Tool Use by a Temperate Wrasse, California Sheephead Semicossyphus Pulcher

Journal of Fish Biology (2015) doi:10.1111/jfb.12856, available online at wileyonlinelibrary.com

BRIEF COMMUNICATION Tool use by a temperate wrasse, California sheephead Semicossyphus pulcher

R. P. Dunn* Department of Biology and Coastal & Marine Institute, San Diego State University, N. Life Sciences Room 102, 5500 Campanile Dr., San Diego, CA 92182, U.S.A.

(Received 19 June 2015, Accepted 2 November 2015)

Multiple individuals of a temperate reef fish species (California sheephead Semicossyphus pulcher) were observed using an anvil to crush hard-bodied invertebrate prey. Potential implications for this behaviour extend from individuals, which may experience reduced likelihood of injury and increased reproduction, to communities, which could see changes in prey abundance and size-distribution, with particularly important consequences for communities regulated by top-down processes. Until relatively recently, the use of simple tools by fishes was overlooked compared with observations of tool useby primates and birds; however, observations of tool use, and interesting foraging behaviours in general, by aquatic organisms should increase with improved underwater monitoring technology. © 2015 The Fisheries Society of the British Isles

Key words: foraging behaviour; labrid; remote underwater videography; sea urchin; Strongylocentro- tus purpuratus.

Animals must take in food to survive, and a number of remarkable foraging behaviours have evolved to deal with the various needs that foraging presents. In particular, extract- ing food once it has been located has led to the evolution of a number of interesting behaviours, including the use of tools. Originally thought to be a behaviour exclu- sive to humans, tool use has recently been observed in numerous animals, ranging from insects and crabs to birds and mammals, with primates in particular receiving much attention (Griffin, 2001). The use of tools by animals was defined as ‘[using]an external object as an extension of mouth or hand in the attainment of an immediate goal’ (Van Lawick-Goodall, 1970). This broad definition allows for manipulation of the goal, often prey, rather than only direct manipulation of the tool. This is an important distinction for fishes, as they lack the appendages needed to hold a tool. Fishes also inhabit an aquatic environment that does not lend itself to the standard use of tools due to the viscosity of water and buoyancy of many objects (Brown, 2012). Relatively few observations of the use of tools by fishes have been reported, and many of those reports describe the use of tools by individuals in the wrasse family (Labridae) (Brown, 2012). Multiple wrasse species across three phylogenetic tribes have been reported to

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© 2015 The Fisheries Society of the British Isles 2 R. P. DUNN use rocks as an anvil against which to crush their hard-bodied invertebrate prey (Cow- man et al., 2009; Brown, 2012), typically bivalves or sea urchins (Heiser, 1981; Coyer, 1995; Pasko,´ 2010; Jones et al., 2011; Bernardi, 2012). All previous reports of tool use by wrasse species have come from tropical regions or for tropical species within an aquarium setting. California sheephead Semicossyphus pulcher (Ayres 1854) are large-bodied temperate wrasse and important predators in kelp forests and on rocky reefs of southern Cali- fornia, U.S.A., and Baja California, Mexico. They are protogynous hermaphrodites, changing from female to male with accompanying morphological changes in size, colour and jaw structure (Warner, 1975). Males are generally much larger than females from the same population (Warner, 1975), although size-selective fishing can decrease the mean standard length (LS) of both sexes in addition to reducing the level of sex- ual dimorphism displayed (Hamilton et al., 2007). Warner (1975) found that coloura- tion alone is not sufficient to determine the sex of large S. pulcher, as some smaller, uniform-coloured individuals have male gonads. In this study, all individuals observed using tools were assumed to be females, as they were uniform in colour and lacked both the characteristic nuchal hump and large jaw seen in males. From June to September 2014, remote underwater video cameras were deployed during daylight hours to small experimental reefs constructed in the Point Loma kelp forest offshore of San Diego, California, U.S.A. Reefs were built at 11–13 m depth on sand patches embedded within the surrounding kelp forest, and were seeded with purple urchins Strongylocentrotus purpuratus at the beginning of each camera deployment. More than 13 h of video was collected and analysed, and of the 37 total S. purpuratus mortality events recorded, the majority involved predation by S. pulcher (c. 80%). Of these predation events, there were four instances (c. 13%) of tool use in which female S. pulcher used rocks as an anvil to crack the test of S. purpuratus [Fig. 1 and Video S1 (Supporting Information), https://goo.gl/5wpRqd]. Typically, S. pulcher extracted an urchin from the reef with its mouth [Fig. 1(a)], either from the reef surface or by excavating rocks with its mouth and then grabbing any prey sheltering underneath. This method of extraction was the same for males and females. After a prey item was extracted, a large male would simply crush the urchin in its mouth, regardless of the size of the urchin. While females were also observed crushing smaller S. purpuratus in their mouths, they were the only sex observed using an anvil to crush their prey. Generally, a female thrashed its head towards a rock while holding an urchin in its mouth, using the rock as an anvil [Fig. 1(b), (c)] as has been described for other labrids (Coyer, 1995; Jones et al., 2011; Bernardi, 2012). Once the test was cracked or broken, the S. pulcher used its mouth to manipulate the orientation of the urchin [Fig. 1(d), (e)] in order to bite down at the compromised location of the urchin test [Fig. 1(f) and Video S1 (Supporting Information)]. One S. pulcher used both a rock and the cement block anchoring the video camera during a continuous sequence in which it used an anvil nearly 10 times in <2 min. Of the four instances of tool use observed, two involved relatively large S. pulcher > ( 300 mm LS) crushing urchins that were small enough to be consumed without the aid of an anvil (c. 35 mm test diameter, DT), while the other two instances involved < > smaller S. pulcher ( 250 mm LS) crushing larger urchins ( 50 mm DT). This lack of a trend in S. pulcher size, prey size and tool use could be due to the relatively few observations available. Alternatively, this pattern could also suggest that tool use not only occurs out of necessity by smaller S. pulcher consuming larger urchins, but is also

(a) (d)

(b) (e)

Fig. 1. Female Semicossyphus pulcher using a rock as an anvil to break open a large urchin, Strongylocentrotus purpuratus.TheS. pulcher (a) picks up a S. purpuratus in its mouth from the reef, (b) carries it and hovers beside a rock and (c) violently smashes the urchin against the rock, (d) forcing the urchin loose from its mouth. The S. pulcher (e) then uses its mouth to reorient the urchin on the substratum before (f) biting it at the cracked portion of the test. See https://goo.gl/5wpRqd beginning at 3:33 mark for the complete sequence. perhaps chosen as a handling mechanism in some cases by larger S. pulcher consuming smaller urchins. While female S. pulcher commonly were seen crushing small urchins in their mouths, the use of an anvil has obvious benefits for the smaller sex of S. pulcher, including increasing the size range of consumable prey. Only one prior description of tool use by a labrid indicated the sex of the individual: a male yellowhead wrasse Halichoeres garnoti (Valenciennes 1839) at Key Largo, FL, U.S.A., that crushed a scallop (Pectinidae) against a rock (Coyer, 1995). While the observations presented here are preliminary, at first glance, they suggest that female S. pulcher are more likely to use tools than males, because no males were observed using this behaviour despite recording multiple predation events by large males. Given their greater size, male S. pulcher have larger mouths and are less gape limited than females. Males can probably also exert a stronger bite force than females, as the diet of S. pulcher generally shifts from soft-bodied to increasingly armoured prey items through ontogeny (Hobson & Chess, 2001). Thus, male S. pulcher may have the ability to crush even the largest S. purpuratus, and the sizes of urchin prey provided in these manipulative experiments may have been insufficient to require large males to usean anvil. Because of their protogynous hermaphroditic life history, it is likely that males also know how to use an anvil to crush prey. While labrids can show distinct ontogenetic shifts in behaviour (Jones, 2002), which could account for the lack of observations of male tool use in this study, the more likely explanation is that males simply did not need to use an anvil to consume the size range of urchins presented. Experiments with

© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12856 4 R. P. DUNN the larger, longer-spined red urchin Mesocentrotus franciscanus are ongoing and will provide insight on this possibility. Previous examples of anvil use by labrids have noted the use of a feeding station to which the fish repeatedly returned to crack open their prey (Pasko,´ 2010; Jones et al., 2011). In each of the observations of tool-use behaviour reported here, S. pulcher generally used the same rock multiple times, suggesting that feeding stations for tool use are common. The percentage of predation events in which an anvil was used to crack prey (13%) was not inconsequential and probably implies that tool use by S. pulcher is far more frequent than currently recognized, and is probably a common behaviour among labrids more generally. This report expands the use of tools by labrids to include a temperate species, as all previous reports describing this behaviour have come from tropical species. Whether other families of fishes show similar degrees of tool use will require continued study. These observations also offer a third example of tool use by a species in the Hypsigenyines tribe, the ancestral group within the Labridae, providing further support that this behaviour can be found in species across the evolutionary history of labrids, which spans some 50 million years and contains over 600 species in 82 genera (Cowman et al., 2009). The use of tools by fishes [other than the archerfish Toxotes chatareus (Hamilton 1822); Dill, 1977] was infrequently discussed in the scientific literature until a series of recent papers describing specific observations of wrasse using anvils (Coyer, 1995; Pasko,´ 2010; Jones et al., 2011; Bernardi, 2012), in addition to a comprehensive review of tool use by fishes (Brown, 2012). Despite the paucity of information about these behaviours, tool use probably has important implications for the biology of individuals, including avoiding injury from attempting to crush prey that is too hard or large, and increasing reproductive potential due to increased food availability. The use of tagging, in concert with large-scale underwater monitoring using videography or time-lapse photography, should provide insight on the relative frequency of tool use by fishes of various sizes and sexes as well as reveal other interesting foraging behaviours among individual fish. There are also potential community-level effects of tool useby predatory fishes, such as increased foraging breadth. By including larger prey intheir resource-base, tool-using predators could alter the size distribution of prey thereby affecting prey population level reproduction (Nakaoka, 2000) or reducing recruitment and refuge habitat (Tegner & Dayton, 1977). Sea urchins are the dominant herbivore found on rocky reefs globally (Harrold & Pearse, 1987; Steneck et al., 2002; Ling et al., 2015), and the ability of predators to regulate urchin populations in southern California, in the absence of the historical apex predator in this system, the sea otter Enhydra lutris, remains contentious (Tegner & Dayton, 1981; Cowen, 1983; Tegner & Levin, 1983; Foster et al., 2006; Halpern et al., 2006; Foster & Schiel, 2010). Given the potential importance of top-down control in determining rocky-reef community structure, the ability of predators to expand their prey base through the use of tools could have consequences for the entire rocky-reef community. As exploration of sub- tidal marine ecosystems increases and technology for remote underwater monitoring becomes more widely available, scientific understanding of important, yet generally overlooked, higher-order behaviours in aquatic species should increase.

Many divers provided vital field assistance in support of this project, but A. Harrington andM. Yeager deserve particular mention. K. Hovel, C. Brown and two anonymous reviewers provided insightful comments on the previous versions of this manuscript. The San Diego State University diving and boating programme provided research vessels and tanks. This project was funded by

© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12856 TOOL USE BY A TEMPERATE WRASSE 5 a National Science Foundation Graduate Research Fellowship (grant no. DGE-1252376) as well as the Joint Doctoral Programme in Ecology at SDSU and UC Davis. This is Contribution No. 46 of the Coastal and Marine Institute Laboratory, San Diego State University.

Supporting Information Supporting Information may be found in the online version of this paper: Appendix S1. A Semicossyphus pulcher uses multiple rocks as an anvil to crack the test of a small purple urchin Strongylocentrotus purpuratus.

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