Largest bird from the Early Cretaceous and its implications for the earliest avian ecological diversification

With only one known exception, early Cretaceous birds were smaller than their closest theropod dinosaur relatives. Here we report on a new bird from the Early Cretaceous feathered-dinosaur-bearing continental deposits of Liaoning, northeast China, which is not only larger than Archaeopteryx but is nearly twice as large as the basal dromaeosaur Microraptor. The new taxon, Sapeornis chaoyangensis gen. et sp. nov., has a more basal phylogenetic position than all other birds except for Archaeopteryx. Its exceptionally long forelimbs, well-developed deltoid crest of the humerus, proximally fused metacarpals, relatively short hindlimbs and short pygostyle indicate powerful soaring capability and further suggest that by the Early Cretaceous ecological diversification of early birds was greater than previously assumed. Electronic supplementary material to this paper can be obtained by using the Springer LINK server located at http://dx.doi.org/10.1007/s00114-001-0276-9.     

Split-second escape decisions in blue tits (Parus caeruleus)

Bird mortality is heavily affected by birds of prey. Under attack, take-off is crucial for survival and even minor mistakes in initial escape response can have devastating consequences. Birds may respond differently depending on the character of the predator's attack and these split-second decisions were studied using a model merlin (Falco columbarius) that attacked feeding blue tits (Parus caeruleus) from two different attack angles in two different speeds. When attacked from a low attack angle they took off more steeply than when attacked from a high angle. This is the first study to show that escape behaviour also depends on predator attack speed. The blue tits responded to a high-speed attack by dodging sideways more often than when attacked at a low speed. Escape speed was not significantly affected by the different treatments. Although they have only a split-second before escaping an attack, blue tits do adjust their escape strategy to the prevailing attack conditions.     

Sex- and age-related differences in the timing and body condition of migrating Reed Warblers Acrocephalus scirpaceus and Sedge Warblers Acrocephalus schoenobaenus

The migration strategies of birds may vary strongly between species and also between age and/or sex groups. We studied the autumn migration and body condition of molecularly sexed Reed Warblers Acrocephalus scirpaceus and Sedge Warblers Acrocephalus schoenobaenus (211 and 208 ind., respectively) at a stopover site on Lake Druzno, Northern Poland, in 2008. Immature male Reed Warblers were caught significantly later than females (median dates 9 days later), but in the Sedge Warbler, both sexes of immatures migrated at about the same time. Adult males and females of both species did not differ in their time of migration. Adult and immature males of both species were larger (wing length and body mass) than females. In both species, fat reserves were similar in both sexes of both age classes. Adults of both sexes of Reed and Sedge Warbler were generally caught earlier than immatures. In both species, the body mass and fat reserves of immatures were generally less than in adults. The autumn protogyny of immature Reed Warblers may allow smaller females to limit competition with bigger males during migration and at the wintering grounds. In the Sedge Warbler, which tends to match its migration to peak of occurrence of superabundant food at stopover sites, both sexes gain an advantage from migrating at the same time. Since part of the measured wing length variation in both species was explained by sex differences, temporal trends in wing length recorded at stopover sites should be interpreted with caution.     

Sexual dimorphism in immune function changes during the annual cycle in house sparrows

Difference between sexes in parasitism is a common phenomenon among birds, which may be related to differences between males and females in their investment into immune functions or as a consequence of differential exposure to parasites. Because life-history strategies change sex specifically during the annual cycle, immunological responses of the host aiming to reduce the impact of parasites may be sexually dimorphic. Despite the great complexity of the immune system, studies on immunoecology generally characterise the immune status through a few variables, often overlooking potentially important seasonal and gender effects. However, because of the differences in physiological and defence mechanisms among different arms of the immune system, we expect divergent responses of immune components to environmental seasonality. In male and female house sparrows (Passer domesticus), we measured the major components of the immune system (innate, acquired, cellular and humoral) during four important life-history stages across the year: (1) mating, (2) breeding, (3) moulting and (4) during the winter capture and also following introduction to captivity in aviary. Different individuals were sampled from the same population during the four life cycle stages. We found that three out of eight immune variables showed a significant life cycle stage × sex interaction. The difference in immune response between the sexes was significant in five immune variables during the mating stage, when females had consistently stronger immune function than males, while variables varied generally non-significantly with sex during the remaining three life cycle stages. Our results show that the immune system is highly variable between life cycle stages and sexes, highlighting the potential fine tuning of the immune system to specific physiological states and environmental conditions.     

Carotenoids,immune response and the expression of sexual ornaments in male greenfinches (<Emphasis Type="Italic">Carduelis chloris</Emphasis>)

Allocation trade-offs of carotenoids between their use in the immune system and production of sexual ornaments have been suggested as a proximate mechanism maintaining honesty of sexual signals. To test this idea, we experimentally examined whether carotenoid availability in the diet was related to variation in antibody response to novel antigens in male greenfinches (Carduelis chloris aurantiiventris), a species with extensive carotenoid-dependent plumage colouration. We also measured the cost of mounting a humoral response in terms of circulating carotenoids. Finally, we examined the relationship between plumage colour, immune response and circulating carotenoids. We found that males with carotenoid-supplemented diets showed stronger antibody response than non-supplemented birds. We also found that activation of the immune system significantly reduced circulating carotenoids (24.9% lower in immune-challenged birds than in control birds). Finally, intensity (chroma) of ventral plumage colouration of males, a character directly related to concentration of total carotenoids in feathers, was negatively correlated with the immune response and circulating carotenoids in winter. These results support the idea that carotenoids are a limiting resource and that males trade ornamental colouration against immune response.     

Dietary antioxidants, lipid peroxidation and plumage colouration in nestling blue tits Cyanistes caeruleus

Carotenoid pigments are responsible for many of the red, yellow and orange plumage and integument traits seen in birds. One idea suggests that since carotenoids can act as antioxidants, carotenoid-mediated colouration may reveal an individual's ability to resist oxidative damage. In fact, there is currently very little information on the effects of most dietary-acquired antioxidants on oxidative stress in wild birds. Here, we assessed the impacts on oxidative damage, plasma antioxidants, growth and plumage colouration after supplementing nestling blue tits Cyanistes caeruleus with one of three diets; control, carotenoid treatment or α-tocopherol treatment. Oxidative damage was assessed by HPLC analysis of plasma levels of malondialdehyde (MDA), a by-product of lipid peroxidation. Contrary to predictions, we found no differences in oxidative damage, plumage colouration or growth rate between treatment groups. Although plasma lutein concentrations were significantly raised in carotenoid-fed chicks, α-tocopherol treatment had no effect on concentrations of plasma α-tocopherol compared with controls. Interestingly, we found that faster growing chicks had higher levels of oxidative damage than slower growing birds, independent of treatment, body mass and condition at fledging. Moreover, the chromatic signal of the chest plumage of birds was positively correlated with levels of MDA but not plasma antioxidant concentrations: more colourful nestlings had higher oxidative damage than less colourful individuals. Thus, increased carotenoid-mediated plumage does not reveal resistance to oxidative damage for nestling blue tits, but may indicate costs paid, in terms of oxidative damage. Our results indicate that the trade-offs between competing physiological systems for dietary antioxidants are likely to be complex in rapidly developing birds. Moreover, interpreting the biological relevance of different biomarkers of antioxidant status represents a challenge for evolutionary ecology.     

Supercooling ability in the house spider, Achaearanea tepidariorum: effect of field-collected and laboratory-reared prey

The influence of prey animals on the supercooling ability of the house spider, Achaearanea tepidariorum, was studied by feeding spiders with field-collected and laboratory-cultured prey animals. Irrespective of the prey species supplied, spiders given field-collected prey had a higher supercooling point than those given laboratory-cultured counterparts. This means that (1) the field prey animals contained some efficient ice nucleators, whereas the laboratory animals were free from such substances and (2) the ice nucleators must be of external origin. Several lines of evidence also suggest that, under natural conditions, potential prey animals for the house spider are highly contaminated with ice nucleators.     

Carotenoid-based bill and eye ring coloration as honest signals of condition: an experimental test in the red-legged partridge (<Emphasis Type="Italic">Alectoris rufa</Emphasis>)

Carotenoid pigments cannot be synthesized by vertebrates but must be ingested through the diet. As they seem to be a limited resource, carotenoid-based ornaments are particularly interesting as possible honest signals of individual quality, in particular of foraging efficiency and nutritional status. Some studies have demonstrated the condition dependence of carotenoid-based plumage in birds. However, many other carotenoid-pigmented bare parts (i.e. skin, caruncles, bills, cere, and tarsi) are present in birds but, in comparison with plumage, little is known about these traits as indicators of individual quality. Here, we show that the eye ring pigmentation and bill redness of the red-legged partridge (Alectoris rufa) are positively associated to body condition and recent changes in body mass. Also, we found a negative relationship between these two traits and heterophil-to-lymphocyte ratio, an indicator of physiological stress (the relationship with bill redness being significant only for males). In an experiment, we found that after a period of reduction in food intake (with the consequent loss of body mass), food-restricted birds showed lower eye ring pigmentation than ad-libitum-fed birds. Therefore, different ornaments seem to reflect changes in body condition but at different speeds or intensities (eye ring, a fleshy ornament, appears to respond more rapidly to changes in the nutritional status than a keratinized structure as the bill). These results indicate that carotenoid-based ornaments are condition-dependent traits in the red-legged partridge, being therefore susceptible to be employed as honest signals of quality in sexual selection.     

Sexually dichromatic coloration reflects size and immunocompetence in female Spanish terrapins, Mauremys leprosa

Many studies have shown the importance of colorful ornamentation in mate choosiness or intrasexual conflict. However, research on color ornaments has focused mainly on birds, lizards or fish, but remains practically unknown in other animal groups such as turtles. In addition, female ornaments and their relation with sexual selection also remain almost unknown. Here, we measured the coloration of the shell and the limb stripes of male and female Spanish terrapins Mauremys leprosa and explored the existence of sexual dichromatism and the relation of color characteristics with body size and health state estimated from the immune response to the injection of an antigen (phytohaemagglutinin test). Our results showed that shell coloration, which could be constrained by natural selection to be cryptic, changed with body size, but did not differ between sexes. In contrast, females had brighter and less ultraviolet-saturated and more orange-saturated limb stripes than males. In females, interindividual variation in limb stripe coloration was related with body size and immune response suggesting that this coloration may inform honestly about multiple traits that could be important in sexual selection. In contrast, coloration of limb stripes of males was duller than in females, and was not related with any trait suggesting that coloration is not important in sexual selection for males.     

Differential autumn migration of the aquatic warbler Acrocephalus paludicola

Relatively little attention has been paid to sex differences in the migration of birds in autumn. We studied the autumn migration strategy of molecularly sexed males and females in the globally threatened aquatic warbler Acrocephalus paludicola. We captured 176 birds at a stopover site in the Loire estuary at Donges, France. The median date for the passage of adults was 8 days earlier in males than females, although the timing of migration in first-year males and females was similar. This indicates that males, who are without parental duties, can start their migration earlier than females and first-year birds. Adults were significantly heavier than immature birds but did not have higher fat scores. In both age categories, more males (two to three times more) were captured. However, various factors (including tape-luring) can affect observed sex ratio.     

Attractants from Bartlett pear for codling moth, Cydia pomonella (L.), larvae

The alkyl ethyl and methyl esters of (2E,4Z)-2,4-decadienoic acid found in head-space samples of ripe Bartlett pear (Pyrus communis L.) stimulated a response from neonate larvae of the codling moth (CM), Cydia pomonella (L.), in both static-air Petri-plate and in upwind Y-tube and straight-tube olfactometer bioassays. In comparison with the known CM neonate attractant, (E,E)-!-farnesene, ethyl (2E,4Z)-2,4-decadienoate was attractive at 10-fold and 1,000-fold lower threshold dosages in the Petri-plate and in the Y-tube bioassays, respectively. Methyl (2E,4Z)-2,4-decadienoate was attractive to CM neonates in these bioassays at much higher doses than ethyl (2E,4Z)-2,4-decadienoate. Other principal head-space volatiles from ripe pear fruit and pear leaves, including butyl acetate, hexyl acetate, (Z)-3-hexenyl acetate, and (E)-#-ocimene, were not attractive to CM neonates. The potential uses of these pear kairomones for monitoring and control of CM in walnuts and apple are discussed.     

Fat and fed: frequent use of summer torpor in a subtropical bat

A widely held view is that torpor is avoided by mammals whenever possible because of potential costs associated with reduced body temperatures and slowed metabolic processes. We examined this hypothesis by quantifying use of torpor in relation to body condition of free-ranging northern long-eared bats (Nyctophilus bifax, approximately 10 g), a species known to hibernate, from a subtropical region during the austral summer when insects were abundant. Temperature-telemetry revealed that bats used torpor on 85% of observation days and on 38% of all nights. Torpor bouts ranged from 0.7 to 21.2 h, but the relationship between duration of torpor bouts and ambient temperature was not significant. However, skin temperature of torpid bats was positively correlated with ambient temperature. Against predictions, individuals with a high body condition index (i.e., good fat/energy reserves) expressed longer and deeper torpor bouts and also employed torpor more often during the activity phase at night than those with low body condition index. We provide the first evidence that use of torpor in a free-ranging subtropical mammal is positively related with high body condition index. This suggests that employment of torpor is maximised and foraging minimised not because of food shortages or low energy stores but likely to avoid predation when bats are not required to feed.     

Habitat quality affects stress responses and survival in a bird wintering under extremely low ambient temperatures

Animals normally respond to stressful environmental stimuli by releasing glucocorticoid hormones. We investigated whether baseline corticosterone (CORT), handling-induced corticosterone concentration(s), and body condition indices of members of willow tit (Poecile montanus) groups differed while wintering in old growth forests and managed young forests in mild weather conditions and during cold spells. Willow tits spend the winter season in non-kin groups in which dominant individuals typically claim their priority to access resources, while subordinate individuals may experience greater levels of stress and higher mortality, especially during cold spells. We captured birds to measure baseline CORT and levels of handling-induced CORT secretion after 20 min of capture. Willow tits in the young forests had higher baseline CORT and a smaller increase in CORT in response to capture than individuals in the old forests. Baseline CORT was higher in females and juvenile birds compared to adult males, whereas handling-induced CORT secretion did not differ between birds of different ages. During cold spells, baseline CORT of willow tits increased and handling-induced CORT secretion decreased, especially in birds in young forests. Willow tits’ survival was higher in the old forests, with dominant individuals surviving better than subordinates. Our results show that changes in CORT secretion reflect responses to habitat quality and climate harshness, indicating young managed coniferous forests as a suboptimal habitat for the willow tit.     

Plumage coloration and nutritional condition in the great tit<Emphasis Type="Italic"> Parus major</Emphasis>: the roles of carotenoids and melanins differ

The size and coloration of some body characters seem to influence mate choice in many species. Most animal colours are either structural or based on melanin or carotenoid pigments. It has recently been suggested that carotenoid-based or structural coloration may be a condition-dependent trait, whereas melanin-based coloration is not; a difference that may be highly relevant when studying the evolution of multiple mating preferences. We tested this hypothesis in the great tit (Parus major). The size of the melanin breast band was not correlated to nutritional condition as estimated by the rate of tail growth (ptilochronology), controlling for locality, age, sex, year and season effects. However, the correlation was significant for the hue of yellow breast (carotenoid-based coloration), and the slopes of the regressions of the two pigments to growth bars differed significantly. These results suggest that the expression of the two traits may be regulated by different mechanisms.     

Cycads: their evolution,toxins, herbivores and insect pollinators

Palaeobiological evidence indicates that gymnosperms were wind-pollinated and that insect pollination began in angiosperms in the Lower Cretaceous (ca. 135 mya) leading to close associations between higher plants and their pollinators. Cycads, which were widespread and pervasive throughout the Mesozoic (250-65 mya) are among the most primitive living seed-plants found today. Because pollination by beetles and by thrips has now been detected in several modern cycads, it is attractive to speculate that some insects and cycads had already developed similar mutualistic interactions in the Triassic (250-205 mya), long before the advent of angiosperms. We also draw attention to another key factor in this insect-plant relationship, namely secondary, defensive plant substances which must always have controlled interspecific interactions. Cycads mainly produce toxic azoglucosides and neurotoxic non-protein amino acids (e.g. BMAA), which apparently are crucial elements in the development and maintenance of mutualism (pollination) and parasitism (herbivory) by cycad-linked herbivores. We now add new results on the uptake and storage of the main toxin, cycasin, of the Mexican cycad Zamia furfuracea by its pollinator, the weevil Rhopalotria mollis, and by a specialist herbivore of Zamia integrifolia, the aposematic Atala butterfly Eumaeus atala.     

Monogamy in a new species of wild guinea pigs (Galea sp.)

A new species of wild guinea pigs from Bolivia was recently discovered: Galea sp. So far no data are available concerning its social and mating systems. We therefore investigated behavioural compatibility, sexual dimorphism, paternity in a male-competing situation, testicular and epididymal size, and sperm morphology and motility. The results showed a complete intrasexual and moderate intersexual behavioural incompatibility between unfamiliar animals, a reversed sexual dimorphism with females larger than males, and litters always fathered by single males. Furthermore, both the reproductive organ weights and the percentage of motile sperm and sperm with intact acrosomes were significantly lower compared with the promiscuous congeneric Galea musteloides. In summary, these data strongly suggest a monogamous social and mating system for the recently discovered Galea sp.     

Prenuptial perfume: Alloanointing in the social rituals of the crested auklet (<Emphasis Type="Italic">Aethia cristatella</Emphasis>) and the transfer of arthropod deterrents

Alloanointing, the transfer of chemicals between conspecifics, is known among mammals, but hitherto, the behavior has not been documented for birds. The crested auklet (Aethia cristatella), a colonial seabird of Alaskan and Siberian waters, alloanoints during courtship with fragrant aldehydes that are released from specialized wick-like feathers located in the interscapular region. Crested auklets solicit anointment at the colony, and prospective mates rub bill, breast, head, and neck over wick feathers of their partners. This distributes aldehydes over the head, neck, and face where the birds cannot self-preen. The resulting chemical concentrations are sufficient to deter ectoparasites. Auklets that emit more odorant can transfer more defensive chemicals to mates and are thus more sexually attractive. Behavioral studies showed that crested auklets are attracted to their scent. Wild birds searched for dispensers that emitted their scent and rubbed their bills on the dispensers and engaged in vigorous anointment behaviors. In captive experiments, naïve crested auklets responded more strongly to synthetic auklet scent than controls, and the greatest behavioral response occurred during early courtship. This study extends scientific knowledge regarding functions of alloanointing. Alloanointing had previously been attributed to scent marking and individual recognition in vertebrates. Alloanointing is described here in the context of an adaptive social cue — the transfer of arthropod deterrents between prospective mates.     

Immunity in a Social Insect

 Although pathogens appear to have exerted significant selective pressure on various aspects of sociality, mechanisms of disease resistance in the social insects are poorly understood. We report here on an immune response to infection by the dampwood termite, Zootermopsis angusticollis. Nymphs immunized with an injection of 7.6×10⁷, 7.6×10⁵, or 7.6×10⁴ cells/ml glutaraldehyde-killed solution of the bacterium Pseudomonas aeruginosa had significantly higher survivorship than controls following a challenge with a lethal concentration of active bacteria. Similarly, nymphs exposed to a 9×10^–1 spores/ml suspension of the fungus Metarhizium anisopliae had higher survivorship than controls after a challenge with a lethal concentration of spores. Prior exposure to a pathogen thus conferred upon termites a degree of protection during a subsequent encounter with the same pathogen. This represents the first demonstration of immune function in vivo in a social insect. Received: 18 May 1999 / Accepted in revised form: 26 August 1999     

Sex,age, spleen size,and kidney fat of red deer relative to infection intensities of the lungworm <Emphasis Type="Italic">Elaphostrongylus cervi</Emphasis>

We analyzed the relationships among spleen size, body condition (measured as kidney fat), and larval counts of the nematode Elaphostrongylus cervi in red deer (Cervus elaphus). The aim was to investigate the interaction between host body condition and intensity of infection with parasites. As red deer are highly polygynous, we also tested whether these relationships varied with sex and age of the hosts. Kidney fat and spleen size were positively correlated in subadults (2–3 years old) and adults (>3 years old), but not in calves (<1 year old) or yearlings (1–2 years old). Spleen size was negatively associated with nematode load in subadult females and in adult males. These two age classes are potentially the most nutritionally stressed, as subadult hinds are still growing and often engaging in rearing their first calf, and adult stags were sampled just after the rut, which is recognized as a substantial energy drain in this age–sex class, as they compete to hold females during the mating season. Body condition related negatively to parasite count only in adult males. In the context of red deer life history, these findings suggest that spleen size is dependent on body condition and that it could be affected by variation in resource partitioning among immune defense, growth, and reproductive effort in red deer. For the first time in a wild mammal, the spleen mass is shown to be positively related to body condition and negatively related to parasite infection. We conclude that elucidating whether spleen mass reflects immune defense investment or a measure of general body condition should contribute to understanding topical issues in mammal ecology.     

Where to find a mate? Resource-based sexual communication of webbing clothes moth

Mate location in moths typically entails long-range attraction of males to female-produced pheromone. Here, we show that male and female webbing clothes moths, Tineola bisselliella, seek larval habitats (dry carrion, animal lairs, etc) to encounter mates. With males seeking, and arriving at, larval habitat earlier at night than females, male-produced pheromonal and sonic signals enhance the habitat's attractiveness to females. This resource-based mating strategy of T. bisselliella differs from that known for most other moths. It may have evolved in response to larval habitats that are patchy and temporary, but that disseminate attractive semiochemicals so abundantly that T. bisselliella encounter them more readily than their own pheromones.