Trophic downgrading reduces spatial variability on rocky reefs

www.nature.com/scientificreports OPEN Trophic downgrading reduces spatial variability on rocky reefs Matthew S. Edwards 1* & Brenda Konar 2 Trophic downgrading in coastal waters has occurred globally during recent decades. On temperate rocky reefs, this has resulted in widespread kelp deforestation and the formation of sea urchin barrens. We hypothesize that the intact kelp forest communities are more spatially variable than the downgraded urchin barren communities, and that these differences are greatest at small spatial scales where the influence of competitive and trophic interactions is strongest. To address this, benthic community surveys were done in kelp forests and urchin barrens at nine islands spanning 1230 km of the Aleutian Archipelago where the loss of predatory sea otters has resulted in the trophic downgrading of the region’s kelp forests. We found more species and greater total spatial variation in community composition within the kelp forests than in the urchin barrens. Further, the kelp forest communities were most variable at small spatial scales (within each forest) and least variable at large spatial scales (among forests on different islands), while the urchin barren communities followed the opposite pattern. This trend was consistent for different trophic guilds (primary producers, grazers, filter feeders, predators). Together, this suggests that Aleutian kelp forests create variable habitats within their boundaries, but that the communities within these forests are generally similar across the archipelago. In contrast, urchin barrens exhibit relatively low variability within their boundaries, but these communities vary substantially among different barrens across the archipelago. We propose this represents a shift from small-scale biological control to large-scale oceanographic control of these communities. Trophic downgrading occurs when apex predators have been extirpated over large geographic regions, which can lead to important consequences for ecosystem functioning due to both direct and indirect cascading effects1. This has been observed globally across a variety of terrestrial and marine e cosystems2–7. Often, trophic downgrading triggers increases in herbivore populations, thereby changing overall community structure6,8,9 and altering patterns of ecosystem productivity10–12. Trophic downgrading can be especially important if it ultimately affects ecosystem engineers that provide habitat, which modifies the physical environment, regulates primary production and energy flow, and generally supports high biodiversity. For example, the extirpation of gray wolves from Yellowstone National Park, USA in the early 1900s resulted in reduced predation on elk and increased herbivory on forest-forming t rees13. This ultimately led to changes in the morphology and hydrology of the region’s river systems and its riparian plant communities14,15. Similarly, the loss of sea otters from the nearshore habitats of the Aleutian Archipelago during the 1980s and 1990s resulted in reduced predation on herbivorous sea urchins and a subsequent overgrazing of the regions kelp f orests2. This led to reduced b iodiversity16, altered 17 12 food web dynamics , and reduced benthic ecosystem productivity in the coastal environment. Further, when a community has been downgraded, its resilience (i.e., recovery and stability after a disturbance) can decrease in comparison to intact communities3. This has been an important consideration in the design of marine protected areas (MPAs) and terrestrial parks and reserves, which typically protect apex predators to maintain diversity and normal ecosystem f unctioning7,18–20. Spatial and temporal variability in community structure are important components of ecological systems, and understanding how variability changes in space and time can infer a wide range of ecological processes21–27. For example, resistance to biological invasions is strongly correlated with variability in environmental c onditions28 and community s tructure29, with less variable communities being more resistant to invasion than highly variable communities. However, the loss of foundation species can increase susceptibility to biological invasions30,31. Moreover, patterns of variability can themselves change at different temporal and spatial scales coincident with environmental and demographic forcing factors21,25,26,32,33. Indeed, Levin21 noted that the problem of pattern and scale is the central problem in ecology and that it is important to find ways to quantify patterns of variability in space and time, understand how patterns change with scale, and understand the causes and consequences 1 Department of Biology, San Diego State University, 5500 Campanile Dr., San Diego, CA 92182, USA. 2Institute of Marine Science, University of Alaska Fairbanks, Fairbanks, USA. *email: Scientific Reports | (2020) 10:18079 | https://doi.org/10.1038/s41598-020-75117-2 1 Vol.:(0123456789) www.nature.com/scientificreports/ Figure 1.  Map of study area showing the nine islands sampled across the Aleutian Archipelago (inset shows portion of archipelago where islands are located). Coordinates in decimal degrees for approximate sampling locations are: Attu: 52.92°, 173.20°; Nizki/Alaid: 52.74°, 174.00°; Kiska: 51.97°, 177.58°; Amchitka: 51.41°, 179.28°; Tanaga: 51.81°, − 177.94°; Adak: 51.87°, − 176.66°; Atka: 52.10°, − 174.69°; Yunaska: 52.66°, − 170.74°; and Chuginadak: 52.84°, − 169.75°. Image from Metzger et al. 2019. of pattern. This can be especially important in ecosystems where different forcing factors affect communities across a range of spatial scales33–35. Kelp forests are benthic, biogenic habitats that include highly productive primary producers rivaling those of cultivated agricultural fields and tropical rainforests in p roductivity36–39. This productivity and the associated formation of complex, three-dimensional biogenic habitat enhances local biodiversity and secondary productivity16,40,41. However, kelp forests in many areas of the world have been trophically downgraded as their apex predators have been removed42,43. For example, in Tasmania, the loss of predatory lobsters has led to increases in sea urchin abundance and an increased risk of catastrophic shifts to widespread sea urchin b arrens44. Such deforestation of kelp forests due to sea urchin grazing is becoming more common in mid-latitudes45–47 (see also citations in Steneck et al.9). This generally results in a loss of biodiversity and associated ecosystem services, as kelp forests generally support more s pecies16,48 (this study) and exhibit greater primary productivity and habitat complexity12,49,50 than sea urchin barrens. Consequently, we expected there would be more combinations of species that could spatially differentiate the kelp forest communities than the sea urchin barren communities. This would be especially important at small spatial scales where the influence of biologi (...truncated)