Histologic, neurologic, and immunologic effects of methylmercury in captive great egrets

Captive great egret (Ardea albus) nestlings were maintained as controls or were dosed with methylmercury chloride at low (0.5), and high doses (5 mg/kg, wet weight) in fish. Low dosed birds were given methylmercury at concentrations comparable to current exposure of wild birds in the Everglades (Florida, USA). When compared with controls, low dosed birds had lower packed cell volumes, dingy feathers, increased lymphocytic cuffing in a skin test, increased bone marrow cellularity, decreased bursal wall thickness, decreased thymic lobule size, fewer lymphoid aggregates in lung, increased perivascular edema in lung, and decreased phagocytized carbon in lung. High dosed birds became severely ataxic and had severe hematologic, neurologic, and histologic changes. The most severe lesions were in immune and nervous system tissues. By comparing responses in captive and wild birds, we found that sublethal effects of mercury were detected at lower levels in captive than in wild birds, probably due to the reduced sources of variation characteristic of the highly controlled laboratory study. Conversely, thresholds for more severe changes (death, disease) occurred at lower concentrations in wild birds than in captive birds, probably because wild birds were exposed to multiple stressors. Thus caution should be used in applying lowest observed effect levels between captive and wild studies.     

Brain cholinesterase activity of apparently normal wild birds

Organophosphorus and carbamate pesticides are potent anticholinesterase substances that have killed large numbers of wild birds of various species. Cause of death is diagnosed by demonstration of depressed brain cholinesterase (ChE) activity in combination with chemical detection of anticholinesterase residue in the affected specimen. ChE depression is determined by comparison of the affected specimen to normal ChE activity for a sample of control specimens of the same species, but timely procurement of controls is not always possible. Therefore, a reference file of normal whole brain ChE activity is provided for 48 species of wild birds from North America representing 11 orders and 23 families for use as emergency substitutes in diagnosis of anticholinesterase poisoning. The ChE values, based on 83 sets of wild control specimens from across the United States, are reproducible provided the described procedures are duplicated. Overall, whole brain ChE activity varied nearly three-fold among the 48 species represented, but it was usually similar for closely related species. However, some species were statistically separable in most families and some species of the same genus differed as much as 50%.     

Hematological, protein electrophoresis and cholinesterase values of free-living nestling peregrine falcons in Spain

Protein electrophoresis, hematological and cholinesterase values were determined in 32 nestling free-living peregrine falcons (Falco peregrinus) (15- to 27-days-old) in order to establish normal reference values for this population. The following values (mean +/- SD) were observed: prealbumin 0.31 +/- 0.04 g/dl, albumin 1.25 +/- 0.06 g/dl, alpha1 and alpha2-globulin 0.23 +/- 0.02 and 0.16 +/- 0.02 g/dl respectively, beta-globulin 1.02 +/- 0.05 g/dl, gamma-globulin 0.060 +/- 0.08 g/dl, total protein 3.79 +/- 0.18 g/dl, 21.26 +/- 1.30 white blood cells/microl (1 x 10(3)), 2.17 +/- 0.07 red blood cells/microl (1 x 10(6)), packed cell volume 37.58 +/- 0.82%, hemoglobin 20.96 +/- 0.29 g/dl, heterophils 61.14 +/- 2.50% and cholinesterase 1,184 +/- 75 IU/L. There were no difference in any of these parameters among males and females. The hematological values obtained could be considered as representative values in free-living nestling peregrine falcons.     

Carotenoid-based nestling colouration and parental favouritism in the great tit

While elaborate carotenoid-based traits in adult birds may have evolved as honest signals of individual quality in the context of sexual selection or other social interactions, the function of carotenoid-based colours in juveniles is less well understood. We investigated the hypothesis that carotenoid-based nestling colouration has evolved in response to parental preference of intensely coloured offspring during food provisioning. In a field experiment, we manipulated nestling plumage colouration by a carotenoid-supplementation and analysed the parental food provisioning behaviour before feather appearance and at the end of the nestling stage. Carotenoids per se did not influence the nestlings begging behaviour or parental feeding decisions and we found no evidence that carotenoid-based colouration in nestling great tits has a signalling function in parent-offspring interactions. Parents did not discriminate between intensely coloured and control offspring in their food provisioning and in accordance with this finding intensely coloured nestlings were not heavier or larger at the end of the nestling stage. Alternative explanations for the evolution of carotenoid-based colours in nestling birds are discussed.     

Begging, food provisioning, and nestling competition in great tit broods infested with ectoparasites

Ectoparasites are a ubiquitous environmental component of breedingbirds, and it has repeatedly been shown that hematoph-agousectoparasites such as fleas and mites reduce the quality andnumber of offspring of bird hosts, thereby lowering the valueof a current brood. Selection acting on the hosts will favorphysiological and behavioral responses that will reduce theparasites' impact. However, the results of the few bird studiesthat addressed the question of whether parasitism leads to ahigher rate of food provisioning are equivocal, and the beggingresponse to infestation has rarely been quantified. A changein begging activity and parental rate of food provisioning couldbe predicted in either direction: parents could reduce theirinvestment in the brood in order to invest more in future broods,or they could increase their investment in order to compensatefor the parasites' effect on the current brood. Since the nestlingsare weakened by the ectoparasites they may beg less, but onthe other hand they may beg more in order to obtain more food.In this study we show experimentally that (1) hen fleas (Ceratophyllusgallinae) reduce the body mass and size of great tit (Parusmajor) nestlings, (2) nestlings of parasitized broods more thandouble their begging rate, (3) the male parents increase thefrequency of feeding trips by over 50%, (4) the females do notadjust feeding rate to the lowered nutritional state of nestlings,and (5) food competition among siblings of parasitized broodsis increased. Ultimately the difference in the parental feedingresponse may be understood as the result of a sex-related differencein the trade-off of i0vesting in current versus future broods.     

Methylmercury accumulation in tissues and its effects on growth and appetite in captive great egrets

To test the hypothesis that fledging wading birds would be more at risk from mercury toxicosis than younger nestlings, captive great egret nestlings were maintained as controls or were dosed from 1- to 14-wk-old with 0.5 or 5 mg methylmercury chloride/kg wet weight in fish. Birds dosed with 5 mg/kg suffered from subacute toxicosis at wk 10-12. Growing feather concentrations were the most closely correlated with cumulative mercury consumed per weight. Blood concentrations of mercury increased more rapidly after 9 wk in all groups when feathers stopped growing. Total mercury accumulated in tissues in concentrations in the following order: growing scapular feathers > powderdown > mature scapular feathers > liver > kidney > blood > muscle > pancreas > brain > bile > fat > eye. The proportion of total mercury that was methylated depended upon tissue type and dose group. Selenium accumulated in liver in direct proportion to liver mercury concentrations. After wk 9, appetite and weight index (weight/bill length) declined significantly in both dosed groups. At current exposure levels in the Everglades (Florida, USA) mercury deposited in rapidly growing feathers may protect nestlings from adverse effects on growth until feathers cease growing.     

Induced responses of nestling great tits reduce hen flea reproduction

The dynamics of host–parasite interactions depend to a large extent on the effect of host responses on parasite fitness. Exposure to parasites may induce behavioural or physiological responses in hosts that may reduce the subsequent survival or reproductive output of the parasite. Neonate hosts may further directly obtain immunologically active substances from their mother, for instance via milk in mammals or egg yolk in birds. However, the relative importance of maternally‐derived and self‐generated responses in inducing parasite resistance is poorly understood, especially in free‐living vertebrates. Here we investigate the complementary effect of experimentally induced maternal and neonate responses in great tit (Parus major) hosts on the reproductive success of their common ectoparasite, the hen flea (Ceratophyllus gallinae). In the laboratory we measured the number of eggs and larvae produced by individual flea females collected from host nests. In addition, the total number of larvae produced by an experimentally set number of flea females in the host's nestbox was assessed under field conditions. There was no indication of maternally‐transferred parasite resistance, since exposing the mother to fleas during the laying period did not affect the reproductive rate of fleas exploiting her offspring early or late in the nestling cycle. Independent of the maternal treatment, exposure of neonates to fleas early in the nestling period reduced the reproductive output of fleas late in the nestling cycle. The effect of the induced nestling response was seasonal, reducing flea reproduction in nests of early‐breeding hosts but not in nests of late‐breeding ones. Larvae production in the nestbox and in the laboratory was positively correlated, but under natural conditions the neonate response did not affect the size of the flea larvae population. Our results indicate induced responses as a means by which neonate avian hosts resist ectoparasites. Other factors, such as the environmental temperature and density‐dependent larval competition, may be more important in determining the size of the future parasite populations.     

Immunocompetence of nestling great tits in relation to rearing environment and parentage

Theoretical models of host–parasite coevolution assume a partially genetic basis to the variability in susceptibility to parasites among hosts, for instance as a result of genetic variation in immune function. However, few empirical data exist for free-living vertebrate hosts to support this presumption. In a cross-fostering experiment with nestling great tits, by comparing nestlings of the same origin we investigated (i) the variance in host resistance against an ectoparasite due to a common genetic origin, (ii) the effect of ectoparasite infestation on cell-mediated immunity and (iii) the variance in cell-mediated immunity due to a common genetic origin. Ectoparasitic hen fleas can impair the growth of nestling great tits and nestling growth was therefore taken as a measure of host susceptibility. A common origin did not account for a significant part of the variation in host susceptibility to fleas. There was no significant overall effect of fleas on nestling growth or cell-mediated immunity, as assessed by a cutaneous hypersensitivity response. A common rearing environment explained a significant part of the variation in cell-mediated immunity among nestlings, mainly through its effect on nestling body mass. The variation in cell-mediated immunity was also related to a common origin. However, the origin-related variation in body mass did not account for the origin-related differences in cell-mediated immunity. The results of the present study thus suggest heritable variation in cell-mediated immunity among nestling great tits.     

Carotenoid diet and nestling provisioning in urban and rural great tits Parus major

Considering the importance of dietary constraints for the widely held view of carotenoid pigmentation as an honest quality indicator, there is surprisingly little data on carotenoid availability in different natural diets or along environmental gradients. Here we investigate the carotenoid availability in the main diet of breeding great tits Parus major , living in urban and rural environments with known differences in carotenoid pigmentation. Carotenoid availability for nestling great tits was investigated in two respects: (1) quantity and quality of diet (i.e., caterpillar abundance and their carotenoid concentration), and (2) parental feeding frequency. First, caterpillars were generally more abundant in the urban environment and the four common Lepidoptera (i.e., caterpillars) genera studied were also heavier here. Second, as determined by HPLC analysis of the caterpillar genera, carotenoid concentration was significantly lower in the urban caterpillars. Furthermore, all except one of the caterpillar genera had higher lutein/zeaxanthin ratio in urban areas, which is in accordance with earlier studies of carotenoid composition in great tit yolk. Third, parental feeding frequency was about twice as high to urban broods compared to rural broods. This result may simply reflect the higher caterpillar abundance (shorter search time) in the urban environment. Poor food quality (low carotenoid concentration) seems therefore to be compensated by quantity in the urban environment. As a consequence the carotenoid availability seems to be similar for nestlings in the two environments.     

Effects of testosterone on song, aggression, and nestling feeding behavior in male great tits, Parus major

As outlined in the trade-off hypothesis of testosterone (T) secretion, fluctuations in T during the breeding season might reflect how males allocate their time and energy to competitive behaviors for mates and territories, associated with high T levels, and parental activities, associated with low T levels. In the present study, great tit, Parus major, males were implanted with T-filled or empty silastic capsules at the start of the breeding season and the behavior of these two male categories was compared during the entire breeding season. As a measure of competitive behavior we looked at song behavior and territorial responsiveness to a male decoy, during the three main stages of the breeding period (the egg-laying, incubation, and nestling stages). As a measure of parental care we looked at feeding behavior during the nestling stage. Our results only partly supported the trade-off hypothesis. T implants increased plasma androgen levels and enhanced spontaneous song activity and the production of aggressive vocalizations in response to a decoy. However, our results suggest that the degree of physical aggression might be less than fully coupled with T. First, approach to the decoy was not affected by the treatment. Second, although T levels are known to vary from high during egg laying to low while feeding young, control and T-treated males spent similar amounts of time close to the decoy in the three breeding stages. Our results thus suggest that vocal and physical aggression might be regulated differently in the great tit. Furthermore, in contrast with most other studies on temperate bird species but in agreement with a previous study on the great tit, T treatment did not affect male feeding rates. As the dose of T we used was lower than that typically used in other studies, we cannot at present completely exclude the possibility that the latter result reflects this lower dose of T rather than the species used.     

Experimental removal of the male parent negatively affects growth and immunocompetence in nestling great tits

Given the available empirical evidence on the benefits and costs associated with immune defence, a role for the immune system in the trade-off between current and future reproduction has been predicted. This hypothesis was studied in a free-living population of great tits (Parus major) by examining the effects of male removal on the immunocompetence, body condition, and recapture probability in the widowed females and their nestlings. Furthermore, we investigated whether growth and its relation to immunocompetence were affected in the nestlings. For a short-lived species such as the great tit, one could predict that widowed females will compensate for the lack of any male assistance in feeding of their chicks and that they consequently might jeopardize their own health. However, we did not find any negative effects of male removal on body mass or condition, nor on humoral immunocompetence against sheep red blood cells in the widowed females by the end of the feeding period. In contrast, we observed significantly reduced body mass and size as well as a reduced T-lymphocyte cell-mediated immune response (expressed as the thickness of the swelling to a subcutaneous injection with phytohemagglutinin) in the experimental nestlings compared to the control nestlings. In addition, the experimental nestlings showed a tendency for a reduced chance to be found breeding the following year. Furthermore, our results showed that in the experimental nestlings, which suffered from unfavourable growth conditions, tarsus length was inversely related to cell-mediated immunocompetence, whereas in control nestlings this relationship was significantly positive. The relationship between cell-mediated immunity and body condition was found to be significantly positive in the experimental nestlings while in control nestlings there was no relationship between both variables. The latter finding suggests different priorities of investment in body condition between different growth conditions.