Few studies of wild animal performance account for parasite infections: A systematic review.

Wild animals have parasites. This inconvenient truth has far-reaching implications for biologists measuring animal performance traits: infection with parasites can alter host behaviour and physiology in profound and sometimes counterintuitive ways. Yet, to what extent do studies on wild animals take individual infection status into account? We performed a systematic review across eight scientific journals primarily publishing studies in animal behaviour and physiology over a 5-year period to assess the proportion of studies which acknowledge, treat or control for parasite infection in their study design and/or analyses. We explored whether parasite inclusion differed between studies that are experimental versus observational, conducted in the field vs the laboratory and measured behavioural vs physiological traits. We also investigated the importance of other factors such as the journal, the trait category (e.g. locomotion, reproduction) measured, the vertebrate taxonomic group investigated and the host climatic zone of origin. Our results show that parasite inclusion was generally lacking across recent studies on wild vertebrates. In over 680 filtered papers, we found that only 21.9% acknowledged the potential effects of infections on animal performance in the text, and only 5.1% of studies treated animals for infection (i.e. parasite control) or considered infection status in the statistical analyses (i.e. parasite analysis). Parasite inclusion, control and analysis were higher in laboratory compared to field studies and higher for physiological studies compared to behavioural studies but did not differ among journals, performance trait categories and taxonomic groups. Among climatic zones, parasite inclusion, control and analysis were higher in tropical, subtropical and temperate zones than in boreal and polar zones. Overall, our literature review suggests that parasites are sorely under-acknowledged by researchers in recent years despite growing evidence that infections can modify animal performance. Given the ubiquity of parasites in the environment, we encourage scientists to consider individual infection status when assessing performance of wild animals. We also suggest ways for researchers to implement such practices in both experimental and observational studies.

Increased parasite load is associated with reduced metabolic rates and escape responsiveness in pumpkinseed sunfish.

Wild animals have parasites that can compromise their physiological and/or behavioural performance. Yet, the extent to which parasite load is related to intraspecific variation in performance traits within wild populations remains relatively unexplored. We used pumpkinseed sunfish (Lepomis gibbosus) and their endoparasites as a model system to explore the effects of infection load on host aerobic metabolism and escape performance. Metabolic traits (standard and maximum metabolic rates, aerobic scope) and fast-start escape responses following a simulated aerial attack by a predator (responsiveness, response latency and escape distance) were measured in fish from across a gradient of visible (i.e. trematodes causing black spot disease counted on fish surfaces) and non-visible (i.e. cestodes in fish abdominal cavity counted post-mortem) endoparasite infection. We found that a higher infection load of non-visible endoparasites was related to lower standard and maximum metabolic rates, but not aerobic scope in fish. Non-visible endoparasite infection load was also related to decreased responsiveness of the host to a simulated aerial attack. Visible endoparasites were not related to changes in metabolic traits or fast-start escape responses. Our results suggest that infection with parasites that are inconspicuous to researchers can result in intraspecific variation in physiological and behavioural performance in wild populations, highlighting the need to more explicitly acknowledge and account for the role played by natural infections in studies of wild animal performance.

Social Group Size and Shelter Availability Influence Individual Metabolic Traits in a Social Fish.

Group living is widespread among animal species and yields both costs and benefits. Presence of conspecifics can restrict or enhance the expression of individual behavior, and the recent social environment is thought to affect behavioral responses in later contexts, even when individuals are alone. However, little is known about how social group size influences the expression of individual physiological traits, including metabolic rates. There is some evidence that shoaling can reduce fish metabolic rates but this variable may be affected by habitat conditions such as shelter availability via density-dependent processes. We investigated how social group size and shelter availability influence Eurasian minnow (Phoxinus phoxinus) metabolic rates estimated by respirometry. Respirometry trials were conducted on fish in isolation before and after they were housed for 3 weeks in a social treatment consisting in a specific group size (n = 4 or 8) and shelter availability (presence or absence of plant shelter in the experimental tank). Plant shelter was placed over respirometers for half of the duration of the respirometry trials, allowing estimation of minimum daytime and nighttime metabolic rates in both conditions (in the presence or absence of plant shelter). Standard metabolic rate (SMR), maximum metabolic rate (MMR), and aerobic scope were also estimated over the entire trial. Minimum daytime and nighttime metabolic rates estimated while in presence of plant shelter were lower than when estimated in absence of plant shelter, both before and after individuals were housed in their social treatment. After the social treatment, SMRs were higher for fish that were held in groups of 4 as compared with those of fish held in groups of 8, while MMR showed no difference. Plant shelter availability during the social treatments did not influence SMR or MMR. Our results suggest that social group size may directly influence energy demands of individuals, highlighting the importance of understanding the role of group size on variations in physiological traits associated with energy expenditure.

Pour les animaux sociaux, la vie en groupe est associée à plusieurs coûts et bénéfices. La présence de congénères peut limiter ou amplifier l'expression des comportements individuels. L'environnement social peut également affecter les réponses comportementales ultérieures d'un individu dans d'autres contextes, même lorsqu'il se retrouve seul. Or, les effets de l'environnement social sur l'expression des traits physiologiques individuels, comme les taux métaboliques, sont très peu connus. La vie en banc pourrait réduire les taux métaboliques des poissons. Cela dit, la compétition pour des composantes limitantes de l'habitat comme la présence de refuges pourrait influencer les taux métaboliques individuels. L'objectif de cette étude était de quantifier et de comparer les effets de l'environnement social et de la présence de refuges sur les taux métaboliques des ménés communs Phoxinus phoxinus estimés par respirométrie. Notre design expérimental consistait en une expérience sociale de trois semaines précédée et suivie par des expériences de respirométrie. Durant l'expérience sociale, les poissons étaient gardés en groupes de quatre ou huit poissons dans des aquariums qui contenaient un refuge (plante aquatique) ou non. Durant la respirométrie, les poissons étaient placés en isolation dans des chambres qui étaient couvertes par des plantes aquatiques pour la moitié de la durée des expériences. Ainsi, les taux métaboliques minimum de jour et de nuit, en présence ou en absence de refuge ont été estimés à chaque expérience, en plus des taux métaboliques standard (SMR) et maximum (MMR). Les taux métaboliques minimum de jour et de nuit estimés en présence de refuge étaient moins élevés que ceux estimés en absence de refuge, et ce, autant avant et après l'expérience sociale. Après l'expérience sociale, les SMR étaient plus élevés pour les poissons qui avaient été gardés en groupes de quatre que pour les poissons gardés en groupes de huit, alors qu'aucune différence n'a été observée pour les MMR. La présence de refuge dans les aquariums durant l'expérience sociale n'a pas influencé les taux métaboliques. Nos résultats démontrent que la taille des groupes peut influencer les dépenses énergétiques des individus, ce qui souligne l'importance de comprendre le rôle des dynamiques sociales sur les variations dans les traits métaboliques.

Does shelter influence the metabolic traits of a teleost fish?

Availability of shelter is an important component of habitat selection for animals as it can influence survival (protection against harsh physical conditions and predation) and growth (energy acquisition and expenditure). Few studies address the effect of shelter on metabolic expenditures associated with non-mechanical tasks (excluding station holding or movement). The main goal of this study was to investigate the influence of shelter use on metabolic traits of smallmouth bass (Micropterus dolomieu) from two populations (Kiamika River and Lake Long). Respirometry experiments on smallmouth bass were conducted to measure standard metabolic rate (SMR), resting metabolic rate (RMR), aerobic scope (AS), recovery time (RT) and excess post-exercise oxygen consumption (EPOC) in the presence or absence of shelter. The presence of shelter did not affect most metabolic traits, except for RMR, which was reduced in the presence of shelter for Lake Long fish. The results of this study also show that larger fish had lower SMR in the presence of shelter than when it was absent. When accounting for social hierarchy, there were no differences in most metabolic traits in dominant or subordinate fish in the presence or absence of shelter, except for RT, which was significantly lower in the presence of shelter for dominant fish. These results do not support the existence of an unequivocal relationship between individual metabolic traits and the presence of shelter. If physiological motives may influence the use of shelter, sheltering in itself might not have important consequences on energy expenditures required for non-mechanical tasks.

Divergence in aerobic scope and thermal tolerance is related to local thermal regime in two populations of introduced Nile perch (Lates niloticus).

We tested whether thermal tolerance and aerobic performance differed between two populations of Nile perch (Lates niloticus) originating from the same source population six decades after their introduction into two lakes in the Lake Victoria basin in East Africa. We used short-term acclimation of juvenile fish to a range of temperatures from ambient to +6°C, and performed critical thermal maximum (CTmax ) and respirometry tests to measure upper thermal tolerance, resting and maximum metabolic rates, and aerobic scope (AS). Across acclimation temperatures, Nile perch from the cooler lake (Lake Nabugabo, Uganda) tended to have lower thermal tolerance (i.e., CTmax ) and lower aerobic performance (i.e., AS) than Nile perch from the warmer waters of Lake Victoria (Bugonga region, Uganda). Effects of temperature acclimation were more pronounced in the Lake Victoria population, with the Lake Nabugabo fish showing less thermal plasticity in most metabolic traits. Our results suggest phenotypic divergence in thermal tolerance between these two introduced populations in a direction consistent with an adaptive response to local thermal regimes.

Tropical fish in a warming world: thermal tolerance of Nile perch Lates niloticus (L.) in Lake Nabugabo, Uganda.

Key to predicting the response of fishes to climate change is quantifying how close fish are to their critical thermal limits in nature and their ability to adjust their thermal sensitivity to maintain performance. Here, we evaluated the effects of body size and habitat on aerobic scope (AS) and thermal tolerance of Nile perch Lates niloticus (L.), a fish of great economic and food security importance in East Africa, using respirometry and critical thermal maximum (CTmax) trials. Juvenile Nile perch from distinct habitats (high or low dissolved oxygen concentrations) of Lake Nabugabo, Uganda were exposed for 4.6 ± 0.55 days to a temperature treatment (25.5, 27.5, 29.5 or 31.5°C) prior to experimentation, with the lowest temperature corresponding to the mean annual daytime temperature in Lake Nabugabo and the highest temperature being 3°C higher than the maximal monthly average. As expected, metabolic rates increased with body mass. Although resting metabolic rate increased with temperature, maximal metabolic rate showed no change. Likewise, AS did not vary across treatments. The CTmax increased with acclimation temperature. There was no effect of habitat on maximal metabolic rate, AS or CTmax; however, there was a trend towards a lower resting metabolic rate for Nile perch captured in the low-dissolved oxygen habitat than in well-oxygenated waters. This study shows that juvenile Nile perch maintain a large AS at temperatures near the upper limit of their natural thermal range and provides evidence that Nile perch have physiological mechanisms to deal with acute exposure to thermal stress.