Does environmental enrichment promote recovery from stress in rainbow trout?

Highlights

• We investigated how habitat enrichment may promote welfare of captive rainbow trout.

• Environmental enrichment promotes recovery following stressful treatments.

• Habitat enrichment may not affect the magnitude of inter-individual variation.

• Painful stimulus appeared to override benefits provided by enrichment.

• Enrichment should be implemented in experimental studies using rainbow trout.

Abstract

The EU Directive on animal experimentation suggests that all protected animals should have enrichment to improve welfare yet relatively little research has been conducted on the impact of enrichment in fish. Studies employing enrichment in zebrafish have been contradictory and all fish species should be provided with species-specific enrichments relevant to their ecology. Salmonids are important experimental models in studies within aquaculture, toxicology and natural ecosystems. This study therefore sought to establish whether an enriched environment in an experimental aquarium may promote improved welfare in rainbow trout (Oncorhynchus mykiss) by enhancing their recovery from invasive procedures. Trout were held individually in either barren (no tank ornamentation) or enriched (gravel, plants and an area of cover) conditions. Recovery rates after a noxious stimulus and a standard stressor were investigated by monitoring behaviour, opercular beat rate and plasma cortisol concentrations. Fish were randomly assigned to one of four treatment groups: Control (undisturbed), Sham (handled but not manipulated), Stress (air emersion) and Pain (subcutaneous injection of acetic acid). The results suggest that for rainbow trout environmental enrichment appears to promote recovery and ameliorate adverse effects following a stressor. However, recovery rate did not differ between environments in the pain treatment groups. Thus environmental enrichment may not be an important factor when the fish is responding to a painful stimulus. These results have important implications for the husbandry and welfare of captive rainbow trout and possibly other salmonids and suggest that enriched environments may be preferable to barren environments in experimental studies.

Introduction

There is a plethora of evidence supporting the benefits of enrichment for animals held in captivity, particularly mammals (Simpson and Kelly, 2011, Singhal et al., 2014). However, evidence for the benefits or otherwise of enriched environments for fish is lacking. Fish are a widely exploited research model, second only to mice in numbers used (UK Home Office, 2013), but more importantly they also constitute a major source of protein with an estimated two million tonnes of farmed fish being produced across Europe annually (FEAP, 2014). Globally, aquaculture is a growing industry and this growth is inevitably accompanied by concerns about the welfare of intensively-farmed fish employed in research aimed at resolving production problems.

Natural environments are more heterogeneous than those found in captivity and this disparity may result in stress or impaired cognitive function among captive animals with obvious implications for welfare (e.g. Kellison et al., 2000, Brown and Day, 2002, Huntingford, 2004, Sundstrom et al., 2004, Araki et al., 2008). For animals kept in captivity the EU directive on the protection of animals used for scientific purposes (EU Directive, 2010) recommends, although does not enforce, that captive-held fish should be kept in enriched conditions. However, despite this recommendation, relatively little is known about the benefits of enrichment for captive fish and what is required to maintain a high standard of welfare. In captivity for example the habitat often remains non-enriched (from this point onward referred to as barren) with no heterogeneity, for ease of cleaning, removal and transfer of fish, reduction of the spread of disease etc. Whilst there are many different definitions of environmental enrichment, the same general concept applies: increasing environmental complexity within an animal's surroundings that is in some way beneficial to not only maintaining but also improving general animal welfare. Enrichment can be further categorised into areas that target the different aspects of an animal's life; social, diet, cognitive, sensory, and physical (Näslund and Johnsson, 2014).

The results of research on environmental enrichment in fish are contradictory and highlight the extensive variation between and even within species. As reviewed in Näslund and Johnsson (2014), there are several studies demonstrating the positive effects of environmental enrichment on welfare across many fish species. Compared with captive-held fish in barren environments, those provided with some form of enrichment have been found to have increased brain development (Marchetti and Nevitt, 2003, Kihslinger and Nevitt, 2006, von Krogh et al., 2010, Salvanes et al., 2013), reduced impact from stressors (Braithwaite and Salvanes, 2005, Naslund et al., 2013, Batzina et al., 2014), improved foraging ability (Brown et al., 2003, Strand et al., 2010, Rodewald et al., 2011), improved post-release survival (D'Anna et al., 2012) and positive effects on growth (Leon, 1975, Hansen and Moller, 1985, Batzina et al., 2014). This general increase in neural plasticity results in the development of behaviourally flexible fish that are better at coping with a variety of situations. Although it must be noted that there are also studies demonstrating negative and neutral associations of environmental enrichment (See Näslund and Johnsson, 2014).

As a consequence of the diversity in natural histories exhibited in fish, as well as the wide range of both physiological and behavioural traits, it is likely that the ideal enrichment will have to be judged on a species by species and possibly even on a life stage basis. Here we examine the rainbow trout (Oncorhynchus mykiss), a commercially important salmonid with more than 380,000 t (FEAP, 2014) being produced annually through aquaculture in Europe and as such this species is also widely used in scientific research (Thorgaard et al., 2002) but there remains a paucity of information on enrichment in captivity in this species.

If a lack of environmental enrichment affects fish behaviour, physiology or welfare then this would undoubtedly be a confounding factor when interpreting experimental results and might lead to erroneous conclusions from experiments (Williams et al., 2009, Killen et al., 2013). In laboratory rodent studies, enrichment can improve the health and welfare of the test subjects but may also reduce individual variation such that the data sets are more robust and scientifically valid (Singhal et al., 2014). The present study was conducted to investigate the effects of simple environmental enrichment on (i) the recovery of rainbow trout from stressors and invasive procedures, and (ii) the degree of inter-individual variability among the data collected.