Allee Effect and the Uncertainty of Population Recovery

Recovery of depleted populations is fundamentally important for conservation biology and sustainable resource harvesting. At low abundance, population growth rate, a primary determinant of population recovery, is generally assumed to be relatively fast because competition is low (i.e., negative density dependence). But population growth can be limited in small populations by an Allee effect. This is particularly relevant for collapsed populations or species that have not recovered despite large reductions in, or elimination of, threats. We investigated how an Allee effect can influence the dynamics of recovery. We used Atlantic cod (Gadus morhua) as the study organism and an empirically quantified Allee effect for the species to parameterize our simulations. We simulated recovery through an individual‐based mechanistic simulation model and then compared recovery among scenarios incorporating an Allee effect, negative density dependence, and an intermediate scenario. Although an Allee effect significantly slowed recovery, such that population increase could be negligible even after 100 years or more, it also made the time required for biomass rebuilding much less predictable. Our finding that an Allee effect greatly increased the uncertainty in recovery time frames provides an empirically based explanation for why the removal of threat does not always result in the recovery of depleted populations or species. El Efecto Allee y la Incertidumbre de la Recuperación de Poblaciones     

Making a stand: five centuries of population growth in colonizing populations of Pinus ponderosa

The processes underlying the development of new populations are important for understanding how species colonize new territory and form viable long-term populations. Life-history-mediated processes such as Allee effects and dispersal capability may interact with climate variability and site-specific factors to govern population success and failure over extended time frames. We studied four disjunct populations of ponderosa pine in the Bighorn Basin of north-central Wyoming to examine population growth spanning more than five centuries. The study populations are separated from continuous ponderosa pine forest by distances ranging from 15 to >100 km. Strong evidence indicates that the initial colonizing individuals are still present, yielding a nearly complete record of population history. All trees in each population were aged using dendroecological techniques. The populations were all founded between 1530 and 1655 cal yr CE. All show logistic growth patterns, with initial exponential growth followed by a slowing during the mid to late 20th century. Initial population growth was slower than expectations from a logistic regression model at all four populations, but increased during the mid-18th century. Initial lags in population growth may have been due to strong Allee effects. A combination of overcoming Allee effects and a transition to favorable climate conditions may have facilitated a mid-18th century pulse in population growth rate.     

The effects of helpers in cooperatively breeding purple gallinules

Summary The effects of helpers in a population of cooperatively breeding purple gallinules (Porphyrula martinica) were examined. All young birds past the age of 2 months helped feed and protect subsequent broods of chicks and participated in territorial defense. Most helpers remained on their natal territories for approximately 1 year. The number of helpers varied both among and within breeding groups. Clutch production and chick survival were related positively to the number of helpers in the group. The increase in chick survival was independent of several measures of territory quality. Helpers possibly aided chick survival by provicing extra food for the chicks and decreasing predation risk. Helpers were necessary in order for a breeding pair to keep a territory long enough to produce more than one clutch of eggs. A change in the number of helpers (increase or decrease) often was followed by a similar change in territory size. These results suggest that purple gallnule helpers can increase the reproductive success of the breeding group and may be vital for the continued maintenance of a breeding territory.     

The consequences of being colonial: Allee effects in metapopulations of seabirds

Most seabirds live in large colonies. This fact signifies that there is an advantage in living and breeding together. Four explanations are put fore ward for this colonial behaviour, more birds have: (1) a reduced per capita predation of chicks in colonies, (2) a better anti-predator defence, (3) a more efficient foraging in temporally patchy environments and (4) sex ratios that are more likely to be close to one. These factors induce a strong Allee-type density-dependent relation, a positive relation between density and population growth rate at low density. Nevertheless, these Allee effects are generally ignored in seabird population studies. Therefore we study the consequences of introducing Allee-type density-dependent relations in a spatially explicit metapopulation model for the Common Tern (Sterna hirundo). Simulations show that Allee effects might be responsible for a 20-fold decline in the recolonization distances, causing patches and parts of metapopulations to effectively become more isolated. This leads to long recolonization times of empty breeding patches which consequently cause slower metapopulation expansion and recovery. Additionally, we show that the typical early warning signals, that show that a population is near its critical threshold induce by Allee effects, is less pronounced in colonies that are part of a metapopulation. Hence, we offer some simple equations to estimate critical densities and thresholds in a colony.     

Experimental Demonstration of an Allee Effect in American Ginseng

Abstract: Harvesting of wild American ginseng (   Panax quinquefolius ) for the herbal trade has lowered natural population sizes. We tested for reproductive limitation due to small population size (a form of the Allee effect) by experimentally planting "natural" populations numbering 4, 16, and 64 using 4-year-old cultivated plants. Plant size traits and reproductive traits ( bud, flower, green fruit, and mature fruit) were recorded through the ensuing summer. Fruit production per flower and per plant increased in proportion to flowering population size (  p = 0.0063 and p = 0.0017, respectively), strongly suggesting that an Allee effect occurs in very small populations. The increase in fruit production was not explained by either plant or inflorescence size differences. Although population size-dependent pollination, through insufficient pollinator visitation rate or pollen transfer rate, seems the most likely cause of the observed effects, our limited observations of pollinators were not sufficient to demonstrate a change in pollination rates as a function of population size. Knowledge of the presence as well as the mechanism underlying this Allee effect may be especially useful for management and determination of minimum viable population size of the species in the wild.     

Invading parasitoids suffer no Allee effect: a manipulative field experiment

One frequent explanation for the failure of biological invasions is the Allee effect: due to positive density dependence, initially small invading populations may fail to establish and spread. Populations released for biological control are similar to fortuitous invading populations and may therefore suffer from Allee effects. However, unlike fortuitous invasions, biological control allows the experimental manipulation of initial population size and, thus, offers a unique opportunity to test for the occurrence of Allee effects. We manipulated the initial size of 45 populations of a parasitoid wasp introduced for the biological control of a phytophagous insect and followed the population dynamics of both parasitoids and hosts during three years. Our results suggest an absence of Allee effects but clear negative density dependence instead: (1) the probability of establishment after three years was not affected by initial population size; (2) net reproductive rate was highest at low parasitoid density and high host density; (3) the sex ratio, reflecting the proportion of virgin females, did not increase at low density, suggesting that low densities did not impede mate-finding; (4) the depression of host populations did not depend upon the number of parasitoids introduced. This is, to our knowledge, the first experimental test of the Allee effect in an invading parasitoid. It leads us to propose that a number of behavioral and life-history features of many parasitoids could protect them from Allee effects.     

Consequences for predators of rescue and Allee effects on prey

The size of a population can be augmented by enriching the carrying capacity of its limiting resource, or by subsidising the renewal of the resource. The well known ‘paradox of enrichment’ models the first case, in which enrichment can force consumers and their limiting resource into destabilising limit cycles, whereas impoverishment stabilises the dynamics. In this paper we model the case of resource subsidy, where the resource is a limiting prey to predators. In contrast to enrichment, the system is stabilised by an influx of prey in the form of a rescue effect, and destabilised by an outflux of prey in the form of an Allee effect. Limit cycles are not sustained by the Allee effect; instead both populations collapse to zero over a large region of the predator-prey phase plane. The catastrophic extinction of prey requires the presence of both an Allee effect on prey and a predator with a type II functional response, though neither needs to contribute a large impact to prey dynamics. The novel implication is that consumers exaggerate the impact of Allee effects on a renewing resource. Conversely, an Allee effect in the form of a cull of resource, even of small value, can trigger local extinction of resource-dependent consumers.     

Modulation of predator-prey interactions by the Allee effect

An Allee effect arising from density-dependent mating success can have significant impacts at the ecosystem level when considered in the context of predator-prey interactions. These are captured by a mathematical model for the exchange of biomass between a structured predator population (continuous weight distribution) and a resource. Because the predator’s mating success affects the amount of resources required for the production of offsprings and their future growth into mature organisms, it influences the flux of biomass between trophic levels. Under simple assumptions, the equations can be reduced to an equivalent unstructured predator-prey model in which the Allee effect modulates the predation rate: the mating probability multiplies the rate of predator growth as well as the rate of resource depletion. Implications of the Allee effect for the bifurcation structure and equilibrium densities are examined. The model is compared to a modified version in which the Allee effect instead modulates the assimilation efficiency, hence the mating probability does not appear in the dynamical equation for the resource density. Both models exhibit qualitatively similar dynamics. However, compared to the model in which the Allee effect modulates predation, the model in which the Allee effect modulates assimilation efficiency predicts (i) unrealistically inefficient resource assimilation when predator density is low, (ii) a higher risk of catastrophic extinction resulting from a change in the parameter controlling the strength of the Allee effect, and (iii) no possibility of an increase in population size when the density dependence is enhanced.     

Modeling the dynamic habitat and breeding population of Southwestern Willow Flycatcher

To aid in the management and conservation of Southwestern Willow Flycatcher (Empidonax traillii extimus, hereafter “Flycatcher”), we developed numerous models of flycatcher breeding habitat at Roosevelt Lake, AZ. For model development and testing, we compiled 10 years of flycatcher territory data that were obtained from intensive fieldwork between 1996 and 2005. We identified riparian vegetation annually in the project area from Landsat Thematic Mapper images, and extracted floodplain features from a digital elevation model. We created a novel class of temporal (i.e., multiyear) variables by characterizing the stability and variability in breeding habitat over a 6-year time interval. We used logistic regression to determine associations between environmental variables and flycatcher territory occurrence, and to test specific hypotheses. We mapped the probability of territory occurrence with a GIS and determined model accuracies with a classification table and a 10-year population database. Environmental features that were associated with breeding flycatchers included floodplain size, proximity to water, and the density, heterogeneity, age and stability of riparian vegetation. Our best model explained 79% of the variability in the flycatcher breeding population at Roosevelt Lake. The majority of predicted flycatcher habitat formed between 1996 and 2004 on an exposed lakebed ～3 years after water levels receded during a prolonged drought. A high correlation between annual reservoir levels and predicted breeding habitat (r = ?0.82) indicates that we can create and manage habitat for conservation purposes. Our predictive models quantify and assess the relative quality of flycatcher breeding habitat remotely, and can be used to evaluate the effectiveness of habitat restoration activities. Numerous techniques we developed can be used to characterize riparian vegetation and patch dynamics directly off of satellite imagery, thereby increasing its utility for conservation purposes.     

Alternative reproductive tactics in the territorial damselflyCalopteryx maculata: sneaking by older males

Summary We conducted daily censuses on a marked population of the damselflyCalopteryx maculata for two complete breeding seasons to document the reproductive tactics of individual males. Overall, 78% of the 600 males studied defended territories and 14% of those territorial males were also observed engaged in sneaking behaviour on some days. When sneaking, males did not defend territories but attempted to steal females from other males' territories. Sneakers were usually previously successful territorial males who emerged early in the season and began sneaking relatively late in their lives (Fig. 2). Thus the adoption of sneaking was conditional and related to both male age and population density. We suggest that sneaking, in this species, is a “make the best of a bad situation” tactic adopted when intense male-male competition forced older males to abandon territoriality. Thus, sneaking allowed males with declining resource holding potential to prolong their reproductive careers after they were no longer able to hold a territory.     

The Role of Behavior in Recent Avian Extinctions and Endangerments

Abstract: Understanding patterns of differential extinction and predicting the relative risks of extinction among extant species are among the most important problems in conservation biology. Although recent studies reveal that behavior can be a critical component in many species' extinctions or endangerments, current approaches to the problem of predicting extinction patterns largely ignore behavior. I reviewed how behavior can affect population persistence and then used recent avian extinctions and endangerments to illustrate behaviors relevant to extinction risk. Behaviors that affect population persistence can be grouped as aggregation, interspecific responses, dispersal, habitat selection, intraspecific behavior, and maladaptive behavior. Behavior that can affect extinction risk is not limited to birds; for example, in many taxonomic groups (vertebrate and invertebrate) there is evidence of socially facilitated reproduction in colonial species, Allee effects on reproductive success and survival, behavioral regulation of population size, and conspecific attraction to breeding sites. Incorporating specific behaviors into models predicting extinction probabilities and patterns should improve their predictions.     

Spatial and temporal dynamics at manakin leks: reconciling lek traditionality with male turnover

Leks, display grounds where males congregate and females visit to copulate, are typically traditional in location, despite often high turnover of individual males. How leks can persist in face of male turnover is not well understood, in part due to a lack of detailed field data allowing for a clear understanding of lek dynamics. We followed the fate of individual males at 11 to 15 leks of the blue-crowned manakin Lepidothrix coronata across four breeding seasons to gain insights on how leks are formed and changed in space and time. Between years, leks were traditional in location despite changes in territory ownership due to male disappearance and recruitment. New males were equally likely to recruit by taking over existing territories or by establishing new territories. Recruitment was influenced by age, as recruits were more likely to be adults than subadults. Lek size did not affect the probabilities of a male recruiting or persisting at a territory, and vocalization rate, a correlate of mating success in this population, did not affect male persistence. We used our field data to model changes in lek size and composition over longer periods of time (100 years) to understand how lek traditionality can be reconciled with high male turnover. Our simulations showed that leks in our population rapidly stabilize in size despite changes in territory ownership and that rates of male recruitment and disappearance compensate each other, such that leks have the potential to persist for several decades after the original males have disappeared from them.     

Nonideal breeding habitat selection: a mismatch between preference and fitness

The selection of breeding sites in heterogeneous habitats should ideally be based on cues closely reflecting habitat quality and thus predicting realized individual fitness. Using long-term population data and data on territory establishment of male Northern Wheatears (Oenanthe oenanthe), we examined whether territory characteristics linked to individual fitness (reproductive performance and survival) also were linked to territory preference. Breeding territories varied in their physical characteristics and their potential effects on reproductive performance, and this variation among territories was correlated from one year to the next. Of all measured territory characteristics (from the focal and the previous year) only territory field layer height predicted individual fitness, i.e., reproductive performance was higher in territories with permanently short rather than growing field layers. Territory preference, instead, was only linked to the size of territory aggregations, i.e., males settled earlier at territory sites sharing borders with several adjacent sites than at those with few or no adjacent sites. This mismatch between territory characteristics linked to fitness and those linked to territory preference was not explained by site fidelity or compensated for by the different fitness components measured. Because the results were not in agreement with an ecological trap scenario, where poor habitats are preferred over high-quality habitats, our results suggest a more general case of nonideal habitat selection. Whereas nonideal selection with respect to territory field layer height may be explained by its poor temporal predictability within the breeding season, the preference for territory aggregations is still open to alternative adaptive explanations. Our study suggests that nonideal habitat selection should be investigated by direct estimates of preferences (e.g., order of territory establishment) and their links to habitat characteristics and fitness components. Furthermore, we suggest that the probability of establishing a territory needs to be included as a factor influencing patterns of habitat selection.     

Polygyny in the great reed warbler,Acrocephalus arundinaceus: a possible case of deception

Summary Polygyny was studied for 1 year in a great reed warbler population breeding in southern Germany. Data on various parameters of male and territory characteristics were collected and subjected to multivariate statistical analysis in order to assess their relative importance in female choice. Differences in territory characteristics appeared to be more important (Tab. 1), but there was a strong correlation between male and territory characteristics (Fig. 2, 3). Although the evolutionary advantages of polygyny to males are obvious (Fig. 5), those to females are far from clear. Models based upon the polygyny threshold and sexy son hypotheses predict that females should gain evolutionary advantage in either the short or long-term. Our data did not confirm such predictions, and secondary females showed greatly reduced breeding success (Fig. 4). If females were able to assess the status of mated males, they should instead select unmated males. Great reed warblers are a migrant species with a short breeding cycle in which the male plays relatively little part. They defend large territories in reed beds where visibility is reduced. These factors may permit males to practice a form of deception, by moving and attracting a second female who has little chance to assess that he is already mated.     

Current analyses do not resolve whether extra-pair paternity is male or female driven

Recent studies question the importance of indirect genetic effects in explaining female benefits of extra-pair matings in socially monogamous species. Compiling data on 14 wild bird species, Arnqvist and Kirkpatrick (Am Nat 165:S26–S37, 2005) estimated the average direct cost in terms or reduced parental care to be an order of magnitude larger than the potential effect of genetic benefits. This study has sparked a debate regarding potential confounding factors but no consensus appears to have been reached. Here we focus on the implicit assumption that all individuals face the same selective pressures and argue that this assumption is probably too strong in most cases. Using a theoretical model we show that when the amount of resources that a male provides depends on territory quality, his physical condition or prospects for alternative breeding opportunities, a female may respond to such differences by altering her mating behaviour. Such confounding factors may lead to direct fitness effects that result in negative correlations between paternal care and paternity even if females that produce extra-pair young experience a net benefit. Negative correlations can also result when males forcefully seek copulations and females resist them. We discuss the studies included in the analysis in this light, and conclude that current analyses on the net selective pressures remain uninformative. In addition to considering average effects across individuals and species we suggest giving attention to individual differences and the influence of ecological factors such as territory quality and predation pressures on female mating behaviour.     

Site fidelity and territorial movements of males in a rapidly declining population of yellow-headed blackbirds

We tested several hypotheses to explain low between-year territory fidelity in a breeding population of yellow-headed blackbirds (Xanthocephalus xanthocephalus). During a 5-year study the population of territorial males declined by two-thirds and some of the marshes that supported territories significantly deteriorated. Individual males held territories and bred for an average of 1.9 years. Of males that bred for at least 2 years, 30% skipped owning a territory in the study area during at least 1 year of their breeding lifetimes. Our information suggests that they may have bred outside of the area in those years. Of males with territories in two or more breeding seasons, 60% changed breeding marshes at least once. Males changed territories during 42.9% of between-year opportunities to do so. We found no support for the hypotheses that male yellow-headed blackbirds: (1) are more likely to move when territory density is low; (2) are likely to abandon territories that are deteriorating; or (3) change territories to improve their reproductive success. We suggest three non-mutually exclusive explanations for the yellow-headed blackbird's weak site fidelity: (1) it is a response to habitat deterioration and to other factors that may be causing the population's decline; (2) the males, being migratory, make fresh settlement decisions each year after they arrive on the breeding grounds in the general vicinity of their previous year's breeding; (3) yellow-headed blackbirds may have evolved in, and be adapted to, highly unstable habitats, moving frequently in response to changes in local breeding site conditions. Correspondence to: L.D. Beletsky     

Territory choice during the breeding tenure of male sedge warblers

A territorial male can shift the location of its territory from year to year in order to increase its quality. The male can base its decision on environmental cues or else on its breeding experiences (when territory shift is caused by breeding failure in previous seasons). We tested these possible mechanisms of territory choice in the sedge warbler (Acrocephalus schoenobaenus), a territorial migrating passerine that occupies wetlands. This species bases its territory choices on an environmental cue: tall wetland vegetation cover. We found that the magnitude of territory quality improvement between seasons (measured as the area of tall wetland vegetation) increased throughout the early stages of a male's breeding career as a result of territory shifts dependent on the earliness of arrival. The distance the territory was shifted between seasons depended negatively on the previous year's territory quality and, less clearly, on the previous year's mating success. On the other hand, previous mating or nesting success had no influence on territory quality improvement between seasons as measured in terms of vegetation. The results imply that tall wetland vegetation is a long-term, effective environmental cue and that a preference for territories in which this type of landcover prevails has evolved into a rigid behavioral mechanism, supplemented by short-term individual experiences of breeding failure.     

Long-term mate and territory fidelity in neotropical buff-breasted wrens (Thryothorus leucotis)

Among sedentary species, mate and site fidelity may be imposed by year-round territoriality and high annual survivorship, both of which theoretically lead to few opportunities to move between mates and breeding territories. We examined mate and territory fidelity in sedentary neotropical buff-breasted wrens (Thryothorus leucotis) in relation to the opportunities to divorce (vacancies on neighbouring territories), breeding experience and site of origin (within vs outside local breeding population). Overall, buff-breasted wrens showed high rates of mate and territory fidelity between years, with individuals significantly more faithful to their territories than to their partners. Mate and territory fidelity was not forced upon buff-breasted wrens, as most individuals had opportunities to switch mates and territories. However, this was not uniform among all individuals. Individuals that had bred together displayed 100% mate and territory fidelity despite the fact that males and females in almost all experienced pairs had opportunities to switch mates and territories. Local recruits (philopatric offspring that acquired territories in the local breeding population) also displayed mate and territory fidelity, but fidelity occurred because recruits rarely had the opportunity to divorce prior to initiating their first breeding attempt. By contrast, almost half of all territorial individuals that originated outside the local breeding population (immigrants) had opportunity to divorce, with approximately two thirds of them switching mates and territories. Divorces occurred within the first 5 months of pairing, suggesting that immigrants may have sampled mates and territories before forming permanent partnerships.     

Multiple mating opportunities boost protandry in a pied flycatcher population

Protandry, the earlier arrival of males than females to breeding areas, is widespread in birds, but its underlying mechanisms are far from well understood. The two, not mutually exclusive most highly supported hypotheses to explain avian protandry postulate that it has evolved from intrasexual male competition to acquire the best territories (“rank advantage” hypothesis) and/or to maximize the number of mates (“mate opportunity” hypothesis). We studied for two consecutive years the relative importance of both hypotheses in a population of pied flycatchers (Ficedula hypoleuca), a territorial songbird with a mixed mating strategy. We measured territory quality using a long-term dataset on nest occupation and breeding output, and we used molecular techniques to assess male fitness across the range of social and genetic mating options. Territory quality was unrelated to breeding date and had no influence on extra-pair paternity or social polygynous events. However, males breeding early increased their chances of becoming socially polygynous and/or of attaining extra-pair paternity and, as a consequence, increased their total reproductive success. These results support the “mate opportunity” hypothesis, suggesting that sexual selection is the main mechanism driving protandry in this population.     

Male's return rate, rather than territory fidelity and breeding dispersal, explains geographic variation in song sharing in two populations of an oscine passerine (Oreothlypis celata)

Males of some oscine passerines learn and share songs of neighboring males. This process can lead to the formation of song pattern neighborhoods or microhabitat song dialects. The degree to which song sharing occurs between populations and the spatial scale over which neighboring males share songs, however, can vary widely, and interpopulation comparisons have suggested that song sharing is more common in residents than in migrants. Here, we examine two populations of the orange-crowned warbler (Oreothlypis celata) to quantify patterns of song sharing at the northern (long-distance migrant) and southern (short-distance migrant) edges of the breeding distribution and to test if return rate, territory fidelity, and breeding dispersal explain the patterns found in the two populations. The southern population (O. celata sordida breeding on Santa Catalina Island, California; 33°N) had a higher annual return rate to their territories and exhibited higher song sharing in neighborhoods than their counterparts (O. celata celata breeding in Fairbanks, Alaska; 64°N). Year-to-year patterns of territory fidelity and breeding dispersal distances were similar between populations. Our results suggest that if migratory distance generally covaries with the proportion of returning males, this could explain different levels of song sharing between the short- and long-distance migrants.