Journal of Threatened Taxa |
www.threatenedtaxa.org | 26 December 2020 | 12(17): 17374–17379
ISSN 0974-7907 (Online) | ISSN 0974-7893
(Print)
doi: https://doi.org/10.11609/jott.5740.12.17.17374-17379
#5740 | Received 28 January 2020 | Final
received 10 November 2020 | Finally accepted 04 December 2020
Larvae of the blow fly Caiusa testacea (Diptera: Calliphoridae) as egg
predators of Polypedates cruciger Blyth, 1852 (Amphibia: Anura:
Rhacophoridae)
W.G.D. Chathuranga
1, K. Kariyawasam 2 , Anslem de
Silva 3 & W.A.Priyanka P. de Silva 4
1,2,4 Department of Zoology, Faculty of
Science, University of Peradeniya, Peradeniya, Sri Lanka.
1 Postgraduate Institute of
Science, University of Peradeniya, Peradeniya, Sri Lanka.
3 No 15/1, Dolosbage
Road, Gampola, Sri Lanka.
1 dilanchathuranga9@gmail.com, 2
kalpakdkc@gmail.com, 3 kalds@sltnet.lk, 4 depriyanka@pdn.ac.lk
(corresponding author)
Editor: Daniel Whitmore, State Museum of
Natural History Stuttgart, Rosenstein, Germany. Date
of publication: 26 December 2020 (online & print)
Citation: Chathuranga,
W.G.D., K. Kariyawasam, A.D. Silva & W.A.P.P. de
Silva (2020). Larvae of the blow fly Caiusa testacea (Diptera: Calliphoridae) as egg
predators of Polypedates cruciger Blyth, 1852 (Amphibia: Anura:
Rhacophoridae). Journal of Threatened Taxa 12(17): 17374–17379. https://doi.org/10.11609/jott.5740.12.17.17374-17379
Copyright: © Chathuranga
et al. 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: National Research Council Sri Lanka
(Grant No: NRC 16-059) and
Amphibian Specialist Group/IUCN/ SSC Seed Grant.
Competing interests: The authors
declare no competing interests.
Acknowledgements: Financial assistance from
National Research Council Sri Lanka (Grant No: NRC 16-059) to W.A.P.P. de
Silva. Amphibian Specialist
Group/IUCN/SSC Seed Grant to A. de Silva for threats to amphibians of Sri Lanka
study.
Habitat destruction and
alteration have been identified as the most detrimental causes of amphibian
decline (Kiesecker 2003). The effects of climate change and amphibian
diseases, however, are emerging topics, and have taken increased attention in
conservation approaches regarding the amphibian fauna (Hayes et al. 2010; Li et
al. 2013). Predatory pressure during
different life stages of amphibians is another factor that significantly
affects populations (Chivers et al. 2001; Blaustein et al. 2012).
Diverse invertebrate and vertebrate fauna prey on eggs and tadpoles of
aquatic and terrestrial nesting anurans (De Silva 2001a,b; Lingnau
& Di-Bernardo 2006). According to Downie (1990), terrestrial foam nests of Rhacophoridae have evolved to protect eggs and embryos from
aquatic predators. Some vertebrates
(e.g., monkeys and snakes) and invertebrates (e.g., beetles, ephydrid flies,
phorid flies, spiders, ants, and blow flies), however, have been identified as
egg predators of anuran foam nests (Vonesh 2000; Rödel et al. 2002; Menin & Giaretta 2003; Lingnau &
Di-Bernardo 2006; Banerjee et al. 2018).
Blow flies of the genus Caiusa (Diptera: Calliphoridae) are one
of the major predators of terrestrial Rhacophoridae
eggs (Rognes 2015).
These flies are one of the major reasons for embryo mortality of some
rhacophorid genera, including Chiromantis, Feihyla, Polypedates,
and Rhacophorus (Lin & Lue 2000).
So far, seven known species of Caiusa
(C. borneoensis Rognes,
2015, C. coomani Séguy, 1948, C. indica
Surcouf, 1920, C. karrakerae
Rognes, 2015, C. kurahashii
Rognes, 2015, C. violacea
Séguy, 1925, and C. pooae Rognes, 2015) have
been identified as foam nest predators and predators of jelly-like egg masses
of anurans (Lin & Lue 2000; Rognes 2015; Banerjee
et al. 2018). The emerging larvae of
these fly species consume eggs and developing embryos in egg masses. There are knowledge gaps in our understanding
of the fly-anuran interactions and the wider impact of these flies on anuran population
dynamics.
Sri Lanka is a tropical country
with more than 120 species of anurans, nearly 104 of which are endemic to the
country (De Silva & Wijayathilaka 2019). Approximately 83 (69%) of the reported
species belong to the family Rhacophoridae, including
arboreal foam nesting Polypedates and Taruga species (Meegaskumbura
et al. 2010). The majority (more than
75%) of anuran species in the country are categorized as threatened, mainly due
to anthropogenic activities (Manamendra-Arachchi
& Meegaskumbura 2012; De Silva & Wijayathilaka 2019).
Current conservation approaches are mainly aimed at minimizing habitat
destruction and other adverse human activities.
Only a few studies, however, have reported the effect of amphibian
diseases on the population structure of anurans in Sri Lanka (De Silva 1999; Rajakaruna et al. 2007; Jayawardena et al. 2010; De Silva
2011), and hardly any studies have investigated predatory pressure on different
life stages of amphibians in the country.
Morgan-Davies (1958) reported Caiusa
indica as predatory in foam nests of Polypedates cruciger Blyth,
1852 (Anura: Rhacophoridae)
in Sri Lanka. According to De Silva
& De Silva (2000), a species of Calliphoridae fly
acts as an egg predator of P. cruciger
frogs, however, these authors did not provide a species-level identification
for the flies. Therefore, there are some
literature gaps in information about predatory flies and their pressure on the
developmental stages of anurans in Sri Lanka.
Thus, detailed investigations including systematic and quantified
studies to assess the damage caused by the egg predators to anuran eggs are
important in relation to conservation actions.
In this study, we identified natural dipteran predators of foam nests of
P. cruciger, an endemic Rhacophoridae species in Sri Lanka. Further, we quantified the egg mortality of P.
cruciger due to the infestation of the predatory
dipteran fly.
The study was conducted from May
2019 to August 2019, at two localities [Gampola
(7.1500N, 80.5550E) and Peradeniya (7.2590N, 80.5970E)] in the Kandy District of Sri
Lanka. Spawns were searched for in
microhabitats with P. cruciger (i.e.,
man-made ponds, cement water tanks, domestic wells, tree-holes, and organically
managed agricultural lands). When a
fresh spawn was located, it was observed and video recorded for about 10-15 minutes to
report spawn visitors. The location of
the foam nest and the height from the ground level to the nest were
recorded. The spawns were examined daily
at both selected localities until the embryos developed into tadpoles. A plastic container filled with 1,000ml of
dechlorinated water was kept below each egg mass to collect emerging
tadpoles. Observations were made at
24-hour intervals and the developed tadpoles were released to the respective
water sources after recording the number.
A similar procedure was followed for both infected and non-infected
spawns. The presence of maggots, color
changes, and the shape of the foam nests were used to distinguish infected
nests from uninfected ones. Three
severely infected spawns were carefully removed from the attached substrates
and brought to the Insectary, Department of Zoology, University of Peradeniya
for further investigations. At the
laboratory, the foam nests were placed in dechlorinated water in a tray and transferred
to fine-mesh mosquito rearing cages (50 × 50 × 50 cm) for maintenance of the
fly colonies (at 25°C temperature, 75% relative humidity, and 12 D: 12 L
photoperiodicity). Emerged flies were
euthanized at -20°C in a freezer and pinned for identification. Morphological identification was done using
the standard taxonomic key in Rognes (2015).
To confirm the identity of the
dipteran species, DNA barcoding was also performed. DNA was extracted from some of the collected
flies following Livak (1984). The mitochondrial Cytochrome Oxidase I (COI)
gene was amplified using the previously described primers C1-J-1718F (5’-GGA GGA TTT
GGA AAT TGA TTA GTT CC-3’) and C1-N-2191R (5’-CCC GGT AAA
ATT AAA ATA TAA ACT TC-3’) (Simon et al. 1994). PCR amplification was done in a thermal
cycler (Techne-Flexigene, England) following Nolan et al. (2007). Positive PCR products were sequenced using an
automatic DNA sequencer (Applied Biosystems Series 3500, U.S.A.) in the
Department of Molecular Biology and Biotechnology, University of
Peradeniya. The sequence trace files
were manually inspected using MEGA V7 (Kumar et al. 2016) and low-quality
sequences were excluded from the analysis.
The DNA sequences were annotated using the GenBank database
(https://www.ncbi.nlm.nih.gov/) and BLASTn tool. The newly generated sequences were deposited
in GenBank under the accession numbers MN786865 and MN786866.
The dissection and examination of
male genitalia were done following Rognes
(2009). The tip of the abdomen (from
tergite 4) was removed and transferred to a 10% potassium hydroxide solution,
then heated in a water bath for about 20 minutes. The abdomen was then transferred to distilled
water and rinsed with 95% ethanol for 10 minutes to fix the integument. The male genital organs were separated using
fine forceps, for preparation of microscopic slides. The separated male genitalia were mounted
using Canada Balsam, and photographs of the prepared slides were taken using an
Olympus BX53 Digital Upright Microscope (Olympus Corporation, Florida, USA).
Morphological identification
confirmed that the emerged flies belonged to Caiusa
testacea Senior-White, 1923 of the family Calliphoridae.
According to Rognes (2015), the following
morphological features were identified for them. Cerci short, backwardly bent, and with a
pronounced distal separation between the apices in dorsal view. Base of cerci
wide proximal to separation (Image 2A).
In lateral view, surstylus rather broad and
short, very gently curved below.
Thoracic dorsum yellow and tergites 4 and 5 of abdomen with slight
darkening and lack of metallic bluish sheen (Image 2D). A BLAST search of the GenBank database showed
a 96.92% identity to available Caiusa testacea sequences together with a 100% query cover.
A total of 24 spawns of P.
cruciger were studied (Image 1a-1d). Observations were carried out on 10 spawns in
Gampola (including the three collected spawns) and 14
spawns from the Peradeniya study site.
These spawns were located at a height of 0.1–3.0 m above the
ground. Plant species such as Polyscias scutellaria (Araliaceae), Nelumbo
nucifera (Nelumbonaceae), Gliricidia
sepium (Fabaceae), Echinodorus
palifolius (Alismataceae),
Persea americana (Lauraceae), and artificial substrates including
cement walls, metal wire mesh, ceiling sheets, metal or plastic pipes just
above a water source, were the most common spawning sites of P. cruciger. Of
the examined spawns, 16 (66.7%) were not infected while eight (33.3%) were
infected with fly larvae (Image 1f). All
the infected spawns were reported from the Gampola
study location, representing 80% of the total.
During this study, we observed
oviposition of C. testacea flies only
three times (Image 1e) on fresh foam nests of P. cruciger,
and the larvae of C. testacea emerged
from two-day-old infected spawns. An
average of 354 ± 67 embryos developed into tadpoles (Image 1c) from healthy
spawns (n=15), except one that produced an exceptionally high number of
tadpoles (approximately 800). When
compared with the healthy spawns, none of the embryos of the infected spawns
(n=8) developed into tadpoles (Image 1d).
According to our observation of eight infected spawns, approximately 400
embryos were destroyed with a single nest infestation. An average of 52 ± 9 C. testacea larvae pupariated (Image 1g) and 17 ± 8
emerged as adults from the three collected spawns (Image 1h). Accordingly, an average of 33% (17/52) of the
larvae were able to complete their life cycle from a single spawn. The 1st to 3rd instar
larval stages of the fly lasted around 6-7 days, while the puparial period lasted 8-11 days. The life cycle of C. testacea was completed within 18 to 20 days. Emerged adult flies were freeze-killed and
pinned for identification. Larval
instars, puparia, and a few adults of C. testacea were also preserved in 70% ethanol
as voucher specimens and deposited in the Zoonotic and Disease Ecology
Laboratory of the Department of Zoology, University of Peradeniya, Sri
Lanka. Different morphological body
aspects of C. testacea, including
taxonomic features, are shown in Images 1h, 2A-2D.
Our study highlights the threat
caused by C. testacea flies to the foam
nests of Polypedates cruciger
frogs and provides an indication of the major impact of these flies on the
population dynamics of P. cruciger. Even though studies have reported the impact
of predatory pressure causing the population decline of amphibians (Lin &
Lue 2000; Kiesecker 2003), it has not been listed as
a priority factor in conservation approaches in Sri Lanka. In this study, we provide data on the natural
predatory pressure of the calliphorid fly Caiusa
testacea on the population structure of the
rhacophorid tree frog Polypedates cruciger.
Further, our results provide evidence of natural threats of Rhacophoridae anurans in Sri Lanka.
The presence of these flies had
been reported from Sri Lanka, India, and Nepal by Rognes
(2015), however, these flies had not been identified as egg predators of Sri
Lankan Rhacophoridae species by any of the earlier
studies. Our results reveal that larvae of C. testacea
flies destructively consume eggs and embryos of P. cruciger. In
an earlier study, Caiusa indica was identified as an egg predator of P. cruciger in Sri Lanka (Morgan-Davies 1958); however,
previous studies had not identified C. testacea
as a predator of foam nests of Rhacophoridae, and
this is the first study that reports on the feeding behavior and the life
history of C. testacea.
Rognes (2015) estimated that the time
from the infestation of spawns by Caiusa flies
to the completion of metamorphosis is nearly a week. In contrast, we observed a relatively longer
developmental period, where C. testacea
flies complete metamorphosis within three weeks. Lin et al. (2000) and Lin & Lue (2000)
described the oviposition behavior of Caiusa
violacea (as C. coomani). According to those authors, the flies lay
their eggs when the outer surface of the foam nest is soft, within a few hours
after the foam nest is formed.
Similarly, Banerjee et al. (2018) reported that Caiusa
flies lay their eggs on foam nests seven hours after the construction of the
nest. Our study confirmed the oviposition of C. testacea
flies on fresh foam nests of P. cruciger
(Image 1e), however, we were not able to provide more specific information
about the timeframe during which the flies are attracted to the nests. Our observations showed that larvae appeared
within 2 to 3 days after oviposition and that the life cycle was completed (to
metamorphosis) within 18 days.
Rognes (2015) reported that most of the
dipteran predators of foam nests are able to respond to chemical cues released
from the fresh foam nests built by the frogs.
Thus, the gravid females of C. testacea
flies may respond to chemical cues of freshly formed foam nests or chemical
signals produced by P. cruciger frogs
during spawning. Our data could not,
however, confirm this hypothesis. There
are interesting hypotheses explaining the selection of foam nests by dipteran
flies as oviposition sites. For example,
Banerjee et al. (2018) hypothesized that the frog eggs represent easier prey
for Caiusa larvae compared to mobile tadpoles,
which may allow these flies to overcome environmental constraints and resource
limitations.
The distribution of P. cruciger extends 1,500m in the wet zone of
central and southwestern parts of Sri Lanka (De Silva & De Silva
2000). Caiusa
testacea has also been reported from similar
locations in the central part of Sri Lanka, including Maskeliya,
Suduganga, Kandy, and Niroddumunai
(Rognes 2015), where P. cruciger
is also reported. This habitat
overlap of the predatory flies and P. cruciger
may have driven the evolution of the predatory behavior of this fly species
on the foam nests of P. cruciger. At the same time, this habitat overlap may
negatively affect P. cruciger as it
gives more opportunities for C. testacea
flies to attack their nests. According to IUCN Red list 2012 categories, P.
cruciger is listed as a Least Concern (LC)
anuran species (Manamendra-Arachchi & Meegaskumbura 2012); however, the continual increase of
anthropogenic impacts and changing climatic factors, together with infestations
of C. testacea, may negatively affect P.
cruciger populations, causing it to
become a ‘threatened species’.
Furthermore, Sri Lanka harbors four more foam nesting anuran species in
the family Rhacophoridae [(Polypedates
maculates Gray 1830, Taruga eques Günther,
1858, Taruga fastigo
(Manamendra-Arachchi & Pethiyagoda,
2001), and Taruga longinasus
(Ahl, 1927)] (Meegaskumbura
et al. 2010). As a result, there are
possibilities for all other foam nesting Rhacophoridae
anurans to be endangered by nest predation by Caiusa
testacea flies.
As we have seen the habitat overlap of Rhacophoridae
species and these flies, there is a high chance of egg predation by Caiusa on these tree frogs in Sri Lanka. A proper understanding of the biology,
distribution, and population assessments of both C. testacea
and P. cruciger, however, will be vital
in assessing the threats of C. testacea
flies on the population dynamics of P. cruciger
in the country.
In summary, we report C. testacea as a predator of foam nests of P.
cruciger frogs of the family Rhacophoridae in Sri Lanka for the first time. More importantly, we recognize the predatory
pressure of these flies on spawns of P. cruciger,
highlighting their needful consideration in conservation approaches concerning
these frogs.
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