vol. 174, no.

the american naturalist

september 2009

Determining the Functional Form of Density Dependence: Deductive Approaches for Consumer-Resource Systems Having a Single Resource
Peter A. Abrams*
Department of Ecology and Evolutionary Biology, University of Toronto, 25 Harbord Street, Toronto, Ontario M5S 3G5, Canada Submitted September 24, 2008; Accepted April 10, 2009; Electronically published July 23, 2009 Online enhancement: appendix.

abstract: Consumer-resource models are used to deduce the functional form of density dependence in the consumer population. A general approach to determining the form of consumer density dependence is proposed; this involves determining the equilibrium (or average) population size for a series of different harvest rates. The relationship between a consumers mortality and its equilibrium population size is explored for several one-consumer/one-resource models. The shape of density dependence in the resource and the shape of the numerical and functional responses all tend to be inherited by the consumers density dependence. Consumer-resource models suggest that density dependence will very often have both concave and convex segments, something that is impossible under the commonly used v-logistic model. A range of consumer-resource models predicts that consumer population size often declines at a decelerating rate with mortality at low mortality rates, is insensitive to or increases with mortality over a wide range of intermediate mortalities, and declines at a rapidly accelerating rate with increased mortality when mortality is high. This has important implications for management and conservation of natural populations. Keywords: consumer-resource interaction, density dependence, functional response, numerical response, theta-logistic model.

Introduction As the population density of an organism increases, it must at some point suffer a decrease in its per capita population growth rate. This negative feedback is the essence of density dependence, a concept central to much of population and community ecology. There are many types, causes, and denitions of density dependence. This article will be largely conned to density dependence driven by depletion of consumable, renewing resources (the most likely cause according to Begon et al. [2006]). I will therefore ignore positive density dependence (Allee effects) and density de* E-mail: peter.abrams@utoronto.ca. Am. Nat. 2009. Vol. 174, pp. 321330. 2009 by The University of Chicago. 0003-0147/2009/17403-50760$15.00. All rights reserved. DOI: 10.1086/603627

pendence due to aggressive interactions and nonconsumed resources such as nesting sites or space. It is impossible to cover all aspects of density dependence, and consumptive competition for resources is the mechanism that leads most readily to general theory. Most of the literature on interspecic density dependence (i.e., competition) is based on effects that arise via resource depletion, and eld experiments show this is the most common mechanism of interspecic competition (Schoener 1983). A large body of theory based on consumer-resource models has been developed to describe consumptive interspecic competition (e.g., MacArthur 1970, 1972; Schoener 1974, 1976, 1986; Abrams 1975, 1977, 1980, 1998; Abrams et al. 2008). Purely intraspecic competition (density dependence) must frequently involve the same consumptive mechanisms, but surprisingly few consumer-resource models of density dependence exist, and they have examined very specic models (Schoener 1973; Royama 1992; Johst et al. 2008). Most models of density dependence do not explicitly represent resources. Demographic rates are expressed directly as a function of consumer population density. The v-logistic model of Gilpin and Ayala (1973) is by far the most commonly used model; here per capita growth rate is expressed as a power function of population size. The dynamics of a population of size N is described by

dN p rN 1 dt

[ ( )]
v

N . K

(1)

The parameter K is the equilibrium density, r is the maximum per capita growth (realized at very low population size), and v is a positive exponent that determines the shape of density dependence. If v p 1, population growth is logistic. A value of v much larger than 1 implies that there is little density-dependent reduction in the per capita

322 The American Naturalist growth rate until N is close to K; v values much !1 imply that the most rapid reduction in per capita growth with increasing N occurs at low densities. This article asks whether equation (1) is exible enough to represent most forms of density dependence that arise from resource depletion and, if so, whether the range of likely values for the exponent can be predicted from knowledge about the consumer-resource interaction. The analysis has implications that are broader than the adequacy of equation (1), since it argues that, for many systems, no differential equation model in which per capita growth rate is a monotonically decreasing function of population size is adequate. The analysis determines what aspects of the consumer-resource interaction are likely to rule out the traditional form. The work was motivated by the need to develop a deductive approach to assessing the form of density dependence. Direct measurements of growth while holding population size constant are impractical and are not employed in studies of density dependence. Time series analysis (e.g., Sther et al. 2002; Sibly et al. 2005) cannot adequately account for the continuously distributed delayed effects caused by resource depletion and often have a variety of other problems (e.g., Doncaster 2006, 2008; Getz and Lloyd-Smith 2006; Ross 2006). Time lags due to resource competition and life-history delays can interact in surprisingly complex ways (McCauley et al. 2008), and only the latter has been incorporated into a time series analysis that analyzed density dependence (Coulson et al. 2008). A potential alternative empirical approach for quantifying density dependence is to apply a series of different harvest rates to otherwise identical experimental populations and to record the resulting population density at equilibrium (or the long-term mean density). Because the harvest must equal population growth, this approach simply reverses the axes of the relationship between per capita population size and per capita growth rate. This approach avoids the problem of time lags and can generate meaningful results for cycling populations. It has been applied to determine how population size varies with different exploitation strategies in protist systems in the laboratory (Fryxell et al. 2005). However, that study had too few treatments to determine the shape of density dependence. The harvesting method cannot be applied to most natural systems because of the lack of replicate populations and the large effort required. This makes developing a deductive approach even more important. The deductive approach also contributes to food web theory by providing guidelines for when one can adequately approximate consumer dynamics without explicitly representing the resources that control its population growth. The remainder of this work investigates density dependence that arises from dynamic models of a single consumer and a single resource population. Systems with multiple resources are treated in another article (Abrams 2009a). The shape of density dependence is illustrated by plotting population size versus per capita harvest rate because, as noted above, this is the one experimental approach that avoids the artifacts of controlling consumer density and accounts fully for time-lagged effects. Consumer-Resource Models of Density Dependence General Considerations The interaction between consumers, with population size N, and resources, with population size R, is represented by the following differential equations: dR p Rf(R) dt CRg(R, N )N, dN. (2a) (2b)

dN p Nb(CRg(R, N )) dt

Here f is the per capita growth rate of the resource. The term CRg is the consumers functional response to the resource; this consists of a mass action term, CR, multiplied by a foraging intensity function, g, which reects all processes that modify the mass action term. These include satiation, handling time, adaptive foraging, and plastic resource defensives. Abrams (1990) presents several alternatives to the disk equation that may be described using the foraging intensity multiplier. The function b is the consumers per capita birth rate as a function of resource intake rate. This function will be referred to as the numerical response. The nal parameter, d, is the consumers death rate, which is the sum of a minimum natural mortality, d0, and any additional mortality (e.g., harvest), denoted dh. MacArthur (1970, 1972) pioneered the use of models like equations (2) to study competition. He showed that logistic resource growth (f(R) p r[1 (R/K )]) together with linear functional (g p 1) and numerical responses of the consumer made growth of the consumer effectively logistic; the equilibrium N (Neq) decreases linearly with d in this case. I use this work as a baseline case for examining the impacts of different forms for the three functions in equations (3). The three functions that may inuence the shape of density dependence in the consumer species in equations (2) are the resource growth function, the consumers functional response, and the consumers numerical response. The appendix in the online edition of the American Naturalist presents a general analysis that derives expressions for the rst and second derivatives (slope and curvature) of the relationship between equilibrium consumer density

Density Dependence 323 and mortality rate. The impact of each of the models component functions on the slope and curvature of this relationship is discussed below. Resource Growth The rst factor that inuences resource-based density dependence is the nature of the resource growth function. Assuming linear functional and numerical responses means that the amount of resource eaten per unit time by an average consumer is CR (i.e., g p 1), and the function b in equation (2b) is BCR, where B is a conversion efciency constant. If equations (2) are solved under these assumptions, N p f/C, where f is evaluated at R p d/(BC). This leads to the following expressions for the rst two partial derivatives of Neq with respect to d: Neq 1 p f d BC 2
2

shapes. For Hollings (1959) disk equation, g(R) is 1/(1 ChR). More generally, a Type II response increases at a decreasing rate as resource density increases; this implies that g p dg/dR ! 0, g Rg 1 0, and 2g Rg ! 0. The appendix derives the general expression for how the equilibrium consumer population size changes with its per capita mortality rate: Neq gf fg p . 2 2 d b C g (g Rg ) (5)

F F

(3a)

Rpd/(BC)

Neq 1 p 2 3f 2 d BC

(3b)

Given the conditions on g mentioned above, equation (5) must be negative when g f fg ! 0 at equilibrium, which in turn is required for stability of the equilibrium point. However, equation (5) implies an increase in the equilibrium density with increasing mortality in unstable systems, a phenomenon implicit in Rosenzweig and MacArthurs (1963) analysis of predator-prey dynamics and discussed in greater detail by Abrams (2002, 2009b), Matsuda and Abrams (2004), and Abrams and Matsuda (2005). The second derivative of Neq with respect to d is given by a rather complicated formula (see appendix):
2

Rpd/(BC)

where d/(BC) is the equilibrium resource density and the primes denote derivatives with respect to the argument of the function. Equation (3a) means that Neq decreases with d (because f ! 0), while equation (3b) implies that the curvature of the relationship between N and d must be the same as that between f (the resource per capita growth rate) and R. For example, if f is the v-logistic formula from equation (1), the resulting equilibrium consumer population size is

Neq p d2 g (f Rf )] .

2g (g R

2g)(g f

f g) g 2[f (g Rg ) B 2C 3g 3(g Rg )3

(6) In the case considered here, logistic growth implies that f p 0, so there is a slight simplication of the numerator of equation (6). Many of the component quantities in equation (6) have known signs, and the appendix shows that expression (6) must always be negative (Neq declines at an accelerating rate with d) when the functional response has a Holling (1959) Type II shape, resource growth is logistic, and the system is stable. If the system is unstable, the curvature is indeterminate, although, in this case, expression (6) must be positive when R is sufciently small. This means that Neq increases at an accelerating rate when d is small and the system is unstable. For any type of saturating functional response, equation (6) implies that there will be an accelerating decline in Neq with d at large values of d. Numerical results assuming logistic resource growth and a Holling Type II functional response are shown in gure 1 of Abrams (2002); here Neq in an unstable system increases at an accelerating rate at low mortality, which shifts to a decelerating increase before Neq peaks at the mortality that is just sufcient to stabilize the system. At higher mortality, Neq undergoes a steep accel-

1 Neq p r C

( )]
v

dr . BCK

(4)

As predicted by equation (3a), this expression decreases with d, and the curvature of this decrease is described by the same exponent and the curvature in the resource density dependence (v). The principle of inheritance of the curvature of density dependence, embodied in equation (3b), is a relatively general one. However, this inheritance via resource dynamics can potentially be modied or reversed by nonlinear functional and numerical responses of the consumer, as shown below. Functional Response Form Here I begin with a more general analysis of a saturating (Type II) functional response and then consider other

324 The American Naturalist

Figure 1: Equilibrium consumer density as a function of mortality for a model with a linear consumer functional response and abiotic resource
growth whose parameters are B p I p E p C p 1 ; d0 p 0.02. The gure shows how Neq changes with mortality for several v-logistic models of consumer growth that share the same maximum per capita growth rate and equilibrium density. These include the best-t v (v p 1/21 ) based on minimizing the absolute difference between the two curves between mortalities of 0.02 and 1.0.

erating decline. The mean N often differs from Neq, as is shown in gure 2 of Abrams (2009b). Dropping the assumption that the resource per capita growth function, f, is linear complicates the interpretation of equation (6) with a Type II response. However, the appendix shows that the Neq versus d relationship is an accelerating decrease when the system is stable unless f is large and positive. Both abiotic growth and v-logistic growth with v ! 1 can have an arbitrarily large (positive) f if R is very small. Resource density, R, increases as consumer mortality increases. Thus, the general analysis suggests that when g reects consumer satiation, resource growth has a large abiotic component, and the system is stable, consumer population size will decrease at a decelerating rate with mortality at low mortalities but may then decrease in an accelerating fashion as the mortality rate becomes high (see examples in g. 2). Some functional responses, such as Hollings Type III, are characterized by a unimodal g. Type III responses increase at an accelerating rate over a range of low resource densities. In most cases, this makes expression (6) larger (i.e., more likely to be positive) at low densities. If there is logistic resource growth and a simple Type III response with g p R/(1 ChR 2), equation (6) must be positive at low values of R, where the functional response accelerates; this means a decelerating decrease of N with d when d is small and an accelerating decrease when d is large. Numerical Response Form The inuence of the consumers response on the shape of the Neq versus d relationship is easy to derive when the

consumers functional response is linear. The equilibrium N declines with d when the functional response is linear and there is no Allee effect in the resource growth. The methods used to derive equation (6) show that the curvature of the relationship between Neq and d is
2

Neq bf Cb f p . 2 3 3 d C b

(7)

This means that, for logistic resource growth (f p 0), the curvature has the sign of b ; if the numerical response saturates (b ! 0), consumer population size will decline at an accelerating rate with mortality. For nonlogistic growth, the curvature is inuenced additively by both the curvature of resource growth and the curvature of the numerical response. Incorporating a nonlinear functional response increases the complexity of expression for the second derivative of N. However, most of the preceding analysis of nonlinear functional responses is not changed qualitatively by also having a nonlinear numerical response. Is the v-Logistic an Adequate Model When Neq Is Decreasing and Uniformly Concave (or Convex)? The preceding section derived expressions for curvature but did not evaluate the full Neq versus d relationship for any particular set of the three component functions in the consumer-resource model. This section will focus on an example of a commonly used consumer-resource model with a concave N versus d relationship. Here it is shown

Density Dependence 325

Figure 2: A gives the equilibrium and temporal average consumer population size as a function of its per capita mortality in a system where the
resource is a sum of biotic (logistic) and abiotic growth and the consumer has a linear functional response. The parameter values are I p 0.01, E p 0.01, r p 1, K p 1, C p 1, h p 3, B p 1. B shows the same relationship for a similar system that differs in that there are two patches; the consumer is conned to patch 1, and the resource has a lower carrying capacity and intrinsic growth rate in the refuge patch (patch 2). The parameters that differ from (or are not present in) A are as follows: K1 p 2 , K2 p 0.5 , r2 p 0.5 . There is a range of intermediate mortalities producing limit cycles, but these are of modest amplitude and have little effect on average densities.

that the best v-logistic model is still a very poor description of this system. The next section determines the ecological circumstances leading to population-mortality relationships that are qualitatively inconsistent with the v-logistic model, either because they have changes in the sign of the second derivative or because the population increases with mortality. One of the simplest consumer-resource models for which the second derivative of population size with mortality does not change sign is MacArthurs (1972) alternative model, in which the resource has abiotic rather than logistic growth:

dR pI dt

ER

CRN.

(8)

Here I is a resource input rate and E is the rate of loss per unit of resource present. This is one of the most widely used models in consumer-resource theory. Combining equation (8) with a consumer species that changes according to dN/dt p N(BCR d 0 ) d h N yields BI d0 dh E , C

Neq p

(9)

326 The American Naturalist where mortality has again been divided into a minimum natural mortality, d0, and an imposed mortality, dh. The relationship between Neq and dh is hyperbolic (concave). This would seem to make it a promising candidate for being approximated by the v-logistic formula: and lead to an approximately linear relationship, but that is rarely if ever true. The following paragraphs argue that, in each of these two cases, the most likely shape for the overall relationship is a concave decrease at low mortality and a convex decrease at high mortalities, with a relatively at portion in between. Functional responses may exhibit both concave and convex segments. A uniformly convex shape (i.e., a Type II response) has been observed in the majority of experimental studies (Jeschke et al. 2004). However, this may be in part a reection of the fact that most experiments have been done in the laboratory and over very short time periods (Abrams and Ginzburg 2000). Theory suggests that sigmoid forms (Type III responses) should be relatively common either because of the presence of alternative foods (Holling 1959) or because of costly foraging being reduced when little food is available (Abrams 1982). Type III responses have been observed by more careful studies (e.g., Sarnelle and Wilson 2008) in some cases that had previously been thought to have Type I or II responses. A Type III response leads to a decelerating decline in Neq with mortality when the mortality rate is low and an accelerating decline when mortality is high. The growth function of the resource may also exhibit segments having a different sign of the second derivative with respect to resource density. This will also frequently lead to a change in the sign of 2Neq / d 2 as d increases. One general reason for a change in second derivatives is the combination of biotic and abiotic elements in the resource growth function. Immigration of the resource from outside the consumers habitat or from a refuge represents an abiotic component of growth. Turchin and Batzli (2001) suggest such a combined model for the grasses eaten by voles; here, belowground plant tissue is a refuge from aboveground herbivory. The movement of individuals of the resource species into easily caught categories (diseased, senescent, or simply outside a refuge) can also be modeled using a combination of the abiotic equation (8) and a v-logistic expression for the self-reproducing component of growth. The abiotic component becomes a larger part of the resource reproduction at low densities (i.e., low consumer mortality) because the supply is independent of current resource density, even when density is low. If the self-reproducing component of growth is v-logistic with v 1 1, f(R) in a combined abiotic/biotic growth model will be concave at low R and convex at high R. Numerical response functions are largely determined by the relationship between food intake and reproduction. Sshaped relationships between food intake and per capita birth rate seem very likely on the basis of the fact that a certain amount of energy investment into reproductive structures is necessary before any reproduction can occur, resulting in an accelerating increase in the realized birth

Neq p K

( )
r dh r

1/v

(10)

where d0 does not appear because it is incorporated into r. If we assume equal equilibrium densities in the absence of harvesting, K p (BI/d 0 E/C). If the dh value that causes extinction is identical in the two cases, then r p (BIC/E d 0 ). With these formulas used for r and K in equation (10), it is possible to t a value of v that minimizes the absolute value of the difference between equations (9) and (10) over the range between d0 and the maximum dh. Figure 1 illustrates Neq versus d (p d 0 d h) for an example where the exponent v that minimizes the difference is approximately 1/21. Using this and several larger values of v, expression (10) is compared with the actual population (eq. [9]) in gure 1. All of the values of v vastly underestimate population size at high mortality rates. For example, the best-t v produces population sizes that are too small by more than four orders of magnitude for the highest 50% of possible mortality rates. The conclusion is that the v-logistic model is not an adequate approximation for one of the simplest and most widely used consumer-resource models and one whose concavity seemed to make it a good candidate for being represented by the v-logistic. This conclusion is maintained for a wide range of other nonlinear models in which the functional and/or numerical responses are nonlinear (P. A. Abrams, unpublished data). This is not surprising, since the simple power function embodied in the v-logistic is not very exible. The fact that, when v ! 1, the slope of the N versus d relationship must be 0 at the maximum mortality means that very large underestimates of population size at high mortalities almost always occur. How Common Are Conditions That Produce a Mixture of Concave and Convex Sections? A common feature of consumer-resource models that is impossible in the v-logistic is the presence of both concave and convex sections of the population size versus mortality relationship. This can arise when only one of the three basic component functions is nonlinear if that function has concave and convex sections. It can also arise when different members of this set of three component functions have different second derivatives. It might seem that, in this second case, the different curvatures should cancel

Density Dependence 327 rate at low food densities. On the other hand, there must be an upper limit to the birth rate that results in a leveling off at high food densities, which implies a change in the sign of the second derivative of the numerical response at high mortality Even if each of the three component functions can be characterized as uniformly accelerating or decelerating, the N versus d relationship can include both accelerating and decelerating (convex and concave) sections when a pair of these three functions differs in the sign of their curvature. Functional or numerical responses must display some saturation at high enough food availability, which tends to make N decrease at an accelerating rate with mortality. On the other hand, either large abiotic components of resource renewal or biotic renewal according to the v-logistic model with v ! 1 will tend to produce a concave N versus d relationship. Times series analyses have suggested that v ! 1 is more common than v 1 1 (Sther et al. 2002; Sibly et al. 2005). While time series analysis is problematic (Doncaster 2006, 2008), there seems to be little doubt that many species are characterized by v ! 1 over at least some ranges of density. However, the inuences of the resource growth function and the functional response on the N versus d relationship are likely to shift in their relative strength as the consumer mortality rate increases. Under abiotic growth (eq. [8]), f is given by 2I/R 3, which becomes very large in magnitude when R is small (i.e., when consumer mortality is low). On the other hand, the inuence of the functional and numerical responses will be greatest at high mortality rates, when resources are so abundant that the responses are saturated. Thus, the combined effect of resource growth and consumer functional response is likely to be a consumer population size versus mortality relationship that changes curvature from decelerating to accelerating (concave to convex) as consumer mortality increases. Two simple examples of the pattern predicted in the preceding paragraph are shown in gure 2, which assumes that logistic resource growth (v p 1) is supplemented by immigration and emigration in the form of an abiotic growth equation. In addition, the consumer has a Type II functional response. The functions f and g have opposite inuences on the sign of the N versus d relationship, because resource growth is concave while the functional response is convex. Figure 2A presents an example of the typical shape for the relationship between N and d under this scenario when there is a relatively small contribution of immigration compared with the maximum of the biotic growth component of the resource. Here the relationship is complicated by a range of d values producing instability. However, the average density does not differ greatly from the equilibrium over this range. At very low death rates of the consumer, the abiotic component of resource growth dominates, and consumer population size decreases at a decelerating rate. At higher death rates, the inuence of the saturating functional response dominates, and N declines at an accelerating rate. A variant of the preceding system assumes that there are habitat patches where the resource has a refuge from the consumer and others where both are present. Each patch has logistic resource growth, and there is bidirectional movement between two types of patches. The dynamics of this system were discussed by Abrams and Walters (1996); if the consumer is efcient and has a relatively large handling time, there are sustained cycles for a range of intermediate mortality rates. The resulting relationship between mean consumer population size and consumer mortality is shown in gure 2B. The relationship is similar to that shown in gure 2A; both have a broad range of mortalities over which population size exhibits very little change. If the consumer dynamics in systems like those in gure 2 are represented by a density-dependent growth function, that function would have the form shown in gure 2 with the axes reversed. Thus, at low consumer density, the consumers per capita growth rate is relatively insensitive to density but declines at an accelerating rate. A sharp drop in per capita growth occurs at the density corresponding to the nearly at section in the examples in gure 2. At high consumer densities, consumer per capita growth declines in a decelerating (concave) manner. The prey per capita growth function, f(N ), experienced by a predator of that consumer would then be relatively at but accelerating (f ! 0) at low N and decelerating (f 1 0) at high N. If the predator (with population P) on this consumer had linear functional and numerical responses, its densitydependent growth would inherit the form of the preys per capita growth function. This means that, when plotted against its own mortality, its population density would exhibit a concave decrease at low mortality and a convex decrease at high mortality. Type II functional responses are known for producing cycles. On the basis of equation (5), the equilibrium consumer population size will increase with increases in its own mortality over the range of mortality rates where cycles occur. This pattern (termed the hydra effect in Abrams and Matsuda 2005 and reviewed in Abrams 2009b) is also inconsistent with all standard single-species models of density dependence. Although the hydra effect in gure 2 is relatively small in magnitude, it is easy to produce examples where it is much larger and where it occurs in stable systems (Abrams and Vos 2003; Abrams and Matsuda 2005; Abrams and Quince 2005). None of these can be represented by any continuous-time single-species model of density dependence.

328 The American Naturalist Alternative Consumer-Resource Models Here I mention some of the factors that have been left out of the models considered here and discuss how these might affect the relationship between a consumers density and its per capita mortality. Most consumers are generalists; the impact of use of multiple resources is discussed elsewhere (Abrams, in review). The presence of many resources having different vulnerabilities to the consumer usually creates a decelerating decline in a consumer population as its mortality increases from very low levels. This comes about because apparent competition is relaxed and more vulnerable resources recover as consumer mortality increases. Many consumers are likely to have consumerdependent functional responses in which g is a function of N as well as R (Abrams and Ginzburg 2000; Skalski and Gilliam 2001). Preliminary explorations (P. A. Abrams, unpublished data) show that the Beddington-DeAngelis response (Beddington 1975; DeAngelis et al. 1975) makes N decrease in a more strongly decelerating manner with mortality than when consumer (predator) dependence is absent. The basic reason is that higher mortality decreases N, which increases the consumers per individual capture rate, partially offsetting the negative impact of the mortality. Stage- or size-structured consumers and/or resources may also exhibit different N versus d relationships. Abrams and Quince (2005) showed that increasing consumer population size with increasing mortality is more likely when consumers are restricted to consuming juvenile prey, and De Roos et al. (2007) have also explored how size structure alters the impact of mortality on population size. However, density dependence in structured populations is still poorly understood. Temporal variation in parameters has also been ignored here, and it may alter the nature of resourcebased density dependence considerably. Discussion It is a basic axiom of theory that the predictions of simplied models should be qualitatively consistent with the predictions of a wide range of more detailed models of the process they are designed to represent (Ruefer et al. 2006). If this is not true, then the original simplication is obviously excessive. All populations that have been modeled by traditional density-dependent growth are actually resource consumers, and at least part of their density dependence is likely to result from resource depletion. Thus, consumer-resource models should provide guidance in determining the single-species model that is most appropriate for representing the consumers dynamics as well as whether resource depletion can be meaningfully represented by a single-species model of consumer dynamics. Here, I have examined the density dependence in a consumer species that results from different assumptions about its underlying interactions with its resources. The functional form of density dependence is quantied by examining how the equilibrium (or long-term mean) consumer density changes as a function of the per capita density-independent mortality (harvest) rate. The analyses suggest that density dependence arising from resources is likely to differ in systematic ways from the density dependence in the most commonly used exible singlespecies model, the v-logistic (Gilpin and Ayala 1973). This model is the only alternative to the simple logistic model considered in theoretical analyses of many topics (e.g., Turchin 2003; Filin et al. 2008). Almost all work on large food webs assumes logistic density dependence. We know very little about how this may have affected the conclusions of theoretical studies of such webs. Finally, the possibility of population size increasing with mortality, which arises in many consumer-resource models (Abrams 2009b), is fundamentally inconsistent with any continuous-time single-species model of density dependence. Even in cases where a uniformly decreasing concave (or convex) relationship between population size and mortality occurs, the v-logistic is often a very poor approximation, as in the abiotic resource growth model (g. 1). Common features of natural systems, including resource immigration and saturating and/or consumer-dependent consumer functional and numerical responses, are likely to result in equilibrium consumer population size decreasing at a decelerating rate when mortality is relatively low and at an accelerating rate when mortality is high. Unfortunately, we know little about the nature of density dependence in natural populations. One careful experimental analysis found that the curvature of density dependence changed with resource quality (Miller 2007), which is certainly consistent with the present theory. Time series analyses depend on natural variation, so they are likely to be sampling only part of the full range of densities that are possible. Thus, even if such analyses could circumvent the various problems discussed in the Introduction, any shape measured at relatively high densities will not necessarily hold for low densities, and vice versa. Time series analysis also requires long-term data, which are usually not available. Brook and Bradshaw (2006) analyzed 1,198 time series of abundances and noted that clear evidence for any density dependence was lacking in approximately 25% of those studies. They attributed this primarily to large sampling errors and time series that were too short. These same factors are more of a problem in estimating shape parameters. Given the rapid pace of environmental change, some type of deductive approach is likely to be required to make informed guesses about the nature of density dependence in species of management

Density Dependence 329 or conservation concern. The theory developed here shows how functional and numerical response shapes and the nature of resource density dependence can be used to deduce the shape of density dependence in the consumer. While there are many unknowns in all of these relationships, even qualitative knowledge of the natural history is likely to provide some guidance in narrowing the range of possible shapes. This is likely to prove important for improving harvesting and conservation policies. Acknowledgments This research was supported by a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada. I thank several reviewers for their comments on earlier drafts. Literature Cited
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Associate Editor: Michael Neubert Editor: Donald L. DeAngelis

Acoloithus americana, a little dark blue moth, with a deep orange color, whose black and yellow larva is gregarious, living in companies of a dozen or more, and eating the softer parts of leaves, from Review: Economical Entomology in Missouri (American Naturalist, 1870, 4:610615).