Ectoparasitic mites and their Drosophila hosts

Only two parasite interactions are known for Drosophila to date: Allantonematid nematodes associated with mycophagous Drosophilids and the ectoparasitic mite Macrocheles subbadius with the Sonoran Desert endemic Drosophila nigrospiracula. Unlike the nematode-Drosophila association, breadth of mite parasitism on Drosophila species is unknown. As M. subbadius is a generalist, parasitism of additional Drosophilids is expected. We determined the extent and distribution of mite parasitism in nature Drosophilids collected in Mexico and southern California. Thirteen additional species of Drosophilids were infested. Interestingly, 10 belong to the repleta species group of the subgenus Drosophila, despite the fact that the majority of flies collected were of the subgenus Sophophora. In all cases but 2, the associated mites were M. subbadius. Drosophila hexastigma was found to have not only M. subbadius, but another Mesostigmatid mite, Paragarmania bakeri, as well. One D. hydei was also found to have a mite from genus Lasioseius attached. In both choice and no-choice experiments, mites were more attracted to repleta group species than to Sophophoran. The extent of mite parasitism clearly is much broader than previously reported and suggests a host bias mediated either by mite preference and/or some mechanism of resistance in particular Drosophilid lineages.     

Host defense in Nicrophorus quadripunctatus against brood parasitism by Ptomascopus morio (Coleoptera: Silphidae: Nicrophorinae)

Few studies have been conducted on the host defenses of insects against brood parasitism. We investigated whether the silphid beetle Ptomascopus morio, a brood parasite of related silphid species Nicrophorus concolor, can also parasitize another silphid species Nicrophorus quadripunctatus and the manner in which N. quadripunctatus defends itself against parasitism. Successful brood parasitism under natural conditions was not observed at the time of year when P. morio and N. quadripunctatus are both reproductively active. Follow-up experiments revealed that P. morio attempts to oviposit near N. quadripunctatus nests, but is rarely successful if adult hosts are present. When P. morio larvae were experimentally introduced to N. quadripunctatus broods, some P. morio larvae survived when the host and parasite larvae were at the same stage. We concluded that N. quadripunctatus defends itself against brood parasitism in two ways: (1) potential brood parasites are repelled, thus limiting their access to the resource; and (2) the young of the parasitic species are killed.     

Sex-specific defence behaviour against brood parasitism in a host with female-only incubation

Nest protection against intruders is an indispensable component of avian parental care. In species with biparental care, both mates should evolve nest defence behaviour to increase their reproductive success. In most host-parasite systems, host females are predicted to have more important roles in nest defence against brood parasites, because they typically are primarily responsible for clutch incubation. Male antiparasitic behaviour, on the other hand, is often underestimated or even not considered at all. Here we investigated sex-specific roles in four aspects of great reed warbler (Acrocephalus arundinaceus) nest defence against a brood parasite—the cuckoo (Cuculus canorus), namely (1) mobbing, (2) nest attendance/guarding, (3) nest checking and (4) egg ejection. Using dummy experiments, simulating brood parasitism and by video-monitoring of host nests we found that males took the key roles in cuckoo mobbing and nest guarding, while females were responsible for nest checking and egg ejection behaviours. Such partitioning of parental roles may provide a comprehensive clutch protection against brood parasitism.     

Diversity in interspecific interactions between a nest-associating species, Pungtungia herzi, and multiple host species

Nest association in fishes affects the reproductive success of the host to varying degrees, from complete failure of the host’s reproduction to fitness advantages. Such varying impacts of nest association are considered to result from both the associate’s behavior and the characteristics of the host’s reproduction. To investigate the relationship between the impact of nest associate and host/associate ecology as well as evolutionary strategies involving nest association, we compared reproductive strategies and success between an associate East Asian minnow, Pungtungia herzi, and two host fishes (a goby, Odontobutis obscura, and a catfish, Pseudobagrus nudiceps) that have different reproductive ecologies. The associate frequently spawned around the days on which both hosts spawned, and gained a fitness advantage through continuous egg protection. Spawning by the associate had a negative effect on the survival of O. obscura eggs. Male O. obscura tended to abandon their nest when it was parasitized during the pre-spawning period. This is likely a tactic to alleviate the costs of brood parasitism. In contrast, survival of P. nudiceps eggs was consistently high in all nests, regardless of the intensity of associate’s spawning, and P. nudiceps young fed on cyprinid offspring (most probably the associate’s eggs/young) in the nest. Both P. nudiceps and P. herzi populations likely gain fitness benefits from their relationship. When comparing these two hosts with another known host, the freshwater perch Coreoperca kawamebari, the observed differences in the impact of nest association to the associate species likely correspond to differences in the spatial reproductive resources used by the respective hosts.     

Multiple effects of brood parasitism reduce the reproductive success of prothonotary warblers, Protonotaria citrea

Avian brood parasitism often has multiple negative effects on the reproductive success of the host. Most studies have focused on one or two of these effects, but rarely have they all been studied simultaneously for one species. I studied prothonotary warblers to quantify the effects of different intensities of (i.e. multiple) brood parasitism by brown-headed cowbirds, Molothrus ater, on the production of host and cowbird young and on the between-year returns of adult warblers. Host clutch size decreased with an increase in the number of cowbird eggs laid in nests. The hatching success of warbler and cowbird eggs decreased with increased cowbird eggs in nests, but was always higher for cowbird eggs than warbler eggs. The survival of warbler nestlings, but not cowbird nestlings, decreased with increased cowbird nestlings in the brood. An increase in the number of cowbird nestlings in broods resulted in a reduction in the average mass of warbler nestlings but not cowbird nestlings. The number of cowbird eggs or nestlings present did not affect nest predation, and the fledging of cowbirds did not influence the renesting interval of female warblers. In addition, the between-year returns of adult warblers were not negatively affected by brood parasitism. Decreased hatching success and nestling survival reduced the reproductive output of the warblers the most. These effects were substantial and appear to favour the evolution of behavioural responses that reduce the effects of brood parasitism on prothonotary warblers. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour      

Experiments and observations of prothonotary warblers indicate a lack of adaptive responses to brood parasitism

It has been suggested that prothonotary warblers, Protonotaria citrea, respond adaptively to brood parasitism by brown-headed cowbirds, Molothrus ater, even though they lack historical habitat and range overlap with cowbirds. I studied behaviours functioning as potential defences against brood parasitism in the prothonotary warbler, a cavity-nesting host species. Opening sizes preferred by prothonotary warblers were not small enough to exclude cowbirds, and warblers were parasitized heavily in nests with larger openings. Male and female prothonotary warblers were always away from their nests before sunrise when cowbirds laid eggs in their nests. Prothonotary warblers infrequently (∼6% of 560 nests) deserted nests that were parasitized during the egg-laying period, but frequently (56% of 151 nests) deserted nests that were parasitized before a female warbler laid her first egg. Prothonotary warblers also deserted 60-70% of nests where a cowbird egg, warbler egg or die were experimentally added before egg laying. However, the experimental addition of one of these three objects during the egg-laying period did not elicit desertion. The desertion of parasitized nests was not affected by nest site availability as has been reported elsewhere in the literature. This lack of a response to brood parasitism by prothonotary warblers may be an example of evolutionary lag, because it is likely that they have only recently been exposed to widespread parasitism, and they accept parasitism at a high cost to their own reproductive success. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Who parasitizes the endangered Jankowski’s Bunting Emberiza jankowskii?

ABSTRACT

We report nine cases of brood parasitism in the endangered Jankowski’s Bunting Emberiza jankowskii by cuckoos in Inner Mongolia Province, China in 2018 and 2019. DNA-based and morphological evidence suggested that five chicks and four eggs of brood parasites were all Common Cuckoo Cuculus canorus, for which the Jankowski’s Bunting is a regular host.     

Effect of Density and Extra Dung on Brood Parasitism in the Dung Beetle, Onthophagus Taurus

Kleptoparasitism has not been well documented in insects and intraspecific brood parasitism is even less well known. This study examines the effect of extra resources and density on the probability of kleptoparasitism in the bull headed dung beetle Onthophagus taurus. A high level (>60 %) of kleptoparasitism was found across all treatments and suggest that although density may not affect the probability to kleptoparasitize, it may influence brood ball production. This study also documents for the first time that male O. taurus kleptoparasitize.     

The phylogenetic position of the bumble bee inquiline Bombus inexspectatus and implications for the evolution of social parasitism

The high alpine European bumble bee Bombus (Thoracobombus) inexspectatus is one of three taxa in which obligate social parasitism has evolved in bumble bees. Until now, the phylogenetic placement of this species has not been analyzed quantitatively because it is rare in nature. Here a specimen of B. inexspectatus is sequenced for five genes to assess its phylogenetic position relative to other bumble bee species. Phylogenetic estimation of B. inexspectatus places this species within the subgenus Thoracobombus, as expected based on morphology. This provides strong support for the acquisition of social parasitism in B. inexspectatus separate from that found in the bumble bees of the subgenus Psithyrus and B. (Alpinobombus) hyperboreus. Furthermore, B. inexspectatus is not the sister taxon of its host but is a near relative, suggesting a loose but not strict adherence to Emery’s rule. B. inexspectatus is a sister taxon to a clade including B. veteranus, a frequent nest usurper that has been suggested to be a facultative social parasite. The phylogenetic placement of all bumble bee social parasites relative to their hosts is discussed.     

Experimental transmission of Leishmania (Mundinia) parasites by biting midges (Diptera: Ceratopogonidae)

Leishmania parasites, causative agents of leishmaniasis, are currently divided into four subgenera: Leishmania, Viannia, Sauroleishmania and Mundinia. The recently established subgenus Mundinia has a wide geographical distribution and contains five species, three of which have the potential to infect and cause disease in humans. While the other Leishmania subgenera are transmitted exclusively by phlebotomine sand flies (Diptera: Psychodidae), natural vectors of Mundinia remain uncertain. This study investigates the potential of sand flies and biting midges of the genus Culicoides (Diptera: Ceratopogonidae) to transmit Leishmania parasites of the subgenus Mundinia. Sand flies (Phlebotomus argentipes, P. duboscqi and Lutzomyia migonei) and Culicoides biting midges (Culicoides sonorensis) were exposed to five Mundinia species through a chicken skin membrane and dissected at specific time intervals post bloodmeal. Potentially infected insects were also allowed to feed on ear pinnae of anaesthetized BALB/c mice and the presence of Leishmania DNA was subsequently confirmed in the mice using polymerase chain reaction analyses. In C. sonorensis, all Mundinia species tested were able to establish infection at a high rate, successfully colonize the stomodeal valve and produce a higher proportion of metacyclic forms than in sand flies. Subsequently, three parasite species, L. martiniquensis, L. orientalis and L. sp. from Ghana, were transmitted to the host mouse ear by C. sonorensis bite. In contrast, transmission experiments entirely failed with P. argentipes, although colonisation of the stomodeal valve was observed for L. orientalis and L. martiniquensis and metacyclic forms of L. orientalis were recorded. This laboratory-based transmission of Mundinia species highlights that Culicoides are potential vectors of members of this ancestral subgenus of Leishmania and we suggest further studies in endemic areas to confirm their role in the lifecycles of neglected pathogens.     

The ghosts of parasitism past: lingering frontline anti-brood parasite defenses in a former host

Coevolutionary arms races between brood parasites and hosts provide tractable systems for understanding antagonistic coevolution in nature; however, little is known about the fate of frontline antiparasite defenses when the host “wins” the coevolutionary arms race. By recreating bygone species interactions, using artificial parasitism experiments, lingering defensive behaviors that evolved in the context of parasitism can be understood and may even be used to identify the unknown agent of parasitism past. Here we present the first study of this type by evaluating lingering “frontline” nest defenses that have evolved to prevent egg laying in a former brood parasite host. The Australian reed warbler Acrocephalus australis is currently not parasitized but is known to exhibit fine-tuned egg discrimination—a defensive behavior indicative of a past brood parasite–host arms race and common in closely related parasitized species. Here, using 3D-printed models of adult brood parasites, we examined whether the Australian reed warbler also exhibits frontline defenses to adult brood parasites, and whether we could use these defenses to identify the warbler’s “ghost of parasitism past.” Our findings provide evidence that the Australian reed warbler readily engages in frontline defenses that are considered adaptive specifically in the context of brood parasitism. However, individuals were unable to discriminate between adults of different brood parasite species at their nest. Overall, our results demonstrate that despite a relaxation in selection, defenses against brood parasitism can be maintained across multiple stages of the host’s nesting cycle, and further suggest that, in accordance with previous findings, that learning may be important for fine-tuning frontline defense.     

Feeding on Host Plants with Different Concentrations and Structures of Pyrrolizidine Alkaloids Impacts the Chemical-Defense Effectiveness of a Specialist Herbivore

Sequestration of chemical defenses from host plants is a strategy widely used by herbivorous insects to avoid predation. Larvae of the arctiine moth Utetheisa ornatrix feeding on unripe seeds and leaves of many species of Crotalaria (Leguminosae) sequester N-oxides of pyrrolizidine alkaloids (PAs) from these host plants, and transfer them to adults through the pupal stage. PAs confer protection against predation on all life stages of U. ornatrix. As U. ornatrix also uses other Crotalaria species as host plants, we evaluated whether the PA chemical defense against predation is independent of host plant use. We fed larvae from hatching to pupation with either leaves or seeds of one of eight Crotalaria species (C. incana, C. juncea, C. micans, C. ochroleuca, C. pallida, C. paulina, C. spectabilis, and C. vitellina), and tested if adults were preyed upon or released by the orb-weaving spider Nephila clavipes. We found that the protection against the spider was more effective in adults whose larvae fed on seeds, which had a higher PA concentration than leaves. The exceptions were adults from larvae fed on C. paulina, C. spectabilis and C. vitellina leaves, which showed high PA concentrations. With respect to the PA profile, we describe for the first time insect-PAs in U. ornatrix. These PAs, biosynthesized from the necine base retronecine of plant origin, or monocrotaline- and senecionine-type PAs sequestered from host plants, were equally active in moth chemical defense, in a dose-dependent manner. These results are also partially explained by host plant phylogeny, since PAs of the host plants do have a phylogenetic signal (clades with high and low PA concentrations in leaves) which is reflected in the adult defense.     

The cephalic labial gland secretions of two socially parasitic bumblebees Bombus hyperboreus (Alpinobombus) and Bombus inexspectatus (Thoracobombus) question their inquiline strategy

Social parasitic Hymenopterans have evolved morphological, chemical, and behavioral adaptations to overcome the sophisticated recognition and defense systems of their social host to invade host nests and exploit their worker force. In bumblebees, social parasitism appeared in at least 3 subgenera independently: in the subgenus Psithyrus consisting entirely of parasitic species, in the subgenus Alpinobombus with Bombus hyperboreus, and in the subgenus Thoracobombus with B. inexspectatus. Cuckoo bumblebee males utilize species‐specific cephalic labial gland secretions for mating purposes that can impact their inquiline strategy. We performed cephalic labial gland secretions in B. hyperboreus, B. inexspectatus and their hosts. Males of both parasitic species exhibited high species specific levels of cephalic gland secretions, including different main compounds. Our results showed no chemical mimicry in the cephalic gland secretions between inquilines and their host and we did not identify the repellent compounds already known in other cuckoo bumblebees.     

Why brown-headed cowbirds do not influence red-winged blackbird parent behaviour

Brown-headed cowbirds, Molothrus ater, frequently parasitize red-winged blackbirds,Agelaius phoeniceus . The presence of a brood parasite, unrelated to both host nestlings and parents, has provoked speculation regarding within-brood food allocation and parental provisioning. This study is the first to compare directly the effect of brood parasitism on host parent and offspring behaviour in younger and older broods. We videotaped 28 unparasitized red-winged blackbird broods and compared them to 22 parasitized broods. Red-winged blackbird nestling begging appears largely unaffected by cowbird parasitism. The presence of the cowbird in the nest affected neither the latency nor duration of host nestling begging, but stimulated more frequent begging by red-winged blackbird nestlings following food distribution. Begging by cowbirds was unique in two ways: (1) cowbirds maintained a consistent begging effort throughout the nestling period (but did not receive a consistent food share); and (2) cowbirds begged longer and more frequently following the allocation of food. Persistent begging by the cowbird following the allocation of food has implications for the division of parental care, if by doing so the brood parasite is able to provoke the foster parent to increase provisioning, at the expense of brooding. We found no evidence for the adjustment of parental care. Neither the foraging rates nor the lengths of the parental feeding visits differed markedly between parasitized and unparasitized broods. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

A laboratory study of host use by the cuckoo catfish <Emphasis Type="Italic">Synodontis multipunctatus</Emphasis>

The only known non-avian vertebrate obligate brood parasite is the cuckoo catfish (Synodontis multipunctatus), a Lake Tanganyikan endemic. The cuckoo catfish parasitizes Tanganyikan mouthbrooding cichlids, and under captive conditions, will also parasitize cichlids from other Rift Valley lakes. Here we examine the frequency of parasitism by the cuckoo catfish of Ctenochromis horei from Lake Tanganyika and three species from Lake Malawi and the greater Lake Victorian system in a laboratory setting. C. horei was parasitized significantly less (17%) than the allopatric species Haplochromis latifasciatus, Haplochromis nubilus, and Metriaclima estherae (combined parasitism rate of 28%). The lower rates of parasitism in C. horei may be due to differences in the mating ritual, oviposition (e.g., long periods of pseudo-spawning before actual oviposition), and behavioral adaptations (e.g., increased aggression towards the cuckoo catfish). The number of catfish eggs per parasitized brood was similar between C. horei, H. latifasciatus, H. nubilus, and M. estherae. Our results are comparable to findings from the field for C. horei parasitism frequency and number of cuckoo catfish per brood. We also analyzed the parasitism rate of the albino morph of Metriaclima zebra, a domestic strain. Parasitism rates and number of catfish per brood were the highest in the albino morphotype suggesting that the higher levels of parasitism may be related to lower aggressive behavior, lower visual acuity, or captive influence. Cuckoo catfish and mouthbrooding cichlids provide a model system for testing brood parasitism in a laboratory setting.     

The role of kin recognition in the evolution of conspecific brood parasitism

Conspecific brood parasitism (CBP) is a common strategy in several species of birds. Currently, some studies suggest that relatedness between host and parasite enhances CBP, since indirect fitness benefits could select for acceptance of related eggs by hosts. Conversely, parasites should avoid laying eggs in nests of relatives if this is costly for the host. Based on the latter argument, kinship should not promote brood parasitism. A recent model clarified this relationship, and showed that kinship can promote brood parasitism, assuming kin recognition. However, in that model kin recognition was assumed perfect. Here we present a model that addresses the role of relatedness and kin selection in CBP, when kin recognition is not perfect and hosts do not always detect parasitism. We consider both the indirect fitness of the parasite and the possible responses of the host. Our results indicate that the existence and accuracy of a kin recognition system is crucial to the final outcome. When CBP represents a cost to the host, a parasitic female that has the choice should avoid parasitizing relatives, unless (1) the costs are not too high and (2) hosts can accurately enough recognize eggs laid by relatives, rejecting them less often than eggs laid by nonkin. But if ‘parasitism’ enhances the direct fitness of the host (which is possible in species with precocial young) parasites should choose relatives whenever possible, even if hosts do not recognize kin eggs. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

The effect of multi‐species host density on superparasitism and sex ratio in a gregarious parasitoid

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