How do we study the impact of whale watching?

Clara Bird, PhD Candidate, OSU Department of Fisheries, Wildlife, and Conservation Sciences, Geospatial Ecology of Marine Megafauna Lab

Since its start, the GEMM Lab has been interested in the effect of vessel disturbance on whales. From former student Florence’s masters project to Leila’s PhD work, this research has shown that gray whales on their foraging grounds have a behavioral response to vessel presence (Sullivan & Torres, 2018) and a physiological response to vessel noise (Lemos et al., 2022). Presently, our GRANITE project is continuing to investigate the effect of ambient noise on gray whales, with an emphasis on understanding how these effects might scale up to impact the population as a whole (Image 1).

To date, all this work has been focused on gray whales feeding off the coast of Oregon, but I’m excited to share that this is about to change! In just a few weeks, Leigh and I will be heading south for a pilot study looking at the effects of whale watching vessels on gray whale mom/calf pairs in the nursing lagoons of Baja California, Mexico.

Image 1. Infographic for the GRANITE project. Credit: Carrie Ekeroth

We are collaborating with a Fernanda Urrutia Osorio, a PhD candidate at Scripps Institute of Oceanography, to spend a week conducting fieldwork in one of the nursing lagoons. For this project we will be collecting drone footage of mom/calf pairs in both the presence and absence of whale watching vessels. Our goal is to see if we detect any differences in behavior when there are vessels around versus when there are not. Tourism regulations only allow the whale watching vessels to be on the water during specific hours, so we are hoping to use this regulated pattern of vessel presence and absence as a sort of experiment.

Image 2. A mom and calf pair.  NOAA/NMFS permit #21678.

The lagoons are a crucial place for mom/calf pairs, this is where calves nurse and grow before migration, and nursing is energetically costly for moms. So, it is important to study disturbance responses in this habitat since any change in behavior caused by vessels could affect both the calf’s energy intake and the mom’s energy expenditure. While this hasn’t yet been investigated for gray whales in the lagoons, similar studies have been carried out on other species in their nursing grounds.

Video 1. Footage of “likely nursing” behavior. NOAA/NMFS permit #21678.

We can use these past studies as blueprints for both data collection and processing. Disturbance studies such as these look for a wide variety of behavioral responses. These include (1) changes in activity budgets, meaning a change in the proportion of time spent in a behavior state, (2) changes in respiration rate, which would reflect a change in energy expenditure, (3) changes in path, which would indicate avoidance, (4) changes in inter-individual distance, and (5) changes in vocalizations. While it’s not necessarily possible to record all of these responses, a meta-analysis of research on the impact of whale watching vessels found that the most common responses were increases in the proportion of time spent travelling (a change in activity budget) and increased deviation in path, indicating an avoidance response (Senigaglia et al., 2016).

One of the key phrases in all these possible behavioral responses is “change in ___”. Without control data collected in the absence of whale watching vessels, it impossible to detect a difference. Some studies have conducted controlled exposures, using approaches with the research vessel as proxies for the whale watchers (Arranz et al., 2021; Sprogis et al., 2020), while others use the whale watching operators’ daily schedule and plan their data collection schedule around that (Sprogis et al., 2023). Just as ours will, all these studies collected data using drones to record whale behavior and made sure to collect footage before, during, and after exposure to the vessel(s).

One study focused on humpback mom/calf pairs found a decrease in the proportion of time spent resting and an increase in both respiration rate and swim speed during the exposure (Sprogis et al., 2020). Similarly, a study focused on short-finned pilot whale mom/calf pairs found a decrease in the mom’s resting time and the calf’s nursing time (Arranz et al., 2021). And, Sprogis et al.’s  study of Southern right whales found a decrease in resting behavior after the exposure, suggesting that the vessels’ affect lasted past their departure (Sprogis et al., 2023, Image 3). It is interesting that while these studies found changes in different response metrics, a common trend is that all these changes suggest an increase in energy expenditure caused by the disturbance.

However, it is important to note that these studies focused on short term responses. Long term impacts have not been thoroughly estimated yet. These studies provide many valuable insights, not only into the response of whales to whale watching, but also a look at the various methods used. As we prepare for our fieldwork, it’s useful to learn how other researchers have approached similar projects.

Image 3. Visual ethogram from Sprogis et al. 2023. This shows all the behaviors they identified from the footage.

I want to note that I don’t write this blog intending to condemn whale watching. I fully appreciate that offering the opportunity to view and interact with these incredible creatures is valuable. After all, it is one of the best parts of my job. But hopefully these disturbance studies can inform better regulations, such as minimum approach distances or maximum engine noise levels.

As these studies have done, our first step will be to establish an ethogram of behaviors (our list of defined behaviors that we will identify in the footage) using our pilot data. We can also record respiration and track line data. An additional response that I’m excited to add is the distance between the mom and her calf. Former GEMM Lab NSF REU intern Celest will be rejoining us to process the footage using the AI method she developed last summer (Image 4). As described in her blog, this method tracks a mom and calf pair across the video frames, and allows us to extract the distance between them. We look forward to adding this metric to the list and seeing what we can glean from the results.

Image 4. Example of a labelled frame from SLEAP, highlighting labels: rostrum, blowhole, dorsal, dorsal-knuckle, and tail. This labels are drawn to train the software to recognize the whales in unlabelled frames.

While we are just getting started, I am excited to see what we can learn about these whales and how best to study them. Stay tuned for updates from Baja!

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References

Arranz, P., Glarou, M., & Sprogis, K. R. (2021). Decreased resting and nursing in short-finned pilot whales when exposed to louder petrol engine noise of a hybrid whale-watch vessel. Scientific Reports, 11(1), 21195. https://doi.org/10.1038/s41598-021-00487-0

Lemos, L. S., Haxel, J. H., Olsen, A., Burnett, J. D., Smith, A., Chandler, T. E., Nieukirk, S. L., Larson, S. E., Hunt, K. E., & Torres, L. G. (2022). Effects of vessel traffic and ocean noise on gray whale stress hormones. Scientific Reports, 12(1), Article 1. https://doi.org/10.1038/s41598-022-14510-5

Senigaglia, V., Christiansen, F., Bejder, L., Gendron, D., Lundquist, D., Noren, D., Schaffar, A., Smith, J., Williams, R., Martinez, E., Stockin, K., & Lusseau, D. (2016). Meta-analyses of whale-watching impact studies: Comparisons of cetacean responses to disturbance. Marine Ecology Progress Series, 542, 251–263. https://doi.org/10.3354/meps11497

Sprogis, K. R., Holman, D., Arranz, P., & Christiansen, F. (2023). Effects of whale-watching activities on southern right whales in Encounter Bay, South Australia. Marine Policy, 150, 105525. https://doi.org/10.1016/j.marpol.2023.105525

Sprogis, K. R., Videsen, S., & Madsen, P. T. (2020). Vessel noise levels drive behavioural responses of humpback whales with implications for whale-watching. ELife, 9, e56760. https://doi.org/10.7554/eLife.56760

Sullivan, F. A., & Torres, L. G. (2018). Assessment of vessel disturbance to gray whales to inform sustainable ecotourism. Journal of Wildlife Management, 82(5), 896–905. https://doi.org/10.1002/jwmg.21462

Rock-solid GRANITE: Scaling the disturbance response of individual whales up to population level impacts

By Lisa Hildebrand, PhD student, OSU Department of Fisheries & Wildlife, Geospatial Ecology of Marine Megafauna Lab

Since early May, much of the GEMM Lab has been consumed by the GRANITE project, which stands for Gray whale Response to Ambient Noise Informed by Technology and Ecology. Two weeks ago, PhD student Clara Bird discussed our field work preparations, and since May 20th we have conducted five successful days of field work (and one unsuccessful day due to fog). If you are now expecting a blog about the data we have collected so far and whales we encountered, I am sorry to disappoint you. Rather, I want to take a big step back and provide the context of the GRANITE project as a whole, explain why this project and data collection is so important, and discuss what it is that we hope to achieve with our ever-growing, multidisciplinary dataset and team.

We use the Pacific Coast Feeding Group (PCFG) of gray whales that forage off the Oregon coast as our study system to better understand the ecological and physiological response of baleen whales to multiple stressors. Our field methodology includes replicate physiological and ecological sampling of this accessible baleen whale population with synoptic measurement of multiple types of stressors. We collect fecal samples for hormone analysis, conduct drone overflights of whales to collect body condition and behavioral data, record the ambient soundscape through deployment of two hydrophones, and conduct whale photo-identification to link all data streams to each individual whale of known sex, estimated age, and reproductive status. We resample these data from multiple individuals within and between summer foraging seasons, while exposed to different potential stressors occurring at different intensities and temporal periods and durations. The hydrophones are strategically placed with one in a heavily boat-trafficked (and therefore noisy) area close to the Port of Newport, while the second is located in a relatively calm (and therefore quieter) spot near the Otter Rock Marine Reserve (Fig. 1). These hydrophones provide us with information about both natural (e.g. killer whales, wind, waves) and anthropogenic (e.g. boat traffic, seismic survey, marine construction associated with PacWave wave energy facility development) noise that may affect gray whales. During sightings with whales, we also drop GoPro cameras and sample for prey to better understand the habitats where whales forage and what they might be consuming.

Figure 1. Map of GRANITE study area from Seal Rock to Lincoln City with gray whale sightings (yellow circles) and and fecal samples collected (red triangles) from the 2020 field season. Green stars represent the two hydrophone locations. Source: L. Torres.

GEMM Lab PI Dr. Leigh Torres initiated this research project in 2015 and established partnerships with acoustician Dr. Joe Haxel and (then) PhD student Dr. Leila Lemos. Since then, the team working on this project has grown considerably to provide expertise in the various disciplines that the project integrates. Leigh is currently joined at the GRANITE helm by 4 co-PIs: Dr. Haxel, endocrinologist Dr. Kathleen Hunt, biological statistician Dr. Leslie New, and physiologist Dr. Loren Buck. Drs. Alejandro Fernandez Ajo, KC Bierlich and Enrico Pirotta are postdoctoral scholars who are working on the endocrinology, photogrammetry, and biostatistical modelling components, respectively. Finally, Clara and myself are partially funded through this project for our PhD research, with Clara focusing on the links between behavior, body condition, individualization, and habitat, while I am tackling questions about the recruitment and site fidelity of the PCFG (more about these topics below). 

Faculty Research Assistant Todd Chandler supervises PhD student Clara Bird during her maiden drone flight over a whale. Source: L. Torres.

The ultimate goal of this project is to use the PCFG as a case study to quantify baleen whale physiological response to different stressors and model the subsequent impacts on the population by implementing our long-term, replicate dataset into a framework called Population consequences of disturbance (PCoD; Fig. 2). PCoD is built upon the underlying concept that changes in behavior and/or physiology caused by disturbance (i.e. noise) affect the fitness of individuals by impacting their health and vital rates, such as survival, reproductive success, and growth rate (Pirotta et al. 2018). These impacts at the individual level may (or may not) affect the population as a whole, depending on what proportion of individuals in the population are affected by the disturbance and the intensity of the disturbance effect on each individual. The PCoD framework requires quantification of four stages: a) the physiological and/or behavioral changes that occur as a result of exposure to a stressor (i.e. noise), b) the acute effects of these physiological and/or behavioral responses on individual vital rates, and their chronic effects via individual health, c) the way in which changes in health may affect the vital rates of individuals, and d) how changes in individual vital rates may affect population dynamics (Fig. 2; Pirotta et al. 2018). While four stages may not sound like a lot, the amount and longevity of data needed to quantify each stage is immense. 

Figure 2. Conceptual framework of the population consequences of disturbance (PCoD). Letters (A-D) represent the four stages that require quantification in order for PCoD to be implemented. Each colored box represents external (ecological drivers, stressors) and internal (physiology, health, vital rates, behavior) factors that can change over time that are measured for each individual whale (dashed grey boundary line). The effects are then integrated across all individuals in the population to project their effects on the population’s dynamics. Figure and caption adapted from Pirotta et al. 2018.

The ability to detect a change in behavior or physiology often requires an understanding of what is “normal” for an individual, which we commonly refer to as a baseline. The best way to establish a baseline is to collect comprehensive data over a long time period. With our data collection efforts since 2015 of fecal samples, drone flights and photo identification, we have established useful baselines of behavioral and physiological data for PCFG gray whales. These baselines are particularly impressive since it is typically difficult to collect repeated measurements of hormones and body condition from the same individual baleen whale across multiple years. These repeated measurements are important because, like all mammals, hormones and body condition vary across life history phases (i.e., with pregnancy, injury, or age class) and across time (i.e., good or bad foraging conditions). To achieve these repeated measurements, GRANITE exploits the high degree of intra- and inter-annual site fidelity of the PCFG, their accessibility for study due to their affinity for nearshore habitat use, and the long-term sighting history of many whales that provides sex and approximate age information. Our work to-date has already established a few important baselines. We now know that the body condition of PCFG gray whales increases throughout a foraging season and can fluctuate considerably between years (Soledade Lemos et al. 2020). Furthermore, there are significant differences in body condition by reproductive state, with calves and pregnant females displaying higher body conditions (Soledade Lemos et al. 2020). Our dataset has also allowed us to validate and quantify fecal steroid and thyroid hormone metabolite concentrations, providing us with putative thresholds to identify a stressed vs. not stressed whale based on its hormone levels (Lemos et al. 2020).

PhD student Lisa Hildebrand and GRANITE co-PI Dr. Kathleen Hunt collecting a fecal sample. Source: L. Torres.

We continue to collect data to improve our understanding of baseline PCFG physiology and behavior, and to detect changes in their behavior and physiology due to disturbance events. All these data will be incorporated into a PCoD framework to scale from individual to population level understanding of impacts. However, more data is not the only thing we need to quantify each of the PCoD stages. The implementation of the PCoD framework also depends on understanding several aspects of the PCFG’s population dynamics. Specifically, we need to know whether recruitment to the PCFG population occurs internally (calves born from “PCFG mothers” return to the PCFG) or externally (immigrants from the larger Eastern North Pacific gray whale population joining the PCFG as adults). The degree of internal or external recruitment to the PCFG population should be included in the PCoD model as a parameter, as it will influence how much individual level disturbance effects impact the overall health and viability of the population. Furthermore, knowing residency times and home ranges of whales within the PCFG is essential to understand exposure durations to disturbance events. 

To assess both recruitment and residency patterns of the PCFG, I am undertaking a large photo-identification effort, which includes compiling sightings and photo data across many years, regions, and collaborators. Through this effort we aim to identify calves and their return rate to the population, the rate of new adult recruits to the population, and the spatial residency of individuals in our study system. Although photo-id is a basic, commonplace method in marine mammal science, its role is critical to tracking individuals over time to understand population dynamics (in a non-invasive manner, no less). A large portion of my PhD research will focus on the tedious yet rewarding task of photo-id data management and matching in order to address these pressing knowledge gaps on PCFG population dynamics needed to implement the PCoD model that is an ultimate goal of GRANITE. I am just beginning this journey and have already pinpointed many analytical and logistical hurdles that I need to overcome. I do not anticipate an easy path to addressing these questions, but I am extremely eager to dig into the data, reveal the patterns, and integrate the findings into our rock-solid GRANITE project.  

Funding for the GRANITE project comes from the Office of Naval Research, the Department of Energy, Oregon Sea Grant, the NOAA/NMFS Ocean Acoustics Program, and the OSU Marine Mammal Institute.

References

Lemos, L.S., Olsen, A., Smith, A., Chandler, T.E., Larson, S., Hunt, K., and L.G. Torres. 2020. Assessment of fecal steroid and thyroid hormone metabolites in eastern North Pacific gray whales. Conservation Physiology 8:coaa110.

Pirotta, E., Booth, C.G., Costa, D.P., Fleishman, E., Kraus, S.D., Lusseau, D., Moretti, D., New, L.F., Schick, R.S., Schwarz, L.K., Simmons, S.E., Thomas, L., Tyack, P.L., Weise, M.J., Wells, R.S., and J. Harwood. 2018. Understanding the population consequences of disturbance. Ecology and Evolution 8(19):9934-9946.

Soledade Lemos, L., Burnett, J.D., Chandler, T.E., Sumich, J.L., and L.G. Torres. 2020. Intra- and inter-annual variation in gray whale body condition on a foraging ground. Ecosphere 11(4):e03094.

The complex relationship between behavior and body condition

Clara Bird, Masters Student, OSU Department of Fisheries and Wildlife, Geospatial Ecology of Marine Megafauna Lab

Imagine that you are a wild foraging animal: In order to forage enough food to survive and be healthy you need to be healthy enough to move around to find and eat your food. Do you see the paradox? You need to be in good condition to forage, and you need to forage to be in good condition. This complex relationship between body condition and behavior is a central aspect of my thesis.

One of the great benefits of having drone data is that we can simultaneously collect data on the body condition of the whale and on its behavior. The GEMM lab has been measuring and monitoring the body condition of gray whales for several years (check out Leila’s blog on photogrammetry for a refresher on her research). However, there is not much research linking the body condition of whales to their behavior. Hence, I have expanded my background research beyond the marine world to looked for papers that tried to understand this connection between the two factors in non-cetaceans. The literature shows that there are examples of both, so let’s go through some case studies.

Ransom et al. (2010) studied the effect of a specific type of contraception on the behavior of a population of feral horses using a mixed model. Aside from looking at the effect of the treatment (a type of contraception), they also considered the effect of body condition. There was no difference in body condition between the treatment and control groups, however, they found that body condition was a strong predictor of feeding, resting, maintenance, and social behaviors. Females with better body condition spent less time foraging than females with poorer body condition. While it was not the main question of the study, these results provide a great example of taking into account the relationship between body condition and behavior when researching any disturbance effect.

While Ransom et al. (2010) did not find that body condition affected response to treatment, Beale and Monaghan (2004) found that body condition affected the response of seabirds to human disturbance. They altered the body condition of birds at different sites by providing extra food for several days leading up to a standardized disturbance. Then the authors recorded a set of response variables to a disturbance event, such as flush distance (the distance from the disturbance when the birds leave their location). Interestingly, they found that birds with better body condition responded earlier to the disturbance (i.e., when the disturbance was farther away) than birds with poorer body condition (Figure 1). The authors suggest that this was because individuals with better body condition could afford to respond sooner to a disturbance, while individuals with poorer body condition could not afford to stop foraging and move away, and therefore did not show a behavioral response. I emphasize behavioral response because it would have been interesting to monitor the vital rates of the birds during the experiment; maybe the birds’ heart rates increased even though they did not move away. This finding is important when evaluating disturbance effects and management approaches because it demonstrates the importance of considering body condition when evaluating impacts: animals that are in the worst condition, and therefore the individuals that are most vulnerable, may appear to be undisturbed when in reality they tolerate the disturbance because they cannot afford the energy or time to move away.

Figure 1.  Figure showing flush distance of birds that were fed (good body condition) and unfed (poor body condition).

These two studies are examples of body condition affecting behavior. However, a study on the effect of habitat deterioration on lizards showed that behavior can also affect body condition. To study this effect, Amo et al. (2007) compared the behavior and body condition of lizards in ski slopes to those in natural areas. They found that habitat deterioration led to an increased perceived risk of predation, which led to an increase in movement speed when crossing these deteriorated, “risky”, areas. In turn, this elevated movement cost led to a decrease in body condition (Figure 2). Hence, the lizard’s behavior affected their body condition.


Figure 2. Figure showing the difference in body condition of lizards in natural and deteriorated habitats.

Together, these case studies provide an interesting overview of the potential answers to the question: does body condition affect behavior or does behavior affect body condition? The answer is that the relationship can go both ways. Ransom et al. (2004) showed that regardless of the treatment, behavior of female horses differed between body conditions, indicating that regardless of a disturbance, body condition affects behavior. Beale and Monaghan (2004) demonstrated that seabird reactions to disturbance differed between body conditions, indicating that disturbance studies should take body condition into account. And, Amo et al. (2007) showed that disturbance affects behavior, which consequently affects body condition.

Looking at the results from these three studies, I can envision finding similar results in my gray whale research. I hypothesize that gray whale behavior varies by body condition in everyday circumstances and when the whale is disturbed. Yet, I also hypothesize that being disturbed will affect gray whale behavior and subsequently their body condition. Therefore, what I anticipate based on these studies is a circular relationship between behavior and body condition of gray whales: if an increase in perceived risk affects behavior and then body condition, maybe those affected individuals with poor body condition will respond differently to the disturbance. It is yet to be determined if a sequence like this could ever be detected, but I think that it is important to investigate.

Reading through these studies, I am ready and eager to start digging into these hypotheses with our data. I am especially excited that I will be able to perform this investigation on an individual level because we have identified the whales in each drone video. I am confident that this work will lead to some interesting and important results connecting behavior and health, thus opening avenues for further investigations to improve conservation studies.

References

Beale, Colin M, and Pat Monaghan. 2004. “Behavioural Responses to Human Disturbance: A Matter of Choice?” Animal Behaviour 68 (5): 1065–69. https://doi.org/10.1016/j.anbehav.2004.07.002.

Ransom, Jason I, Brian S Cade, and N. Thompson Hobbs. 2010. “Influences of Immunocontraception on Time Budgets, Social Behavior, and Body Condition in Feral Horses.” Applied Animal Behaviour Science 124 (1–2): 51–60. https://doi.org/10.1016/j.applanim.2010.01.015.

Amo, Luisa, Pilar López, and José Martín. 2007. “Habitat Deterioration Affects Body Condition of Lizards: A Behavioral Approach with Iberolacerta Cyreni Lizards Inhabiting Ski Resorts.” Biological Conservation 135 (1): 77–85. https://doi.org/10.1016/j.biocon.2006.09.020.