Variation in Consumer Pressure Along 2500 Km in a Major Upwelling System: Crab Predators Are More Important at Higher Latitudes
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Marine Biology (2019) 166:142 https://doi.org/10.1007/s00227-019-3587-0 ORIGINAL PAPER Variation in consumer pressure along 2500 km in a major upwelling system: crab predators are more important at higher latitudes 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 / Published online: 10 October 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 coast (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 kelp 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 crustaceans and the blenniid fsh Scartichthys spp. varied across sites. Consumption of P. laevigatus and kelp did not vary with latitude, 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. Fish 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 redundancy 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- temperatures (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 ocean. strength of consumer pressure, being higher at low than at While most previous studies confrmed higher predation high latitudes (Schemske et al. 2009). Temperature 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 Marine Biology (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 sea urchins (Tetrapygus 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 Chile (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 Meyenaster 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 Current 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 Humboldt Current System, which is characterized cancito (30°S) and Playa Blanca (28°S), which were open by high primary and secondary productivity 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 kelps 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 1 3.