Marine Environmental Research 159 (2020) 104991

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Marine Environmental Research

journal homepage: http://www.elsevier.com/locate/marenvrev

Biodiversity of an Antarctic rocky subtidal community and its relationship with meltdown processes

Nelson Valdivia a,b,*, Ignacio Garrido a,b,c, Paulina Bruning b,c, Andrea Pinones~ a,b,d, Luis Miguel Pardo a,b a Instituto de Ciencias Marinas y Limnologicas,� Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile b Centro FONDAP de Investigacion� en Dinamica� de Ecosistemas Marinos de Altas Latitudes (IDEAL), Valdivia, Chile c Department of Biology and Quebec-Ocean Institute, Universit�e Laval, Qu�ebec, QC, Canada d Centro de Investigacion� Oceanografica� COPAS Sur-Austral, Universidad de Concepcion,� Concepcion,� Chile

ARTICLE INFO ABSTRACT

Keywords: Glacier meltdown is a major environmental response to climate change in the West Antarctic Peninsula. Yet, the Bellingshausen dome consequences of this process for local biodiversity are still not well understood. Here, we analyse the diversity Benthic communities and structure of a species-rich marine subtidal macrobenthic community (consumers and primary producers) Collins glacier across two abiotic environmental gradients defined by the distance from a glacier (several km) and depth (be­ Diversity tween 5 and 20 m depth) in Fildes Bay, King George Island. The analysis of spatially extensive records of Environmental filtering Glacier retreat seawater turbidity, high-frequency temperature and salinity data, and suction dredge samples of macrobenthic Maxwell bay organisms revealed non-linear and functional group-dependent associations between biodiversity, glacier in­ South Shetland Islands fluence, and depth. Turbidity peaked in shallow waters and in the nearby of the glacier. Temperature and salinity, on the other hand, slightly decreased in the proximity of the glacier relative to reference sites. According to the spatial pattern in turbidity, species richness of consumers was lowest in shallow waters and near to the glacier. Also, Shannon’s diversity of consumers significantly decreased in the nearby of glacier across depths. Moreover, the spatial variation in community structure of consumers and primary producers depended on both glacier distance and depth. These results suggest that glacier melting can have significanteffects on diversity and community structure. Therefore, the accelerated glacier meltdown may have major consequences for the biodiversity in this ecosystem.

1. Introduction increasing atmospheric temperatures (Vaughan et al., 2003), length­ ening of the sea ice-melting season (Stammerjohn et al., 2012), and Understanding the spatial variation of biodiversity across abiotic increasing heat transport from below the ocean surface (Nakayama environmental gradients is central for applied and fundamental et al., 2018). The consequences of glacier meltdown for marine biodi­ ecological research (e.g. Vellend, 2016). In this line, environmental versity are, however, still unclear (but see Cauvy-Fraunie and Dangles, filtering encompasses abiotic limitations to organism physiology, 2019; Sahade et al., 2015; Lagger et al., 2018). The state of the current limiting individual survival probability and thus the number of species climate system compels us therefore to improve our understanding of that can develop viable populations in a given site (Somero, 2010). Due how drive marine biodiversity in WAP. to extreme environmental conditions, the Western Antarctic Peninsula Distance to glaciers defines a major environmental gradient for (WAP) is a model system to assess the role of abiotic environmental macrobenthic communities in WAP (Barnes and Clarke, 2011; Jerosch filtering in underpinning biodiversity. In this region, glacial processes et al., 2019). Glacial melting is related to adverse environmental con­ strongly influence local abiotic conditions and thus constitute a source ditions for macrobenthic assemblages due to decreased seawater salinity of environmental filtering in marine communities (e.g. Barnes and and temperature, in addition to increased turbidity, sedimentation, and Clarke, 2011; Jerosch et al., 2019). WAP is currently undergoing a rapid physical disturbance by ice (e.g. Barnes and Clarke, 2011; Ziegler et al., glacial retreat (Cook et al., 2005; Rückamp et al., 2011) as a result of 2017; Krzeminska and Kuklinski, 2018). In contrast, accelerated glacial

* Corresponding author. Instituto de Ciencias Marinas y Limnologicas,� Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile. E-mail addresses: [email protected] (N. Valdivia), [email protected] (L.M. Pardo). https://doi.org/10.1016/j.marenvres.2020.104991 Received 25 February 2020; Received in revised form 10 April 2020; Accepted 12 April 2020 Available online 25 April 2020 0141-1136/© 2020 Elsevier Ltd. All rights reserved. N. Valdivia et al. Marine Environmental Research 159 (2020) 104991

Fig. 1. Location of sampling sites in Fildes Bay, King George Island, West Antarctic Peninsula. Sites, sorted at increasing distances from glacier, are Collins (COLL), Artigas (ARTI), Suffield(SUFF), and Albatross (ALBA). The black asterisks (*) are the location of sampling sites and the circular symbols are the stations of turbidity. In panel A, the red asterisk is the Julio Escudero Research Station and the colour continuous scale is depth. In panels B, C, and D, the continuous colour scale denotes water turbidity (NTU) at 5, 10, and 20 m depth, respectively. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

meltdown in WAP is exposing ice-free rocky bottoms to colonisation by local species richness and diversity, and variations in community species-rich macrobenthic assemblages (Quartino et al., 2013; Lagger structure, with increasing distance from glacier are expected. Also, we et al., 2018). Thus, abiotic environmental conditions associated with predict that these patterns of biodiversity depend on subtidal depth, due glacial melting can be expected to account for a significantproportion of to the influence of glacier melting-associated stressors that decrease biodiversity in WAP. with depth and distance from glacier. To test these predictions, we The effects of glacial processes on macrobenthic communities can be analyse biodiversity in relation to seawater turbidity, salinity, and dependent on subtidal depth. For instance, the effects of glacier- temperature in Fildes Bay, King George Island. associated sedimentation are expected to vary with increasing depth (Sahade et al., 2015). Also, sharp vertical gradients in light availability 2. Materials and methods modulate the distribution of dominant macroalgae (Huovinen and Gomez,� 2013). King George Island offers an opportunity to assess the 2.1. Study area role of both gradients in defining macrobenthic biodiversity. Early and recent observations hint for an accelerated glacial retreat (Rückamp The study was conducted during the austral summer 2017 in Fildes et al., 2011) that boosts mineral suspension in different bays of the is­ Bay, King George Island (14 km long, 6–14 km wide, and 500 m land (Pecherzewski, 1980; Hofer€ et al., 2019). Moreover, glacier melt­ maximum depth; Fig. 1A). The water surface of Fildes Bay regularly water inputs act as a local source of Fe and promotes water column freezes in austral winter, from late July to mid-September (Kim, 2001; stability, which in turn drives the primary productivity of Fildes Khim et al., 2007; Bick and Arlt, 2013). The Collins Glacier—or Bel­ (Maxwell) Bay (Hofer€ et al., 2019). In this system, therefore, glacier lingshausen Dome—is a small ice dome (ca. 15 km2) located next to the � meltdown should influencethe depth-dependent diversity and structure northeast border of Fildes Bay and centred at ca. À 62.2 S and � of subtidal macrobenthic communities (e.g. Valdivia et al., 2014). À 58.95 W. The dome is slowly responding to regional climate change, Here we test the prediction that, since glacier melting acts as an with a retreat rate that correlates with monthly temperature and annual abiotic filter that limits the settlement and growth of macrobenthic or­ number of days of melting-degree temperatures (Simoes et al., 2015). ganisms (invertebrates and macroalgae > 5 mm), significantincreases in The subtidal rocky assemblages between 10 and 30 m in Fildes Bay

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Table 1 List of taxonomic identities identifiedin four rocky shore subtidal sites in Fildes Bay, King George Island. The occurrence of each taxon at a given site and depth is indicated by the coloured cell. Site codes as in Fig. 1.

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are characterised by large brown algae such as Himantothallus grandi­ 2.3. Abiotic environmental conditions folius and Desmarestia anceps, and red algae such as Trematocarpus ant­ arcticus, Plocamium cartilagineum, and Palmaria decipiens (Huovinen and A spatially extensive sampling of the water column turbidity was Gomez,� 2013; Valdivia et al., 2015). The grazer gastropods Nacella analysed for an array of stations distributed in order to represent the concinna, Margarella , the sea urchin Sterechinus neumayeri, and spatial variability of turbidity at Fildes Bay and Collins Glacier melt the sea stars Odontaster validus and Diplasterias brucei are described as water influence (Fig. 1). Turbidity was registered between 14 and 19 conspicuous benthic mobile invertebrates, in addition to sessile in­ January 2018 with a SeaBird Electronics 25plus Conductivity Temper­ vertebrates such as bryozoans, ascidians, and sponges (Sakurai et al., ature Depth (CTD) profiler, equipped with a Wet Labs turbidity sensor. 1996; Nonato et al., 2000; Kim, 2001; Khim et al., 2007; Valdivia et al., The CTD was lowered at each sampling station along the entire water 2015). column, but only the records for 5, 10, and 20 m depths are reported here. While the CTD measurements were appropriate for describing the 2.2. Sampling design and setup spatial coverage and influenceof the Collins Glacier plume, the temporal changes of the plume were not included in this study. However, previous The study was conducted at four sites located at increasing along­ work describing temporal variability of ocean water properties in Fildes � shore distances from Collins Glacier. The sites were “Collins” (À 62.18 S, Bay highlights the persistent influence of freshwater from the Collins � � � � À 58.82 W), “Artigas” (À 62.20 S, À 58.96 W), “Suffield” (À 62.19 S, Glacier during the austral summer (Hofer€ et al., 2019). � � � À 58.92 W), and “Albatross” (À 62.19 S, À 58.87 W). These sites are At each site, we deployed a self-contained thermistor (Star-Oddi DST � hereafter referred to as COLL, ARTI, SUFF, and ALBA, respectively CT), recording seawater salinity (PSU) and temperature ( C) every 30 (Fig. 1A). Across the four sites, only hard bottom epibenthic organisms min. Each sensor was encased in a PVC pipe, housed in a concrete block, were collected and analysed. The exception was the inclusion of and deployed by SCUBA divers at ca. 10 m depth from mean low water demersal fish, such as notothenioid Antarctic spiny plunder-fish. (MLW). All thermistors were deployed in February 2017 and the data At each site, we located five 50 � 50 cm plots at 5–10, 10–15, and were retrieved every 12 months until January 2019. Due to overgrowth 15–20 m depths by means of SCUBA diving (hereafter referred to as 5, of the sensors’ conductivity plates by encrusting organisms, however, 10, and 20 m for simplicity). The exception to this design was COLL, only the firsttwo months of the salinity timeseries was used for analyses. where no rocky substratum at the deepest stratum was available. The CT temperature sensors are not as sensitive as the conductivity plates; plots were separated ca. 10 m from each other. Plots were haphazardly therefore, the temperature records were not affected by biofouling. located within areas of similar slopes and lacking large crevices to Moreover, the temperatures obtained during the summer months were � reduce the within-group variation. Plot slopes ranged between 20 and similar to previously recorded values in the bay (e.g. Hofer€ et al., 2019; � 40 . Llanillo et al., 2019). For each plot, we used suction dredge sampling to collect all sessile and mobile macrobenthic organisms (>5 mm length; see also Wahle and 2.4. Statistical analyses Steneck, 1991). A portable underwater venture-suction sampler was used, which consisted of an auxiliary SCUBA cylinder connected, The timeseries of seawater temperature were analysed using a through a BCD hose and an air-feed valve, to the wall of a 2.3 m long, 10 Generalised Additive Model (GAM, Hastie and Tibshirani, 1986; Wood, cm diameter polyvinylchloride pipe. One of the extremes of the pipe was 2006). The model included the monthly moving average of temperature used to dredge the surface of each plot—the other extreme of the pipe as response variable, and Site (four levels: COLL, ARTI, SUFF, and was equipped with a 5-mm pore mesh that received the extracted ma­ ALBA), the smooth function of month, and the site-dependent smooth 2 terial. Before the sampling, a 0.5 m metallic frame was placed on each function of month as explanatory variables. We used cyclic penalised plot to standardise the sampled area. Additionally, each plot was scra­ cubic regression splines for the smooth terms of the model. The appro­ ped with a spatula to collect seaweeds and invertebrates that remained priate smoothness for the model was found by means of Generalised attached to the rocky substratum. Cross Validation (GCV). We used a “treatment” contrast to set COLL (site After suction dredging, samples were placed into independent and located nearest to glacier) as the reference site for the between-site labelled plastic bags on the boat and refrigerated within few hours after comparisons. returning to the facilities of the Julio Escudero Research Station (Insti­ The relationship between distance to the glacier and biodiversity was 0 tuto Nacional Antartico,� INACh). The samples were frozen and then tested separately for S and H , and for consumers and primary producers, transported to the facilities of the Universidad Austral de Chile in Val­ with Generalised Linear Models (GLM). The models included Site and divia, south-central Chile, for species sorting and identification. In the Depth (three levels: 5, 10, and 20 m) as fixed and crossed factors. laboratory, organisms were sorted and identified to the lowest taxo­ Graphical inspections of residuals suggested that Poisson and Gamma nomic level possible, usually to species level (Table 1). The abundance of structure of errors were appropriate for S and H’, respectively. invertebrate species (hereafter referred to as consumers) was expressed Goodness-of-fit was assessed for each model by means of a likelihood -2 as number of individuals 0.25 m , while that of primary producers was ratio based pseudo-coefficient of determination (R2). A “treatment” -2 expressed as wet weight (g 0.25 m ; 0.01 g accuracy). contrast was used for the factor Site (setting COLL as reference group) The abundance data were used to estimate species richness (S), and a linear contrast was used for Depth. Since the 20-m-depth stratum definedas the number of taxonomic identities, and Shannon’s diversity P was absent in COLL, only the 5- and 10-m-depth strata were used to test 0 ¼ À S ð � Þ (H ), definedas H’ i ¼ 1 pi ln pi , where pi is the proportion of the interaction between site and depth. species i’ abundance relative to the total abundance of the community. Community structure, summarised as Bray-Curtis dissimilarities, was For each site by depth combination, we calculated the bias-corrected analysed separately for consumers and primary producers in Permuta­ Chao estimator of extrapolated species richness (Chao, 1987). This tional Multivariate Analyses of Variance (PERMANOVA; Anderson, index estimates the number of unseen species and add them to the 2001). The analyses used 999 permutations of raw data and were based observed species richness (Colwell and Coddington, 1994). Also, a ma­ on the same model used for S and H’. After PERMANOVA, we used trix of Bray-Curtis dissimilarities was computed to analyse community Similarity Percentage (SIMPER) routines to determine the relative 0 structure. All estimators (S, H , Chao, and Bray-Curtis dissimilarities) contribution of each species to the overall between-site dissimilarity. were calculated and analysed separately for consumers and primary Since the 20 m stratum was unavailable in COLL, the between-site producers. SIMPER routines were computed only for the 5 and 10 m depths. The spatial patterns of community structure were described in a constrained Principal Coordinates Analysis (PCoA) ordination (Borcard et al., 2011).

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Fig. 2. Temporal patterns of seawater temperature (A) and salinity (B) at four sites located at increasing distances from Collins Glacier. Temperature is provided as 30-day moving averages between February 2017 and January 2019; salinity, on the other hand, is provided as daily moving averages between February and April 2017. Site codes and locations as in Fig. 1.

Fig. 3. Species-accumulation curves of invertebrates (A) and seaweeds (B) across four sites located at increasing distances from Collins Glacier. Cumulative number of species is reported as mean � SD for each random combination of plots (50 � 50 cm areas). Site codes and locations as in Fig. 1.

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Table 2 consumers, on the other hand, the species accumulation curves hinted Descriptive statistics of observed and extrapolated species richness for each site for a small proportion of unseen species (see also Table 2). Pearson by depth combination. Extrapolated species richness was estimated by means of product-moment correlations between S and Chao were positive and � Chao ( Standard Error) index. No hard-bottom substrate was available in COLL statistically significant for both consumers and primary producers (r ¼ at 20 m depth (NA). 0.63 and P ¼ 0.04; r ¼ 0.97 and P < 0.01, respectively). Site Depth Consumers Primary producers At the plot scale, S of consumers was lowest at COLL and increased Observed Chao Chao Observed Chao Chao with depth across the study area (Fig. 4A). The GLM analysis hinted for a SE SE systematic increase in S from COLL to the other sites (Table A2 in Ap­ COLL 5 23 39.9 13.3 3 3.0 0.3 pendix A). In addition, the difference in S between 5 and 10 m depth was ARTI 5 48 58.0 6.3 8 9.2 1.9 significantly larger in COLL than in ARTI and ALBA, indicating an SUFF 5 28 58.0 23.9 13 18.0 6.1 interactive effect of depth and site on species richness (Table A2). This ALBA 5 37 54.1 11.8 7 8.8 2.8 model accounted for 76% (R2 ¼ 0.76) of the variation in S of in­ COLL 10 36 84.1 36.2 6 7.8 2.8 ARTI 10 53 65.6 7.4 6 6.8 1.5 vertebrates. On the contrary, the statistical model poorly fitted on the 2 ¼ SUFF 10 53 94.0 20.5 10 14.8 5.3 data of primary producer S (R 0.19; Fig. 4B) and all parameters were ALBA 10 43 53.7 6.5 8 9.7 2.6 undistinguishable from zero (Table A2). 0 COLL 20 NA NA NA NA NA NA Shannon’ diversity (H ) of invertebrates was lowest in COLL relative ARTI 20 56 84.8 16.5 12 20.5 8.3 to ARTI and ALBA (Fig. 4C; Table A2 in Appendix A). No other com­ SUFF 20 47 58.3 7.8 6 6.8 1.5 ALBA 20 54 76.5 12.0 7 7.8 1.5 parison was statistically significant for this variable (Table A2). The model accounted for the 36% of the variation in invertebrate H’. Shannon’ diversity of primary producers exhibited a small variation This method allowed us to show the multivariate axes that accounted for across sites and depth (Fig. 4D), a pattern that was supported by the poor most of the variation in the species abundance dataset according to our fit of the statistical model (3% of explained variation). predictive model (i.e. the separate and joint site by depth effect on The between-site variation in community structure depended on community structure). To reduce the distortion in the ordination of depth (Fig. 5). For consumers, the plots located in COLL grouped consumers, we used only species occurring with at least one individual together in the ordination. In addition, the other sites showed a high per plot (i.e. mean abundance �1). For both, consumers and primary overlap, and depth bottoms tended to form groups in the ordination producers, abundances were standardised by their maximum values to (Fig. 5A). For primary producers, the communities located in COLL and � reduce horseshoe effects (Podani and Miklos, 2002). All analyses were at 5 m depth were segregated from the rest of the assemblages in the conducted in R environment, version 3.6.1 (R Core Team, 2019). multivariate space (Fig. 5B). Communities of primary producers at 20 m depth distinguished from the others in the ordination (Fig. 5B). Ac­ 3. Results cording to these observations, PERMANOVA supported a significant fit of the joint effects of site and depth on community structure for both 3.1. Abiotic environmental conditions consumers and primary producers (Table A3 in Appendix A). The contribution of individual species to the between-site differences Turbidity ranged from ca. 0 NTU in the centre of the bay to ca. 2 NTU in community structure was highly inconsistent across replicate plots. in the nearby of Collins Glacier (Fig. 1B–D). At 5 m depth, turbidity was This was evidenced by the comparatively high standard deviations highest in the north-northwest margin of the bay (Fig. 1B). Turbidity (relative to the mean) of the species-specific contributions to overall tended to decrease with depth, particularly at 20 m depth (Fig. 1C and dissimilarities (Figs. 6–9). Nevertheless, we were able to identify few D). In this way, we detected a glacier-associated vertical turbidity particular patterns across depths. For instance, the spatial patterns of the gradient. structure of shallow water (5 m) invertebrate communities were The high frequency timeseries showed a marked seasonal pattern in accounted for, in average, by the lowest abundance of most species in seawater temperature (Fig. 2A, see also GAM-predicted temperatures in COLL (see negative Δi values in Fig. 6). The amphipod Eurymera mon­ Fig. A1). Seawater was coldest in COLL, the site located nearest to ticulosa, however, peaked in COLL (Fig. 6). Palmaria decipiens accounted Collins Glacier. However, this difference was comparatively small and for most of the variation (70%) of the structure of shallow water mac­ season dependent, as it was evident during summer and winter, but not roalgal communities—this species was generally more abundant in during spring and autumn (Fig. 2A). The site-dependent seasonal pattern COLL than in the other sites of the bay (Fig. 7). 2 of seawater temperature was well described by the GAM (R ¼ 0.94, At 10 m depth, the gastropod Laevilitorina caligosa accounted for an deviance explained ¼ 94.2%; Fig. A1 and Table A1 in Appendix A). important variation in community structure of invertebrates; it was During the austral summer 2017, seawater salinity was consistently more abundant in COLL relative to the rest of the bay (Fig. 8). Still, the lower in COLL than the sites located at increasing distances from the rest of the species in the community were less abundant in COLL than the glacier (Fig. 2B). COLL, ARTI, SUFF, and ALBA exhibited mean (�SD) other sampling sites. The largest abundance of P. decipiens in COLL was salinities of 32.4 � 0.3, 33.2 � 0.2, 33.2 � 0.1, and 33.5 � 0.2 PSU, important to explain the multivariate patterns of macroalgal commu­ respectively. Nevertheless, salinity tended to decrease over the summer nities at 10 m depth (Fig. 9A). In addition, Desmarestia anceps and Plo­ months in COLL (Fig. 2B). camium cartilagineum were scarcer in COLL compared to SUFF and ALBA, respectively (Fig. 9B and C, respectively). 3.2. Patterns of biodiversity associated to glacier proximity Fifteen species accounted for the 70% of the variation in consumer community structure between 5 and 10 m depth across sites. These A total of 122 taxa were identifiedacross the four sites. One-hundred dissimilarities were mainly accounted for by the decreases in abundance and three taxa of consumers and 19 taxa of primary producers were of Laevilacunaria antarctica, Gondogeneia antarctica, E. monticulosa, and identified (Table 1). The lowest richness of both functional groups was Oradarea bidentata, and the increases of Schraderia gracilis, Margarella registered in COLL (Fig. 3). The maximum values, on the other hand, antarctica, and L. caligosa. For the same between-depth comparison, were estimated in ARTI (consumers; Fig. 3A) and SUFF (primary pro­ three species accounted for the 70% of the multivariate dissimilarities ducers; Fig. 3B). In the case of consumers, the species-accumulation between communities of primary producer. The abundance of curves suggested the presence of a high number of unobserved spe­ P. decipiens decreased—and those of D. anceps and P. cartilagineum cies, which was corroborated by the differences between the observed increased—from 5 to 10 m depth. species richness and the Chao estimator (Table 2). For primary Between 10 and 20 m depth, fourteen species accounted for 70% of

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Fig. 4. Spatial variation in species richness (A and B) and Shannon’ diversity (C and D) of consumers (A and C) and primary producers (B and D) in Fildes Bay. Sites are sorted at increasing distances from Collins Glacier (COLL). Colour scale denotes three depth ranges. Site codes and locations as in Fig. 1. Values are provided as mean � 95% CI. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

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Fig. 5. Constrained PCoA ordination, based on Bray-Curtis dissimilarities, depicting the patterns of spatial variation in community structure at three subtidal depths (5, 10, and 20 m) and four sites located at increasing distances from Collins Glacier (COLL) in Fildes Bay, West Antarctic Peninsula. Site codes and locations as in Fig. 1. Values of brackets indicate the contribution each axis (eigenvalues in percentages) to the dissimilarities between plots.

the between-group dissimilarities of consumers. From these, S. gracilis, discharge can be further related with a reduced proportion of available Prostobbingia brevicornis, and O. bidentata increased in abundance, while food for suspension feeders (Krzeminska and Kuklinski, 2018), and L. caligosa, Oraera sp., and M. antarctica decreased with increasing excessive sedimented material can clog their feeding appendages (see depth. For primary producers, three species accounted for the 70% of the Topçu et al., 2019 for an example elsewhere). Enhanced sedimentation, dissimilarities between 10 and 20 m depth. The three species, therefore, can compromise individual fitnessand population numbers of P. cartilagineum, D. anceps, and P. decipiens, decreased with increasing an important fraction of the community. And third, turbidity increases depth in this pairwise comparison. the rate of light attenuation with depth, generating a steeper vertical stress gradient for primary producers in the glacier’s nearby (Huovinen 4. Discussion and Gomez,� 2013). This gradient could have supported the observed change in community structure observed for primary producers. This study showed significant and non-linear associations between Generally speaking, sedimentation has been suggested as a central biodiversity, glacier-melting influence, and depth in a species-rich glacier melting-associated factor affecting the structure of Antarctic Antarctic macrobenthic community. Coupled with environmental communities in hard- (e.g. Krzeminska and Kuklinski, 2018) and data, the biological data indicate that glaciers can have important, but at soft-bottom habitats (Gutt et al., 2019; Vause et al., 2019). the same time spatially confined, effects on diversity and community In addition to turbidity, salinity and temperature showed glacier- structure in Fildes Bay. Seawater temperature and salinity evidenced associated spatial patterns of variation, with lower salinities and tem­ small decreases when compared to the increased turbidity in the gla­ peratures in the proximity of Collins Glacier. In the case of salinity, such cier’s nearby and shallow waters. The reduced species richness and “freshening” is related to anomalous sea ice records that reached a particular structure observed in shallow waters near Collins Glacier historically minimum extent in winter 2016 (Turner et al., 2017), which could be explained by multiple interacting factors, including glacier allowed surface waters in coastal areas to heat up and enhance the meltdown-related (1) high levels of suspended particles, (2) sedimen­ glacial meltwater influence within Fildes Bay (Hofer€ et al., 2019). tation, and (3) unmeasured factors such as ice scouring. However, the observed spatial variation in salinity, in addition to � Seawater turbidity was higher—but decreased with depth—in the seawater temperature (less than ca. 1 PSU and 0.3 C lower in COLL nearby of Collins glacier. Turbidity can be used as an appropriate proxy relative to the other sites, respectively), seemed to be too small to for sedimentation (Tait, 2019), which in turn affects macrobenthic generate significant biological responses in these communities. For communities exposed to glacial melting by multiple, non-exclusive instance, seawater salinities of 25 PSU combined with temperatures of 5 � mechanisms (Barnes and Clarke, 2011; Sahade et al., 2015). First, C are necessary to increase the metabolic rates of the Antarctic increased sedimentation reduces the availability of rocky substrates for amphipod Gondogeneia antarctica under experimental conditions settlement of both consumers and primary producers (e.g. Khim et al., (Gomes et al., 2013). The notothenioid fishHarpagifer antarcticus shows, 2007)—indeed, we were unable to localise rocky substratum at 20 m moreover, non-significant responses to 10-day experimental decreases � depth in the nearby of Collins Glacier. Second, the discharge of mineral in salinity (23 PSU) and increases in temperature (5 C; Navarro et al., suspension increases the metal accumulation and cellular oxidative 2019; Vargas-Chacoff et al., 2019). Salinities of 30 PSU combined with � stress in subtidal filter feeders (Husmann et al., 2012). The mineral temperatures between 4 and 5 C hamper the vital functions of the

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Fig. 6. Consumers (5 m depth): Breakdown of cumulative species contributions to between-site Bray-Curtis dissimilarities. Species with a cumulative contribution �70% are shown. The continuous colour scale (Δi) indicates the difference in mean abundance of each species between Collins Glacier (COLL) and each of the three sampling sites (ARTI, SUFF, and ALBA). For instance, Δi ¼ À 10 in ARTI indicates that the abundance of species i is in average ten units lower in COLL than ARTI. Species contributions are provided as mean � SD. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

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Fig. 7. Primary producers (5 m depth): Breakdown of cumulative species contributions to between-site Bray-Curtis dissimilarities. Species with a cumulative contribution �70% are shown. soft-bottom isopod Serolis polita in climate change experiments (Janecki the distance from nearest local glacier (Gutt, 2001). On the other hand, et al., 2010). Thus, it is likely that the observed horizontal spatial primary producers did not exhibit a clear trend in richness and diversity variation in salinity and temperature accounted for a small fraction in with distance from glacier and depth. The turnover of macroalgal spe­ the variation in biodiversity. cies across both environmental gradients could explain this pattern. For It is relevant to discuss the potential effects of other, non-measured instance, the opportunistic macroalga Palmaria decipiens was numeri­ factors on biodiversity in our study. For example, ice scouring, the cally dominant at 5 m depth and in the nearby of Collins glacier, being process of ice removing sessile and semi-sessile organisms from the replaced by perennial macroalgae with distance from glacier and depth. seabed (Smale et al., 2008), has been proposed to significantly disturb Previous observational work demonstrates that P. decipiens is able to both intertidal and subtidal Antarctic communities in Antarctic ecosys­ colonise recently ice-scoured substratum in association with a severe tems (Gutt and Starmans, 2001; Barnes and Souster, 2011). Albeit ice glacial retreat in Potter Cove, King George Island (Quartino et al., 2013). scour seems to have little influenceon the diversity and composition of Seasonal changes in ice scouring and other factors, such as turbidity, Antarctic soft-bottom communities (Vause et al., 2019), this factor can should also be considered as potential drivers of biodiversity in Fildes be an important driver of hard-bottom assemblages. These effects are Bay. Seawater turbidity can increase during summer months due to expected to be less intense far to the glacier and deeper zones, which enhanced primary productivity, and the individuals in these population could account for the increase in species richness of consumers with both could be adapted to such environmental changes (Clarke et al., 2007; gradients. However, large icebergs can be moved by currents from Vause et al., 2019). Despite these apparent shortcomings, our work is neighbouring bays, which may affect local biodiversity independently of well in line with previous evidence demonstrating that accelerated

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Fig. 8. Consumers (10 m depth): Breakdown of cumulative species contributions to between-site Bray-Curtis dissimilarities. Species with a cumulative contribution �70% are shown. glacier meltdown has the potential of largely modify the seascape in biodiversity of this region. these marine habitats (e.g. Sahade et al., 2015; Lagger et al., 2018). Declaration of competing interest 5. Conclusions The authors declare that they have no known competing financial In summary, glacial melting can have a significant but localised in­ interests or personal relationships that could have appeared to influence fluence on biodiversity in a species-rich Antarctic community. We the work reported in this paper. described a reduced diversity (species richness and Shannon’s diversity of consumers) and specificcommunity structure in the nearby of glacier. CRediT authorship contribution statement The glacier-associated variation in species richness and community structure was, however, dependent on subtidal depth. The observed Nelson Valdivia: Conceptualization, Software, Validation, Formal small range of variation in seawater temperature and salinity suggests analysis, Writing - original draft, Visualization. Ignacio Garrido: & that both factors accounted for a limited proportion of variation in Investigation, Writing - review editing. Paulina Bruning: Investiga­ & ~ & biodiversity in comparison to turbidity, which peaked in the glacier’s tion, Writing - review editing. Andrea Pinones: Writing - review nearby and shallow waters. Other glacier melting-related factors, like ice editing, Visualization. Luis Miguel Pardo: Conceptualization, Data & scouring and seasonal changes in turbidity, could have also influenced curation, Writing - review editing, Supervision. the observed patterns of ecological variation. Climate change-associated glacial meltdown, therefore, will have profound consequences for the

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Fig. 9. Primary producers (10 m depth): Breakdown of cumulative species contributions to between-site Bray-Curtis dissimilarities. Species with a cumulative contribution �70% are shown.

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