Alessandro Catenazzi

Recent shifts in the occurrence, cause, and magnitude of animal mass mortality events

Significance Mass mortality events (MMEs), the rapid, catastrophic die-off of organisms, are an example of a rare event affecting natural populations. Individual reports of MMEs clearly demonstrate their ecological and evolutionary importance, yet our understanding of the general features characterizing such events is limited. Here, we conducted the first, to our knowledge, quantitative analysis of MMEs across the animal kingdom, and as such, we were able to explore novel patterns, trends, and features associated with MMEs. Our analysis uncovered the surprising finding that there have been recent shifts in the magnitudes of MMEs and their associated causes. Our database allows the recommendation of improvements for data collection in ways that will enhance our understanding of how MMEs relate to ongoing perturbations to ecosystems. Mass mortality events (MMEs) are rapidly occurring catastrophic demographic events that punctuate background mortality levels. Individual MMEs are staggering in their observed magnitude: removing more than 90% of a population, resulting in the death of more than a billion individuals, or producing 700 million tons of dead biomass in a single event. Despite extensive documentation of individual MMEs, we have no understanding of the major features characterizing the occurrence and magnitude of MMEs, their causes, or trends through time. Thus, no framework exists for contextualizing MMEs in the wake of ongoing global and regional perturbations to natural systems. Here we present an analysis of 727 published MMEs from across the globe, affecting 2,407 animal populations. We show that the magnitude of MMEs has been intensifying for birds, fishes, and marine invertebrates; invariant for mammals; and decreasing for reptiles and amphibians. These shifts in magnitude proved robust when we accounted for an increase in the occurrence of MMEs since 1940. However, it remains unclear whether the increase in the occurrence of MMEs represents a true pattern or simply a perceived increase. Regardless, the increase in MMEs appears to be associated with a rise in disease emergence, biotoxicity, and events produced by multiple interacting stressors, yet temporal trends in MME causes varied among taxa and may be associated with increased detectability. In addition, MMEs with the largest magnitudes were those that resulted from multiple stressors, starvation, and disease. These results advance our understanding of rare demographic processes and their relationship to global and regional perturbations to natural systems.

Thermal Physiology, Disease, and Amphibian Declines on the Eastern Slopes of the Andes

Rising temperatures, a widespread consequence of climate change, have been implicated in enigmatic amphibian declines from habitats with little apparent human impact. The pathogenic fungus Batrachochytrium dendrobatidis (Bd), now widespread in Neotropical mountains, may act in synergy with climate change causing collapse in thermally stressed hosts. We measured the thermal tolerance of frogs along a wide elevational gradient in the Tropical Andes, where frog populations have collapsed. We used the difference between critical thermal maximum and the temperature a frog experiences in nature as a measure of tolerance to high temperatures. Temperature tolerance increased as elevation increased, suggesting that frogs at higher elevations may be less sensitive to rising temperatures. We tested the alternative pathogen optimal growth hypothesis that prevalence of the pathogen should decrease as temperatures fall outside the optimal range of pathogen growth. Our infection-prevalence data supported the pathogen optimal growth hypothesis because we found that prevalence of Bd increased when host temperatures matched its optimal growth range. These findings suggest that rising temperatures may not be the driver of amphibian declines in the eastern slopes of the Andes. Zoonotic outbreaks of Bd are the most parsimonious hypothesis to explain the collapse of montane amphibian faunas; but our results also reveal that lowland tropical amphibians, despite being shielded from Bd by higher temperatures, are vulnerable to climate-warming stress.

Co-Infection by Chytrid Fungus and Ranaviruses in Wild and Harvested Frogs in the Tropical Andes

While global amphibian declines are associated with the spread of Batrachochytrium dendrobatidis (Bd), undetected concurrent co-infection by other pathogens may be little recognized threats to amphibians. Emerging viruses in the genus Ranavirus (Rv) also cause die-offs of amphibians and other ectotherms, but the extent of their distribution globally, or how co-infections with Bd impact amphibians are poorly understood. We provide the first report of Bd and Rv co-infection in South America, and the first report of Rv infections in the amphibian biodiversity hotspot of the Peruvian Andes, where Bd is associated with extinctions. Using these data, we tested the hypothesis that Bd or Rv parasites facilitate co-infection, as assessed by parasite abundance or infection intensity within individual adult frogs. Co-infection occurred in 30% of stream-dwelling frogs; 65% were infected by Bd and 40% by Rv. Among terrestrial, direct-developing Pristimantis frogs 40% were infected by Bd, 35% by Rv, and 20% co-infected. In Telmatobius frogs harvested for the live-trade 49% were co-infected, 92% were infected by Bd, and 53% by Rv. Median Bd and Rv loads were similar in both wild (Bd = 101.2 Ze, Rv = 102.3 viral copies) and harvested frogs (Bd = 103.1 Ze, Rv = 102.7 viral copies). While neither parasite abundance nor infection intensity were associated with co-infection patterns in adults, these data did not include the most susceptible larval and metamorphic life stages. These findings suggest Rv distribution is global and that co-infection among these parasites may be common. These results raise conservation concerns, but greater testing is necessary to determine if parasite interactions increase amphibian vulnerability to secondary infections across differing life stages, and constitute a previously undetected threat to declining populations. Greater surveillance of parasite interactions may increase our capacity to contain and mitigate the impacts of these and other wildlife diseases.

Conservation Status of Amphibians in Peru1

Abstract: Peru hosts a rich amphibian fauna with approximately 571 species described to date. Many of these species have been formally described only recently, and many more remain to be discovered and recognized. Despite the increase in the number of known species, some reports indicate recent, and in some cases enigmatic, loss of species richness at several sites in the Peruvian Andes. Similar population declines have been observed in neighboring Andean countries. The pathogenic fungus Batrachochytrium dendrobatidis is associated with some of these declines, and we include a timeline of records of this pathogen in Peruvian amphibians. However, the paucity of standardized, long-term surveys limits our ability to understand the causes of declines and to assess the conservation status of Peruvian amphibians. Here we provide updated information on the conservation status of amphibians in Peru, and we discuss the possible causes of the observed declines. Furthermore, we discuss present and future threats to amphibian biodiversity, and we outline actions needed to promote the survival of this globally endangered group. We include a list of candidate sites for long-term surveys.

Batrachochytrium dendrobatidis in the live frog trade of Telmatobius (Anura: Ceratophryidae) in the tropical Andes

Species of frogs in the genus Telmatobius are traded and sold for human consumption in the Andes and in coastal cities of Peru and Bolivia. These frogs are harvested from wild populations. We report high prevalence of infection by the pathogenic fungus Batrachochytrium dendrobatidis in live frogs purchased at the main market in Cusco, Peru, from January 2008 to January 2010. We suggest that the transport of native anurans through the live frog trade could facilitate the spread of this fungus among Andean frogs. The tropical Andes are the most important biodiversity hotspot for amphibians. Because many neotropical taxa are known to be susceptible to chytridiomycosis, the presence of a large reservoir of infection in the frog trade poses a significant threat to amphibian conservation.

A New Species of Minute Noblella (Anura: Strabomantidae) from Southern Peru: The Smallest Frog of the Andes

Abstract We describe a new species of Noblella from the upper Cosñipata Valley in southern Peru (Cusco Region). Specimens were found in the leaf litter of a cloud forest between 3025 and 3190 m elevation. The most distinctive character of the new species is its diminutive size (maximum SVL female 12.4 mm, male 11.1 mm). With an average snout–vent length of 11.4 mm (n  =  7) in adult specimens, the new species is the smallest Andean frog, and one of the smallest anurans in the world. The new frog is rare (between 30 and 75 frogs/ ha) and found only in montane scrub and forest habitats near the ecotone with the high-Andean puna grasslands. Although the amphibian fungal infection (Batrachochytrium dendrobatidis) has been recorded in southern Peru, no infections were detected in the new species.

Seasonal and Geographic Eurythermy in a Coastal Peruvian Lizard

Abstract We contrasted the summer and winter field body temperatures of the tropidurid lizard Microlophus peruvianus at the Paracas Peninsula in southern Peru. We also compared our winter data to those gathered by >Huey (1974) at the Illescas Peninsula in northern Peru to test the hypothesis that southern lizards would tolerate lower temperatures than northern lizards. Cloud cover is more persistent in Paracas than it is in Illescas. During the austral winter, lizards at Paracas reduced surface activity to midday hours and had body temperatures below the mean set-point temperature (as measured in a photo-thermal gradient). Lizards from southern Peru were active over a wider range of temperatures than were lizards from Illescas. Mean body temperature of field-active lizards in the cloudy Paracas site was 33.0 ± 0.44 C, significantly lower than the mean field body temperature at the sunnier Illescas site (36.3 ± 0.26 C, t = −6.19, P < 0.001). Although thermal preferences tend to be conserved among related lizard species, we found considerable variation in body temperatures and activity patterns of two populations of this species.

The amphibians and reptiles of Manu National Park and its buffer zone, Amazon basin and eastern slopes of the Andes, Peru

We compile a list of all amphibians and reptiles known to occur within Manu National Park, Peru and its buffer zone, located in one of the worlds biodiversity hotspots. Covering approximately 0.01% of the planets terrestrial surface, this protected area preserves 155 species of amphibians and 132 species of reptiles, corresponding to 2.2% and 1.5% respectively of the known diversity for these groups. Moreover, Manu National Park preserves natural habitats and populations of one critically endangered (Atelopus erythropus), three endangered (Bryophryne cophites, Pristimantis cosnipatae and Psychrophrynella usurpator), three vulnerable amphibians (Atelopus tricolor, Gastrotheca excubitor, Rhinella manu) and two vulnerable reptiles (Chelonoidis denticulata, Podocnemis unifilis), according to the threat categories of the IUCN Red List.

Three New Species of Bryophryne (Anura: Strabomantidae) from the Region of Cusco, Peru

ABSTRACT. We describe three new species of Bryophryne from the Region of Cusco in southern Peru, increasing the number of currently known Bryophryne to six. One of the new species differs from all species of Bryophryne in having a tympanic annulus and tympanic membrane. Males of this species have vocal slits, a vocal sac, and produce a call, which we analyze herein. This species is found at San Luis, a montane cloud forest along the road from Abra Malaga to Quillabamba at elevations between 3272 and 3354 m. The second new species has an orange throat and groin and is found along the Ericsson trail that connects Acjanaco to Pillahuata in Manu National Park and near Abra Acjanaco along the Paucartambo-Pilcopata road at elevations between 3266 and 3430 m. The third new species has the throat and chest mottled pale gray and tan, whereas the belly is black with white flecks. This species is only known from the upper Marcapata valley along the road from Abra Huallahualla to Quincemil at elevations between 3129 and 3285 m. Ecological observations for all new species are described and a map showing the type localities of all currently known species of Bryophryne is presented.

Seabird nutrient subsidies benefit non-nitrogen fixing trees and alter species composition in South American coastal dry forests

Marine-derived nutrients can increase primary productivity and change species composition of terrestrial plant communities in coastal and riverine ecosystems. We hypothesized that sea nutrient subsidies have a positive effect on nitrogen assimilation and seedling survival of non-nitrogen fixing species, increasing the relative abundance of non-nitrogen fixing species close to seashore. Moreover, we proposed that herbivores can alter the effects of nutrient supplementation by preferentially feeding on high nutrient plants. We studied the effects of nutrient fertilization by seabird guano on tree recruitment and how these effects can be modulated by herbivorous lizards in the coastal dry forests of northwestern Peru. We combined field studies, experiments and stable isotope analysis to study the response of the two most common tree species in these forests, the nitrogen-fixing Prosopis pallida and the non-nitrogen-fixing Capparis scabrida. We did not find differences in herbivore pressure along the sea-inland gradient. We found that the non-nitrogen fixing C. scabrida assimilates marine-derived nitrogen and is more abundant than P. pallida closer to guano-rich soil. We conclude that the input of marine-derived nitrogen through guano deposited by seabirds feeding in the Pacific Ocean affects the two dominant tree species of the coastal dry forests of northern Peru in contrasting ways. The non-nitrogen fixing species, C. scabrida may benefit from sea nutrient subsidies by incorporating guano-derived nitrogen into its foliar tissues, whereas P. pallida, capable of atmospheric fixation, does not.