Demographic consequences of invasion by a native, controphic competitor to an insular bird population.

Species invasions and range shifts can lead to novel competitive interactions between historically resident and colonizing species, but the demographic consequences of such interactions remain controversial. We present results from field experiments and 45 years of demographic monitoring to test the hypothesis that the colonization of Mandarte Is., BC, Canada, by fox sparrows (Passerella iliaca) caused the long-term decline of the resident population of song sparrows (Melospiza melodia). Several lines of evidence indicate that competition with fox sparrows for winter food reduced over-winter survival in juvenile song sparrows by 48% from 1960 to 2015, enforcing population decline despite an increase in annual reproductive rate in song sparrows over the same period. Preference for locally abundant seeds presented at experimental arenas suggested complete overlap in diet in song and fox sparrows, and observations at arenas baited with commercial seed showed that fox sparrows displaced song sparrows in 91-100% of interactions in two periods during winter. In contrast, we found no evidence of interspecific competition for resources during the breeding season. Our results indicate that in the absence of marked shifts in niche dimension, range expansions by dominant competitors have the potential to cause the extirpation of historically resident species when competitive interactions between them are strong and resources not equitably partitioned.

Genetic covariance between components of male reproductive success: within-pair vs. extra-pair paternity in song sparrows.

The evolutionary trajectories of reproductive systems, including both male and female multiple mating and hence polygyny and polyandry, are expected to depend on the additive genetic variances and covariances in and among components of male reproductive success achieved through different reproductive tactics. However, genetic covariances among key components of male reproductive success have not been estimated in wild populations. We used comprehensive paternity data from socially monogamous but genetically polygynandrous song sparrows (Melospiza melodia) to estimate additive genetic variance and covariance in the total number of offspring a male sired per year outside his social pairings (i.e. his total extra-pair reproductive success achieved through multiple mating) and his liability to sire offspring produced by his socially paired female (i.e. his success in defending within-pair paternity). Both components of male fitness showed nonzero additive genetic variance, and the estimated genetic covariance was positive, implying that males with high additive genetic value for extra-pair reproduction also have high additive genetic propensity to sire their socially paired female's offspring. There was consequently no evidence of a genetic or phenotypic trade-off between male within-pair paternity success and extra-pair reproductive success. Such positive genetic covariance might be expected to facilitate ongoing evolution of polygyny and could also shape the ongoing evolution of polyandry through indirect selection.

The effects of contemporary processes in maintaining the genetic structure of western song sparrows (Melospiza melodia).

Historic events and contemporary processes work in concert to create and maintain geographically partitioned variation and are instrumental in the generation of biodiversity. We sought to gain a better understanding of how contemporary processes such as movement and isolation influence the genetic structure of widely distributed vagile species such as birds. Song sparrows (Melospiza melodia) in western North America provide a natural system for examining the genetics of populations that have different patterns of geographic isolation and migratory behavior. We examined the population genetics of 576 song sparrows from 23 populations using seven microsatellite loci to assess genetic differentiation among populations and to estimate the effects of drift and immigration (gene flow) on each population. Sedentary, isolated populations were characterized by low levels of immigration and high levels of genetic drift, whereas those populations less isolated displayed signals of high gene flow and little differentiation from other populations. Contemporary dispersal rates from migratory populations, estimated by assignment test, were higher and occurred over larger distances than dispersal from sedentary populations but were also probably too low to counter the effects of drift in most populations. We suggest that geographic isolation and limited gene flow facilitated by migratory behavior are responsible for maintaining observed levels of differentiation among Pacific coastal song sparrow populations.

Testing evolutionary models of senescence in a natural population: age and inbreeding effects on fitness components in song sparrows.

Mutation accumulation (MA) and antagonistic pleiotropy (AP) have each been hypothesized to explain the evolution of 'senescence' or deteriorating fitness in old age. These hypotheses make contrasting predictions concerning age dependence in inbreeding depression in traits that show senescence. Inbreeding depression is predicted to increase with age under MA but not under AP, suggesting one empirical means by which the two can be distinguished. We use pedigree and life-history data from free-living song sparrows (Melospiza melodia) to test for additive and interactive effects of age and individual inbreeding coefficient (f) on fitness components, and thereby assess the evidence for MA. Annual reproductive success (ARS) and survival (and therefore reproductive value) declined in old age in both sexes, indicating senescence in this short-lived bird. ARS declined with f in both sexes and survival declined with f in males, indicating inbreeding depression in fitness. We observed a significant agexf interaction for male ARS (reflecting increased inbreeding depression as males aged), but not for female ARS or survival in either sex. These analyses therefore provide mixed support for MA. We discuss the strengths and limitations of such analyses and therefore the value of natural pedigreed populations in testing evolutionary models of senescence.

Interactive effects of environmental stress and inbreeding on reproductive traits in a wild bird population.

1. Conservation biologists are concerned about the interactive effects of environmental stress and inbreeding because such interactions could affect the dynamics and extinction risk of small and isolated populations, but few studies have tested for these interactions in nature. 2. We used data from the long-term population study of song sparrows Melospiza melodia on Mandarte Island to examine the joint effects of inbreeding and environmental stress on four fitness traits that are known to be affected by the inbreeding level of adult birds: hatching success, laying date, male mating success and fledgling survival. 3. We found that inbreeding depression interacted with environmental stress to reduce hatching success in the nests of inbred females during periods of rain. 4. For laying date, we found equivocal support for an interaction between parental inbreeding and environmental stress. In this case, however, inbred females experienced less inbreeding depression in more stressful, cooler years. 5. For two other traits, we found no evidence that the strength of inbreeding depression varied with environmental stress. First, mated males fathered fewer nests per season if inbred or if the ratio of males to females in the population was high, but inbreeding depression did not depend on sex ratio. Second, fledglings survived poorly during rainy periods and if their father was inbred, but the effects of paternal inbreeding and rain did not interact. 6. Thus, even for a single species, interactions between the inbreeding level and environmental stress may not occur in all traits affected by inbreeding depression, and interactions that do occur will not always act synergistically to further decrease fitness.

Morphological and microsatellite differentiation in Melospiza melodia (Aves) at a microgeographic scale.

Geographical variation in microsatellite allele frequencies and morphology were compared for five subspecies of Melospiza melodia (song sparrow; M. m. samuelis, M. m. maxillaris, M. m. pusillula, M. m. gouldii, and M. m. heermanni) in 14 populations in the San Francisco Bay region to (a) assess divergence based on these estimates and (b) test the hypothesis that drift is responsible for morphological and genetic divergence. Morphological differentiation between subspecies was high despite low differentiation at microsatellite loci, indicating high gene flow and large effective population sizes. Low concordance of morphological and genetic estimates of divergence suggests that selection or phenotypic plasticity in morphology has caused morphological differentiation among the subspecies.

Human demography and reserve size predict wildlife extinction in West Africa.

Species-area models have become the primary tool used to predict baseline extinction rates for species in isolated habitats, and have influenced conservation and land-use planning worldwide. In particular, these models have been used to predict extinction rates following the loss or fragmentation of natural habitats in the absence of direct human influence on species persistence. Thus, where direct human influences, such as hunting, put added pressure on species in remnant habitat patches, we should expect to observe extinction rates higher than those predicted by simple species-area models. Here, we show that extinction rates for 41 species of large mammals in six nature reserves in West Africa are 14-307 times higher than those predicted by models based on reserve size alone. Human population and reserve size accounted for 98% of the observed variation in extinction rates between reserves. Extinction occurred at higher rates than predicted by species-area models for carnivores, primates and ungulates, and at the highest rates overall near reserve borders. Our results indicate that, where the harvest of wildlife is common, conservation plans should focus on increasing the size of reserves and reducing the rate of hunting.

Immigration and the ephemerality of a natural population bottleneck: evidence from molecular markers.

Population bottlenecks are often invoked to explain low levels of genetic variation in natural populations, yet few studies have documented the direct genetic consequences of known bottlenecks in the wild. Empirical studies of natural population bottlenecks are therefore needed, because key assumptions of theoretical and laboratory studies of bottlenecks may not hold in the wild. Here we present microsatellite data from a severe bottleneck (95% mortality) in an insular population of song sparrows (Melospiza melodia). The major findings of our study are as follows: (i) The bottleneck reduced heterozygosity and allelic diversity nearly to neutral expectations, despite non-random survival of birds with respect to inbreeding and wing length. (ii) All measures of genetic diversity regained pre-bottleneck levels within two to three years of the crash. This rapid recovery was due to low levels of immigration. (iii) The rapid recovery occurred despite a coincident, strong increase in average inbreeding. These results show that immigration at levels that are hard to measure in most field studies can lead to qualitatively very different genetic outcomes from those expected from mutations only. We suggest that future theoretical and empirical work on bottlenecks and metapopulations should address the impact of immigration.

Estimating the time to extinction in an island population of song sparrows.

We estimated and modelled how uncertainties in stochastic population dynamics and biases in parameter estimates affect the accuracy of the projections of a small island population of song sparrows which was enumerated every spring for 24 years. The estimate of the density regulation in a theta-logistic model (theta = 1.09 suggests that the dynamics are nearly logistic, with specific growth rate r1 = 0.99 and carrying capacity K = 41.54. The song sparrow population was strongly influenced by demographic (sigma2(d) = 0.66) and environmental (sigma2(d) = 0.41) stochasticity. Bootstrap replicates of the different parameters revealed that the uncertainties in the estimates of the specific growth rate r1 and the density regulation theta were larger than the uncertainties in the environmental variance sigma2(e) and the carrying capacity K. We introduce the concept of the population prediction interval (PPI), which is a stochastic interval which includes the unknown population size with probability (1 - alpha). The width of the PPI increased rapidly with time because of uncertainties in the estimates of density regulation as well as demographic and environmental variance in the stochastic population dynamics. Accepting a 10% probability of extinction within 100 years, neglecting uncertainties in the parameters will lead to a 33% overestimation of the time it takes for the extinction barrier (population size X = 1) to be included into the PPI. This study shows that ignoring uncertainties in population dynamics produces a substantial underestimation of the extinction risk.

Estradiol and progesterone metabolite concentration in white-tailed deer (Odocoileus virginianus) feces.

Assays of reproductive hormone metabolites require validation in each animal species. For validation of methodology in white-tailed deer (Odocoileus virginianus), fecal samples were collected from females that had been injected by blowgun with estradiol, progesterone, or a control substance. Analysis by radioimmunoassay revealed that estradiol and pregnanediol were more abundant fecal metabolites of estrogens and progestins than were estrone or progesterone. Peak excretion rates of estradiol and pregnanediol occurred within 12 and 24 hr of injection, respectively. Ovulation time was estimated by measuring the frequency of occurrence of eight behavior patterns, including copulation. Profiles were compiled for three deer over the course of estrus and early pregnancy for estradiol, estrone, progesterone, and pregnanediol using radioimmunoassay. Pregnanediol was excreted at concentrations about 1,000 times higher than those of the other three fecal steroid metabolites, and pregnanediol differed in concentration during estrus, the luteal phase, and early pregnancy. Consequently, a simpler enzyme immunoassay was adapted and used to measure pregnanediol levels over the course of estrus and early pregnancy for seven deer. Measurement of fecal pregnanediol is useful for monitoring reproductive events in female white-tailed deer.

Scent marking in a territorial African antelope: II. The economics of marking with faeces.

Faeces may be ideal substances for scent marking because they have a minimal energetic cost to the signaller. However, marking with faeces is also constrained by the animal's ability to produce faeces. This study examined whether limits on the volume of faeces produced by oribi Ourebia ourebi, in Serengeti National Park, Tanzania, caused territorial males to regulate their output and prioritize the placement of faecal marks. Territorial males marked with faeces more often, and with a smaller volume per defecation, than did juvenile males and females. Territorial males also defecated only on established dung middens along borders shared with other territorial males or on top of a female's urine and faeces. In contrast, juvenile males and females defecated randomly with regard to their location in territories. Territorial males with larger harems marked with faeces at higher rates and less volume than males with few or no females. This difference suggests that when males overmark female excretions they reduce the amount of faeces available for marking other preferred sites, such as along territory borders shared with other males. Dominant males with adult subordinates marked with faeces less often, and with a greater volume per mark, than males that defended territories without the aid of subordinates. Dominant males also reduced the volume of marks less as the number of females on their territory increased than did males without subordinates. Territories occupied by more than one adult male also were marked with faeces at higher rates, and with marks of greater volume, than territories held by single males. These results suggest that the presence of subordinate males reduced the demand on dominant males to regulate the volume and placement of faecal marks. Overall, these results suggest that territorial male oribi regulate their faecal marking behaviour in response to a limited supply of faeces. Copyright 1999 The Association for the Study of Animal Behaviour.

Scent marking in a territorial African antelope: I. The maintenance of borders between male oribi.

Scent marking is ubiquitous among the dwarf antelope and gazelles of Africa, but its function has been the subject of debate. This study examined preorbital gland scent marking in the oribi, Ourebia ourebi, a territorial African antelope. Several hypotheses for the function of scent marking by territorial antelope were tested with observational data. Of these, the hypotheses that scent marking is driven by intrasexual competition between neighbouring males, and that marks serve as an honest advertisement of a male's ability to defend his territory from rivals, were supported best. Thirty-three territorial male oribi on 23 territories marked most at borders shared with other territorial males, and territorial males marked more often at borders shared with multimale groups than at borders shared with a single male. This suggests that males perceived neighbouring male groups as a greater threat to territory ownership than neighbouring males that defended their territories without the aid of adult subordinates. Marking rate was unrelated to territory size or the number of females on adjacent territories, but males with many male neighbours marked at higher rates than those with fewer male neighbours. These results suggest that the presence of male neighbours has a greater effect on the scent marking behaviour of territorial antelope than has been considered previously. Copyright 1999 The Association for the Study of Animal Behaviour.

Effect of auxiliary males on territory ownership in the oribi and the attributes of multimale groups.

I observed free-ranging oribi, Ourebia ourebi, in Serengeti National Park, Tanzania, to determine whether group formation by males provides evidence for cooperative territory defence, a behaviour that is rare among male vertebrates. Socially dominant males that shared territories with subordinate auxiliary males were replaced by rivals less often than males that defended territories without auxiliary males. Auxiliary males marked territories with preorbital glands, dung and urine, and territories defended by male groups were marked more thoroughly than those defended by single males. Fifteen of 24 (62.5%) auxiliary males whose histories were known were born on territories defended by males that probably were their fathers. But 37.5% of auxiliary males probably were unrelated to dominant males, because male groups also formed when territory owners accepted adult male immigrants as subordinates, and when owners allowed young males to remain philopatric after evicting a male likely to have been the young male's father. All males in groups probably had some mating access to females, but dominant males may have minimized matings of auxiliary males by guarding fertile females. These results suggest that auxiliary male oribi aided dominant males in territory defence, and that dominants traded off the risks of losing matings to auxiliaries, or being overthrown by them, in exchange for a reduction in their chance of being evicted by rival neighbours or immigrants. Copyright 1999 The Association for the Study of Animal Behaviour.

No evidence for inbreeding avoidance in a natural population of song sparrows (Melospiza melodia).

We studied mate choice and inbreeding avoidance a natural population of song sparrows (Melospiza melodia) on Mandarte Island, Canada. Inbreeding occurred regularly: 59% all matings were between known relatives. We tested for inbreeding avoidance by comparing the observed levels of inbreeding to those expected if mate choice had been random with respect to relatedness. Independent of our assumptions about the availability of mates in the random mating model, we found that the expected and observed distributions of inbreeding coefficients were similar, as was the expected and observed frequency of close (f >/= 0.125) inbreeding. Furthermore, there was no difference in relatedness observed pairs and those that would have resulted had birds mated instead with their nearest neighbors. The only evidence to suggest any inbreeding avoidance was a reduced rate of parent-offspring matings as compared to one random mating model but not the other. Hence, despite substantial inbreeding depression in this population, we found little evidence for inbreeding avoidance through mate choice. We present a simple model to suggest that variation in inbreeding avoidance behaviors in birds may arise from differences in survival rates: in species with low survival rates, the costs of forfeiting matings to avoid inbreeding may exceed the costs of inbreeding.

Nest predation by cowbirds and its consequences for passerine demography.

Brood parasitism by brown-headed cowbirds (Molothrus ater) reduces reproductive success in many passerines that nest in fragmented habitats and ecological edges, where nest predation is also common. We tested the hypothesis that parasitism and predation are often linked because cowbirds depredate nests discovered late in the host's nesting cycle to enhance future opportunities for parasitism. Over a 20-year study period, brood parasitism by cowbirds was a prerequisite to observing marked inter- and intraannual variation in the rate of nest failure in an insular song sparrow (Melospiza melodia) population. Nest failure increased with the arrival and laying rate of cowbirds and declined when cowbirds ceased laying. The absence or removal of cowbirds yielded the lowest nest failure rates recorded in the study. The absence of cowbirds also coincided with the absence of an otherwise strong positive correlation between host numbers and the annual rate of nest failure. Host numbers, cowbird parasitism, and nest failure may be correlated because cowbirds facilitate nest failure rather than cause it directly. However, an experiment mimicking egg ejection by cowbirds did not affect nest failure, and, contrary to the main prediction of the predation facilitation hypothesis, naturally parasitized nests failed less often than unparasitized nests. Higher survival of parasitized nests is expected under the cowbird predation hypothesis when female cowbirds defend access to hosts because cowbirds should often depredate unparasitized nests but should not depredate nests they have laid in. Where female cowbirds have overlapping laying areas, we expect parasitized nests to fail more often than others if different cowbirds often discover the same nests. We suggest that nest predation by cowbirds represents an adaptation for successful parasitism and that cowbirds influence host demography via nest predation.

Selection against inbred song sparrows during a natural population bottleneck.

The genetic and demographic consequences of population subdivision have received considerable attention from conservation biologists. In particular, losses of genetic variability and reduced viability and fecundity due to inbreeding (inbreeding depression) are of concern. Studies of domestic, laboratory and zoo populations have shown inbreeding depression in a variety of traits related to fitness. Consequently, inbreeding depression is widely accepted as a fact. Recently, however, the relative impact of inbreeding on the viability of natural populations has been questioned. Work on the cheetah (Acinonyx jubatus), for example, has emphasized the overwhelming importance of environmental factors on mortality in the wild. Here we report that song sparrows (Melospiza melodia) that survived a severe population bottleneck were a non-random subset of the pre-crash population with respect to inbreeding, and that natural selection favoured outbred individuals. Thus, inbreeding depression was expressed in the face of an environmental challenge. Such challenges are also likely to be faced by inbred populations of endangered species. We suggest that environmental and genetic effects on survival may interact and, as a consequence, that their effects on individuals and populations should not be considered independently.

Does competition regulate ungulate populations? Further evidence from Serengeti, Tanzania.

Changes in populations of several ungulate species in the Serengeti-Mara region of East Africa over the past 30 years suggest several hypotheses for their regulation and coexistence. Recent censuses in the 1980s have allowed us to test the hypotheses that: (1) there was competition between wildebeest (Connochaetes taurinus) and Thomson's gazelle (Gazella thomsoni). This predicted that gazelle numbers should have declined in the 1980s when wildebeest were food limited. Census figures show no change in gazelle numbers between 1978 and 1986, a result contrary to the interspecific competition hypothesis; (2) wildebeest and African buffalo (Syncerus caffer) populations were regulated by intraspecific competition for food. Since both populations reached food limitation in the 1970s, the hypothesis predicted that the populations should have been stable in the 1980s. The results confirm these predictions for wildebeest and the buffalo population in the Mara reserve. In the Serengeti the buffalo population declined 41% over the period 1976-1984. The decline was not evenly distributed over the park, some areas showing an 80-90% decline, others no change or an increase in numbers. The decline was associated with proximity to human habitation; (3) an outbreak of the viral disease, rinderpest, in 1982 may have been the cause of the drop in buffalo population. Blood serum samples to measure the prevalence of antibodies were collected from areas of decreasing, stable and increasing populations. If rinderpest was the cause of decrease there should be a negative relationship between the prevalence of rinderpest and the instantaneous rate of increase (r). The results showed no relationship. We conclude that rinderpest was not the major cause of the drop in buffalo numbers. Elephant (Loxodonta africana) numbers dropped 81% in Serengeti in the period 1977-1986. In the Mara there was little change. The evidence suggests that extensive poaching in northern and western Serengeti during 1979-1984 accounted for the drop in both elephant and buffalo numbers.