Dangerously few liaisons: a review of mate-finding Allee effects

In this paper, we review mate-finding Allee effects from ecological and evolutionary points of view. We define ‘mate-finding’ as mate searching in mobile animals, and also as the meeting of gametes for sessile animals and plants (pollination). We consider related issues such as mate quality and choice, sperm limitation and physiological stimulation of reproduction by conspecifics, as well as discussing the role of demographic stochasticity in generating mate-finding Allee effects. We consider the role of component Allee effects due to mate-finding in generating demographic Allee effects (at the population level). Compelling evidence for demographic Allee effects due to mate-finding (as well as via other mechanisms) is still limited, due to difficulties in censusing rare populations or a failure to identify underlying mechanisms, but also because of fitness trade-offs, population spatial structure and metapopulation dynamics, and because the strength of component Allee effects may vary in time and space. Mate-finding Allee effects act on individual fitness and are thus susceptible to change via natural selection. We believe it is useful to distinguish two routes by which evolution can act to mitigate mate-finding Allee effects. The first is evolution of characteristics such as calls, pheromones, hermaphroditism, etc. which make mate-finding more efficient at low density, thus eliminating the Allee effect. Such adaptations are very abundant in the natural world, and may have arisen to avoid Allee effects, although other hypotheses are also possible. The second route is to avoid low density via adaptations such as permanent or periodic aggregation. In this case, the Allee effect is still present, but its effects are avoided. These two strategies may have different consequences in a world where many populations are being artificially reduced to low density: in the first case, population growth rate can be maintained, while in the second case, the mechanism to avoid Allee effects has been destroyed. It is therefore in these latter populations that we predict the greatest evidence for mate-finding Allee effects and associated demographic consequences. This idea is supported by the existing empirical evidence for demographic Allee effects. Given a strong effect that mate-finding appears to have on individual fitness, we support the continuing quest to find connections between component mate-finding Allee effects (individual reproductive fitness) and the demographic consequences. There are many reasons why such studies are difficult, but it is important, particularly given the increasing number of populations and species of conservation concern, that the ecological community understands more about how widespread demographic Allee effects really are, and why.     

Effects of size on predation risk,behavioural response to fish,and cost of reduced feeding in larval Ischnura verticalis (Coenagrionidae: Odonata)

Summary We used laboratory studies to examine the role of predation risk and cost of anti-predator behaviour in determining the behavioural response of several larval instars of Ischnura verticalis to a fish predator (Lepomis gibbosus). Smaller larvae were less susceptible to fish predation than larger larvae. Smaller larvae depressed movement to a greater degree in the presence of fish than did larger larvae; large larvae were generally less active than small larvae regardless of fish presence. Reduced feeding resulted in smaller larvae suffering more in terms of reduced growth than did large larvae. In general, our results tend to support the hypothesis that individuals that suffer high costs of anti-predator behaviour but little risk of predation may only exhibit anti-predator behaviours in the presence of predators, whereas individuals with a higher risk of predation and a lower cost of anti-predator behaviour may evolve anti-predator mechanisms that are in effect even in the absence of predators.     

Trade-off between resource seasonality and predation risk explains reproductive chronology in impala

We investigated the variation in birth synchrony displayed by impala Aepyceros melampus populations across their distribution from southern to eastern Africa. Our analysis was based on field data from Chobe National Park in Botswana and Mala Mala Private Game Reserve in South Africa (4 and 13 years of monitoring, respectively). We compared our results with those from other studies conducted across the impala species range. Impala lambing was highly synchronized in Chobe with 90% of lambs born within 2 weeks in mid-November. Variation in rainfall in the preceding wet season explained 74% of variation in the dates of the first lamb observation in Mala Mala. In Chobe, the earliest birth peak occurred after the highest rainfall and the body condition of lambs in that cohort was also best for both males and females. No association was found between the lunar cycle and the estimated onset of the conception period, despite previous studies having found an association between the lunar cycle and the rutting behaviour in males. On a regional scale, impalas in areas with a marked dry season (several months with no rain) tend to synchronize births with the onset of the rains, when grass quality is highest. Number of months with rain explained 78% of the regional variation in birth synchrony. Neither latitude nor total rainfall contributed significantly to a stepwise multiple regression model. These data support the theory that impalas synchronize births in areas with a highly seasonal food supply, and temporally space births in less seasonal (equatorial) areas to reduce predation risks.     

Allee effects, mating systems and the extinction risk in populations with two sexes

The Allee effect is one of the population consequences of sexual reproduction that has received increased attention in recent years. Due to its impact on small population dynamics, it is commonly accepted that Allee effects should render populations more extinction prone. In particular, monogamous species are considered more susceptible to the Allee effect and hence, more extinction prone, than polygamous species. Although this hypothesis has received theoretical support, there is little empirical evidence. In this study, we investigate (1) how variation in tertiary sex ratio affects the presence and intensity of the Allee effect induced by mating system, as well as (2) how this effect contributes to extinction risk. In contrast with previous predictions, we show that all mating systems are likely to experience a strong Allee effect when the operational sex ratio (OSR) is balanced. This strong Allee effect does not imply being exceptionally extinction prone because it is associated with an OSR that result in a relatively small extinction risk. As a consequence, the impact of Allee effects on overall extinction risk is buffered. Moreover, the OSR of natural populations appears to be often male biased, thus making it unlikely that they will suffer from an Allee effect induced by mating system.     

Trade-off between mating and predation risk in the marine snail, Littorina plena

Abstract. We investigated the hypothesis that predation risk affects mating decisions in the intertidal snail Littorina plena in Bamfield Inlet, Northeast Pacific. First, we conducted a field tethering experiment to test the assumption that mating pairs of snails are more susceptible to predation than solitary individuals, and then performed a laboratory experiment to quantify the effect of predation threat on the propensity of snails to form mating pairs. Our results support the hypothesis, in that "mating pairs" were more frequently killed than single snails in the field, and snails were less likely to form mating pairs in the laboratory when simulated predation risk was high (chemical cues from crushed conspecifics were added to the water) than when it was low (no risk cues were added to the water). In contrast to several earlier studies, we found no effect of individual size on snail susceptibility to predation, perhaps because our two size classes were contiguous and snails within them were not dissimilar enough. The results of the behavioral experiment were consistent with this lack of individual size effect on snail vulnerability; both size classes of snails showed a significant and similar tendency to decrease mating when predation risk was high. Taken together, the results of this and recent studies indicate that predators can considerably affect the behavior of littorinid snails, including their movement patterns, feeding, and reproduction. We argue that greater consideration should be given to how marine invertebrates trade off predation risk and activities related to reproduction.     

Habitat destruction and the extinction debt revisited: The Allee effect

Habitat destruction, often caused by anthropogenic disturbance, can lead to the extinction of species at an unprecedented rate. It is important, therefore, to consider habitat destruction when assessing population viability. Another factor often ignored in population viability analysis, is the Allee effect that adds to the risk of populations already on the verge of extinction. Understanding the Allee effect on species dynamics and response to habitat destruction has intrinsic value in conservation prioritization. Here, the Allee effect was considered in a multi-species hierarchical competition model. Results showed that species persistence declines dramatically due to the Allee effect, and certain species become more susceptible to habitat destruction than others. Two extinction orders emerged under habitat destruction: either the best competitor becomes extinct first or the best colonizer first. The extinction debt and order, as well as the time lag between habitat destruction and species extinction, were found to be determined by species abundance and the intensity of the Allee effect.     

Predicting extinctions: interspecific competition,predation and population variability in experimental Daphnia populations

We examine how interspecific competition and two types of size-selective predation affect population density, variability and persistence in laboratory cultures of two species of Daphnia, D. magna and D. longispina. When both species were analysed together, and for D. longispina alone, there were weak negative relationships between mean population density and population variability. Interspecific competition resulted in lower population densities and higher population variability. Extinct populations had lower densities and were also more variable than persisting ones. There was still an effect of population variability on extinction probability after the effect of density on population variability had been accounted for. Hence, the effects of population density and variability on population persistence were partly independent of each other. The effects of size-selective predation on population persistence were more species-specific and not directly related to density or variability. Since the effects of species interactions on persistence were large, we suggest that it is likely that population vulnerability analyses not incorporating effects of interspecific interactions are often misleading.     

Variation in Allee effects: evidence,unknowns, and directions forward

Allee effects, positive effects of population size or density on per-capita fitness, are of broad interest in ecology and conservation due to their importance to the persistence of small populations and to range boundary dynamics. A number of recent studies have highlighted the importance of spatiotemporal variation in Allee effects and the resulting impacts on population dynamics. These advances challenge conventional understanding of Allee effects by reframing them as a dynamic factor affecting populations instead of a static condition. First, we synthesize evidence for variation in Allee effects and highlight potential mechanisms. Second, we emphasize the “Allee slope,” i.e., the magnitude of the positive effect of density on the per-capita growth rate, as a metric for demographic Allee effects. The more commonly used quantitative metric, the Allee threshold, provides only a partial picture of the underlying forces acting on population growth despite its implications for population extinction. Third, we identify remaining unknowns and strategies for addressing them. Outstanding questions about variation in Allee effects fall broadly under three categories: (1) characterizing patterns of natural variability; (2) understanding mechanisms of variation; and (3) implications for populations, including applications to conservation and management. Future insights are best achieved through robust interactions between theory and empiricism, especially through mechanistic models. Understanding spatiotemporal variation in the demographic processes contributing to the dynamics of small populations is a critical step in the advancement of population ecology.     

Environmental variation and the predator-specific responses of tropical stream insects: effects of temperature and predation on survival and development of Australian Chironomidae (Diptera)

The threat posed by predation varies among predator species and with environmental context, and prey species often adjust their responses accordingly. We investigated such effects within an insect assemblage from a tropical Australian stream. These systems are frequently subjected to catastrophic floods, often suggested to reduce the importance of predation in streams, and invertebrate faunas are characterised by relatively broad environmental tolerances. Impacts of the hunting predator Australopelopia prionoptera (Diptera: Chironomidae) and an undescribed ambush predator from the Polycentropodidae (Trichoptera) on survival and development of two species of tubicolous Chironomidae, Echinocladius martini (Orthocladiinae) and Polypedilum australotropicus (Chironominae), were assessed in laboratory microcosms. A further experiment investigated how impacts of Australopelopia varied over a broad range of temperatures, exceeding that experienced annually by the studied populations. Neither predator impacted survivorship for E. martini, but the presence of the polycentropodid caused E. martini to spend longer as larvae and reduced adult longevity, and adult females were smaller-sized and had smaller oocytes. In contrast, both predators reduced survivorship of P. australotropicus, but only Australopelopia affected its development, causing reductions in pupal duration and oocyte size. The observed non-lethal impacts of predation reflect the threat each predator is known to pose to each prey species in situ. Impacts of predation varied little with temperature, reflecting the broad thermal tolerances of all study species. The predator-specific responses of the prey species imply that predation is a significant selective force in tropical Australian streams, although fluctuation in intensity of predation associated with flooding may limit its importance for community structure and prey diversity at larger scales. Our results indicate a more limited scope for environmental modification of predator–prey relationships in faunas characterised by broad physiological tolerances.     

Vigilance in Przewalski's gazelle: effects of sex, predation risk and group size

Vigilance in social animals is often aimed at detecting predators. Many social and environmental factors influence vigilance, including sex, predation risk and group size. During the summer of 2007, we studied Przewalski's gazelle Procapra przewalskii , an endemic ungulate to the Qinghai-Tibet Plateau, to test whether and how these three factors affect vigilance. We distinguished groups consisting of males, mothers with lambs and females without lambs making observations on groups in the presence or absence of nearby predators. We assessed the group-size effect on vigilance and how this varied with levels of predation risk and sex. Males and mothers scanned longer and with a higher frequency than females without lambs. Individuals were more vigilant under direct predation threat. Although vigilance generally decreased with group size, the extent of the decrease was independent of predation risk and was not significant in males. The results suggest that mothers are more vigilant suggesting greater vulnerability and that males may have increased their vigilance to compete for higher social ranks. The positive correlation between vigilance and predation risk and the negative correlation between vigilance and group size are consistent with earlier findings, but we failed to find an interaction between group size and predation risk on vigilance perhaps because vigilance levels are low even in small groups, thus making similar vigilant upward adjustments in both small and large groups.     

Population growth and predation interference between two species of predatory phytoseiid mites (Acarina: Phytoseiidae) in interactive systems

Summary Populations of two species of phytoseiid mite predators, Phytoseiulus persimilis Athias-Henriot and Amblyseius degenerans (Berlese), feeding on a tetranychid prey, Tetranychus pacificus McGregor, were allowed to grow separately as well as together on bush lima bean (Phaseolus lunatus Var.) arenas in the laboratory. The population plateau attained by P. persimilis was nearly 5 times higher than that for A. degenerans when each species was on separate leaf arenas. When they were on the same arena, P. persimilis was outcompeted by A. degenerans after about 70 days of population growth. When dispersal to other arenas was necessary for the predators to find prey in another experiment, P. persimilis survived well but not A. degenerans. The mechanisms underlying species displacement were explored further. The differential mortality of immature predators at different developmental stages due to interspecific predation was concluded to be responsible for the population decline of P. persimilis, and the decline of A. degenerans in another experiment was attributed to its sedentary tendency regardless of prey distribution and to the lack of alternative food sources in the system. The implications to biological control of mutual predation between predator species is discussed briefly.     

Extinction risk assessments at the population and species level: implications for amphibian conservation

Amphibian populations are declining worldwide and this is causing growing concern. High levels of population declines followed by the expansion of red lists are creating demands for effective strategies to maximize conservation efforts for amphibians. Ideally, integrated and comprehensive strategies should be based on complementary information of population and species extinction risk. Here we evaluate the congruence between amphibian extinction risk assessments at the population level (Declining Amphibian Database––DAPTF) and at species level (GAA––IUCN Red List). We used the Declining Amphibian Database––DAPTF that covers 967 time-series records of amphibian population declines assigned into four levels of declines. We assigned each of its corresponding species into GAA––IUCN red list status, discriminated each species developmental mode, and obtained their geographic range size as well. Extinction risk assessments at the population and species level do not fully coincide across geographic realms or countries. In Paleartic, Neartic and Indo-Malayan realms less than 25% of species with reported population declines are formally classified as threatened. In contrast, more than 60% of all species with reported population declines that occur in Australasia and the Neotropics are indeed threatened according to the GAA––IUCN Red List. Species with aquatic development presented proportionally higher extinction risks at both population and species level than those with terrestrial development, being this pattern more prominent at Australasia, Paleartic, and Neartic realms. Central American countries, Venezuela, Mexico and Australia presented the highest congruence between both population and species risk. We address that amphibian conservation strategies could be improved by using complementary information on time-series population trends and species threat. Whenever feasible, conservation assessments should also include life-history traits in order to improve its effectiveness.     

How predator functional responses and Allee effects in prey affect the paradox of enrichment and population collapses

In Rosenzweig-MacArthur models of predator-prey dynamics, Allee effects in prey usually destabilize interior equilibria and can suppress or enhance limit cycles typical of the paradox of enrichment. We re-evaluate these conclusions through a complete classification of a wide range of Allee effects in prey and predator's functional response shapes. We show that abrupt and deterministic system collapses not preceded by fluctuating predator-prey dynamics occur for sufficiently steep type III functional responses and strong Allee effects (with unstable lower equilibrium in prey dynamics). This phenomenon arises as type III functional responses greatly reduce cyclic dynamics and strong Allee effects promote deterministic collapses. These collapses occur with decreasing predator mortality and/or increasing susceptibility of the prey to fall below the threshold Allee density (e.g. due to increased carrying capacity or the Allee threshold itself). On the other hand, weak Allee effects (without unstable equilibrium in prey dynamics) enlarge the range of carrying capacities for which the cycles occur if predators exhibit decelerating functional responses. We discuss the results in the light of conservation strategies, eradication of alien species, and successful introduction of biocontrol agents.     

Scaring Nemo: Contrasting effects of observer presence on two anemonefish species

Behaviours of Clark's anemonefish Amphiprion clarkii and the dusky anemonefish Amphiprion melanopus were studied in Vanuatu. Six anemones and their resident fish were observed for typical behaviours (hiding, watching, roaming, inter-, and intraspecific behaviour) with and without the presence of a snorkelling observer. Observer presence had significant but contrasting effects on hiding behaviour in A. clarkii and A. melanopus. Bolder anemonefish species may be able to outcompete other species in areas with high human presence.     

Behavioural activity levels and expression of stress proteins under predation risk in two damselfly species

Abstract 1. It has become apparent that predators may strongly decrease prey fitness without direct contact with the prey, as they induce the development of defence systems that limit the availability of energy for growth and reproduction. Recent studies suggest that stress proteins may help prey organisms deal with this stress. The pattern is not general, however, and little is known about species differences in physiological traits in coping with predator stress, and covariation of physiological with other antipredator traits. 2. To explore these issues, we quantified levels of constitutive and fish‐induced stress proteins (Hsp60 and Hsp70) and anti‐predator behaviours in larvae of two damselfly species that differ in lifestyle. Both stress proteins were fixed at higher levels in Erythromma najas, which has a slow lifestyle, than in Lestes sponsa, which has a fast lifestyle. Similarly, anti‐predator behaviours were fixed at safer levels in E. najas than in L. sponsa. 3. These results suggest that stress proteins may be part of anti‐predator syndromes of damselfly larvae, and there may be trait co‐specialisation between stress proteins and behavioural anti‐predator traits. Studies formally testing these hypotheses in more species may prove rewarding in advancing our understanding of the functional integration of physiological anti‐predator traits in relation to the prey’s lifestyle.     

Variation in predation risk and vole feeding behaviour: a field test of the risk allocation hypothesis

Many prey animals experience temporal variation in the risk of predation and therefore face the problem of allocating their time between antipredator efforts and other activities like feeding and breeding. We investigated time allocation of prey animals that balanced predation risk and feeding opportunities. The predation risk allocation hypothesis predicts that animals should forage more in low- than in high-risk situations and that this difference should increase with an increasing attack ratio (i.e. difference between low- and high-risk situations) and proportion of time spent at high risk. To test these predictions we conducted a field test using bank voles (Clethrionomys glareolus) as a prey and the least weasel (Mustela nivalis nivalis) as a predator. The temporal pattern and intensity of predation risk were manipulated in large outdoor enclosures and the foraging effort and patch use of voles were measured by recording giving-up densities. We did not observe any variation in feeding effort due to changes in the level of risk or the proportion of time spent under high-risk conditions. The only significant effect was found when the attack ratio was altered: the foraging effort of voles was higher in the treatment with a low attack ratio than in the treatment with a high attack ratio. Thus the results did not support the predation risk allocation hypothesis and we question the applicability of the hypothesis to our study system. We argue that the deviation between the observed pattern of feeding behaviour of bank voles and that predicted by the predation risk allocation hypothesis was mostly due to the inability of voles to accurately assess the changes in the level of risk. However, we also emphasise the difficulties of testing hypotheses under outdoor conditions and with mammals capable of flexible behavioural patterns.     

Allee effects and population regulation: a test for biotic resistance against an invasive leafroller by resident parasitoids

Resident natural enemies can impact invasive species by causing Allee effects, leading to a reduction in establishment success of small founder populations, or by regulating or merely suppressing the abundance of established populations. Epiphyas postvittana, the Light Brown Apple Moth, an invasive leafroller in California, has been found to be attacked by a large assemblage of resident parasitoids that cause relatively high rates of parasitism. Over a 4-year period, we measured the abundance and per capita growth rates of four E. postvittana populations in California and determined parasitism rates. We found that at two of the sites, parasitism caused a component Allee effect, a reduction in individual survivorship at lower E. postvittana population densities, although it did not translate into a demographic Allee effect, an impact on per capita population growth rates at low densities. Instead, E. postvittana populations at all four sites exhibited strong compensatory density feedback throughout the entire range of densities observed at each site. As we found no evidence for a negative relationship between per capita population growth rates and parasitism rates, we concluded that resident parasitoids were unable to regulate E. postvittana populations in California. Despite a lack of evidence for regulation or a demographic Allee effect, the impact of resident parasitoids on E. postvittana populations is substantial and demonstrates significant biotic resistance against this new invader.     

Specialist versus generalist parasites: the interactions between host diversity,environment and geographic barriers in avian malaria

The specialist versus generalist strategies of hemoparasites in relation to their avian host, as well as environmental factors, can influence their prevalence, diversity and distribution. In this paper we investigated the influence of avian host species, as well as the environmental and geographical factors, on the strategies of Haemoproteus and Plasmodium hemoparasites. We determined prevalence and diversity by targeting their cytochrome b (Cytb) in a total of 2,590 passerine samples from 138 localities of Central and South America, and analysed biogeographic patterns and host-parasite relationships. We found a total prevalence of 23.2%. Haemoproteus presented a higher prevalence (15.3%) than Plasmodium (4.3%), as well as a higher diversity and host specificity. We determined that Plasmodium and Haemoproteus prevalences correlated positively with host diversity (Shannon index) and were significantly influenced by bird diversity, demonstrating a possible “amplification effect”. We found an effect of locality and the avian family for prevalences of Haemoproteus and Plasmodium. These results suggest that Haemoproteus is more specialist than Plasmodium and could be mostly influenced by its avian host and the Andes Mountains.     

Pushed beyond the brink: Allee effects,environmental stochasticity,and extinction

To understand the interplay between environmental stochasticity and Allee effects, we analyse persistence, asymptotic extinction, and conditional persistence for stochastic difference equations. Our analysis reveals that persistence requires that the geometric mean of fitness at low densities is greater than one. When this geometric mean is less than one, asymptotic extinction occurs with high probability for low initial population densities. Additionally, if the population only experiences positive density-dependent feedbacks, conditional persistence occurs provided the geometric mean of fitness at high population densities is greater than one. However, if the population experiences both positive and negative density-dependent feedbacks, conditional persistence only occurs if environmental fluctuations are sufficiently small. We illustrate counter-intuitively that environmental fluctuations can increase the probability of persistence when populations are initially at low densities, and can cause asymptotic extinction of populations experiencing intermediate predation rates despite conditional persistence occurring at higher predation rates.