Acacia-ants swarm a katydid that I attached to their host

Between-species and temporal variation in acacia-ant-herbivore interactions

Greg Cronin

University of North Carolina at Chapel Hill, Institute of Marine Sciences,

Morehead City, North Carolina 28557 USA

Herbivores can have dramatic negative impacts on the growth, reproduction, and population size of plants (Howe and Westley 1988, Rosenthal and Berenbaum 1992, Marquis and Whelan 1994). Plants possess numerous traits that protect them from herbivore attack, including trichomes (Levin 1973), toughness (Grubb 1986), and a diverse arsenal of deterrent secondary metabolites (Rosenthal and Janzen 1979, Hay and Fenical 1988, Rosenthal and Berenbaum 1992). In addition to defensive plant traits, plants can also reduced herbivory via symbiotic relationships with plants (Hay 1986), fungi (Clay 1988), or animals (Janzen 1966).

Spatial and temporal variability in defensive plant traits is common (McKey 1979, Denno and McClure 1983), perhaps because variability in defenses may reduce the likelihood of herbivores countering plant defenses by presenting the herbivores with a moving target (Denno and McClure 1983, Karban et al. 1997). In a static world, herbivores could easily focus on habitats that had suitable resources and were free of natural enemies. However, plant defenses change phenologically (McKey 1979, Cronin and Hay 1996c) and in response to herbivore damage (Baldwin 1994, Cronin and Hay 1996a), light and nutrient availability (Bryant et al. 1983), and environmental stresses (Cronin and Hay 1996b). Additionally, plants can attract enemies of herbivores following grazing damage (Dicke 1994). This variation in defenses makes it more difficult for herbivores to locate suitable habitats and can increase their exposure to predators or other natural enemies.

In defensive plant-ant relationships, antiherbivore activity of plant-ants often varies among ant species (Janzen 1966, McKey 1984, Rico-Gray and Thien 1989, Longino 1991), within ant species (Rocha and Bergallo 1992), among plant parts (McKey 1984, Letourneau et al. 1993, Fonseca 1994, Agrawal 1996), or temporally (Janzen 1966, Downhower 1975, McKey 1984, Young et al. 1990, Fonseca 1994, Agrawal 1996). Some mechanisms that produces variation in defenses, such as induction or activation of defenses, can also reduce the putative costs of defenses (Harvell 1990, Baldwin 1994). Constitutive defenses require expenditure of resources even when consumers are absent and the benefits of protection are not realized. In contrast, inducible defenses allow costs of defenses to be deferred until enemies have been detected, at which time the costs can be offset by the benefits of protection (Rhoades 1985). The activity of plant-ants increases shortly after a disturbance (McKey 1984, Young et al. 1990, Agrawal 1996), and can be viewed as an inducible response that could reduce defensive costs.

One of the best studied examples of a defensive plant-animal symbiosis is the obligate mutualism between Acacia trees and Pseudomyrmex ants in Central America (Belt 1874, Janzen 1966, 1967, 1983). Ant-acacia trees provide the Pseudomyrmex ants with shelter in the form of large hollow thorns and nutrition from the extrafloral nectaries and Beltian bodies. Acacia-ants vigorously defend their host and colony from mammals, lizards, snakes, and insects that contact the ant-acacias, including most herbivores (Brown 1960, Janzen 1966, 1969). Ant-acacias depend on protection afforded by ants and can not grow in the absence of acacia-ants (Janzen 1966). Because of acacia-ants’ protective role, ant-acacias have apparently lost the capability to produce chemical defenses (Rehr et al. 1973).

Acacia collinsii in Palo Verde, Costa Rica has a mutualistic relationship with three species of stinging ants, Pseudomyrmex spinicola, P. nigrocinctus, and P. flavicornis, although individual trees usually contain only one ant species. Pseudomyrmex spinicola and P. nigrocinctus are two aggressive red-colored ants that were grouped because they were indistinguishable in the field. Pseudomyrmex spinicola removes more litter and plant competitors from around ant-acacias and is reportedly more aggressive than P. flavicornis (Janzen 1966, Gill et al. 1988, Young et al. 1990), suggesting P. spinicola may be the better mutualist. In addition to this interspecific variation in activity, Janzen (1966) noted that although acacia-ants are active 24 hours a day, there is a daily rhythm with high activity during maximum nectar flow (dawn) and maximum insect activity (noon and dusk). Ants also display reduced activity during the last month of the dry season (Janzen 1969).

Because variation in anti-herbivore defenses reduces the opportunity for counteradaptation, I monitored interspecific and temporal variation in acacia-ant activity and aggressiveness against herbivores. Experiments were performed at the Organization for Tropical Studies (OTS) Palo Verde Biological Station (10°N, 85°W), Guanacaste Province, Costa Rica during the dry season on 13-14 February, 1993. Acacia collinsii, Pseudomyrmex spinicola, P. nigrocinctus, and P. flavicornis are common in dry sites near the biological station. Only trees with a diameter at breast height of at least 3 cm were used because they had sufficiently established ant colonies. Trees of the proper size were selected haphazardly by flagging the first 42 trees with separate Pseudomyrmex spinicola or P. nigrocinctus colonies and the first 42 trees with separate P. flavicornis colonies that were encountered.

To assess temporal variation in the activity of each Pseudomyrmex species, half of the replicates was sampled in the morning (0830-1100) and the remaining half was sampled in the afternoon (1430-1700), resulting in a sample size of 21 for each ant species x sampling period combination. Because I could not sample 42 trees simultaneously, tree samples were interspersed temporally by ant species (i.e., 1-4 trees with P. spinicola or P. nigrocinctus followed by 1-4 trees with P. flavicornis) to avoid temporal variation on time scales shorter than several hours from confounding results.

The patrolling activity of ants was measured by counting the number of ants that entered a 2 x 5 cm rectangle marked about 1.5m up the main trunk in a 30s period. Because ants were too numerous to keep track of individuals, it is likely that some individuals were counted multiple times during this and subsequent measurements. A live katydid was attached to a branch near the main trunk at breast height with a plastic clothespin. This procedure did not injure the plant and the katydid was unable to graze the tree. Thus, ants were responding to the presence of a clothespin and katydid, not to grazing damage. The elapsed time to the initial bite or sting (=attack) inflicted to the katydid and the total number of attacks during the 90s period the katydid was attached to the tree were recorded as "response time" and "attack rate", respectively. In the 19 cases (out of a total of 84) where the katydid was not attacked, a response time of 90s and an attack rate of zero were used as data. After removing the katydid, I struck the tree 7 times to assure the ants were disturbed. I then counted the number of ants that entered the 2 x 5 cm rectangle in 30s and termed this value "post-disturbance activity".

Data for each variable (i.e., patrolling activity, response time, attack rate, and post-disturbance activity) were analyzed with a two-factor ANOVA with ant species (P. spinicola and P. nigrocinctus group vs. P. flavicornis) and time period (morning vs. afternoon) as the two factors and a species x time interaction term.

Measures of antiherbivore effectiveness of ants (i.e., patrolling activity, response time, attack rate, and post-disturbance activity) did not differ significantly between ant species or time of day (Table 1). However, there were significant species x time interactions that indicated the P. spinicola / P. nigrocinctus group was more active in the morning while P. flavicornis was more active in the afternoon (Table 1, Fig. 1). During the morning and afternoon, the "constitutive" levels of patrolling activity of all ant species were less than the "induced" levels of activity following disturbance (Fig. 1A). It is important to note that ants attacked the katydid simply because of its presence and not due to grazing damage caused by the katydid, which did not graze on the trees. Katydids responded to attacks by acacia-ants by attempting to escape, demonstrating that the ants could successfully defend their host from herbivory. Because the katydids were unable to escape the ants, several were killed by the attacking ants.

The belief that P. spinicola is more aggressive, and thus a better mutualist than P. flavicornis, was not supported by the data. All species of ants (1) had similar levels of patrolling activity and post-disturbance activity (Table 1, Fig. 1A), (2) responded to the presence of an herbivore with similar swiftness (Table 1, Fig. 1B), and (3) inflicted similar numbers of attacks to the herbivore (Table 1, Fig. 1C). Differences between the Pseudomyrmex species only emerge when the temporal component of their activity is considered (Table 1). In the morning, the P. spinicola / P. nigrocinctus group appears to be the superior mutualist (i.e., responds quickly and attacks aggressively) and in the afternoon, P. flavicornis appears to be the better mutualist. Ecologists recognize that temporal and spatial variation in chemical and other defenses make it more difficult for herbivores to circumvent these defenses by presenting grazers with a moving target (Denno and McClure 1983, Karban et al. 1997). Having multiple species of mutualistic ants could be advantageous because the temporal and spatial (i.e., among-tree) variation created by multiple ant species make it more difficult for grazers to predictably choose safe foraging periods.

Interspecific variation occurs in other plant-ant systems, and can range from ant species being very effective against herbivores to species being so ineffective that they are considered parasites of plant x ant mutualisms (Janzen 1975, McKey 1984, Rico-Gray and Thien 1989, Longino 1991). However, little is known about how interspecific differences in ant activity varies temporally. For ant species that protect their host from herbivores, their levels of activity can be rapidly induced by disturbance (McKey 1984, Young et al. 1989, Agrawal 1996), which could minimize costs associated with the defense. For example, the difference in the "constitutive" pre-disturbance (i.e., patrolling) activity and the "induced" post-disturbance activity observed in Fig. 1A probably represents a large difference in the energy being expended by the ant colony, whose energy ultimately comes from its host tree. Maintaining minimal patrolling activity and increasing activity only when the host is threatened, at which time the additional cost of maintaining the increased activity can be offset by higher levels of protection, could minimize costs of ant defenses, in the same manner that induction or activation of structural or chemical defenses are believed to minimize defensive costs (Harvell 1990, Baldwin 1994)

Acknowledgments

This project originated from discussions with Rodolfo Dirzo. Nancy Greig and John Blake provided valuable instruction and other OTS 93-1 friends provided much enjoyment and moral support. Many thanks go to the Organization for Tropical Studies, the University of North Carolina at Chapel Hill, and Mark Hay for encouragement and financial support during this project. Steve Blumenshine, John Longino, and an anonymous reviewer provided helpful comments on earlier versions of the manuscript.

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Figure Legends

 

Figure 1. Responsiveness of P. spinicola / P. nigrocinctus (squares) and P. flavicornis (triangles) during the morning and afternoon, plotted as means (± 1 SE) of 21 samples each. (A) Pre-disturbance activity (open symbols) versus post-disturbance activity (filled symbols). (B) Time required for a katydid to be first attacked. (C) Number of times a katydid was attacked during 90s following attachment to an ant-acacia.

 

 

Table 1. ANOVA table for the four measures of ant activity which are graphed in Figure 1.