Allee Effects

Allee effects occur in small or sparse populations and, although rarely detected, are widely believed to be
common in nature. Population growth of populations subject to Allee effects is reduced at low density. The
originator and namesake of the phenomenon was Warder Clyde Allee (1885–1955), a University of Chicago
zoologist and animal ecologist, whose special interest was group behavior in animals.

Charles Darwin observed that large population size is an important hedge against extinction in the presence of
predators or other natural enemies (Darwin 1872, quoted in Stephens et al. 1999). Nevertheless, early twentieth
century biologists typically accepted as given both the Malthusian principle — that intra-specific competition
does not decrease with population size — and its mathematical expression in the logistic model for population
growth (Gause 1934).

Allee, an astute observer of animal behavior, noticed that in many species it was undercrowding, not
competition, that limited population growth. He observed, for instance, that aggregation had positive effects on
the survival of land isopods, which were subject to rapid desiccation when isolated (Allee 1927). His empirical
examples of the benefits of aggregation seemed to contradict both the Malthusian paradigm and the logistic
model. Much of Allee's early work focused on documenting this phenomenon in animal populations (Allee
1931).

In modern biology, Allee effects are considered to have two manifestations:

1. component Allee effects are exhibited by a population in which there is a positive association between some
fitness component (e.g., viability, juvenile survivorship, fecundity; Orr 2009) and population size;

2. demographic Allee effects that occur when these component Allee effects produce a positive association
between per capita population growth and population size.

Keeping in mind that competition, for instance for resources or space, will limit a population's size, and noting
that per capita growth rate of a population at small size equals average absolute individual fitness (Lande et al.
2003), both kinds of Allee effects may be captured by the following general definition.

An Allee effect is a positive association between absolute average individual fitness and population size over
some finite interval.

Such a positive association may (but does not necessarily) give rise to a critical population size below which the
population cannot persist (Stephens et al. 1999). Allee effects that cause critical population sizes are called
strong, while Allee effects that do not result in critical sizes are called weak. Other names for the Allee effect
are positive density dependence (in contrast to classical negative density dependence) and depensatory dynamics
(in contrast to classical compensatory dynamics).

Mechanisms That Cause Allee Effects

A positive relationship between fitness and population size can be caused by a variety of mechanisms that affect
reproduction and survival. A well established example, mate limitation, may result in undercrowding in species
that reproduce sexually, because sexual reproduction requires contact between male and female gametes. Mate
limitation reduces reproduction when plants or animals release gametes into the environment or when males and
females have difficulty locating each other. When behaviors such as breeding, feeding, and defense are
cooperative, they become more efficient or successful in larger social groups, resulting in increased reproductive
success or survivorship (Courchamp et al. 1999). Although cooperative behaviors are most obvious in social
vertebrates, such as prairie dogs, ungulates or birds, Allee effects resulting from group feeding or defense can
also arise in insects, such as bark beetles, and aquatic organisms, such as cichlid fish (Friedenberg et al. 2007,
Balshine et al. 2001).

Other mechanisms do not require cooperation in the behavioral sense, but merely the presence of conspecific
individuals. For example, the per capita risk of predation is smaller in large prey populations than small prey
populations (Dennis 1989, Gascoigne and Lipcius 2004). It is also known that the presence of multiple
individuals can alter environmental or biotic conditions in favorable ways. Examples of such niche construction
include reducing physical damage in intertidal zones (Bertness and Grosholz 1985) or exclusion of competitors
via allelopathy (Cappuccino 2004).
Finally, demographic and genetic mechanisms may give rise to Allee effects. In animals, active dispersal away
from low-density populations can result in decreased rates of population growth (Bonte et al. 2004). For many
organisms, when population size is small, inbreeding depression can cause an Allee effect by reducing average
fitness as population size declines (Fischer et al. 2003). While these phenomena differ in form, in the way they
affect fitness, and in which species are affected, they all result in the same general pattern: small populations
suffer from reduced average individual fitness.

Evidence of Allee Effects

Evidence for Component Allee Effects

There is evidence from natural populations for component Allee effects due to all of these mechanisms (see
references above, Courchamp et al 2008, Kramer et al. 2009; Figure 1). The most commonly observed
mechanism is mate limitation, which causes Allee effects in both animals and plants (in the form of pollen
limitation). Positive density dependence in survivorship due to either cooperative defense or predator satiation is
also found across taxonomic groups. Indeed, because the tendency of predators to become satiated and stop
increasing consumption depends on the predator rather than the prey, predator satiation has the potential to
affect any population fed upon by a predator that does not numerically track the abundance of the small prey
population, such as when a generalist predator feeds on multiple species (Kramer & Drake 2010). Evidence for
the other mechanisms described above is less abundant, but each has been found in multiple taxonomic groups,
and some studies have detected positive density dependence in reproduction or survival without identifying the
mechanism (Kramer et al. 2009), making it likely that there are other mechanisms that lead to component Allee
effects. The population level impacts of these mechanisms are less clear.
Evidence for Demographic Allee Effects

Demographic Allee effects have been harder to demonstrate. Two reasons for this include:

1. Allee effects in one component of fitness may be offset at low density by increases in other components of
fitness, such as decreased competition for resources;

2. Natural populations at low density are often difficult to detect and the high variance that results from small
sample sizes obscures statistical analysis.

For these reasons, unusual cases of population growth are important to the ongoing study of Allee effects. In
particular, monitoring data from invasive species provides an opportunity for improving understanding of Allee
effects. Some likely effects of positive density dependence are easier to observe, extinction, for instance, but it is
difficult to confirm that an Allee effect was to blame.

Dynamics of Populations with Allee Effects

The most dramatic consequences of Allee effects are associated with strong Allee effects, although weak Allee
effects are also predicted to give rise to measurable dynamical differences. The difference between Allee effects
and the classical (Malthusian) logistic theory is seen most clearly in the correlation between per capita growth
rate and population size. This correlation can be generated using :
The classical logistic theory predicts that per capita growth rate will not increase with population size (Figure
2b). By the definition above, a population with an Allee effect will exhibit an increase over some interval of
population size (Figure 2b). This distinction between Allee and non-Allee populations is the same regardless of
whether the y-axis depicts per capita intrinsic rate of increase, the reproductive multiplier, λ, or lifetime
reproductive output. Strong and weak Allee effects are distinguished according to whether the y-intercept falls
below or above the replacement value (1/x dx/dt = 0 or λ = 1), respectively (Figure 2b). These plots do not
distinguish whether the Allee effect is endogenous to the dynamics of the population, such as result from mate
limitation, or due to interactions with other species, such as the predator-induced Allee effect exhibited by the
crown-of-thorns starfish Acanthaster planci (Dulvy et al. 2004; Figure. 3).

Other dynamical consequences of strong Allee effects include:

1. A sigmoidal relationship between the probability of rapid extinction and the initial population size (Dennis
1989), a pattern which contrasts with the concave shape predicted by the classical logistic theory (Dennis 2002)
(Figure 4a);

2. A critical area that the population must occupy for it to persist (Lewis & Kareiva 1993, Vercken et al. 2011)
(Figure 4b);

Evolution

The negative effects of low density, such as difficulty finding mates or increased vulnerability to predators, is
expected to often result in strong selection for traits that reduce the influence of these mechanisms. For instance,
rare species, which are typically at low density, often have adaptations that allow positive growth at low density,
or they will become extinct. However, aggregation and sociality are not adaptations that eliminate Allee effects
per se. Rather, they increase population densities so that the densities at which Allee effects are manifest are
avoided (Stephens and Sutherland 1999). Other traits may be the result of selection on low-density populations.
For example, displays, calls, and pheromones all widen the area over which males and females perceive mates,
thus reducing mate limitation. These adaptations can also increase fitness in other ways, however, such as
signaling mate quality, so it is difficult to assign causality (Courchamp et al. 2008). Similarly, sperm storage,
hermaphroditism, and parthenogenesis are all favored when chances of encountering mates are low, but may
provide fitness benefits in other contexts as well, such as accelerated local adaptation (Cousyn et al. 2001). It is
reasonable to conclude that species most likely to suffer Allee effects are those that usually have large
populations but have suffered a recent reduction in size, such as due to habitat fragmentation or catastrophic
natural events. Such populations will be more likely to suffer from mechanisms that reduce fitness at low
density, especially if traits conferring fitness at low density incur a cost at high density. Finding such a trade-off
may provide the best indication that a trait is an evolutionary response to persistence at low density (Courchamp
et al. 2008).

Environmental applications

When the size of populations subject to strong Allee effects is low, then these populations tend towards
extinction. This fact argues for a thorough understanding of Allee effects and their mechanisms in order to
develop sound management practices for a number of environmental issues. An obvious case is the conservation
of rare species. It has been shown, for instance, that small patches of the flowering herb Clarkia concinna
concinna attract pollinating insects in fewer numbers than do large patches. As a result, small patches are more
prone to extinction (Groom 1998). In general, persistence of species subject to strong Allee effects requires that
a minimum population size — specific to each population — be distributed over a population-specific minimal
area. This conclusion also applies to efforts to restore extirpated populations through captive breeding and
reintroduction.

Another environmental issue that involves the Allee effect is the management of invasive species. Population
biologists have long wondered why only a small fraction of introduced species ultimately persist in their
introduced locations (Williamson & Fitter 1996). A partial answer to this question is that many introductions are
below the critical size associated with Allee effects (Grevstad 1999). It follows that risk management for
invasive species could be improved by a better understanding of the comparative biology of Allee effects (i.e.,
the relative frequency and strength of Allee effects across species) (Drake et al. 2004), coupled with a
quantitative understanding of the rates at which introductions occur, a concept referred to as propagule pressure
(Leung et al. 2004, Lockwood et al. 2005).

Even populations with weak Allee effects may require consideration of Allee effects for effective management.
For instance, the invasive smooth cordgrass, Spartina alterniflora, is known to exhibit Allee effects due to
pollination limitation. As a result, new patches of cordgrass initially grow quite slowly. An observer of such an
invasion might wrongly conclude that this species' potential for spread is low. However, once the incipient
colony grows to a certain size its potential to spread increases dramatically (Taylor 2004).

Conclusion

Allee effects are a small population phenomenon in which population growth rate is reduced by undercrowding.
Although Allee effects are widely believed to be common and are important to environmental management,
clear documentation of demographic Allee effects in nature has mostly proved elusive.