The 1988 and 2002 phocine distemper virus epidemics in European harbour seals

We present new and revised data for the phocine distemper virus (PDV) epidemics that resulted in the deaths of more than 23 000 harbour seals Phoca vitulina in 1988 and 30,000 in 2002. On both occasions the epidemics started at the Danish island of Anholt in central Kattegat, and subsequently spread to adjacent colonies in a stepwise fashion. However, this pattern was not maintained throughout the epidemics and new centres of infection appeared far from infected populations on some occasions: in 1988 early positive cases were observed in the Irish Sea, and in 2002 the epidemic appeared in the Dutch Wadden Sea, 6 wk after the initiation of the outbreak at Anholt Island. Since the harbour seal is a rather sedentary species, such 'jumps' in the spread among colonies suggest that another vector species could have been involved. We discussed the role of sympatric species as disease vectors, and suggested that grey seal populations could act as reservoirs for PDV if infection rates in sympatric species are lower than in harbour seals. Alternatively, grey seals could act as subclinical infected carriers of the virus between Arctic and North Sea seal populations. Mixed colonies of grey and harbour seal colonies are found at all locations where the jumps occurred. It seems likely that grey seals, which show long-distance movements, contributed to the spread among regions. The harbour seal populations along the Norwegian coast and in the Baltic escaped both epidemics, which could be due either to genetic differences among harbour seal populations or to immunity. Catastrophic events such as repeated epidemics should be accounted for in future models and management strategies of wildlife populations.     

Acquired immunity and stochasticity in epidemic intervals impede the evolution of host disease resistance

Disease can generate intense selection pressure on host populations, but here we show that acquired immunity in a population subject to repeated disease outbreaks can impede the evolution of genetic disease resistance by maintaining susceptible genotypes in the population. Interference between the life-history schedule of a species and periodicity of the disease has unintuitive effects on selection intensity, and stochasticity in outbreak period further reduces the rate of spread of disease-resistance alleles. A general age-structured population genetic model was developed and parameterized using empirical data for phocine distemper virus (PDV) epizootics in harbor seals. Scenarios with acquired immunity had lower levels of epizootic mortality compared with scenarios without acquired immunity for the first PDV outbreaks, but this pattern was reversed after about five disease cycles. Without acquired immunity, evolution of disease resistance was more rapid, and long-term population size variation is efficiently dampened. Acquired immunity has the potential to significantly influence rapid evolutionary dynamics of a host population in response to age-structured disease selection and to alter predicted selection intensities compared with epidemiological models that do not consider such feedback. This may have important implications for evolutionary population dynamics in a range of human, agricultural, and wildlife disease settings.     

The 2002 European seal plague: epidemiology and population consequences

We present the first epidemiological data on the 2002 outbreak of phocine distemper virus (PDV) in European harbour seals (Phoca vitulina). The epizootic curve to date supports a mortality rate and probability of infection identical to that of the 1988 outbreak, which killed 58% of the population. Thus immunity is playing no significant role in the dynamics of the current outbreak. Because the timing of the outbreak is important in determining local mortality rates, we predict higher mortality rates on the European continent than in Great Britain or Ireland. A stochastic model is used to quantify how recurrent epizootics affect the long‐term growth, fluctuation, and persistence of the population. Recurrent PDV epizootics with the observed frequency and severity would reduce the long‐term stochastic growth rate of the harbour seal population by half, and significantly increase the risk of quasi‐extinction.     

现代狩猎在野生动物管理中的作用

尽管现代狩猎有别于传统狩猎,但仍是一个备受争议的话题.国际上有大量学者从生态学、行为学、遗传学、经济学等角度研究狩猎对野生动物的影响.本文综合国内外文献,综述了狩猎在种群动态、行为、基因及表型方面可能对野生动物产生的影响.研究表明： 规范管理下的适当狩猎是管理野生动物种群的有效方式,有利于野外种群数量的恢复甚至增加.但过度或不当的狩猎会影响野生动物种群性比、出生率和死亡率,改变动物觅食行为及社群空间行为,对动物基因及表型产生人工选择.国际上很多国家已成功开展适当的狩猎活动,而我国要想在野生动物管理中科学应用狩猎,应基于生态学、经济学理论,参考国际上的成功案例,科学制定狩猎限额,加强狩猎监督管理,兼顾生态保护与经济发展.     

Acute phase protein haptoglobin in blood plasma samples of harbour seals (Phoca vitulina) of the Wadden Sea and of the isle Helgoland

Haptoglobin (Hp) which is synthesized in response to infection, inflammation, trauma or toxicological damage is known as a major acute phase protein in numerous species. Quantification of the circulating concentration of this protein can provide an objective measure of the health status, but there is a lack of investigations on harbour seals. We investigated the Hp concentration in samples of 123 seals (Phoca vitulina) from the German and Danish Wadden Sea to study physiological ranges of Hp levels. Hp levels between 2002, the end of the phocine distemper virus epidemic (PDV), and 2007 were considered, and Hp concentrations between animals of different sex, ages as well as living areas were compared. Furthermore, as a case study, six animals from the open sea isle Helgoland were investigated in 2006. Influences on the health status of the seal population e.g. the PDV epidemic were reflected by increased Hp levels in North Sea seals in 2002. The results of the Wadden Sea seals showed no significant age-, sex-, or geographical area-related differences. Interestingly, for the seals of the open sea isle Helgoland higher Hp values were measured compared to the Wadden Sea seals. The present study demonstrates that Hp can be used as a diagnostic tool to monitor the health status of harbour seals.     

Development and testing of a genetic marker‐based pedigree reconstruction system ‘PR‐genie’ incorporating size‐class data

For wildlife populations, it is often difficult to determine biological parameters that indicate breeding patterns and population mixing, but knowledge of these parameters is essential for effective management. A pedigree encodes the relationship between individuals and can provide insight into the dynamics of a population over its recent history. Here, we present a method for the reconstruction of pedigrees for wild populations of animals that live long enough to breed multiple times over their lifetime and that have complex or unknown generational structures. Reconstruction was based on microsatellite genotype data along with ancillary biological information: sex and observed body size class as an indicator of relative age of individuals within the population. Using body size‐class data to infer relative age has not been considered previously in wildlife genealogy and provides a marked improvement in accuracy of pedigree reconstruction. Body size‐class data are particularly useful for wild populations because it is much easier to collect noninvasively than absolute age data. This new pedigree reconstruction system, PR‐genie, performs reconstruction using maximum likelihood with optimization driven by the cross‐entropy method. We demonstrated pedigree reconstruction performance on simulated populations (comparing reconstructed pedigrees to known true pedigrees) over a wide range of population parameters and under assortative and intergenerational mating schema. Reconstruction accuracy increased with the presence of size‐class data and as the amount and quality of genetic data increased. We provide recommendations as to the amount and quality of data necessary to provide insight into detailed familial relationships in a wildlife population using this pedigree reconstruction technique.     

Length of intervals between epidemics: evaluating the influence of maternal transfer of immunity

The length of intervals between epidemic outbreaks of infectious diseases is critical in epidemiology. In several species of marine mammals and birds, it is pivotal to also consider the life history of the species of concern, as the contact rate between individuals can have a seasonal flux, for example, due to aggregations during the breeding season. Recently, particular interest has been given to the role of the dynamics of immunity in determining the intervals between epidemics in wild animal populations. One potentially powerful, but often neglected, process in this context is the maternal transfer of immunity. Here, we explore theoretically how the transfer of maternal antibodies can delay the recurrence of epidemics using Phocine Distemper in harbor seals as an example of a system in which epidemic outbreaks are followed by pathogen extinction. We show that the presence of temporarily protected newborns can significantly increase the predicted interval between epidemics, and this effect is strongly dependent on the degree of synchrony in the breeding season. Furthermore, we found that stochasticity in the onset of epidemics in combination with maternally acquired immunity increases the predicted intervals between epidemics even more. These effects arise because newborns with maternal antibodies temporarily boost population level immunity above the threshold of herd immunity, particularly when breeding is synchronous. Overall, our results show that maternal antibodies can have a profound influence on the dynamics of wildlife epidemics, notably in gregarious species such as many marine mammals and seabirds.     

Antibodies to phocine herpesvirus-1 are common in North American harbor seals (Phoca vitulina)

Phocine herpesvirus-1 (PhHV-1) has been associated with morbidity and high mortality in neonatal harbor seals (Phoca vitulina) along the Pacific coast of California (USA) and in northern Europe. Seals dying with PhHV-1 associated disease in California primarily have histopathologic evidence of adrenal necrosis or adrenalitis with herpesviral inclusion bodies. Little is known about prevalence of exposure to PhHV-1, modes of disease transmission, and viral pathogenesis in free-ranging harbor seal populations. To evaluate the prevalence in North America, 866 serum samples collected between 1994 and 2002 from harbor seals captured or stranded on the Pacific and Atlantic coasts of North America were assayed by enzyme linked immunosorbent assay (ELISA) for evidence of PhHV-1 exposure. Samples from three harbor seal age classes (pre-weaned, weaned, and subadults/adults) were obtained from each of four regions to compare exposure among sex, age class, and region. We found increasing prevalence with age as 37.5% of pre-weaned pups, 87.6% of weaned pups, and 99.0% of subadults and adults were seropositive. When accounting for age, no associations between seropositivity and sex or location of harbor seals were detected. These data indicate that PhHV-1 is endemic in the harbor seal populations of North America.     

Harvesting can increase severity of wildlife disease epidemics

Theoretical studies of wildlife population dynamics have proved insightful for sustainable management, where the principal aim is to maximize short-term yield, without risking population extinction. Surprisingly, infectious diseases have not been accounted for in harvest models, which is a major oversight because the consequences of parasites for host population dynamics are well-established. Here, we present a simple general model for a host species subject to density dependent reproduction and seasonal demography. We assume this host species is subject to infection by a strongly immunizing, directly transmitted pathogen. In this context, we show that the interaction between density dependent effects and harvesting can substantially increase both disease prevalence and the absolute number of infectious individuals. This effect clearly increases the risk of cross-species disease transmission into domestic and livestock populations. In addition, if the disease is associated with a risk of mortality, then the synergistic interaction between hunting and disease-induced death can increase the probability of host population extinction.     

Stage-structured transmission of phocine distemper virus in the Dutch 2002 outbreak

Heterogeneities in transmission among hosts can be very important in shaping infectious disease dynamics. In mammals with strong social organization, such heterogeneities are often structured by functional stage: juveniles, subadults and adults. We investigate the importance of such stage-related heterogeneities in shaping the 2002 phocine distemper virus (PDV) outbreak in the Dutch Wadden Sea, when more than 40 per cent of the harbour seals were killed. We do this by comparing the statistical fit of a hierarchy of models with varying transmission complexity: homogeneous versus heterogeneous mixing and density- versus frequency-dependent transmission. We use the stranding data as a proxy for incidence and use Poisson likelihoods to estimate the ‘who acquires infection from whom’ (WAIFW) matrix. Statistically, the model with strong heterogeneous mixing and density-dependent transmission was found to best describe the transmission dynamics. However, patterns of incidence support a model of frequency-dependent transmission among adults and juveniles. Based on the maximum-likelihood WAIFW matrix estimates, we use the next-generation formalism to calculate an R₀ between 2 and 2.5 for the Dutch 2002 PDV epidemic.     

Feline immunodeficiency virus in puma: Estimation of force of infection reveals insights into transmission

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Seasonality and wildlife disease: how seasonal birth, aggregation and variation in immunity affect the dynamics of Mycoplasma gallisepticum in house finches

We examine the role of host seasonal breeding, host seasonal social aggregation and partial immunity in affecting wildlife disease dynamics, focusing on the dynamics of house finch conjunctivitis (Mycoplasma gallisepticum (MG) in Carpodacus mexicanus). This case study of an unmanaged emerging infectious disease provides useful insight into the important role of seasonal factors in driving ongoing disease dynamics. Seasonal breeding can force recurrent epidemics through the input of fresh susceptibles, which will clearly affect a wide variety of wildlife disease dynamics. Seasonal patterns of social aggregation and foraging behaviour could change transmission dynamics. We use latitudinal variation in the timing of breeding, and social systems to model seasonal dynamics of house finch conjunctivitis across eastern North America. We quantify the patterns of seasonal breeding, and social aggregation across a latitudinal gradient in the eastern range of the house finch, supplemented with known field and laboratory information on immunity to MG in finches. We then examine the interactions of these factors in a theoretical model of disease dynamics. We find that both forms of seasonality could explain the dynamics of the house finch-MG system, and that these factors could have important effects on the dynamics of wildlife diseases generally. In particular, while either alone is sufficient to create recurrent cycles of prevalence in a population with an endemic disease, both are required to produce the specific semi-annual pattern of disease prevalence seen in the house finch conjunctivitis system.     

Evaluating the influence of epidemiological parameters and host ecology on the spread of phocine distemper virus through populations of harbour seals

Background

Outbreaks of phocine distemper virus (PDV) in Europe during 1988 and 2002 were responsible for the death of around 23,000 and 30,000 harbour seals, respectively. These epidemics, particularly the one in 2002, provided an unusual opportunity to estimate epidemic parameters for a wildlife disease. There were marked regional differences in the values of some parameters both within and between epidemics.

Methodology and Principal Findings

We used an individual-based model of seal movement that allowed us to incorporate realistic representations of space, time and animal behaviour into a traditional epidemiological modelling framework. We explored the potential influence of a range of ecological (foraging trip duration, time of epidemic onset, population size) and epidemiological (length of infectious period, contact rate between infectious and susceptible individuals, case mortality) parameters on four readily-measurable epidemic characteristics (number of dead individuals, duration of epidemic, peak mortality date and prevalence) and on the probability that an epidemic would occur in a particular region. We analysed the outputs as if they were the results of a series of virtual experiments, using Generalised Linear Modelling. All six variables had a significant effect on the probability that an epidemic would be recognised as an unusual mortality event by human observers.

Conclusions

Regional and temporal variation in contact rate was the most likely cause of the observed differences between the two epidemics. This variation could be a consequence of differences in the way individuals divide their time between land and sea at different times of the year.     

Seasonality, cohort-dependence and the development of immunity in a natural host-nematode system

Acquired immunity is known to be a key modulator of the dynamics of many helminth parasites in domestic and human host populations, but its relative importance in natural populations is more controversial. A detailed long-term dataset on the gastrointestinal nematode Trichostrongylus retortaeformis in a wild population of European rabbits (Oryctolagus cuniculus) shows clear evidence of seasonal acquired immunity in the age-structured infection profiles. By fitting a hierarchy of demographic infection-immunity models to the observed age-structured infection patterns, we are able to quantify the importance of different components (seasonality, immunity and host age structure) of the parasite dynamics. We find strong evidence that the hosts' immunocompetence waxes and wanes with the seasons, but also contains a lifelong cohort factor, possibly acting through a maternal effect dependent on the host's month of birth. These observations have important and broad implications for the ecology of parasite infection in seasonal natural herbivore systems.     

Innate immunity in free-ranging African buffalo (Syncerus caffer): associations with parasite infection and white blood cell counts

Mammalian immunology has been studied in great detail in laboratory animals, but few of the tools and less of the insight derived from these studies have been placed in the context of natural, outbred wildlife populations subject to variable environments. We investigated patterns of innate immunity in free-ranging African buffalo in relation to host traits (age, reproductive status, body condition, white blood cell counts) and disease status (bovine tuberculosis [BTB], gastrointestinal nematodes, coccidia, ticks). We evaluated and used an in vitro assay measuring bactericidal competence of blood to assess a component of innate immunity in 200 female buffalo captured at Kruger National Park, South Africa, in June/July and October 2008. Animals with BTB had higher bactericidal competence of blood. Animals with higher neutrophil counts had higher bactericidal competence, whereas animals with lower lymphocyte counts had higher bactericidal competence. This pattern was driven by animals captured at the end of the dry season (October) and may be evidence of immune polarization, whereby individuals are unable to upregulate multiple components of immunity simultaneously. Bactericidal competence did not vary with host pregnancy status, body condition, age, lactation, tick infestation, nematode egg count, or coccidia oocyst count. Overall, we demonstrate that the bactericidal competence assay is practical and informative for field-based studies in wild bovids. Our results also show a correlation between bactericidal competence and bovine tuberculosis infection and reveal possible functional polarizations between different types of immune response in a free-ranging mammal.     

Specificity and success of oral-bait delivery to Eurasian wild boar in Mediterranean woodland habitats

Eurasian wild boar (Sus scrofa) is an important reservoir host for pathogens affecting humans and domestic animals. The eradication of these diseases may require the development of control strategies that reduce pathogen transmission between wildlife and domestic animals. Baiting for oral vaccine delivery is often considered for wildlife disease control. The effective and efficient field vaccination of wildlife requires species-specific baits as delivery vehicles for oral vaccines and designing appropriate baiting strategies. The objective of this study was to determine the proportion of young and adult wild boar and non-target animals that consumed baits containing a chemical marker, iophenoxic acid (IPA), in delivery trials conducted in summer in four different sites in the Mediterranean region of Spain where wild boar are abundant. The proportion of wild boar showing IPA markers in serum in autumn ranged from 11.5% to 56.4%. When attending to age classes, 12.6% to 72.7% of young individuals presented IPA. The results evidenced that the percent of wild boar that ingested the baits varied among study sites and age classes. Placing baits inside selective cages (for juveniles) and under heavy pavel stones (for adults) contributed to improve age specificity in bait consumption. We suggest ways for improving the age specificity of bait delivery systems used for young and adult wild boar.     

Mycoplasmosis in wildlife: a review

Mycoplasma, the smallest self-replicating life-forms, are responsible for a variety of diseases in humans, domestic animals, insects, and plants. Although the exact role of these organisms in wildlife is not available, now it is increasingly recognized that mycoplasmosis is an emerging disease in many wildlife populations. As only scattered data regarding these are available, an attempt has been made to assemble the available literature. To our knowledge, this is the first review paper regarding mycoplasmosis in wildlife. The outbreaks of mycoplasmoses such as contagious pleuropneumonia (CCPP), infectious keratoconjunctivitis (IKC), Mycoplasma ovipneumoniae and Mycoplasma capricolum subspp. capricolum infections, and contagious agalactia in wild ruminants; mycoplasmosis in raccoons; upper respiratory tract disease (URTD) and Mycoplasma crocodyli and Mycoplasma alligatoris infections in wild reptiles; and house finch conjunctivitis are showing that the prevalence of mycoplasmosis in wildlife has reached an alarming level, thus raising concerns for the conservation of many endangered species in captivity and free-ranging populations. These also emphasize the urgent need for increased surveillance and control of mycoplasma in wildlife. Some control approaches that can be followed are prevention of the spillover from domestic livestock and birds, proper quarantine of newly received animals along with mycoplasma screening, isolation of affected and suspected animals, screening of mycoplasmoses before the release of captive animals into free-ranging population, etc. At the same time, the previous dogma that mycoplasma have strict host specificity should be reconsidered in the light of new findings.     

The potential effects of repeated outbreaks of phocine distemper among harbour seals: a response to Harding et al. (2002)

In 2002 phocine distemper virus (PDV) reappeared in the European harbour seal (Phoca vitulina) population. This outbreak seems to have followed a similar pattern to the 1988 one which killed almost 60% of individuals in most localities. Harding et al. (2002) suggested that there is a relatively high (18%) risk that recurrent outbreaks of PDV could reduce the European harbour seal population by 90%. We show that incorporating the effects of observation error during population surveys and of the long‐term immunity of survivors of morbillivirus outbreaks indicate a much lower level of risk (<1%). This suggests that, while the immediate effects of the disease are dramatic, it is unlikely that recurrent epidemics will pose serious conservation problems for this species under current conditions.