The endangered brain: actively preserving ex-situ animal behaviour and cognition will benefit in-situ conservation

Review The endangered brain: actively preserving ex-situ animal behaviour and cognition will benefit in-situ conservation

Endangered species have small, unsustainable population sizes that are geographically or genetically restricted. Ex-situ conservation programmes are therefore faced with the challenge of breeding sufficiently sized, genetically diverse populations earmarked for reintroduction that have the behavioural skills to survive and breed in the wild. Yet, maintaining historically beneficial behaviours may be insufficient, as research continues to suggest that certain cognitive-behavioural skills and flexibility are necessary to cope with human-induced rapid environmental change. This paper begins by reviewing interdisciplinary studies on the 'captivity effect' in laboratory, farmed, domesticated and feral vertebrates and finds that captivity imposes rapid yet often reversible changes to the brain, cognition and behaviour. However, research on this effect in ex-situ conservation sites is lacking. This paper reveals an apparent mismatch between ex-situ enrichment aims and the cognitive-behavioural skills possessed by animals currently coping with human-induced rapid environmental change. After synthesizing literature across neuroscience, behavioural biology, comparative cognition and field conservation, it seems that ex-situ endangered species deemed for reintroduction may have better chances of coping with human-induced rapid environmental change if their natural cognition and behavioural repertoires are actively preserved. Evaluating the effects of environmental challenges rather than captivity per se is recommended, in addition to using targeted cognitive enrichment.

One. Introduction

We are currently experiencing the planet's sixth mass extinction. The United Nations established twenty 'AICHI' biodiversity targets in twenty ten to address and mitigate rapid biodiversity loss across the globe; we failed to meet most targets by twenty twenty including the target to prevent species extinction. As this environmental crisis intensifies, conservation programmes are under increasing pressure to justify actions to governments, funders, the public and other stakeholders. Among the most scrutinized conservation actions is ex-situ conservation.

The International Union for Conservation of Nature classifies species by their level of risk of extinction, and these classifications are used globally for species conservation. Vulnerable, endangered and critically endangered species are considered to be threatened with extinction. These threatened categories have criteria describing the species' population size and geographical range. Currently, around twenty percent of all assessed vertebrates are threatened with extinction, and conservation breeding programmes are a growing strategy to halt extinction. In line with International Union for Conservation of Nature categorization, ex-situ conservation programmes have focused on maximizing the total numbers, and genetic diversity, of individuals bred in ex-situ sites, via species survival plans. Ex-situ sites are therefore commonly referred to as metaphorical arks or safety nets against extinction.

However, the physical body of an animal is not the only thing at risk of extinction; animal cognition and behaviour, and the neural substrates underlying them, are also at risk (at least of permanent maladaptive change). Yet this 'endangered brain' concept is a paradox. Conservation breeding aims to produce individuals that survive and reproduce, but living in captivity can significantly hinder the development and expression of cognitive and behavioural skills required for survival, therefore putting the species at further risk of extinction. This paper reviews evidence that captivity is linked to cognitive or behavioural loss or modification, and that certain changes can detrimentally impact animal survival. Most evidence for the captivity effect comes from laboratory and farmed animals, in addition to a handful of historical zoo specimens (particularly carnivores) with no accompanying cognitive or behavioural records. This is concerning, given that approximately fifteen percent of threatened species are housed in zoos. Furthermore, cognition rarely features in conservation action plans.

A recently published review of phenotypic effects of captivity gave significantly more focus to physical and physiological health than cognition. To address this gap in the literature, the current paper focuses primarily on what we know about the vertebrate brain in a captive state, synthesizing across multiple disciplines: neuroscience, sensory biology, behavioural biology and comparative cognition. It then considers the vertebrate brain in its wild state under human-induced rapid environmental change, before considering the challenged brain, i.e. the extent to which enrichment has been used in ex-situ sites for reintroduction purposes, and more widely in captivity. Finally, we propose a new framework to evaluate environments by the level of challenge they provide, rather than a captive or wild dichotomy or placing laboratories, farms, zoos, etc. into artificial siloes.

This paper does not evaluate the ethics or success of the existing practice of conservation breeding. Instead, readers should refer to a number of comprehensive reviews spanning the last five decades including high-profile success stories such as the Przewalski's horse and black-footed ferret. Furthermore, the paper does not address how the in-situ geographical ranges or genetic pools of various species became threatened in the first place, in other words, we do not review the causes of human-induced rapid environmental change. Species conservation has always been a holistic venture with practitioners working collaboratively in-situ and ex-situ. So, the focus of this paper is to question whether individuals housed in ex-situ programmes have the mental and behavioural tools necessary for ongoing survival, a topic that has been relatively overshadowed by other collaborative efforts.