Endoparasitic flies,pollen-collection by bumblebees and a potential host-parasite conflict

Summary Conopid flies (Conopidae, Diptera) are common larval parasites of bumblebees. The larva develops inside the abdomen of workers, queens and males. Development is completed within 10–12 days after oviposition when the host is killed and the parasite pupates in situ. Development results in parasitised bees becoming unable to carry large loads of nectar, as the conopid larvae reside where the honey crop is normally located. Furthermore, an addition to the bee's unloaden body mass is likely (average larval weight reached at pupation by the common parasite species Sicus ferrugineus: ±SD 36.3±12.3 mg, n=59; by Physocephala rufipes: 55.8±16.9 mg, n=108). We here asked whether the propensity of workers of the bumblebee Bombus pascuorum to collect nectar rather than pollen is related to the presence of conopid larvae. For samples of bees (n=2254 workers) collected over 3 years of field studies in northwestern Switzerland, there was no difference in the frequency of bees caught as pollen collectors among parasitised (38.1% of cases, n=210) as compared to non-parastised bees (43.9%, n=360) ( ²=1.83, n.s.). However, compared to the non-parasitised bees (n=360), those hosts containing a third (last) instar larva (n=9) were less likely to collect pollen than expected by chance ²=6.91, P=0.003. Similarly, hosts with short survival time between capture and being killed by the developing larva (which hence must have harboured a late instar parasite at time of capture) were less likely to collect pollen (8%, n=25) than those found not parasitised (37.6%, n=891 ²=9.16, P<0.001). Late instar larvae grow so big that they fill the entire abdomen. Although there was also a tendency for presumably older bees to collect less pollen, this is unlikely to explain the observations. We also discuss whether these changes in foraging behaviour of bumblebees may reflect a host-parasite conflict over the type of resource to be collected.     

EFFECT OF ECTOPARASITIC MITES ON SEXUAL SELECTION IN A SONORAN DESERT FRUIT FLY

We conducted a field study and a laboratory experiment to test whether ectoparasitic mites, Macrocheles subbadius, generate parasite-mediated sexual selection in the Sonoran desert endemic fruit fly, Drosophila nigrospiracula. Male flies gather on the outer surfaces of necrotic saguaro cacti where they engage in male–male competitive interactions and vigorous female-directed courtship. At these sites, operational sex ratios were significantly skewed toward males. The degree to which mites were aggregated among flies varied across the 25 fly populations sampled. The degree of mite aggregation across fly populations was strongly positively related to the mean number of mites per fly (intensity of infestation). Both the intensity and prevalence of infestation (fraction of flies infested) increased with the age of the cactus necrosis. Infested flies of both sexes were significantly less likely to be found in copula than uninfested flies, and mean intensity of infestation was significantly more pronounced in noncopulating than in copulating flies. The effect of attached mites on copulatory success exhibited dose-dependency, and this effect was more stringent in males: males or females with more than two and four mites, respectively, were never found in copula. The magnitude of parasite-mediated sexual selection was estimated for 12 fly populations by calculating selection differentials for each sex separately. The relation between intensity of infestation and magnitude of parasite-mediated sexual selection was stronger in males but significant for both sexes. We also assayed copulatory success of field-caught males in the laboratory, both during infestation and after experimental removal of mites. Males infested with two mites copulated less frequently than uninfested individuals, and in mating trials after mites had been removed, previously infested males copulated as many times as flies with no history of infestation. These findings, and the lack of difference in the number of mite-induced scars on copulating and single individuals in nature, strongly suggest that the reduced copulatory success of infested flies is attributable to an effect of mites per se, rather than to a character correlated with parasitism or previous parasite infestation.     

Roost selection and roost switching of female Bechstein’s bats (<Emphasis Type="Italic">Myotis bechsteinii</Emphasis>) as a strategy of parasite avoidance

Ectoparasites of vertebrates often spend part of their life cycle in their hosts’ home. Consequently, hosts should take into account the parasite infestation of a site when selecting where to live. In a field study, we investigated whether colonial female Bechstein’s bats (Myotis bechsteinii) adapt their roosting behaviour to the life cycle of the bat fly Basilia nana in order to decrease their contact with infective stages of this parasite. B. nana imagoes live permanently on the bat’s body but deposit puparia in the bat’s roosts. The flies metamorphose independently in the roosts, but after metamorphosis emerge only in the presence of a potential host. In a field experiment, the bats preferred non-contagious to contagious day-roosts and hence were able to detect either the parasite load of roosts or some correlate with infestation, such as bat droppings. In addition, 9 years of observational data on the natural roosting behaviour of female Bechstein’s bats indicate that the bats largely avoid re-occupying roosts when highly contagious puparia are likely to be present as a result of previous occupations of the roosts by the bat colony. Our results indicate that the females adapted their roosting behaviour to the age-dependent contagiousness (emergence probability) of the puparia. However, some infested roosts were re-occupied, which we assume was because these roosts provided advantages to the bats (e.g. a beneficial microclimate) that outweighed the negative effects associated with bat fly infestation. We suggest that roost selection in Bechstein’s bats is the outcome of a trade-off between the costs of parasite infestation and beneficial roost qualities.     

Estimation of the effects of buffalo fly (Haematobia irritans exigua) on the milk production of dairy cattle based on a meta-analysis of literature data

Published reports on the effect of buffalo fly Haematobia irritans exigua De Meijere (Diptera: Muscidae) and the closely related horn fly (H. irritans) were examined and analysed using non-linear weighted regression techniques in an attempt to establish the relationship between daily production loss (D), average number of parasites (n) and the average damage per parasite per day (d), and to provide estimates of expected losses in milk yield (MYD) and live-weight gain (LWG) in dairy cattle. A Mitscherlich three-parameter model was used to explain the relationship between the total loss of production attributable to buffalo flies and the average number of flies associated with cattle. This model was significant (P<0.01), with R2 = 20.2% and predicted a threshold number of flies (n = 30) below which no adverse effects would be noted. At a moderate level of infestation (n = 200) dMYD was 2.6 ml/fly/day and dLWG was 0.14 g/fly/day, resulting in estimated daily losses in milk yield (D(MYD)) and live-weight gain (D(LWG)) of 520 ml and 28 g, respectively.     

FURTHER OBSERVATIONS ON THE BIOLOGY OF THE CABBAGE ROOT FLY, ERIOISCHIA BRASSJCAE BCHÉ

In 1951, eggs of Erioischia brassicae were first found in the field on 2 May, and the peak period of egg-laying occurred 19–31 May. This was up to a month later than in the period 1948-50.
The periodic removal and examination of the surface soil showed that eggs of E. brassicae were continuously present on the host plants from mid-June to early November. Plants under observation during this period showed an average of 285 eggs per plant and other plants exposed to attack from July to November showed an average of 162 eggs per plant. Peak periods of egg-laying, as indicated by numbers of eggs per plant per day, occurred in late June and early July, in mid-August and, to a less extent, in the first half of October. The plants showed no increase in the rate of infestation as the season advanced, although E. brassicae has a reproductive capacity of about 100 eggs per female and three to four generations a year.
The difference between the observed egg populations and pupal populations indicated that E. brassicae had a heavy mortality rate in its immature stages. The condition of puparia showed that the species was subject to a high degree of natural control, a fact for consideration when direct control measures are formulated.
Pupal diapause extending from October 1949 to May 1951 was observed in one specimen of E. brassicae and from October 1949 to August 1951 in one specimen of its Hymenopterous parasite, Trybliographa rapae Westw.
Tests with tar-oil winter wash showed that at a concentration of 1 1/4% it killed eggs of Erioischia brassicae and repelled gravid females for approximately a week. Laboratory tests with BHC indicated that it had no adverse effects on the eggs but was larvicidal.     

Besprechungen

Book reviewed in this article: Lorenz, K. (1967): Die instinktiven Grundlagen menschlicher Kultur Lawick-Goodall, Jane van (1967): My friends the wild chimpanzees Smith, W. J. (1966): Communication and relationships in the genusTyrannus     

Field infestation of rambutan fruits by internal-feeding pests in Hawaii

More than 47,000 mature fruits of nine different varieties of rambutan (Nephelium lappaceum L.) were harvested from orchards in Hawaii to assess natural levels of infestation by tephritid fruit flies and other internal feeding pests. Additionally, harvested, mature fruits of seven different rambutan varieties were artificially infested with eggs or first-instars of Mediterranean fruit fly, Ceratitis capitata (Wiedemann), or oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) to assess host suitability. When all varieties were combined over two field seasons of sampling, fruit infestation rates were 0.021% for oriental fruit fly, 0.097% for Cryptophlebia spp. (Lepidoptera: Tortricidae), and 0.85% for pyralids (Lepidoptera). Species of Cryptophlebia included both C. illepida (Butler), the native Hawaiian species, and C. ombrodelta (Lower), an introduced species from Australia. Cryptophlebia spp. had not previously been known to attack rambutan. The pyralid infestation was mainly attributable to Cryptoblabes gnidiella (Milliere), a species also not previously recorded on rambutan in Hawaii. Overall infestation rate for other moths in the families Blastobasidae, Gracillariidae, Tineidae, and Tortricidae was 0.061%. In artificially infested fruits, both species of fruit fly showed moderately high survivorship for all varieties tested. Because rambutan has such low rates of infestation by oriental fruit fly and Cryptophlebia spp., the two primary internal-feeding regulatory pests of rambutan in Hawaii, it may be amenable to the alternative treatment efficacy approach to postharvest quarantine treatment.     

Infestation of cassava genotypes by Neosilba perezi (Romero & Ruppell) (Diptera: Lonchaeidae)

The objectives of this work were to assess the infestation of ten genotypes of cassava by the shoot fly Neosilba perezi (Romero & Ruppell) and to investigate effects of plant age, temperature or precipitation on cassava plants infestation by the shoot fly. Thirty-two individuals of each cassava genotype were planted and analyzed every two weeks in order to calculate the percentage of plants infested by shoot fly larvae at each sampling event and per genotype. Infestation by the fly was different across the genotypes. Genotype IAC Caapora 105-66 and genotype IAC Cascuda were resistant to shoot fly infestation, whereas the genotype IAC 15 was the most susceptible to this insect. Plant age may have an influence on infestation by shoot flies. Advanced plant age apparently favors lower or even inexistent infestation rates. However, infestation rate does not seem to be affected by temperature or precipitation.     

The predators of wheat-bulb fly

Wheat bulb fly, a pest of winter weat, has one generation a year and all stages exist for at least a month. The feeding larva inside the shoot is protected, except when moving to a new shoot, but all the other stages are exposed to attack by non-specific predators, either by soil-living beetles feeding on eggs and puparia in the soil, or predatory flies and birds feeding on the adults.     

Community of bat flies (Streblidae and Nycteribiidae) on bats in the Cerrado of Central-West Brazil: hosts,aggregation, prevalence,infestation intensity,and infracommunities

Streblidae and Nycteribiidae are families of bloodsucking flies that parasitize bats exclusively. We studied the community of these flies in a Cerrado area in the Central-West Brazil. We captured 708 bats over 17 nights from October 2012 to March 2013. Forty-five per cent of the hosts were parasitized by 836 specimens of bat flies of 22 species. The most abundant flies were Trichobius joblingi on Carollia perspicillata, followed by Megistopoda aranea on Artibeus planirostris, and Strebla guajiro on C. perspicillata. All bat flies showed a high level of specificity for their hosts. Trichobius joblingi was the bat fly with the highest prevalence (80%) and mean intensity of infestation (3.5) on hosts with a representative sample size (n > 20). This result is likely related to the type of roosting (cavity) used by C. perspicillata, primary host of this fly species. Anoura caudifer hosted the largest infracommunities (n = 7). However, most bats were parasitized by a single fly species, suggesting a pattern in infestations. The aggregation index was high, indicating an unequal occurrence in parasite infestations. The majority of hosts were infested by few or no flies and few hosts were highly infested, showing a negative binomial distribution.     

Energetic cost of bot fly parasitism in free-ranging eastern chipmunks

The energy and nutrient demands of parasites on their hosts are frequently invoked as an explanation for negative impacts of parasitism on host survival and reproductive success. Although cuterebrid bot flies are among the physically largest and most-studied insect parasites of mammals, the only study conducted on metabolic consequences of bot fly parasitism revealed a surprisingly small effect of bot flies on host metabolism. Here we test the prediction that bot fly parasitism increases the resting metabolic rate (RMR) of free-ranging eastern chipmunks (Tamias striatus), particularly in juveniles who have not previously encountered parasites and have to allocate energy to growth. We found no effect of bot fly parasitism on adults. In juveniles, however, we found that RMR strongly increased with the number of bot fly larvae hosted. For a subset of 12 juveniles during a year where parasite prevalence was particularly high, we also compared the RMR before versus during the peak of bot fly prevalence, allowing each individual to act as its own control. Each bot fly larva resulted in a ~7.6% increase in the RMR of its host while reducing juvenile growth rates. Finally, bot fly parasitism at the juvenile stage was positively correlated with adult stage RMR, suggesting persistent effects of bot flies on RMR. This study is the first to show an important effect of bot fly parasitism on the metabolism and growth of a wild mammal. Our work highlights the importance of studying cost of parasitism over multiple years in natural settings, as negative effects on hosts are more likely to emerge in periods of high energetic demand (e.g. growing juveniles) and/or in harsh environmental conditions (e.g. low food availability).     

Developmental strategy of the endoparasite Xenos vesparum (strepsiptera, Insecta): host invasion and elusion of its defense reactions

To successfully complete its endoparasitic development, the strepsipteran Xenos vesparum needs to elude the defense mechanisms of its host, the wasp Polistes dominulus. SEM and TEM observations after artificial infections allow us to outline the steps of this intimate host-parasite association. Triungulins, the mobile 1st instar larvae of this parasite, are able to "softly" overcome structural barriers of the larval wasp (cuticle and epidermis) without any traumatic reaction at the entry site, to reach the hemocoel where they settle. The parasite molts 48 h later to a 2nd instar larva, which moves away from the 1st instar exuvium, molts twice more without ecdysis (a feature unique to Strepsiptera) and pupates, if male, or develops into a neotenic female. Host encapsulation involves the abandoned 1st larval exuvium, but not the living parasite. In contrast to the usual process of encapsulation, it occurs only 48 h after host invasion or later, and without any melanization. In further experiments, first, we verified Xenos vesparum's ability to reinfect an already parasitized wasp larva. Second, 2nd instar larvae implanted in a new host did not evoke any response by hemocytes. Third, we tested the efficiency of host defense mechanisms by implanting nylon filaments in control larval wasps, excluding any effect due the dynamic behavior of a living parasite; within a few minutes, we observed the beginning of a typical melanotic encapsulation plus an initial melanization in the wound site. We conclude that the immune response of the wasp is manipulated by the parasite, which is able to delay and redirect encapsulation towards a pseudo-target, the exuvia of triungulins, and to elude hemocyte attack through an active suppression of the immune defense and/or a passive avoidance of encapsulation by peculiar surface chemical properties.     

Visual recognition of the host in the parasitoid fly Exorista japonica

We presented the tachinid fly Exorista japonica with moving host models: a freeze-dried larva of the common armyworm Mythimna separata, a black rubber tube, and a black rubber sheet, to examine the effects of size, curvature, and velocity on visual recognition of the host. The host models were moved around the fly on a metal arm driven by motor. The size of the larva, the velocity of movement, and the length and diameter of the rubber tube were varied. During the presentation of the host model, fixation, approach, and examination behaviours of the flies were recorded. The fly fixated on, approached, and examined the black rubber tube as well as the freeze-dried larva. Furthermore, the fly detected the black rubber tube at a greater distance than the larva. The rubber tube elicited higher rates of approach and examination responses than the rubber sheet, suggesting that curvature affects the responses of the flies. The length, diameter, and velocity of host models had little effect on response rates of the flies. During host pursuit, the fly appeared to walk towards the ends of the tube. These results suggest that the flies respond to the leading or trailing edges of a moving object and ignore the length and diameter of the object.     

Eradication of the melon fly,Dacus cucurbitae,from Kume is., Okinawa with the sterile insect release method

The sterile insect release method was applied to eradicate the melon fly, Dacus cucurbitae, from the 58.5 km² island of Kume, in the Okinawa Islands group. Weekly releases of 1 to 1.5 million flies irradiated as pupae with 6–7 kR from a cobalt-60 source did not decrease the wild melon fly population. Releases of 1.5–2 million pupae per week made from September, 1975 to January, 1976 decreased the percent egg-hatch of females caught on Kume Is., but did not decrease the percent infestation significantly. The number of pupae released was increased from February, 1976 to accelerate the eradication process. When the number of pupae released exceeded 3.5 million per week, a rapid increase in the ratio of marked (sterile) to unmarked (wild) flies, a remarkable decrease in percent egg-hatch, and a decrease in percent infestation of fruits were observed. There has been no sign of melon fly infestation in wild cucurbit fruits from October, 1976 to the present time (April, 1977), despite the fact that more than 70,000 fruits were carefully examined. The eradication of the melon fly from Kume Is. was thus achieved by April, 1977, after the release of 264 million sterile fly pupae.     

What determines the number of ovarioles in a fly ovary?

The relation between the size of a fly and the number of ovarioles in its ovary was investigated in Phormia regina and Sarcophaga bullata. Small flies of varying size were produced by taking larvae prematurely off the food. The smallest flies thus obtained were derived from larvae only $\text{1}\text{8}$ of the weight of a normal larva. The number of ovarioles in an ovary is directly proportional to the size of the fly and, in the extreme case, is about $\text{1}\text{5}$ the normal number in Sarcophaga and about $\text{1}\text{3}$ in Phormia. Larvae prematurely taken off the food, but fed again after starving for several days, grow to normal or almost normal size and develop ovaries with about the normal number of ovarioles. Small or re-fed Sarcophaga do not show any changes in the anatomy of individual ovarioles but in Phormia disorders in ovariole development and a consequent reduction of fertility are frequent. The number of ovarioles remains identical from the early pupal stage all through the development of the pharate fly and then through ovarian development in the adult fly: it is determined by the size of the larva when it was taken off the food. This shows that it is not lack of space in a small adult fly abdomen which determines the number nor the occurrence of degenerative processes during ovarian development.     

Accessibility of blood affects the attractiveness of cattle to horn flies

The burden of infestation of the horn fly, Haematobia irritans (Linnaeus) (Diptera: Muscidae), differs among bovines within the same herd. We hypothesized that these differences might be related to the epidermal thickness of the cattle and the blood intake capacity of the fly. Results showed that dark animals carried more flies and had a thinner epidermis than light‐coloured animals, which was consistent with the greater haemoglobin content found in flies caught on darker cattle. Similarly, epidermal thickness increased with body weight, whereas haemoglobin content decreased. Overall, we suggest that accessibility of blood is a factor that partially explains cattle attractiveness to flies.     

Assembly rules for functional groups of North American shrews: effects of geographic range and habitat partitioning

Trophic cascades exist in numerous terrestrial systems, including many systems with ants as the top predator. Many studies show how behavioral modifications of herbivores are especially important in mediating species interactions and trophic cascades. Although most studies of trophic cascades focus on predator-herbivore-plant links, the trophic cascades concept could be applied to almost any level of trophic interactions. Especially considering the importance of parasites we consider here the interactions between the parasitic phorid fly, Pseudacteon sp. (Diptera: Phoridae), its ant host, Azteca instabilis (F. Smith) (Hymenoptera: Formicidae), and the herbivore, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) in the coffee agroecosystem. We investigated the effects of phorid flies on ant behavior by monitoring ant recruitment to tuna baits over a 30-min period in the presence or absence of phorid flies. To study the indirect effects of phorids on larvae, we placed baits on coffee plants to elevate ant foraging levels to levels near to ant nests, placed larvae near baits, and recorded the effects of ants on larvae either in the presence or absence of phorid flies. We found that phorid fly presence significantly reduced ant ability to recruit to baits through behavioral modifications and also significantly lessened ant ability to attack, carry away, or force herbivores off plants. We conclude there is a behaviorally-modified species-level trophic cascade in the coffee agroecosystem, with potentially important effects in ant and herbivore communities as well as for coffee production.     

Effects of decomposition on carcass attendance in a guild of carrion-breeding flies

Many forensically important calliphorids, sarcophagids and muscids (Diptera) oviposit or larviposit on corpses only during the early stages of decomposition, yet individuals may attend bodies throughout decay. A field study was conducted to investigate how patterns of carcass use and attendance by some fly species are affected by decomposition. Five fly traps were placed in the forest and baited with whole, fresh piglet carcasses. Piglets decomposed in traps throughout the experiment, and all were skeletonized within 6 days. Flies were trapped at both early and late decomposition stages, and the species and population structures of trap catches were compared. More flies attended carcasses early rather than late in decay. For all species, flies attending early were mainly gravid females, but few gravid females attended late in decay. No females ovi- or larviposited late in decay, whereas females of all fly species deposited offspring early in decay. The number of males trapped of each species correlated positively with the number of females with eggs at early development stages. Observations were made of fly predation by European wasps Vespula germanica Fabricius (Hymenoptera, Vespidae) and jumper ants Myrmecia pilosula Smith (Hymenoptera, Formicidae) throughout the experiment. There was a higher risk for smaller fly species of being killed following predator attack. Ants and wasps attacked smaller fly species, whereas only wasps attacked larger fly species.     

Parasite preferences for large host body size can drive overdispersion in a fly-mite association

Body size generally correlates intraspecifically with insect fitness but can also correlate with parasite abundance (number of parasites). Host preferences by parasites, and variation in host immunity, could contribute to this trend. We investigated the effect of host size on mite-fly interactions (Macrocheles subbadius and Drosophila nigrospiracula). Mites strongly preferred to infect larger flies in pair-wise choices, and larger flies were more likely to be infected and acquired more mites in infection microcosms. Preferences of parasites resulted in size-biased infection outcomes. We discuss the implications of this heterogeneity in infection on parasite overdispersion and fly populations.