Allee effect limits colonization success of sexually reproducing zooplankton

Understanding the dynamics of populations at low density and the role of Allee effects is a priority due to concern about the decline of rare species and interest in colonization/invasion dynamics. Despite well-developed theory and observational support, experimental examinations of the Allee effect in natural systems are rare, partly because of logistical difficulties associated with experiments at low population density. We took advantage of fish introduction and removal in alpine lakes to experimentally test for the Allee effect at the whole-ecosystem scale. The large copepod Hesperodiaptomus shoshone is often extirpated from the water column by fish and sometimes fails to recover following fish disappearance, despite the presence of a long-lived egg bank. Population growth rate of this dioecious species may be limited by mate encounter rate, such that below some critical density a colonizing population will fail to establish. We conducted a multi-lake experiment in which H. shoshone was stocked at densities that bracketed our hypothesized critical density of 0.5-5 copoepods/m3. Successful recovery by the copepod was observed only in the lake with the highest initial density (3 copepods/m3). Copepods stocked into small cages at 3000 copepods/m3 survived and reproduced at rates comparable to natural populations, confirming that the lakes were suitable habitat for this species. In support of mate limitation as the mechanism underlying recovery failure, we found a significant positive relationship between mating success and density across experimental and natural H. shoshone populations. Furthermore, a mesocosm experiment provided evidence of increased per capita population growth rate with increasing population density in another diaptomid species, Skistodiaptomus pallidus. Together, these lines of evidence support the importance of the Allee effect to population recovery of H. shoshone in the Sierra Nevada, and to diaptomid copepods in general.     

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.     

The Population Dynamics and Conservation of Primate Populations

Abstract: Primates are among the most threatened taxa, with more than half of all species in jeopardy. In this paper we develop population models to use the kind of data on wild primates that primatologists actually collect. Our survey of recentprimate journals suggests that the average field study uses 1.5 years of data from 50 animals The models are based on the simple Leslie-Lefkovitch matrix. They suggest a simple method that allows assessment from a few years'data, of whether a population is collapsing and requires intervention To a good approximation, populations will collapse when adult survival, per inter-birth interval, is less than 70 percent.
Modifications of the basic model incorporate more realistic assumptions about social organization and densitydependent resource limitation. These allow us to identify population densities at which potential Allee effects operate, and permit more precise estimates of the minimum population sizes and compositions required for successful reintroductions to the wild The most important result is that populations of primates that live in small family groups may be more prone to "demographic" extinction than are more promiscuous species that live in more extended groups.     

Trajectories of zooplankton recovery in the Little Rock Lake whole-lake acidification experiment.

Understanding the factors that affect biological recovery from environmental stressors such as acidification is an important challenge in ecology. Here we report on zooplankton community recovery following the experimental acidification of Little Rock Lake, Wisconsin, USA. One decade following cessation of acid additions to the northern basin of Little Rock Lake (LRL), recovery of the zooplankton community was complete. Approximately 40% of zooplankton species in the lake exhibited a recovery lag in which biological recovery to reference basin levels was delayed by 1-6 yr after pH recovered to the level at which the species originally responded. Delays in recovery such as those we observed in LRL may be attributable to "biological resistance" wherein establishment of viable populations of key acid-sensitive species following water quality improvements is prevented by other components of the community that thrived during acidification. Indeed, we observed that the recovery of species that thrived during acidification tended to precede recovery of species that declined during acidification. In addition, correspondence analysis indicated that the zooplankton community followed different pathways during acidification and recovery, suggesting that there is substantial hysteresis in zooplankton recovery from acidification. By providing an example of a relatively rapid recovery from short-term acidification, zooplankton community recovery from experimental acidification in LRL generally reinforces the positive outlook for recovery reported for other acidified lakes.     

Floater mortality within settlement areas can explain the Allee effect in breeding populations

The Allee effect (the positive relationship between population growth rate and population size) is a constraint of some animal populations at low numbers, which increases their likelihood of extinction because of a decrease in reproduction and/or survival. We were able to demonstrate that the Allee effect can be the result of a mortality increase affecting floaters (i.e. dispersing individuals able to enter as breeders in the reproductive population when a breeding territory or a potential mate – owner of a suitable breeding territory – becomes available). Previously, potential mechanisms underlying Allee effects were always related to the breeding portion of a population only. In contrast, our understanding of or solutions to population declines due to the Allee effects can reside elsewhere, away from breeding territories.     

On the elasticity of range limits during periods of expansion

Dispersal is known to play a crucial role in the formation of species' ranges. Recent studies demonstrate that dispersiveness increases rapidly during the range expansion of species due to a fitness increase for dispersers at the expanding front. R. D. Holt concluded, however, that emigration should decline after the period of invasion and hence predicted some range contraction following the initial expansion phase. In this study, we evaluate this hypothesis using a spatially explicit individual-based model of populations distributed along environmental gradients. In our experiments we allow the species to spread along a gradient of declining conditions. Results show that range contraction did emerge in a gradient of dispersal mortality, caused by the rapid increase in emigration probability during invasion and selection disfavoring dispersal, once a stable range is formed. However, gradients in growth rate, local extinction rate, and patch capacity did not lead to a noticeable contraction of the range. We conclude, that the phenomenon of range contraction may emerge, but only under conditions that select for a reduction in dispersal at the range edge in comparison to the core region once the expansion period is over.     

Large nonlethal effects of an invasive invertebrate predator on zooplankton population growth rate

We conducted a study to determine the contribution of lethal and nonlethal effects to a predator's net effect on a prey's population growth rate in a natural setting. We focused on the effects of an invasive invertebrate predator, Bythotrephes longimanus, on zooplankton prey populations in Lakes Michigan and Erie. Field data taken at multiple dates and locations in both systems indicated that the prey species Daphnia mendotae, Daphnia retrocurva, and Bosmina longirostris inhabited deeper portions of the water column as Bythotrephes biomass increased, possibly as an avoidance response to predation. This induced migration reduces predation risk but also can reduce birth rate due to exposure to cooler temperatures. We estimated the nonlethal (i.e., resulting from reduced birth rate) and lethal (i.e., consumptive) effects of Bythotrephes on D. mendotae and Bosmina longirostris. These estimates used diel field survey data of the vertical gradient of zooplankton prey density, Bythotrephes density, light intensity, and temperature with growth and predation rate models derived from laboratory studies. Results indicate that nonlethal effects played a substantial role in the net effect of Bythotrephes on several prey population growth rates in the field, with nonlethal effects on the same order of magnitude as or greater (up to 10-fold) than lethal effects. Our results further indicate that invasive species can have strong nonlethal, behaviorally based effects, despite short evolutionary coexistence with prey species.     

Microsite-limited recruitment controls fern colonization of post-agricultural forests

Assessing the relative roles of dispersal limitation and environmental effects in population dynamics and community assembly is fundamental to understanding patterns of species distribution and diversity. In forests growing on abandoned agricultural lands, both legacies of vegetation disturbance and changes in the abiotic environment shape the diversity and composition of recovering communities. Here I specify how interactions among historical, environmental, and biological factors influence species distributions, focusing on three fern species with contrasting distributions across forests of different history in central New York, USA: Dryopteris carthusiana, Dryopteris intermedia, and Polystichum acrostichoides. Using population surveys, spore-trap and spore-bank studies, and a three-year field experiment, I compare demographic rates among species and between forest types to determine which life history stages limit colonization and which traits explain species distributions. Adult plants of all three species were larger and more likely to produce spores in post-agricultural forests than in adjacent, uncleared stands. Though lower population densities led to fewer spores in post-agricultural soils, spore availability still exceeded recruitment by four to five orders of magnitude. Sowing additional spores had relatively little effect, while microhabitat conditions had the greatest impact on establishment rates. Given similar microsites, the two forest types had equal rates of establishment, but some forest-floor features preferentially occupied by juvenile plants were less frequent in post-agricultural stands. The availability of suitable sites for establishment, created by small-scale heterogeneity on forest floors, thus limits both the growth of fern populations and the colonization of new habitats. In fact, reduced microtopographic variation in post-agricultural forests may represent a greater hindrance to plant establishment than changes in mean environmental conditions. Among the three fern species, establishment rates differed as species distributions would predict, with the strongest colonizer consistently having the highest rates and the slowest colonizer the lowest. Rather than random or trait-mediated dispersal, the different distributions of these species reflect life history traits that determine establishment rates and thus colonization ability. This case study demonstrates that ecological interactions based on the unique life histories of individual species can override dispersal in determining species distributions.     

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.     

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 role of environmental and spatial processes in structuring lake communities from bacteria to fish

We assessed the relative roles of local environmental conditions and dispersal on community structure in a landscape of lakes for the major trophic groups. We use taxonomic presence-absence and abundance data for bacteria, phytoplankton, zooplankton, and fish from 18 lakes in southern Quebec, Canada. The question of interest was whether communities composed of organisms with more limited dispersal abilities, because of size and life history (zooplankton and fish) would show a different effect of lake distribution than communities composed of good dispersers (bacteria and phytoplankton). We examine the variation in structure attributable to local environmental (i.e., lake chemical and physical variables) vs. dispersal predictors (i.e., overland and watercourse distances between lakes) using variation partitioning techniques. Overall, we show that less motile species (crustacean zooplankton and fish) are better predicted by spatial factors than by local environmental ones. Furthermore, we show that for zooplankton abundances, both overland and watercourse dispersal pathways are equally strong, though they may select for different components of the community, while for fish, only watercourses are relevant dispersal pathways. These results suggest that crustacean zooplankton and fish are more constrained by dispersal and therefore more likely to operate as a metacommunity than are bacteria and phytoplankton within this studied landscape.     

Dispersal Can Limit Local Plant Distribution

The ability of species to establish new populations at unoccupied sites is a critical feature in the maintenance of biological diversity, and it has taken on new importance as a result of global climate change and expected changes in species distribution. To examine the dispersal potential of plant species, seeds of four annual plant species were experimentally dispersed 40 to 600 m from existing populations in Massachusetts (U.S.A.) to 34 nearby unoccupied but apparently suitable sites. At three of these sites new populations were established that persisted for four generations and expanded slowly in area. At seven sites, a small initial population eventually died out. At the 24 other sites, new populations did not become established, indicating that the sites were in some way unsuitable, that not enough seeds arrived, or that conditions suitable for seed germination do not occur every year. These results suggest that some species may be unable to disperse naturally out of their existing ranges in response to global climate change, particularly if habitat fragmentation creates barriers to dispersal. These species may have to be assisted to reach suitable sites nearby to prevent their extinction in the wild.     

Dispersal limitation and environmental heterogeneity shape scale-dependent diversity patterns in plant communities

Understanding the large-scale distribution of species diversity requires distinguishing two of the primary factors that cause compositional differences: dispersal limitation and environmental variation. In a community with a naturally discontinuous spatial structure, we asked (1) at what scale(s) nonrandom variation in species composition occurs and (2) at what scale(s) such variation is associated with spatial separation, indicative of dispersal limitation, and at what scale(s) variation is associated with environmental heterogeneity? We sampled 50 seeps (small wetlands) on five serpentine outcrops. Using a randomization model, we showed that additive beta diversity (a measure of community dissimilarity) was lower than random within seeps and higher than random among both seeps and outcrops. Using Mantel tests, we showed that plant community dissimilarity, in both the full seep assemblage as well as in a subset of seep endemics, at the two larger scales was associated with different forms of environmental heterogeneity and, at the largest scale, was also associated with geographic distance. We conclude that diversity in this system is shaped by multiple scales of heterogeneity and by dispersal limitation at the largest scale.     

Simulation of the Effect of Spatial and Temporal Variation in Fire Regimes on the Population Viability of a Banksia Species

Populations of plants that rely on seeds for recovery from disturbance by fire (obligate seeders) are sensitive to regimes of frequent fire. Obligate seeders are prominent in fire-prone heathlands of southern Australia and South Africa. Population extinction may occur if there are successive fires during a plant's juvenile period. Research on the population biology of obligate seeders has influenced the management of fire in these heath and shrublands, but work on the effects of the spatial variability of fires is lacking. We hypothesize that extinction maybe avoided under an adverse fire frequency if fires are patchy. We present a model that simulates the effects of spatial and temporal variations in fire regimes on the viability of a plant population in a grid landscape. Seedling establishment, maturation, senescence, and seed dispersal determine the presence or absence of plants in each cell. We used values typical of serotinous Banksia species to estimate probability of extinction in relation to fire frequency and size. We examined the sensitivity of predictions to dispersal, senescence, fire frequency, spatial burning pattern and size variance, and the size of the grid. Simulations 200 years in length indicated that extinction probability was lowest when mean fire frequency was intermediate and mean fire size was large. When fire frequency was high, extinction probability was high irrespective of fire size. Senescence was more important than high-frequency fire as a cause of extinction in cells. Interactions between dispersal, fire frequency, and size were complex, indicating that extinction is governed by intercell connectivity. The model indicates that fire patchiness cannot be assumed to ensure avoidance of extinction of populations. Conservation of populations is most likely when fire patchiness is relatively low—when the size of fires is moderate to large and when burned patches are contiguous.     

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.     

Multiple socioecological factors influence timing of natal dispersal in kangaroo rats

Natal dispersal is an important event in the life history of many species. Timing of natal dispersal can influence survivorship and subsequent reproductive success. A variety of individual proximal factors determine if and when offspring disperse from the natal territory by influencing the costs of dispersing and the benefits of delaying dispersal. I examined the influence of multiple factors on dispersal age in the banner-tailed kangaroo rat (Dipodomys spectabilis), a solitary species lacking extreme sex-biased dispersal. I used an information theoretic approach to compare Cox proportional hazards regression models of dispersal age for 121 offspring over a 3-year period consisting of low and high population densities. The top-ranked models indicated that dispersal age was influenced by a combination of socioecological factors related to resource competition, environmental conditions, kin competition, and a lesser extent sex. Circumstances that likely reduced the probability of successful dispersal such as intense resource competition at high population density and being born earlier in the breeding season when environmental conditions were poor lead to longer delays in natal dispersal. Offspring in larger litters also dispersed earlier possibly to avoid competition with kin. Sex was weakly supported in top models but may only influence dispersal age at high population densities. These results suggest that the proximal factors that trigger dispersal are influenced by a combination of multiple effects related to the costs of dispersing and the benefits of remaining at home, even in species that do not form long-term social groups or have extreme sex-biased dispersal.     

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.     

Extinction Dynamics in the American Marten (Martes americana)

We constructed a model of marten population dynamics and used it to investigate extinction processes across a wide range of parameter values. The model was based on rules governing the behavior and physiology of individual martens and focused on energy balance. Spatial dynamics and demographic and environmental stochasticity were incorporated. The outcome was the probability of extinction and quasiextinction (20 females remaining) over 500 years. Three qualitative forms of extinction were delineated. The first was deterministic extinction, associated with those parameter combinations leading to a negative population growth rate. The second was probabilistic extinction in systems with a strong positive growth rate but restricted population size due to habitat constraint. The transition from 100% persistence to 100% quasiextinction, as the input habitat size was decreased, was abrupt. The final form of extinction was in systems with a growth rate of approximately zero. Prey availability maintained an upper limit on these populations, but otherwise fluctuations in population size were essentially random, leading to nontrivial probabilities of extinction in even relatively large populations. A number of issues requiring further empirical research were identified. These included the relationship between habitat quality and marten reproduction, dispersal patterns and dispersal mortality, the effect of habitat edge on marten reproduction and mortality, and the characterization of the severity and frequency of catastrophic mortality as experienced by marten populations.     

Erosion of Heterozygosity in Fluctuating Populations

Abstract: Demographic, environmental, and genetic stochasticity threaten the persistence of isolated populations. The relative importance of these intertwining factors remains unresolved, but a common view is that random demographic and environmental events will usually drive small populations to the brink of extinction before genetic deterioration poses a serious threat. To evaluate the potential importance of genetic factors, we analyzed a model linking demographic and environmental conditions to the loss of genetic diversity in isolated populations undergoing natural levels of fluctuation. Nongenetic processes—environmental stochasticity and population demography—were modeled according to a bounded diffusion process. Genetic processes were modeled by quantifying the rate of drift according to the effective population size, which was predicted from the same parameters used to describe the nongenetic processes. We combined these models to predict the heterozygosity remaining at the time of extinction, as predicted by the nongenetic portion of the model. Our model predicts that many populations will lose most or all of their neutral genetic diversity before nongenetic random events lead to extinction. Given the abundant evidence for inbreeding depression and recent evidence for elevated extinction rates of inbred populations, our findings suggest that inbreeding may be a greater general threat to population persistence than is generally recognized. Therefore, conservation biologists should not ignore the genetic component of extinction risk when assessing species endangerment and developing recovery plans.     

Sink or swim? Copepod population maintenance in the Columbia River estuarine turbidity-maxima region

Maintenance of estuarine zooplankton populations in large river-dominated estuaries with short residence times has been an intriguing subject of investigation. During three different hydrological seasons, autumn 1990, summer 1991, and spring 1992, we intensively sampled zooplankton populations in the estuarine turbidity maxima (ETM) region of the Columbia River estuary of Oregon and Washington, USA. One of the principal objectives was to investigate retention mechanisms of the predominant zooplankton species, the harpacticoid copepod Coullana canadensis and the epibenthic calanoid copepod Eurytemora affinis. In the ETM, C. canadensis densities mirrored those of turbidity gradients and were almost always greater at the river bed, while E. affinis densities were greater higher in the water column during the flood and lower in the water column during the ebb. Cross-correlation and time-series analyses determined that C. canadensis densities were highly positively correlated with turbidity and that most of the variability was explained by the lunisolar diurnal (K₁) and principal lunar (M₂) tidal components occurring once every 23.93  h and once every 12.42 h, respectively. This indicates that C. canadensis populations are most probably maintained in the estuary through the same near-bottom circulation features that trap and concentrate particles in the ETM. In contrast, densities of the more motile species E. affinis were highly correlated with negative velocities, or ebb tide, and most of the variability in population densities could be explained by the principal lunar tidal component; therefore, we hypothesize that this species is probably vertically migrating on a tidal cycle into different flow layers to avoid population losses out of the estuary. Received: 7 April 1997 / Accepted: 22 April 1997