Marine Biology (2019) 166:142 https://doi.org/10.1007/s00227-019-3587-0

ORIGINAL PAPER

Variation in consumer along 2500 km in a major upwelling system: crab predators are more important at higher

Catalina A. Musrri1 · Alistair G. B. Poore2 · Iván A. Hinojosa3,4 · Erasmo C. Macaya4,5,6 · Aldo S. Pacheco7 · Alejandro Pérez‑Matus8 · Oscar Pino‑Olivares1 · Nicolás Riquelme‑Pérez1 · Wolfgang B. Stotz1 · Nelson Valdivia6,9 · Vieia Villalobos1,10 · Martin Thiel1,4,11

Received: 21 January 2019 / Accepted: 10 September 2019 © Springer-Verlag GmbH Germany, part of Springer Nature 2019

Abstract Consumer pressure in benthic communities is predicted to be higher at low than at high latitudes, but support for this pat- tern has been ambiguous, especially for herbivory. To understand large-scale variation in biotic interactions, we quantify consumption (predation and herbivory) along 2500 km of the Chilean (19°S–42°S). We deployed tethering assays at ten sites with three diferent baits: the crab Petrolisthes laevigatus as living prey for predators, dried squid as dead prey for predators/scavengers, and the Lessonia spp. for herbivores. Underwater videos were used to characterize the consumer community and identify those species consuming baits. The species composition of consumers, frequency of occurrence, and maximum abundance (MaxN) of and the blenniid fsh Scartichthys spp. varied across sites. Consumption of P. laevigatus and kelp did not vary with , while squid baits were consumed more quickly at mid and high latitudes. This is likely explained by the increased occurrence of predatory crabs, which was positively correlated with consumption of squidpops after 2 h. Crabs, rather than fsh, were the principal consumers of squid baits (91% of all recorded predation events) at sites south of 30°S. and crustaceans preyed in similar proportion on P. laevigatus, with most fsh predation events at northern sites. The absence of any strong latitudinal patterns in consumption rate of tethered prey is likely due to among consumers across the latitudinal range, with crustaceans gaining in importance with increasing latitude, possibly replacing fsh as key predators.

Introduction processes and modifying consumption rates of both pred- ators and herbivores on large scales (Doney et al. 2012). Consumer pressure varies over large scales due to natural Understanding these large-scale patterns is needed to test gradients in abiotic factors including solar radiation and how consumer pressure relates to latitudinal patterns in bio- (Valentine 1983; Reynolds et al. 2018). Cur- diversity, and how the strength of top-down control may be rently available evidence suggests a latitudinal pattern in the altered in a warming . strength of consumer pressure, being higher at low than at While most previous studies confrmed higher predation high latitudes (Schemske et al. 2009). is a key pressure at low latitudes (Heck and Wilson 1987; Peterson driver of this gradient, having a strong efect on metabolic et al. 2001; Schemske et al. 2009; Freestone and Osman 2011; Freestone et al. 2011; Manyak-Davis et al. 2013; Sheppard-Brennand et al. 2017; Rodemann and Brandl Reviewed by Undisclosed experts 2017; Roslin et al. 2017; Reynolds et al. 2018) with just some exceptions (e.g., Harper and Peck 2016), evidence for Responsible Editor: P. Kraufvelin. latitudinal patterns in herbivory is mixed (Freidenburg et al. Electronic supplementary material The online version of this 2007; Poore et al. 2012; but see Longo et al. 2018). Sev- article (https​://doi.org/10.1007/s0022​7-019-3587-0) contains eral studies revealed increasing herbivore pressure at lower supplementary material, which is available to authorized users. latitudes (Pennings and Silliman 2005; Longo et al. 2014; Salazar and Marquis 2012; Baskett and Schemske 2018), * Martin Thiel [email protected] but others reported the expected relationship for some her- bivore groups only (Pennings et al. 2009), or even opposing Extended author information available on the last page of the article

Vol.:(0123456789)1 3 142 Page 2 of 17 (2019) 166:142 patterns (Anstett et al. 2014; Moreira et al. 2015). Meta- 2010; Uribe et al. 2015), or barren grounds dominated by analyses of studies that have contrasted herbivory of primary urchins ( niger) or snails (Tegula sp.) and producers across latitudes (Moles et al. 2011) and the efect covered by crustose calcareous algae (Stotz et al. 2016). of herbivore exclusion experiments on seaweeds and sea- Species composition is relatively consistent along the con- grass (Poore et al. 2012; Vergés et al. 2018) have found no tinental coast of (between 18°S and 42°S), and the evidence for latitudinal patterns in the strength of herbivory. most important predators are fshes (Ojeda et al. 2000), such In contrast, Longo et al. (2018) recently demonstrated that as Cheilodactylus variegatus, Pinguipes chilensis, Graus fsh herbivory became less prevalent at high latitudes (shift- nigra, Semicossyphus darwini and others (Pérez-Matus et al. ing to omnivory), while invertivory remained constant at all 2007), and invertebrates such as the crustaceans Romaleon latitudes. In addition to diferences among functional groups setosum (Fischer and Thatje 2008; Pacheco et al. 2013) and of consumers, the absence of a clear latitudinal pattern in Homalaspis plana (Fernández and Castilla 2000), the sea- consumer pressure could result from methodological difer- star gelatinosus (Urriago et al. 2011), Heliaster ences among studies (Anstett et al. 2016). helianthus (Gaymer and Himmelman 2008), and the mol- Several studies have contrasted consumption pressure lusc Concholepas concholepas (Dye 1991). These predators between a few sites in tropical and temperate regions (e.g., occur throughout most of the study area (Ojeda et al. 2000; Heck and Wilson 1987; Peterson et al. 2001; Pennings et al. Jesse and Stotz 2003) and infuence community structure 2009; Matassa and Trussell 2015), but the understanding of by preying on crustaceans, gastropods, bivalves and other the fuctuations in consumption intensity at mid-temperate benthic invertebrates (Pérez-Matus et al. 2012, 2017a). locations is incipient. More recent studies have used greater As subtidal hard-bottom communities are very similar numbers of sites (Harper and Peck 2016; Reynolds et al. across the Humboldt System (Aguilera et al. 2019), 2018; Longo et al. 2018) or meta-analyses (Poore et al. 2012; we hypothesize a latitudinal gradient in consumer pressure, Sheppard-Brennand et al. 2017; Vergés et al. 2018) to pro- with lower predation and herbivory pressure at higher lati- vide quantitative tests of the relationship between latitude tudes. Here, we studied latitudinal gradients in herbivore and and consumer pressure, with not all of them following the predation pressure in shallow subtidal communities, using expected latitudinal pattern (Poore et al. 2012; Harper and the same methodology over an extensive geographic range Peck 2016). To rigorously examine latitudinal patterns in in the SE Pacifc (19°S–42°S). consumer pressure without possible confounding efects, it is desirable to use the same methodology across multiple sites with similar habitat characteristics and coverage of substra- Methodology tum and organisms. The understanding of large-scale patterns in consumer Study sites pressure can also be improved by quantifying predation and herbivory simultaneously. Given that predators can con- Herbivory and predation assays were conducted at ten study trol the abundance of grazers (Manyak-Davis et al. 2013; sites along the Chilean coast from 19°S to 42°S between Haavisto and Jormalainen 2014; Miller et al. 2014; Östman November 2017 and March 2018 (see Table S1). Our study et al. 2016), variations in their abundance or feeding activ- area covered a latitudinal range of 2500 km along the con- ity could obscure any latitudinal patterns in herbivory or tinental coast of Chile (Aguilera et al. 2019), where annual even result in unexpected patterns (e.g., Rizzari et al. 2014). average sea surface temperatures range from 18 °C at low Analyzing those interactions in combination across the same latitudes (19°S) to 12 °C at high latitudes (42°S, data from latitudinal gradient seems necessary to understand poten- Bio-ORACLE, Tyberghein et al. 2012). The ten sampling tial gradients in consumer pressure and predict the outcome sites were distributed across the latitudinal gradient of of changes in temperature and species distributions (Miller the Chilean coast as evenly as possible, with distances of et al. 2014). 111–528 km between sites (Fig. 1). The Chilean coast is an ideal study system to examine The study sites were subtidal rocky habitats exposed or the above questions and to determine variation in consumer semi-exposed to wave action. Most sites were management pressure across a wide latitudinal gradient. Many species areas where only the local fshermen’s associations are and communities have extensive geographic distributions allowed to harvest assigned resources, except for Guaya- along the System, which is characterized cancito (30°S) and Playa Blanca (28°S), which were open by high primary and secondary due to intense access areas (Table S1). The macrobenthic community and year-round upwelling (Thiel et al. 2007). Subtidal habi- structure at each site was quantifed by visual estimates of tats comprise extensive rocky reefs with seaweed beds (Agu- the cover of sand, bare rocks (including rocks with encrust- ilera et al. 2019), including large such as Lessonia ing coralline algae), kelps, and understory algae on images trabeculata or Macrocystis pyrifera (Macaya and Zuccarello that were extracted from the videos recorded at each site

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Fig. 1 Study sites along the Chilean coast (squares) and reference images of subtidal locations where experiment were deployed. Map Source: ShapeFile Diva-Gis, Photo Credit: Oscar Pino-Olivares and Nicolás Riquelme-Pérez

(see below); all sites were dominated by barren grounds, sites was lower than at most other sites, except at 37°S for interspersed with kelp patches at most sites, except for Chome in southern-central Chile (Table S1). Isla Santa María (23°S) and Guayacancito (30°S, Fig. S1). During feld work, surface temperature was meas- Abundance and occurrence of consumers ured using a (model Cressi Newton) and along the latitudinal gradient visibility was determined from the boat or kayak using a Secchi disk. If the bottom was visible from the boat, water We contrasted the consumer community attracted to three depth was taken as minimum estimate of visibility. The diferent types of baits (two -based and one algal) summer temperatures during the feld assays varied from across latitudes by recording consumer activity with autono- 12 to 19 °C (Table S1). Visibility at the three northernmost mous camera systems at each site. During recent years, the

1 3 142 Page 4 of 17 Marine Biology (2019) 166:142 use of basic underwater cameras has greatly enhanced our From these observations, we calculated the species rich- understanding of the identity, behavior, and abundance of ness of all consumers and the maximum abundance (MaxN) marine consumers (e.g., Hinojosa et al. 2015; Gauf et al. as the maximum number of individuals from the same spe- 2018; Riquelme-Pérez et al. 2019), thus avoiding destructive cies seen at any counting point (Malcolm et al. 2007; Har- sampling (Malcolm et al. 2007). asti et al. 2015). To estimate residence times of consumers Our system consisted of GoPro cameras fxed to PVC during the assay, we calculated the frequency of occurrence tubes (diameter = 20 mm, length = 38 cm) with (FO) as the number of frames in which at least one indi- added aside. A foating rope was attached to the structure to vidual of each species or group appeared, divided by the keep the system upright (similar to the setup used by Mal- total number of possible frames. colm et al. 2007). This system was attached to the consump- Changes in community composition of consumers across tion trials (see below) with the camera facing the baits. The site/latitude were visualized using non-metric multidimen- consumer assays were conducted on hard bottoms of 6–10 m sional scaling (nMDS) with the Bray–Curtis dissimilarity water depth, at distances of approximately 50–300 m from metric and data standardized by total abundance per video. the shore, depending on the inclination of the slope. Deploy- The efect of latitude was tested with a one-way permuta- ment (usually between 11 and 12 am) and recovery of the tional multivariate analysis of variance (PERMANOVA) assays were done by SCUBA divers and access to assay loca- using the same community data and dissimilarity matrix. tions was by kayak (if distances to shore were < 100 m) or Both multivariate analyses were performed using the R by small boats (when > 100 m from the shore). At each site, package vegan (Oksanen et al. 2016). The contribution of fve recordings were done for each of the three bait types, individual species to the changes in community composition resulting in a total of 15 videos per site. evident on the nMDS ordination was visualized by vector From each video, we recorded the duration (min) and an overlays created in the R package ggord (Beck 2017). estimate for the bottom area ­(m2) captured by the camera Frequency of occurrence was contrasted with latitude for (measured as the area of a trapezium from the camera). For the three most abundant or frequently occurring fsh species, analyses, from the total of 118 videos, we excluded the 7 for the total number of predatory fsh, for the “rock shrimp” videos with a duration of less than 10 min (resulting from Rhynchocinetes typus, the total number of predatory crabs issues with low batteries) as these videos contained only the (carnivorous and omnivorous brachyuran crabs), the total initial phase immediately after deployment, when predators number of predatory crustaceans (carnivorous and omnivo- might still have remained in hiding due to the presence of rous crustaceans), and the species richness of fsh and crus- divers. Similarly, we excluded the 16 videos (of the remain- taceans using generalized additive mixed models (GAMM) ing 111) that captured very small areas (< 0.5 m2) of the run in the R package mgcv (Wood 2011). seafoor as the area was too small for observing large organ- isms. At one site (Chipana, 21°S), we were unable to deploy Rates of animal and algal consumption the cameras due to bad environmental conditions and strong across latitudes currents. The video duration ranged from 17.5 to 139.5 min with approximate survey areas from 0.5 m2 to 2.7 m2 per To contrast consumer pressure along the Chilean coast, video. three consumption assays were conducted at each site. Field All consumer organisms present in the videos were assays with tethered prey are often used to examine her- counted every 30 s and identifed to the lowest possible bivore (Zarco-Perello et al. 2017) and predation pressure taxonomic level, without diferentiation between size or (Dumont et al. 2011; Gutow et al. 2012; Urriago et al. 2012; life cycle stage (as in Harasti et al. 2018). There were some Ory et al. 2012; Pérez-Matus et al. 2016; Reynolds et al. individuals that were not possible to identify to species level 2018). Recently, standardized pieces of dried squid mantle due to low visibility and/or difculties for visual identif- called “squidpops” (Dufy et al. 2015) have been used suc- cation of the species. These individuals were identifed to cessfully to examine the predation rates in marine communi- the genus level. Species from the genus Scartichthys were ties (Rodemann and Brandl 2017; Gauf et al. 2018; Gusmao called Scartichthys spp., since they include S. viridis or S. et al. 2018; Rhoades et al. 2019; Ruesink et al. 2019). While gigas, of which visual diferentiation was not possible in the squidpops are a useful and standardized prey item for some occasions (see also Riquelme-Pérez et al. 2019). If a assessing relative predation rates, they are not a natural prey species appeared along the video but not in a frame (every and the response of the community and consequently the 30 s), its abundances were counted and added to the clos- consumption rates might difer from that to natural prey. est frame only once, to avoid underestimations for species Therefore, we assessed consumption rates using two animal- richness. Consumers were grouped by functional (predators, based prey types, squidpops and Petrolisthes laevigatus, a herbivores, omnivores, and planktivorous) and taxonomic common crab in habitats along the Chilean coast groups (fsh, crustaceans, , and others). (at all sites) to compare between consumption of a dead and

1 3 Marine Biology (2019) 166:142 Page 5 of 17 142 a living prey. Petrolisthes laevigatus was chosen because proportion of diferent baits consumed after 2 and 24 h, com- these crabs are easy to manipulate compared with other puting Pearson product–moment correlation coefcients, by species and porcellanid crabs are common prey of several using the rcorr function in the R package Hmisc (Harrell coastal fshes, showing high predation rates in previous teth- Jr and Dupont 2018). We also used Pearson correlation to ering experiments (Riquelme-Pérez et al. 2019). examine whether consumption at 2 h for squidpops and P. For herbivory, we used vegetative blades from two conge- laevigatus was correlated with the mean of predation (stand- neric kelp species that are present along the entire selected ardized) observed in videos at each site, to examine if the latitudinal range, Lessonia berteroana (17°S–30°S) and predation patterns recorded in the videos corresponded to Lessonia spicata (30°S–42°S) (González et al. 2012), as the consumption rates determined over a similar timescale standardized algal to compare relative herbivory rates in the feld assays. across study sites. It is important to note that consumption rates assessed through tethering assays could be afected by site-specifc variations, such as refuge availability or char- acteristic of the habitat (Aronson and Heck 1995), but these Results assays continue being a great tool to compare relative con- sumption rates across sites, and can be especially useful to Abundance and occurrence of consumers assess these rates across an extensive study area. along the latitudinal gradient At all sites, we deployed ten lines for each bait type at depths from 6 to 10 m. Squidpops (14 mm diameter) and A total of 38 species were recorded from the video surveys, living individuals of P. laevigatus (15–25 mm cephalotho- including echinoderms, crustaceans, mixinoids, fshes, and rax length) were tethered on nylon flaments (0.2 mm in cephalopods. The number of species per site varied from diameter and 50 mm long) to the lines, attaching to each 8 species at 23°S (ISM) to 16 species at 31°S (MT). At all line a total of fve baits that were separated from each other sites, predatory fshes were observed (Fig. 2), but the only by 25 cm. Non-reproductive algal blades (200 mm) were fsh species seen at all ten sites was Pinguipes chilensis. directly attached to the rope by opening a loop in the rope Carnivorous crustaceans observed in our videos included and inserting the algal blade; these were also separated from the crabs Homalaspis plana, Romaleon setosum, and Par- each other by 25 cm. For the animal prey, a SCUBA diver axanthus barbiger, the rock shrimp Rhynchocinetes typus, monitored and scored the number of baits remaining at 2 and the omnivorous crab Taliepus sp. The species composi- and 24 h after deployment (as per Dufy et al. 2015). For the tion of consumers varied signifcantly with latitude (pseudo- algae, fnal blade length and damage on the blade surface F = 15.5, df = 1.93, p < 0.001), with the most obvious dif- (e.g., presence of scrape marks by grazers) were recorded ferences between the southern sites (> 35°S) and central/ after 24 h. northern sites (~ 30°S; Fig. 3). Many diferent species con- Using video recordings, we identifed predators that were tributed to the observed shifts in community composition responsible for the consumption observed in videos. Each along the latitudinal gradient (Fig. S3). time a consumer was observed feeding on a bait in the vid- Neither the species richness of fsh nor that of crustaceans eos (reference images in Fig. S2), we recorded the iden- varied signifcantly with latitude (p = 0.47 and p = 0.08, tity of predators, the exact time, and whether the bait was respectively; Fig. S4). The average species richness of fsh consumed totally, partially, or not damaged. We considered per video (± SD) ranged from 1.15 ± 1.72 at 42°S (Pun) to predators as those species that consumed the entire bait, 5.40 ± 1.07 at 30°S (Gua). The highest species making a lethal attack on the prey (in the case of P. laeviga- richness per video (2.21 ± 1.02) was observed at 31°S (MT), tus) or consuming all the remaining part of the bait (in the and no crustaceans were recorded at 23°S (ISM; Fig. S4). case of squidpops). We considered grazers as those species The frequency of occurrence (FO) of all predatory fshes that had started to graze on a blade or consumed a part of it. and of each of the most abundant predatory fsh species The consumption rate of the animal prey was contrasted did not vary signifcantly with latitude along the Chilean across latitudes using generalized additive mixed models coast (Fig. 4, p > 0.05), except for Scartichthys spp. (Fig. 4a, as described above with separate analyses for P. laevigatus smooth term, F = 10.34, p < 0.001, R2 = 0.50). Crustacean and squidpops at each of the 2-h and 24-h time periods. The predators started to appear frequently south of 30°S and consumption rate of algae was contrasted across latitudes 31°S (Fig. 5). Latitude had a strong efect on FO of Rhyn- using a GAMM with the length of each blade consumed chocinetes typus (Fig. 5a, F = 4.42, p = 0.004, R2 = 0.20) (mm) as the dependent variable, latitude as a fxed factor, and all predatory crustaceans (Fig. 5c, F = 5.24, p = 0.04, and site and rope as random factors. R2 = 0.12), but we detected no efect on predatory crabs We tested whether there was a correlation between the alone (Fig. 5b, F = 3.75, p = 0.05). These predatory brachy- means of consumer variables (FO and MaxN) with the uran crabs reached the highest FO at MT (31°S). On the

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Fig. 2 Species and maxi- mum abundance of consum- ers observed in all videos (also including videos with durations < 10 min and areas < 0.5 m2) from each study location. Black dots indicate presence, and the size of the dot shows the maximum abun- dance (MaxN) of the respective species observed at each site. Maximum richness is the total number of species recorded per site. and crustaceans were grouped by functional group. ND—no data available for this site (for details, see “Methodology”)

other hand, Rhynchocinetes typus was abundant from 30°S of crabs at either 2 h (F = 2.52, p = 0.11) or 24 h (F = 1.22, to 33°S, principally at sites dominated by barren grounds. p = 0.19) (Fig. 6b–e). There was no clear pattern in her- MaxN of predatory fshes remained relatively similar bivory (the proportion of Lessonia blades consumed) across along this latitudinal gradient (Fig. S5). Outliers at 30°S the latitudinal range (F = 3.49, p = 0.06), with moderate to (Gua) corresponded to schools of Isacia conceptionis which low herbivory at most sites except for 23°S (ISM). passed in of the video camera. MaxN of crustaceans Consumption of squidpops at 2 h was positively cor- (Fig. S6) reached the highest values from 30°S southward. related with FO of all predatory crustaceans (r = 0.81, p = 0.009) and predatory crabs (r = 0.73, p = 0.03) and Sum Rates of animal and algal consumption MaxN of predatory crabs (r = 0.69, p = 0.04) (Table S2). across latitudes However, none of the other consumption variables (squid- pops at 24 h, P. laevigatus at 2 and 24 h, Lessonia spp.) In general, there was no consistent gradient in consumption were correlated with any of the considered FO and MaxN along the latitudinal range studied (Fig. 6a). We observed (Table S2). changes across latitude only for squidpop consumption A total of 16 species attacked or bit the baits on at least after 2 h (F = 5.89, p = 0.02, R2 = 0.07), with generally high one occasion, with 11 of them preying at least once (see consumption toward higher latitudes and peaks at central details in Table 1). Some species were commonly observed, sites. There was no efect of latitude on the consumption of but they did not seem interested in the baits (e.g., Aplodac- squidpops after 24 h (F = 0.58, p = 0.45) or the consumption tylus punctatus or Chromis crusma). Although species listed

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in Table 1 were sometimes interested in the prey items, most individuals of these species just passed in front of the cam- era without attacking the bait. We recorded 81 successful predator attacks, 25 on P. laevigatus and 56 on squidpops (Fig. 7). Crustaceans were responsible for 91% of all successful attacks observed on squidpops. Predation on P. laevigatus was by both fsh and crabs (44% and 56% of successful attacks observed, respec- tively). Most predation events were observed south of 28°S, especially for squidpops where 92% of all consumed baits were south of 30°S, mainly by crustaceans (Fig. 7). The crab Homalaspis plana preyed on the greatest num- ber of P. laevigatus, being responsible for 40% of the attacks identifed in the videos, followed by the blenny Labrisomus philippii (20% of predation). We also observed the brachy- uran crabs Taliepus sp. and Romaleon setosum and the fsh Scartichthys Calliclinus geniguttatus, Labri- Fig. 3 Community composition of consumers across latitude repre- species spp., sented by non-metric multidimensional scaling based on Bray–Curtis somus philippii, Auchenionchus variolosus, and Prolatilus dissimilarities (stress value = 0.17). There are no data for 21°S (Chi); jugularis preying on this bait. Homalaspis plana was also for details see “Methodology” the main predator of squidpops, being responsible for 53%

Fig. 4 Frequency of occurrence observed in the videos of the three the frst and third quartiles, while the bold lines in the boxes show most common predatory fsh species a Scartichthys spp., b Pinguipes the medians of FO; vertical lines denote 1.5*IQR or the interquartile chilensis, c Cheilodactylus variegatus, and d all predatory fsh (which range; dots show jittered raw data points, and dots outside the IQR includes omnivorous and carnivorous fsh). Frequency of occurrence range are outliers. The ftted line and 95% confdence intervals are is proportion of frames in which a species appeared out of the total from generalized additive mixed models when there was a signifcant number of frames examined in each video (one frame every 30 s). efect of the smooth term (latitude). ND—no data available for this Frequency of occurrence for all predatory fsh considered frames in site (for details, see “Methodology”) which at least one type of predatory fsh was observed. Boxes show

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and the seastar Meyenaster gelatinosus. Taliepus sp. was the only grazer species observed to consume Lessonia spp. in the video recordings, seen grazing on the assays at 33°S (LV), 40°S (EH) and 42°S (Pun). However, divers occasion- ally observed the sea urchin Tetrapygus niger on the blades when they recovered the assays after 24 h; there were also signs of grazing on the kelp blades after 24 h, but these did not result in length reduction of the blades. The consumption of squidpops at 2 h showed a positive correlation (r = 0.8, t = 3.5433, df = 7, p = 0.009) with preda- tion observed in videos. On the contrary, the consumption of P. laevigatus was not correlated with predation observed in videos (r = 0.4, t = 1.1387, df = 7, p = 0.3).

Discussion

Despite latitudinal patterns in the composition of consumer assemblages, there was little evidence for latitudinal varia- tion in the consumption rates of either animal prey or mac- roalgae on subtidal reefs along 2500 km in the SE Pacifc. This is likely due to functional redundancy among consum- ers, with crabs replacing fshes at higher latitudes, and high variability among sites driven by site-specifc upwelling conditions. The abundance and frequency of occurrence of fshes did not correlate with latitude, except for the blen- niid Scartichthys spp. On the contrary, the abundance of crustaceans varied with latitude, being most common at the central study sites and south of 30°S. Only the consumption of squidpops after 2 h showed some latitudinal variation, fnding a non-monotonic and multimodal pattern, with peaks at central sites, which contrasts with the pattern observed in most other studies (higher consumption at low latitudes). This largely resulted from a shift in the identity of predators, with squidpops being mostly consumed by predatory crabs whose abundance was positively correlated with consump- tion after 2 h. There was no latitudinal gradient in consump- tion of Petrolisthes laevigatus, possibly because predatory Fig. 5 Frequency of occurrence observed in the videos of crusta- fsh and crabs consumed this prey in similar proportions, ceans a Rhynchocinetes typus, b predatory crabs (which includes with more attacks by fsh at northern sites and by crusta- observed carnivorous and omnivorous brachyuran crabs), and c all ceans at southern sites. Similarly, there was no latitudinal crustaceans (which includes all observed carnivorous and omnivorous pattern in herbivory, which could be due to site-specifc vari- crustaceans). Frequency of occurrence for predatory crabs considered frames in which at least one of these species was observed. The ft- ation, predators afecting feeding rates of grazers, or because ted lines and 95% confdence intervals are from generalized additive few herbivores were observed along the latitudinal range. mixed models when there was a signifcant efect of the smooth term (latitude); ND—no data available for this site (for details, see “Meth- Patterns in composition of consumer assemblage odology” and Fig. 4) along the Chilean coast of successful attacks observed on squidpops, followed by The species composition of consumer assemblages observed the crab Taliepus sp. and the rock shrimp R. typus, which in our video surveys varied with latitude, with the two south- were responsible for 28% and 9% of all successful attacks on ernmost sites difering substantially from all others. The squidpops, respectively. Other predators included fshes such most frequently sighted fsh species across our study were as A. variolosus, Scartichthys spp., and Pinguipes chilensis, Pinguipes chilensis, Scartichthys spp., Chromis crusma,

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Fig. 6 The proportion of squidpops consumed after 2 (a) and 24 h from generalized additive mixed models when there was a signifcant (b), Petrolisthes laevigatus consumed after 2 (c) and 24 h (d), and the efect of the smooth term (latitude); for details, see “Methodology” proportion of Lessonia blade length consumed after 24 h (e) across and Fig. 4 the latitudinal range. The ftted line and 95% confdence intervals are

Aplodactylus punctatus, and Cheilodactylus variegatus, as northern-central Chile (28°S–30°S). Cheilodactylus variega- also reported by Pérez-Matus et al. (2007) for study sites tus was present only at sites north of 33°S, although its range from 18°S to 32°S (range of the study). The frst three fsh extends to 40°S (Ojeda et al. 2000). species were very abundant at most sites where they were Some fsh predators were only seen at the three south- present, especially Scartichthys spp., which were the most ernmost sites (from 37°S), in particular Patagonotothen common and abundant species at central sites (30°S–33°S), brevicauda and Bovichtus chilensis, which have narrow dis- confrming the results by Varas and Ojeda (1990) for inter- tributional ranges, and are present in southern Chile (Ojeda tidal rocky shores from the same region, and by Riquelme- et al. 2000). On the contrary, other important top fsh preda- Pérez et al. (2019) for kelp forests and barren grounds of tors were only observed at northern sites (e.g., Hemilutjanus

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Table 1 Species that attacked the tethered baits (Petrolisthes laevigatus, squidpops, and Lessonia spp.) Group Species Squidpops Petrolisthes Lessonia spp.

Carnivorous and invertivorous fshes Labrisomus philippii X XX Auchenionchus variolosus XX XX Cheilodactylus variegatus X Pinguipes chilensis XX X Prolatilus jugularis X XX Schroederichthys chilensis (Shark) X Calliclinus geniguttatus XX X Bovichtus chilensis X Omnivorous fshes Scartichthys spp. XX XX Patagonotothen brevicauda X Carnivorous crustaceans Romaleon setosum XX Rhynchocinetes typus XX Homalaspis plana XX XX Omnivorous crustaceans Taliepus sp. XX XX XX Sea stars Meyenaster gelatinosus XX Stichaster striatus X

X shows species that attacked or bit the bait in at least one occasion but did not consume the bait, and XX shows species that consumed (in the case of Lessonia spp.). or preyed on the ofered bait (did a lethal attack on the prey, in the case of P. laevigatus, or consumed all the remaining part of the bait, in the case of squidpops)

Fig. 7 Number of consumed squidpops and Petrolisthes by type of for the corresponding predator. c, d The percentage of total consumed predator (type) and percentage of consumed baits (%) related to the baits by type of predator. We considered a bait consumed when some total number of baits consumed in videos for each site (a, b). Num- predator took or ate a bait completely and it was clearly observable. bers inside each bar are the number of attacks observed at each site ND—no data available for this site (for details, see “Methodology”)

1 3 Marine Biology (2019) 166:142 Page 11 of 17 142 macrophthalmos, Paralichthys microps, Graus nigra, and more signifcant roles toward higher latitudes (Rodemann Paralabrax humeralis), and although they are present along and Brandl 2017). almost the entire latitudinal range of this study (Ojeda et al. Latitudinal variation in predation was only found for 2000), they were only observed at one or two sites dur- squidpops and not for consumption on P. laevigatus, and ing few occasions, which could be due to low abundances only when measured over a short time frame (2 h). Reynolds caused by overfshing (Godoy et al. 2010, 2016). et al. (2018) also observed contrasting predation patterns for Crustaceans were observed more commonly at sites south two diferent bait types: consumption of gastropods was very of 30°S, especially predatory crabs (from 31°S). While the low at all sites with little diferences between them, while geographic range of these consumers extends across the consumption of amphipods was higher and showed a clear entire study area (Jesse and Stotz 2003; Fischer and Thatje latitudinal pattern being higher at low latitudes. The same 2016), in this study predatory crabs were rarely or never occurred in the study of Riquelme-Pérez et al. (2019), where observed at northern sites, possibly because they are more the consumption rates of P. laevigatus were substantially common and abundant in soft-bottom habitats (Pacheco et al. higher than those on the sea urchin Tetrapygus niger; these 2013). However, these crustaceans have been exploited for diferences (Reynolds et al. 2018 and Riquelme-Pérez et al. decades without efcient regulation (Fernández and Castilla 2019) were attributed to the identity and characteristics of 2000; Thatje et al. 2008; Fischer and Thatje 2016), which predators and prey in the corresponding habitats. Our study could also be a reason for their low abundances in northern revealed similar fndings, where squidpops (basically repre- Chile. The rock shrimp Rhynchocinetes typus, an important senting carrion) attracted predators, such as Rhynchocine- prey and predator on subtidal hard bottoms (Caillaux and tes typus, which could not consume living crabs, or preda- Stotz 2003; Dumont et al. 2009; Ory et al. 2012), was the tory crabs and small fshes that are commonly attracted to only non-brachyuran crustacean observed in our videos. carrion. On the other hand, P. laevigatus attracted typical These patterns were not associated with shifts in species predators of living prey such as the fsh at the northern sites. richness, which showed minor variations, for both fsh and Using diferent prey types helps to better understand the pre- crustaceans. The species richness of fsh remained similar dation pattern on subtidal hard bottoms. along our latitudinal range as also reported by Ojeda et al. There was no latitudinal pattern in herbivore pressure, (2000) and Navarrete et al. (2014) who found species rich- which is not entirely unexpected, with evidence from mul- ness of subtidal fsh to remain almost constant up to around tiple studies and habitats showing a variety of patterns 40°S, south of where it decreases. (Pennings et al. 2009; del-Val and Armesto 2010; Poore et al. 2012; Anstett et al. 2014; Moreira et al. 2015). Those studies, however, have used a wide variety of methods to Latitudinal variation in consumption pressure quantify herbivore pressure, ranging from long-term grazer exclusion plots (that measure the net result of production There was no clear latitudinal pattern in consumption pres- minus grazing) to short-term loss of leaf tissue area, and sure and the observed shift in species composition with these diferences in methodology might explain the incon- latitude was not strongly associated with the consumption sistent patterns reported in herbivory (Anstett et al. 2016; of either animal or algal baits along ~ 2500 km of the tem- Poore et al. 2012). Here, we examined consumption on kelp perate Chilean coast. This result contrasts with most studies blades in a standardized way and within a narrow period of on geographical variation in predator–prey interactions in time, so that the infuence of confounding factors such as marine environments (Freestone et al. 2011; Manyak-Davis latitudinal variation in rates of can be et al. 2013; Sheppard-Brennand et al. 2017; Rodemann and excluded. However, our experiments are unable to rule out Brandl 2017; Reynolds et al. 2018). In particular, the fnd- the possibility that latitudinal patterns in the consumption ing of a non-monotonic and multimodal pattern, with peaks rates of individual herbivores are confounded by latitudinal in squidpop consumption at central sites, was unexpected. variation in the degree to which predators control the abun- Nevertheless, Harper and Peck (2016), using shell repair dance of herbivores (predation risk). indicators, also found a pattern in predation pressure with Patterns in herbivory could also be complicated by any peaks at central sites, which they attributed to low preda- variation in the of defensive compounds in tion in the due to biotic variables (such as size of the algal blades used (e.g., the phenol contents in kelp tis- the prey or type of predators). The pattern found is likely sues; Martínez 1996) and site-specifc conditions that can caused by increased abundances of predatory crabs at be responsible for the high site-to-site variability observed southern sites as they were responsible for most attacks on (Anstett et al. 2016). Sites with high consumption were squidpops, and their abundances were positively correlated dominated by barren grounds with the high presence of with the observed consumption pattern. This is consistent Tetrapygus niger and Tegula sp. (common grazers on Les- with the expectation that invertebrate consumers can play sonia spp.; Vásquez and Buschmann 1997; Perreault et al.

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2014) and low densities of kelps. On the contrary, high den- importance as predator in subtidal habitats (Dumont et al. sities of kelp could reduce the attractivity of the ofered algal 2011, Ory et al. 2012, Urriago et al. 2012, Riquelme-Pérez blades. The same occurs with predation, possibly infuenced et al. 2019). by the natural abundance of prey organisms at each site, and There are several other fsh species that are important predators might be less attracted to the bait at sites where consumers on hard-bottom communities, and which could alternative prey is abundant (Miller et al. 2018). Future stud- have consumed our baits, because they are known as con- ies are needed to disentangle processes that operate at broad sumers of decapod crabs (Varas and Ojeda 1990; Angel and and local scales to understand the occurrence of non-linear Ojeda 2001; Pérez-Matus et al. 2012; Cornejo-Acevedo et al. ecological latitudinal patterns. 2014). But most of them were recorded very rarely in our The fnding of no clear latitudinal pattern in consumption videos (e.g., Semicossyphus darwini and Paralabrax humer- is possibly also related to the particular conditions within alis) or were not observed at all (e.g., Nexilosus latifrons the Humboldt Current System. Most studies reporting lati- and Acanthistius pictus). This is likely because these species tudinal patterns (fnding mainly higher consumption toward are either less abundant or have narrow distribution ranges low latitudes) have been carried out in poleward-fowing, (Ojeda et al. 2000). Furthermore, piscivorous species tend to warm, western boundary currents (Heck and Wilson 1987; increase their consumer pressure in kelp forests as opposed Peterson et al. 2001; Freestone and Osman 2011; Freestone to barren grounds (Pérez-Matus et al. 2016), as top predators et al. 2011; Manyak-Davis et al. 2013; Rodemann and Brandl are facilitated in structurally complex habitats (Miller et al. 2017; Longo et al. 2018). In contrast, we assessed consumer 2018). Some local fsh species such as Aplodactylus punc- pressure in an equatorward-fowing, cool, eastern boundary tatus, Girella laevifrons, and Scartichthys spp. are known to current along the west coast of . Variation in feed on Lessonia kelps (Quijada and Caceres 2000; Angel upwelling intensity along the Chilean coast, with an oceano- and Ojeda 2001, Berrios and Vargas 2004; Cornejo-Acevedo graphic break at 30°S and more persistent and strong coastal et al. 2014; Ruz et al. 2018). Even though some particular upwelling in northern Chile (Aguilera et al. 2019), might be seaweeds often dominate in their stomach contents, as for afecting environmental variables and communities at our example Lessonia trabeculata in A. punctatus (Cáceres et al. sampling sites. Bottom-up efects might drive community 1993), it is very likely that these kelp consumers might also structure and afect the consumption pressure, with coastal feed on intertidal Lessonia species (as used herein), which upwelling modifying energy sources of the trophic webs, have lower concentrations of defensive compounds than interspecifc interactions, and abundances of consumers L. trabeculata (phlorotannins, Storz et al. 2009). Thus, we (Nielsen and Navarrete 2004; Reddin et al. 2015; Docmac consider that the probability of herbivorous fshes consum- et al. 2017; Pérez-Matus et al. 2017b). ing L. berteroana/spicata is high, making these kelp species an appropriate bait for our herbivore assays. However, they Identity of consumers: fsh and crustaceans were not observed consuming Lessonia spp. in our video recordings. This could be due to the fact that some of these The taxonomic identity of consumers was likely the most herbivores do not consume adult kelp but rather their epi- important driver of diferences in consumption among sites, phytes, and also due to the availability of alternative food, and even though we only identifed predators and herbivores including other seaweeds and small prey organisms, which during the initial hour of the assays, the data provide useful should be estimated in future studies. information about consumer species of each bait. Predators Besides fshes, crustaceans were very important consum- consuming our baits included several fsh species, which ers of our baits. Homalaspis plana was the main consumer are known to be important predators in Chilean subtidal of squidpops and an important consumer of P. laevigatus. communities. Auchenionchus variolosus, C. geniguttatus, This species inhabits soft- and hard-bottom communities and L. philippii, from the family Labrisomidae, were the (Jesse and Stotz 2003) and preys on a wide variety of marine main consumers of P. laevigatus, which is consistent with invertebrates, including crabs (Morales and Antezana 1983), previous studies that report them as common predators on as does Romaleon setosum (Cerda and Wolf 1993), which decapod crustaceans (Quijada and Caceres 2000; Angel and we also observed preying on tethered crabs. The shrimp Ojeda 2001; Berrios and Vargas 2004). On the other hand, R. typus, which is known as an important benthic predator we frequently observed Scartichthys spp. trying to prey on (Dumont et al. 2009) and scavenger (e.g., Dennenmoser and both crabs and squidpops, typically in aggregations of > 10 Thiel 2007), was observed consuming squidpops. Taliepus individuals, although species of this genus have been rec- sp. is mainly considered a herbivore, but was observed con- ognized as omnivores, which feed primarily on algae and suming all bait types (crabs, squidpops and algae), consist- only occasionally on small invertebrates (Muñoz and Ojeda ent with the fndings of Camus et al. (2008) and Jofré et al. 2000; Berrios and Vargas 2004). Other recent studies con- (2013). For omnivores such as Taliepus sp. and the blen- frmed the predation behavior of Scartichthys spp. and its niid Scartichthys spp., we might expect increased carnivory

1 3 Marine Biology (2019) 166:142 Page 13 of 17 142 toward higher latitudes due to higher energetic demands in that the observed consumption patterns are not only due to colder , as observed for fsh in the south-west Atlan- natural gradients in environmental conditions but are also tic (Longo et al. 2018). Taliepus sp. was the only species infuenced by human activities. Future studies in this system that we observed feeding on seaweeds, while several other should thus also focus on environmental variables, because invertebrate grazers (e.g., the urchins Tetrapygus niger and there are many local processes (e.g., upwelling, overfshing snails Tegula sp.) are important herbivores and very com- or establishment of management areas), which can interfere mon across the study sites (Vásquez and Buschmann 1997), with the observed pattern in consumption. This will help to but were not observed grazing in our videos. better understand the variations in the observed consumption In general, most consumption of squidpops can be attrib- along the Humboldt Current System. uted to H. plana and other decapods, whereas consumption of P. laevigatus is by fsh predators in northern Chile and by Acknowledgements We are grateful to the local fishermen who allowed us to work in their fshing areas and helped with logistics at crabs in southern Chile. In addition, predation observed in many of our study sites. We also thank Boris Lopez for his help with videos is consistent with consumption in the assays. Addi- Fig. 1 and Maria de los Angeles Gallardo for her help in identifying tional species not recorded in our videos (e.g., nocturnal some brachyuran crabs. Two anonymous reviewers provided many con- species) may also contribute to the observed consumption structive suggestions that helped to improve the original manuscript. pattern; however, with many baits already lost after 2 h, it is Author contributions MT conceived the study, with the support of unlikely that nocturnal predators play an important role in WBS, IAH, ECM, ASP, AP-M, and NV. CAM, MT, and AGBP wrote the observed consumption. the manuscript. OP-O, NR-P, and VV developed the experimental design and conducted the feld and laboratory experiments. CAM reviewed videos and organized data and together with AGBP did the Conclusion statistical analyses. All authors commented on previous versions of the manuscript and all authors read and approved the fnal version of the manuscript. The lack of any strong latitudinal patterns in consumption is likely due to the relatively similar consumer communi- Funding This study was fnanced by a FONDECYT Grant (CONI- ties and predator abundance along the Chilean coast, and CYT-FONDECYT 1161383). redundancy among consumers with crustaceans replacing Data availability The datasets during and/or analyzed during the cur- fsh toward southern sites. For fsh predators, which con- rent study are available from the corresponding author on reasonable sumed more at northern sites, there seems to be a latitudinal request. pattern in predation pressure, but the general consumption pattern is obscured by the activity and abundance of large Compliance with ethical standards crustaceans at southern sites. It thus appears that crustaceans are important predators, which drive the observed trends in Conflict of interest All authors declare that they have no conficts of predation pressure along the Chilean coast. Diferences in interest. the consumption of the baits and the predators attracted by Ethical approval This article does not contain any studies with human the diferent baits in this and in other studies (see Reynolds participants performed by any of the authors. All applicable interna- et al. 2018; Riquelme-Pérez et al. 2019) highlight the impor- tional, national, and/or institutional guidelines for the care and use of tance of prey selection for tethering studies. While squid- were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institu- pops are a standardized tool to assess predation and several tion at which the studies were conducted and ethical approval was recent studies used this bait as single prey type to measure obtained from the Comité Ético Científco de la Universidad Católica predation intensity (Rodemann and Brandl 2017; Gusmao del Norte, Sede Coquimbo (resolution 2019-4), following applicable et al. 2018; Rhoades et al. 2019; Ruesink et al. 2019), they international, national, and/or institutional guidelines for the care and use of animals. All feld surveys were conducted under the resolution can also attract predators that might not be dominant or top 2649 from the “Subsecretaría de Pesca y Acuicultura” (SUBPESCA) predators in their communities, including crustaceans and published in the “Ofcial Newspaper of Chilean Republic”, num. small fshes. 41,553 on September 2016. On the other hand, abundances of several well-known fsh predators and the lack of crustaceans at northern sites might be afected by overfshing. Commercial fshing sup- presses the abundances of species with high economic value References (Godoy et al. 2010; Fischer and Thatje 2016), which are the typical top predators in subtidal habitats of the Hum- Aguilera MA, Aburto JA, Bravo L, Broitman BR, García RA, boldt Current System (Pérez-Matus et al. 2017a). Consumer Gaymer CF, Gelcich S, López BA, Montecino V, Pauchard A, Ramos M, Rutllant JA, Sáez CA, Valdivia N, Thiel M (2019) assemblages along the Chilean coast, as in many other areas Chile: environmental status and future perspectives. In Shep- of the world, are diminished by fshing, and it is thus likely pard C (ed) World : an environmental evaluation, 2nd edn.

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Afliations

Catalina A. Musrri1 · Alistair G. B. Poore2 · Iván A. Hinojosa3,4 · Erasmo C. Macaya4,5,6 · Aldo S. Pacheco7 · Alejandro Pérez‑Matus8 · Oscar Pino‑Olivares1 · Nicolás Riquelme‑Pérez1 · Wolfgang B. Stotz1 · Nelson Valdivia6,9 · Vieia Villalobos1,10 · Martin Thiel1,4,11

1 Departamento de Biología Marina, Facultad de Ciencias del 7 Facultad de Ciencias del Mar y Recursos Biológicos, Mar, Universidad Católica del Norte, Coquimbo, Chile Instituto de Ciencias Naturales Alexander von Humboldt, Universidad de Antofagasta, Antofagasta, Chile 2 Evolution and Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University 8 Subtidal Ecology Laboratory, Estación Costera de of New South Wales, Sydney, NSW 2052, Australia Investigaciones Marinas, Facultad de Ciencias Biologicas, Pontifcia Universidad Católica de Chile, Santiago, Chile 3 Departamento de Ecología and Centro de Investigación en Biodiversidad y Ambientes Sustentables, Facultad de 9 Facultad de Ciencias, Instituto de Ciencias Marinas y Ciencias, CIBAS, Universidad Católica de la Santísima Limnológicas, Universidad Austral de Chile, Valdivia, Chile Concepción, Concepción, Chile 10 Centro de Investigación y Desarrollo Tecnológico en Algas 4 Millennium Nucleus Ecology and Sustainable Management (CIDTA), Facultad de Ciencias del Mar, Universidad of Oceanic Island (ESMOI), Coquimbo, Chile Católica del Norte, Coquimbo, Chile 5 Departamento de Oceanografía, Universidad de Concepción, 11 Centro de Estudios Avanzados en Zonas Áridas (CEAZA), Concepción, Chile Coquimbo, Chile 6 Centro FONDAP de Investigación de Dinámicas de Ecosistemas Marinos de Altas Latitudes (IDEAL), Valdivia, Chile

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