Unusual feather structure allows partial plumage wettability in diving great cormorants Phalacrocorax carbo

The great cormorant Phalacrocorax carbo is thought to have a wettable plumage, providing low body insulation during foraging. Great cormorants should thus be constrained by water temperatures, and show high energy requirements. Surprisingly, this species has one of the widest breeding distributions of all diving birds, and does not require more food than these other species. We explored this apparent paradox by comparing the insulative properties of body plumage in four subspecies of great cormorants ranging from tropical to polar regions. We found that all subspecies retained an insulating air layer in their plumage, which was, however, much thinner than for other species of diving birds. Detailed examination of the plumage showed that each cormorant body feather has a loose, instantaneously wet, outer section and a highly waterproof central portion. This indicates that the plumage of great cormorants is only partly wettable, and that birds maintain a thin layer of air in their plumage. Our findings suggest an unusual morphological-functional adaptation to diving which balances the antagonist constraints of thermoregulation and buoyancy.     

Behavioural strategies of cormorants (Phalacrocoracidae) foraging under challenging light conditions

Diving is indicative of foraging in cormorants (Phalacrocoracidae). We have investigated a range of parameters associated with diving in Great Cormorants Phalacrocorax carbo to provide insight into the bases of cormorant predatory strategies. We hypothesize that if vision is important in cormorant foraging behaviour, and if they are not constrained by the position of their prey in the water column, then diving behaviour will be modulated primarily in response to the diel variation in ambient light levels. Specifically, we propose that cormorants forage at shallower depths when light levels are low, and more deeply when light levels are high. We provide evidence that this is the case. We recorded the occurrence of cormorant diving behaviour using implanted data loggers and recorded ambient light levels and water temperature using leg-mounted loggers in a sample of free-living Great Cormorants in Greenland. Our results show that dives are shallower at the beginning and end of each day when light levels are lower. We suggest that these data support the hypothesis that cormorant foraging is visually-guided even though recent evidence has shown that their underwater visual acuity is poor.     

Cormorants dive through the Polar night

Most seabirds are visual hunters and are thus strongly affected by light levels. Dependence on vision should be problematic for species wintering at high latitudes, as they face very low light levels for extended periods during the Polar night. We examined the foraging rhythms of male great cormorants (Phalacrocorax carbo) wintering north of the Polar circle in West Greenland, conducting the first year-round recordings of the diving activity in a seabird wintering at high latitudes. Dive depth data revealed that birds dived every day during the Arctic winter and did not adjust their foraging rhythms to varying day length. Therefore, a significant proportion of the dive bouts were conducted in the dark (less than 1 lux) during the Polar night. Our study underlines the stunning adaptability of great cormorants and raises questions about the capacity of diving birds to use non-visual cues to target fish.     

Moving towards acceleration for estimates of activity-specific metabolic rate in free-living animals: the case of the cormorant

1. Time and energy are key currencies in animal ecology, and judicious management of these is a primary focus for natural selection. At present, however, there are only two main methods for estimation of rate of energy expenditure in the field, heart rate and doubly labelled water, both of which have been used with success; but both also have their limitations. 2. The deployment of data loggers that measure acceleration is emerging as a powerful tool for quantifying the behaviour of free-living animals. Given that animal movement requires the use of energy, the accelerometry technique potentially has application in the quantification of rate of energy expenditure during activity. 3. In the present study, we test the hypothesis that acceleration can serve as a proxy for rate of energy expenditure in free-living animals. We measured rate of energy expenditure as rates of O2 consumption (VO2) and CO2 production (VCO2) in great cormorants (Phalacrocorax carbo) at rest and during pedestrian exercise. VO2 and VCO2 were then related to overall dynamic body acceleration (ODBA) measured with an externally attached three-axis accelerometer. 4. Both VO2 and VCO2 were significantly positively associated with ODBA in great cormorants. This suggests that accelerometric measurements of ODBA can be used to estimate VO2 and VCO2 and, with some additional assumptions regarding metabolic substrate use and the energy equivalence of O2 and CO2, that ODBA can be used to estimate the activity specific rate of energy expenditure of free-living cormorants. 5. To verify that the approach identifies expected trends in from situations with variable power requirements, we measured ODBA in free-living imperial cormorants (Phalacrocorax atriceps) during foraging trips. We compared ODBA during return and outward foraging flights, when birds are expected to be laden and not laden with captured fish, respectively. We also examined changes in ODBA during the descent phase of diving, when power requirements are predicted to decrease with depth due to changes in buoyancy associated with compression of plumage and respiratory air. 6. In free-living imperial cormorants, ODBA, and hence estimated VO2, was higher during the return flight of a foraging bout, and decreased with depth during the descent phase of a dive, supporting the use of accelerometry for the determination of activity-specific rate of energy expenditure.     

Foraging energetics of arctic cormorants and the evolution of diving birds

Efficient body insulation is assumed to have enabled birds and mammals to colonize polar aquatic ecosystems. We challenge this concept by comparing the bioenergetics of cormorants ( Phalacrocorax carbo ) living in temperate and arctic conditions. We show that although these birds have limited insulation, they maintain high body temperature (42.3 °C) when diving in cold water (1–10 °C). Their energy demand at these times is extremely high (up to 60 W kg⁻¹). Free-living cormorants wintering in Greenland (water temperature −1 °C) profoundly alter their foraging activity, thus minimizing time spent in water and the associated high thermoregulatory costs. They then meet their daily food demand within a single intense dive bout (lasting 9 min on average). Their substantial energy requirements are balanced by the highest predatory efficiency so far recorded for aquatic predators. We postulate that similar behavioural patterns allowed early diving birds (Cretaceous) to colonize cold coastal areas before they evolved efficient insulation.     

Pedestrian locomotion energetics and gait characteristics of a diving bird, the great cormorant, Phalacrocorax carbo

Great cormorants Phalacrocorax carbo are foot propelled diving birds that seem poorly suited to locomotion on land. They have relatively short legs, which are presumably adapted for the generation of high forces during the power stroke of aquatic locomotion, and walk with a pronounced "clumsy waddle". We hypothesise (1) that the speed, independent minimum cost of locomotion (C min, ml O2 m(-1)) will be high for cormorants during treadmill exercise, and (2) that cormorants will have a relatively limited speed range in comparison to more cursorial birds. We measured the rate of oxygen consumption (V02) of cormorants during pedestrian locomotion on a treadmill, and filmed them to determine duty factor (the fraction of stride period that the foot is in contact with the ground), foot contact time (tc), stride frequency (f), swing phase duration and stride length. C min was 2.1-fold higher than that predicted by their body mass and phylogenetic position, but was not significantly different from the C min of runners (Galliformes and Struthioniformes). The extrapolated gamma-intercept of the relationship between V02 and speed was 1.9-fold higher than that predicted by allometry. Again, cormorants were not significantly different from runners. Contrary to our hypothesis, we therefore conclude that cormorants do not have high pedestrian transport costs. Cormorants were observed to use a grounded gait with two double support phases at all speeds measured, and showed an apparent gait transition between 0.17 and 0.25 m s(-1). This transition occurs at a Froude number between 0.016 and 0.037, which is lower than the value of approximately 0.5 observed for many other species. However, despite the use of a limited speed range, and a gait transition at relatively low speed, we conclude that the pedestrian locomotion of these foot propelled diving birds is otherwise generally similar to that of cursorial birds at comparable relative velocities.     

Water retention in the plumage of diving great cormorants Phalacrocorax carbo sinensis

Cormorants are assumed to have a "partially wettable" plumage as a mechanism to reduce buoyancy while swimming underwater. This assumption is mainly based on 3 observations: 1) the volume of air in the plumage of submerged carcasses is small compared to other water birds, 2) cormorants assume a "wing drying" posture when they exit the water, and 3) the feather structure of the plumage. An alternative mechanism to reduce buoyancy is to release air out of the plumage by ptilomotion without allowing water to penetrate. How wet cormorants actually get is an open issue that has important implications for the energy budget of these warm blooded aquatic predators. Here we report empirical measurements on the amount of water retained in the plumage of live great cormorant Phlacrocorax carbo sinensis during voluntary swimming and diving in an experimental design that simulates a foraging diving bout. The amount of water retained in the plumage increased as a function of time spent in water. However the birds limited their dive bouts to less than 18 minutes so that the added mass of retained water did not exceed 6% of their body mass. This maximal level of water retention is estimated to reduce the buoyancy of the dry bird by 18%. This maximal level is also similar to measurements of water retention of carcasses and suggests that measurements preformed on carcasses yield only the upper level of water absorption while live birds slow down water penetration, allowing longer periods of foraging.     

Intersexual differences in the diving behaviour of foraging subantarctic cormorant (Phalacrocorax albiventer) and Japanese cormorant (P. filamentosus).

Cormorants feed by feet-propelled diving. How cormorants optimize foraging is of a particular interest in relation to the understanding of the feeding strategies of diving birds, as well as within the debate about cormorants' impact on sustainable resources. Using microdata loggers that recorded diving depth, we investigated the foraging strategy of males and females of subantarctic cormorants, which inhabit cold regions, and of Japanese cormorants, which live in the northern temperate zone. For both species, males and females daily spent the same amount of time submerged, and apparently captured the same amount of fish. However, males dived deeper and longer, which could be explained by their 15-20% larger body mass and may minimize potential competition for food.     

Estimating Competition between Wildlife and Humans–A Case of Cormorants and Coastal Fisheries in the Baltic Sea

Cormorants and other wildlife populations have come in real or perceived conflicts with humans over exploited fish stocks. From gut contents of cormorants, and using an extension of the Catch equation, we estimated the degree of short term competition between great cormorants and coastal fisheries in two areas along the Swedish Baltic Sea. Cormorants consumed 10 and 44%, in respective area, of the fish biomass of six fish species harvested by humans; eel, flounder, herring, perch, pike, and whitefish. On average, cormorants consumed smaller individuals than harvested in fisheries. But for perch, cod and flounder, cormorants consumed harvestable sized fish corresponding >20% of human catches. Our competition model estimated the direct decrease in fisheries catches due to cormorant predation to be <10% for all species except flounder (>30%) and perch (2–20%). When also including the indirect effects of cormorant predation on smaller fish that never reached harvestable size, the estimated decrease in fisheries catches at least doubled for perch (13–34%) and pike (8–19%). Despite large uncertainties, our model indicates that cormorants may locally have a direct impact on human catches of at least flounder, and when incorporating indirect effects also on perch and pike. The study indicates that the degree of competition between cormorants and humans varies substantially between areas. We also included economical values in the model and concluded that for the commercially most important species, eel and cod, the estimated economic impact of cormorants on fisheries was low.     

Stable isotopes indicate the extent of freshwater feeding by cormorants Phalacrocorax carbo shot at inland fisheries in England

1. The numbers of cormorants Phalacrocorax carbo feeding at English freshwater fisheries during winter have increased rapidly over the last 20 years, causing concern among fishery managers and anglers.
2. In order to assess the extent of freshwater feeding, stable isotope ratios of carbon and nitrogen (δ¹³C and δ¹⁵N) in feathers of wild cormorants from inland freshwater fisheries were compared with those in the feathers of piscivorous birds with marine diets (captive 'marine-fed' cormorants, free-ranging shags Phalacrocorax aristotelis ) and freshwater diets (juvenile goosanders Mergus merganser ).
3. Isotope signatures of feathers represent the diet at the time of growth. Feathers grown at different times of the year were taken from wild cormorants; each feather type therefore represented the diet over a different temporal scale.
4. Isotopic analyses of feathers indicated that, when shot, nearly all of the cormorants had been feeding entirely on freshwater prey. The mean δ¹³C value of primary feathers growing when birds were shot was –22·2‰, indicative of an entirely freshwater diet.
5. The move to freshwater habitats from coastal breeding grounds occurred over several months, but once established cormorants appear to have fed at freshwater sites throughout the autumn and winter.
6. The suitability of using a two-source isotopic mixing model in order to quantify the extent of freshwater feeding in piscivorous birds is discussed.
7. Although the results indicate long-term residency and feeding in freshwater systems, they do not indicate whether birds were feeding regularly at the sites at which they were shot, or the composition of the diet. It is recommended that further studies using telemetry and multiple isotope analyses be carried out in order to address these issues.     

Diving in shallow water: the foraging ecology of darters (Aves: Anhingidae)

Diving birds have to overcome buoyancy, especially when diving in shallow water. Darters and anhingas (Anhingidae) are specialist shallow-water divers, with adaptations for reducing their buoyancy. Compared to closely-related cormorants (Phalacrocoracidae), darters have fully wettable plumage, smaller air sacs and denser bones. A previous study of darter diving behaviour reported no relationship between dive duration and water depth, contrary to optimal dive models. In this study I provide more extensive observations of African darters Anhinga melanogaster rufa diving in water<5 m deep at two sites. Dive duration increases with water depth at both sites, but the relationship is weak. Dives were longer than dives by cormorants in water of similar depth (max 108 s in water 2.5 m deep), with dives of up to 68 s observed in water<0.5 m deep. Initial dives in a bout were shorter than expected, possibly because their plumage was not fully saturated. Dive efficiency (dive:rest ratio) was 5–6, greater than cormorants (2.7±0.4 for 18 species) and other families of diving birds (average 0.2–4.3). Post-dive recovery periods increased with dive duration, but only slowly, resulting in a strong increase in efficiency with dive duration. All dives are likely to fall within the theoretical anaerobic dive limit. Foraging bouts were short (17.8±4.3 min) compared to cormorants, with birds spending 80±5% of time underwater. Darters take advantage of their low buoyancy to forage efficiently in shallow water, and their slow, stealthy dives are qualitatively different from those of other diving birds. However, they are forced to limit the duration of foraging bouts by increased thermoregulatory costs associated with wettable plumage.     

Histologic changes in thyroid glands from great cormorant (Phalacrocorax carbo) in Tokyo Bay, Japan: possible association with environmental contaminants

We compared morphologic changes in thyroid glands of great cormorants (Phalacrocorax carbo) from the Tokyo Bay and Lake Biwa areas in Japan with presence of residues of polychlorinated dibenzo-dioxins (PCDDs), polychlorinated dibenzo-furans (PCDFs), and coplanar polychlorinated biphenyls (Co-PCBs). Prominent morphologic changes in thyroid glands included increased density of small follicles and increased number of epithelial cells surrounding follicular lumens. The extent of morphologic changes in the thyroid gland was higher in cormorants captured from Tokyo Bay than in those captured from Lake Biwa. Increased thyroid change in cormorants from the Tokyo Bay area was associated with significantly higher levels of PCDFs and Co-PCBs. Thus, we suggest that morphologic changes in thyroid glands from the cormorants are associated with increased levels of dioxin contamination in Japan.     

Space utilization by a cormorant (Phalacrocorax carbo L.) colony in a multi-wetland complex in relation to feeding strategies

In this study, we investigated the response of inland breeding cormorants Phalacrocorax carbo to a complex spatial configuration of feeding habitats in relation to social and individual feeding strategies. The numbers of feeding trips outside the colony site (Lake Grand-Lieu, western France), where only solitary fishing is used by cormorants, and the number of birds fishing on the lake where social fishing predominates were investigated during the breeding season and compared with the fledging period. From the investigation of feeding trip traffic, we identified three major habitats used by cormorants in the vicinity of the colony site (< 25 km around the colony site) that accounted for 94.1 of the IN flights and 92.0% of the OUT flights (n = 1745 arrivals and 2404 departures respectively), and notably one area that accounted for 58% of total flights although it is the furthest away. No fundamental change in the relative significance of these feeding grounds for solitary fishing cormorants was found throughout the breeding season, even in a between-years comparison (1996-2001), in contrast to what has often been found elsewhere. Although the peak of foraging activity in the surrounding habitats and also within the lake waters largely coincided with the time when the majority of young had fledged, the index of cormorant numbers (ratio between bird numbers at a given time and that for a baseline date) on the lake remained at a high level until late August compared to movements outside the lake, as a result of regular social fishing (84.9 +/- 4.0% of fishing numbers). From these findings, we discuss factors governing the selection of feeding grounds throughout the breeding season in relation to energy considerations, feeding strategies and food resources.     

Computational modelling of cormorant swarm

The great cormorant (Phalacrocorax carbo) is a species with a strong impact on the environment in the areas inhabited by breeding colonies or migrating colonies. Depending on the size of colonies, destruction of tree cover, soil sterilization due to the supply of enormous amounts of aggressive faeces and overpreying on fish from nearby water bodies can be observed. In this study, an iterative algorithm for modelling the annual life cycle of a swarm of cormorants was described. The procedure was based on a mathematical model of a herd of birds, taking into account both fixed biological factors, such as food demand, availability of habitats and the reproductive cycle, and random factors occurring in the environment, e.g., flooding, storms or human activity. Additionally, the algorithm included the variable time of inhabitance depending on the duration of the ice cover over water bodies, and the possibility of conducting a killing programme. The proposed procedure was tested and verified positively using data obtained from the literature.     

Foraging and breeding performance of Japanese cormorants in relation to prey type

Seabirds are high trophic predators in marine ecosystems and are sensitive to change in food supply and thus seabirds can be used as monitors of the marine environment. In order to study the foraging responses of Japanese cormorants Phalacrocorax filamentosus breeding at Teuri Island, Hokkaido to changes in fish availability, the diet was assessed from the regurgitations of parents and chicks, and diving behavior was measured by using time-depth recorders. Breeding performance (brood size, chick growth, breeding success) was monitored using conventional methods to study their breeding responses. Japanese cormorants changed the diet and foraging behavior over four summers. The birds fed mainly on epipelagic schooling fish when they were available and on demersal fish when pelagic fish availability was low. They tended to dive deeper and longer in a year when they fed mainly on demersal fish than the other years, reflecting the change in the depth distribution of prey fish. Chick growth rate did not differ among years, but fledging success was lower in the years of demersal fish as their meal delivery rate was low. When epipelagic schooling fish were considered scare, parents maintained chick growth by reducing brood size. High variability and unpredictability in pelagic fish abundance are key factors affecting the foraging and breeding performance of Japanese cormorants, which could potentially be used to monitor fish resources.     

Impact of externally attached loggers on the diving behaviour of the king penguin

The impact of relatively small externally attached time series recorders on some foraging parameters of seabirds was investigated during the austral summer of 1995 by monitoring the diving behaviour of 10 free-ranging king penguins (Aptenodytes patagonicus) over one foraging trip. Time-depth recorders were implanted in the abdominal cavities of the birds, and half of the animals also had dummy loggers attached on their backs. Although most of the diving behaviour was not significantly affected by the external loggers (P>0.05), the birds with externally attached loggers performed almost twice as many shallow dives, between 0 and 10 m depth, as the birds without external loggers. These shallow dives interrupted more frequently the deep-diving sequences in the case of birds with external loggers (percentage of deep dives followed by deep dives: 46% for birds with implants only vs. 26% for birds with an external attachment). Finally, the distribution pattern of the postdive durations plotted against the hour of the day was more heterogeneous for the birds with an external package. In addition, these penguins had extended surfacing times between two deep dives compared to birds without external attachments (P<0.0001). These results suggest the existence of an extra energy cost induced by externally attached loggers.     

Effects of air and water temperatures on resting metabolism of auklets and other diving birds

For small aquatic endotherms, heat loss while floating on water can be a dominant energy cost, and requires accurate estimation in energetics models for different species. We measured resting metabolic rate (RMR) in air and on water for a small diving bird, the Cassin's auklet (Ptychoramphus aleuticus), and compared these results to published data for other diving birds of diverse taxa and sizes. For 8 Cassin's auklets (~165 g), the lower critical temperature was higher on water (21 °C) than in air (16 °C). Lowest values of RMR (W kg?1) averaged 19% higher on water (12.14 ± 3.14 SD) than in air (10.22 ± 1.43). At lower temperatures, RMR averaged 25% higher on water than in air, increasing with similar slope. RMR was higher on water than in air for alcids, cormorants, and small penguins but not for diving ducks, which appear exceptionally resistant to heat loss in water. Changes in RMR (W) with body mass either in air or on water were mostly linear over the 5- to 20-fold body mass ranges of alcids, diving ducks, and penguins, while cormorants showed no relationship of RMR with mass. The often large energetic effects of time spent floating on water can differ substantially among major taxa of diving birds, so that relevant estimates are critical to understanding their patterns of daily energy use.     

Conspecific reproductive success affects age of recruitment in a great cormorant, Phalacrocorax carbo sinensis, colony.

Few studies have addressed the proximate factors affecting the age at which individuals of long-lived bird species are recruited into the breeding population. We use capture-recapture analysis of resightings of 16 birth cohorts of colour-ringed great cormorants, Phalacrocorax carbo sinensis, in a Danish colony to assess the evidence for two hypotheses: conspecific attraction (earlier recruitment when the colony is large) and conspecific reproductive success (earlier recruitment following years of high breeding success). For both males and females, conspecific reproductive success was the most important covariate explaining the interannual variation in age of recruitment; colony size was also important for females. These covariates explained nearly 60% of the year-to-year variation for both sexes. The age of recruitment increased for cohorts born after 1990, and this increase was correlated with a decline in breeding success in the colony; we interpret this as an indirect and delayed density-dependent effect. Females were recruited earlier than males (mean age of recruitment for cohorts born before 1990: 2.98 years versus 3.53 years); the most plausible reason for this is a skewed sex ratio in favour of males in the adult population. Recruitment of males may thus, to some extent, be constrained by the availability of females. This study provides the first evidence that conspecific reproductive success can affect the age at which individual birds start to breed.     

Food-habitat relationship of harbour seals and black cormorants in Skagerrak and Kattegat

Comparative studies on the food of the black cormorant Phalacrocorax carbo and the harbour seal Phoca vitulina were carried out in two contrasting habitat types. Both species feed predominantly on bottom-dwelling fish. Black cormorants are able to utilize fish found both on vegetation-covered and naked sea beds at a water depth of less than 10 m, while harbour seals feed mainly on soft sea bottoms above 30 m where vegetation is scarce or lacking. The food overlap of the two piscivores is large in environments where large shallow sea bottoms are available, and small in areas where sea bottoms of soft material is found at greater depth. In areas where the shallow bottoms are covered by vegetation only, cormorants are able to feed on the fish species inhabiting this kind of environment. There is no evidence that these predators make a choice regarding prey species.     

Dispersal and recruitment during population growth in a colonial bird, the great cormorant Phalacrocorax carbo sinensis

While the factors influencing reproduction and survival in colonial populations are relatively well studied, factors involved in dispersal and settlement decisions are not well understood. The present study investigated exchanges of great cormorants Phalacrocorax carbo sinensis among six breeding colonies over a 13‐year period when the breeding population in Denmark increased from 2800 to 36 400 nests. We used a multistate capture‐recapture model that combined multisite resightings and recoveries to examine simultaneously recruitment, natal dispersal, breeding dispersal and annual survival of first‐year, immature and breeding great cormorants. Mean survival of first‐year birds (0.50±0.09, range=0.42–0.66 among colonies) was lower than survival of breeders (0.90±0.06, range=0.81–0.97). Mean survival of immature birds over the study period was 0.87±0.08. Dispersal from a colony increased with decreasing mean brood size in the colony in both first‐time and experienced breeders. The choice of the settlement colony in first‐time breeders was affected by conditions in the natal colony and in the colonies prospected during the pre‐breeding years. In particular, first‐time breeders recruited to colonies where they could expect better breeding success. Experienced breeders relied mainly on cues present early in the season and on their own breeding experience to choose a new breeding colony. Newly established colonies resulted mainly from the immigration of first‐time breeders originating from denser colonies. Dispersal was distance‐dependent and first‐time breeders dispersed longer distances than breeders. We suggest that the prospecting behaviour allows first‐time breeders to recruit in nearby as well as more distant potential breeding colonies. Dispersing breeders preferred to settle in neighbouring colonies likely to benefit from their experience with foraging areas. We discuss the importance of these movements for growth and expansion of the breeding population.