Resource availability affects competition and predation. If suitable resources (plants or animal prey) become more abundant, resource discovery becomes easier, and consumer
245 II. fACTorS AffECTIng InTErACTIonS
populations grow. Increased probability of close contact and competition among con- sumers leads to densities at which superior competitor(s) suppress or exclude inferior competitors. As a result, the intensity of interspecific competition may peak at inter- mediate levels of resource availability, although the overall rate of resource use may continue to rise with increasing availability (depending on functional and numerical re- sponses). Population outbreaks reduce resource availability and also reduce populations of competing species.
Interactions are affected by landscape heterogeneity. Sparse resources in heteroge- neous habitats tend to maintain small, low-density populations of associated species. The energetic and nutrient costs of detoxifying current resources or searching for more suit- able resources limit growth, survival and reproduction (see Chapters 3 and 4). Under these conditions, potentially interacting species are decoupled in time and space, co-occurring infrequently among landscape patches (Covich et al. 2009, Tack et al. 2009). Hence, com- petition is minimized, and predator-free space is maximized. In contrast, more homoge- neous environments facilitate population spread of associated species and maximize the probability of co-occurrence.
Palmer (2003) explored the effect of termite-generated heterogeneity in resource availability on the competitive interactions of four ant species that reside on acacia, Aca- cia drepanolobium, in East Africa. Only one ant species occupied an individual tree at any given time, and violent interspecific competition for host trees by adjacent colonies was common. Acacia shoot production and densities of litter invertebrates increased with proximity to termite mounds. The competitively dominant ant, Crematogaster sjostedti, displaced other acacia ants, Crematogaster mimosae, Crematogaster nigriceps, and Tetraponera penzigi, near termite mounds, whereas the probability of subordinate species displacing C. sjostedti increased with distance from termite mounds. This variation in the outcome of competition for acacia hosts appeared to result from differential responses among the ant species to resource heterogeneity on the landscape.
Species interactions also affect habitat heterogeneity and/or resource availability. Car- dinale et al. (2002) manipulated the composition of three suspension-feeding caddisfly species at the same total density in experimental stream mesocosms. They reported that the total consumption of suspended particulate food was 66% higher in mixtures, com- pared to single-species treatments. Facilitation of food capture by these potentially com- peting species in mixture resulted from increased stream bed complexity (reflecting varia- tion in silk catchnet size), which in turn increased eddy turbulence and near-bed velocity, factors that controlled the rate of food delivery.
c. Indirect effects of other Species
Research has focused on pairs of species that interact directly, i.e., through energy or material transfers, as described above. Indirect interactions have received less attention but may be at least as important. Pollinators can augment plant reproduction sufficiently to compensate for herbivory, thereby indirectly affecting plant–herbivore interaction (L. Adler et al. 2001, Strauss and Murch 2004). On the other hand, Segraves (2008) dem- onstrated that a florivorous beetle, Hymenorus densus, consumed 1–2 yucca moth eggs, Tegeticula cassandra, per yucca flower, Yucca filamentosa, thereby increasing seed produc- tion per flower by 16–32%. These results indicated that the beetle limits yucca moth popu- lations and reduces the costs to the yucca of its mutualism with the yucca moth. Batzer et al. (2000b) reported that the 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.
Tri-trophic level interactions are recognized as having indirect effects on both herbivore–plant and predator–prey interactions (e.g., Boethel and Eikenbary 1986, Price et al. 1980). Even these interactions represent highly simplified models of com- munities (Gutierrez 1986, C.G. Jones et al. 1998) in which species potentially interact directly or indirectly with hundreds of other species to alter environmental conditions for all (see Chapters 9 and 10). Bezemer et al. (2005) reported that manipulation of soil nematodes and microorganisms significantly altered the amino acid and phenolic content of plants, thereby altering aphid and parasitoid performance. The abundance of tick vectors of lyme disease is related to the abundance of small mammal reservoirs, which reflect acorn production that, in turn, is affected by gypsy moth, Lymantria dispar, defoliation (C.G. Jones et al. 1998). 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 stabil- ity depends on predator–prey interactions (negative feedback) being more common than mutualistic interactions (positive feedback). Because multi-species interactions control rates of energy and nutrient fluxes through ecosystems, resolution of the ex- tent to which indirect interactions reduce variation in community structure will con- tribute significantly to our understanding of ecosystem stability.
Associated species affect particular interactions in a variety of ways. Much research has addressed the negative effects of plant defenses induced by early-season herbivores on later colonists (Fig. 8.12) (e.g., Harrison and Karban 1986, M.D. Hunter 1987, Kogan and Paxton 1983, N. Moran and Whitham 1990, Sticher et al. 1997, Van Zandt and Agraw- al 2004, Wold and Marquis 1997) and on decomposers (Grime et al. 1996). K. Anderson et al. (2009) extended the Lotka–Volterra competition model to describe plant-mediated interactions between two herbivore species. Their model for induction of multiple plant traits with negative or positive effects on a second herbivore is:
H1(t+1)=H1t+r1H1((K1−H1−f1I2+g1I1/K1)) (8.20) H2(t+1)=H2t+r2H2((K2−H2−f2I1+g2I2/K2)) (8.21)
I1(t+1)=I1t+p1(I1,H1)−d1I1 (8.22)
I2(t+1)=I2t+p2(I2,H2)−d2I2 (8.23)
where H1and H2 are herbivores 1 and 2, respectively, I1 and I2 are induced responses of the plant with effect strength f and g, respectively, and d1I1 and d2I2 represent decay in induc- tion over time.
Herbivore-induced defenses can affect interactions with other members of the com- munity, as well. Callaway et al. (1999) reported that the tortricid moth, Agapeta zoegana, introduced to the western U.S. for biological control of spotted knapweed, Centaurea maculosa, increased the negative effect of its host on native grass, Festuca idahoensis. The reproductive output of the grass was lower when neighboring knapweed had been defoli- ated by the moth, compared to grass that was surrounded by non-defoliated 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.
247 II. fACTorS AffECTIng InTErACTIonS
Baldwin and Schultz (1983) and Rhoades (1983) independently found evidence that damage by herbivores is communicated chemically among plants, leading to induction of defense in plants in advance of herbivory (see Chapter 3). Although their hypoth- esis that plants communicate the herbivore threat chemically with each other was chal- lenged widely because of its apparent incongruency with natural selection theory (e.g., Fowler and Lawton 1985), numerous studies have confirmed the induction of chemical defenses by volatile chemical elicitors, particularly jasmonic acid (Fig. 8.13), salicylic acid and ethylene (Farmer and Ryan 1990, McCloud and Baldwin 1997, Schmelz et al.
2002, Sticher et al. 1997, Thaler 1999a, Thaler et al. 2001, see Chapter 3). Jasmonate induces the production of proteinase inhibitors and other defenses against multiple in- sects and pathogens when applied at low concentrations to a variety of plant species (Fig. 8.14, Chamberlain et al. 2001, Hudgins et al. 2003, 2004, Thaler et al. 2001). Inter- plant communication via jasmonate induces production of defenses among neighboring plants (Fig. 8.15, Dolch and Tscharntke 2000, Hudgins et al. 2004, M. Stout et al. 2006, Tscharntke et al. 2001), including unrelated plant species (Farmer and Ryan 1990, Kar- ban 2001, Karban and Maron 2002, Karban et al. 2000, Schmelz et al. 2002, Thaler et al.
2001), although the fitness consequences of interspecific communication are not clear (Karban and Maron 2002).
Plant defense elicitors also affect herbivores indirectly through other associated species.
Thaler (1999b) demonstrated that tomato, Lycopersicon esculentum, defenses that were in- duced by jasmonate treatment doubled the rate of parasitism of armyworm, Spodoptera exigua, by the wasp, Hyposoter exiguae. However, some induced proteinase inhibitors may reduce the pupal weight and survival of attracted parasitoids (Rodriguez-Saona et al. 2005). Zeng et al.
(2009) found that herbivore production of P450 detoxification enzymes in response to fIG. 8.12 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 follow- ing damage. Vertical lines represent standard errors of the mean. D. flagella larvae feeding on regrowth foliage show both reduced survival to pupation and reduced pupal weight. From M.D.
Hunter (1987) with permission from John Wiley & Sons.
plant signaling chemicals, an adaptive response to induced plant defense, increased the toxicity of aflatoxins ingested with plant material (Fig. 8.16, see next paragraph).
Endophytic or mycorrhizal fungi affect interactions between other organisms (E. Al- len and Allen 1990, G. Carroll 1988, Clay 1990, Chapter 3). G. Carroll (1988) and Clay et al. (1985) reported that mycotoxins produced by mutualistic endophytic fungi can complement host defenses in deterring insect herbivores. Clay et al. (1993) documented the complex effects of insect herbivores and endophytic fungi on the competitive in- teractions among grass species. Tall fescue, Festuca arundinacea, competed poorly with fIG. 8.13 Structure of jasmonic acid, a volatile plant chemical that communicates plant damage and induces defensive chemical production in neighboring plants.
fIG. 8.14 Survival of beet armyworm, Spodoptera exigua, larvae and pupae and cab- bage 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 John Wiley & Sons.
249 II. fACTorS AffECTIng InTErACTIonS
orchard grass, Dactylis glomerata, when herbivores were absent, but fescue which was infected with its fungal endophyte, Acremonium spp., competed better than either or- chard 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 the effects on aphids, Myzus persicae, and butterfly, Polyommatus icarus, larvae, respectively. In both stud- ies, mycorrhizal inoculation increased insect growth and survival, apparently related to increased P concentrations in the foliage of mycorrhizal plants. Goverde et al. (2000) further reported that herbivore performance was related to the mycorrhizal species colo- nizing the host plant. Sooty molds growing on foliage also may affect palatability for herbivores (Fig. 8.17).
Volatile defenses that are induced by defoliators often attract predators and parasites (e.g., Chamberlain et al. 2001, Kessler and Baldwin 2001, Price 1986, Thaler 1999b, Turlings et al. 1990, 1993, 1995). At the same time, however, plant defenses that are sequestered by herbivores also affect herbivore–predator and herbivore–pathogen interactions (L. Brow- er et al. 1968, Stamp et al. 1997, Tallamy et al. 1998, Traugott and Stamp 1996). Preda- tion on pollinators affects pollinator–plant interactions (Knight et al. 2005b, Louda 1982).
fIG. 8.15 Maximum proportion of leaves that were damaged by grasshoppers on tobacco plants that were near sagebrush plants that were artificially clipped or unclipped (mean + SE).
Effects of clipping were significant all five years (P < 0.0001). Reprinted from Karban, (2001), with permission from Elsevier.
fIG. 8.16 Effects of methyl jasmonate (MeJA, top) and salicylic acid (SA, bottom) on mor- tality of fourth instar Helicoverpa zea exposed to 1 mg g−1 aflatoxin B1 (AFB1) after 8 da. Cater- pillars were reared on diets containing either 0.2% DMSO (control), MeJA (100 mg g−1 H-MeJA or 2.9 mg g−1L-MeJA), SA (1mg g−1 H-SA or 12 mg g−1L-SA), 1 mg g−1AFB1, MeJA (H-MeJA or L-MeJA) + 1 mg g−1AFB1, or SA (H-SA or L-SA) + 1 mg g−1AFB1. Values are means and stan- dard errors for three replicates with 20 caterpillars per treatment. Significant differences among treatments in a group are designated by different letters above bars. From Zeng et al. (2009) with permission from the authors and from Springer Science + Business Media.
251 II. fACTorS AffECTIng InTErACTIonS
Herbivores feeding above ground frequently deplete root resources, through compensa- tory 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 xy- lostella, resistance to Bacillus thuringiensis on within-host interactions between the patho- gen 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 parasi- toid was symmetrical: each had a significant negative effect on the other. Highly resistant hosts provided a refuge from competition for the parasitoid.
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 Brandâo 1991, Tilman 1978). The strength of this interaction varies inversely with distance from ant nests. Tilman (1978) reported that visits by ants 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.
fIG. 8.17 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; foliage prior to 1993 was produced during extended drought. Sooty mold exploits moist conditions, especially honey- dew accumulations and, in turn, may affect foliage quality for folivores.
f0090
C. Currie (2001) and C. Currie et al. (1999a, b) reported complex interactions between fungus-growing ants (especially leaf-cutting species of Atta and Acromyrmex) their mu- tualistic fungi, Leucocoprinus spp. and Leucoagaricus spp., and associated microorgan- isms. 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. However, fungus gardens often host a virulent fungal pathogen, Escovopsis, that is capable of destroying both the fungus garden and the dependent ant colony. The ants have an additional mutualistic association with an ac- tinomycete bacterium that produces specialized antibiotics with potent inhibitory activity against Escovopsis.
Complex interactions among a community of invertebrates and fungi affect bark beetle interactions with host trees (see above). The southern pine beetle interaction with blue stain fungus was thought at one time to be mutualistic, with beetles providing transport and fungus contributing to tree death and beetle reproduction. However, more recent studies have demonstrated that this beetle can colonize trees in the absence of the fungus (Bridges et al. 1985), that the blue stain fungus is 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 (M. Ayres et al.
2000, Bridges and Perry 1985). The blue-stain fungus is associated only indirectly with the beetle. Spores are collected by phoretic tarsonemid mites in specialized sporothecae (Fig.
8.18) (Bridges and Moser 1983, J. 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 nematode parasites of the beetle (Kinn 1980). Finally, folivorous insects increase tree susceptibility to colonization by bark beetles (Wallin and Raffa 2001).
The interaction between termites and mutualistic gut symbionts is affected by wood chemistry and associated wood-colonizing fungi. Mankowski et al. (1998) found that ter- mite preferences among combinations of wood and fungal species generally reflected the suitability of the resource for termite gut fauna, as indicated by changes in gut faunal den- sities when termites were forced to feed on particular wood–fungus combinations.
Competitive interactions between a pair of species may be modified by the presence of additional competitors or predators. Pianka (1981) proposed a model in which two spe- cies with modest competitive overlap over a range of resource values could become “com- petitive mutualists” with respect to a third species that would 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). A predator that preys indiscrimi- nately on competing prey species, as they are encountered, will prevent the most abun- dant prey species from competitively suppressing others. R. Paine (1966, 1969a, b) intro- duced the term keystone species for top predators that maintain balanced populations of competing prey species. However, this term has become used more broadly to include any species with a disproportionate effect on the structure or function of a community and/or ecosystem, based on its abundance (Bond 1993, Power et al. 1996). Herbivorous insects that selectively reduce the density of abundant host species, and thereby balance the abundances of host and non-host plants (Louda et al. 1990a, Schowalter and Lowman 1999) and their associated species, function in a keystone capacity.
Herbivore behavior can be affected by the presence of predators to a greater extent than the actual rate of predation (M.L. Johnson et al. 2006). Predators can be distract- ed by alternate prey that are less suitable. Meisner et al. (2007) evaluated the effect of
253 III. ConSEqUEnCES of InTErACTIonS
the spotted alfalfa aphid, Therioaphis maculata, on two parasitoids, the native Praon pe- quodorum and the introduced Aphidius ervi, of the pea aphid, Acyrthosiphum pisum. The spotted alfalfa aphid had a greater distraction effect on the more common A. ervi, there- by contributing to persistence of P. pequodorum in this system. Furthermore, intraguild predation or competition affects predator foraging activity (e.g., Finke and Denno 2002, 2006, Schmitz 2007).
Although it often is convenient to emphasize the adaptive aspects of species interac- tions, especially symbiotic interactions, extant associations do not always represent co- evolved relationships. Connell (1980) noted that niche partitioning and other adaptations which minimize competition among living species may reflect competition among their ancestors. Janzen and Martin (1982) suggested that modern seed dispersing animals may have replaced extinct species with which plants co-evolved mutualistic associations in the past. For example, the large-seeded fruits of some plants in North and South America probably reflect adaptation for dispersal by extinct gomphotheres and ground sloths; the smaller extant vertebrates are less capable of transporting such seeds over the distances that are necessary for adequate dispersal.
III. conSeQuenceS of InteRActIonS
Each species interacts with many others in a variety of ways (competing for various food, habitat and other resources, preying, or being preyed, on, and cooperating with mutualists), fIG. 8.18 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, Den- droctonus frontalis. Reprinted from Transactions of the British Mycological Society 84, J. Moser, Use of sporothecae by phoretic Tarsonemus mites to transport ascospores of coniferous bluestain fungi, Figure 2, Page 752, copyright 1985, with permission from Elsevier.
with varying degrees of positive and negative feedback on abundance. Therefore, the popu- lation status of each species represents the net effects of these feedbacks.