Recent and future threats to the Endangered Cuban toad Peltophryne longinasus: potential additive impacts of climate change and habitat loss
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Recent and future threats to the Endangered Cuban
toad Peltophryne longinasus: potential additive
impacts of climate change and habitat loss
M A R L O N E . C O B O S and R O B E R T O A L O N S O B O S C H
Abstract Habitat loss and climate change are major threats Introduction
to amphibian species worldwide. We combined niche mod-
elling under various climatic scenarios with analysis of habi-
tat loss and the appropriateness of Cuban protected areas to T he causes of global amphibian decline are diverse but
the majority are anthropogenic (Carey & Alexander,
; Beebee & Griffiths, , Brum et al., ). Given
identify major risk zones for the Endangered Cuban toad
Peltophryne longinasus. Four subspecies with disjunct distri- the complexity of ecological processes the causes of species
butions associated with mountain forests are recognized. decline are typically studied and managed in isolation but
Our results suggest that the western subspecies, P. longina- multiple threats, such as climate change and habitat loss
sus longinasus and P. longinasus cajalbanensis, are at risk (Mantyka-Pringle et al., ), can affect species and ecosys-
from global warming, habitat degradation and potential tems concurrently (Rohr et al., ). Furthermore, changes
additive effects. Peltophryne longinasus dunni, in central in climate could modify dispersion and infection character-
Cuba, has the lowest threat level related to climate change istics of the chytrid fungus, Batrachochytrium dendrobatidis
and habitat loss but could become increasingly threatened (Pounds et al., ; Rödder et al., ). Although a global
by the presence of the infectious disease chytridiomycosis. estimate of areas at risk from the occurrence of these threats
The eastern subspecies, P. longinasus ramsdeni, faces mod- has been developed (Hof et al., ), variation in local con-
erate impacts of climate change and habitat loss; however, ditions and species necessitates greater precision in identify-
low opportunity of migration to new areas and population ing priority areas for conservation and management
decline justify a high threatened status for this subspecies. (Mantyka-Pringle et al., ).
Our results predict minor temperature increases and pre- Peltophryne longinasus is a bufonid endemic to Cuba and
cipitation decreases in the future. Nevertheless, at the bio- is a uniquely polytypic species of the genus in the Caribbean
logical level these changes could generate variations in basin (Henderson & Powell, ). There are four recog-
species physiology, vocal behaviour and prey availability, nized subspecies, with disjunct distributions in mountain-
and could probably increase the risk of predation. In Cuba ous areas (Díaz & Cádiz, ). Peltophryne longinasus
protected areas have contributed to avoiding excessive forest longinasus and P. longinasus cajalbanensis inhabit the
loss but the potential impact of climate change was not con- Alturas de Pizarras in the south of Pinar del Río province
sidered in their original design. Our findings confirm that all and Cajálbana upland, respectively. Peltophryne longinasus
subspecies of P. longinasus are threatened but management dunni is distributed in the Guamuhaya mountain range in
measures should be tailored according to the various pre- the centre of the island and is threatened by the chytrid fun-
dicted impacts. gus (Díaz et al., ). Although only one sick and dying in-
dividual has been found, in October , the presence of
Keywords Amphibian decline, Bufonidae, climate change, the disease in this population was confirmed. Since that
forest cover loss, habitat suitability models, Peltophryne, date no more cases have been reported. Peltophryne longina-
protected areas sus ramsdeni is known only from the Guaso upland in
To view supplementary material for this article, please visit Guantanamo province, in eastern Cuba, but it has not
https://doi.org/./S been found since (Valdes de la Osa & Ruiz García,
).
This diurnal species occupies a variety of vegetation
types, mainly woodlands (pinewoods and mesic broadleaf
forests) and secondary vegetation, at altitudes of – m
(Valdes de la Osa & Ruiz García, ; Díaz & Cádiz, ),
MARLON E. COBOS Departamento de Biología Animal y Humana, Facultad de and reproduces in mountain streams (Valdés de la Osa &
Biología, Universidad de La Habana, Havana, Cuba Ruiz García, ). Peltophryne longinasus is categorized
ROBERTO ALONSO BOSCH (Corresponding author) Museo de Historia Natural as Endangered on the IUCN Red List because its Area of
Felipe Poey, Facultad de Biología, Universidad de La Habana, street 25 #455. Occupancy is , km, its distribution is severely frag-
Vedado, Plaza de la Revolución, Havana, 10400, Cuba
E-mail ralonso@fbio.uh.cu mented and the extent of its upland forest habitat is declin-
Received January . Revision requested March .
ing (Hedges & Díaz, ). Its threat status, ecological and
Accepted June . First published online October . morphological features and disjunct distribution make it an
Oryx, 2018, 52(1), 116–125 © 2016 Fauna & Flora International doi:10.1017/S0030605316000612
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https://doi.org/10.1017/S0030605316000612Threats to an Endangered Cuban toad 117
ideal species to evaluate the additive threats of climate predict rather than infer, as it may lead to a ‘less wrong’ re-
change and habitat loss. sult than when operating with only a single, irrelevant pre-
Habitat fragmentation and climate change have been re- dictor arbitrarily.
cognized as two principal threats to biodiversity in Cuba To evaluate the effect of climate change by and
(CITMA, ) but their possible additive impacts on am- on the potential distribution of P. longinasus we used two
phibian diversity have received little consideration. Here Representative Concentration Pathway (RCP) scenarios
we () evaluate the potential impact of predicted climate (. and .) of the general circulation model of the
change scenarios for and on habitats suitable Beijing Climate Center. These scenarios describe two cli-
for P. longinasus, () estimate habitat loss (measured as for- matic configurations based on different concentrations of
est lost) during – in the areas suitable for this spe- greenhouse gases (Moss et al., ). The RCP . scenario
cies, () identify suitable areas for P. longinasus affected by assumes that concentrations of greenhouse gases will in-
additive stressors (habitat loss, disease and climate change), crease in the future, reaching a maximum by , and
and () assess the representation of suitable areas for the the RCP . assumes that concentrations will continue to in-
species (for , and scenarios) and the threats crease even up to (IPCC, ). Future bioclimatic vari-
it faces within Cuban protected areas. ables were obtained from the WorldClim database.
Study area Habitat suitability models and projections
The study area (the Cuban archipelago) was divided into We used distribution records (Alonso, ) and the afore-
four physical–geographical regions (Fig. ), simplifying the mentioned bioclimatic variables as presence and environmen-
regionalization of Mateo & Acevedo (). Regions inhab- tal data. To prevent possible errors duplicate records were
ited by P. longinasus (western, central and eastern Cuba) removed. With the remaining samples and selected vari-
comprise the more densely forested areas of the archipelago ables we created habitat suitability models in MaxEnt ..k
(Mateo & Acevedo, ). (Phillips et al., ), using its default configuration and
replicates for bootstrapping. To obtain presence–absence
data from the mean logistic model we used the th percentile
Methods threshold (Peterson et al., ), which should not be sensitive
We used ecological niche models to identify areas suitable to extreme environmental values (Radosavljevic & Anderson,
for P. longinasus and predict future changes in these areas. ). We consider it to be appropriate because a small sample
We evaluated recent forest loss using the results of Hansen size could increase the weight of extreme records in the model
et al. (), to identify patterns and levels of habitat degrad- (Araujo & Peterson, ) and consequently the estimated
ation. We also assessed climate change in areas where suit- area of suitable habitat for the species. To evaluate model per-
able conditions will decline in the future, using the formance we used the area under the receiver operating char-
bioclimatic variables of the WorldClim database (Hijmans acteristic curve (AUC; Phillips et al., ), difference of AUC
et al., ). With the resultant information we identified (AUCDIFF; Warren & Seifert, ) and % training omission
suitable areas potentially affected by additive threats from rate (Peterson et al., ).
climate change, habitat loss and chytridiomycosis. We also Habitat suitability models created for the year were
evaluated the representation of the suitable areas and threats projected to and using MaxEnt. Results of each
in protected areas. projection were compared with the initial model, consider-
ing the change in suitable areas (presence areas). For the
future projections we identified areas where suitable
Climatic data climatic conditions for P. longinasus could be lost, suitable
areas consistent with compared scenarios, and potentially
The modelling dataset included bioclimatic variables new suitable areas. The conserved range is the area of over-
(Table ) obtained from the WorldClim database version lap between each of the projected ranges and the range.
. (S data group) at a resolution of arc-seconds Where a loss of suitable habitat was predicted we used
(Hijmans et al., ). We selected these variables on the as- QGIS . (QGIS Development Team, ) to calculate dif-
sumption that they are most strongly related to the natural ferences in variables between and projected values for
history of the studied species. We did not check for collin- and (using all pixel values) for the two scenarios
earity among our selected variables. We followed the criteria (RCP . and .).
of Braunisch et al. (), who stated that the inclusion of We used data from the Global Forest Change database
several correlated, potentially relevant variables in the (Hansen et al., ) to evaluate loss of forest cover, which
same model may be preferable when the intention is to we considered to be an indicator of fragmentation and
Oryx, 2018, 52(1), 116–125 © 2016 Fauna & Flora International doi:10.1017/S0030605316000612
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https://doi.org/10.1017/S0030605316000612118 M. E. Cobos and R. Alonso Bosch
FIG. 1 Distribution of records of
Peltophryne longinasus in Cuba,
which is divided into physical–
geographical regions, based on
Mateo & Acevedo ().
habitat loss. We estimated annual forest loss (resolution variables were annual mean temperature (BIO), maximum
m) in the quadrants that include the Cuban archipelago, and temperature of warmest month (BIO), and temperature
extracted the areas of interest in the layer composition of seasonality (BIO). The logistic output for revealed a
forest cover loss (–), using the suitable areas iden- high probability of presence of P. longinasus in mountain
tified by habitat suitability modelling. In QGIS we calculated zones in all three regions inhabited by the species. In the
the surface area of deteriorated areas by year for each region initial binary results (Fig. a,b) derived from reclassification
and for all areas of suitable habitat, attempting to discrim- of the mean logistic model (probability of presence
inate between vegetation types according to the vegetation . . = mean th percentile threshold) we observed a
map of Estrada et al. (). fragmented pattern with suitable areas in all regions except
To detect areas affected by additive stressors we created a Camagüey-Maniabón.
map of known distribution records of P. longinasus subspe-
cies, projected climate change, trends in temperature and Potential modifications of suitable areas Suitable areas for
precipitation, habitat loss (density of forest cover loss), P. longinasus (Fig. a,b) in represented .% of all
and reported presence of Batrachochytrium dendrobatidis. Cuban territory, with substantial decreases predicted by
Potential impacts of climate change were categorized as future projections (Fig. c,d). By losses of .%
High, Medium or Low (based on projected habitat loss), (RCP .) and .% (RCP .) of suitable habitat are
and were compared among regions. We also identified expected, and the western region will be most affected,
areas predicted to become more suitable for P. longinasus with reductions of . and .% in the respective
as a result of climate change. scenarios (Table ). Projections for are similar, with
We assessed the importance of protected areas for decreases of .% (RCP .) and .% (RCP .).
conservation of P. longinasus and its habitats using the However, in the Sierra Maestra mountain range (eastern
map of Cuba’s national system of protected areas (CNAP, region) the area of suitable habitat is predicted to increase
). We calculated the area of current and future suitable significantly in scenario RCP . (Fig. c,d), but P.
habitat for the species within protected areas. We also longinasus has never been found there. In scenario RCP
estimated the area of suitable habitat that will potentially ., even though suitable habitat is predicted to diminish
be lost under future climate scenarios. Finally, we com- by , an improvement relative to is expected by
pared the areas of forest loss in suitable habitat areas , especially in the central and western regions. The
inside and outside protected areas in each region of the conserved range (suitable areas consistent with compared
study area. scenarios) will be proportionally higher in the central and
eastern regions in comparison with the western region
(Table ). Suitable areas are expected to be found at higher
Results altitudes in the future (relative to ). By mean
altitudinal increases of . m (RCP .) and . m
Habitat suitability models Habitat suitability models (RCP .) are projected. By the altitude of suitable
yielded high mean values of AUC (. ± SD .), low habitat could increase by m (RCP .) and . m
AUCDIFF (. ± SD .) and a mean % training (RCP .) relative to .
omission rate of . ± SD .. The AUC results indicate
good predictive power, and AUCDIFF and the % training
omission rate indicate that overfitting could be avoided Expected climate change in areas predicted to become
in these models. The major contributing bioclimatic unsuitable for P. longinasus In areas where suitable
Oryx, 2018, 52(1), 116–125 © 2016 Fauna & Flora International doi:10.1017/S0030605316000612
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https://doi.org/10.1017/S0030605316000612Threats to an Endangered Cuban toad 119
TABLE 1 The potential distribution range of the Cuban toad Peltophryne longinasus in western, central and eastern Cuba in , and pro-
jected values for and under two climate change scenarios (RCP . and RCP .). The conserved range is the area of overlap
between each of the projected ranges with the range.
Western Central Eastern Total
Potential Conserved Potential Conserved Potential Conserved Potential Conserved
distribution range distribution range distribution range distribution range
Scenario* Year range (km2) (km2) range (km2) (km2) range (km2) (km2) range (km2) (km2)
2000 1,012.02 1,015.89 1,270.27 3,298.18
RCP 2.6 2050 156.97 156.71 578.13 577.84 1,053.33 880.46 1,788.43 1,615.01
2070 257.84 257.22 611.20 610.96 951.55 814.54 1,820.59 1,682.72
RCP 8.5 2050 66.24 66.24 459.27 459.27 964.43 706.43 1,489.93 1,231.93
2070 0.00 0.00 336.35 336.35 595.63 381.54 931.98 717.89
*RCP . assumes that concentrations of greenhouse gases will increase in the future, reaching a maximum by , and RCP . assumes that concentra-
tions will continue to increase even up to .
conditions for the species will be lost, values of all change and chytridiomycosis, and habitat loss and
temperature variables (except mean diurnal range, chytridiomycosis. The first combination was detected
BIO) are expected to increase in both climate scenarios throughout the species’ range (Fig. ) but the level of
(Table ). Significant increases of temperature and impact varied among regions, and therefore the subspecies
decreases of three of six precipitation variables by will be affected differentially. The greatest impacts of climate
are predicted (RCP .). Precipitation in the driest change with habitat loss were observed in the western
month and driest quarter (BIO and BIO ) is region, intermediate impacts were detected in the eastern
predicted to decrease significantly by (RCP .). region, and the lowest impact was observed in the central
Similarly, a reduction in precipitation seasonality region. The second and third types of additive threats
(coefficient of variation) by is expected (RCP .). appear to occur only in the central region, as a result of
We also recorded increments in precipitation in the the reported presence of chytridiomycosis in this zone and
wettest month (BIO) and precipitation seasonality the absence of connectivity with other regions.
(BIO) by (RCP .) and (RCP .) (Table ).
Importance of protected areas The current percentage of
Habitat loss in areas that were suitable in 2000 Total initial suitable habitat area for P. longinasus (Fig. b) within
forest cover () in areas suitable for P. longinasus protected areas is .% but this is expected to decrease
comprised ,. km, with the majority of the under all future scenarios (Supplementary Table S). The
vegetation distributed in the eastern region (Fig. ). The eastern region had the highest initial and future
most significant forest loss during – took place representations of suitable habitat within protected areas
in the western region (Figs & ), where major losses in all evaluated scenarios. We predict that by (RCP
were recorded in . Significant reductions in forest .) suitable areas within protected areas will be reduced
cover occurred in the central and eastern regions in by .%, and by .%. In the RCP . scenario
and , respectively (Fig. b). Peltophryne longinasus we predict reductions of . and .% by and
has been recorded in at least eight distinct vegetation , respectively. Nevertheless, the majority of the
formations (Supplementary Table S). These formations reduction in suitable areas in the future (Fig. c,d) will
occupy .% of the species’ total suitable area. We occur outside protected areas, with only .–.% of
identified that secondary vegetation, Pinus caribaea and P. losses occurring within protected areas (Supplementary
tropicalis pinewoods, were most affected in the western Table S). We detected considerable differences in forest
region, submontane mesophyllous evergreen forests and loss during – inside and outside protected areas
secondary vegetation in the central, and submontane (Supplementary Table S), with only .% of the forest
mesophyllous evergreen forests in the eastern region. loss occurring inside protected areas.
Areas affected by additive stressors Predicted future trends Discussion
include an increase in temperature and a decrease in
precipitation throughout the entire area of suitable habitat Our results indicate that, in the future, areas of habitat suit-
for P. longinasus. Three types of additive threats have also able for P. longinasus will be reduced. Similar studies have
been identified: climate change and habitat loss, climate reported spatial changes in suitable areas (decrease and
Oryx, 2018, 52(1), 116–125 © 2016 Fauna & Flora International doi:10.1017/S0030605316000612
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120
M. E. Cobos and R. Alonso Bosch
TABLE 2 Mean values (min., max.) of bioclimatic variables for the initial () distribution range of P. longinasus, and differences between projected values for and under two
climate scenarios (RCP . and RCP .) and values.
Variables 2000 2050–2000, RCP 2.6 2050–2000, RCP 8.5 2070–2000, RCP 2.6 2070–2000, RCP 8.5
BIO1 (annual mean temperature) 22.26 (16.71, 24.93) 0.99 (0.90, 1.10) 1.51 (1.40, 1.60) 0.99 (0.90, 1.10) 2.21 (2.10, 2.30)
BIO2 (mean diurnal range) 9.48 (7.78, 10.11) −0.02 (−0.10, 0.09) −0.03 (−0.10, 0.00) −0.02 (−0.10, 0.10) −0.03 (−0.10, 0.00)
BIO4 (temperature seasonality) 18.72 (14.88, 21.67) 0.53 (−0.18, 0.98) 0.50 (−0.38, 1.20) 0.09 (−0.23, 0.39) 0.96 (−0.64, 2.15)
BIO5 (maximum temperature of 29.39 (23.01, 32.23) 1.06 (0.90, 1.10) 1.54 (1.40, 1.60) 1.00 (0.80, 1.10) 2.23 (2.10, 2.40)
warmest month)
BIO6 (minimum temperature of 14.48 (10.05, 16.77) 0.97 (0.90, 1.00) 1.38 (1.30, 1.46) 0.91 (0.80, 1.00) 1.98 (1.70, 2.30)
coldest month)
Oryx, 2018, 52(1), 116–125 © 2016 Fauna & Flora International doi:10.1017/S0030605316000612
BIO8 (mean temperature of wet- 24.11 (18.19, 27.23) 1.01 (0.07, 1.70) 1.27 (0.60, 2.05) 1.08 (0.20, 1.60) 2.17 (1.30, 2.47)
test quarter)
BIO10 (mean temperature of 24.37 (18.59, 27.23) 1.08 (0.91, 1.20) 1.55 (1.40, 1.69) 0.97 (0.90, 1.09) 2.27 (2.10, 2.40)
warmest quarter)
BIO12 (annual precipitation) 1,621.43 (1,350.64, 2,083.59) −132.79 (−192.81, 7.29) −88.56 (−156.67, −46.13) −150.67 (−210.64, −107.86) −310.49 (−449.32, −168.52)
BIO13 (precipitation of wettest 245.25 (203.77, 316.36) −17.45 (−72.60, 15.67) 16.37 (−26.12, 58.78) 11.73 (−63.22, 72.69) −27.04 (−69.41, 37.26)
month)
BIO14 (precipitation of driest 45.21 (16.61, 78.58) −0.41 (−20.93, 7.00) −1.37 (−15.27, 7.12) −11.19 (−24.59, 1.76) −2.40 (−16.47, 6.00)
month)
BIO15 (precipitation seasonality) 52.61 (35.87, 67.49) −3.88 (−9.00, 0.15) 1.53 (−4.28, 8.97) 5.27 (−0.84, 16.89) −3.13 (−11.00, 6.08)
BIO16 (precipitation of wettest 630.59 (486.02, 795.28) −43.83 (−114.71, 18.36) −14.46 (−86.73, 50.78) −30.64 (−113.50, 12.30) −135.21 (−246.68, −20.99)
quarter)
BIO17 (precipitation of driest 171.30 (90.36, 260.33) −1.20 (−13.36, 25.77) −10.59 (−44.64, 11.05) −23.90 (−47.43, 4.04) −11.88 (−40.58, 3.83)
quarter)Threats to an Endangered Cuban toad 121
FIG. 2 Result of habitat suitability
models for Peltophryne longinasus:
Potential distribution range of
Peltophryne longinasus for
(a & b). Predicted change in
species potential distribution
ranges by (c) and (d) .
displacement of ranges) for many herpetofaunal species in needed to investigate the capability of each subspecies to
Europe and South America (Araújo et al., ; Zank et al., move to higher altitudes, and to obtain a better understand-
; Courtois et al., ). Suitable areas for P. longinasus ing of the impact of climate change on this species sensu
will be found at high altitudes; this concurs with the general lato.
evidence of changes in species’ distributions in response to Projected decreases in precipitation could also affect the
global warming (Walther et al., ; Raxworthy et al., typical reproductive phenology of P. longinasus. Such de-
). However, the archipelagic nature of Cuba, the lack creases could reduce the spatial and temporal accessibility
of connectivity among ranges and the presence of barriers of sites for calling and breeding, and also affect nesting suc-
will impede future movement of the subspecies of P. longi- cess and optimum larval development. In the microhabitat
nasus to places with suitable conditions at other latitudes of P. longinasus longinasus air temperature is –°C (Díaz
(i.e. the Sierra Maestra mountain range). Displacement to & Cádiz, ) and forecasted changes in bioclimatic vari-
adjacent locations at higher altitudes within the same region ables include temperature changes. At the biological level
is therefore the most likely alternative. these could generate variations in physiology, vocal behav-
Not all subspecies have the same opportunity and ability iour and the availability and accessibility of prey, and could
to move to higher altitudes in the same region. Our results potentially increase the risk of predation (Blaustein et al.,
suggest that P. longinasus dunni has more opportunities for ; Li et al., ).
displacement because suitable areas adjacent to its current Amphibian species with small ranges tend to have more
range will be less affected compared to other subspecies in habitat specificity, which makes them vulnerable to habitat
other regions. Further studies on movement patterns are alterations (Williams & Hero, ). The deterioration in
Oryx, 2018, 52(1), 116–125 © 2016 Fauna & Flora International doi:10.1017/S0030605316000612
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https://doi.org/10.1017/S0030605316000612122 M. E. Cobos and R. Alonso Bosch
FIG. 3 (a) Forest cover in the
potential distribution range of
Peltophryne longinasus in ,
and total forest loss during –
, in the western, central and
eastern regions of Cuba (Fig. ).
(b) Forest loss per year during
– in each region.
FIG. 4 Density of forest cover loss
during – in areas of
initially suitable habitat for
Peltophryne longinasus in the
western, central and eastern
regions of Cuba.
FIG. 5 Additive stressors of
climate change and habitat loss on
the distribution range of
Peltophryne longinasus in Cuba.
forest cover is resulting in loss and fragmentation of habitats Other studies have suggested potential synergistic effects
of P. longinasus in some of its most frequented vegetation of climate change and other stressors when they co-occur
types (e.g. Pinus forests). Although we have taken into ac- (Pyke, ; Brook et al., ; Mantyka-Pringle et al.,
count a period of only years prior to our future projec- ). We have identified areas where additive effects of glo-
tions, there was no apparent decrease in deforestation bal warming and habitat loss could be occurring, alerting us
within this period, and deforestation is likely to continue, es- to potential synergies between these threats (Fig. ).
pecially outside protected areas. In fragmented landscapes Peltophryne longinasus longinasus and P. longinasus ca-
dispersion is often insufficient to maintain population via- jalbanensis will face major risks from the additive effects of
bility (Cushman, ), and processes such as habitat split global warming and habitat degradation. Peltophryne long-
are common in fragmented landscapes with complex topog- inasus dunni (which may represent a distinctive form and is
raphy (Becker et al., ). Forest cover loss is therefore a probably a ninth species of Cuban Peltophryne; Alonso et al.,
significant concern, as it has been shown that habitat split, ) is the subspecies with the lowest level of risk linked to
loss and fragmentation affect principally species with aquat- these threats; however, it may also be threatened by the pres-
ic larvae (Fonseca et al., ). ence of the chytrid fungus. This pathogen disperses rapidly
Oryx, 2018, 52(1), 116–125 © 2016 Fauna & Flora International doi:10.1017/S0030605316000612
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https://doi.org/10.1017/S0030605316000612Threats to an Endangered Cuban toad 123
(Lips et al., ) and its spread may be facilitated by an- Acknowledgements
thropogenic activities (Weldon et al., ; Fisher &
Garner, ). Establishment and intensity of infection Many people helped RAB during the field expeditions to lo-
are highest in elevated places with lower temperatures and cate and verify the presence of the Cuban toad: Ariel
higher precipitation (Drew et al., ). Nevertheless, Rodríguez, L. Yusnaviel García, Arturo Hernández, Luis
there is evidence that warmer years favour the development Alvarez Lajonchere, and Rafael García-Morera. RAB thanks
of the fungus at high elevations (Pounds et al., ; Harvell the National Center of Cuban Protected Areas and the
et al., ). Peltophryne longinasus ramsdeni will suffer Center for Inspection and Environmental Control for sup-
intermediate effects in comparison with the other three sub- port and permission to access the study areas. Rafael
species. The almost non-existent possibility of migration to Marquez and Chrystal S. Mantyka-Pringle provided com-
new, potentially suitable areas and the absence of records of ments on the text. Boris Fabres and Sergio J. Pastrana helped
this subspecies since justify its highly threatened status. to improve the English. Prof. Tim Halliday offered valuable
However, it cannot yet be categorized as Extinct, given the suggestions and corrections to the language, and helped
few observations in the field and the lack of information on enhance the quality of the article. Two anonymous re-
its biology, population size and habitat use. Based on our viewers provided constructive criticism. MEC is grateful
precautionary criteria we therefore categorize this subspe- for the support received during his postgraduate studies
cies as Critically Endangered, Possibly Extinct (CR Aac; from the Secretaria Nacional de Educación Superior,
IUCN, ), until further surveys confirm, or not, that no Ciencia y Tecnología and the Instituto de Fomento del
individuals remain. Talento Humano.
Our results show that all subspecies of P. longinasus are
threatened; however, each one requires different research
and management priorities according to the identified im- Author contributions
pacts. Habitat protection and restoration efforts could be a
priority, especially in western areas where the major risks MEC and RAB conceived the study and wrote the article.
are potentially the additive effects of climate change and RAB conducted all fieldwork and compiled the original
habitat loss. Further efforts are required to clarify the exist- database of geographical localities. MEC analysed the data
ence, prevalence, dissemination and pathogenicity of the and performed the modelling.
chytrid fungus in relation to other natural and anthropogen-
ic stressors in the central region. Some ex situ conservation
initiatives began years ago with a preliminary captive
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V A L D É S D E L A O S A , A. & R U I Z G A R C Í A , F. () Consideraciones MA R L O N E. CO B O S ’ research interests are focused on the biogeog-
sistemáticas sobre Bufo longinasus (Anura: Bufonidae) y descripción raphy, ecology and conservation of tropical fauna, particularly amphi-
de una nueva subespecie. Poeyana, , –. bians. RO B E R T O AL O N S O BO S C H ’ s research interests are focused on
W A LT H E R , G.R., P O S T , E., C O N V E Y , P., M E N Z E L , A., P A R M E S A N , C., the natural history, behaviour, evolution and conservation of
B E E B E E , T.J.C. et al. () Ecological responses to recent climate Caribbean amphibians and reptiles, with special emphasis on the en-
change. Nature, , –. demic toads of Cuba.
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