Parasitism, immune response and reproductive success in the house martin Delichonurbica

Parasites often exert strong selection pressures on their hosts that have evolved anti-parasite defences to counter the negative effects of parasites. We studied the relationship between intensity of parasitism, one aspect of host immune response, and host reproductive success, using the house martin bug Oeciacushirundinis and its house martin Delichonurbica host as a model system. Experimental manipulation of parasite load of nests during laying of the first clutch altered the intensity of parasitism. Parasites reduced the reproductive success of their hosts measured in terms of body condition and survival of nestlings. Host immune response, measured as the concentration of gammaglobulins and total plasma proteins, was positively associated with parasite reproduction, estimated as the number of juvenile parasites, but was only weakly related to the intensity of adult parasites. The concentration of gammaglobulins was negatively related to nestling body mass, implying a trade-off between immune function and body condition. Parasite reproduction thus exerts a cost on hosts by increasing the immune response. Received: 25 August 1997 / Accepted: 3 November 1997     

Increased detrimental effects of ectoparasites on their bird hosts during adverse environmental conditions

Parasites are usually assumed to negatively affect fitness components of their hosts, particularly during adverse environmental conditions. We experimentally tested whether the ectoparasitic house martin bug (Oeciacus hirundinis) had larger negative effects on its house martin (Delichon urbica) host during second clutches. Conditions for reproduction decreased during the season, being less favourable for the second clutch than the first clutch. This was demonstrated by smaller clutch sizes, lower breeding success and smaller and lighter nestlings during the second clutch, as compared to the first, in the absence of parasites. Experimental manipulation of the intensity of parasitism resulted in the reproductive success of the host being reduced with increasing numbers of house martin bugs. This effect was much stronger during the second, as compared to the first, clutch. The house martin bug therefore had a greater detrimental effect on the reproduction of its host when conditions for reproduction were poor.     

Intraseasonal variation in immune defence,body mass and hematocrit in adult house martins Delichon urbica

The intensity of parasite infections often increases during the reproductive season of the host as a result of parasite reproduction, increased parasite transmission and increased host susceptibility. We report within‐individual variation in immune parameters, hematocrit and body mass in adult house martins Delichon urbica rearing nestlings in nests experimentally infested with house martin bugs Oeciacus hirundinis and birds rearing nestlings in initially parasite‐free nests. From first to second broods body mass and hematocrit of breeding adult house martins decreased. In contrast leucocytes and immunoglobulins became more abundant. When their nests were infested with ectoparasites adults lost more weight compared with birds raising nestlings in nests treated with pyrethrin, whereas the decrease in hematocrit was more pronounced during infection with blood parasites. Neither experimental infestation with house martin bugs nor blood parasites had a significant effect on the amount of immune defences.     

Effects of the parasitic botfly Philornis carinatus on nestling house wrens,Troglodytes aedon,in Costa Rica

I studied the life cycle of a botfly (Diptera: Muscidae: Philornis carinatus) and examined the effects of botfly ectoparasitism on nestling house wrens (Passeriformes: Troglodytidae: Troglodytes aedon) during three years in Costa Rica. At three study sites, I found that nestlings were relatively unaffected by botflies, in contrast to all other studies of birds infected with philornid botflies. At Monteverde, the main study site, infected chicks grew slightly slower and had slightly shorter tarsi and wing chords than uninfected chicks, but both groups fledged at similar weights. Since weight at fledging is the only growth character associated with post-fledging survivorship, botfly infections likely cost wrens little in terms of fitness. At all sites, fledging success did not differ between infected and uninfected nests. Botfly infections were more prevalent at two lower elevation sites than at the high elevation Monteverde side. Infection prevalence increased during the nesting season at all study sites, which suggests a botfly life cycle in which adult population levels increase during the wren breeding season and then decline during a dormant period when wrens are not nesting. Finally, botflies may attack chicks throughout the period before fledging, but there is no indication they locate nests before hatching. In sum, botfly parasitism on wrens appears to be benign, perhaps because the study sites are at the edge of the botfly's range or because wrens are not a preferred host.     

Increase in a heat-shock protein from blood cells in response of nestling house martins (Delichon urbica) to parasitism: an experimental approach

Heat-shock proteins (HSPs) are synthesized by animals and plants in response to various stressors. The level of the HSP60 stress protein was measured from the cell fraction of peripheral blood obtained from nestling house martins (Delichon urbica) to test whether ectoparasitism increased the concentration of stress protein. We assessed HSP from nestlings raised in nests previously treated with an insecticide or infested with 50 martin bugs (Oeciacus hirundinis). In addition, haematozoa infections were checked in blood smears. Nestlings from parasite-infested nests, or nestlings infected with trypanosomes, had increased levels of HSP in their blood cells. Nestling growth as determined from wing length was negatively related to HSP60 levels and within-brood variation in wing length increased with increasing levels of the stress protein independently of treatment and infection by trypanosomes. These results suggest HSPs may play a role in host-parasite interactions, and that they can be used reliably for measuring physiological responses to parasites. Received: 4 February 1998 / Accepted: 4 May 1998     

Changes in abundance of native and introduced parasites (Hymenoptera: Braconidae), and of the target and non-target plant bug species (Hemiptera: Miridae), during two classical biological control programs in alfalfa.

High numbers of tarnished plant bugs [Lygus lineolaris (Palisot)], were once common in alfalfa, as was a low level of parasitism (9%) by the native Peristenus pallipes (Curtis). After the bivoltine European parasite Peristenus digoneutis Loan became well established, average parasitism of the first and second generations increased to 64%, and tarnished plant bug numbers dropped by 65%. This reduced host density eventually caused a decline in total parasitism by both parasite species to 22%. A few P. digoneutis also attacked the alfalfa plant bug, Adelphocoris lineolatus (Goeze), but did not reduce this pest or increase its parasitism rate. At another location, where P. digoneutis is not established, parasitism of first generation alfalfa plant bugs, an adventive (accidently introduced) pest, was increased to 21% by the introduced univoltine parasite, Peristenus conradi Marsh, and a slight reduction in the pest may have resulted. P. digoneutis did not parasitize the meadow plant bug, Leptopterna dolabrata (L.), an adventive pest of forage grasses, so did not affect this mirid or its parasite. Neither introduced parasite eliminated the native parasites of the tarnished or alfalfa plant bugs. The narrow host ranges of the braconid parasites of mirid nymphs are contrasted with the broad host range of the native tachinid parasite [Phasia robertsoni (Towns.)] of adult mirids. The major changes in mirid abundance and their mortality by parasites that slowly occurred during this 19-year study demonstrate the need for long-term field research, to adequately document and understand these complex interactions.     

Offspring sex ratio skew in the sexually monomorphic house martin Delichon urbicum

Sex ratio at conception may be under selection pressure, given that male and female offspring differ in the cost of production or generate different fitness returns under specific conditions. We studied adjustments in the primary, secondary and tertiary sex ratio in house martin Delichon urbicum, which is a sexually monomorphic, socially monogamous, colonial bird. Males of this species engage in extra‐pair copulations with heavy males acquiring the highest fertilization success. We analyzed variation in the sex ratio in relation to clutch size and parental characteristics including body condition, wing length, as well as length and pigmentation of the white rump patch during three breeding seasons. The only variable which significantly explained the variation in the sex ratio was wing length of the social father and mother. The proportion of sons among offspring was positively correlated to wing length of the social father and negatively correlated to mother wing length. Social father wing length positively correlated with mean brood body mass at fledging, which may suggest that females that mated with long‐winged males produced sons, which acquired the highest total fertilization success. Consequently, our results indicate that house martin females may adaptively adjust offspring sex composition at egg laying in relation to the characteristics of their social mate.     

Fitness consequences of hybridization between house sparrows (Passer domesticus) and tree sparrows (P. montanus)

Gene transfer may occur following hybridization between closely related species if hybrids are viable and able to breed with individuals of one or both of the parental species. House (Passer domesticus) and tree sparrows (P. montanus) occasionally hybridize and produce viable offspring. Previously, we concluded that male tree × house sparrow hybrids are most probably fertile based on the observation of a male F1 hybrid feeding the nestlings with a female house sparrow in two consecutive clutches. However, recent DNA analyses based on blood samples revealed that all nestlings (4) in the first clutch were sired by a neighbouring house sparrow male, whereas nestlings in the second clutch (2) were not blood sampled and most probably died before fledging. This indicates that extensive extra-pair fertilization confounded our previous conclusion, and indicates that social partnership and attending behaviour can be imprecise measures of paternity.     

North‐African house martins endure greater haemosporidian infection than their European counterparts

Afro‐Palearctic migrant species are exposed to parasites at both breeding and over‐wintering grounds. The house martin Delichon urbicum is one such migratory species facing high instances of blood parasite infection. In an attempt to determine whether breeding European house martins harbour similar blood parasite communities to populations breeding in North Africa, birds were sampled at their breeding grounds in Switzerland and Algeria. Moreover, haemosporidian prevalence and parasite communities were compared to published data sets on Spanish and Dutch breeding populations. This study furthermore wanted to establish whether co‐infection with multiple genera or lineages of parasites had negative e?ects on host body condition. Breeding house martins caught in Algeria showed a higher prevalence of avian haemosporidian parasites than did European populations. Swiss house martins showed a prevalence comparable to that of Spanish and Dutch populations. There were slight differences in the haemosporidian community between European and North‐African populations in terms of composition and abundance of each lineage. Similar to the Dutch house martins, but in contrast to the Spanish population, infection status and number of genera of parasites infecting single hosts did not in?uence Swiss house martin body condition.     

Malarial parasites decrease reproductive success: an experimental study in a passerine bird

Malarial parasites are supposed to have strong negative fitness consequences for their hosts, but relatively little evidence supports this claim due to the difficulty of experimentally testing this. We experimentally reduced levels of infection with the blood parasite Haemoproteus prognei in its host the house martin Delichon urbica, by randomly treating adults with primaquine or a control treatment. Treated birds had significantly fewer parasites than controls. The primaquine treatment increased clutch size by 18%; hatching was 39% higher and fledging 42% higher. There were no effects of treatment on quality of offspring, measured in terms of tarsus length, body mass, haematocrit or T-cell-mediated immune response. These findings demonstrate that malarial parasites can have dramatic effects on clutch size and other demographic variables, potentially influencing the evolution of clutch size, but also the population dynamics of heavily infected populations of birds.     

Ontogeny of metabolism,thermoregulation and torpor in the house martin Delichon u. urbica (L.) and its ecological significance

Summary Special energetic adaptations are of great evolutionary significance for birds that encounter transient problems in finding food during the breeding season. House martins, as aerial insectivores, encounter such problems during spells of bad weather, when they must survive on body reserves. This species employs the following behavioural and physiological adaptations to save energy: Low basal metabolic rate (only 43% of the values predicted by allometric equations); low thermal conductance 51% (day) and 67% (night) of the predicted values; clustering behaviour; high tolerance of the young to periods of low food supply; and the ability to become torpid, found in adults and young from the age of 11 days on. House martins are the first passerine birds in which torpor has been found. These adaptations might have played a role in the great success of the house martin, one of the 10–15 most abundant bird species in Europe.Abbreviations BMR Basal metabolic rate, J/g·h - C Thermal conductance, J/g·h°C - M Energy metabolism, J/g·h - Ta Ambient temperature, °C - Tb Body temperature, °C - W Body mass, g A great part of these investigations were done in the laboratory of Prof. Dr. E. Kulzer, Physiologische Ökologie, Auf der Morgenstelle 28, D-7400 Tübingen, FRG     

Hopeless solicitation? Host-absent vocalization in the common cuckoo has no effect on feeding rate of reed warblers

Begging behavior of nestlings can signal both hunger and competitive ability. Studies of begging in evicting avian brood parasites exclude the influence of nestling competition and may provide new insights into the host–parasite conflict and the evolution of signaling. Apart from the begging call, common cuckoo Cuculus canorus nestlings use special vocal displays in the absence of their hosts, termed here host-absent vocalization (HAV). Since these conspicuous calls can increase the risk of predation and require energy, their costs should be balanced by some benefits, such as increased food provisioning. However, there has been no evidence that chicks convey information about their hunger by HAV. We therefore tested experimentally whether cuckoo chicks use HAV as an additional signal to enhance food-delivery rate by their hosts. We used playback of HAV recorded from cuckoo nestlings to determine whether their hosts, reed warblers Acrocephalus scirpaceus, increase their provisioning in response to an apparent increase in HAV. Older chicks spent more time in HAV than younger chicks, suggesting that HAV is not caused by inaccurate discrimination of host arrival stimuli. Negative correlation of HAV with feeding rate and mass gain between the two experiments suggested that hunger was the motivation of HAV. The playback experiment, however, did not prove that HAV affects host provisioning rate. We discuss possible reasons for this result and provide alternative explanations for HAV, such as creating a bond between the hosts and the parasitic young used later in the postfledging care.     

Strength in numbers: high parasite burdens increase transmission of a protozoan parasite of monarch butterflies (<Emphasis Type="Italic">Danaus plexippus</Emphasis>)

Parasites often produce large numbers of offspring within their hosts. High parasite burdens are thought to be important for parasite transmission, but can also lower host fitness. We studied the protozoan Ophryocystis elektroscirrha, a common parasite of monarch butterflies (Danaus plexippus), to quantify the benefits of high parasite burdens for parasite transmission. This parasite is transmitted vertically when females scatter spores onto eggs and host plant leaves during oviposition; spores can also be transmitted between mating adults. Monarch larvae were experimentally infected and emerging adult females were mated and monitored in individual outdoor field cages. We provided females with fresh host plant material daily and quantified their lifespan and lifetime fecundity. Parasite transmission was measured by counting the numbers of parasite spores transferred to eggs and host plant leaves. We also quantified spores transferred from infected females to their mating partners. Infected monarchs had shorter lifespans and lower lifetime fecundity than uninfected monarchs. Among infected females, those with higher parasite loads transmitted more parasite spores to their eggs and to host plant leaves. There was also a trend for females with greater parasite loads to transmit more spores to their mating partners. These results demonstrate that high parasite loads on infected butterflies confer a strong fitness advantage to the parasite by increasing between-host transmission.     

Development of thermoregulation and torpor in a marsupial: energetic and evolutionary implications

Altricial mammals and birds become endothermic at about half the size of adults and presumably would benefit energetically from entering torpor at that time. Because little is known about torpor during development in endotherms, we investigated whether after the establishment of endothermic thermoregulation (i.e. the ability to maintain a high body temperature during cold exposure), Sminthopsis macroura, a small (∼25 g) insectivorous marsupial, is capable of entering torpor and whether torpor patterns change with growth. Endothermic thermoregulation was established when the nest young reached a body mass of ∼10 g, and they were capable of entering torpor early during development at ∼10–12 g, lending some support to the view that torpor is a phylogenetically old mammalian trait. Torpor bout length shortened significantly and the minimum metabolic rate during torpor increased as juveniles approached adult size, and consequently total daily energy expenditure increased steeply with age. Relationships between total daily energy expenditure and body mass during development of S. macroura (slope ∼1.3) differed substantially from the relationship between basal metabolism and body mass in adult endotherms (slope ∼0.75) suggesting that the energy expenditure–size relationship during the development differs substantially from that in adults under thermo-neutral conditions. Our study shows that while torpor can substantially reduce energy expenditure during development of endotherms and hence is likely important for survival during energy bottlenecks, it also may enhance somatic growth when food is limited. We therefore hypothesize that torpor during the development in endotherms is far more widespread than is currently appreciated.     

Energy allocation for reproduction in a marsupial arboreal folivore,the common ringtail possum (Pseudocheirus peregrinus)

This study examines the annual energetics of a small folivorous marsupial, Pseudocheirus peregrinus. Particular attention was given to the energy and time allocated to reproduction by the females. Daily energy expenditure was measured directly using the doubly labelled water technique. Energy transferred to the young via the milk was estimated from information on milk composition and production. There was no significant seasonal variation in the energy expenditure or water influx of males or females. The mean daily energy expenditure of a 1-kg non-lactating adult ringtail possum was 615 kJ day^–1 or 2.2 times standard metabolic rate. Females showed significant changes in daily energy expenditure according to their reproductive status. Without the burden of lactation the total annual energy expenditure of an adult female was estimated as 212.4 MJ kg^–1 year^–1. The total annual energy expenditure of a female rearing two young was 247.5 MJ kg^–1 year^–1, with the late stage of lactation constituting the most energetically expensive period accounting for 30% of the total yearly energy expenditure during 24% of the time. Total metabolisable energy allocation during reproduction (22 MJ kg) was similar to estimates available for other herbivores, although, the peak metabolisable energy allocation during lactation (759 kJ day^–1) was lower than values available for other herbivores. The total energy requirement for reproduction (metabolisable energy plus potential energy exported to young via milk) suggests that the ringtail possum also has a relatively low overall energy investment in reproduction. It is suggested that the lactational strategy of the ringtail possum has been selected in order to spread the energy demands of reproduction over time due to constraints on the rate of energy intake imposed by a leaf diet and/or to prolong the mother-young bond. The strategies a female ringtail possum may employ to achieve energy balance when faced with the energy demands of reproduction are discussed.     

Physiological and haematological consequences of a novel parasite on the red-rumped swallow Hirundo daurica

Parasite virulence has been hypothesised to increase with the degree of host sociality because highly social hosts have a greater probability of encountering horizontal transmission of parasites and experiencing infections with multiple strains of the same parasites than do solitary hosts. As compared with the defences of closely related social host species, we predicted that solitary hosts should have relatively weak defences against parasites, thus being relatively more affected when parasitised by a novel parasite. We tested this prediction by either experimentally infesting 12 nests of the solitarily nesting red-rumped swallow Hirundo daurica with 50 individuals of the generalist martin bug Oeciacus hirundinis or by fumigation of nine nests. Nestlings 13 days old from the parasite addition group experienced increased mortality, attained lower body mass and tended to have shorter tarsi compared to nestlings from fumigated nests. Surprisingly, nestlings from the parasite addition group had higher packed cell volume (cellular fraction of blood) and lower levels of heat shock proteins (HSP60) than nestlings from the fumigation group. A measure of immunocompetence was not significantly affected by treatment, but its magnitude was positively related to packed cell volume and negatively related to level of HSP60. Solitary hosts like the red-rumped swallow have weak immune responses and low levels of heat shock proteins when infested with ectoparasites while highly social hosts have strong immune responses and high levels of heat shock proteins when infested. These findings partially support the hypothesis that potential host species with weak defences are more susceptible to infection and the deleterious effects of evolving parasites than potential hosts with strong defences.     

Parent-offspring regression suggests heritable susceptibility to ectoparasites in a natural population of kittiwake Rissa tridactyla

Little information is available on the genetic variability of host susceptibility to parasites in natural populations despite its importance for the understanding of the evolution of host-parasite interactions. A long-term demographic and epidemiologic survey of a seabird population allowed us to investigate the potential correlation between parent and offspring ectoparasite load, while controlling for various environmental factors. In particular, parasite loads were measured for all individuals (i.e., parents and offspring) when they were nestlings and the effect of the year and breeding cliff were taken into account. The positive correlation found between parent and offspring parasite loads suggests a heritable susceptibility to ectoparasitism by ticks in this host population and that this character has the potential to respond to natural selection.     

Fitness-related consequences of egg mass in nestling house wrens

The fitness-related consequences of egg mass, independent of confounding influences associated with parental quality, remain poorly understood for wild birds in general and for passerines in particular. We performed cross-fostering experiments to test the hypothesis that egg mass, independent of parental quality, is the primary determinant of fitness-related traits in nestling house wrens (Troglodytes aedon), an insectivorous passerine. Nestling mass was significantly correlated with the mass of the eggs from which nestlings hatched early but not late in the nestling period in early-season broods. In contrast, in late-season broods, nestling mass was correlated with egg mass until nestlings achieved asymptotic mass. Neither nestling growth nor survival to nest leaving was related to egg mass in either early- or late-season broods; however, nestlings in late-season broods grew more slowly than did nestlings in early-season broods. We propose that nestling mass and egg mass remained correlated throughout the nestling period in late-season broods because decreased arthropod food resources late in the breeding season constrain parents'' ability to provision nestlings. We conclude that female house wrens in this population trade-off clutch size for greater egg mass to maximise reproductive success in late-season broods.     

Effect of body mass and water temperature on the standard metabolic rate of juvenile yellow perch, Perca flavescens (Mitchill)

Fish respiration rates that are presumed to represent standard metabolic rates (SMR) may sometimes include an unspecified energy expenditure associated with activity and digestion. This situation may introduce a bias in bioenergetics models because standard metabolism, digestion, and activity may not be affected by the same environmental conditions. The aim of this study was to (1) develop a SMR model for juvenile yellow perch, Perca flavescens (Mitchill), that represent the minimum energy expenditure required to maintain life and (2) compare the results of this study with published perch metabolic rates and bioenergetics models. SMR was estimated for yellow perch over a range of body␣mass (4.4–24.7 g) and water temperature (12–20°C). The intercept of the relationship between fish respiration and swimming velocity obtained during forced swimming experiments was used to determine SMR. SMR estimated by the present study were comparable to values presented by two published studies on Eurasian perch, Perca fluviatilis L. However, estimated SMR were 4.1–20.9 times lower than values of a third respirometry study and predictions of bioenergetics models for perch. The present study suggests that published SMR models may sometimes include a significant fraction of energy expenditures (39.2–75.9%) associated with digestion and activity. This may complicate the implementation and the interpretation of fish bioenergetics models. The present study indicates that the intercept of respiration-velocity relationships and long-term respiration rates during starvation experiments may provide similar and reliable SMR values.     

Group size and nest spacing affect Buggy Creek virus (Togaviridae: Alphavirus) infection in nestling house sparrows

The transmission of parasites and pathogens among vertebrates often depends on host population size, host species diversity, and the extent of crowding among potential hosts, but little is known about how these variables apply to most vector-borne pathogens such as the arboviruses (arthropod-borne viruses). Buggy Creek virus (BCRV; Togaviridae: Alphavirus) is an RNA arbovirus transmitted by the swallow bug (Oeciacus vicarius) to the cliff swallow (Petrochelidon pyrrhonota) and the introduced house sparrow (Passer domesticus) that has recently invaded swallow nesting colonies. The virus has little impact on cliff swallows, but house sparrows are seriously affected by BCRV. For house sparrows occupying swallow nesting colonies in western Nebraska, USA, the prevalence of BCRV in nestling sparrows increased with sparrow colony size at a site but decreased with the number of cliff swallows present. If one nestling in a nest was infected with the virus, there was a greater likelihood that one or more of its nest-mates would also be infected than nestlings chosen at random. The closer a nest was to another nest containing infected nestlings, the greater the likelihood that some of the nestlings in the focal nest would be BCRV-positive. These results illustrate that BCRV represents a cost of coloniality for a vertebrate host (the house sparrow), perhaps the first such demonstration for an arbovirus, and that virus infection is spatially clustered within nests and within colonies. The decreased incidence of BCRV in sparrows as cliff swallows at a site increased reflects the "dilution effect," in which virus transmission is reduced when a vector switches to feeding on a less competent vertebrate host.