Article

Isotope-based inferences of the seasonal foraging and migratory strategies of blue whales in the eastern Pacific Ocean

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  • CONACYT - Ensenada Center for Scientific Research and Higher Education
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Abstract

Migratory marine megafauna generally move vast distances between productive foraging grounds and environmentally stable breeding grounds, but characterizing how they use these habitats to maintain homeostasis and reproduce is difficult. We used isotope analysis of blue whale skin strata (n = 621) and potential prey (n = 300) to examine their migratory and foraging strategies in the eastern Pacific Ocean. Our results suggest that most whales in the northeast Pacific use a mixed income and capital breeding strategy, and use the California Current Ecosystem as their primary summer-fall foraging ground. A subset of individuals exhibited migratory plasticity and spend most of the year in the Gulf of California or Costa Rica Dome, two regions believed to be their primary winter-spring breeding grounds. Isotope data also revealed that whales in the southern Eastern Tropical Pacific generally do not forage in the northeast Pacific, which suggests a north-south population structure with a boundary near the equator

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... Consequently, some income breeding species with high energetic demands migrate long distances to access these productive foraging areas. For example, the population of blue whales (Balaenoptera musculus) in the northeast Pacific Ocean migrates seasonally and feeds year round in highly productive ecosystems like the California Current Ecosystem (summer-fall) (Palacios et al., 2019;Rockwood et al., 2020), the Gulf of California (winter-spring) (Gendron, 1992;Gendron, 2002;Sears et al., 2013;Busquets-Vass et al., 2021), and the Costa Rica Dome (winter-spring) (Mate et al., 1999) where seasonal aggregations of their primary prey (euphausiids) occur in high abundance (Gendron, 1992;Fiedler et al., 1998;Fiedler, 2002;Croll et al., 2005;Lluch-Cota et al., 2007;Matteson, 2009). In contrast to strict capital breeders that may fast for months on the wintering/breeding grounds (i.e., southern right whales, Eubalaena australis, Carroll et al., 2021), blue whales likely fast for short periods of time while transiting between summer and winter foraging grounds (Bailey et al., 2009). ...
... Studying the migratory and dietary strategies of baleen whales is challenging due to their wide range distribution and long dive patterns, which limit observation. The development of satellite tagging technology (Mate et al., 1999;Palacios et al., 2019) and analysis of intrinsic biomarkers (Busquets-Vass et al., 2017;Busquets-Vass et al., 2021) have emerged in response to the growing need for data on migratory marine mammal populations (Hobson, 1999;Newsome et al., 2010). ...
... Specifically, the use of stable isotope analysis (SIA) has increased exponentially in the past three decades to study the foraging ecology (Bentaleb et al., 2011;Witteveen et al., 2012;Fleming et al., 2016;Busquets-Vass et al., 2021), habitat use (Gendron et al., 2001;Gauffier et al., 2020), migratory patterns (Lee et al., 2005;Busquets-Vass et al., 2017), and physiology (Schell et al., 1989;Busquets-Vass et al., 2017) of this elusive taxonomic group. Several factors influence variation in carbon (d 13 C) and nitrogen (d 15 N) isotope values of animals, including: (1) spatial and temporal variation in the isotopic composition of the base of the food web can cascade up food chains to top consumers like marine mammals; (2) physiologically-mediated isotopic discrimination that occurs between a consumer and its diet; and (3) physiological controls on isotopic incorporation and growth rates for metabolically active and inactive tissues, respectively. ...
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Migration is a complex behavior that has evolved in multiple taxonomic groups as a means of accessing productive foraging grounds and environmentally stable areas suitable for reproduction. For migratory whales that forage throughout the year because of their high energetic demands, changes in the abundance of prey in different areas along their migratory route(s) can have serious implications for individual fitness and population viability. Thus, identifying the regions these species use to forage and breed while evaluating their migratory plasticity at the individual level can provide key information for their management and conservation. Serial stable isotope analysis of whale baleen, a continuously growing but metabolically inert tissue, has proven useful in generating individual migratory and foraging records over several years prior to death. We measured carbon ( δ ¹³ C) and nitrogen ( δ ¹⁵ N) isotope values along the length of baleen plates collected from thirteen blue whales of different sex and age classes, representing the largest collection analyzed to date in the northeast Pacific Ocean. Adult females exhibited relatively stable seasonal movements between temperate latitude foraging grounds and subtropical breeding grounds, although two skipped migration one year and subsequently moved to the same subtropical breeding ground near the Costa Rica Dome, potentially to give birth. Adult males exhibited two movement strategies with most remaining at temperate latitudes for 3-4 years before death, while two migrated to subtropical breeding grounds. In contrast, movement patterns in juveniles were erratic. These results are potentially driven by the energetic requirements during pregnancy and nursing in adult females, intra-specific competition among adult males, and inexperience in locating prey in juveniles. We also describe baleen δ ¹⁵ N patterns in recently weaned whales (<16.5m) that reflect switching from the consumption of milk to solid food (krill). In addition, baleen δ ¹³ C data suggest that weaned whales continue to use stored nutrients (blubber) acquired during the nursing period long after they are weaned. These results broaden our understanding of habitat selection in this species, highlight the importance of nursing for the critical period after weaning, and indicate that the Costa Rica Dome is an important calving region for this endangered population.
... Blue (Balaenoptera musculus) and gray (Eschrichtius robustus) whale populations from the eastern North Pacific (ENP) have been studied extensively over the past three decades. However, most postcommercial whaling studies have focused on photo-identification and population abundance, habitat, migration, and behavior (Busquets-Vass et al., 2021;Calambokidis & Barlow, 2020;Calambokidis & Perez, 2017;Calambokidis et al., 1990;Gendron et al., 2015;Lang et al., 2014;Paniagua-Mendoza et al., 2017). Much of the initial research on the physiology of blue and gray whales was conducted during commercial whaling (Mackintosh & Wheeler, 1929;Rice & Wolman, 1971), and updated with studies in the past decade Busquets-Vass et al., 2017;Hayden et al., 2017;Hunt et al., 2018;Lemos et al., 2020;Melica et al., 2021aMelica et al., , 2021bTrumble et al., 2013;Valenzuela-Molina et al., 2018). ...
... Much of the initial research on the physiology of blue and gray whales was conducted during commercial whaling (Mackintosh & Wheeler, 1929;Rice & Wolman, 1971), and updated with studies in the past decade Busquets-Vass et al., 2017;Hayden et al., 2017;Hunt et al., 2018;Lemos et al., 2020;Melica et al., 2021aMelica et al., , 2021bTrumble et al., 2013;Valenzuela-Molina et al., 2018). Feeding on lower trophic levels, these species play an important role in the ecosystems: on one hand, whales exercise top-down effects on prey abundances (Burnham & Duffus, 2016; on the other hand, they are the ultimate recipient of bottom-up driven systems (Busquets-Vass et al., 2021;Croll et al., 2005;Szesciorka et al., 2020). Therefore, their population dynamics can be affected by environmental changes and oceanographic perturbations (Calambokidis et al., 2009;Moore, 2008;Szesciorka et al., 2020). ...
... The GoC is the only studied reproductive area for this population, with about 300 whales estimated to be present annually between January and April, many of which are females sighted multiple times with calves (Busquets-Vass et al., 2017;Gendron, 2002;Paniagua-Mendoza et al., 2017;Valenzuela-Molina et al., 2018). Unlike other seasonal breeders, blue whales are not fasting while in the GoC (Gendron, 2002), which has been confirmed to be an important feeding area for the ENP population (Busquets-Vass et al., 2021). Our study complemented Atkinson et al. (2020) by evaluating hormone concentrations in blubber biopsies collected from important reproductive and feeding grounds for ENP blue whales, the GoC and the USWC, respectively. ...
Article
The goal of the present study was to carry out a thorough methodological validation and describe baseline profiles for glucocorticoid hormones (cortisol and corticosterone) in blubber from blue (n = 77) and gray (n = 103) whales from the eastern North Pacific Ocean. For each species, we modelled cortisol and corticosterone concentrations in response to life history parameters (age, sex, reproductive status) and season or geographic location. In blue whales, cortisol concentrations did not vary significantly by age class, sex, or reproductive status, whereas corticosterone was significantly lower in immature than in adult females (p < .001). In gray whales, cortisol concentrations were significantly higher in lactating whales (p < .05), while corticosterone was significantly different between females and males (p = .001) and elevated in calves (p = .003). In gray whales, corticosterone concentrations were significantly lower in males sampled later in the year (August to November) compared to both sexes sampled between March and August (p = .05), but no seasonal trend occurred in blue whales. Our results indicate that glucocorticoid actions vary between species and sex in large whales. Analysis of multiple hormones improves our understanding of the physiology of maintaining metabolic homeostasis or coping with chronic stressors.
... In this analysis reproductive class is lactating female, calf, or other (IDs that did not have a known sex or age class assigned); and proportion of image seen is the score on the three-point scale (see Supplementary Material for details) for the primary image being scored. Since blue whales are highly mobile (Calambokidis et al., 1990;Mate et al., 1999;Busquets-Vass et al., 2021) and body condition would be determined by feeding success over an extended period and range, we used a single annual average value for both the PDO and the LUSI. In each model the year was included as random effects to account for pseudoreplication. ...
... Other body condition studies have found that cows who are nursing their calves are in the worst condition of observed whales (Pettis et al., 2004;Bradford et al., 2012;Soledade Lemos et al., 2020). The high reproductive costs of nursing a mysticete whale calf has been well documented, as cows must consume enough during their feeding season to sustain themselves and their quickly growing calf while in calving grounds, although all North Pacific blue whales forage year-round (Busquets-Vass et al., 2021). Blue whale calves are nursed over a period of 7-8 months during which their size more than doubles (Mackintosh and Wheeler, 1929;Jefferson et al., 2015) and this period of lactation is the costliest part of reproduction, requiring 3-5 times more energy than gestation (Miller et al., 2012). ...
... It has been hypothesized that when foraging around California is poor due to decreased krill availability or increased competition, some blue whales may continue elsewhere to look for better foraging opportunities. It is likely that the pattern in blue whale body condition we observed results from a combination of some whales shifting foraging grounds and others being influenced by the feeding conditions off of California Busquets-Vass et al., 2021). ...
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Large marine mammals can serve as an indicator of the overall state of the environment due to their apex position in marine food webs and their functions as sentinels of change. Reductions in prey, driven by changes in environmental conditions can manifest in reduced fat stores that are visible on whales. We developed a non-invasive technique using photographs of blue whales taken on the US west coast from 2005-2018 (n=3,660) and scored body condition based on visible undulations from the vertebral processes and body shape. We analyzed patterns in the body condition of whales across years and their relation to oceanographic conditions. Females with calves had significantly poorer body conditions and calves had significantly better body conditions compared to other adult whales (Chi-Square, x2 = 170.36, df=6, p<2.2e-16). Year was a significant factor in body condition (Chi-Square, x2 = 417.73, df=39, p<0.001). The highest proportion of whales in poor body condition was observed for 2015 (one of the only two years along with 2017 where >50% had poor body condition) coincides with the marine heat wave that affected the NE Pacific 2014-2016. A cumulative mixed model examining the relationship between body condition and environmental variables revealed that negative Pacific Decadal Oscillation and longer upwelling seasons correlated with better blue whale body condition, likely to be due to higher primary productivity and prey availability. This study indicates that with an adequate scoring method, photographs collected during boat based surveys can be used to effectively evaluate whale health in response to a changing ocean.
... Multiple studies over time have shown the GC's food web to be enriched in 13 C and 15 N relative to the Pacific (e.g. Porras-Peters et al., 2008;Ruiz-Cooley et al., 2011;Aurioles-Gamboa et al., 2013;Richert et al., 2015;Ordiano-Flores et al., 2021), including studies that have analyzed the same tissue type from the same species in both regions (Elorriaga-Verplancken and Garcıá-Aguilar, 2018;Rosas-Hernańdez et al., 2018;Busquets-Vass et al., 2021). Fur from adult female California sea lions (Zalophus californianus) sampled in the Pacific off the central Baja California Peninsula had lower d 15 N values than those from the southwestern GC (17.8 ± 0.2‰ vs 20.7 ± 1.1‰, Elorriaga-Verplancken and Garcıá-Aguilar, 2018). ...
... In this case, the limited difference in nitrogen isotopic composition is likely due to the influence of denitrified waters off the southern extent of the Baja California Peninsula (Altabet et al., 1999). Skin tissue of filter-feeding blue whales (Balaenoptera musculus) was also significantly higher in the GC compared to the Pacific (14.8 ± 0.1‰ vs. 13.3 ± 0.1‰; Busquets-Vass et al., 2021). Therefore, the d 15 N values reported in these studies are consistent with the well-documented enrichment in 15 N within the GC, which is consistent among years. ...
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The conservation and management of highly migratory sharks relies on understanding age-related movements and nursery habitat utilization. We reconstructed the habitat use and migratory history of young White Sharks ( Carcharodon carcharias ), a highly protected species, by utilizing natural chemical tracers (element:Ca ratios and stable isotope analysis, SIA) in vertebral cartilage growth bands. Two nursery areas in the northeastern Pacific are known, but migration patterns of immature White Sharks within the Gulf of California (GC) and natal philopatry are poorly understood. Vertebrae from coastal Mexican artisanal fisheries off central Baja California in the Pacific (12 neonates and juveniles; 139-280 cm total length) and the GC (3 subadults; 289-355 cm TL) were analyzed to characterize (1) trophic histories from collagen δ ¹³ C and δ ¹⁵ N values, and (2) in utero patterns and post-birth environmental histories from element:Ca time-series. Mean δ ¹⁵ N values from vertebral edges of GC sharks, representing the most recent feeding, was +5‰ higher than in the Pacific, reflecting the intense denitrification that permeates the regional food web and supporting SIA as tracers of migration between regions. A subadult from the GC likely resided within the system throughout its life, and two subadults migrated into the GC. Most neonate and juvenile sharks caught in the Pacific had SIA that did not overlap with those of the GC, but a single subadult likely migrated to the GC. Element:Ca ratios displayed ontogenetic trends, with Li:Ca, Zn:Ca, and Ba:Ca significantly higher before the birth mark in sharks captured in the GC. Edge values were significantly higher in Zn:Ca and Ba:Ca in the GC compared to the Pacific, suggesting elemental ratios may serve as tracers of migration between regions. Subadult sharks collected from GC displayed elevated maternal Zn:Ca and Ba:Ca, suggesting mothers may have resided in the GC for an extensive period pre-birth. Some White Sharks may reside within the GC from birth until at least the subadult stage (ca. 3 m TL), and there may be an unidentified nursery. Chemical tracers, coupled with genomic and tagging studies, should improve understanding of the importance of the GC to White Shark populations in the northeast Pacific.
... Stable isotope analysis (SIA) is commonly applied in studies investigating the feeding habits, foraging areas, and movement patterns of mobile and elusive organisms like marine mammals (e.g., Kiszka et al., 2014;Troina et al., 2020Troina et al., , 2021Busquets-Vass et al., 2021). This method is based on the principle that the naturally occurring variation in the stable isotope composition observed in consumer tissues reflects the isotopic composition of their assimilated prey. ...
Article
We analyzed δ13C and δ15N values in different tooth portions (Growth Layer Groups, GLGs) of franciscanas, Pontoporia blainvillei, to investigate their effect on whole tooth (WT) isotopic values and the implications for dietary estimates. Tooth portions included the dentin deposited during the prenatal development (PND), the first year of life (GLG1) deposited during the nursing period and the central part of the tooth with no distinction amongst subsequent GLGs (Center). Isotopic mixing models estimating the contribution of PND, GLG1 and Center to WT showed that GLG1 has a strong effect on WT isotope values in juveniles, while Center only starts to affect WT isotopic values from age four. Isotopic mixing models estimating prey contribution to the diet of juveniles using WT vs Center tooth portions significantly differed in dietary outputs, demonstrating that GLG1 influence on WT isotope values affects dietary estimates in young franciscanas. As the small tooth size and narrowness of the last GLGs hinder the analysis of individual layers, we recommend excluding GLG1 in studies based on teeth isotope composition in franciscanas and caution when interpreting isotopic values from the WT of other small cetaceans.
... The potentially high levels of feeding plasticity highlighted in this study requires further investigations, with a specific focus on the analysis of the isotopic composition of all gray whale possible prey items. As it is already suggested for other baleen whale species, as the humpback 91 , fin 92,93 and blue 29,93 whale, our results suggest that gray whale could limit fasting to certain periods. If this is true, other sources than those examined here could contribute importantly to the reproductive success of this species. ...
Article
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Eastern gray whales’ distribution range and plasticity in feeding behavior complicates the understanding of critical life-history such as pregnancy and lactation. Our goal was to determine if females who experienced gestation, gave birth, and lactated their calves, assimilated a high proportion of benthic amphipods from the Bering Sea, which are considered the species’ main prey. We used Bayesian stable isotope mixing models to estimate the probability of contribution of food items sampled along the species’ distributional range, using isotopic data on amphipods from the Bering Sea, mysids from Vancouver Island, and amphipods and polychaetes from Ojo de Liebre Lagoon. We sampled epidermal tissue from lactating females (n = 25) and calves (n = 34) and analyzed their carbon and nitrogen isotopic composition. Model outcome indicated that benthic amphipods from the Bering Sea were not the primary food for the eastern gray whale. Each mother performed a different feeding strategy, and prey from Vancouver Island were generally as important as that from the Bering Sea. Moreover, model results indicate a constant use of Ojo de Liebre Lagoon as a feeding ground. Our results appear to agree with previous studies that report continuous feeding by females to satisfy certain physiological requirements (e.g., fatty acids omega-6) during migration and breeding time. Future investigations of the isotopic composition of all those prey items that could be assimilated by the eastern gray whale emerge as critical. Both historical and recent information, that would provide insights in the species feeding ecology under past and present environmental conditions, should be considered as equally important to establish conservation and management plans.
... Biological tissues archived in scientific collections provide a unique opportunity to assess historical shifts in diet, habitat preference, and migratory movements (e.g., Borrell et al., 2018;Busquets-Vass et al., 2020). Despite its potential for comparing historic and modern specimens, researchers should be aware that archived tissues are usually preserved in formalin, dimethyl sulfoxide (DMSO) buffer, 70% ethanol (EtOH), or formalin-EtOH, which can have different effects on δ 13 C and δ 15 N values (Lesage et al., 2010;Logan et al., 2008). 2 | METHODS ...
Article
Trophic ecology information about cetaceans is essential to understand their role in ecosystem dynamics. Stable isotope analysis is a valuable complementary approach to conventional methods usually applied to the study of the foraging behavior of cetaceans because it provides dietary information over different time scales and can potentially use tissues archived in scientific collections. However, the considerable increase in stable isotope analysis by a growing number of cetacean research groups demands the use of proper protocols to ensure that accurate isotopic data are obtained. We provide a theoretical background of stable isotope analysis and its application to assess cetaceans‘ trophic ecology. We review the factors that can influence isotopic measurements and propose a practical guideline with suitable techniques for sample preparation of biological tissues to be employed by researchers to yield reliability in the interpretation of isotopic data. We summarized the main assumptions and inherent limitations that can lead to confounding interpretations of isotopic data, such as species‐ and tissue‐specific discrimination factors, temporal or spatial variation in prey, and baseline isotopic values in the context of cetacean ecology. Our detailed review offers important guidance for researchers who want to use stable isotope analysis to address different ecological questions with cetacean species. A practical guide on stable isotope analysis for cetacean research.
... The reproductive grounds are less known, where the Gulf of California (GoC) is the only studied reproductive area for this population, with about 300 whales annually present between January and April (Gendron, 2002). Stable isotopes analysis has also shown that blue whales do forage in the GoC, indicating this is a feeding-reproductive ground (Busquets-Vass et al., 2021). Confirmation that these whales are part of the ENP population came from photo ID matches (Calambokidis et al., 1990), satellite tags (Bailey et al., 2010), genetics (Costa-Urrutia et al., 2013), acoustics (Paniagua-Mendoza et al., 2017;Stafford et al., 2001) and stable isotope analyses (Busquets-Vass et al., 2017). ...
Article
The goal of the present study was to complement existing data of testosterone and progesterone in blue whale (Balaenoptera musculus) blubber from the eastern North Pacific Ocean to evaluate effects of seasonality and location on these hormones, and to better assess reproductive status of individuals. Physiological parameters regarding reproduction are fundamental for describing population dynamics, and hormones can be a valid tool to estimate those for wildlife populations. In this study, blubber tissue was validated for testosterone and progesterone assays. Hormone concentrations were measured in 69 (35 males and 34 females) blubber samples from live (n= 66) and stranded (n= 3) animals collected between 2002 and 2016 from a known winter reproductive ground in the Gulf of California (GoC) and summer feeding areas along the United States West Coast (USWC), specifically off the states of California and Oregon. Results were combined with sighting histories as a tool to determine reproductive status of individual whales. Testosterone concentrations in adult male blue whales were significantly higher (p< 0.05) in blubber biopsies sampled off the USWC between the months of June and November compared to those sampled in the GoC between February and April. Elevated testosterone concentrations likely indicate physiological preparation for reproductive activity while the animals were present off the USWC. Progesterone concentrations were significantly elevated in pregnant females, confirming progesterone as an indicator of pregnancy in blue whales. Probabilities of being pregnant were estimated for adult females with unknown sighting histories based on progesterone concentrations. Testosterone in females was detected and measured only in pregnant whales suggesting its biosynthesis or metabolism is altered during gestation. These results provide updated and new information on the reproductive cycle of blue whales in the eastern North Pacific, posing new milestones to better estimate the timing of the mating season for this endangered population.
Thesis
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In this study, the trophic structure of the pelagic copepod community was analyzed in six geographical zones in the eastern tropical Pacific Ocean. Zooplankton samples were collected on two oceanographic cruises from August to December 2003 using a bongo cone net (333 μm mesh light). The isotopic signatures were measured as δ¹⁵N and δ¹³C in twelve selected species based on their dominance and their feeding types. We observed a significant latitudinal gradient in δ¹⁵N values, generally increasing northwards. The values of δ¹³C isotopes did not show a significant longitudinal gradient, but geographical differences occurred in some species. Pleuromamma robusta was recognized as the species with the highest trophic position in the copepod community. In general, there was a positive relationship between average body size and trophic position, except for the herbivorous species Eucalanus inermis, which was detected in the lowest trophic position. The isotopic niche was similar for each of the 12 species of copepods studied, but in most cases, the niche overlap between each pair of species was low and not higher than 50%. While the differences in isotopic signatures can be attributed mainly to the dominant nutrient sources in each zone, the low trophic niche overlap may be explained by the differential spatial distribution of species, reducing competition for food resources.
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The ongoing evolution of tracer mixing models has resulted in a confusing array of software tools that differ in terms of data inputs, model assumptions, and associated analytic products. Here we introduce MixSIAR, an inclusive, rich, and flexible Bayesian tracer (e.g., stable isotope) mixing model framework implemented as an open-source R package. Using MixSIAR as a foundation, we provide guidance for the implementation of mixing model analyses. We begin by outlining the practical differences between mixture data error structure formulations and relate these error structures to common mixing model study designs in ecology. Because Bayesian mixing models afford the option to specify informative priors on source proportion contributions, we outline methods for establishing prior distributions and discuss the influence of prior specification on model outputs. We also discuss the options available for source data inputs (raw data versus summary statistics) and provide guidance for combining sources. We then describe a key advantage of MixSIAR over previous mixing model software-the ability to include fixed and random effects as covariates explaining variability in mixture proportions and calculate relative support for multiple models via information criteria. We present a case study of Alligator mississippiensis diet partitioning to demonstrate the power of this approach. Finally, we conclude with a discussion of limitations to mixing model applications. Through MixSIAR, we have consolidated the disparate array of mixing model tools into a single platform, diversified the set of available parameterizations, and provided developers a platform upon which to continue improving mixing model analyses in the future.
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Background The most traditional scheme for migration among baleen whales comprises yearly migrations between productive waters at high latitude summer feeding grounds and warmer waters at lower latitudes where whales calve and mate, but rarely feed. Evidence indicates, however, that large departures from this scheme exist among populations and individuals. Furthermore, for some populations there is virtually no information on migratory pathways and destinations. Such is the case of Chilean blue whales throughout the Eastern South Pacific; hence, the goal of this study was to assess its migratory behavior. Methods Dedicated marine surveys and satellite tagging efforts were undertaken during the austral summer and early autumn on blue whale feeding grounds off Chilean Northern Patagonia (CNP) during 2013, 2015 and 2016. Positional data derived from satellite tags regarding movement patterns and behavior were analyzed using Bayesian switching first-difference correlated random walk models. Results We instrumented 10 CNP blue whales with satellite transmitters and documented individual variation in departure time, northbound migratory routes and potential wintering grounds. The onset of migration occurred from mid/late austral autumn to well into the austral winter. Blue whales moved in various directions, but ultimately converged toward a general NW movement direction along a wide corridor exceeding 2,000 km. Area-Restricted Search behavior was exhibited within fjords and channels of CNP and also South of Galapagos Archipelago (GA) and northern Peru, but never during migration. Interestingly, dive profiles for one whale that reached GA showed a sharp and consistent increase in depth north of 5°S and extreme deep dives of up to 330 m. Discussion Information derived from satellite tagged blue whales in this study is the first of its kind off the Eastern Southern Pacific. Our results provide valuable information on their migratory timing, routes and behavior on their northbound migration, particularly regarding the varied migratory plasticity for this particular population. Our results also highlight the first record of two complete migratory paths between CNP and GA and strengthen the hypothesis that GA waters correspond to a potential wintering destination for CNP blue whales. We further hypothesize that this area might be selected because of its biological productivity, which could provide feeding opportunities during the breeding season. Our results suggest that special efforts should be put forward to identify blue whale critical areas and understand key behavioral aspects in order to provide the basis for their conservation on a regional context (i.e., reducing potential ship strike and promote Marine Protected Area (MPA) implementation in Chile, Ecuador and Peru). Indeed, we suggest joint blue whale conservation efforts at the regional level in order to identify and determine potential threats and impacts and, most importantly, implement prospective management actions.
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Integrating behavior and physiology is critical to formulating new hypotheses on the evolution of animal life-history strategies. Migratory capital breeders acquire most of the energy they need to sustain migration, gestation, and lactation before parturition. Therefore, when predicting the impact of environmental variation on such species, a mechanistic understanding of the physiology of their migratory behavior is required. Using baleen whales as a model system, we developed a dynamic state variable model that captures the interplay among behavioral decisions, energy, reproductive needs, and the environment. We applied the framework to blue whales (Balaenoptera musculus) in the eastern North Pacific Ocean and explored the effects of environmental and anthropogenic perturbations on female reproductive success. We demonstrate the emergence of migration to track prey resources, enabling us to quantify the trade-offs among capital breeding, body condition, and metabolic expenses. We predict that periodic climatic oscillations affect reproductive success less than unprecedented environmental changes do. The effect of localized, acute anthropogenic impacts depended on whales’ behavioral response to the disturbance; chronic, but weaker, disturbances had little effect on reproductive success. Because we link behavior and vital rates by modeling individuals’ energetic budgets, we provide a general framework to investigate the ecology of migration and assess the population consequences of disturbance, while identifying critical knowledge gaps.
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Stable isotope analysis in mysticete skin and baleen plates has been repeatedly used to assess diet and movement patterns. Accurate interpretation of isotope data depends on understanding isotopic incorporation rates for metabolically active tissues and growth rates for metabolically inert tissues. The aim of this research was to estimate isotopic incorporation rates in blue whale skin and baleen growth rates by using natural gradients in baseline isotope values between oceanic regions. Nitrogen (δ 15 N) and carbon (δ 13 C) isotope values of blue whale skin and potential prey were analyzed from three foraging zones (Gulf of Cali-fornia, California Current System, and Costa Rica Dome) in the northeast Pacific from 1996–2015. We also measured δ 15 N and δ 13 C values along the lengths of baleen plates collected from six blue whales stranded in the 1980s and 2000s. Skin was separated into three strata: basale, externum, and sloughed skin. A mean (±SD) skin isotopic incorporation rate of 163±91 days was estimated by fitting a generalized additive model of the seasonal trend in δ 15 N values of skin strata collected in the Gulf of California and the California Current System. A mean (±SD) baleen growth rate of 15.5±2.2 cm y-1 was estimated by using seasonal oscillations in δ 15 N values from three whales. These oscillations also showed that individual whales have a high fidelity to distinct foraging zones in the northeast Pacific across years. The absence of oscillations in δ 15 N values of baleen sub-samples from three male whales suggests these individuals remained within a specific zone for several years prior to death. δ 13 C values of both whale tissues (skin and baleen) and potential prey were not distinct among foraging zones. Our results highlight the importance of considering tissue isotopic incorporation and growth rates when studying migratory mysticetes and provide new insights into the individual movement strategies of blue whales.
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Natural-abundance stable isotope ratios provide a wealth of ecological information relating to food web structure, trophic level, and location. The correct interpretation of stable isotope data requires an understanding of spatial and temporal variation in the isotopic compositions at the base of the food web. In marine pelagic environments, accurate interpretation of stable isotope data is hampered by a lack of reliable, spatio-temporally distributed measurements of baseline isotopic compositions. In this study, we present a relatively simple, process-based carbon isotope model that predicts the spatio-temporal distributions of the carbon isotope composition of phytoplankton (here expressed as δ13CPLK) across the global ocean at one degree and monthly resolution. The model is driven by output from a coupled physics-biogeochemistry model, NEMO-MEDUSA, and operates offline; it could also be coupled to alternative underlying ocean model systems. Model validation is challenged by the same lack of spatio-temporally explicit data that motivates model development, but predictions from our model successfully reproduce major spatial patterns in carbon isotope values observed in zooplankton, and are consistent with simulations from alternative models. Model predictions represent an initial hypothesis of spatial and temporal variation in carbon isotopic baselines in ocean areas where a few data are currently available, and provide the best currently available tool to estimate spatial and temporal variation in baseline isotopic compositions at ocean basin to global scales.
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Cetacean energy stores are known to vary according to life history, reproductive status and time of year; however, the opportunity to quantify these relationships is rare. Using a unique set of historical whaling records from Western Australia (1952–1963), we investigated energy stores of large cetaceans with differing life histories, and quantified the relationship between total body lipid and length for humpback whales (Megaptera novaeangliae) (n = 905) and sperm whales (Physeter macrocephalus) (n = 1961). We found that total body lipid increased with body length in both humpback and sperm whales, consistent with size-related energy stores. Male humpback whales stored 2.49 kl (15.6 barrels) (31.9–74.9%) more lipid than male sperm whales of equivalent length, to fuel their annual migration. Relative lipid stores of sperm whales (males) were constant throughout the year, while those of humpback whales varied with reproductive class and sampling date. Pregnant female humpback whales had higher relative energy stores than non-pregnant females and males (26.2% and 37.4%, respectively), to fuel the energy demands of gestation and lactation. Those that reached the sampling site later (en route to their breeding grounds) carried higher lipid stores than those that arrived earlier, possibly reflecting individual variation in residency times in the Antarctic feeding grounds. Importantly, longer pregnant females had relatively larger energy stores than the shorter pregnant females, indicating that the smaller individuals may experience higher levels of energetic stress during the migration fast. The relationships we developed between body lipid and length can be used to inform bioenergetics and ecosystem models when such detailed information is not available.
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Since 1970, blue whales (Balaenoptera musculus) have been seen feeding in the waters off southern Chile during the summer and autumn (December to May). Investigation of the genetic, acoustic and morphological characteristics of these blue whales shows that they are a distinct but unnamed subspecies, called the Chilean blue whales. Photo-identification surveys have been conducted in the waters off northwestern Isla Grande de Chiloé , southern Chile from 2004–2012 and Isla Chañaral, central Chile in 2012. Over this time, 1,070 blue whales were encountered yielding, after photo-quality control, 318 and 267 unique photographs of the left and right side of the flank respectively. Using mark-recapture analysis of left and right side photographs collected from Isla Grande de Chiloé (2004–2012), open population models estimate that ~570–760 whales are feeding seasonally in this region. POPAN superpopulation abundance estimates for the same feeding ground in 2012 are 762 (95% confidence intervals, CI = 638–933) and 570 (95% CI 475–705) for left and right side datasets respectively, very similar to results from closed population models. Estimates of trend revealed strong variation in abundance, peaking in 2009 and [suggesting] fluctuating use in the survey area over time, likely related to the density of their prey. High inter-annual return rates suggest a degree of site-fidelity of individuals to Isla Grande de Chiloé and that the number of whales using this feeding ground is relatively small.
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Mixing models are statistical tools that use biotracers to probabilistically estimate the contribution of multiple sources to a mixture. These biotracers may include contaminants, fatty acids, or stable isotopes, the latter of which are widely used in trophic ecology to estimate the mixed diet of consumers. Bayesian implementations of mixing models using stable isotopes (e.g. MixSIR, SIAR) are regularly used by ecologists for this purpose, but basic questions remain about when each is most appropriate. In this study, we describe the structural differences between common mixing model error formulations in terms of their assumptions about the predation process. We then introduce a new parameterization that unifies these mixing model error structures, as well as implicitly estimates the rate at which consumers sample from source populations (i.e. consumption rate). Using simulations and previously published mixing model datasets, we demonstrate that the new error parameterization outperforms existing models and provides an estimate of consumption. Our results suggest that the error structure introduced here will improve future mixing model estimates of animal diet. This article is protected by copyright. All rights reserved.
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Most otariids have colony-specific foraging areas during the breeding season, when they behave as central place foragers. However, they may disperse over broad areas after the breeding season and individuals from different colonies may share foraging grounds at that time. Here, stable isotope ratios in the skull bone of adult Galapagos sea lions (Zalophus wollebaeki) were used to assess the long-term fidelity of both sexes to foraging grounds across the different regions of the Galapagos archipelago. Results indicated that the stable isotope ratios (δ13C and δ15N) of sea lion bone significantly differed among regions of the archipelago, without any significant difference between sexes and with a non significant interaction between sex and region. Moreover, standard ellipses, estimated by Bayesian inference and used as a measure of the isotopic resource use area at the population level, overlapped widely for the sea lions from the southern and central regions, whereas the overlap of the ellipses for sea lions from the central and western regions was small and non-existing for those from the western and southern regions. These results suggest that males and females from the same region within the archipelago use similar foraging grounds and have similar diets. Furthermore, they indicate that the exchange of adults between regions is limited, thus revealing a certain degree of foraging philopatry at a regional scale within the archipelago. The constraints imposed on males by an expanded reproductive season (~ 6 months), resulting from the weak reproductive synchrony among females, and those imposed on females by a very long lactation period (at least one year but up to three years), may explain the limited mobility of adult Galapagos sea lions of both sexes across the archipelago.
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Large, migratory predators are often cited as sentinel species for ecosystem processes and climate related changes, but their utility as indicators is dependent upon an understanding of their response to environmental variability. Documentation of the links between climate variability, ecosystem change and predator dynamics is absent for most top predators. Identifying species that may be useful indicators and elucidating these mechanistic links provides insight into current ecological dynamics, and may inform predictions of future ecosystem responses to climatic change. We examine humpback whale response to environmental variability through stable isotope analysis of diet over a dynamic twenty year period (1993-2012) in the California Current System (CCS). Humpback whale diets captured two major shifts in oceanographic and ecological conditions in the CCS. Isotopic signatures reflect a diet dominated by krill during periods characterized by positive phases of the North Pacific Gyre Oscillation (NPGO), cool sea-surface temperatures, strong upwelling, and high krill biomass. In contrast, humpback whale diets are dominated by schooling fish when the NPGO is negative, sea surface temperatures are warmer, seasonal upwelling is delayed and anchovy and sardine populations display increased biomass and range expansion. These findings demonstrate that humpback whales trophically respond to ecosystem shifts and as a result, their foraging behavior is a synoptic indicator of oceanographic and ecological conditions across the CCS. Multi-decadal examination of these sentinel species thus provides insight into biological consequences of interannual climate fluctuations, fundamental to advancing ecosystem predictions related to global climate change. This article is protected by copyright. All rights reserved.
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Consumer foraging behaviors are dynamic, changing in response to prey availability, seasonality, competition, and even the physiological states of the consumers. The isotopic composition of a consumer is a product of these factors as well as the isotopic landscape of its prey, i.e. the isotopic mixing space. Here we build a mechanistic framework that links the ecological and physiological processes of an individual consumer to the isotopic distribution that describes its diet, and ultimately to the isotopic composition of its own tissues, defined as its isotopic niche. By coupling these processes, we systematically investigate under what conditions the isotopic niche of a consumer changes as a function of both the geometric properties of its mixing space and foraging strategies that may be static or dynamic over time. Results of our analytical derivations reveal general insight into the conditions that impact isotopic niche width as a function of consumer specialization on prey, as well as its ability to transition between diets over time. We show analytically that moderate specialization on isotopically unique prey can serve to maximize a consumer's isotopic niche width, while temporally dynamic diets will tend to result in peak isotopic variance during dietary transitions. We demonstrate the relevance of our theoretical findings by examining a marine system composed of nine invertebrate species commonly consumed by sea otters. In general, our analytical framework highlights the complex interplay of mixing space geometry and consumer dietary behavior in driving expansion and contraction of the isotopic niche. Because this approach is established on ecological mechanism, it is well-suited for enhancing the ecological interpretation, and uncovering the root causes, of observed isotopic data.
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During summer 2010, we investigated phytoplankton production and growth rates at 19 stations in the eastern tropical Pacific, where winds and strong opposing currents generate the Costa Rica Dome (CRD), an open-ocean upwelling feature. Primary production (14C-incorporation) and group-specific growth and net growth rates (two-treatment seawater dilution method) were estimated from samples incubated in situ at eight depths. Our cruise coincided with a mild El Niño event, and only weak upwelling was observed in the CRD. Nevertheless, the highest phytoplankton abundances were found near the dome center. However, mixed-layer growth rates were lowest in the dome center (∼0.5–0.9 day−1), but higher on the edge of the dome (∼0.9–1.0 day−1) and in adjacent coastal waters (0.9–1.3 day−1). We found good agreement between independent methods to estimate growth rates. Mixed-layer growth rates of Prochlorococcus and Synechococcus were largely balanced by mortality, whereas eukaryotic phytoplankton showed positive net growth (∼0.5–0.6 day−1), that is, growth available to support larger (mesozooplankton) consumer biomass. These are the first group-specific phytoplankton rate estimates in this region, and they demonstrate that integrated primary production is high, exceeding 1 g C m−2 day−1 on average, even during a period of reduced upwelling.
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Blue whales (Balaenoptera musculus) were among the most intensively exploited species of whales in the world. As a consequence of this intense exploitation, blue whale sightings off the coast of Chile were uncommon by the end of the 20th century. In 2004, a feeding and nursing ground was reported in southern Chile (SCh). With the aim to investigate the genetic identity and relationship of these Chilean blue whales to those in other Southern Hemisphere areas, 60 biopsy samples were collected from blue whales in SCh between 2003 and 2009. These samples were genotyped at seven microsatellite loci and the mitochondrial control region was sequenced, allowing us to identify 52 individuals. To investigate the genetic identity of this suspected remnant population, we compared these 52 individuals to blue whales from Antarctica (ANT, n = 96), Northern Chile (NCh, n = 19) and the eastern tropical Pacific (ETP, n = 31). No significant differentiation in haplotype frequencies (mtDNA) or among genotypes (nDNA) was found between SCh, NCh and ETP, while significant differences were found between those three areas and Antarctica for both the mitochondrial and micro-satellite analyses. Our results suggest at least two breeding population units or sub-species exist, which is also supported by other lines of evidence such as morphometrics and acoustics. The lack of differences detected between SCh/NCh/ETP areas supports the hypothesis that eastern South Pacific blue whales are using the ETP area as a possible breeding area. Considering the small population sizes previously reported for the SCh area, additional conservation measures and monitoring of this population should be developed and prioritized.
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The Gulf of California has three main natural fertilization mechanisms: upwelling, tidal mixing, and water exchange with the Pacific Ocean. Waters high in nutrients occur at very shallow depths in the gulf, and little energy is required for these nutrients to reach the euphotic zone. Upwelling off the eastern coast is strong, chlorophyll a concentration (Chl) can exceed 10 mg m-3 , and because of eddy circulation it increases the phytoplankton biomass across the gulf. Because of strong stratification during summer, upwelling off the western coast causes Chl to increase only to ∼ 0.5 mg m-3 . The annual cycle is the dominant mode of Chl variability in most of the gulf. El Niño events cause the suppression of Chl mostly in areas on the eastern side of the central and southern gulf, with the effect decreasing from the mouth to the central gulf. 14C data show that highest productivities occur during winter – spring, and in the Guaymas Basin (up to > 4 g C m-2 day-1 ). Averages of total integrated production (PTint ) for “ winter” and for whole regions within the gulf estimated from satellite imagery are in good agreement with averages of 14C estimates (∼1.8 g C m-2 day-1 ). PTint values for “ summer ” are ∼30% of those for “ winter.”
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Because consumers integrate components of their habitat through diet over time and space, stable isotope ratios from animal tissues can track spatial variation in baseline values across marine systems. To understand large-scale geographic patterns in the eastern Pacific ocean, muscle δ13C and δ15N from epi-mesopelagic squid (n = 404) were collected from 39° S to 53° N and analyzed in relation to hemisphere, latitude, geographic area and current systems. Geographic patterns were controlled for effects of secondary factors such as squid size, species (Dosidicus gigas and Sthenoteuthis oualaniensis), tissue and year of collection. Joint latitudinal variation of δ13C and δ15N was also described for the first time. Both δ13C and δ15N, as well as the standardized difference between them, had distinct patterns by latitude. δ13C was the highest at 22°S and decreased north and south of that latitude, with lower values at mid-northern latitudes than near the equator. δ15N had the lowest values near the equator and gradually increased towards mid-latitudes. The standardized difference between δ13C and δ15N was highest (C was higher relative to N) near the equator and declined to mid-latitudes. Overall, the δ13C and δ15N geographic patterns agreed with previous studies for δ15N from surface NO3−, but not for δ13C in plankton, POM and squid. We suggest that the biochemical processes for carbon and nitrogen are spatially more variable than what has previously been reported because squid isotope ratios varied also among current systems and geographic areas. These geographic patterns in δ13C and δ15N, indicated by consumers such as cephalopods, could improve our understanding about the interaction between the carbon and nitrogen cycle and the heterogeneity in biochemical cycling processes in marine systems. Read More: http://www.esajournals.org/doi/abs/10.1890/ES12-00094.1
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Stable nitrogen and carbon isotope analyses have increasingly been used to investigate the foraging ecology of marine mammals, particularly in response to the limitations of using conventional dietary analysis techniques. In this study, we compared nitrogen (δ 15 N) and carbon (δ 13 C) values of four different tissues (i.e., fur, red blood cells, serum, and plasma) from California sea lions (Zalophus californianus; n = 58) of various age classes (i.e., pup, yearling, juvenile, and adult). Metabolically active tissues with relatively high turnover rates (plasma and serum) had similar δ 15 N and δ 13 C values, but these two tissues had significantly higher δ 15 N values and lower δ 13 C values in comparison to red blood cells or fur. In general, δ 15 N values decreased with increasing age; δ 15 N values for pups were between 1.2‰ (fur) to 2.0‰ (serum) greater in comparison to adult females. In general, δ 13 C values increased with age (except red blood cells). Pups had mean δ 13 C values that were 0.4‰ (plasma) to 0.5‰ (fur and serum) lower than mean values of adult females. Stable isotope analysis of various tissues can provide dietary information at the individual level on different temporal and spatial scales, as well as reveal patterns of the foraging ecology among groups of animals.
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The unique physical and biogeochemical characteristics of oxygen minimum zones (OMZs) influence plankton ecology, including zooplankton trophic webs. Using carbon and nitrogen stable isotopes, this study examined zooplankton trophic webs in the Eastern Tropical North Pacific (ETNP) OMZ. δ13C values were used to indicate zooplankton food sources, and δ15N values were used to indicate zooplankton trophic position and nitrogen cycle pathways. Vertically stratified MOCNESS net tows collected zooplankton from 0 to 1000 m at two stations along a north-south transect in the ETNP during 2007 and 2008, the Tehuantepec Bowl and the Costa Rica Dome. Zooplankton samples were separated into four size fractions for stable isotope analyses. Particulate organic matter (POM), assumed to represent a primary food source for zooplankton, was collected with McLane large volume in situ pumps.
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Knowledge of reproduction in baleen whales such as the blue whale Balaenoptera musculus is still limited. Here, we combined the sighting histories of 24 yr of reproductively active female blue whales from the United States (US) west coast and the Gulf of California (GoC), Mexico. The latter region is a nursing ground for some of the blue whales that feed off the US west coast during the summer months. We report here that females show site fidelity to the GoC even when not lactating. The mean calving interval based on consecutive sighting histories was 2.57 yr. Two female calves returned with their own offspring after 11 and 13 yr, indicating an apparent age of first parturition of >10 yr. While 60% of females identified in the GoC were also sighted off the US west coast, only 30% of the females from the latter area were seen in the GoC. Thus only a part of the US Californian population migrates to the GoC, suggesting the existence of additional calving and nursing grounds for this population. Despite the presence of killer whales, female blue whales presumably migrate to the GoC to benefit from high prey abundance. The lack of documented births in the GoC may indicate that female blue whales choose open, pelagic waters for calving and move to the GoC when the calves are older. Cite this article as: Sears R, Ramp C, Douglas AB, Calambokidis J (2013) Reproductive parameters of eastern North Pacific blue whales Balaenoptera musculus. Endang Species Res 22:23-31 Export citation: Endnote - Reference Manager Mail this link - Contents Mailing Lists - RSS - Tweet - lang: en_US
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Humpback whales are considered generalist predators, feeding on schooling fish, and zooplankton, but variability likely exists among regional feeding aggregations. We explored the diet of one feeding aggregation of humpback whales near Kodiak Island, Alaska, through analysis of the stable carbon (d13C) and nitrogen (d15N) isotope ratios of their skin and regional prey sources. Humpback whales were sampled during the summer feeding season over 3 yr (n= 93; 20042006). Prey samples were collected from the same region during trawl surveys conducted between 2003 and 2005. Isotope values of humpback whale skin and prey were entered into a Bayesian dietary mixing model to estimate feasible contributions of prey to humpback diets. Diet results indicated that humpbacks feed heavily on euphausiids, but also consume juvenile walleye pollock, capelin, and Pacific sand lance. The diet of humpback whales in 2004 was the most diverse, while diets in 2005 and 2006 showed a higher proportion of euphausiids. Our results reveal annual differences in humpback diets from the Kodiak region due to either individual prey preferences or prey availability. Application of a Bayesian mixing model to stable isotope analysis improves description of regional diets and comparison of these diets to resource availability and quality.
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The frequency of occurrence of naturally sloughed skin was investigated to verify the feasibility of this method to study blue whale genetics off Baja California. Sloughed skin was recorded in 97% of 337 surfacing intervals with blue whales, Balaenoptera musculus, along the Baja California peninsula, Mexico. No significant difference (P > 0.05) was found in size of pieces of skin sloughed from whales in different habitats, sea surface temperatures or whether they were alone or in pairs. Samples were recoverable independent of gender and age and could be linked to individuals. While yield of extracted DNA was low (0-0.15mg/mg tissue), gender determination was successful in 55% of the samples assayed.
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During February, March and April, 57% of the euphausiids were in breeeding condition; males possessed developed spermatophores while females were carrying eggs and metanauplii. Sex ratios of female:male were between 1:1 and 2:1. Swarm samples contained high numbers of eggs and metanauplii. Swarming is related to reproductive activity, but analysis of one swarm sample of N. simplex showed that only 8% were in breeding condition. Highest biomass found was 32.6 g wet wt m-3, correlated with the high trophic activity observed in the sample area. -from Author
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Spatial or temporal isotopic variation, or both, in primary producers must be controlled for when investigating the foraging and trophic ecology of top consumers using isotopic data. Populations of the sister species Zalophus californianus and Z. wollebaeki are separated by approximately 3,350 km in the eastern tropical Pacific Ocean, which prevents contact and mixing between the 2 populations. To explore differences in trophic ecology between these species, as well as the impact of differences in baseline food-web isotope values between the 2 regions, we compared conventional dietary data derived from analyses of scat contents to isotopic values of hair collected from pups at 13 rookeries in the Gulf of California (Z. californianus) and 11 rookeries on the Galpagos Islands (Z. wollebaeki). Mean ± 1 SD δ13C and δ15N values were -15.9‰ ± 0.5‰ and 21.8 ± 0.7‰ in the Gulf of California, whereas for the Galpagos they were -14.5‰ ± 0.5‰ and 13.1‰ ± 0.5‰. Examination of scat data suggested overlap in 6 of the 10 most common prey consumed by sea lions. Trophic level (TL) derived from scat analysis was positively related with δ15N values for the Gulf of California rookeries, but estimates of TL for each region were similar (4.4 for Galpagos and 4.1 for Gulf of California), suggesting that foraging behavior makes a limited contribution to the large difference in δ15N value between the 2 populations. Particulate organic matter δ15N values near the Galpagos Islands are ∼5.3‰ lower than values in the Gulf of California, suggesting that the baseline food-web values account for approximately two-thirds of the observed difference in pup hair δ15N values. This study may provide clues to better understand isotopic values of marine top predators migrating across the eastern Pacific Ocean.
Book
Statistical Rethinking: A Bayesian Course with Examples in R and Stan builds readers’ knowledge of and confidence in statistical modeling. Reflecting the need for even minor programming in today’s model-based statistics, the book pushes readers to perform step-by-step calculations that are usually automated. This unique computational approach ensures that readers understand enough of the details to make reasonable choices and interpretations in their own modeling work. The text presents generalized linear multilevel models from a Bayesian perspective, relying on a simple logical interpretation of Bayesian probability and maximum entropy. It covers from the basics of regression to multilevel models. The author also discusses measurement error, missing data, and Gaussian process models for spatial and network autocorrelation. By using complete R code examples throughout, this book provides a practical foundation for performing statistical inference. Designed for both PhD students and seasoned professionals in the natural and social sciences, it prepares them for more advanced or specialized statistical modeling. Web Resource The book is accompanied by an R package (rethinking) that is available on the author’s website and GitHub. The two core functions (map and map2stan) of this package allow a variety of statistical models to be constructed from standard model formulas.
Article
We describe the mandibular morphology of the eight most abundant euphausiid species in the California Current and report regression relationships between mandible size and body total length. We applied these species-specific characters to the mandibles recovered from fecal samples of 18 blue whales (Balaenoptera musculus (Linnaeus, 1758)) collected between 1998 to 2015 off Southern California to test for selective feeding on the euphausiid assemblage. The diets of blue whales were consistently and overwhelmingly dominated by the large neritic euphausiid Thysanoessa spiniferaHolmes, 1900, even when other species were present or dominant in closely collected net samples. More than 99% of the ingested euphausiids were longer than 10 mm, indicating that blue whales in this region are highly selective by prey species and size class, and dependent upon aggregations of juveniles or adults of a limited number of coastally associated euphausiid species.
Article
Steroid hormone assessment using non-invasive sample collection techniques can reveal the reproductive status of aquatic mammals and the physiological mechanisms by which they respond to changes in their environment. A portion of the eastern North Pacific blue whale (Balaenoptera musculus) population that seasonally visits the Gulf of California, Mexico has been monitored using photo-identified individuals for over 30 years. The whales use the area in winter-early spring for nursing their calves and feeding and it therefore is well suited for fecal sample collection. Using radioimmunoassays in 25 fecal samples collected between 2009-2012 to determine reproductive state and stress, we validated three steroid hormones (progesterone, corticosterone and cortisol) in adult female blue whales. Females that were categorized as pregnant had higher mean fecal progesterone concentrations (1292.6 ± 415.6 ng·g-1) than resting and lactating females (14.0 ± 3.7 ng·g-1; 23.0 ± 5.4 ng·g-1, respectively). Females classified as pregnant also had higher concentrations of corticosterone (37.5 ± 9.9 ng·g-1) than resting and lactating females (17.4 ± 2.0 ng·g-1; 16.8 ± 2.8 ng·g-1, respectively). In contrast, cortisol concentrations showed high variability between groups and no significant relationship to reproductive state. We successfully determined preliminary baseline parameters of key steroid hormones by reproductive state in adult female blue whales. The presence of pregnant or with luteal activity and known lactating females confirms that the Gulf of California is an important winter-spring area for the reproductive phase of these blue whales. The baseline corticosterone levels we are developing will be useful for assessing the impact of the increasing coastal development and whale-watching activities on the whales in the Gulf of California.
Article
Stable isotope analysis (SIA) has rapidly become a useful tool to study the ecology of wild animal populations, especially for elusive, wide-ranging predators like marine mammals. The development of projectile biopsy techniques resulted in the collection of thousands of cetacean tissue samples that were archived in a dimethyl sulfoxide (DMSO) solution for long-term, multidecadal preservation. Here we examine the influence of DMSO preservation on carbon (δ13C) and nitrogen (δ15N) values by comparing a set of paired delphinid skin samples stored frozen without preservative and in DMSO for up to 22 yr. Treatment of paired frozen and DMSO-preserved skin in a 2:1 chloroform:methanol solution yielded similar δ13C and δ15N values, revealing that DMSO and lipid contamination have similar isotopic effects on skin, and that these effects can be removed using routine lipid-extraction methods. Further, amino acid concentrations in DMSO-preserved and frozen skin tissue were similar, providing independent evidence of minimal protein alteration due to preservation. Access to a rich archive of skin samples preserved in DMSO will expand our ability to examine temporal and spatial variability in the isotope values of cetaceans, which will aid our understanding of how their ecology has been influenced by historical changes in environmental conditions.
Book
Berta and Sumich have succeeded yet again in creating superior marine reading! This book is a succinct yet comprehensive text devoted to the systematics, evolution, morphology, ecology, physiology, and behavior of marine mammals. The first edition, considered the leading text in the field, is required reading for all marine biologists concerned with marine mammals. Revisions include updates of citations, expansion of nearly every chapter and full color photographs. This title continues the tradition by fully expanding and updating nearly all chapters.
Article
A three-dimensional, process-based model of the ocean's carbon and nitrogen cycles, including 13C and 15N isotopes, is used to explore effects of idealized changes in the soft-tissue biological pump. Results are presented from one preindustrial control run (piCtrl) and six simulations of the Last Glacial Maximum (LGM) with increasing values of the spatially constant maximum phytoplankton growth rate μmax, which accelerates biological nutrient utilization mimicking iron fertilization. The default LGM simulation, without increasing μmax and with a shallower and weaker Atlantic Meridional Overturning Circulation and increased sea ice cover, leads to 280 Pg more respired organic carbon (Corg) storage in the deep ocean with respect to piCtrl. Dissolved oxygen concentrations in the colder glacial thermocline increase, which reduces water column denitrification and, with delay, nitrogen fixation, thus increasing the ocean's fixed nitrogen inventory and decreasing δ15NNO3 almost everywhere. This simulation already fits sediment reconstructions of carbon and nitrogen isotopes relatively well, but it overestimates deep ocean δ13CDIC and underestimates δ15NNO3 at high latitudes. Increasing μmax enhances Corg and lowers deep ocean δ13CDIC, improving the agreement with sediment data. In the model's Antarctic and North Pacific Oceans modest increases in μmax result in higher δ15NNO3 due to enhanced local nutrient utilization, improving the agreement with reconstructions there. Models with moderately increased μmax fit both isotope data best, whereas large increases in nutrient utilization are inconsistent with nitrogen isotopes although they still fit the carbon isotopes reasonably well. The best fitting models reproduce major features of the glacial δ13CDIC, δ15N, and oxygen reconstructions while simulating increased Corg by 510–670 Pg compared with the preindustrial ocean. These results are consistent with the idea that the soft-tissue pump was more efficient during the LGM. Both circulation and biological nutrient utilization could contribute. However, these conclusions are preliminary given our idealized experiments, which do not consider changes in benthic denitrification and spatially inhomogenous changes in aeolian iron fluxes. The analysis illustrates interactions between the carbon and nitrogen cycles as well as the complementary constraints provided by their isotopes. Whereas carbon isotopes are sensitive to circulation changes and indicate well the three-dimensional Corg distribution, nitrogen isotopes are more sensitive to biological nutrient utilization.
Article
In the California Current ecosystem, krill availability is a well-known influence on the demography of commercially and ecologically valuable fish, seabirds, and marine mammals. Modeling factors that enhance or inhibit krill aggregations, or 'hotspots', will benefit management of marine predators of conservation concern and contribute to ecosystem approaches to fisheries. Here, we link an oceanographic model (ROMS) and an individual-based model (IBM) parameterized for the krill species Euphausia pacifica to test the hypothesis that occurrences of krill hotspots are disassociated from centers of upwelling along the central-northern California coast due to strong advective currents that transport zooplankton away from the productive continental shelf environment. We compare the distribution of modeled to observed hotspots derived from hydroa-coustic surveys from 2000 to 2008. Both acoustic data and modeled hotspots show the greater Gulf of the Farallones and Monterey Canyon as areas of persistent krill hotspots. In this large retention zone, we found no clear relationships between krill hotspots and proxies of upwelling. In contrast, modeled hotspots were associated with reduced upwelling (warmer sea surface temperature [SST] and lower alongshore currents) to the north of Pt. Reyes, and with enhanced upwelling (cooler SST and greater alongshore currents) south of Pt. Sur. Our model highlights the role spatial variability of physical forcing plays in determining the likelihood of krill hotspots forming in particular regions. Notably, our model reproduced the spatial organization of krill hotspots using only simple oceanographic forcing mechanisms and diurnal vertical migration behavior.
Article
Blue whales (Balaenoptera musculus) were among the most intensively exploited species of whales in the world. As a consequence of this intense exploitation, blue whale sightings off the coast of Chile were uncommon by the end of the 20th century. In 2004, a feeding and nursing ground was reported in southern Chile (SCh). With the aim to investigate the genetic identity and relationship of these Chilean blue whales to those in other Southern Hemisphere areas, 60 biopsy samples were collected from blue whales in SCh between 2003 and 2009. These samples were genotyped at seven microsatellite loci and the mitochondrial control region was sequenced, allowing us to identify 52 individuals. To investigate the genetic identity of this suspected remnant population, we compared these 52 individuals to blue whales from Antarctica (ANT, n = 96), Northern Chile (NCh, n = 19) and the eastern tropical Pacific (ETP, n = 31). No significant differentiation in haplotype frequencies (mtDNA) or among genotypes (nDNA) was found between SCh, NCh and ETP, while significant differences were found between those three areas and Antarctica for both the mitochondrial and microsatellite analyses. Our results suggest at least two breeding population units or subspecies exist, which is also supported by other lines of evidence such as morphometrics and acoustics. The lack of differences detected between SCh/NCh/ETP areas supports the hypothesis that eastern South Pacific blue whales are using the ETP area as a possible breeding area. Considering the small population sizes previously reported for the SCh area, additional conservation measures and monitoring of this population should be developed and prioritized. © 2014 John Wiley & Sons Ltd.
Article
Blue whales were targeted in the North Pacific from 1905–1971 and are listed as endangered by the IUCN. Despite decades without whaling, abundance estimates for eastern North Pacific (ENP) blue whales (Balaenoptera musculus) suggest little evi-dence for a recent increase. One possible reason is fatal strikes by large ships, which have affected populations of other cetaceans and resulted in mitigation. We used a population dynamics model to assess the trends and status of ENP blue whales, and the effects of ship strikes. We estimate the population likely never dropped below 460 individuals, and is at 97% of carrying capacity (95% interval 62%–99%). These results suggest density dependence, not ship strikes, is the key reason for the observed lack of increase. We also estimate future strikes will likely have a minimal impact; for example, an 11-fold increase in vessels would lead to a 50% chance the long-term population would be considered depleted. Although we estimate ship strike mitigation would have minimal impacts on population trends and status, cur-rent levels of ship strikes are likely above legal limits set by the U.S. The recovery of ENP blue whales from whaling demonstrates the ability of blue whale populations to rebuild under careful management.
Article
Bayesian statistics has exploded into biology and its sub-disciplines such as ecology over the past decade. The free software program WinBUGS and its open-source sister OpenBugs is currently the only flexible and general-purpose program available with which the average ecologist can conduct their own standard and non-standard Bayesian statistics. Introduction to WINBUGS for Ecologists goes right to the heart of the matter by providing ecologists with a comprehensive, yet concise, guide to applying WinBUGS to the types of models that they use most often: linear (LM), generalized linear (GLM), linear mixed (LMM) and generalized linear mixed models (GLMM).Introduction to WinBUGS for Ecologists combines the use of simulated data sets "paired" analyses using WinBUGS (in a Bayesian framework for analysis) and in R (in a frequentist mode of inference) and uses a very detailed step-by-step tutorial presentation style that really lets the reader repeat every step of the application of a given mode in their own research.- Introduction to the essential theories of key models used by ecologists- Complete juxtaposition of classical analyses in R and Bayesian Analysis of the same models in WinBUGS- Provides every detail of R and WinBUGS code required to conduct all analyses- Written with ecological language and ecological examples- Companion Web Appendix that contains all code contained in the book, additional material (including more code and solutions to exercises)- Tutorial approach shows ecologists how to implement Bayesian analysis in practical problems that they face.
Article
To monitor the composition and the vertical flux of particulate matter from the sea surface, a sediment trap was moored in Cuenca Alfonso, Bahía de La Paz, a zone of high productivity in the southwestern Gulf of California. Carbonate-free samples from 2002 to 2005 were analyzed for Corg, N, δ13C, and δ15N. The results show seasonal and interannual variability, with the δ13C and δ15N values larger in spring and summer than in fall and winter. The C:N ratio and δ13C increased by 1.5 units from 2002 to 2003–2005, suggesting a change in the supply of organic matter and-or the use or preferential degradation of Norg. There was no interannual variation in δ15N. The occasional high δ15N values suggest that physical mechanisms, such as the shoaling and advection into the bay of 15N-rich subsurface equatorial water, occur over short time periods. The latter is presumed to be related to the periodic development of a significant cyclonic gyre in the southern Gulf.
Article
Dissolved nitrate in the subsurface water (200-650 m) off southern California is unusually high in 615N compared with waters from the same depth in the central and western Pacific, which have 6r5N values similar to the deep oceans. Marc than 150 seawater samples from the sea off southern California and the North Atlantic were analyzed for the 615N of nitrate. The mean 615N (& 1 SD) of deep waters (> 1,500 m) is 5.7 40.7%. The mean iY5N in the "N-anomaly zone off southern California is 9.0*0.7%~. Maxima of 615N were found to coincide with salinity maxima, which occurred in the same isopycnal levels as the 15N-enriched denitrifying zone in the eastern tropical North Pacific (ETNP). Using the correlation between ti15N and salinity, we can show the southern California waters to be of mixed origin with the denitrifying water from the ETNP as one end member. Our observations support the notion that the oxygen-deficient waters in the eastern tropical Pacific arc important sources of 15N-enriched nitrate. Sweeney et al. (1978) studied the isotopic composition of particulate organic matter (POM) in sediments from the southern Cal- ifornia borderland and showed that the av- crage 615N of marine organic nitrogen was higher than that of terrigenous organic ni- trogen by 7%~. Wada et al. (1975) suggested that the high 615N of nitrogenous com- pounds in the sea, and in planktonic pro- teins, is mainly attributable to the isotopic composition of nitrate in seawater, which is enriched in 15N due to preferential removal of 14N03- during denitrification. Saino and Hattori (1987) reported geographic varia- tion of the 615N value of POM and attrib- uted the difference primarily to isotopic al- tcration in nitrate. This paper demonstrates geographic inhomogeneity in the nitrogen isotopic composition of nitrate and offers some explanations for the variation. The
Article
Hydrographic data (salinity, temperature, O2, PO4, NO3 and SiO2) collected in the northern Gulf of California between February 27 and March 3, 1988, reveal that bottom water formation took place that winter. North of 30.5°N, salinity increased with depth from ∼35.30 practical salinity units (psu) at the surface to 35.57 psu at the bottom of the 200-m deep Wagner Basin; below ∼25 m, temperature was almost homogeneous, at ∼15°C (±0.4°C), with some inversions. The TS diagrams and the distribution of dissolved oxygen and nutrients suggest that the most likely origin of this bottom water is the shallow coastal region (22 μM; and silicate, >35 μM) indicate the presence of oceanic water from Guaymas Basin, probably Subsurface Subtropical Water. The boundary between the two regimes was ∼18 km wide, with clearly defined bottom fronts and intrusions at all depths. Of the several late-winter hydrographic data sets available, only that from March 1973 presents a similar distribution of high-salinity bottom water. Therefore interannual variability (not necessarily El Niño-Southern Oscillation (ENSO) related) can have a profound effect on vertical convection, which can occur both in ENSO and non-ENSO years. An important and as yet unexplained difference between the two data sets is that there was more Gulf of California Water in the northern Gulf of California in 1973 than in 1988.
Article
The nitrogen isotopic composition of time-series sediment trap samples, dissolved NO-3, and surficial sediments was determined in three regions along the margin of the eastern North Pacific: Monterey Bay, San Pedro Basin, and the Gulf of California (Carmen and Guaymas Basins). Complex physical regimes are present in all three areas, and each is influenced seasonally by coastal upwelling. Nevertheless, sediment trap material evidently records the isotopic composition of new nitrogen sources, since average δ15N is generally indistinguishable from δ15N values for subsurface NO-3. Surficial sediments are also very similar to the average δ15N value of the sediment traps, being within 1‰. This difference in δ15N between trap material and sediment is much less than the previously observed 4‰ difference for the deep sea. Better organic matter preservation at our margin sites is a likely explanation, which may be due to either low bottom O2 concentrations or higher organic matter input to the sediments. All sites have δ15N for sub-euphotic zone NO-3 (8–10‰) substantially elevated from the oceanic average (4.5–5‰). This isotopic enrichment is a result of denitrification in suboxic subsurface waters (Gulf of California) or northward transport of denitrification influenced water (Monterey Bay and San Pedro Basin). Our results therefore suggest that downcore δ15N data, depending on site location, would record the intensity of denitrification and the transport of its isotopic signature along the California margin. Temporal variations in δ15N for the sediment traps do appear to respond to upwelling or convective injections of NO-3 to surface waters as a result of isotopic fractionation during phytoplankton uptake. Overall, though, the coupling between NO-3 injection, δ15N, and flux is looser than previously observed for the open-ocean, most likely the result of the smaller time/space scales of the events. In the Gulf of California, wintertime convective mixing/upwelling does produce distinct δ15N minima co-occurring with particle flux maxima. Interannual variations are apparent in this region when these winter-time δ15N minima fail to occur during El Niño conditions. There appears to be a positive relationship between the Southern Oscillation Index (SOI) anomaly and annual average δ15N. One explanation calls for hydrographic changes altering the δ15N of subeuphotic zone NO-3.
Article
Euphasiid crustaceans in the Gulf of California were examined from four bimonthly CalCOFI grid cruises during February through August of 1957. Of the nine species found to regularly inhabit the Gulf, Nematoscelis dificilis and Nyctiphanes simplex are common to the warm-temperate California Current. These have the broadest ranges in the Gulf, peaking in abundance and reproducing maximally during February-April and Feb- ruary-June respectively, before intense August heating takes place in the Gulf. Euphausia eximia, a species having high densities at zones considered marginal to the eastern tropical Pacific, also varies little in range during the year, consistently occupying the southern half of the Gulf. Tropical Nematoscelis gracilis shows a range com- plementary to that of N. dificilis; these species overlap in the southern Gulf. Three Euphausia species of the tropi- cal Pacific occupy the southern Gulf in February-April, expanding northward during June-August but, like the cool-water species, scarcely reproducing in the Gulf dur- ing the warm season. The distributions and abundances of the species and their life stages, particularly the youngest larvae, are described in relation to seasonal variation in flow and temperature in the Gulf. RESUMEN Se examinaron cruskiceos eufausidos del Golfo de California tornados durante cuatro cruceros bimensuales de CalCOFI entre febrero y agosto de 1957. De las nueve especies encontradas que regularmente habitan en el Golfo, Nematoscelis dificilis y Nyctiphanes simplex son comunes en las aguas templada-calidas de la Co- rriente de California. Estas especies presentan una dis- tribucion amplia en el Golfo, alcanzando una maxima abundancia y reproduccion durante febrero-abril y febre- ro-junio, respectivamente, antes de llegar el calor intenso de agosto. Euphausia eximia, una especie de altas den- sidades en las zonas consideradas marginales a1 Pacifico tropical oriental, tambien varia poco en su amplitud de distribucion durante el aiio, ocupando consistentemente la mitad sur del Golfo. Nematoscelis gracilis, es tropical y muestra una distribucion complementaria con N. d$- ficilis; estas especies concurren en el sur del Golfo. Tres especies de Euphausia del Pacifico tropical ocupan el sur del Golfo en febrero-abril, extendiendose hacia el norte durante junio-agosto, pero, como las especieg de agua fria, escasamente se reproducen en el Golfo durante la estacion calida. Las distribuciones y abundancias de IManuxript reccivcd 14 April I960 I las especies y de sus etapas de vida, en particular las de las larvas mas juveniles, se describen en relacion con las variaciones estacionales en el flujo y las temperaturas de las aguas del Golfo.