Are there picky eaters in the PCFG?

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

As anyone who has ever been, or raised, a picky eater knows, humans have a wide range of food preferences. The diversity of available cuisines is a testament to the fact that we have individual food preferences. While taste is certainly a primary influence, nutritional benefits and accessibility are other major factors that affect our eating choices. But we are not the only species to have food preferences. In cetacean research, it is common to study the prey types consumed by a population as a whole. Narrowing these prey preferences down to the individual level is rare. While the individual component is challenging to study and to incorporate into population models, it is important to consider what the effects of individual foraging specialization might be.

To understand the role and drivers of individual specialization in population ecology, it is important to first understand the concepts of niche variation and partitioning. An animal’s ecological niche describes its role in the ecosystem it inhabits (Hutchinson, 1957). A niche is multidimensional, with dimensions for different environmental conditions and resources that a species requires. One focus of my research pertains to the dimensions of the niche related to foraging. As discussed in a previous blog, niche partitioning occurs when ecological space is shared between competitors through access to resources varies across different dimensions such as prey type, foraging location, and time of day when foraging takes place. Niche partitioning is usually discussed on the scale of different species coexisting in an ecosystem. Pianka’s theory stating that niche partitioning will increase as prey availability decreases uses competing lizard species as the example (Pianka, 1974). Typically, niche partitioning theory considers inter-specific competition (competition between species), but niche partitioning can take place within a species in response to intra-specific competition (competition between individuals of the same species) through individual niche variation.

A species that consumes a multitude of prey types is considered a generalist while one with a specific prey type is considered a specialist. Gray whales are considered generalists (Nerini, 1984). However, we do not know if each individual gray whale is a generalist or if the generalist population is actually composed of individual specialists with different preferences. One way to test for the presence of individual specialization is to compare the niche width of the population to the niche width of each individual (Figure 1, Bolnick et al., 2003).  For example, if a population eats five different types of prey and each individual consumed those prey types, those individuals would be generalists. However, if each individual only consumed one of the prey types, then those individuals would be specialists within a generalist population.

Figure 1. Figure from Bolnick et al. 2003. The thick curve represents the total niche of the population and the thin curves represent individual niches. Note that in both panels the population has the same total niche. In panel A, the individual curves overlap and are all pretty wide. These curves represent individual generalists that make up a generalist population. In panel B, the thin curves are narrower and do not overlap as much as those in panel A. These curves represent individual specialists that make up a generalist population.

If individual specialization is present in a population the natural follow-up question is why? To answer this, we look for common characteristics between the individuals that are similarly specialized. What do all the individuals that feed on the same prey type have in common? Common characterizations that may be found include age, sex, or distinct morphology (such as different beak or body shapes) (Bolnick et al., 2003).

Woo et al. (2008) studied individual specialization in Brünnich’s guillemot, a generalist sea bird species, using diet and tagging data. They found individual specialization in both diet (prey type) and behavior (dive depth, shape, and flight time). Specialization occurred across multiple timescales but was higher over short-time scales. The authors found that it was more common for an individual to specialize in a prey-type/foraging tactic for a few days than for that specialization to continue across years, although a few individuals were specialists for the full 15-year period of the study. Based on reproductive success of the studies birds, the authors concluded that the generalist and specialist strategies were largely equivalent in terms of fitness and survival. The authors searched for common characteristics in the individuals with similar specialization and they found that the differences between sexes or age classes were so small that neither grouping explained the observed individual specialization. This is an interesting result because it suggests that there is some missing attribute, that of the authors did not examine, that might explain why individual specialists were present in the population.

Hoelzel et al. (1989) studied minke whale foraging specialization by observing the foraging behaviors of 23 minke whales over five years from a small boat. They identified two foraging tactics: lunge feeding and bird-associated feeding. Lunge feeding involved lunging up through the water with an open mouth to engulf a group of fish, while bird-associated feeding took advantage of a group of fish being preyed on by sea birds to attack the fish from below while they were already being attacked from above. They found that nine individuals used lunge feeding, and of those nine, six whales used this tactic exclusively. Five of those six whales were observed in at least two years. Seventeen whales were observed using bird-associated feeding, 14 exclusively. Of those 14, eight were observed in at least two years. Interestingly, like Woo et al. (2008), this study did not find any associations between foraging tactic use and sex, age, or size of whale. Through a comparison of dive durations and feeding rates, they hypothesized that lunge feeding was more energetically costly but resulted in more food, while bird-associated feeding was energetically cheaper but had a lower capture rate. This result means that these two strategies might have the similar energetic payoffs.

Both of these studies are examples of questions that I am excited to ask using our data on the PCFG gray whales feeding off the Oregon coast (especially after doing the research for this blog). We have excellent individual-specific data to address questions of specialization because the field teams for  this project always carefully link observed behaviors with individual whale ID.  Using these data, I am curious to find out if the whales in our study group are individual specialists or generalists (or some combination of the two). I am also interested in relating specific tactics to their energetic costs and benefits in order to assess the payoffs of each foraging tactic. I then hope to combine the results of both analyses to assess the payoffs of each individual whale’s strategy.

Figure 2. Example images of two foraging tactics, side swimming (left) and headstanding (right). Images captured under NOAA/NMFS permit #21678.

Studying individual specialization is important for conservation. Consider the earlier example of a generalist population that consumes five prey items but is composed of individual specialists. If the presence of individual specialization is not accounted for in management plans, then regulations may protect certain prey types or foraging tactics/areas of the whales and not others. Such a management plan could be a dangerous outcome for the whale population because only parts of the population would be protected, while other specialists are at risk, thus potentially losing genetic diversity, cultural behaviors, and ecological resilience in the population as a whole. A plan designed to maximize protection for all the specialists would be better for the population because populations with increased ecological resilience are more likely to persist through periods of rapid environmental change. Furthermore, understanding individual specialization could help us better predict how a population might be affected by environmental change. Environmental change does not affect all prey species in the same way. An individual specialization study could help identify which whales might be most affected by predicted environmental changes. Therefore, in addition to being a fascinating and exciting research question, it is important to test for individual specialization in order to improve management and our overall understanding of the PCFG gray whale population.

References

Bolnick, D. I., Svanbäck, R., Fordyce, J. A., Yang, L. H., Davis, J. M., Hulsey, C. D., & Forister, M. L. (2003). The ecology of individuals: Incidence and implications of individual specialization. American Naturalist, 161(1), 1–28. https://doi.org/10.1086/343878

Hoelzel, A. R., Dorsey, E. M., & Stern, S. J. (1989). The foraging specializations of individual minke whales. Animal Behaviour, 38(5), 786–794. https://doi.org/10.1016/S0003-3472(89)80111-3

Hutchinson, G. E. (1957). Concluding Remarks. Cold Spring Harbor Symposia on Quantitative Biology, 22(0), 415–427. https://doi.org/10.1101/sqb.1957.022.01.039

Nerini, M. (1984). A Review of Gray Whale Feeding Ecology. In The Gray Whale: Eschrichtius Robustus (pp. 423–450). Elsevier Inc. https://doi.org/10.1016/B978-0-08-092372-7.50024-8

Pianka, E. R. (1974). Niche Overlap and Diffuse Competition. 71(5), 2141–2145.

Woo, K. J., Elliott, K. H., Davidson, M., Gaston, A. J., & Davoren, G. K. (2008). Individual specialization in diet by a generalist marine predator reflects specialization in foraging behaviour. Journal of Animal Ecology, 77(6), 1082–1091. https://doi.org/10.1111/j.1365-2656.2008.01429.x

Connecting Research Questions

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

The field season can be quite a hectic time of year. Between long days out on the water, trouble-shooting technology issues, organizing/processing the data as it comes in, and keeping up with our other projects/responsibilities, it can be quite overwhelming and exhausting.

But despite all of that, it’s an incredible and exciting time of year. Outside of the field season, we spend most of our time staring at our computers analyzing the data that we spend a relatively short amount of time collecting. When going through that process it can be easy to lose sight of why we do what we do, and to feel disconnected from the species we are studying. Oftentimes the analysis problems we encounter involve more hours of digging through coding discussion boards than learning about the animals themselves. So, as busy as it is, I find that the field season can be pretty inspiring. I have recently been looking through our most recent drone footage of gray whales and feeling renewed excitement for my thesis.

At the moment, my thesis has four central questions: (1) Are there associations between habitat type and gray whale foraging tactic? (2) Is there evidence of individualization? (3) What is the relationship between behavior and body condition? (4) Do we see evidence of learning in the behavior of mom and calf pairs? As I’ve been organizing my thoughts, what’s become quite clear is how interconnected these questions are. So, I thought I’d take this blog to describe the potential relationships.

Let’s start with the first question: are there associations between habitat types and gray whale foraging tactics? This question is central because it relates foraging behavior to habitat, which is ultimately associated with prey. This relationship is the foundation of all other questions involving foraging tactics because food is necessary for the whales to have the energy and nutrients they need to survive. It’s reasonable to think that the whales are flexible and use different foraging tactics to eat different prey that live in different habitats. But, if different prey types have different nutritional value (this is something that Lisa is studying right now; check out the COZI project to learn more), then not all whales may be getting the same nutrients.

The next question relates to the first question but is not necessarily dependent on it. It’s the question of individualization, a topic Lisa also explored in a past blog. Within our Oregon field sites we have documented a variety of gray whale foraging tactics (Torres et al. 2018; Video 1) but we do not know if all gray whales use all the tactics or if different individuals only use certain tactics. While I think it’s unlikely that one whale only uses one tactic all the time, I think we could see an individual use one tactic more often than the others. I reason that there could be two reasons for this pattern. First, it could be a response to resource availability; certain tactics are more efficient than others, this could be because the tactic involves capturing the more nutritious prey or because the behavior is less energetically demanding. Second, foraging tactics are socially learned as calves from their mothers, and hence individuals use those learned tactics more frequently. This pattern of maternally inherited foraging tactics has been documented in other marine mammals (Mann and Sargeant 2009; Estes et al. 2003). These questions between foraging tactic, habitat and individualization also tie into the remaining two questions.

My third question is about the relationship between behavior and body condition. As I’ve discussed in a previous blog, I am interested in assessing the relative energetic costs and benefits of the different foraging tactics. Is one foraging tactic more cost-effective than another (less energy out per energy in)? Ever since our lab’s cetacean behavioral ecology class, I’ve been thinking about how my work relates to niche partitioning theory (Pianka 1974).This theory states that when there is low prey availability, niche partitioning will increase. Niche partitioning can occur across several different dimensions: for instance, prey type, foraging location, and time of day when active. If gray whales partition across the prey type dimension, then different whales would feed on different kinds of prey. If whales partition resources across the foraging location dimension, individuals would feed in different areas. Lastly, if whales partition resources across the time axis, individuals would feed at different times of day. Using different foraging tactics to feed on different prey would be an example of partitioning across the prey type dimension. If there is a more preferable prey type, then maybe in years of high prey availability, we would see most of the gray whales using the same tactics to feed on the same prey type. However, in years of low prey availability we might expect to see a greater variety of foraging tactics being used. The question then becomes, does any whale end up using the less beneficial foraging tactic? If so, which whales use the less beneficial tactic? Do the same individuals always switch to the less beneficial tactic? Is there a common characteristic among the individuals that switched, like sex, age, size, or reproductive status? Lemos et al. (2020) hypothesized that the decline in body condition observed from 2016 to 2017 might be a carryover effect from low prey availability in 2016. Could it be that the whales that use the less beneficial tactic exhibit poor body condition the following year?

My fourth, and final, question asks if foraging tactics are passed down from moms to their calves. We have some footage of a mom foraging with her calf nearby, and occasionally it looks like the calf could be copying its mother. Reviewing this footage spiked my interest in seeing if there are similarities between the behavior tactics used by moms and those used by their calves after they have been weaned. While this question clearly relates to the question of individualization, it is also related to body condition: what if the foraging tactics used by the mom is influenced by her body condition at the time?

I hope to answer some of these fascinating questions using the data we have collected during our long field days over the past 6 years. In all likelihood, the story that comes together during my thesis research will be different from what I envision now and will likely lead to more questions. That being said, I’m excited to see how the story unfolds and I look forward to sharing the evolving ideas and plot lines with all of you.

References

Estes, J A, M L Riedman, M M Staedler, M T Tinker, and B E Lyon. 2003. “Individual Variation in Prey Selection by Sea Otters: Patterns, Causes and Implications.” Source: Journal of Animal Ecology. Vol. 72.

Mann, Janet, and Brooke Sargeant. 2009. “ Like Mother, like Calf: The Ontogeny of Foraging Traditions in Wild Indian Ocean Bottlenose Dolphins ( Tursiops Sp.) .” In The Biology of Traditions, 236–66. Cambridge University Press. https://doi.org/10.1017/cbo9780511584022.010.

Pianka, Eric R. 1974. “Niche Overlap and Diffuse Competition” 71 (5): 2141–45.

Soledade Lemos, Leila, Jonathan D Burnett, Todd E Chandler, James L Sumich, and Leigh G. Torres. 2020. “Intra‐ and Inter‐annual Variation in Gray Whale Body Condition on a Foraging Ground.” Ecosphere 11 (4). https://doi.org/10.1002/ecs2.3094.

Torres, Leigh G., Sharon L. Nieukirk, Leila Lemos, and Todd E. Chandler. 2018. “Drone up! Quantifying Whale Behavior from a New Perspective Improves Observational Capacity.” Frontiers in Marine Science 5 (SEP). https://doi.org/10.3389/fmars.2018.00319.

Who Am I? Exploring the theory of individualisation among marine mammals

By Lisa Hildebrand, MSc student, OSU Department of Fisheries and Wildlife, Geospatial Ecology of Marine Megafauna Lab

“Just be yourself!” is a phrase that everyone has probably heard at least once in their lives. The idea of being an individual who is distinctly different from other individuals is a concept that is focal to the society we live in today. While historically it may have been frowned upon to be the “black sheep in the crowd”, nowadays that seems to be the goal.

Source: Go Comics.

This quest for uniqueness has resulted in different styles of fashion, speech, profession, interest in art, music, literature, automobile types – the list is endless. The American Psychological Association defines personality as the “individual differences in characteristic patterns of thinking, feeling and behaving”1. So, all of the choices we make on a daily basis shape our behaviour, and our behaviour in turn shapes our personality.

Since personality is something that is so engrained within human society, it isn’t surprising that ecologists have explored this concept among non-humans. Decades of research have resulted in an abundance of literature detailing personality in many different taxa and species, ranging from chimpanzees to mice to ants2. Naturally, the definition of personality for animals differs from that for humans since the assessment of animal thoughts and feelings is still somewhat of a locked box to us. Nevertheless, the behavioural aspect of the two definitions remains consistent whereby animal personality is broadly defined as “consistent variation in behavioural traits between individuals”3.

Although I am an early career marine mammal ecologist finding my footing in this rapidly expanding field, I have a keen interest in teasing apart possible cases of individual specialisation within marine mammal populations. So, before getting straight into the nitty gritty of individual specialisation, it is important for me to take a small step back and consider the concept of specialisation as applied to small subgroups or populations of marine mammals.

Specialisations are mostly related to foraging or feeding behaviour whereby a subgroup of individuals will develop a novel method to locate and capture prey. These behaviours have been reported for several marine mammal species, and are strongly coupled to intra and inter-specific competition with other predators for prey and habitat characteristics. Furthermore, it is posited that factors such as resource benefits (e.g. energy content of prey), prey escape rates, and handling times can be minimised if specialisation for a particular prey type or habitat occurs4.

In Florida Bay, Torres & Readdocumented two distinct foraging strategies employed by two bottlenose dolphin ecotypes. One dolphin ecotype was found to forage using deep diving with erratic surfacings, whereas the second ecotype chose to forage through mud ring feeding and were mostly seen in shallow habitats. The latter ecotype is in fact so adapted to shallow depths that dolphins were typically observed foraging in waters <2 m deep. In this example, the foraging tactics of the two ecotypes are strongly driven by habitat conditions, specifically depth. The video below is aerial footage of bottlenose dolphins performing mud ring feeding.

Such group specialisations have been identified not only in several other bottlenose dolphin populations around the world6,7, but also in other cetacean species, including killer whales (distinct differences in target prey between transients and residents8), Guiana dolphins (mud-plume feeding9), humpback dolphins (strand feeding10), and several others. Noticeable here is that these records concern Odontocete species, which is not surprising since these toothed whales are vastly different to baleen whales in that they often live in structured groups with bonds between individuals sometimes lasting for decades11. Long-term relationships are conducive to developing specialised group hunting strategies as individuals will spend considerable time with one another and the success of obtaining prey depends on the cooperation and coordination of the group.

For baleen whales and other marine mammals, such as pinnipeds, where life history and social organisation is more geared toward a solitary life, examples of group specialisations are relatively rare (with the exception of the well-documented bubble-net feeding exhibited by humpback whales12). While group specialisation may not be as prevalent in Mysticetes, the same problems of inter and intra-specific competition persists among these more solitary species too, which would suggest that individuals should develop their own unique foraging tactics and preferences. Evidence for individualisation is hard to obtain since it requires repeated observations of the same individuals over time with good knowledge of the prey type being consumed and/or the habitat being used to forage in.

Nevertheless, examples do exist. Perhaps the most well-documented case of individualisation within a population for marine mammals is of the sea otter. Estes et al. (2003) describe 10 female sea otters in Monterey Bay that had high inter-individual variation in diet, which they investigated over a scale of 8 years13. Most females specialised on 1-4 types of prey, with marked differences between the diets chosen by each female, despite habitat overlap. This individualisation of diet was not attributable to variation in prey availability; hence, authors concluded that this extreme specialisation occurred to reduce intra-population competition for prey.

Ecologists have historically (and probably still to this day) disagreed on whether individualisation actually matters in the grand scheme of things. There are generally three schools of thought on the matter: (1) individual specialisation is rare and/or weakly influences population dynamics and so is not very important; (2) while individual specialisation does occur and may in fact be commonplace, it does not affect ecological processes at the large population scale; and (3) individual specialisation is widespread and can significantly impact population dynamics and/or ecosystem function.

As you might have guessed by this point, I find myself in the third school of thought. There are many arguments supporting this theory, and what I believe to be very good arguments against statements 1 and 2. While I have only provided one specific named example for individual specialisation in a marine mammal, there are several documented cases of such occurrences among other marine taxa (e.g., pinnipeds14, sharks15, fish16) and a much larger number of studies for terrestrial species4. Thus, the claim that it is rare or weak, seems implausible to me.

Statement 2 is a little more complicated to tackle as it involves understanding how actions on a relatively small scale affect a whole population or even an ecosystem. For instance, consider two female sea otters living in a small coastal area where one sea otter prefers to eat turban snails and the other exclusively feeds on abalone. The sudden decline in abundance of either of these prey could lead to serious health and reproductive issues for those females. Should the low prey abundance persist, then poor health and reproduction of several females in a population that specialise on that prey item can rapidly lead to genetic loss and an overall population decline. Particularly if an individual’s or species’ home range is rather restricted or small. In the case of the sea otter, which are often touted as a keystone species due to its presence preventing sea urchin barren formation that is known to wreak havoc on kelp forests, knock-on effects of such a population decline could result in poor overall ecosystem health.

It may be easy to assume that one individual dolphin, otter, seal or whale cannot possibly make a difference to a whole population or ecosystem. This assumption strikes me as a little odd since humans are always told to ‘be the change they wish to see in the world’ and that ‘every person can make a difference’. Why then should these sentiments not be applicable to non-humans? While a gray whale may not hold a sign at a protest or run for president (actions commonly considered to cause change in the human world), perhaps the choice that a gray whale makes every day to only consume one species of zooplankton, can influence other gray whales in the area, predators from other taxa, habitat structure, other prey availability, and/or cause trophic cascades.

Through my research, I aim to elucidate whether the gray whales display some level of foraging individualisation while feeding in Port Orford, Oregon. I will use data from four years to compare tracks of individual whales with zooplankton samples collected in the area to correlate each individual’s movement patterns with prey availability. I will assess the quality of prey through bomb calorimetry and microplastic analysis of the zooplankton samples to determine energetic content and pollutant levels, respectively. This prey assessment will describe the potential effects of prey specialization on whales, which is fundamental to assessing overall population health. Individualisation can strongly affect fitness of individuals, either positively or negatively depending on several factors, which will undoubtedly have an impact at the population level.

(The videos below are examples of two different tactics we see the gray whales display while foraging along the Oregon coast in the summer months. The first video shows a whale foraging among kelp with some very acrobatic moves, while the second is of a whale employing the ‘sharking’ method where the whale is feeding benthically in such shallow depths that both the pectoral fin and the fluke stick out of the water, making the whale look like a ‘shark’.)

References

  1. American Psychological Association, Personality. Retrieved from: https://www.apa.org/topics/personality/.
  2. Carere C., & Locurto, C., Interaction between animal personality and animal cognition. Current Zoology, 2015. 57(4): 491-498.
  3. Gosling, S.D., From mice to men: what can we learn about personality from animal research?Psychological Bulletin, 2001. 127(1): 45-86.
  4. Bolnick, D.I., et al., The ecology of individuals: incidence and implications of individual specialisation. The American Naturalist, 2003. 161(1): 1-28.
  5. Torres, L.G., & Read, A. J., Where to catch a fish? The influence of foraging tactics on the ecology of bottlenose dolphins (Tursiops truncatus) in Florida Bay, Florida. Marine Mammal Science, 2009. 25(4): 797-815.
  6. Gisburne, T.J., & Connor, R.C., Group size and feeding success in strand-feeding bottlenose dolphins (Tursiops truncatus) in Bull Creek, South Carolina. Marine Mammal Science, 2015. 31(3): 1252-1257.
  7. Gazda, S.K., et al., A division of labour with role specialization in group-hunting bottlenose dolphins (Tursiops truncatus) off Cedar Keys, Florida.Proceedings of the Royal Society: Biological Sciences, 2005. 272(1559): 135-140.
  8. Ford, J.K.B., et al., Dietary specialization in two sympatric populations of killer whales (Orcinus orca) in coastal British Columbia and adjacent waters. Canadian Journal of Zoology, 1998. 76(8): 1456-1471.
  9. Rossi-Santos, M.R., & Wedekin, L.L., Evidence of bottom contact behaviour by estuarine dolphins (Sotalia guianensis) on the Eastern Coast of Brazil.Aquatic Mammals, 2006. 32(2): 140-144.
  10. Peddemors, V.M., & Thompson, G., Beaching behaviour during shallow water feeding by humpback dolphins (Sousa plumbea). Aquatic Mammals, 1994. 20(2): 65-67.
  11. Tyack, P., Population biology, social behavior and communication in whales and dolphins. Trends in Ecology & Evolution, 1986. 1(6): 144-150.
  12. Wiley, D., et al., Underwater components of humpback whale bubble-net feeding behaviour.Behaviour, 2011. 148(5/6): 575-602.
  13. Estes, J.A., et al., Individual variation in prey selection by sea otters: patterns, causes and implications. Journal of Animal Ecology, 2003. 72(1): 144-155.
  14. Cherel, Y., et al., Stable isotopes document seasonal changes in trophic niches and winter foraging individual specialization in diving predators from the Southern Ocean. Journal of Animal Ecology, 2007. 76(4): 826-836.
  15. Matich, P., et al., Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. Journal of Animal Ecology, 2010. 80(1): 294-305.
  16. Svanbäck, R., & Persson, L., Individual diet specialization, niche width and population dynamics: implications for trophic polymorphisms. Journal of Animal Ecology, 2004. 73(5): 973-982.