dans, & de Guia, 1995). In fact, an
exceptional group of mammal modified their forelimbs into fully functional wings that enabled
them to thrive in the air.
The Philippines houses a highly diverse fauna. Currently, there are about 90 recognized
bat species in the Philippines placed under 7 families (Wilson & Reeder, 2005). These include 31
frugivorous and 59 insectivorous bat species and greater parts of these are endemic to the
country. These volant mammals dwell mostly in forests and caves and are mainly nocturnal
animals.
Bats have adapted to a variety of food source and most bat species present in the country
prefer fruit, flowers, and insects among others. It is because of these diets that most of them are
considered pests, especially in a country that rely mostly on crops for income, since they feed
and/or roost in fruit plantations. In some areas, bats are hunted by locals as a meat source, thus
greatly affecting their population negatively. In others, people have learned to live with them
peacefully since bats pollinate fruit trees and regenerate forests. Moreover, they serve as a means
for controlling insect pest population or as a tourist attraction. Some locals even use their dung as
fertilizer (Wund & Myers, Chiroptera, 2005).
Objectives of the Study
This study aimed to determine the reproductive status of the insect and fruit bat species
found in Mt. Makiling.
Rhinolophus arcuatus
Rhinolophus arcuatus (Arcuate horseshoe bat) is a member of Family Rhinolophidae. It
occurs in agricultural, montane, mossy, primary, and secondary forests throughout the
Philippines (Rossell-Amball, Tabaranza, & Wright, 2008). It is also found in Sumatra to New
Guinea. This species has two morphotypes: R. arcuatus-s and R. arcuatus-l. The first one is
relatively smaller with a narrower noseleaf, and it usually occurs in lowland caves (Heaney &
Ingle, 1992).
In terms of reproduction, it gives birth only once a year. This is true to all temperate
rhinolophids (Wund & Myers, Rhinolophidae, 2009). This species was found to have gestation
periods in March on Mt. Isarog (Heaney, et al., 1999), in April on Biliran, Leyte, and Maripipi
(Rickart, et al., 1993), and in May on Camiguin (Heaney, et al., 2006) and Palawan (Esselstyn, et
al., 2004).
For the study in Mt. Isarog (Heaney, et al., 1999), 3 males and 2 females were collected
from secondary lowland, disturbed lowland and montane forests on March 1988. One of the
females was primiparous (CRL=6mm) and the other was nulliparous. One male had inguinal
testes and two males had abdominal testes. In Biliran, Leyte, and Maripipi (Rickart, et al., 1993),
all the females collected in April were pregnant (CRL=10-17mm).
In Camiguin, Heaney, et al. (2006) examined 10 individuals of this species, in which 8
males and 2 are females. One female was pregnant (CRL=28mm) and the other female was
lactating. No testicular measurements were given for the males.
In Palawan, Esselstyn, et al. (2004) found out that most of the captured bats in the month
of May are either pregnant or lactating. On the other hand, for those that are captured in the July,
14 bats were lactating and 155 showed absence of reproductive activity.
Rhinolophus inops
Rhinolophus inops (Philippine forest horseshoe bat) is a member of Family
Rhinolophidae. It is endemic to the Philippines and is most commonly observed in Biliran and
Leyte (Heaney, et al., 1999). There is a variation in this species per geographic area (Heaney, et
al., 2006).
The females of this species have a pair teat-like appendages in their abdomen that are
not involved in milk production. Juvenile bats use these to hold on to their mother during flight
(Nowak 1994, as cited in Keller 2013). In addition, females usually give birth to only one young
per year. The gestation period lasts up to 7 weeks and the lactation period lasts up to 8 weeks
(Heaney, et al. 2010, as cited in Keller 2013).
In Mt. Isarog, Heaney, et al. (1999) captured three males only, and they did not provide
testicular measurement for these specimens. In another study in Biliran, Leyte and Maripipi by
Rickart, et al. (1993), the females captured from Biliran and Leyte on March to April 1987 were
pregnant (CRL=8-18mm) with a single embryo. According to Heaney, et al. in 1991 (as cited by
Rickart, et al., 1993), the individuals from Leyte, Biliran and Catanduanes are similar, and those
that are from Negros are relatively smaller. In Kitanglad (Heaney, et al., 2006), pregnancies were
observed in March and September (CRL=20mm) while in Catanduanes (Heaney, et al., 1991), it
was observed on February.
Rhinolopus macrotis
Rhinolopus macrotis (big-eared horseshoe bat) is a member of Family Rhinolophidae. It
occurs from India to Sumatra, including the Philippines. Only a limited number of this species
were captured here in the Philippines. They are most commonly found in caves and man-made
tunnels, where they roost (Heaney, et al., 2006). Very little is known about the reproductive
condition of this species. The first records of this species from Palawan were captured on May
and July 2000 (Esselstyn, et al., 2004). They were found in disturbed lowland forests. Two
females, both of which are pregnant, were captured in May while eight females were captured in
July, none of which is pregnant or lactating.
Ptenochirus jagori
The species commonly known as greater musky fruit bat is endemic to the
Philippines, and occurs throughout the country with the exception of Batanes and Babuyan
Islands, and Palawan Faunal regions (Heaney, et al., 2005, 2006). Males are typically larger than
females. According to Heaney, et al. (2006), the species are commonly found in lowland forest
and secondary forest but unusual at higher elevations and disturbed lower elevation mossy
forests. A study conducted by Heideman and Powell (as cited in Heaney, et al., 2006) revealed
that there are two birthing seasons for the species in late March or early April and in August
and females give birth to a solitary offspring. Heideman and Powell also stated that primiparous
females of Ptenochirus jagori can undergo delayed implantation lasting up to 5 months, thus, the
parturition by young females is only once during first year and is concurrent with the second
parturition of adult females. Moreover, a study of Heaney, et al. in Mt. Isarog, Luzon recorded
some pregnant females in the month of May (as cited in Heaney, et al., 2006). Another study of
Heaney, et al. (1999) showed that the testes of adult males are significantly larger than the young
males, 3 x 5 mm to 9 x 12 and 3 x 3 to 6 x 7 mm, respectively.
METHODOLOGY
Selection of Study Area
The study site, Camp Malaboo, is situated in Mt. Makiling at Luzon Island, Philippines
(Fig. 1). Specifically, Camp Malaboo (140803.09 N, 1211227.71 E) is located at Station 15
of Mt. Makiling National Park, Los Baos in the province of Laguna (Fig. 2). The elevation of
the site is estimated to be 650m above sea level. The site in bounded by Los Baos and Calamba
City in the north. Collection sites for volant mammals were chosen near the campsite.
Collection of Specimens
A total of mist nets 4 mist nets per collection site were positioned along the possible
flyways of bats and near feeding trees in the late afternoon. The mist nets were tended
continuously during the peak activity period from 6 oclock in the evening until 7 oclock in the
evening, and checked again from 9 oclock to 10 oclock in the evening for two nights. The nets
were left open thereafter. The nets were checked again at dawn on the following day. The caught
bats were removed and placed in cloth bags.
10
reproductive stage, and the condition of mammae were observed for the female bats. Moreover,
for pregnant females, the crown to rump length (CRL) of the embryo was measured.
Table 1. Summary of the number of male and female individual bats captured per species.
SPECIES NAME
Hipposideros diadema
Ptenochirus jagori
Rhinolophus arcuatus
Rhinolophus inops
Rhinolophus macrotis
TOTAL
SEX
NO. OF INDIVIDUALS
2
7
2
8
14
3
2
2
3
1
44
11
SUBORDER MEGACHIROPTERA
Family Pteropodidae Fruit Bat
Ptenochirus jagori (Peters, 1861), also known as the musky fruit bat, is commonly
found anywhere in the Philippines except in the islands of Batanes, Babuyan and Palawan. It was
recently reported to be capable of delayed implantation like other endemic species such as
Haplonycteris fischeri and Otopteropus cartilagonodus. Male is usually bigger than female.
(Heaney, Tabaranza, Balete, & Rigertas, 2006). Of the ten individuals caught, 8 individuals were
male and 2 were female.
The average CRL of P. jagori observed in Makiling was 37mm (Table 3). The two
pregnant females were both multiparous characterized by their swollen vagina and nipples. The
smallest average CRL was found in Catanduanes (3.5mm). In May, the pregnant bats were more
prominent though in some places like Catanduanes and Mt. Kitanglad, P. jagori could be
observed to gestate also in the months of February, March, July, and August based on previous
studies of mammalian diversity surveys (Table 3). In the study of Heideman and Powell (1998),
facultative post-implantational delay in embryonic development was observed in young females
that would be reproducing for the first time. The delay occurred during gastrulation that could
last up to 5 months in young females and no evidence was found if adult females could delay
embryonic development. The delay would synchronize young pregnant female to the parturition
of the adults. The adult females gave birth twice a year - on late March and early April, and in
August - and each gestation period lasted for four months. (Heideman & Powell, Age-specific
Reproductive Strategies and Delayed Embryonic Development in an Old World Fruit Bat,
Ptenochirus jagori, 1998). It could imply that the pregnant female accounts in other places in the
12
Philippines were at the middle of either the first gestation period or the second gestation period
of P. jagori.
The average testes size, of P. jagori observed from the captured male bats in Mt.
Makiling was 8.38mm (Table 4). Among the eight male individuals, five were adults and three
were sub-adults. Most of the adult males have testes size more than 9mm while the sub-adult
males have testes size around 7mm. In another Pteropodidae species like Haplonycteris fischeri,
if a male is born in May or June, its testes volume will still be low but will gradually increase up
to 12 months gaining equivalent testes volume of an adult just in time when the females begin to
be receptive in May and June (Heideman P. D., Delayed development in Fischer's pygmy fruit
bat, Haplonycteris fischeri, in the Philippines, 1989). This may hold true also for P. jagori since
the female has two gestation period every year.
13
Primiparous
Nulliparous
Ptenochirus jagori
Hipposideros diadema
Rhinolopus arcuatus
Rhinolophus inops
Rhinolophus macrotis
14
Table 3. Gestation months and average crown-rump length (CRL) of pregnant some female bats
in selected study areas in the Philippines.
PLACE
of
STUDY
SPECIES NAME
Hipposideros
diadema
Ptenochirus
jagori
Rhinolophus
arcuatus
Rhinolophus
inops
Rhinolophus
macrotis
Mt. Makiling
May
(20.50mm)
May
(15.08mm)
May
(24mm)
March,
September
(5.71mm)
May
(18.50mm)
Mt. Kitanglad
May
(37mm)
March, May,
July, August
May
(33mm)
March
(3mm)
April
(13.50mm)
March, April
(13mm)
February
(3mm)
Mt. Isarog
Palawan
Leyte
(12mm)
May
March
(15mm)
Catanduanes
Camiguin
February
(3.5mm)
May
(15mm)
May
(14mm)
May
-
*References: (Heaney, et al., 1999) (Heaney & Rabor, 1982) (Heaney, et al., 1991) (Heaney, et al., 2006) (Heaney, et al., 2006) (Heideman &
Heaney, 1989) (Rickart, et al., 1993)
Hipposideros diadema
6.86
Ptenochirus jagori
8.38
Rhinolophus arcuatus
3.50
Rhinolophus inops
4.00
Rhinolophus macrotis
2.00
15
SUBORDER MICROCHIROPTERA
Family Rhinolophidae Horse-shoe nosed Bats
Hipposideros diadema (E. Geoffroy, 1813) is an insectivorous bat that can be found
from Burma to the Solomon Islands and the Philippines with the exception of Batanes and
Babuyan Islands. It is commonly known as the diadem roundleaf bat. Males are a little bigger
than females. The average CRL observed from the two specimens collected in Mt. Makiling was
20.50mm. Both were considered multiparous because of the presence of placental scars and the
swelling of nipples. Pregnancies occur on May in Mt. Makiling and Palawan, and March in
Leyte (Table 3) (Heaney, Tabaranza, Rickart, Balete, & Ingle, 2006). According to Medway,
species of Hipposideros are gregarious, thus H. diadema tends to congregate during March and
April to give birth (Nowak, 1994). In Rickarts account, species of H. diadema in Luzon will
start the gestation period on March and May (Heaney, Tabaranza, Rickart, Balete, & Ingle,
2006).
Seven male H. diadema - 5 adults and 2 sub-adults - were captured during the first
netting night. Their average testes size was 6.86mm (Table 4). The adult males had more than
6mm testes size while sub-adult males had a testes size of around 5-6mm.
16
Rhinolophus arcuatus (Peters, 1871) is a widespread bat in the Philippines with two
physical differences - a wide ovate-shaped sella and a narrow, rectangular sella (Figure 7)
(Sedlock & Gomez), that have once been suggested by J.E. Hill to be R.arcuatus and R.
anderseni (Heaney, Gonzales, Utzurrum, & Rickart, 1991). Sedlock and Gomez used narrow
and wide to attach difference while Heaney, et al. (1991) designated -s and -l to
differentiate the two similar looking bats. It is believed that R. arcuatus was consisted of two or
more species by many researchers (Esselstyn, Widmann, & Heaney, 2004). Based on Table 3, R.
arcuatus captured in Mt. Makiling has an average CRL of 15.08mm, which is the same as in
Camiguin and close in Leyte, but a lot smaller in Mt. Isarog since a small number of individuals
were captured by Heaney, et al. in 1999.
17
a) wide sella
b) narrow sella
Figure 7. The two morphs of Rhinolophus arcuatus observed from captured specimens.
Among the 14 adult female caught, only one was nulliparous and the rest are pregnant.
The pregnant females were either primiparous (8 individuals) or multiparous (5 individuals)
(Table 2). The pregnancy occurs in May in Makiling and Camiguin while in Palawan, pregnancy
occurs in the months of May, July, August, September; March in Mt. Isarog, and April in Leyte
(Table 3). Lekagul and McNeely in 1977 described that the gestation of period of the species
Rhinolophus takes about 7 weeks producing a young that attains sexual maturity in 2 years
(Nowak, 1994). In temperate regions, rhinolophids reproduce once a year (Wund & Myers,
2009).
Of the three captured male individuals in Mt. Makiling, two were sub-adult and one was
adult with testes size of 1mm and 2mm, and 6mm, respectively. Their average testes size was 3.5
mm (Table 4).
Rhinolophus inops K. Andersen, 1905 (Philippine Forest Horseshoe bat) is an endemic
species of insectivorous bat found in Luzon, Mindanao, Mindoro, and Negros-Panay. It is a
common bat and the males are bigger than females. There were only two specimen caught from
the study - one primiparous female (CRL=24mm) and one nulliparous (Table 2). The occurrence
18
of pregnancy increases in the months of May in Makiling, March to Late April in Biliran and
Leyte, March and September in Mt. Kitanglad and February in Catanduanes (Table 3). An
account of a lactating female was recorded in July on Mt. Makiling by Ingle in 1992. (Heaney,
Tabaranza, Rickart, Balete, & Ingle, 2006). Gestation period of R. inops could last for 7 weeks
followed by lactation period of up to 8 weeks (Keller, 2013)
Two males captured on the mistnet but only one was measured because the other male
has testes too small to be measured by a ruler. The measured adult male has a testes size of 4mm.
19
Rhinolophus macrotis (Blyth, 1844) - little is known about big-eared horseshoe bat that
is distributed from India to Sumatra and the Philippine. This uncommon bat could be found in
lowland forest and caves. In Palawan, two pregnant female were captured in May and 8 nonpregnant adult females were captured in July (Esselstyn, Widmann, & Heaney, 2004) while in
Mt. Kitanglad, there were only two preserved specimen available and Heaney, et. al (2006) were
unable to capture a specimen. Last May, two out of three captured female bats in Makiling were
pregnant (one multiparous and one primiparous) with an average CRL of 18.50mm, while the
other one was nulliparous.
Only one male was caught during the netting night. Its testes size was 2mm. Based on the
biometrics obtained, the male bat was a sub-adult not reaching maturity yet. In Himalayas, male
R. macrotis were observed to be sexually active during September (Jnawali, et al., 2011).
Implications of Pregnancy in Female Bats
Since bats are volant mammals, reproduction is energy expensive and is a highly risky
activity (Chaverri & Kunz, 2006). Female bats during pregnancy are more vulnerable to different
stressors most especially to anthropogenic activities like logging, hunting and cave tours
(Sedlock & Gomez). They are also in need to forage double and could go distance to find food.
Fortunately, gestation periods are mostly synchronized to the flowering and fruiting patterns of
plants in the forest as observed by Bronson in 1985 (Chaverri & Kunz, 2006). Since Mt.
Makiling can provide food all-year round being in a tropical country, the species of bats
observed may have synchronized their reproductive activity to the time when the fruit trees of
the mountain is also reproducing.
20
21
22
LITERATURE CITED
Chaverri, G., & Kunz, T. H. (2006). Reproductive biology and postnatal development in the tentmaking bat Artibeus watsoni (Chiroptera:Phyllostomidae). Journal of Zoology, 270, 650656.
Danmaigoro, A., Onu, J. E., Sonfada, M. L., Umaru, M. A., Hena, S. A., & Mahmuda, A. (2014).
Gross and Morphometric Anatomy of the Male Reproductive System of Bats (Eidolon
helvum). Veterinary Medicine International, 1-5.
Esselstyn, J. A., Widmann, P., & Heaney, L. R. (2004). The mammals of Palawan Island,
Philippines. Proceedings of the Biological Society of Washington, 3(117), 271-302.
Gonzales, J. C., Afuang, L. E., Alviola, P. I., Dans, A. T., & de Guia, A. P. (1995). A Laboratory
Manual in Wildlife 101: Introduction to Philippine Wildlife. Los Baos, Laguna.
Heaney, L. R., Gonzales, P. C., Utzurrum, R. C., & Rickart, E. A. (1991). The Mammals of
Catanduanes Island: Implications for the Biogeography of small land-bridge islands in
the Philippines. Proceedings of the Biological Society of Washington, 2(104), 399-415.
Heaney, L. R., Tabaranza, B. R., Balete, D. S., & Rigertas, N. (2006). Synopsis and
Biogeography of the Mammals of Camiguin Island, Philippines.
FIELDIANA:ZOOLOGY(106), 28-48.
Heaney, L. R., Tabaranza, B. R., Rickart, E. A., Balete, D. S., & Ingle, N. R. (2006). The
Mammals of Mt. Kitanglad Nature Park, Mindanao, Philippines. FIELDIANA:
ZOOLOGY(112), 1-63.
Heideman, P. D. (1989). Delayed development in Fischer's pygmy fruit bat, Haplonycteris
fischeri, in the Philippines. Journal of Reproduction & Fertility(85), 363-382.
Heideman, P. D., & Powell, K. S. (1998). Age-specific reproductive strategies and delayed
embryonic development in an old worl fruit bat Ptenochirus jagori. Journal of
Mammalogy, 79(1), 295-311.
Heideman, P. D., & Powell, K. S. (1998). Age-specific Reproductive Strategies and Delayed
Embryonic Development in an Old World Fruit Bat, Ptenochirus jagori. Journal of
Mammalogy, 1(79), 295-311.
Jnawali, S. R., Baral, H. S., Lee, S., Acharya, K. P., Upadhyay, G. P., Pandey, M., et al. (2011).
The Status of Nepals Mammals:The National Red List Series. Kathmandu, Nepal:
Department of National Parks and Wildlife Conservation.
23
Keller, K. (2013). Rhinolophus inops. Retrieved May 26, 2015, from Animal Diversity Web:
http://animaldiversity.org/accounts/Rhinolophus_inops/
Nowak, R. M. (1994). Walker's Bats of the World (5th ed.). Maryland,USA: The Johns Hopkins
Univeristy Press.
Rossell-Amball, G., Tabaranza, B., & Wright, D. (2008). Rhinolophus arcuatus. Retrieved May
23, 2015, from The IUCN Red List of Threatened Species:
http://www.iucnredlist.org/details/19525/0
Sedlock, J. L., & Gomez, R. (n.d.). A Survey of Bats on Siquijor Island.
Wilson, D. E., & Reeder, D. M. (Eds.). (2005). Mammal Species of the World (3 ed.).
Washington, DC: Johns Hopkins University Press.
Wund, M., & Myers, P. (2005, August 31). Chiroptera. Retrieved May 22, 2015, from The
Animal Diversity Web: http://www.animaldiversity.org/accounts/Chiroptera
Wund, M., & Myers, P. (2009). Rhinolophidae. Retrieved May 26, 2015, from Animal Diversity
Web: http://animaldiversity.org/accounts/Rhinolophidae
24
APPENDICES
Appendix I. Reproductive condition of female bats captured in Mt. Makiling (May 2015).
SPECIES NAME
TAG
NUMBER
CRL
(mm)
PARITY
UTERINE
HORN WITH
EMBRYO
PLACENTAL
SCAR
Hipposideros diadema
JDVA 0846
21
multiparous
left
present
Hipposideros diadema
JDVA 0851
20
multiparous
left
present
Ptenochirus jagori
JDVA 0810
38
multiparous*
left
present
Ptenochirus jagori
JDVA 0817
36
multiparous
right
present
Rhinolophus arcuatus
JDVA 0835
19
multiparous
left
present
Rhinolophus arcuatus
JDVA 0839
19
multiparous
left
present
Rhinolophus arcuatus
JDVA 0824
17
multiparous
left
present
Rhinolophus arcuatus
JDVA 0826
12
multiparous
left
present
Rhinolophus arcuatus
JDVA 0844
12
primiparous
left
absent
Rhinolophus arcuatus
JDVA 0845
17
primiparous
left
absent
Rhinolophus arcuatus
JDVA 0809
12
primiparous
left
absent
Rhinolophus arcuatus
JDVA 0815
18
primiparous
left
absent
Rhinolophus arcuatus
JDVA 0821
15
primiparous
left
absent
Rhinolophus arcuatus
JDVA 0823
primiparous
left
absent
Rhinolophus arcuatus
JDVA 0827
18
primiparous
left
absent
Rhinolophus arcuatus
JDVA 0822
n/a
nulliparous
n/a
absent
Rhinolophus arcuatus
JDVA 0838
15
multiparous
right
present
Rhinolophus arcuatus
JDVA 0819
13
primiparous
right
absent
Rhinolophus inops
JDVA 0848
24
primiparous
left
absent
Rhinolophus inops
JDVA 0808
n/a
nulliparous
n/a
absent
Rhinolophus macrotis
JDVA 0849
20
primiparous
left
absent
Rhinolophus macrotis
JDVA 0855
n/a
nulliparous
n/a
absent
Rhinolophus macrotis
JDVA 0847
17
multiparous
right
present
25
Appendix II. Reproductive condition of male bats captured in Mt. Makiling (May 2015).
SPECIES NAME
TAG NUMBER
Hipposideros diadema
JDVA 0825
Hipposideros diadema
JDVA 0834
Hipposideros diadema
JDVA 0840
Hipposideros diadema
JDVA 0841
Hipposideros diadema
JDVA 0843
Hipposideros diadema
JDVA 0852
Hipposideros diadema
JDVA 0854
Ptenochirus jagori
JDVA 0812
Ptenochirus jagori
JDVA 0816
Ptenochirus jagori
JDVA 0818
10
Ptenochirus jagori
JDVA 0829
Ptenochirus jagori
JDVA 0831
Ptenochirus jagori
JDVA 0832
Ptenochirus jagori
JDVA 0833
Ptenochirus jagori
JDVA 0837
10
Rhinolophus arcuatus
JDVA 0828
Rhinolophus arcuatus
JDVA 0830
Rhinolophus arcuatus
JDVA 0836
Rhinolophus inops
JDVA 0814
n/a*
Rhinolophus inops
JDVA 0820
Rhinolophus macrotis
JDVA 0850