Interactions Among Defensive and Escape Strategies in Sabellid Worms
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Oecologia (2007) 151:161–173 DOI 10.1007/s00442-006-0567-0 BEHAVIORAL ECOLOGY To avoid or deter: interactions among defensive and escape strategies in sabellid worms Cynthia E. Kicklighter · Mark E. Hay Received: 15 October 2005 / Accepted: 31 August 2006 / Published online: 29 November 2006 © Springer-Verlag 2006 Abstract Numerous studies demonstrate how sessile than the other species. Their tubes were weak, they did marine organisms utilize chemical, structural, and not retract until disturbances were very close, and B. nutritional deterrents to persist in predator-rich envi- brunnea retracted slowly and incompletely even when ronments. Little is known, however, about how mobile, touched. Other species generally had stronger tubes more behaviorally complex species minimize predation and/or retracted when disturbances were farther away. by integrating avoidance and deterrence strategies. We This trade-oV of deterrence versus escape even investigated this using sabellid polychaete worms from occurred within a single species when populations the Caribbean and temperate western Atlantic. Sabel- diVered in palatability. Populations of B.variegata from lids extend their feather-like radioles beyond their pro- North Carolina and Georgia were chemically deterrent tective tubes for feeding and respiration; the body to both temperate and tropical consumers, while popu- remains inside the tube and the radioles retract when lations from Panama and Florida were palatable. The threatened. We used co-occurring consumers to deter- more palatable Panama population retracted in mine the palatability of radioles and bodies for each of response to distant movement, while the unpalatable the eight species tested. In addition, we examined North Carolina population did not retract until nearly chemical or structural traits aVecting palatability and touched. Thus, most species utilize a combination of evaluated predator escape traits, such as tube strength, predator avoidance and deterrence strategies, but speed of radiole retraction, completeness of retraction, more deterrent populations of species utilized avoid- and sensitivity to a nearby disturbance. All species had ance less. unpalatable radioles that were chemically or structur- ally defended, but only two species had unpalatable Keywords Chemical defense · Polychaete · Predator bodies. Thus, most species allocated defenses to tissues defense · Predator–prey · Sabellidae that were most exposed to predation. The two species with chemically defended bodies, Bispira brunnea and Bispira variegata, relied less on behavioral escapes Introduction Numerous studies have demonstrated how organisms, such as terrestrial plants, marine invertebrates, and Communicated by Steven Kohler. seaweeds, use chemical and structural (e.g., spines, toughness, spicules) deterrents as defenses against con- C. E. Kicklighter (&) Department of Biological Sciences, Goucher College, sumers (e.g., Rosenthal and Berenbaum 1992; Hay 1021 Dulaney Valley Rd., Baltimore, MD 21204-2794, USA 1996; McClintock and Baker 2001). In some cases, e-mail: [email protected] there appears to be a trade-oV between these defensive strategies. As examples: (1) some terrestrial plants M. E. Hay School of Biology, Georgia Institute of Technology, Atlanta, show a negative correlation between physical and GA 30332-0230, USA chemical deterrents (Twigg and Socha 1996); (2) some 123 162 Oecologia (2007) 151:161–173 seaweeds have high levels of chemical defenses in tis- Sabellid worms (polychaete annelids) are good sues that are poorly defended structurally, but model organisms for investigations of how predator decrease chemical defenses as structural defenses deterrence (chemical, structural) and avoidance increase (Hay et al. 1988); and (3) marine hydroids (behavioral escape, refuge use) strategies may be inte- deter consumers with stinging nematocysts or with grated by marine invertebrates. Sabellids, commonly chemical defenses, but not with both (Stachowicz and called “feather duster” worms, are tube-dwelling spe- Lindquist 2000). cies that have a crown of feathery radioles for feeding In other cases, however, chemical and structural and respiration that project from a protective tube. For defenses are used simultaneously, as occurs for some most species, the body always remains inside the tube seaweeds (Paul and Hay 1986; Hay et al. 1994), soft (Fauchald 1977; Fauchald and Jumars 1979) and many corals (Van Alstyne and Paul 1992), sponges (Hill et al. species can quickly and completely retract their radi- 2005; Jones et al. 2005), echinoderms (Bryan oles in response to a physical disturbance, shadow, or et al.1997), and terrestrial plants (Ramachandran and approaching consumer. The worm constructs the tube Khan 1991). The use of multiple defenses might be from organic secretions or a mix of mucous secretions selected for in predator-rich environments (such as and size-selected particles (Brusca and Brusca 1990). tropical habitats) where consumer diversity and attack Tube-building is an eVective antipredation strategy for strategies are both high (Lubchenco and Gaines 1981; insects (Hershey 1987; Robinson 2000) and some poly- Hay 1984). In some cases, chemical and structural chaetes (Matilla 1997; C. Kicklighter, personal obser- deterrents may even interact synergistically to enhance vation), so tubes likely protect sabellids as well. resistance to consumers, as has been shown for a soft Sabellids commonly occur in areas of high consumer coral (Gerhart et al. 1988), two seaweed species (Hay activity, such as coral reefs, where chemically defended et al. 1994), and potentially some sponges (Jones et al. species such as seaweeds, sponges, soft corals, and asci- 2005). dians are also common (e.g., Hay and Fenical 1988; While many studies examine structural and chemical McClintock and Baker 2001; Paul et al. 2006). While defenses in sessile marine species (i.e., seaweeds, chemical defenses are uninvestigated in sabellid sponges, soft-corals, ascidians), few study use or alloca- worms, it seems likely that they might rely on both tion of these defenses in more mobile species that also deterrence and avoidance to persist in predator-rich utilize behavioral escapes from consumers (Stachowicz environments. 2001). Investigations regarding the potential integra- We use two ecologically relevant Wshes and a crab to tion of deterrence and avoidance strategies are needed examine the palatability, chemical and structural deter- to increase our understanding of defensive tactics used rence, and various behavioral and avoidance traits of by more behaviorally complex species. Two studies eight species of sabellid worms from the Republic of have examined the use of deterrence and refuging in Panama, the Bahamas, Florida, Georgia, and North two freshwater vertebrates. Stickleback Wsh that are Carolina. We used these data to evaluate how multiple structurally unpalatable (due to spines; Hoogland et al. traits were integrated to deter or avoid consumers. 1957) used refuges less and were faster to emerge from their refuges in the presence of a simulated aerial pred- ator than were palatable minnows (which lack spines Materials and methods or other deterrents) (Krause et al. 2000). Similarly, unpalatable tadpoles often refuged less than palatable Worms were collected September 2000–June 2003 tadpoles in the presence of water containing predatory near: (1) Bocas del Toro, Republic of Panama ([09° Wsh (Kats et al. 1988). Terrestrial species may show 21ЈN, 82° 15ЈW]—Anamobaea orstedii, Branchiomma similar trade-oVs. Unpalatable caterpillars tend to be nigromaculata, and Sabellastarte magniWca from coral overt, occur gregariously, and feed during the day rock and rubble on coral reefs, Megalomma sp. from when predators are active, while palatable species that soft-sediments on reefs and reef-Xats, and Bispira var- lack defenses tend to be solitary, cryptic, and refuge iegata from soft-sediments around mangroves); (2) from predators by feeding on the undersides of leaves San Salvador, Bahamas ([24° 03ЈN, 74° 32ЈW]— or within rolled leaves (Heinrich 1993). These studies Bispira brunnea from weathered coral rock); (3) Key suggest that behavioral avoidance is used more by spe- Largo, Florida ([25° 07ЈN, 80° 25ЈW]—Branchiomma cies lacking predator deterrents and less by species sp. from the alga Halimeda optunia around man- with eVective consumer deterrents. More studies on a groves, and B. variegata from mangrove prop roots); greater diversity of prey types are needed to determine (4) Shackleford Island, North Carolina ([34° 40ЈN, 76° if this is a general pattern. 37ЈW]—Bispira variegata from submerged boulders); 123 Oecologia (2007) 151:161–173 163 (5) Skidaway Island, Georgia ([31° 57ЈN, 81° 00ЈW]— we were concerned that the consumers we were using Sabella sp. from a Xoating dock), and (6) near Gray’s may not have previously encountered the prey and reef oV the coast of Savannah, Georgia ([31° 24ЈN, 80° might have needed to learn from an initial encounter, 53ЈW]—B. variegata from limestone rock). Palatability we fed consumers for two consecutive days in order to of species from North Carolina and Georgia were allow consumer learning. These Wshes and crabs will assayed using the co-occurring Wsh Fundulus heterocli- learn to reject defended, novel foods within this time tus (mummichog) and the crab Callinectes similis period (Lindquist and Hay 1995; Kicklighter et al. (lesser blue crab). Worms from Panama, the Bahamas, 2004; Long and Hay 2005). and Florida