skip to main content


Title: Climate and fishing drive regime shifts in consumer‐mediated nutrient cycling in kelp forests
Abstract

Globally, anthropogenic pressures are reducing the abundances of marine species and altering ecosystems through modification of trophic interactions. Yet, consumer declines also disrupt important bottom‐up processes, like nutrient recycling, which are critical for ecosystem functioning. Consumer‐mediated nutrient dynamics (CND) is now considered a major biogeochemical component of most ecosystems, but lacking long‐term studies, it is difficult to predict how CND will respond to accelerating disturbances in the wake of global change. To aid such predictions, we coupled empirical ammonium excretion rates with an 18‐year time series of the standing biomass of common benthic macroinvertebrates in southern California kelp forests. This time series of excretion rates encompassed an extended period of extreme ocean warming, disease outbreaks, and the abolishment of fishing at two of our study sites, allowing us to assess kelp forest CND across a wide range of environmental conditions. At their peak, reef invertebrates supplied an average of 18.3 ± 3.0 µmol NH4+ m−2 hr−1to kelp forests when sea stars were regionally abundant, but dropped to 3.5 ± 1.0 µmol NH4+ m−2 hr−1following their mass mortality due to disease during a prolonged period of extreme warming. However, a coincident increase in the abundance of the California spiny lobster,Palinurus interupptus(Randall, 1840), likely in response to both reduced fishing and a warmer ocean, compensated for much of the recycled ammonium lost to sea star mortality. Both lobsters and sea stars are widely recognized as key predators that can profoundly influence community structure in benthic marine systems. Our study is the first to demonstrate their importance in nutrient cycling, thus expanding their roles in the ecosystem. Climate change is increasing the frequency and severity of warming events, and rising human populations are intensifying fishing pressure in coastal ecosystems worldwide. Our study documents how these projected global changes can drive regime shifts in CND and fundamentally alter a critical ecosystem function.

 
more » « less
Award ID(s):
1831937 1232779
NSF-PAR ID:
10450056
Author(s) / Creator(s):
 ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Global Change Biology
Volume:
25
Issue:
9
ISSN:
1354-1013
Page Range / eLocation ID:
p. 3179-3192
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Kelp beds provide significant ecosystem services and socioeconomic benefits globally, and prominently in coastal zones of the California Current. Their distributions and abundance, however, vary greatly over space and time. Here, we describe long-term patterns of Giant Kelp (Macrocystis pyrifera) sea surface canopy area off the coast of San Diego County from 1983 through 2019 along with recent patterns of water column nitrate (NO3-) exposure inferred fromin situtemperature data in 2014 and 2015 at sites spanning 30 km of the coastline near San Diego California, USA. Site-specific patterns of kelp persistence and resilience were associated with ocean and climate dynamics, with total sea surface kelp canopy area varying approximately 33-fold over the almost 4 decades (min 0.34 km2in 1984; max 11.25 km2in 2008, median 4.79 km2). Site-normalized canopy areas showed that recent kelp persistence since 2014 was greater at Point Loma and La Jolla, the largest kelp beds off California, than at the much smaller kelp bed off Cardiff. NO3-exposure was estimated from an 11-month time series ofin situwater column temperature collected in 2014 and 2015 at 4 kelp beds, using a relationship between temperature and NO3-concentration previously established for the region. The vertical position of the 14.5°C isotherm, an indicator of the main thermocline and nutricline, varied across the entire water column at semidiurnal to seasonal frequencies. We use a novel means of quantifying estimated water column NO3-exposure integrated through time (mol-days m-2) adapted from degree days approaches commonly used to characterize thermal exposures. Water column integrated NO3-exposure binned by quarters of the time series showed strong seasonal differences with highest exposure in Mar - May 2015, lowest exposure in Sep - Dec 2014, with consistently highest exposure off Point Loma. The water column integrated NO3-signal was filtered to provide estimates of the contribution to total nitrate exposure from high frequency variability (ƒ >= 1 cycle 30 hr-1) associated predominantly with internal waves, and low frequency variability driven predominantly by seasonal upwelling. While seasonal upwelling accounted for > 90% of NO3-exposure across the full year, during warm periods when seasonal upwelling was reduced or absent and NO3-exposure was low overall, the proportion due to internal waves increased markedly to 84 to 100% of the site-specific total exposure. The high frequency variability associated with internal waves may supply critical nutrient availability during anomalously warm periods. Overall, these analyses support a hypothesis that differences in NO3-exposure among sites due to seasonal upwelling and higher frequency internal wave forcing contribute to spatial patterns in Giant Kelp persistence in southern California. The study period includes anomalously warm surface conditions and the marine heatwave associated with the “Pacific Warm Blob” superimposed on the seasonal thermal signal and corresponding to the onset of a multi-year decline in kelp canopy area and marked differences in kelp persistence among sites. Our analysis suggests that, particularly during periods of warm surface conditions, variation in NO3-exposure associated with processes occurring at higher frequencies, including internal waves can be a significant source of NO3-exposure to kelp beds in this region. The patterns described here also offer a view of the potential roles of seasonal and higher frequency nutrient dynamics for Giant Kelp persistence in southern California under continuing ocean surface warming and increasing frequency and intensity of marine heatwaves.

     
    more » « less
  2. ABSTRACT

    Sandy beaches are iconic interfaces that functionally link the ocean with the landviathe flow of organic matter from the sea. These cross‐ecosystem fluxes often comprise uprooted seagrass and dislodged macroalgae that can form substantial accumulations of detritus, termed ‘wrack’, on sandy beaches. In addition, the tissue of the carcasses of marine animals that regularly wash up on beaches form a rich food source (‘carrion’) for a diversity of scavenging animals. Here, we provide a global review of how wrack and carrion provide spatial subsidies that shape the structure and functioning of sandy‐beach ecosystems (sandy beaches and adjacent surf zones), which typically have littlein situprimary production. We also examine the spatial scaling of the influence of these processes across the broader land‐ and seascape, and identify key gaps in our knowledge to guide future research directions and priorities. Large quantities of detrital kelp and seagrass can flow into sandy‐beach ecosystems, where microbial decomposers and animals process it. The rates of wrack supply and its retention are influenced by the oceanographic processes that transport it, the geomorphology and landscape context of the recipient beaches, and the condition, life history and morphological characteristics of the macrophyte taxa that are the ultimate source of wrack. When retained in beach ecosystems, wrack often creates hotspots of microbial metabolism, secondary productivity, biodiversity, and nutrient remineralization. Nutrients are produced during wrack breakdown, and these can return to coastal waters in surface flows (swash) and aquifers discharging into the subtidal surf. Beach‐cast kelp often plays a key trophic role, being an abundant and preferred food source for mobile, semi‐aquatic invertebrates that channel imported algal matter to predatory invertebrates, fish, and birds. The role of beach‐cast marine carrion is likely to be underestimated, as it can be consumed rapidly by highly mobile scavengers (e.g. foxes, coyotes, raptors, vultures). These consumers become important vectors in transferring marine productivity inland, thereby linking marine and terrestrial ecosystems. Whilst deposits of organic matter on sandy‐beach ecosystems underpin a range of ecosystem functions and services, they can be at variance with aesthetic perceptions resulting in widespread activities, such as ‘beach cleaning and grooming’. This practice diminishes the energetic base of food webs, intertidal fauna, and biodiversity. Global declines in seagrass beds and kelp forests (linked to global warming) are predicted to cause substantial reductions in the amounts of marine organic matter reaching many beach ecosystems, likely causing flow‐on effects for food webs and biodiversity. Similarly, future sea‐level rise and increased storm frequency are likely to alter profoundly the physical attributes of beaches, which in turn can change the rates at which beaches retain and process the influxes of wrack and animal carcasses. Conservation of the multi‐faceted ecosystem services that sandy beaches provide will increasingly need to encompass a greater societal appreciation and the safeguarding of ecological functions reliant on beach‐cast organic matter on innumerable ocean shores worldwide.

     
    more » « less
  3. null (Ed.)
    Marine ecosystems are vulnerable to climate driven events such as marine heatwaves yet we have a poor understanding of whether they will collapse or recover. Kelp forests are known to be susceptible, and there has been a rise in sea urchin barrens around the world. When temperatures increase so do physiological demands while food resources decline, tightening metabolic constraints. In this case study, we examine red abalone ( Haliotis rufescens ) looking at sublethal impacts and their prospects for recovery within kelp forests that have shifted to sea urchin barrens. Abalone are a recreationally fished species that once thrived in northern California’s bull kelp forests but have recently suffered mass mortalities since the 2014–2016 marine heatwave. Quantitative data exist on the health and reproduction of abalone both prior to and after the collapse. The survivors of the mass mortality show a 2-year lag in body and gonad condition indices. After the lag, body and gonad indexes decreased substantially, as did the relationship between shell length and body weight. Production of mature eggs per female declined by 99% ( p < 0.001), and the number of eggs per gram of female body weight (2,984/g) declined to near zero (9/g). The number of males with sperm was reduced by 33%, and the sperm abundance score was reduced by 28% ( p = 0.414). We observed that these reductions were for mature eggs and sperm while immature eggs and spermatids were still present in large numbers. In the lab, after reintroduction of kelp, weight gains were quickly lost following a second starvation period. This example illustrates how climate-driven declines in foundation species can suppress recovery of the system by impacting body condition and future reproduction of surviving individuals. Given the poor reproductive potential of the remaining abalone in northern California, coupled with ongoing mortality and low kelp abundances, we discuss the need to maintain the fishing moratorium and implement active abalone restoration measures. For fished species, such as abalone, this additional hurdle to recovery imposed by changes in climate is critical to understand and incorporate into resource management and restoration. 
    more » « less
  4. Abstract

    Ocean warming has both direct physiological and indirect ecological consequences for marine organisms. Sessile animals may be particularly vulnerable to anomalous warming given constraints in food acquisition and reproduction imposed by sessility. In temperate reef ecosystems, sessile suspension feeding invertebrates provide food for an array of mobile species and act as a critical trophic link between the plankton and the benthos. Using 14 years of seasonal benthic community data across five coastal reefs, we evaluated how communities of sessile invertebrates in southern California kelp forests responded to the “Blob”, a period of anomalously high temperatures and low phytoplankton production. We show that this event had prolonged consequences for kelp forest ecosystems. Changes to community structure, including species invasions, have persisted six years post-Blob, suggesting that a climate-driven shift in California kelp forests is underway.

     
    more » « less
  5. null (Ed.)
    Abstract Climate change is responsible for increased frequency, intensity, and duration of extreme events, such as marine heatwaves (MHWs). Within eastern boundary current systems, MHWs have profound impacts on temperature-nutrient dynamics that drive primary productivity. Bull kelp ( Nereocystis luetkeana ) forests, a vital nearshore habitat, experienced unprecedented losses along 350 km of coastline in northern California beginning in 2014 and continuing through 2019. These losses have had devastating consequences to northern California communities, economies, and fisheries. Using a suite of in situ and satellite-derived data, we demonstrate that the abrupt ecosystem shift initiated by a multi-year MHW was preceded by declines in keystone predator population densities. We show strong evidence that northern California kelp forests, while temporally dynamic, were historically resilient to fluctuating environmental conditions, even in the absence of key top predators, but that a series of coupled environmental and biological shifts between 2014 and 2016 resulted in the formation of a persistent, altered ecosystem state with low primary productivity. Based on our findings, we recommend the implementation of ecosystem-based and adaptive management strategies, such as (1) monitoring the status of key ecosystem attributes: kelp distribution and abundance, and densities of sea urchins and their predators, (2) developing management responses to threshold levels of these attributes, and (3) creating quantitative restoration suitability indices for informing kelp restoration efforts. 
    more » « less