This week Tropical Conservation Science publishes our last contribution to a survey of chytrid prevalence in lowland Amazonian forests led by our collaborator Dr. Rudolf von May from the University of Michigan. The chytrid fungus has caused precipitous population declines and the collapse of many amphibian species throughout the world, especially in mountains and in places that are moist and moderately cool - just the conditions many amphibians like.
However warm and moist places such as tropical lowland forests are the ecosystem of greatest amphibian species richness. The highest species richness is found in lowland Amazonian forests, known to be home to over 90 species of amphibians at a single site. Considering that chytrid is capable to infect and cause mortality in multiple amphibian hosts, there is potential for for this disease to wreak havoc in these mega diverse places. Yet most of the lowland Amazon amphibian communities that are being surveyed are not declining due to chytrid.
One reason this might not be happening has traditionally been associated to the constant high temperatures found in the lowland Amazon, which are supposed to exceed the thermal tolerance of the fungus. When grown in the lab, the chytrid fungus does not grow and zoospores are killed at temperatures above 28C. Our study shows that temperatures above 28C occur frequently at Los Amigos, a biological station in lowland Amazonian Peru.
Therefore one would expect not to find chytrid in the lowland Amazon, or to find very few infected animals. That's not what we found after surveying the frog community of Los Amigos, in southeastern Peru, because nine species, including Adenomera andreae shown here and Hamptophryne boliviana shown above, were infected by chytrid. Although infection levels were low, our findings suggest that the chytrid can affect amphibians even in very warm places.
At the beginning of the month we traveled to Pampas Galeras National Reserve in Peru for the field course on ecology and conservation of high-Andean amphibians. This course gathered 24 participants coming from throughout the Americas, including Peru, Chile, Colombia, Venezuela, the US and Canada, and ranging from undergraduate to graduate students and professionals in biological and veterinary sciences.
The field course was organized in collaboration with the Reserve and with the local NGO Pro Fauna Silvestre. The course was led by instructors Alessandro Catenazzi and Sarah Kupferberg, with lectures by our collaborator Victor Vargas of SERFOR and Pro Fauna Silvestre, and by Allan Flores, head of the Reserve. We emphasized field applications in stream and tadpole ecology, and experimental approaches with mesocosms in the stunning landscape of Pampas Galeras.
The main objectives of the course were to develop skills in experimental design and execution of ecological studies, and to learn new field techniques in population monitoring, field experiments, environmental sampling, and data analysis. Lectures ranged from introduction to physical processes and flow regime adaptations in streams, to tadpole feeding ecology, amphibian ecophysiology, frog skin microbiota and disease ecology. Students then split into six groups to conduct field projects, and everyone helped search for tadpoles and frogs in the frigid nights of Pampas Galeras.
The star of the course was the Water Andean frog, Telmatobius sp., which despite epizootics of chytridiomycosis that have swept central and southern Peru since the early 2000s, persists at Pampas Galeras with good populations. In the picture we are measuring the body temperature of a female, the surface of the creek where she lives often freezes at night.
The six group projects covered the following topics: (1) effects of water depth and stream microhabitat on biofilm productivity; (2) estimating population abundance of adult Telmatobius frogs using photographic recognition and mark recapture estimation; (3) study of skin symbiotic bacterial diversity in adult Telmatobius; (4) effects of mouthpart degradation caused by chytrid on tadpole feeding ecology; (5) bioacoustics of Telmatobius intermedius and Telmatobius sp. and (6) thermal ecology of aquatic frogs.
Last July we embarked on a search for Atelopus loettersi, shown in the picture here taken from the description by I. De la Riva and colleagues. The type locality is near Quincemil, in a trib of the Nusiniscato river. Sadly this river, similarly to many other rivers in the upper Madre de Dios, Araza and Inambari watersheds, is the target of indiscriminate gold mining, which is affecting river turbidity and sedimentation, and likely introducing mercury into the riverine ecosystems.
The original description already warned us the task would not be easy, since a single adult had been found at this locality. However, some juveniles had also been found during a previous visit, so we were hopeful we could again confirm presence of this species. Harlequin toads have declined throughout their geographic range from Costa Rica to Bolivia, yet lowland and submontane species such as A. loettersi (the type locality is at 480 m a.s.l.) have generally fared better than mid-and high-elevation species..
We spent two nights at the stream where the species was first discovered, and at an adjacent stream which also looked like great harlequin toad habitat. Both streams had rich macroinvertebrate communities, and although one had water withdrawals for a nearby miner's camp, they generally appeared to be in good shape. We unfortunately did not see any sleeping A. loettersi at night. We again went back during the day and similarly failed to spot or hear any harlequin toad, or to find any of their tadpoles in side pools of the creek. During the two nights, the concomitant full moon and mostly clear skies certainly did not help with making the night surveys very successful. Despite these shortcomings, we were able to swab the skin of ~20 frogs of other species, which will provide information on presence of cythrid fungus. We also helped an Engystomops freibergi have one of her best nights, after inadvertently destroying a short segment of a termite tunnel.
During the month of March we resurveyed amphibian communities along the elevational gradient in the Kosñipata Valley of southern Peru, near Manu National Park. These amphibian communities collapsed during the early 2000s during epizootics of chytridiomycosis, as we have previously documented. Our previous surveys compared anuran communities observed in 2008 and 2009, after chytridiomycosis invaded the valley, with those observed from 1996 to 1999, when we started working in this region. Furthermore, there are rich specimen collections made by teams of the Smithsonian in the early 90s, and Kansas University in the early 70s, which further document the diversity of anuran communities prior to epizootics of chytridiomycosis. Nine years after our last comprehensive survey (2009), we decided to return to the valley and re-sample the same localities from 1200 to 3700 m.
Our previous comprehensive surveys in the wet seasons of 1999, 2008 and 2009 consisted of two approaches: surveys of leaf-litter frogs using 10x10m quadrats, with four quadrats within each 100-m elevational band; and nocturnal surveys along the road that connects the mountain pass of Acjanaco at 3400 m to the town of Chontachaca at 900 m. We returned to the same sites along the road, and repeated the same sampling design during this last wet season. Our field crew included students and recent graduates from the University in Cusco, along with field assistants from the nearby town of Pilcopata, including two people who had already participated in previous surveys. We were able to sample all 100 leaf-litter quadrats (each takes about 2 hours to complete by three people), and to survey at night at elevations up to 3100 m (above 3100 m, nocturnal surveys are not effective because few frogs are active at night).
We captured over 600 frogs over the course of three weeks. Ccommunities of arboreal and stream-breeding frogs observed during nocturnal surveys continue to show a substantial deficit in species richness (see graph). Our data are preliminary because we still need to compute sampling effort, but the snapshot shows a slight recovery in species richness. This pattern is corroborated by "rediscoveries" of a few species that were abundant in 1999, but absent in 2008 and 2009. However, our preliminary data also suggest a decrease in frog density, and confirm that most species that disappeared from 2000 to 2008 continue to be absent from the valley.
We will next process swab samples to examine how infection dynamics have changed over the years. In the years following the epizootics of the early 2000s, prevalence varied widely along the elevational gradient, with populations at mid elevation (1500-2000 m) most infected by the chytrid fungus. We are especially interested in studying current infection patterns in species that have persisted despite being susceptible to chytridiomycosis. Understanding how susceptible species are able to persist and even recover despite the continuous presence of the pathogen may help develop strategies to mitigate the negative effects of the fungal disease on amphibians.
The work of our collaborator Vanessa Uscapi is featured in this beautiful video made by Katie Garrett. Vanessa, seen below weighing a frog with the help of a field assistant, has been working with the frogs of the Madre Selva montane forest near Quincemil, in the Peruvian Andes, for several years. As part of her field work, she discovered a new, minute terrestrial-breeding frog, Noblella madreselva, which we described in 2015. Her studies contribute to the protection of this fragile ecosystem. Many montane forests in the Andes are threatened by logging and the expansion of agriculture. Yet they often contain highly endemic species such as Noblella madreselva and other small frogs that inhabit the humid leaf litter at high elevations.
After our contributions on tadpole thermal performance, we continued investigating the effects of dam-altered thermal regimes on river-breeding amphibians by looking at the consequences of hypolimnetic releases (cold water being released from the bottom of artificial reservoirs) for digestion, assimilation and vulnerability to predators of tadpoles. Our study Consequences of dam‐altered thermal regimes for a riverine herbivore's digestive efficiency, growth and vulnerability to predation, was a collaboration with Dr. Sarah Kupferberger and was published this week in Freshwater Biology.
We again worked on the foothill yellow-legged frog, Rana boylii in California. At present, R. boylii occupies less than half its historic range, due to the existence of large dams in many river systems. During the springs and summers of 2008, 2009 and 2010 we monitored temperature conditions at many breeding sites of R. boylii in regulated (i.e., downstream of dams) and unregulated rivers in northern California (see sensor placed by a rock that was subsequently used as egg attachment site in the image above) to understand changes in thermal regime caused by hypolimnetic releases. We then mimicked the colder conditions existing downstream of dams in experimental settings and investigated how tadpole's digestive efficiency responded to lower temperatures. Finally, we exposed tadpoles of different sizes and developmental stages to natural odonate and hemipteran predators (see a Ranatra eating a tadpole in one of our experimental enclosures in the image below).
Tadpoles reared in cold water had the lowest digestive efficiency of epilithic periphyton, albeit efficiency was ameliorated when tadpoles had access to highly nutritious dinitrogen‐fixing diatoms. However, these nutritious diatoms, which can be common in natural, unregulated rivers are often replaced by unpalatable, poorly nutritious periphyton downstream of rivers. In our experiments, growth rate of tadpoles correlated with assimilation efficiency, which is crucial for R. boylii because tadpoles need to metamorphose and get out of the water by the end of summer and before the fall rains cause deadly river floods. Low growth rate also affected tadpole survival, with small tadpoles much more likely to succumb to predation. Non‐lethal effects of predators on tadpole growth and tail injury, however, depended on both rearing temperature and exposure temperature. Contrary to the expectation that the cost of predator avoidance behaviours may be greater at warmer exposure temperatures because basal metabolic rates are higher, our results indicated that the energetic cost of foraging less was amplified at cool temperatures. Therefore, tadpoles growing in cold water face multiple, synergistic hurdles from lower assimilation efficiency and growth to increased predation by invertebrates, thus contributing to population recruitment bottlenecks.
The lab photo below won first place of the FIU Tropics Photo Contest! Young vicuña (Vicugna vicugna) taking a bath in a high-Andean creek at 13,000 feet. Vicuñas are the smallest of the four species of South American camelids, but they are highly prized because of the very fine fiber that can be produced with their wool. As a consequence of the high economic value of this fiber, vicuñas were driven to near extinction in the 1960s, until biologists promoted the sustainable management of wild populations in the high-Andes of southern Peru. One of the first and most successful project was conducted at Pampas Galeras in Ayacucho (shown in the photograph), today a national reserve honoring the memory of environmental journalist Barbara D'Achille.
Our lab contributed a publication naming two new species of frogs from Manu National Park, further increasing the number of amphibian species of the park. Manu NP already boasts the highest number of amphibian species living inside a natural protected area. The two new species, Pristimantis antisuyu (in the image below) and Pristimantis erythroinguinis (in the image on the left), are closely related but their elevational distributions do not overlap.
Pristimantis antisuyu lives in the cloud forest (image on right with good old Shigella), while P. erythroinguinis is found the Andean foothills and adjacent Amazon lowlands. Both species share with P. cruciocularis the unique pattern of having an iris with a cruciform pattern. Our molecular analyses suggest that P. cruciocularis and the two new species are part of the P. platydactylus-P. llojsintuta species complex, which is likely to contain more cryptic species.
Our paper on frog skin bacteria along the Amazon-Andes elevational transect (500 - 3800 m a.s.l.) was published today in Frontiers in Microbiology. We found lower numbers of anti-Bd isolates at elevations where amphibian declines had been greatest, and high proportion of anti-Bd isolates of high inhibitory strength in Bd-resistant frogs, supporting the idea that symbiotic bacteria play a functional role in amphibian skin defense. Yet this association does not consistently explain the fate of amphibian hosts along the elevational gradient, suggesting complex interactions among bacterial symbionts, hosts, and environmental factors in determining frog persistence in a region of high disease prevalence.
Our lab contributed a new species of small strabomantid frog (Holoadeninae) with the description of Psychrophrynella glauca from the southern Peruvian department of Puno. These frogs breed on land and lay eggs in moist places in the leaf litter. There is no tadpole stage and the embryos develop entirely within the egg. Small froglets abandon the nest once they hatch, but one or both of the parents (unknown in this species) may guard the egg nest and protect it from desiccation and predators. With the discovery of P. glauca, the geographic distribution of Psychrophrynella is extended to the Department of Puno, where it was no longer represented after the description of the genus Microkayla. Furthermore, the Cordillera de Carabaya is the only mountain range known to be home to four of the seven genera of Holoadeninae (Bryophryne, Microkayla, Noblella, and Psychrophrynella), suggesting an intriguing evolutionary history for this group in southern Peru.
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