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Habitat Complexity Modiwes Ant–Parasitoid Interactions: Implications for Community Dynamics and the Role of Disturbance

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Habitat Complexity Modiwes Ant–Parasitoid Interactions: Implications for Community Dynamics and the Role of Disturbance Oecologia (2007) 152:151–161 DOI 10.1007/s00442-006-0634-6 COMMUNITY ECOLOGY Habitat complexity modiWes ant–parasitoid interactions: implications for community dynamics and the role of disturbance Elliot B. Wilkinson · Donald H. Feener Jr Received: 4 November 2006 / Accepted: 27 November 2006 / Published online: 22 December 2006 © Springer-Verlag 2006 Abstract Species must balance eVective competition itat complexity was also studied, and demonstrated with avoidance of mortality imposed by predators or that the immediate negative impact of Wre on habitat parasites to coexist within a local ecological commu- complexity can persist for multiple years. Our Wndings nity. Attributes of the habitat in which species interact, indicate that habitat complexity can increase dominant such as structural complexity, have the potential to host competitive success even in the presence of parasi- aVect how species balance competition and mortality toids, which may have consequences for coexistence of by providing refuge from predators or parasites. Dis- subordinate competitors and community diversity in turbance events such as Wre can drastically alter habitat general. complexity and may be important modiWers of species interactions in communities. This study investigates Keywords Competition · Formicidae · Fire · whether the presence of habitat complexity in the form Trade-oVs · Indirect interactions of leaf litter can alter interactions between the behav- iorally dominant host ants Pheidole diversipilosa and Pheidole bicarinata, their respective specialist dipteran Introduction parasitoids (Phoridae: Apocephalus sp. 8 and Apoceph- alus sp. 25) and a single species of ant competitor Trade-oVs resulting from variability in resource acqui- (Dorymyrmex insanus). We used a factorial design to sition, competition and mortality are central to our manipulate competition (presence/absence of competi- understanding of coexistence in local ecological com- tors), mortality risk (presence/absence of parasitoids) munities (Tilman 1994; Kneitel and Chase 2004). Spe- and habitat complexity (presence/absence of leaf cies coexist by trading oV the beneWts of one strategy litter). Parasitoid presence reduced soldier caste forag- for those of another in ways that minimize competition ing, but refuge from habitat complexity allowed and mortality while maximizing energy intake. Species increased soldier foraging in comparison to treatments with parasites or predators must therefore balance two in which no refuge was available. Variation in soldier conXicting demands: competing eVectively for limited foraging behavior correlated strongly with foraging resources and escaping parasitism/predation. Contin- success, a proxy for colony Wtness. Habitat complexity ued coexistence of such species in the community allowed both host species to balance competitive suc- depends on successfully balancing demands imposed cess with mortality avoidance. The eVect of Wre on hab- by competition and predation/parasitism. A mechanis- tic understanding of how organisms balance both com- petitor and predator-related trade-oVs is needed if we Communicated by Andrew Gonzales. are to understand forces controlling community struc- ture and composition. E. B. Wilkinson (&) · D. H. Feener Jr A variety of factors have been posited to aVect how Department of Biology, University of Utah, X 257 South 1400 East, Salt Lake City, UT 84112, USA species balance these con icting demands, including e-mail: [email protected] organismal attributes such as host energy state (Alonzo 123 152 Oecologia (2007) 152:151–161 2002), competitive environment (LeBrun and Feener and leads in some cases to loss of resources to competi- 2002), and variation in parasitoid abundance through tors (LeBrun and Feener 2002; Orr et al. 1995). As a space and time (Morrison et al. 2000). However, physi- result, parasitoid presence can render some dominant cal attributes of the habitat such as structural complex- competitors ineVective, which may lead to heightened ity can work alongside organismal attributes to species diversity or altered community structure inXuence species’ abilities to balance the conXicting (Feener 2000; LeBrun 2005). The coincidence of indi- demands of competition and escape from parasitism/ rect eVects on competition that dwarf the direct eVects predation. Examples from many diVerent systems high- of mortality from parasitoids, and the fact that parasi- light the importance of mortality risk in inXuencing toids specialize on a single species, make ant–parasit- prey/host behavior (Fraser and Huntingford 1986; oid interactions especially likely to inXuence ant Lima and Dill 1990; Rothley et al. 1997; Ripple and community coexistence (Chase et al. 2002). However, Beschta 2004). In some systems, habitat complexity such trait-mediated indirect interactions are wide- enhances mortality risk by aggregating prey or provid- spread and thought to be important in the dynamics of ing favorable habitats/hiding places for predators most communities (Werner and Peacor 2003). Small- (Gosselin and Bourget 1989; Finke and Denno 2002). scale habitat complexity in the form of leaf litter has Habitat complexity may also oVset mortality risk by the potential to provide refuge for host ants and ame- increasing prey/host ability to escape from predators or liorate negative eVects from parasitoids, thereby allow- parasites. We focus on the role of habitat complexity in ing hosts to continue competing eVectively while also enhancing prey/host escape because habitat complexity avoiding parasitism. is likely to impede movement of the Xying predators/ This study investigates whether small-scale habitat parasitoids used in this study. complexity alters ant–parasitoid interactions in ways Habitat complexity may facilitate escape by provid- that can impact ant community structure. For two ing a refuge to which parasites/predators do not have diVerent host–parasitoid systems, we use a multi-fac- access. Examples of such refuge eVects on predator– tor experiment to determine the eVects of parasitoids, prey dynamics include the protective services that aca- habitat complexity and competitors on the number of rodomatia provide for non-plant feeding mites (Norton soldier ants defending and harvesting resources. Sol- et al. 2001), lowered aphid accessibility to predacious diers are the best choice to measure eVects of habitat lacewing larvae on architecturally complex grasses complexity on host ant–parasitoid–competitor interac- (Clark and Messina 1998), lowered intraguild preda- tions because parasitoids only attack soldiers tion in salt marshes with higher vegetation complexity (although release of alarm pheromone after attack (Finke and Denno 2002) and lower mortality of thysan- soon induces colony-wide response) and because sol- opteran prey species in complex shaped arenas (Hod- diers are critical in the defense and harvest of large dle 2003). Limited evidence suggests that habitat resources. Within the context of our multi-factor complexity can provide lepidopteran crop pests with experiment, we ask Wve questions regarding the rela- refuge from hymenopteran parasitoids (Andow and tionship between habitat complexity and ant–parasit- Prokrym 1990). In addition, multiple ant hosts of the oid interactions: (1) can habitat complexity beneWt the genus Pheidole may exhibit behavioral responses to colony by providing refuge from parasitoids and parasitoid presence by hiding in nearby leaf litter allowing soldiers to harvest resources when parasi- (D. H. Feener, personal observation). toids are present, or (2) does habitat complexity have Ant communities are model systems for studying a positive eVect on soldiers even in the absence of par- community ecology, yet little attention has been given asitoids? To address whether habitat complexity to the potentially important role of predation in such allows hosts to balance the conXicting demands of communities because of the common view that ants are competition and escape from parasitism, we ask: (3) relatively immune to predators (Hölldobler and Wil- can hosts in simple (no complexity) habitats balance son 1990; Holway 1999). However, a growing body of the conXicting demands of competition and parasitoid knowledge has provided support for top-down inXu- avoidance by competing at the same level as treat- ence on ant community coexistence and structure in ments with no parasitoids and no habitat complexity, the form of behavioral responses to Dipteran parasi- (4) can hosts in complex habitats balance competition toids, which specialize on a single, usually dominant, and parasitoid avoidance by competing at the same ant species (Feener 1981; Morrison 1999; LeBrun and levels as treatments with no parasitoids and no habitat Feener 2002; LeBrun 2005). Behavioral response to the complexity, and (5) do hosts compete any diVerently threat of mortality from parasitoid attack usually con- in complex and simple habitats when parasitoids are sists of colony-wide alteration of foraging behavior, absent? 123 Oecologia (2007) 152:151–161 153 Materials and methods mates is a pervasive phenomenon in ants and is known as alarm recruitment (Hölldobler and Wilson 1990). Study sites and systems Alarm recruitment typically consists of alarm phero- mones being released either alone or in conjunction This study focuses on two ant species of the Pheidole with odor trails when an enemy is encountered, and genus that host specialist Apocephalus parasitoids has been studied in detail with Pheidole dentata,
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