Tropical Snake Diversity Collapses After Widespread Amphibian Loss Elise F
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RESEARCH BIODIVERSITY LOSS assessed species has an unknown conserva- tion status (13). The diets of tropical snakes Tropical snake diversity collapses after widespread include amphibians and their eggs, inverte- brates (including oligochaetes and mollusks), amphibian loss lizards, snakes, birds, and mammals, with most species feeding on amphibians to some extent Elise F. Zipkin1*, Graziella V. DiRenzo1,2, Julie M. Ray3, Sam Rossman1,4, Karen R. Lips5 (table S1). Although amphibian declines are likely to negatively affect snakes through the Biodiversity is declining at unprecedented rates worldwide. Yet cascading effects of biodiversity loss on loss of diet items, presumably many species other taxa are largely unknown because baseline data are often unavailable. We document the collapse could persist by shifting to other prey. of a Neotropical snake community after the invasive fungal pathogen Batrachochytrium dendrobatidis Our study occurred in Parque Nacional G. D. caused a chytridiomycosis epizootic leading to the catastrophic loss of amphibians, a food source for Omar Torríjos Herrera, 8 km north of El Copé, snakes. After mass mortality of amphibians, the snake community contained fewer species and was Panama. The amphibian community at the more homogeneous across the study site, with several species in poorer body condition, despite no other studysite(hereafter“El Copé”)contained systematic changes in the environment. The demise of the snake community after amphibian loss >70 species pre-epizootic (11). Amphibian abun- demonstrates the repercussive and often unnoticed consequences of the biodiversity crisis and calls dance declined by >75% immediately after attention to the invisible declines of rare and data-deficient species. the Bd epizootic in late 2004, with extirpation of at least 30 species (11, 12). The study site is composed of mature secondary forest that re- ong-term biodiversity trends indicate that Without a clear understanding of these cascad- mained undisturbed with no systematic changes Downloaded from species extinction rates over the past two ing sequences, we risk undermining options documented within the abiotic environment centuries are up to 100 times higher than availableforeffectiveconservation(5). (e.g., habitat, water quality, or contaminants; L throughout the rest of human history (1). Nowhere has biodiversity loss been more materials and methods). We conducted 594 Despite tremendous data collection ef- acute than in the tropics, which harbor two- surveys targeting all amphibians and reptiles forts worldwide, empirical evidence of the eco- thirds of described species (6). Recent assess- on seven permanent transects during the 7 years logical impacts of these losses is often lacking. ments suggest that nearly 12% of animal species pre-epizootic (December 1997 to December http://science.sciencemag.org/ Scientists rarely have the ability to predict in tropical countries are classified as endan- 2004) and 513 surveys on the same transects impending change, precluding the opportunity gered, vulnerable, or near threatened, represent- during the 6 years post-epizootic (September to collect adequate pre- and postdata to eva- ing 64% of all such classified species worldwide 2006 to July 2012). luate ecosystem responses to species declines. (7). Amphibians, in particular, have suffered In El Copé, as with many tropical commun- Yet biodiversity loss can cause cascading effects severe declines in the tropics from habitat loss, ities, a large fraction of species are rare and within ecosystems, such as coextinction of mu- disease, and climate change (8, 9). Given that most are difficult to detect. For example, of the tualist species, changes in energy flow and amphibians are important as both consumers 36 snake species ever observed on our stand- primary production, and reduced resiliency and prey in aquatic and terrestrial habitats and ardized transect surveys during the 13-year to climate and environmental change (2–4). that their abundance in the tropics can be quite study, 12 were detected only once. In an effort high, the effects of amphibian losses likely per- to include the data from rarely observed spe- meate to other taxa within ecosystems (10). cies while also accounting for imperfect detec- on February 13, 2020 1Department of Integrative Biology; Ecology, Evolutionary We evaluated a Neotropical snake commu- tion and ecological variations among species, Biology, and Behavior Program, Michigan State University, nity for changes in species richness, commu- we developed a hierarchical community model 2 East Lansing, MI 48824, USA. Ecology, Evolution, and nity composition, occurrence rates, and body using a Bayesian approach for parameter es- Marine Biology, University of California, Santa Barbara, CA 93101, USA. 3La MICA Biological Station, El Copé de La condition after the mass mortality of amphib- timation (14). Our model estimated occurrence Pintada, Coclé, Republic of Panama. 4Hubbs-SeaWorld ians from chytridiomycosis caused by the rates, or the probability that both observed Research Institute, Melbourne Beach, FL 32951, USA. invasive fungal pathogen Batrachochytrium and unobserved species used the survey tran- 5Department of Biology, University of Maryland, College Park, MD 20742, USA. dendrobatidis (Bd)(11, 12). Snakes are an un- sects, which we utilized to calculate species *Corresponding author. Email: [email protected] derstudiedtaxoninwhichalmostoneinfour richness pre- and post-epizootic (materials and Fig. 1. Snake species richness and AB composition before and after the 0.03 40.1 Mode 1.0 Pre epizootic that led to amphibian loss. Mean Post 52.7 (A) Observed (dashed lines) and esti- Number of Npost 48.8 observed species mated snake species richness (posterior 61.7 0.5 N density plots with mean and mode) pre- 0.02 pre epizootic (Npre, blue) and post-epizootic 0.0 (Npost,orange).(B) Standard ellipses Axis 2 representing observed snake composition 0.01 P[Npost < Npre] = 0.85 pre-epizootic (blue) and post-epizootic −0.5 (orange). Points within the ellipses show Posterior density 21 30 the dimensionless values of community −1.0 0.00 P[Area < Area ] = 0.99 composition for the seven transects pre- post pre and post-epizootic. The smaller area of the 20 40 60 80 100 120 −1.0 −0.5 0.0 0.5 1.0 post-epizootic ellipse indicates a more Species richness (N) Axis 1 homogeneous snake community compared with pre-epizootic. Zipkin et al., Science 367, 814–816 (2020) 14 February 2020 1of3 RESEARCH | REPORT methods). We focused on estimating proba- (61.7 versus 48.8), median (58 versus 45), and community has fewer species and is more homo- bilities that species diversity and occurrence mode (52.7 versus 40.1) values of posterior geneous post-epizootic. metrics changed from pre- to post-epizootic distributions all indicate that snake species Individual snake species responses to the rather than reporting absolute values of these richness was higher pre-epizootic than post- loss of amphibians were variable, but most metrics, which are inherently imprecise owing epizootic (Fig. 1A), although the 95% credible fared worse post-epizootic. Despite low detec- to the many rare species within tropical snake intervals on richness estimates were wide both tion power for many species (figs. S1 and S2), communities. pre-epizootic (38 to 105) and post-epizootic (28 we were able to confidently estimate the prob- After the epizootic, the total number of to 89). Results of a nonmetric multidimen- ability that occurrence rates changed from pre- observed snake species declined from 30 to sional scaling analysis show that the observed to post-epizootic for almost half of the observed 21, with an estimated 0.85 probability that snake community composition also changed snake species (tables S2 and S3). Of the 17 speciesrichnesswaslowerpost-epizooticthan from pre- to post-epizootic, as indicated by a species with at least five total observations, pre-epizootic (Fig. 1A). Estimated species rich- shift of the centroid (0.93 probability of change) nine had occurrence rates that were lower post- ness was considerably higher than the number and reduction in area (0.99 probability of epizootic (with ≥0.72 probability), four had of observed snake species because of a high decrease) of standard ellipses comparing com- occurrence rates that were higher, and the probability that many species were present and position across survey transects (Fig. 1B). remaining four species experienced no sub- went undetected during sampling. The mean Collectively, these results reveal that the snake stantial change (Fig. 2). We compared body condition (ratio of mass to snout-to-vent length squared) for the six snake species with at least Detections five samples both pre- and post-epizootic (table Pre Post S4). Four of the six species had ≥0.97 prob- Downloaded from 13 0 ability of decreased body condition post-epizootic, 149 49 whereas two had body conditions that in- 41 creased (Fig. 3). Although there is no single life 41 70 history or diet attribute that provides a clear 70 explanation of the species results (table S1), 21 8 snakes that declined post-epizootic may have http://science.sciencemag.org/ 50 had a difficult time switching their diets as am- 42 phibians declined and prey availability shifted. 69 69 For example, Sibon argus, which has been doc- 47 57 umented feeding on amphibian eggs at higher 45 35 levels than the three other Sibon species [primar- 19 59 ily molluscivores; (15)], experienced the most 13 38 severe declines of its genus despite otherwise 15 similar habitat requirements and behaviors. 332 Although most snake species were negatively 0.00 0.25 0.50 0.75 1.00 affected by the loss of amphibians, a few ex- on February 13, 2020 P[Occurrencepost < Occurrencepre] ploited this change, increasing in occurrence and/or body condition. Thus, the Bd epizootic Fig. 2. Changes in snake species occurrence rates after the epizootic that led to amphibian loss. indirectly produced a large number of “loser” Probabilities (black circles) that occurrence rates were lower post-epizootic than pre-epizootic for snake species but also a few “winners,” an the 17 snake species with at least five total detections across both time periods.