Chytrid infections exhibit historical spread and contemporary seasonality in a declining stream-breeding frog

A M Belasen; R A Peek; A J Adams; I D Russell; M E De León; M J Adams; J Bettaso; K G H Breedveld; A Catenazzi; C P Dillingham; D A Grear; B J Halstead; P G Johnson; P M Kleeman; M S Koo; C W Koppl; J D Lauder; G Padgett-Flohr; J Piovia-Scott; K L Pope; V Vredenburg; M Westphal; K Wiseman; S J Kupferberg

doi:10.1098/rsos.231270

Chytrid infections exhibit historical spread and contemporary seasonality in a declining stream-breeding frog

R Soc Open Sci. 2024 Jan 31;11(1):231270. doi: 10.1098/rsos.231270. eCollection 2024 Jan.

Authors

A M Belasen^{1

2}, R A Peek³, A J Adams⁴, I D Russell⁵, M E De León⁶, M J Adams⁷, J Bettaso⁸, K G H Breedveld⁹, A Catenazzi¹⁰, C P Dillingham¹¹, D A Grear¹², B J Halstead¹³, P G Johnson¹⁴, P M Kleeman¹³, M S Koo¹⁵, C W Koppl¹¹, J D Lauder¹⁶, G Padgett-Flohr¹⁷, J Piovia-Scott¹⁸, K L Pope¹⁹, V Vredenburg²⁰, M Westphal²¹, K Wiseman²², S J Kupferberg²³

Affiliations

¹ Department of Integrative Biology, University of Texas at Austin, Austin, TX, USA.
² Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, USA.
³ California Department of Fish and Wildlife, West Sacramento, CA, USA.
⁴ Earth Research Institute, University of California, Santa Barbara, CA, USA.
⁵ Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, CA, USA.
⁶ Genome Center, University of California, Davis, CA, USA.
⁷ U.S. Geological Survey, Forest and Rangeland Ecosystem Science Center, Corvallis, OR, USA.
⁸ Six Rivers National Forest, Lower Trinity Ranger District, USDA Forest Service, P.O. Box 68, Willow Creek, CA, USA.
⁹ Spring Rivers Ecological Sciences LLC, Cassel, CA, USA.
¹⁰ Department of Biological Sciences, Florida International University, Miami, FL, USA.
¹¹ Plumas National Forest, USDA Forest Service, Quincy, CA, USA.
¹² U.S. Geological Survey, National Wildlife Health Center, Madison, WI, USA.
¹³ Point Reyes Field Station, U.S. Geological Survey, Western Ecological Research Center, Point Reyes Station, CA, USA.
¹⁴ Pinnacles National Park, National Park Service, Paicines, CA, USA.
¹⁵ Museum of Vertebrate Zoology, University of California, Berkeley, CA.
¹⁶ Sierra Streams Institute, Nevada City, CA, USA.
¹⁷ HELIX Environmental Planning, Inc, Roseville, CA, USA.
¹⁸ School of Biological Sciences, Washington State University, Vancouver, WA, USA.
¹⁹ Pacific Southwest Research Station, USDA Forest Service, Arcata, CA, USA.
²⁰ Department of Biology, San Francisco State University, San Francisco, CA, USA.
²¹ Central Coast Field Office, United States Bureau of Land Management, Marina, CA, USA.
²² Department of Herpetology, California Academy of Sciences, San Francisco, CA, USA.
²³ Department of Integrative Biology, University of California, Berkeley, CA, USA.

Abstract

Species with extensive geographical ranges pose special challenges to assessing drivers of wildlife disease, necessitating collaborative and large-scale analyses. The imperilled foothill yellow-legged frog (Rana boylii) inhabits a wide geographical range and variable conditions in rivers of California and Oregon (USA), and is considered threatened by the pathogen Batrachochytrium dendrobatidis (Bd). To assess drivers of Bd infections over time and space, we compiled over 2000 datapoints from R. boylii museum specimens (collected 1897-2005) and field samples (2005-2021) spanning 9° of latitude. We observed a south-to-north spread of Bd detections beginning in the 1940s and increase in prevalence from the 1940s to 1970s, coinciding with extirpation from southern latitudes. We detected eight high-prevalence geographical clusters through time that span the species' geographical range. Field-sampled male R. boylii exhibited the highest prevalence, and juveniles sampled in autumn exhibited the highest loads. Bd infection risk was highest in lower elevation rain-dominated watersheds, and with cool temperatures and low stream-flow conditions at the end of the dry season. Through a holistic assessment of relationships between infection risk, geographical context and time, we identify the locations and time periods where Bd mitigation and monitoring will be critical for conservation of this imperilled species.

Keywords: Mediterranean climate; Rana boylii; amphibian chytridiomycosis; freshwater conservation; seasonality; spatio-temporal disease model.

Associated data

figshare/10.6084/m9.figshare.c.7041551