skip to main content


Title: Behavioral responses across a mosaic of ecosystem states restructure a sea otter–urchin trophic cascade

Consumer and predator foraging behavior can impart profound trait-mediated constraints on community regulation that scale up to influence the structure and stability of ecosystems. Here, we demonstrate how the behavioral response of an apex predator to changes in prey behavior and condition can dramatically alter the role and relative contribution of top-down forcing, depending on the spatial organization of ecosystem states. In 2014, a rapid and dramatic decline in the abundance of a mesopredator (Pycnopodia helianthoides) and primary producer (Macrocystis pyrifera) coincided with a fundamental change in purple sea urchin (Strongylocentrotus purpuratus) foraging behavior and condition, resulting in a spatial mosaic of kelp forests interspersed with patches of sea urchin barrens. We show that this mosaic of adjacent alternative ecosystem states led to an increase in the number of sea otters (Enhydra lutris nereis) specializing on urchin prey, a population-level increase in urchin consumption, and an increase in sea otter survivorship. We further show that the spatial distribution of sea otter foraging efforts for urchin prey was not directly linked to high prey density but rather was predicted by the distribution of energetically profitable prey. Therefore, we infer that spatially explicit sea otter foraging enhances the resistance of remnant forests to overgrazing but does not directly contribute to the resilience (recovery) of forests. These results highlight the role of consumer and predator trait-mediated responses to resource mosaics that are common throughout natural ecosystems and enhance understanding of reciprocal feedbacks between top-down and bottom-up forcing on the regional stability of ecosystems.

 
more » « less
Award ID(s):
1538582
NSF-PAR ID:
10216672
Author(s) / Creator(s):
; ; ; ; ;
Publisher / Repository:
Proceedings of the National Academy of Sciences
Date Published:
Journal Name:
Proceedings of the National Academy of Sciences
Volume:
118
Issue:
11
ISSN:
0027-8424
Page Range / eLocation ID:
Article No. e2012493118
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. null (Ed.)
    Shifts between the alternate stable states of sea urchin barren grounds and kelp forests correspond to sea urchin density. In the Aleutian Archipelago, green sea urchins Strongylocentrotus polyacanthus are the dominant herbivores that graze kelp forests. Sea urchin recruitment is an important driver that influences sea urchin density, particularly in the absence of top-down control from a keystone predator such as the sea otter Enhydra lutris . To understand how the biological community may influence patterns of sea urchin recruitment, we compared sea urchin recruit (size ≤20 mm) densities with biomass of other benthic organisms in both barren ground and kelp forest habitats at 9 islands across the Aleutian Archipelago. Patterns of biological community structure between the 2 habitats did not explain patterns of sea urchin recruits; however, the same 10 specific taxa were found to correlate with sea urchin recruits in each habitat. Taxa that showed strong positive correlations included Codium, Constantinea, Schizymenia, and hydrozoans, while strong negative correlations were observed with Pachyarthron and Pugettia . Weak positive correlations were observed with Alcyonidium and ascidiaceans in both habitats, while weak variable relationships were detected with Polysiphonia and Corallina between habitats. The observed species-specific relationships may be due to small sea urchin displacement by larger conspecifics, larval responses to settlement cues, post-settlement survival via biogenic refugia, or potentially predation. These potential species-specific interactions were apparent, regardless of habitat, and it can be inferred that they would be preserved in the presence or absence of keystone predation. 
    more » « less
  2. Abstract

    Temporally consistent individual differences in behavior impact many ecological processes. We simultaneously examined the effects of individual variation in prey activity level, covering behavior, and body size on prey survival with predators using an urchin–lobster system. Specifically, we tested the hypothesis that slow‐moving purple sea urchins (Strongylocentrotus purpuratus) and urchins who deploy extensive substrate (pebbles and stones) covering behavior will out‐survive active urchins that deploy little to no covering behavior when pitted against a predator, the California spiny lobster (Panulirus interruptus). We evaluated this hypothesis by first confirming whether individual urchins exhibit temporally consistent differences in activity level and covering behavior, which they did. Next, we placed groups of four urchins in mesocosms with single lobster and monitored urchin survival for 108 hr. High activity level was negatively associated with survival, whereas urchin size and covering behavior independently did not influence survival. The negative effect of urchin activity level on urchin survival was strong for smaller urchins and weaker for large urchins. Taken together, these results suggest that purple urchin activity level and size jointly determine their susceptibility to predation by lobsters. This is potentially of great interest, because predation by recovering lobster populations could alter the stability of kelp forests by culling specific phenotypes, like foraging phenotypes, from urchin populations.

     
    more » « less
  3. Abstract

    How strongly predators and prey interact is both notoriously context dependent and difficult to measure. Yet across taxa, interaction strength is strongly related to predator size, prey size and prey density, suggesting that general cross‐taxonomic relationships could be used to predict how strongly individual species interact.

    Here, we ask how accurately do general size‐scaling relationships predict variation in interaction strength between specific species that vary in size and density across space and time?

    To address this question, we quantified the size and density dependence of the functional response of the California spiny lobsterPanulirus interruptus, foraging on a key ecosystem engineer, the purple sea urchinStrongylocentrotus purpuratus, in experimental mesocosms. Based on these results, we then estimated variation in lobster–urchin interaction strength across five sites and 9 years of observational data. Finally, we compared our experimental estimates to predictions based on general size‐scaling relationships from the literature.

    Our results reveal that predator and prey body size has the greatest effect on interaction strength when prey abundance is high. Due to consistently high urchin densities in the field, our simulations suggest that body size—relative to density—accounted for up to 87% of the spatio‐temporal variation in interaction strength. However, general size‐scaling relationships failed to predict the magnitude of interactions between lobster and urchin; even the best prediction from the literature was, on average, an order of magnitude (+18.7×) different than our experimental predictions.

    Harvest and climate change are driving reductions in the average body size of many marine species. Anticipating how reductions in body size will alter species interactions is critical to managing marine systems in an ecosystem context. Our results highlight the extent to which differences in size‐frequency distributions can drive dramatic variation in the strength of interactions across narrow spatial and temporal scales. Furthermore, our work suggests that species‐specific estimates for the scaling of interaction strength with body size, rather than general size‐scaling relationships, are necessary to quantitatively predict how reductions in body size will alter interaction strengths.

     
    more » « less
  4. Abstract

    The sea otter (Enhydra lutris) population of Southeast Alaska has been growing at a higher rate than other regions along the Pacific coast. While good for the recovery of this endangered species, rapid population growth of this apex predator can create a human‐wildlife conflict, negatively impacting commercial and subsistence fishing. Previous foraging studies throughout the sea otter range have shown they will reduce invertebrate prey biomass when recolonizing an area. The goal of this study was to examine and quantify the energy content of sea otter diets through direct foraging observations and prey collection. Our study area, Prince of Wales Island in southern Southeast Alaska, exhibits a gradient of sea otter recolonization, thus providing a natural experiment to test diet change in regions with different recolonization histories. Sea otter prey items were collected in three seasons (spring, summer, and winter) to measure caloric value and lipid and protein content. We observed 3523 sea otter dives during the spring and summer. A majority of the sea otter diet consisted of clams. Sea otters in newly recolonized areas had lower diet diversity, higher energetic intake rates (EIR, kcal/min), and prey had higher energy content (kcal/g). Females with pups had the highest diet diversity and the lowest EIR. Sea otter EIR were higher in the fall and winter vs. spring and summer. Sea cucumber energy and lipid content appeared to correspond with times when sea otters consumed the highest proportion of sea cucumbers. These caloric variations are an important component of understanding ecosystem‐level effects sea otters have in the nearshore environment.

     
    more » « less
  5. Abstract

    Sea otter (Enhydra lutris) populations in southwest Alaska declined substantially between about 1990 and the most recent set of surveys in 2015. Here we report changes in the distribution and abundance of sea otters, and covarying patterns in reproduction, mortality, body size and condition, diet and foraging behavior, food availability, health profiles, and exposure to environmental contaminants over this 25‐yr period. The population decline, which resulted in densities on the order of 5% of environmental carrying capacity, ranged from Attu Island in the west to about Castle Cape (on the south side of the Alaska Peninsula) in the east. Remaining sea otters moved closer to shore and into shallow, protected habitats. Reproductive rates appeared unchanged with the decline. Although the demographic cause of the decline was clearly elevated mortality, stranded carcasses were rare or absent. The net rate of energy gain by foraging sea otters, body length and condition, and prey biomass density, all increased after the decline and varied inversely with sea otter population density beyond the area of decline. Sea otters within the area of decline showed no increases in health anomalies, disease, contaminant exposure, or abnormal gene transcription patterns as compared to animals outside the area of decline. These collective findings are inconsistent with nutritional limitation, disease, or environmental contaminants, and consistent with predation (or possibly some other density‐independent factor) as the reason for the sea otter population decline. Our approach and analyses provide a broad conceptual template for thinking about and assessing the causes of wildlife population declines.

     
    more » « less