Reliability of flipper-banded penguins as indicators of climate change.

In 2007, the Intergovernmental Panel on Climate Change highlighted an urgent need to assess the responses of marine ecosystems to climate change. Because they lie in a high-latitude region, the Southern Ocean ecosystems are expected to be strongly affected by global warming. Using top predators of this highly productive ocean (such as penguins) as integrative indicators may help us assess the impacts of climate change on marine ecosystems. Yet most available information on penguin population dynamics is based on the controversial use of flipper banding. Although some reports have found the effects of flipper bands to be deleterious, some short-term (one-year) studies have concluded otherwise, resulting in the continuation of extensive banding schemes and the use of data sets thus collected to predict climate impact on natural populations. Here we show that banding of free-ranging king penguins (Aptenodytes patagonicus) impairs both survival and reproduction, ultimately affecting population growth rate. Over the course of a 10-year longitudinal study, banded birds produced 41% [corrected] fewer chicks and had a survival rate 16 percentage points [corrected] lower than non-banded birds, demonstrating a massive long-term impact of banding and thus refuting the assumption that birds will ultimately adapt to being banded. Indeed, banded birds still arrived later for breeding at the study site and had longer foraging trips even after 10 years. One of our major findings is that responses of flipper-banded penguins to climate variability (that is, changes in sea surface temperature and in the Southern Oscillation index) differ from those of non-banded birds. We show that only long-term investigations may allow an evaluation of the impact of flipper bands and that every major life-history trait can be affected, calling into question the banding schemes still going on. In addition, our understanding of the effects of climate change on marine ecosystems based on flipper-band data should be reconsidered.

Laridae: A neglected reservoir that could play a major role in avian influenza virus epidemiological dynamics.

Avian influenza viruses (AIVs) are of great concern worldwide due to their economic impact and the threat they represent to human health. As wild birds are the natural reservoirs of AIVs, understanding AIV dynamics in different avian taxa is essential for deciphering the epidemiological links between wildlife, poultry and humans. To date, only the Anatidae (ducks, geese and swans) have been widely studied. Here, we aim to shed light on the current state of knowledge on AIVs in Laridae (gulls, terns and kittiwakes) versus that in Anatidae by setting forth four fundamental questions: how, when, where and to which host species are AIVs transmitted? First, we describe ecological differences between Laridae and Anatidae and discuss how they may explain observed contrasts in preferential transmission routes and the evolution of specific AIV subtypes. Second, we highlight the dissimilarities in the temporal patterns of AIV shedding between Laridae and Anatidae and address the role that immunity likely plays in shaping these patterns. Third, we underscore that Laridae may be key in promoting intercontinental exchanges of AIVs. Finally, we emphasize the crucial epidemiological position that Laridae occupy between wildlife, domestic birds and humans.

Impacts of extreme climatic events on the energetics of long-lived vertebrates: the case of the greater flamingo facing cold spells in the Camargue.

Most studies analyzing the effects of global warming on wild populations focus on gradual temperature changes, yet it is also important to understand the impact of extreme climatic events. Here we studied the effect of two cold spells (January 1985 and February 2012) on the energetics of greater flamingos (Phoenicopterus roseus) in the Camargue (southern France). To understand the cause of observed flamingo mass mortalities, we first assessed the energy stores of flamingos found dead in February 2012, and compared them with those found in other bird species exposed to cold spells and/or fasting. Second, we evaluated the monthly energy requirements of flamingos across 1980-2012 using the mechanistic model Niche Mapper. Our results show that the body lipids of flamingos found dead in 2012 corresponded to 2.6±0.3% of total body mass, which is close to results found in woodcocks (Scolopax rusticola) that died from starvation during a cold spell (1.7±0.1%), and much lower than in woodcocks which were fed throughout this same cold spell (13.0±2%). Further, Niche Mapper predicted that flamingo energy requirements were highest (+6-7%) during the 1985 and 2012 cold spells compared with 'normal' winters. This increase was primarily driven by cold air temperatures. Overall, our findings strongly suggest that flamingos starved to death during both cold spells. This study demonstrates the relevance of using mechanistic energetics modelling and body condition analyses to understand and predict the impact of extreme climatic events on animal energy balance and winter survival probabilities.

Incidence of adult brain cancers is higher in countries where the protozoan parasite Toxoplasma gondii is common.

We explored associations between the common protozoan parasite Toxoplasma gondii and brain cancers in human populations. We predicted that T. gondii could increase the risk of brain cancer because it is a long-lived parasite that encysts in the brain, where it provokes inflammation and inhibits apoptosis. We used a medical geography approach based on the national incidence of brain cancers and seroprevalence of T. gondii. We corrected reports of incidence for national gross domestic product because wealth probably increases the ability to detect cancer. We also included gender, cell phone use and latitude as variables in our initial models. Prevalence of T. gondii explained 19 per cent of the residual variance in brain cancer incidence after controlling for the positive effects of gross domestic product and latitude among nations. Infection with T. gondii was associated with a 1.8-fold increase in the risk of brain cancers across the range of T. gondii prevalence in our dataset (4-67%). These results, though correlational, suggest that T. gondii should be investigated further as a possible oncogenic pathogen of humans.

King penguin population threatened by Southern Ocean warming.

Seabirds are sensitive indicators of changes in marine ecosystems and might integrate and/or amplify the effects of climate forcing on lower levels in food chains. Current knowledge on the impact of climate changes on penguins is primarily based on Antarctic birds identified by using flipper bands. Although flipper bands have helped to answer many questions about penguin biology, they were shown in some penguin species to have a detrimental effect. Here, we present for a Subantarctic species, king penguin (Aptenodytes patagonicus), reliable results on the effect of climate on survival and breeding based on unbanded birds but instead marked by subcutaneous electronic tags. We show that warm events negatively affect both breeding success and adult survival of this seabird. However, the observed effect is complex because it affects penguins at several spatio/temporal levels. Breeding reveals an immediate response to forcing during warm phases of El Niño Southern Oscillation affecting food availability close to the colony. Conversely, adult survival decreases with a remote sea-surface temperature forcing (i.e., a 2-year lag warming taking place at the northern boundary of pack ice, their winter foraging place). We suggest that this time lag may be explained by the delay between the recruitment and abundance of their prey, adjusted to the particular 1-year breeding cycle of the king penguin. The derived population dynamic model suggests a 9% decline in adult survival for a 0.26 degrees C warming. Our findings suggest that king penguin populations are at heavy extinction risk under the current global warming predictions.

[Persistence of influenza A viruses in relation with environmental factors]. / Persistance des virus influenza A en fonction des paramètres environnementaux.

Wild waterfowl represents the natural reservoir of influenza A viruses. Transmission within bird populations occurs through an indirect fecal-oral route implying contaminated water. Within human populations, influenza A viruses can be transmitted through large droplets, aerosols, or direct contact with secretions. Thus, in the human compartment as in the avian one, influenza A viruses have to experiment a free living stage. The knowledge of factors influencing viral persistence during that key step is needed to understand their transmission dynamic. Data gathered here describe the major role played by temperature, pH and salinity on viral persistence in aquatic environment and the importance of UV radiations, humidity and temperature in mid air. We discuss mechanisms underlying these roles and the potential influence of other factors. We point out the need to develop researches to improve our understanding on influenza A virus stability and thus transmission.

Reliability of animal counts and implications for the interpretation of trends.

Population time series analysis is an integral part of conservation biology in the current context of global changes. To quantify changes in population size, wildlife counts only provide estimates because of various sources of error. When unaccounted for, such errors can obscure important ecological patterns and reduce confidence in the derived trend. In the case of highly gregarious species, which are common in the animal kingdom, the estimation of group size is an important potential bias, which is characterized by high variance among observers. In this context, it is crucial to quantify the impact of observer changes, inherent to population monitoring, on i) the minimum length of population time series required to detect significant trends and ii) the accuracy (bias and precision) of the trend estimate.We acquired group size estimation error data by an experimental protocol where 24 experienced observers conducted counting simulation tests on group sizes. We used this empirical data to simulate observations over 25 years of a declining population distributed over 100 sites. Five scenarios of changes in observer identity over time and sites were tested for each of three simulated trends (true population size evolving according to deterministic models parameterized with declines of 1.1%, 3.9% or 7.4% per year that justify respectively a "declining," "vulnerable" or "endangered" population under IUCN criteria).We found that under realistic field conditions observers detected the accurate value of the population trend in only 1.3% of the cases. Our results also show that trend estimates are similar if many observers are spatially distributed among the different sites, or if one single observer counts all sites. However, successive changes in observer identity over time lead to a clear decrease in the ability to reliably estimate a given population trend, and an increase in the number of years of monitoring required to adequately detect the trend.Minimizing temporal changes of observers improve the quality of count data and help taking appropriate management decisions and setting conservation priorities. The same occurs when increasing the number of observers spread over 100 sites. If the population surveyed is composed of few sites, then it is preferable to perform the survey by one observer. In this context, it is important to reconsider how we use estimated population trend values and potentially to scale our decisions according to the direction and duration of estimated trends, instead of setting too precise threshold values before action.

Persistence of highly pathogenic avian influenza viruses in natural ecosystems.

Understanding of ecologic factors favoring emergence and maintenance of highly pathogenic avian influenza (HPAI) viruses is limited. Although low pathogenic avian influenza viruses persist and evolve in wild populations, HPAI viruses evolve in domestic birds and cause economically serious epizootics that only occasionally infect wild populations. We propose that evolutionary ecology considerations can explain this apparent paradox. Host structure and transmission possibilities differ considerably between wild and domestic birds and are likely to be major determinants of virulence. Because viral fitness is highly dependent on host survival and dispersal in nature, virulent forms are unlikely to persist in wild populations if they kill hosts quickly or affect predation risk or migratory performance. Interhost transmission in water has evolved in low pathogenic influenza viruses in wild waterfowl populations. However, oropharyngeal shedding and transmission by aerosols appear more efficient for HPAI viruses among domestic birds.

Avian influenza circulation in the Camargue (south of France) during the 2006-07 season.

Situated at the crossroads of numerous migratory routes of Palaearctic birds, the Camargue is considered a high-risk area for the introduction and transmission of numerous avian-borne pathogens. We investigated the epidemiologic cycles of avian influenza viruses (AIVs) in the local bird community by performing regular sampling on a large variety of bird species during 11 consecutive months in 2006-07. To detect the presence of AIV, SYBR green reverse transcriptase-PCR targeting the M gene was performed on 2901 samples from 66 bird species. A clear seasonal pattern of AIV circulation in ducks was observed during autumn and winter, with higher prevalence rates in early fall. Our results also support an absence of circulation of AIV in passerine birds during spring and the wintering periods. Finally, even if the prevalence of infection was very low, AIVs were found in gulls in breeding colonies, indicating a possible specific circulation in spring in these birds.

Wintering French mallard and teal are heavier and in better body condition than 30 years ago: effects of a changing environment?

Animal populations are exposed to large-scale anthropogenic impact from, e.g., climate change, habitat alteration and supplemental stocking. All of these may affect body condition in wintering dabbling ducks, which in turn may affect an individual's survival and reproductive success. The aim of this study was to assess whether there have been morphometric changes in Mallard (Anas platyrhynchos) and Teal (Anas crecca) over the last 30 years at a major wintering site. Body mass and condition increased from the 1950s-1960s to the 2000s in both species. The increase in body mass amounted to as much as 11.7%, with no corresponding change in body size. Improved body condition was maintained from early to mid-winter, but then converged with historical values for late winter. Our interpretation is that increasingly benign ambient winter conditions permit ducks to maintain better energetic "safety margins" throughout winter, and that converging spring departure values may be related to evolutionary flight energetic optima. The observed changes are consistent with large-scale climate amelioration and local/regional habitat improvement (both anthropogenic).

Prevalence of West Nile virus neutralizing antibodies in wild birds from the Camargue area, southern France.

The Camargue area of southern France experienced the re-emergence of West Nile Virus (WNV) in the late summer of 2000 and 2004. Immediately preceding the 2004 outbreak, samples were collected from 432 birds of 32 different species captured in mist nets and from 201 Cattle Egret (Bubulcus ibis) nestlings sampled in their nests between 1 April and 12 June 2004. West Nile virus neutralizing titers of >/=40 were detected in 4.8% (95% confidence limit, 2.9-7.5%) of the adult birds and in 1.6% (0.3-4.6%) of the egret nestlings. Migratory passerines had a higher prevalence of WNV neutralizing antibodies (7.0%) than did resident and short-distance migratory passerines (0.8%), suggesting exposure to WNV or a related flavivirus during overwintering in Africa.

Absence of detection of highly pathogenic H5N1 in migratory waterfowl in southern France in 2005-2006.

During fall 2005, the rapid and wide spread of highly pathogenic (HP) H5N1 avian influenza viruses (AIV) outside Asia alerted European health authorities. Because of abnormal and recurrent field mortality, wild migratory birds were considered to be the main dispersing agent of the virus at an intercontinental scale. European wintering wetlands, such as the Camargue (Rhône delta, France), are identified as potential hot spots for the risk of introduction and transmission of bird-borne diseases. In this study, we investigated the role of migratory waterbirds (mainly ducks) in the spread of HP H5N1 viruses. We combined molecular analysis of living and freshly killed birds with population surveillance (aerial censuses and death surveillance). We sampled 1345 birds belonging to 17 waterbird species (3 orders) in the Camargue between September 2005 and March 2006. The prevalence of AIV was 1.8%. We did not detect HP H5N1 virus. Population censuses did not reveal any population decreases nor abnormal mortalities. We discuss, in the light of these results, the implication of wild migratory ducks in the arrival of HP H5N1 AIV in Europe.

Influenza A virus in birds during spring migration in the Camargue, France.

Wild aquatic birds are considered to be the natural reservoir for influenza A viruses, and previous studies have focused mainly on species in the orders Anseriformes and Charadriiformes. In this study, we surveyed a larger spectrum of potential hosts belonging to 10 avian orders. Cloacal swabs (n=1,044) from 72 free-living bird species, were analysed by reverse transcription-polymerase chain reaction for the presence of avian influenza virus. Only two Mediterranean Gulls (Larus melanocephalus) tested positive; one of these viruses was identified as an H9N2 subtype. The absence of infection among passerine birds supports the idea that the prevalence of avian influenza virus infection in terrestrial species is low.

Impact of the insecticide Alphacypermetrine and herbicide Oxadiazon, used singly or in combination, on the most abundant frog in French rice fields, Pelophylax perezi.

The potential impact of agricultural pesticides is a major concern with regard to biodiversity conservation. Pesticides are considered as one of the main causes of the worldwide decline of Amphibians. They are rarely used singly, but their cumulative impact and interaction are often neglected, as is the importance of the age or stage of the animal on which the impact of the molecules is assessed. We therefore tested the potential cumulative impact of the only authorized insecticide (Alphacypermetrine) and the main herbicide (Oxadiazon) used in French rice fields on four replicates of 25 eggs, young larvae and prometamorphosis tadpoles of the most abundant frog in paddies (Pelophylax perezi). We found no significant effect of the insecticide and herbicide, used singly or in combination, on hatching and young tadpoles. However, we found a strong impact of insecticide and herbicide used singly and a highly deleterious impact of their combined use on prometamorphosis tadpoles. Among the four replicates, only one of the prometamorphosis tadpoles did not reach this adult stage in the control against 9, 9, 6, 4 and 13, 9, 8, 7 with the herbicide and insecticide, respectively. But when the two pesticides were used in combination, only two prometamorphosis tapdoles reached the adult stage. Our results emphasize the potential impact on amphibians of pesticides used in agriculture and highlight the necessity of testing their role as cocktails. They also stress the importance of the age and/or stage of the target organism, the choice of which can lead to contrasting conclusions. Finally, our results suggest a possible underestimation of the impact of pesticides on non-targeted fauna in the rice fields in particular, and on living organisms in general.

Recurrent evolution of host-specialized races in a globally distributed parasite.

The outcome of coevolutionary interactions is predicted to vary across landscapes depending on local conditions and levels of gene flow, with some populations evolving more extreme specializations than others. Using a globally distributed parasite of colonial seabirds, the tick Ixodes uriae, we examined how host availability and geographic isolation influences this process. In particular, we sampled ticks from 30 populations of six different seabird host species, three in the Southern Hemisphere and three in the Northern Hemisphere. We show that parasite races have evolved independently on hosts of both hemispheres. Moreover, the degree of differentiation between tick races varied spatially within each region and suggests that the divergence of tick races is an ongoing process that has occurred multiple times across isolated areas. As I. uriae is vector to the bacterium responsible for Lyme disease Borrelia burgdorferi sensu lato, these results may have important consequence for the epidemiology of this disease. With the increased occurrence of novel interspecific interactions due to global change, these results also stress the importance of the combined effects of gene flow and selection for parasite diversification.

Mercury concentrations in king penguin (Aptenodytes patagonicus) feathers at Crozet Islands (sub-Antarctic): temporal trend between 1966--1974 and 2000--2001.

Remote sub-Antarctic islands and their wildlife may be contaminated by mercury via atmospheric and oceanic currents. Because of mercury's high toxicity and its capacity to be biomagnified in marine food chains, top predators like seabirds may be threatened by secondary poisoning. The present study provides data regarding mercury concentrations in breast feathers sampled in 2000 and 2001 on king penguins (Aptenodytes patagonicus) living at Crozet Islands. These contemporary concentrations were compared to those measured in feathers of king penguins sampled in the same colony between 1966 and 1974 and preserved in a museum (1970s sample). The average concentration of the contemporary sample is 1.98 microg g(-1) (dry mass) and is significantly different than the concentrations reported in some other penguin species. The concentration of the contemporary sample is significantly lower than the concentration of the 1970s sample (2.66 microg g(-1)). This suggests that mercury concentrations in southern hemisphere seabirds do not increase, which conflicts with the trends observed in the northern hemisphere. This difference in temporal trends between the northern and southern hemispheres usually is attributed mainly to a higher degree of pollutant emission in the northern hemisphere. Parameters that may explain the interspecies differences in mercury concentrations are discussed. These first results may constitute a basis for further ecotoxicological and/or biomonitoring studies of king penguins in these remote ecosystems.

Waterfowl foraging in winter-flooded ricefields: Any agronomic benefits for farmers?

Winter-flooding of ricefields provides foraging habitat to waterfowl, which in return may bring agronomic benefits to farmers. Our study experimentally tested the effect of mallards (Anas platyrhynchos) on the standing stalks and weed seed bank in the Camargue (France), both of which present major challenges for farmers. Three duck densities were tested: (D1) 5 ducks ha(-1) (historical nocturnal density), (D2) 23 ducks ha(-1) (present nocturnal density), and (D3) 300 ducks ha(-1) (Asian rice-duck farming density). The ducks reduced the stalks significantly: -27 % (D1), -52 % (D2), and -91 % (D3). Conversely, they decreased the number of seeds by only 3 % (D3) and the seed mass by about 21 % (D1 and D3), which was not significant. Besides they had no effect on seed species richness. This study clearly demonstrates that the winter-flooding effect on straw decomposition can be enhanced by waterfowl foraging, hence showing an agronomic benefit from ducks to farmers. However, there was no clear effect in terms of seed bank reduction.

Combining correlative and mechanistic habitat suitability models to improve ecological compensation.

Only a few studies have shown positive impacts of ecological compensation on species dynamics affected by human activities. We argue that this is due to inappropriate methods used to forecast required compensation in environmental impact assessments. These assessments are mostly descriptive and only valid at limited spatial and temporal scales. However, habitat suitability models developed to predict the impacts of environmental changes on potential species' distributions should provide rigorous science-based tools for compensation planning. Here we describe the two main classes of predictive models: correlative models and individual-based mechanistic models. We show how these models can be used alone or synoptically to improve compensation planning. While correlative models are easier to implement, they tend to ignore underlying ecological processes and lack accuracy. On the contrary, individual-based mechanistic models can integrate biological interactions, dispersal ability and adaptation. Moreover, among mechanistic models, those considering animal energy balance are particularly efficient at predicting the impact of foraging habitat loss. However, mechanistic models require more field data compared to correlative models. Hence we present two approaches which combine both methods for compensation planning, especially in relation to the spatial scale considered. We show how the availability of biological databases and software enabling fast and accurate population projections could be advantageously used to assess ecological compensation requirement efficiently in environmental impact assessments.

First detection of Borrelia burgdorferi sensu lato DNA in king penguins (Aptenodytes patagonicus halli).

The hard tick Ixodes uriae parasitises a wide range of seabird species in the circumpolar areas of both Northern and Southern hemispheres and has been shown to be infected with Borrelia burgdorferi sensu lato, the bacterial agents of Lyme borreliosis. Although it is assumed that seabirds represent viable reservoir hosts, direct demonstrations of infection are limited to a single study from the Northern hemisphere. Here, the blood of 50 tick-infested adult king penguins (Aptenodytes patagonicus halli) breeding in the Crozet Archipelago (Southern Indian Ocean) was examined for B. burgdorferi sl exposure by serology and for spirochetemia by in vitro DNA amplification. Four birds were found positive by serology, whereas B. burgdorferi sl DNA was detected in two other birds. Our data therefore provide the first direct proof of Borrelia burgdorferi sl spirochetes in seabirds of the Southern hemisphere and indicate a possible reservoir role for king penguins in the natural maintenance of this bacterium. Although the bacterial genetic diversity present in these hosts and the infectious period for tick vectors remain to be elucidated, our results add to a growing body of knowledge on the contribution of seabirds to the complex epizootiology of Lyme disease and the global dissemination of B. burgdorferi sl spirochetes.