Environmental effects on the ontogenesis of tadpole personality

Castellano, Sergio; Friard, Olivier

doi:10.1016/j.anbehav.2021.03.002

Cited by 7 publications

(5 citation statements)

References 47 publications

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“…Activity time was longer in larvae from transparent ponds, irrespective of treatment. In the light of previous research stating that Hyla intermedia tadpoles raised under greater perceived predation risk are less active (Castellano & Friard, 2021), it could be inferred that larvae from turbid ponds are under greater perceived predation risk. However, there is also contrasting evidence, for example, Brachyraphis episcopi fish are more active and bolder when raised under greater predation risk (Archard & Braithwaite, 2011), whereas Chlamydogobius eremius gobies behave more boldly when predation pressure is milder (Moran et al, 2016).…”

Section: Discussionmentioning

confidence: 97%

Larval newts from turbid and transparent waterbodies exhibit different morphological and behavioural traits

Zamora‐Camacho,

Aragón

2023

Freshwater Biology

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Turbidity represents an obstacle to visual acuity underwater that might entail considerable consequences for multiple faunal traits. Morphology, especially eye size, could be adjusted to cope with reduced visibility in turbid water. Moreover, turbidity could interfere with colour signals or crypsis. Turbid water may simultaneously impair the ability of prey and predators to detect each other, which may cause reduced speed, flight initiation distance, activity time, boldness, and exploratory behaviour by prey. In this work, we compared these traits in larvae of the newt Pleurodeles waltl from transparent and turbid ponds (around 100 and 300 FTU, respectively). Body size did not differ between pond types, but larvae from turbid ponds had smaller eyes, probably because visual acuity is structurally hindered by the environment. Colouration did not differ between transparent and turbid ponds on average, but it was more variable in larvae from transparent than turbid ponds, probably because transparent ponds trigger crypsis towards diverse background colours, whereas turbid ponds promote reduced pigmentation in all cases. In addition, behavioural traits were gauged in larvae from both types of ponds, in tests conducted in either transparent or turbid water. Speed was unaffected by turbidity, but larvae from turbid ponds increased their flight initiation distance when tested in transparent water. In all cases, larvae from transparent ponds were more active, and bolder in transparent water, and all larvae were more exploratory when tested in transparent water (regardless of which pond type they came from). Turbidity could trigger more cautious behaviours, probably because it makes predators harder to track. Alternatively, transparent water could stimulate a more expansive use of space through improved visibility, or it might encourage a more active search for shelter. These results shed light on the role of turbidity as a promotor of morphological and behavioural variability in amphibian larvae. These ecological consequences of water turbidity can be framed in terms of energy allocation and detectability in the context of predator–prey interactions.

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Section: Discussionmentioning

confidence: 97%

Larval newts from turbid and transparent waterbodies exhibit different morphological and behavioural traits

Zamora‐Camacho,

Aragón

2023

Freshwater Biology

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“…For instance, aggression (Wilson et al, 2011), boldness (Boulton et al, 2014), activity (Cote et al, 2010;Biro and Adriaenssens, 2013;Blake and Gabor, 2014), and exploration (Blake and Gabor, 2014;Heinen-Kay et al, 2016) have been established as personality traits in other swordtail and mosquitofish species. Variation in some of these personality traits such as boldness and aggression has previously been shown to correlate with predation (Huntingford, 1976;Bell, 2005;Dingemanse et al, 2007;Blake and Gabor, 2014;Heinen-Kay et al, 2016;Castellano and Friard, 2021), but this is among the first to explore how specific social experiences shape the development of these traits.…”

Section: Personalitymentioning

confidence: 99%

“…Early social experiences are known to have powerful effects on adult physiology (stress-response, Murthy and Gould, 2018;Laubach et al, 2021) and behavior (e.g., mate preferences, ten Cate et al, 2006), and are expected to be important factors shaping a multitude of adult behaviors (Stamps and Groothuis, 2010a,b;Taborsky, 2016;Cabrera et al, 2021). Researchers have manipulated early-life experience with variation in food availability (Groothuis et al, 2005;Edenbrow and Croft, 2013), immune stress (Butler et al, 2012;DiRienzo et al, 2015), predation (Bell and Sih, 2007;Niemelä et al, 2012;Edenbrow and Croft, 2013;Castellano and Friard, 2021), heterospecific exposure (Delclos et al, 2020), social isolation (Naguib et al, 2011;Liedtke et al, 2015), and physical enrichment (Liedtke et al, 2015;Xu et al, 2021) -all showing that these developmental experiences can shape traits like boldness, activity, aggression, and exploration. These traits are often studied in the context of animal personality [i.e., consistent inter-individual variation in behavior (Bergmüller and Taborsky, 2010;Stamps and Groothuis, 2010a,b)] and behavioral syndromes [i.e., correlated behaviors across time and context (Sih et al, 2004a,b)].…”

Section: Introductionmentioning

confidence: 99%

Complex sexual-social environments produce high boldness and low aggression behavioral syndromes

Queller

Shirali²,

Wallace³

et al. 2022

Front. Ecol. Evol.

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IntroductionEvidence of animal personality and behavioral syndromes is widespread across animals, yet the development of these traits remains poorly understood. Previous research has shown that exposure to predators, heterospecifics, and urbanized environments can influence personality and behavioral syndromes. Yet, to date, the influence of early social experiences with conspecifics on the development of adult behavioral traits is far less known. We use swordtail fish (Xiphophorus nigrensis), a species with three genetically-determined male mating strategies (courtship display, coercion, or mixed strategy) to assess how different early-life social experiences shape adult behavioral development.MethodsWe raised female swordtails from birth to adulthood in density-controlled sexual-social treatments that varied in the presence of the type of male mating tactics (coercers only, displayers only, coercers and displayers, and mixed-strategists only). At adulthood, we tested females’ boldness, shyness, aggression, sociality, and activity.ResultsWe found that the number of different mating strategies females were raised with (social complexity) shaped behavioral development more than any individual mating strategy. Females reared in complex environments with two male mating tactics were bolder, less shy, and less aggressive than females reared with a single male mating tactic (either courtship only or coercion only). Complex sexual-social environments produced females with behavioral syndromes (correlations between aggression and activity, shyness and aggression, and social interaction and activity), whereas simple environments did not.DiscussionImportantly, the characteristics of these socially-induced behavioral syndromes differ from those driven by predation, but converge on characteristics emerging from animals found in urban environments. Our findings suggest that complexity of the sexual-social environment shapes the development of personality and behavioral syndromes to facilitate social information gathering. Furthermore, our research highlights the previously overlooked influence of sexual selection as a significant contributing factor to diverse behavioral development.

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“…Research in various animal taxa has provided inconclusive results when looking at consistency of personality traits across different life stages ( van Berkum et al 1989 ; Monceau et al 2017 ). The few previous studies in amphibians that have tried to track individual tadpoles throughout development, rarely found behavioural traits to be consistent across metamorphosis ( Watkins 1997 ; Brodin et al 2013 ; Castellano and Friard 2021 ). If animals are experiencing major re-organization of their body, including changes in their physiology, instability and/or decoupling of personality traits could be expected ( Stamps 2007 ; Biro and Stamps 2008 ; Careau et al 2008 ; Stamps and Groothuis 2010 ).…”

Section: Repeatabilitymentioning

confidence: 99%

“…The fact that lab-reared animals show generally less repeatability than individuals from wild populations could be due to low variation in environmental conditions during the early development, as breeding facilities typically follow a standardized procedure for animal husbandry. A study using tadpoles of the treefrog Hyla intermedia , demonstrated strong environmental effects on the development of tadpole personality; tadpoles that were reared under different biotic (predation risk) and abiotic (shading) conditions differed considerably in their behaviour at a later time point ( Castellano and Friard 2021 ). Similarly, in agile frog ( Rana dalmatina ) tadpoles reared alone and without predator cues showed no evidence for repeatability or the existence of a behavioural syndrome, while the exposure to cues from predators and/or conspecifics resulted in the development of activity and risk-taking personalities and the existence of a behavioural syndrome ( Urszán et al 2015 ).…”

Section: Repeatabilitymentioning

confidence: 99%

Behavioural consistency across metamorphosis in a neotropical poison frog

Bégué,

Tschirren,

Peignier

et al. 2023

Evol Ecol

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Animals often show consistency in their behavioural repertoire across time and/or contexts that differs from other individuals of the same population, i.e. animal personality. We currently have quite an incomplete understanding of the factors that lead to behavioural traits remaining stable – or becoming decoupled – over an animal’s lifetime. In this study, we investigated the role of metamorphosis in the development of animal personality in a Neotropical poison frog, a species that undergoes drastic morphological and ecological changes during its development. We used lab-reared individuals of the brilliant-thighed poison frog Allobates femoralis to assess if consistent individual differences are already present at the tadpole stage, and if these differences are maintained throughout metamorphosis. We found evidence for two personality traits, exploration and boldness, already present in A. femoralis tadpoles. Despite the drastic changes in morphology, physiology, and habitat in the transition from tadpoles to metamorphs, personality traits persisted throughout metamorphosis, suggesting a physiological and/or genetic basis for the measured behavioural traits. We also found that exploration and boldness related behaviours were correlated with growth speed. Very bold and explorative individuals took fewer days until metamorphosis compared to very shy and non-explorative ones, which is in line with the concept of a Pace-of-Life Syndrome. These findings provide important insights into the proximate mechanisms that generate personality in species with complex life cycles.

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Environmental effects on the ontogenesis of tadpole personality

Cited by 7 publications

References 47 publications

Larval newts from turbid and transparent waterbodies exhibit different morphological and behavioural traits

Larval newts from turbid and transparent waterbodies exhibit different morphological and behavioural traits

Complex sexual-social environments produce high boldness and low aggression behavioral syndromes

Behavioural consistency across metamorphosis in a neotropical poison frog

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