Small Variations in Early-Life Environment Can Affect Coping Behaviour in Response to Foraging Challenge in the Three-Spined Stickleback.

M Rohaa Langenhof,Rienk Apperloo,Jan Komdeur,Cheryl S Rosenfeld

doi:10.1371/journal.pone.0147000

Abstract

ContextAn increasing concern in the face of human expansion throughout natural habitats is whether animal populations can respond adaptively when confronted with challenges like environmental change and novelty. Behavioural flexibility is an important factor in estimating the adaptive potential of both individuals and populations, and predicting the degree to which they can cope with change.Study DesignThis study on the three-spined stickleback (Gasterosteus aculeatus) is an empiric illustration of the degree of behavioural variation that can emerge between semi-natural systems within only a single generation. Wild-caught adult sticklebacks (P, N = 400) were randomly distributed in equal densities over 20 standardized semi-natural environments (ponds), and one year later offspring (F1, N = 652) were presented with repeated behavioural assays. Individuals were challenged to reach a food source through a novel transparent obstacle, during which exploration, activity, foraging, sociability and wall-biting behaviours were recorded through video observation. We found that coping responses of individuals from the first generation to this unfamiliar foraging challenge were related to even relatively small, naturally diversified variation in developmental environment. All measured behaviours were correlated with each other. Especially exploration, sociability and wall-biting were found to differ significantly between ponds. These differences could not be explained by stickleback density or the turbidity of the water.FindingsOur findings show that a) differences in early-life environment appear to affect stickleback feeding behaviour later in life; b) this is the case even when the environmental differences are only small, within natural parameters and diversified gradually; and c) effects are present despite semi-natural conditions that fluctuate during the year. Therefore, in behaviourally plastic animals like the stickleback, the adaptive response to human-induced habitat disturbance may occur rapidly (within one generation) and vary strongly based on the system’s (starting) conditions. This has important implications for the variability in animal behaviour, which may be much larger than expected from studying laboratory systems, as well as for the validity of predictions of population responses to change.

Highlights

Animals are very sensitive to their environment [1]
A total of 400 adults (P) were caught overnight with minnow traps for three consecutive days and transported to the Netherlands by car. Upon arrival they were randomly distributed in equal densities over 20 small, semi-natural ponds at the University of Groningen. In each of these ponds, offspring (F1) were born and naturally reared by their fathers, where they lived with 40–85 conspecifics depending on the breeding success of the 20 initial wild-caught sticklebacks placed in each pond
The differences we found across ponds in the time it took sticklebacks to manoeuvre through the obstacle, in the amount of conspecifics they surrounded themselves with, and the amount of stress-related behaviour they showed, indicate that the early-life environment these sticklebacks experienced did–at least in some of the ponds–affect their ability to handle the humaninduced disturbance of their feeding routine

Summary

Introduction

Animals are very sensitive to their environment [1]. For example, most animals are keenly aware of changes in daylight [2], temperature [3], and social dynamics within their population [4]. Sensitivity to the surrounding world confers great evolutionary advantages, as many aspects of population structure and species ecology are constrained by the environment [5]. In addition to being affected by their current surroundings, animals are often influenced by the circumstances they experienced during or shortly after birth. This phenomenon is commonly referred to as developmental plasticity [9]. The habitat that animals experience in their early life has a strong influence on both their physiological development, such as growth rate and the development of physical traits [10], and their behavioural development, such as the strategies they deploy later in life [9,11]. The importance of the early-life environment to the development of many aspects of adult functioning, but even on evolutionary processes themselves, has recently become more recognised [18]

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