Amino acid-specific isotopes reveal changing five-dimensional niche segregation in Pacific seabirds over 50 years.

Hutchison's niche theory suggests that coexisting competing species occupy non-overlapping hypervolumes, which are theoretical spaces encompassing more than three dimensions, within an n-dimensional space. The analysis of multiple stable isotopes can be used to test these ideas where each isotope can be considered a dimension of niche space. These hypervolumes may change over time in response to variation in behaviour or habitat, within or among species, consequently changing the niche space itself. Here, we use isotopic values of carbon and nitrogen of ten amino acids, as well as sulphur isotopic values, to produce multi-isotope models to examine niche segregation among an assemblage of five coexisting seabird species (ancient murrelet Synthliboramphus antiquus, double-crested cormorant Phalacrocorax auritus, Leach's storm-petrel Oceanodrama leucorhoa, rhinoceros auklet Cerorhinca monocerata, pelagic cormorant Phalacrocorax pelagicus) that inhabit coastal British Columbia. When only one or two isotope dimensions were considered, the five species overlapped considerably, but segregation increased in more dimensions, but often in complex ways. Thus, each of the five species occupied their own isotopic hypervolume (niche), but that became apparent only when factoring the increased information from sulphur and amino acid specific isotope values, rather than just relying on proxies of δ15N and δ13C alone. For cormorants, there was reduction of niche size for both species consistent with a decline in their dominant prey, Pacific herring Clupea pallasii, from 1970 to 2006. Consistent with niche theory, cormorant species showed segregation across time, with the double-crested demonstrating a marked change in diet in response to prey shifts in a higher dimensional space. In brief, incorporating multiple isotopes (sulfur, PC1 of δ15N [baselines], PC2 of δ15N [trophic position], PC1 and PC2 of δ13C) metrics allowed us to infer changes and differences in food web topology that were not apparent from classic carbon-nitrogen biplots.

Warming in the land of the midnight sun: breeding birds may suffer greater heat stress at high- versus low-Arctic sites.

Rising global temperatures are expected to increase reproductive costs for wildlife as greater thermoregulatory demands interfere with reproductive activities. However, predicting the temperatures at which reproductive performance is negatively impacted remains a significant hurdle. Using a thermoregulatory polygon approach, we derived a reproductive threshold temperature for an Arctic songbird-the snow bunting (Plectrophenax nivalis). We defined this threshold as the temperature at which individuals must reduce activity to suboptimal levels (i.e. less than four-time basal metabolic rate) to sustain nestling provisioning and avoid overheating. We then compared this threshold to operative temperatures recorded at high (82° N) and low (64° N) Arctic sites to estimate how heat constraints translate into site-specific impacts on sustained activity level. We predict buntings would become behaviourally constrained at operative temperatures above 11.7°C, whereupon they must reduce provisioning rates to avoid overheating. Low-Arctic sites had larger fluctuations in solar radiation, consistently producing daily periods when operative temperatures exceeded 11.7°C. However, high-latitude birds faced entire, consecutive days when parents would be unable to sustain required provisioning rates. These data indicate that Arctic warming is probably already disrupting the breeding performance of cold-specialist birds and suggests counterintuitive and severe negative impacts of warming at higher latitude breeding locations.

Stable Mercury Trends Support a Long-Term Diet Shift Away from Marine Foraging in Salish Sea Glaucous-Winged Gulls over the Last Century.

Marine predators are monitored as indicators of pollution, but such trends can be complicated by variation in diet. Glaucous-winged gulls (Larus glaucescens) have experienced a dietary shift over the past century, from mainly marine to including more terrestrial/freshwater inputs, with unknown impacts on mercury (Hg) trends. We examined 109-year trends in total mercury (THg) and methylmercury (MeHg) concentrations in glaucous-winged gull feathers (1887-1996) from the Salish Sea. Adult flank feathers had higher MeHg concentrations than immature feathers, and males head feathers had higher THg concentrations than females. Overall, we found no evidence of a trend in feather MeHg or THg concentrations over time from 1887 to 1996. In the same individuals, δ15N, δ13C, and δ34S declined over time in gull feathers. In comparison, egg THg concentrations declined from 1970 to 2019 in two species of cormorants, likely reflecting decreases in local Hg sources. We conclude that diet shifts through time may have countered increased Hg deposition from long-range transport in glaucous-winged gulls. The lack of Hg trends over time in glaucous-winged gull feathers provides additional support that these gulls have decreased the amount of marine forage fish in their diet.

Mercury, legacy and emerging POPs, and endocrine-behavioural linkages: Implications of Arctic change in a diving seabird.

Arctic species encounter multiple stressors including climate change and environmental contaminants. Some contaminants may disrupt hormones that govern the behavioural responses of wildlife to climatic variation, and thus the capacity of species to respond to climate change. We investigated correlative interactions between legacy and emerging persistent organic pollutants (POPs), mercury (Hg), hormones and behaviours, in thick-billed murres (Uria lomvia) (N = 163) breeding in northern Hudson Bay (2016-2018). The blood profile of the murres was dominated by methylmercury (MeHg), followed by much lower levels of sum (∑) 35 polychlorinated biphenyls (PCBs), hexachlorobenzene (HCB) and p,p'-dichlorodiphenyltrichloroethylene (DDE), polybrominated diphenyl ethers (PBDEs) BDE-47, -99 and BDE-100; all other measured organochlorine pesticides and replacement brominated flame retardants had low concentrations if detected. Inter-annual variations occurred in MeHg, circulating triiodothyronine (T3), thyroxine (T4), and the foraging behaviours of the murres, identified using GPS-accelerometers. Compared to the 50-year mean date (1971-2021) for 50% of sea-ice coverage in Hudson Bay, sea-ice breakup was 1-2 weeks earlier (2016, 2017) or comparable (2018). Indeed, 2017 was the earliest year on record. Consistent with relationships identified individually between MeHg and total T3, and T3 and foraging behaviour, a direct interaction between these three parameters was evident when all possible interactions among measured chemical pollutants, hormones, and behaviours of the murres were considered collectively (path analysis). When murres were likely already stressed due to early sea-ice breakup (2016, 2017), blood MeHg influenced circulating T3 that in turn reduced foraging time underwater. We conclude that when sea-ice breaks up early in the breeding season, Hg may interfere with the ability of murres to adjust their foraging behaviour via T3 in relation to variation in sea-ice.

Potential disruption of thyroid hormones by perfluoroalkyl acids in an Arctic seabird during reproduction.

Arctic marine ecosystems are experiencing rapid change, such as ocean warming and enhanced pollutants. Perfluoroalkyl acids (PFAAs) arriving via long-range transport have been detected in Arctic wildlife, including seabirds which are considered sentinels of marine ecosystem health. There is evidence that PFAA exposure leads to the disruption of thyroid hormones (THs), such as thyroxine (T4) and triiodothyronine (T3), which play important roles in metabolism, incubation, and thermoregulation in seabirds. Here, we investigated relationships between PFAAs and THs [total T4 (TT4), free T4 (FT4), total T3 (TT3) and free T3 (FT3)] in blood plasma collected from 63 thick-billed murres (Uria lomvia) at a colony located in northern Hudson Bay (2016-2018). We then tested if PFAAs and TH levels were related to fitness-associated reproductive traits, such as body mass and hatch dates. PFUdA, PFOS, and PFTrDA were the dominant PFAAs in murre blood, accounting for approximately 77% of ∑PFAA. Females had higher PFAAs than males, possibly due to higher trophic feeding. While FT3 increased with PFOS, PFNA, PFDA, PFDoA, PFTeDA, ∑PFCA7, and ∑PFAA in murres, TT3 decreased with PFOS, PFDoA, and PFTeDA in males, but not females, suggesting thyroid disruption. TT3 increased with body mass, whereas several long-chain PFAAs were negatively correlated with body mass. Negative relationships between PFNA, PFDoA, PFTrDA, PFTeDA, and ∑PFAA with hatch dates may be the result of a disruption in incubation behaviour, resulting in earlier hatch dates. Consequently, TT3 concentrations were highest in males and females in 2018, a year in which PFAAs were lowest and hatch dates were delayed relative to 2017. As an Arctic seabird experiencing several indirect effects of climate change, the interaction of PFAAs on thyroid activity may cause additional stress to murres.

Resting costs too: the relative importance of active and resting energy expenditure in a sub-arctic seabird.

Breeding is costly for many animals, including birds that must deliver food to a central place (i.e. nest). Measuring energy expenditure throughout the breeding season can provide valuable insight into physiological limitations by highlighting periods of high demand, and ultimately allows improvement of conservation strategies. However, quantifying energy expenditure in wildlife can be challenging, as existing methods do not measure both active (e.g. foraging) and resting energy costs across short and long time scales. Here, we developed a novel method for comparing active and resting costs in 66 pre-breeding and breeding seabirds (black-legged kittiwakes, Rissa tridactyla) by combining accelerometry and triiodothyronine (T3) as proxies for active and resting costs, respectively. Active energy costs were higher during incubation (P=0.0004) and chick rearing (P<0.0001) than during pre-laying, because of an increase in the time spent in flight of 11% (P=0.0005) and 15% (P<0.0001), respectively. Levels of T3, reflecting resting costs, peaked marginally during incubation with a mean (±s.d.) concentration of 4.71±1.97 pg ml-1 in comparison to 2.66±1.30 pg ml-1 during pre-laying (P=0.05) and 3.16±2.85 pg ml-1 during chick rearing (P=0.11). Thus, although chick rearing is often assumed to be the costliest breeding stage by multiple studies, our results suggest that incubation could be more costly as a result of high resting costs. We highlight the importance of accounting for both active and resting costs when assessing energy expenditure.

Limited heat tolerance in a cold-adapted seabird: implications of a warming Arctic.

The Arctic is warming at approximately twice the global rate, with well-documented indirect effects on wildlife. However, few studies have examined the direct effects of warming temperatures on Arctic wildlife, leaving the importance of heat stress unclear. Here, we assessed the direct effects of increasing air temperatures on the physiology of thick-billed murres (Uria lomvia), an Arctic seabird with reported mortalities due to heat stress while nesting on sun-exposed cliffs. We used flow-through respirometry to measure the response of body temperature, resting metabolic rate, evaporative water loss and evaporative cooling efficiency (the ratio of evaporative heat loss to metabolic heat production) in murres while experimentally increasing air temperature. Murres had limited heat tolerance, exhibiting: (1) a low maximum body temperature (43.3°C); (2) a moderate increase in resting metabolic rate relative that within their thermoneutral zone (1.57 times); (3) a small increase in evaporative water loss rate relative that within their thermoneutral zone (1.26 times); and (4) a low maximum evaporative cooling efficiency (0.33). Moreover, evaporative cooling efficiency decreased with increasing air temperature, suggesting murres were producing heat at a faster rate than they were dissipating it. Larger murres also had a higher rate of increase in resting metabolic rate and a lower rate of increase in evaporative water loss than smaller murres; therefore, evaporative cooling efficiency declined with increasing body mass. As a cold-adapted bird, murres' limited heat tolerance likely explains their mortality on warm days. Direct effects of overheating on Arctic wildlife may be an important but under-reported impact of climate change.

Limited heat tolerance in an Arctic passerine: Thermoregulatory implications for cold-specialized birds in a rapidly warming world.

Arctic animals inhabit some of the coldest environments on the planet and have evolved physiological mechanisms for minimizing heat loss under extreme cold. However, the Arctic is warming faster than the global average and how well Arctic animals tolerate even moderately high air temperatures (T a) is unknown.Using flow-through respirometry, we investigated the heat tolerance and evaporative cooling capacity of snow buntings (Plectrophenax nivalis; ≈31 g, N = 42), a cold specialist, Arctic songbird. We exposed buntings to increasing T a and measured body temperature (T b), resting metabolic rate (RMR), rates of evaporative water loss (EWL), and evaporative cooling efficiency (the ratio of evaporative heat loss to metabolic heat production).Buntings had an average (±SD) T b of 41.3 ± 0.2°C at thermoneutral T a and increased T b to a maximum of 43.5 ± 0.3°C. Buntings started panting at T a of 33.2 ± 1.7°C, with rapid increases in EWL starting at T a = 34.6°C, meaning they experienced heat stress when air temperatures were well below their body temperature. Maximum rates of EWL were only 2.9× baseline rates at thermoneutral T a, a markedly lower increase than seen in more heat-tolerant arid-zone species (e.g., ≥4.7× baseline rates). Heat-stressed buntings also had low evaporative cooling efficiencies, with 95% of individuals unable to evaporatively dissipate an amount of heat equivalent to their own metabolic heat production.Our results suggest that buntings' well-developed cold tolerance may come at the cost of reduced heat tolerance. As the Arctic warms, and this and other species experience increased periods of heat stress, a limited capacity for evaporative cooling may force birds to increasingly rely on behavioral thermoregulation, such as minimizing activity, at the expense of diminished performance or reproductive investment.

Body condition impacts blood and muscle oxygen storage capacity of free-living beluga whales (Delphinapterus leucas).

Arctic marine ecosystems are currently undergoing rapid environmental changes. Over the past 20 years, individual growth rates of beluga whales (Delphinapterus leucas) have declined, which may be a response to climate change; however, the scarcity of physiological data makes it difficult to gauge the adaptive capacity and resilience of the species. We explored relationships between body condition and physiological parameters pertaining to oxygen (O2) storage capacity in 77 beluga whales in the eastern Beaufort Sea. Muscle myoglobin concentrations averaged 77.9 mg g-1, one of the highest values reported among mammals. Importantly, blood haematocrit, haemoglobin and muscle myoglobin concentrations correlated positively to indices of body condition, including maximum half-girth to length ratios. Thus, a whale with the lowest body condition index would have ∼27% lower blood (26.0 versus 35.7 ml kg-1) and 12% lower muscle (15.6 versus 17.7 ml kg-1) O2 stores than a whale of equivalent mass with the highest body condition index; with the conservative assumption that underwater O2 consumption rates are unaffected by body condition, this equates to a >3 min difference in maximal aerobic dive time between the two extremes (14.3 versus 17.4 min). Consequently, environmental changes that negatively impact body condition may hinder the ability of whales to reach preferred prey sources, evade predators and escape ice entrapments. The relationship between body condition and O2 storage capacity may represent a vicious cycle, in which environmental changes resulting in decreased body condition impair foraging, leading to further reductions in condition through diminished prey acquisition and/or increased foraging efforts.

Latitudinal variation in ecological opportunity and intraspecific competition indicates differences in niche variability and diet specialization of Arctic marine predators.

Individual specialization (IS), where individuals within populations irrespective of age, sex, and body size are either specialized or generalized in terms of resource use, has implications on ecological niches and food web structure. Niche size and degree of IS of near-top trophic-level marine predators have been little studied in polar regions or with latitude. We quantified the large-scale latitudinal variation of population- and individual-level niche size and IS in ringed seals (Pusa hispida) and beluga whales (Delphinapterus leucas) using stable carbon and nitrogen isotope analysis on 379 paired ringed seal liver and muscle samples and 124 paired beluga skin and muscle samples from eight locations ranging from the low to high Arctic. We characterized both within- and between-individual variation in predator niche size at each location as well as accounting for spatial differences in the isotopic ranges of potential prey. Total isotopic niche width (TINW) for populations of ringed seals and beluga decreased with increasing latitude. Higher TINW values were associated with greater ecological opportunity (i.e., prey diversity) in the prey fish community which mainly consists of Capelin (Mallotus villosus) and Sand lance (Ammodytes sp.) at lower latitudes and Arctic cod (Boreogadus saida) at high latitudes. In beluga, their dietary consistency between tissues also known as the within-individual component (WIC) increased in a near 1:1 ratio with TINW (slope = 0.84), suggesting dietary generalization, whereas the slope (0.18) of WIC relative to TINW in ringed seals indicated a high degree of individual specialization in ringed seal populations with higher TINWs. Our findings highlight the differences in TINW and level of IS for ringed seals and beluga relative to latitude as a likely response to large-scale spatial variation in ecological opportunity, suggesting species-specific variation in dietary plasticity to spatial differences in prey resources and environmental conditions in a rapidly changing ecosystem.

The impact of municipal wastewater effluent on field-deployed freshwater mussels in the Grand River (Ontario, Canada).

To examine effects of municipal wastewater effluent (MWWE) on sentinel organisms, the authors deployed caged freshwater mussels (Lasmigona costata) in the Grand River (ON, Canada) upstream and downstream of an MWWE outfall. Passive sampling devices were deployed alongside caged mussels to confirm exposure. Biomarkers of xenobiotic biotransformation, oxidative stress, estrogenicity, and immunomodulation were investigated. Elevated concentrations of selected pharmaceutical and personal care products (PPCPs) and a natural estrogen (estrone) were found at the downstream sites. Mussels caged downstream of the effluent for 2 wk showed minimal evidence of exposure, while those deployed for 4 wk exhibited significantly higher levels of lipid peroxidation (LPO) and glutathione S-transferase (GST) activity, demonstrating that MWWE-exposed mussels exhibit increased activity in xenobiotic conjugation and oxidative stress. With respect to immune responses, a significant increase in plasma lysozyme activity and hemocyte viability was observed in MWWE-exposed mussels. Vitellogenin (vtg)-like protein in male mussels showed a trend toward induction after 4 wk of deployment at the first downstream site, but mean levels were not significantly different. Discriminant function analysis indicated that mussels deployed for 4 wk upstream and downstream of the MWWE discharge could be discriminated on the basis of LPO, GST, plasma lysozyme, and vtg responses. The physiological stress observed in caged mussels indicates that wild mussels chronically exposed to MWWE in this ecosystem would also be negatively impacted.

Contamination of an arctic terrestrial food web with marine-derived persistent organic pollutants transported by breeding seabirds.

At Cape Vera, Devon Island (Nunavut, Canada), a colony of northern fulmars (Fulmarus glacialis) concentrates and releases contaminants through their guano to the environment. We determined whether persistent organic pollutants (POPs) from seabirds were transferred to coastal food webs. Snow buntings (Plectrophenax nivalis) were the most contaminated species, with ∑PCB and ∑DDT (mean: 168, 106 ng/g ww) concentrations surpassing environmental guidelines for protecting wildlife. When examined collectively, PCB congeners and DDT in jewel lichen (Xanthoria elegans) were lower in samples taken farther from the seabird colony, and increased with increasing δ(15)N values. However, only concentrations of p'p-DDE:∑DDT and PCB-95 were significantly correlated inversely with distance from the seabird cliffs. Linkages between marine-derived POPs and their concentrations in terrestrial mammals were less clear. Our study provides novel contaminant data for these species and supports biovector transport as a source of organic contaminants to certain components of the terrestrial food web.

An isotopic investigation of mercury accumulation in terrestrial food webs adjacent to an Arctic seabird colony.

At Cape Vera (Devon Island, Nunavut, Canada), a seabird colony of northern fulmars (Fulmarus glacialis) congregates and releases nutrients through the deposition of guano to the coastal terrestrial environment, thus creating nutrient-fertilized habitats important to insects, birds, and mammals. Here we determined whether mercury was similarly enriched in various terrestrial food web components in this High Arctic coastal ecosystem due to seabird inputs. Stable isotopes (delta(15)N, delta(13)C) were used to identify trophic linkages and possible routes of contaminant transfer in the food web. Values of delta(15)N were significantly higher in lichens and certain plants collected closer to the bird colony, demonstrating a gradient of seabird influence, and were higher at Cape Vera than our reference site at Cape Herschel, on eastern Ellesmere Island, an area relatively unaffected by seabirds. In contrast, delta(13)C showed little variation among terrestrial species, suggesting minimal influence by seabirds. Concentrations of total mercury (THg) in primary producers and phyto/zooplankton were not significantly correlated with distance from the seabird colony or delta(15)N values, and were similar to other taxa from the High Arctic. Our results provide novel data on THg in several Arctic taxa where concentrations have not been reported previously. Moreover, the analyses indicate that delta(15)N is significantly enriched in the adjacent environment by guano fertilization, but our study was unable to show an enrichment of THg and delta(13)C in the terrestrial food web near the seabird colony.

Spatial and temporal trends of mercury concentrations in young-of-the-year spottail shiners (Notropis hudsonius) in the St. Lawrence River at Cornwall, ON.

The St. Lawrence River at Cornwall, Ontario is an "Area of Concern" because of mercury (Hg) biomagnification from bottom sediments. To assess the spatial and temporal distribution of Hg in the food web, young-of-the-year (YOY) spottail shiners (Notropis hudsonius) were collected in August 2005 from five sites along the Cornwall waterfront within a Hg-contaminated zone and two reference zones. The results were compared to analyses made between 1979 and 2000 by the Ontario Ministry of the Environment. Total Hg concentrations in spottail shiners from the contaminated zone were significantly higher than in reference zones, confirming previous observations. Within the contaminated zone, there were significant differences in Hg concentrations among three sites spaced about 500 m apart, consistent with a high degree of site fidelity of YOY fish and suggesting a possible internal source of Hg. Hg concentrations in spottail shiners are decreasing regionally, although year-to-year variability was high, particularly in the contaminated zone. Stable isotope analyses of spottail shiners did not reveal any differences in nitrogen isotope composition among zones that would indicate differences in food-web structure and Hg biomagnification. However, carbon sources at an upstream reference zone were not the same as within the Area of Concern. Differences in carbon isotope composition at two sites within the contaminated zone corresponded to differences in Hg concentrations, consistent with a unique internal source of Hg. The variation in Hg contamination of YOY spottail shiners over fine spatial and temporal scales provide important insights about the potential release of Hg from contaminated sediments and the role of climate in regional trends. Sessile YOY fish provide a precise indicator for demonstrating these differences and for assessing their cause.