Measuring The Effects Of Pollinators And Herbivores: Evidence For Non-Additivity In A Perennial Herb - Statistical Data Included

Ecology, August, 2000 by Carlos M. Herrera

CARLOS M. HERRERA [1]

Estacion Biologica de Donana

Abstract. Using an experimental approach, this study addresses the following two questions for the perennial herb Paeonia broteroi (Paeoniaceae) at a location in southeastern Spain. (1) What are the relative magnitudes of the effects of pollinators and herbivores (invertebrates and vertebrates feeding on flowers and developing fruits) on maternal fecundity (total seed production per plant)? (2) Are the effects of pollinators and herbivores on fecundity additive, or is there some significant interaction between them? A two-factor ("Pollinators" and "Herbivores," each with two levels, "present" and "excluded") experimental design was used, with individual plants being treated as experimental units and maternal fecundity as the response variable. On average, the effects of pollinators and herbivores were of opposite sign and roughly similar absolute magnitude ([sim]7.5 seeds per plant), thus approximately canceling each other. A significant interaction (non-additivity) between factors did exist, with plants exp osed to pollinators experiencing a disproportionately higher incidence of herbivores than those from which pollinators had been excluded. This was mainly due to mammals browsing only on the larger fruits from flowers that had been exposed to pollinators. Only in the absence of herbivores did pollinators account for a significant amount of between-plant variance in maternal fecundity. It is concluded that the interaction between pollinators and herbivores will lead to variable, herbivore-dependent "opportunity for selection" (sensu Arnold and Wade 1984) on P. broteroi by its pollinators. Regional variation in herbivore incidence experienced by P. broteroi populations will presumably generate local variation in the degree of adaptedness of the plant to its pollinators.

Key words: fruit selection; herbivory; indirect interactions; mammalian herbivores; maternal fecundity; Mediterranean; non-additive effects; Paconia broteroi; perennial herbs; pollination; seed production.

INTRODUCTION

Possibly because of their inherent biological complexities, plant--animal interactions traditionally have been studied after exercising some sort of conceptual abstraction based on functionality. With relatively few exceptions, the research program on plant--animal interactions has generally produced "single-interaction" studies focusing on just one kind of interaction (i.e., herbivory, pollination, or seed predation studies, some of the most commonly studied interaction categories). This compartmentalization, albeit convenient, leads to an artificial oversimplification, as most plant populations and individuals presumably "perceive," over ecological and evolutionary time, the composite result of their interactions with a broad array of animal interactors. Whenever efforts at realism and completeness have been undertaken, evidence has been gathered showing that different sets of plant interactors (e.g., herbivores, pollinators, seed predators, seed dispersers) combine to exert an intricate influence on plant s (e.g., Heithaus et al. 1982, Schemske and Horvitz 1988, Herrera 1989, 1993, Cunningham 1995). Considering the most popular cases of herbivores and pollinators, a number of recent studies have illustrated that interaction between herbivory and pollination is not confined to the relatively infrequent case in which the same organisms play a dual role as both herbivores and pollinators (e.g., Wiebes 1979, Pellmyr 1992, Pettersson 1992, Powell 1992), and have documented the complex influence frequently exerted on plants by the combined action of these two sets of functionally contrasting interactors. These investigations have shown, for example, that herbivores have the capacity to indirectly modulate the nature, strength, and consequences of the interaction between plants and their animal pollinators (Karban and Strauss 1993, Quesada et al. 1995, Lohman et al. 1996, Mutikainen and Delph 1996, Strauss et al. 1996, Lehtila and Strauss 1997, Strauss 1997). It has also been shown that plant reproductive traits may sometimes reflect a compromise between the conflicting selective pressures exerted by pollinators and herbivores (Brody 1992, Euler and Baldwin 1996, Brady and Mitchell 1997, Ehrlen 1997, Strauss 1997, Kudoh and Whigham 1998) and that the concurrent interaction of plants with their herbivores and pollinators may help to explain the macroevolutionary patterns of defense and reward systems in some plant lineages (Armbruster 1997, Armbruster et al. 1997).

The present paper is an attempt at contributing to this recent line of inquiry, which focuses on the implications of the interaction between herbivores and pollinators. Using an experimental approach, I will evaluate the relative importance of pollinators and herbivores as determinants of maternal fecundity in the perennial herb Paeonia broteroi. As a way of illustrating some of the perils involved in studying plant--animal interactions as dissociated functional categories, particular attention will be paid to the issue of possible non-additive effects of these two particular sets of interactors. Specifically, I address two questions. (1) What are the respective magnitudes of the effects of pollinators and herbivores on the maternal fecundity of Paeonia broteroi individuals? (2) Do the effects of pollinators and herbivores on fecundity merely add up, or, alternatively, is there some significant interaction (non-additivity) between them?