Coronary circulation enhances the aerobic performance of wild Pacific salmon.

Female Pacific salmon often experience higher mortality than males during their once-in-a-lifetime up-river spawning migration, particularly when exposed to secondary stressors (e.g. high temperatures). However, the underlying mechanisms remain unknown. One hypothesis is that female Pacific salmon hearts are more oxygen-limited than males and are less able to supply oxygen to the body's tissues during this demanding migration. Notably, female hearts have higher coronary blood flow, which could indicate a greater reliance on this oxygen source. Oxygen limitations can develop from naturally occurring coronary blockages (i.e., coronary arteriosclerosis) found in mature salmon hearts. If female hearts rely more heavily on coronary blood flow but experience similar arteriosclerosis levels as males, they will have disproportionately impaired aerobic performance. To test this hypothesis, we measured resting (RMR) and maximum metabolic rate (MMR), aerobic scope (AS) and acute upper thermal tolerance in coho salmon (Oncorhynchus kisutch) with an intact or artificially blocked coronary oxygen supply. We also assessed venous blood oxygen and chemistry (cortisol, ions, and metabolite concentrations) at different time intervals during recovery from exhaustive exercise. We found that coronary blockage impaired MMR, AS, and the partial pressure of oxygen in venous blood (PvO2) during exercise recovery but did not differ between sexes. Coronary ligation lowered acute upper thermal tolerance by 1.1°C. Though we did not find evidence of enhanced female reliance on coronary supply, our findings highlight the importance of coronary blood supply for mature wild salmon, where migration success may be linked to cardiac performance, particularly during warm water conditions.

Despite plasticity, heatwaves are costly for a coral reef fish.

Climate change is intensifying extreme weather events, including marine heatwaves, which are prolonged periods of anomalously high sea surface temperature that pose a novel threat to aquatic animals. Tropical animals may be especially vulnerable to marine heatwaves because they are adapted to a narrow temperature range. If these animals cannot acclimate to marine heatwaves, the extreme heat could impair their behavior and fitness. Here, we investigated how marine heatwave conditions affected the performance and thermal tolerance of a tropical predatory fish, arceye hawkfish (Paracirrhites arcatus), across two seasons in Moorea, French Polynesia. We found that the fish's daily activities, including recovery from burst swimming and digestion, were more energetically costly in fish exposed to marine heatwave conditions across both seasons, while their aerobic capacity remained the same. Given their constrained energy budget, these rising costs associated with warming may impact how hawkfish prioritize activities. Additionally, hawkfish that were exposed to hotter temperatures exhibited cardiac plasticity by increasing their maximum heart rate but were still operating within a few degrees of their thermal limits. With more frequent and intense heatwaves, hawkfish, and other tropical fishes must rapidly acclimate, or they may suffer physiological consequences that alter their role in the ecosystem.

Impairing cardiac oxygen supply in swimming coho salmon compromises their heart function and tolerance to acute warming.

Climatic warming elevates mortality for many salmonid populations during their physically challenging up-river spawning migrations, yet, the mechanisms underlying the increased mortality remain elusive. One hypothesis posits that a cardiac oxygen insufficiency impairs the heart's capacity to pump sufficient oxygen to body tissues to sustain up-river swimming, especially in warm water when oxygen availability declines and cardiac and whole-animal oxygen demand increases. We tested this hypothesis by measuring cardiac and metabolic (cardiorespiratory) performance, and assessing the upper thermal tolerance of coho salmon (Oncorhynchus kisutch) during sustained swimming and acute warming. By surgically ligating the coronary artery, which naturally accumulates arteriosclerotic lesions in migrating salmon, we partially impaired oxygen supply to the heart. Coronary ligation caused drastic cardiac impairment during swimming, even at benign temperatures, and substantially constrained cardiorespiratory performance during swimming and progressive warming compared to sham-operated control fish. Furthermore, upper thermal tolerance during swimming was markedly reduced (by 4.4 °C) following ligation. While the cardiorespiratory capacity of female salmon was generally lower at higher temperatures compared to males, upper thermal tolerance during swimming was similar between sexes within treatment groups. Cardiac oxygen supply is a crucial determinant for the migratory capacity of salmon facing climatic environmental warming.

Mechanisms of cardiac collapse at high temperature in a marine teleost (Girella nigrians).

Heat-induced mortality in ectotherms may be attributed to impaired cardiac performance, specifically a collapse in maximum heart rate (fHmax), although the physiological mechanisms driving this phenomenon are still unknown. Here, we tested two proposed factors which may restrict cardiac upper thermal limits: noxious venous blood conditions and oxygen limitation. We hypothesized elevated blood [K+] (hyperkalemia) and low oxygen (hypoxia) would reduce cardiac upper thermal limits in a marine teleost (Girella nigricans), while high oxygen (hyperoxia) would increase thermal limits. We also hypothesized higher acclimation temperatures would exacerbate the harmful effects of an oxygen limitation. Using the Arrhenius breakpoint temperature test, we measured fHmax in acutely warmed fish under control (saline injected) and hyperkalemic conditions (elevated plasma [K+]) while exposed to hyperoxia (200% air saturation), normoxia (100% air saturation), or hypoxia (20% air saturation). We also measured ventricle lactate content and venous blood oxygen partial pressure (PO2) to determine if there were universal thresholds in either metric driving cardiac collapse. Elevated [K+] was not significantly correlated with any cardiac thermal tolerance metric. Hypoxia significantly reduced cardiac upper thermal limits (Arrhenius breakpoint temperature [TAB], peak fHmax, temperature of peak heart rate [TPeak], and temperature at arrhythmia [TARR]). Hyperoxia did not alter cardiac thermal limits compared to normoxia. There was no evidence of a species-wide threshold in ventricular [lactate] or venous PO2. Here, we demonstrate that oxygen limits cardiac thermal tolerance only in instances of hypoxia, but that other physiological processes are responsible for causing temperature-induced heart failure when oxygen is not limited.

Fish feces reveal diverse nutrient sources for coral reefs.

Consumers mediate nutrient cycling through excretion and egestion across most ecosystems. In nutrient-poor tropical waters such as coral reefs, nutrient cycling is critical for maintaining productivity. While the cycling of fish-derived inorganic nutrients via excretion has been extensively investigated, the role of egestion for nutrient cycling has remained poorly explored. We sampled the fecal contents of 570 individual fishes across 40 species, representing six dominant trophic guilds of coral reef fishes in Moorea, French Polynesia. We measured fecal macro- (proteins, carbohydrates, lipids) and micro- (calcium, copper, iron, magnesium, manganese, zinc) nutrients and compared the fecal nutrient quantity and quality across trophic guilds, taxa, and body size. Macro- and micronutrient concentrations in fish feces varied markedly across species. Genera and trophic guild best predicted fecal nutrient concentrations. In addition, nutrient composition in feces was unique among species within both trophic guilds (herbivores and corallivores) and genera (Acanthurus and Chaetodon). Particularly, certain coral reef fishes (e.g., Thalassoma hardwicke, Chromis xanthura, Chaetodon pelewensis and Acanthurus pyroferus) harbored relatively high concentrations of micronutrients (e.g., Mn, Mg, Zn and Fe, respectively) that are known to contribute to ocean productivity and positively impact coral physiological performances. Given the nutrient-rich profiles across reef fish feces, conserving holistic reef fish communities ensures the availability of nutritional pools on coral reefs. We therefore suggest that better integration of consumer egestion dynamics into food web models and ecosystem-scale processes will facilitate an improved understanding of coral reef functioning.

Population variability in thermal performance of pre-spawning adult Chinook salmon.

Climate change is causing large declines in many Pacific salmon populations. In particular, warm rivers are associated with high levels of premature mortality in migrating adults. The Fraser River watershed in British Columbia, Canada, supports some of the largest Chinook salmon (Oncorhynchus tshawytscha) runs in the world. However, the Fraser River is warming at a rate that threatens these populations at critical freshwater life stages. A growing body of literature suggests salmonids are locally adapted to their thermal migratory experience, and thus, population-specific thermal performance information can aid in management decisions. We compared the thermal performance of pre-spawning adult Chinook salmon from two populations, a coastal fall-run from the Chilliwack River (125 km cooler migration) and an interior summer-run from the Shuswap River (565 km warmer migration). We acutely exposed fish to temperatures reflecting current (12°C, 18°C) and future projected temperatures (21°C, 24°C) in the Fraser River and assessed survival, aerobic capacity (resting and maximum metabolic rates, absolute aerobic scope (AAS), muscle and ventricle citrate synthase), anaerobic capacity (muscle and ventricle lactate dehydrogenase) and recovery capacity (post-exercise metabolism, blood physiology, tissue lactate). Chilliwack Chinook salmon performed worse at high temperatures, indicated by elevated mortality, reduced breadth in AAS, enhanced plasma lactate and potassium levels and elevated tissue lactate concentrations compared with Shuswap Chinook salmon. At water temperatures exceeding the upper pejus temperatures (Tpejus, defined here as 80% of maximum AAS) of Chilliwack (18.7°C) and Shuswap (20.2°C) Chinook salmon populations, physiological performance will decline and affect migration and survival to spawn. Our results reveal population differences in pre-spawning Chinook salmon performance across scales of biological organization at ecologically relevant temperatures. Given the rapid warming of rivers, we show that it is critical to consider the intra-specific variation in thermal physiology to assist in the conservation and management of Pacific salmon.

Differences in the behavior and diet between shoaling and solitary surgeonfish (Acanthurus triostegus).

Variation in behavior within marine and terrestrial species can influence the functioning of the ecosystems they inhabit. However, the contribution of social behavior to ecosystem function remains underexplored. Many coral reef fish species provide potentially insightful models for exploring how social behavior shapes ecological function because they exhibit radical intraspecific variation in sociality within a shared habitat. Here, we provide an empirical exploration on how the ecological function of a shoaling surgeonfish (Acanthurus triostegus) may differ from that of solitary conspecifics on two Pacific coral reefs combining insight from behavioral observations, stable isotope analysis, and macronutrient analysis of gut and fecal matter. We detected important differences in how the social mode of A. triostegus affected its spatial and feeding ecology, as well as that of other reef fish species. Specifically, we found increased distance traveled and area covered by shoaling fish relative to solitary A. triostegus. Additionally, shoaling A. triostegus primarily grazed within territories of other herbivorous fish and had piscivorous and nonpiscivorous heterospecific fish associated with the shoal, while solitary A. triostegus grazed largely grazed outside of any territories and did not have any such interactions with heterospecific fish. Results from stable isotope analysis show a difference in δ15N isotopes between shoaling and solitary fish, which suggests that these different social modes are persistent. Further, we found a strong interaction between social behavior and site and carbohydrate and protein percentages in the macronutrient analysis, indicating that these differences in sociality are associated with measurable differences in both the feeding ecology and nutrient excretion patterns. Our study suggests that the social behavior of individuals may play an important and underappreciated role in mediating their ecological function.

Response of toadfish (Opsanus tau) utricular afferents to multimodal inputs.

The inner ear of teleost fishes is composed of three paired multimodal otolithic end organs (saccule, utricle, and lagena), which encode auditory and vestibular inputs via the deflection of hair cells contained within the sensory epithelia of each organ. However, it remains unclear how the multimodal otolithic end organs of the teleost inner ear simultaneously integrate vestibular and auditory inputs. Therefore, microwire electrodes were chronically implanted using a 3-D printed micromanipulator into the utricular nerve of oyster toadfish (Opsanus tau) to determine how utricular afferents respond to conspecific mate vocalizations termed boatwhistles (180 Hz fundamental frequency) during movement. Utricular afferents were recorded while fish were passively moved using a sled system along an underwater track at variable speeds (velocity: 4.0-12.5 cm/s; acceleration: 0.2-2.6 cm/s2) and while fish freely swam (velocity: 3.5-18.6 cm/s; acceleration: 0.8-29.8 cm/s2). Afferent fiber activities (spikes/s) increased in response to the onset of passive and active movements; however, afferent fibers differentially adapted to sustained movements. In addition, utricular afferent fibers remained sensitive to playbacks of conspecific male boatwhistle vocalizations during both passive and active movements. Here, we demonstrate in alert toadfish that utricular afferents exhibit enhanced activity levels (spikes/s) in response to behaviorally relevant acoustic stimuli during swimming.NEW & NOTEWORTHY The inner ear of teleost fishes is composed of three paired multimodal otolithic end organs, which are sensitive to vestibular and auditory inputs. Previous studies investigating inner ear functions have primarily focused on the effects of unimodal stimuli; therefore, it remains unclear how otolithic end organs simultaneously encode multiple stimuli. Here, we show that utricular afferents remain sensitive to behaviorally relevant acoustic stimuli during swimming.

Infection at an ecotone: cross-system foraging increases satellite parasites but decreases core parasites in raccoons.

Ecotones can increase free-living species richness, but little is known about how parasites respond to ecotones. Here, we use parasite communities in raccoons (Procyon lotor) to test the hypothesis that parasite communities can be divided into core and satellite species, each with fundamentally different responses to ecotones. We used published parasite surveys to classify parasites as common core or rare satellite species, and then surveyed raccoons in coastal California to examine how proximity to two aquatic ecotones altered parasite communities. Raccoons near ecotones had more satellite and fewer core parasite species. Specifically, the marine ecotone increased parasite diversity by adding satellite species to a persistent core community, whereas the freshwater ecotone shifted the community from core to satellite species without a net change in parasite richness. We hypothesize that increased parasite richness at the marine ecotone resulted from increased diet diversity, but that raccoons were sinks for some parasites. Increased exposure to rare parasites at ecotones has implications for wildlife health and provides insight into observed associations between ecotones and emerging disease.

Southern California and range-wide raccoon gastrointestinal helminth database.

Local and global measurements of parasite prevalence and abundance are critical for understanding the dynamics that underlie the diversity, distribution, and evolution of infectious diseases. Here, we present a data set of gut helminths found in (1) raccoons throughout their range, based on primary literature from 1925-2017 and (2) raccoons in Santa Barbara County, California, USA surveyed from 2012 to 2015. The range-wide data set has 1,256 parasite entries from 217 literature sources across three continents and 32 states in the USA. This data set includes a list of all recorded raccoon gut helminths (n = 100) and their presence and prevalence in surveyed raccoon populations. The Santa Barbara data set includes gut helminth data from 182 raccoons from one Southern California County. In addition to the presence and abundance data for 13 parasite species, this data set includes measurements of 7,465 individual raccoon roundworms (Baylisascaris procyonis). For both range-wide and Santa Barbara data sets, we include information on parasite site of infection in host, sampling method, and sample size. We also provide geographic coordinates for infected raccoon populations (range-wide database) and individuals (Santa Barbara). In the associated metadata, we include sampling methods and summary figures for both the range-wide and Santa Barbara raccoon gut helminth records. There are no copyright or proprietary restrictions for research and/or teaching purposes. S. B. Weinstein and J. C. Van Wert contributed equally to this manuscript and are shared first authors.

Seasonal and Daily Patterns of the Mating Calls of the Oyster Toadfish, Opsanus tau.

Acoustic communication is vital across many taxa for mating behavior, defense, and social interactions. Male oyster toadfish, Opsanus tau, produce courtship calls, or "boatwhistles," characterized by an initial broadband segment (30-50 ms) and a longer tone-like second part (200-650 ms) during mating season. Male calls were monitored continuously with an in situ SoundTrap hydrophone that was deployed in Eel Pond, Woods Hole, Massachusetts, during the 2015 mating season. At least 10 vocalizing males were positively identified by their unique acoustic signatures. This resident population was tracked throughout the season, with several individuals tracked for extended periods of time (72 hours). Toadfish began calling in mid-May when water temperature reached 14.6 °C with these early-season "precursor" boatwhistles that were shorter in duration and contained less distinct tonal segments compared to calls later in the season. The resident toadfish stopped calling in mid-August, when water temperature was about 25.5 °C. The pulse repetition rate of the tonal part of the call was significantly related to ambient water temperature during both short-term (hourly) and long-term (weekly) monitoring. This was the first study to monitor individuals in the same population of oyster toadfish in situ continuously throughout the mating season.

Lateral line sensitivity in free-swimming toadfish Opsanus tau.

A longstanding question in aquatic animal sensory physiology is the impact of self-generated movement on lateral line sensitivity. One hypothesis is that efferent modulation of the sensory hair cells cancels self-generated noise and allows fish to sample their surroundings while swimming. In this study, microwire electrodes were chronically implanted into the anterior lateral line nerve of oyster toadfish and neural activity was monitored during forward movement. Fish were allowed to freely swim or were moved by a tethered sled. In all cases, neural activity increased during movement with no evidence of efferent modulation. The anterior lateral line of moving fish responded to a vibrating sphere or the tail oscillations of a robotic fish, indicating that the lateral line also remains sensitive to outside stimulus during self-generated movement. The results suggest that during normal swim speeds, lateral line neuromasts are not saturated and retain the ability to detect external stimuli without efferent modulation.

An implantable two axis micromanipulator made with a 3D printer for recording neural activity in free-swimming fish.

BACKGROUND: Chronically implanted electrodes allow monitoring neural activity from free moving animals. While a wide variety of implanted headstages, microdrives and electrodes exist for terrestrial animals, few have been developed for use with aquatic animals. NEW METHOD: A two axis micromanipulator was fabricated with a Formlabs 3D printer for implanting electrodes into free-swimming oyster toadfish (Opsanus tau). The five piece manipulator consisted of a base, body, electrode holder, manual screw drive and locking nut. The manipulator measured approximately 25×20×30mm (l×w×h) and weighed 5.28g after hand assembly. RESULTS: Microwire electrodes were inserted successfully with the manipulator to record high fidelity signals from the anterior lateral line nerve of the toadfish. COMPARISON WITH EXISTING METHOD(S): The micromanipulator allowed the chronically implanted electrodes to be repositioned numerous times to record from multiple sites and extended successful recording time in the toadfish by several days. CONCLUSIONS: Three dimensional printing allowed an inexpensive (<$US 5 material), two axis micromanipulator to be printed relatively rapidly (<2h) to successfully record from multiple sites in the anterior lateral line nerve of free-swimming toadfish.