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Proportion of time spent in each state. Top panel: proportion of time spent in each state by sex and vessel distance, light purple = females with close vessels, dark purple = females with far vessels, light teal = males with close vessels, and dark teal = males with far vessels. Bottom panel: difference in the proportion of time spent in each state with vessel distance (proportion of time with far vessels minus proportion of time with close vessels) for both sexes. Error bars in both plots indicate the 95% credible interval.
Source publication
Accurate knowledge of behavior is necessary to effectively manage the effects of human activities on wildlife, including vessel-based whale-watching. Yet, the wholly aquatic nature of cetaceans makes understanding their basic behavioral ecology quite challenging. An endangered population of killer whales faces several identified threats including p...
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Citations
... However, a habitat model failed to identify shipping traffic as a significant correlate of beluga habitat use in the St. Lawrence Estuary 98 . While females may be less risk-adverse than males as documented in other species 99 , there is no evidence for females avoiding the shipping lane in the SLE, which runs through both adult male habitat in the Laurentian Channel, and female and calf habitat in the UE 100 . It is worth nothing, however, that in 2020 when COVID-19 reduced vessel traffic in many areas including the SLE, diet composition, and the importance of pelagic prey from the LE in the diet somewhat differed compared to other years within the period (2015 -2020). ...
Changes in trophodynamics may affect trophic niche both at the individual and population levels. Using stable isotope ratios, we showed how contrasting oceanographic and trophic conditions in 1997–2003 and 2015–2020 have altered the diet and degree of individual specialization of St. Lawrence Estuary beluga (Delphinapterus leucas). The trophic niche of all sex and age classes changed over time, with beluga consuming more small pelagic prey during the first than the second period. Adult male diets differed from that of adult females and juveniles during the first period due to the other prey that were consumed. In 2015–2020, diet contributions by small pelagic prey decreased in all segments of the population and led to marginally significant differences in diet between adult males and females. These dietary changes were concomitant to a diversification of diet at the individual level and to an increase in diet heterogeneity among conspecifics and years within the 2015–2020 period. Whether these patterns emerged from an environment-driven reduction in prey biomass or from an increase in intra- and/or interspecific competition is unknown. Our findings illustrate the importance of considering individuals and not just the population when studying the foraging ecology of endangered species.
... The development of sound recording tags (digital acoustic recording tag, "D-tag"; Johnson et al., 2009;Shorter et al., 2017) made it possible to record the SPL experienced by a moving subject. Captive subjects can be trained to carry D-tags on harnesses; other methods have been used to attach them to wild marine mammals, such as suction cups for cetaceans that have a smooth skin (Miller et al, 2012(Miller et al, , 2014Holt et al., 2021) and glue for pinnipeds that have hair (Mikkelsen et al., 2019;Nachtsheim et al., 2023). ...
Investigating anthropogenic acoustic disturbance and sound exposure in marine mammals requires evaluation of experimental approaches used to measure the sound levels experienced by the subjects. In previous research, exposure of California sea lions (Zalophus californianus) to eight narrow noise bands was estimated as the mean sound pressure level (SPL) measured by hydrophones placed at multiple locations and depths in a pool. We compare this method of SPL estimation with SPLs measured with a sound recording tag (“D-tag”). Measurements were taken from (1) hydrophones at locations on a grid; (2) a D-tag at the same locations; (3) a D-tag attached in its housing to a harness on a sea lion swimming freely in the pool; (4) a D-tag in its housing in one position in the pool; (5) a D-tag on the sea lion in one position in the pool; and (6) a D-tag turning in one location in the pool without its housing, in its housing, and on the sea lion while she rotated on her body axis. The SPLs recorded by the D-tag on a free-swimming sea lion were ~8 to 10 dB lower than those measured by the grid hydrophones, and the differences varied by frequency. These differences in SPL are caused by a combination of the directionality associated with the D-tag itself, the presence of the housing, acoustic effects of the sea lion’s body, and periods that the D-tag was out of the water during respirations. Measuring mean sound levels in test pools using hydrophones deployed on grids is valid; however, attaching tags to wild marine mammals may be more feasible than using hydrophone grids at sea. We summarize considerations when selecting a method to fit the design of future research.
... Using UAVs to collect breath samples permitted us to keep the research vessel substantially further from animals than the close approach (≤7.62 m) required for collecting breath with a petri dish mounted on a pole (Raverty et al., 2017). This is critical considering that vessel presence and proximity can alter the behavioral state of endangered SRKWs during biologically significant activities like foraging and resting (e.g., Giles, 2014;Holt, Tennessen, Ward, et al. 2021;Lusseau et al., 2009;Tennessen, Holt, Hansen, et al., 2019;Tennessen, Holt, Ward, et al., 2019). The few responses noted in this study were minor compared to evasive reactions to UAVs noted in other species. ...
... Studies of southern resident killer whales carrying suction cupped sound and movement tags have found the probability of killer whales capturing prey increases as salmon abundance increases, but is negatively affected by the movements and noise of nearby vessels [62,63]. Vessel noise can mask communication between pod members and interfere with foraging and navigation [64,65]-while the physical presence of vessels can reduce the foraging effort of resident killer whales [63,66]. ...
... Studies of southern resident killer whales carrying suction cupped sound and movement tags have found the probability of killer whales capturing prey increases as salmon abundance increases, but is negatively affected by the movements and noise of nearby vessels [62,63]. Vessel noise can mask communication between pod members and interfere with foraging and navigation [64,65]-while the physical presence of vessels can reduce the foraging effort of resident killer whales [63,66]. Killer whales are more likely to encounter greater numbers of vessels in the Salish Sea than in the North Island Waters, which could mean that salmon are less accessible to southern residents than to northern residents despite there being a higher abundance of Chinook. ...
Differences in the availability of prey may explain the low numbers of southern resident killer whales and the increase in northern resident killer whales in British Columbia and Washington State. However, in-situ data on the availability of their preferred prey (Chinook salmon, Oncorhynchus tshawytscha) in the core feeding areas used by these two populations of fish-eating killer whales have been lacking to test this hypothesis. We used multi-frequency echosounders (38, 70, 120, and 200 kHz) to estimate densities of adult Chinook (age-4+, > 81 cm) within 16 hot-spot feeding areas used by resident killer whales during summer 2020 in the Salish Sea and North Island Waters. We found Chinook were generally concentrated within 50 m from the bottom in the deep waters, and tended to be absent near the surface in the shallow waters (< 50 m). In general, the densities of Chinook we encountered were highest as the fish entered the Salish Sea (from Swiftsure Bank in the south) and Johnstone Strait (from Queen Charlotte Strait to the north)—and declined as fish migrated eastward along the shoreline of Vancouver Island. Median densities of Chinook for all sampled areas combined were 0.4 ind.·1000 m⁻² in northern resident foraging areas, and 0.9 ind.·1000 m⁻² in southern resident killer whale areas (p < 0.05, Mann–Whitney U test). Thus, Chinook salmon were twice as prevalent within the hot-spot feeding areas of southern versus northern resident killer whales. This implies that southern resident killer whales have greater access to Chinook salmon compared to northern residents during summer—and that any food shortage southern residents may be encountering is occurring at other times of year, or elsewhere in their range.
... Given the lack of evidence of a sex difference in the source level of echolocation clicks or buzzes, it is unlikely that the observed differences in response by sex are due to an unequal ability to detect female and male buzzes in high noise. Instead, these different responses to noise may support the different foraging strategies employed by males and females in these populations (Holt, Tennessen, Ward, et al., 2021;Tennessen, Holt, Hanson, et al., 2019;Tennessen, Holt, Ward, et al., 2019;Tennessen et al., 2023;Wright et al., 2016). ...
... Females, some of whom may be lactating, need to tend to vulnerable calves. The presence of a calf reduces its mother's likelihood of prey capture (Tennessen et al., 2023), and females with vulnerable offspring often forage in shallower areas and are unlikely to continue foraging in the presence of nearby vessels (Holt, Tennessen, Ward, et al., 2021). Consequently, females may be less likely to engage in energetically costly prey pursuit that may not be successful in greater noise. ...
... While we cannot completely rule out this prediction, it is unlikely that this alone explains the increase in searching effort as noise level increased, for two reasons. First, when resident-type killer whales are engaged in a searching behavioral state, they are more likely to continue searching on the next dive than transition to any other state (Holt, Tennessen, Ward, et al., 2021;Tennessen, Holt, Ward, et al., 2019). This high persistence in searching behavior is characteristic of foraging behavior in other cetaceans as well (e.g., Isojunno & Miller, 2018;Quick et al., 2017;Schwarz et al., 2021). ...
Understanding how the environment mediates an organism's ability to meet basic survival requirements is a fundamental goal of ecology. Vessel noise is a global threat to marine ecosystems and is increasing in intensity and spatiotemporal extent due to growth in shipping coupled with physical changes to ocean soundscapes from ocean warming and acidification. Odontocetes rely on biosonar to forage, yet determining the consequences of vessel noise on foraging has been limited by the challenges of observing underwater foraging outcomes and measuring noise levels received by individuals. To address these challenges, we leveraged a unique acoustic and movement dataset from 25 animal‐borne biologging tags temporarily attached to individuals from two populations of fish‐eating killer whales ( Orcinus orca ) in highly transited coastal waters to (1) test for the effects of vessel noise on foraging behaviors—searching (slow‐click echolocation), pursuit (buzzes), and capture and (2) investigate the mechanism of interference. For every 1 dB increase in maximum noise level, there was a 4% increase in the odds of searching for prey by both sexes, a 58% decrease in the odds of pursuit by females and a 12.5% decrease in the odds of prey capture by both sexes. Moreover, all but one deep (≥75 m) foraging attempt with noise ≥110 dB re 1 μPa (15–45 kHz band; n = 6 dives by n = 4 whales) resulted in failed prey capture. These responses are consistent with an auditory masking mechanism. Our findings demonstrate the effects of vessel noise across multiple phases of odontocete foraging, underscoring the importance of managing anthropogenic inputs into soundscapes to achieve conservation objectives for acoustically sensitive species. While the timescales for recovering depleted prey species may span decades, these findings suggest that complementary actions to reduce ocean noise in the short term offer a critical pathway for recovering odontocete foraging opportunities.
... However, attempts to identify behaviours using kinematic variables, time-depth data, and Hidden Markov models (HMMs) have tended to categorize abstract activity states (e.g. State 1, 2 and 3) rather than biologically meaningful behavioural states [e.g., foraging, travelling and resting; [12][13][14][15]. Such descriptions and assertions of behavioural states derived from analysis of movements (e.g., HMMs) need validation, as well as clearly defined functions that are biologically meaningful to be useful for predicting energetic costs. ...
... Many analyses have applied HMMs to cetacean data to predict behaviors that occurred during individual dives lasting a few minutes rather than describe behaviours that occur over longer sequences of dives lasting 10 minutes or more [12][13][14][15][16]. Unfortunately, counting breaths over short durations can result in inaccurate predictions of energy expenditure if animals have not had enough time to off-load CO 2 and balance their O 2 stores [17][18][19]. ...
... Lastly, we found that VO 2 predicted from respiration rate significantly varied among behaviours for both adult males and juveniles with both age categories of killer whales spending significantly less energy while resting, and juveniles expending less energy overall than the larger males. 40], and killer whales [12,15,20,41]. These studies demonstrate that HMMs are a robust method to categorize behaviours using movement data in cetaceans. ...
Measuring breathing rates is a means by which oxygen intake and metabolic rates can be estimated to determine food requirements and energy expenditure of killer whales (Orcinus orca) and other cetaceans. This relatively simple measure also allows the energetic consequences of environmental stressors to cetaceans to be understood but requires knowing respiration rates while they are engaged in different behaviours such as resting, travelling and foraging. We calculated respiration rates for different behavioural states of southern and northern resident killer whales using video from UAV drones and concurrent biologging data from animal-borne tags. Behavioural states of dive tracks were predicted using hierarchical hidden Markov models (HHMM) parameterized with time-depth data and with labeled tracks of drone-identified behavioural states (from drone footage that overlapped with the time-depth data). Dive tracks were sequences of dives and surface intervals lasting ≥ 10 minutes cumulative duration. We calculated respiration rates and estimated oxygen consumption rates for the predicted behavioural states of the tracks. We found that juvenile killer whales breathed at a higher rate when travelling (1.6 breaths min⁻¹) compared to resting (1.2) and foraging (1.5)—and that adult males breathed at a higher rate when travelling (1.8) compared to both foraging (1.7) and resting (1.3). The juveniles in our study were estimated to consume 2.5–18.3 L O2 min⁻¹ compared with 14.3–59.8 L O2 min⁻¹ for adult males across all behaviours based on estimates of mass-specific tidal volume and oxygen extraction. Our findings confirm that killer whales take single breaths between dives and indicate that energy expenditure derived from respirations requires using sex, age, and behavioural-specific respiration rates. These findings can be applied to bioenergetics models on a behavioural-specific basis, and contribute towards obtaining better predictions of dive behaviours, energy expenditure and the food requirements of apex predators.
... Whale-watching can cause short- (Christiansen et al., 2010;Constantine et al., 2004) and long-term negative effects on cetaceans (e.g., relative decreases in abundance, population shifts) (Bejder et al., 2006;Lusseau et al., 2006). There are several drivers for behavioural changes, including vessel approach type (e.g., in-path or line-abreast) (Constantine, 2001;Sprogis et al., 2020a,b;Williams et al., 2002a,b), speed (Holt et al., 2021;Sprogis et al., 2023), proximity (Williams et al., 2002a,b), the number of vessels present (Constantine et al., 2004;Villagra et al., 2021; and underwater vessel noise level (Sprogis et al., 2020a,b). Noise disturbance has received comparatively less research in the literature on whale-watching impacts. ...
... The mother/non-parent whale was continuously tracked unless it was impossible (i.e., the adult dove to depth), in which case only the calf was followed. Different sexes may have various sensitivities to stressors (Holt et al., 2021;Symons et al., 2014;Williams et al., 2002a,b); thus, it only assumed that females were targeted to reduce any sex differences. Different age classes may have different sensitivities to stressors; therefore, only adult-calf pairs were the targets. ...
... Physical and acoustic disturbance from vessels is recognized as a primary threat to recovery in killer whale (Orcinus orca) populations in the eastern North Pacific (Fisheries and Oceans Canada 2017). Studies on the southern resident killer whale (SRKW) population indicate that when vessels are close, whales spend less time foraging and more time travelling (Lusseau et al. 2009), are more likely to perform surface active behaviours , and have decreased rates of prey capture (Holt et al. 2021). Additionally, increases in vessel number and proximity correspond to changes in SRKW swimming paths that are consistent with vessel avoidance (Williams et al. 2009a). ...
Area-based protection is an important tool for safeguarding key habitat. Reserves that focus on mitigation of specific threats are particularly effective and are more likely to support a measurable outcome. In the marine environment, reserves that limit vessel presence have the potential to reduce disturbance to marine mammals. However, assessing the efficacy of reserves has been an ongoing challenge. Physical and acoustic disturbance from vessels is recognized as a primary threat to recovery for the northern resident killer whale (NRKW) population in Canadian Pacific waters. The Robson Bight Michael Bigg Ecological Reserve (RBMBER) was developed to support the behaviour of beach rubbing, a culturally distinct and traditionally important activity. Beach rubbing provides a rare opportunity to quantify vessel disturbance of a behaviour associated with a fixed geographic location, identifiable by visual cues, and verifiable acoustically. Observations on vessel presence, NRKW rubbing frequency, and duration were collected from a beach inside the reserve and compared to a beach in proximity to, but outside of, the RBMBER. In 2019-2022, vessel counts near the RBMBER beach were significantly lower than near the unprotected beach, and overall, rubbing occurred more frequently inside the reserve (78% of visits) than outside (35%). However, outside the reserve, concurrent vessel presence did not predict the occurrence of rubbing activity, indicating that vessel presence may negatively affect beach rubbing through long-term learned avoidance of frequently impacted areas.
... Based on our study, we found that HMMs can be useful in this context for three major reasons. First, when applied in movement ecology HMMs help visualize behavioral dynamics that cannot easily be observed, which is especially important when studying aquatic animals [2,23,30]. Second, HMMs can uncover dynamics that are normally unobservable and might be counterintuitive. For example, in one case an HMM approach revealed that while roads can often be barriers to movement for terrestrial carnivores, areas near roads can also simultaneously be preferred for foraging [20]. ...
Background
Freshwater ecosystems are some of the most affected by biological invasions due, in part, to the introduction of invasive carp worldwide. Where carp have become established, management programs often seek to limit further range expansion into new areas by reducing their movement through interconnected rivers and waterways. Lock and dams are important locations for non-physical deterrents, such as carbon dioxide (CO2), to reduce unwanted fish passage without disrupting human use. The purpose of this study was to evaluate the behavioral responses of common carp (Cyprinus carpio) to non-physical deterrents within a navigation structure on the Fox River, Wisconsin. Acoustic telemetry combined with hidden Markov models (HMMs) was used to analyze variation in carp responses to treatments. Outcomes may inform CO2 effectiveness at preventing invasive carp movement through movement pinch-points.
Methods
Carbon dioxide (CO2) was recently registered as a pesticide in the United States for use as a deterrent to invasive carp movement. As a part of a multi-component study to test a large-scale CO2 delivery system within a navigation lock, we characterized the influence of elevated CO2 and forced water circulation in the lock chamber on carp movements and behavior. Through time-to-event analyses, we described the responses of acoustic-tagged carp to experimental treatments including (1) CO2 injection in water with forced water circulation, (2) forced water circulation without CO2 and (3) no forced water circulation or CO2. We then used hidden Markov models (HMMs) to define fine-scale carp movement and evaluate the relationships between carp behavioral states and CO2 concentration, forced water circulation, and temperature.
Results
Forced water circulation with and without CO2 injection were effective at expelling carp from the lock chamber relative to null treatments where no stimulus was applied. A portion of carp exposed to forced water circulation with CO2 transitioned from an exploratory to an encamped behavioral state with shorter step-lengths and a unimodal distribution in turning angles, resulting in some carp remaining in the lock chamber. Whereas carp exposed to forced water circulation only remained primarily in an exploratory behavioral state, resulting in all carp exiting the lock chamber.
Conclusion
Our findings illustrate the potential of forced water circulation, alone, as a non-physical deterrent and the efficacy of CO2 injection with forced water circulation in expelling carp from a navigation lock. Results demonstrate how acoustic telemetry and HMMs in an experimental context can describe fish behavior and inform management strategies.
... After an approximately 20% population decline in the late 1990s and early 2000s, the Southern Resident killer whales (SRKW) were listed as Endangered in Canada in 2001(Fisheries and Oceans Canada, 2018) and the USA in 2005(National Marine Fisheries Service, 2008, with identified risk factors inhibiting their recovery including reduced prey availability, toxic contamination, and vessel effects. Their endangered status has prompted a wide array of additional studies focused on topics such as their diet (Hanson et al., 2010;Hanson et al., 2021), hormone levels (Ayres et al., 2012), body condition (Stewart et al., 2021), and responses to vessel disturbance (Houghton et al., 2015;Holt et al., 2021). ...
The fish-eating Southern Resident killer whales ( Orcinus orca ) of the northeastern Pacific are listed as Endangered in both the USA and Canada. The inland waters of Washington State and British Columbia, a region known as the Salish Sea, are designated as Southern Resident critical habitat by both countries. The whales have historically had regular monthly presence in the Salish Sea, with peak abundance occurring from May through September. In recent years, at least partially in response to shifting prey abundance, habitat usage by the Southern Residents has changed. As conservation measures aim to provide the best possible protection for the whales in their hopeful recovery, it is key that policies are based both on historic trends and current data. To this aim, our study shares 2018–2022 daily occurrence data to build upon and compare to previously published whale presence numbers and to demonstrate more recent habitat shifts. Based on reports from an extensive network of community scientists as well as online streaming hydrophones, every Southern Resident occurrence was confirmed either visually or acoustically. Documented here are the first-ever total absence of the Southern Residents in the Salish Sea in the months of May, June, and August, as well as their continued overall declining presence in the spring and summer, while fall and winter presence remains relatively high. It is key that management efforts consider these shifting presence patterns when setting both seasonal and regional protection measures aimed at supporting population recovery.
