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Widespread presence and high prevalence of Batrachochytrium dendrobatidis in Gabon

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Gregory Jongsma at New Brunswick Museum
Gregory Jongsma
Abraham Bamba Kaya at National Center for Scientific and Technological Research
Abraham Bamba Kaya
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Herpetological Review 47(2), 2016
AMPHIBIAN AND REPTILE DISEASES 227
Herpetological Review, 2016, 47(2), 227–230.
© 2016 by Society for the Study of Amphibians and Reptiles
Widespread Presence and High Prevalence of
Batrachochytrium dendrobatidis in Gabon
Despite its small size, Gabon is a biodiversity hotspot with
198 mammal species, 680 bird species, 138 reptile species, 184
fish species, and 97 amphibian species (Lee et al. 2006; Pauwels
and Vande weghe 2008). Emerging infectious diseases and habi-
tat degradation pose the most immediate threats to amphibian
diversity in Gabon. Batrachochytrium dendrobatidis (Bd) and
B. salamandrivorans (Bsal) are the causative agents of the am-
phibian disease chytridiomycosis which has been implicated in
worldwide population decline and extinction (Berger et al. 1998;
Lips et al. 2006; Wake and Vredenburg 2008; Martel et al. 2013).
Across sub-Saharan Africa, Bd has been widely reported (Con-
radie et al. 2016). Despite extensive sampling, Bd has not been
reported from West Africa (west of Nigeria; Penner et al. 2013).
In Gabon, there have been four independent surveys for Bd with
varied results. Bell et al. (2011) reported high prevalence of Bd
from three sites in northern Gabon. Three subsequent studies
at other sites across Gabon did not find Bd (Daversa et al. 2011;
Gratwicke et al. 2011; Zimkus and Larson 2013). Here we present
results from the most extensive survey for Bd in Gabon to date,
based on the number of individuals, diversity of species, and
geographic area sampled.
Gabon is a small equatorial country (267,667 km2) that is
dominated by continuous tropical moist forest (80% total land
GREGORY F. M. JONGSMA*
New Brunswick Museum, 277 Douglas Avenue,Saint John, NB,
Canada E2K 1E5
ABRAHAM BAMBA KAYA
JEAN-AIMÉ YOGA
JEAN-DANIEL MBEGA
JEAN-HERVÉ MVE BEH
Institut de Recherches Agronomiques et Forestières, Libreville, Gabon
ELIE TOBI
Center for Conservation and Sustainability Smithsonian
Conservation Biology Institute, Gamba, Gabon
ANDREA M. EMRICH
141 Wentworth Ave., Saint John, NB, Canada E2L 2S7
GRAHAM P. DIXON-MacCALLUM
Department of Biology, University of Victoria, P.O. Box 3020,
STN CSC, Victoria, BC, Canada V8W 3N5
DREW R. DAVIS
JACOB L. KERBY
Department of Biology, University of South Dakota, 414 E. Clark St.,
Vermillion, South Dakota 57069, USA
DAVID C. BLACKBURN
Florida Museum of Natural History, University of Florida, Gainesville,
Florida 32611, USA
*Corresponding author; e-mail: Gregor.Jongsma@gmail.com
Fig. 1. Map of Gabon showing Batrachochytrium dendrobatidis (Bd) sampling locations for this study. Pie-charts are scaled by the total num-
ber of individuals swabbed at each site. Numbers refer to sites described in Table 1.
Herpetological Review 47(2), 2016
228 AMPHIBIAN AND REPTILE DISEASES
cover; Lee et al. 2006). The dominant hydrological feature is the
Ogooué River basin. There are four seasons: a long rainy season
from January to May, a long cold dry season from June to Sep-
tember, a short rainy season from October to December, and a
short dry season from December to January. The average annual
temperature is 26°C (Lee et al. 2006).
We visited seven sites in three provinces: Moyen-Ogooué;
Ogooué-Lolo; and Haut-Ogooué. We hand-caught individu-
als and stored them in separate plastic bags. The next morning,
we swabbed live amphibians following protocols described by
Hyatt et al. (2007) using sterile medical swabs (MW113; Medi-
cal Wire and Equipment Co., Wiltshire, UK). Our swab samples
were stored in 1.5-mL snap-cap tubes with 95% EtOH and kept
as cool as possible in the field. A subset of individuals was eutha-
nized, tissued, stored in formalin and deposited at the California
Academy of Sciences (CAS, San Francisco, California, USA) or in
Gabon’s national collection (curated by the Smithsonian Institu-
tion’s Gabon Biodiversity Program in Gamba, Gabon).
Samples were extracted following the PrepMan Ultra extrac-
tion protocol (Hyatt et al. 2007) and diluted 1:10 with TE buffer
to reduce potential inhibition during quantitative polymerase
chain reaction (qPCR) analysis. Following fast qPCR methods de-
scribed by Kerby et al. (2013), we used 10μL reactions (3μL DNA
extract plus 7μL cocktail) to determine if samples were Bd-pos-
itive or Bd-negative. Additionally, each plate contained a nega-
tive control (nanopure water) and four synthetic DNA (sDNA)
standards. Samples were run on a StepOnePlus qPCR machine
and the number of Bd gene copies was quantified with StepOne
software v2.3 (Applied Biosystems). All samples were run in trip-
licate and considered Bd-positive if: 1) amplification occurred in
at least two of the three wells; and 2) the quantity was above 1.0.
Samples were rerun if there were two wells with quantities near
1.0, or if independent values for a sample differed by an order
of magnitude. All qPCR analyses were conducted at the Disease
Testing Center at the University of South Dakota.
We swabbed a total of 463 frogs, representing 46 species from
18 genera in 10 families, across 7 sites (Table 1; Fig. 1). The overall
prevalence across all sites was 18.6% with 60% of the sampled
species testing Bd-positive, and Bd-positive results from all seven
sites (across three provinces) (Table 2). Our results support Bell
et al.’s (2011) findings that Bd is present in Gabon with high prev-
alence. In addition, we demonstrate that Bd is widespread across
much of the country. Our raw data, including field and catalogue
numbers are available at amphibiandisease.org: <https://n2t.
net/ark:/21547/ANU2>.
There does not appear to be a strong association between
the presence of Bd and specific taxa tested. The genus Amni-
rana (Ranidae) had both the highest prevalence and highest Bd
gene copy number of any genus or family. One individual Am-
nirana albolabris (field# ORB-010) had a gene copy count of
43,422 (Fig. 2). Phrynobatrachidae was the only family that did
not test positive for Bd during this study. However, because Sker-
ratt et al. (2008) reported that >59 animals should be sampled
to detect Bd when prevalence is low and our sampling includes
only 23 individuals of Phrynobatrachus, this family may still be
susceptible to Bd in Gabon. Bell et al. (2011) did report positive
cases for three Phrynobatrachus auritus from northern Gabon.
The Hyperoliidae, the most species-rich group sampled, had a
prevalence of 18.7%. There were 6 species that made up 51% of
the total sampling and each of these species had over 25 total
individuals sampled (Table 2). Scotobleps gabonicus (19.2% prev-
alence), Conraua crassipes (19.2%), Hyperolius cinnamomeoven-
tris (19.2%), H. ocellatus (16.7%) all had Bd prevalence close to
the total prevalence. Sclerophrys regularis (10.7%) had the lowest
prevalence of any highly sampled species, and Amnirana albola-
bris (38.7%) had the highest prevalence.
There was a lower prevalence of Bd at forest-savanna sites (N
= 2 sites; mean = 9.4%, ± 1.1% SD) versus strictly forested sites
(N = 5 sites; mean = 23.6%, ± 6.70% SD; t = 2.84, P = 0.036, d.f.
= 5). Because there is no significant difference in the species
composition of these sites based on a Sørensen similarity test,
this suggests that either environmental variables are driving
this difference in Bd prevalence, or there are transmission fac-
tors at play. For example, savanna-forest mosaic sites in Gabon
are known to exhibit greater seasonal temperature fluctuations
than surrounding forest sites (Bonnefille 2011). This temperature
taBLe 1. Summary information on sampling locations for Batrachochytrium dendrobatidis in Gabon. Site numbers correspond with numbers
in Fig. 1.
# Site Province Lat/Long Elevation (m) Dates Habitat
1 Mitone Moyen-Ogooué 00.6410°S, 10.2176°E 43 3–7 April 2015 Forest
2 Carivenville Moyen-Ogooué 00.1770°S, 10.7795°E 44 8–13 April 2015 Forest
3 Junkville Moyen-Ogooué 00.0621°S, 11.1587°E 86 15–18 April 2015 Forest-Savanna mosaic
4 Ogooué Cinq Ogooué-Lolo 00.8105°S, 12.7995°E 419 4–5 May 2015 Forest
5 Madoukou Ogooué-Lolo 00.8683°S, 12.6724°E 246 6–7 May 2015 Forest
6 Mboua Haut-Ogooué 02.1532°S, 13.6398°E 504 26 April–1 May 2015 Forest
7 Doumaye Haut-Ogooué 02.2402°S, 13.5812°E 526 21–25 April 2015 Forest-Savanna mosaic
Fig. 2. An apparently healthy adult male Amnirana albolabris (field#
ORB-010) infected with Batrachochytrium dendrobatidis (43,422
zoospores equivalent).
PHOTO BY A. EMRICH
Herpetological Review 47(2), 2016
AMPHIBIAN AND REPTILE DISEASES 229
taBLe 2. Amphibians sampled for Batrachochytrium dendrobatidis (Bd) in Gabon. Numbers indicate no. Bd-positive individuals/total no.
sampled by species and site. Sites are numbered (1–7) in correspondence to Table 1.
Family/Species Site
1 2 3 4 5 6 7 Total
Arthroleptidae
Arthroleptis poecilonotus - - - - 2/3 - 0/2 2/5
Arthroleptis sylvaticus 0/1 1/1 - - - - - 1/2
Arthroleptis variabilis 0/2 1/3 1/2 - - - 0/1 2/8
Astylosternus batesi - - - - - 0/1 0/6 0/7
Cardioglossa gracilis 0/1 - - - - - 0/3 0/4
Cardioglossa leucomystax 0/1 - - - - - - 0/1
Leptodactylodon sp. 0/2 - - - - - - 0/2
Leptopelis aubryi 0/2 0/5 1/2 - - - - 1/9
Leptopelis calcaratus - - - - - - 0/3 0/3
Leptopelis millsoni 0/2 1/4 0/2 - - - - 1/8
Leptopelis notatus 0/2 - - - - - - 0/1
Leptopelis ocellatus - - 0/1 - 2/2 - 0/2 2/4
Leptopelis rufus - - 1/1 - - - - 1/1
Leptopelis sp. 0/1 - - - - - - 0/1
Scotobleps gabonicus 4/21 - 1/5 2/11 2/5 0/5 1/5 10/52
Bufonidae
Sclerophrys gracilipes 1/2 0/1 - - - - 0/1 1/4
Sclerophrys regularis 1/15 1/4 0/5 - 1/5 - - 3/28
Sclerophrys superciliaris - - - - - - 0/1 0/1
Conrauidae
Conraua crassipes 2/3 - 3/20 - 0/3 - - 5/26
Dicroglossidae
Hoplobatrachus occipitalis - - - - - - 0/2 0/2
Hyperoliidae
Afrixalus dorsalis 0/2 - 1/10 - - - - 1/12
Afrixalus paradorsalis 0/1 0/5 - - - - - 0/6
Cryptothylax greshoffii - - - - - 1/3 - 1/3
Hyperolius adspersus - - - - - - 1/10 1/10
Hyperolius cinnamomeoventris 4/12 3/5 1/22 - - 1/8 - 9/47
Hyperolius concolor - - - - - - 2/12 2/12
Hyperolius guttulatus 5/6 - - - - - - 5/6
Hyperolius ocellatus 2/6 2/3 0/9 - 1/5 3/12 1/19 9/54
Hyperolius pardalis - - - - 1/5 - 1/8 2/13
Hyperolius phantasticus - - - - - - 0/3 0/3
Hyperolius platyceps 0/1 - - - - - - 0/1
Hyperolius sp. 1 - - - - - - 0/1 0/1
Hyperolius sp. 2 - 0/1 - - - - - 0/1
Hyperolius tuberculatus 0/3 5/15 0/5 - - - - 5/23
Phlyctimantis leonardi - 0/6 1/4 - - - 0/1 1/11
Phrynobatrachidae
Phrynobatrachus africanus 0/6 - - - 0/1 - 0/5 0/12
Phrynobatrachus auritus 0/1 0/1 - - 0/1 - - 0/3
Phrynobatrachus sp. - - - - - - 0/5 0/5
Pipidae
Xenopus cf. mellotropicalis 1/3 0/2 - - - - - 1/5
Xenopus amieti sp. group - 2/4 0/2 - - - - 2/6
Ptychadenidae
Ptychadena perreti - 0/2 0/1 - 1/4 - - 1/7
Ranidae
Amnirana albolabris 9/12 1/1 0/7 - - 0/4 2/7 12/31
Amnirana amnicola 0/1 - - - - - 0/5 0/6
Amnirana lepus - - - - - - 1/3 1/3
Rhacophoridae
Chiromantis rufescens 0/1 2/8 0/1 - 1/1 - - 3/11
Total: 29/109 19/71 10/99 2/11 11/35 5/33 9/105 85/463
%: 26.6 26.8 10.1 18.2 31.4 15.2 8.6 18.6
Herpetological Review 47(2), 2016
230 AMPHIBIAN AND REPTILE DISEASES
fluctuation might be expected to influence the prevalence of Bd
(Berger et al. 2004; Gaertner et al. 2012; Kinney et al. 2011; Kriger
and Hero 2006; Whitfield et al. 2012). However, given our small
sample sizes, many more forest and forest-savanna sites should
be sampled to test this possible correlation.
All frogs that we encountered in the field appeared healthy.
However, the high prevalence and widespread nature of Bd in
Gabon demands future work to determine its impact on amphib-
ians. A better understanding is needed of: 1) the historical pres-
ence of Bd in Gabon; 2) the contemporary genomic make-up of
Bd in the country; and 3) which species, if any, exhibit symptoms
of chytridiomycosis. Each of these will help to establish the ex-
tent to which Bd poses a threat to amphibians in tropical forests
in Gabon and Central Africa.
Acknowledgments.—We thank the Centre National de la Recher-
che Scientifique et Technologique (CENAREST; permit #AR008/15/
CSAR) for scientific permits and the Direction de la Faune et de la
Chasse for export permits. For logistical support, we thank The Na-
ture Conservancy (Marie-Claire Paiz) and Smithsonian Institution
(Lisa Korte). We thank our lovely hosts in Libreville, Glen Ratel and
Marie Coupé. For assistance in the field, we thank Freye Pavel for get-
ting us safely to our destination and keeping us fed once there. We are
indebted to the chiefs of each village (Mitoné, Carivenville, Junkville,
Ogooué Cinq, Madoukou, Doumaye, and Mboa) for their hospital-
ity, warmth, and knowledge. And finally, we thank our local guides
from each village that never led us astray during our nocturnal quests
for frogs. This project was supported by the NSF grant (#1202609) to
DCB and funding by Shell Gabon and the Smithsonian Conservation
Biology Institute for ET.
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... By contrast, amphibians colonized the oceanic islands in the Gulf of Guinea via sweepstakes overseas dispersal (Bell et al., 2015;Measey et al., 2007), and thus, the islands host lower overall amphibian diversity: four frog and one caecilian species on São Tomé and three frog species on Príncipe, all of which are endemic (Bell, 2016;Jones, 1994;Uyeda, Drewes, & Zimkus, 2007). Recent surveys in Nigeria (Imasuen et al., 2011;Reeder, Cheng, Vredenburg, & Blackburn, 2011), Cameroon (Balaz, Kopecky, & Gvoždík, 2012;Doherty-Bone et al., 2013;Hirschfeld et al., 2016), Gabon (Bell, Gata Garcia, Stuart, & Zamudio, 2011;Jongsma et al., 2016), and São Tomé Island (Hydeman, Bell, Drewes, & Zamudio, 2013) report Bd across a range of host species, elevations, and habitats in these assemblages. Thus, Lower Guinean forests present a unique opportunity to characterize Bd prevalence among related amphibian assemblages that naturally differ in species richness. ...
... This pattern may be due in part to taxonomic bias in our sampling of fully aquatic species, which was primarily represented by the genera Silurana and Xenopus that typically exhibit low prevalence and infection intensity in natural populations (Kielgast et al., 2010;Soto-Azat et al., 2010;Weldon et al., 2004). Riparian species with aquatic larvae (aquatic index = 2.5) have high infection intensities in field surveys in Kenya (Kielgast et al., 2010) and Gabon (Jongsma et al., 2016) indicating that species with these life histories are highly suscep- 2010), studies in Central American, South American, and Australian amphibian communities demonstrate that species with aquatic larvae are more likely to decline (Carvalho, Becker, & Toledo, 2017;Hero & Morrison, 2004;Lips et al., 2008), and those that are tolerant may spread Bd between aquatic and terrestrial habitats (Brem & Lips, 2008 ...
... pled is similar to that of surveys in recent and historical Bd-positive communities in continental Africa and is consistent with a long-term and widespread distribution of Bd in African amphibiansJongsma et al., 2016;Kielgast et al., 2010;Soto- Azat et al., 2010;Weldon, Du Preez, Hyatt, Muller, & Speare, 2004). ...
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... Their boundaries were given by Vande weghe et al. (2016: Figures 771 and 779) and are detailed in the first chapter of this book (pages 24 and 25). The main bibliographic references for the area are those of Peters (1876), Boulenger (1900Boulenger ( , 1906, Jongsma et al. (2016), Lötters et al. (2001), Loveridge (1936), Mocquard (1897aMocquard ( b, 1902, and Pauwels (2016). Some older works simply reference "Ogooué" (without further precision) as a locality for various species, but since it is unclear what portion of Ogooué is being referenced, they have not been included here. ...
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Full-text available
  • Dec 2021
I provide a list of the amphibian species found in the Lower Ogooué region, its delta and wetlands, western Gabon, Equatorial Africa, from Ndjolé and Lambaréné to Port-Gentil and Omboué. The list includes 44 species (Dermophiidae, Arthroleptidae, Bufonidae, Conrauidae, Hyperoliidae, Phrynobatrachidae, Pipidae, Ptychadenidae, Pyxicephalidae, Ranidae and Rhacophoridae). Among them are the endemics Hymenochirus feae and Phrynobatrachus ogoensis. Citation: Pauwels, O.S.G. 2021. Chapter 7. Amphibians. Pp. 250-255 in: Vande weghe, J.P. & Stévart, T. (eds). The Ogooué Delta. Missouri Botanical Garden Press, Saint Louis: 328 pp.
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... Dans la zone d'étude, la batrachologie est restée le parent pauvre de l'herpétologie. Cependant, grâce notamment aux collectes de l'exploratrice anglaise Mary de Boulenger (1900de Boulenger ( , 1906, Jongsma et al. (2016), Lötters et al. (2001), Loveridge (1936), Mocquard (1897ab, 1902) et Pauwels (2016. Certaines références anciennes citent 'Ogooué' -sans plus de détails -comme localité pour diverses espèces mais, faute de savoir à quelle portion de l'Ogooué elles se rapportent, nous ne les avons pas intégrées. ...
... La principale menace pour la conservation des amphibiens du bas Ogooué est sans doute la dégradation de la forêt, qui affecte les espèces strictement sylvicoles. Jongsma et al. (2016) (Pauwels, 2007) ; il n'est pas du tout exclu que cette espèce remonte jusque dans la zone du delta marin de l'Ogooué. Tout porte à croire que la diversité globale des amphibiens du bas Ogooué doit inclure au moins 60 espèces. ...
Les amphibiens. In: Le Delta de l'Ogooué
Chapter
Full-text available
  • Nov 2017
We provide a commented list of the amphibian species found in the Lower Ogooué region, western Gabon, Equatorial Africa, from Ndjolé and Lambaréné to Port-Gentil and Omboué. The list includes 43 species (Dermophiidae, Arthroleptidae, Bufonidae, Conrauidae, Hyperoliidae, Phrynobatrachidae, Pipidae, Ptychadenidae, Pyxicephalidae, Ranidae and Rhacophoridae). Among them are the endemics Hymenochirus feae and Phrynobatrachus ogoensis. Citation: Pauwels, O.S.G. 2017. Chapitre 8. Les amphibiens. Pp. 250-255 in: Vande weghe, J.P. & Stévart, T. Le delta de l’Ogooué. Agence Nationale des Parcs Nationaux, Libreville: 324 pp.
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... Several studies have reported a small number of Bd-infected amphibians collected in the early 20 th century in Africa (Weldon et al., 2004;Soto-Azat et al., 2010). More recent African amphibian studies have revealed much higher Bd infection prevalence that may be associated with host declines (Goldberg et al., 2007;Kielgast et al., 2010;Bell et al., 2011;Gower et al., 2012;Tarrant et al., 2013;Seimon et al., 2015;Hirschfeld et al., 2016;Jongsma et al., 2016). Although these Bd-host infection data vary in spatial and temporal resolution, they suggest a pattern of Bd emergence that may represent a threat to African amphibian species, warranting a comprehensive analysis encompassing the broadest possible temporal and geographic scales. ...
Continent-wide recent emergence of a global pathogen in African amphibians
Article
Full-text available
  • Mar 2023
Introduction: Emerging infectious diseases are increasingly recognized as a global threat to wildlife. Pandemics in amphibians, caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), have resulted in biodiversity loss at a global scale. Genomic data suggest a complex evolutionary history of Bd lineages that vary in pathogenicity. Africa harbors a significant proportion of global amphibian biodiversity, and multiple Bd lineages are known to occur there; yet, despite the decline of many host species, there are currently no described Bd-epizootics. Here, we describe the historical and recent biogeographical spread of Bd and assess its risk to amphibians across the continent of Africa. Methods: We provide a 165-year view of host-pathogen interactions by (i) employing a Bd assay to test 4,623 specimens (collected 1908-2013); (ii) compiling 12,297 published Bd records (collected 1852-2017); (iii) comparing the frequency of Bd-infected amphibians through time by both country and region; (iv) genotyping Bd lineages; (v) histologically identifying evidence of chytridiomycosis, and (vi) using a habitat suitability model to assess future Bd risk. Results: We found a pattern of Bd emergence beginning largely at the turn of the century. From 1852–1999, we found low Bd prevalence (3.2% overall) and limited geographic spread, but after 2000 we documented a sharp increase in prevalence (18.7% overall), wider geographic spread, and multiple Bd lineages that may be responsible for emergence in different regions. We found that Bd risk to amphibians was highest in much of eastern, central, and western Africa. Discussion: Our study documents a largely overlooked yet significant increase in a fungal pathogen that could pose a threat to amphibians across an entire continent. We emphasize the need to bridge historical and contemporary datasets to better describe and predict host-pathogen dynamics over larger temporal scales.
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... Central Africa.-Batrachochytrium dendrobatidis is widespread in Central Africa, with recent field surveys of frogs and caecilians reporting the pathogen in Gabon (Bell et al. 2011;Jongsma et al. 2016;Hydeman et al. 2017;this study, Supplemental Material S3), Cameroon (Doherty-Bone et al. 2013;Gower et al. 2013b;Hirschfeld et al. 2016;Miller et al. 2018;this study, Supplemental Material S3), the oceanic islands of São Tomé and Príncipe (Hydeman et al. 2013(Hydeman et al. , 2017, the land-bridge island Bioko (Hydeman et al. 2017;P. McLaughlin, personal Tomé and Bioko Island specimens (Supplemental Material S1). ...
Chytrid Pathogen (Batrachochytrium dendrobatidis) in African Amphibians: A Continental Analysis of Occurrences and Modeling of Its Potential Distribution
Article
Full-text available
  • Jun 2020
The fungal pathogen Batrachochytrium dendrobatidis (Bd) is implicated in global declines of amphibian populations and has been documented in African specimens originally collected as far back as the 1930s. Numerous recent surveys focusing on regional pathogen prevalence have greatly increased the number of known occurrences of Bd in African species, but few studies have focused on continental distribution patterns. We analyzed all known positive occurrences of Bd in African amphibians to date, including newly reported data from Cameroon, the Democratic Republic of the Congo, Gabon, Namibia, and the Republic of the Congo. Records from both Namibia and the Republic of the Congo reported herein represent first positive occurrences for these countries. With this most comprehensive sampling of the African continent to date we identified patterns of Bd-positive occurrences associated with (1) location (i.e., biogeographic region, country), (2) taxonomy, (3) life history, and (4) threat of extinction. We used fine-grained (30 arc seconds) environmental niche models (ENMs) to predict the continental distribution of Bd and identify hotspots for the pathogen, including areas not previously modeled to have high suitability for the fungus, and areas of high amphibian biodiversity from which Bd has not yet been documented. Our ENMs predicted that the environmentally suitable range of Bd encompasses vast areas of high amphibian biodiversity, including the Congo Basin and the Albertine Rift. Although our ENMs indicated that West Africa is environmentally suitable for Bd, the fungus has not been reported west of the Dahomey Gap. Likewise, the ENMs also identified regions across the Congo Basin and coastal Angola that are environmentally suitable for the pathogen but from which Bd has not yet been reported, underscoring a need for Bd surveys in these regions. Although amphibian declines in Africa have not been directly attributed to chytridiomycosis, Bd has been detected in over one fifth of the most-threatened African amphibians. Given the presence of the hypervirulent Bd global panzootic lineage (BdGPL) in Africa, we believe that the threat of Bd as a novel pathogen may be underestimated and that focused research is urgently needed to identify which species are susceptible to Bd-driven declines.
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... In contrast to the island endemics, the biogeographical history of H. olivaceus is more nuanced; however, its range appears to have remained allopatric with its closest relative on the continent, Hyperolius cinnamomeoventris Bocage, 1866, since the Late Miocene (Bell et al., 2017). The anuran assemblages of the lowland forests of Gabon and Republic of the Congo are also much more diverse than those of São Tomé and Príncipe; consequently, in some parts of its range, H. olivaceus shares breeding sites with upwards of six Hyperolius species and these diverse breeding assemblages can include representatives from up to ten anuran families (Pauwels & Rödel, 2007;Jongsma et al., 2016). ...
Evolution of advertisement calls in an island radiation of African reed frogs
Article
Full-text available
  • Jan 2018
Differences in mating signals among incipient species are an important mechanism driving reproductive isolation and speciation. Here, we investigate male advertisement call divergence across a radiation of reed frogs from the Gulf of Guinea archipelago and the most closely related species on the African continent (Hyperolius olivaceus). The two species endemic to the island of São Tomé (Hyperolius molleri and Hyperolius thomensis) differ in body size, coloration and breeding ecology, yet they hybridize where their habitats overlap. A third species, Hyperolius drewesi, is sister to H. molleri and endemic to Príncipe Island. We found significant differences in average dominant frequency and average number of pulses per call among the four species. The strong relationship between body size and dominant frequency irrespective of geographical history, breeding habitat or acoustic environment suggests that differences in this component of the mating signal may be a by-product of adaptive changes in body size among the four species. Hybrid males are intermediate in size between H. molleri and H. thomensis and produce calls at intermediate dominant frequencies. Future efforts to characterize courtship behaviour and breeding habitat preference in allopatric and sympatric populations will provide additional insights as to the potential for reinforcement in this system. © 2017 The Linnean Society of London, Biological Journal of the Linnean Society.
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Tracking Batrachochytrium dendrobatidis Infection Across the Globe
Article
Full-text available
  • Sep 2020
Infection records of Batrachochytrium dendrobatidis (Bd), a pathogen that has devastated amphibian populations worldwide, have rapidly increased since the pathogen’s discovery. Dealing with so many records makes it difficult to (a) know where, when and in which species infections have been detected, (b) understand how widespread and pervasive Bd is and (c) prioritize study and management areas. We conducted a systematic review of papers and compiled a database with Bd infection records. Our dataset covers 71 amphibian families and 119 countries. The data revealed how widespread and adaptable Bd is, being able to infect over 50% of all tested amphibian species, with over 1000 confirmed host species and being present in 86 countries. The distribution of infected species is uneven among and within countries. Areas where the distributions of many infected species overlap are readily visible; these are regions where Bd likely develops well. Conversely, areas where the distributions of species that tested negative overlap, such as the Atlantic Coast in the USA, suggest the presence of Bd refuges. Finally, we report how the number of tested and infected species has changed through time, and provide a list of oldest detection records per country.
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Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America
Article
Full-text available
  • Jul 1998
  • P NATL ACAD SCI USA
Epidermal changes caused by a chytridiomycete fungus (Chytridiomycota; Chytridiales) were found in sick and dead adult anurans collected from montane rain forests in Queensland (Australia) and Panama during mass mortality events associated with significant population declines. We also have found this new disease associated with morbidity and mortality in wild and captive anurans from additional locations in Australia and Central America. This is the first report of parasitism of a vertebrate by a member of the phylum Chytridiomycota. Experimental data support the conclusion that cutaneous chytridiomycosis is a fatal disease of anurans, and we hypothesize that it is the proximate cause of these recent amphibian declines.
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Seasonal Pattern of Batrachochytrium dendrobatidis Infection and Mortality in Lithobates areolatus: Affirmation of Vredenburg's “10,000 Zoospore Rule”
Article
Full-text available
To fully comprehend chytridiomycosis, the amphibian disease caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd), it is essential to understand how Bd affects amphibians throughout their remarkable range of life histories. Crawfish Frogs (Lithobates areolatus) are a typical North American pond-breeding species that forms explosive spring breeding aggregations in seasonal and semipermanent wetlands. But unlike most species, when not breeding Crawfish Frogs usually live singly--in nearly total isolation from conspecifics--and obligately in burrows dug by crayfish. Crayfish burrows penetrate the water table, and therefore offer Crawfish Frogs a second, permanent aquatic habitat when not breeding. Over the course of two years we sampled for the presence of Bd in Crawfish Frog adults. Sampling was conducted seasonally, as animals moved from post-winter emergence through breeding migrations, then back into upland burrow habitats. During our study, 53% of Crawfish Frog breeding adults tested positive for Bd in at least one sample; 27% entered breeding wetlands Bd positive; 46% exited wetlands Bd positive. Five emigrating Crawfish Frogs (12%) developed chytridiomycosis and died. In contrast, all 25 adult frogs sampled while occupying upland crayfish burrows during the summer tested Bd negative. One percent of postmetamorphic juveniles sampled were Bd positive. Zoospore equivalents/swab ranged from 0.8 to 24,436; five out of eight frogs with zoospore equivalents near or >10,000 are known to have died. In summary, Bd infection rates in Crawfish Frog populations ratchet up from near zero during the summer to over 25% following overwintering; rates then nearly double again during and just after breeding--when mortality occurs--before the infection wanes during the summer. Bd-negative postmetamorphic juveniles may not be exposed again to this pathogen until they take up residence in crayfish burrows, or until their first breeding, some years later.
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Assessment of the amphibians of Batéké Plateau National Park, Gabon, including results of chytrid pathogen tests
Article
  • Oct 2013
We report on the amphibians of five sites within the Batéké Plateau National Park in southeastern Gabon. During our survey we recorded 11 genera and at least 18 frog species, including four new country records (Kassina maculosa, Phrynobatrachus ruthbeateae, Ptychadena uzungwensis and Xenopus pygmaeus). Most of the recorded frogs were typical savanna or farmbush species; some preferred forested habitats and were collected in gallery forest or small forest patches within the savanna. Larvae were also collected, and the identifications of tadpoles and select adults were confirmed using mtDNA. The presence of Batrachochytrium dendrobatidis (Bd), the fungus that causes the amphibian disease chytridiomycosis, was tested using Taqman PCR, including community-level sampling. All samples were Bd-negative. This amphibian survey represents the first within Batéké Plateau National Park and is valuable because the fauna of this expansive, true savanna habitat differs from other protected areas that have isolated savanna pockets. The results of this survey also assist in predicting which species may exist in the contiguous savanna habitat in the Republic of the Congo. © 2013 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Mannheim, Germany.
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Utilization of fast qPCR techniques to detect the amphibian chytrid fungus: A cheaper and more efficient alternative method
Article
A pathogen of great significance to amphibian populations is the chytrid fungus, Batrachochytrium dendrobatidis ( Bd ). It has been demonstrated as causing recent epizootics in wild populations and is also widely found in captive animals. It is listed as a notifiable disease within the pet, bait and food trade because of its risk of introduction into wild populations. Due to this status, there has been much emphasis on reliably identifying and quantifying the pathogens in amphibians. Quantitative polymerase chain reaction ( qPCR ) has served as the recent standard for identifying this pathogen's presence. Newer technologies have greatly improved these reactions enabling researchers to use smaller volumes and run the reactions in less time. These ‘fast’ qPCR chemistries are gaining popularity because the reduced volumes required to run the reactions can save funding resources and reduce the time to data acquisition. In this study, we compare the results from differing reaction methodologies using the same DNA extracts from pathogens collected from wild sampled amphibians. In addition to comparing the standard methodology and fast methodology for both pathogens, we also conducted a reduced volume methodology using the standard TaqMan chemistry for Bd . Estimated pathogen loads from 114 field swab samples were compared among methodologies. We found that for Bd , all three methodologies produced similar results for prevalence (presence/absence) estimates. In terms of estimating pathogen loads in the samples, both the standard and fast methodologies produced comparable estimates but the reduced volume methodology exhibited significantly lower values. Therefore, it appears that the fast methodology is adequate for use with Bd , and potentially several other wildlife pathogens, in estimating both prevalence and quantity, but the reduced volume methodology is inadequate and not recommended for use in quantifying samples.
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Temporal Variation in Infection Prevalence by the Amphibian Chytrid Fungus in Three Species of Frogs at La Selva, Costa Rica
Article
  • Nov 2012
The emerging infectious disease chytridiomycosis, caused by the amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd), is implicated in widespread population declines, extirpations, and extinctions of amphibians throughout the world. In the Neotropics, most amphibian declines have occurred in cool mid- to high-elevation sites (> 400 m asl), and it is hypothesized that high temperatures limit the growth of Bd in lowland tropical sites, despite few data available on the distribution of Bd in lowland forests. Here, we report the results of a 12-mo pathogen surveillance program for three common species of frogs at a warm lowland site in northeastern Costa Rica. We combine standard non-invasive skin swabbing techniques with a quantitative polymerase chain reaction assay to analyze the infection prevalence and Bd load across a 1-yr period. Our data indicate an overall Bd infection rate of 6.1 percent, but prevalence varies from < 5 percent in warmer months to a peak of 34.7 percent in the coolest months of the year. Despite very little seasonal variation in temperature (< 4°C), our data indicate strong seasonal variation in the prevalence of Bd, with highest prevalence of infection in months with coolest air temperatures. While it has been suggested that Bd is primarily a riparian fungus, we find no difference in prevalence of infection among our species despite considerable differences in affiliation of these species with water. Our study provides further evidence that infection by Bd is regulated by temperature and shows that warm temperatures in lowland forests may restrict, but not prevent, infection by Bd.
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Rainforest responses to past climatic changes in tropical Africa
Chapter
  • Jul 2011
In Africa the lowland rainforest occurs under significantly drier conditions than in other continents, within an average precipitation of 1,600 to 2,000mmyr_1, although higher rainfall is observed around the Atlantic coast of Cameroon, Gabon, and in the Central Zaire Basin. Seasonal distribution of precipitation is far from being uniform (White, 1983). Variations in the duration of the dry season follow the distance from the equator in both hemispheres and also along a west-to-east gradient. The Biafran Gulf is the only region where the minimum monthly precipitation value always exceeds the 50-mm threshold for the driest month, therefore experiencing no dry season.
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