bioRxiv Science⌕ Search

Biology subjects

Binning, S. A.

Publications and source records attributed to Binning, S. A..

8 recordsLinked to original sources

Alterations to cellular metabolism are linked to multiple natural parasite infections across populations of a freshwater fish

Exposure to environmental stressors can induce physiological responses in organisms, which can lead to population-level differences in physiological traits. However, the mechanisms underlying these responses both within individuals and among populations are often unknown. Parasite infections, in particular, are important biotic stressors that can induce a range of effects in hosts, including altered whole-organism metabolism. However, few studies have explored sub-cellular alterations to metabolic performance across both an individual infection gradient and population-level differences in infection prevalence. We compared mitochondrial enzyme activities across five distinct populations of pumpkinseed sunfish (Lepomis gibbosus) differing in the prevalence of cestode and trematode parasites. Overall, we found that enzymes from the OXPHOS pathway (cytochrome c oxidase, NADH dehydrogenase and coenzyme Q : cytochrome c oxidoreductase), the anaerobic pathway (lactate dehydrogenase), the TCA cycle (citrate synthase) and lipid metabolism (carnitine palmitoyl transferase) were positively correlated with parasite density with trends depending on the organ, parasite species and host population studied. Our results suggest complex and nuanced relationships among infections and host physiological performance and provide strong evidence of parasite-induced alterations to mitochondrial metabolism which may explain previously reported whole-organism responses to infections.

ecology↗

Evaluation of parasitic contamination and effects on estimates of mitochondrial enzymatic activities in infected fish livers

Parasites can impair host performance through various physiological processes, including alterations to host metabolism. Since mitochondria are responsible for cellular energy production, it is likely that disruptions in host cellular metabolism contribute to changes in metabolism at the organismal level. However, some studies investigating parasite-induced alteration in cellular metabolism have not taken the presence of parasites in the target tissues into account, potentially biasing results. It is therefore critical to confirm that the measured enzyme activities reflect those of the hosts rather than the parasites themselves. Here, we tested a parasite extraction protocol to evaluate the extent to which parasite contamination impacts estimates of cellular enzyme activities in hepatic tissues of wild pumpkinseed sunfish (Lepomis gibbosus) infected with bass tapeworm cestodes (Proteocephalus ambloplitis). We tested four treatments: uninfected livers, cleaned infected livers, infected livers (repopulated) and parasites alone. We then compared the activity of key metabolic enzymes among groups. PCR tests were used to assess parasitic contamination of samples after applying the parasite extraction protocol on hepatic tissue. Enzyme activities of cleaned livers and contaminated livers were similar despite PCR tests revealing contamination. The intensity of cestode infection also did not influence enzyme activity, which suggests that parasite presence in liver tissues does not impact the accuracy of the enzyme activity estimates. These results suggest that studying the organs of heavily parasitized individuals is possible. Nevertheless, we recommend that our cleaning protocol is applied to infected organs to avoid any perception of biases in highly infected individuals.

ecology↗

Perceived and observed biases within scientific communities: a case study in movement ecology

Who conducts biological research, where, and how the results are disseminated varies among geographies and identities. Identifying and documenting these forms of bias by research communities is a critical first step towards addressing them. We documented perceived and observed biases in movement ecology. Movement ecology is a rapidly expanding sub-discipline of biology, which is strongly underpinned by fieldwork and technology use. First, we surveyed attendees of an international conference, and discussed the results at the conference (comparing uninformed vs informed perceived bias). Although most researchers identified as bias-aware, only a subset of biases were discussed in conversation. Next, by considering author affiliations from publications in the journal Movement Ecology, we found among-country discrepancies between the country of the authors affiliation and study site location related to national economics. At the within-country scale, we found that race-gender identities of postgraduate biology researchers in the USA differed from national demographics. We discuss the role of potential specific causes for the emergence of bias in the sub-discipline, e.g. parachute-science or accessibility to fieldwork. Undertaking data-driven analysis of bias within research sub-disciplines can help identify specific barriers and first steps towards the inclusion of a greater diversity of participants in the scientific process.

ecology↗

Acclimation temperature and parasite infection drive metabolic changes in a freshwater fish at different biological scales

O_LIEnvironmental stressors such as elevated temperature and parasite infection can impact individual energy metabolism. However, organismal responses to co-occurring stressors and their effects across biological scales remain unexplored despite the importance of integrative studies for accurately predicting the resilience of natural populations in changing environments. C_LIO_LIUsing wild-caught, naturally parasitized pumpkinseed sunfish, Lepomis gibbosus, we quantified changes in cellular and whole-organism metabolism in response to temperature and parasite infection. We acclimated pumpkinseeds for three weeks at 20{degrees}C, 25{degrees}C, or 30{degrees}C before measuring whole-organism oxygen uptake ([M]O2) using intermittent flow-respirometry to quantify maximal and standard metabolic rates (MMR and SMR, respectively) and aerobic scope (AS). We also measured the maximal activity of enzymes (citrate synthase (CS), respiratory complexes I + III and IV of the electron transport system, and lactate dehydrogenase (LDH)) linked with cellular bioenergetics in fish heart, brain, spleen and gills using spectrophotometry. C_LIO_LIWe found no interactions between acclimation temperatures and parasite intensity on cellular or whole-organism metabolism. However, both stressors were independently related to fish metabolism, with differing impacts across biological scales. C_LIO_LIWhereas MMR increased with acclimation temperature, this was not mirrored by increasing SMR or decreasing AS, suggesting thermal compensation across acclimation temperatures at the whole-organism level. C_LIO_LIOn a cellular level, acclimation responses were similar across organs, with maximal activity of all enzymes decreasing with increasing acclimation temperature. However, LDH activity remained higher than aerobic enzyme activities (CS, ETS complexes I + III and IV) across acclimation temperatures and organs, especially in gills, where LDH activity drastically increased at 30{degrees}C. This may indicate a stronger reliance on anaerobic metabolism to sustain whole-organism metabolic performance. C_LIO_LIFish with greater trematode infection had lower MMR and AS. There were no relationships between parasite intensity and SMR nor maximal enzyme activity. C_LIO_LIOur work shows that co-occurring stressors have distinct impacts on fish metabolism: parasites are primarily related to whole-organism metabolism while temperature impacts metabolism across biological scales. This highlights that interactions among co-occurring stressors are important for ecological realism and accurate predictions regarding population resilience to environmental changes. C_LI

physiology↗

The importance of visual and chemical cues in infection detection and avoidance in a freshwater fish

The characteristics of infected animals, including their smell, appearance, behaviour or sound, can greatly differ from those of uninfected conspecifics. These differences can serve as cues to recognize and avoid infected individuals to minimize the risk of infection. Avoidance of infected conspecifics is a risk-sensitive behaviour that can be influenced by various factors such as sensory cues and environmental parasite load, which both remain poorly understood in fish. We investigated the ability of two populations of wild caught pumpkinseed sunfish (Lepomis gibbosus) to distinguish between conspecifics infected with parasitic worms versus uninfected individuals in two-choice experiments using visual and chemical cues separately. One population was from a lake without parasites (parasite naive) whereas the other population originated from a lake with a high prevalence of trematode and cestode worms (parasite experienced). Both populations preferred to be with conspecifics, regardless of their infection level, over being alone when given visual cues but avoided conspecifics and remained alone when given chemical cues, suggesting that visual and chemical cues are not redundant. Neither population showed any preference between infected and uninfected conspecifics when given visual cues. However, in the presence of chemical cues, there was a great interindividual variation: some fish preferred uninfected conspecifics while others preferred infected ones. On average, naive fish avoided infected conspecifics whereas experienced fish did not show any preferences, suggesting that fish from lakes with high prevalence of infection habituate to infection cues. We suggest that pumpkinseeds use chemical rather than visual cues to discriminate between infected and uninfected conspecifics and make a shoaling decision. Our study highlights the importance of considering different sensory cues as well as parasite load when studying avoidance and shoaling behaviours, especially in a time of modifying sensory landscape and parasites abundance of freshwater ecosystems through global changes.

animal behavior and cognition↗

Thermal tolerance and survival are modulated by a natural gradient of infection in differentially acclimated hosts

Wild ectotherms are exposed to multiple stressors, including parasites, which can affect their responses to environmental change. Simultaneously, unprecedented warm temperatures are being recorded worldwide, increasing both the average and maximum temperatures experienced in nature. Understanding how ectotherms, such as fishes, will react to the combined stress of parasites and higher average temperatures can help predict the impact of extreme events such as heat waves on populations. The critical thermal method (CTM), which assesses upper (CTmax) and lower (CTmin) thermal tolerance, is often used in acclimated ectotherms to help predict their tolerance to various temperature scenarios. Yet, few studies have characterized the response of naturally infected fish to extreme temperature events or how acute thermal stress affects subsequent survival. We acclimated naturally infected pumpkinseed sunfish (Lepomis gibbosus), to four ecologically relevant temperatures (10, 15, 20 and 25{degrees}C) and one future warming scenario (30{degrees}C) for three weeks, before measuring CTmax and CTmin. We also assessed individual survival the week following CTmax. Interestingly, trematode parasites causing black spot disease were negatively related to CTmax, suggesting that heavily infected fish are less tolerant to acute warming. Moreover, fish infected with yellow grub parasites showed decreased survival in the days following CTmax implying that the infection load has negative survival consequences on sunfish during extreme warming events. Our findings indicate that parasite infection and high prolonged average temperatures can affect fish thermal tolerance and survival, emphasizing the need to better understand the concomitant effects of stressors on health outcomes in wild populations. Summary statementThis study shows that parasites influence thermal tolerance and survival of fish, suggesting that such stressors are important to increase the ecological relevance of thermal tolerance studies of wild animals.

ecology↗

Mitochondrial metabolism and body condition of naturally infected sunfish (Lepomis gibbosus)

Parasites can affect host behavior, cognition, locomotion, body condition and many other physiological traits. Changes to host aerobic metabolism are likely responsible for these parasite-induced performance alterations. Whole-organism metabolic rate is underpinned by cellular energy metabolism driven most prominently by the mitochondria. However, few studies have explored how mitochondrial enzymatic activity relates to body condition and parasite infection despite being a putative site for metabolic disruptions related to health status. We studied correlations among natural parasite infection, host body condition and the activity of key mitochondrial enzymes in target organs from wild-caught pumpkinseed sunfish (Lepomis gibbosus) to better understand the cellular responses of fish hosts to endoparasite infection. Enzymatic activities in the gills, spleen, and brain of infected fish were not significantly related to parasite infection or host body condition. However, the activity of cytochrome C oxidase, an enzyme involved in oxidative phosphorylation, in fish hearts was higher in individuals with lower body condition. Activities of citrate synthase, complexes I and III and carnitine palmitoyltransferase were also significantly different among organ types. These results provide preliminary information regarding the likely mitochondrial pathways affecting host body condition, the maintenance energetic requirements of different organs and their specific dependency on particular mitochondrial pathways. These results help pave the way for future studies on the effects of parasite infection on mitochondrial metabolism.

ecology↗

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

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 nor fast-start escape responses. Our results suggest that infection with parasites that are inconspicuous to researchers can result in intraspecific variation in physiological and behavioral 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.

physiology↗