Tag: sea urchins

Kelp to whales: New GEMM Lab publication explores indirect effects of a classic trophic cascade on gray whales

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

As many of our avid readers already know, the Pacific Coast Feeding Group (PCFG) of gray whales employs a wide range of foraging tactics to feed on a number of different prey items in various benthic substrate types (Torres et al. 2018). One example foraging tactic is when PCFG whales, particularly when they are in the Oregon portion of their feeding range, forage on mysid shrimp in and near kelp beds on rocky reefs. We have countless drone video clips of whales weaving their large bodies through kelp and many photographs of whales coming to the surface to breath completely covered in kelp, looking more like a sea monster than a whale (Figure 1). So, when former intern Dylan Gregory made an astute observation during the 2018 TOPAZ/JASPER field season in Port Orford about a GoPro video the field team collected that showed many urchins voraciously feeding on an unhealthy-looking kelp stalk (Figure 2a), it made us wonder if and how changes to kelp forests may impact gray whales. 

Fig 1. Gray whale surfacing in a large kelp patch. Photograph captured under NOAA/NMFS research permit #16111. Source: GEMM Lab.

Kelp forests are widely used as a marine example of trophic cascades. Trophic cascades are trigged by the addition/removal of a top predator to/from a system, which causes changes further down the trophic chain. Sea urchins are common inhabitants of kelp forests and in a balanced, healthy system, urchin populations are regulated by predators as they behave cryptically by hiding in crevices in the reef and individual urchins feed passively on drift kelp that breaks off from larger plants. When we think about who controls urchins in kelp forests, we probably think of sea otters first. However, sea otters have been absent from Oregon waters for over a century (Kone et al. 2021), so who controls urchins here? The answer is the sunflower sea star (Figure 2b). Sunflower sea stars are large predators with a maximum arm span of up to 1 m! Unfortunately, a disease epidemic that started in 2013 known as sea star wasting disease caused 80-100% population decline of sunflower sea stars along the coastline between Mexico and Alaska (Harvell et al. 2019). Shortly thereafter, a record-breaking marine heatwave caused warm, nutrient-poor water conditions to persist in the northeast Pacific Ocean from 2014 to 2016 (Jacox et al. 2018). These co-occurring stressors caused unprecedented and long-lasting decline of a previously robust kelp forest in northern California (Rogers-Bennett & Catton 2019), where sea otters are also absent. Given the biogeographical similarity between southern Oregon and northern California and the observation made by Dylan in 2018, we decided to undertake an analysis of the eight years of data collected during the TOPAZ/JASPER project in Port Orford starting in 2016, to investigate the trends of four trophic levels (purple sea urchins, bull kelp, zooplankton, and gray whales) across space and time. The results of our study were published last week in Scientific Reports and I am excited to be able to share them with you today.

Fig 2a. Sea urchins actively feeding on kelp stalks. Source: GEMM Lab.
Fig 2b. Diver holding a sunflower sea star near Port Orford, OR. Source: Scott Groth.

Every day during the TOPAZ/JASPER field season, two teams head out to collect data. One team is responsible for tracking gray whales from shore using a theodolite, while the other team heads out to sea on a tandem research kayak to collect prey data (Figure 3). The kayak team samples prey in multiple ways, including dropping a GoPro camera at each sampling station. When the project was first developed, the original goal of these GoPro videos was to measure the relative abundance of prey. Since the sampling stations occur on or near reefs that are shallow with dense surface kelp, traditional methods to assess prey density, such as using a boat with an echosounder, are not suitable options. Instead, GEMM Lab PI Leigh Torres, together with the first Master’s student on this project Florence Sullivan, developed a method to score still images extracted from the GoPro videos to estimate relative zooplankton abundance. However, after we saw those images of urchins feeding on kelp in 2018, we decided to develop another protocol that allowed us to use these GoPro videos to also characterize sea urchin coverage and kelp condition. Once we had occurrence values for all four species, we were able to dig into the spatiotemporal trends.

Figure 3. Map of Port Orford, USA study area showing the 10 kayak sampling stations (white circles) within the two study sites (Tichenor Cove and Mill Rocks). The white triangle represents the cliff top location where theodolite tracking of whales was conducted. Figure and caption taken from Hildebrand et al. 2024.

When we examined the trends for each of the four study species across years, we found that purple sea urchin coverage in both of our study sites within Port Orford increased dramatically within our study period (Figure 4). In 2016, the majority of our sampled stations contained no visible urchins. However, by 2020, we detected urchins at every sampling station. For kelp, we saw the reverse trend; in 2016 all sampling stations contained kelp that was healthy or mostly healthy. But by 2019, there were many stations that contained kelp in poor health or where kelp was absent entirely. Zooplankton and gray whales experienced similar temporal trends as the kelp, with their occurrence metrics (abundance and foraging time, respectively) having higher values at the start of our study period and declining steadily during the eight years. While the rise in urchin coverage across our study area occurred concurrently with the decrease in kelp condition, zooplankton abundance, and gray whale foraging, we wanted to explicitly test how these species are related to one another based on prior ecological knowledge.

Figure 4. Temporal trends of purple sea urchin coverage, bull kelp condition, relative zooplankton abundance, and gray whale foraging time by year across the eight-year study period (2016–2023), from the generalized additive models. The colored ribbons represent approximate 95% confidence intervals. Line types represent the two study sites, Mill Rocks (MR; solid) and Tichenor Cove (TC; dashed). All curves are statistically significant (P < 0.05). Figure and caption taken from Hildebrand et al. 2024.

To test whether urchin coverage had an effect on kelp condition, we hypothesized that increased urchin coverage would be correlated with reduced kelp condition based on the decades of research that has established a negative relationship between the two when a trophic cascade occurs in kelp forest systems. Next, we wanted to test whether kelp condition had an effect on zooplankton abundance and hypothesized that increased kelp condition would be correlated with increased zooplankton abundance. We based this hypothesis on several pieces of prior knowledge, particularly as they pertain to mysid shrimp: (1) high productivity within kelp beds provides food for mysids, including kelp zoospores (VanMeter & Edwards 2013), (2) current velocities are one third slower inside kelp beds compared to outside (Jackson & Winant 1983), which might support the retention of mysids within kelp beds since they are not strong swimmers, and (3) the kelp canopy may serve as potential protection for mysids from predators (Coyer 1984). Finally, we wanted to test whether both kelp condition and zooplankton abundance have an effect on gray whales and we hypothesized that increased values for both would be correlated with increased gray whale foraging time. While the reasoning behind our hypothesized correlation between zooplankton prey and gray whales is obvious (whales eat zooplankton), the reasoning behind the kelp-whale connection may not be. We speculated that since kelp habitat may aggregate or retain zooplankton prey, gray whales may use kelp as an environmental cue to find prey patches. 

When we tested our hypotheses through generalized additive models, we found that increased urchin coverage was significantly correlated with decreased kelp condition in both study sites, providing evidence that a shift from a kelp forest to an urchin barren may have occurred in the Port Orford area. Additionally, increased kelp condition was correlated with increased zooplankton abundance, supporting our hypothesis that kelp forests are an important habitat and resource for nearshore zooplankton prey. Interestingly, this relationship was bell-shaped in one of our two study sites, suggesting that there are other factors besides healthy bull kelp that influence zooplankton abundance, which likely include upwelling dynamics, habitat structure, and local oceanographic characteristics. For the whale model, we found that increased kelp condition was significantly correlated with increased gray whale foraging time, which may corroborate our hypothesis that gray whales use kelp as an environmental cue to locate prey. Zooplankton abundance was significantly correlated with gray whale foraging time in one of our two sites. Once again, this relationship was bell-shaped, which suggests other factors influence gray whale foraging time, including prey quality (Hildebrand et al. 2022) and density.

Figure 5. Effects derived from trophic path generalized additive models of purple sea urchin coverage on kelp condition (A), kelp condition on relative zooplankton abundance (B), and kelp condition and relative zooplankton abundance on gray whale foraging time (C). The colored ribbons represent approximate 95% confidence intervals. Line types represent the two study sites, Mill Rocks (MR; solid) and Tichenor Cove (TC; dashed). Curves with asterisks indicate statistically significant (P < 0.05) relationships. Figure and caption taken from Hildebrand et al. 2024.

Our results highlight the potential larger impacts of reduced gray whale foraging time as a result of these trophic dynamics may cause at the individual and population level. If an area that was once a reliable source of food (like Port Orford) is no longer favorable, then whales likely search for other areas in which to feed. However, if the areas affected by these dynamics are widespread, then individuals may spend more time searching for, and less time consuming, prey, which could have energetic consequences. While our study took place in a relatively small spatial area, the trophic dynamics we documented in our system may be representative of patterns across the PCFG range, given ecological and topographic similarities in habitat use patterns. In fact, in the years with the lowest kelp, zooplankton, and whale occurrence (2020 and 2021) in Port Orford, the GRANITE field team also noted low whale numbers and minimal surface kelp extent in the central Oregon field site off of Newport. However, ecosystems are resilient. We are hopeful that the dynamics we documented in Port Orford are just short-term changes and that the system will return to its former balanced state with less urchins, more healthy bull kelp, zooplankton, and lots of feeding gray whales.

If you are interested in getting a more detailed picture of our methods and analysis, you can read our open access paper here: https://www.nature.com/articles/s41598-024-59964-x

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References

Coyer, J. A. (1984). The invertebrate assemblage associated with the giant kelp, Macrocystis pyrifera, at Santa Catalina Island, California: a general description with emphasis on amphipods, copepods, mysids, and shrimps. Fishery Bulletin, 82(1), 55-66.

Harvell, C. D., Montecino-Latorre, D., Caldwell, J. M., Burt, J. M., Bosley, K., Keller, A., … & Gaydos, J. K. (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), eaau7042.

Hildebrand, L., Sullivan, F. A., Orben, R. A., Derville, S., & Torres, L. G. (2022). Trade-offs in prey quantity and quality in gray whale foraging. Marine Ecology Progress Series, 695, 189-201.

Jackson, G. A., & Winant, C. D. (1983). Effect of a kelp forest on coastal currents. Continental Shelf Research, 2(1), 75-80.

Jacox, M. G., Alexander, M. A., Mantua, N. J., Scott, J. D., Hervieux, G., Webb, R. S., & Werner, F. E. (2018). Forcing of multi-year extreme ocean temperatures that impacted California Current living marine resources in 2016. Bull. Amer. Meteor. Soc, 99(1).

Kone, D. V., Tinker, M. T., & Torres, L. G. (2021). Informing sea otter reintroduction through habitat and human interaction assessment. Endangered Species Research, 44, 159-176.

Rogers-Bennett, L., & Catton, C. A. (2019). Marine heat wave and multiple stressors tip bull kelp forest to sea urchin barrens. Scientific reports, 9(1), 15050.

Torres, L. G., Nieukirk, S. L., Lemos, L., & Chandler, T. E. (2018). Drone up! Quantifying whale behavior from a new perspective improves observational capacity. Frontiers in Marine Science, 5, 319.

VanMeter, K., & Edwards, M. S. (2013). The effects of mysid grazing on kelp zoospore survival and settlement. Journal of Phycology, 49(5), 896-901.

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.

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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.