Host-Plant Mediation of Insect Mutualisms: Variable Outcomes in Herbivore-Ant Interactions
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Host-Plant Mediation of Insect Mutualisms: Variable Outcomes in Herbivore-Ant Interactions J. Hall Cushman Oikos, Vol. 61, No. 1. (May, 1991), pp. 138-144. Stable URL: http://links.jstor.org/sici?sici=0030-1299%28199105%2961%3A1%3C138%3AHMOIMV%3E2.0.CO%3B2-N Oikos is currently published by Nordic Society Oikos. Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/about/terms.html. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/journals/oikos.html. 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Sci., Macquarie Univ., Sydney, NSW 2109, Australia Summary. I present and evaluate the hypothesis that host plants Ants are one of the most ubiquitous mutualists found indirectly affect the fitness of many homopterans and lepidop- in nature, forming close and often mutualistic associa- terans by mediating the outcome of their interactions with ants. W o conditions must be met to support this contention. First, tions with a variety of plants, fungi, and animals, partic- the attractiveness of herbivores to ants must vary predictably ularly herbivorous insects in the Homoptera and Lep- with intra- andlor interspecific changes in host-plant quality. idoptera (Wilson 1971, Carroll and Janzen 1973. Bent- Such variation will occur if a) the chemical composition andlor quantity of ant attractants (excretions and secretions) produced ley 1977, Thompson 1982, Beattie 1985, Sudd and by herbivores varies with changes in host quality and b) ants Franks 1987, Holldobler and Wilson 1990). While herb- preferentially tend those herbivores that produce the most nu- ivore-ant associations have received considerable atten- tritionally rewarding attractants. Second, the number of tend- tion during the past century (see reviews by Hinton ing ants must have a significant effect on the fitness of herb- 1951, Nixon 1951, Way 1963, Cottrell 1984, Buckley ivores. While there is abundant evidence to support these indi- vidual conditions, few studies have examined both conditions 1987, Pierce 1987, Sudd 1987), few studies address the for a single herbivore-ant association. influence of host plants on the outcome of herbivore-ant I outline a series of testable predictions based on the host- interactions and no study outlines the mechanisms by mediation hypothesis. 1) The effects of host plants will vary with which such effects can occur. the degree to which herbivores depend on ants. 2) Hosts will affect the ability of herbivores to compete for ant mutualists. 3) In this paper, I develop the hypothesis that host Tended herbivores will exhibit host-selection behaviors that in- plants -g enerate si-g nificant variabilitv in the outcome of crease their ability to attract ants. And most importantly, 4) interactions between herbivores and their tending ants. variation in host quality will predict fluctuations in the strength and sign of herbivore-ant interactions. I present a graphical I argue that such host-plant mediation can influence model to illustrate 1) the ways in which plant-induced variation these interactions, and the selection pressures which in the value of attractants to ant colonies can be used to predict accompany them, in two fundamentally different ways. switchpoints in the behavior of ants and 2) the effects of distance First, the strength of mutualistic interactions can fluctu- to servicing ant nests and nutritional status of these colonies on +). the predictions. ate from strong to weak ( + + + t o In these situa- tions. selection pressures will be weak but consistent (i.e., in the same direction). By contrast, the sign of interactions can fluctuate from mutualism to antag- onism (+ to -). When such reversals occur, the actual An increasing number of studies demonstrate the vari- direction of selection changes and selection becomes a able and context-dependent nature of mutualistic inter- disruptive force, favoring traits (behaviors and mor- actions (see Thompson 1982, 1988, Addicott 1984, Jor- phologies) that facilitate the association in certain sit- d a n ~19 87, Herrera 1988, Cushman and Addicott in uations and favoring very different and perhaps oppos- press). The outcome of these interactions varies in ing traits in others. space and time in response to a range of biotic and Here, I present and evaluate the mechanisms by abiotic factors. Unfortunately, very little is known which host plants can indirectly mediate herbivore-ant about the extent, mechanisms, and implications of this interactions. I then use this framework to address vari- variation, and such information is essential for devel- ous implications of host-plant mediation, with particular oping a realistic understanding of the ecology and evo- emphasis on how plants alter the strength and sign of lution of mutualism. these insect interactions. ants independently. Herbivore aggregations that form Herbivore-ant associations on plants with extrafloral nectaries will be more likely to Both homopteran-ant and lepidopteran-ant associations be located and subsequently tended by ants than aggre- are common mutualisms found in temperate and trop- gations forming on hosts without such structures. This is ical regions. In homopteran-ant associations, ants tend supported by Buckley (1983), Maschwitz et al. (1984). phloem-feeding homopterans (primarily those in the and Sudd and Sudd (1985) who show or suggest that Aphididae. Membracidae, Coccidae, and Pseudococci- ants commonly switch from visiting extrafloral nectaries dae) and harvest their excretions ("honeydew"). In lep- to visiting tended herbivores (although see Becarra and idopteran-ant associations, ants tend leaf-chewing but- Venable (1989) who claim that the reverse can also terfly larvae (those in the Lycaenidae and Riodinidae), occur). Given that oviposition by many lycaenid species and harvest their secretions (see also DeVries and Baker is dependent upon the presence of ants (Atsatt 1981b, (1989) who document that larvae of a riodinid species Pierce and Elgar 1985, Smiley et al. 1988. Baylis 1989, consume their host's extrafloral nectar). Through their Baylis and Pierce in press), host plants with extrafloral tending, ants can provide a range of beneficial services nectaries may influence tended lepidopterans in a simi- to both homopterans and lepidopterans, particularly lar fashion. protection from natural enemies, but also increased In this paper, I examine a second and potentially feeding rates. decreased emigration, reduced fungal in- more common mechanism for indirect host mediation festations, construction of protective shelters. and pro- that involves the response of ants to herbivore excre- vision of parental care (see reviews by Hinton 1951, tions and secretions of variable composition and quan- Nixon 1951, Way 1963, Cottrell 1984, Beattie 1985, tity. Clearly, other indirect effects can also operate in Buckley 1987, Pierce 1987). such associations, but I will not discuss them because The excretions and secretions of tended herbivores they concern the ways in which host plants can in- provide an important food source for associating ant directly benefit from being infested by ant-tended ho- colonies (Way 1963, Carroll and Janzen 1973, Pierce et mopterans (Messina 1981, Buckley 1983, 1987, Fritz al. 1987, Fiedler and Maschwitz 1988. Nash 1989, Pierce 1983, Beattie 1985, Compton and Robertson 1988). 1989). The chemical composition of homopteran honey- dew closely parallels that of host-plant phloem fluids and contains a variety of sugars, organic acids, alcohols, plant hormones, salts, vitamins. amino acids, and Mechanisms and evidence amides (Auclair 1963, Dixon 1985, Klingauf 1987). Al- though not as well documented, lepidopteran secretions Two conditions must be met to document that host have also been shown to consist of numerous sugars and plants indirectly mediate the fitness of tended herb- amino acids (Maschwitz et al. 1975, Pierce 1984, 1987, ivores via ants. First, the attractiveness of herbivores to 1989. Fiedler and Maschwitz 1988). ants must vary predictably with intra- andlor interspec- ific changes in host-plant quality. Such variation will occur if a) the chemical composition andlor quantity of ant attractants produced by herbivores varies with Direct and indirect effects of plants