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Benthic Ecosystem Cascade Effects in Antarctica Using Bayesian Network Inference ✉ Emily G

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Benthic Ecosystem Cascade Effects in Antarctica Using Bayesian Network Inference ✉ Emily G ARTICLE https://doi.org/10.1038/s42003-020-01310-8 OPEN Benthic ecosystem cascade effects in Antarctica using Bayesian network inference ✉ Emily G. Mitchell 1 , Rowan J. Whittle2 & Huw J. Griffiths 2 1234567890():,; Antarctic sea-floor communities are unique, and more closely resemble those of the Palaeozoic than equivalent contemporary habitats. However, comparatively little is known about the processes that structure these communities or how they might respond to anthropogenic change. In order to investigate likely consequences of a decline or removal of key taxa on community dynamics we use Bayesian network inference to reconstruct ecolo- gical networks and infer changes of taxon removal. Here we show that sponges have the greatest influence on the dynamics of the Antarctic benthos. When we removed sponges from the network, the abundances of all major taxa reduced by a mean of 42%, significantly more than changes of substrate. To our knowledge, this study is the first to demonstrate the cascade effects of removing key ecosystem structuring organisms from statistical analyses of Antarctica data and demonstrates the importance of considering the community dynamics when planning ecosystem management. 1 Department of Zoology, University of Cambridge, Downing St, Cambridge CB2 3EJ, UK. 2 British Antarctic Survey, High Cross, Madingley Road, Cambridge ✉ CB3 0ET, UK. email: [email protected] COMMUNICATIONS BIOLOGY | (2020) 3:582 | https://doi.org/10.1038/s42003-020-01310-8 | www.nature.com/commsbio 1 ARTICLE COMMUNICATIONS BIOLOGY | https://doi.org/10.1038/s42003-020-01310-8 he ecological structure of modern Antarctic benthic marine from within the South Orkney MPA and the surrounding area, at communities differs from the rest of the world. There is a the shelf break. Using in situ photographs, ten dominant phyla T fi paucity of shell crushing predators (sharks, rays, dur- can be identi ed from the SOISS benthic invertebrate commu- ophagous decapods), leading to dominance by epifaunal suspen- nity. The community is dominated by VME taxa (these are sion feeding groups such as sponges1–5. Disturbance to dominant habitat forming taxa which could not be confidently identified benthic taxa, such as the sponges, has the potential to alter the from photographs), echinoderms and cnidarians, with frequent ecosystem, but it is not known how. Generally, there are limited bryozoan and poriferan taxa10. data on the structure and function of Southern Hemisphere New approaches for assessing biodiversity across MPA’s are benthic ecosystems compared with other areas globally. Despite increasingly important given their increased prevalence in inter- this limited data, Antarctic benthic marine communities are national conservation strategies and the associated costs of abundant and diverse6 with complex functional diversity and a assessment and monitoring10. Our study determines the com- highly structured, three-dimensional, physical configuration1,7–9. munity structure on different spatial scales using Bayesian Net- The South Orkney Islands (SOI) are located in the Southern work Inference (BNI) analysis. BNI is a technique to statistically Ocean, 604 kilometres north-east of the tip of the Antarctic infer the causal relationships (or dependencies) between different Peninsula, at a latitude of around 60° 35′ S. The seafloor around variables, which in this study are different taxa and different the SOI has an exceptionally high biodiversity; one-fifth of the environmental factors such as substrate type and depth16. In the animals found in the entire Southern Ocean are represented10,11. BNI presented here, the variables such as a taxon, or an envir- Benthic biodiversity in the SOI has been studied previously10–12. onmental factor, are described as ‘nodes’, and the relationship Brasier et al.10 showed that benthic communities in the SOI were between them as ‘connections’ (more usually known as ‘edges' in strongly correlated with the hardness of the seafloor. Soft sedi- network literature), so that the network consists of a series of ments were dominated by deposit feeders, hard surfaces had a connected nodes. The strength of the relationship between two greater abundance and richness of taxa, and an overall higher nodes (i.e., the strength of the connection) is given by the biomass. They were also dominated by filter feeding Vulnerable Influence Score (IS), which is calculated as a cumulative fre- Marine Ecosystem (VME) taxa10. VME’s are marine areas that quency distribution over all possible discrete states17. Discrete are vulnerable to the effects of anthropogenic activities, such as Bayesian Network Inference Algorithms (BNIAs) enable the fishing13. inference of causal relationships (over just mutual correlations), The South Orkney Islands Southern Shelf (SOISS) was the first as well as non-linear interactions. We use BNIAs to determine the designated Marine Protected Area (MPA) from the high seas on key taxa and environmental factors that underpin Antarctic the planet (Fig. 1), established in 200910,14. MPA’s are clearly benthic community dynamics and use the Bayesian networks to defined geographically, and managed using legal and protective infer likely changes of taxon removal within this MPA. measures for the long-term conservation of nature, associated The BNIA Banjo16 was used to generate two different Bayesian ecosystem services, and cultural values15. The SOISS MPA is networks over different spatial scales18. The fine-scale analysis managed under the Commission for the Conservation of Ant- used 527 individual photographs, which covered 0.51 m2 for each arctic Marine Living Resources (CCAMLR)10. Our data come sample and the large-scale analyses grouped photographs within Fig. 1 Locality map. a Location map of South Orkney Islands sampling and b–e photographs of key taxa and habitats from the South Orkney Region. b Soft sediments dominated by echinoderms and arthropoda; c soft sediment with dropstones colonised by cnidaria, bryozoans, sponges, and encrusting taxa; d hard substrate dominated by echinoderms and encrusting taxa; e large sponge-dominated habitat. 2 COMMUNICATIONS BIOLOGY | (2020) 3:582 | https://doi.org/10.1038/s42003-020-01310-8 | www.nature.com/commsbio COMMUNICATIONS BIOLOGY | https://doi.org/10.1038/s42003-020-01310-8 ARTICLE Region Porifera 0.1485 0.1668 0.1884 0.4260 0.0364 0.4617 0.1322 0.2152 Substrate 0.4984 Depth 0.6328 0.4710 VME Unknown Substrate 0.2985 -0.1655 Echinodermata Ophiuroidea 0.4439 0.1483 0.2625 0.0298 0.1859 0.0063 % Encrusting 0.4017 Bryozoa Porifera Cnidaria Echinodermata Fig. 2 Fine-scale Bayesian network. Dependencies between nodes are indicated by the lines connecting them, the width of which indicates the Cnidaria Bryozoa Mollusca Euryalida occurrence rate in the bootstrap analyses (wider lines indicate higher 0.1329 0.4017 -0.1664 occurrence). Arrows indicate nonmutual dependence between two nodes where the head of the arrow is dependent taxa, for example the arrow from % Encrusting region to substrate indicates that substrate depends on region. Mutual Arthropoda dependencies are indicated as double headed arrows. Mean interaction strengths of the correlations are indicated; positive interaction strengths Fig. 3 Bayesian networks of large-scale data. Dependencies between indicating aggregation, negative interaction strengths indicating nodes are indicated by the lines connecting them, the width of which segregation. Taxa that have no dependencies on another node are not indicates the occurrence rate in the bootstrap analyses (wider lines indicate shown. Purple arrows depict dependencies on substrate. The dark blue higher occurrence). Single-headed arrows indicate nonmutual dependence arrow is between two physical nodes (Region and Substrate). Red arrows between two taxa; mutual dependencies are indicated by double headed are those dependencies resulting from Region and light blue arrows are arrows. Mean interaction strengths of the correlations are indicated; those that affect percent encrusting. positive interaction strengths indicating aggregation, negative interaction strengths indicating segregation. Taxa that have no dependencies with 21 transects of 1.2 km long for each sample. The raw data were another node are not shown. Light blue depicts dependencies between filtered to avoid Type I errors through zero-inflation. The fine- different taxa and purple between physical nodes and taxa. scale analysis included the physical nodes: Depth, Substrate and Region (Fig. 1, Supplementary Table 1) and seven taxonomic Large-scale network. The large-scale network (between sampling groups (Supplementary Table 2). The large-scale analysis inclu- events) had 14 nodes within the analyses, of which Depth, fi ded Depth, Substrate and Region (Supplementary Table 3) and 12 Actinopteri ( sh) and Annelids were not connected (Fig. 3). At fi taxonomic groups (Supplementary Table 4). The data were dis- this spatial-scale there were insuf cient samples in the different cretized into zero, low, and high groups19, using medians to Region groups to include Region in the analysis. Porifera was the fi differentiate the boundary for the low and high abundances. For most connected taxon ( ve connections) and substrate the most percentage encrusting and depth, quartiles were used, and modes connected physical variable (three connections). The strongest for region and substrate (Supplementary Tables 5–6). Quartiles dependency was between bryozoans and percentage of encrusting are used for percent encrusting and depth rather than medians organisms
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