No evidence for innate differences in tadpole behavior between natural, urbanized, and invasive populations

Abstract

Animals are increasingly challenged to respond to novel or rapidly changing habitats due to urbanization and/or displacement outside their native range by humans. Behavioral differences, such as increased boldness (i.e., propensity for risk-taking), are often observed in animals persisting in novel environments; however, in many cases, it is unclear how these differences arise (e.g., through developmental plasticity or evolution) or when they arise (i.e., at what age or developmental stage). In the Guttural Toad ( Sclerophrys gutturalis ), adult urban toads from both native and invasive ranges are bolder than conspecifics in natural habitats. Here, we reared Guttural Toad tadpoles in a common garden experiment, and tested for innate differences in boldness across their development and between individuals whose parents and lineage came from rural-native, urban-native, and urban-invasive localities (i.e., origin populations). Tadpoles did not differ in their boldness or in how their boldness changed over ontogeny based on their origin populations. In general, tadpoles typically became less bold as they aged, irrespective of origin population. Our findings indicate that differences in boldness in free-living adult Guttural Toads are not innate in the tadpole stage and we discuss three possible mechanisms driving phenotypic divergence in adult boldness for the focus of future research: habitat-dependent developmental effects on tadpole behavior, decoupled evolution between the tadpole and adult stage, and/or behavioral flexibility, learning, or acclimatization during the adult stage. Significance statement To determine if animals can persist in urban areas or become invasive outside their native ranges, it is important to understand how they adapt to life in the city. Our study investigates if differences in boldness that have been found in adult Guttural Toads ( Sclerophrys gutturalis ) represent heritable differences that can also be found in early life stages by rearing tadpoles from eggs in a common garden experiment. We did not find any differences in boldness among tadpoles from rural-native, urban-native, and urban-invasive origin populations. Our findings suggest that differences in boldness are not innate and/or that boldness is a behavioral trait that is decoupled between the tadpole and the adult stage.

Dietary tannins alter growth, behavior, and the gut microbiome of larval amphibians

“…It is possible that our assay design did not fully capture the boldness behavior, as it was limited to 10 min, and similarly may not truly capture dispersal behavior in tadpoles. Other studies that measure boldness and exploration used assays that lasted 20 and 25 min (Urszán et al 2015b;Mühlenhaupt et al 2022). Boldness can also change as tadpoles age (Mühlenhaupt et al 2022), so it is possible that dietary effects on boldness are more distinguished in adulthood.…”

“…Other studies that measure boldness and exploration used assays that lasted 20 and 25 min (Urszán et al 2015b;Mühlenhaupt et al 2022). Boldness can also change as tadpoles age (Mühlenhaupt et al 2022), so it is possible that dietary effects on boldness are more distinguished in adulthood. Ultimately, addressing this fear-food tradeoff in aquatic herbivores will require more studies.…”

“…Boldness can also change as tadpoles age (Mühlenhaupt et al. 2022), so it is possible that dietary effects on boldness are more distinguished in adulthood. Ultimately, addressing this fear‐food tradeoff in aquatic herbivores will require more studies.…”

The relationships between toad behaviour, antipredator defences, and spatial and sexual variation in predation pressure

“…Other traits seem to be aligned with this spatial pattern of predation pressure: agrosystem toads have a more intermittent locomotion mode ( Zamora-Camacho, 2018 ), are brighter ( Zamora-Camacho & Comas, 2019 ), and have larger and more contrasting parotoid glands than pine grove conspecifics ( Zamora-Camacho, 2021 ), which could signify greater antipredator defences, likely triggered by more intense predation pressure. Remarkably, while habitat alone does not innately affect boldness behaviour of S. gutturalis tadpoles ( Mühlenhaupt et al, 2022 ), predation pressure can explain spatial divergence in behavioural and morphological traits of other anurans, such as Bombina variegata toads ( Kang et al, 2017 ). Spatial differences in boldness may have implications at other levels.…”