Microhabitat Use and Spatial Distribution in Picado's Bromeliad Treefrog, Isthmohyla picadoi (Anura, Hylidae)
Abstract and Figures
Microhabitat use and spatial distribution in Picado's Bromeliad Treefrog, Isthmohyla picadoi (Anura, Hylidae). Isthmohyla picadoi is a Neotropical hylid frog found in upper humid montane forests of Costa Rica and Panama. The species is of particular interest because it continues to persist in an area in which the amphibian community has otherwise been decimated by the pathogenic fungus, Batrachochytrium dendrobatidis. Ground search, ladder climbing, and tree climbing techniques were used to locate 32 individuals; including adult males and females, juveniles, and metamorphosing frogs. The majority of frogs were found in bromeliads, although some individuals were found on plants of the Euphorbiaceae, Musaceae, and Heliconiaceae families. Most frogs were found in larger bromeliads (45 cm or wider). There was a positive correlation between SUL and bromeliad width within the population but not within maturity classes (adult males, adult females, all adults, non-metamorphosing juveniles), suggesting that juvenile and adult frogs differ in bromeliad usage. Ranges of SUL and body weight in this particular population are much greater than those reported in previous species accounts.
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... In these areas, the cumulative time individuals of a species spend in riparian habitats significantly increases the likelihood of decline [5,[9][10][11][12]. Therefore, even in these hotspots of chytridiomycosis-driven declines, a proportion of species are less affected [9,13,14], a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 especially those with arboreal, bromeliad-associated habits [15][16][17][18]. The reasons for these differential infection and disease dynamics of Bd have been suggested to be multifactorial and dependent on local environmental-, host-and pathogen-associated factors [13,[19][20][21][22][23][24]. ...
... Thirty-two bromeliads and twelve sampling locations derived from the main stream running through CNP were selected for sampling. Large bromeliads (circumference >45 cm) were sampled in order to allow sufficient water volumes (30 ml) to be withdrawn and due to the preference of bromeliad-associated amphibians for larger specimens [16]. For each bromeliad and stream site, GPS coordinates, canopy openness (improved Moosehorn design [35]), water pH (pH test kit, JBL GmbH & co, Neuhofen Germany), water temperature and ambient air temperature were recorded. ...
... Although the IUCN dataset used for these calculations also include non-peer reviewed literature and expert opinions, it does indicate a clear difference in the conservation status and susceptibility to Bd of bromeliad-and stream-associated amphibians in Central America. This agrees with previous studies suggesting that Central American amphibian species associated with bromeliads may be less affected in Bd outbreaks than riparian species in the same region [15][16][17][18]. Within Cusuco National Park (CNP), this same trend is observed: there are three declining riparian amphibian species in which chytridiomycosis is a suspected driver, while no negative population trends are reported for the bromeliad-associated species [18,25]. ...
The fungal pathogen Batrachochytrium dendrobatidis (Bd) drives declines and extinctions in amphibian communities. However, not all regions and species are equally affected. Here, we show that association with amphibian aquatic habitat types (bromeliad phytotelmata versus stream) across Central America results in the odds of being threatened by Bd being five times higher in stream microhabitats. This differential threat of Bd was supported in our study by a significantly lower prevalence of Bd in bromeliad-associated amphibian species compared to riparian species in Honduran cloud forests. Evidence that the bromeliad environment is less favorable for Bd transmission is exemplified by significantly less suitable physicochemical conditions and higher abundance of Bd-ingesting micro-eukaryotes present in bromeliad water. These factors may inhibit aquatic Bd zoospore survival and the development of an environmental reservoir of the pathogen. Bromeliad phytotelmata thus may act as environmental refuges from Bd, which contribute to protecting associated amphibian communities against chytridiomycosis-driven amphibian declines that threaten the nearby riparian communities.
... Picado's Bromeliad Treefrog, Isthmohyla picadoi (Dunn 1937), is an arboreal, bromeliad-dwelling species found in primary, secondary, and transitional humid montane forests of Costa Rica and Panama (Duellman 2001;Faivovich et al. 2005;Savage 2002;Solis et al. 2008). Stuckert et al. (2009) found that I. picadoi inhabits phytotelmata with source water temperatures that fall within the reproductive thermal range of Bd in laboratory settings as found by Piotrowski et al. (2004). The population of I. picadoi from the highlands of western Panama studied by Stuckert et al. (2009) persists despite catastrophic declines and extinctions of other amphibian species in the region due to Bd (Lips 1999). ...
... Stuckert et al. (2009) found that I. picadoi inhabits phytotelmata with source water temperatures that fall within the reproductive thermal range of Bd in laboratory settings as found by Piotrowski et al. (2004). The population of I. picadoi from the highlands of western Panama studied by Stuckert et al. (2009) persists despite catastrophic declines and extinctions of other amphibian species in the region due to Bd (Lips 1999). Although no data on the population exists prior to the arrival of Bd, the population currently appears to be stable based on the number of vocalizations heard throughout the study site over multiple years ranging from 2000 to 2008 (pers. ...
... obs.). Stuckert et al. (2009) suggested I. picadoi may be a potential vector of vertical stream-to-canopy Bd zoospore transfer as well as stream-to-terrestrial dispersal. However, their study did not present evidence of Bd infection in I. picadoi, nor any correlation between infection in I. picadoi and presence of Bd in phytotelmata. ...
The pathogenic fungus Batrachochytrium dendrobatidis (Bd) has been implicated as the cause of many global am-phibian declines (Berger et al. 1998; Bosch et al. 2001; Briggs et al. 2005; Longcore et al. 1999; Ron and Merino 2000; Skerratt et al. 2007). Central American amphibians have experienced substantial declines (Stuart et al. 2004, 2008) and Bd has been identified as the cause in a number of these (Crawford et al. 2010; Lips et al. 2006). A more thorough understanding of the natural history and ecology of Bd is still needed, and knowl-edge of the geographic distribution of this fungal pathogen is important for biological conservation (Adams et al. 2007; Young et al. 2001). Likewise, modes of Bd dispersal are poorly understood; amphibians and water sources are implicated as the primary vectors, but birds and soil are potentially im-portant vectors as well (Johnson and Speare 2005). Bd has also been implicated in historic die-offs in the highlands of western Panama (Lips 1999; pers. obs) and has been detected in environmental water gathered from both lotic and lentic sources (arboreal phytotelmata) in the region (Cossel and Lindquist 2009). Picado's Bromeliad Treefrog, Isthmohyla picadoi (Dunn 1937), is an arboreal, bromeliad-dwelling species found in primary, secondary, and transitional humid montane for-ests of Costa Rica and Panama (Duellman 2001; Faivovich et al. 2005; Savage 2002; Solis et al. 2008). Stuckert et al. (2009) found that I. picadoi inhabits phytotelmata with source wa-ter temperatures that fall within the reproductive thermal range of Bd in laboratory settings as found by Piotrowski et al. (2004). The population of I. picadoi from the highlands of western Panama studied by Stuckert et al. (2009) persists despite catastrophic declines and extinctions of other am-phibian species in the region due to Bd (Lips 1999). Although no data on the population exists prior to the arrival of Bd, the population currently appears to be stable based on the number of vocalizations heard throughout the study site over multiple years ranging from 2000 to 2008 (pers. obs.). Stuck-ert et al. (2009) suggested I. picadoi may be a potential vector of vertical stream-to-canopy Bd zoospore transfer as well as stream-to-terrestrial dispersal. However, their study did not present evidence of Bd infection in I. picadoi, nor any cor-relation between infection in I. picadoi and presence of Bd in phytotelmata. In this study, we set out to determine: 1) whether Bd is detectable in the population of I. picadoi at the study site described by Stuckert et al. (2009) and Cossel and Lindquist (2009); and if so, 2) the prevalence of infection; and 3) whether any connection exists between Bd infections in individual frogs and phytotelmic water sources. We studied a population of I. picadoi immediately north of Guadalupe Arriba, Chiriquí Province, in the Republic of Panama (8.869444°N, 82.566806°W) between 3 and 29 Janu-ary 2008 [same population as Stuckert et al. (2009)]. Study sites included primary, secondary, and transitional riparian humid forest, ranging in elevation from 1,950 to 2,300 m el-evation. Sites were located in a private forest preserve owned by Los Quetzales Lodge and Spa, and in a small forest tract in the Finca Dracula, owned by Andrés Maduro. Both proper-ties border the Parque Internacional La Amistad and Parque Nacional Volcán Barú. We located I. picadoi, via two techniques: 1) randomly searching bromeliads (leaf axils and phytotelmata) at both day and night; and 2) triangulating male nocturnal position immediately after vocalization. Epiphytic bromeliads and mosses were searched at heights ranging from 0 to 33.5 m AMPHIBIAN DISEASES AMPHIBIAN DISEASES
... [7,12,13,14]). Several bromeliad traits are associated with the presence of anurans, including humidity, water availability and phytotelmata size [15][16][17][18]. More generally, the high microhabitat stability of phytotelmata makes them potentially important refuges during adverse environmental conditions. ...
... More salamanders were found in bromeliads with larger phytotelmata and cooler water. This is broadly in concordance with previous studies that have reported that humidity, water availability, and phytotelm size have been reported to play a major role in anuran microhabitat selection [15][16][17][18]. Such correlations are potentially driven by the role of bromeliad phytotelmata as refuges from temperature extremes and low humidity [7,12,19]. ...
Bromeliad phytotelmata are frequently used by several Neotropical amphibian taxa, possibly due to their high humidity, microclimatic stability, and role as a refuge from predators. Indeed, the ability of phytotelmata to buffer against adverse environmental conditions may be instrumental in allowing some amphibian species to survive during periods of environmental change or to colonize sub-optimal habitats. Association between bromeliad traits and salamanders has not been studied at a fine scale, despite the intimate association of many salamander species with bromeliads. Here, we identify microhabitat characteristics of epiphytic bromeliads used by two species of the Bolitoglossa morio group (B. morio and B. pacaya) in forest disturbed by volcanic activity in Guatemala. Specifically, we measured multiple variables for bromeliads (height and position in tree, phytotelma water temperature and pH, canopy cover, phytotelma size, leaf size, and tree diameter at breast height), as well as salamander size. We employed a DNA barcoding approach to identify salamanders. We found that B. morio and B. pacaya occurred in microsympatry in bromeliads and that phytotelmata size and temperature of bromeliad microhabitat were the most important factors associated with the presence of salamanders. Moreover, phytotelmata with higher pH contained larger salamanders, suggesting that larger salamanders or aggregated individuals might modify pH. These results show that bromeliad selection is nonrandom with respect to microhabitat characteristics, and provide insight into the relationship between salamanders and this unique arboreal environment.
... Despite E. salvaje not being associated with 'traditional' sites for Bd transmission i.e. streams, pools and bromeliads, there is potential for Bd transmission into canopy environments through residue left on vegetation from other sympatric amphibian species that move between aquatic and terrestrial habitats (Kolby et al. 2015a), as well as potentially being transmitted by wind, waterfall spray and rainfall (Kolby et al. 2015b). Studies outside of Cnp have suggested that canopy-dwelling frogs may act as vectors for Bd (Stuckert et al. 2009;Lindquist et al. 2011), and that the damp arboreal refuges they inhabit (e.g. bromeliads) might serve as chytrid reservoirs (Cossel & Lindquist, 2009). ...
Cusuco National Park (CNP), a montane cloud forest in north-western Honduras, harbours what is thought to be among the last known populations of the Endangered Copán Fringe-limbed Tree Frog, Ecnomiohyla salvaje. This paper provides novel information that may inform the conservation status of this species whilst simultaneously building on its poorly known natural history. We add to the four total confirmed adult records from 1982-2014
by reporting an additional three adult individuals encountered between 2014 and 2018. Additionally, we provide the first descriptions of two late stage tadpoles (herein referred to as metamorphs), which adds to the information given on adults and earlier life stages in the species authority paper. We also correct and include formal photographs for the original known, but as yet ‘unvouchered’ E. salvaje observation in 2009 at CNP. We present morphometrics for most individuals encountered, as well as details of their natural habitat, defensive behaviour and ecology. Our observations of E. salvaje support
the hypothesis that this canopy adapted species may be dependent on tree holes within intact forest. Being a tree-hole breeding species, the simultaneous presence of adult E. salvaje in tree holes with late stage tadpoles nearby, suggests that there may be an element of parental care towards offspring. Skin swabs from four E. salvaje individuals were tested via QPCR analysis for the presence of amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd); all these individuals tested positive for Bd, with infection loads ranging 0.24 - 53.96 Bd Genomic Equivalents. These results may have significant implications for the conservation of E. salvaje, considering chytridiomycosis
likely led to severe population declines and/or the possible extinction of its congener E. rabborum.
... Based on the IUCN criterion, this frog should be assessed in a more restrictive EN category. All the 1900-2650Dunn 1937, Duellman 1970, Lips 1998, Savage 2002, Stuckert et al. 2009, Frost 2016 Isthmohyla zetecki NT Unidentified 1200-1804 Dunn 1937, Duellman 1970, Savage 2002, Frost 2016 Osteocephalus deridens Osteocephalus planiceps ...
Bromeliads constitute a good example of symbiosis with organisms that spend their entire life cycle inside the plants, and often depend on them to breed. The bromeliads benefit from this interaction by increasing their nutrients intake. Conservation efforts tend to focus on a single endangered species, but in symbiotic associations, the viability of one species depends on that of the other. Based on IUCN criteria, any species that depends on another to complete its life cycle should be assigned a conservation status equivalent to that of the host taxon, where appropriate. We gathered published plus fieldwork data on the frog-bromeliad mutualism and compiled a checklist of 99 bromeligenous frogs species associated to 69 bromeliad hosts, and found threatened bromeliads hosting non-threatened frogs. We found that 62% bromeligenous frogs inhabit unspecified bromeliads. Finally, we propose strategies for improving understanding and conservation of the frog-bromeliad mutualism.
... But based on the predator/prey size ratios (Table 1) we can deduce from literature data that the frogs ('1.5-3 cm body length) devoured by P. regius had an estimated mass of '0.375-2 g (comp. frog body mass data by Stuckert et al. 2009; Costa-Pereira et al. 2010), whereas the captured lizards ('2.3-5 cm snout-vent length) had an estimated mass of '0.5-3 g (comp. lizard body mass data by Meiri 2010;Senczuk et al. 2014). ...
The salticid spider Phidippus regius C.L. Koch, 1846 is documented preying on small frogs (Hyla spp., Osteopilus septentrionalis) and lizards (Anolis carolinensis and Anolis sagrei) in Florida, USA. Female as well as male P. regius were engaged in feeding on this type of vertebrate prey. A total of eight incidents of P. regius devouring vertebrates have been witnessed in seven Florida counties. Furthermore, we report an incident of a large unidentified Phidippus sp. (possibly P. bidentatus F. O. Pickard-Cambridge, 1901) preying on an immature anole lizard in Costa Rica. P. regius, otherwise known to feed almost exclusively on insects and spiders, is one of the world's largest salticid spiders reaching a maximum recorded body length of 2.2 cm. Most other salticid spiders appear to be too small in body size to overcome vertebrate prey. Vertebrate predation by salticid spiders has not been previously documented in the scientific literature. Together with Salticidae, spiders from 27 of 114 families (24%) are currently known to occasionally consume vertebrate prey.
... Isthmohyla species, such as bromeliad-dwelling I. picadoi and I. zeteki and pond-breeding I. pseudopuma, persist in Bd-positive areas (Stuckert et al., 2009) and were considered less susceptible (Table 2). ...
Amphibians around the world are declining from threats that cannot currently be mitigated, making it impossible to safeguard some species in their natural habitats. Amphibians in the mountainous neotropics are one example where severe disease-related declines prompted calls for the establishment of captive assurance colonies to avoid extinctions. We surveyed experts in Panamanian amphibians to determine the probability of avoiding chytridiomycosis-related extinctions using captive breeding programs. We ranked Panamanian amphibian species by perceived susceptibility to chytridiomycosis, then calculated the likelihood of avoiding extinction as the product of three probabilities, which include (1) finding sufficient founder animals, (2) successfully breeding these species in captivity and (3) becoming extinct in the wild. The likelihood of finding enough animals to create a captive founding population was low for many rare species, especially for salamanders and caecilians. It was also low for frogs which were once regularly encountered, but have already disappeared including Atelopus chiriquiensis, Craugastor emcelae, C. obesus, C. punctariolus, C. rhyacobatrachus, Ecnomiohyla rabborum, Isthmohyla calypsa and Oophaga speciosa. Our results indicate that captive breeding could improve the odds of avoiding extinction for species that have severely declined or are likely to decline due to chytridiomycosis including Atelopus certus, A. glyphus, A. limosus, A. varius, A. zeteki, Anotheca spinosa, Gastrotheca cornuta, Agalychnis lemur and Hemiphractus fasciatus. Priority species that experts predicted were highly susceptible to chytridiomycosis that might also benefit from ex situ management include Craugastor tabasarae, C. azueroensis, C. evanesco, Strabomantis bufoniformis and Colostethus panamansis. In spite of high levels of uncertainty, this expert assessment approach allowed us to refine our priorities for captive amphibian programs in Panama and identify priority conservation actions with a clearer understanding of the probability of success.
... Isthmohyla picadoi was described from the southwestern slope of Volcán Barba, Cantón de Santa Barbara, Provincia de Heredia, in the Cordillera Central of north-central Costa Rica (Dunn, 1937; Savage, 1974). It inhabits the Lower Montane and Montane Rainforest life zones, approximately between 1900 and 2800 m asl, where it is markedly associated with bromeliad phytotelmata, that serve as calling site, mating place and nursery ground (Stuckert et al., 2009). It is only exceptionally found on rocks in streams (Duellman, 2001). ...
I report an episode of anuran mortality and decline in the Reserva Forestal Fortuna, Chiriquí, Panama. The symptoms of decline at this site include population reductions, the presence of dead or dying adults, and tadpole abnormalities. Streamside anurans were abundant and diverse in 1993–1995, were restricted to a few streams in December 1996–January 1997, and then became rare throughout the reserve in July–August 1997. Between December 1996 and January 1997, I found 54 dead or dying frogs belonging to 10 species, and 12% of tadpoles had abnormalities of the oral disc. In July–August 1997 I monitored nine streams 37 times and captured only six individuals, whereas 13 terrestrial surveys along five trails resulted in 18 captured individuals. No dead or dying animals were found during those two months, but 11% of tadpoles had mouthpart abnormalities. Necropsies revealed that 18 of 18 dead anurans had a fungal infection of the skin; because this fungus was the only infection shared among all dead frogs, I suggest that it killed them and contributed to the decline of these populations. The presence of mouthpart abnormalities during a period of adult mortality suggests that this symptom may also be linked to the fungus infection. Clinical signs of decline in the anurans of Fortuna are similar to those found in the anurans of Monteverde and Las Tablas, Costa Rica, and I hypothesize that this pathogen was involved in the declines at all three sites.
Data were collected on epiphyte occurrence on tree trunks of four diameter classes in a Guatemalan cloud forest in order to document the vascular epiphyte flora and to explore aspects of species associations. Of the 68 species recorded, the largest groups were the Orchidaceae (29 species) and the Polypodiaceae (18 species). Conditional clustering and constellation analyses revealed associations of small, closely related species on smaller and consequently younger trunks, and associations of larger, less closely related species on larger, and hence older, trunks. The associations of small species possess characteristics correlated with the earlier stages of plant succession and the density-independent and non-equilibrium diversity model. The associations of larger species possess characteristics correlated with the later stages of plant succession and appear to approach equilibrium in species composition.
The faunas of tank bromeliads were sampled over two years in three forest types at different elevations in the Luquillo Experimental Forest, Puerto Rico, and the diversity of their animal communities compared. Bromeliad plants behaved as islands in that, within forests, the species richness and abundance of their animal communities were significantly and positively correlated with increase in plant size. The amount of canopy debris they accumulated was similarly correlated with increase in plant size. Overall diversity was lowest in the dwarf forest, where plants were uniformly small. Animal communities were stable from year to year, and could be characterised for each forest type and for compartments within the plant. They showed a pattern of high dominance, which increased with elevation (Mc-Naughton index 37, 54, and 73, respectively, for the tabonuco, palo Colorado, and dwarf forest). Alpha-diversity for sites sampled in each year reflected net primary productivity (NPP) of the forest, declining with increasing elevation when animal abundance measures were used (jackknife estimates of Simpson's diversity index 6.54 & 11.04 [tabonuco], 3.53 & 6.22 [palo Colorado], and 2.75 & 2.17 [dwarf forest]). Species richness over the two years, however, was highest in the intermediate palo Colorado forest (187 species), compared to 146 and 88 in the tabonuco and dwarf forests, respectively. These figures were close to jackknife estimates of maximum species richness. The difference in species richness between tabonuco and palo Colorado forests was significant in one year only. In addition to NPP, other factors, such as litter quality and the structural complexity of the habitat in the palo Colorado forest, may have influenced species richness. The most abundant species in individual plants were also the most widely occurring, confirming known patterns of abundance and distribution in other functional groups. Diversity within bromeliad microcosms at different elevations supported known relationships between diversity, productivity, and habitat complexity along gradients and was not related to differences in the total bromeliad habitat available for colonization.