April 2022 – Geospatial Ecology of Marine Megafauna Laboratory

Dive into Oregon’s underwater forests

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

When I was younger, I aspired to be a marine mammal biologist. I thought it was purely about knowing as much about marine mammal species as possible. However, over time and with experience in this field, I have realized that in order to understand a species, you need to have a holistic understanding of its prey, habitat, and environment. When I first applied to be advised by Leigh in the GEMM Lab, I had no idea how much of my time I would spend looking at tiny zooplankton under a microscope, thinking about the different benefits of different habitat types, or reading about oceanographic processes. But these things have been incredibly vital to my research to date and as a result, I now refer to myself as a marine ecologist. This holistic understanding that I am gaining will only grow throughout my PhD as I am broadly looking at the habitat use, site fidelity, and population dynamics of the Pacific Coast Feeding Group (PCFG) of gray whales for my thesis research.

The PCFG display many foraging tactics and occupy several habitat types along the Oregon coast while they spend their summer feeding seasons here (Torres et al. 2018). Here, I will focus on one of these habitats: kelp. When you hear the word kelp, you probably conjure an image of long, thick stalks that reach from the ocean floor to the surface, with billowing fronds waving around (Figure 1a). However, this type is only one of three basic morphologies (Filbee-Dexter & Scheibling 2014) and it is called canopy kelp, which often forms extensive forests. The other two morphologies are stipitate and prostrate kelps. The former forms midwater stands (Figure 1b) while the latter forms low-lying kelp beds (Figure 1c). All three of these morphologies exist on the Oregon coast and create a mosaic of understory and canopy kelp patches that dot our coastline.

Figure 1. Examples of the three different kelp morphologies. a: bull kelp (*Nereocystis luetkeana*) is a type of canopy kelp and the dominant kelp on the Oregon coast (Source: Oregon Coast Aquarium); b: sea palm (*Postelsia palmaeformis*) is a type of stipitate kelp that forms mid-water stands (Source: Oregon Conservation Strategy); c: sea cabbage (*Saccharina sessilis*) is a type of prostrate kelp that is stipeless and forms low-lying kelp beds (Source: Central Coast Biodiversity).

One of the most magnificent things about kelp is that it is not just a species itself, but it provides critical habitat, refuge, and food resources to a myriad of other species due to its high rates of primary production (Dayton 1985). Kelp is often referred to as a foundation species due to all of these critical services it provides. In Oregon, many species of rockfish, which are important commercial and recreational fisheries, use kelp as habitat throughout their life cycle, including as nursery grounds. Lingcod, another widely fished species, forages amongst kelp. A large number of macroinvertebrates can be found in Oregon kelp forests, including anemones, limpets, snails, sea urchins, sea stars, and abalone, to name a fraction of them.

Kelps grow best in cold, nutrient-rich waters (Tegner et al. 1996) and their growth and distribution patterns are highly naturally variable on both temporal and spatial scales (Krumhansl et al. 2016). However, warm water, low nutrient or light conditions, intensive grazing by herbivores, and severe storm activity can lead to the erosion and defoliation of kelp beds (Krumhansl et al. 2016). While these events can occur naturally in cyclical patterns, the frequency of several of these events has increased in recent years, as a result of climate change and anthropogenic impacts. For example, Dawn’s blog discussed increasing marine heatwaves that represent an influx of warm water for a prolonged period of time. In fact, kelps can be useful sentinels of change as they tend to be highly responsive to changes in environmental conditions (e.g., Rogers-Bennet & Catton 2019) and their nearshore, coastal location directly exposes them to human activities, such as pollution, harvesting, and fishing (Bennett et al. 2016).

Due to its foundational role, changes or impacts to kelp can reverberate throughout the ecosystem and negatively affect many other species. As mentioned previously, kelp is naturally highly variable, and like many other ecological processes, undergoes boom and bust cycles. For over four decades, dense, productive kelp forests have been shown to transition to sea urchin barrens, and back again, in natural cycles (Sala et al. 1998; Pinnegar et al. 2000; Steneck et al. 2002; Figure 2). These transitions are called phase shifts. In a healthy, balanced kelp forest, sea urchins typically passively feed on detrital plant matter, such as broken off pieces of kelp fronds that fall to the seafloor. A phase shift occurs when the grazing intensity of sea urchins increases, resulting in them actively feeding on kelp stalks and fronds to a point where the kelp in an area can become greatly reduced, creating an urchin barren. Sea urchin grazing intensity can change for a number of reasons, including reduction in sea urchin predators (e.g., sea otters, sunflower sea stars) or poor kelp recruitment events (e.g., due to warm water temperature). Regardless of the reason, the phases tend to transition back and forth over time. However, there is concern that sea urchin barrens may become an alternative stable state of the subtidal ecosystem from which kelp in an area cannot recover (Filbee-Dexter & Scheibling 2014).

Figure 2. Screenshots from GoPro videos from 2016 (left) and 2018 (right) at the same kayak sampling station in Port Orford showing the difference between a dense kelp forest and what appears to be an urchin barren. (Source: GEMM Lab).

For example, in 2014, bull kelp canopy cover in northern California was reduced by >90% and has not shown signs of recovery since (Rogers-Bennet & Catton 2019; Figure 3). This massive decline was attributed to two major events: 1) the onset of sea star wasting disease (SSWD) in 2013 and 2) the “warm blob” of 2014-2016. SSWD affected over 20 sea star species along the coast from Mexico to Alaska, with the predatory sunflower sea star, which consumes purple sea urchins, most affected, including population declines of 80-100% along the coast (Harvell et al. 2019). Following this SSWD outbreak, the “warm blob”, which was an extreme marine heatwave in the Pacific Ocean, caused ocean temperatures to spike. These two events allowed purple sea urchin populations to grow unchecked by their predators, and created nutrient-poor and warm water conditions, which limited kelp growth and productivity. Intense grazing on bull kelp by growing urchin populations resulted in the >90% reduction in bull kelp canopy cover and has left behind widespread urchin barrens instead (Rogers-Bennet & Catton 2019). Consequently, there have been ecological and economic impacts on the ecosystem and communities in northern California. Without bull kelp, red abalone and red sea urchin populations starved, leading to a subsequent loss of the recreational red abalone (estimated value of $44 million/year) and commercial red urchin fisheries in northern California (Rogers-Bennet & Catton 2019).

Figure 3. Surface kelp canopy area pre- and post-impact from sites in Sonoma and Mendocino counties, northern California from aerial surveys (2008, 2014-2016). Figure and figure caption taken from Rogers-Bennett & Catton (2019).

As I mentioned earlier, while phase shifts between kelp forests and urchin barrens are common cycles, the intensity of the events described above in northern California are an example of sea urchin barrens potentially becoming a stable state of the subtidal ecosystem (Filbee-Dexter & Scheibling 2014). Given that marine heatwaves are only expected to increase in intensity and frequency in the future (Frölicher et al. 2018), the events documented in northern California may not be an isolated incidence.

Considering that parts of the Oregon coast, particularly the southern portion, are very similar to northern California biogeographically, and that it was not exempt from the “warm blob”, similar changes in kelp forests may be occurring along our coast. There are many individuals and groups that are actively working on this issue to examine potential impacts to kelp and the species that depend on the services it provides. For more information, check out the Oregon Kelp Alliance.

Figure 4. A gray whale surfaces in a large kelp bed during a foraging bout along the Oregon coast. (Source: GEMM Lab).

So, what does all of this information have to do with gray whales? Given their affinity for kelp habitats (Figure 4) and their zooplankton prey that aggregates there, changes to kelp ecosystems may affect gray whale health and ecology. This aspect of the complex kelp trophic web has not been examined to date; thus one of my PhD chapters focuses on the response of gray whales to changing kelp ecosystems along the southern Oregon coast. To do this, I am examining 6 years of data collected during the TOPAZ/JASPER project in Port Orford, to look at the relationships between kelp health, sea urchin density, zooplankton abundance, and gray whale foraging effort over space and time. Documenting impacts of changing kelp forests on gray whales is important to assist management efforts as healthy and abundant kelp seems critical in providing ample food opportunities for these iconic Pacific Northwest marine predators.

Did you enjoy this blog? Want to learn more about marine life, research, and conservation? Subscribe to our blog and get a weekly alert when we make a new post! Just add your name into the subscribe box on the left panel.

References

Bennett S, et al. The ‘Great Southern Reef’: Social, ecological and economic value of Australia’s neglected kelp forests. Marine and Freshwater Research 67:47-56.

Dayton PK (1985) Ecology of kelp communities. Annual Review of Ecology and Systematics 16:215-245.

Filbee-Dexter K, Scheibling RE (2014) Sea uechin barrens as alternative stable states of collapsed kelp ecosystems. Marine Ecology Progress Series 495:1-25.

Frölicher TL, Fischer EM, Gruber N (2018) Marine heatwaves under global warming. Nature 560:360-364.

Harvell CD, et al. (2019) Disease epidemic and a marine heat wave are associated with the continental-scale collapse of a pivotal predator (Pycnopodia helianthoides). Science Advances 5(1) doi:10.1126/sciadv.aau7042.

Krumhansl KA, et al. (2016) Global patterns of kelp forest change over the past half-century. Proceedings of the National Academy of Sciences of the United States of America 113(48):13785-13790.

Pinnegar JK, et al. (2000) Trophic cascades in benthic marine ecosystems: lessons for fisheries and protected-area management. Environmental Conservation 27:179-200.

Rogers-Bennett L, Catton CA (2019) Marine heat wave and multiple stressors tip bull kelp forest to sea urchin barrens. Scientific Reports 9:15050.

Sala E, Boudouresque CF, Harmelin-Vivien M (1998) Fishing, trophic cascades and the structure of algal assemblages; evaluation of an old but untested paradigm. Oikos 82:425-439.

Steneck RS, et al. (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environmental Conservation 29:436-459.

Tegner MJ, Dayton PK, Edwards PB, Riser KL (1996) Is there evidence for the long-term climatic change in southern California kelp forests? California Cooperative Oceanic Fisheries Investigations Report 37:111-126.

Torres LG, Nieukirk SL, Lemos L, Chandler TE (2018) Drone up! Quantifying whale behavior from a new perspective improves observational capacity. Frontiers in Marine Science doi:10.3389/fmars.2019.00319.

A pregnancy test for whales?! Why and how?

Dr. Alejandro A. Fernández Ajó, Postdoctoral Scholar, Marine Mammal Institute – OSU Department of Fisheries, Wildlife, & Conservation Sciences, Geospatial Ecology of Marine Megafauna (GEMM) Lab.

I often receive two reactions when asked what I am currently working on; one is “Wow! That is a very cool job, it must be amazing to work with such incredible animals!”, the other is “How do you do that and why is that important?”. So, today I decided to blog about some of the reasons why it is important to develop a pregnancy test for gray whales and how we are doing this.

In a previous blogpost, I described the many ways in which whales play critical roles in sustaining marine ecosystem. Briefly, whales can enhance marine productivity by vertically and horizontally mixing of ocean waters, promoting primary production, and mitigating climate change by sequestering carbon with their large biomass and long life-span (1-3). Even after they die, their carcasses can contribute to biodiversity creating new habitat on the seafloor (4). But, over several decades, the whaling industry drastically removed whales around the globe, with some species and populations depleted to near extinction (5). Consequently, these depleted whale populations now play a diminished role in ocean ecosystem processes and their recovery is currently challenged by an increasing number of modern anthropogenic impacts. Hence, working towards whale conservation is essential for keeping a healthy marine ecosystem.

Working and designing effective strategies for conservation biology often involves gaining knowledge regarding the reproductive parameters of individual animals in wild populations. This information is critical for understanding population trends and the underlaying mechanisms that affect animal welfare and their potential for recovery. However, getting such information from free-living whales can be challenging (see Hunt et al. 2013). While we know that whales typically have long life-spans, lengthy generation times, extended parental care, and high survival rates, detailed knowledge on the life history and general reproductive biology of free-ranging whales is limited for the majority of the whale populations. In fact, much of what we do know about whale reproduction is derived from whaling records. Only recently, conservation physiology approaches (see our previous post here) have contributed alternative and non-invasive methods for monitoring key physiological processes that can help monitor a whale’s reproductive biology and determine reproductive parameters such as sexual maturity and pregnancy (6-9).

In this clip you can see an example of a fecal sample collection from a gray whale off the Oregon coast. We can look at hormones in the fecal samples which are useful indicators for endocrine assessments of free-swimming whales. Fecal sample and footage filmed under NOAA/NMFS permit #16111.

Gray whales (Eschrichtius robustus) in the Eastern North Pacific (ENP) typically undertake annual migrations between their lower latitude breeding grounds in the coastal waters of the Baja California Peninsula, Mexico, and the foraging grounds located on the Bering and Chukchi Seas (10). However, among the ENP whales a distinct subgroup of about 230 whales shorten their migration to feed in the coastal waters of Northern California, Oregon, and southeastern Alaska (11). This group of whales is known as the gray whale Pacific Coast Feeding Group (PCFG).

Since 2016, the GEMM Lab has monitored individual gray whales within the PCFG off the Oregon coast (check the GRANITE project). Gray whales have a distinct mottled skin; and each individual whale presents a unique pigmentation pattern that allows for the individual identification of whales. We can identify who is who among the whales who visit the Oregon coast. In this way, we can keep a detailed record of re-sightings of known individuals (visit our new web site to know more about the lives of individual whales that visit the Oregon coast). We have high individual re-sighting rates, so this unique opportunity helps us keep a long-term data series for individual whales to monitor their health, body condition, and reproductive status over time, and thus further develop and advance our non-invasive study methods.

We are combining behavioral and feeding ecology with drone photogrammetry and endocrinology of the same individual whales to help us understand the relationships between natural and anthropogenic drivers with biological parameters. In this way, following individual whales, we are developing sensitive biomarkers to monitor and infer about the population health, population trends, and identify stressors that impact their recovery and welfare. In particular, we are now working to develop a noninvasive approach to detect pregnancy in gray whales based on fecal hormone analyses.

In this picture you can see “Rose”, a gray whale calf, on top of her mother “Scarlett”. Scarlett is one of the most recognizable whales from the PCFG, due to a large scar on the right side of her back (not visible in this picture). She has been observed along the Pacific NW coast since 1996, so she is at least 26 years old today. We know 3 of her calves. Following individual whales like Scarlett is helping us to better understand the gray whale reproductive biology. Photo by Alejandro Fernandez Ajo taken under NOAA/NMFS permit #21678.

In marine mammals, the progesterone hormone is secreted in the ovaries during the estrous cycle and gestation, and is the predominant hormone responsible for sustaining pregnancy (12). As the hormones are cleared from the blood into the gut, they are metabolized and eventually excreted in feces; fecal samples represent a cumulative and integrated concentration of hormone metabolites (13-14), which are useful indicators for endocrine assessments of free-swimming whales. Several studies show that changes in hormone concentration correlate in meaningful ways with exposure to stressors (15-16) and changes in reproductive status (17-19). We are using our long data series of fecal hormones and individual life histories to advance our understanding on the gray whales’ reproductive biology. We are close to developing a technique that will allow us to detect pregnancy in whales based in fecal hormones analyses and photogrammetry. Stay tuned for results from this pregnancy test!

References:

1- Pershing AJ, Christensen LB, Record NR, Sherwood GD, Stetson PB (2010) The impact of whaling on the ocean carbon cycle: Why bigger was better. PLoS ONE 5(8): e12444.

2- Roman J and McCarthy JJ. 2010. The whale pump: marine mammals enhance primary productivity in a coastal basin. PLoS ONE. 5(10): e13255.

3- Morissette L, Kaschner K, and Gerber LR. 2010. “Whales eat fish”? Demystifying the myth in the Caribbean marine ecosystem. Fish Fish 11: 388–404.

4- Smith CR, Roman J, Nation JB. A metapopulation model for whale-fall specialists: The largest whales are essential to prevent species extinctions. J. Mar. Res. 77, 283–302 (2019).

5- Branch TA, Williams TM. Legacy of industrial whaling. Whales. Whal. Ocean Ecosyst. 2006, 262–278 (2006).

6- Kellar NM, Keliher J, Trego ML, Catelani KN, Hanns C, George JC, et al. Variation of bowhead whale progesterone concentrations across demographic groups and sample matrices. Endanger Species Res 2013; 22:61–72. https://doi.org/10.3354/esr00537.

7- Pallin L, Robbins J, Kellar N, Berube M, Friedlaender A. Validation of a blubber-based endocrine pregnancy test for humpback whales. Conserv Physiol 2018;6:1 11. https://doi.org/10.1093/conphys/coy031PMID:29942518.

8-Hunt KE, Robbins J, Buck CL, Bérubé M, Rolland RM (2019) Evaluation of fecal hormones for noninvasive research on reproduction and stress in humpback whales (Megaptera novaeangliae). Gen Comp Endocrinol 280: 24–34.

9-Melica, V., Atkinson, S., Calambokidis, J., Lang, A., Scordino, J., & Mueter, F. (2021). Application of endocrine biomarkers to update information on reproductive physiology in gray whale (Eschrichtius robustus). Plos one, 16(8), e0255368.

10-Swartz SL. Gray Whale. In: Wursig B, Thewissen JGM, Kovacs KM, editors. Encyclopedia of Marine Mammals (Third Edition). Elsevier;2018,p. 422–8.https://doi.org/10.1016/B978-0-12-804327-1.00140–0.

11-Calambokidis J, Darling JD, Deecke V, Gearin P, Gosho M, Megill W, et al. Abundance, range and movements of a feeding aggregation of gray whales (Eschrichtius robustus) from California to south-eastern Alaska in 1998. J Cetacean Res Manag 2002;4:267–76.

12- Bronson, F. H. (1989). Mammalian reproductive biology. University of Chicago Press.

13-Wasser SK, Hunt KE, Brown JL, Cooper K, Crockett CM, Bechert U, Millspaugh JJ, Larson S, Monfort SL (2000) A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. Gen Comp Endocrinol120:260–275.

14- Hunt, K.E., Rolland, R.M., Kraus, S.D., Wasser, S.K., 2006. Analysis of fecal glucocorticoids in the North Atlantic right whale (Eubalaena glacialis). Gen. Comp. Endocrinol. 148, 260–272. https://doi.org/10.1016/j.ygcen.2006.03.01215.

15- Lemos, L.S., Olsen, A., Smith, A., Burnett, J.D., Chandler, T.E., Larson, S., Hunt, K.E., Torres, L.G., 2021. Stressed and slim or relaxed and chubby? A simultaneous assessment of gray whale body condition and hormone variability. Mar. Mammal Sci. 1–11. https://doi.org/10.1111/mms.12877

16- Rolland, R., McLellan, W., Moore, M., Harms, C., Burgess, E., Hunt, K., 2017. Fecal glucocorticoids and anthropogenic injury and mortality in North Atlantic right whales Eubalaena glacialis. Endanger. Species Res. 34, 417–429. https://doi.org/10.3354/esr00866.

17-Rolland, R.M., Hunt, K.E., Kraus, S.D., Wasser, S.K., 2005. Assessing reproductive status of right whales (Eubalaena glacialis) using fecal hormone metabolites. Gen. Comp. Endocrinol. 142, 308–317. https://doi.org/10.1016/j.ygcen.2005.02.002

18- Valenzuela Molina M, Atkinson S, Mashburn K, Gendron D, Brownell RL. Fecal steroid hormones reveal reproductive state in female blue whales sampled in the Gulf of California, Mexico. Gen Comp Endocrinol 2018;261:127–35.https://doi.org/10.1016/j.ygcen.2018.02.015 PMID:29476760.

19- Hunt, K. E., Robbins, J., Buck, C. L., Bérubé, M., & Rolland, R. M. (2019). Evaluation of fecal hormones for noninvasive research on reproduction and stress in humpback whales (Megaptera novaeangliae). General and Comparative Endocrinology, 280, 24-34.

What drives individual specialization?

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

When I wrote my first blog on individual specialization well over a year ago, I just skimmed the surface of the literature on this topic and only started to recognize the importance of studying individual specialization. The question, “is there individual specialization in the PCFG of gray whales?” is the focus of my first thesis chapter and the results will affect all my subsequent work. Therefore, the literature and concepts of individual specialization are a focus of my literature review and studies.

In my previous blog I focused on common characteristics of individuals that are similarly specialized as an underlying driver of individual specialization. While these characteristics (often attributable to age, sex, or physical traits) are important to consider, I’ve learned that the list of drivers of individual specialization is long and that many variables are dynamic. Of all the drivers I’ve learned about, competition is among the most common.

Competition is a major driver of individual specialization, and a common driver of competition is resource availability. When resource availability decreases, whether caused by increasing population density or changing environmental conditions, competition for that resource increases. As competition increases, individuals have a choice. They can choose to engage in competition, either by racing, fighting, or sharing [1], which can be costly, or they can diffuse the competition by focusing on a different resource. This second approach would be considered niche partitioning in the prey dimension. Niche partitioning is a way for individuals to share ecological space by using different resources. Essentially, individuals can share habitat without having to engage in direct competition by pursuing different prey types [2].

This switch to different prey types can change the degree of individual specialization present in the population (Figure 1). But the direction of the change is not constant. If all individuals were pursuing the same prey type under low competition conditions but then switched to different alternate prey types under high competition, then individual specialization would increase (Figure 1a). This direction has been observed across a range of species including sharks [3], otters [4]–[7], dolphins [8], [9], stickleback fish [10], [11], largemouth bass [12], banded mongoose [13], fur seals [14], and baleen whales [15].

However, if individuals were pursuing different prey types under low competition conditions (maybe because of underlying differences such as age or sex) but then switched to the same alternate prey types under high competition, diet overlap would increase, and individual specialization would decrease (Figure 1b). Furthermore, an individual might not switch to an entirely new prey type but instead add prey items to its diet [16]. This diet expansion under competition would also decrease individual specialization. Fewer studies have reported this direction but it’s been found in the common bumblebee [17] and in several neotropical vertebrate species [18], [19].

**Figure `1.** Figure 3 from Araújo et al. 2011 [20]. Illustration of how ecological mechanisms may affect the degree of individual specialization. Arrows linking resources to individual consumers indicate resource consumption (relative thickness indicates proportional contribution).
Horizontal arrows indicate the sign (positive or negative) of the effect on the degree of individual specialization. (a) Consumers share the same preferred resource (dark gray tangle) but have different alternative resources (white and light gray triangles). As the preferred resource becomes scarce, consumers switch to different alternatives, increasing the degree of individual specialization. (b) Alternatively, consumers have distinct preferred resources, so that as resources become scarce, individuals converge to the alternative resource (dark gray triangle), reducing diet variation.

Interestingly, its hypothesized that individual specialization driven by competition is one of the factors that facilitates the formation and existence of stable groups [21]. For example, a study on resident female dolphins in Sarasota Bay, FL, USA found that females with high spatial overlap used distinct foraging specializations [8](Figure 2). This study illustrates how partitioning prey enabled spatial and social coexistence. A study on banded mongooses reached a similar conclusion [13]. They found that specialization was highest in the biggest groups (with the most competition) and not explained by sex, age, or other inherent differences. They hypothesized that specialization increasing with competition reduced conflict and allowed the groups to remain stable. This study also highlighted the role of learning to determine an individual’s specialization.

**Figure 2.** A bottlenose dolphin.
*Source: https://sarasotadolphin.org*

Learning drives the distribution of knowledge throughout a population, which can lead to either specialization or generalization. ‘One-to-one’ learning, where one individual learns from one demonstrator, tends to promote individual specialization [21]. This form of transmission drives specialization because the individuals who learn the specialization tend to then carry on using, and eventually teaching, that specialization [6]. A common example of ‘one-to-one’ learning is vertical transmission from parent to offspring. It has been shown to transmit specializations in dolphins [22] and otters [6]. ‘One-to-one’ learning can occur outside of parent-offspring pairs; non-parent-offspring ‘one-to-one’ learning has been shown to drive specialization in banded mongooses [13](Figure 3).

However, other forms of social learning can promote more generalized foraging strategies. ‘Many-to-one’ or ‘one-to-many’ learning can reduce the presence of specialization in species [13], [21] as can the presence of conformity in a group [23], [24].

**Figure 3.** A group of banded mongooses.
Source: http://socialisresearch.org/about-the-banded-mongoose-project/

The multiple drivers of specialization and their dynamic quality means that it is important to contextualize specialization. For example, a study on four species of neotropical frogs found varying degrees of specialization across multiple populations of each species [18]. The degree of specialization was dependent on a variety of drivers including predation and both intra- and inter-specific competition. Notably, the direction of the relationship between degree of specialization and each driver was species specific. This study highlights that one species may not always be more specialized than another, but that a populations’ specialization is context dependent.

Therefore, it is important to not only be aware of the degree of specialization present in a population, but to also understand its dynamics and drivers. These relationships can then be used to understand how, and why, a population may react to competition from other species, predators, and changes in resource availability [20]. A population’s specialization can also affect the specialization of other populations and community dynamics [25], therefore, it’s important to consider and study individual specialization on both the population and community level. I am excited to start using our incredible six-year dataset to start investigating these questions for PCFG gray whales, so stay tuned for results!

References

[1] M. Taborsky, M. A. Cant, and J. Komdeur, The Evolution of Social Behaviour. Cambridge: Cambridge University Press, 2021. doi: 10.1017/9780511894794.

[2] E. R. Pianka, “Niche Overlap and Diffuse Competition,” vol. 71, no. 5, pp. 2141–2145, 1974.

[3] P. Matich et al., “Ecological niche partitioning within a large predator guild in a nutrient-limited estuary,” Limnol. Oceanogr., vol. 62, no. 3, pp. 934–953, 2017, doi: https://doi.org/10.1002/lno.10477.

[4] S. D. Newsome et al., “The interaction of intraspecific competition and habitat on individual diet specialization: a near range-wide examination of sea otters,” Oecologia, vol. 178, no. 1, pp. 45–59, May 2015, doi: 10.1007/s00442-015-3223-8.

[5] M. T. Tinker, G. Bentall, and J. A. Estes, “Food limitation leads to behavioral diversification and dietary specialization in sea otters,” Proc. Natl. Acad. Sci., vol. 105, no. 2, pp. 560–565, Jan. 2008, doi: 10.1073/pnas.0709263105.

[6] M. T. Tinker, M. Mangel, and J. A. Estes, “Learning to be different: acquired skills, social learning, frequency dependence, and environmental variation can cause behaviourally mediated foraging specializations,” Evol. Ecol. Res., vol. 11, pp. 841–869, 2009.

[7] M. T. Tinker et al., “Structure and mechanism of diet specialisation: testing models of individual variation in resource use with sea otters,” Ecol. Lett., vol. 15, no. 5, pp. 475–483, 2012, doi: 10.1111/j.1461-0248.2012.01760.x.

[8] S. Rossman et al., “Foraging habits in a generalist predator: Sex and age influence habitat selection and resource use among bottlenose dolphins (Tursiops truncatus),” Mar. Mammal Sci., vol. 31, no. 1, pp. 155–168, 2015, doi: https://doi.org/10.1111/mms.12143.

[9] L. G. Torres, “A kaleidoscope of mammal , bird and fish : habitat use patterns of top predators and their prey in Florida Bay,” vol. 375, pp. 289–304, 2009, doi: 10.3354/meps07743.

[10] M. S. Araújo et al., “Network Analysis Reveals Contrasting Effects of Intraspecific Competition on Individual Vs. Population Diets,” Ecology, vol. 89, no. 7, pp. 1981–1993, 2008, doi: 10.1890/07-0630.1.

[11] R. Svanbäck and D. I. Bolnick, “Intraspecific competition drives increased resource use diversity within a natural population,” Proc. R. Soc. B Biol. Sci., vol. 274, no. 1611, pp. 839–844, Mar. 2007, doi: 10.1098/rspb.2006.0198.

[12] D. E. Schindler, J. R. Hodgson, and J. F. Kitchell, “Density-dependent changes in individual foraging specialization of largemouth bass,” Oecologia, vol. 110, no. 4, pp. 592–600, May 1997, doi: 10.1007/s004420050200.

[13] C. E. Sheppard et al., “Intragroup competition predicts individual foraging specialisation in a group-living mammal,” Ecol. Lett., vol. 21, no. 5, pp. 665–673, 2018, doi: 10.1111/ele.12933.

[14] L. Kernaléguen, J. P. Y. Arnould, C. Guinet, and Y. Cherel, “Determinants of individual foraging specialization in large marine vertebrates, the Antarctic and subantarctic fur seals,” J. Anim. Ecol., vol. 84, no. 4, pp. 1081–1091, 2015, doi: 10.1111/1365-2656.12347.

[15] E. M. Keen and K. M. Qualls, “Respiratory behaviors in sympatric rorqual whales: the influence of prey depth and implications for temporal access to prey,” J. Mammal., vol. 99, no. 1, pp. 27–40, Feb. 2018, doi: 10.1093/jmammal/gyx170.

[16] R. H. MacArthur and E. R. Pianka, “On Optimal Use of a Patchy Environment,” Am. Nat., vol. 100, no. 916, pp. 603–609, 1966, doi: 10.1086/282454.

[17] C. Fontaine, C. L. Collin, and I. Dajoz, “Generalist foraging of pollinators: diet expansion at high density,” J. Ecol., vol. 96, no. 5, pp. 1002–1010, 2008, doi: 10.1111/j.1365-2745.2008.01405.x.

[18] R. Costa-Pereira, V. H. W. Rudolf, F. L. Souza, and M. S. Araújo, “Drivers of individual niche variation in coexisting species,” J. Anim. Ecol., vol. 87, no. 5, pp. 1452–1464, 2018, doi: 10.1111/1365-2656.12879.

[19] M. M. Pires, P. R. Guimarães Jr, M. S. Araújo, A. A. Giaretta, J. C. L. Costa, and S. F. dos Reis, “The nested assembly of individual-resource networks,” J. Anim. Ecol., vol. 80, no. 4, pp. 896–903, 2011, doi: 10.1111/j.1365-2656.2011.01818.x.

[20] M. S. Araújo, D. I. Bolnick, and C. A. Layman, “The ecological causes of individual specialisation,”Ecol. Lett., vol. 14, no. 9, pp. 948–958, 2011, doi: https://doi.org/10.1111/j.1461-0248.2011.01662.x.

[21] C. E. Sheppard, R. Heaphy, M. A. Cant, and H. H. Marshall, “Individual foraging specialization in group-living species,” Anim. Behav., vol. 182, pp. 285–294, Dec. 2021, doi: 10.1016/j.anbehav.2021.10.011.

[22] S. Wild, S. J. Allen, M. Krützen, S. L. King, L. Gerber, and W. J. E. Hoppitt, “Multi-network-based diffusion analysis reveals vertical cultural transmission of sponge tool use within dolphin matrilines,” Biol. Lett., vol. 15, no. 7, p. 20190227, Jul. 2019, doi: 10.1098/rsbl.2019.0227.

[23] L. M. Aplin, D. R. Farine, J. Morand-Ferron, A. Cockburn, A. Thornton, and B. C. Sheldon, “Experimentally induced innovations lead to persistent culture via conformity in wild birds,” Nature, vol. 518, no. 7540, pp. 538–541, Feb. 2015, doi: 10.1038/nature13998.

[24] E. Van de Waal, C. Borgeaud, and A. Whiten, “Potent Social Learning and Conformity Shape a Wild Primate’s Foraging Decisions,” Science, Apr. 2013, doi: 10.1126/science.1232769.

[25] D. I. Bolnick et al., “Why intraspecific trait variation matters in community ecology,” Trends Ecol. Evol., vol. 26, no. 4, pp. 183–192, Apr. 2011, doi: 10.1016/j.tree.2011.01.009.

The many dimensions of a fat whale: Using drones to measure the body condition of baleen whales

Dr. KC Bierlich, Postdoctoral Scholar, OSU Department of Fisheries, Wildlife, & Conservation Sciences, Geospatial Ecology of Marine Megafauna (GEMM) Lab

In my last blog, I discussed how to obtain morphological measurements from drone-based imagery of whales and the importance of calculating and considering uncertainty, as different drone platforms have varying levels of measurement uncertainty. But how does uncertainty scale and propagate when multiple measurements are combined, such as when measuring body condition of the whole animal? In this blog, I will discuss the different methods used for measuring body condition of baleen whales from drone-based imagery and how uncertainty differs between these metrics.

Body condition is defined as the energy stored in the body as a result of feeding and is assumed to indicate an animal’s overall health, as it reflects the balance between energy intake and investment toward growth, maintenance and reproduction (Peig and Green, 2009). Thus, body condition reflects the foraging success of an individual, as well as the potential for reproductive output and the quality of habitat. For example, female North American brown bears (Ursus arctos) in high quality habitats were in better body condition, produced larger litter sizes, and lived in greater population densities compared to females in lower quality habitats (Hilderbrand et al., 1999). As Dawn Barlow and Will Kennerley discussed in their recent blog, baleen whales are top predators and serve as ecosystem sentinels that shed light not only on the health of their population, but on the health of their ecosystem. As ocean climate conditions continue to change, monitoring the body condition of baleen whales is important to provide insight on how their population and ecosystem is responding.

As discussed in a previous blog, drones serve as a valuable tool for obtaining morphological measurements of baleen whales to estimate their body condition. Images are imported into photogrammetry software, such as MorphoMetriX (Torres and Bierlich, 2020), to measure the total length of an individual and that is then divided into perpendicular width segments (i.e., in 5 or 10% increments) down the body (Fig. 1). These total length and width measurements are then used to estimate body condition in either 1-, 2-, or 3-dimensions: a single width (1D), a projected dorsal surface area (2D), or a body volume measure (3D). These 1D, 2D, and 3D measurements of body condition can then be standardized by total length to produce a relative measure of an individual’s body condition to compare among individuals and populations.

Figure 1. An example of a Pacific Coast Feeding Group (PCFG) gray whale measured in MorphoMetriX (Torres & Bierlich, 2020).

While several different studies have used each of these dimensions to assess whale body condition, it is unclear how these measurements compare amongst each other. Importantly, it is also unclear how measurement uncertainty scales across these multiple dimensions and influences inference, which can lead to misinterpretation of data. For example, the surface area and volume of two geometrically similar bodies of different sizes are not related to their linear dimensions in the same ratio, but rather to the second and third power, respectively (i.e., x² vs. x³). Similarly, uncertainty should not be expected to scale linearly across 1D, 2D, and 3D body condition measurements.

The second chapter of my dissertation, which was recently published in Frontiers in Marine Science and includes Clara Bird and Leigh Torres as co-authors, compared the uncertainty associated with 1D, 2D, and 3D drone-based body condition measurements in three baleen whale species with different ranges in body sizes: blue, humpback, and Antarctic minke whales (Figure 2) (Bierlich et al., 2021). We used the same Bayesian model discussed in my last blog, to incorporate uncertainty associated with each 1D, 2D, and 3D estimate of body condition.

Figure 2. An example of total length and perpendicular width (in 5% increments of total length) measurements of an individual blue, humpback and Antarctic minke whale. Each image measured using MorphoMetriX (Torres and Bierlich, 2020).

We found that uncertainty does not scale linearly across multi-dimensional measurements, with 2D and 3D uncertainty increasing by a factor of 1.45 and 1.76 compared to 1D, respectively. This result means that there is an added cost of increased uncertainty when utilizing a multidimensional body condition measurement. Our finding is important to help researchers decide which body condition measurement best suits their scientific question, particularly when using a drone platform that is susceptible to greater error – as discussed in my previous blog. However, a 1D measurement only relies on a single width measurement, which may be excluding other regions of an individual’s body condition that is important for energy storage. In these situations, a 2D or 3D measure may be more appropriate.

We found that when comparing relative measures of body condition (standardized by total length of the individual), each standardized metric was highly correlated with one another. This finding suggests that 1D, 2D, and 3D metrics will draw similar relative predictions of body condition for individuals, allowing researchers to be confident they will draw similar conclusions relating to the body condition of individuals, regardless of which standardized metric they use. However, when comparing the precision of each of these metrics, the body area index (BAI) – a 2D standardized metric – displayed the highest level of precision. This result highlights how BAI can advantageously detect small changes in body condition, which is useful for comparing individuals or even tracking the same individual over time.

BAI was developed by the GEMM Lab (Burnett et al., 2018) and was designed to be similar to body mass index (BMI) in humans [BMI = mass (kg)/(height (m))²], where BAI uses the calculated surface area as a surrogate for body mass. In humans, a healthy BMI range is generally considered 18.5–24.9, below 18.5 is considered underweight, above 24.9 is considered overweight, and above 30 is considered obese (Flegal et al., 2012). Identifying a healthy range in BAI for baleen whales is challenged by a limited knowledge of what a “healthy” body condition range is for a whale. We found strong evidence that a healthy range of BAI is species-specific, as each species displayed a distinctive range in BAI: blue whales: 11–16; AMW: 17–24; humpback whales: 23–32; humpback whale calves: 23–28 (Fig. 3). These differences in BAI ranges likely reflect differences in the body shape of each species (Fig. 4). For example, humpbacks have the widest range of BAI compared to these other two species, which was also reflected in their larger variation in perpendicular widths (Figs. 2-4). Thus, it seems that BAI offers conditionally “scalefree” comparisons between species, yet it is unreasonable to set a single, all-whale BAI threshold to determine “healthy” versus “unhealthy” body condition. Collecting a large sample of body condition measurements across many individuals and demographic units over space and time with information on vital rates (e.g., reproductive capacity) will help elucidate a healthy BAI range for each species.

Figure 3. Body area index (BAI) for each species. AMW = Antarctic minke whale. Figure from Bierlich et al. (2021).

Figure 4. A) Absolute widths (m) and B) relative widths, standardized by total length (TL) to help elucidate the different body shapes of Antarctic minke whales (AMW; n = 40), blue whales (n = 32), humpback whales (n = 40), and humpback whale calves (n = 15). Note how the peak in body width occurs at a different percent body width between species, demonstrating the natural variation in body shape between baleen whales. Figure from Bierlich et al. (2021).

Over the past six years, the GEMM Lab has been collecting drone images of Pacific Coast Feeding Group (PCFG) gray whales off the coast of Oregon to measure their BAI (see GRANITE Project blog). Many of the individuals we encounter are seen across years and throughout the foraging season, providing an opportunity to evaluate how an individual’s BAI is influenced by environmental variation, stress levels, maturity, and reproduction. These data will in turn help determine what the healthy range in BAI for gray whales is. For example, linking BAI to pregnancy – whether a whale is currently pregnant or becomes pregnant the following season – will help determine what BAI is needed to support calf production. We are currently analyzing hundreds of body condition measurements from 2016 – 2021, so stay tuned for upcoming results!

References

Bierlich, K. C., Hewitt, J., Bird, C. N., Schick, R. S., Friedlaender, A., Torres, L. G., … & Johnston, D. W. (2021). Comparing Uncertainty Associated With 1-, 2-, and 3D Aerial Photogrammetry-Based Body Condition Measurements of Baleen Whales. Frontiers in Marine Science, 1729.

Burnett, J. D., Lemos, L., Barlow, D., Wing, M. G., Chandler, T., & Torres, L. G. (2018). Estimating morphometric attributes of baleen whales with photogrammetry from small UASs: A case study with blue and gray whales. Marine Mammal Science, 35(1), 108–139.

Flegal, K. M., Carroll, M. D., Kit, B. K., & Ogden, C. L. (2012). Prevalence of Obesity and Trends in the Distribution of Body Mass Index Among US Adults, 1999-2010. JAMA, 307(5), 491. https://doi.org/10.1001/jama.2012.39

Hilderbrand, G. V, Schwartz, C. C., Robbins, C. T., Jacoby, M. E., Hanley, T. A., Arthur, S. M., & Servheen, C. (1999). The importance of meat, particularly salmon, to body size, population productivity, and conservation of North American brown bears. Canadian Journal of Zoology, 77(1), 132–138.

Peig, J., & Green, A. J. (2009). New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos, 118(12), 1883–1891.

Torres, W., & Bierlich, K. C. (2020). MorphoMetriX: a photogrammetric measurement GUI for morphometric analysis of megafauna. Journal of Open Source Software, 5(45), 1825–1826.

Share this:

Share this:

References

Share this:

Share this: