skip to main content


Title: Low‐pH seawater alters indirect interactions in rocky‐shore tidepools
Abstract

Ocean acidification is expected to degrade marine ecosystems, yet most studies focus on organismal‐level impacts rather than ecological perturbations. Field studies are especially sparse, particularly ones examining shifts in direct and indirect consumer interactions. Here we address such connections within tidepool communities of rocky shores, focusing on a three‐level food web involving the keystone sea star predator,Pisaster ochraceus, a common herbivorous snail,Tegula funebralis, and a macroalgal basal resource,Macrocystis pyrifera. We demonstrate that during nighttime low tides, experimentally manipulated declines in seawater pH suppress the anti‐predator behavior of snails, bolstering their grazing, and diminishing the top‐down influence of predators on basal resources. This attenuation of top‐down control is absent in pools maintained experimentally at higher pH. These findings suggest that as ocean acidification proceeds, shifts of behaviorally mediated links in food webs could change how cascading effects of predators manifest within marine communities.

 
more » « less
NSF-PAR ID:
10368802
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Ecology and Evolution
Volume:
12
Issue:
2
ISSN:
2045-7758
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Variability in primary producers' responses to environmental change may buffer higher trophic levels against shifts in basal resource composition. Then again, in instances where there is a lack of functional redundancy because consumers rely on a few species to meet their energetic requirements at specific times of the year, altered community production dynamics may significantly impact food web resilience. In high‐latitude kelp forests, a complementary annual phenology of seaweed production supports coastal marine consumers' metabolic needs across large seasonal variations in their environment. Yet, marine consumers in these systems may face significant metabolic stress under the pronounced low pH conditions expected in future winters, particularly if they lack the resources to support their increased energetic demands. In this study, we investigate how the growth and nutritional value of three dominant, coexisting macroalgal species found in subpolar kelp forests will respond to ocean acidification and warming in future winter and summer seasons. We find that the three kelpsMacrocystis pyrifera,Hedophyllum nigripes, andNeoagarum fimbriatumdiffer in their vulnerability to future environmental conditions, and that the seasonal environmental context of nutrient and light availability shapes these responses. Our results suggest that poleward fringe populations ofM. pyriferamay be relatively resilient to anticipated ocean warming and acidification. In contrast, ocean warming conditions caused a decrease in the biomass and nutritional quality of both understory kelps. Considering the unique production phenology ofH. nigripes, we emphasize that negative impacts on this species in future winters may be of consequence to consumer energetics in this system. This work highlights how interspecific variation in autotrophs' responses to global change can disrupt the diversity and phenological structure of energy supply available to higher trophic levels.

     
    more » « less
  2. Griffen, Blaine D. (Ed.)
    Ocean acidification (OA) represents a serious challenge to marine ecosystems. Laboratory studies addressing OA indicate broadly negative effects for marine organisms, particularly those relying on calcification processes. Growing evidence also suggests OA combined with other environmental stressors may be even more deleterious. Scaling these laboratory studies to ecological performance in the field, where environmental heterogeneity may mediate responses, is a critical next step toward understanding OA impacts on natural communities. We leveraged an upwelling-driven pH mosaic along the California Current System to deconstruct the relative influences of pH, ocean temperature, and food availability on seasonal growth, condition and shell thickness of the ecologically dominant intertidal mussel Mytilus californianus. In 2011 and 2012, ecological performance of adult mussels from local and commonly sourced populations was measured at 8 rocky intertidal sites between central Oregon and southern California. Sites coincided with a large-scale network of intertidal pH sensors, allowing comparisons among pH and other environmental stressors. Adult California mussel growth and size varied latitudinally among sites and inter-annually, and mean shell thickness index and shell weight growth were reduced with low pH. Surprisingly, shell length growth and the ratio of tissue to shell weight were enhanced, not diminished as expected, by low pH. In contrast, and as expected, shell weight growth and shell thickness were both diminished by low pH, consistent with the idea that OA exposure can compromise shell-dependent defenses against predators or wave forces. We also found that adult mussel shell weight growth and relative tissue mass were negatively associated with increased pH variability. Including local pH conditions with previously documented influences of ocean temperature, food availability, aerial exposure, and origin site enhanced the explanatory power of models describing observed performance differences. Responses of local mussel populations differed from those of a common source population suggesting mussel performance partially depended on genetic or persistent phenotypic differences. In light of prior research showing deleterious effects of low pH on larval mussels, our results suggest a life history transition leading to greater resilience in at least some performance metrics to ocean acidification by adult California mussels. Our data also demonstrate “hot” (more extreme) and “cold” (less extreme) spots in both mussel responses and environmental conditions, a pattern that may enable mitigation approaches in response to future changes in climate. 
    more » « less
  3. Abstract

    We investigate where bottom‐up and top‐down control regulates ecological communities as a mechanism linking ecological gradients to the geography of consumer abundance and biomass. We use standardized surveys of 54 North American grasslands to test alternate hypotheses predicting 100‐fold shifts in the biomass of four common grassland arthropod taxa—Auchenorrhyncha, sucking herbivores, Acrididae, chewing herbivores, Tettigoniidae, omnivores, and Araneae, predators.

    Bottom‐up models predict that consumer biomass tracks plant quantity (e.g. productivity and standing biomass) and quality (nutrient content) and that ectotherm access to food increases with temperature. Each of the focal trophic groups responded differently to these drivers: the biomass of sucking herbivores and omnivores increased with plant biomass; that of chewing herbivores tracked plant quality; and predator biomass did not depend on plant quality, plant quantity or temperature.

    The Exploitation Ecosystem Hypothesis is a top‐down hypothesis that predicts a shift from resource limitation of herbivores when plant production is low, to predator limitation when plant production is high. In grasslands where spider biomass was low, herbivore biomass increased with plant biomass, whereas bottom‐up structuring was not evident when spiders were abundant. Furthermore, neither predator biomass nor trophic position (via stable isotope analysis) increased with plant biomass, suggesting predators themselves are top‐down limited.

    Stable isotope analysis revealed that trophic position of the chewing herbivore and omnivore increased significantly with plant biomass, suggesting these groups increased scavenging and meat consumption in grasslands with higher carbohydrate availability.

    Taken together, our snapshot sampling documents gradients of food web structure across 54 grasslands, consistent with multiple hypotheses of bottom‐up and top‐down regulation.

     
    more » « less
  4. Abstract

    Climate change is increasing the frequency, severity, and extent of wildfires and drought in many parts of the world, with numerous repercussions for the physical, chemical, and biological characteristics of streams. However, information on how these perturbations affect top predators and their impacts on lower trophic levels in streams is limited.

    The top aquatic predator in southern California streams is nativeOncorhynchus mykiss, the endangered southern California steelhead trout (trout). To examine relationships among the distribution of trout, environmental factors, and stream invertebrate resources and assemblages, we sampled pools in 25 stream reaches that differed in the presence (nine reaches) or absence (16 reaches) of trout over 12 years, including eight reaches where trout were extirpated during the study period by drought or post‐fire flood disturbances.

    Trout were present in deep pools with high water and habitat quality. Invertebrate communities in trout pools were dominated by a variety of medium‐sized collector–gatherer and shredder invertebrate taxa with non‐seasonal life cycles, whereas tadpoles and large, predatory invertebrates (Odonata, Coleoptera, Hemiptera [OCH]), often with atmospheric breather traits, were more abundant in troutless than trout pools.

    Structural equation modelling of the algal‐based food web indicated a trophic cascade from trout to predatory invertebrates to collector–gatherer taxa and weaker direct negative trout effects on grazers; however, both grazers and collector–gatherers also were positively related to macroalgal biomass. Structural equation modelling also suggested that bottom‐up interactions and abiotic factors drove the detritus‐based food web, with shredder abundance being positively related to leaf litter (coarse particulate organic matter) levels, which, in turn, were positively related to canopy cover and negatively related to flow. These results emphasise the context dependency of trout effects on prey communities and of the relative importance of top‐down versus bottom‐up interactions on food webs, contingent on environmental conditions (flow, light, nutrients, disturbances) and the abundances and traits of component taxa.

    Invertebrate assemblage structure changed from a trout to a troutless configuration within a year or two after trout were lost owing to post‐fire scouring flows or drought. Increases in OCH abundance after trout were lost were much more variable after drought than after fire. The reappearance of trout in one stream resulted in quick, severe reductions in OCH abundance.

    These results indicate that climate‐change induced disturbances can result in the extirpation of a top predator, with cascading repercussions for stream communities and food webs. This study also emphasises the importance of preserving or restoring refuge habitats, such as deep, shaded, perennial, cool stream pools with high habitat and water quality, to prevent the extirpation of sensitive species and preserve native biodiversity during a time of climate change.

     
    more » « less
  5. Abstract

    Tropical floodplains secure the protein supply of millions of people, but only sound management can ensure the long‐term continuity of such ecosystem services. Overfishing is a widespread threat to multitrophic systems, but how it affects ecosystem functioning is poorly understood, particularly in tropical freshwater food webs. Models based on temperate lakes frequently assume that primary producers are mostly bottom‐up controlled by nutrient and light limitations, with negligible effects of top‐down forces. Yet this assumption remains untested in complex tropical freshwater systems experiencing marked spatiotemporal variation.

    We use consolidated community‐based fisheries management practices and spatial zoning to test the relative importance of bottom‐up versus top‐down drivers of phytoplankton biomass, controlling for the influence of local to landscape heterogeneity. Our study focuses on 58 large Amazonian floodplain lakes under different management regimes that resulted in a gradient of apex‐predator abundance. These lakes, distributed along ~600 km of a major tributary of the Amazon River, varied widely in size, structure, landscape context, and hydrological seasonality.

    Using generalised linear models, we show that community‐based fisheries management, which controls the density of apex predators, is the strongest predictor of phytoplankton biomass during the dry season, when lakes become discrete landscape units. Water transparency also emerges as an important bottom‐up factor, but phosphorus, nitrogen and several lake and landscape metrics had minor or no effects on phytoplankton biomass. During the wet‐season food pulse, when lakes become connected to adjacent water bodies and homogenise the landscape, only lake depth explained phytoplankton biomass.

    Synthesis and applications. Tropical freshwaters fisheries typically assume that fish biomass is controlled by bottom‐up mechanisms, so that overexploitation of large predators would not affect overall ecosystem productivity. Our results, however, show that top‐down forces are important drivers of primary productivity in tropical lakes, above and beyond the effects of bottom‐up factors. This helps us to understand the enormous success of community‐based ‘fishing agreements’ in the Amazon. Multiple stakeholders should embrace socio‐ecological management practices that shape both bottom‐up and top‐down forces to ensure biodiversity protection, sustainable fisheries yields and food security for local communities and regional economies.

     
    more » « less