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Social Recognition in Amphipods: an Overview

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Social Recognition in Amphipods: an Overview Chapter 6 Social Recognition in Amphipods: An Overview Jan Beermann, Jaimie T.A. Dick and Martin Thiel Abstract Many amphipod species occur in dense aggregations, cohabit with mating partners for long time periods, or live in family groups. Although this confers ample opportunities for social interactions among conspecifics, little is known about social recognition patterns in these species. Current research indicates that social recogni- tion in amphipods is largely limited to mate and female-offspring recognition. In many amphipod species, the males are capable of assessing the reproductive status/quality of females and choose mates accordingly. While females of some species are capable of recognizing their own brood, in other species females seem to be indiscriminate towards their own or unrelated embryos. Some observations, however, suggest kin recognition within family units and even ranking of conspecifics seems to be likely. Central-place foraging has not been reported for amphipod families thus far, and also their potential for fortress defense is very limited. It thus appears that higher level J. Beermann Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research, Biologische Anstalt Helgoland, Postbox 180, 27483 Helgoland, Germany e-mail: [email protected] J.T.A. Dick Institute for Global Food Security, School of Biological Sciences, Queen’s University Belfast, 97 Lisburn Road, Belfast BT9 7BL, Northern Ireland, UK e-mail: [email protected] M. Thiel (*) Facultad Ciencias del Mar, Universidad Católica del Norte, Larrondo 1281, Coquimbo, Chile e-mail: [email protected] J.T.A. Dick Charles Darwin University, Darwin, NT 0909, Australia M. Thiel Millennium Nucleus Ecology and Sustainable Management of Oceanic Island (ESMOI), Coquimbo, Chile M. Thiel Centro de Estudios Avanzados en Zonas Áridas (CEAZA), Coquimbo, Chile © Springer International Publishing Switzerland 2015 85 L. Aquiloni and E. Tricarico (eds.), Social Recognition in Invertebrates, DOI 10.1007/978-3-319-17599-7_6 86 J. Beermann et al. social recognition may not have evolved in amphipods, although we recognize a lack of research in this area. Given their easy maintenance in laboratory cultures and tech- nological advances in video recording and analysis, we believe that selected amphipod species could be ideal model organisms to study the evolution of social behavior. Introduction Amphipods often occur in dense aggregations (e.g. Aumack et al. 2011; Rigolet et al. 2012; Vitaliano et al. 2013) and frequent interactions among conspecifics can thus be expected. Courting individuals must recognize potential mates of their own species (Dick and Elwood 1992; Cothran et al. 2013) and distinguish between mem- bers of the same and the opposite sex (Thiel 2011a). Once the correct species has been identified, individuals might choose preferred mating partners, for example, based on moult stage, size and parasite status (Poulton and Thompson 1987; Dick and Elwood 1989; Thomas et al. 1996; Thiel 2011a, b). If mates stay together after fertilization, there might be a need for individual recognition. Similar to isopods (e.g. Linsenmair 2007), amphipods feature direct development and parents might care for their offspring after these are born (have emerged from the maternal brood pouch); in this case, the need for family recognition (parents and offspring mutually recogniz- ing each other) might have evolved (Thiel 2007). In addition to such post-emergence juvenile care, pre-emergence brood care, such as egg retrieval following loss from the marsupium, is also facilitated by kin recognition in amphipods (Patterson et al. 2008). All these social interactions require sensory and neuronal systems that permit exchange and processing of information between individuals (e.g. Wyatt 2011). While there are some suggestive observations, very few studies have rigorously examined whether and how individual amphipods distinguish conspecifics or might even recognize particular individuals. In the present overview, we provide exam- ples for each applicable form of recognition described in Gherardi et al. (2012): mate and kin recognition as well as the evaluation of higher- and lower-ranking individuals. In each section, we first describe the best studied cases and then report examples that are highly suggestive of recognition but without observational or experimental evidence. We wish to emphasize upfront that little is known about social recognition in amphipods, but we hope that we will be able to convince read- ers that this group can be a fertile ground for exciting discoveries in the future. Life Styles and Habitats Amphipods inhabit all aquatic habitats from the deep ocean and hydrothermal vents to cold mountain springs and even terrestrial habitats (e.g. Barnard and Karaman et al. 1991; Väinölä et al. 2008). Many species are highly mobile, being constantly on the move in search of food and mates. For example, some pelagic amphipods form 6 Social Recognition in Amphipods: An Overview 87 dense feeding swarms that continuously change shape, density and extension (Lobel and Randall 1986; Sheader et al. 2000). How coordination is maintained between the neighboring individuals in these dense swarms is not known at present but it is sus- pected that vision and mechano-reception might be involved (Ritz et al. 2011). Scavenging amphipods roam above the seafloor in search of food: once they receive a chemical stimulus indicating nearby carrion, they rapidly track and follow the chemical cues to the food source (Sainte-Marie 1992; Premke et al. 2003). On large carcasses, hundreds and even thousands of scavenging amphipods will rapidly congregate in dense and voracious feeding aggregations, which might result in fre- quent intra- and interspecific interactions (e.g. Thurston 1979; Moore 1994; Moore and Wong 1995; Premke et al. 2006). Herbivorous amphipods move around between living macrophytes or plant detritus, i.e. they live in and on their food sources. Some species are widespread on their host-plants, and interactions are probably infrequent, while others form dense aggregations in favorable locations, where individuals are in continuous contact with conspecifics (e.g. Gunnill 1984; Duffy 1990). Many amphipods also have a semi-sessile life style, inhabiting self-constructed tubes from which they capture suspended food particles, graze epiphytes and/or con- sume macroalgal or seagrass tissue on which they construct their tubes (e.g. Brawley and Adey 1981; Dixon and Moore 1997; McDonald and Bingham 2010). Other spe- cies excavate underground galleries in soft-bottoms where they consume organic matter that they sort out of the sediment (Atkinson et al. 1982). Tube- and burrow- dwellers usually cohabit only with mates and/or offspring in their domiciles, but, espe- cially among the suspension-feeders in favorable feeding locations, there might be extraordinarily high densities of tubes, resulting in frequent intraspecific interactions. Several authors have suggested gregariousness in amphipods (e.g. Drolet et al. 2013), but the underlying mechanisms and individual detection of conspecific aggregations is not well understood. Amphipods are also prey to a wide range of vertebrate and invertebrate predators, and it is thus not surprising that they adjust their behavior in response to predators (e.g. MacNeil et al. 1999; Wisenden et al. 2001). Some species aggregate when exposed to predator cues (Kullmann et al. 2008; Durieux et al. 2012), but it is not known how amphipods interact within these aggregations. In addition, such aggregations may rather be a predatory/scavenging response to such cues, as some amphipods such as Gammarus spp. are well known to be omnivorous and opportunistic in their feeding (MacNeil et al. 1997). When sensing the presence of a predator, some amphipod species shift their substratum preferences (Baumgärtner et al. 2003), or they are less inclined to form mating pairs during reproduction (Dunn et al. 2008; Ahlgren et al. 2011). Parasitism might also negatively affect the tendency of amphipods to aggregate (Durieux et al. 2012). In dense aggregations, amphipods may aggressively interact with conspecifics (Van Tomme et al. 2012). Aggression may depend on the availability of resources and the conspecific densities within these aggregations. Furthermore, some amphipod species appear to be much more aggressive than others, even in closely related species (Dick et al. 1995; Van Tomme et al. 2012). Some adults can be aggressive towards juveniles and cannibalize these when food availability is limited (Duarte et al. 2010) and these effects may be reinforced at high densities (Wenngren and Ólafson 2002). However, 88 J. Beermann et al. the occurrence of filial cannibalism can also depend on the brooding status of indi- viduals and may be reduced by juvenile avoidance behaviors (Lewis et al. 2010), with evidence of kin recognition reducing cannibalism of eggs (Patterson et al. 2008). Signals and Communication Channels Amphipods employ a wide variety of communication channels, but chemical cues are by far the most important in exchanging information between conspecifics (see Thiel 2011a and references therein). The specific substances used for communication are not well known, but molt hormones may play an important role in reproductive interactions. Perception of chemical stimuli happens via specific sensillae that are concentrated on the antennae, but can also take place on other body parts (Hallberg and Skog 2011). Visual communication may also play a role in amphipod
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