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Chytrid Fungus (Batrachochytrium dendrobatidis) Undetected in the Two Orders of Seychelles Amphibians

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Herpetological Review 46(1), 2015
AMPHIBIAN DISEASES 41
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© 2015 by Society for the Study of Amphibians and Reptiles
Chytrid Fungus (Batrachochytrium dendrobatidis)
Undetected in the Two Orders of Seychelles Amphibians
Infection by the fungal pathogen Batrachochytrium
dendrobatidis (Bd) is a major driver in global amphibian
declines (Berger et al. 1998; Skerratt et al. 2007) and can occur
in all three orders of Amphibia, having been most recently
documented in the Gymnophiona (Doherty-Bone et al. 2013;
Gower et al. 2013). Bd has been detected in 71 countries and
695 amphibian species (Olson and Ronnenberg 2014) but to our
knowledge no screening for its presence or anecdotal evidence
of chytridiomycosis has been reported from the Seychelles
Archipelago, a biodiversity hotspot (Myers et al. 2000) with
a very high proportion (86%) of endemic amphibian genera
(Poynton 1999) (Fig. 1).
Eleven of the 12 species of Seychelles amphibians (Table
1) are globally significant. The four species of sooglossid
frog are unique in being the only amphibian family endemic
to an island group, and the three genera of caecilians (all
endemic, comprising a radiation of six species) are the
only gymnophionan genera confined to islands. The single
hyperoliid frog species occurring here is endemic to the
Seychelles, leaving the single ptychadenid frog as the only
non-endemic amphibian (Nussbaum 1984). Being primarily
fossorial, caecilians are considered difficult study organisms
JIM LABISKO*
Durrell Institute of Conservation and Ecology,
School of Anthropology and Conservation,
University of Kent, Canterbury CT2 7NR, UK
SIMON T. MADDOCK
Department of Life Sciences, The Natural History Museum,
Cromwell Road, London SW7 5BD, UK; Department of Genetics,
Evolution and Environment, University College London,
Gower Street, London WC1E 6BT, UK
MICHELLE L. TAYLOR
Durrell Institute of Conservation and Ecology,
School of Anthropology and Conservation,
University of Kent, Canterbury CT2 7NR, UK
LINDSAY CHONG-SENG
Plant Conservation Action group,
P O Box 392, Victoria, Mahé, Seychelles
DAVID J. GOWER
Department of Life Sciences, The Natural History Museum,
Cromwell Road, London SW7 5BD, UK
FELICITY J. WYNNE
Institute of Zoology, Zoological Society of London,
Regents Park, London NW1 4RY, UK
EMMA WOMBWELL
Durrell Institute of Conservation and Ecology,
School of Anthropology and Conservation, University of Kent,
Canterbury CT2 7NR, UK; Institute of Zoology,
Zoological Society of London, Regents Park, London NW1 4RY, UK
CHARLES MOREL
Natural History Museum, Victoria, Mahé, Seychelles
GEORGIA C. A. FRENCH
Amphibian and Reptile Conservation Trust,
655a Christchurch Road, Boscombe, BH1 4AP, UK
NANCY BUNBURY
Seychelles Islands Foundation, PO BOX 853, Victoria, Mahé, Seychelles
KAY S. BRADFIELD
Perth Zoo, South Perth, WA 6151, Australia
*Corresponding author; e-mail: jl412@kent.ac.uk
Fig. 1. Location map showing the position of the Seychelles Archi-
pelago in relation to the African coast and Madagascar. Zoomed
panel shows the main inner islands. Map generated using ArcMap
10.1 (ESRI 2012).
Herpetological Review 46(1), 2015
42 AMPHIBIAN DISEASES
and collection usually requires dedicated digging (Gower and
Wilkinson 2005), such that there have been few caecilian Bd
field surveys (Gower et al. 2013). Similarly, sooglossid frogs
are cryptic in their habits, undergoing direct development as
part of a completely terrestrial life cycle in often inaccessible,
elevated areas of moist forest (Nussbaum 1984; Nussbaum and
Wu 2007). In contrast, the Seychelles Treefrog (Tachycnemis
seychellensis: see Maddock et al. 2014), and the likely introduced
Mascarene Ridged Frog (Ptychadena mascareniensis: see
Vences et al. 2004) can be easier to encounter, forming breeding
aggregations around marshes, streams, and temporary pools,
especially in the evening (T. seychellensis) and/or after rain
events (P. mascareniensis) (Nussbaum 1984). Bd is known to
infect P. mascareniensis in mainland Africa (www.bd-maps.net/
surveillance/s_species.asp; accessed 3 March 2014; Goldberg
2007), while Olson et al. (2013) identified a 50% prevalence of
Bd in African Hyperoliidae, the family to which T. seychellensis
belongs.
Between May 2010 and March 2013, skin swabs were taken
from wild-caught caecilians and metamorphosed anurans at
multiple locations across six of the Seychelles’ inner islands
(Fig. 2). All sampled specimens were swabbed alive and within
24 hours of capture, using rayon-tipped MW100 fine-tip swabs
(Medical Wire and Equipment, Corsham, Wiltshire, England).
Swabbing protocol generally followed best-practice methods
available at the time (e.g., Smith 2011). However, our sampling
was undertaken by three separate research groups operating
over the period, with differing primary research aims. Therefore,
some deviation from standard biosecurity protocol did occur,
including capture and initial handling of amphibians without
gloves, and (although infrequent) housing more than one animal
(but always of the same species) in the same plastic bag upon
capture. The principle aim was to gather a representative sample
from sites within broadly separate locations, and not to swab
every individual encountered or captured. A large proportion
of sooglossid frog swabbing was undertaken in the field by a
single person (JL). These mostly very small anurans (except for
individuals of Sooglossus thomasseti measuring greater than
25 mm snout–vent length) were cleaned of debris and soil by
transferring them to a small plastic zip-lock bag and rinsing with
fresh water sourced at the sampling locality. Although this rinsing
may have removed some zoospores, it was performed to reduce
the increased likelihood of PCR inhibition. The water was then
drained and the animal gently restrained and swabbed within the
tABle 1. Distribution of Seychelles amphibians (adapted from Nussbaum 1984), including the 2009 discovery of Sooglossidae on Praslin ( Tay-
lor et al. 2012) and their IUCN Red List status (IUCN 2013): LC – Least Concern; EN – Endangered; CR – Critically Endangered. Caecilian
taxonomy follows Wilkinson et al. (2011).
Order Family Species Islands present Conservation status
Anura Hyperolidae Tachycnemis seychellensis La Digue, Mahé, Praslin, Silhouette LC
Anura Ptychadenidae Ptychadena mascareniensis Cerf, Curieuse, Frégate, Grand Soeur, LC
La Digue, Mahé, Northa, Praslin, Silhouette
Anura Sooglossidae Sooglossus sechellensis Mahé, Praslin, Silhouette EN
Anura Sooglossidae Sooglossus thomasseti Mahé, Silhouette CR
Anura Sooglossidae Sechellophryne gardineri Mahé, Silhouette EN
Anura Sooglossidae Sechellophryne pipilodryas Silhouette CR
Gymnophiona Indotyphlidae Grandisonia alternans Félicité, Frégate, La Digue, Mahé, LC
St. Anne, Silhouette
Gymnophiona Indotyphlidae Grandisonia larvata Félicité, La Digue, Mahé, Praslin, LC
St. Anne, Silhouette
Gymnophiona Indotyphlidae Grandisonia sechellensis Mahé, Praslin, Silhouette LC
Gymnophiona Indotyphlidae Hypogeophis brevis Mahé EN
Gymnophiona Indotyphlidae Hypogeophis rostratus Cerf, Curieuse, Félicité, Frégate, Grand Soeur, LC
La Digue, Mahé, Praslin, St. Anne, Silhouette
Gymnophiona Indotyphlidae Praslinia cooperi Mahé, Praslin EN
a New locality record
Herpetological Review 46(1), 2015
AMPHIBIAN DISEASES 43
bag, removing the need for direct handling and minimizing risk
of cross-contamination. Larger anurans, and sooglossid frogs
processed when field assistance was available, were sampled
using the standard technique (Smith 2011). Caecilians were
swabbed dorsally, laterally, and ventrally along the length of the
body, and also around the vent and head. Gloves were changed
between each individual except where two or more specimens
had been housed in the same plastic bag. All amphibians not
retained as vouchers as part of broader research aims were
released at their place of capture. Swabs were kept in the dark
and transferred to cool storage, mostly refrigerated within 12 h
and frozen within one week of completed fieldwork.
DNA extractions and quantitative real time Taqman®
polymerase chain reaction (qPCR) assays were performed at the
Institute of Zoology (London, UK), using methods adapted from
Boyle et al. (2004). DNA was extracted from swabs using bead
beating with 0.5 mm silica beads and 60 µl PrepMan Ultra (Hyatt
et al. 2007). The qPCR amplifications were performed in 25 µl
reactions using Bd primers ITS-1 (forward): 5’-CCT TGA TAT AAT
ACA GTG TGC CAT ATG TC-3’ and 5.8S (reverse): 5’-AGC CAA
GAG ATC CGT TGT CAA A-3’, specific to the ITS-1/5.8S region of
rDNA (Boyle et al. 2004). Standards of 100, 10, 1 and 0.1 Bd DNA
genomic equivalents and negative controls were used in each
run. Bovine serum albumin (BSA) was included in the TaqMan®
master mix, to reduce inhibition of the PCR (Garland et al. 2010).
Each sample was run in duplicate and no amplification in either
replicate indicated a negative result.
A total of 291 skin swabs were obtained from Seychelles
amphibians, representing 10 of the 12 species known to occur
across the archipelago. All 213 anurans and 78 caecilians tested
negative for Bd (comprising 66 Sooglossus sechellensis [Fig. 3];
13 S. thomasseti, 14 Sechellophryne gardineri, 99 Tachycnemis
seychellensis, 21 Ptychadena mascareniensis, 18 Grandisonia
alternans [Fig. 4], 7 G. larvata, 10 G. sechellensis, 6 Hypogeophis
brevis, 23 H. rostratus, 14 unidentified caecilians) (Table 2). No
macroscopic presentation of chytridiomycosis-like symptoms
or associated mortality was observed in any sampled individual,
or in any amphibian encountered during the fieldwork. Our
results suggest a widespread absence of Bd between 2010 and
2013 across six of the eleven amphibian-inhabited islands of
the Seychelles archipelago. Some caution should be exercised in
interpreting our results as indicating that the Seychelles are free
of Bd. Many of the locations sampled were in close proximity to
one another and/or linked by contiguous habitat, and so could
be described as a single location for the purposes of achieving
the recommended minimum sample size of 30 amphibians per
site (Smith 2011), but the temporal differences between site
surveys and overall limited sampling invariably resulted in this
not being achieved (Table 2), leading to the possibility of type II
errors. Also, the recommendation for sampling >59 individuals
to detect Bd when infection rate is low (Skerratt et al. 2008)
was achieved for only two species sampled (T. seychellensis, S.
sechellensis), two islands sampled (Mahé and Praslin), and for the
two pooled samples of all anurans and all caecilians. Prevalence
of Bd infection in anurans indicates seasonal peaks in the cooler
months (Berger et al. 2004; Retallick et al. 2004; Kriger and Hero
2007) even with little seasonal temperature variation (Whitfield at
al. 2012). Sampling of Seychelles amphibians was not undertaken
during the two (historically) coolest months of July and August.
However, housing more than one animal in the same capture bag,
although limited in occurrence, increased the opportunity for
cross-contamination from chytrid zoospores, making detection of
Bd more likely by fostering false-positive results for infection.
Fig. 2. Sampling localities for Batrachochytrium dendrobatidis across
the Seychelles inner islands. Map generated using ArcMap 10.1 (ESRI
2012).
Fig. 3. Sooglossus sechellensis from Mahé, Seychelles Archipelago.
IMAGE BY JIM LABISKO
Fig. 4. Grandisonia alternans from Silhouette, Seychelles Archipelago.
IMAGE BY DAVID GO WER
Herpetological Review 46(1), 2015
44 AMPHIBIAN DISEASES
Direct development—a reproductive mode adopted by
the Sooglossidae and at least one Seychelles caecilian (H.
rostratus; Nussbaum 1984)—may provide a limiting factor to
the transmission of Bd between and among amphibians (Todd
2007; but see Longo and Burrowes 2010). The probably more
vagile T. seychellensis and P. mascareniensis require water bodies
for aquatic larval development, and potentially present more
suitable hosts for the dispersal and spread of Bd. Due to previous
evidence of human-mediated trans-oceanic dispersal (Vences
et al. 2004), P. mascareniensis in particular may lend itself to
continuing introduction and transportation by way of tourist and/
or domestic traffic, especially among the main islands of Mahé,
Praslin, and La Digue (Fig. 1). This species’ propensity for dispersal
was evidenced first-hand during fieldwork following the discovery
of a novel, reproducing population on North Island. Similarly, and
despite no currently recorded infection or capacity as a host for
Bd (www.bd-maps.net/surveillance/s_species.asp; accessed 21
September 2014), the recent discovery of Asian Common Toads
(Duttaphrynus melanostictus) on the east coast of Madagascar,
having likely arrived in shipping containers from Asia (Kolby
2014a), highlights a further risk to Seychelles endemic fauna as
a potential disease vector. The significantly shorter shipping
distances among Madagascar, the Mascarenes, and Seychelles
islands undoubtedly elevates the risk of further human-mediated
dispersal of this potentially invasive species.
Links between climate, temperature, and Bd have been
documented (see Pounds et al. 2006; Bosch et al. 2007; Lips et al.
2008; Rohr and Raffel 2010; Olson et al. 2013). In tropical regions,
elevated, moist, and riparian habitats are home to amphibian
species considered most likely to be severely threatened by Bd
(Wake and Vredenburg 2008). The endemic Seychelles amphibians
fall into at least two, and often all three of these categories which,
combined with their restricted range, highlights the requirement
for targeted conservation measures (Sodhi et al. 2008). In light of
the recent discovery of Bd in Malagasy anurans (Kolby 2014b),
and given the potential susceptibility of Seychelles amphibians,
continued disease monitoring warrants consideration as part of
ongoing conservation work for this globally significant amphibian
community. Effective implementation of Seychelles’ recently
approved Biosecurity Act (Animal and Plant Biosecurity Act, 2014)
is consistent with maintaining such vigilance.
Acknowledgments.─—This research was supported by the Durrell
Institute of Conservation and Ecology; The Natural History Museum,
London; University College London; Seychelles Islands Foundation;
Institute of Zoology; Seychelles National Parks Authority; The System-
atics Association; BBSRC’s SynTax scheme; and the Darwin Initiative
(grant 19-002). We thank T. Garner for facilitating laboratory work at
the Institute of Zoology, London; Seychelles Bureau of Standards for
permission to carry out fieldwork; Seychelles Department of Environ-
ment for permission to collect and export samples; Islands Develop-
ment Company for permissions and hosting on Silhouette; Island
Conservation Society for field assistance on Silhouette; M. La Bus-
chagne for access to Coco de Mer Hotel land on Praslin; North Island
Seychelles for permissions and hosting on North Island; R. Bristol, R.
Griffiths, and J. Groombridge for organisational and field assistance; K.
Beaver, D. Birch, P. Haupt, M. Jean-Baptiste, C. Kaiser-Bunbur y, J. Mou-
gal, M. Pierre, N. Pierre, D. Quatre, A. Reuleaux, H. Richards, A. Rob-
erts, and many other NGO staff, researchers, and Seychellois for their
in- and ex-situ support. We also thank D. Olson and an anonymous
reviewer for helpful suggestions on a previous draft of this manuscript.
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... The frog family Sooglossidae Noble, 1931 are of Gondwanan origin (Biju & Bossuyt, 2003;Feng et al., 2017;Frazão et al., 2015), and endemic to the inner islands of the Seychelles archipelago (being emergent sections of an isolated Gondwanan fragment) and includes four species: Sooglossus sechellensis (Boettger, 1896), Sooglossus thomasetti (Boulenger 1909), Sechellophryne gardineri (Boulenger, 1911), and Sechellophryne pipilodryas (Gerlach & Willi, 2002). Known primarily from two islands in the Seychelles-Mahé and Silhouette-in 2009, a population of So. sechellensis was discovered on a third island: Praslin (Labisko et al., 2015(Labisko et al., , 2019Taylor et al., 2012;Figure 1). Praslin (367 m elev.) ...
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How will organisms cope when forced into warmer-than-preferred thermal environments? This is a key question facing our ability to monitor and manage biota as average annual temperatures increase, and is of particular concern for range-limited terrestrial species unable to track their preferred climatic envelope. Being ectothermic, desiccation prone, and often spatially restricted, island-inhabiting tropical amphibians exemplify this scenario. Pre-Anthropocene case studies of how insular amphibian populations responded to the enforced occupation of warmer-than-ancestral habitats may add a valuable, but currently lacking, perspective. We studied a population of frogs from the Seychelles endemic family Sooglossidae which, due to historic sea-level rise, have been forced to occupy a significantly warmer island (Praslin) than their ancestors and close living relatives. Evidence from thermal activity patterns, bioacoustics, body size distributions, and ancestral state estimations suggest that this population shifted its thermal niche in response to restricted opportunities for elevational dispersal. Relative to conspecifics, Praslin sooglossids also have divergent nuclear genotypes and call characters, a finding consistent with adaptation causing speciation in a novel thermal environment. Using an evolutionary perspective, our study reveals that some tropical amphibians have survived episodes of historic warming without the aid of dispersal and therefore may have the capacity to adapt to the currently warming climate. However, two otherwise co-distributed sooglossid species are absent from Praslin, and the deep evolutionary divergence between the frogs on Praslin and their closest extant relatives (~8 million years) may have allowed for gradual thermal adaptation and speciation. Thus, local extinction is still a likely outcome for tropical frogs experiencing warming climates in the absence of dispersal corridors to thermal refugia.
... Pakistan represents the westernmost limit of the geographic range of Duttaphrynus melanostictus. This species has been introduced outside its natural range into many parts of the world, and in these places it is considered a nuisance predator, a potential disease vector, and the cause of many other ecological problems (Labisko et al. 2015;Piludu et al. 2015). Studying the ecology and biology of D. melanostictus in its native range could help manage this species in Pakistan as well as elsewhere. ...
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... Pakistan represents the westernmost limit of the geographic range of Duttaphrynus melanostictus. This species has been introduced outside its natural range into many parts of the world, and in these places it is considered a nuisance predator, a potential disease vector, and the cause of many other ecological problems (Labisko et al. 2015;Piludu et al. 2015). Studying the ecology and biology of D. melanostictus in its native range could help manage this species in Pakistan as well as elsewhere. ...
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Research on amphibians and their conservation have gained worldwide attention, as the group includes the highest number of threatened and Data Deficient species when compared to other vertebrates. However , amphibians have long been neglected in wildlife conservation, management decisions, policy making , and research agendas in Pakistan. In this paper, an annotated checklist of the 21 amphibian species of Pakistan, a key to their identification, and detailed discussions on variation in species, including the genera Minervarya and Sphaerotheca, are provided. We found a statistically significant difference in the morphometric measurements of males but non-significant difference in the females of the two forms (rusty dorsum and dotted dorsum) of S. maskeyi. Some genera, such as Microhyla, Uperodon, Minervarya, Allopaa, Chrysopaa, Euphlyctis, Nanorana, and Sphaerotheca, in Pakistan are in need of additional data for molecular and morphological comparisons with taxa in other South Asian countries. The predicaments of amphibian research in Pakistan are discussed, gaps identified, and suggestions are made. Although the occurrence of chytrid fungus in Pakistan is predicted of low likelihood, a lack of data merits studying the prevalence of the fungus, particularly in the northern regions of the country which exhibit complex and dynamic ecosystems. It is recommended that systematic and coordinated surveys are conducted throughout the country to build a database of species occurrences and distributions. Additionally, the monitoring of wild populations and threat mitigation, as well as appropriate legislation, are suggested as long-term measures. By adopting an inclusive wildlife conservation approach in Pakistan, amphibians could be integrated into wildlife conservation and management efforts. A peer-reviewed open-access journal Muhammad Rais et al. / ZooKeys 1062: 157-175 (2021) 158
... We examined mitochondrial (mt) DNA sequence data to test the hypotheses that the Mascarene frog, Ptychadena mascareniensis (Duméril & Bibron, 1841), and Brahminy blind snake, Indotyphlops braminus (Daudin, 1803), are introduced species in the Seychelles (Nussbaum, 1980;Vences et al., 2004a). The Mascarene frog has been reported from nine of the Seychelles islands (Labisko et al., 2015) and, based on molecular genetic data for the single Seychelles individual thus far sampled, is hypothesised to have been introduced by humans from Madagascar in the recent past (Vences et al., 2004a). The Brahminy blind snake, sometimes considered native to India (Hedges et al., 2014), has a global distribution including Asia, Europe, the Middle East, Africa, Australia and the Americas (Uetz et al., 2019). ...
... 19 Fresh insights have been gained into caecilians' unique anatomy, reproductive biology, physiology, and evolution 8,17,32,33,39,42 and there is increased focus on their conservation. 13, 16,21,24 The captive requirements of amphib-ians are often complex and difficult to fulfill 36 and relatively few species of caecilian have been kept in zoological living collections. Further research is needed to establish husbandry requirements and increase our veterinary knowledge so that different species can be maintained in conservation breeding initiatives. ...
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Between July 2007 and June 2017 there were 86 deaths in the populations of eight caecilian species at the Zoological Society of London (ZSL) London Zoo. The mortality rate (deaths per animal-year at risk) ranged from 0.03 in the Congo caecilian (Herpele squalostoma) to 0.85 in Kaup's caecilian (Potomotyphlus kaupii). Among the 73 individuals examined post mortem, no cause of death or primary diagnosis could be established in 35 cases, but of the others the most common cause of death was dermatitis (22 cases). When all significant pathological findings were considered, skin lesions of varying types were again the commonest (56 cases), particularly among the aquatic species: Typhlonectes compressicauda (18 out of 21 cases), T. natans (8/10) and P. kaupii (12/14). Other common findings were poor gut-fill (35 cases), kidney and gastrointestinal lesions (10 cases each), generalized congestion (8 cases) and poor body condition (6 cases). This review adds to the growing body of knowledge regarding the presentations and causes of disease in captive caecilians.
... The cryptic diversity we have uncovered indicates a total of eight independent island lineages that should be managed accordingly. Such management action should include regular long-term population and habitat assessments, support of the genetic integrity of each ESU by carrying out no interisland translocations, and the establishment of regular screening activities for invasive pathogens including Batrachochytrium dendrobatidis, B. salamandrivorans and Ranavirus; notably, the Seychelles is one of only two global regions where pathogenic chytrids have yet to be detected (Labisko et al, 2015;Lips, 2016). The identification of distinct, island-specific populations of these frogs warrants continued investigation of their intraspecific relationships, and further insights are likely to reveal additional factors important for their future conservation. ...
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Cryptic diversity corresponding with island of origin has been previously reported in the endemic, geographically restricted sooglossid frogs of the Seychelles archipelago. The evolutionary pattern behind this has not been fully explored, and given current amphibian declines and the increased extinction risk faced by island species, we sought to identify evolutionarily significant units (ESUs) to address conservation concerns for these highly threatened anurans. We obtained genetic data for two mitochondrial (mtDNA) and four nuclear (nuDNA) genes from all known populations of sooglossid frog (on the islands of Mahé, Praslin and Silhouette) for phylogenetic analyses and to construct nuDNA haplotype networks. Bayesian and maximum likelihood analyses of mtDNA support the monophyly and molecular differentiation of populations in all species that occur on multiple islands. Haplotype networks using statistical parsimony revealed multiple high-frequency haplotypes shared between islands and taxa, in addition to numerous geographically distinct (island-specific) haplotypes for each species. We consider each island-specific population of sooglossid frog as an ESU and advise conservation managers to do likewise. Furthermore, our results identify each island lineage as a candidate species, evidence for which is supported by analyses of mtDNA based on Bayesian Poisson tree processes, and independent analyses of mtDNA and nuDNA using the multispecies coalescent. Our findings add to the growing understanding of the biogeography and hidden diversity within this globally important region.
... The cryptic diversity we have uncovered indicates a total of eight independent island lineages that should be managed accordingly. Such management action should include regular long-term population and habitat assessments, support of the genetic integrity of each ESU by carrying out no interisland translocations, and the establishment of regular screening activities for invasive pathogens including Batrachochytrium dendrobatidis, B. salamandrivorans and Ranavirus; notably, the Seychelles is one of only two global regions where pathogenic chytrids have yet to be detected (Labisko et al, 2015;Lips, 2016). The identification of distinct, island-specific populations of these frogs warrants continued investigation of their intraspecific relationships, and further insights are likely to reveal additional factors important for their future conservation. ...
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Full-text available
Cryptic diversity corresponding with island of origin has been previously reported in the endemic, geographically restricted sooglossid frogs of the Seychelles archipelago. The evolutionary pattern behind this has not been fully explored, and given current amphibian declines and the increased extinction risk faced by island species, we sought to identify evolutionarily significant units (ESUs) to address conservation concerns for these highly threatened anurans. We obtained genetic data for two mitochondrial (mtDNA) and four nuclear (nuDNA) genes from all known populations of sooglossid frog (on the islands of Mahé, Praslin and Silhouette) for phylogenetic analyses and to construct nuDNA haplotype networks. Bayesian and maximum likelihood analyses of mtDNA support the monophyly and molecular differentiation of populations in all species that occur on multiple islands. Haplotype networks using statistical parsimony revealed multiple high-frequency haplotypes shared between islands and taxa, in addition to numerous geographically distinct (island-specific) haplotypes for each species. We consider each island-specific population of sooglossid frog as an ESU and advise conservation managers to do likewise. Furthermore, our results identify each island lineage as a candidate species, evidence for which is supported by analyses of mtDNA based on Bayesian Poisson tree processes, and independent analyses of mtDNA and nuDNA using the multispecies coalescent. Our findings add to the growing understanding of the biogeography and hidden diversity within this globally important region. ADDITIONAL KEYWORDS: candidate species-cryptic diversity-evolutionarily significant unit-Indian Ocean-insular amphibians-islands-Sechellophryne-Seychelles-Sooglossidae-Sooglossus.
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Research on amphibians and their conservation have gained worldwide attention, as the group includes-ever, amphibians have long been neglected in wildlife conservation, management decisions, policy making , and research agendas in Pakistan. In this paper, an annotated checklist of the 21 amphibian species genera Minervarya and Sphaerotheca (rusty dorsum and dotted dorsum) of S. maskeyi. Some genera, such as Microhyla, Uperodon, Minervarya, Allopaa, Chrysopaa, Euphlyctis, Nanorana, and Sphaerotheca, in Pakistan are in need of additional data for occurrence of chytrid fungus in Pakistan is predicted of low likelihood, a lack of data merits studying the prevalence of the fungus, particularly in the northern regions of the country which exhibit complex and dynamic ecosystems. It is recommended that systematic and coordinated surveys are conducted throughout the country to build a database of species occurrences and distributions. Additionally, the monitoring of wild populations and threat mitigation, as well as appropriate legislation, are suggested as long-term measures. By adopting an inclusive wildlife conservation approach in Pakistan, amphibians could be inte
This article updates the understanding of two extirpation-driving infectious diseases, Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans, and Ranavirus. Experimental studies and dynamic, multifactorial population modeling have outlined the epidemiology and future population impacts of B dendrobatidis, B salamandrivorans, and Ranavirus. New genomic findings on divergent fungal and viral pathogens can help optimize control and disease management strategies. Although there have been major advances in knowledge of amphibian pathogens, controlled studies are needed to guide population recovery to elucidate and evaluate transmission routes for several pathogens, examine environmental control, and validate new diagnostic tools to confirm the presence of disease.
Conference Paper
This thesis investigates evolutionary patterns of variation in endemic amphibians from the Seychelles archipelago. Focal groups include the treefrog (Tachycnemis seychellensis), and a radiation of caecilians in three genera (Grandisonia, Hypogeophis and Praslinia), and attempts to place these into a phylogenetic context. The introduction (Chapter 1) discusses the importance of islands in the study of evolution and examines patterns of intraspecific variation that have been reported in other Seychelles organisms. Chapter 2 provides the first intraspecific molecular study of the monotypic Seychelles treefrog Tachycnemis, implementing a species tree approach in order to investigate its relationship with its closest living relatives (Heterixalus) from Madagascar and test whether its ancestor colonised the Seychelles via overseas dispersal. Chapters 3 and 4 explore variation in the six species of Seychelles caecilian, all of which overlap in range on at least one island. To assess within- and among-island intraspecific variation in these subterranean amphibians, Chapter 3 uses genetic data from both mitochondrial and nuclear markers, while Chapter 4 uses morphometric and meristic data. Differing patterns of geographic structure was observed among the caecilian species. The final two data chapters analyse species-level relationships among the Seychelles caecilians. Chapter 5 utilises Next Generation Sequencing to obtain mitogenomic data, and multiple approaches to infer phylogeny, and the effectiveness of alternative methods are evaluated. Chapter 6 attempts to resolve relationships of the island caecilians using 11 nuclear loci and multiple methods of phylogenetic inference. Chapter 7 discusses how the thesis has increased knowledge of the study taxa and of the evolution of amphibians on islands, particularly the Seychelles.
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Ronald A. Nussbaum and Sheng-Hai Wu (2007) Morphological assessments and phylogenetic relationships of the Seychellean frogs of the family Sooglossidae (Amphibia: Anura). Zoological Studies 46(3): 322-335. The frog family Sooglossidae is endemic to the Seychelles Is. in the Indian Ocean, and consists of 2 genera and 4 species, the monotypic Nesomantis and Sooglossus (3 species). Many previous studies have suggested that Sooglossus sechellensis is more similar to Nesomantis thomasseti than to its congener, S. gardineri. Based on an extensive dataset of 188 morphological characters, we concluded that Nesomantis and S. sechellensis form a monophyletic group with the exclusion of S. gardineri (and S. pipilodryas). We therefore have established a new genus, Sechellophryne, to accommodate the latter 2 species. http://zoolstud.sinica.edu. tw/Journals/46.3/322.pdf.
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The emerging infectious disease chytridiomycosis is driven by the spread of amphibian chytrid fungus (Batrachochytrium dendrobatidis, Bd), a highly virulent pathogen threatening global amphibian biodiversity. Although pandemic in distribution, previous intensive field surveys have failed to detect Bd in Madagascar, a biodiversity hotspot home to hundreds of endemic amphibian species. Due to the presence of Bd in nearby continental Africa and the ecological crisis that can be expected following establishment in Madagascar, enhanced surveillance is imperative. I sampled 565 amphibians commercially exported from Madagascar for the presence of Bd upon importation to the USA, both to assist early detection efforts and demonstrate the conservation potential of wildlife trade disease surveillance. Bd was detected in three animals via quantitative PCR: a single Heterixalus alboguttatus, Heterixalus betsileo, and Scaphiophryne spinosa. This is the first time Bd has been confirmed in amphibians from Madagascar and presents an urgent call to action. Our early identification of pathogen presence prior to widespread infection provides the necessary tools and encouragement to catalyze a swift, targeted response to isolate and eradicate Bd from Madagascar. If implemented before establishment occurs, an otherwise likely catastrophic decline in amphibian biodiversity may be prevented.
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The hyperoliid frog Tachycnemis seychellensis, the only species of its genus, is endemic to the four largest granitic islands of the Seychelles archipelago and is reliant on freshwater bodies for reproduction. Its presence in the Seychelles is thought to be the product of a transoceanic dispersal, diverging from the genus Heterixalus, its closest living relative (currently endemic to Madagascar), between approximately 10-35Ma. A previous study documented substantial intraspecific morphological variation among island populations and also among populations within the largest island (Mahé). To assess intraspecific genetic variation and to infer the closest living relative(s) of T. seychellensis, DNA sequence data were generated for three mitochondrial and four nuclear markers. These data support a sister-group relationship between T. seychellensis and Heterixalus, with the divergence between the two occurring between approximately 11-19Ma based on cytb p-distances. Low levels of genetic variation were found among major mitochondrial haplotype clades of T. seychellensis (maximum 0.7% p-distance concatenated mtDNA), and samples from each of the islands (except La Digue) comprised multiple mitochondrial haplotype clades. Two nuclear genes (rag1 and tyr) showed no variation, and the other two (rho, pomc) lacked any notable geographic structuring, counter to patterns observed within presumably more vagile Seychelles taxa such as lizards. The low levels of genetic variation and phylogeographic structure support an interpretation that there is a single but morphologically highly variable species of Seychelles treefrog. The contrasting genetic and morphological intraspecific variation may be attributable to relatively recent admixture during low sea-level stands, ecophenotypic plasticity, local adaptation to different environmental conditions, and/or current and previously small population sizes. Low genetic diversity but substantial morphological variation is unusual within anurans.
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Batrachochytrium dendrobatidis (Bd) is commonly termed the 'amphibian chytrid fungus' but thus far has been documented to be a pathogen of only batrachian amphibians (anurans and caudatans). It is not proven to infect the limbless, generally poorly known, and mostly soil-dwelling caecilians (Gymnophiona). We conducted the largest qPCR survey of Bd in caecilians to date, for more than 200 field-swabbed specimens from five countries in Africa and South America, representing nearly 20 species, 12 genera, and 8 families. Positive results were recovered for 58 specimens from Tanzania and Cameroon (4 families, 6 genera, 6+ species). Quantities of Bd were not exceptionally high, with genomic equivalent (GE) values of 0.052-17.339. In addition, we report the first evidence of lethal chytridiomycosis in caecilians. Mortality in captive (wild-caught, commercial pet trade) Geotrypetes seraphini was associated with GE scores similar to those we detected for field-swabbed, wild animals.
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The rapid worldwide emergence of the amphibian pathogen () is having a profound negative impact on biodiversity. However, global research efforts are fragmented and an overarching synthesis of global infection data is lacking. Here, we provide results from a community tool for the compilation of worldwide presence and report on the analyses of data collated over a four-year period. Using this online database, we analysed: 1) spatial and taxonomic patterns of infection, including amphibian families that appear over- and under-infected; 2) relationships between occurrence and declining amphibian species, including associations among occurrence, species richness, and enigmatic population declines; and 3) patterns of environmental correlates with , including climate metrics for all species combined and three families (Hylidae, Bufonidae, Ranidae) separately, at both a global scale and regional (U.S.A.) scale. These associations provide new insights for downscaled hypothesis testing. The pathogen has been detected in 52 of 82 countries in which sampling was reported, and it has been detected in 516 of 1240 (42%) amphibian species. We show that detected infections are related to amphibian biodiversity and locations experiencing rapid enigmatic declines, supporting the hypothesis that greater complexity of amphibian communities increases the likelihood of emergence of infection and transmission of . Using a global model including all sampled species, the odds of detection decreased with increasing temperature range at a site. Further consideration of temperature range, rather than maximum or minimum temperatures, may provide new insights into -host ecology. Whereas caution is necessary when interpreting such a broad global dataset, the use of our pathogen database is helping to inform studies of the epidemiology of , as well as enabling regional, national, and international prioritization of conservation efforts. We provide recommendations for adaptive management to enhance the database utility and relevance.
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Amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) has been hypothesised to be an indigenous parasite of African amphibians. In Cameroon, however, previous surveys in one region (in the northwest) failed to detect this pathogen, despite the earliest African Bd having been recorded from a frog in eastern Cameroon, plus one recent record in the far southeast. To reconcile these contrasting results, we present survey data from 12 localities across 6 regions of Cameroon from anurans (n = 1052) and caecilians (n = 85) of ca. 108 species. Bd was detected in 124 amphibian hosts at 7 localities, including Mt. Oku, Mt. Cameroon, Mt. Manengouba and lowland localities in the centre and west of the country. None of the hosts were observed dead or dying. Infected amphibian hosts were not detected in other localities in the south and eastern rainforest belt. Infection occurred in both anurans and caecilians, making this the first reported case of infection in the latter order (Gymnophiona) of amphibians. There was no significant difference between prevalence and infection intensity in frogs and caecilians. We highlight the importance of taking into account the inhibition of diagnostic qPCR in studies on Bd, based on all Bd-positive hosts being undetected when screened without bovine serum albumin in the qPCR mix. The status of Bd as an indigenous, cosmopolitan amphibian parasite in Africa, including Cameroon, is supported by this work. Isolating and sequencing strains of Bd from Cameroon should now be a priority. Longitudinal host population monitoring will be required to determine the effects, if any, of the infection on amphibians in Cameroon.
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Amidst a worldwide decline in amphibian populations, those species endemic to islands remain an important focus for conservation efforts. The Sooglossidae are a family of frog species endemic to the Seychelles islands that are believed to have evolved in isolation for approximately 75 million years. Formerly thought to inhabit just two Seychelles islands (Mahé and Silhouette), a third population was discovered on Praslin in 2009. Phy-logenetic analysis based on 438 bp of mitochondrial 16S rRNA suggests that the Praslin population is most closely related to Sooglossus sechellensis from Silhouette, and identifies these as two separate clades which together sit distinct from the population on Mahé. An average of 4.06% uncorrected pairwise sequence divergence between the Praslin and Silhouette populations suggests substantial evolutionary divergence rather than recent introduction. Discriminant function analysis also revealed differences in morphology in frogs from Praslin and Mahé. DNA sequences of two Praslin specimens group more closely with the Mahé population, indicating some shared haplo-types that suggest recent secondary contact. Tests for a genetic signature of recent population expansion on either island were not significant. Our results suggest substantial evolutionary divergence between the three populations of S. sechellensis, most likely following isolation due to changes in sea level in the Indian Ocean. Whilst further genetic sampling and ecological studies are needed, our initial phylogenetic analyses suggest that the sooglossid population on Praslin should be managed as an evolu-tionarily significant unit to retain the uniqueness of its genetic diversity and its evolutionary trajectory within this ancient family of amphibians.
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Most of the available data on declining populations of amphibians pertain to frogs and, to a lesser extent, salamanders. In keeping with their generally less understood biology, the population trends and conservation status of caecilian amphibians (Gymnophiona) are also much less known. We reviewed reports of threats to and declines of populations of caecilians. Despite a lack of field-study details (e.g., localities, dates, and sampling methods) and quantitative data, there are several recent reports of threats to and declines and extinctions of caecilians. A range of causal explanations (habitat loss, pollution, chytridiomycosis, and scientific collecting) for these perceived declines have been proposed but little or no associated evidence has been given. Although caecilians are often considered rare and thought to require pristine habitat, published, quantitative data demonstrate that at least some species can occur in high abundance in disturbed, synanthropic environments. Few estimates of caecilian population parameters have been made and very few field methods have been tested, so the assumed rarity of any taxa remains inadequately demonstrated. Distribution and taxonomic data are also inadequate. Because they are generally poorly known and often cryptic, caecilians can be overlooked in standard faunal surveys, meaning that lack of opportunistic collection over several years might not represent evidence of decline. The conservation status of most species must be considered data deficient. More precise assessments will require a substantial increase in all areas of caecilian research, especially those involving new fieldwork. Future reports of caecilian conservation biology need to be explicit and more quantitative.