Facilitated exploitation of pollination mutualisms: fitness consequences for plants

Abstract

Summary1. Mutualisms are only rarely one-to-one interactions: each species generally interacts with multiple mutualists. Exploitation is ubiquitous in mutualisms, and we would therefore expect that each mutualist interacts with multiple exploiters as well. Exploiter species may also interact with one another. For example, the action of one exploiter species might open the opportunity for exploitation by a second species. 2. Exploitation is common in many plant-pollinator mutualisms: 'primary' nectar robbers feed through holes they make in flowers, which can be subsequently used by 'secondary' nectar robbers unable to create holes themselves. The overall effect of nectar robbing on plant fitness is often (although not always) negative. No study has separated the effects of interacting with primary vs. secondary robbers. 3. Here, we examine the effects of primary vs. secondary nectar robbing on pollinator visitation rate and female fitness in Ipomopsis aggregata. Manipulating the type of nectar robbing that flowers experienced, we found that secondary nectar robbing inflicted fitness costs to plants beyond that inflicted by primary robbing alone. Secondary nectar robbing significantly reduced pollen receipt to flowers, as well as fruit and seed production. Although the causes are elusive, the effect may be attributed to changes in pollinator behaviour at these plants. 4. Synthesis. Our findings provide evidence that interacting with multiple exploiters can lead to increased negative effects for mutualists, and highlight the importance of incorporating multiple exploiters into the conceptual framework of mutualism.

Nectar robbers deter legitimate pollinators by mutilating flowers

“…Although nectar robbing is ubiquitous in various bee families, genera and species, long‐tongued bees belonging to Apidae predominate in the list (Irwin et al ). Regardless of taxonomic affiliation, the robbed flowers have a long corolla tube or nectar spur (Irwin et al , Maruyama et al , Richman et al , Ye et al ). Reports of short‐tongued bees as primary nectar robbers are scarce in the literature despite the mismatch of their short tongue lengths with the long corolla tubes of many flowers.…”

“…These changes in pollinator traits occur if robbing alters crucial floral traits that attract pollinators to the flowers, such as nectar dynamics and flower morphology (Irwin and Brody , Dohzono et al , Irwin et al , Ye et al ). The effect of nectar robbing on nectar dynamics and the associated changes in pollinator fauna and behavior have received some attention (Morris , Irwin and Brody , Dohzono et al , Irwin et al , Mayer et al , Richman et al , Ye et al ). In some plants, the altered nectar resecretion pattern led to desertion of robbed flowers by the legitimate nectar foragers, which in turn negatively affected plant reproduction (Roubik ).…”

“…In L. aspera , the robber slits the most conspicuous part of the flower – the lower petal – altering the overall appearance of the flower from the front. Some pollinators have behaviorally adapted to robbing and learned to harvest nectar as secondary nectar robbers (Richman et al , Varma and Sinu ). But, this is possible only if the pollinators can at least land on the robbed flowers.…”

“…They are considered secondary nectar robbers (Irwin and Maloof , Irwin et al , Richman et al ). The secondary nectar‐robbers consist of either a new set of flower visitors that previously had no access to floral nectar through the legitimate flower entrance (Varma and Sinu ) or some existing legitimate visitors (Richman et al , Varma and Sinu ). Short‐tongued bees are likely to be primary nectar robbers owing to a mismatch in the floral (long tube) and the animal trait (short tongue).…”

“…The impact of nectar robbing is often assessed from the plants’ perspective (Bronstein et al , citations in Irwin et al ). Only a few studies assess it from the perspective of the forager (Zimmerman and Cook , Irwin and Brody , Maloof and Inouye , Gonzalez‐Gomez and Valdivia , Richman et al , Varma and Sinu ). Some studies suggested that nectar robbing has an indirect favorable outcome for plants as it increases both the legitimate and illegitimate visitation rates of pollinators to robbed flowers (Navarro , Sampson et al , Varma and Sinu ).…”