Pollen limitation and Allee effect related to population size and sex ratio in the endangered Ottelia acuminata (Hydrocharitaceae): implications for conservation and reintroduction

Small populations may suffer more severe pollen limitation and result in Allee effects. Sex ratio may also affect pollination and reproduction success in dioecious species, which is always overlooked when performing conservation and reintroduction tasks. In this study, we investigated whether and how population size and sex ratio affected pollen limitation and reproduction in the endangered Ottelia acuminata, a dioecious submerged species. We established experimental plots with increasing population size and male sex ratio. We observed insect visitation, estimated pollen limitation by hand‐pollinations and counted fruit set and seed production per fruit. Fruit set and seed production decreased significantly in small populations due to pollinator scarcity and thus suffered more severe pollen limitation. Although frequently visited, female‐biased larger populations also suffered severe pollen limitation due to few effective visits and insufficient pollen availability. Rising male ratio enhanced pollination service and hence reproduction. Unexpectedly, pollinator preferences did not cause reduced reproduction in male‐biased populations because of high pollen availability. However, reproductive outputs showed more variability in severe male‐biased populations. Our results revealed two component Allee effects in fruit set and seed production, mediated by pollen limitation in O. acuminata. Moreover, reproduction decreased significantly in larger female‐biased populations, increasing the risk of an Allee effect.     

REPLICATED ORIGIN OF FEMALE‐BIASED ADULT SEX RATIO IN INTRODUCED POPULATIONS OF THE TRINIDADIAN GUPPY (POECILIA RETICULATA)

There are many theoretical and empirical studies explaining variation in offspring sex ratio but relatively few that explain variation in adult sex ratio. Adult sex ratios are important because biased sex ratios can be a driver of sexual selection and will reduce effective population size, affecting population persistence and shapes how populations respond to natural selection. Previous work on guppies (Poecilia reticulata) gives mixed results, usually showing a female‐biased adult sex ratio. However, a detailed analysis showed that this bias varied dramatically throughout a year and with no consistent sex bias. We used a mark‐recapture approach to examine the origin and consistency of female‐biased sex ratio in four replicated introductions. We show that female‐biased sex ratio arises predictably and is a consequence of higher male mortality and longer female life spans with little effect of offspring sex ratio. Inconsistencies with previous studies are likely due to sampling methods and sampling design, which should be less of an issue with mark‐recapture techniques. Together with other long‐term mark‐recapture studies, our study suggests that bias in offspring sex ratio rarely contributes to adult sex ratio in vertebrates. Rather, sex differences in adult survival rates and longevity determine vertebrate adult sex ratio.     

Ecological basis of heterochrony in early-ontogenesis gonad development in different races of Kura sturgeon (Acipenser guldenstadti persicus Borodin)

Early germ cell development in Persian sturgeon appears to be faster in the marine environment than in aquaculture conditions. Adaptation plasticity differs significantly for gonad formation and sex determination in the sturgeon fry and depends to differing extents on the temperature. The sturgeon gonads are more sensitive to low temperatures on the early stages of sex determination than in the period of gonad formation; the differences between sexes are preconditioned by the earlier start of sex determination in females when compared to males. The rates of the early gonad and germ cell development in sturgeon are conditioned by its reproduction season. In the population of the late spring race, the delay in both early sex determination and germ cell development stays even for the ages of 1+, 2+, and 3+ when compared to the population of the early spring race. The biophysiological quality of parents is transmitted to their offspring.     

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.     

Effect of paternal age on the birth sex ratio in captive populations of aye‐aye (Daubentonia madagascariensis (Gmelin))

For the management of captive populations of zoo animals, it is important to elucidate factors that affect the offspring birth sex ratio. On the basis of the sex allocation theory, the Trivers–Willard and mate attractive/quality hypotheses predict that maternal and paternal conditions affect offspring birth sex ratios. We examined these predictions for the birth sex ratio of aye‐aye Daubentonia madagascariensis (Gmelin) by analyzing the pedigree information in the International Studbook. We found that the birth sex ratio of the aye‐aye was affected by the paternal age, but not maternal age and other environmental factors (birth year, season, and institution). The younger the sire, the more the offspring sex ratio was biased toward males. These results are useful for the effective population management of captive aye‐aye and illustrated the usefulness of the sex allocation theory in the sex ratio management of zoo animals.     

Reproductive costs of mating with a sibling male: sperm depletion and multiple mating in Cephalonomia hyalinipennis

Polygynous parasitoid males may be limited by the amount of sperm they can transmit to females, which in turn may become sperm limited. In this study, I tested the effect of male mating history on copula duration, female fecundity, and offspring sex ratio, and the likelihood that females will have multiple mates, in the gregarious parasitoid Cephalonomia hyalinipennis Ashmead (Hymenoptera: Bethylidae: Epyrinae), a likely candidate for sperm depletion due to its local mate competition system. Males were eager to mate with the seven females presented in rapid succession. Copula duration did not differ with male mating history, but latency before a first mating was significantly longer than before consecutive matings. Male mating history had no bearing on female fecundity (number of offspring), but significantly influenced offspring sex ratio. The last female to mate with a given male produced significantly more male offspring than the first one, and eventually became sperm depleted. In contrast, the offspring sex ratio of first‐mated females was female biased, denoting a high degree of sex allocation control. Once‐mated females, whether sperm‐depleted or not, accepted a second mating after a period of oviposition. Sperm‐depleted females resumed production of fertilized eggs after a second mating. Young, recently mated females also accepted a second mating, but extended in‐copula courtship was observed. Carrying out multiple matings in this species thus seems to reduce the cost of being constrained to produce only haploid males after accepting copulation with a sperm‐depleted male. I discuss the reproductive fitness costs that females experience when mating solely with their sibling males and the reproductive fitness gain of males that persist in mating, even when almost sperm‐depleted. Behavioural observations support the hypothesis that females monitor their sperm stock. It is concluded that C. hyalinipennis is a species with a partial local mating system.     

Modelling the mating system of polar bears: a mechanistic approach to the Allee effect

Allee effects may render exploited animal populations extinction prone, but empirical data are often lacking to describe the circumstances leading to an Allee effect. Arbitrary assumptions regarding Allee effects could lead to erroneous management decisions so that predictive modelling approaches are needed that identify the circumstances leading to an Allee effect before such a scenario occurs. We present a predictive approach of Allee effects for polar bears where low population densities, an unpredictable habitat and harvest-depleted male populations result in infrequent mating encounters. We develop a mechanistic model for the polar bear mating system that predicts the proportion of fertilized females at the end of the mating season given population density and operational sex ratio. The model is parametrized using pairing data from Lancaster Sound, Canada, and describes the observed pairing dynamics well. Female mating success is shown to be a nonlinear function of the operational sex ratio, so that a sudden and rapid reproductive collapse could occur if males are severely depleted. The operational sex ratio where an Allee effect is expected is dependent on population density. We focus on the prediction of Allee effects in polar bears but our approach is also applicable to other species.     

Plant sex alters Allee effects in aggregating plant parasites

Species interactions are central to our understanding of population dynamics. While density typically strengthens competition, reducing absolute fitness, Allee effects can reverse this pattern, increasing fitness with density. Allee effects emerge in host–parasite systems when higher parasite densities dilute immune responses or increase resource‐mobilization. The optimal density of individuals in these systems should be influenced by how host quality alters the rates at which facilitative and competitive effects change across densities. We tested these ideas using sumac Rhus typhina and a gall‐forming parasite Melaphis rhois that attacks sumac leaves. Fitness peaked at intermediate densities, indicating an Allee effect, but the fitness peak depended on host sex. Patterns of abundance mirrored fitness patterns, with galls clustered on leaves and female hosts supporting greater numbers of galls. Within leaves, galls near the stem were more fit, and gall‐makers preferentially oviposited near to the stem. The patterns of fitness and abundance are consistent with Allee effects caused by increased resource mobilization at higher gall‐maker densities rather than diluted immune responses. Our results suggest that Allee effects in parasites can be described as the summative effects of competitive and facilitative processes and, because both are common, Allee effects are likely common in host–parasite systems.     

Does breeding population trajectory and age of nesting females influence disparate nestling sex ratios in two populations of Cooper's hawks?

Offspring sex ratios at the termination of parental care should theoretically be skewed toward the less expensive sex, which in most avian species would be females, the smaller gender. Among birds, however, raptors offer an unusual dynamic because they exhibit reversed size dimorphism with females being larger than males. And thus theory would predict a preponderance of male offspring. Results for raptors and birds in general have been varied although population‐level estimates of sex ratios in avian offspring are generally at unity. Adaptive adjustment of sex ratios in avian offspring is difficult to predict perhaps in part due to a lack of life‐history details and short‐term investigations that cannot account for precision or repeatability of sex ratios across time. We conducted a novel comparative study of sex ratios in nestling Cooper's hawks (Accipiter cooperii) in two study populations across breeding generations during 11 years in Wisconsin, 2001–2011. One breeding population recently colonized metropolitan Milwaukee and exhibited rapidly increasing population growth, while the ex‐Milwaukee breeding population was stable. Following life‐history trade‐off theory and our prediction regarding this socially monogamous species in which reversed sexual size dimorphism is extreme, first‐time breeding one‐year‐old, second‐year females in both study populations produced a preponderance of the smaller and cheaper sex, males, whereas ASY (after‐second‐year), ≥2‐year‐old females in Milwaukee produced a nestling sex ratio near unity and predictably therefore a greater proportion of females compared to ASY females in ex‐Milwaukee who produced a preponderance of males. Adjustment of sex ratios in both study populations occurred at conception. Life histories and selective pressures related to breeding population trajectory in two age cohorts of nesting female Cooper's hawk likely vary, and it is possible that these differences influenced the sex ratios we documented for two age cohorts of female Cooper's hawks in Wisconsin.     

French wasps in the New World: experimental biological control introductions reveal a demographic Allee effect

Many populations introduced into a novel environment fail to establish. One underlying process is the Allee effect, i.e., the difficulty of individuals to survive and reproduce when rare, and the consequently low or negative population growth. Although observations showing a positive relation between initial population size and establishment probability suggest that the Allee effect could be widespread in biological invasions, experimental tests are scarce. Here, we used a biological control program against Diuraphis noxia (Mordvilko) (Hemiptera: Aphididae) in the United States to manipulate initial population size of the introduced parasitoid Aphelinus asychis Walker (Hymenoptera: Aphelinidae) originating from France. For eight populations and three generations after introduction, we studied spatial distribution and spread, density, mate-finding, and population growth. Dispersal was lower in small populations during the first generation. Smaller initial population size nonetheless resulted in lower density during the three generations studied. The proportion of mated females and the population sex ratio were not affected by initial population size or population density. Net reproductive rate decreased with density within each generation, suggesting negative density-dependence. But for a given density, net reproductive rate was smaller in populations initiated with few individuals than in populations initiated with many individuals. Hence, our results demonstrate a demographic Allee effect. Mate-finding is excluded as an underlying mechanism, and other component Allee effects may have been overwhelmed by negative density-dependence in reproduction. Impact of generalist predators could provide one potential explanation for the relationship between initial population size and net reproductive rate. However, the continuing effect of initial population size on population growth suggests genetic processes may have been involved in the observed demographic Allee effect.     

Genetic structure,spatial organization,and dispersal in two populations of bat‐eared foxes

We incorporated radio‐telemetry data with genetic analysis of bat‐eared foxes (Otocyon megalotis) from individuals in 32 different groups to examine relatedness and spatial organization in two populations in South Africa that differed in density, home‐range sizes, and group sizes. Kin clustering occurred only for female dyads in the high‐density population. Relatedness was negatively correlated with distance only for female dyads in the high‐density population, and for male and mixed‐sex dyads in the low‐density population. Home‐range overlap of neighboring female dyads was significantly greater in the high compared to low‐density population, whereas overlap within other dyads was similar between populations. Amount of home‐range overlap between neighbors was positively correlated with genetic relatedness for all dyad‐site combinations, except for female and male dyads in the low‐density population. Foxes from all age and sex classes dispersed, although females (mostly adults) dispersed farther than males. Yearlings dispersed later in the high‐density population, and overall exhibited a male‐biased dispersal pattern. Our results indicated that genetic structure within populations of bat‐eared foxes was sex‐biased, and was interrelated to density and group sizes, as well as sex‐biases in philopatry and dispersal distances. We conclude that a combination of male‐biased dispersal rates, adult dispersals, and sex‐biased dispersal distances likely helped to facilitate inbreeding avoidance in this evolutionarily unique species of Canidae.     

Estimation of gonad volume, fecundity, and reproductive stage of shovelnose sturgeon using sonography and endoscopy with application to the endangered pallid sturgeon

Most species of sturgeon are declining in the Mississippi River Basin of North America including pallid (Scaphirhynchus albus F. and R.) and shovelnose sturgeons (S. platorynchus R.). Understanding the reproductive cycle of sturgeon in the Mississippi River Basin is important in evaluating the status and viability of sturgeon populations. We used non‐invasive, non‐lethal methods for examining internal reproductive organs of shovelnose and pallid sturgeon. We used an ultrasound to measure egg diameter, fecundity, and gonad volume; endoscope was used to visually examine the gonad. We found the ultrasound to accurately measure the gonad volume, but it underestimated egg diameter by 52%. After correcting for the measurement error, the ultrasound accurately measured the gonad volume but it was higher than the true gonad volume for stages I and II. The ultrasound underestimated the fecundity of shovelnose sturgeon by 5%. The ultrasound fecundity was lower than the true fecundity for stage III and during August. Using the endoscope, we viewed seven different egg color categories. Using a model selection procedure, the presence of four egg categories correctly predicted the reproductive stage ± one reproductive stage of shovelnose sturgeon 95% of the time. For pallid sturgeon, the ultrasound overestimated the density of eggs by 49% and the endoscope was able to view eggs in 50% of the pallid sturgeon. Individually, the ultrasound and endoscope can be used to assess certain reproductive characteristics in sturgeon. The use of both methods at the same time can be complementary depending on the parameter measured. These methods can be used to track gonad characteristics, including measuring Gonadosomatic Index in individuals and/or populations through time, which can be very useful when associating gonad characteristics with environmental spawning triggers or with repeated examinations of individual fish throughout the reproductive cycle.     

Sons do not take advantage of a head start: parity in herring gull offspring sex ratios despite greater initial investment in males

Skewed adult sex ratios sometimes occur in populations of free‐living animals yet the proximate mechanisms, timing of sex‐biases, and the selective agents contributing to skew remain a source of debate with contradictory evidence from different systems. We investigated potential mechanisms contributing to sex biases in a population of herring gulls with an apparent female skew in the adult population. Theory predicts that skewed adult sex ratios will adaptively lead to skewed offspring sex ratios to restore balance in the effective breeding population. Parents may also adaptively bias offspring sex ratios to increase their own fitness in response to environmental factors. Therefore, we expected to detect skewed sex ratios either at hatching or at fledging as parents invest differentially in offspring of different sexes. We sampled complete clutches (n = 336 chicks) at hatching to quantify potential skews in sex ratios by position in the hatch order, time of season, year, and nesting context (nest density), finding no departure from equal sex ratios at hatching related to any of these factors. Further, we sampled 258 chicks at near‐fledging to investigate potential sex biases in survival at the chick stage. Again, no biases in sex ratios were recorded. Male offspring were favored in this population via greater maternal investment in eggs carrying male embryos and greater parental provisioning of male offspring which reached greater sizes by fledging. Despite the advantages realized by male offspring, females were equally as likely to fledge as males. Thus, biased adult sex ratios apparently arise in the post‐fledging and pre‐recruitment stage in our population.     

Brood sex ratio varies with diet composition in a generalist raptor

While sex allocation has been investigated productively at both population and family levels, as yet no general theory has been developed that is capable of linking processes at these two ecological scales, and very few empirical studies have examined cross‐scale patterns. In Finnish northern goshawks (Accipiter gentilis), nestling sex ratio of local subpopulations is related to the spatial and temporal variation in the abundance of their principal avian prey, woodland grouse. Using data from an urban breeding population in Hamburg, Germany, I investigated: (1) whether brood sex ratio of goshawks varies with diet composition at the family level; (2) whether such variation could reflect adaptive adjustment; and (3) how family‐level allocation can drive population‐level patterns, such as those observed in Finland. Feral pigeons (Columba livia) were the most important prey species, with a pooled contribution to total diet of 36%. Brood sex ratio varied significantly with the proportion of pigeons in the breeding‐season diet of pairs (increasing male bias). However, there was no evidence for sex‐differential effects of diet composition, so it remains unclear whether the observed sex‐ratio variation was an adaptive response. As all study pairs inhabited an (urban) environment where pigeons were unusually abundant, family‐level sex‐ratio adjustment caused a marked male bias in offspring sex ratio at the population level (male‐biased nestling sex ratio in four of five years; pooled data: 60% males). This suggests that the large‐scale variation observed in Finnish goshawk populations mirrors sex‐ratio adjustment shown by individual families in response to small‐scale environmental conditions. Apart from linking patterns empirically across ecological scales, this study is, to my knowledge, the first to demonstrate that family‐level brood sex ratio varies with realized resource use (diet composition) in a raptor species. Previous studies either failed to find significant associations or, more commonly, violated theoretical assumptions by measuring environmental prey abundance (often integrated over large areas) rather than realized prey use of individual breeding pairs. I conducted a meta‐analysis of offspring sex‐ratio data from 17 goshawk populations across Europe to put my results into perspective. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 937–951.     

Offspring sex ratio and development are determined by copulation activity in Echinothrips americanus MORGAN 1913 (Thysanoptera: Thripidae)

The costs of parthenogenetic reproduction are more or less unknown in thrips. However, IPM strategies require an understanding of temporal and spatial life‐history variations and sex ratios. Hence, different circumstances with regard to mating and sperm storage, and their effects on the life history of the adults and progeny, were tested in Echinothrips americanus. Different conditions were investigated: (1) one female and one male with permanent access to each other, (2) one female and one male with limited access to each other, (3) one virgin male only, (4) one virgin female only and (5) two virgin females permanently associated. Mating or not mating has a significant effect on the longevity of females and males, and on female fecundity. As a result of tested condition (2), limited access has a positive effect on longevity of a male. On the other hand, permanent access (1) or no access to a female (3) leads to shorter longevity of a male. For a female with permanent access to a male (1), longevity and oviposition rate are reduced. In addition, test conditions of parents have a significant effect on developmental time of the offspring and their sex ratio. Compared to a female under condition (1), a female with limited access to a male (2) delivers offspring with a more male‐biased sex ratio, independent of the period of time after last male access. Concerning the time for development of the offspring, females under condition (2) and under condition (4) deliver an F1 generation with a shorter developmental time than those under condition (1). Therefore, E. americanus seems to have a feedback system, that is offspring in low male‐biased populations develop faster and generate an adapted sex ratio. Hence, the assumption of a lower infestation risk in arrhenotokous than in thelytokous parthenogenesis should be reconsidered.     

Synchrony's double edge: transient dynamics and the Allee effect in stage structured populations

In populations subject to positive density dependence, individuals can increase their fitness by synchronizing the timing of key life history events. However, phenological synchrony represents a perturbation from a population's stable stage structure and the ensuing transient dynamics create troughs of low abundance that can promote extinction. Using an ecophysiological model of a mass-attacking pest insect, we show that the effect of synchrony on local population persistence depends on population size and adult lifespan. Results are consistent with a strong empirical pattern of increased extinction risk with decreasing initial population size. Mortality factors such as predation on adults can also affect transient dynamics. Throughout the species range, the seasonal niche for persistence increases with the asynchrony of oviposition. Exposure to the Allee effect after establishment may be most likely at northern range limits, where cold winters tend to synchronize spring colonization, suggesting a role for transient dynamics in the determination of species distributions.     

Sperm storage reduces the strength of the mate‐finding Allee effect

Mate searching is a key component of sexual reproduction that can have important implications for population viability, especially for the mate‐finding Allee effect. Interannual sperm storage by females may be an adaptation that potentially attenuates mate limitation, but the demographic consequences of this functional trait have not been studied. Our goal is to assess the effect of female sperm storage durability on the strength of the mate‐finding Allee effect and the viability of populations subject to low population density and habitat alteration. We used an individual‐based simulation model that incorporates realistic representations of the demographic and spatial processes of our model species, the spur‐thighed tortoise (Testudo graeca). This allowed for a detailed assessment of reproductive rates, population growth rates, and extinction probabilities. We also studied the relationship between the number of reproductive males and the reproductive rates for scenarios combining different levels of sperm storage durability, initial population density, and landscape alteration. Our results showed that simulated populations parameterized with the field‐observed demographic rates collapsed for short sperm storage durability, but were viable for a durability of one year or longer. In contrast, the simulated populations with a low initial density were only viable in human‐altered landscapes for sperm storage durability of 4 years. We find that sperm storage is an effective mechanism that can reduce the strength of the mate‐finding Allee effect and contribute to the persistence of low‐density populations. Our study highlights the key role of sperm storage in the dynamics of species with limited movement ability to facilitate reproduction in patchy landscapes or during population expansion. This study represents the first quantification of the effect of sperm storage durability on population dynamics in different landscapes and population scenarios.     

Are time delays always destabilizing? Revisiting the role of time delays and the Allee effect

One of the main challenges in ecology is to determine the cause of population fluctuations. Both theoretical and empirical studies suggest that delayed density dependence instigates cyclic behavior in many populations; however, underlying mechanisms through which this occurs are often difficult to determine and may vary within species. In this paper, we consider single species population dynamics affected by the Allee effect coupled with discrete time delay. We use two different mathematical formulations of the Allee effect and analyze (both analytically and numerically) the role of time delay in different feedback mechanisms such as competition and cooperation. The bifurcation value of the delay (that results in the Hopf bifurcation) as a function of the strength of the Allee effect is obtained analytically. Interestingly, depending on the chosen delayed mechanism, even a large time delay may not necessarily lead to instability. We also show that, in case the time delay affects positive feedback (such as cooperation), the population dynamics can lead to self-organized formation of intermediate quasi-stationary states. Finally, we discuss ecological implications of our findings.     

Lake sturgeon population characteristics in Rainy Lake, Minnesota and Ontario

Rainy Lake contains a native population of lake sturgeon Acipenser fulvescens that has been largely unstudied. The aims of this study were to document the population characteristics of lake sturgeon in Rainy Lake and to relate environmental factors to year‐class strength for this population. Gill‐netting efforts throughout the study resulted in the capture of 322 lake sturgeon, including 50 recaptures. Lake sturgeon in Rainy Lake was relatively plump and fast growing compared with a 32‐population summary. Population samples were dominated by lake sturgeon between 110 and 150 cm total length. Age–structure analysis of the samples indicated few younger (<10 years) lake sturgeon, but the smallest gill net mesh size used for sampling was 102 mm (bar measure) and would not retain small sturgeon. Few lake sturgeon older than age 50 years were captured, and maximum age of sampled fish was 59 years. Few correlations existed between lake sturgeon year‐class indices and both annual and monthly climate variables, except that mean June air temperature was positively correlated with year‐class strength. Analysis of Rainy Lake water elevation and resulting lake sturgeon year‐class strength indices across years yielded consistent but weak negative correlations between late April and early June, when spawning of lake sturgeon occurs. The baseline data collected in this study should allow Rainy Lake biologists to establish more specific research questions in the future.