Flexible foraging movements of leatherback turtles across the North Atlantic Ocean

Some marine species have been shown to target foraging at particular hotspots of high prey abundance. However, we show here that in the year after a nesting season, female leatherback turtles (Dermochelys coriacea) in the Atlantic generally spend relatively little time in fixed hotspots, especially those with a surface signature revealed in satellite imagery, but rather tend to have a pattern of near continuous traveling. Associated with this traveling, distinct changes in dive behavior indicate that turtles constantly fine tune their foraging behavior and diel activity patterns in association with local conditions. Switches between nocturnal vs. diurnal activity are rare in the animal kingdom but may be essential for survival on a diet of gelatinous zooplankton where patches of high prey availability are rare. These results indicate that in their first year after nesting, leatherback turtles do not fit the general model of migration where responses to resources are suppressed during transit. However, their behavior may be different in their sabbatical years away from nesting beaches. Our results highlight the importance of whole-ocean fishing gear regulations to minimize turtle bycatch.     

Biological and environmental influences on the trophic ecology of leatherback turtles in the northwest Atlantic Ocean

Understanding the causes and consequences of variability in trophic status is important for interpreting population dynamics and for identifying important habitats for protected species like marine turtles. In the northwest Atlantic Ocean, many leatherback turtles (Dermochelys coriacea) from distinct breeding stocks throughout the Wider Caribbean region migrate to Canadian waters seasonally to feed, but their trophic status during the migratory and breeding cycle and its implications have not yet been described. In this study, we used stable carbon and nitrogen isotope analyses of bulk skin to characterize the trophic status of leatherbacks in Atlantic Canadian waters by identifying trophic patterns among turtles and the factors influencing those patterns. δ¹⁵N values of adult males and females were significantly higher than those of turtles of unknown gender (i.e., presumed to be subadults), and δ¹⁵N increased significantly with body size. We found no significant differences among average stable isotope values of turtles according to breeding stock origin. Significant inter-annual variation in δ¹⁵N among cohorts probably reflects broad-scale oceanographic variability that drives fluctuations in stable isotope values of nutrient sources transferred through several trophic positions to leatherbacks, variation in baseline isotope values among different overwintering habitats used by leatherbacks, or a combination of both. Our results demonstrate that understanding effects of demographic and physiological factors, as well as oceanographic conditions, on trophic status is key to explaining observed patterns in population dynamics and for identifying important habitats for widely distributed, long-lived species like leatherbacks.     

Developing a common currency for stable isotope analyses of nesting marine turtles

Understanding geospatial linkages is critical to the development of appropriate management and conservation strategies for migratory species. Stable isotope analysis is a powerful tool that is performed routinely across taxa to unravel migratory connectivity. Marine turtles are a highly migratory and widely distributed taxon, but are largely studied at breeding areas. Isotopic values of several slow turnover rate tissues have been used to identify often distant foraging areas. However, as more isotopic data from various tissues become available, the relationships between tissues need to be calculated to permit meta-analyses to elucidate isotopic patterns across broader spatiotemporal scales. We used several commonly collected tissues (blood, skin, fresh eggs and unhatched eggs) collected simultaneously from loggerhead turtles (Caretta caretta) to develop a common currency for stable isotope analysis studies conducted on the nesting beach. We found highly significant relationships between the tissue signatures (r ² ranged from 0.83 to 0.96) and developed equations to convert isotopic values from one tissue to another. We examined inter- and intra-clutch isotopic variability and found that a single sampling event over the 4-month nesting season adequately defined the loggerhead female foraging area. Consequently, we propose using unhatched eggs as a common currency in stable isotope studies of nesting loggerheads. Unhatched eggs represent a noninvasive and nondestructive method that enables more extensive (both numerically and spatially) sampling. Given similar physiologies, analogous relationships might be derived in other sea turtle species.     

Investigating stock structure and trophic relationships among island-associated dolphins in the oceanic waters of the North Atlantic using fatty acid and stable isotope analyses

Short-beaked common dolphins (Delphinus delphis) and Atlantic spotted dolphins (Stenella frontalis) are the two most abundant cetacean species in the oceanic waters of Madeira and the Azores. They are of similar size, occur in similar habitats and are regularly observed in mixed-species groups to forage together. Genetic analyses suggested that, within each species, dolphins ranging around both archipelagos belong to the same panmictic population. We tested the hypotheses that (1) within each species, individuals from the two archipelagos belong to a single ecological stock; (2) between species, common and spotted dolphins have distinct trophic niches; using fatty acid (FA) and stable isotope (SI) analyses. Fatty acids and stable isotopes were analysed from 86 blubber and 150 skin samples of free-ranging dolphins, respectively. Sex-related differences were not significant, except for common dolphin FA profiles. In S. frontalis, FA and SI differences between archipelagos suggested that individuals belonged to different ecological stocks, despite the existence of gene flow between the two archipelagos. In D. delphis, differences were more pronounced, but it was not possible to distinguish between stock structure and a seasonal effect, due to differential sampling periods in the Azores and Madeira. Inter-specific comparisons were restricted to the Azores where all samples were collected during summer. Differences in FA proportions, noticeably for FA of dietary origin, as well as in nitrogen SI profiles, confirmed that both species feed on distinct resources. This study emphasizes the need for an integrated approach including both genetic and biochemical analyses for stock assessment, especially in wide-ranging marine top predators.     

Identifying oceanic foraging grounds of sea turtles in the Atlantic using lead isotopes

Many species of marine organisms go through ontogenetic shifts that occur in unknown or inaccessible locations. Finding these areas is crucial to understand connectivity and resilience of populations, both of which have conservation implications. When extrinsic markers are not suitable to track organisms, intrinsic markers can be useful to infer the location of inaccessible areas where these cryptic stages occur. Our study focuses on the location of oceanic foraging areas of the cryptic early juvenile stage of green turtles, Chelonia mydas, in the Atlantic. Due to the small size of hatchlings, the use of telemetry is limited to short periods of time and small spatial ranges, which do not allow determining the location of oceanic foraging areas. We used lead (Pb) stable isotopes to determine the possible location of oceanic foraging areas of small green turtles in the Atlantic Ocean. Pb stable isotope ratios in the scute tissue deposited when turtles were in the oceanic habitat were compared to ratios of major sources of lead in the Atlantic and oceanic areas in the Atlantic to determine the location of oceanic foraging grounds. The Pb isotope ratios in the scute of oceanic-stage green turtles indicated that turtles use different regions in the Atlantic and that they are capable of transatlantic migrations. We compare the oceanic locations identified by this study with those suggested by two previous studies.     

Feeding ecology of juvenile rockfishes off Oregon and Washington based on stomach content and stable isotope analyses

The feeding habits of pelagic, juvenile rockfishes (Sebastes spp.) collected off Oregon in 2002, and Oregon and Washington in 2006, were examined using stomach content and stable isotope analyses. Sampling occurred along a series of transects across the shelf between Crescent City, California (Lat. 41°54.0′), and Newport, Oregon (Lat. 44°39.0′), in 2002, and off Willapa Bay, Washington (Lat. 46°40.0′), and the Columbia River, Oregon (Lat. 46°10.0′), in 2006. Species composition varied both years with distance from shore, but the predominant species were darkblotched (Sebastes crameri), canary (S. pinniger), yellowtail (2006 only; S. flavidus), and widow (S. entomelas) rockfishes. Stomach content analysis revealed that darkblotched rockfish had highly variable diets, and canary, yellowtail, and widow rockfishes exhibited a high degree of overlap in 2006. Multivariate analysis showed significant differences in diet based on distance from shore where caught, fish size, and species. Stable isotope analysis indicated that all species were feeding at about the same trophic level within each year, with a 1.5 ‰ difference in δ¹⁵N between years and regions. The difference in δ¹⁵N values may indicate a greater contribution of mesotrophic zooplankton such as euphausiids, hyperiid amphipods, and chaetognaths to fish diets in 2006. Depleted ¹³C values were indicative of diets based on primary production from a more offshore origin, suggesting that these rockfish had previously inhabited offshore waters. These results add to our understanding of some of the important environmental factors that affect young-of-the-year rockfishes during their pelagic phase.     

Food web structure of a restored macroalgal bed in the eastern Korean peninsula determined by C and N stable isotope analyses

Loss of macroalgae habitats has been widespread on rocky marine coastlines of the eastern Korean peninsula, and efforts for restoration and creation of macroalgal beds have increasingly been made to mitigate these habitat losses. Deploying artificial reefs of concrete pyramids with kelps attached has been commonly used and applied in this study. As a part of an effort to evaluate structural and functional recovery of created and restored habitat, the macroalgal community and food web structure were studied about a year after the establishment of the artificial macroalgal bed, making comparisons with nearby natural counterparts and barren ground communities. Dominant species, total abundance, and community structure of macroalgal assemblage at the restored macroalgal bed recovered to the neighboring natural bed levels during the study period. The main primary producers (phytoplankton and macroalgae) were isotopically well separated. δ¹³C and δ¹⁵N values of consumers were very similar between restored and natural beds but varied greatly among functional feeding groups. The range of consumer δ¹³C was as wide as that of primary producers, indicating the trophic importance of both producers. There was a stepwise trophic enrichment in δ¹⁵N with increasing trophic level. A comparison of isotope signatures between primary producers and consumers showed that, while suspension feeders are highly dependent on pelagic sources, invertebrates of other feeding guilds and fishes mainly use macroalgae-derived organic matter as their ultimate nutritional sources in both macroalgal beds, emphasizing the high equivalency of trophic structure between both beds. Isotopic signatures of a few mollusks and sea urchins showed that they use different dietary items in macroalgal-barren grounds compared with macroalgal beds, probably reflecting their feeding plasticity according to the low macroalgal biomass. However, isotopic signatures of most of the consumers at the barren ground were consistent with those at the macroalgal beds, supporting the important trophic role of drifting algae. Our results revealed the recoveries of the macroalgal community and trophic structure at the restored habitat. Further studies on colonization of early settlers and the following succession progress are needed to better understand the process and recovery rate in the developing benthic community.     

Descriptive ecology of offshore,deep-water,benthic algae in the temperate western North Atlantic Ocean

The vertical distribution, floristic composition and habitat ecology of sublittoral, benthic algae are described for two deep water, offshore stations in the Gulf of Maine, based on in situ observations and collections to 47 m depth during SCUBA and submarine dives. Twenty species of macroscopic algae were collected between 29 and 45 m. These occurred in two benthic algal associations: a Ptilota serrata association of fleshy, almost exclusively red algae from 29 to 37 m; and a deeper Lithothamnium glaciale association dominated by encrusting corallines and extended from ca 38 m to the lowest limit of macroscopic vegetation at 44 to 45 m. Below 45 m only endozoic and epizoic diatoms associated with sponges were observed. Owing to the seasonal stability, homogeneous composition and clear extinction depths of the two associations, we propose that the extinction depth of benthic seaweeds may provide a useful bioassay for making temporal comparison of water conditions at a single geographic region and, where substrata are similar, spatially among different geographic regions. Data obtained during the Jeffreys Ledge study are discussed in relation to this hypothesis.     

Symbiosis between bacteria and oceanic clonal sea star larvae in the western North Atlantic Ocean

Bacteria were present in the majority of clonal sea star bipinnariae (Luidia sp.) collected between June 1987 and August 1990 from oceanic populations in the subtropical western North Atlantic Ocean. Light and electron microscopy revealed dense aggregations of bacteria within lobes of the epidermal cuticle in the gastric region of larvae. Gram-negative rods and less-common elongate spiral bacteria were observed, always in close association with branching epidermal microvilli. Intact and partially digested bacteria occurred in vesicles and phagosomes within epidermal cells, a probable indication of phagocytotic activity by the host. The association of larvae of Luidia sp. and bacteria ranged widely on both geographical and temporal scales. During July and August 1988, larvae were abundant (1.6 to 11.1 m³) in the mixed surface layer (<10 to 100 m) of stations in the Gulf Stream, the Sargasso Sea and the North Equatorial Drift, and 96% (mean of 5 stations, n=8 to 10 larvae in each station) of the individuals surveyed harbored bacteria beneath their cuticle. In a single station on the Florida Current sampled during winter, spring, and summer months between 1989 and 1991, 79 to 90% of the larvae harbored bacteria. The incidence of symbiosis was higher in actively cloning larvae than in non-cloning larvae. This is the first documentation of a symbiosis in field populations of echinoderm larvae.     

Migration,distribution, and diving behavior of adult male loggerhead sea turtles (<Emphasis Type="Italic">Caretta caretta</Emphasis>) following dispersal from a major breeding aggregation in the Western North Atlantic

Sixteen satellite-tagged adult male loggerhead sea turtles (Caretta caretta) dispersed widely from an aggregation near Port Canaveral, Florida, USA (28°23′N, −80°32′W) after breeding. Northbound males migrated further (990 ± 303 km) than southbound males (577 ± 168 km) and transited more rapidly (median initial dive duration = 6 (IQR = 4–16) versus 19 (IQR = 10–31) min, respectively).. Migration occurred along a depth corridor (20–40 m) except where constricted by a narrow continental shelf width. Males foraged in areas 27 ± 41 km² day⁻¹ at locations <1–80 km from shore for 100.1 ± 60.6 days, with variability in foraging patterns not explained by turtle size or geography. Post-breeding dispersal patterns were similar to patterns reported for adult female loggerhead sea turtles in this region and adult male loggerhead sea turtles elsewhere in the northern hemisphere; however, foraging ground distributions were most similar to adult female loggerhead sea turtles in this region.     

Temporal, spatial, and body size effects on growth rates of loggerhead sea turtles (Caretta caretta) in the Northwest Atlantic

In response to a call from the US National Research Council for research programs to combine their data to improve sea turtle population assessments, we analyzed somatic growth data for Northwest Atlantic (NWA) loggerhead sea turtles (Caretta caretta) from 10 research programs. We assessed growth dynamics over wide ranges of geography (9–33°N latitude), time (1978–2012), and body size (35.4–103.3 cm carapace length). Generalized additive models revealed significant spatial and temporal variation in growth rates and a significant decline in growth rates with increasing body size. Growth was more rapid in waters south of the USA (<24°N) than in USA waters. Growth dynamics in southern waters in the NWA need more study because sample size was small. Within USA waters, the significant spatial effect in growth rates of immature loggerheads did not exhibit a consistent latitudinal trend. Growth rates declined significantly from 1997 through 2007 and then leveled off or increased. During this same interval, annual nest counts in Florida declined by 43 % (Witherington et al. in Ecol Appl 19:30–54, 2009) before rebounding. Whether these simultaneous declines reflect responses in productivity to a common environmental change should be explored to determine whether somatic growth rates can help interpret population trends based on annual counts of nests or nesting females. Because of the significant spatial and temporal variation in growth rates, population models of NWA loggerheads should avoid employing growth data from restricted spatial or temporal coverage to calculate demographic metrics such as age at sexual maturity.     

Physiological ecology of picoplankton in the North Sea

The distribution of cyanobacteria in the surface waters of the North Sea was measured during July 1987. Numbers of cyanobacteria ranged from 2.5x10⁶ to 1.7x10⁸ cells 1^-1. In the majority of stations, cyanobacterial numbers were highest in the near-surface water and a subsurface maximum was found at only one station. The distribution of ¹⁴C among the end-products of photosynthesis was determined for picoplankton (<1 m) and other phytoplankton >1 m throughout the North Sea. The majority of label was found in the protein fraction of both picoplankton and >1 m phytoplankton; incorporation into lipids and polysaccharides plus nucleic acids was much lower. We interpret the large incorporation into protein to be a consequence of nutrient limitation of these natural assemblages. Photosynthetic parameters of the two size fractions were also determined. Assimilation number (P _m ^B ) and initial slope were greater for the picoplankton fraction than for phytoplankton >1 m but there was no evidence of significant photoinhibition of either fraction at irradiances up to 1 000 E m^-2 s^-1.     

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.     

Foraging in a variable environment: weather patterns and the behavioral ecology of baboons

We investigated the long-standing premise in behavioral ecology that the environment affects behavior and demography. We did this by evaluating the extent to which year-to-year variability in the behavioral ecology of a nonhuman primate population could be modeled from meteorological patterns. Data on activity profiles and home range use for baboons (Papio cynocephalus) in Amboseli, Kenya, were obtained over a 10-year period for three social groups: two completely wild-foraging ones, and a third that supplemented its diet with refuse from a nearby tourist lodge. The relationships across years among activity budgeting, travel distance, group size, and measures of temperature and rainfall patterns differed among the social groups. Although meteorological variation generally correlated with behavioral variation in the completely wild-foraging groups, different weather variables and direction of relationships resulted for each group. In addition, different relationships among variables were found before and after home-range shifts. The food-enhanced group spent half as much time foraging as did the other groups and therefore could be used to evaluate the relative extent to which foraging time was a limiting factor for resting and social time. Under their relaxed ecological conditions, the food-enhanced animals increased resting time much more than social time. These findings, combined with supplementary information on the population, lead us to suggest that baboons use a suite of interrelated responses to ecological variability that includes not only changes in activity budgets, but also home-range shifts, changes in the length of the active period, and changes in group size through fissions. Moreover, our results imply that group differences as well as interpopulational and interspecific differences in behavioral ecology provide significant sources of variability. Therefore, social groups rather than populations may be the appropriate unit of analysis for understanding the behavioral ecology of baboons and other highly social primates. The different patterns we observed among groups may have fitness consequences for the individuals in those groups and thereby affect population structure over time. Received: 18 February 1995/Accepted after revision: 6 January 1996     

Winter food utilisation by sympatric mysids in the Baltic Sea,studied by combined gut content and stable isotope analyses

We studied the winter dietary characteristics of two sympatric mysid species, Mysis mixta and M. relicta, which exploit both benthic and pelagic habitats during diel vertical migrations. Samples collected before and after the ice-covered period in the northern Baltic Sea were investigated using both stomach content analyses and stable isotope analyses of carbon and nitrogen. Both of the mysid species were omnivorous during winter and utilised both benthic and pelagic food sources. The main food source before the ice period was calanoid copepods (40 and 36% for M. mixta and M. relicta, respectively), and after ice-out calanoid copepods (23%) and zooplankton resting eggs (23%) for M. mixta and diatoms (44%) and calanoids (25%) for M. relicta. Their patterns of food utilisation broadly followed seasonal fluctuations in the abundance of the main prey groups. Although pelagic food availability is low in winter both mysid species utilised pelagic prey widely. We also show that when combining these different diet analysis methods it is important to take into account the time lag in isotopic signatures, otherwise the obtained results do not correspond but instead show the feeding history at different times.