Balancing anti‐herbivore benefits and anti‐pollinator costs of defensive mutualists

Abstract

Abstract. Quantifying costs and benefits of ostensibly mutualistic interactions is an important step toward understanding their evolutionary trajectories. In food-for-protection interactions between ants and extrafloral nectar (EFN)-bearing plants, tending by aggressive ants may deter herbivores, but it may also deter pollinators. The fitness costs of pollinator deterrence are not straightforward for long-lived iteroparous plants, because reproductive vital rates often contribute weakly to fitness relative to growth and survival (vital rates that may be enhanced by ant defense). We used field manipulations of ant and pollinator activity and demographic modeling to examine how pollination costs of ant defense translate to plant fitness, given the benefits of ant defense elsewhere in the plant life cycle. We contrasted the net fitness effects of alternative ant partner species. Our work focused on the tree cholla cactus, Opuntia imbricata, an EFN-bearing plant associated with two ant species (Crematogaster opuntiae and Liometopum apiculatum) that differ in quality of defense against insect herbivores. We found that ant defense imposed pollination costs, despite evidence for antrepellent floral volatiles and temporal partitioning of ant and pollinator activity. The two partner species similarly reduced pollinator visitation and seed mass, and one (C. opuntiae) additionally reduced seed number. We used the experimental data and other long-term demographic data to parameterize an integral projection model that integrated costs and benefits of ant defense over the complete plant life cycle. Model results indicated that the pollination costs of L. apiculatum were balanced by beneficial effects on growth, leading to a net fitness effect that was neutral to positive. By contrast, pollination costs outweighed benefits for C. opuntiae, the weaker defender, rendering this species a reproductive parasite. Thus, we infer that pollination costs destabilize mutualism with one partner species, but are offset by strong defensive benefits provided by the other, leading to contrasting selective pressures imposed by alternative associations. Accounting for ontogenetic turnover in ant partner identity indicated that most plants avoid the parasitic effects of C. opuntiae by associating nonrandomly with L. apiculatum at reproductive life stages. Our results highlight the value of a demographic approach to quantifying the costs and benefits of mutualism.

Net neutral effects of a generalist vertebrate predator on seed production result from simultaneous suppression of plant antagonists and mutualists

“…Our findings are inconsistent with some previous studies, in which the net effects of generalist predators on plant seed production are all positive (e.g., ants in Altshuler 1999; Ohm & Miller 2014;crab spiders in Louda 1982;Romero & Vasconcellos-Netor 2004;and Romero et al 2008). One possible explanation is that the intermediate herbivore species utilize different plant parts.…”

“…Similar effects were also found in the flower-dwelling spider species Misumenops argenteus (Romero & Vasconcellos-Netor 2004). More recently, Ohm and Miller (2014) revealed that several ant species (Crematogaster opuntiae and Liometopum apiculatum) reduced pollinator visitation and seed production in the cholla cactus Opuntia imbricate, and this negative effect on plants could be balanced by the benefits of long-term protection from herbivores provided by the ants. Nevertheless, these studies focus exclusively on invertebrate predators, and the empirical evidence for the dual functional role of predators on plant fitness is still sparse for single predator species, and completely lacking for terrestrial vertebrate predators.…”

“…This study, together with several other case studies (Louda 1982;Romero & Vasconcellos-Netor 2004;Romero et al 2008;Ohm & Miller 2014), suggests that a single generalist predator can affect plant fitness in an alternative direction through negative and positive trophic cascading effects by simultaneously suppressing plant mutualists and antagonists. Moreover, because generalist predators often stand simultaneously at different trophic positions in different types of food webs (e.g.…”

The effect of demographic correlations on the stochastic population dynamics of perennial plants

“…Helianthella quinquenervis occurs in wet and boggy montane meadows of Western North America (Weber 1952). Our data came from a population at Sevilleta National Wildlife Refuge in central New Mexico, USA (34°20′5.3″ N, 106°37′53.2″ W), where 1001 unique individuals were censused between 2004 and 2015 (see Miller et al [2009] and Ohm and Miller [2014] for details of study site and data collection). Opuntia imbricata is a cactus found throughout the deserts and arid grasslands of Southwestern North America (Benson 1982).…”

The Ecology of Extrafloral Nectar in Senna mexicana var. chapmanii

“…Flower visits by this insect were significantly more frequent, and their duration significantly longer, on plants with ants present. This result was surprising, as aggressive ants have more often been seen to deter pollinators (Ness 2006;Assunção et al 2014;Ohm and Miller 2014), and pollinators have been observed to recognize the danger posed by ants (Hernández-Cumplido et al 2010;Assunção et al 2014). We are not alone, however, in observing increased pollination rates in the presence of ants.…”