Allee dynamics generated by protection mutualisms can drive oscillations in trophic cascades
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Understanding the relative effect of top predators and primary producers on intermediate trophic levels is a key question in ecology. Most previous work, however, has not considered either realistic nonlinearities in feedback between trophic levels or the effect of mutualists on trophic cascades. Here, we develop a realistic model for a protection mutualism that explicitly includes interactions between a protected herbivore and both its food plant and generalist predators. In the absence of protection, herbivores and plant resources approach a stable equilibrium, provided that predation is not so high as to cause herbivore extinction. In contrast, adding protection by mutualists increases the range of dynamical outcomes to include unstable equilibria, stable and unstable limit cycles, and heteroclinic orbits. By reducing the impact of predators, protection by mutualists can allow herbivores to exert strong negative effects on their host plants, which in turn can lead to repeated cycles of overexploitation and recovery. Our results indicate that it may be essential to consider protection mutualisms to understand the dynamics of trophic cascades. Conversely, it may be essential to explicitly include dynamical feedback between plants and herbivores to fully understand the population and community dynamical consequences of protection mutualism.
KeywordsHopf bifurcation Host-plant quality Limit cycle Protection mutualism Trophic cascade
Since its introduction, Hairston, Smith and Slobodkin’s (Hairston et al. 1960) hypothesis of top–down trophic regulation (HSS) has played a key role in extending models of pairwise species interactions to a community context. HSS is based on the assumption of alternating predator and food limitation for sequentially lower trophic levels. From this assumption, HSS predicts a positive effect of top predators on primary producers in communities with three trophic levels but a negative effect of top predators on primary producers for communities with four trophic levels (Fretwell 1977).
More recently, theoretical models and empirical studies have refined HSS to include greater realism by evaluating the effect of predator diversity on the magnitude of top–down control (Finke and Denno 2004; McCann et al. 1998) and by considering the effect of omnivory (feeding between nonadjacent trophic levels) on community dynamics (Diehl and Feißel 2000). Overall, there has been a shift away from categorizing communities as controlled by either bottom–up or top–down forces and toward evaluating variability in the relative effect of predator or resource limitation on community dynamics (Hunter and Price 1992).
Despite these advances, significant gaps remain in our understanding of trophic cascades. For example, although there has been a call to develop a community perspective on mutualism (Stanton 2003), few studies have addressed the effect of mutualism on the dynamics of trophic cascades. Empirical studies that have considered the effect of plant and herbivore mutualists on trophic cascades (Knight et al. 2006; Styrsky and Eubanks 2007) suggest that mutualism can be an important, albeit understudied, component of trophic dynamics. We are unaware, however, of any theoretical studies that have considered the effect of mutualism on the interactions between higher- and lower-level consumers—e.g., the inhibition of top predators caused by protection mutualists.
In protection mutualisms, a protector species benefits a host species by removal of the host’s natural enemies in return for a resource reward (Bronstein and Barbosa 2002). Protection mutualisms are geographically and taxonomically diverse, and include interactions between cleaner species (fish or arthropods) and their hosts, between ants and plants that produce extrafloral nectar or other food rewards for the ants, and between ants and herbivores. Protection mutualisms are common adjuncts of trophic cascades (Halaj and Wise 2001; Schmitz et al. 2004), perhaps because protection mutualists can generate simplified local communities (Risch and Carroll 1982; Wimp and Whitham 2001) in which trophic cascades are predicted to be more likely (Hunter and Price 1992).
According to HSS, predators may prevent consumers from greatly depressing their resources. By reducing predation on bottom consumers, protection may facilitate resource overexploitation, raising the possibility that protection mutualism may lead to cyclic dynamics in which a period of consumer population growth and resource overexploitation is followed by a period of consumer decline and resource recovery, which can then initiate a new cycle, and so on. Although most previous studies have focused on the effect of the number of trophic levels on equilibrium densities (e.g., Power 1992), feedback between trophic levels can also generate nonequilibrial dynamics (Hastings and Powell 1991).
Given the potential importance of mutualism in trophic dynamics and the intrinsically trophic nature of protection mutualism, we develop a model to evaluate how protection mutualism influences the dynamics of multi-trophic-level interactions. Our model incorporates generalist top predators and protectors, immigration of the top predator and protector to a bottom consumer (e.g., a herbivore) with emigration in proportion to its density, and feedback from the bottom consumer to the basal resource (e.g., a plant). We assume that protectors and predators respond to herbivores on a behavioral time scale and that their densities rapidly equilibrate to the current herbivore density. To assess the role of protection mutualism for dynamics of consumer populations, we compare the range of dynamical possibilities in a simple food-chain model with and without protectors. In the Discussion, we place our results in the context of past theoretical work on trophic cascades, on the impact of mutualism on community stability, and on the likelihood of herbivore fluctuations driven by feedback to host-plant quality.
A trophic cascade model with protection mutualism
Ant-tended herbivores are insects (e.g., aphids and caterpillars) that excrete or secrete sugar rewards in return for protection from predators (Buckley 1987; Cushman and Whitham 1989; Morales 2000b; Pierce and Easteal 1986). Often the rewards are metabolic byproducts that involve little or no cost to produce. The ant species that tend herbivores and the predators of those herbivores are typically generalists, even in cases where the ant-tended herbivores are obligately dependent on ant protection (Buckley 1987; Devries 1991; Way 1963). Ant-protected herbivores are usually tended in aggregations and are characterized by limited mobility and ant-dependent host–plant selection (Axén and Pierce 1998; Dyck et al. 2000; Morales 2002). As a consequence, an ant-tended herbivore aggregation is largely restricted to a single plant chosen by a foundress. For a given plant or small patch of plants, the processes controlling local ant and predator densities are largely behavioral and thus operate on a faster time scale than the dynamics of herbivore density (Morales 2000a, b) or host-plant quantity or quality.
Given the typically limited mobility of ant-tended herbivores, we model the dynamics of birth and death of herbivores on a single plant, but we assume that generalist ant and predator populations on the plant are open, with immigration and emigration dependent on behavioral processes that are, in part, a response to the local herbivore density. We assume that regional ant and predator densities are largely determined by resources other than those provided by the local herbivore population (as is reasonable for highly generalist species). We also assume that the protection mutualism is strictly indirect: mutualists benefit herbivores solely via their effect on local predator density and neither consume herbivores nor benefit them in any other way (e.g., by increasing feeding rates). Finally, feeding by the local herbivore population influences the size or the nutritional quality of the single plant on which it is located.
In the absence of herbivores, I M mutualists immigrate to the plant per unit time, and the per-capita emigration rate is δ M . The equilibrium density of mutualists in the absence of herbivores is therefore I M /δ M . The link to the other populations is provided by a saturating increase in mutualist recruitment in response to herbivores, with a maximum increase of α/β at high herbivore density and half saturation when H = 1/β. Saturating mutualist recruitment assumes that the availability of mutualists is limited (Breton and Addicott 1992; Cushman and Addicott 1989; Cushman and Whitham 1991; Morales 2000a,b) and produces the realistic result that run-away population growth driven by the mutualism cannot occur (cf. May 1978; Vandermeer and Boucher 1978; Wolin and Lawlor 1984). In the absence of herbivores and their mutualists, predators arrive at and leave host plants in a manner similar to mutualists but at rates controlled by I P and δ P , respectively. The predator population is coupled to the food web in two different ways. First, the predator’s emigration rate declines to zero (at a rate scaled by φ) as the density of its prey, the herbivores, increases. Second, mutualists protecting herbivores increase the predator’s rate of emigration from the plant, at a rate scaled by γ. Therefore, the magnitude of benefit to herbivores is proportional to γ. Herbivores suffer mortality in proportion to predators at a per-capita rate ɛ. Equation 1d could represent logistic growth of plant biomass with type I consumption by herbivores, or herbivore-induced changes in plant quality (Morris and Dwyer 1997). In either case, Q is scaled so that its maximum is 1. In the absence of herbivores, Q increases at a rate determined by r Q . Q declines with increasing herbivore density at a rate governed by η. If Q = 1, herbivores are born at a per-capita rate r H , but herbivore birth declines linearly as Q declines.
(where we have dropped primes for clarity).
Community dynamics in the absence of mutualism and with rapidly equilibrating predators
The effect of protection mutualists on community dynamics
The resulting model is highly nonlinear, reducing the utility of standard linear stability analysis, so instead, we used bifurcation diagrams and numerical solutions to assess the existence and stability properties of the equilibria, as well as the dynamics away from equilibria (Ermentrout 2002).
Protection mutualists increase the range of dynamical possibilities beyond those predicted by the mutualist-free model. For some parameter combinations, we see an unstable, low-density herbivore equilibrium, as is often seen in models of obligate mutualism (e.g., May 1978; Vandermeer and Boucher 1978; Wolin 1985; Morris et al. 2003). We also observe equilibria undergoing subcritical and supercritical Hopf bifurcations (Kuznetsov 1995) and the existence of unstable and stable limit cycles. That is, unlike the model without protection mutualism (Eq. 3), the model with implicit mutualists (Eq. 4) can produce sustained oscillations in herbivores and plants (Fig. 2).
The destabilizing effect of protectors is caused by an Allee effect in the herbivores—specifically, an initial decrease in the herbivore’s per-capita death rate with increasing herbivore density. This Allee effect means that herbivores will recover relatively slowly when depressed to low density, thus introducing a lag that allows Q to increase before herbivores recover, which then allows herbivores to overexploit Q and then decline to low levels, reinitiating the cycle.
δ P , δ M , I P , I M
Set immigration and emigration rates of mutualists and predators equal. Set parameter value at 1 to facilitate the interpretation of nondimensionalized parameter groupings
Herbivore growth rates are large relative to the arrival and leaving rates of mutualists and predators in the absence of herbivores
Set predation rate at 1 to facilitate the interpretation of nondimensionalized parameter groupings
Plant-quality recovers relatively slowly
Set the carrying capacity (r Q /η) of herbivores in the absence of either predators or mutualists to 1
Recruitment increases strongly with herbivore density, and the half-saturation point (1/β = 1) is high (Morales 2000a) relative to the carrying capacity of herbivores in the absence of predators or mutualists
Predator density responds much more strongly to mutualist density than to herbivore density (Morales, unpublished data)
In the zone with a single, unstable equilibrium, changing the negative effect of herbivores on host plants (h) so that it is sufficiently lower or higher than its default value stabilizes the system [Fig. 5b, which shows a subcritical Hopf bifurcation at h ≈ 0.6 and a supercritical Hopf bifurcation (i.e., the stable equilibrium and the stable limit cycle emanating from it exist on opposite sides of the bifurcation point) at h ≈ 4]. Low values of h are stabilizing because feedback from herbivores to plants is weak, and hence, herbivore density is controlled by predation, whereas high values of h are stabilizing because Q can never attain sufficiently high levels to allow herbivores to experience high population growth rates. In contrast, decreasing R Q (the recovery rate of Q) destabilizes the system by increasing the lag period before herbivores can again increase (Fig. 5c). Interestingly, increasing g (the positive effect of mutualists on herbivores mediated through predator removal) is destabilizing (Fig. 5d). Cyclical dynamics are also associated with high values of the maximum mutualist recruitment rate (α, Fig. 5e) and low values of the mutualist departure rate (d M , Fig. 5f), which indicates that increasing the potential range of the protection benefit is destabilizing. Finally, cycles are observed for high values of m P (Fig. 5g) and low values of k (Fig. 5h), two parameters that control predation intensity. Because m P controls herbivore-independent predator arrival, predator density declines at low m P , such that mutualists provide little benefit and the system resembles the stable, mutualist-free model (Eq. 3). In contrast, k controls the herbivore-dependent recruitment of predators. If k is large, predators increase quickly as herbivore density increases so that herbivore density can never get large enough to depress Q and drive cycles.
Our results show that adding a protection mutualist to a trophic cascade can produce community oscillations when three-way equilibria in the absence of the mutualism would be strictly stable. Therefore, sustained fluctuations of a consumer population driven by a dynamical interaction with its resource may be facilitated when the consumer is engaged in a protection mutualism with generalist protectors and preyed upon by mobile, generalist predators. This scenario describes well the mutualism between insect herbivores and their defenders, but it may also capture some essential features of other protection mutualisms. In the following paragraphs, we discuss our results in the light of previous theoretical studies of trophic cascades, of mutualism, and of herbivore population dynamics, and we outline several caveats that apply to our analysis.
Although the focus of trophic cascade theory has been on the factors that determine population density at equilibrium, results presented here and previous studies suggest that the dynamical properties of trophic communities may be equally important. For example, strong feedback between trophic levels can generate chaotic dynamics in a simple food-chain model (Hastings and Powell 1991). Implicit spatial dynamics of resources and consumers has also been shown to destabilize trophic communities (Nisbet et al. 1997). Here we add another factor, protection mutualism, that may destabilize trophic dynamics by introducing an Allee effect into predator-driven herbivore death rates.
The question of whether mutualism stabilizes or destabilizes communities has a checkered past, with some theoretical studies favoring each answer. Several overlapping factors have contributed to the divergent results. One is the use by different researchers of different definitions of “stability,” including the absence of explosive population growth (Gause and Witt 1935; May 1976; Heithaus et al. 1980; Kooi et al. 2004), avoidance of extinction (Ringel et al. 1996), qualitative local stability of equilibria (May 1974), and a rapid rate of return to a stable equilibrium following a small perturbation (Addicott 1981; Wolin and Lawlor 1984; Ringel et al. 1996). A second factor is whether models assume (unrealistically) that benefits increase indefinitely as the density of a mutualistic partner increases (Gause and Witt 1935; May 1976; Heithaus et al. 1980; Addicott 1981; Ringel et al. 1996) or whether more realistic saturating benefits are assumed (May 1978; Vandermeer and Boucher 1978; Dean 1983; Wolin and Lawlor 1984; Armstrong 1987; Wright 1989; Holland and DeAngelis 2001; Morris et al. 2003; Kooi et al. 2004). Yet a third factor is whether a model includes two or more species. Given this diversity of approaches, it is not surprising that no consensus has emerged. Indeed, rather than asking whether mutualism stabilizes or destabilizes communities in general, a far more relevant question is how specific types of mutualism may alter the dynamics of multispecies communities, as portrayed by tailored models that capture essential features of those mutualisms (cf. Kooi et al. 2004). In attempting to model the community centered on herbivores with protective mutualists, we have used realistic saturating benefits, have incorporated the interactive effects of three other species (including the fact that mutualists benefit herbivores indirectly through their effects on local predator density), and have allowed for differences in the time scales at which different processes in this community operate. Using this tailored model, we have shown that elevating the protection benefit that herbivores receive from mutualists can cause the community to undergo a transition from stability to sustained oscillations. We have also partially explored how other biological factors, such as the herbivores’ birth rates, rates of decline and host-plant recovery, and mutualist and predator immigration and emigration rates, influence whether the systems with protection mutualism will be stable or oscillatory (Fig. 5). Estimating these parameters for real protection mutualisms and censusing the herbivore population over time would allow the predictive power of the model to be assessed.
In building a trophic model for protection mutualisms, we have also linked two areas of theoretical investigation that have largely developed in isolation from one another: mutualism models and models of herbivore population dynamics driven by induced changes in host-plant quality. The simplest host-plant quality models do not produce persistent herbivore fluctuations. For example, Edelstein-Keshet and Rausher (1989) found that continuous time models similar to Eqs. 2c and 2d are stable. Indeed, it is easy to show that Eqs. 2c and 2d with P fixed, which is equivalent to a predator–prey model with logistically growing prey and a type I functional response, is strictly stable. More complex models that incorporate quality-dependent and aggregative movement of herbivores (Lewis 1994) or time lags in the decline or recovery of plant quality following herbivory (Turchin 2003; Underwood 1999) can produce sustained oscillations. By explicitly including interactions with predators and mutualists, our model adds another factor (protection mutualism) that may increase the likelihood that plant quality feedback will drive persistent herbivore fluctuations. Specifically, the increased potential for local herbivore populations to grow under the protective umbrella provided by their mutualists may have the detrimental effect of allowing them to overexploit their host plants (e.g., by imposing nutritional stress or by inducing plant defenses), leading to herbivore decline followed by plant recovery and, eventually, a reinitiation of the cycle. Somewhat paradoxically, this sometimes leads to the situation in which the herbivore is both obligately dependent on its mutualist (as indicated by the existence of a lower, unstable equilibrium) and susceptible to extinction driven by high-amplitude oscillations made possible by the mutualist (Fig. 6b).
As in any modeling analysis, our conclusions may depend on the model assumptions. We assume that predation on herbivores is primarily via generalist predators and that mutualists act as generalists in their interactions with herbivores. We formulated the increase of predators and mutualists to herbivores as a behavioral “aggregation response” with no numerical feedback on mutualist or predator population densities, arguing that this formulation applies for many protection mutualisms (cf. Buckley 1987; Hölldobler and Wilson 1990; Stadler and Dixon 2005). This approach is typical of the distinction between generalist and specialist predators in predator–prey-based consumer-resource models (Gilg et al. 2003; Turchin and Hanski 1997). That being said, few studies have explicitly tested the degree of benefit received by mutualists in protection mutualisms (Beattie 1991; Cushman and Beattie 1991), although a few studies of ant-protection mutualism suggest the potential for feedback dynamics, especially on densities of the worker population (Cushman et al. 1994; Cushman and Beattie 1991). Further analyses exploring the effect of adding numerical dynamics of the protector or mutualist, or of making consumption of resource by the herbivore a type II function, are warranted.
To simplify our analysis, we have not included a cost to herbivores from interacting with their protectors (Stadler and Dixon 1999) or a positive indirect effect of protectors on plants mediated by the removal of nonmutualist herbivores (reviewed in Styrsky and Eubanks 2007). Our assumptions are consistent with a number of ant-protection mutualisms (Flatt and Weisser 2000; Morales 2000b; Morales and Beal 2006; Stadler and Dixon 1999; Styrsky and Eubanks 2007), and we emphasize that relaxing these assumptions is not likely to change the conclusions reached here. For example, our results suggest that even if protectors increase plant quantity or quality over the short term by removing nonmutualist herbivores, herbivore population growth in response to elevated plant resource (in addition to protection from predators) over the longer term may cause plants, and then herbivores, to decline. In a preliminary analysis of a modification of Eq. 4 with an indirect positive effect of mutualists on plant quantity/quality, we have found that long-term oscillations are still possible (results not shown).
We conclude that mutualism can magnify the top–down effect of one partner on lower trophic levels and that this effect can engender oscillatory dynamics. The effect of herbivory on the subsequent performance of herbivores has been established for herbivore populations in general (Brown and Weis 1995; Root 1996; Uriarte 2000; Awmack and Leather 2002), and our results suggest that this effect is likely to be especially pronounced for herbivores that also engage in mutualisms. While the focus of protection mutualisms has understandably been on higher (i.e., predator) trophic levels, focusing on the effect of lower trophic levels will be an important new direction for future studies.
The authors thank A. de Roos for helpful comments on an earlier draft. This work was supported by sabbatical funding from Williams College to MAM and by NSF Grant DEB-0087096 to WFM.
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