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1.  Storms drive altitudinal migration in a tropical bird 
Although migration is a widespread and taxonomically diverse behaviour, the ecological factors shaping migratory behaviour are poorly understood. Like other montane taxa, many birds migrate along elevational gradients in the tropics. Forty years ago, Alexander Skutch postulated that severe storms could drive birds to migrate downhill. Here, we articulate a novel mechanism that could link storms to mortality risks via reductions in foraging time and provide, to our knowledge, the first tests of this hypothesis in the White-ruffed Manakin (Corapipo altera), a small partially migratory frugivore breeding on the Atlantic slope of Costa Rica. As predicted, variation in rainfall was associated with plasma corticosterone levels, fat stores, plasma metabolites and haematocrit. By collecting data at high and low elevation sites simultaneously, we also found that high-elevation residents were more adversely affected by storms than low elevation migrants. These results, together with striking temporal capture patterns of altitudinal migrants relative to storms, provide, to our knowledge, the first evidence that weather-related risks incurred by species requiring high food intake rates can explain altitudinal migrations of tropical animals. These findings resolve conflicting evidence for and against food limitation being important in the evolution of this behaviour, and highlight how endogenous and exogenous processes influence life-history trade-offs made by individuals in the wild. Because seasonal storms are a defining characteristic of most tropical ecosystems and rainfall patterns will probably change in ensuing decades, these results have important implications for understanding the ecology, evolution and conservation of tropical animals.
PMCID: PMC2894928  PMID: 20375047
allostasis; climate change; foraging; metabolism; partial migration; tropical forest
2.  Energetics of the acrobatic courtship in male golden-collared manakins (Manacus vitellinus) 
In lek mating systems, females choose mates through indicators of quality, which males may exhibit by their performance of courtship displays. In temperate regions, displaying seasons are brief (one to two months), whereas in the tropics courtship seasons may be prolonged. Moreover, in temperate-breeding animals lekking behaviour can be energetically demanding, but little is known about the energy costs of lekking in tropical animals. Daily, over the course of a nearly seven-month-long breeding season, male golden-collared manakins (Manacus vitellinus) of Panamanian rainforests perform acrobatic courtship displays that markedly elevate heart rates, suggesting that they require high energy investment. Typically, animals of tropical lowland forests (such as manakins) exhibit a ‘slow pace of life’ metabolic strategy. We investigated whether male manakin courtship is indeed metabolically costly or whether the birds retain a low daily energy expenditure (DEE), as seen in other tropical species. To assess these questions, we calibrated manakin heart rate against metabolic rate, examined daily lek activity and, using telemetry, obtained heart rates of individual wild, lekking male manakins. Although metabolic rates peak during courtship displays, we found that males actually invest minimal time (only approx. 5 min d−1) performing displays. As a consequence, the DEE of approximately 39 kJ d−1 for male manakins is comparable to other lowland tropical species. The short, intense bursts of courtship by these birds make up only approximately 1.2% of their total DEE. Presumably, this cost is negligible, enabling them to perform daily at their arenas for months on end.
PMCID: PMC3871312  PMID: 24352944
energetics; heart rate telemetry; courtship; tropics; manakins
3.  When the Seasons Don't Fit: Speedy Molt as a Routine Carry-Over Cost of Reproduction 
PLoS ONE  2013;8(1):e53890.
The failure of animals to fit all life-cycle stages into an annual cycle could reduce the chances of successful breeding. In some cases, non-optimal strategies will be adopted in order to maintain the life-cycle within the scope of one year. We studied trade-offs made by a High Arctic migrant shorebird, the red knot Calidris canutus islandica, between reproduction and wing feather molt carried out in the non-breeding period in the Dutch Wadden Sea. We compared primary molt duration between birds undertaking the full migratory and breeding schedule with birds that forego breeding because they are young or are maintained in captivity. Molt duration was ca. 71 days in breeding adults, which was achieved by an accelerated feather replacement strategy. Second-year birds and captive adults took ca. 22% and 27% longer, respectively. Second-year birds start molt in late June, more than four weeks before captive adults, and almost seven weeks before adults that return from breeding in late July–August. Adults finish molt in October when steeply increasing thermostatic costs and reductions in food availability occur. Primary molt duration was longer in female than in male knots (all ages), which was accordance with the somewhat larger body size of females. Since fast growth leads to lower quality feathers, the speedy wing molt shown by Arctic-breeding birds may represent a time constraint that is an unavoidable and routine cost of reproduction. So far it was hypothesized that only birds over 1 kg would have difficulty fitting molt within a year. Here we show that in birds an order of magnitude smaller, temporal imperatives may impose the adoption of non-optimal life-cycle routines in the entire actively breeding population.
PMCID: PMC3547963  PMID: 23349758
4.  Optimal Conservation of Migratory Species 
PLoS ONE  2007;2(8):e751.
Migratory animals comprise a significant portion of biodiversity worldwide with annual investment for their conservation exceeding several billion dollars. Designing effective conservation plans presents enormous challenges. Migratory species are influenced by multiple events across land and sea–regions that are often separated by thousands of kilometres and span international borders. To date, conservation strategies for migratory species fail to take into account how migratory animals are spatially connected between different periods of the annual cycle (i.e. migratory connectivity) bringing into question the utility and efficiency of current conservation efforts.
Methodology/Principal Findings
Here, we report the first framework for determining an optimal conservation strategy for a migratory species. Employing a decision theoretic approach using dynamic optimization, we address the problem of how to allocate resources for habitat conservation for a Neotropical-Nearctic migratory bird, the American redstart Setophaga ruticilla, whose winter habitat is under threat. Our first conservation strategy used the acquisition of winter habitat based on land cost, relative bird density, and the rate of habitat loss to maximize the abundance of birds on the wintering grounds. Our second strategy maximized bird abundance across the entire range of the species by adding the constraint of maintaining a minimum percentage of birds within each breeding region in North America using information on migratory connectivity as estimated from stable-hydrogen isotopes in feathers. We show that failure to take into account migratory connectivity may doom some regional populations to extinction, whereas including information on migratory connectivity results in the protection of the species across its entire range.
We demonstrate that conservation strategies for migratory animals depend critically upon two factors: knowledge of migratory connectivity and the correct statement of the conservation problem. Our framework can be used to identify efficient conservation strategies for migratory taxa worldwide, including insects, birds, mammals, and marine organisms.
PMCID: PMC1937026  PMID: 17710150
5.  Travelling on a budget: predictions and ecological evidence for bottlenecks in the annual cycle of long-distance migrants 
Long-distance migration, and the study of the migrants who undertake these journeys, has fascinated generations of biologists. However, many aspects of the annual cycles of these migrants remain a mystery as do many of the driving forces behind the evolution and maintenance of the migrations themselves. In this article we discuss nutritional, energetic, temporal and disease-risk bottlenecks in the annual cycle of long-distance migrants, taking a sandpiper, the red knot Calidris canutus, as a focal species. Red knots have six recognized subspecies each with different migratory routes, well-known patterns of connectivity and contrasting annual cycles. The diversity of red knot annual cycles allows us to discuss the existence and the effects of bottlenecks in a comparative framework. We examine the evidence for bottlenecks focusing on the quality of breeding plumage and the timing of moult as indicators in the six subspecies. In terms of breeding plumage coloration, quality and timing of prealternate body moult (from non-breeding into breeding plumage), the longest migrating knot subspecies, Calidris canutus rogersi and Calidris canutus rufa, show the greatest impact of bottlenecking. The same is true in terms of prebasic body moult (from breeding into non-breeding plumage) which in case of both C. c. rogersi and C. c. rufa overlaps with southward migration and may even commence in the breeding grounds. To close our discussion of bottlenecks in long-distance migrants, we make predictions about how migrants might be impacted via physiological ‘trade-offs’ throughout the annual cycle, using investment in immune function as an example. We also predict how bottlenecks may affect the distribution of mortality throughout the annual cycle. We hope that this framework will be applicable to other species and types of migrants, thus expanding the comparative database for the future evaluation of seasonal selection pressures and the evolution of annual cycles in long-distance migrants. Furthermore, we hope that this synthesis of recent advancements in the knowledge of red knot annual cycles will prove useful in the ongoing attempts to model annual cycles in migratory birds.
PMCID: PMC2606749  PMID: 17638692
red knot; Calidris canutus; migration; annual cycle; plumage; moult
6.  Female Preference and Predation Risk Models Can Explain the Maintenance of a Fallow Deer (Dama dama) Lek and Its ‘Handy’ Location 
PLoS ONE  2014;9(3):e89852.
We tested the predictions of three models (female preference; hotspot; predator avoidance) on lek formation in the fallow deer population of San Rossore, Tuscany. We collected behavioural observations in two leks and radiotracking data on 67 deer over 7 years. Two deer sub-populations were present in the northern and southern sides of the area, respectively, the two sectors being delimited by a river and including one lek each. Predictions were tested for one lek (SG), located in the south-side where we set up our 7-year radiotracking program. Data from a second lek (FO, north-side) were used to test those predictions which imply the occurrence of multiple leks in the same population. We showed that the majority of females made one single visit to one lek, only during the rut. The lek was located outside areas of higher female traffic and home range overlap, and females increased home range sizes during the rut to reach it. Twilight routes of females never crossed the lek; instead, females walked atypical routes and at a faster pace to reach the lek and mate. The distance between the two leks was higher than the average diameter of female home ranges, and only one lek was present within female home ranges. Males reached the lek one month before the arrival of females, corroborating that lekking is a female-initiated process (females moving towards large clumped male aggregations) rather than a male-initiated process (males moving towards female hotspots). Our results supported the female preference model, and rejected the predictions of the hotspot model. Also, leks were located far from areas with higher predation risk, supporting the predator avoidance model. The position of lek SG resulted ‘handy’ at the sub-population level because of the optimal trade-off between travel costs for females to reach it and avoidance of human predators.
PMCID: PMC3943860  PMID: 24599036
7.  Bats on a Budget: Torpor-Assisted Migration Saves Time and Energy 
PLoS ONE  2014;9(12):e115724.
Bats and birds must balance time and energy budgets during migration. Migrating bats face similar physiological challenges to birds, but nocturnality creates special challenges for bats, such as a conflict between travelling and refueling, which many birds avoid by feeding in daylight and flying at night. As endothermic animals, bats and birds alike must expend substantial amounts of energy to maintain high body temperatures. For migratory birds refueling at stopovers, remaining euthermic during inactive periods reduces the net refuelling rate, thereby prolonging stopover duration and delaying subsequent movement. We hypothesized that bats could mitigate similar ambient-temperature dependent costs by using a torpor-assisted migration strategy. We studied silver-haired bats Lasionycteris noctivagans during autumn migration using a combination of respirometry and temperature-sensitive radiotelemetry to estimate energy costs incurred under ambient temperature conditions, and the energy that bats saved by using torpor during daytime roosting periods. All bats, regardless of sex, age, or body condition used torpor at stopover and saved up to 91% of the energy they would have expended to remain euthermic. Furthermore, bats modulated use of torpor depending on ambient temperature. By adjusting the time spent torpid, bats achieved a rate of energy expenditure independent of the ambient temperature encountered at stopover. By lowering body temperature during inactive periods, fuel stores are spared, reducing the need for refuelling. Optimal migration models consider trade-offs between time and energy. Heterothermy provides a physiological strategy that allows bats to conserve energy without paying a time penalty as they migrate. Although uncommon, some avian lineages are known to use heterothermy, and current theoretical models of migration may not be appropriate for these groups. We propose that thermoregulatory strategies should be an important consideration of future migration studies of both bats and birds.
PMCID: PMC4281203  PMID: 25551615
8.  Understanding testosterone variation in a tropical lek-breeding bird 
Biology Letters  2011;7(4):506-509.
Male reproductive coalitions, in which males cooperate to attract females, are a rare strategy among vertebrates. While some studies have investigated ultimate aspects of these relationships, little is known about the mechanistic role that hormones play in modulating cooperative behaviours. Here, we examined male testosterone variation in a tropical lekking bird, the wire-tailed manakin (Pipra filicauda), which exhibits cooperative male–male display coalitions. We found that testosterone levels in territorial males were comparable to those of temperate breeding birds, a surprising result given their environmental, social and reproductive dynamics. In addition, social status rather than plumage was a strong predictor of testosterone variation. Territorial males had significantly higher testosterone levels than did two other plumage classes of floater males, who do not hold territories. We hypothesize that testosterone variation plays an important role in the establishment of male dominance hierarchies (competition), while concurrently facilitating stable display partnerships (cooperation).
PMCID: PMC3130229  PMID: 21325306
cooperation; competition; lekking; reproductive coalitions; testosterone; wire-tailed manakin
9.  A Currency for Offsetting Energy Development Impacts: Horse-Trading Sage-Grouse on the Open Market 
PLoS ONE  2010;5(4):e10339.
Biodiversity offsets provide a mechanism to compensate for unavoidable damages from new energy development as the U.S. increases its domestic production. Proponents argue that offsets provide a partial solution for funding conservation while opponents contend the practice is flawed because offsets are negotiated without the science necessary to backup resulting decisions. Missing in negotiations is a biologically-based currency for estimating sufficiency of offsets and a framework for applying proceeds to maximize conservation benefits.
Methodology/Principal Findings
Here we quantify a common currency for offsets for greater sage-grouse (Centrocercus urophasianus) by estimating number of impacted birds at 4 levels of development commonly permitted. Impacts were indiscernible at 1–12 wells per 32.2 km2. Above this threshold lek losses were 2–5 times greater inside than outside of development and bird abundance at remaining leks declined by −32 to −77%. Findings reiterated the importance of time-lags as evidenced by greater impacts 4 years after initial development. Clustering well locations enabled a few small leks to remain active inside of developments.
Documented impacts relative to development intensity can be used to forecast biological trade-offs of newly proposed or ongoing developments, and when drilling is approved, anticipated bird declines form the biological currency for negotiating offsets.
Monetary costs for offsets will be determined by true conservation cost to mitigate risks such as sagebrush tillage to other populations of equal or greater number. If this information is blended with landscape level conservation planning, the mitigation hierarchy can be improved by steering planned developments away from conservation priorities, ensuring compensatory mitigation projects deliver a higher return for conservation that equate to an equal number of birds in the highest priority areas, provide on-site mitigation recommendations, and provide a biologically based cost for mitigating unavoidable impacts.
PMCID: PMC2860982  PMID: 20442770
10.  Size and accumulation of fuel reserves at stopover predict nocturnal restlessness in a migratory bird 
Biology Letters  2013;9(6):20130712.
Early arrival at the breeding site positively affects the breeding success of migratory birds. During migration, birds spend most of their time at stopovers. Therefore, determining which factors shape stopover duration is essential to our understanding of avian migration. Because the main purpose of stopover is to accumulate fat as fuel for the next flight bout, fuel reserves at arrival and the accumulation of fuel are both expected to affect stopover departure decisions. Here, we determined whether fuel reserves and fuel accumulation predict a bird's motivation to depart, as quantified by nocturnal migratory restlessness (Zugunruhe), using northern wheatears (Oenanthe oenanthe) that were captured and temporarily contained at spring stopover. We found that fuel reserves at capture were positively correlated with Zugunruhe, and negatively correlated with fuel accumulation. This indicates that fat birds were motivated to depart, whereas lean birds were set on staying and accumulating fuel. Moreover, the change in fuel reserves was positively correlated with the concurrent change in Zugunruhe, providing the first empirical evidence for a direct link between fuel accumulation and Zugunruhe during stopover. Our study indicates that, together with innate rhythms and weather, the size and accumulation of fuel reserves shape stopover duration, and hence overall migration time.
PMCID: PMC3871357  PMID: 24132097
fuel reserves; migratory restlessness; Zugunruhe; stopover; migration; bird
11.  Testing an Emerging Paradigm in Migration Ecology Shows Surprising Differences in Efficiency between Flight Modes 
PLoS ONE  2012;7(4):e35548.
To maximize fitness, flying animals should maximize flight speed while minimizing energetic expenditure. Soaring speeds of large-bodied birds are determined by flight routes and tradeoffs between minimizing time and energetic costs. Large raptors migrating in eastern North America predominantly glide between thermals that provide lift or soar along slopes or ridgelines using orographic lift (slope soaring). It is usually assumed that slope soaring is faster than thermal gliding because forward progress is constant compared to interrupted progress when birds pause to regain altitude in thermals. We tested this slope-soaring hypothesis using high-frequency GPS-GSM telemetry devices to track golden eagles during northbound migration. In contrast to expectations, flight speed was slower when slope soaring and eagles also were diverted from their migratory path, incurring possible energetic costs and reducing speed of progress towards a migratory endpoint. When gliding between thermals, eagles stayed on track and fast gliding speeds compensated for lack of progress during thermal soaring. When thermals were not available, eagles minimized migration time, not energy, by choosing energetically expensive slope soaring instead of waiting for thermals to develop. Sites suited to slope soaring include ridges preferred for wind-energy generation, thus avian risk of collision with wind turbines is associated with evolutionary trade-offs required to maximize fitness of time-minimizing migratory raptors.
PMCID: PMC3338847  PMID: 22558166
12.  Different Means to the Same End: Long-Distance Migrant Seabirds from Two Colonies Differ in Behaviour, Despite Common Wintering Grounds 
PLoS ONE  2011;6(10):e26079.
Although seabirds that are trans-equatorial migrants show apparently broad overlap among populations in the non-breeding season, such large-scale pattern may conceal subtle but nevertheless key differences in migratory behaviour. These specializations could reflect adaptation to different environments during the breeding season, carry-over effects from the breeding to the nonbreeding period, or asymmetries in competitive ability of birds of different origin. We compared the migratory and wintering behaviour of Cory's shearwaters Calonectris diomedea nesting in Berlengas and in the Selvagens, two colonies in contrasting oceanographic environments, separated by ca. 1200 km. Although no differences were found in winter distribution, there was a marked divergence in timing, route and the use of staging areas during the postbreeding (autumn) migration. Birds from Berlengas typically travelled to oceanic waters in the North Atlantic for an extended stopover, whereas those from Selvagens rarely did so. In the South Atlantic, birds from Selvagens spent more time in flight, perhaps because they had higher energy and nutrient requirements for feather replacement compared to birds from Berlengas, which moult more flight feathers during breeding. Stable isotope analyses of feathers suggested that this variation in activity patterns was unrelated to trophic ecology. Differences in migration routes and stopovers may expose populations to distinct threats, and should be taken into consideration when defining units for conservation purposes and developing appropriate management strategies.
PMCID: PMC3191162  PMID: 22022513
13.  Weather, host and vector — their interplay in the spread of insect-borne animal virus diseases 
The Journal of Hygiene  1980;85(1):65-102.
The spread of insect-borne animal virus diseases is influenced by a number of factors. Hosts migrate, move or are conveyed over long distances: vectors are carried on the wind for varying distances in search of hosts and breeding sites; weather and climate affect hosts and vectors through temperature, moisture and wind. As parasites of host and vector, viruses are carried by animals, birds and insects, and their spread can be correlated with the migration of hosts and the carriage of vectors on winds associated with the movements of the Intertropical Convergence Zone (ITCZ) and warm winds to the north and south of the limits of the ITCZ. The virus is often transmitted from a local cycle to a migratory cycle and back again.
Examples of insect-borne virus diseases and their spread are analysed. Japanese, Murray Valley, Western equine, Eastern equine and St Louis encephalitis represent viruses transmitted by mosquito—bird or pig cycles.
The areas experiencing infection with these viruses can be divided into a number of zones: A, B, C, D, E and F. In zone A there is a continuous cycle of virus in host and vector throughout the year; in zone B, there is an upsurge in the cycle during the wet season, but the cycle continues during the dry season; there is movement of infected vectors between and within zones A and B on the ITCZ and the virus is introduced to zone C by infected vectors on warm winds; persistence may occur in zone C if conditions are right. In zone D, virus is introduced each year by infected vectors on warm winds and the arrival of the virus coincides with the presence of susceptible nestling birds and susceptible piglets. The disappearance of virus occurs at the time when migrating mosquitoes and birds are returning to warmer climates. The virus is introduced to zone E only on occasions every 5-10 years when conditions are suitable. Infected hosts introduced to zone F do not lead to circulation of virus, since the climate is unsuitable for vectors. Zones A, B and C correspond to endemic and zones D and E to epidemic conditions.
Similar zones can be recognized for African horse sickness, bluetongue, Ibaraki disease and bovine ephemeral fever — examples of diseases transmitted in a midge-mammal cycle. In zones A and B viruses are transported by infected midges carried on the wind in association with the movement of ITCZ and undergo cycles in young animals. In these zones and in zone C there is a continual movement of midges on the warm wind between one area and another, colonizing new sites or reinforcing populations of midges already present. Virus is introduced at times into fringe areas (zones D and E) and, as there is little resistance in the host, gives rise to clinical signs of disease. In some areas there is persistence during adverse conditions; in others, the virus is carried back to the endemic zones by infected midges or vectors.
Examples of viruses maintained in a mosquito/biting fly—mammal cycle are Venezuelan equine encephalitis and vesicular stomatitis. These viruses enter a migratory cycle from a local cycle and the vectors in the migratory cycle are carried over long distances on the wind. Further examples of virus spread by movement of vectors include West Nile, Rift Valley fever, yellow fever, epizootic haemorrhagic disease of deer and Akabane viruses.
In devising means of control it is essential to decide the relationship of host, vector and virus and the nature of the zone in which the area to be controlled lies. Because of the continual risk of reintroduction of infected vectors, it is preferable to protect the host by dipping, spraying or by vaccination rather than attempting to eliminate the local population of insects.
PMCID: PMC2134001  PMID: 6131919
14.  Maladaptive Habitat Selection of a Migratory Passerine Bird in a Human-Modified Landscape 
PLoS ONE  2011;6(9):e25703.
In human-altered environments, organisms may preferentially settle in poor-quality habitats where fitness returns are lower relative to available higher-quality habitats. Such ecological trapping is due to a mismatch between the cues used during habitat selection and the habitat quality. Maladaptive settlement decisions may occur when organisms are time-constrained and have to rapidly evaluate habitat quality based on incomplete knowledge of the resources and conditions that will be available later in the season. During a three-year study, we examined settlement decision-making in the long-distance migratory, open-habitat bird, the Red-backed shrike (Lanius collurio), as a response to recent land-use changes. In Northwest Europe, the shrikes typically breed in open areas under a management regime of extensive farming. In recent decades, Spruce forests have been increasingly managed with large-size cutblocks in even-aged plantations, thereby producing early-successional vegetation areas that are also colonised by the species. Farmland and open areas in forests create mosaics of two different types of habitats that are now occupied by the shrikes. We examined redundant measures of habitat preference (order of settlement after migration and distribution of dominant individuals) and several reproductive performance parameters in both habitat types to investigate whether habitat preference is in line with habitat quality. Territorial males exhibited a clear preference for the recently created open areas in forests with higher-quality males settling in this habitat type earlier. Reproductive performance was, however, higher in farmland, with higher nest success, offspring quantity, and quality compared to open areas in forests. The results showed strong among-year consistency and we can therefore exclude a transient situation. This study demonstrates a case of maladaptive habitat selection in a farmland bird expanding its breeding range to human-created open habitats in plantations. We discuss the reasons that could explain this decision-making and the possible consequences for the population dynamics and persistence.
PMCID: PMC3184164  PMID: 21984940
15.  What shall I do now? State-dependent variations of life-history traits with aging in Wandering Albatrosses 
Ecology and Evolution  2014;4(4):474-487.
Allocation decisions depend on an organism's condition which can change with age. Two opposite changes in life-history traits are predicted in the presence of senescence: either an increase in breeding performance in late age associated with terminal investment or a decrease due to either life-history trade-offs between current breeding and future survival or decreased efficiency at old age. Age variation in several life-history traits has been detected in a number of species, and demographic performances of individuals in a given year are influenced by their reproductive state the previous year. Few studies have, however, examined state-dependent variation in life-history traits with aging, and they focused mainly on a dichotomy of successful versus failed breeding and non-breeding birds. Using a 50-year dataset on the long-lived quasi-biennial breeding wandering albatross, we investigated variations in life-history traits with aging according to a gradient of states corresponding to potential costs of reproduction the previous year (in ascending order): non-breeding birds staying at sea or present at breeding grounds, breeding birds that failed early, late or were successful. We used multistate models to study survival and decompose reproduction into four components (probabilities of return, breeding, hatching, and fledging), while accounting for imperfect detection. Our results suggest the possible existence of two strategies in the population: strict biennial breeders that exhibited almost no reproductive senescence and quasi-biennial breeders that showed an increased breeding frequency with a strong and moderate senescence on hatching and fledging probabilities, respectively. The patterns observed on survival were contrary to our predictions, suggesting an influence of individual quality rather than trade-offs between reproduction and survival at late ages. This work represents a step further into understanding the evolutionary ecology of senescence and its relationship with costs of reproduction at the population level. It paves the way for individual-based studies that could show the importance of intra-population heterogeneity in those processes.
PMCID: PMC3936393  PMID: 24634731
Bienniality; breeding probability and success; capture–mark–recapture; cost of reproduction; Diomedea exulans; failure; survival.
16.  The evolution of cuckoo parasitism: a comparative analysis. 
Cuckoos (family Cuculidae) show the highest diversity of breeding strategies within one bird family (parental care, facultative and obligate brood parasites). We used independent contrasts from two phylogenies to examine how this variation was related to 13 ecological and life-history variables. The ancestral state was probably tropical, resident, forest cuckoos with parental care. The evolution of brood parasitism was correlated with a shift to more open habitats, a change in diet, increases in species breeding-range size and migration, and a decrease in egg size. Once parasitism had evolved, more elaborate parasitic strategies (more harmful to host fitness) were correlated with decreased egg size, a change in diet, increased breeding-range size and migration, a shortened breeding season and a decrease in local abundance. Establishing the most probable evolutionary pathways, using the method of Pagel, shows that changes in ecological variables (such as migration, range size and diet type) preceded the evolution of brood parasitism, which is likely to be a later adaptation to reduce the cost of reproduction. By contrast, brood parasitism evolved before changes in egg size occurred, indicating that egg size is an adaptive trait in host--parasite coevolution. Our results suggest that the evolution of cuckoo brood parasitism reflects selection from both ecological pressures and host defences.
PMCID: PMC1690908  PMID: 11886625
17.  Do the Ticks of Birds at an Important Migratory Hotspot Reflect the Seasonal Dynamics of Ixodes ricinus at the Migration Initiation Site? A Case Study in the Danube Delta 
PLoS ONE  2014;9(2):e89378.
Migratory birds play important roles as distributors of ticks within and between continents. In the Old World, the most important migratory route of birds links Asia, Europe and Africa. During their migration, birds use various stopover sites, where they feed and rest and where ticks may attach or detach, creating new natural foci for vector-borne diseases. Danube Delta is one of the most important migration hotspots and so far no studies were focused on ticks of migratory birds herein. The aim of the present study was to assess the species diversity and seasonal dynamics of ticks parasitizing migratory birds in Danube Delta Biosphere Reserve. Migratory birds were trapped on Grindul Lupilor (44°41′N; 28°56′E) using mist nets during 4 migratory seasons (2 spring and 2 autumn) in 2011 and 2012. From each bird, all the ticks were collected and identified based on morphological features. Epidemiological parameters (prevalence, mean abundance, mean intensity) were calculated and all data were analysed statistically based on the season (spring and autumn), regional status of birds (migrants and breeding) and foraging behaviour (ground feeders, reed-bed feeders, foliage feeders). A total of 1434 birds (46 species) were captured. Ticks were found on 94 birds (10 species). Significantly more migratory birds hosted ticks, compared to resident birds. The 400 collected ticks belonged to four species: Ixodes ricinus (92.25%), I. arboricola (6.25%), I. redikorzevi (1.00%) and Haemaphysalis punctata (0.50%). A higher prevalence was found for I. ricinus in spring, with higher prevalence of nymphs in this season, while larvae occurred with the same prevalence in both seasons. Larval intensity was higher during spring and nymphs were more abundant during autumn. The seasonal differences in our study may be related not to the local seasonal dynamics of ticks, but on the seasonal dynamics at the site of migration initiation.
PMCID: PMC3929702  PMID: 24586732
18.  The annual cycle of a trans-equatorial Eurasian–African passerine migrant: different spatio-temporal strategies for autumn and spring migration 
The small size of the billions of migrating songbirds commuting between temperate breeding sites and the tropics has long prevented the study of the largest part of their annual cycle outside the breeding grounds. Using light-level loggers (geolocators), we recorded the entire annual migratory cycle of the red-backed shrike Lanius collurio, a trans-equatorial Eurasian-African passerine migrant. We tested differences between autumn and spring migration for nine individuals. Duration of migration between breeding and winter sites was significantly longer in autumn (average 96 days) when compared with spring (63 days). This difference was explained by much longer staging periods during autumn (71 days) than spring (9 days). Between staging periods, the birds travelled faster during autumn (356 km d–1) than during spring (233 km d–1). All birds made a protracted stop (53 days) in Sahelian sub-Sahara on southbound migration. The birds performed a distinct loop migration (22 000 km) where spring distance, including a detour across the Arabian Peninsula, exceeded the autumn distance by 22 per cent. Geographical scatter between routes was particularly narrow in spring, with navigational convergence towards the crossing point from Africa to the Arabian Peninsula. Temporal variation between individuals was relatively constant, while different individuals tended to be consistently early or late at different departure/arrival occasions during the annual cycle. These results demonstrate the existence of fundamentally different spatio-temporal migration strategies used by the birds during autumn and spring migration, and that songbirds may rely on distinct staging areas for completion of their annual cycle, suggesting more sophisticated endogenous control mechanisms than merely clock-and-compass guidance among terrestrial solitary migrants. After a century with metal-ringing, year-round tracking of long-distance migratory songbirds promises further insights into bird migration.
PMCID: PMC3259926  PMID: 21900322
avian migration; geolocator; passerine; migration speed; phenology; migration routes
19.  Clock Gene Variation Is Associated with Breeding Phenology and Maybe under Directional Selection in the Migratory Barn Swallow 
PLoS ONE  2012;7(4):e35140.
In diverse taxa, photoperiodic responses that cause seasonal physiological and behavioural shifts are controlled by genes, including the vertebrate Clock orthologues, that encode for circadian oscillator mechanisms. While the genetic network behind circadian rhythms is well described, relatively few reports exist of the phenological consequences of and selection on Clock genes in the wild. Here, we investigated variation in breeding phenology in relation to Clock genetic diversity in a long-distance migratory bird, the barn swallow (Hirundo rustica).
Methodology/Principal Findings
In a sample of 922 adult barn swallows from a single population breeding in Italy we found one very common (Q7) and three rare (Q5, Q6, Q8) length variants of a functionally significant polyglutamine repeat. Rare (2.9%) Q7/Q8 heterozygous females, but not males, bred significantly later than common (91.5%) Q7/Q7 females, consistent with the expectation that ‘long’ alleles cause late breeding, as observed in a resident population of another bird species. Because breeding date depends on arrival date from migration, present results suggest that the association between breeding date and Clock might be mediated by migration phenology. In addition, fecundity selection appears to be operating against Q7/Q8 because late migrating/breeding swallows have fewer clutches per season, and late breeding has additional negative selection effects via reduced offspring longevity. Genotype frequencies varied marginally non-significantly with age, as Q7/Q8 frequency showed a 4-fold reduction in old individuals. This result suggests negative viability selection against Q7/Q8, possibly mediated by costs of late breeding.
This is the first study of migratory birds showing an association between breeding phenology and Clock genotype and suggesting that negative selection occurs on a phenologically deviant genotype. Low polymorphism at Clock may constrain microevolutionary phenological response to changing climate, and may thus contribute to the decline of barn swallow populations.
PMCID: PMC3323641  PMID: 22506071
20.  A Trade-Off between Reproduction and Feather Growth in the Barn Swallow (Hirundo rustica) 
PLoS ONE  2014;9(5):e96428.
Physiological trade-offs mediated by limiting energy, resources or time constrain the simultaneous expression of major functions and can lead to the evolution of temporal separation between demanding activities. In birds, plumage renewal is a demanding activity, which accomplishes fundamental functions, such as allowing thermal insulation, aerodynamics and socio-sexual signaling. Feather renewal is a very expensive and disabling process, and molt is often partitioned from breeding and migration. However, trade-offs between feather renewal and breeding have been only sparsely studied. In barn swallows (Hirundo rustica) breeding in Italy and undergoing molt during wintering in sub-Saharan Africa, we studied this trade-off by removing a tail feather from a large sample of individuals and analyzing growth bar width, reflecting feather growth rate, and length of the growing replacement feather in relation to the stage in the breeding cycle at removal and clutch size. Growth bar width of females and length of the growing replacement feather of both sexes were smaller when the original feather had been removed after clutch initiation. Importantly, in females both growth bar width and replacement feather length were negatively predicted by clutch size, and more strongly so for large clutches and when feather removal occurred immediately after clutch completion. Hence, we found strong, coherent evidence for a trade-off between reproduction, and laying effort in particular, and the ability to generate new feathers. These results support the hypothesis that the derived condition of molting during wintering in long-distance migrants is maintained by the costs of overlapping breeding and molt.
PMCID: PMC4020794  PMID: 24826890
21.  Variation in annual and lifetime reproductive success of lance-tailed manakins: alpha experience mitigates effects of senescence on siring success 
The causes of variation in individual reproductive success over a lifetime are not well understood. In long-lived vertebrates, reproductive output usually increases during early adulthood, but it is difficult to disentangle the roles of development and learning on this gain of reproductive success. Lekking lance-tailed manakins provide an opportunity to separate these processes, as the vast majority of male reproduction occurs after a bird obtains alpha status and maintains a display area in the lek, but the age at which males achieve alpha status varies widely. Using 11 years of longitudinal data on age, social status and genetic siring success, I assessed the factors influencing variation in siring success by individuals over their lifetimes. The data show increases in annual reproductive success with both age and alpha experience. At advanced ages, these gains were offset by senescence in fecundity. Individual ontogeny, rather than compositional change of the population, generated a nonlinear relationship of breeding tenure with lifetime success; age of assuming alpha status was unrelated to tenure as a breeder, or success in the alpha role. Importantly, these findings suggest that social experience can mitigate the negative effects of senescence in older breeders.
PMCID: PMC3282336  PMID: 22090386
sexual selection; longevity; reproductive tenure; senescence; Chiroxiphia; cooperative breeding
22.  Experimental Chronic Noise Is Related to Elevated Fecal Corticosteroid Metabolites in Lekking Male Greater Sage-Grouse (Centrocercus urophasianus) 
PLoS ONE  2012;7(11):e50462.
There is increasing evidence that individuals in many species avoid areas exposed to chronic anthropogenic noise, but the impact of noise on those who remain in these habitats is unclear. One potential impact is chronic physiological stress, which can affect disease resistance, survival and reproductive success. Previous studies have found evidence of elevated stress-related hormones (glucocorticoids) in wildlife exposed to human activities, but the impacts of noise alone are difficult to separate from confounding factors. Here we used an experimental playback study to isolate the impacts of noise from industrial activity (natural gas drilling and road noise) on glucocorticoid levels in greater sage-grouse (Centrocercus urophasianus), a species of conservation concern. We non-invasively measured immunoreactive corticosterone metabolites from fecal samples (FCMs) of males on both noise-treated and control leks (display grounds) in two breeding seasons. We found strong support for an impact of noise playback on stress levels, with 16.7% higher mean FCM levels in samples from noise leks compared with samples from paired control leks. Taken together with results from a previous study finding declines in male lek attendance in response to noise playbacks, these results suggest that chronic noise pollution can cause greater sage-grouse to avoid otherwise suitable habitat, and can cause elevated stress levels in the birds who remain in noisy areas.
PMCID: PMC3502302  PMID: 23185627
23.  Consistent annual schedules in a migratory shorebird 
Biology Letters  2006;2(4):517-520.
Many migratory birds start prebreeding moult and premigratory fuelling some months before the breeding season and face severe time constraints, while travelling up to 15 000 km between non-breeding and breeding grounds. Shorebirds typically leave Southern Hemisphere non-breeding areas over a 3–4 week period, but whether they benefit from interannually consistent timing of departure is unknown. Here, I show that individual bar-tailed godwits (Limosa limosa baueri) from New Zealand are highly consistent in their migratory scheduling. Most birds left within the same week each year (between-year repeatability, r, of 0.83) and adult males, which moult into a bright breeding plumage, were also highly repeatable in the extent of their prebreeding moult (r=0.86). This is consistent with the hypothesis that birds have individually optimized migration schedules. Within adult males, but not females, smaller birds tended to migrate earlier than large birds. Whether this reflects differences in size-related migration speed, optimal breeding time at different sites or size-related natural or sexual selection pressures, remains unknown.
PMCID: PMC1833993  PMID: 17148277
migration; timing; repeatability; plumage; shorebird; age differences
24.  Effects of influenza A virus infection on migrating mallard ducks 
The natural reservoir of influenza A virus is waterfowl, particularly dabbling ducks (genus Anas). Although it has long been assumed that waterfowl are asymptomatic carriers of the virus, a recent study found that low-pathogenic avian influenza (LPAI) infection in Bewick's swans (Cygnus columbianus bewickii) negatively affected stopover time, body mass and feeding behaviour. In the present study, we investigated whether LPAI infection incurred ecological or physiological costs to migratory mallards (Anas platyrhynchos) in terms of body mass loss and staging time, and whether such costs could influence the likelihood for long-distance dispersal of the avian influenza virus by individual ducks. During the autumn migrations of 2002–2007, we collected faecal samples (n=10 918) and biometric data from mallards captured and banded at Ottenby, a major staging site in a flyway connecting breeding and wintering areas of European waterfowl. Body mass was significantly lower in infected ducks than in uninfected ducks (mean difference almost 20 g over all groups), and the amount of virus shed by infected juveniles was negatively correlated with body mass. There was no general effect of infection on staging time, except for juveniles in September, in which birds that shed fewer viruses stayed shorter than birds that shed more viruses. LPAI infection did not affect speed or distance of subsequent migration. The data from recaptured individuals showed that the maximum duration of infection was on average 8.3 days (s.e. 0.5), with a mean minimum duration of virus shedding of only 3.1 days (s.e. 0.1). Shedding time decreased during the season, suggesting that mallards acquire transient immunity for LPAI infection. In conclusion, deteriorated body mass following infection was detected, but it remains to be seen whether this has more long-term fitness effects. The short virus shedding time suggests that individual mallards are less likely to spread the virus at continental or intercontinental scales.
PMCID: PMC2679067  PMID: 19129127
influenza A virus; disease ecology; migration
25.  Fixed and Flexible: Coexistence of Obligate and Facultative Migratory Strategies in a Freshwater Fish 
PLoS ONE  2014;9(3):e90294.
Migration is an important event in many animal life histories, but the degree to which individual animals participate in seasonal migrations often varies within populations. The powerful ecological and evolutionary consequences of such partial migration are now well documented, but the underlying mechanisms are still heavily debated. One potential mechanism of partial migration is between-individual variation in body condition, where animals in poor condition cannot pay the costs of migration and hence adopt a resident strategy. However, underlying intrinsic traits may overrule such environmental influence, dictating individual consistency in migratory patterns. Unfortunately, field tests of individual consistency compared to the importance of individual condition on migratory propensity are rare. Here we analyse 6 years of field data on roach migration, gathered by tagging almost 3000 individual fish and monitoring their seasonal migrations over extended periods of time. Our aims were to provide a field test of the role of condition in wild fish for migratory decisions, and also to assess individual consistency in migratory tendency. Our analyses reveal that (1) migratory strategy, in terms of migration/residency, is highly consistent within individuals over time and (2) there is a positive relationship between condition and the probability of migration, but only in individuals that adopt a migratory strategy at some point during their lives. However, life-long residents do not differ in condition to migrants, hence body condition is only a good predictor of migratory tendency in fish with migratory phenotypes and not a more general determinant of migratory tendency for the population. As resident individuals can achieve very high body condition and still remain resident, we suggest that our data provides some of the first field evidence to show that both facultative and obligate strategies can co-exist within populations of migratory animals.
PMCID: PMC3940839  PMID: 24594698

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