Amphibian species vary in their learned avoidance response to the deadly fungal pathogen Batrachochytrium dendrobatidis

Abstract

1. Lethal and sublethal effects of pathogens should theoretically select for host avoidance of these pathogenic organisms. Some amphibians can learn to avoid the pathogenic fungus Batrachochytrium dendrobatidis (Bd) after one infectionclearance event.2. Here, we investigated whether four taxonomically distinct amphibians, Cuban tree frogs Osteopilus septentrionalis, southern toads Anaxyrus (Bufo) terrestris, greenhouse frogs Eleutherodactylus planirostris and pine woods tree frogs Hyla femoralis, exhibited any innate or learned avoidance of Bd on a moist substrate and, if so, what cues they used to identify the fungus.3. Cuban tree frogs, pine woods tree frogs and greenhouse frogs did not appear to exhibit detectable innate or learned avoidance of Bd. However, southern toads learned to avoid Bd after only one exposure. Southern toads avoided any treatment containing Bd metabolites but did not avoid treatments that lacked Bd metabolites even when dead zoospores were present.4. Bd metabolites appeared to be the cues that amphibians use to avoid Bd. These metabolites may have a distinct smell or may cause discomfort, which would be consistent with a classical or Pavlovian conditioning response. Synthesis and applications.Not all species of amphibians respond the same way to Bd exposure; some can learn to avoid Bd and the metabolites it produces, while others do not. These findings have important implications for both management practices and policy, and should be considered when developing disease models and conservation plans for amphibians.

Amphibian infection tolerance to chytridiomycosis

“…In association with these transmission sources, exposure risk is further mediated by (i) the proximity to and relative density of infectious zoospores in the environmental pool [ 23 , 42 , 43 ], or (ii) the relative density and shedding rate of conspecifics that are in direct contact [ 44 ]. Clinically infected amphibians are anecdotally reported to give off a recognizable smell (likely associated with the metabolite putrescine; [ 28 ]), and there is currently some evidence to suggest that amphibians may be able to detect and actively avoid [ 1 , 45 ] infected conspecifics or other sources of infection thereby reducing exposure risk [ 46 ]. Regardless of potential avoidance behaviours, however, variable exposure risk is thought to be a confounder of resistance and tolerance measures.…”

Biological mechanisms matter in contemporary wildlife conservation

“… 116 , 117 , 118 , 119 Equally, an understanding of mechanism has been essential to interpret important host behavioral responses to infection such as increased skin shedding 120 and thermoregulatory changes 121 to manage pathogen loads and learned avoidance of the pathogen. 122 Importantly, an understanding of mechanism has been central to the development of effective treatments for infected frogs 117 , 123 , 124 and to the management of chytridiomycosis in conservation-significant amphibian populations worldwide. 125 …”

Juvenile agile frogs spatially avoid ranavirus-infected conspecifics, but do not show generalized social distancing or self-isolation

“…Nonetheless, behavioural changes following exposure to a pathogen were seldom studied in amphibians. The handful of studies that did so (Kiesecker et al 1999; McMahon et al 2014; McMahon et al 2021; Le Sage et al 2022) reported that healthy individuals avoided infected conspecifics or contaminated surfaces and did not show generalized social distancing. Infected amphibians can show anorexia and lethargy (Gray et al 2009; Landsberg et al 2013), but whether these result in passive self-isolation and whether amphibians display active self-isolation is not yet known.…”