Oecologia DOI 10.1007/s00442-012-2340-x PLANT-ANIMAL INTERACTIONS - ORIGINAL RESEARCH Plant defense, herbivory, and the growth of Cordia alliodora trees and their symbiotic Azteca ant colonies Elizabeth G. Pringle • Rodolfo Dirzo • Deborah M. Gordon Received: 25 March 2011 / Accepted: 16 April 2012 Ó Springer-Verlag 2012 Abstract The effects of herbivory on plant fitness are herbivore pressure in larger trees. These results suggest that integrated over a plant’s lifetime, mediated by ontogenetic in this system the tree can decrease herbivory by promoting changes in plant defense, tolerance, and herbivore pressure. ant-colony growth, i.e., sustaining space and food invest- In symbiotic ant–plant mutualisms, plants provide nesting ment in ants, as long as the tree continues to grow. space and food for ants, and ants defend plants against herbivores. The benefit to the plant of sustaining the growth Keywords Allometry Á Ant–plant mutualism Á of symbiotic ant colonies depends on whether defense by Chamela-Cuixmala Biosphere Reserve Á Mexico Á the growing ant colony outpaces the plant’s growth in Ontogeny Á Positive feedback defendable area and associated herbivore pressure. These relationships were investigated in the symbiotic mutualism between Cordia alliodora trees and Azteca pittieri ants in a Introduction Mexican tropical dry forest. As ant colonies grew, worker production remained constant relative to ant-colony size. Anti-herbivory defense strategies and the impacts of her- As trees grew, leaf production increased relative to tree bivore damage can change considerably in the course of size. Moreover, larger trees hosted lower densities of ants, plant ontogeny. Greater investment in defense or tolerance suggesting that ant-colony growth did not keep pace with may occur at life stages when a plant has more resources for tree growth. On leaves with ants experimentally excluded, defense allocation (Weiner 2004) or when the plant is most herbivory per unit leaf area increased exponentially with vulnerable to herbivores (Stowe et al. 2000). Synthesizing tree size, indicating that larger trees experienced higher these theories, Boege and Marquis (2005) predicted non- herbivore pressure per leaf area than smaller trees. Even linear, substantial changes in defense in the course of a with ant defense, herbivory increased with tree size. plant’s life. However, empirical data for many plant species Therefore, although larger trees had larger ant colonies, ant suggest that ontogenetic patterns in defense are idiosyn- density was lower in larger trees, and the ant colonies did cratic, depending on plant growth form, herbivore guild, not provide sufficient defense to compensate for the higher and defensive trait strategy (Barton and Koricheva 2010). When plants employ biotic defenses, by providing rewards to defending mutualists, ontogenetic changes in plant Communicated by John Silander. defense depend on concurrent changes in the defensive efficacy of the mutualists. In symbiotic ant–plant protection E. G. Pringle Á R. Dirzo Á D. M. Gordon mutualisms, plants (known as myrmecophytes) provide ants Biology Department, Stanford University, Stanford, CA 94305, USA with nesting cavities known as domatia and, directly or indirectly, with food rewards. Ants, in turn, provide defense Present Address: against herbivores and encroaching vegetation (Heil and & E. G. Pringle ( ) McKey 2003), and, in some systems, supply the plant with Michigan Society of Fellows, University of Michigan, Ann Arbor, MI 48109, USA additional nutrients (e.g., Defossez et al. 2011; Fischer et al. e-mail: [email protected] 2003; Solano and Dejean 2004). 123 Oecologia The effectiveness of ant defense over the host plant’s contrast, Frederickson and Gordon (2009) measured plant life is related to the timing of ant colonization, the identity growth and domatia occupation by ant colonies in two sys- of the ant species, and the relative growth rates of the plant tems in the Peruvian Amazon, and found evidence for and its symbiotic ant colony. Myrmecophytes are colonized positive feedback between ant-colony and plant growth by ants some time after germination and production of the rates: when larger ant colonies do a better job of protecting first domatia. Ant–plant systems differ in whether levels of plants, plants can grow larger because of this superior pro- direct (i.e., abiotic) defenses change after ant colonization tection, and ant colonies grow as plants add domatia. (Del Val and Dirzo 2003; Llandres et al. 2010; Nomura Herbivore pressure can change as trees grow, but few et al. 2001; Trager and Bruna 2006). Once colonized, studies have measured herbivory continuously during plant myrmecophytes spend most of their lives hosting ant development (but see Thomas et al. 2010). Larger trees mutualists, and the density of ant workers per unit leaf area, attract higher abundances and richness of insect herbivores as opposed to colony size per se, determines how well than smaller trees (Campos et al. 2006; Guedes et al. 2000). plants are defended. The higher the density of ants in a The greater relative architectural complexity of larger trees plant, the more patrolling workers per unit leaf area, and than of smaller trees may support more insects per unit of thus the more likely ants are to encounter, attack, and chase leaf area, or larger trees may support certain herbivore away or consume herbivores (Duarte-Rocha and Godoy- species that are rarely found on smaller trees (Lawton Bergallo 1992; Pringle et al. 2011b). Young leaves are 1983). If larger plants experience higher herbivore pressure particularly valuable to plants (Harper 1989) and vulnera- per unit of leaf area than smaller ones, and if ant defense ble to herbivores (Coley and Kursar 1996), so high densi- scales linearly with colony growth, the relative growth of ties of patrolling ants on young leaves in particular may ant colonies must be greater than leaf production by the confer important benefits to plants (Heil et al. 2004). host plant to maintain a constant level of anti-herbivore Both ant colonies and plants are modular organisms that defense. However, ant defense may not scale linearly with grow by addition of sterile workers and shoots, respectively colony growth—for example, larger colonies may coordi- (Wulff 1985). The relative rates of worker and shoot pro- nate activities more effectively than smaller ones (e.g., duction determine the density of ants per unit leaf area and Gordon 1987)—in which case even slow rates of ant-col- therefore whether the ant colony continues to provide the ony growth relative to tree leaf production may be suffi- same level of defense as the plant grows. The relative rates cient to maintain low levels of herbivory. of worker and shoot production may also change as colonies To evaluate how ant-colony growth is related to plant and trees grow, depending on the allometric relationships growth, and whether plants benefit from sustaining continu- between the production of workers or shoots and increasing ous ant-colony growth over time, we measured herbivory, ant ant-colony or tree size, respectively. In some ground-nest- worker production, and tree shoot production in a range of ing ant species, as colonies grow, they may produce fewer ant-colony and juvenile-tree sizes in an ant–plant mutualism new ant workers per unit size, exhibiting negative allometry in a seasonally dry forest in Western Mexico. Azteca pittieri (Smith and Tschinkel 2006; Tschinkel 1993, 1999); in other Forel (Formicidae: Dolichoderinae) ants form colonies in the species, colonies produce the same number of new ant domatia of Cordia alliodora (Ruiz and Pavo´n) Oken (Bora- workers per unit size, exhibiting isometry (Gordon 1992). ginaceae) trees, and defend their leaves from herbivores As juvenile trees grow into mature trees, they tend to pro- (Pringle et al. 2011b; Tillberg 2004). Using this system, we duce more crown area per unit size, exhibiting positive ask: (1) How does the rate of worker production change as A. allometry (Oliver and Larson 1990). pittieri ant colonies grow? (2) How do the rates of leaf and Few studies have assessed the effects of ant-colony domatium production change as C. alliodora trees grow? (3) growth over host-plant ontogeny, and the results to date have Do ant colonies produce new workers as quickly as trees been variable. Fonseca (1993) found that the number of produce new leaves that need to be defended? (4) Do bigger Pseudomyrmex concolor workers was highly correlated with trees sustain more herbivore pressure per unit area than total domatia space in Tachigali plants, and suggested that smaller trees? and (5) How do changes in both ant defense and the size of the ant colony is limited by the number and size of herbivore pressure affect herbivory rates as trees grow? domatia. If ant colonies grow faster than plants, colonies may grow so large that the marginal cost to the plant of providing food and space for each additional ant worker is greater than Materials and methods that worker’s marginal contribution to herbivory reduction (Bronstein 1998; Fonseca 1993; Ness et al. 2006). In such Study system cases, Fonseca (1993) argued, the plant should limit its investment in ants to keep colony size from surpassing the This study was conducted at the Chamela-Cuixmala Bio- point where marginal costs exceed marginal benefits. In sphere Reserve (19°300N, 105°020W) in Jalisco, Mexico in 123 Oecologia July–August 2008 and July 2009. The site (hereafter Mexico, and Guanacaste, Costa Rica. The coefficient of the ‘‘Chamela’’) is a seasonally dry tropical forest, with 85 % relationship was consistent across sites (Chamela only: of the *750 mm of yearly rain occurring from June to m = 1.08; all sites: m = 0.94), and statistical significance November (Bullock 1986). increased as data from additional sites were added. For Cordia alliodora is a common tree in the dry-season consistency, the analysis presented here includes only the deciduous forest at the site (*80 individuals/ha; E.G.