Upload
j-n
View
213
Download
0
Embed Size (px)
Citation preview
Ann. Rev. Ecol. Syst. 1988. 19:65�7 Copyright © 1988 by Annual Reviews Inc. All rights reserved
VARIATION IN INTERSPECIFIC
INTERACTIONS
John N. Thompson
Departments of Botany and Zoology, Washington State University, Pullman, Washington 99164
INTRODUCTION
The study of evolving interactions between species has progressed from descriptions of adaptations and counteradaptations to a search for patterns and constraints affecting the evolution of interactions and the conditions favoring coevolution. This search for patterns and constraints requires a populational approach to species interactions. It is not enough to understand in a typological way that one species has a particular trait, another species has a particular counter-trait, and that the interaction of the two species can be described in general terms as antagonism, commensalism, or mutualism. Individuals vary in their expression of traits, populations vary in their structure, and, as a consequence, interactions vary in their outcomes.
Just as variation in traits in populations is the raw material for the evolution of species, variation in outcome is the raw material for the evolution of interactions. Nonetheless, only in recent years has the analysis of variation in the outcome of interactions become a focus of evolutionary research. A glance through the major evolution journals from two decades ago would show few papers confronting the problem of how interspecific interactions can vary in outcome and how this variation can affect the evolution of interactions (e.g. 38, 93, 111). Not until the mid 1970s did any text in ecology include chapters on the evolution of species interactions (e.g. 108, 120, 124). And not until the appearance of Futuyma's book in 1979 (46) did any major textbook in evolution include a chapter on coevolution or the evolution of interactions. The first book devoted to issues on coevolution of animals and plants did not appear until 1975 (53), and the first books devoted to the general problem of coevolution did not appear until 1982 and 1983 (49, 98, 149).
65 0066-4162/88/1120-0065$02.00
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.
66 THOMPSON
In this paper I review the kinds of analyses that provide the raw material for understanding how interspecific interactions evolve under different ecological conditions. The review focuses on variation in the outcome of interactions at the level of the individual, rather than the effects of interactions on the dynamics of populations. In writing the review, I generally avoided covering the same ground as two previous reviews that focused on the ways in which two-species interactions are affected by interactions with a third trophic level (112) or parasites (113). The studies I consider here are divided broadly into two kinds: (a) those showing distributions of outcome within populations (distributed outcomes) because of variation in age or size of individuals, density, size, and subdivision of populations, or distribution of genotypes; and (b) those showing variation in outcome across environmental gradients (interaction norms). These terms, and their use in the study of evolving interactions, are developed below.
TYPOLOGICAL VERSUS POPULATIONAL
APPROACHES
The traditional classifications of interactions as (-, - ), (+, -), (+ ,0), etc mask the kinds of information needed to understand the evolution of interactions. These classifications lump together interactions that can differ fundamentally in the mechanisms that produce the outcomes; both predator/ prey interactions and Batesian mimicry, for example, are classified as (+ ,-) interactions (1). Moreover, this typological approach to thinking about interactions ignores the variation in outcome that is central to the study of evolving interactions.
For example, ground-foraging beetles attack Lomatium dissectum seeds after the seeds are dispersed by wind. These beetles, however, do not kill all the seeds they attack. Lomatium seeds are flat and have a prominent wing. Both in the field and in the laboratory, the beetles consistently eat only the wings of seeds from some L. dissectium plants within a population, whereas they consistently chew past the wings and into the endosperm and embryo of seeds from other plants within the population. Consequently, the interaction varies from predation to commensalism within a population, with subgroups of plants consistently experiencing different outcomes (150). No simple typological label can accurately describe the interaction. An understanding of the ecological dynamics of the interaction and the potential effect of the beetles on plant genotypes (if the differences in seeds are genetically determined) requires an understanding of the distribution of outcomes. The mean outcome provides little information, for the outcome differs among the subgroups within the plant population.
A second problem with typological descriptions arises in mutualistic in-
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.
V ARIA nON IN SPECIES INTERACTIONS 67
teractions. Few if any mutualistic interactions impose no costs on the interacting species. Many mutualisms probably derive evolutionarily from antagonistic interactions (149), and the antagonistic components of the interactions often remain as costs of the mutualism, as in the ovules killed by larvae of pollinating fig wasps (71) and yucca moths (2). Within a population, the cost/benefit ratio is likely to vary, and it is precisely this variation that provides the information important to understanding how slight shifts in life histories, age, sizes, morphologies, and physiologies can affect interactions. To describe simply the mean outcome of an interaction or to describe the benefits without an analysis of the costs is to lose the information fundamental for studying the evolution of the interaction.
A third problem in typological descriptions occurs in interactions that involve several components of life histories. Some species may be mutualistic for some aspects of their life histories while being antagonistic for others. By forming Miillerian mimicry complexes, adult Heliconius butterflies are mutualistic for avoidance of enemies, but compete for adult nectar sources. Consequently, as Templeton & Gilbert (146) argued, it is misleading to describe these interactions as having some net outcome and meaningless to argue that one of these kinds of interactions can outweigh the other. Both kinds of interaction occur within these populations, and they must both be considered in evaluating the evolution of these interactions. Coevolution of the mutualistic traits can affect coevolution of the competitive traits, and vice versa.
A fourth problem is that all popUlations have age or size structure, which can affect the outcomes of interactions. Therefore, an analysis of the mean outcome of an interaction on a random sample of individuals masks the variation in outcome that can depend upon age or size. Furthermore, a random sample probably provides a mean estimate that most closely applies to young or small individuals, since they will be the largest group in any random sample of a stable or growing population.
Finally, both the mean and the distribution of outcomes in an interaction can vary among environments. Some mycorrhizal associations, for example, can be mostly mutualistic on infertile soil but antagonistic on more fertile soil, depressing the growth rate of the host plant (18). Therefore, the outcomes of interactions may be environment-specific. The study of plasticity in outcomes is as important to understanding the evolution of interactions as the study of plasticity in morphology, physiology, and life histories is to an understanding of the evolution of species.
The first four of these problems with typological descriptions of interactions concern distributions of outcomes within populations, and the fifth relates to variation in the distributions among environments or across gradients. The study of the evolution of interactions will increasingly demand
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.
68 THOMPSON
analyses of the distributions of outcomes both within and among environments. This is hardly a new idea. Nonetheless, the analysis of the distributions of outcomes-rather than simply a mean outcome or a mean costlbenefit analysis-has not yet become a standard part of studies on the evolution of interactions.
DISTRIBUTED OUTCOMES
Many, perhaps most, interactions between populations vary with age, size, or genotype of the interacting individuals. Roughgarden & Diamond (126)
argued that population models of species interactions will need to be improved by subdividing populations into groups within which the interactions are on average similar. They referred to such models as distributed interactions.
We can think of distributed interactions as having two components: distributed probabilities and distributed outcomes. Individuals differing in age, size, or genotype may differ in their probabilities of encountering another species, and mathematical models of distributed probabilities of encounter based upon age (101) or size (156) are beginning to appear. Similarly, outcomes can vary among ages, sizes, and genotypes, and the following sections focus on these distributed outcomes.
Age-Dependent Outcomes
Ontogenetic changes in susceptibility to diseases are common in animals (3, 40, 145) and plants (23). Some viral infections such as viral hepatitis and poliomyelitis in humans may sometimes produce no symptoms or only mild symptoms if infection occurs in early childhood but may produce more symptomatic and even severe disease if infection first occurs at a later age (41, 91). Maternal antibodies apparently confer protection against some diseases such as measles and parainfluenza viruses in infants up to 4-6 months of age, after which the incidence of these diseases increases (15, 56).
In plants, the effects of herbivory or survivorship can vary with plant age. In two grasses, Bromus tectorum (an annual) and Agropyron spicatum (a perennial), the probability of dying after being grazed by microtines decreases with age at initial grazing (115). Herbivory on a young plant is an act of predation, killing the plant immediately, whereas herbivory on a larger plant often results only in reduced growth and reproduction. Consequently, the timing of the interaction relative to plant age can affect the extent to which selection on these populations is primarily "viability selection" or "fecundity selection." Such differences in selection could affect the kinds of defenses that evolve within plant popUlations (149).
Age structure may also influence the evolution of mutualism. In environ-
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.
VARIATION IN SPECIES INTERACTIONS 69
ments in which life spans of hosts are short, some potential mutual isms may be preempted. Under these conditions, host lifespans may not permit sufficient time for development of the symbiont or sufficient time for the symbiont to have an effect on host growth or reproduction. At the other extreme, if host lifespans are already long, it may require a large input on the part of any symbiont to have a significant effect on the host. Hence, some kinds of symbiotic mutualism may be most likely to develop in populations in which hosts have intermediate lifespans that can be readily affected by a small input by a symbiont (123, 125) in environments with intermediate disturbance regimes (149, 152).
Relative age structures and generation times of hosts and parasites may affect the distribution of outcomes and potentially the evolution of reduced virulence in parasites. Analyses of the evolution of reduced or intermediate virulence in parasites living in hosts with much longer generation times have invoked interdemic selection (80, 176), rapid rates of evolution within individual hosts (138), mode of transmission (42), and/or maximum transmissibility of parasites at intermediate levels of virulence (4, 87, 89). How the evolution of pathogenicity varies among populations differing in age structure if susceptibility is age-dependent has not yet been thoroughly explored in models.
Size-Dependent Outcomes
In many taxa, size is as important as age as an influence on the demography of a population (e.g. 127a) and on interactions with other species. Outcomes of competition can depend upon size in a variety of taxa (19, 96, 103, 131). Similarly, the outcomes of trophic interactions can depend upon size, as in the effects of phytophagous insects on plant reproduction (68, 85), and the likelihood of successful predation on particular prey sizes by gastropods (73) and fish (174). Nonetheless, only recently have there been attempts to develop mathematical theory for species interactions in size-structured populations (156, 174). Shifts in the distributions of sizes and growth rates within a population can affect both the probability that an individual with a given growth rate will ever encounter some other species during its lifetime (156) and the population outcomes of interspecific interactions (174).
Differences in outcome that depend upon size can result in a population in which individuals of different sizes interact with different species. Within the population of Darwin's Medium Ground Finch (GeospizaJortis) on Daphne Major in the Galapagos, individuals differ in bill size and their ability to crack large seeds (114). Only the finches with relatively large bills are able to crack seeds of Opuntia echois and Tribulus cis to ides . The smaller birds can crack only the smaller, softer seeds produced by some other plant species. Consequently, the birds in this population vary in the proportion of large seeds
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.
70 THOMPSON
they incorporate in their diets, and large-seeded plants are susceptible to predation from only a subgroup of this avian population.
Species chosen as prey can also vary ontogenetically, when individuals grow in size as they get older. In reviewing the literature on ontogenetic shifts in species interactions, Werner & Gilliam (174) referred to these size-related differences in species interactions (and habitat use) accompanying age as the "ontogenetic niche." Hence, the distribution of outcomes of some interactions will depend upon current size distributions and growth rates of individuals within the interacting populations. Successful predation by naticid drilling gastropods on their bivalve prey varies with prey size, and Kitchell et al (74) argued that coevolution of these predator/prey interactions has been governed by this size-dependent variation in outcome.
The relationship between size and outcome in interactions is reciprocal: the distribution of sizes affects the outcomes of interactions, and interactions affect the distribution of sizes. Studies of competition have analyzed and displayed distributions of outcome in size more often than studies of any other kind of interaction. One of the common consequences of competition between plant species is an increased skewness of inequality in the distribution of plant
sizes (63, 1 72). Decreased inequality is also possible if competition is symmetric; that is, if competition affects all individuals equally so that no one species or one group of individuals has a competitive edge (163, 1 73). Asymmetric outcomes of competition, however, appear to be much more common than symmetric outcomes in both plants and animals (10, 76, 1 49), so an increase in inequality is probably the more common outcome in interspecific interactions. In experiments on plant competition this increased inequality seems often to take the form of a highly skewed distribution in which a few plants grow to a large size, usurping light and other resources from surrounding plants. The effect of competition on skewness or inequality of plant sizes has, in fact, been the basis of recently proposed measures of plant competition: the jackknifed skewness coefficient (63) and the bootstrapped Gini coefficient (172).
The outcomes of interactions between ants and trees that produce extrafloral nectaries may also vary with plant size. These interactions may be mutualistic primarily when trees are saplings (100, 132, 159) and may become less mutualistic as trees become too large for ants to patrol the entire plant effectively. In Prunus serotina, for example, the number of buds per tree increases approximately exponentially with trunk circumference (159). Tilman (159) estimated that if a colony of ants with 20,000 workers could forage on a small sapling at a rate of 100 ants/lOOO buds, then that rate would drop to 8 ants/1000 buds on a tree larger than 30 cm in circumference. At the other extreme, small plants may not produce enough reward to attract many ants. O'Dowd (100) found that doubling the leaf area of juvenile Ochroma
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.
VARIATION IN SPECIES INTERACTIONS 71
pyramidale more than doubled the number of ants visiting the foliar nectaries at any one time.
GENOTYPES AND DISTRIBUTIONS OF OUTCOMES
Multiple outcomes of interspecific interactions can be maintained within populations through genetic polymorphisms arising from a variety of mechanisms, including frequency-dependent selection or heterozygote advantage (124, 139). Mathematical models of gene-for-gene interactions between species indicate that frequency-dependent selection can result in stable polymorphisms within populations (77, 89). If the parasites also regulate the density of host populations, polymorphism may still result, unless the host develops resistance without a cost, or parasite virulence becomes very low without loss in transmissibility (88). Differential outcomes of interactions based upon different combinations of parasite and host genotypes could, in fact, be a major factor maintaining polymorphisms within populations (22, 27). Variation in outcome dependent upon the particular combination of parasite and host genotypes has been shown repeatedly (e.g. 60, 84, 94, 121, 134, 177) and is the basis of models of gene-for-gene interactions (6, 23, 33, 136).
Other polymorphisms in traits affecting outcomes of interactions may be maintained through conflicting selection pressures. The coexistence of cyanogenic and acyanogenic plants within populations of Lotus corniculatus along the coast of Anglesey in Britain may result partly from selective grazing on acyanogenic plants balanced by a lower salt tolerance of cyanogenic plants (28). Variation within plant populations in characters that can affect the probability and extent of herbivory has been observed in a variety of other plant species (13, 26, 36). These variations in outcome highlight the need to study and report distributions of outcome rather than just the average outcome of interactions between two or more populations.
In interactions between plants and pathogens, the extent of infection within individual plants is an important component of the outcome of an interaction. High levels of infection can result in lower growth rates, survivorship, or reproduction than in plants with low levels of infection (107). Although studies in phytopathology often divide plants into only two categories (resistant, susceptible) and pathogens into two complementary categories (virulent, avirulent), intermediate levels of susceptibility or virulence can occur. These distributions, however, are seldom reported.
Only recently have studies of interactions between plants and pathogens begun reporting distributions of both susceptibility and virulence in natural populations of plants and pathogens (24, 34, 99). Burdon et al (24, 99) analyzed variation in interactions between wild oats (Avena spp.) and Pucci-
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.
72 THOMPSON
nia rusts in Australia. The results showed that both the mean and the distribution of susceptibility to Puccinia differed greatly among Avena populations. Northern populations exhibited broad, symmetrical distributions, whereas southern populations exhibited narrow, skewed, or bimodal distributions. Similarly the distributions of virulence in the rusts varied among populations, ranging from almost normal distributions to more bimodal distributions. Burdon et al attributed the differences among populations in distributions of susceptibility to differences in the selection pressures placed upon the plant populations by the pathogens (99). In the more seasonal southern popUlations, the interactions between plants and pathogens are more ephemeral and in
termittent than in the warmer, northern populations, and the accumulation of multiple resistance alleles is less common in the southern populations.
The outcomes of interactions between plants and pathogens can vary broadly even on a much more local scale. Parker (106) found that populations of an annual legume Amphicarpaea bracteata separated by as little as 1 Ian differed in susceptibility to a particular strain of a fungal pathogen Syn
chytrium decipiens. Moreover, there was significant variation among families in susceptibility to the pathogen along a transect of only 160 m. The distribution of outcomes along the transect was bimodal. In natural populations the distributions of disease severity should be expected to change over time both within and between generations, if survivorship depends upon disease severity. Yet other interactions vary within populations because of differences among individuals in genotype or the microenvironment in which the interaction takes places. Coleopteran seed parasites of Lomatium grayi affect not only the seeds they attack but also the masses of surrounding unattacked seeds on the same plant. The extent to which seed parasitism affects unattacked seeds, however, differs among plants within a population (39).
POPULATION SIZE, DENSITY, SUBDIVISION, AND OUTCOMES
The outcomes and selection pressures on interactions can vary with the numbers of individuals within populations and their spatial and social subdivision, and the result can be interactions that vary between antagonism and mutualism. Studies of phenological overlap in flowering plants have indicated that plants relying upon the same pollinators may potentially compete for those pollinators or suffer reduced seed set due to interspecific pollen transfer when the plants occur in moderate or high densities (e.g. 5, 25). But at low densities, the flowers of any one species may be too rare to attract pollinators. Several low-density species flowering at the same time, however, may attract pollinators, thereby increasing pollination success over what would occur if the species differed in flowering time. Hence, pollinator-mediated in-
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.
VARIATION IN SPECIES INTERACTIONS 73
teractions between plants may vary from facilitation to competition as density changes from low to high, and selection for convergence or divergence of flowering phenology may vary accordingly (43, 44, 116, 130, 157, 158). How such variation in outcome affects the evolution of an interaction will depend upon the relative frequency of the different outcomes.
Mutualisms between ants and plants may depend upon a minimum threshold of ant density necessary to patrol plant surfaces effectively. The effect of ants on plant growth or reproduction is in some cases positively correlated with ant density or activity, and produces a range of outcomes (75, 129). Consequently, the outcomes of these interactions can potentially vary within populations not only with plant size, but also with the distance of a plant from an ant colony and the size of the colony visiting surrounding plants. As Beattie (9) noted, studies of the outcomes of ant/plant interactions will vary in their conclusions as variables such as ant density, herbivore density, and reward density vary. Such variation in outcome again argues for reporting distributions of outcomes together with means.
Some other interactions can persist only above a minimum threshold population size. Measles does not persist in human populations on islands with less than 500,000 people (14). Individuals acquire lifetime immunity after contracting the disease once. Consequently, after an initial epidemic, there are too few individuals lacking immunity on small islands to maintain the parasite population. The effect of population size on disease persistence within populations should be expected to vary among diseases depending upon the length of time of immunity after infection, the length of the latency period of the disease, the social and genetic structure of the population, and the age distribution of those susceptible.
Some hypotheses on the evolution of avirulence in interactions between parasites and hosts rely directly on the differing success of parasite genotypes under different densities. Levin & Lenski (77) argued that when host density is low, the evolution of temperate phage may be favored over virulent phage, for the probability of finding a new host would be low. Moreover, they argued that at high host densities, coevolution between bacteria and viruses would generally be antagonistic, whereas at low densities coevolution might tend not only just toward commensalism but also toward mutualism. Similarly, Gill & Mock (54) suggested that low host densities in red-spotted newt populations may favor apathogenicity in the trypanosomes that attack these populations. These newts reproduce in temporary ponds that historically may have been produced by beavers. Gill & Mock predicted a time sequence in mean outcome of these interactions within a pond: selection initially favors apathogenic trypanosome genotypes, but as a pond ages �d newt populations become higher, selection on the trypanosomes favors pathogenic genotypes. In modelling the low density hypothesis for the evolution of temperate phage,
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.
74 THOMPSON
Stewart & Levin (143) found that constant low density alone would not favor temperance. With constant low density set by a constant level of resource, the equilibrium density of the bacterial population does not vary, and the conditions for invasion by temperate or virulent phage do not differ. But with fluctuating densities, including extended periods too low to support virulent phage, temperate phage are favored over time as virulent phage fluctuate to ever lower levels as the bacterial host population fluctuates.
Selection on hosts in other interactions, such as those involving pollination or protection of a host, may vary with density in other ways. If the probability of encounter between two species is low, then selection for commensalistic or mutualistic genotypes may be ineffective. As the probability of encounter increases to the point of becoming inevitable within the lifetime of an individual host, then selection may favor host genotypes that decrease the antagonistic effect of the other species or increase the mutualistic effect (123, 125, 149, 152). Hence, selection for specific mutualistic coevolution between a plant and pollinator population would be effective only if the probability was consistently high that the plants would be visited by that pollinator species and the plants were sufficiently abundant to be consistently available to the pollinator.
The relative densities of interacting species also have the potential to influence both the direction of evolution in an interaction and the likelihood of coevolution. Gilbert (52) suggested that coevolution in Mullerian mimicry between two or more distasteful species is most likely when the populations are approximately equal in size but fluctuate in relative abundances over time.
If one species is consistently less abundant than the other, simple convergence in color pattern of the less abundant on the more abundant species is probably more likely than coevolution. In Batesian mimicry (distasteful model, edible mimic converging on the model), coevolution is probably most likely when the edible mimic is at least occasionally more abundant than the model. High relative abundance of the edible mimic could exert selection on the model to diverge in color pattern, for the predators would be encountering a high proportion of edible prey with the current aposematic pattern.
PATCH DYNAMICS OF INTERACTIONS
AND THEIR OUTCOMES
In the process of succession within patches, popUlations change in age and size distributions, densities, relative abundances, and relative proportions of genotypes (7,31,58,104,110,140,147,151,170). Moreover, populations may over time alter their local environment by changing such resources as light, nutrients, and water (66, 169). These changes in populations and resources can, in tum, affect the outcomes of interactions. Consequently,
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.
VARIATION IN SPECIES INTERACTIONS 75
there can be a patch dynamics of interactions as there is a patch dynamics of species distributions, abundances, and compositions (149, 151) . Walker &
Chapin (171) found that, in primary succession on an Alaskan floodplain, alder (Alnus tenuifolia) can both facilitate the establishment of other plants because of its nitrogen-fixing ability and compete with other species through shading of seedlings. Hence, succession along the floodplain apparently results from an interaction of these conflicting outcomes of facilitation and competition, life history differences, and stochastic processes.
The extent to which disturbance and succession within habitat patches affect interactions depends, of course, upon the mobilities and biologies of the species and changes over time in species composition within patches. Feinsinger et al (45) found little variation between natural-disturbance patches of different sizes in interactions between highly mobile hummingbirds and flowers. They argued that the scale of natural disturbance in the Costa Rican cloud forest where they studied these interactions was too small relative to the normal movement patterns of the hummingbirds to have any effect.
Changes induced in hosts by interactions can also influence the outcomes of subsequent interactions, thereby changing the overall distribution of outcomes within a patch or population over time. Herbivory on plants can induce the production of secondary compounds (127), produce juvenilization in tissues with concomitant changes in secondary compounds (20), and potentially rearrange the carbon/nutrient balance (20, 162). These changes can affect the palatability of plant tissues, the amount of plant tissue eaten, and the growth rates of herbivores (21, 62). Such changes have been hypothesized to affect fluctuations in the sizes of some insect populations (61, 1I8).
CORRELATED OUTCOMES
Few populations interact with only one other species. Selection on an interaction between two species can in tum affect how these species interact with yet other species. The result can be positive or negative correlations of outcomes of interactions between a popUlation and several other species. The distributions of outcome in an interaction can therefore result from constraints and selection arising from other interactions affecting a population. Analyses of what can be called correlated outcomes are still few. There are no analyses showing how the� distribution of outcomes in a two-species interaction is affected by interactions with other species.
Studies of performance (survivorship, growth, reproduction) in phytophagous insects have shown from the insect's perspective the variety of possible correlated outcomes that can result from insect attack on two plant species. One of the most commonly suggested hypotheses for the evolution of restricted host use in insects is that adaptation to one plant species will come
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.
76 THOMPSON
at the expense of the ability to do well feeding on other plant species; actual results range from this effect to a variety of much more diverse effects (e.g. 48, 51, 95, 117). For example, parthenogenetic genotypes of the moth Alsophila pometaria differ in whether the moths feed on oak or maple foliage. Futuyma et al (51) found that these host-specific genotypes did not differ in any simple way that would suggest better physiological adaptation of the genotypes to their normal host. The maple-feeding genotype achieved higher weights on both maple and oak than did the oak-feeding genotype. Furthermore, compared to the maple-feeding genotype, the oak-feeding genotype performed more poorly on oak than on maple. In an experiment designed to study rates of adaptation to different host plants, Gould (57) found that selection on a subdivided population of two-spotted spider mites (Tetranychus urticae) produced cross-adaptation to other hosts. After 21 months, the subpopulation fed on a combination of lima beans and cucumbers had higher survivorship on two novel hosts (tobacco and potato) than did the population that had been maintained on lima beans alone. That is, selection on the outcome of the interaction between the mites and the beans and cucumbers affected indirectly the outcome of interaction between the mites and tobacco and potatoes. In tortoise beetles (Deloya/a guttata), which vary among populations in use of /pomaea species, Rausher (117) found no evidence of negative genetic correlations in performance on different hosts. In other species, the patterns of performance on different hosts may vary among genotypes within a population (168).
For the most part the genetics of performance and preference in phytophagous insects are still mostly unknown (47,50, 155). Progress in our understanding of the evolution of interactions will demand rigorous analyses of the genetics of these correlations. Such analyses are particularly important for interactions between insects and plants, which are probably the most abundant and diverse interspecific interactions in both natural and managed terrestrial communities.
INDIRECT OUTCOMES
The outcomes of interactions between any two species can also be affected indirectly by additional interactions with other species within communities. Interactions between herbivores and plants can be shaped by predators or parasites of the herbivores (1 12), and the outcomes of a variety of competitive and other interactions can be influenced by parasites that attack one or more of the species (113). Indirect mutualisms or other populational effects that become apparent only when three or more species are studied simultaneously have now been indicated and modelled for a variety of other interactions as
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.
V ARIA TION IN SPECIES INTERACTIONS 77
well (78, 128, 164, 165). The results show that the outcomes of two-species interactions can vary broadly as additional species are added or removed from an interaction. In addition, the results emphasize that evolutionary studies of relationships between species will need to be based upon broader evolutionary units of interaction: groups of interacting species through which any twospecies interaction is shaped in evolutionary time (113, 149).
INTERACTION NORMS
The means and distributions of outcomes in interactions can vary among environments as changes occur in the phenotypic expression of genotypes or the effectiveness of traits involved in interactions. The range in expression of a genotype among environments is sometimes called a reaction norm (59,
141, 168). Similarly, the range of outcomes of interactions among environments due to variation in the expression of genes or variation in the effectiveness of particular traits can be called an interaction norm; that is, the reaction norm of species interactions (152, 153). Analyses of interaction norms are
needed to understand how different environmental conditions can affect selection on interactions, how interactions are restricted geographically, and how differences in outcome among populations can affect divergence of populations (154).
Differences in outcome among environments can potentially be great enough to shift the mean outcome along the continuum of antagonism, commensalism, and mutualism. Some of these differences could occur di
rectly through variation in the expression of genes. The gene-for-gene interaction between barley and Ustilago hordei fungi can vary with the environment. In the interaction between V2V2: R2R2 genes, the parasite is usually avirulent. But in a test comparing responses in California and British Columbia for the barley variety Excelsior, the interaction of these genes resulted in no pathogenicity in California but low levels of pathogenicity in British Columbia (37).
In some interactions, outcomes are clearly mutualistic only in environments in which a small input to host nutrition by a symbiont can have a large effect on host survivorship or reproduction. Hence, some plants benefit from mycorrhizae in nutrient-poor soils but grow better without mycorrhizae in fertile soils (69). Ant-fed plants, in which ants live and dump their debris in absorptive chambers within host plants, are restricted mostly to ephiphytes in relatively dry tropical canopies where nutrient flow through the canopy is low (55,67, 70, 148, 149). Reef-building corals, which are common in tropical waters in areas of low productivity, seem to depend upon the endosymbiotic dinoflagellates that they harbor mostly within the cells of their oral endoderm
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.
78 THOMPSON
(97). Nutricnt-poor marine environments are, in fact, rich in a variety of mutualistic symbioses often involving unicellular algae (64, 79, 86, 97, 167,
175, 178).
Other interactions vary in more complex ways along gradients, cautioning against any simple conclusion on how an interaction affects fitness at different points along the gradient. In the grass species Agryoyron smithii the effect of mycorrhizae varies with soil phosphorus. At low phosphorus levels mycorrhizal plants produce 35% more biomass than do nonmycorrhizal plants; at high phosphorus levels there is no difference in biomass production. At all phosphorus levels, however, mycorrhizal plants are shorter but have more tillers (92). Which of these effects of mycorrhizal association is more important for lifetime fitness cannot be readily assessed without concomitant demographic studies.
Interactions between symbionts and hosts that differ significantly among environments may even provide a basis for symbiont-induced speciation in hosts (154). Differential coadaptation of hosts and symbionts along environmental gradients or among habitats may potentially cause rapid divergence of host populations. Such divergence could be especially pronounced if the interaction norms resulted in the symbionts and hosts being mutualistic in some environments but antagonistic in other environments, for different sets of alleles and loci may then be under selection in the different populations.
Ideally, studies of interactions along gradients or between habitats would analyze variation in outcome for both (or all) species simultaneously. In practice most studies, except for many on competition, analyze the outcome for only one of the species. Competitive outcomes between animals vary between environments both in laboratory experiments (e.g. 12, 105) and in natural populations (e.g. 29). The outcomes of plant competition vary along gradients of soil moisture (109, 119), nutrients and light (16, 160, 161), and CO2 concentration (8). These results emphasize how the distribution of outcomes and, potentially, selection on competitive interactions can vary among environments. Most studies of reversals in competitive outcome along gradients, however, have not been done in natural communities, and rarely have field experiments on competition been repeated in different environments (30).
Similarly, very few studies analyze variation in outcome among environments for both species in interactions between parasites, grazers, or predators and their hosts or prey. Most studies analyze variation in outcome in only one of the species, and few actually report how the distributions in outcome vary among environments. Much more commonly reported is variation in mean outcome among environments for one of the species, as exemplified by studies of interactions between herbivores and plants. Growth rates of phytophagous insects have been shown to vary with light intensities, water
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.
V ARIA TION IN SPECIES INTERACTIONS 79
and nitrogen content in plant parts, and levels of secondary compounds (133, 137, 144). When fed on Rudbeckia laciniata under high and low light intensities and high and low water levels, clones of Uroleucon rudbeckiae aphids differed in mean survivorship or fecundity among treatments due to water treatment, aphid clone, the interaction of aphid clone and light intensity, and uncontrolled phenotypic differences among individual host plants (135). Fed on plants sprayed with N fertilizer, Cyrtobagus sp. beetles showed higher rates of popUlation increase than did beetles grown on unsprayed plots (122). In feeding trials on Melanoplus bivittatus grasshoppers, nymphal survival and development rate varied with the mix of plant species in the diet and the temperature at which the trials were run (81). Environmental gradients also affect interactions between plants and mammalian herbivores. Secondary chemistry and palatability to snowshoe hares vary with soil fertility and shade in Alaska paper birch (Betula resinifera) but not in green alder (Alnus crispa) (21).
Effects of herbivory on plant growth, survivorship, and reproduction also vary among environments (e.g. 35). Growth and reproduction in tansy ragwort (Senecio jacobaea) following defoliation by cinnabar moths (Tyria jacobaeae) was positively, although weakly, correlated with levels of irrigation in field plots (32). This study displayed the distribution of outcomes for each watering treatment, and the displayed results potentially indicate changes among treatments in the skewness, kurtosis, and modality of the distributions.
Outcomes of interactions between plants and pathogens can be influenced by temperature, light, moisture levels, and nutrition (23). For example, some genes for stem and leaf rust resistance in wheat vary in their effectiveness with temperature. Wheat plants with the Sr15 gene are resistant to some races of Puccinia graminis tritici at 15°C, show increased infection at 20°C, and exhibit a fully susceptible response at 26°C (23). Even different forms of nutrients can influence disease severity in plants. Ammonium and nitrate nitrogen often have opposite effects on disease levels (65). Few of these studies, however, report the distributions. In interactions between wild barley and powdery mildew in Israel, the distributions of disease severity differ between plants grown in sun or shade (34). In some extreme cases, the distribution of disease severity in shaded plants is skewed heavily to the right whereas in plants grown in the sun the distribution is skewed to the left.
EVOLUTIONARY CHANGES IN MODES OF
INTERACTION
The distributions of outcomes within and among populations can provide evidence for the ways in which new modes of interaction evolve, including
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.
80 THOMPSON
the evolution of sublethal grazing interactions from predator/prey interactions. Interactions between predators and prey are not always either strictly successful or unsuccessful from either the predator or prey viewpoint. There can be variation in the amount of damage that a predator inflicts on a prey individual that gets away and variation in the parts of a prey individual that a predator can capture or eat (the reward per captured prey). Variation within populations in failure rates at capturing prey and variation in the levels of sublethal damage on prey both provide opportunities for understanding how different combinations of traits affect the outcomes of interactions (166). In some cases sublethal damage to a prey individual may provide no nutrition to the predator, as in unsuccessful drilling or shell-breaking by marine predators (166) or beak damage by birds on butterfly wings (72). But in other cases sublethal damage may provide the predator with some nutrition, such as loss of leaf tissue to herbivores or loss of a tail to vertebrate predators in some lizards.
Some interactions that result in sublethal damage to the victim but provide some nutrition to the attacker may in fact be evolutionary consequences of selection on prey with modular structure to minimize the negative effects of inevitable interactions with predators (149). In modular organisms such as plants, some body parts can be lost without the individual dying. Grasses and large herbivorous mammals have been undergoing diffuse coevolution for millions of years (142). The current outcomes of interactions between grasses and large, hooved mammals vary geographically, depending upon the morphology of the plants (83). In North America, grasses in the Great Plains have a long evolutionary history of interactions with large , hooved mammals. The major grasses in these communities have morphological traits, including rhizomatous growth, well-adapted to such grazing. In contrast, grasses in the northern Intermountain West were never subjected to the large herds of grazing mammals common east of the Rockies. These caespitose grasses were readily killed when large, grazing mammals (cows) were placed in these steppe communities (83). Hence, the interaction between grasses and large, grazing mammals in North America varies from predation on individual plants to "grazing," in which plants lose leaves but generally are not killed by the interaction. Similar differences in response to herbivory by large hooved mammals occur among grasslands on other continents as well (82).
The conflicting results and viewpoints on the effects of herbivory on plant growth and reproduction together highlight the need for analyses of the distributions of outcome (11, 90, 102). Few studies of herbivory display the distributed outcomes for plant growth or seed production, report whether the distributions become skewed or change in kurtosis relative to control plants without herbivory, or partition the results by plant age or size. Moreover, few
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.
VARIATION IN SPECIES INTERACTIONS 81
studies of herbivory are conducted under several environmental conditions to see how the results vary among environments. Yet these results are as important as the means in understanding the effects of herbivory on individual plants, plant populations, and selection. In the absence of reported distributions of outcome, it is not possible to know whether the increased means in flower and fruit production with herbivory result from increases in (a) all plants, (b) a majority of plants with a nonnal distribution around the mean, (c) a small number of plants that do very well with herbivory thereby producing a highly skewed distribution, or (d) one or several subgroups of plants, producing a bimodal or multimodal distribution of outcomes.
FINAL REMARKS
Evolutionary history is the record of diversification in species and the interactions that link their life histories. The interactions partly shape the evolution of species and are partly shaped themselves as species change. The result is the ever-changing mix of species and interactions called biological communities. Consequently, the two most general problems for evolutionary theory are to understand how populations and species evolve, and to understand how interactions are molded, changed, or diversified under different ecological and genetic conditions.
Just as the study of the evolution of species requires that we understand the origins and partitioning of variation among individuals, the study of the evolution of interspecific interactions requires that we understand the origins and partitioning of variation in outcomes of interactions between species. The study of distributed outcomes, correlated outcomes, the patch dynamics of interactions, and interaction norms can show how different aspects of po pulation structure and environmental conditions affect interactions. Achieving realistic evolutionary models of species interactions will demand detailed studies of these distributions of outcome. Analyses of distributions as well as mean outcomes are becoming more common, but they are not yet a standard part of studies of species interactions. The study of the patterns of variation in the outcomes of interactions provides a route toward understanding both selection and constraints on evolving interactions.
ACKNOWLEDGMENTS
I am grateful to Jeremy Burdon, Peter Feinsinger, Douglas Futuyma, Olle Pellmyr, Peter Price, and Wayne Wehling for very helpful comments on the manuscript. This work was supported by USDA Competitive Grant (Biological Stress) 84(86)-CRCR-1-1395 and NSF grant BSR 8705394.
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.
82 THOMPSON
Literature Cited
I . Abrams, P. A. 1 987. On classifying interactions between populations. Oecologia 73:272-8 1
2. Addicott, J . F. 1 986. Variation in the costs and benefits of mutualism: the interaction between yuccas and yucca moths . Oecologia 70:486--94
3 . Anderson, R. M . , Crombie, J . A. 1 985. Experimental studies of age-intensity and age-prevalence profiles of infection: Schistosoma mansoni in snails and mice. See Ref. 1 2 1 , pp. 1 1 1-45
4. Anderson, R. M . , May, R. M. 1 982. Coevolution of hosts and parasites. Parasitology 85:41 1-26
5. Armbruster, W. S. 1 986. Reproductive interactions between sympatric Dalechampia species: are natural assemblages "random" or organized? Ecology 67:522-33
6. Barrett, 1. 1 985. The gene-for-gene hypothesis: parable or paradigm. See Ref. 1 2 1 , pp. 2 1 5-25
7. Bazzaz, F. A. 1983. Characteristics of populations in relation to disturbance in natural and man-modified ecosystems. In Disturbance and Ecosystems, ed. H. A. Mooney, M . Godron, pp. 259-77. Berlin/New York: Springer-Verlag. 292 pp.
8. Bazzaz, F. A . , Carlson, R. W . 1 984. The response of plants to elevated CO2, I. Competition among an assemblage of annuals at two levels of soil moisture. Oecologia 62: 1 96--8
9. Beattie, A. 1. 1 985. The Evolutionary Ecolo/?y of Ant-Plant Mutualisms. Cambridge: Cambridge Dniv. Press. 1 82 pp.
1 0 . Begon, M. 1 984. Density and individual fitness: asymmetric competition. In Evolutionary Ecology, ed. B . Shorrocks, pp. 1 75-94. Oxford: Blackwell. 4 1 8 pp.
I I . Belsky, A. 1. 1 986. Does herbivory benefit plants? A review of the evidence Am. Nat. 1 27:870-92
1 2 . Bengtsson, 1. 1 986. Life histories and interspecific competition between three Daphnia species in rockpools. 1. Anim. Ecol. 55:641-55
1 3 . Berenbaum, M. R . , Zangerl, A. R . , Nitao, 1 . K. 1 986. Constraints o n chemical coevolution: wild parsnips and the parsnip webworm. Evolution 40: 1 2 1 5-28
14. Black, F. L. 1 966. Measles endemicity in insular populations: critical size and its evolutionary implications. 1. Theor. Biol. 1 1 :207- 1 1
1 5 . Black, F. L . 1 984. Measles. See Ref. 40, pp. 397-41 8
1 6 . Boryslawski , Z . , Bentley, B . L . 1 985. The effect of nitrogen and clipping on
interference between C3 and C4 grasses. 1. Ecol. 73: 1 1 3-21
1 7 . Boucher, D. H . , ed. 1 985. The Biology of Mutualism: Ecology and Evolution. Oxford: Oxford Dniv. Press. 388 pp.
1 8 . Bowen, G. D. 1980. Mycorrhizal roles in tropical plants and ecosystems. In Tropical Mycorrhiza Research, ed. P. Mikola, pp. 1 1 6--90. Oxford: Clarendon. 270 pp.
19 . Brown, 1. H . , Munger, 1. C. 1 985. Experimental manipulation of a desert rodent community: food addition and species removal. Ecology 66: 1 545-63
20. Bryant, 1. P. , Chapin, F. S . III , Klein, D. R . 1 983. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357-68
2 1 . Bryant, 1. P . , Chapin, F. S. III , Reichardt, P. B . , Clausen, T. P. 1987. Response to winter chemical defense in Alaska paper birch and green alder to manipulation of plant carbOn/nutrient balance. Oecologia 72:5 1 0-14
22. Burdon, J . J . 1 982. The effect of fungal pathogens on plant communities. In The Plant Community as a Working Mechanism, ed. E. I. Newman, pp. 99- 1 1 2 . Spec. Publ. Ser. Br. Ecol. Soc. No. I . 1 28 pp.
23. Burdon, 1 . 1 . 1 987. Diseases and Plant Population Biology. Cambridge: Cambridge Dniv. Press. 208 pp.
24. Burdon, 1. J . , Oates, J. D. , Marshall , D . R . 1 983. Interactions between Avena and Puccillia species I. The wild hosts: A vella barbata Pott ex Link, A . fatua L . , A . ludovicialla Durieu. 1. Appl. Ecol. 20:57 1-84
25. Campbell, D . R . , Motten, A. F. 1 985. The mechanism of competition for pollination between two forest herbs. Ecology 66:554-63
26. Cates, R. G. 1 975. The interface between slugs and wild ginger: some evolutionary aspects. Ecology 56:391-400
27. Clarke, B. 1 979. The evolution of genetic diversity. Proc. R. Soc. LOlldon Ser B 205:453-74
28. Compton, S. G . , Beesley, S. G . , lones, D. A. 1983. On the polymorphism of cyanogenesis in Lotus corniculatus L. IX. Selective herbivory in natural populations at Porthdafarch, Anglesey. Heredity 5 1 :537-48
29. Connell, J. H. 1 96 1 . The influence on interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology 42:7 1 0-23
30. Connell , J . H. 1983 . On the prevalence and relative importance of interspecific
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.
V ARIA TION IN SPECIES INTERACTIONS 83
compeuuon. evidence from field experiments. Am. Nat. 1 22:66 1-96
3 1 . Connell , J. H . , Keough , M. J. 1 985. Disturbance and patch dynamics of subtidal marine animals on hard substrata. See Ref. 1 1 0, pp. 1 25-5 1
32. Cox, C. S . , McEvoy, P. B. 1983 . Effect of summer moisture stress on the capacity of tansy ragwort (Senecio jacobaea) to compensate for defoliation by cinnabar moth (Tyria jacobaeae). J. Appl. £Col. 20: 225-34
33. Day, P. R. 1 974. Genetics of HostParasite Interactions. San Francisco: Freeman. 238 pp.
34. Dinoor, A . , Eshed, N. 1 987. The analysis of host and pathogen populations in natural ecosystems. In Populations of Plant Pathogens : Their Dynamics and Genetics ed. M. S . Wolfe . C. E. Caten. pp. 75-88. Blackwell: Oxford. 280 pp.
35. Dirzo, R. 1 984. Herbivory: a phytocentric overview. In Perspectives on Plant Population Ecology, ed. R. Dirzo, J. Sarukhan, pp. 1 4 1-65. Sunderland, Massachusetts: Sinauer Associates. 478 pp.
36. Dino, R . , Harper, J. L. 1982. Experimental studies on slug-plant interactions. III. Differences in the acceptability of individual plants of Trifolium repens to slugs and snails. J. Ecol. 70: 1 0 1 - 1 7
3 7 . Ebba, T. , Person, C. 1 975. Genetic control of virulence in Ustilago hordei, IV. Duplicate genes for virulence and genetic and environmental modification of a gene-for-gene relationship. Can. J. Gen . Cytol. 1 7:63 1-36
38. Ehrlich, R. R . , Raven, P. H. 1 964. Butterflies and plants: a study in coevolution. Evolution 1 8:586--608
39. Ellison, R. L . , Thompson, J. N. 1 987. Variation in seed and seedling size: the effects of seed herbivores on Lomatium grayi (Umbelliferae) . Oikos 49:269-80
40. Evans, A. S . , ed. 1 984. Viral Infections of Humans: Epidemiology and Control. New York: Plenum Medical Book Company. 720 pp.
4 1 . Evans, A. S. 1984. Epidemiological concepts and methods. See Ref. 40, pp. 3-42
42. Ewald, P. W. 1 983. Host-parasite relations, vectors , and the evolution of disease severity . Annu. Rev. Ecol. Syst. 1 4:465-85
43. Feinsinger, P. 1 987. Effects of plant species on each other's pollination: is community structure influenced? Trends Ecol. Evol. 2: 1 23-26
44. Feinsinger, P . , Murray, K. G . , Kinsman, S . , Busby, W. H. 1 986. Floral
neighborhood and poIlination success in four hummingbird-pollinated cloud forest plant species. Ecology 67:449-64
45 . Feinsinger, P. , Beach, J. H., Linhart, Y. B . , Busby, W. H . , Murray, G. 1 987. Disturbance, pollinator predictability , and pollination success among Costa Rican cloud forest plants. Ecology 68: 1 294-1305
46. Futuyma, D. J. 1 979. Evolutionary Biology. Sunderland, Mass: Sinauer. 565 pp.
47. Futuyma, D. J. 1 983. Selective factors in the evolution of host choice by phytophagous insects. In Herbivorous Insects: Host-Seeking Behavior and Mechanisms, ed. S . Ahmad. pp . 227-44. New York: Academic. 257 pp.
48. Futuyma, D. J. 1 988. The evolution of ecological specialization. Annu. Rev. Ecol. Syst. 1 9:207-33
49. Futuyma, D. J . , Slatkin, M . , ed. 1 983. Coevolution . Sunderland, Mass: Sinauer. 555 pp.
50. Futuyma, D. J . , Peterson , S. C . 1 985. Genetic variation in the use of resources by insects. Annu. Rev. Entomol. 30: 2 1 7-38
5 1 . Futuyma, D. J . , Cort, R. P . , van Noordwijk , I. 1 984. Adaptation to host plants in the fall cankerworm (Alsophila pometaria) and its bearing on the evolution of host affiliation in phytophagous insects. Am. Nat. 1 23: 287-96
52. Gilbert, L. E. 1 983. Coevolution and mimicry. See Ref. 49, pp. 263-8 1
53. Gilbert, L. E . , Raven, P. H . , eds. 1 975. Coevolution of Animals and Plants . Austin, Tex: Univ. Tex. Press. 246 pp.
54. Gill, D. E . , Mock. B. A. 1 985. Ecological and evolutionary dynamics of parasites: the case of Trypanosoma diemyctyli in the red-spotted newt Notophthalmus viridenscens. See Ref. 1 2 1 , pp. 1 57-83
55. Givnish, T. J . , Burkhardt, E. L . , Happel, R. E . , Weintraub, J. D. 1 984. Carnivory in the bromeliad Brocchinia reducta, with a cost/benefit model for the general restriction of carnivorous plants to sunny, moist, nutrient-poor habitats. Am. Nat. 1 24:479-97
56. Glezen, W. P . , Loda, F. A . , Denny, R . W . 1 984. Parainfluenza viruses. See Ref. 40, pp. 441-54
57. Gould, F. 1 979. Rapid host range evolution in a population of the phytophagous mite Tetranychus urticae Koch. Evolution 33:791-802
58. Grubb, P. J. 1 977. The maintenance of species-richness in plant communities: the importance of the regeneration niche. Bioi. Rev. 52: 1 07-45
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.
84 THOMPSON
59. Gupta, A. P . , Lewontin, R. C. 1982. A study of reaction norms in natural populations of Drosophila pseudoobscura. Evolution 36:934-48
60. Hatchett, J. H . , Gallun, R. L. 1970. Genetics of the ability of the Hessian fly, Mayetiola destructor, to survive on wheats having different genes for resistance. Ann. Entomol. Soc. Am. 63: 1 400-7
6 1 . Haukioja, E. 1980. On the role of plant defenses in the fluctuation of herbivore populations. Oikos 35:202-1 3
6 2 . Haukioja, E . , Neuvonen, S . 1985. Induced long-term resistance of birch foliage against defoliators: defensive or incidental? Ecology 66: 1 303-8
63. Higgins, S . S . , Bendel, R. B . , Mack, R. N. 1 984. Assessing competition among skewed distributions of plant biomass: an application of the jackknife. Biomet· rics 40: 1 3 1-37
64. Holl, W. 1983. Interactions between plants and animals in marine systems. Physiol. Plant. Ecol. 3:469-88
65 . Huber, D. M . , Watson, R. D. 1974. Nitrogen form and plant disease. Annu. Rev. Phytopathol. 1 2: 139-65
66. Huston, M . , Smith, T. 1 987. Plant succession: life history and competition. Am. Nat. 130: 1 68-98
67. Huxley, C. 1 980. Symbiosis between ants and epiphytes. Bioi. Rev. 55:321-40
68. Islam, Z. , Crawley, M. J. 1983 . Com· pensation and regrowth in ragwort (Senecio jacobaea) attacked by cinnabar moth (Tyria jacobaeae). J. Ecol. 7 1 : 829-43
69. Janos, D. P. 1 980. Mycorrhizae influence tropical succession. Biotropica 1 2 (Suppl.):56-64
70. Janzen, D. H. 1974. Epiphytic myrmecophytes in Sarawak: mutualism through the feeding of plants by ants. Biotropica 6:237-59
7 1 . Janzen, D. H. 1 979. How many babies do figs pay for babies? Biotropica 1 1 :48-50
72. Jeffords, M. R . , Stemburg, J. G . , Waldbauer, G. P. 1 979. Batesian mimicry: field demonstration of the survival value of pipevine swallowtail and monarch color patterns. Evolution 22:275-86
73. Kitchell, J. A. 1986. The evolution of predator-prey behavior: naticid gastropods and their molluscan prey. In Evolution of Animal Behavior: Paleontological and Field Approaches, ed. M. H. Nitecki, J. A. Kitchell, pp. 88- 1 10. New York: Oxford Univ. Press. 1 84 pp.
74. Kitchell, J. A . , Boggs, C. H. , Kitchell, J. F . , Rice, J. A. 1 98 1 . Prey selection
by naticid gastropods: experimental tests and application to the fossil record. Paleobiology 7:533-52
75. Koptur, S . , Lawton, J. H. 1988. Interactions among vetches bearing extrafloral nectaries, their biotic protective agents, and herbivores. Ecology 69:278-83
76. Lawton, J. H . , Hassell, M. P. 198 1 . Asymmetrical competition i n insects. Nature 289:793-95
77. Levin, B . R . , Lenski, R. E. 1983. Coevolution in bacteria and their viruses and plasmids. See Ref. 49, pp. 99-1 27
78. Levine, S. H. 1976. Competitive interactions in ecosystems. Am. Nat. 1 10:903-1 0
7 9 . Lewis, D. H. 1973. The relevance of symbiosis to taxonomy and ecology, with particular reference to mutua1istic symbioses and the exploitation of marginal habitats . In Taxonomy and Ecology, ed. V. H. Heywood, pp. 1 5 1-72. New York: Academic Press. 370 pp.
80. Lewontin, R. C. 1970. The units of selection. Annu. Rev. Ecol. Syst. 1 : 1- 1 8
8 1 . MacFarlane, 1 . H . , Thorsteinson, A. J . 1980. Development and survival of the twostriped grasshopper, Melanoplus bivittatus (Say) (Orthoptera: Acrididae), on various single and multiple plant diets . Acrida 9:63-76
82. Mack, R. N. 1988. Temperate grasslands vulnerable to plant invasion: characteristics and consequences. In Biological Invasions: A Global Perspective. ed. J. Drake, F. di Castri, R. Groves, F. Kruger, et al. New York: Wiley & Sons. In press
83. Mack. R. N . • Thompson. J. N. 1982. Evolution in steppe with few large, hooved mammals. Am. Nat. 1 19:757-73
84. Maddox, G. D . , Root, R. B . 1987. Resistance to 16 diverse species of herbivorous insects within a population of goldenrod, Solidago altissima: genetic variation and heritability. Oecologia 72:8-14
85. Marquis, R. I. 1984. Leaf herbivores decrease fitness of a tropical plant. Science 226:537-39
86. Martinez, L. , Silver, M . W . , King, 1. M., Alldredge, A. L. 1983. Nitrogen fixation by floating diatom mats: a source of new nitrogen to oligotrophic ocean waters. Science 221 : 152-54
87. Massad, E. 1987. Transmission rates and the evolution of pathogenicity. Evolution 4 1 : 1 127-30
88. May, R. M. 1985. Host-parasite associations: their population biology and population genetics. See Ref. 1 2 1 , pp. 243-62
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.
V ARIA TION IN SPECIES INTERACTIONS 85
89. May, R. M . , Anderson, R. M . 1983. Epidemiology and genetics on the coevolution of parasites and hosts. Proc. R. Soc. Lond. B. 2 1 9:281-3 1 3
90. McNaughton, S . J . 1 986. On plants and herbivores. Am. Nat. 1 28:765-70
9 1 . Melnick. J. L. 1984. Enterviruses. See Ref. 40, pp. 1 87-251
92. Miller, R. M., larstfer, A . G., PiIlai, 1 . K. 1 987. Biomass allocation in an Agropyron smithii-glomus symbiosis. Am. J. Bot. 74: 1 14-22
93. Mode, C. 1. 1958. A mathematical model for the co-evolution of obligate parasites and their hosts. Evolution 1 2 : 1 58-65
94. Moran, N. 1 98 1 . Intraspecific variability in herbivore performance and host quality: a field study of Uroleucon caligatum (Homoptera: Aphididae) and its Solidago hosts (Asteraceae) . Ecol. Entomol. 6:301-06
95. Moran, N. 1986. Benefits of host plant specificity in Uroleucon (Homoptera: Aphididae). Ecology 67: 1 08-1 5
96. Morse, D. H . 1 974. Niche breadth as a function of social dominance. Am. Nat. 1 08:81 8-30
97. Muscatine, L. , Porter, 1. W. 1977. Reef corals: mutualistic symbioses adapted to nutrient-poor environments. BioScience 27:454-60
98. Nitecki , M. H . , ed. 1 983. Coevolution. Chicago: Univ. Chicago Press. 392 pp.
99. Oates, 1. D . , Burdon, 1. J . , Brouwer, 1. B. 1983. Interactions between Avena and Puccinia species II. The pathogens: Puccinia coronata Cda and P. graminis Pers. f. sp. avenae Eriks & Henn. J. Appl. Ecol. 20:585-96
100. O'Dowd, D. 1 . 1 979. Foliar nectar production and ant activity on a neotropical tree, Ochroma pyramidale. Oecologia 43:233-48
1 0 1 . Oster, G . , Takahashi , Y. 1974. Models for age-specific interactions in a periodic environment. Ecol. Monogr. 44:483-501
102. Paige, K . N., Whitham, T. G. 1987. Overcompensation in response to mammalian herbivory: the advantage of being eaten. Am. Nat. 1 29:407- 1 6
! O3 . Pacala, F. , Roughgarden, J . 1 9 8 2 . Resource partitioning and interspecific competition in two two-species insular Anolis lizard communities. Science 2 1 7 : 444-46
104. Paine, R. T . , Levin, S . A . 1 98 1 . Intertidal landscapes: disturbance and the dynamics of pattern. Ecol. Monogr. 5 1 : 1 45-78
1 05 . Park, T. 1954. Experimental studies of interspecies competition. II. Tempera-
ure, humidity and competition in two species of Tribolium. Physiol. Zool. 27: 1 77-238
1 06. Parker, M. A. 1 985. Local population differentiation for compatibility in an annual legume and its host-specific fungal pathogen. Evolution 39:7 1 3-23
1 07 . Parker, M. A. 1 986. Individual variation in pathogen attack and differential reproductive success in the annual legume, Amphicarpaea bracteata. Oecologia 69: 253-59
1 08. Pianka, E. R. 1974. Evolutionary Ecology. New York: Harper & Row. 356 pp.
109. Pickett, S. T. A . , Bazzaz, F. A. 1 978. Organization of an assemblage of early successional species on a soil moisture gradient. Ecology 59: 1 248-55
1 10. Pickett, S. T. A . , White, P. S . , eds. 1 985. The Ecology of Natural Disturbance and Patch Dynamics. New York: Academic Press. 472 pp.
1 1 1 . Pimentel , D. 1 96 1 . Animal population regUlation by the genetic-feedback mechanism. Am. Nat. 95:65-79
1 I 2. Price, P. W . , Bouton, C. E. , Gross, P. , McPheron, B . A . , Thompson, 1. N . , Weis, A . E. 1980. Interactions among three trophic levels: influence of plants on interactions between insect herbivores aM natural enemies. Annu. Rev. £Col. Syst. 1 1 :4 1-65
1 1 3 . 'Price, P. W . , Westoby, M . , Rice, B . , Fritz, R. S . , Thompson, J . N . , Mobley, K. 1986. Parasite mediation in ecological interactions. Annu. Rev. Ecol. Syst. 1 7:487-505
1 14. Price, T. 1987. Diet variation in a population of Darwin's finches. Ecology 68: 1 0 1 5-28
1 1 5 . Pyke, D. A. 1 987. Demographic responses of Bromus 'tectorum and seedlings of Agropyron spicatum to grazing by small mammals: the influence of grazing frequency and plant age. J. Ecol. 75 :825-35
1 16. Rathcke, B. 1984. Competition and facilitation among plants for pollination. In Pollination Biology, ed. L. Real , pp. 305-29. New York: Academic Press. 338 pp.
i l7. Rausher, M. D. 1984. Trade-offs 'in performance on different hosts: evidence from within- and between-site variation in the beetle Deloyala guttata. Evolution 38:582-95
1 1 8 . Rhoades , D. F. 1985. Offensive-defensive interactions between herbivores and plants: their relevance in herbivore population dynamics and ecological theory. Am. Nat. 1 25 :205-38
1 1 9. Rice, K. 1 . , Menke, 1 . W. 1 985. Competitive reversals and environment-
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.
86 THOMPSON
dependent resource partitioning in Ero� dium. Oecologia 67:430-34
1 20. Ricklefs, R. E. 1 973. Ecology. Newton, Mass: Chiron. 861 pp.
1 2 1 . Rollinson, D . , Anderson, R. M. eds. 1 985. Ecology and Genetics of Host� Parasite Interactions. New York: Aca� demic. 266 pp.
1 22 . Room, P. M . , Thomas, P. A . 1 985. Nitrogen and establishment of a beetle for biological control of the floating weed Salvinia in Papua New Guinea. J. Appl. Eco!. 22: 1 39-56
123. Roughgarden, J. 1 975. Evolution of marine symbiosis-a simple cost�benefit model. Ecology 56: 1 20 1-08
1 24. Roughgarden, J. 1 979. Theory of Pop� ulation Genetics and Evolutionary Ecology: An Introduction. New York: Macmillan. 634 pp.
1 25 . Roughgarden, J . 1 983. The theory of coevolution. See Ref. 49, pp. 33-64
1 26. Roughgarden , J . , Diamond, J. 1 986. Overview: the role of species interactions in community ecology. In Community Ecology, ed. J. Diamond, T. 1. Case, pp. 333-43. New York: Harper & Row, 704 pp.
1 27. Ryan, C. A. 1 979. Proteinase inhibitors. In Herbivores: Their Interaction with Plant Secondary Metabolites, ed. G . A. Rosenthal, D . H . Janzen, pp. 599-6 1 8. New York: Academic. 7 1 8 pp.
1 27a. Sauer, J. R. , Slade, N. A. 1987. Sizebased demography of vertebrates. Annu. Rev. Evol. Syst. 1 8:71-90
128. Schaffer, W. M. 1 98 1 . Ecological abstraction: the consequences of reduced dimensionality in ecological models. Eco!. Monogr. 5 1 :383-40 1
129. Schemske, D. W. 1 980. The evolution� ary significance of extrafloral nectar production by Costus woodsonii (Zingiberaceae): an experimental analysis of ant protection. J. Ecol. 68:959-67
1 30. Schemske, D . W. 1 98 1 . Floral convergence and pollinator sharing in two bee-pollinated tree herbs. Ecology 62: 946-54
1 3 1 . Schoener, T. W. 1 983. Field experiments on interspecific competition. Am. Nat. 1 22:240-85
1 32. Schupp, E. W . 1 986. Azteca protection of Cecropia: ant occupation benefits ju� venile trees. Oecologia 70:379-85
1 3 3 . Scriber, J. M . , Slansky, F. Jr. 1 98 1 . The nutritional ecology of immature insects. Annu. Rev. Entomo!' 26: 1 83-2 1 1
1 34. Service, P . 1 984. Genotypic interactions in an aphid-host plant relationship: Uroleucon rudbeckiae and Rudbeckia laciniata . Oecologia 6 1 :27 1-76
1 35 . Service, P. M . , Lenski, R. E. 1 982. Aphid genotypes, plant phenotypes, and genetic diversity: a demographic analysis of experimental data. Evolution 36: 1 276-82
1 36 . Sidhu, G. S . , Webster, 1. M. 1 98 1 . The genetics of plant-nematode parasitic systems. Bot. Rev. 47:387-4 1 9
1 37. Slansky, F . , Jr. , Scriber, J . M . 1 985 . Food consumption and utilization. In Comprehensive Insect Physiology, Biochemistry, and Pharmacology, Vol. 4 , ed. G. A . Kerkut, L. I . Gilbert, pp. 87- 1 63. Oxford: Pergamon. 639 pp.
1 38 . Slatkin, M. 1987. Gene flow and the geographic structure of natural populations. Science 236:787-92
1 39 . Slatkin, M . , Maynard Smith, J. 1979. Models of coevolution. Q . Rev. BioI. 54:233-63
140. Sousa, W. P. 1985 . Disturbance and patch dynamics on rocky intertidal shores. See Ref. 1 10, pp. 1 01-24
1 4 1 . Steams, S. C . , Koella, 1. C. 1 986. The evolution of phenotypic plasticity in lifehistory traits: predictions of reaction norms for age and size at maturity. Evolution 40:893-91 3
1 42 . Stebbins, G . L . 1 98 1 . Coevolution of grasses and herbivores. Ann. Missouri Bot. Gard. 68:75-86
143. Stewart, F. M . , Levin, B. R . 1984. The population biology of bacterial viruses: why be temperate? Theor. Pop . Bioi. 26:93-1 1 7
144. Tabashnik, B. E . , Slansky" F. Jr. 1 987 . Nutritional ecology of forb foliagechewing insects. In Nutritional Ecology of Insects, Mites, Spiders, and Related Invertebrates, ed. F. Slansky, Jr. , J. G . Rodriguez, pp. 7 1-103. New York: Wiley. 1 0 1 6 pp.
145. Teakle, R. E. , Jensen, J. M . , Giles, J . E . 1 986. Age-related susceptibility of Heliothis punctiger to a commercial formulation of nuclear polyhedrosis virus. J. Invert. Patho!. 47:82-92
146. Templeton, A. R . , Gilbert, L. E. 1 985. Population genetics and the coevolution of mutualism. See Ref. 1 7 , pp. 1 28-44
1 47. Thompson, J. N. 1978. Within-patch structure and dynamics in Pastinaca sativa and resource availability to a specialized herbivore . Ecology 59:443-48
1 48 . Thompson, J. N. 1 98 1 . Reversed animal-plant interactions: the evolution of insectivorous and ant-fed plants. Bioi. J. Linn. Soc. 1 6 : 147-55
1 49. Thompson, J. N. 1 982. Interaction and Coevolution. New York: Wiley. 1 79 pp.
1 50. Thompson, J . N. 1 985. Postdispersal seed predation in Lomatium spp.
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.
VARIATION IN SPECIES INTERACTIONS 87
(Umbelliferae): vanatlOn among individuals and species. Ecology 66: 1 608-1 6
1 5 1 . Thompson, J . N . 1 985. Within-patch dynamics of life histories, populations, and interactions: selection over time in small spaces. See Ref. 1 10, pp. 253-64
152 . Thompson, J. N. 1 986. Pattems in coevolution. In Coevolution and systematics, ed. A . R. Stone, D . L. Hawksworth, pp. 1 19- 1 43. Oxford: Clarendon Press. 1 47 pp.
1 5 3 . Thompson, J . N. 1 986. Constraints on arms races in coevolution. Trends Ecol. Evol. 1 : 105-7
1 54. Thompson, J. N. 1 987. Symbiontinduced speciation. Bioi. J. Linn. Soc. 32:385-93
155 . Thompson, J. N. 1988. Evolutiunary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol. Exp . Appl. In press
1 56. Thompson, J. N . , Moody, M. E. 1 985. Assessing probability of interaction in size-structured populations: Depressaria attack on Lomatium. Ecology 66: 1597-1607
1 57. Thomson, 1. D. 1 982. Visitation rate patterns in animal-pollinated plants. Oikos 39:241 -50
158. Thomson, J. D . 1983. Component analysis of community-level interactions in pol lination systems. In Handbook oj Experimental Pollination Biology, ed. C. E. Jones, R . J . Little, pp. 45 1 -60. New York: Van Nostrand Reinhold. 558 pp.
159. Tilman, D. 1978. Cherries, ants and tent caterpillars: timing of nectar production in relation to susceptibility of caterpillars to ant predation. Ecology 59:686-92
160. Tilman, D. 1 982. Resource Competition and Community Structure . Princeton: Princeton Univ. Press. 296 pp.
1 6 1 . Tilman, D. 1 987. Secondary succession and the pattern of plant dominance along experimental nitrogen gradients. Ecol. Monogr. 57: 1 89-21 4
1 62. Tuomi, J . , Niemeliin, P . , Haukioja, E . , S ire , S . , Neovonen, S . 1984. Nutrient stress: an explanation for plant antiherbivore responses to defoliation. Oecologia 6 1 :208- 1 0
1 63 . Turner, M. D . , Rabinowitz, D. 1983. Factors affecting frequency distributions of plant mass: the absence of dominance and suppression in competing monocul-
tures of Festuca paradoxa. Ecology 64:469-75
1 64. Vandermeer, 1 . 1980. Indired mutualism: variations on a theme by Stephen Levine. Am. Nat. 1 16:441-48
1 65. Vandermeer, J . , Hazlett, B . , Rathcke, B. 1985. Indirect facilitation and mutualism. See Ref. 1 7 , pp. 326-43
1 66. Vermeij , G. J. 1 982. Unsuccessful predation and evolution. Am. Nat. 1 20: 701-20
1 67. Vermeij , G. J. 1 983. Intimate association and coevolution in the sea. See Ref. 49, pp. 3 1 1-27
168. Via, S. 1 984. The quantitative genetiCS of polyphagy in an insect herbivore . I . Genotype-environment interaction in larval performance on different host plant species. Evolution 38:88 1-95
1 69. Vitousek, P. M . , Walker, L. R . , Whiteaker, L . D . , Mueller-Dombois, D . , Matson, P. A. 1987. Biological invasion of Myrica Jaya alters ecosystem developments in Hawaii. Science 238: 802-4
1 70. Vrijenhoek, R. C. 1 985. Animal population genetics and disturbance: the effects of local extinctions and recolonizations on heterogeneity and fitness. See Ref. 1 09 , pp. 265-85
1 7 1 . Walker, L. R . , Chapin, F. S. III. 1 986. Physiological controls over seedling growth in primary successiun on an Alaskan floodplain . Ecology 67: 1508-23
1 72. Weiner, J. 1 985. Size hierarchies in experimental populations of annual plants. Ecology 66:743-52
173. Weiner, J . , Thomas, S. C. 1986. Size variability and competition in plant monocultures. Oikos 47:21 1-22
1 74 . Werner, E. E. , Gi lliam , J . F. 1984. The ontogenetic niche and species interactions in size-structured populations. Annu. Rev. Ecol. Syst. 1 5 :393-425
175 . Wilkinson, C. R. 1987. Interocean differences in size and nutrition of coral reef sponge popUlations. Science 236: 1 654--57
1 76. Wilson, D. S . 1 983. The group selection controversy: history and current status. Annu. Rev. Ecol. Syst. 1 4 : 1 59-87
1 77. Windle, P. N . , Franz, E. H. 1 979. The effects of insect parasitism on plant competition: greenbugs on barley. Ecology 60:521-529
1 7 8 . Yonge, C. M. 1 968 . Living corals. Proc. R . Soc. Lond, B 1 69:329-44
Ann
u. R
ev. E
col.
Syst
. 198
8.19
:65-
87. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Sher
broo
ke o
n 06
/10/
14. F
or p
erso
nal u
se o
nly.