Time series analysis of elemental and isotopic data from biomineralized whale tissue

A temporal record of environmental conditions is often contained within accretionary biological tissue. These records can provide knowledge of the environmental conditions that existed at the time the tissue was formed. In this study, we look at trace element concentrations and isotopic ratios of carbon and nitrogen as contained in baleen from bowhead whales in the eastern and western Arctic Ocean. Time series techniques, including maximum likelihood method and likelihood ratio tests, are applied to analysis of data and inference about their mean structures.     

Bowhead whale (Balaena mysticetus) growth and feeding as estimated by δ13C techniques

Tissue ¹³C of bowhead whale, Balaena mysticetus, varies seasonally in response to geographic variations in the ¹³C of prey organisms consumed along the annual migratory route between the Bering, Chukchi and Beaufort Seas. Seasonal changes in body ¹³C of whales taken in 1986 from Alaskan waters provide a means of estimating energy intake from the different habitats in which the whales feed. Adult bowheads do not show significant seasonal shifts in the ¹³C of muscle and visceral fat. Their enrichment in ¹³C relative to subadult whales suggests that they acquire most of their food from fall and winter feeding or from unsampled parts of the summer range where zooplankton are enriched in ¹³C. Young individuals however, undergo marked seasonal shifts indicating that they feed heavily both in the summer and autumn or winter. Oscillations in ¹³C along the length of the baleen also provide a measure of age. Baleen growth rates decline as the whales age and provide a means of correcting for wear loss and allow aging of individuals less than 12 yr old. Although body length is a poor indicator of age in young bowhead whales, baleen length is closely correlated. Growth rates of bowheads after Year 1 are slow ( 0.4m yr^-1) and up to 20 yr are required to reach the assumed length of sexual maturity at 13 to 14m.     

Exploring the effects of reductions in krill biomass in the Southern Ocean on blue whales using a state-dependent foraging model

Many species of baleen whales were hunted to near extinction in the Southern Hemisphere. The recovery of these populations will be affected by the availability of krill, a major dietary component, in the Southern Ocean. We combine a novel energetics model for baleen whales with a state dependent foraging model to explore the impacts of an expanding krill fishery on baleen whales. We parameterize the model for blue whales, but with simple modifications it could be applied to most baleen whales. We predict that an expanding fishery will have a small but significant impact on the blue whale population through decreased birth rates. However, spreading the catch limit throughout the range of krill can reduce these effects. In addition, whales may be able to reduce these impacts through adaptive changes in foraging behavior. The relationship between krill abundance and blue whale foraging and reproductive success is nonlinear, such that larger reductions in krill biomass, potentially following a loss of sea ice due to climate change, could have a much larger negative impact on the recovery of blue whales.     

Remote Antarctic feeding ground important for east Australian humpback whales

Understanding the dynamics of population recovery is particularly complex when an organism has multiple, remote breeding and feeding grounds separated by one of the longest known migration routes. This study reports on the most comprehensive assessment of humpback whale (Megaptera novaeangliae) movements between remote Antarctic waters south of New Zealand and east Australia (EA), and the migratory corridors and breeding grounds of Australia and Oceania. A total of 112 individual whales were identified; 57 from microsatellites and 61 by fluke with 23 % (n = 26) matched to sites outside Antarctica. Despite large datasets from other southern regions being included in the comparison, the whales were predominantly linked to EA (n = 24). Only two matches to the Oceania catalogues directly north was surprising; therefore the primary feeding grounds of these endangered whales still remain unknown. The confirmation of the Balleny Islands as an important feeding ground for EA whales could provide an insight into reasons behind the rapid recovery of this population. Determining the feeding grounds of Oceania’s whales may explain whether prey energetics or migration length are limiting factors to their recovery and will allow an understanding of future ecosystem changes in these whales.     

Contrasting C and N isotope ratios from sperm whale skin and squid between the Gulf of Mexico and Gulf of California: effect of habitat

To investigate feeding variation between populations of an apex oceanic predator, stable isotope ratios of carbon (δ¹³C) and nitrogen (δ¹⁵N) have been compared in skin of female and immature male sperm whales (Physeter macrocephalus) from the northern Gulf of Mexico (GoM) and the Gulf of California (GC). Whale sexes were determined genetically. The δ¹³C and δ¹⁵N values from squid muscle were used from the GC, and from inshore and offshore sites in the GoM. We documented contrastingly lower δ¹³C and δ¹⁵N from whales and squid of the GoM compared with those from the GC. While this difference may be associated with variation in trophic position, geographic variation in biochemical cycling influenced significantly the contrasting isotope values between gulfs. Within the northern GoM, the highly distinct δ¹⁵N values of neritic squid versus mesopelagic squid provide further evidence of habitat specificity in δ¹⁵N.     

Stable isotope analysis in two sympatric populations of bottlenose dolphins <Emphasis Type="Italic">Tursiops truncatus</Emphasis>: evidence of resource partitioning?

Skin and muscle from 43 bottlenose dolphins (38 juveniles/adults, 5 calves) stranded in NW Spain were analysed to determine whether stable isotope ratios (δ¹³C and δ¹⁵N) could be used to assess dietary variation, habitat segregation and population substructure. Results were compared with published stomach contents data. Stable isotope ratios from 17 known prey species were also determined. Isotope ratios of the main prey (blue whiting, hake) varied significantly in relation to fish body size. Dolphin calves showed significant heavy isotope enrichments compared to adult females. Excluding calves, δ¹⁵N decreased with increasing dolphin body size, probably related to an ontogenetic shift in diet towards species at lower trophic levels, e.g. on blue whiting as suggested by stomach content results. Bottlenose dolphins were divided into two putative populations (North, South) based on previous genetic studies, and values of δ¹³C and δ¹⁵N differed significantly between these two groups, confirming the existence of population structuring.     

Geographical variations in the trophic ecology of Japanese anchovy, Engraulis japonicus, inferred from carbon and nitrogen stable isotope ratios

Carbon and nitrogen stable isotope ratios of Japanese anchovy (Engraulis japonicus) and their stomach contents were examined and compared among various regions around Japan. Geographical variations in the isotope ratios were found between inshore and Pacific offshore regions. While most of the anchovy samples had isotope ratios around −17.6‰ for δ¹³C and 10.0‰ for δ¹⁵N as median values, higher (more enriched) isotope values were found in the anchovy sampled from inshore regions. On the contrary, lower (more depleted) values were found mostly in the anchovy from the Pacific offshore region including the Kuroshio Extension and Kuroshio-Oyashio transition zones. Higher carbon isotope ratios in the inshore regions may reflect a carbon source from benthic primary producers in addition to phytoplankton possibly through the consumption of the larvae of benthic organisms such as bivalves or decapods, which were found in the stomach contents of the inshore anchovy. Variations in the nitrogen isotope ratio may reflect not only differences in the trophic level of prey species, but also variations in the baseline level of food webs. Stable isotope ratios are potentially a useful tool for understanding the stock/population structure and migration of anchovy. The present findings indicate the potential importance of the “inshore–offshore” variations in the biology of Japanese anchovy populations in the northwestern Pacific waters.     

Trophic ecology of Grey-headed albatrosses from Marion Island, Southern Ocean: insights from stomach contents and diet tracers

During chick-rearing, albatrosses can alternate between long foraging trips that provide the main source of food for the adults and short foraging trips that they use to feed their young. This flexibility in foraging behaviour can lead to differences in diet composition between adults and chicks and implies that they may be vulnerable in different ways to food shortages. The trophic ecology of the Grey-headed albatross Thalassarche chrysostoma was investigated at the sub-Antarctic Prince Edward Islands during the chick-rearing period in April 2006 using a combination of approaches. Diets of adults and chicks were assessed using stable isotope ratios and fatty acid (FA) profiles of blood and/or stomach oils, in addition to stomach contents analysis. Fish from the family Macrouridae and cephalopods (particularly the onychoteuthid Kondakovia longimana) were the primary prey, whereas crustaceans (krill Euphausia superba) represented a smaller proportion of the stomach contents. Stomach oil FA profiles contained more monounsaturated FA than the profiles of plasma, which were richer in saturated FA and arachidonic acid (20:4n-6). There was also a distinct separation of adults from chicks, with higher levels of monounsaturates in chick plasma, and higher saturated FA levels (particularly 16:0) in the adult plasma. Stable carbon isotope ratios of whole blood were similar in adults and chicks, whereas stable nitrogen isotope ratios showed significant enrichment by >1‰ in chicks. The combined FA, stable isotopes and stomach contents analyses suggest clear differences in diet quality between adults and chicks, with chicks feeding at a higher trophic position through feeding more on highly nutritious fish and adults keeping much of the less nutritious zooplankton for themselves.     

Age-related multi-year associations in female humpback whales (Megaptera novaeangliae)

Analyses of social structures in baleen whales are rare, and so far, they are thought to consist of mostly short and unstable associations. We investigated the association patterns of individual humpback whales from a summer feeding aggregation in the Gulf of St. Lawrence from 1997 to 2005. Photo-identified animals were sexed using genetic methods and were grouped into five categories: juvenile males/females, mature males and lactating/non-lactating females. We calculated half-weight association indices within and between the groups and found that 45% of the observation showed single animals and another 45% small groups (two to three) consisting mainly of mature animals besides lactating females. Using permutation tests, we found evidence for long-term associations between mature males and non-lactating females as well as among non-lactating females. Standardised lagged association rates revealed that these male–female groups disassociated quickly over about 2 weeks, whereas associations increased again towards the beginning of the breeding season. Non-lactating females of similar age engaged in multi-seasonal stable pairs for up to six consecutive feeding seasons; no mature male–female association was observed in consecutive years. The females with the most stable and long-term associations also had the highest reproductive output. While the risk of predation could not explain these long-term bonds, feeding cooperation seemed the most plausible explanation for group forming behaviour during the summer months.     

Distribution,growth and life cycle of the mesopelagic amphipod Primno abyssalis (Hyperiidea: Phrosinidae) in the southern Japan sea

The vertical distribution, growth, maturation, brood size and life cycle of the hyperiid amphipod Primno abyssalis (formerly P. macropa) were investigated using seasonal samples collected from Toyama Bay, southern Japan Sea, during the period June 1986 to September 1992. Over four different seasons of the year, P. abyssalis was most abundant in the 200 to 350 m strata at night and the 350 to 400 m strata during the day, indicating 100 to 150 m as the general distance of diel vertical movement. Some differences in vertical migrating behavior were noted among juveniles, adult males and females. Population-structure analysis revealed the occurrence of three cohorts aged 0+, 1+ and 2+ yr. Growth as body length in this species is linear with time. Estimated time to complete one life cycle is 1.8 to 2.5 yr for females, but only 0.8 yr for males. Maximum longevity is 2.8 yr. Instar analysis based on the segment number of pleopod rami indicated that newly hatched juveniles molt ten times to reach adult male, and four more times to reach adult female. Adult instar number was found to be only 1 for males and 5 for females. Ovigerous females occurred throughout the year, but the annual peak of release of juveniles from the female's marsupium is estimated to be arly March. Brood size was not correlated with female size, a maximum brood size of 214 eggs was recorded. The dry and ash-free dry weights of instars suggested that juveniles in the female marsupium, adult males, and older adult females are less active feeding or non-feeding stages. Except for the reduced growth rate and the occurrence of small, short-lived males, most characteristics of P. abyssalis are consistent with the present view of the life modes of mesopelagic animals, including linear growth in length, aseasonal reproduction, and smaller brood size coupled with larger eggs.     

Shift in foraging grounds and diet broadening during ontogeny in southern elephant seals from Kerguelen Islands

Highly dimorphic species like southern elephant seals (Mirounga leonina, SES hereafter) frequently exhibit resource partitioning according to sex and/or age classes. We measured carbon and nitrogen stable isotopes (δ¹³C and δ¹⁵N) of 404 blood samples (136 males and 268 females from Kerguelen Islands, 49°21′S, 70°18′E) from 2004 to 2011. Assuming that the distribution of carbon isotopes (δ¹³C value) reflects the two main foraging grounds (Polar Frontal and Antarctic Zones), we quantified the proportion of SES foraging within each zone in relation with size, a proxy for their age. We found a clear shift from Polar Frontal to Antarctic waters as male SES aged, but no relation as far as females is concerned. We also observed a widening range of nitrogen isotopic (δ¹⁵N) values, suggesting that both males and females expanded their diet spectra with age. Whereas males increased their trophic level, females remained constant on average, with some adult females feeding both at lower and at higher trophic levels than juveniles.     

Differences in stable isotopes in blood and feathers of seabirds are consistent across species, age and latitude: implications for food web studies

Stable isotopes of growing feathers and blood both represent assimilated diet, and both tissues are used to study the diet and foraging distribution of marine and terrestrial birds. Although most studies have assumed that both tissues represent a difference of one trophic level to diet, the enrichment factors of blood and feathers may differ, especially where endogenous reserves are used as precursors during feather synthesis. In this study, we compare carbon and nitrogen stable isotopes of blood and simultaneously growing feathers of five species of Procellariiformes, representing five genera, different geographical regions and different life stages (chicks and adults). In all species, feathers were enriched in ¹⁵N and ¹³C compared with blood. Isotopic values of carbon and nitrogen were correlated in different tissues growing simultaneously for most species analyzed, suggesting that mathematical corrections could be used to compare different tissues. Our results imply that more care needs to be taken when comparing stable isotope signatures across studies assuming different tissues are equivalent indicators of trophic ecology.     

Diet of the social groups of long-finned pilot whales (<Emphasis Type="Italic">Globicephala melas</Emphasis>) in the Strait of Gibraltar

The Strait of Gibraltar is inhabited throughout the year by a group of pilot whales (Globicephala melas), but their spatial distribution varies between Summer and Autumn. In this paper, we have used carbon (¹³C/¹²C) and nitrogen (¹⁵N/¹⁴N) stable isotope signatures to investigate the differences in diet amongst seasons, sex and stable social units. Skin samples were collected from 56 individually photo-identified pilot whales during Autumn 2005 and Summer 2006. These individuals were genetically sexed and their isotopic signature determined. The level of inter-individual association both within and between stable social units were compared to Euclidean distances between individual isotopes signatures. No differences in either δ¹⁵N or δ¹³C were found according to the sex of individuals, but significant seasonal differences were found in δ¹⁵N, although not in the δ¹³C values. This suggests that pilot whales are resident year round in the Strait, a finding supported by independent photo-identification. The variation in δ¹⁵N could reflect a shift in pilot whale diet through the year, with pilot whales feeding at a higher trophic level in Autumn compared to Summer. This could also represent a change in the diet of pilot whale prey species. The δ¹³C values were significantly different amongst the four stable social units sampled and individual δ¹³C values were significantly related to the level of inter-individual association, while no relationship was found for δ¹⁵N. These results suggest that within the same general area (i.e. the Strait of Gibraltar), there is some level of specialisation in habitat or prey choice between pilot whales social units.     

Stable isotope ratios of a tropical marine predator: confounding effects of nutritional status during growth

Stable isotope analysis of carbon and nitrogen is frequently used to study the diets and foraging ecology of marine predators. However, isotopic values may also be affected by an individual’s nutritional status and associated physiological processes. Here, we use C and N stable isotopes in blood and feathers of blue-footed booby chicks at the Galápagos Islands to examine how isotopic values are related to body condition and growth rate, and to assess the consistency in the isotope ratios of individuals during growth. Size dimorphism in blue-footed boobies provided an additional opportunity to examine how isotope ratios differ between sexes in relation to body size and growth rate. There was no significant difference between sexes but both C and N stable isotopes were significantly negatively related to the body condition of chicks. These data were consistent with individual variation in physiological processes affecting fractionation, although we cannot rule out the possibility that they were also influenced to some extent by population-level variation in the stable isotope ratios of prey fed to chicks, for instance related to prey size, depth or lipid content. Our results highlight the need for methods that take proper account of confounding physiological factors in isotopic studies of foraging ecology and diet.     

Tracking habitat and resource use for the jumbo squid Dosidicus gigas: a stable isotope analysis in the Northern Humboldt Current System

To determine the habitat and resource use of Dosidicus gigas in the Northern Humboldt Current System, we analysed carbon and nitrogen stable isotopes of 234 individuals collected during 2008–2010. Large variations in mantle stable isotope ratios were recorded, with values ranging from −19.1 to −15.1 ‰ (δ¹³C) and from 7.4 to 20.5 ‰ (δ¹⁵N). Most of the variation was explained by latitude, followed by distance to shelf break for carbon and by squid size for nitrogen. Latitudinal variations with increasing values from north to south were also found in zooplankton samples and were related to changes in isotope baseline values probably due to oxygen minimum zones that occur off Peru. This similar latitudinal trend in both zooplankton and D. gigas samples reveals that D. gigas is a relatively resident species at the scale of its isotopic turnover rate (i.e. a few weeks), even if this is not necessarily the case at the scale of its life. A small but significant size effect on δ¹³C values suggests that jumbo squid perform offshore–onshore ontogenic migration, with juveniles distributed offshore. For nitrogen, the high inter-individual variability observed with mantle length indicates that D. gigas can prey on a high variety of resources at any stage of their life cycle. This large-scale study off the coast of Peru provides further evidence that D. gigas have the capability to explore a wide range of habitats and resources at any stage of their life.     

Exploring thermal and trophic preference of Balaenoptera physalus in the central Tyrrhenian Sea: a new summer feeding ground?

In the 1990s, the central Tyrrhenian Sea was regarded as a transit region for fin whales’ (Balaenoptera physalus) summer migration. In recent years, a much higher presence of fin whales during the entire summer season was reported in the region. The hypothesis that the central Tyrrhenian Sea may have become a summer feeding ground was tested gathering data from summer presence of whales in the region (40–42.5°N; 9–13°E) and investigating whether it might be related to sea surface temperature and chlorophyll-a concentration, considered as proxies of food availability. Results showed that whales always aggregate in the more productive portions of the investigated area; the general productivity of the area, however, did not directly influence the frequency of occurrence of whales. We concluded that the complex dynamics of the balance between feeding activities and avoiding pressures may have led fin whales to use the region as an opportunistic feeding ground.     

The foraging ecology of Arctic cod (Boreogadus saida) during open water (July–August) in Allen Bay, Arctic Canada

Arctic cod (Boreogadus saida) is a schooling fish providing a critical link between lower and upper trophic levels in the Arctic. This study examined foraging of Arctic cod collected from Allen Bay, Cornwallis Island, Canada (~75 N 95 W), during summer 2010 using temporal indicators of diet including stomach content, and carbon (δ¹³C) and nitrogen (δ¹⁵N) stable isotopes of liver and muscle. Foraging at the time of capture reflected sympagic and epi-benthic habitats indicated by the prevalence of cyclopoid and harpacticoid copepods in stomachs, whereas stable isotope data, which provide an estimate of feeding over a longer period, indicated pelagic prey as important. Prey selection of juveniles differed from adults based on stable isotopes, while large adults showed the most separation based on stomach contents, suggesting size-related diet shifts. Compared to studies near Resolute in the 1970s, 1980s, and 1990s, growth and pre-spawning gonadal conditions of Arctic cod have not changed.     

Using stable isotopes to monitor anthropogenic nitrogen inputs to estuaries

Use of stable nitrogen isotope ratios is one method that has been proposed to indicate anthropogenic nutrient enrichment in estuarine systems. However, the role of stable isotopes as a tool in long-term ecosystem monitoring has not been fully developed. Resident producer and consumer species were collected from marshes dominated by Spartina alterniflora and subject to a range of anthropogenic impacts in Cape Cod, Massachusetts, and in Great South Bay and Jamaica Bay, New York. Tissue isotope ratios of Spartina alterniflora, Ulva lactuca, Fundulus heteroclitus, and Geukensia demissa were analyzed in order to determine which organisms are the most sensitive indicators of changes in anthropogenic nitrogen source and loading. Power analysis was used to determine the sample sizes necessary to detect change in nutrient source using the species sampled. Relationships between the delta15N values of the species sampled and watershed population density and residential development were evaluated. Population density was a better indicator of anthropogenic nitrogen impact than residential development, since most anthropogenic nitrogen in the study marshes was derived from wastewater. Consumer species demonstrated lower within-site variability than producer species and would therefore require smaller sample sizes to detect changes in nitrogen source and loading.     

The use of RNA:DNA ratios to predict growth limitation of juvenile summer flounder (Paralichthys dentatus) from Delaware and North Carolina estuaries

Nutritional indices were used to develop biochemical correlates of feeding and growth rates for juvenile summer flounder, Paralichthys dentatus (Linnaeus), from North Carolina (NC) and Delaware (DE). Six parameters (Fulton's condition K=10⁴xweight/(length³), wet weight/dry weight, [protein], [RNA], [DNA], and RNA:DNA) were related to feeding and growth rates of fish from previously reported 10 to 14-d experiments at temperatures ranging from 2 to 20 °C with varying feeding levels (0 to 100% and libitum). RNA:DNA ratios were the best predictors of growth rates, but inclusion of a temperature term improved the relationship between RNA:DNA ratios and growth rate for Delaware fish. Feeding rates were poorly correlated with all parameters. RNA:DNA ratios of fish in the laboratory changed significantly within 1 d of starvation and refeeding at 16 °C. RNA:DNA of juvenile summer flounder collected from one site in Indian River Bay, DE and two sites in the Newport River Estuary, NC, between January and June 1992 were used to estimate in situ growth rates following settlement. Predicted growth rates in both estuaries were close to maximum (suggesting ad libitum feeding) until early May. Growth rates of juveniles from Delaware were <0% d^-1 from December through early March, and were higher (0.6 to 3% d^-1) from April through early June. However, growth rates of DE juveniles during May were <50% of maxinum. North Carolina juveniles had growth rates of 2 to 5% d^-1 from February through early April. Juveniles from one of the Newport River sites (a marsh habitat) were also severely growth limited (<20% of maximum) after April. Prolonged periods of sub-optimal growth may be important to survival and recruitment of juvenile summer flounder in northern mid-Atlantic estuaries. A model is presented which illustrates the potential impact that small changes in temperature and growth limitation can have on recruitment success in both delaware and North Carolina estuaries.     

Ecological niche segregation among five toothed whale species off the NW Iberian Peninsula using ecological tracers as multi-approach

This study aims to assess niche segregation among the five main toothed whales that frequent the NW Iberian Peninsula waters: the common dolphin, the harbour porpoise, the bottlenose dolphin, the striped dolphin and the long-finned pilot whale. We used cadmium (Cd) and stable isotope ratios (δ¹³C and δ¹⁵N) as ecological tracers to assess degree of segregation in diet/trophic level and in foraging habitat, over various time-scales. δ¹³C values highlighted different habitats, while Cd concentrations highlighted feeding differences between oceanic and neritic species. Moreover, δ¹⁵N values suggest different trophic levels of prey targeted within oceanic and neritic species. Hence, results revealed long-term ecological segregation among five toothed whales that coexist in the NWIP and demonstrated the ability of ecological tracers to discriminate ecological niches among closely related species.