Tomoharu Eguchi

Stable isotope tracking of endangered sea turtles: validation with satellite telemetry and δ15N analysis of amino acids.

Effective conservation strategies for highly migratory species must incorporate information about long-distance movements and locations of high-use foraging areas. However, the inherent challenges of directly monitoring these factors call for creative research approaches and innovative application of existing tools. Highly migratory marine species, such as marine turtles, regularly travel hundreds or thousands of kilometers between breeding and feeding areas, but identification of migratory routes and habitat use patterns remains elusive. Here we use satellite telemetry in combination with compound-specific isotope analysis of amino acids to confirm that insights from bulk tissue stable isotope analysis can reveal divergent migratory strategies and within-population segregation of foraging groups of critically endangered leatherback sea turtles (Dermochelys coriacea) across the Pacific Ocean. Among the 78 turtles studied, we found a distinct dichotomy in δ15N values of bulk skin, with distinct “low δ15N” and “high δ15N” groups. δ15N analysis of amino acids confirmed that this disparity resulted from isotopic differences at the base of the food chain and not from differences in trophic position between the two groups. Satellite tracking of 13 individuals indicated that their bulk skin δ15N value was linked to the particular foraging region of each turtle. These findings confirm that prevailing marine isoscapes of foraging areas can be reflected in the isotopic compositions of marine turtle body tissues sampled at nesting beaches. We use a Bayesian mixture model to show that between 82 and 100% of the 78 skin-sampled turtles could be assigned with confidence to either the eastern Pacific or western Pacific, with 33 to 66% of all turtles foraging in the eastern Pacific. Our forensic approach validates the use of stable isotopes to depict leatherback turtle movements over broad spatial ranges and is timely for establishing wise conservation efforts in light of this species’ imminent risk of extinction in the Pacific.

Large‐scale movements and high‐use areas of western Pacific leatherback turtles, Dermochelys coriacea

The western Pacific leatherback turtle (Dermochelys coriacea), one of three genetically distinct stocks in the Indo-Pacific region, has declined markedly during past decades. This metapopulation nests year-round at beaches of several western Pacific island nations and has been documented through genetic analysis and telemetry studies to occur in multiple regions of the Pacific Ocean. To provide a large-scale perspective of their movements, high-use areas, and habitat associations, we report and synthesize results of 126 satellite telemetry deployments conducted on leatherbacks at western Pacific nesting beaches and at one eastern Pacific foraging ground during 2000-2007. A Bayesian switching state-space model was applied to raw Argos-acquired surface locations to estimate daily positions and behavioral mode (either transiting or area-restricted search) for each turtle. Monthly areas of high use were identified for post- nesting periods using kernel density estimation. There was a clear separation of migratory destinations for boreal summer vs. boreal winter nesters. Leatherbacks that nested during boreal summer moved into Large Marine Ecosystems (LMEs) of the temperate North Pacific Ocean or into tropical waters of the South China Sea. Turtles that nested during boreal winter moved into temperate and tropical LMEs of the southern hemisphere. Area-restricted search occurred in temperate and tropical waters at diverse pelagic and coastal regions exhibiting a wide range of oceanographic features, including mesoscale eddies, coastal retention areas, current boundaries, or stationary fronts, all of which are known mechanisms for aggregating leatherback prey. Use of the most distant and temperate foraging ground, the California Current LME, required a 10-12 month trans-Pacific migration and commonly involved multiple years of migrating between high-latitude summer foraging grounds and low-latitude eastern tropical Pacific wintering areas without returning to western Pacific nesting beaches. In contrast, tropical foraging destinations were reached within 5-7 months and appeared to support year-round foraging, potentially allowing a more rapid return to nesting beaches. Based on these observations, we hypothesize that demographic differences are likely among nesting females using different LMEs of the Indo-Pacific. The differences in movements and foraging strategies underscore the importance of and the need for ecosystem-based management and coordinated Pacific-wide conservation efforts.

Identification of distinct movement patterns in Pacific leatherback turtle populations influenced by ocean conditions

Interactions with fisheries are believed to be a major cause of mortality for adult leatherback turtles (Dermochelys coriacea), which is of particular concern in the Pacific Ocean, where they have been rapidly declining. In order to identify where these interactions are occurring and how they may be reduced, it is essential first to understand the movements and behavior of leatherback turtles. There are two regional nesting populations in the East Pacific (EP) and West Pacific (WP), comprising multiple nesting sites. We synthesized tracking data from the two populations and compared their movement patterns. A switching state-space model was applied to 135 Argos satellite tracks to account for observation error, and to distinguish between migratory and area-restricted search behaviors. The tracking data, from the largest leatherback data set ever assembled, indicated that there was a high degree of spatial segregation between EP and WP leatherbacks. Area-restricted search behavior mainly occurred in the southeast Pacific for the EP leatherbacks, whereas the WP leatherbacks had several different search areas in the California Current, central North Pacific, South China Sea, off eastern Indonesia, and off southeastern Australia. We also extracted remotely sensed oceanographic data and applied a generalized linear mixed model to determine if leatherbacks exhibited different behavior in relation to environmental variables. For the WP population, the probability of area-restricted search behavior was positively correlated with chlorophyll-a concentration. This response was less strong in the EP population, but these turtles had a higher probability of search behavior where there was greater Ekman upwelling, which may increase the transport of nutrients and consequently prey availability. These divergent responses to oceanographic conditions have implications for leatherback vulnerability to fisheries interactions and to the effects of climate change. The occurrence of leatherback turtles within both coastal and pelagic areas means they have a high risk of exposure to many different fisheries, which may be very distant from their nesting sites. The EP leatherbacks have more limited foraging grounds than the WP leatherbacks, which could make them more susceptible to any temperature or prey changes that occur in response to climate change.

Predicting bycatch hotspots for endangered leatherback turtles on longlines in the Pacific Ocean

Fisheries bycatch is a critical source of mortality for rapidly declining populations of leatherback turtles, Dermochelys coriacea. We integrated use-intensity distributions for 135 satellite-tracked adult turtles with longline fishing effort to estimate predicted bycatch risk over space and time in the Pacific Ocean. Areas of predicted bycatch risk did not overlap for eastern and western Pacific nesting populations, warranting their consideration as distinct management units with respect to fisheries bycatch. For western Pacific nesting populations, we identified several areas of high risk in the north and central Pacific, but greatest risk was adjacent to primary nesting beaches in tropical seas of Indo-Pacific islands, largely confined to several exclusive economic zones under the jurisdiction of national authorities. For eastern Pacific nesting populations, we identified moderate risk associated with migrations to nesting beaches, but the greatest risk was in the South Pacific Gyre, a broad pelagic zone outside national waters where management is currently lacking and may prove difficult to implement. Efforts should focus on these predicted hotspots to develop more targeted management approaches to alleviate leatherback bycatch.

Prediction of fishing effort distributions using boosted regression trees.

Concerns about bycatch of protected species have become a dominant factor shaping fisheries management. However, efforts to mitigate bycatch are often hindered by a lack of data on the distributions of fishing effort and protected species. One approach to overcoming this problem has been to overlay the distribution of past fishing effort with known locations of protected species, often obtained through satellite telemetry and occurrence data, to identify potential bycatch hotspots. This approach, however, generates static bycatch risk maps, calling into question their ability to forecast into the future, particularly when dealing with spatiotemporally dynamic fisheries and highly migratory bycatch species. In this study, we use boosted regression trees to model the spatiotemporal distribution of fishing effort for two distinct fisheries in the North Pacific Ocean, the albacore (Thunnus alalunga) troll fishery and the California drift gillnet fishery that targets swordfish (Xiphias gladius). Our results suggest that it is possible to accurately predict fishing effort using < 10 readily available predictor variables (cross-validated correlations between model predictions and observed data -0.6). Although the two fisheries are quite different in their gears and fishing areas, their respective models had high predictive ability, even when input data sets were restricted to a fraction of the full time series. The implications for conservation and management are encouraging: Across a range of target species, fishing methods, and spatial scales, even a relatively short time series of fisheries data may suffice to accurately predict the location of fishing effort into the future. In combination with species distribution modeling of bycatch species, this approach holds promise as a mitigation tool when observer data are limited. Even in data-rich regions, modeling fishing effort and bycatch may provide more accurate estimates of bycatch risk than partial observer coverage for fisheries and bycatch species that are heavily influenced by dynamic oceanographic conditions.

Estimating At-Sea Mortality of Marine Turtles from Stranding Frequencies and Drifter Experiments

Strandings of marine megafauna can provide valuable information on cause of death at sea. However, as stranding probabilities are usually very low and highly variable in space and time, interpreting the results can be challenging. We evaluated the magnitude and distribution of at-sea mortality of marine turtles along the Pacific coast of Baja California Sur, México during 2010–11, using a combination of counting stranded animals and drifter experiments. A total of 594 carcasses were found during the study period, with loggerhead (62%) and green turtles (31%) being the most common species. 87% of the strandings occurred in the southern Gulf of Ulloa, a known hotspot of loggerhead distribution in the Eastern Pacific. While only 1.8% of the deaths could be definitively attributed to bycatch (net marks, hooks), seasonal variation in stranding frequencies closely corresponded to the main fishing seasons. Estimated stranding probabilities from drifter experiments varied among sites and trials (0.05–0.8), implying that only a fraction of dead sea turtles can be observed at beaches. Total mortality estimates for 15-day periods around the floater trials were highest for PSL, a beach in the southern Gulf of Ulloa, ranging between 11 sea turtles in October 2011 to 107 in August 2010. Loggerhead turtles were the most numerous, followed by green and olive ridley turtles. Our study showed that drifter trials combined with beach monitoring can provide estimates for death at sea to measure the impact of small-scale fisheries that are notoriously difficult to monitor for by-catch. We also provided recommendations to improve the precision of the mortality estimates for future studies and highlight the importance of estimating impacts of small–scale fisheries on marine megafauna.

Cost-effectiveness of alternative conservation strategies with application to the Pacific leatherback turtle.

Although holistic conservation addressing all sources of mortality for endangered species or stocks is the preferred conservation strategy, limited budgets require a criterion to prioritize conservation investments. We compared the cost-effectiveness of nesting site and at-sea conservation strategies for Pacific leatherback turtles (Dermochelys coriacea). We sought to determine which conservation strategy or mix of strategies would produce the largest increase in population growth rate per dollar. Alternative strategies included protection of nesters and their eggs at nesting beaches in Indonesia, gear changes, effort restrictions, and caps on turtle takes in the Hawaiian (U.S.A.) longline swordfish fishery, and temporal and area closures in the California (U.S.A.) drift gill net fishery. We used a population model with a biological metric to measure the effects of conservation alternatives. We normalized all effects by cost to prioritize those strategies with the greatest biological effect relative to its economic cost. We used Monte Carlo simulation to address uncertainty in the main variables and to calculate probability distributions for cost-effectiveness measures. Nesting beach protection was the most cost-effective means of achieving increases in leatherback populations. This result creates the possibility of noncompensatory bycatch mitigation, where high-bycatch fisheries invest in protecting nesting beaches. An example of this practice is U.S. processors of longline tuna and California drift gill net fishers that tax themselves to finance low-cost nesting site protection. Under certain conditions, fisheries interventions, such as technologies that reduce leatherback bycatch without substantially decreasing target species catch, can be cost-effective. Reducing bycatch in coastal areas where bycatch is high, particularly adjacent to nesting beaches, may be cost-effective, particularly, if fisheries in the area are small and of little commercial value.

Morphology and Growth Rates of the Green Sea Turtle (Chelonia mydas) in a Northern-most Temperate Foraging Ground

Abstract We examined the morphology and somatic growth rate of Green Sea Turtles living in San Diego Bay, California; one of the northern-most foraging areas for the species in the eastern Pacific. A power plant had discharged heated effluent into the urbanized bay from 1960 to 2010. Straight carapace lengths of 101 Green Sea Turtles were recorded from 31 March 1990 to 15 April 2011 (45.4 to 110.4 cm). Green Sea Turtles in San Diego Bay were morphologically indistinguishable from those foraging in Baja California Sur, Mexico. The median growth rate was 1.03 cm/yr (−1.6 to 11.4 cm/yr) for all turtles and was 4.9 cm/yr for turtles ≤90 cm. These growth rates were one of the fastest for the species in temperate areas and comparable to those reported for tropical regions. The estimated growth parameter of the von Bertalanffy growth function (mean growth coefficient  =  0.21, 95% posterior interval  =  0.19–0.23) also was greater than for other populations of Green Sea Turtles. Based on behavioral observations and information from other diet studies, we think that the altered environment from the power plant effluent affected the growth of the Green Sea Turtles directly (longer active periods) and via shifts in the environment (changes in prey composition, abundance, and distribution). With the termination of the power plant operation at the end of 2010, the ecosystem is reverting to its natural state, which we expect will result in decreased growth rates of these turtles in the coming years.

An analytical approach to sparse telemetry data

Horizontal behavior of highly migratory marine species is difficult to decipher because animals are wide-ranging, spend minimal time at the ocean surface, and utilize remote habitats. Satellite telemetry enables researchers to track individual movements, but population level inferences are rare due to data limitations that result from difficulty of capture and sporadic tag reporting. We introduce a Bayesian modeling framework to address population level questions with satellite telemetry data when data are sparse. We also outline an approach for identifying informative variables for use within the model. We tested our modeling approach using a large telemetry dataset for Shortfin Makos (Isurus oxyrinchus), which allowed us to assess the effects of various degrees of data paucity. First, a permuted Random Forest analysis is implemented to determine which variables are most informative. Next, a generalized additive mixed model is used to help define the relationship of each remaining variable with the response variable. Using jags and rjags for the analysis of Bayesian hierarchical models using Markov Chain Monte Carlo simulation, we then developed a movement model to generate parameter estimates for each of the variables of interest. By randomly reducing the tagging dataset by 25, 50, 75, and 90 percent and recalculating the parameter estimates, we demonstrate that the proposed Bayesian approach can be applied in data-limited situations. We also demonstrate how two commonly used linear mixed models with maximum likelihood estimation (MLE) can be similarly applied. Additionally, we simulate data from known parameter values to test each model’s ability to recapture those values. Despite performing similarly, we advocate using the Bayesian over the MLE approach due to the ability for later studies to easily utilize results of past study to inform working models, and the ability to use prior knowledge via informed priors in systems where such information is available.

Habitat Use and Behavior of the East Pacific Green Turtle, Chelonia mydas, in an Urbanized System

Abstrac Green sea turtles, Chelonia mydas, are known to inhabit populated and often urbanized areas. To understand turtle habitat use and behavior within these unique habitats, seven juvenile green turtles were fitted with acoustic transmitters (September 2012 – August 2014), of which two transmitters included an accelerometer (AP transmitter). One individual fitted with an AP transmitter was tracked using a passive acoustic array in an urbanized river, the San Gabriel River, Long Beach, CA (33°45’ N, 118°05’ W). Three additional turtles in this river and three turtles (one with AP transmitter) in a restored estuary (33°44’ N, 118°03’ W) in southern California were actively tracked for two non-consecutive 24-h periods. Those fitted with AP transmitters indicated that turtles were less active at night (0.58 ± 0.56 m/s2 and 0.50 ± 0.63 m/s2) than during the day (0.86 ± 0.63 m/s2 and 0.78 ± 0.60 m/s2) at both sites. Activity data and corresponding movements of the actively tracked turtle fitted with the AP transmitter were used to infer resting periods for other tracked individuals. Turtles rested near bridge pilings and runoff outflows in the river to potentially shelter from tidal flow. Turtles used significantly larger daily areas in the urbanized river (0.046 ± 0.023 km2) where resources may be patchier and less abundant, compared to turtles in the estuary (0.024 ± 0.012 km2) where large, dense eelgrass beds are present. Based on the habitat use and behaviors of green sea turtles, it appears that some green sea turtles are able to make use of both highly developed and restored habitats and likely benefit from certain aspects of development.