Entanglement is a costly life history stage in large whales

Data and figures associated with the project. See ReadMe for data descriptionIndividuals store energy to balance deficits in natural cycles; however, unnatural events can also lead to unbalanced energy budgets. Entanglement in fishing gear is one example of an unnatural but relatively common circumstance that imposes energetic demands of a similar order of magnitude and duration of life history events such as migration and pregnancy in large whales. We present two complementary bioenergetic approaches to estimate the energy associated with entanglement in North Atlantic right whales, and compare these estimates to the natural energetic life history of each individual whale.This work was supported by grants from the Herrington-Fitch Family Foundation, the M.S. Worthington Foundation, the North Pond Foundation, and the Cooperative Institute for the North Atlantic Region [CINAR; NA14OAR4320158] to MJM and JvdH. JvdH was supported by a Postgraduate Scholarship from the Natural Sciences and Engineering Research Council of Canada, and an MIT Martin Family for Sustainability Fellowship

Absolute probability estimates of lethal vessel strikes to North Atlantic right whales in Roseway Basin, Scotian Shelf

Author Posting. © Ecological Society of America, 2012. This article is posted here by permission of Ecological Society of America for personal use, not for redistribution. The definitive version was published in Ecological Applications 22 (2012): 2021–2033, doi:10.1890/11-1841.1.Vessel strikes are the primary source of known mortality for the endangered North Atlantic right whale (Eubalaena glacialis). Multi-institutional efforts to reduce mortality associated with vessel strikes include vessel-routing amendments such as the International Maritime Organization voluntary “area to be avoided” (ATBA) in the Roseway Basin right whale feeding habitat on the southwestern Scotian Shelf. Though relative probabilities of lethal vessel strikes have been estimated and published, absolute probabilities remain unknown. We used a modeling approach to determine the regional effect of the ATBA, by estimating reductions in the expected number of lethal vessel strikes. This analysis differs from others in that it explicitly includes a spatiotemporal analysis of real-time transits of vessels through a population of simulated, swimming right whales. Combining automatic identification system (AIS) vessel navigation data and an observationally based whale movement model allowed us to determine the spatial and temporal intersection of vessels and whales, from which various probability estimates of lethal vessel strikes are derived. We estimate one lethal vessel strike every 0.775–2.07 years prior to ATBA implementation, consistent with and more constrained than previous estimates of every 2–16 years. Following implementation, a lethal vessel strike is expected every 41 years. When whale abundance is held constant across years, we estimate that voluntary vessel compliance with the ATBA results in an 82% reduction in the per capita rate of lethal strikes; very similar to a previously published estimate of 82% reduction in the relative risk of a lethal vessel strike. The models we developed can inform decision-making and policy design, based on their ability to provide absolute, population-corrected, time-varying estimates of lethal vessel strikes, and they are easily transported to other regions and situations.This research was supported by the Environment Canada Habitat Stewardship Programme, the Canadian Whale Institute, and R. K. Smedbol (St. Andrews Biological Station)

Estimating energetics in cetaceans from respiratory frequency : why we need to understand physiology

© The Author(s), 2016. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Biology Open 5 (2016): 436-442, doi:10.1242/bio.017251.The accurate estimation of field metabolic rates (FMR) in wild animals is a key component of bioenergetic models, and is important for understanding the routine limitations for survival as well as individual responses to disturbances or environmental changes. Several methods have been used to estimate FMR, including accelerometer-derived activity budgets, isotope dilution techniques, and proxies from heart rate. Counting the number of breaths is another method used to assess FMR in cetaceans, which is attractive in its simplicity and the ability to measure respiration frequency from visual cues or data loggers. This method hinges on the assumption that over time a constant tidal volume (VT) and O2 exchange fraction (ΔO2) can be used to predict FMR. To test whether this method of estimating FMR is valid, we measured breath-by-breath tidal volumes and expired O2 levels of bottlenose dolphins, and computed the O2 consumption rate (V̇O2) before and after a pre-determined duration of exercise. The measured V̇O2 was compared with three methods to estimate FMR. Each method to estimate V̇O2 included variable VT and/or ΔO2. Two assumption-based methods overestimated V̇O2 by 216-501%. Once the temporal changes in cardio-respiratory physiology, such as variation in VT and ΔO2, were taken into account, pre-exercise resting V̇O2 was predicted to within 2%, and post-exercise V̇O2 was overestimated by 12%. Our data show that a better understanding of cardiorespiratory physiology significantly improves the ability to estimate metabolic rate from respiratory frequency, and further emphasizes the importance of eco-physiology for conservation management efforts.Funding for this project was provided by the Office of Naval Research [ONR YIP Award # N000141410563]. M.J.M. received funding from National Oceanographic Partnership Program [9N00014-11-1-0113]

Response to ‘On the importance of understanding physiology when estimating energetics in cetaceans’

© The Author(s), 2017. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Biology Open 6 (2017): 307-308, doi:10.1242/bio.023143.We are grateful for the interest in our paper by two eminent physiologists and hope this response to their comments will clarify the objectives of our paper. The analysis in Fahlman et al. (2016) was not intended to provide an accurate method to estimate field metabolic rate (FMR) in large mysticetes; the objective was to measure the dynamic changes in physiology associated with recovery from exercise and show that they are important to consider when estimating FMR. While static averages can provide useful estimates of FMR for a variety of situations, these need to be appropriately selected. For example, we illustrate that it is not possible to use selected average values chosen from excised tissues or resting animals (as in Blix and Folkow, 1995) to provide meaningful estimates of FMR for animals at different activities (i.e. the dolphins in our study). Our study highlights the importance of temporal variation in physiological models: the Blix and Folkow (1995) estimates rely on the assumption that only breathing frequency (fR) changes with activity, while we argue that both the tidal volume (VT) and mixed lung O2 content also vary with activity and recovery from a dive (Ridgway et al., 1969). Including this variation in all three parameters reduces temporal uncertainty in the same conceptual model (see Eqn. 1 in Fahlman et al., 2016)

Swimming kinematics and efficiency of entangled North Atlantic right whales

© The Author(s), 2017. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Endangered Species Research 32 (2017): 1-17, doi:10.3354/esr00781.Marine mammals are streamlined for efficient movement in their relatively viscous fluid environment and are able to alter their kinematics (i.e. fluke stroke frequency, amplitude, or both) in response to changes in force balance. Entanglement in fishing gear adds significant drag and buoyant forces that can impact swimming behaviors across a range of timescales. We deployed biologging tags during the disentanglement of 2 North Atlantic right whales Eubalaena glacialis to (1) examine how their kinematics changed in response to drag and buoyancy from entanglement in fishing gear, and (2) calculate resultant changes in swimming efficiency for one individual. We observed variable responses in dive behavior, but neither whale appeared to exploit added buoyancy to reduce energy expenditure. While some of the observed changes in behavior were individually specific, some swimming kinematics were consistently modulated in response to high drag and buoyancy associated with entangling gear, affecting thrust production. In high drag and buoyancy conditions, fluke strokes were significantly shorter and more variable in shape, and gliding was less frequent. Thrust and efficiency significantly differed among dive phases. Disentanglement reduced thrust coefficients ~4-fold, leading to 1.2 to 1.8-fold lower power (W). Ideal propulsive efficiency was significantly lower when entangled, though we detected no difference in observed propulsive efficiency between the conditions. Similar to carrying heavy objects or changing shoes, we present another condition where animals perceive unique movement constraints over seconds to minutes and develop compensatory strategies, altering their movement accordingly.J.M.v.d.H was supported by a postgraduate scholarship from the Natural Sciences and Engineering Research Council of Canada, the MIT Martin Family for Sustainability Fellowship, the Herrington Fitch Family Foundation, a NOAA Award #NA14OAR4320158 to The Cooperative Institute for the North Atlantic Region, and a WHOI-Duke Fellowship through the WHOI Marine Mammal Center

Swimming Energy Economy in Bottlenose Dolphins Under Variable Drag Loading

Instrumenting animals with tags contributes additional resistive forces (weight, buoyancy, lift, and drag) that may result in increased energetic costs; however, additional metabolic expense can be moderated by adjusting behavior to maintain power output. We sought to increase hydrodynamic drag for near-surface swimming bottlenose dolphins, to investigate the metabolic effect of instrumentation. In this experiment, we investigate whether (1) metabolic rate increases systematically with hydrodynamic drag loading from tags of different sizes or (2) whether tagged individuals modulate speed, swimming distance, and/or fluking motions under increased drag loading. We detected no significant difference in oxygen consumption rates when four male dolphins performed a repeated swimming task, but measured swimming speeds that were 34% (>1 m s-1) slower in the highest drag condition. To further investigate this observed response, we incrementally decreased and then increased drag in six loading conditions. When drag was reduced, dolphins increased swimming speed (+1.4 m s-1; +45%) and fluking frequency (+0.28 Hz; +16%). As drag was increased, swimming speed (-0.96 m s-1; -23%) and fluking frequency (-14 Hz; 7%) decreased again. Results from computational fluid dynamics simulations indicate that the experimentally observed changes in swimming speed would have maintained the level of external drag forces experienced by the animals. Together, these results indicate that dolphins may adjust swimming speed to modulate the drag force opposing their motion during swimming, adapting their behavior to maintain a level of energy economy during locomotion.Summary Statement: Biologging and tracking tags add drag to study subjects. When wearing tags of different sizes, dolphins changed their swimming paths, speed, and movements to modulate power output and energy consumption

Bottlenose dolphins modify behavior to reduce metabolic effect of tag attachment

Author Posting. © The Author(s), 2014. This is the author's version of the work. It is posted here by permission of The Company of Biologists for personal use, not for redistribution. The definitive version was published in Journal of Experimental Biology 217 (2014): 4229-4236, doi:10.1242/​jeb.108225.Attaching bio-telemetry or -logging devices (‘tags’) to marine animals for research and monitoring adds drag to streamlined bodies, thus affecting posture, swimming gaits and energy balance. These costs have never been measured in free-swimming cetaceans. To examine the effect of drag from a tag on metabolic rate, cost of transport and swimming behavior, four captive male dolphins (Tursiops truncatus) were trained to swim a set course, either non-tagged (n=7) or fitted with a tag (DTAG2; n=12), and surface exclusively in a flow-through respirometer in which oxygen consumption (Graphic) and carbon dioxide production (Graphic; ml kg−1 min−1) rates were measured and respiratory exchange ratio (Graphic/Graphic) was calculated. Tags did not significantly affect individual mass-specific oxygen consumption, physical activity ratios (exercise Graphic/resting Graphic), total or net cost of transport (COT; J m−1 kg−1) or locomotor costs during swimming or two-minute recovery phases. However, individuals swam significantly slower when tagged (by ~11%; mean ± s.d., 3.31±0.35 m s−1) than when non-tagged (3.73±0.41 m s−1). A combined theoretical and computational fluid dynamics model estimating drag forces and power exertion during swimming suggests that drag loading and energy consumption are reduced at lower swimming speeds. Bottlenose dolphins in the specific swimming task in this experiment slowed to the point where the tag yielded no increases in drag or power, while showing no difference in metabolic parameters when instrumented with a DTAG2. These results, and our observations, suggest that animals modify their behavior to maintain metabolic output and energy expenditure when faced with tag-induced drag.This project was funded by the National Oceanographic Partnership Program [National Science Foundation via the Office of Naval Research, N00014-11-1-0113]. J.v.d.H. was supported by a Postgraduate Scholarship from the Natural Sciences and Engineering Research Council of Canada.2015-10-1

Future directions in Eubalaena spp. : comparative research to inform conservation

All three extant right whales [Eubalaena australis (Southern; SRW), glacialis (North Atlantic; NARW), and japonica (North Pacific; NPRW)] were heavily exploited, and the status of the two northern hemisphere species remains precarious. Recently, limited gains made by the NARW have been reversed and urgent changes to management approaches are needed if extinction is to be averted. By contrast, some SRW populations are recovering. Given their close phylogenetic relationship, morphological, demographic, and ecological similarities, the contrasting recovery rates between populations and species provide an opportunity to apply a comparative approach to inform the differences in recovery as follows. (1) Recovery: All right whale species were internationally protected in 1931, but NARW, eastern NPRW and some SRW populations have barely recovered from whaling, while others are doing so at maximal rates. Are these differences a legacy of extreme depletion (e.g., loss of genetic diversity and cultural knowledge) or primarily due to anthropogenic factors (e.g., high mortality from ship strike and fisheries entanglement)? If modern anthropogenic threats are not affecting remote SRW populations, can these serve as baseline populations for comparison with NARW and NPRW? (2) Linking individuals to population-level responses: In wild mammals, strong links exist between reproductive indices and environmental conditions within the context of life-history strategies. Individual identification of whales provides the ability to track survival, reproduction and other demographic parameters, and their population-level consequences, providing the tools with which to uncover these links. Robust life-history analyses are now available for NARW and several SRW populations, linking demography with environmental conditions, providing the potential for teasing out important influencing factors. (3) Adapting to shifting resources: Recent reproductive declines in NARW appear linked to changing food resources. While we know some large-scale movement patterns for NARW and a few SRW populations, we know little of mesoscale movements. For NPRW and some SRW populations, even broad-scale movements are poorly understood. In the face of climate change, can methodological advances help identify Eubalaena distributional and migratory responses? (4) Emergent diseases and the vulnerability of populations under stress: Marine mammals are vulnerable to infectious diseases, particularly when subjected to stressors such as fishing gear entanglements, acoustic disturbance, and prey shortages. New tools to assess large whale health include body condition imaging, viromes, microbiomes, as well as metabolic and stress hormones. Comparative analysis of the three Eubalaena spp. could identify causes of varying recovery. (5) Comparative synthesis and cumulative effects: The lack of a good analytical approach for cumulative effects is an urgent bio-statistical problem in conservation biology. Without such a framework every stressor is managed in isolation, limiting efficacy. We propose a comparative synthesis to inform future cumulative effect analyses and outline future research priorities to achieve these goals.Publisher PDFPeer reviewe

Behavioral impacts of disentanglement of a right whale under sedation and the energetic cost of entanglement

Author Posting. © The Author(s), 2013. This is the author's version of the work. It is posted here by permission of Society for Marine Mammalogy for personal use, not for redistribution. The definitive version was published in Marine Mammal Science 30 (2014): 282–307, doi:10.1111/mms.12042.Protracted entanglement in fishing gear often leads to emaciation through reduced mobility and foraging ability, and energy budget depletion from the added drag of towing gear for months or years. We examined changes in kinematics of a tagged entangled North Atlantic right whale (Eg 3911), before, during and after disentanglement on 15 Jan 2011. To calculate the additional drag forces and energetic demand associated with various gear configurations, we towed three sets of gear attached to a load-cell tensiometer at multiple speeds. Tag analyses revealed significant increases in dive depth and duration; ascent, descent and fluke stroke rates; and decreases in root mean square fluke amplitude (a proxy for thrust) following disentanglement. Conservative drag coefficients while entangled in all gear configurations (mean ± SD Cd,e,go = 3.4x10-3 ± 0.0003, Cd,e,gb = 3.7x10-3 ± 0.0003, Cd,e,sl = 3.8x10-3 ± 0.0004) were significantly greater than in the nonentangled case (Cd,n = 3.2x10-3±0.0003; P = 0.0156, 0.0312, 0.0078 respectively). Increases in total power input (including standard metabolism) over the nonentangled condition ranged 1.6%-120.9% for all gear configurations tested; locomotory power requirements increased 60.0%-164.6%. These results highlight significant alteration to swimming patterns, and the magnitude of energy depletion in a chronically entangled whale.Funding sources include NOAA Cooperative Agreement NA09OAR4320129, PO EA133F09SE4792, the M.S. Worthington Foundation, the North Pond Foundation, Sloan and Hardwick Simmons.2014-05-2

Rebuttal to published article “A review of ghost gear entanglement amongst marine mammals, reptiles and elasmobranchs” by M. Stelfox, J. Hudgins, and M. Sweet

Author Posting. © The Author(s), 2016. This is the author's version of the work. It is posted here under a nonexclusive, irrevocable, paid-up, worldwide license granted to WHOI. It is made available for personal use, not for redistribution. The definitive version was published in Marine Pollution Bulletin 117 (2017): 554-555, doi:10.1016/j.marpolbul.2016.11.052.We reviewed the findings of the recently published article by Stelfox et al. (2016): “A review of ghost gear entanglement amongst marine mammals, reptiles and elasmobranchs” published in this journal (Volume 111, pp 6–17) and found that they are both flawed and misleading as they do not accurately reflect the prevalence of “ghost gear” cases reported in the literature. While we commend the authors for recognizing the importance of attempting to quantify the threat and for recommending more comprehensive databases, the methods, results and conclusions of this review have not advanced the understanding of the issue. As authors of the papers on whale entanglements in the North Atlantic that were reviewed by Stelfox et al. (2016) and others who are knowledgeable about the topic, we provide specific comments regarding misrepresentations of both the source of entanglement (e.g., actively fished gear versus “ghost gear”) and the number of reported entanglements for whale species included in the North Atlantic