Indirect Effects of Other Species

Ecologists traditionally have focused on pairs of species that interact directly (i.e., through energy or material transfers, as described earlier in this chapter). However, indirect interactions, such as reduced predation on mimics when the models are present, have received less attention but may be at least as important as direct effects. For example, pollinators can augment plant reproduction suffi ciently to compensate for herbivory, thereby indirectly affecting plant-herbivore interaction (L. Adler et al. 2001, Strauss and Murch 2004). Batzer et al. (2000b) reported that indirect effects of predaceous fish on invertebrate predators and competitors of midge prey had a greater effect on midge abundance than did direct predation on midges.

Tritrophic-level interaction has been recognized as a key to understanding both herbivore-plant and predator-prey interactions (e.g., Boethel and Eiken-bary 1986, Price et al. 1980). Even tritrophic-level interaction represents a highly simplified model of communities (Gutierrez 1986) in which species interactions with many other species are affected by changing environmental conditions (see Chapters 9 and 10). The tendency for multiple interactions to stabilize or destabilize species populations and community structure has been debated (Goh 1979, May 1973, 1983, Price 1997). May (1973) proposed that community stability depends on predator-prey interactions being more common than mutualistic interactions. Because multispecies interactions control rates of energy and nutrient fluxes through ecosystems, resolution of the extent to which indirect interactions contribute to stability of community structure will contribute significantly to our understanding of ecosystem stability.

Associated species affect particular interactions in a variety of ways. For example, much research has addressed the negative effects of plant defenses induced by early-season herbivores on later colonists (Fig. 8.11) (e.g., Harrison and Karban 1986, M. Hunter 1987, Kogan and Paxton 1983, N. Moran and Whitham 1990, Sticher et al. 1997, Van Zandt and Agrawal 2004, Wold and

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Differential survival to pupation (a) and mean female pupal weight (b) of Diurnea flagella on foliage that was undamaged, naturally damaged by folivores, and produced following damage. Vertical lines represent standard errors of the mean. Diurnea flagella larvae feeding on regrowth foliage show both reduced survival to pupation and reduced pupal weight. From M. Hunter (1987) with permission from Blackwell Scientific.

Marquis 1997) and on decomposers (Grime et al. 1996). Survival and development of late-season herbivores usually are reduced by defenses induced by early-season herbivores.

Herbivore-induced defenses can affect other interactions as well. Callaway et al. (1999) reported that the tortricid moth, Agapeta zoegana, introduced to the western United States for biological control of spotted knapweed, Centaurea maculosa, increased the negative effect of its host on native grass, Festuca ida-hoensis. Reproductive output of grass was lower when neighboring knapweed had been defoliated by the moth, compared to grass surrounded by nondefoli-ated neighbors. Callaway et al. (1999) suggested that defenses induced by the moth also had allelopathic effects on neighboring plants or altered root exudates that affected competition via soil microbes.

Baldwin and Schultz (1983) and Rhoades (1983) independently found evidence that damage by herbivores can be communicated chemically among plants, leading to induced defenses in plants in advance of herbivory (see also Zeringue 1987). Although their hypothesis that plants communicate herbivore threat chemically with each other was challenged widely because of its apparent incon-gruency with natural selection theory (e.g., Fowler and Lawton 1985), studies have confirmed the induction of chemical defenses by volatile chemical elicitors, particularly jasmonic acid (Fig. 8.12) and ethylene (Farmer and Ryan 1990, McCloud and Baldwin 1997, Schmelz et al. 2002, Sticher et al. 1997,Thaler 1999a, Thaler et al. 2001). Jasomonate has been shown to induce production of pro-teinase inhibitors and other defenses against multiple insects and pathogens when applied at low concentrations to a variety of plant species (Fig. 8.13),including conifers (Hudgins et al. 2003, 2004, Thaler et al. 2001). Interplant communication via jasmonate has been demonstrated among unrelated species and even unrelated families (e.g., Farmer and Ryan 1990), although the fitness consequences of interspecific communication are not clear (Karban and Maron 2002). Thaler (1999b) demonstrated that tomato, Lycopersicon esculentum, defenses induced by jasmonate treatment doubled the rate of parasitism of armyworm, Spodoptera exigua, by the wasp, Hyposoter exiguae.

Endophytic or mycorrhizal fungi (see Chapter 3) can affect interactions between other organisms (E. Allen and Allen 1990, G. Carroll 1988, Clay 1990). G. Carroll (1988) and Clay et al. (1985) reported that mycotoxins produced by mutualistic endophytic fungi complement host defenses in deterring insect herbivores. Clay et al. (1993) documented complex effects of insect herbivores and communicates plant damage and induces defensive chemical production in neighboring plants. From Farmer and Ryan (1990) with permission from National Academy of Sciences.

communicates plant damage and induces defensive chemical production in neighboring plants. From Farmer and Ryan (1990) with permission from National Academy of Sciences.

Structure of methyl jasmonate, a volatile plant chemical that

Structure of methyl jasmonate, a volatile plant chemical that

Control I Low JA I High JA

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Armyworm larvae

Armyworm pupae

Looper larvae

Survival of beet armyworm, Spodoptera oexigua, larvae and pupae and cabbage looper, Trichoplusia ni, larvae on field-grown tomatoes sprayed with low (0.5 mM) or high (1.5 mM) doses of jasmonic acid, or unsprayed (control). Vertical lines represent 1 SE. From Thaler et al. (2001) with permission from Blackwell Scientific Ltd. Please see extended permission list pg 571.

endophytic fungi on the competitive interactions among grass species. For example, tall fescue, Festuca arundinacea, competed poorly with orchard grass, Dactylis glomerata, when herbivores were absent, but fescue infected with its fungal endophyte, Acremonium spp., competed better than either orchard grass or uninfected fescue when herbivores were present. Mycorrhizae transport nutrients among plants through the hyphal network, mediating plant competition (E. Allen and Allen 1990). Gange et al. (1999) and Goverde et al. (2000) experimentally inoculated plants with arbuscular mycorrhizal fungi and evaluated effects on aphids, Myzus persicae, and butterfly, Polyommatus icarus, larvae, respectively. In both studies, mycorrhizal inoculation increased insect growth and survival, apparently related to increased P concentrations in foliage of mycor-rhizal plants. Goverde et al. (2000) further reported that herbivore performance was related to the species of mycorrhizae colonizing the host plant. Sooty molds growing on foliage may affect palatability for herbivores (Fig. 8.14).

Volatile defenses of plants induced by defoliators often attract the herbivore's predators and parasites (e.g., Kessler and Baldwin 2001, Price 1986, Thaler et al. 1999b, Turlings et al. 1990,1993,1995). At the same time, however, plant defenses sequestered by herbivores can affect herbivore-predator and herbi-

Indirect Planting

| Indirect effects of associated species. The light-colored foliage at the ends of shoots is new grand fir, Abies grandis, foliage produced during 1994, a dry year, in western Washington; the blackened 1993 foliage was colonized by sooty mold during a wet year; normal foliage prior to 1993 was produced during extended drought. Sooty mold exploits moist conditions, especially honeydew accumulations and, in turn, may affect foliage quality for folivores.

| Indirect effects of associated species. The light-colored foliage at the ends of shoots is new grand fir, Abies grandis, foliage produced during 1994, a dry year, in western Washington; the blackened 1993 foliage was colonized by sooty mold during a wet year; normal foliage prior to 1993 was produced during extended drought. Sooty mold exploits moist conditions, especially honeydew accumulations and, in turn, may affect foliage quality for folivores.

vore-pathogen interactions (L. Brower et al. 1968, Stamp et al. 1997, Tallamy et al. 1998, Traugott and Stamp 1996). Inflorescence spiders preying on pollinators affect the pollinator-plant interaction (Louda 1982). Herbivores feeding above ground frequently deplete root resources through compensatory translocation and negatively affect root-feeding herbivores (e.g., Masters et al. 1993, Rodgers et al. 1995, Salt et al. 1996).

Chilcutt and Tabashnik (1997) examined the effect of diamondback moth, Plutella xylostella, resistance to Bacillus thuringiensis on within-host interactions between the pathogen and the parasitoid wasp, Cotesia plutellae. Resistant caterpillars reduced the success of both pathogen and parasitoid. In susceptible caterpillars, by contrast, the pathogen had a significant, negative effect on the parasitoid, but the parasitoid had no effect on the pathogen. In moderately resistant hosts, competition between the pathogen and parasitoid was symmetrical:

each had a significant negative effect on the other. Highly resistant hosts provided a refuge from competition for the parasitoid.

Ants affect, and are affected by, a variety of other interactions. Ants attracted to domatia, to floral or extrafloral nectories, or to aphid honeydew commonly affect herbivore-plant interactions (Cushman and Addicott 1991, Fritz 1983, Jolivet 1996, Oliveira and Brandao 1991,Tilman 1978).The strength of this interaction varies inversely with distance from ant nests. Tilman (1978) reported that ant visits to extrafloral nectaries declined with the distance between cherry trees and ant nests. The associated predation on tent caterpillars by nectar-foraging ants also declined with distance from the ant nest.

Currie (2001) and Currie et al. (1999a, b) reported complex interactions between fungus-growing ants, especially leaf-cutting species of Atta and Acromyrmex, their mutualistic fungi, species of Leucocoprinus and Leucoagari-cus, and associated microorganisms. The ants provide live or dead vegetable material for fungal decomposition, tend the gardens by weeding alien microbes, and feed on the fungus. Foundress queens carry fungus inoculum to establish new colonies. The fungus gardens have been discovered to host a virulent fungal pathogen, Escovopsis, capable of destroying the fungus garden and the dependent ant colony. The ants have an additional mutualistic association with an actin-omycete bacterium that produces specialized antibiotics with potent inhibitory activity against Escovopsis.

Similarly complex interactions among a community of invertebrates and fungi affect bark beetle interactions with host trees (see earlier in this chapter). The southern pine beetle once was thought to have a mutualistic association with blue-stain fungi, with beetles providing transport and the fungus contributing to tree death and beetle reproduction. However, several studies have shown that this beetle can colonize trees in the absence of the fungus (Bridges et al. 1985); that the blue-stain fungus is, in fact, detrimental to beetle development and is avoided by the mining beetles (Barras 1970, Bridges 1983, Bridges and Perry 1985); and that other mycangial fungi are necessary for optimal beetle development (Ayres et al. 2000, Bridges and Perry 1985). Subsequent research demonstrated that phoretic tarsonemid mites collect spores of the blue-stain fungus in specialized structures, sporothecae (Fig. 8.15) (Bridges and Moser 1983, Moser 1985). Beetles carrying these mites transport the blue-stain fungus significantly more often than do mite-free beetles (Bridges and Moser 1986). The beetle-tree interaction is affected further by phoretic predaceous mites that prey on nema-tode parasites of the beetle (Kinn 1980). Finally, folivorous insects increase tree susceptibility to colonization by bark beetles (Wallin and Raffa 2001).

Termite interaction with mutualistic gut symbionts is affected by host wood and associated fungi. Using forced feeding and preference tests involving combinations of several conifer species and fungi, Mankowski et al. (1998) found that termite preferences for wood-fungal combinations generally reflected the suitability of the resource for the gut fauna, as indicated by changes in gut faunal densities when termites were forced to feed on wood-fungus combinations.

Competitive interactions between a pair of species may be modified by the presence of additional competitors. Pianka (1981) proposed a model in which two species with modest competitive overlap over a range of resource values could

Species That Benefit From Each Other
| Ascospores of Ceratocystis minor in sporothecae (arrows) formed by tergite 1 on the ventral-lateral sides of a Tarsonemus ips female, phoretic on the southern pine beetle, Dendroctonus frontalis. From Moser (1985) with permission from the British Mycological Society.

become "competitive mutualists" with respect to a third species that could compete more strongly for intermediate resource values. The two species benefit each other by excluding the third species from both sides of its resource spectrum (niche).

Competitive interactions among several species also can be modified by predators. A predator that preys indiscriminately on several competing prey species, as these are encountered, will tend to prey most often on the most abundant prey species, thereby preventing that species from competitively suppressing others. R. Paine (1966, 1969a, b) introduced the term keystone species to refer to top predators that maintain balanced populations of competing prey species. However, this term has become used more broadly to include any species whose effect on community and ecosystem structure or function is disproportionately large, compared to its abundance (Bond 1993, Power et al. 1996). Some insect species play keystone roles. For example, many herbivorous insects affect plant competitive interactions by selectively reducing the density of abundant host species and providing additional space and resources for nonhost plants (Louda et al. 1990a, Schowalter and Lowman 1999), thereby affecting resources available for associated species.

Although it often is convenient to emphasize the adaptive aspects of species interactions, especially symbiotic interactions, modern associations may not represent co-evolved relationships. Connell (1980) noted that niche partitioning and other adaptations that minimize competition among living species may reflect competition among their ancestors. Janzen and Martin (1982) suggested that current seed-dispersing animals may have replaced extinct species with which plants co-evolved mutualistic associations in the past. For example, large-seeded fruits in North and South America may reflect adaptation for dispersal by extinct gomphotheres and ground sloths; smaller extant vertebrates now perform this role but are much less capable of transporting such seeds over distances necessary for colonization.

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