Spatial ecology of non-breeding Eurasian Griffon Vultures Gyps fulvus in relation to natural and artificial food availability

ABSTRACT

Capsule: The movements and spatial ecology of non-breeding Eurasian Griffon Vultures Gyps fulvus in northern Italy, Croatia and Austria do not seem to be affected by feeding station use.

Aims: The purpose of this study was to assess how the creation of a feeding station at the Riserva Naturale Regionale del Lago di Cornino (Forgaria nel Friuli, northeast Italy) during the 1980s might have affected the spatial and behavioural ecology of the Eurasian Griffon Vulture.

Methods: Using global positioning system (GPS) satellite tracking, we studied movements of nine non-breeding Eurasian Griffon Vultures within the Riserva Naturale Regionale del Lago di Cornino in Italy, the Hohe Tauern in Austria and the Kvarner Gulf in Croatia.

Results: Both the average foraging range size and the time spent by the birds in Italy were comparable to those recorded in Croatia and Austria, where the vultures depend on unpredictable food resources. A significant difference in terms of foraging range size was recorded among seasons. In winter it seems to be smaller as a consequence of reduced movements performed by the individuals due to harsh climate conditions.

Conclusions: Our results suggest that the creation of a feeding station in Forgaria does not seem to have affected the spatial ecology of the Eurasian Griffon Vulture. However, due to the limited sample size and the young age of the individuals monitored, which have a long dispersal period, the findings presented should be considered as preliminary. Further research needs to be implemented to inform decisions regarding the management of supplementary feeding stations to promote the recovery and conservation of scavenger species, particularly in areas in which they have declined massively.     

Male-male mountings in polyandrous bearded vultures Gypaetus barbatus: an unusual behaviour in raptors

Male-male mountings appear to be very common in polyandrous bearded vulture Gypaetus barbatus trios. We observed sexual activity in two trios that occupied the same territory in different years. We recorded a total of 167 copulation attempts. The percentage of male-male mountings recorded was 26.1 and 11.4%, in the period of 1991–1992 and 2000–2001, respectively, with respect to total, homo- and heterosexual matings. We conclude that homosexual interactions do not appear to be directly associated with intrasexual competition (i.e. hierarchical dominance, sperm competition). Rather, our results are more consistent with the idea that this behaviour can regulate the aggression of the males in these groups.     

Dusk-copulation of the rock-dwelling ocypodid,Ilyoplax integra (Brachyura)

Pre-copulatory behaviour and surface copulation of the rock-dwelling ocypodid crabIlyoplax integra was studied from May 1989 to June 1990, at Horikawa, Okinawa Island, southern Japan. A male crab would grasp a female near the entrance to her burrow and copulatein situ. Copulation lasted 12.7 minutes on average. Surface copulations were frequently observed during neap tide days, especially in the first quarters during May and June. On these days copulations were quite frequent in the dusk period, during the 1.5 h around sunset. Surface copulation has not been described in otherIlyoplax species, therefore the sexual behaviour ofI. integra is unique within the genus. On rocks, where the number of burrows is in shortage, surface copulation in which a male can mate without evacuating his burrow to the female may be adaptive. Two possibilities were suggested to explain the high frequency of surface copulation during dusk hours; 1) to reduce the risk of predation by plovers and 2) to avoid exposing crabs to higher temperature and stronger radiation in daytime hours during surface copulation.     

A Global Review of Causes of Morbidity and Mortality in Free-Living Vultures

Vulture species worldwide play a key role in ecosystems as obligate scavengers, and several populations have had precipitous declines. Research on vulture health is critical to conservation efforts including free-living vultures and captive breeding programs, but is limited to date. In this systematic review, we determined the reported causes of free-living vulture species morbidity and mortality worldwide. The most commonly reported cause of mortality was from toxins (60%), especially lead and pesticides, followed by traumatic injury (49%), including collisions with urban infrastructure and gunshot. Neglected areas of research in free-living vulture health include infectious diseases (16%), endocrine and nutritional disorders (6%), and neoplasia (<?1%). Almost half of the studies included in the review were conducted in either Spain or the USA, with a paucity of studies conducted in South America and sub-Saharan Africa. The highest number of studies was on Griffon (Gyps fulvus) (24%) and Egyptian vultures (Neophron percnopterus) (19%), while half of all vulture species had five or fewer studies. Future investigations on free-living vulture health should focus on neglected areas of research, such as infectious diseases, and areas with gaps in the current literature, such as South America, sub-Saharan Africa, and under-studied vulture species.

     

Status and structure of the griffon vulture (Gyps fulvus) population in Crete

Griffon vulture (Gyps fulvus) population surveys were conducted during 1996–2002 in the island of Crete (Greece) to document population status and structure. Fieldwork was carried out during the breeding period when birds could be monitored in their colonies. Total population size was estimated at 379 individuals (range = 341–417) with adult birds comprising 63%. The breeding population was estimated at 141 pairs, which were distributed on an average in 23 colonies per year (range = 16–30) while the mean number of breeding pairs that laid eggs was 98 (range= 64–126). Crete thus supports the largest insular population of the species in the world and hosts 70–80% of the breeding population of the species in Greece. Population density was estimated at 6.9 individuals/100 km², 2.6 breeding pairs/100 km² and 1.8 nesting pairs/100 km². The average home range of an occupied colony (i.e., breeding group) was estimated at ca. 204 km² producing a theoretical foraging range of 8 km radius around the breeding cliff. No trends in the total number of individuals and breeding pairs appeared to exist, although significant differences in population size of individual colonies occurred between the years. The majority of the population was concentrated in small-sized colonies, which showed a low occupancy rate. The number of abandoned sites and the colonization of new ones could represent a shift of breeding pairs to alternative colonies provoked by local food abundance and conspesific attraction.     

The effect of kleptoparasite and host numbers on the risk of food‐stealing in an avian assemblage

Kleptoparasitism involves the theft of resources such as food items from one individual by another. Such food‐stealing behaviour can have important consequences for birds, in terms of individual fitness and population sizes. In order to understand avian host–kleptoparasite interactions, studies are needed which identify the factors which modulate the risk of kleptoparasitism. In temperate European intertidal areas, Eurasian oystercatchers Haematopus ostralegus feed primarily on bivalve molluscs, which may be stolen by kleptoparasitic species such as carrion crows Corvus corone and herring gulls Larus argentatus. In this study we combined overwinter foraging observations of oystercatchers and their kleptoparasites on the Exe Estuary, UK, with statistical modelling to identify the factors that influence the likelihood of successful food stealing behaviour occurring. Across the winter, 16.4% of oystercatcher foraging attempts ended in successful kleptoparasitism; the risk of theft was lowest in February (10.8%) and highest in December (36.3%). Using an information theoretic approach to compare multiple logistic regression models we present evidence that the outcome of host foraging attempts varied with the number of kleptoparasites per host within the foraging patch for two out of five individual months, and for all months grouped. Successful, kleptoparasitism was more likely to occur when the total number of all kleptoparasites per host was greater. Across the entire winter study period, oystercatcher foraging attempts that resulted in kleptoparasitism were associated with a mean number of kleptoparasites per host that was more than double that for foraging attempts that ended in the oystercatcher successfully consuming the mussel. Conversely, the stage of the tidal cycle within the estuary did not affect the outcome of oystercatcher foraging attempts. Our study provides evidence that bird numbers influence the risk of kleptoparasitism within avian assemblages.     

Narrow sea crossings present major obstacles to migrating Griffon Vultures Gyps fulvus

The flight behaviour of Griffon Vultures Gyps fulvus was studied at a major migration bottleneck, the Strait of Gibraltar in southernmost Spain, during the autumns of 2004 to 2007. The 14‐km‐wide sea channel significantly impeded the southern migration of the species into Africa, with many birds attempting repeated passage for weeks before crossing, and others not crossing at all and overwintering in Southern Spain. Water‐crossing attempts were restricted to times between 11:00 and 14:00 h on days with light or variable winds, or on days with strong winds from the north or west. No crossing attempts were made on days with strong winds from the south or east. Vultures attempted to cross the Strait in large flocks and never attempted to do so alone. Although 29% of the birds soared during crossing attempts, at least until they flew beyond visible range of approximately 4 km, most engaged in considerable flapping flight when attempting to cross. Overall, birds flying over water flapped more than 10 times as frequently as those flying over land prior to crossing attempts. Vultures did not flap continuously, but intermittently in brief bouts of flapping interspersed with periods of gliding or soaring flight. The number of flaps per bout over water was significantly greater than the number of flaps per bout over land. Vultures flying over water that flapped at rates of 20 flaps or more per minute typically aborted attempted crossings and returned to Spain in intermittent flapping and gliding flight. There are numerous reports of Vultures falling into the Strait and drowning while attempting to cross, as well as reports of returning Vultures collapsing on the beach having reached Spain in spring ( Barrios Partida 2006 ). Our observations indicate that passage of Griffon Vultures at the Strait of Gibraltar is limited by the species’ over‐water flapping‐flight abilities, including its inability to flap continuously for even short periods of time. We suggest that even relatively short sea crossings represent significant obstacles to migrating Vultures and discuss the implications of this limitation on the distribution and abundance of the species.     

Unusual Pre-copulatory Behaviour in the Hermaphroditic Planarian Flatworm,Dugesia gonocephala (Tricladida,Paludicola)

Hermaphrodite mating behaviour is poorly understood, particularly in species with internal fertilization and mutual penis insertion. We collected detailed recordings on the frequency, timing and outcome of the mating sequence of the simultaneous hermaphroditic flatworm Dugesia gonocephala (Tricladida, Paludicola). Mating in this species differs from that in other planarians in that receptive partners show a stereotypic pre-copulatory behaviour which results in copulation in only 17% (n = 342) of all attempts. It includes an unusual phase during which one partner glides on top of the other and first the lower, then both individuals, spread out and flatten. Genital intromission is not possible in this position. All observed copulations (n = 57) were preceded by this behaviour and most mating sequences were interrupted at this stage. Pairs were seen starting new mating sequences up to 11 times. Which animal lay on top varied randomly within a series of attempts. Cocoon production was a good predictor of mating activity, and copulations mainly occurred during the night. Copulations lasted between 24 min and 9.3 h (mean = 4.7 ± 2.3 h) and penises were mutually inserted. In the field, 99% (n = 70) of all matings involved reciprocal spermatophore exchange, compared with only 50% in the laboratory (n = 26). The likelihood of reciprocal spermatophore transfer increased with increasing duration of copulation. Duration was independent of the events that took place during courtship. We discuss the possibility that partners interrupt a copulation when there is no guarantee of reciprocal spermatophore transfer.     

Female lesser kestrel ( falco naumanni ) also accepts extra-pair copulation

The lesser kestrel (Falco naumanni) is considered a socially monogamous species in which extra-pair copulation occurs at a low rate. A wide study of extra-pair mating behaviour carried out on this species found that mated females do not solicit extra-pair copulation and reject all copulation attempts elicited by extra-pair males. In fact, the infrequent instances of extra-pair fertilization found were attributed either to re-mating after divorce, or polygyny. Here I describe an observation indicating that females also promote and accept promiscuous mating, attaining and consummating extra-pair copulation. I suggest the possibility that promiscuous behaviour could vary among different populations in this species, as it has not yet been reported, in spite of the extensive work performed in this respect.     

Agonistic Behaviour and Sexual Conflict in Atypical Reproductive Groups: The Case of Bearded Vulture Gypaetus barbatus Polyandrous Trios

Social behaviour in species forced to form atypical breeding coalitions is poorly documented. The saturation of optimum territories in the Bearded vulture Gypaetus barbatus population in the Pyrenees has led floating males to settle in already occupied territories, thereby forming polyandrous trios. We examined the patterns of intrasexual aggression in five trios (nine reproductive events in total) during courtship. Alpha males initiated 82% of agonistic encounters that were mainly aimed at preventing or disrupting copulations. During the fertile period in recently formed groups, intrasexual aggression had a negative influence on the frequency of heterosexual copulations, which may be a contributing factor to the lower productivity of polyandrous trios. Females rejected a higher proportion of beta male- than alpha male-initiated copulations, and rejected copulations with both alpha and beta males more often when the other male was present close by. These results indicate that alpha males cannot effectively prevent all copulation attempts by beta males and that females avoid harassment by minimizing sexual activity when both males are present. Aggression between males decreased with time, occurring less often in established than in recent trios, despite the fact that the frequency of heterosexual copulations – the cause of conflicts – was similar. The frequency of homosexual interactions tended to increase in established trios, suggesting that this behaviour may help to regulate aggression within these groups, although no significant relationship between homosexual interactions and aggression was found. In summary, reproductive conflicts in trios seem to be unavoidable, although they tend to decrease if the group is maintained. This suggests that, for birds in these groups, the maintenance of a quality territory is more important than solving sexual conflicts.     

Modelling the effect of environmental variables on the reproductive success of Griffon Vulture (Gyps fulvus) in Sardinia,Italy

Old World vultures are experiencing dramatic population declines and now are among the species most threatened with extinction. Understanding the environmental variables that can influence the reproductive indexes of vulture populations can facilitate both habitat and species management. The aim of this study was to identify which environmental variables primarily affect the breeding successes of the Griffon Vulture Gyps fulvus in northern Sardinia by applying a Bayesian hierarchical model. A unique dataset of reproductive records (197 nests monitored over 39 years for a total of 992 breeding records) was used. Eight environmental and topographical variables describing the habitat at the nesting sites were considered as potential predictors of breeding success. These included mean annual temperature, mean annual precipitation, isothermality, elevation, the normalized difference vegetation index, wind speed, and the aspect and slope of the land surface. In addition, we also considered the effect of human disturbance and the type of nest. According to our best model, the probability of successfully raising a chick in Griffon Vultures was higher in nests exposed to a high wind speed, not covered by natural shelters, where the vegetation was mostly represented by shrub and pastures, with low human disturbance and in years with low rainfall. This model will be useful for management of the breeding habitat and to identify the area most suitable for Griffon Vulture reproduction. This information is crucial for programming conservation measures aimed at enlarging the area of occupancy of the species.     

Ultrasonic courtship songs of male Asian corn borer moths assist copulation attempts by making the females motionless

Males of the Asian corn borer moth Ostrinia furnacalis (Guenée) produce an ultrasonic courtship song of extremely low‐intensity during copulation attempts. The song has been shown to significantly increase the mating success of the male; however, the mode of action of the sound in courtship remains to be resolved. Behavioural experiments using pairs with deafened females or muted males show that, without the aid of the sound, 63% of males eventually succeed in mating after several copulation attempts, whereas the remainder (37%) make repeated attempts in vain until interrupted by the escape of the female. Because few (2%) males fail to copulate when females hear the courtship song, it is evident that the song has an effect on females, promoting the success of copulation attempts. In support of this view, males produce louder songs if the first copulation attempt fails, suggesting that the males increase their sound levels to achieve successful copulation. It is suggested that the ultrasonic songs of the male render the females motionless, which is the same response as that to ultrasonic bat calls. Because even slight movements by the female can interfere with the attempt of the male to copulate, it is likely that, by making her motionless, the success rate of a single copulation attempt is increased greatly.     

EVIDENCE FOR WIDESPREAD COURTSHIP DURING COPULATION IN 131 SPECIES OF INSECTS AND SPIDERS,AND IMPLICATIONS FOR CRYPTIC FEMALE CHOICE

Male courtship behavior is generally thought to function prior to copulation, as an inducement to the female to allow the male to copulate with her; this study indicates however, that male courtship during and following copulation (“copulatory courtship”) is common in insects and spiders (81% of 131 species in 102 genera and 49 families, mostly Coleoptera, Hemiptera, Diptera, and Araneioidea). Copulatory courtship is apparently evolutionarily labile, as expected if it is under sexual selection; intrageneric variation occurred in all 17 genera in which more than one species was observed. In 81% of 94 species with copulatory courtship, the male abandoned the female soon after copulation ended; thus, copulatory courtship appears not to function generally to induce acceptance of further copulatory attempts. The most likely explanation for copulatory courtship is that it represents attempts by males to influence cryptic female choice. This suggests that an aspect of sexual selection by female choice not considered by Darwin may be more important than previously appreciated and that the common practice in evolutionary studies of measuring male reproductive success by counting numbers of copulations may sometimes be misleading because of cryptic female choice during and after copulation.     

Implications of bacterial,viral and mycotic microorganisms in vultures for wildlife conservation,ecosystem services and public health

The effects that microorganisms (bacteria, viruses and fungi) have on their hosts remain unexplored for most vulture species. This is especially relevant for vultures, as their diet consists of carcasses in various stages of decomposition, which are breeding grounds for potentially pathogenic microorganisms. Here we review current knowledge of bacterial, viral and mycotic microorganisms present in wild vultures. We consider their potential to cause disease in vultures and whether this poses any population-level threats. Furthermore, we address the question of whether vultures may act as disease spreaders or mitigators. We found 76 articles concerning bacterial, viral and mycotic microorganisms present in 13 vulture species, 57 evaluating bacteria, 13 evaluating viruses and six evaluating mycotic microorganisms. These studies come from all continents where vultures are present, but mainly from Europe and North America, and the most studied species was the Griffon Vulture Gyps fulvus. We found that vultures are colonized by zoonotic pathogens, and even host-specific human pathogens. Some recorded bacteria showed multi-antibiotic resistance, especially those that can be associated with anthropogenic food subsides such as supplementary feeding stations. We found evidence that vulture health can be affected by some microorganisms, producing a wide array of clinical alterations that have the potential to influence mortality risk and fitness. We did not find clear scientific evidence that vultures play an epidemiological role spreading microorganisms to humans and other species. However, there is evidence that vultures could prevent the spread of infectious diseases through their removal of decomposing organic material. The evaluation of vulture exposure to microorganisms is of fundamental importance to design better conservation policies for this threatened group, which may serve a key role as ecosystem cleaners.     

Female walking during copulation reduces the likelihood of sperm transfer from males in the sweet potato weevil,Cylas formicarius

Behaviour during copulation can alter the fate of sperm of the mating males. This behaviour may exert selective pressure, resulting in the evolution of diverse reproductive behaviour, morphology, and physiology. This study examined the role of female copulatory behaviour on sperm fate in the sweet potato weevil, Cylas formicarius (Fabricius) (Coleoptera: Brentidae). In this species, males mount the female during copulation. The female frequently walks during copulation, carrying the male on her back. Here, we describe and quantify the copulatory behaviour of mating pairs and examine the sperm fate. Insemination success, as determined by the presence of sperm in the spermatheca, was lower when females walked for longer periods during copulation. This result emphasizes the value of studying variation in female copulatory behaviour in order to understand the factors that influence sperm fate. We discuss the implications of these results on sexual selection and utility in programs applying sterile insect techniques.     

Unique mating behavior,and reproductive biology of a simultaneous hermaphroditic marine flatworm (Platyhelminthes,Tricladida, Maricola)

Flatworms generally are simultaneous hermaphrodites that exhibit various kinds of mating behavior. Here we report on the mating behavior and reproductive biology of the planarian Paucumara falcata. We recognized three phases in its mating behavior: a courtship, copulation, and postcopulatory phase. During the last‐mentioned phase, the partners showed a unique and very characteristic behavior in which their bodies intertwined, forming a spiral. Histological study of partners in copula revealed that the sclerotic tip of the musculo‐parenchymatic organ pierces the body wall of the partner and then becomes lodged in its parenchyma, suggesting that this organ may act as an anchor, thus stabilizing the worms during copulation. Similar organs in other species of marine triclad may also perform a stabilizing role during copulation. During copulation in individuals of P. falcata, sperm transfer was reciprocal or only unilateral. Copulation duration ranged 13–35 min (average 20 ± 5 min), irrespective of whether the mating was successful (i.e., resulted in the production of fertile cocoons). The spiraling phase lasted on average 10 min; some worms did not show the postcopulatory spiraling phase during their mating behavior. After successful copulation, an individual worm produced 1–12 fertile cocoons over a period of 1–17 days; from a cocoon hatched either one young (in 70% of the cases), or two young worms.     

Isolation and characterization of polymorphic microsatellite markers in Eurasian vulture Gyps fulvus

To obtain polymorphic molecular markers for population genetic and conservation studies in the Eurasian vulture Gyps fulvus populations, we screened a size‐selected partial genomic library enriched for microsatellites with dinucleotide motifs. A total of five polymorphic markers were obtained. The number of alleles ranged from two to nine and the observed and expected heterozygosity were very similar. These markers will be very useful for studying population structure and to evaluate conservation programmes.     

A female‐produced short‐range sex pheromone in the egg parasitoid Trissolcus brochymenae

The potential for short‐range sex pheromone communication by the egg parasitoid wasp Trissolcus brochymenae (Hymenoptera: Platygastridae) was investigated in closed arena bioassays. Males of this parasitoid showed more antennal drumming and more frequent mounting behaviour on 1‐ to 2‐d‐old virgin females compared with 8‐d‐old virgin females. Male copulation attempts were fewer with previously mated females than with virgin females. Males courted and made copulation attempts with 1‐ to 2‐d‐old female cadavers, but not with male cadavers or with female cadavers rinsed in organic solvents of different polarities. Male attraction to female cadavers was re‐established by treating cadavers with acetone extracts of females, but not with ether or hexane extracts. In experiments using female cadavers dissected into head, mesosoma, and gaster, and then reassembled using one unwashed body section and two body sections washed in acetone, males were attracted only to the reassembled cadavers with an unwashed mesosoma. These findings suggest that (1) courtship behaviour in males of T. brochymenae is triggered by a short‐range sex pheromone produced by females; (2) the age and the physiological condition of females (virgin/mated) influence pheromone release or production; (3) the female's mesosoma is the source of the sex pheromone; and (4) polar components of the sex pheromone play a major role in influencing male behaviour. Our results suggest that quasi‐gregarious egg parasitoids are selected for short‐range rather than long‐range sex pheromones.     

Fatal poisoning of a Griffon vulture (Gyps fulvus) with methomyl

A young Griffon vulture died with signs of convulsion, vomiting, tremor, seizures propulsions and lack of co-ordination. Toxicological analysis of the stomach content revealed the presence of methomyl (9.3 mg/kg), methomyloxime (6.7 mg/kg) and deltamethrin (6.1 mg/kg). Concentrations of methomyl and its intermediate methomyloxime, combined with results of other analysis, indicate methomyl as the cause of death of this bird.     

Behavioral and endocrine characteristics of the reproductive cycle in wild muriqui monkeys,Brachyteles arachnoides

The analysis of fecal ovarian steroids provides a powerful noninvasive method to obtain insights into ovulatory cycles, gestation length, and the timing of sexual interactions relative to the periovulatory period in wild primates. Techniques developed to collect and assay feces from free-ranging muriqui monkeys (Brachyteles arachnoides) for estradiol and progesterone yield the first explicit reproductive data on this species, and provide the first opportunity to evaluate the timing of observed copulations with muriqui ovarian cycles. Hormonal profiles from seven females indicate average cycle lengths of 21.0 ± 5.4 days (n=20). Females conceived after 3–6 ovulatory cycles. Gestation length averaged 216.4 ± 1.5 days for the five females for which conception cycles were sampled. Discrete copulation periods spanned an average of 2.1 ± 1.2 days (n=29), with intervals between these concentrated periods of copulations averaging 15.6 ± 6.7 days (n=20). There were no significant differences among females in cycle lengths, copulation period lengths, or copulation interval lengths. Ejaculation was visible following 71.8 ± 26.7% of copulations during the females' preovulatory periods. All females copulated outside the periovulatory period. The proportion of copulation days outside the periovulatory period was slightly greater (p=0.08) for primiparous females (64.8 ± 28.3%) than for multiparous females (28.7 ± 19.7%). Am. J. Primatol. 42:299–310, 1997. © 1997 Wiley-Liss, Inc.