Copyright: © 2014 Michaels et al. This is an open-access article distributed under the terms of the Creative Commons Attribution–NonCommercial–NoDerivs 3.0 Unported Amphibian & Reptile Conservation License, which permits unrestricted use for non-commercial and education purposes only [General Section] 8(1) :7–23. provided the original author and source are credited. The official publication credit source: Amphibian & Reptile Conservation at: amphibian-reptile-conservation.org REVIEW The importance of enrichment for advancing amphibian welfare and conservation goals: A review of a neglected topic 1Christopher J. Michaels , 2J. Roger Downie, and 3Roisin Campbell-Palmer 1,4Preziosi Group, Faculty of Life Sciences, Michael Smith Building, University of Manchester, Manchester, ENGLAND 2School of Life Sciences, Graham Kerr Building, University of Glasgow, Glasgow, SCOTLAND 3Conservation Programmes, The Royal Zoological Society of Scotland, Edinburgh, SCOTLAND Abstract.—Enrichment, broadly the provision of stimuli to improve the welfare of captive animals, is known to be important in husbandry practice and in the success of ex situ conservation and reintroduction programs. Practical evidence of the importance of enrichment exists for a number of taxa, yet amphibians are poorly represented. There is no reason to assume a priori that amphibians would not benefit from enrichment and, given their increasing prominence in captive programs, their requirements in captivity beyond basic husbandry should be the focus of more intense study. We review the existing body of research on enrichment for amphibians, as well as that for fish and reptiles, which may be regarded as behaviorally and neurologically broadly similar to amphibians. We also briefly discuss mechanisms by which enrichment might affect amphibian fitness and, therefore, reintroduction success. Our review supports the contention that there may be important consequences of enrichment for both captive welfare and ex situ conservation success in amphibians and that amphibian enrichment effects may be highly variable taxonomically. In the face of increasing numbers of captive amphibian species and the importance of ex situ populations in ensuring their species level persistence, enrichment for amphibians may be an increasingly important research area. Key words. Behavior, conservation, environmental enrichment, re-introduction, welfare, ex situ, fish, reptiles Citation: Michaels CJ, Downie JR, Campbell-Palmer R. 2014. The importance of enrichment for advancing amphibian welfare and conservation goals: A review of a neglected topic. Amphibian & Reptile Conservation 8(1) [General Section]: 7–23 (e77). Introduction in actual numbers and species held) and their mounting conservation importance, has highlighted the need for A wide range of amphibian species is currently main- a more thorough understanding of amphibian captive tained in captivity. Some species are used as models in husbandry (Gascon et al. 2005), particularly for species laboratory research, including the ubiquitous Xenopus that have no history in captivity and for those that are laevis and the dendrobatid frogs used to study skin pep- intended for release into the wild (Gagliardo et al. 2008; tides (reviewed by Daly 1998) and caecilians used in bio- Gascon et al. 2005). mechanics research (e.g., Summers and O’Reilly 1997) For many other taxa, the importance of enrichment and leaf frogs involved in conservation research (Ogilvy has been identified for not only the welfare, or the physi- et al. 2012a, b). Several species are farmed (in addition cal and psychological wellbeing, of individual animals to the many collected from the wild) for food or other in captivity or those destined for release, but also for products and others are maintained by private individuals the overall/long-term success of reintroduction projects as hobby or pet animals (Gascon et al. 2005). In addition, (Crane and Mathis 2010; Shepherdson et al. 1998; Young the ex situ conservation response to the on-going global 2003). However, the implications of past work on the amphibian extinction crisis (e.g., Gagliardo et al. 2008; value of enrichment schemes for captive species cur- Lee et al. 2006; Norris 2007) has drawn much public- rently has limited scope because enrichment has neither ity to the growing number of amphibians maintained for explicitly used nor well researched in amphibians (de conservation breeding and education in zoos and similar Azevedo et al. 2007; Burghardt 2013). The objective of institutions. This increase in captive amphibians (both this paper is to draw attention to this lack of knowledge Correspondence. Email: [email protected] (Corresponding author). Amphib. Reptile Conserv. | amphibian-reptile-conservation.org (7) June 2014 | Volume 8 | Number 1 | e77 Michaels et al. Table 1. Studies of enrichment in amphibians. Type of enrichment Species Origin Findings Notes Reference investigated No effect on growth rate. Small sample size; Frogs provided with shelter unknown origins Xenopus laevis Unknown Shelter provision Hilken et al. (1995) reluctant to leave it, even and genetics (see when provided with food. Chum et al. 2013) Frogs use any shelter provided, but prefer plastic tubes to plants, rocks and wood. Frogs prefer tanks with Brown and Nixon Xenopus laevis Laboratory bred Shelter provision — shelter to tanks with no shel- (2004) ter. Frogs showed increased activity and reduced panic in tanks with shelter. Provision of plastic tubes reduced aggressive en- Toreilles and Xenopus laevis Laboratory bred Shelter provision — counters, wounds and/or Green (2007) cannibalisation events. No effect on growth rates. Xenopus laevis Laboratory bred Shelter provision — Gouchie et al. (2008) Reluctant to leave shelter. No effect on growth rates or body condition (fat bodies). Xenopus laevis Laboratory bred Shelter provision — Archard (2012) Higher propensity to clump together without shelter. 1. Reduced surface area increased air-breathing behavior Enrichments are 2. Shallow water reduced not ecologically 1. Surface area size growth rates and caused relevant to this spe- Laboratory bred 2. Water depth abnormal floating behavior Calich and Xenopus laevis cies; this work may tadpoles 3. Aquatic partitioning/ (tadpoles could not surface Wassersug (2012) have limited impli- maze to breath properly) cations for captive 3. Tadpoles avoided narrower husbandry passages (2 cm) and preferred wider ones (4 cm) 1. Refuge provision reduced daytime activity and animals used shelter when provided 1. Shelter provision Laboratory bred 2. Addition of conspecific Xenopus laevis 2. Conspecific provision — Archard (2013) females further reduced daytime (always with shelter) activity in increased refuge use. No aggression observed and refuges were shared Environmental com- Improved general welfare Lithobates High density Bang and Mack Farmed/wild-caught plexity (ramps, perches (general aspect and condition catesbeianus laboratory condition (1998) and caves) of animals) Lithobates Reduction in mortality and High density Hedge and Saunders Farmed/wild-caught Shelter provision catesbeianus improvement in condition laboratory condition (2002) Dendrobates Very small sample tinctorius 1. Feeding enrichment 1. Some effects on behavior sizes. Issues with D. azureus (control vs. insect (mainly activity) experimental dispenser vs. D. auratus Zoo bred 2. Effect on activity levels design, includ- Hurme et al. (2003) broadcast feed/aphid D. leucomelas (enclosure switch lead to ing few replicates stem) Mainly reported higher activity levels) and unexplained 2. Enclosure switch as aggregate data measures across species Feeding enrichment Increased foraging duration, (feeding dish control vs. increased duration between Campbell-Palmer Oophaga pumilio Zoo bred feeding dish with leaf — prey capture events and et al. (2006) cover to allow insects to reduced rapid feeding disperse) Amphib. Reptile Conserv. | amphibian-reptile-conservation.org (8) June 2014 | Volume 8 | Number 1 | e77 Enrichment for amphibians Table 1. Studies of enrichment in amphibians (continued). Type of enrichment Species Origin Findings Notes Reference investigated 1. Strong, positive effect on growth rates. No effect on Mannophryne Wild collected as behavior (weak effect on trinitatis tadpoles time spent jumping) 2. Preferred shallow water Substrate prefer- 1. Shelter provision Walsh and Downie ence predicted by Physalaemus 2. Substrate type (2005) 1. No/weak effect on growth habitat pustulosus or behavior Wild collected as 2. Preferred dig-able (sand or spawn Leptodactylus gravel) substrate fuscus Frogs prefer planted to non-planted enclosures. This preference increases when animals are deprived of plants before choice test. Agalychnis Laboratory bred Froglets reared with plants Michaels et al. Shelter provision — callidryas juveniles and adults grow faster and are in better (2014b) condition than those reared without. Frogs reared with plants have more diverse and more abundant cutaneous bacterial communities. Hellbenders were able to learn to exhibit a fright Wild collected as Cryptobranchus Pre-release anti-preda- response to trout scent after Crane and Mathis eggs (head-starting — alleganiensis tor training classical conditioning; control (2010) program) animals showed no such improvement. and to call for more research in order to better understand iors or behavioral repertoires (Shepherdson 1994). Social the importance of enrichment for this taxon. We will ex- enrichment, the provision of