Enrichment for Laboratory Zebrafish—A Review of the Evidence and the Challenges
Abstract
:Simple Summary
Abstract
1. Introduction
2. Defining and Evaluating Environmental Enrichment
2.1. Social Enrichment
2.2. Physical Enrichment
2.3. Nutritional Enrichment
2.4. Occupational Enrichment
2.5. Sensory Enrichment
3. Considerations for Implementing Further Zebrafish Enrichment
4. Discussion
- Plastic plants may be beneficial enrichment if fish need to be isolated for short periods [47].
- Although the welfare benefits of live food have not been empirically demonstrated, plenty of anecdotal evidence suggests that it is beneficial to welfare.
- Although it is highly unlikely that there are any zebrafish facilities which house zebrafish individually as part of their normal practices, the importance of social contact for zebrafish must be emphasised. As facilities may need to house zebrafish individually for short time periods (e.g., after genotyping), more research is needed to establish how provision of visual and olfactory contact between fish will improve welfare.
- How do modifications which do not involve adding items or objects into the tank (images on tank walls, visual contact with conspecifics, tank colour) impact zebrafish welfare?
- Is the provision of live food ‘enriching’?
- Do dawn and dusk phases in facility lighting cycles affect zebrafish behaviour and welfare?
- Which kinds of physical structures have the most impact on zebrafish welfare? Is there an additive effect of different forms of physical structure?
- Are there forms of enrichment which only confer a welfare benefit when provided in combination or certain contexts? For example, might water flow need to be provided in the presence of physical structures to be enriching?
- How does shoal size or stocking density influence the response of zebrafish to physical structures? Can aggression be reduced by providing a higher number of physical structures relative to the number of fish?
Funding
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
References
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Study | Enrichment | Indicator(s) | Effect(s) |
---|---|---|---|
[45] | Presence of other zebrafish | Time spent near stimulus shoal | ↑ |
[46] | Presence of other zebrafish | Distance between members of experimental shoal when mixed wth stimulus shoal (higher distances indicate greater mixing of experimental and stimulus shoals and therefore stronger preference) | ↑ |
[47] | Presence of other zebrafish | Entries to compartment near stimulus shoal | ↑ for fish previously housed in groups or singly in barren tanks. No effect for experimental fish housed singly with an artificial plant. |
Time spent in compartment near stimulus shoal | ↑ for fish previously housed in groups or singly in barren tanks. No effect for experimental fish housed singly with an artificial plant. | ||
[48] | Presence of other zebrafish | Proportion of scan samples in which fish were near to stimulus fish or stimulus shoal | ↑ |
[49] | Choice between shoals | Time spent near larger shoal | ↑ |
[50] | Choice between shoals | Time spent near stimulus shoal | Males: preferred females over males, no preference between a mixed shoal and either a male or female shoal. No preference relating to shoal size. Females: no preferences relating to shoal composition. Preferred larger shoals over smaller shoals. |
[51] | Choice between shoals | Time spent near stimulus shoal | Males: preferred groups of 3 males over single males; preferred single females to groups of 3 females. Females: preferred larger shoals regardless of the sex. |
[53] | Presence of other zebrafish | Cortisol | ↓ |
[54] | Presence of other zebrafish | Cortisol | ↓ in grouped compared with paired zebrafish No effect between grouped and individual zebrafish |
Anxiety | ↓ | ||
Rate of recovery of normal behaviour after stressor | ↑ | ||
[55] | Presence of other zebrafish | Anxiety | ↓ |
[56] | Presence of other zebrafish | Anxiety | ↑ |
Serotonin | ↑ | ||
5HIAA | No effect | ||
Dopamine | No effect | ||
DOPAC | No effect | ||
[57] | Presence of other zebrafish (exposure to stimulus shoal after isolation) | Cortisol | ↑ |
Anxiety | No effect | ||
Serotonin | ↑ | ||
5HIAA | ↓ | ||
Dopamine | ↓ | ||
DOPAC | ↓ | ||
[58] | Presence of other zebrafish | Anxiety | ↑ |
Cortisol | ↑ | ||
[59] | Presence of other zebrafish | Cortisol (resting) | No effect |
Cortisol (after chasing with a net) | ↑ | ||
Cortisol (after predator exposure) | ↓ | ||
[60] | Presence of other zebrafish | Cortisol (resting) | No effect |
Cortisol (after chasing with a net) | ↑ | ||
[61] | Presence of other zebrafish | Cortisol (in fish raised in isolation) | No effect |
Cortisol (in group-raised fish after isolation) | ↓ | ||
Neurogenesis | ↑ | ||
[62] | Presence of other zebrafish | Latency to feed | ↓ |
Neophobia | ↓ | ||
[63] | Presence of other zebrafish | Cortisol (after chasing with a net) | ↑ |
Cortisol (after being moved to novel tank) | ↑ | ||
[71] | Housing in sexually segregated groups (as opposed to mixed-sex groups) | Fecundity | ↑ |
Egg viability | ↑ | ||
[72] | Housing in sexually segregated groups (as opposed to mixed-sex groups) | Weight | ↑ |
Cortisol | ↓ | ||
Inhibitory avoidance | ↑ | ||
Activity in open tank test | No effect |
Study | Enrichment | Indicator(s) | Effect(s) |
---|---|---|---|
[82] | Gravel vs. barren | Preference (occupancy in enriched compartment) | Preference for gravel |
Sand vs. barren | Preference for sand | ||
Gravel vs. sand | Preference for gravel | ||
Submerged plant vs. barren | Preference for submerged plant | ||
Floating plant vs. barren | Preference for floating plant | ||
Floating plant vs. submerged plant | Preference for floating plant | ||
Gravel & floating plant vs. sand and submerged plant | Preference for gravel & floating plant | ||
Gravel and submerged plant vs. sand and floating plant | Preference for gravel & submerged plant | ||
Gravel image vs. barren | Preference for gravel image | ||
Sand image vs. barren | Preference for sand image | ||
Air stone vs. barren | Preference for barren | ||
[83] | Real plants (Ceratopteris thalictroides) and clay pots | Preference (occupancy in enriched compartment) | Preference |
Behavioural diversity | No effect | ||
[84] | Sandy substrate and variety of plastic plants | Preference (occupancy in enriched compartment) | Preference; greater preference when combined with water flow |
[85] | Black tank walls vs. barren | Preference (occupancy in enriched compartments) | No preference |
Underwater image on walls vs. barren | No preference | ||
Sloped gravel vs. barren | Preference for gravel | ||
Flat gravel vs. barren | Preference for gravel | ||
Gravel vs. plastic plants | Preference for gravel | ||
Gravel & plastic plants vs. gravel or plastic plants | Preference for gravel & plastic plants over gravel or plastic plants alone | ||
Number of plastic plants | Preference for greater number of plants | ||
Visual contact with neighbouring tanks | No preference | ||
[86] | Plastic plants and PVC pipes | Preference (occupancy in enriched compartment) | Preference |
[89] | Gravel, real plants (vallis, Vallisneria spp. Including V. spiralis, V. elongata and V. tortifolia, and water trumpet, Cryptocoryne wendtii) | Preference (occupancy in enriched compartment) | No preference |
Anxiety | ↓ | ||
Survival at 30 dpf | ↑ | ||
Body size at 60 dpf | ↓ (but no effect at 120 dpf) | ||
[81] | Shade vs. barren | Preference (occupancy in enriched compartment) | Preference for barren |
Artificial plants vs. barren | No effect | ||
Shade vs. artificial plants | No effect | ||
[90] | Cover | Preference (occupancy in enriched area) | Preference |
Artificial plants | No preference | ||
[60] | Sand and gravel, caps for refuge and natural plants (two branches of Cabombaceae and Pontederiaceae) | Cortisol (after chasing with a net) | ↓ |
[91] | Gravel, plastic ‘ruin’, three submerged plastic plants (two 10 cm tall and one 20 cm tall) | Anxiety (unstressed fish) | ↑ |
Anxiety (after exposure to unpredictable chronic stress) | ↓ | ||
Cortisol (unstressed fish) | No effect | ||
Cortisol (after exposure to unpredictable chronic stress) | ↓ | ||
Levels of reactive oxygen species (unstressed fish) | No effect | ||
Levels of reactive oxygen species (after exposure to unpredictable chronic stress) | ↓ | ||
[92] | Gravel and two 20 cm tall Acorus spp. plastic imitations | Activity | ↓ |
Cortisol | ↑ (but not as high as in fish exposed to a stressor) | ||
Proliferating cell nuclear antigen-expressing cells in the telencephalon | ↑ | ||
[94] | Floating plastic plant | Aggression-induced morbidity and mortality | ↓ |
Cortisol | ↑ (after 5 days); ↓ (after 10 days) | ||
[95] | Sand, plants, artificial rock formation | Anxiety | ↓ |
Exploratory behaviour | ↑ | ||
Inhibitory avoidance | ↓ | ||
Telencephalic expression of genes related to stress response | ↓ | ||
[47] | One artificial plant | Anxiety | ↓ (when combined with presence of other fish) |
[96] | Two plastic plants, one plastic shelter, gravel substrate and a novel object (white PVC pipe, rock, different coloured plants or a plastic bottle—changed weekly). | Anxiety | ↓ |
Learning | ↑ | ||
Brain size | ↑ | ||
[99] | 50 haphazardly placed 50 mm lengths of artificial Elodea canadensis | Body length | ↓ |
Rate of learning | ↑ | ||
[100] | Artificial plants | Initial time to solve maze task | ↓ |
Rate of learning | ↑ | ||
Memory retention | ↑ | ||
[103] | Plastic grass or plastic leaves | Number of eggs | ↑ with plastic grass; no effect with plastic leaves |
Number of fry (6 dpf) | ↑ with grass when parents were 110 or 160 dpf; ↑ with leaves when parents were 173 or 180 dpf | ||
Survivability of fry (6 dpf) | No effect | ||
[104] | Gravel, plastic ‘ruin’, three submerged plastic plants (two 10 cm tall and one 20 cm tall) | Levels of reactive oxygen species in response to unpredictable chronic stress | ↓ |
[105] | Four or five submerged plastic plants | Aggression | ↑ |
Latency to feed | ↓ (one wild strain only) | ||
Shoaling distances | No effect | ||
[35] | One artificial plant, one upturned flower pot and aquarium backing with blue seascape design on rear tank wall | Aggression | ↑ |
Body length | ↓ | ||
Fertilisation success | No effect | ||
Number of eggs | No effect | ||
[34] | Three groups of 12 opaque black glass rods, 50 mm, 100 mm and 180 mm in height | Time for aggression levels to settle. | ↑ |
Activity | No effect | ||
Cortisol | No effect | ||
Shoaling density | No effect | ||
Space use | No effect | ||
[106] | 12 strips of plastic bag in a 3 × 4 arrangement to simulate vegetation | Aggression | ↓ |
Food monopolisation | ↓ | ||
[107] | Three artificial plants (15.24 cm tall, moneywort imitations) and aquarium gravel | Aggression | ↓ |
Fecundity | No effect | ||
[108] | Refuge created by partial wall | Aggression induced by exposure to lead | ↓ |
Study | Enrichment | Indicator(s) | Effect(s) |
---|---|---|---|
[118] | Water flow (forced swimming training) | Survival due to chronic training | ↓ |
Oxygen consumption during swimming | ↓ | ||
Survival when exposed to hypoxia | ↑ | ||
[119] | Water flow (forced swimming training) | Skeletal muscle mass | ↑ |
[120] | Water flow (forced swimming training) | Bone-forming osteoblasts | ↑ |
Bone volume | ↑ | ||
Bone mineralisation | ↑ | ||
[84] | Optional access to water flow | Preference (occupancy in enriched compartment) | Aversion to flow only; preference for flow when combined with physical enrichment (see above) |
[105] | Housed with water flow | Aggression | ↑ |
Latency to feed | No effect | ||
Shoaling distances | No effect | ||
[121] | Water flow (forced swimming training) | Learning | ↑ |
[122] | Water flow (forced swimming training) | Anxiety | ↓ |
[98] | Novel area in structurally enriched tank (sloped gravel substrate, rocks and five artificial plants) (NB: structural enrichment was present in both the main and novel sections of the tank) | Agonistic behaviours | ↓ |
Shoal cohesion and coordination | ↑ |
Study | Enrichment | Indicator(s) | Effect(s) |
---|---|---|---|
[35] | Aquarium backing with blue seascape design on rear tank wall | Aggression | No effect |
Body length | No effect | ||
Fertilisation success | No effect | ||
Egg production | ↑ | ||
[126] | Green, blue, yellow or red walls of tank | Preference (occupancy in enriched compartment) | Preference for green and blue over red and yellow. |
[133] | Green, blue, yellow or red walls of tank | Preference (occupancy in enriched compartment) | Equal preference for red and green over yellow; aversion to blue |
[128] | Green, red or blue doors in tank | Preference (choice of coloured door) | Preferred red over green; green over blue |
[129] | Transparent, black, white, yellow, red or blue tanks | Anxiety | ↓ in blue or black tanks compared with white or transparent tanks |
Cortisol | ↓ in blue tanks compared with white tanks | ||
[131] | Classical music (Vivaldi) | Anxiety | ↓ |
Cortisol | No effect | ||
[132] | Water current intended to provide tactile stimulation | Fear response after exposure to alarm cue | ↓ |
Cortisol | ↓ | ||
Recovery of normal behaviour after exposure to alarm cue | ↑ | ||
[82] | Airstone creating bubbles in water | Preference (occupancy in enriched compartment) | Preference for barren |
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Stevens, C.H.; Reed, B.T.; Hawkins, P. Enrichment for Laboratory Zebrafish—A Review of the Evidence and the Challenges. Animals 2021, 11, 698. https://doi.org/10.3390/ani11030698
Stevens CH, Reed BT, Hawkins P. Enrichment for Laboratory Zebrafish—A Review of the Evidence and the Challenges. Animals. 2021; 11(3):698. https://doi.org/10.3390/ani11030698
Chicago/Turabian StyleStevens, Chloe H., Barney T. Reed, and Penny Hawkins. 2021. "Enrichment for Laboratory Zebrafish—A Review of the Evidence and the Challenges" Animals 11, no. 3: 698. https://doi.org/10.3390/ani11030698