Marine deforestation leads to widespread loss of ecosystem function

PLOS ONE RESEARCH ARTICLE Marine deforestation leads to widespread loss of ecosystem function Matthew Edwards ID1*, Brenda Konar2, Ju-Hyoung Kim ID3, Scott Gabara1,4, Genoa Sullaway1, Tristin McHugh1, Michael Spector ID1, Sadie Small ID1 1 Department of Biology, San Diego State University, San Diego, CA, United States of America, 2 College of Fisheries and Ocean Sciences, University of Alaska Fairbanks, Fairbanks, Alaska, United States of America, 3 Marine Applied Biosciences, Kunsan National University, Gunsan, South Korea, 4 Department of Environmental Science and Policy, University of California, Davis, California, United States of America a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Edwards M, Konar B, Kim J-H, Gabara S, Sullaway G, McHugh T, et al. (2020) Marine deforestation leads to widespread loss of ecosystem function. PLoS ONE 15(3): e0226173. https://doi.org/10.1371/journal.pone.0226173 Editor: Maura (Gee) Geraldine Chapman, University of Sydney, AUSTRALIA Received: November 20, 2019 Accepted: February 13, 2020 Published: March 4, 2020 Peer Review History: PLOS recognizes the benefits of transparency in the peer review process; therefore, we enable the publication of all of the content of peer review and author responses alongside final, published articles. The editorial history of this article is available here: https://doi.org/10.1371/journal.pone.0226173 Copyright: © 2020 Edwards et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: Data are available on our NSF bco-dmo data page at https://www.bcodmo.org/dataset/755658 Funding: This research was funded by grants from the National Science Foundation (OCE1435194) to * Abstract Trophic interactions can result in changes to the abundance and distribution of habitat-forming species that dramatically reduce ecosystem functioning. In the coastal zone of the Aleutian Archipelago, overgrazing by herbivorous sea urchins that began in the 1990s resulted in widespread deforestation of the region’s kelp forests, which led to lower macroalgal abundances and higher benthic irradiances. We examined how this deforestation impacted ecosystem function by comparing patterns of net ecosystem production (NEP), gross primary production (GPP), ecosystem respiration (Re), and the range between GPP and Re in remnant kelp forests, urchin barrens, and habitats that were in transition between the two habitat types at nine islands that spanned more than 1000 kilometers of the archipelago. Our results show that deforestation, on average, resulted in a 24% reduction in GPP, a 26% reduction in Re, and a 24% reduction in the range between GPP and Re. Further, the transition habitats were intermediate to the kelp forests and urchin barrens for these metrics. These opposing metabolic processes remained in balance; however, which resulted in little-to-no changes to NEP. These effects of deforestation on ecosystem productivity, however, were highly variable between years and among the study islands. In light of the worldwide declines in kelp forests observed in recent decades, our findings suggest that marine deforestation profoundly affects how coastal ecosystems function. Introduction Consumers fundamentally affect ecosystems through trophic interactions [1]. These interactions are especially important if they result in changes to the abundance or distribution of ecosystem engineers, such as forest-forming trees, which can lead to changes in microclimates, biodiversity, primary production, nutrient cycling, and energy flow [2]. For example, the reintroduction of gray wolves (Canis lupus) into Yellowstone National Park, USA in the 1990s resulted in increased predation on elk (Cervus elaphus) and subsequently reduced herbivory on canopy-forming trees such as aspens (Populus tremuloides), willows (Salix spp.), and cottonwoods (Populus spp.) [3]. This ultimately led to changes in the morphology and hydrology PLOS ONE | https://doi.org/10.1371/journal.pone.0226173 March 4, 2020 1 / 21 PLOS ONE ME and (OCE1435205) to BK, and the National Research Foundation (NRF-2018R1C1B6008523 and NRF-2015R1C1A1A01054831) to JHK. Competing interests: NO - Authors have no competing interests. Deforestation and loss of ecosystem function of the region’s river systems and its riparian plant communities [4,5]. Similarly, large marine algae, such as kelps, can form subtidal forests whose biogenic structures alter hydrodynamic, nutrient and light conditions, modify patterns of biodiversity, enhance primary production and carbon sequestration, and provide food and habitat for numerous other species [6–9]. Consequently, the loss of these forest-forming kelps and the benthic communities they support can have dramatic impacts to how nearshore ecosystems function, especially if they occur over large geographic areas. Indeed, kelp deforestation has occurred in numerous areas worldwide in recent decades due to a variety of forcing factors [10,11], and the subtidal rocky reefs of the Aleutian Archipelago serve as a model system to investigate the broader impacts of such deforestation. These forests have historically been dominated by dense populations of the surface canopy-forming kelp Eualaria fistulosa, several species of understory kelps such as Laminaria spp. and Agarum spp., the brown alga Desmarestia spp., and numerous species of fleshy read algae. However, the collapse of sea otter (Enhydra lutris) populations led to large increases in their primary prey, herbivorous sea urchins (Strongylocentrotus polyacanthus), which subsequently resulted in overgrazing and widespread losses of the region’s kelp forests [12]. This collapse began in the late 1990s, likely in response to a dietary shift by killer whales toward sea otters, and by 2000 sea otter densities had declined throughout the archipelago to around 5–10% of their estimated equilibrium density [13]. Currently, sea otters are largely absent from or are in very low abundances on many of the islands and most of the kelp forests have either disappeared from the archipelago or are in the process of disappearing, although some small forests remain in their ‘historical state’ at scattered locations on most of the islands [14,15] (Fig 1). These remnant forests provide a valuable benchmark against which we evaluated the effects of widespread deforestation on an important metric of ecosystem function, namely primary productivity. Characterizing patterns of biodiversity and primary productivity is essential to fully understanding ecosystem function [16,17]. The latter includes three basic metrics: gross primary production (GPP), which describes all the CO2 fixed by the autotrophs during photosynthesis, total ecosystem respiration (Re), which describes the rele (...truncated)