Journal of Threatened Taxa |
www.threatenedtaxa.org | 26 September 2020 | 12(13): 16912–16915
ISSN 0974-7907 (Online) | ISSN 0974-7893
(Print)
doi: https://doi.org/10.11609/jott.5308.12.13.16912-16915
#5308 | Received 06 August 2019 | Final
received 14 August 2020 | Finally accepted 29 August 2020
Breeding biology of Malabar Tree
Toad Pedostibes tuberculosus
(Anura: Bufonidae) from
Castle Rock, Karnataka, India
Deepak Deshpande 1 & Nikhil Gaitonde
2
1 Vishwas Hospital, Old Pune
Bangalore Road, Sakharwadi, Nipani,
Karnataka 591237, India.
2 7, Sukhaniwas,
10th lane, Prabhat road, Pune, Maharashtra 411004, India.
1 vishwashospital@rediffmail.com, 2
nngaitonde@gmail.com (corresponding author)
Editor: Neelesh Dahanukar,
Indian Institutes of Science Education and Research (IISER), Pune, India. Date
of publication: 26 September 2020 (online & print)
Citation: Deshpande, D. & N. Gaitonde
(2020). Breeding biology of
Malabar Tree Toad Pedostibes tuberculosus (Anura: Bufonidae) from Castle Rock, Karnataka, India. Journal of Threatened Taxa 12(13): 16912–16915. https://doi.org/10.11609/jott.5308.12.13.16912-16915
Copyright: © Deshpande & Gaitonde 2020. Creative Commons Attribution 4.0
International License. JoTT allows unrestricted use, reproduction, and
distribution of this article in any medium by providing adequate credit to the
author(s) and the source of publication.
Funding: NG was supported by a bridging postdoctoral fellowship from the National Centre for Biological Sciences
during the writing of the manuscript.
Competing interests: The authors declare no competing interests.
The Western
Ghats biodiversity hotspot harbors a wide variety of
herpetofauna, especially anurans, with many endemic and endangered species (Roelants et al. 2004; Naniwadekar
& Vasudevan 2006; Chandramouli & Ganesh 2010;
Van Bocxlaer et al. 2012; Dahanukar
et al. 2016). Anurans in the Western
Ghats face numerous threats such as habitat loss, pollution and changing
climate, and are endangered due to their small populations, specialized
adaptations, and narrow distributions (Naniwadekar
& Vasudevan 2006; Van Bocxlaer et al. 2012; Dahanukar et al. 2013; Gaitonde
et al. 2016; Thorpe et al. 2018).
Despite the endangered status of many Western Ghats endemic anurans,
their natural history is largely unknown, hampering conservation efforts. We, therefore, report the breeding behavior of the Western Ghats endemic toad, Pedostibes tuberculosus
from the northern Western Ghats and highlight the variation in their
reproductive traits from populations distributed along the length of the
Western Ghats. This will not only help
in conservation prioritization, but also aid in the systematics of this group
(Das et al. 2006).
The genus Pedostibes Günther, 1876 (Anura:
Bufonidae) along with other endemic genera such as Xanthophryene and Ghatophryne,
is a part of the Bufonidae lineage that dispersed
into the Western Ghats and diversified during the Miocence
(Van Bocxlaer et al. 2009; Chan et al. 2016). Many species of these endemic genera are
patchily distributed, and are highly specialized to their habitats with strict
micro-habitat requirements, making them vulnerable to climate change (Biju et
al. 2009; Gaitonde et al. 2016; Thorpe et al.
2018). For
example, the northern Western Ghats endemic Xanthophryne
species, exclusively use lateritic rocky outcrops as breeding habitats and lay
eggs only in shallow ephemeral rocky pools/ semi-aquatic rocky habitats which
are vulnerable to desiccation, and their embryos undergo largescale mortality
due to stochastic fluctuations in humidity and temperature (Biju et al. 2009; Gaitonde et al. 2016; Thorpe et al. 2018). Pedostibes
also exhibits several specialized adaptations such as, an arboreal habit, a
short breeding period, and rapidly developing exposed embryos in aquatic/
semi-aquatic conditions and may be vulnerable to environmental fluctuations
during their breeding period (Dinesh & Rahakrishnan
2013; Chan et al. 2016; Sayyed & Nale 2017). There is limited information on the
reproductive biology of P. tuberculosus
and its mating sequence and spawning behavior has not
been documented in details.
Here, we
describe the breeding behavior of P. tuberculosus with a pictorial sequence of their mating
and spawning behavior, opportunistically encountered
during field-work at Castle Rock, Karnataka, India.
Castle Rock
(Latitude 15.41 & Longitude 74.33) is situated at an altitude of 620m, on
the Goa-Karnataka border and has tropical semi-evergreen forests with numerous
mountain streams. Pedostibes tuberculosus is locally abundant at Castle Rock and
is found near perennial streams and agricultural canals. Observations for the current study were taken
in an agricultural water-channel situated in a patch of evergreen forest. The channel was mostly dry and had a single
0.3m wide and 10m long pool of water fed by a small water cascade at one
end. The water column was ~2–3 inches
deep and channel was filled with leaf litter and surrounded by thick
undergrowth.
During a
light pre-monsoon rainfall, we opportunistically encountered an aggregation of P.
tuberculosus males at around 23.00h near an
agricultural canal fed by a perennial stream.
Males were observed calling repeatedly while perched on vegetation at a
height of about ~1m from the ground (Image 1, A). Approximately, 15 males were observed in a
10m2 area. The males were
calling repeatedly, and constantly shifted their positions on nearby
vegetation. At times, they wrestled with
each other in short duels lasting 10–30 seconds. At 01.00h, the first pair in an axillary
amplexus was observed on the ground, initially motionless, but soon started
moving around presumably searching for a suitable oviposition site (Image 1B). At 03.00h the pair entered shallow water but
were chased away by a Duttaphrynus sp. males
in full breeding-color, who had also aggregated to
breed in the same pool, slightly further away.
Eventually, at 03.45h the P. tuberculosus
pair found shallow water where they were not disturbed and started oviposition
(Image 1C). The female was submerged in
water up to her throat whereas; only a small part of the male’s hindquarters
was submerged (Image 1D). The male’s
hind limbs were positioned between the hind limbs of the female and the male’s
feet were spread beneath the female’s abdomen (Image 1C). During oviposition, the female arched her
back downwards and extended her hind limbs and deposited 10–20 eggs at a time. The male simultaneously performed 2–3 pelvic
thrusts presumably to release sperms over the freshly released eggs. After depositing the eggs, the pair moved
10–20 cm away from the previous oviposition site and sat motionless until the
female was ready to lay the next set of eggs.
The female laid eggs in several bouts and the initial clutches contained
20–60 eggs (first two bouts) while subsequent clutches had fewer eggs (next
four to five bouts). The female laid
approximately 150 eggs by the time the mating concluded. The fresh eggs were brownish in color and a clump of eggs laid was later extended as a
loose string with few detached single eggs.
Subsequently, a few more pairs started oviposition at the same
site. After about an hour, the focal
pair had finished laying all the eggs and the male released the female from a
tight axillary amplexus and crawled into the bushes. We observed the female arch her back after
being released from amplexus, and soon left the oviposition site, completing
the mating sequence. The other pairs
formed later continued oviposition in the same manner described above until
early morning (05.00h). Sympatric
anurans at the breeding site of P. tuberculosus
included Raorchestes sp., and Duttaphrynus sp.
We also observed two species of snakes, Macropisthodon
plumbicolor Green Keelback and Xenochrophis piscator Checkered
Keelback, near the breeding site and may be potential predators of P. tuberculosus.
The stagnant water pool where eggs were deposited and tadpoles
developed, contained Chironomus larvae and
plenty of leaf litter.
Anurans
have evolved a high diversity of reproductive behaviors
in response to the varied habitats they occupy, and exhibit distinct
reproductive strategies to overcome numerous biotic and abiotic challenges
(Haddad & Prado 2005; Wells 2007; Crump 2015). The Western Ghats endemic toad lineages have
locally adapted to specific microhabitats (Van Bocxlaer
et al. 2010; Thorpe et al. 2018), and understanding the reproductive biology of
anurans of the Western Ghats will not only help conservation prioritization by
identifying breeding sites and specific micro-habitat requirements, but also
help understand the role of ecological factors in shaping reproductive behaviors and mating systems. Pedostibes
tuberculosus shares several traits with other
Bufonid lineages, such as, a semi-terrestrial adult niche, parotid glands,
ability to use a wide variety of oviposition sites, and, rapidly developing exotrophous tadpoles, that aided the dispersal of the
Bufonid lineage helping it attain a global distribution (Pramuk
et al. 2007; Van Bocxlaer et al. 2010). On the other hand, reproductive traits such
as, a small clutch size and loose single eggs often exposed to semi-aquatic
conditions, seem to have evolved in response to local conditions in Western
Ghats endemic toads Pedostibes and Xanthophryene, and highlight the adaptive nature of
reproductive traits in the Bufonid lineage (Gaitonde
et al. 2016). A novel case of pelvic
thrusts during amplexus was first reported in Xanthophryne
toads (Gaitonde et al. 2016), but we observed similar
behavior in P. tuberculosus
from the northern Western Ghats, and the pelvic thrusts seems to be widespread
among bufonid species, where they possibly function to increase fertilization
success, especially in species breeding in semi-aquatic habitats. Precise estimates of fertilization and
hatching success, however, need to be measured in P. tuberculosus. We observed tadpoles of P. tuberculosus to develop rapidly and metamorphose in
approximately a month, which is consistent with earlier study (Dinesh & Rahakrishnan 2013).
Pedostibes tuberculosus populations in the Western Ghats
exhibit substantial variation in crucial life history traits such as clutch
size and choice of the oviposition site.
For example, P. tuberculosus
populations in southern India are reported to oviposit approximately 1,100 eggs
after a single mating (Chan et al. 2016), whereas, at Castle Rock we observed
females to lay only 150 eggs. A clutch
size of 250 eggs is also reported for P. tuberculosus
from an unknown location as a personal observation (Van Bocxlaer
et al. 2009). Such magnitude differences
in crucial life history traits such as clutch size are unlikely to be observed
within a species; and life history traits of P. tuberculosus
need to be estimated in other populations along with evaluating species
diversity. Apart from clutch size, P.
tuberculosus seems to exhibit substantial
variation in oviposition sites, and populations from southern Western Ghats are
reported to lay eggs in hollow cavities on tree barks, or, in clumps of Ochlandrae (Dinesh & Rahakrishnan
2013; Chan et al. 2016); whereas, populations in the northern Western Ghats lay
eggs in shallow ephemeral pools of water or on wet ground at the edge of
streams without considerable standing water (Van Bocxlaer
et al. 2009; Sayyed & Nale 2017). The variation in oviposition sites indicates
the utilization of suitable sites in local habitats and suggests reproductive behavior of P. tuberculosus
to be influenced by local availability of resources.
References
Biju, S., I. Van Bocxlaer, V.B. Giri, S.P. Loader & F. Bossuyt
(2009). Two new endemic genera and a new species of toad (Anura:
Bufonidae) from the Western Ghats of India. BMC
Research Notes 2(1): 241. https://doi.org/10.1186/1756-0500-2-241
Chan, K.O., L.L. Grismer, A, Zachariah, R.M.
Brown & R.K. Abraham (2016). Polyphyly of Asian Tree Toads,
Genus Pedostibes Günther, 1876 (Anura: Bufonidae), and the
description of a new genus from southeast Asia. PLOS ONE 11(1):
e0145903. https://doi.org/10.1371/journal.pone.0145903
Chandramouli, S.R.
& S.R. Ganesh (2010). Herpetofauna of southern Western Ghats, India −
Reinvestigated after decades. Taprobanica
02(02): 72–85.
Crump, M.L. (2015). Anuran reproductive modes: evolving
perspectives. Journal of Herpetology 49(1): 1–16. https://doi.org/10.1670/14-097
Dahanukar, N., K. Krutha, M.S. Paingankar, A.D. Padhye, N. Modak & S. Molur (2013). Endemic Asian chytrid strain
infection in threatened and endemic anurans of the northern Western Ghats,
India. PLoS ONE 8(10): e77528. https://doi.org/10.1371/journal.pone.0077528
Dahanukar, N., N. Modak, K. Krutha, P.O. Nameer, A.D. Padhye & S. Molur (2016). Leaping frogs (Anura: Ranixalidae) of the
Western Ghats of India: an integrated taxonomic review. Journal of
Threatened Taxa 8(10): 9221–9288. https://doi.org/10.11609/jott.2532.8.10.9221-9288
Das, A., J. Krishnaswamy, K.S. Bawa, M.C.
Kiran, V. Srinivas, N.S. Kumar & K.U. Karanth
(2006). Prioritisation of conservation areas in the Western Ghats, India. Biological
Conservation 133(1): 16–31. https://doi.org/10.1016/j.biocon.2006.05.023
Dinesh, K.P. & C. Rahakrishna (2013). Description
of tadpole stages of the Malabar Tree Toad Pedostibes
tuberculosus Günther, 1875 (Anura:
Bufonidae). Journal of Threatened Taxa 5(14):
4910–4912.; https://doi.org/10.11609/JoTT.o3398.4910-2
Gaitonde, N., V. Giri & K. Kunte (2016). ‘On the
rocks’: reproductive biology of the endemic toad Xanthophryne
(Anura: Bufonidae) from the
Western Ghats, India. Journal of Natural History 2933(July): 1–16. https://doi.org/10.1080/00222933.2016.1200686
Haddad, C.F.B. & C.P.A. Prado (2005). Reproductive
modes in frogs and their unexpected diversity in the Atlantic Forest of Brazil.
BioScience 55(3): 207. https://doi.org/10.1641/0006-3568(2005)
Naniwadekar, R. &
K. Vasudevan (2006). Patterns in diversity of anurans along an
elevational gradient in the Western Ghats, South India. Journal of
Biogeography 34(5): 842–853. https://doi.org/10.1111/j.1365-2699.2006.01648.x
Pramuk, J.B., T.
Robertson, J.W. Sites & B.P. Noonan (2007). Around the
world in 10 million years: biogeography of the nearly cosmopolitan true toads (Anura: Bufonidae). Global
Ecology and Biogeography 17(1): 72–83. https://doi.org/10.1111/j.1466-8238.2007.00348.x
Roelants, K., J.
Jiang & F. Bossuyt (2004). Endemic ranid (Amphibia: Anura) genera in
southern mountain ranges of the Indian subcontinent represent ancient frog
lineages: evidence from molecular data. Molecular Phylogenetics and
Evolution 31(2): 730–740. https://doi.org/10.1016/j.ympev.2003.09.011
Sayyed, A. & A. Nale (2017). New
Distribution Record and Intergeneric Amplexus in the Malabar Tree Toad, Pedostibes tuberculosus
Günther 1875 (Amphibia: Anura: Bufonidae).
Reptiles and Amphibians: Conservation and Natural History 24(3):
193–196.
Thorpe, C.J., T.R. Lewis, S. Kulkarni, A. Watve,
N. Gaitonde, D. Pryce & M.E. Knight (2018). Micro-habitat
distribution drives patch quality for sub-tropical rocky plateau amphibians in
the northern Western Ghats, India. PLOS ONE 13(3): e0194810. https://doi.org/10.1371/journal.pone.0194810
Van Bocxlaer, I., S.D Biju, S.P. Loader &
F. Bossuyt (2009). Toad
radiation reveals into-India dispersal as a source of endemism in the Western
Ghats-Sri Lanka biodiversity hotspot. BMC Evolutionary Biology 9(1):
131. https://doi.org/10.1186/1471-2148-9-131
Van Bocxlaer, I., S.D. Biju, B. Willaert, V.B. Giri, Y.S. Shouche & F. Bossuyt (2012). Mountain-associated
clade endemism in an ancient frog family (Nyctibatrachidae)
on the Indian subcontinent. Molecular Phylogenetics and Evolution 62(3):
839–847. https://doi.org/10.1016/j.ympev.2011.11.027
Van Bocxlaer, I., S.P. Loader, K. Roelants, S.D. Biju, M. Menegon
& F. Bossuyt (2010). Gradual
adaptation toward a range-expansion phenotype initiated the global radiation of
toads. Science 327(5966): 679–682. https://doi.org/10.1126/science.1181707
Wells, K.D.
(2007). The Ecology and Behavior of Amphibians.
University of Chicago Press.