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Habitat Edge Effects Alter Ant-Guard Protection Against Herbivory

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Habitat Edge Effects Alter Ant-Guard Protection Against Herbivory Landscape Ecol (2013) 28:1743–1754 DOI 10.1007/s10980-013-9917-6 RESEARCH ARTICLE Habitat edge effects alter ant-guard protection against herbivory Daniel M. Evans • Nash E. Turley • Joshua J. Tewksbury Received: 25 November 2012 / Accepted: 11 July 2013 / Published online: 20 July 2013 Ó Springer Science+Business Media Dordrecht 2013 Abstract Edge effects are among the most important plants far from edges, where herbivory pressure was drivers of species interactions in fragmented habitats, highest, despite the fact that aphids and ants were least but the impacts of edge effects on multitrophic abundant on these plants. Conversely, ants did not interactions are largely unknown. In this study we provide significant protection near edges, where assess edge effects on species interactions within an herbivory pressure was lowest and aphids and ants ant–plant mutualistic system—where ants protect were most abundant. We conclude that a strong edge plants against herbivory—to determine whether hab- effect on grasshopper abundance was a key factor itat edges alter the amount of protection ants provide. determining the amount of protection ants provided We focus on a single species of myrmecophytic plant, against herbivory. Future studies of the impacts of Solanum americanum, and experimentally manipulate habitat fragmentation on ant–plant mutualisms will ant access to study plants in large-scale fragmented benefit from studies of ant behavior in response to habitat patches at the Savannah River Site National herbivory threats, and studies of edge effects on other Environmental Research Park, USA. In this system, S. species interactions may also need to consider how americanum commonly hosts honeydew-producing species’ behavioral patterns influence the interactions aphids that are tended by ants, and grasshoppers are in question. the primary herbivores. We measured edge effects on the per-plant abundance of aphids and protective ants Keywords Habitat edges Á Multitrophic as well as the abundance of grasshoppers in each species interactions Á Ant–plant mutualism Á habitat patch, and we evaluated levels of ant protection Insect herbivory Á Solanum americanum Á against herbivory near and far from habitat edges. We Savannah River Site, South Carolina, USA found that ants provided significant protection to D. M. Evans (&) Á J. J. Tewksbury Department of Biology, University of Washington, Introduction 24 Kincaid Hall, Box 351800, Seattle, WA 98195-1800, USA e-mail: [email protected] Herbivory is one of the greatest challenges to plant survival and reproduction, and plants have evolved a N. E. Turley diverse arsenal of defenses against it (Futuyma and Department of Biology, University of Toronto Mississauga, 3359 Mississauga Road North, Agrawal 2009; Agrawal 2011). Among the most Mississauga, ON L5L 1C6, Canada effective defenses are ant-guard systems, whereby 123 1744 Landscape Ecol (2013) 28:1743–1754 plants establish mutualisms with ants that can protect herbivores (Beattie 1985; Cushman and Addicott them against herbivores (Beattie and Hughes 2002; 1991; Schupp and Feener 1991; Bronstein 1994; Massad et al. 2011). Myrmecophytes, i.e. ‘‘ant- Stadler and Dixon 2005; Rico-Gray and Oliveira plants,’’ may reward ants directly with domatia or 2007), and edges are also known to alter each of these food (e.g., Janzen 1966, 1967, 1969), or indirectly, by factors (Carvalho and Vasconcelos 1999; Braschler hosting insect herbivores that provide ants with sugar- et al. 2003; Tscharntke and Brandl 2004; Debuse et al. rich honeydew (Reviewed in Way 1963; Rico-Gray 2007; Laurance et al. 2011; Orrock et al. 2011). This and Oliveira 2007); either arrangement can increase evidence, taken together, suggests that edge effects on plant growth and fitness (Messina 1981; Horvitz and the distribution and ‘‘encounter frequencies’’ of Schemske 1984; Beattie 1985; Vasconcelos 1991; honeydew-producing insects, ants, and other herbi- Rico-Gray and Oliveira 2007). Even in indirect cases, vores may determine levels of herbivory and the when ants protect honeydew-producing herbivores, amount of protection ants provide plants in frag- the damage caused to plants by the honeydew- mented habitats. producers is often outweighed by the ants’ deterrence In this study, we assess the impacts of edge effects of other herbivores (Carroll and Janzen 1973; Beattie on levels of herbivory in an ant–plant mutualistic and Hughes 2002; Oliveira and Del-Claro 2005). system. Our study site is a landscape-scale fragmen- Given that ants are among the most abundant and tation experiment that is explicitly designed to test for widespread animal groups in the world and are leading edge effects on plants and plant-animal interactions predators of insects and small invertebrates (Ho¨lldo- (as described in ‘‘Study system’’ section below). We bler and Wilson 1990), it is not surprising that many focus on a single species of myrmecophytic plant, plant species depend on ants for protection against Solanum americanum (Solanaceae), which attracts a herbivory (Oliveira and Freitas 2004 and references variety of ants in our study system by hosting therein). honeydew-producing aphids (hemiptera), and we Habitat edges created by fragmentation can alter focus on herbivory by grasshoppers (orthoptera), patterns of herbivory in habitat fragments (e.g., which are the primary consumers of S. americanum Meiners et al. 2000; Tscharntke et al. 2002; Bach in the study area. Our objectives are twofold: (1) We and Kelly 2004; Lopez-Barrera et al. 2006; Valladares test for edge effects on the per-plant abundance of et al. 2006), but the influence of edges on herbivory in aphids and protective ants as well as the abundance of multitrophic systems, including ant-guard systems, is grasshoppers in the experimentally fragmented habitat unknown (Bruna et al. 2005; Wimp et al. 2011). patches that comprise our study system; and (2) We Ecologists have studied edge effects for more than evaluate whether changes in the abundances of these 100 years, yet the vast majority of edge studies are interacting species alter levels of ant-guard protection focused on single species or pairwise interactions against herbivory near and far from habitat edges. This (Martinson 2009). We do know a good deal about the second question addresses a key issue for myrmeco- causes edge effects: Abiotic conditions, e.g., light, phytic plants. As habitats around the world are moisture, and temperature, near habitat edges often are increasingly fragmented, ant-plants may be increas- very different than conditions far from edges, and ingly exposed to novel gradients in habitat quality, these differences can determine the availability of levels of herbivory, and ant-guard protection against resources and the abundance of organisms as a herbivory. function of distance from the edges (reviewed in Collinge 2009). Study system Current theory describes edge effects on species interactions largely as additive phenomena, resulting We conducted this study in eight experimentally from edge effects on the abundance and ‘‘encounter fragmented landscape replicates (blocks) at the frequencies’’ of the individual species in question Savannah River Site (SRS) National Environmental (Fagan et al. 1999; Ries et al. 2004). Studies of ant– Research Park, USA. The landscapes were created in plant mutualism show that levels of ant protection 1999 and 2000 by clear-cutting habitat patches from against herbivory can vary strongly with the abun- mature loblolly pine (Pinus taeda) plantation forest. dance of honeydew-producing insects, ants, and other The patches in each landscape are early-successional 123 Landscape Ecol (2013) 28:1743–1754 1745 longleaf pine (Pinus palustris) savannah; they have genera, Dorymyrmex, Formica, Myrmica, Pogono- had hardwoods removed and have been burned four myrmex, and Solenopsis typically avoid edges and are times since 1999 to promote savannah restoration, most abundant in the center ‘‘core’’ area of the habitat while the mature forest matrix of each landscape patches; Crematogaster is most abundant in the remains intact. Each landscape is *50 ha, including patches near forest edges (Orrock et al. 2011). With forested matrix area, and consists of five habitat the exception of Pogonomyrmex, ants in each of these patches of approximately equal area (*1 ha) genera consume aphid honeydew and are facultative (Fig. 1a). These experimental landscapes present an plant mutualists that at least occasionally defend excellent system in which to study edge effects on plants against insect herbivores (Ho¨lldobler and plants and plant–animal interactions, for three reasons. Wilson 1990; Stechmann et al. 1996; Hubner 2000; First, because the patches are early-successional Rico-Gray and Oliveira 2007; Warriner et al. 2008; savannah habitat and the matrix is densely planted Shibao et al. 2009; Gibb and Johansson 2010; Styrsky mature forest, the edge boundaries between the and Eubanks 2010). Crematogaster, Formica, and patches and the matrix are ecologically distinct. Solenopsis ants, in particular, will aggressively defend Second, the geometry of the patches permits explicit plants to protect sources of hemipteran honeydew tests of the impacts of edge effects; each patch either is (Kaplan and Eubanks 2005; Rico-Gray and Oliveira a rectangle that is 100 9 137 m or has a square central 2007; Styrsky and Eubanks 2010). region that is 100 9 100 m, so study plants can be Grasshoppers are common consumers of S. amer- located on transects that bisect the right angle
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