What is the fundamental niche of chthamalus

CHAPTER 17

Smith, T. M., & Smith, R. L. (2015). Elements of Ecology (9th ed.). Boston, MA: Pearson.

17.1 Community Structure Is an Expression of the Species’ Ecological Niche

As we discussed in Chapter 16, the biological structure of a community is defined by its species composition, that is, the species present and their relative abundances. For a species to be a component of an ecological community at a given location, it must first and foremost be able to survive. The environmental conditions must fall within the range under which the species can persist—its range of environmental tolerances. The range of conditions under which individuals of a species can function are the consequences of a wide variety of physiological, morphological, and behavioral adaptations. As well as allowing an organism to function under a specific range of environmental conditions, these same adaptations also limit its ability to do equally well under different conditions. As a result, species differ in their environmental tolerances and performance (ability to survive, grow, and reproduce) along environmental gradients. We have explored many examples of this premise. Plants adapted to high-light environments exhibit characteristics that preclude them from being equally successful under low-light conditions (Chapter 6). Animals that regulate body temperature through ectothermy (poikilotherms) are able to reduce energy requirements during periods of resource shortage. Dependence on external sources of energy, however, limits diurnal and seasonal periods of activity and the geographic distribution of poikilotherms (Chapter 7). Each set of adaptations enable a species to succeed (survive, grow, and reproduce) under a given set of environmental conditions, and conversely, restricts or precludes success under different environmental conditions. These adaptations determine the fundamental niche of a species (Section 12.6).

The concept of the species’ fundamental niche provides a starting point to examine the factors that influence the structure of communities. We can represent the fundamental niches of various species with bell-shaped curves along an environmental gradient, such as mean annual temperature or elevation (Figure 17.1a). The response of each species along the gradient is defined in terms of its population abundance. Although the fundamental niches overlap, each species has limits beyond which it cannot survive. The distribution of fundamental niches along the environmental gradient represents a primary constraint on the structure of communities. For a location that corresponds to a given point along the environmental gradient, only a subset of species will be potentially present in the community, and their relative abundances at that point provide a first approximation of the expected community structure (Figure 17.1a). As environmental conditions change from location to location, the possible distribution and abundance of species changes, which changes the community structure. For example, Figure 17.2 is a description of the biological structure of the breeding bird community on the Walker Branch Watershed in east Tennessee (species present and their relative abundances). The figure shows the maps of geographic range and population abundance of four of the bird species that are components of the bird community on the watershed. As we discussed previously, these geographic distributions reflect the occurrence of suitable environmental conditions (within the range of environmental tolerances; Chapter 8). Note that the geographic distributions of the four species are quite distinct, and the Walker Branch Watershed in east Tennessee represents a relatively small geographic region where the distributions of these four species overlap. As we move from this site in east Tennessee to other regions of eastern North America, the set of bird species whose distributions overlap and their corresponding relative abundances change, and subsequently, so does the biological structure of the bird community.

This view of community represents what ecologists refer to as a null model . It assumes that the presence and abundance of the individual species found in a given community are solely a result of the independent responses of each individual species to the prevailing abiotic environment. Interactions among species have no significant influence on community structure. Considering the examples of species interactions that we have reviewed in the chapters of Part Four, this assumption must seem somewhat odd. However, it is helpful as a framework for comparing the actual patterns observed within the community. For example, this particular null model is the basis for experiments in which the interactions between two species (competition, predation, parasitism, and mutualism) are explored by physically removing one species and examining the population response of the other (Part Four). If the population of the remaining species does not differ from that observed previously in the presence of the removed species, we can assume that the apparent interspecific interaction has no influence on the remaining species’ abundance within the community.

A great deal of evidence, however, indicates that species interactions do influence both the presence and abundance of species within communities. As we have seen in the examples presented in the chapters of Part Four, species interactions modify the fundamental niche of species involved, influencing their relative abundance, and in some cases, their distribution along environmental gradients. The resulting shifts in species’ responses as a result of interactions with other species determine their realized niche (Section 12.6). The process of interspecific competition can reduce the abundance of or even exclude some species from a community, and positive interactions such as facilitation and mutualism can enhance the presence of a species or even extend a species’ distribution beyond that defined by its fundamental niche (see this chapter, Field Studies: Sally D. Hacker). In contrast to our null model developed previously, in which our first approximation of community structure was based on the species’ fundamental niche (Figure 17.1a), as we shall see in the following sections, the biological structure of the community is an expression of the species’ realized niches (Figure 17.1b).

17.2 Zonation Is a Result of Differences in Species’ Tolerance and Interactions along Environmental Gradients

We have now seen that the biological structure of a community is first constrained by the species’ environmental tolerances—its fundamental niche. In turn, the fundamental niche is modified through interactions with other species (realized niche). Competitors and predators, for example, can restrict a species from a community; conversely, mutualists can facilitate a species’ presence and abundance within the community. As we move across the landscape, variations in the abiotic environment alter these constraints on species’ distribution and abundance. Differences in environmental tolerances among species and changes in the nature of species interactions (see Sections 12.4 and 13.9) result in shifts in the species present and their relative abundance (see Figure 17.1). These spatial changes in community structure are referred to as zonation (Section 16.8).

Field Studies Sally D. Hacker Department of Zoology, Oregon State University, Corvallis, Oregon

Salt marsh plant communities are ideal for examining the forces that structure natural communities. They are typically dominated by a small number of plant species that form distinct zonation patterns (see Figure 16.16). Seaward distribution of marsh plant species is set by harsh physical conditions such as waterlogged soils and high soil salinities, whereas terrestrial borders are generally set by competitive interactions (see Figure 13.11). Yet marsh plants also have strong ameliorating effects on these harsh physical conditions. Shading by marsh plants limits surface evaporation and the accumulation of soil salts. In addition, the transport of oxygen to the rooting zone (rhizosphere) by marsh plants can alleviate anaerobic substrate conditions. How might these modifying effects of marsh plants on the physical environment influence the structure of salt marsh communities? This question has been central to the research of ecologist Sally Hacker of Oregon State University.

To examine the role of plant–physical environment interactions on salt marsh plant zonation, Hacker focused on the terrestrial border of New England marshes. In southern New England, terrestrial marsh borders are dominated by the perennial shrub Iva frutescens (marsh elder) mixed with the rhizomatous perennial rush Juncus gerardi (black grass), which also dominates the lower marsh elevations (see Figure 17.6). The seaward border of the Iva zone is often characterized by low densities of stunted (35–50 cm) adult plants, whereas at higher elevations Iva are taller (up to 150 cm), more productive, and reach higher densities.

Previous studies suggested that Iva is relatively intolerant of high soil salinities and waterlogged soil conditions. Given the potential role of marsh plants to modify the local environment, Hacker hypothesized that the modifying effects of Juncus on soil environment function to extend the seaward distribution of Iva. To test this hypothesis, Hacker and colleague Mark Bertness of Brown University applied one of three treatments to randomly selected adult Iva shrubs on the seaward border of the Iva zone. The three treatments were designed to examine the effects of Juncus neighbors on established adult Iva: (1) all Juncus within a 0.5-m radius of each Iva plant were regularly clipped to ground level (neighbor removal, or NR), (2) all Juncus were clipped (as in NR) and then the soil was covered with a water-permeable fabric (shaded neighbor removal, or SNR), and (3) control. The use of fabric in the SNR treatment mimics the effect of Juncus shading on soil salinities without the effects of Juncus transporting oxygen to the rhizosphere (increased soil oxygen).

Soil physical conditions (soil salinity and redox [a measure of oxygen content of soils]) and Iva performance (photosynthetic rates and leaf production) were monitored in all treatments for a two-year period.

Removing Juncus plants in the neighborhood of Iva shrubs strongly affected local physical conditions (Figure 1). Removing Juncus neighbors more than doubled soil salinities in contrast to other treatments and led to more than an order-of-magnitude drop in soil redox, suggesting that the presence of Juncus neighbors increases soil oxygen levels. Because shading plots without Juncus (SNR treatment) prevented salinity increases but did not influence soil redox, the NR and SNR treatments separated the effects caused by both salt buffering and soil oxidation from those caused only by soil oxidation.

Photosynthetic rate and leaf production of Iva individuals in the treatment where Juncus neighbors were removed (NR) declined significantly in comparison to either the shaded neighbor removal (SNR) or control (C) treatments (Figure 2). Fourteen months after the experimental treatments were established, all Iva in the NR treatment were dead. These results show that soil salinity is the primary factor influencing the performance of Iva across the gradient. They also show that the presence of Juncus, with its superior ability to withstand waterlogging and salt stress, modifies physical conditions in such a manner as to create a hospitable environment for Iva, and allow this species’ distribution to extend to lower intertidal habitats.

The Iva–Juncus interaction has interesting consequences for higher trophic levels in the marsh. The most common insects living on Iva are aphids (Uroleucon ambrosiae) and their predators, ladybird beetles (Hippodamia convergens and Adalia bipunctata). Interestingly, aphids are most abundant on short, stunted Iva in the lower intertidal zone, despite having far higher growth rates on the taller Iva shrubs in the upper intertidal zone. This reduced growth rate occurs because ladybird beetles prefer tall structures, and increased predation on tall plants restricts aphids to the poorer-quality Iva plants in the lower marsh. These findings prompted the investigators to hypothesize that the Iva–Juncus interaction is critical in maintaining aphid populations in the marsh.

To explore this hypothesis, Hacker examined the abundance of aphids and ladybird beetles on the Iva individuals with (treatment C) and without (treatment NR) Juncus neighbors. To determine how the aphid population growth rates were affected by the absence of Juncus, Hacker calculated aphid population growth rates as the per capita rate of increase per day.

The overall percentage of plants with aphids and ladybird beetle predators was significantly higher for Iva plants without Juncus (NR) than for control (C) plants. This result suggests that Juncus neighbors influence stunted Iva by making the plants less noticeable to potentially colonizing aphids as well as the aphid’s predators (ladybird beetles). Although the removal of neighboring Juncus increased the proportion of Iva individuals colonized by aphids, growth rates for aphid populations (Figure 3) were lower on the stunted Iva without Juncus (NR) than for control individuals (C). Even though aphids are better at finding stunted Iva host plants when Juncus is removed, by late summer (August), population growth rates were negative on Iva individuals without neighbors—indicating that food quality of Iva host plants decreases such that aphids were unable to produce enough offspring to replace themselves.

Results of the study show that the vertical distribution of newly settled larvae of the two species overlap broadly within the intertidal zone, so dispersal was not an important factor determining the pattern of species distribution. Rather, the distribution of the two species is a function in differences in the physiological tolerance and competitive ability along the vertical environmental gradient within the intertidal zone. Balanus is limited to the lower intertidal zone because it cannot tolerate the desiccation that results from prolonged exposure to the air in the upper intertidal zone. Even when Chthamalus was removed from rock surfaces in the upper intertidal zone, Balanus did not colonize the surfaces. In contrast, Connell observed that the larvae of Chthamalus readily established on rock surfaces below where the species persists, but the colonists die out within a short period of time. To test the role of competition as a factor limiting the successful establishment of Chthamalus in the lower intertidal zones, Connell conducted a series of experiments in which he removed Balanus from half of each of the plots from the upper to the lower intertidal zone. The experiments revealed that in the lower intertidal zone Chthamalus survived at higher rates in the absence of Balanus (Figure 17.3b). Chthamalus thrived in the lower regions of the intertidal zone where it does not naturally occur, which indicated that increased time of submergence (tolerance) is not the factor limiting the distribution of the species to higher positions on the shoreline. Observations showed that the two barnacle species compete for space. Balanus has a heavier shell and a much faster growth rate, allowing individuals to smother, undercut, or crush establishing Chthamalus. In addition, crowding caused reduced size and reproduction by surviving Chthamalus individuals, further adding to the population effects of increased mortality.

Connell’s experiments clearly show that the spatial changes in species distribution—community zonation—along the intertidal gradient are a result of the trade-off between tolerance to environmental stress (dessication) and competitive ability. Balanus is limited to middle and lower intertidal zones as a function of restrictions on its physiological tolerance to desiccation (fundamental niche), whereas Chthamalus is restricted to the upper intertidal zone as a result of interspecific competition (realized niche). The asymmetry of competition between these two species leads to the competitive exclusion of Chthamalus from intertidal environments in which it is physiologically capable of flourishing (within its fundamental niche). What accounts for these differences in tolerance and competitive ability? Is there a relationship between tolerance to environmental stress and competitive ability that underlies this pattern of trade-offs that give rise to the pattern of zonation? Often superior competitive ability for resources is associated with a higher metabolic or growth rate, which often restricts (or is physiologically incompatible with) the ability to tolerate environmental stress.

Interpreting Ecological Data

1. Q1. In the hypothetical example in graph (a), under what resource conditions (availability) is the growth rate of each plant species assumed to be optimal?

2. Q2. What is the rank order of the hypothetical plant species in graph (a), moving from most to least tolerant of resource limitation?

3. Q3. If species B was removed from the hypothetical community, how would the predicted distribution of species A along the resource gradient (x-axis) in graph (b) change? How would you expect the distribution of species C to change? Why?

Our previous discussion of plant adaptations to resource availability provides some insight into the trade-off between competitive ability and tolerance to environment stress (Chapter 6) and how this trade-off influences the relative competitive abilities of plant species across environmental gradients (Chapter 13). Adaptations of plants to variations in the availability of light, water, and nutrients result in a general pattern of trade-offs between the characteristics that enable a species to survive and grow under low resource availability and those that allow for high rates of photosynthesis and growth under high resource availability (Figure 17.4a). Competitive success in plants is often linked to their growth rate and the acquisition of resources (see Chapter 13). Species that have the highest growth rate and acquire most of the resources at any given point on the resource gradient often have the competitive advantage there. The differences in adaptations to resource availability among the species in Figure 17.4a result in a competitive advantage for each species over the range of resource conditions under which they have the greatest growth rate relative to the other plant species present (see discussion of changing competitive ability along resource gradients in Section 13.9). The result is a pattern of zonation along the gradient (Figure 17.4b) that reflects the changing relative competitive abilities. The lower boundary of each species along the gradient is defined by its ability to tolerate resource limitation (survive and maintain a positive carbon balance), whereas the upper boundary is defined by competition. Such a trade-off in tolerance and competitive ability can be seen in the examples presented previously of interspecific competition and the distribution of cattail species with water depth (Figure 12.13), zonation in New England salt marshes (Figure 13.11), and in the distribution of grass species in the semi-arid regions of southeastern Arizona (Figure 13.13).

Competition among plant species rarely involves a single resource, however. The greenhouse experiments of R. H. Groves and J. D. Williams examining competition between populations of subterranean clover and skeletonweed (Figure 13.7) and the field experiments of James Cahill (see Section 13.8) clearly show that there is an interaction between competition for both aboveground (light) and belowground resources (water and nutrients). The differences in adaptations relating to the acquisition of above- and belowground resources when they are in short supply can result in changing patterns of competitive ability along gradients where these two classes of resources co-vary. Allocating carbon to the production of leaves and stems provides increased access to the resources of light but at the expense of allocating carbon to the production of roots. Likewise, allocating carbon to the production of roots increases access to water and soil nutrients but limits the production of leaves, and therefore, the future rate of carbon gain through photosynthesis. As the availability of water (or nutrients) increases along a supply gradient, the relative importance of water and light as limiting resources shift. As a result, the competitive advantage shifts from those species adapted to low availability of water (high root production) to those species that allocate carbon to leaf production and height growth but that require higher water availability to survive (Figure 17.5).

This framework of trade-offs between the set of characteristics that enable individuals of a plasnt species to survive and grow under low resource conditions as compared to the set of characteristics that would enable those same individuals to maximize growth and competitive ability under higher resource conditions is a powerful tool for understanding changes in the structure and dynamics of plant community structure along resource gradients. However, applying this simple framework of trade-offs in phenotypic characteristics can become more complicated when dealing with environmental gradients and communities in which there are interactions of resource and nonresource factors (see Section 13.6).

Interpreting Ecological Data

1. Q1. In the transition zone between the areas dominated by Spartina alterniflora and Spartina patens, which of the two species was the superior competitor (dominated) in the experimental plots under control conditions? Was the competitive outcome altered when nutrient availability was enhanced in the experimental plots (fertilized)? How so?

2. Q2. In the transition zone between the areas dominated by Spartina patens and Juncus gerardi, which of the two species was the superior competitor (dominated) in the experimental plots under control conditions? Was the competitive outcome altered when nutrient availability was enhanced in the experimental plots (fertilized)? How so?

3. Q3. What do the results of these experiments suggest about the role of nutrients in limiting the distribution of plant species along the gradient from low (sea side) to high (land side) marsh?

The complex nature of competition along an environmental gradient involving both resource and nonresource factors is nicely illustrated in the pattern of plant zonation in salt marsh communities along the coast of New England (see Figure 16.16). Nancy Emery and her colleagues at Brown University conducted a number of field experiments to identify the factors responsible for patterns of species distribution in these coastal communities, including the addition of nutrients, removal of neighboring plants, and reciprocal transplants (i.e., planting species in areas where they are not naturally found to occur along the gradient). Experiment results indicate that the patterns of zonation reflect an interaction between the relative competitive abilities of species in terms of acquiring nutrients and the ability of plant species to tolerate increasing physical stress. The low marsh is dominated by Spartina alterniflora (smooth cordgrass), which is a large perennial grass with extensive rhizomes. The upper edge of S. alterniflora is bordered by Spartina patens (saltmeadow cordgrass), which is a perennial turf grass, and is replaced at higher elevations in the marsh by Juncus gerardi (black needle rush), which is a dense turf grass (Figure 17.6). Although the low marsh experiences daily flooding by the tides, the S. patens and J. gerardi zones are inundated only during high-tide cycles (see Chapter 3). These differences in the frequency and duration of tidal inundation establish a spatial gradient of increasing salinity, waterlogging, and reduced oxygen levels across the marsh. Individuals of S. patens and J. gerardi that were transplanted to lower marsh positions exhibited stunted growth and increased mortality. Thus, the lower distribution of each species is determined by its physiological tolerance to the physical stress imposed by tidal inundation (its fundamental niche). In contrast, individuals of S. alterniflora and S. patens exhibited increased growth when transplanted to higher marsh positions where the neighboring plants had been removed. They were excluded by competition from higher marsh positions when neighboring plants were present (not removed). These results indicate that the upper distribution of each species in the marsh was limited by competition.

At first, this example would seem to be a clear case of the trade-off between adaptations for stress tolerance and competitive ability (high growth rate and resource use), as suggested in Figure 17.4 (also see competition experiments between S. alterniflora and S. patens in Figure 13.11). However, such was not the case. The experimental addition of nutrients to the marsh indeed changed the outcome of competition but not in the manner that might be predicted. The addition of nutrients completely reversed the relative competitive abilities of the species, allowing the distributions of S. alterniflora and S. patens to shift to higher marsh positions (see Figure 17.6).

J. gerardi, dominant under ambient (low) nutrient conditions, allocates more carbon to root biomass than either species of Spartina does. That renders Juncus more competitive under conditions of nutrient limitation but limits its tolerance of the higher water levels of the lower marsh. In contrast, S. alterniflora allocates a greater proportion of carbon to aboveground tissues, producing taller tillers (stems and leaves), which is an advantage in the high water levels of the lower marsh. The trade-off in allocation to belowground and aboveground tissues results in the competitive hierarchy, and thus, the patterns of zonation observed under ambient conditions. When nutrients are not limiting (nutrient addition experiments), competition for light dictates the competitive outcome among marsh plants. The greater allocation of carbon to height growth by the Spartina species increased its competitive ability in the upper marsh.

In the salt marsh plant community, a trade-off between competitive ability belowground and the ability to tolerate the physical stress associated with the low oxygen and high salinity levels of the lower marsh appears to drive zonation patterns across the salt marsh landscape. In this environment, the stress gradient does not correspond to the resource gradient as in Figure 17.4, which allows the characteristics for stress tolerance to enhance competitive ability under high resource availability.

17.3 Species Interactions Are Often Diffuse

As we have seen in the previous chapters and sections, most studies that examine the role of species interactions on community structure typically focus on the direct interaction between two, or at best, a small subset of the species found within a community. As a result, such studies most likely underestimate the importance of species interactions on the structure and dynamics of communities because interactions are often diffuse and involve a number of species (see Section 12.5).

The late ecologist Robert MacArthur of Princeton University first coined the term diffuse competition to describe the total competitive effects of a number of interspecific competitors. If the relative abundance of a species in the community is a function of competitive interactions with a single competitor (Figure 17.7a), then an experiment that removes that competitor may be able to assess the importance of competition on the focal species. However, if the relative abundance of the focal species is impacted by competition with a variety of other species in the community (Figure 17.7b), an experiment that removes only one or even a small number of those species may show little effect on the abundance of the focal species. In contrast, the removal or population reduction of the suite of competing species may result in a significant positive impact on the focal species. The work of ecologist Norma Fowler at the University of Texas provides an example. She examined competitive interactions within an old-field community by selectively removing species of plants from experimental plots and assessing the growth responses of remaining species. Her results showed that competitive interactions within the community tended to be rather weak and diffuse because removing a single species had relatively little effect. The response to removing groups of species, however, tended to be much stronger, suggesting that individual species compete with several other species for essential resources within the community.

Diffuse interactions in which one species may be influenced by interactions with many different species is not limited to competition. In the example of predator–prey cycles in Chapter 14, a variety of predator species (including the lynx, coyote, and horned owl) are responsible for periodic cycles observed in the snowshoe hare population (Section 14.14). Examples of diffuse mutualisms relating to both pollination and seed dispersal were presented previously in our discussion, where a single plant species may depend on a variety of animal species for successful reproduction (Chapter 15, Sections 15.13 and 15.14). Although food webs present only a limited view of species interactions within a community, they are an excellent means of illustrating the diffuse nature of species interactions. Charles J. Krebs of the University of British Columbia developed a generalized food web for the boreal forest communities of northwestern Canada (Figure 17.8). This food web contains the plant–snowshoe hare–carnivore system discussed previously (Chapter 14, Figure 14.24). The arrows point from prey to predator, and an arrow that circles back to the same box (species) represents cannibalism (e.g., great horned owl and lynx). Although this food web shows only the direct links between predator and prey, it also implies the potential for competition among predators for a shared prey resource, and it illustrates the diffuse nature of species interactions within this community. For example, 11 of the 12 predators present within the community prey on snowshoe hares. Any single predator species may have a limited effect on the snowshoe hare population, but the combined impact of multiple predators can regulate the snowshoe hare population. This same example illustrates the diffuse nature of competition within this community. Although the 12 predator species feed on a wide variety of prey species, snowshoe hares represent an important shared food resource for the three dominant predator species: lynx, great horned owl, and coyote.

17.4 Food Webs Illustrate Indirect Interactions

Food webs also illustrate a second important feature of species interactions within the community: indirect effects. Indirect interactions occur when one species does not interact with a second species directly but instead influences a third species that does directly interact with the second. For example, in the food web presented in Figure 17.8, lynx do not directly interact with white spruce; however, by reducing snowshoe hare and other herbivore populations that feed on white spruce, lynx’s predation can positively affect the white spruce population (survival of seedlings and saplings). The key feature of indirect interactions is that they may arise throughout the entire community because of a single direct interaction between only two component species.

By affecting the outcome of competitive interactions among prey species, predation provides another example of indirect effects within food webs. Robert Paine of the University of Washington was one of the first ecologists to demonstrate this point. The intertidal zone along the rocky coastline of the Pacific Northwest is home to a variety of mussels, barnacles, limpets, and chitons, which are all invertebrate herbivores. All of these species are preyed on by the starfish (Pisaster; Figure 17.9). Paine conducted an experiment in which he removed the starfish from some areas (experimental plots) while leaving other areas undisturbed for purposes of comparison (controls). After he removed the starfish, the number of prey species in the experimental plots dropped from 15 at the beginning of the experiment to 8. In the absence of predation, several of the mussel and barnacle species that were superior competitors excluded the other species and reduced overall diversity in the community. This type of indirect interaction is called keystone predation , in which the predator enhances one or more less competitive species by reducing the abundance of the more competitive species (see discussion of keystone species in Section 16.4).

Ecologist Robert Holt of the University of Florida first described the conditions that might promote a type of indirect interaction he referred to as apparent competition . Apparent competition occurs when two species that do not compete with each other for limited resources affect each other indirectly by being prey for the same predator (Figure 17.10). Consider the example of the red squirrel and snowshoe hare in the food web of the boreal forest presented in Figure 17.8. These two species do not interact directly and draw on different food resources. The red squirrel is primarily a granivore (feeding on seeds), and the snowshoe hare is a browser, feeding on buds, braches, and twigs of low lying woody vegetation. Both species, however, are prey for the goshawk (predatory species of hawk). An increase in the red squirrel population might result in an increase in the goshawk population (numerical response; see Section 14.6), which in turn would negatively affect the population of snowshoe hare as a result of increased predation. The decline in the population of snowshoe hare in response to the increase in population density of red squirrel, which at first might be seen as a result of competition, is in fact a result of an indirect interaction mediated by the numerical increase of a third species, their common predator the goshawk.

Apparent competition is an interesting concept that is illustrated by the structure of food webs. But does it really occur in nature? Many studies have identified community patterns that are consistent with apparent competition, and there is convincing experimental evidence of apparent competition in intertidal, freshwater, and terrestrial communities. Ecologists Christine Müller and H. C. J. (Charles) Godfray of Imperial College (Berkshire, England) conducted one such study. Müller and Godfray examined the role of apparent competition between two species of aphids that do not interact directly, yet share a common predator. The nettle aphid (Microlophium carnosum) feeds only on nettle plants (Urtica spp.), whereas the grass aphid (Rhopalosiphum padi) feeds on a variety of grass species. Although these two aphid species use different plant resources within the field community, they share a common predator: the ladybug beetle (Coccinellidae). In their study, the researchers placed potted nettle plants containing colonies of nettle aphids in plots of grass within the field community that contained natural populations of grass aphids (Figure 17.11). On a subset of the grass plots, they applied fertilizer that led to rapid grass growth and an increase in the local population of grass aphids. Nettle aphid colonies adjacent to the fertilized plots suffered a subsequent decline in population density when compared to colonies that were adjacent to unfertilized plots (control plots with low grass aphid populations). The reduced population of nettle aphids in the vicinity of high population densities of grass aphids (fertilized plots) was the result of increased predation by ladybug beetles, attracted to the area by the high concentrations of grass aphids; it was not as a result of direct resource competition between the two aphid species.

Some indirect interactions have negative consequences for the affected species, as in the preceding case of apparent competition. In other cases, however, indirect interactions between species can be positive. An example comes from a study of subalpine ponds in Colorado by Stanley Dodson of the University of Wisconsin. It involves the relationships between two herbivorous species of Daphnia and their predators, a midge larva (Chaoborus) and a larval salamander (Ambystoma). The salamander larvae prey on the larger of the two Daphnia species, whereas the midge larvae prey on the small species (Figure 17.12). In a study of 24 pond communities in the mountains of Colorado, Dodson found that where salamander larvae were present, the number of large Daphnia was low and the number of small Daphnia, high. However, in ponds where salamander larvae were absent, small Daphnia were absent and midges could not survive. The two species of Daphnia apparently compete for the same resources. When the salamander larvae are not present, the larger of the two Daphnia species can outcompete the smaller. With the salamander larvae present, however, predation reduces the population growth rate of the larger Daphnia, allowing the two species to coexist. In this example, two indirect positive interactions arise. The salamander larvae indirectly benefit the smaller species of Daphnia by reducing the population size of its competitor. Subsequently, the midge apparently depends on the presence of salamander larvae for its survival in the pond. The indirect interaction between the midge and the larval salamander is referred to as indirect commensalism because the interaction is beneficial to the midge but neutral to the larval salamander. When the indirect interaction is beneficial to both species, the indirect interaction is termed indirect mutualism .

This role of indirect interactions can be demonstrated only in controlled experiments involving manipulations of the species populations involved. The importance of indirect interactions remains highly speculative, but experiments such as those just presented strongly suggest that indirect interactions among species—both positive and negative—can be an integrating force in structuring natural communities. There is a growing appreciation within ecology for the role of indirect effects in shaping community structure, and understanding these complex interactions is more than an academic exercise; it has direct implications for conservation and management of natural communities.

As with the example of starfish in the intertidal zone, removing a species from the community can have many unforeseen consequences. For example, Joel Berger of the University of Nevada and colleagues have examined how the local extinctions of grizzly bears (Ursus arctos) and wolves (Canis lupus) from the southern Greater Yellowstone ecosystem, resulting from decades of active predator control, have affected the larger ecological community (see Chapters 17, Ecological Issues & Applications). One unforeseen consequence of losing these large predators is the decline of bird populations that use the vegetation along rivers (riverine habitat) within the region. The elimination of large predators from the community resulted in an increase in the moose population (prey species). Moose selectively feed on willow (Salix spp.) and other woody species that flourish along the river shorelines. The increase in moose populations dramatically affected the vegetation in riverine areas that provide habitat for a wide variety of bird species and led to the local extinction of some populations.

17.5 Food Webs Suggest Controls of Community Structure

The wealth of experimental evidence illustrates the importance of both direct and indirect interactions on community structure. On that basis, rejecting the null model as presented in Section 17.1 would be justified. However, given the complexity of direct and indirect interactions suggested by food webs, how can we begin to understand which interactions are important in controlling community structure and which are not? Are all species interactions important? Does some smaller subset of interactions exert a dominant effect, whereas most have little impact beyond those species directly involved (see discussion of food web compartmentalization in Section 16.5)? The hypothesis that all species interactions are important in maintaining community structure suggests that the community is like a house of cards—that is, removing any one species may have a cascading effect on all others. The hypothesis that only a smaller subset of species interactions control community structure suggests a more loosely connected assemblage of species.

These questions are at the forefront of conservation ecology because of the dramatic decline in biological diversity that is a result of human activity (see Chapters 9 and 12, Ecological Issues & Applications). Certain species within the community can exert a dominant influence on its structure, such as the predatory starfish that inhabits the rocky intertidal communities. However, the relative importance of most species in the functioning of communities is largely a mystery. One approach being used to understand the influence of species diversity on the structure and dynamics of communities is grouping species into functional categories based on criteria relating to their function within the community. For example, the concept of guilds is a functional grouping of species based on sharing similar functions within the community or exploiting the same resource (e.g., grazing herbivores, pollinators, cavity-nesting birds; see Section 16.6). By aggregating species into a smaller number of functional groups, researchers can explore the processes controlling community structure in more general terms. For example, what is the role of mammalian predators in boreal forest communities? This functional grouping of species can be seen in the food web presented in Figure 17.8, in which the categories (boxes) of forbs, grasses, small rodents, insects, and passerine birds represent groups of functionally similar species.

One way to simplify food webs is to aggregate species into trophic levels (Section 16.5). The food web presented in Figure 17.8 has been aggregated into three trophic levels: primary producers, herbivores, and carnivores (Figure 17.13). Although this is an obvious oversimplification, using this approach raises some fundamental questions concerning the processes that control community structure.

As with food webs, the arrows in a simple food chain based on trophic levels point in the direction of energy flow—from autotrophs to herbivores and from herbivores to carnivores. The structure of food chains suggests that the productivity and abundance of populations at any given trophic level are controlled (limited) by the productivity and abundance of populations in the trophic level below them. This phenomenon is called bottom-up control . Plant population densities control the abundance of herbivore populations, which in turn control the densities of carnivore populations in the next trophic level. However, as we have seen from the previous discussion of predation and food webs, top-down control also occurs when predator populations control the abundance of prey species.

Work by Mary Power and her colleagues at the University of Oklahoma Biological Station suggests that the role of top predators (carnivores) on community structure can extend to lower trophic levels, influencing primary producers (autotrophs) as well as herbivore populations. Power and colleagues showed that a top predator, the largemouth bass (Micropterus salmoides), had strong indirect effects that cascaded through the food web to influence the abundance of benthic algae in stream communities of the midwestern United States. In these stream communities, herbaceous minnows (primarily Campostoma anomalum) graze on algae, and in turn, largemouth bass feed on the minnows. During periods of low flow, isolated pools form in the streams. As part of the experiment, bass were removed from some pools and the populations of algae and minnows were monitored. Pools with bass had low minnow populations and a luxuriant growth of algae (Figure 17.14). In contrast, pools from which the bass were removed had high minnow populations and low populations (biomass) of algae. In this example, top predators (carnivores) were shown to control the abundance of plant populations (primary producers) indirectly through their direct control on herbivores (also see Chapter 20, Field Studies: Brian Silliman). This type of top-down control is referred to as a trophic cascade . A trophic cascade occurs when a predator in a food web suppresses the abundance of their prey (intermediate species) such that it increases the abundance of the next lower trophic level (basal species) on which the intermediate species feeds (Figure 17.15).

A now-famous article written by Nelson Hairston, Fred Smith, and Larry Slobodkin first introduced the concept of top-down control with the frequently quoted “the world is green” proposition. These three ecologists proposed that the world is green (plant biomass accumulates) because predators keep herbivore populations in check. Although this proposition is supported by a growing body of experimental studies such as those by Power and her colleagues, experimental data required to test this hypothesis are still limited, particularly in terrestrial ecosystems. However, the proposition continues to cause great debate within the field of community ecology. We will return to the topic when discussing factors that control primary productivity (Chapter 20).