Fishery-Induced Reductions in Density and Size Truncation of Sea Urchin Loxechinus Albus Aﬀects Diversity and Species Composition in Benthic T Communities

Home , Guaitecas Archipelago, Loxechinus albus

Estuarine, Coastal and Shelf Science 219 (2019) 409–419

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Estuarine, Coastal and Shelf Science

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Fishery-induced reductions in density and size truncation of sea urchin Loxechinus albus aﬀects diversity and species composition in benthic T communities

∗ Catalina Contrerasa,b, , Edwin Niklitschekb, Carlos Molinetc, Patricio Díazb, Manuel Díazc a Universidad de Los Lagos, Programa de Magíster en Ciencias, mención Producción, Manejo y Conservación de Recursos Naturales, Chile b Universidad de Los Lagos, Centro i∼mar, Camino a Chinquihue km 6, Puerto Montt, Chile c Universidad Austral de Chile, Instituto de Acuicultura, Los Pinos s/n, Balneario Pelluco, Puerto Montt, Chile

ARTICLE INFO ABSTRACT

Keywords: Fishery assessments are frequently focused on economically important target species, thus, effects of fisheries on Benthic communities associated habitats and communities are often neglected and/or poorly understood. In Northwest Patagonia, Benthic fisheries commercial beds of the red sea urchin Loxechinus albus are subjected to intense fishing, which along with large Sea urchin environmental variability are believed to affect the diversity and structure of benthic communities. We evaluated Patagonia the potential of two types of L. albus demographic indexes: density and size structure, and of three environmental covariates: temperature, salinity and chlorophyll-a concentration to explain the richness, diversity and species composition of L. albus benthic communities. Then, we compared models containing L. albus demographic indexes and environmental covariates, against alternative models based upon simple geographic variables and against null models. Richness and diversity presented positive relationships with both L. albus density and size structure indicators, suggesting that L. albus beds subjected to higher exploitation levels present less rich and diverse communities than less exploited ones. Size structure had a significant effect on richness, diversity and species composition. The environmental variables temperature and salinity had a significant effect on most response variables, while chlorophyll-a concentration had a significant effect only on species composition. Models containing demographic indexes and environmental covariates were more informative than geographic and null models. Our results showed that L. albus fishery affects not only this target population but also the associated benthic communities. These findings highlight the importance of adopting a more integral ecosystem- based approach to assess the impact of benthic fisheries.

1. Introduction impacts upon the environment, most fishery assessments remain focused on target species. As a result, most effects of fisheries upon as- Although fishery assessments are frequently focused on economic- sociated habitats and communities remain poorly understood ally important target species, during the last two decades, it has been (Sainsbury et al., 2000). possible to observe a growing commitment to implement the Ecosystem The present work focuses on beds of the sea urchin Loxechinus albus, Approach to Fisheries (FAO, 2003). This framework implies assessing which is an economically important species in Northwest Patagonia not only the direct effects of fisheries upon target stocks but also con- (NWP), characterized to be part of a highly diverse benthic community sidering their impacts upon the environment, including habitats and (Contreras et al. unpublished data). This species forms large beds of − biodiversity (Garcia and Cochrane, 2005). Several fisheries have been 11,000–2,500,000 individuals, with densities up to 11 individuals·m 2 shown to generate concomitant effects upon non-target benthic species, (Molinet et al., 2016). Chilean landings of L. albus averaged 18,077 t communities and critical habitats (Jennings and Kaiser, 1998), such as between 2010 and 2016, involving around 4300 divers across the habitat destructions by bottom-trawling fisheries (Victorero et al., country (SERNAPESCA, 2016). Over half of these divers concentrated 2018), bycatch (Villalobos-Rojas et al., 2017), modification of trophic their effort in NWP (SERNAPESCA, 2016), causing severe and hetero- networks (Castilla, 1985) and mechanical disturbance (Hall and geneous changes in L. albus density and size structure (Molinet et al., Harding, 1997), among others. Despite these potentially deleterious 2016; Moreno et al., 2007). Nonetheless, no assessments about the

∗ Corresponding author. Universidad de Los Lagos, Programa de Magíster en Ciencias, mención Producción, Manejo y Conservación de Recursos Naturales, Chile. E-mail address: [email protected] (C. Contreras). https://doi.org/10.1016/j.ecss.2019.02.030 Received 20 July 2018; Received in revised form 7 February 2019; Accepted 9 February 2019 Available online 14 February 2019 0272-7714/ © 2019 Elsevier Ltd. All rights reserved. C. Contreras, et al. Estuarine, Coastal and Shelf Science 219 (2019) 409–419

Fig. 1. Northwest Patagonia region (∼41°-47°S) and spatial distribution of the 22 study sites (in colors), corresponding to natural Loxechinus albus beds. Colors represent different zones inside Northwest Patagonia. 1: Carelmapu, 2: Caulín, 3: Quenu Island, 4: Tautil Strait, 5: East Guar Island, 6: South Guar Island, 7: Point Pájaros, 8: Chincui Shoal, 9: Nayahue Island, 10: Point Paula, 11: Point Boigue, 12: Westhoff Island, 13: Leucayec Island, 14: Erizo Islet, 15: Midhurst Island, 16: North Skorpios Channel, 17: South Skorpios Channel, 18: Tahuenahuec Island, 19: Point Nicolás, 20: Stokes Island, 21: Rowlett Island, 22: Goñi Channel. impacts of these demographic changes in L. albus beds upon their re- grazing activity due to increased L. albus density might enhance the lated benthic communities have been carried out. availability of settling substrate and/or modify its physico-chemical While other sea urchin species are known to greatly influence their properties, reducing competition among species and/or favoring re- surrounding communities (Benedetti-Cecchi et al., 1998; Byrnes et al., cruitment of non-dominant species, thus, leading to greater species 2013; Estes et al., 1978; Lawrence, 1975), the effects of L. albus upon its richness and diversity. Loxechinus albus may also have a role in the associated communities in NWP are still unclear. Some authors have transformation of drifting brown macroalgae to particulate organic indicated that this species might play a significant role controlling the matter, whose availability for benthic filter-feeders and suspensivorous abundance of the kelp Macrocystis pyrifera,(Buschmann et al., 2004; (Moreno et al., 2018) would be greater at higher L. albus densities. It Dayton, 1985, 1974), which is a key ecosystem engineer known to has also been observed that large sea urchin aggregations generate determine the structure of its associated communities (Miller et al., spine canopies which provide refuge for juvenile sea urchins (Botsford 2018). Other authors, however, have not found L. albus to be able of et al., 1994). We hypothesize that other species of epibenthic macro- regulating the abundance of M. pyrifera (Castilla, 1985; Castilla and fauna may also benefit from this refuge, leading to richer and more Moreno, 1982; Vásquez et al., 1984; Vásquez and Buschmann, 1997) diverse communities at denser L. albus beds. Therefore, and regardless and therefore to affect, through this mechanism, local communities. of the mechanism, the intense exploitation suffered by L. albus in NWP Despite the uncertainty about the type and intensity of the inter- should have produced severe impacts upon local communities, which actions between L. albus and M. pyrifera, the high densities reached by L. remains to be evaluated. albus in NWP seem to be large enough to regulate the settlement of Human populations across NWP are small and largely concentrated different algae and/or invertebrate species, as observed in other sea towards the northern part of the Chiloé Inner Sea (Molinet et al., 2014). urchin species (Lozano-Cortés et al., 2012; Qiu et al., 2014). Greater Thus, the geographic distribution of the L. albus fishing effort is highly

410 C. Contreras, et al. Estuarine, Coastal and Shelf Science 219 (2019) 409–419 uneven, tending to decrease southward. At the same time, the whole while up to two additional videos were recorded at Sites 2, 7 and 15. In NWP corresponds to a highly heterogeneous mosaic of marine and es- summary, a total of 76 video-transects were recorded between March tuarine habitats, subjected to highly variable environmental conditions, and July 2013, at depths of 2–12 m, using a submarine camera (Sea- characterized by north-south gradients of temperature, east-west gra- viewer Sea Drop Model 960) mounted downwards on a sled. The sled dients of salinity (Molinet et al., 2011, 2007) and patchy variations in was driven by a diver and towed from a vessel (RV Dr. Jürgen Winter)at − chlorophyll-a concentration (Lara et al., 2016). a nominal speed of ∼10 cm s 1. Transect position was triangulated In the present study, we evaluate the potential relationship between from vessel GPS records (Garmin GPS Map Sounder Model 420 s). While L. albus demographics and richness, diversity and species composition the camera had a visual field of ∼28 × 25 cm, the nominal transect of L. albus benthic communities across NWP. To do so, we focused on length was 40 m. To estimate the test diameter of L. albus individuals, two demographic indexes potentially affected by the L. albus fishery: the sled was equipped with a 20-cm ruler (with marks each 5 cm) and density and size-truncation. Density was selected as a suitable index to two lasers separated by 10 cm and parallel to the camera axis. Addi- measure direct grazing or trophic effects, while size truncation was tional information regarding sampling methodology may be found at selected as a proxy for the recent level of exploitation (review of in- Molinet et al. (2016). dicators used in fisheries by Miethe et al., 2016) and its related indirect Video-transect images were analyzed to identify epibenthic organ- and direct effects, such as habitat perturbation and/or incidental re- isms at the lowest possible taxonomic level. Although this identification moval of other species. The large variability in temperature, salinity level ranged from phylum to species, we will make “taxa composition” and chlorophyll-a concentration that characterizes the NWP may affect equivalent to “species composition” hereafter to facilitate reading community structures through direct physiological mechanisms, throughout the text. Taxonomic identification was mainly carried out leading to differential responses in bioenergetics, behaviour or survival using Häussermann and Försterra (2009)´s illustrated guide, followed among species, as well as to be proxies for other correlated oceano- by consultation to local experts (V. Häussermann and others) when graphic processes, such as larval retention or local productivity af- needed. Individual counts were recorded for each species whenever fecting benthic communities (Broitman et al., 2001; Cattaneo-Vietti possible. Otherwise, only presence was registered. The number and et al., 1999; Hillebrand, 2004), Thus, in the present work we assess and diameter of L. albus individuals recorded in the videos were registered try to separate the potential effects of these environmental variables and the substrate was classified into three categories (sand, gravel and upon community responses from those that could be attributed to rock), and their combinations. Given camera resolution and overall fishery induced changes in L. albus demographics. methodological limitations, the study was restricted to epibenthic fauna of body size ≥10 mm. 2. Materials and methods A total of 57,100 individuals were identified to different taxonomic levels, from which richness, diversity indexes and species composition 2.1. Study area were computed for each transect and substrate-type (within transects). Species richness was corrected by rarefaction (Hurlbert, 1971), using a The study was carried out in NWP (Fig. 1), in an area located be- standardized sample size of ten individuals, which excluded the smal- tween 41°40′ and 45°44′S and between 72°32′ and 74°52′W. The NWP lest 25% of the samples. Diversity was measured through the non- region is constituted by an insular (western) section and a continental- parametric Simpson's index (Simpson, 1949) and the parametric Fish- Andean (eastern) section, separated by multiple gulfs, sounds, fjords er's alpha index (Fisher et al., 1943). To increase the intuitiveness of the and channels (Soto, 2009). The insular section is constituted by low Simpson's index value (obtaining greater values when the sample di- height islands, archipelagos and channels, where the main geographic versity is greater), it was expressed as 1-D (Magurran, 2004). To esti- milestone is the Chiloé Island (41°47′S-43°28′S), separated from the mate Fisher's alpha index only samples with at least one species with continent in its northern edge by the Chacao Channel (∼41°47′S). abundance > 1 were considered, excluding 23.3% of the samples. Further south, separated from the Chiloé Island by the Guafo Entrance These three indexes were calculated considering only quantifiable or- (∼43°35′S), is the Chonos Archipelago (43°50′S-45°45′S), constituted ganisms and were restricted to those samples exhibiting a positive by a set of low height islands. The continental section of the NWP re- presence of epibenthic macrofauna (87.9% of video frames). gion is constituted by the Andes Mountain Range, characterized by the presence of highly stratified fjords and channels exhibiting low salinity 2.3. Loxechinus albus demographic variability at their superficial layers. Between the insular and the continental sections, there are three main micro-basins, the Reloncaví Sound Two types of demographic indexes were considered as potential (∼41°40′S), the Gulf of Ancud (∼42°10′S) and the Gulf of Corcovado explanatory variables for species richness, diversity and species com- (∼43°30′S), all which constitute the Chiloé Inner Sea. The gulfs of position of L. albus benthic communities: mean density and size-trun- Ancud and Corcovado are separated by the Desertores Sill Constriction cation. Mean density of L. albus corresponded to the number of in- (∼42°42′S), which limits water exchange and circulation between these dividuals counted at each frame, divided by its nominal view-field two micro-basins (Sievers and Silva, 2006). surface area (0.07 m2), averaged by video-transect and substrate-type. Sampling was carried out at 22 L. albus beds from NWP (Fig. 1), all The size truncation index corresponded to the average test diameter of selected considering reports from local divers, historical fishery records the largest 5% of the sample (Lmax5). This truncation size index was and the experience of the team working in the study area (Molinet selected among several others (comparisons not shown) because prac- et al., 2016). Due to adverse meteorological conditions in the area, tical (lower AIC for most responses) and theoretical reasons. Since this southernmost sites (ID 20–22, Fig. 1) were sampled considering only index is based only on the right side of the size distribution, it is less protected locations. No sites were selected at the continental section of affected by stochasticity in recruitment variability (Lmax5; Miethe the NWP region where L. albus is present, but at very low densities of no et al., 2016). commercial relevance. 2.4. Environmental covariates 2.2. Video-transect recording and analysis Considering most population and community responses of benthic Sampling was based upon video-transects primarily aimed to esti- macrofauna to environmental variability occur in a multi-year scale, a mate L. albus density (Molinet et al., 2016). Three video-transects were compilation of available databases containing NWP environmental data targeted per site. However, due to logistic difficulties, just two video during the 11 years prior to the survey (2003–2013) was performed. transects were recorded at Sites 6, 19 and 22 (numeration from Fig. 1), Reported CTD data of temperature and salinity at 12-m (depth limit of

411 C. Contreras, et al. Estuarine, Coastal and Shelf Science 219 (2019) 409–419 our sampled L. albus benthic communities), were obtained from several fitting a GAMM model with no smoothed terms in gamm4, would be oceanographic cruises and surveys carried out in the area (information equivalent to fitting a Linear Mixed Model (LMM) with lme4. Assump- about oceanographic cruises may be found in Table A1). Chlorophyll-a tions of normality and homoscedasticity were graphically evaluated. data was obtained from the Harmful Algal Bloom Monitoring Program For Simpson's index, there was no evidence to reject these assumptions, of the Chilean Fisheries Institute (IFOP). This chlorophyll-a data cor- while for rarified richness and Fisher's alpha index a logarithmic responded to monthly in situ measurements of chlorophyll-a con- transformation was required. The analyses of variance for richness and centration at 0–10 m depth, only available for the years 2006–2010. In diversity models were performed following a type-II marginal ANOVA, the case of temperature and salinity, to compensate for unequal sam- based on likelihood ratio tests (Fox and Weisberg, 2011). pling through the year, data from all years was first averaged and in- The effects of demographic indexes and environmental covariates terpolated on a seasonal basis and then averaged across seasons. All upon species composition were evaluated by permutational analysis of datasets were interpolated through an inverse distance weighting variance, PERMANOVA (Anderson and Walsh, 2013). In these species method (Shepard, 1968), with a resolution of 2 × 2 km2, using the R composition models, temperature, salinity, chlorophyll-a concentra- package ipdw (Stachelek, 2017) and rasterized using the R package tion, substrate-type and video-transect ID were included as covariates. rgdal (Bivand et al., 2014). First-order interactions between demographic indexes showed no significant effects upon species composition and were excluded from final 2.5. Geographic variability models. To represent species composition data a constrained analysis of proximities (CAP; Oksanen et al., 2018), using Bray-Curtis dissimilarity, We acknowledged that relationships potentially found between L. was performed. Here the relative match between sampling zones, and albus demographic indexes, environmental covariates and observed the multivariate ordination defined by species composition (con- community responses (species richness, diversity and species compo- strained by L. albus demographic indexes and environmental covari- sition) could have just resulted from spatial correlation among ex- ates) was explored graphically. planatory and response variables, caused by other (unknown) under- The degree of support given by the data to selected demographic- lying regional-scale gradients. Although causality could not be directly environmental models, was compared against null and purely geo- tested, we aimed to verify the strength of the relationships we found by graphic models using Akaike (1974)'s information criterium corrected comparing their corresponding explanatory models against null models by small sample size (Symonds and Moussalli, 2011). Thereafter, we and alternative ones based only on geographic variables. Thus, com- used the AICc weights or ‘model probabilities’ to evaluate the prob- munity variables were modeled as responses to site latitude and/or ability that each model selected by AICc was the most informative one longitude, and to a zoning scheme defined considering local oceano- for each community response (Burnham and Anderson, 2003). Simi- graphy and geographic proximity among sites. larly, we selected the most informative geographic model (latitude and/ The zoning scheme was based on oceanographic criteria and geo- or longitude or zoning scheme) using AICc. graphic proximity among sites. An east-west division has previously For richness and diversity indexes, AICc values were obtained di- been proposed by Försterra (2009), who found important longitudinal rectly from the respective GAMM models. In the case of species com- changes in species composition and environmental conditions for this position data, to obtain AICc values, they were fitted to multinomial area. This author also proposed to separate the Chiloé Inner Sea from logit models using Begg and Gray (1984)'s approach. This approach fits the Chonos Archipelago. In addition, we also decided to split this inner S-1 Generalized Linear Mixed Models (binomial distribution, logit link sea by the Desertores Sill Constriction, which is frequently referred as a function), where S is the number of species evaluated. Each of these natural barrier to water exchange and circulation in Northwest Pata- models corresponds to the ratio between the abundance of each species gonia (Sievers and Silva, 2006; Silva et al., 2009; Silva and Vargas, over the abundance of Arbacia dufresnii, selected as reference species 2014). Thus, study sites were divided into five sampling zones (Fig. 1). since it was the most abundant one across the whole study area. The The first zone included the two oceanic sites located at the Chacao overall AICc value of the multinomial logit model was calculated by Channel (ID 1–2). The second zone included all inner sites located north summing the AICc values of all S-1 binomial models. To conduct this or at the Desertores Sill Constriction (ID 3–9). The third zone was analysis, only the 15 species present in > 7 video transects were con- constituted by sites located at the Gulf of Corcovado, including two sites sidered. from southern Chiloé Inner Sea (ID 10–11) and two sites from the Given results indicating L. albus size truncation and density indexes Guaitecas Archipelago (ID 12–13). The fourth and fifth zones included affected species richness, diversity and species composition, we devel- the sites located at the inner (ID 16–19) and outer Chonos Archipelago oped an additional analysis aimed to evaluate correlation between (ID 14–15, 20–22), respectively. species abundance and L. albus demographic indexes. To do so, we first removed environmental effects by fitting binomial GAMMs where the 2.6. Statistical analyses relative abundance (species count/total count) of each species was explained as a function of temperature, salinity, chlorophyll-a and Species richness and diversity indexes were analyzed using substrate type. Then we assessed the non-parametric Spearman's cor- Generalized Additive Mixed Models (GAMM), following Chen (2000). relation between the residuals from each of these models and both This approach fits models which are analogous to traditional linear demographic indexes. Only nine taxa exhibiting positive count means mixed models (Searle, 1987), but use smoothed terms to account for in ≥3 video-transects were considered for this analysis. nonlinear relations between response and explanatory variables. Se- parate GAMMs were fitted for each response. In all models, tempera- 3. Results ture, salinity and chlorophyll-a concentration were included as covariates and video-transect ID as a random factor. Substrate-type was 3.1. Overall demographic and environmental variability also included as a covariate, however it had no significant effect on richness and both diversity indices, so that it was finally excluded from The density of L. albus beds presented great variability among sites, − richness and diversity models. First-order interactions between demo- across the study area, with mean values ranging from 3.0 ind·m 2 to − graphic indexes were tested too, however they had no signifie cant ffect 36.7 ind·m 2 (additional information regarding L. albus beds may be on the richness and diversity indices, so that they were not included in found at Table A2). The highest mean densities were observed in final models. All models were fitted using the R package gamm4 (Wood northern sites from the outer Chonos Archipelago (Sites 14, 15), while and Scheipl, 2017), which uses the fitting functions of mixed linear the lowest density values were observed in two sites located at the inner models provided by the R package lme4 (Bates et al., 2014). In fact, Chonos Archipelago (Sites 17, 19). The index Lmax5 also varied greatly

412 C. Contreras, et al. Estuarine, Coastal and Shelf Science 219 (2019) 409–419

Fig. 2. Interpolations of eleven-year (2003–2013) seasonal average 12-m depth temperature (°C) and salinity and five-year (2006–2010) monthly average 0–10-m − depth chlorophyll-a concentration (mg m 3) in Northwest Patagonia. Data are from a compilation of environmental datasets (Table A1). across the study area (Table A2), ranging from 41.0 mm to 79.2 mm. The highest Lmax5 values were observed in sites located in the Gulf of Corcovado (Site 13), the inner (Site17) and the outer (Sites 20 and 22) Chonos Archipelago, while the lowest Lmax5 values were observed at the Chiloé Inner Sea (Sites 7–9). A southward decreasing gradient of temperature was observed across the study area (Fig. 2A), with the lowest temperature values (10.1–10.6 °C) found in sites from the inner Chonos Archipelago (Sites 14, 16, 17, 19) and the highest (11.6 °C) at the Chacao Channel (Sites 1, 2). Salinity presented an important variability across the study area (Fig. 2B), with 12-m salinity values ranging from 30.9 to 33.0. The sites with the lowest salinity were found at the outer Chonos Archipelago (Sites 21, 22), while the highest salinity values occurred at the Gulf of Corcovado (Sites 10, 11). The Chlorophyll-a concentration also presented an important variability across the study area (Fig. 2C), with − values ranging from 0.66 to 3.17 mg m 3. In general, the lowest values were observed at the Chiloé Inner Sea (Sites 9, 11), while the highest mean chlorophyll-a concentrations were observed at the outer Chonos Archipelago (Sites 20, 21, 22). Fig. 3. Spatial patterns of rarified species richness of Loxechinus albus benthic communities in Northwest Patagonia (A) and its relationship with two demographic indexes of the L. albus beds: density (B) and average test diameter of the 3.2. Epibenthic macrofauna response patterns largest 5% (C). Grey lines in B and C represent the predictions of generalized additive mixed models (GAMM) and light grey areas represent the prediction's Species richness and diversity presented similar spatial patterns standard errors. across the study area (Figs. 3A, 4A and 5A). Mean rarified species richness values ranged between 1.66 and 4.63, while mean Simpson's Corynactis (f = 0.82), respectively. The two sites located at the southern and Fisher's alpha diversity indexes ranged between 0.16 and 0.72, and Gulf of Guafo (Sites 12–13) were also dominated by A. dufresnii between 0.78 and 2.81, respectively. The three indexes exhibited their (f = 0.36). This species, along with P. magellanicus, became also highest mean values at the Southern Gulf of Corcovado (Site 12 and 13) dominant taxa at the Inner Chonos Archipelago (f = 0.52–0.67). and the Outer Chonos Archipelago (Site 15) and their lowest mean Finally, at the Outer Chonos Archipelago, most sites presented high value at one site from Reloncaví Sound (Site 6). abundances of Corynactis, although some of them were rather domi- Species composition of L. albus benthic communities presented a nated by Tegula/Diloma (Site 14, f = 0.42), P. Magellanicus (Site 15, moderate variability across the study area. While some species were f = 0.37) and Actiniaria (Site 22, f = 0.47), respectively. commonly found at most study sites, such as the sea urchin Arbacia dufresnii, the sea snails of genus Tegula or Diloma, the starfish Cosmasterias lurida, limpet-like gastropods, polyplacophorans and sea 3.3. Explanatory models based upon L. albus demographic indexes and anemones of the order Actiniaria, some sites were characterized by the environmental covariates presence of just one or two highly abundant species. The two sites sampled within the Chacao Channel presented im- Rarified species richness, Simpson's diversity and Fisher's alpha di- portant differences in their species composition. While Site 2 was versity presented positive relationships (estimated values of GAMM dominated by the sea urchin Pseudechinus magellanicus, with a total models may be found at Table A3) with both L. albus density (Figs. 3B, relative abundance (f) of 0.53, Site 1 was dominated by the sea ane- 4B and 5B) and Lmax5 (Figs. 3C, 4C and 5C). Loxechinus albus density mone Antholoba achates (f = 0.83) and sea sponges of the class values were highly left-skewed with > 80% of the densities below 25 − − Demospongiae (not quantified). At the northern Chiloé Inner Sea, most ind·m 2 and two extreme values > 90 ind·m 2 (Fig. 3B). Nonetheless, sites were dominated by A. dufresnii (f = 0.61–0.87), while southern the exclusion of these two extreme values showed no effects upon sites (Sites 10 and 11), were dominated by Actiniaria (f = 0.61) and model predictions.

413 C. Contreras, et al. Estuarine, Coastal and Shelf Science 219 (2019) 409–419

Table 2 PERMANOVA results assessing the eﬀects of Loxechinus albus demographic in- − dexes: density (ind·m 2) and test diameter (mm) of the largest 5% (Lmax5), and environmental covariates: temperature (°C), salinity and chlorophyll-a con- − centration (mg·m 3), on the species composition of L. albus benthic communities in Northwest Patagonia. Bold font is used for signiﬁcant values (p < 0.05).

Eﬀect Degrees of Sum of Mean FR2 Pr > F freedom squares squares

Density 1 0.501 0.501 2.614 0.012 0.002 Lmax5 1 1.018 1.018 5.313 0.024 0.001

Temperature 1 1.635 1.635 8.533 0.039 0.001 Salinity 1 1.203 1.203 6.279 0.029 0.001 Chlorophyll-a 1 1.518 1.518 7.921 0.037 0.001

Substrate-type 5 2.195 0.439 2.291 0.053 0.001

Site 18 14.309 0.795 4.148 0.344 0.001 Site/video 43 10.960 0.255 1.330 0.264 0.001 Fig. 4. Spatial patterns of diversity, expressed through Simpson's index, of Residuals 43 8.241 0.192 0.198 Loxechinus albus benthic communities in Northwest Patagonia (A) and its re- Total 114 41.581 1.000 lationship with two demographic indexes of the L. albus beds: density (B) and average test diameter of the largest 5% (C). Grey lines in B and C represent the predictions of generalized additive mixed models (GAMM) and light grey areas Loxechinus albus density (p < 0.05) and Lmax5 (p < 0.01) were represent the prediction's standard errors. found to have significant effects upon species richness (Table 1), as well as the environmental covariate temperature (p < 0.001). Lmax5 was also found to have a significant effect upon both Simpson's diversity (p < 0.01) and Fisher's alpha diversity (p < 0.05), while L. albus density showed significant effects only on Fisher's alpha diversity. Both diversity indices were significantly affected by temperature (p < 0.005 for Simpson's diversity and p < 0.001 for Fisher's alpha diversity) and salinity (p < 0.05 for Simpson's diversity and p < 0.01 for Fisher's alpha diversity). Conversely, any of them was affected by chlorophyll-a concentration. Loxechinus albus density (p < 0.005) and Lmax5 (p < 0.005) were found to have significant effects upon species composition (Table 2), as well as the three environmental covariates: temperature (p < 0.005), salinity (p < 0.005) and chlorophyll-a concentration (p < 0.005). Contrary to richness and diversity models, substrate-type also showed to have a significant effect (p < 0.005) upon species composition. Correlation analyses aimed to assess the relationship between species abundance and L. albus demographic indexes based upon residuals for environmental GAMMs (Fig. 6) showed significant positive correlations between Lmax5 and two species: A. achates and M. gregaria,as Fig. 5. Spatial patterns of diversity, expressed through Fisher's alpha index, of well as a significant negative correlation with A. dufresnii. Density of L. Loxechinus albus benthic communities in Northwest Patagonia (A) and its re- albus, on the other hand, was found to be negatively correlated with lationship with two demographic indexes of the L. albus beds: density (B) and Corynactis and M. gregaria. average test diameter of the largest 5% (C). Grey lines in B and C represent the predictions of generalized additive mixed models (GAMM) and light grey areas represent the prediction's standard errors. 3.4. Explanatory models based upon geographic variables

The single most informative geographic variable selected to explain observed variability in both species richness and Simpson's diversity

Table 1 Results of type-II marginal ANOVA based on likelihood ratio for richness and diversity of Loxechinus albus benthic communities in Northwest Patagonia. Richness was − rariﬁed, and diversity is expressed through Simpson's index and Fisher's alpha index. Explanatory variables include L. albus demographic indexes – density (ind·m 2) − and test diameter (mm) of the largest 5% (Lmax5) – and environmental covariates – temperature (°C), salinity and chlorophyll-a concentration (mg m 3). Bold font is used for signiﬁcant values (p < 0.05).

df Rariﬁed richness Simpson's index Fisher's alpha index

Chisq Pr(> Chisq) Chisq Pr(> Chisq) Chisq Pr(> Chisq)

Density 1 4.381 0.036 3.535 0.060 4.797 0.029 Lmax5 1 7.195 0.007 7.467 0.006 4.736 0.030 Temperature 1 11.569 < 0.001 9.140 0.003 14.213 < 0.001 Salinity 1 0.904 0.342 2.996 0.083 7.759 0.005 Chlorophyll-a 1 0.582 0.445 1.600 0.206 0.246 0.620

414 C. Contreras, et al. Estuarine, Coastal and Shelf Science 219 (2019) 409–419

Fig. 7. Constrained analysis of proximities (CAP) of the species composition of Loxechinus albus benthic communities in Northwest Patagonia. Symbols represent different zones inside the study area. Density: Average L. albus density − Fig. 6. Spearman correlations between Loxechinus albus demographic variables (ind·m 2), Lmax5: test diameter (mm) of the largest 5%, Temp: annual 12-m (Lmax5 and density) and residuals from binomial Generalized Additive Mixed depth temperature, Sal: annual 12-m depth salinity, Chl: annual surface Models (GAMMs) fit to remove environmental effects (temperature, salinity, chlorophyll-a concentration. chlorophyll-a and substrate type) upon the relative abundance (species count/ total count) of species appearing in video-transects. Filled bars indicate sig- 4. Discussion nificant correlations (p < 0.05). Our results indicate that richness, diversity and species composition was latitude. In the case of Fisher's alpha diversity, the most in- of L. albus benthic communities were affected by both L. albus size formative geographic variable corresponded to sampling zone, while truncation indexes, as well as by all environmental covariates. Density for species composition, the most informative geographic model in- of L. albus was also shown to make some lower but still significant cluded both latitude and longitude as explanatory variables. contribution to explain the richness and species composition of the PERMANOVA analysis showed that only 19.4% of the total variance studied communities. These results suggest this fishery affects not only observed in species composition was explained by L. albus demographic L. albus but also its associated benthic communities. Therefore, we indexes, environmental covariates and substrate-type (Table 2). As believe our results highlight the importance of adopting a more integral much as 60.8% of the total variance corresponded to overall differences approach, such as EAF (FAO, 2003), to assess the impact and to achieve among sites and video-transects within sites. CAP sites ordination a truly sustainable management of benthic fishery resources like L. showed a relative match to our sampling zones, with clear segregation albus. among the Chacao Channel, the Northern Chiloé Inner Sea and the Gulf Assuming the size truncation index Lmax5 is an adequate proxy for of Corcovado (Fig. 7). The Outer Chonos Archipelago, on the other exploitation intensity (Miethe et al., 2016), our results indicate a ne- hand, showed great overlapping with the Gulf of Corcovado, while the gative relationship existed between recent exploitation level and both Inner Chonos Archipelago overlapped partially with both the Outer species richness and diversity. The mechanisms behind this negative Chonos Archipelago and the Inner Sea of Chiloé. While both PERMA- relationship remain, however, unclear and deserve further investiga- NOVA and CAP analyses suggested that environmental covariates were tion. No by-catch, mechanical damage or other direct effects of diving more important than demographic variables to explain variability in fisheries upon L. albus benthic communities have been reported in this species composition among sites, the CAP analysis showed that the size area or elsewhere. Therefore, we speculate that indirect biological ef- truncation index Lmax5 was an important variable separating the fects related to fishery induced changes in L. albus size distribution and/ Northern Chiloé Inner Sea and the Chacao Channel sites from those or density may be more important than direct ones. While relatively located in the Gulf of Corcovado and the Outer Chonos Archipelago high (and significant) correlations found between Lmax5 and both A. (Fig. 7). achates and M. gregaria abundances could be related to the trophic role attributed to (larger) L. albus anchoring and shredding drifting macroalgae, its negative correlation with the sea urchin A dufresnii could be 3.5. Comparison of models related to direct interference or competition. The positive relationships found between L. albus density and Models based upon a combination of L. albus demographic indexes community responses such as richness and diversity disagree with most and environmental covariates resulted more informative than geo- observations from more temperate regions, where sites with higher graphic and null models for species richness, diversity and species densities of sea urchins tend to present less diverse benthic commu- composition (Table 3). All these demographic-environmental models nities, which has been related to increased grazing of macroalgae that exhibited very high probabilities of being more informative than geo- serve as refuge, habitat or food for other benthic species (Estes et al., graphic ones, with AICc weights = 1 for richness, Fisher's alpha di- 1978; Lawrence, 1975; Wright et al., 2005). Our results showed density versity and species composition and AICc weight = 0.78 for Simpson's of L. albus was negatively correlated with the colonial anthozoan Cor- index. ynactis and the squat lobster M. gregaria. While the first relationship

415 C. Contreras, et al. Estuarine, Coastal and Shelf Science 219 (2019) 409–419

Table 3 Candidate models explaining richness, diversity and species composition of Loxechinus albus benthic communities in Northwest Patagonia. Demographic models include density and size structure of L. albus beds as explanatory variables and temperature, salinity and chlorophyll-a concentration as environmental covariates. Geographic models include geographic coordinates or a proposed zoning scheme as explanatory variables. k: number of parameters in the model, AICc: Akaike information criterion corrected by small sample size, ΔAICci: AICci – min(AICc), w: AICc weight of the model, LL: Log-likelihood of each model.

Response variable Model k AICc ΔAICc w LL

Rariﬁed richess Demographic 8 333.0 0 1 −157.8 Geographic 4 364.6 39.7 0 −178.1 Null 3 382.9 58.0 0 −188.3

Simpson's index Demographic 8 −61.01 0 0.78 39.2 Geographic 7 −58.48 0.22 0.22 36.7 Null 3 −50.32 10.69 0 28.3

Fisher's alpha index Demographic 8 195.7 0 1 −89.0 Geographic 7 219.8 24.2 0 −102.3 Null 3 235.8 40.1 0 −114.8

Species composition Demographic 168 6120.6 0 1 −2875.6 Geographic 126 6315.7 195.1 0 −3022.4 Null 28 7561.9 1441.3 0 −3752.3 could be related to direct grazing effects upon Corynactis recruits, the Nonetheless, this methodology does not enable the identification of all second should be related to some kind of competition or physical in- organisms until low taxonomic levels. Therefore, rarified richness and terference. Overall, our results make evident the need to clarify the still diversity indexes were certainly underestimated. Given that, the in- unclear role of L. albus structuring benthic communities, particularly in dexes reported on the present study should not be compared with in- NWP (Buschmann et al., 2004; Castilla, 1985; Castilla and Moreno, dexes calculated using other methodologies and/or from different study 1982; Dayton, 1985, 1974; Vásquez et al., 1984; Vásquez and areas. Following a snapshot survey approach, the present study did not Buschmann, 1997). consider any temporal variability in L. albus populations and their as- In order to clarify the potential role of L. albus structuring NWP sociated communities, however, since all videos were recorded between benthic communities, we suggest directing further research to test some March and July (fall-winter) 2013, no major confounding inter-annual of the following hypotheses: i) enhanced grazing by L. albus releases or inter-seasonal effects are expected. and/or improves the quality of settling substrates for non-dominant The benthic systems from the NWP are still poorly studied species; ii) given L. albus role transforming drifting brown macroalgae (Häussermann and Försterra, 2009), however these ecosystems are al- into particulate organic matter, higher L. albus densities imply greater ready exposed to multiple stressors, including fisheries and aquaculture availability of energy for benthic filter-feeders and suspensivorous (Försterra, 2009; Niklitschek et al., 2013). Our results indicate that (Moreno et al., 2018); iii) denser sea urchin aggregations generate commercial exploitation of L. albus, besides having a direct effect on its denser spine canopies that provide additional refuge for juvenile stages target species, might also have an indirect negative effect reducing (Botsford et al., 1994); iv) given its ontogenetic changes in diet species richness and diversity in associated benthic communities. The (González et al., 2008), fishery induced changes in L. albus size-struc- magnitude and direction of these potential effects must be investigated ture affects community responses to its grazing effects. further and considered for managing and exploiting fishing beds lo- The three environmental covariates we studied showed significant cated at vulnerable habitats and/or essential habitats for vulnerable effects upon richness, diversity and species composition of L. albus species. Unfortunately, these habitats are not properly identified and benthic communities. These results highlight the importance of con- lack of any protection within NWP, where there is only one (small) sidering processes operating at different spatial scales, especially in marine protected area up to date. Within this context of limited highly variable environments as NWP. Since no causal relations be- knowledge, growing exploitation and lack of protection (Molinet et al., tween environmental variables and community responses can be es- 2019), we consider our results are an additional argument supporting tablished at this point, additional research and manipulative experi- the urgent need of creating a network of marine protected areas mentation are needed to enhance our understanding about benthic (Häussermann and Försterra, 2007; Outeiro et al., 2015) able to re- community responses to environmental variability in the NWP. present and protect the NWP biotopes. Although a fraction of the variability observed in the attributes that we assessed in L. albus benthic communities was explained by their Declarations of interest geographic distribution across different zoning schemes, geographic models resulted less informative than alternative models based upon L. None. albus demographic and environmental covariates. Nonetheless, it must be considered that L. albus demographic indexes and environmental Acknowledgements variables present latitudinal gradients, whose effects are partially correlated and, therefore, cannot be completely separated from simple Ours thanks to Verena Häussermann for her valuable help with the geographic descriptors. Moreover, the largest fraction of the total identification of several taxa of marine benthic fauna. We also thank the variability observed in different responses remained unexplained, in- Subsecretaría de Pesca y Acuicultura de Chile (SUBPESCA) for issuing dicating some important regional or local-scale processes or factors scientific fish collection permits. This study was funded by the Fondo de were neglected from the current study. Investigación Pesquera FIP Project (2012-14) and the Comisión From a methodological perspective, video-transect surveys had the Nacional de Investigación Científica y Tecnológica CONICYT (Beca de advantage of covering a large sea bottom area in a non-destructive way. Magíster Nacional N°22161612).

416 C. Contreras, et al. Estuarine, Coastal and Shelf Science 219 (2019) 409–419

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.ecss.2019.02.030.

Appendix

Table A1 Oceanographic cruises and expeditions carried out in Northwest Patagonia from which CTD oceanographic data were obtained. SHOA: Servicio Hidrográfico y Oceanográfico de la Armada Chilena, CIMAR: Cruceros de Investigación Marina en Áreas Remotas, IFOP: Instituto de Fomento Pesquero, FIP: Fondo de Investigación Pesquera, SUBPESCA: Subsecretaría de Pesca y Acuicultura de Chile, HAB: Harmful Algal Bloom, UdeC: Universidad de Concepción, COPAS: Centro de Investigación Oceanográfica en el Pacífico Sur-Oriental, FAP: Fondo de Administración Pesquero, FONDECYT: Fondo Nacional de Desarrollo Científico y Tecnológico, i ∼ mar: Centro de Investigación y Desarrollo en Recursos y Ambientes Costeros, UACh: Universidad Austral de Chile.

Institution Project Date Stations

SHOA CIMAR 8 I 2002/07/06–2002/07/ 32 20 IFOP FIP 2002-03 2002/09/04–2002/09/ 3 07 SHOA CIMAR 8 II 2002/11/16–2002/11/ 20 24 SHOA CIMAR 9 I 2003/08/09–2003/08/ 20 23 SHOA CIMAR 9 II 2003/11/07–2003/11/ 16 20 IFOP FIP 2004-09 2004/08/04–2004/08/ 3 08 SHOA CIMAR 10 I 2004/08/21–2004/08/ 50 31 SHOA CIMAR 10 II 2004/11/12–2004/11/ 43 23 IFOP FIP 2005-05 2005/03/19–2005/08/ 3 15 SHOA CIMAR 11 II 2005/11/12–2005/11/ 70 21 UACh SUBPESCA 2006-98 2006/04/28–2006/05/ 18 12 IFOP Chilean HAB Monitoring 2006/05/03–2010/12/ 121 Program 28 SHOA CIMAR 12 I 2006/07/10–2006/07/ 5 15 SHOA CIMAR 12 II 2006/11/04–2006/11/ 36 12 UACh FIP 2007-05 2008/04/21–2008/10/ 42 15 UdeC COPAS 2008 2008/08/02–2008/08/ 9 04 UdeC COPAS 2009 2009/08/02–2009/08/ 7 06 UdeC FAP-Sprattus 2010/01/15–2011/01/ 52 22 UdeC COPAS 2010 2010/08/01–2010/08/ 7 06 IFOP FONDECYT 1111006 2011/08/24–2011/08/ 2 27 SHOA CIMAR 18 2012/06/17–2012/06/ 3 19 i ∼ mar-IFOP FONDECYT 1111006 2012/08/04–2012/08/ 2 12 i ∼ mar-UACh FONDECYT 1111006 2012/11/04–2012/11/ 4 06 i ∼ mar-UdeC FIP 2012-15 2013/10/05–2013/10/ 7 07

Table A2 Loxechinus albus mean demographic indexes per sample site: density, average test diameter, median test diameter and average test diameter of the largest 5% (Lmax5).

− Site Site ID Density (ind·m 2) Average (mm) Median (mm) Lmax5 (mm) N

Carelmapu 1 7.1 40.2 41.5 56.4 263 Caulín 2 3.2 46.7 46.4 64.4 107 Quenu Island 3 19.7 35.1 34.6 53.1 379 Tautil Strait 4 13.0 39.7 38.9 55.6 165 (continued on next page)

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Table A2 (continued)

− Site Site ID Density (ind·m 2) Average (mm) Median (mm) Lmax5 (mm) N

East Guar Island 5 14.9 36.7 36.2 56.2 225 South Guar Island 6 12.9 29.9 27.6 50.3 69 Point Pájaros 7 29.1 19.3 16.9 42.8 1782 Chincui Shoal 8 20.2 24.8 24.7 38.3 604 Nayahue Island 9 14.3 26.4 25.8 45.6 318 Point Paula 10 6.5 37.2 36.0 55.7 112 Point Boigue 11 27.8 33.1 31.9 52.2 1048 Westhoﬀ Island 12 12.9 42.2 41.7 68.0 379 Leucayec Island 13 17.8 51.8 54.0 79.2 326 Erizo Islet 14 36.7 36.2 36.4 53.7 1704 Midhurst Island 15 32.9 47.0 46.3 69.6 738 North Skorpios Channel 16 16.7 35.1 33.0 67.8 295 South Skorpios Channel 17 2.8 54.1 55.7 76.7 107 Tahuenahuec Island 18 22.8 40.6 38.7 65.5 420 Point Nicolas 19 3.0 30.5 27.5 41.0 22 Stokes Island 20 21.6 50.0 50.1 74.0 414 Rowlett Island 21 7.7 45.4 45.4 55.7 92 Goñi Channel 22 13.2 47.5 47.4 73.6 94

Table A3 Estimated values and standard errors (SE) of the ﬁxed eﬀects of GAMM models used to explain the richness and diversity of Loxechinus albus benthic communities in Northwest Patagonia.

Variable Rariﬁed richness Simpson's index Fisher's Alpha index

Estimate SE Estimate SE Estimate SE

Intercept 0.662 0.139 0.224 0.082 −0.016 0.184 Density 0.004 0.002 0.002 0.001 0.005 0.002 Lmax5 0.006 0.002 0.004 0.001 0.006 0.003 Temperature −0.136 0.040 −0.070 0.023 −0.175 0.046 Salinity −0.051 0.005 −0.054 0.031 0.175 0.063 Chlorophyll-a −0.046 0.060 −0.044 0.035 0.034 0.070

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