Bonsai anemones: Growth suppression of sea anemones by their associated kleptoparasitic boxer crab Yisrael Schnytzer a, ⁎, Yaniv Giman a , Ilan Karplus b , Yair Achituv a a The Mina and Everard Goodman Faculty of Life Sciences, Bar Ilan University, Ramat Gan 52900, Israel b Institute of Animal Science, Agricultural Research Organization, The Volcani Center, P.O. Box 6, Bet Dagan 50250, Israel abstract article info Article history: Received 7 November 2012 Received in revised form 8 July 2013 Accepted 21 July 2013 Available online xxxx Keywords: Alicia sp. Boxer crab Growth suppression Kleptoparasitism Lybia leptochelis Sea anemone Kleptoparasitism, the theft of food, is a foraging strategy often overlooked or misinterpreted as a commensal as- sociation. Crabs of the genus Lybia, commonly known as boxer crabs, hold a pair of tiny sea anemones in their claws. The nature of this seemingly commensal association has never been tested empirically. In a laboratory study of food consumption, we show that the boxer crabs Lybia leptochelis regulate the size of their claw-held sea anemones (Alicia sp.). The anemone size is regulated by: (a) distancing the held anemones from presented food – and in the event any food particles are caught – (b) using rapid leg movements to remove most of the food captured by either anemone. Anemones removed from the crabs and grown independently underwent re- markable changes in morphology, color, and size, with over 250% expansion in pedal-disk diameter. The ultimate aim of classical kleptoparasitism is food acquisition by the pirate. We have shown a completely new role of kleptoparasitism, in which the victim is not only robbed of food, but is also regulated in size. The boxer crab thus maintains a “Bonsai” symbiont that is conveniently carried around as a tool to trap its food and provide protection. © 2013 Elsevier B.V. All rights reserved. 1. Introduction Kleptoparasitism, the theft of food collected by another individual, is one of the most widespread forms of exploitation (Barnard, 1984). It is well documented not only for birds (Barnard, 1984; Brockmann and Barnard, 1979; Furness, 1987; Yosef et al., 2011), but also for mammals (Gorman et al., 1998), fish (Dominey and Snyder, 1988), reptiles (Cooper and Perez-Mellado, 2003), a wide range of invertebrates (Fratini et al., 2011; Iyengar, 2002; Lapierre et al., 2007; Morissette and Himmelman, 2000; Vollrath, 1984) and other members of the animal kingdom (see Iyengar, 2008 for a comprehensive review). It has been shown that, if successful, kleptoparasitism is more advanta- geous than foraging or predation, often saving much time and effort (Iyengar, 2002; Morand-Ferron et al., 2007; Yosef et al., 2011). Such associations may be facultative or obligatory on the part of the kleptoparasites (Iyengar, 2008). Kleptoparasitism can also be a major driving force in the evolution of the morphology and behavior of the participants, as hosts and kleptoparasites respond to the selective forces exerted by each other (Iyengar, 2008; Tso and Severinghaus, 1998). For example, in some slave-making ant species, an extreme form of kleptoparasitism, the masters are incapable of feeding themselves and so would go extinct without slaves (Iyengar, 2008). Furthermore, when the theft of food occurs in closely-associated symbiotic species, such as spiders stealing food from other spiders, the kleptoparasite is often the smaller and more stealthful of the two species (Iyengar, 2008; Vollrath, 1984). The focus of most studies is on the kleptoparasite, and little attention is paid to the quantitative impact, in terms of food intake and growth, on the host. While such cases are limited, notable examples include kleptoparasitic snails (Iyengar, 2002, 2004; Pernet and Kohn, 1998) and spiders (Grostal and Walter, 1997), which affect to varying extents the growth of their hosts. Boxer crabs of the genus Lybia carry a pair of small sea anemones or less commonly, nudibranchs, in their claws (Baba and Noda, 1993; Karplus et al., 1998). Previous studies have suggested that the crabs use the anemones and their toxin-releasing nematocysts as a living de- terrent to predators and as a tool for obtaining food (Duerden, 1905; Karplus et al., 1998). Duerden (1905) observed that when presented with food, the crab would “rob” it from the anemone's mouth and in many cases remove all the food particles. The anemone's presumed benefit, as a primarily sessile animal, would come from the mobility the crab gives it (Duerden, 1905), giving the anemone further access to oxygen and its transport to further food sources (Karplus et al., 1998). The crab holds the anemone in highly adapted claws, which have specialized hooks that are slightly embedded in the anemone at all times (Guinot, 1976). These chelae have effectively lost their ability to function in a typical crab manner, as they are “slender and feeble — ill suited for defense, but at the same time mobile and well adapted to wield the anemones they carry” (Duerden, 1905). Indeed, there are no known instances of a Lybia crab being found without a pair of anem- ones, suggesting that this association is obligatory, at least on the part Journal of Experimental Marine Biology and Ecology 448 (2013) 265–270 ⁎ Corresponding author. Tel.: +972 3 5318030 (Office), +972 54 5420032 (Mobile). E-mail address: newsroolchy@gmail.com (Y. Schnytzer). 0022-0981/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.jembe.2013.07.011 Contents lists available at ScienceDirect Journal of Experimental Marine Biology and Ecology journal homepage: www.elsevier.com/locate/jembe