Coexistence of multiple parasitoids on a single host due to differences in parasitoid phenology

There are many well-documented cases in which multiple parasitoids can coexist on a single host species. We examine a theoretical framework to assess whether parasitoid coexistence can be explained through differences in timing of parasitoid oviposition and parasitoid emergence. This study explicitly includes the phenology of host and parasitoid development and explores how this mechanism affects the population dynamics. Coexistence of the host with two parasitoids requires a balance between parasitoid fecundity and survival and occurs most readily if one parasitoid attacks earlier but emerges later than the other parasitoid. The host density can either be decreased or increased when a second coexisting parasitoid is introduced into the system. However, there always exists a single parasitoid type that is most effective at depressing the host density, although this type may not be successful due to parasitoid competition. The coexistence of multiple parasitoids also affects the population dynamics. For instance, population oscillations can be removed by the introduction of a second parasitoid. In general, subtle differences in parasitoid phenology can give rise to different outcomes in a host–multi-parasitoid system, and this may offer some insight into why establishing criteria for the ‘ideal’ biological control agent has been so challenging.     

Ecological interactions of Pseudacteon parasitoids and Solenopsis ant hosts: environmental correlates of activity and effects on competitive hierarchies

1. Solenopsis (Hymenoptera: Formicidae) fire ants are host to Pseudacteon (Diptera: Phoridae) parasitoids. The activity of S. geminata (F.) hosts and relative abundance of Pseudacteon phorids, along with five environmental variables, were measured at weekly intervals over an 8‐month period at two sites. 2. Pseudacteon relative abundances often varied greatly from week to week, and were only weakly positively correlated with S. geminata activity. 3. A quadratic function of soil temperature was the single best predictor of ant activity at both sites, explaining 32 and 73% of the variation in ant activity. A linear function of soil moisture was the single best predictor of phorid relative abundance at one site (r² = 0.23) whereas no measured variables were significant predictors of phorid relative abundance at the other site. 4. Interspecific interactions at 600 baits were monitored at a third site to document dominance hierarchies and determine whether the presence of Pseudacteon phorids mediated interspecific interactions in their host, S. geminata. 5. Solenopsis geminata was near the top of dominance hierarchies, which did not diverge greatly from a linear pattern. Three species (S. geminata, S. invicta Buren, and Crematogaster laeviuscula Mayr) won the majority of their interspecific interactions and appear to be co‐dominants at this microhabitat‐rich site. 6. Overall, the presence of phorids had no significant effect on the outcome of interspecific contests involving S. geminata and all other ant species grouped together. Phorids may have contributed to some of the S. geminata losses against other co‐dominant species.     

Interactions between the egg and larval parasitoids of a gall-forming midge and their impact on the host

1. The gall‐forming midge Rhopalomyia californica was exposed experimentally to parasitism and predation during only the egg stage, during only the larval stage, during neither stage, or during both stages. 2. The combined action of natural enemies that attack during both the egg stage and the larval stage led to the lowest number of midges and total insects (midges + parasitoids) in the next generation, and the highest percentage parasitism. 3. The larval parasitoid killed a large fraction of hosts without producing new parasitoid offspring, while there is some indication that the egg parasitoid on its own tended to produce the most parasitoid offspring. The contrasting implications of host mortality versus parasitoid production for biological control are discussed. 4. Exposure to larval parasitoids resulted in a reduction in the number of egg parasitoid offspring produced, but exposure to the egg parasitoid did not affect the number of larval parasitoid offspring produced significantly.     

Evaluation of Fopius arisanus as a biological control agent for the olive fruit fly in California

1 The egg‐prepupal parasitoid Fopius arisanus (Hymenoptera: Braconidae) was evaluated in quarantine facilities as a potential biological control agent for the olive fruit fly Bactrocera oleae (Diptera: Tephritidae) in California, U.S.A. 2 Nontarget testing of two weed biological control agents confirmed that F. arisanus will not attack Tephritidae that feed in inflorescences or galls. It may, however, pose risks to native Tephritidae that feed in fruit. 3 Females preferentially oviposited in eggs, although first‐instar B. oleae were also attacked. Low lifetime reproductive potential and high rates of direct mortality inflicted on host eggs indicate that rearing on B. oleae may prove difficult. 4 In multiparasitized B. oleae, F. arisanus prevailed in competition against two species of larval–pupal parasitoids, Diachasmimorpha kraussii and Psyttalia concolor (both Hymenoptera: Braconidae). 5 The broad host‐range of F. arisanus with respect to fruit‐feeding Tephritidae may preclude its introduction to California, as may its low fecundity and its intrinsic competitive superiority over larva l–pupal parasitoids, which include specialists on B. oleae that are currently being introduced to California. High rates of direct mortality, however, point to potential uses in augmentative biological control. Whether or not F. arisanus is released in California, its biology as a parasitoid of B. oleae has been little studied to date and the results herein may be applied in other regions worldwide where B. oleae is a problem.     

Functional shifts in the use of parasitized hosts by a tephritid fly: the role of host quality

Superparasitism, a phenomenon in which parasitic insects layeggs in already-exploited hosts, provides a useful context inwhich to examine the dynamics of parental investment. This studyexplored conditions under which female Mediterranean fruit flies(Ceratitis capitata) shift from avoiding superparasitism ofhost fruit to preferring it, even placing eggs direcdy intoexisting egg-laying cavities. An a priori hypothesis of costsand benefits was used to predict how use and avoidance of parasitizedfruit would change in -response to changes in fruit size andripeness. We predicted that avoidance would decrease with increasingfruit size, while use would increase with decreasing ripeness.Using a field-cage assay, ripeness was held constant and thesize of host coffee berries manipulated. Avoidance of parasitizedberries was significandy less pronounced on large berries thanon small ones. In a second experiment, size was held constantand ripeness manipulated. On unripe berries, females depositedthe majority of clutches directly into existing egg-laying cavities.On ripe berries, by contrast, the same females deposited mostclutches in previously unparasitized fruit. Parallel patternsin the frequency of female-female contests were observed, supportingthe notion that a fruit's value is determined by an interactionbetween fruit size or ripeness, on one hand, and the prior occurrenceof eggs, on the other. Laboratory assays suggested that useof existing sites had advantages in terms of time savings; femalebehavior thus constitutes a relatively uncommon example of adaptivesuperparasitism in which parasitized hosts are actually preferredover unparasitized ones.[Behav Ecol 7: 235-242 (1996)]     

Local mate competition with lethal male combat: effects of competitive asymmetry and information availability on a sex ratio game

We constructed a sex allocation model for local mate competition considering the asymmetry of competitive abilities among sons. This model assumes two females of a parasitoid wasp oviposit on the same host in sequential order. The evolutionarily stable strategy will be in either Stackelberg or Nash equilibrium, depending on whether the females can recognize their opponent's sex ratio or not, respectively. The Nash equilibrium predicts the second female produce more males than the first. If the second female is able to know and respond to the strategy of the first (a Stackelberg equilibrium), the first will decide an optimal sex ratio assuming that the second reply to it. Under such an assumption, our model predicts that not producing sons is adaptive for the second female when the sons she produces have low competitive ability. Males of parasitoid wasps Melittobia spp. are engaged in lethal male-male combat, indicating large asymmetry in mating success among sons. If females have the ability to recognize their opponent's sex ratio, our model suggests that the severe lethal male-male combat may be one factor explaining their extremely female-biased sex ratio that is unexplainable by pre-existent models.     

Life history of the tick parasitoid Ixodiphagus hookeri (Hymenoptera: Encyrtidae) in Kenya

We conducted laboratory and field experiments to elucidate the life history of Ixodiphagus hookeri, a parasitoid of the ixodid tick Amblyomma variegatum in Western Kenya. Ixodiphagus hookeri females oviposited in unfed host nymphs as well as engorged nymphs, but rarely in engorged larvae. While I. hookeri developed to adults in engorged nymphs, the eggs laid in unfed nymphs disappeared within 2 days after oviposition. As temperature increased, development time of I. hookeri from oviposition to adult emergence in engorged nymphs decreased from 46 days at 23 °C to 35 days at 28 °C, and their immature survival in engorged nymphs decreased from 67% at 23 °C to 22% at 28 °C. No parasitoid adult emerged from hosts at 30 °C. Individual hosts parasitized by single females produced 42–53 adult wasps, 73% of which were females. As a typical pro-ovigenic species, I. hookeri females had an average of 84 mature eggs at emergence and lived only for a few days. When laboratory-reared, unfed nymphs of A. variegatum were attached to cattle for 4–9 days in subsistence farmers’ fields in Western Kenya, 25% of the engorged nymphs and 4% of the unfed nymphs on cattle were parasitized by I. hookeri, demonstrating that I. hookeri females search for and oviposit in A. variegatum nymphs on cattle. Unlike other strains of I. hookeri that overwinter as eggs in unfed nymphs, I. hookeri could continuously reproduce throughout the year in Western Kenya.     

Effect of larval host food substrate on egg load dynamics, egg size and adult female size in four species of braconid fruit fly (Diptera: Tephritidae) parasitoids

Life history theory predicts that individuals will allocate resources to different traits so as to maximize overall fitness. Because conditions experienced during early development can have strong downstream effects on adult phenotype and fitness, we investigated how four species of synovigenic, larval-pupal parasitoids that vary sharply in their degree of specialization (niche breadth) and life history (Diachasmimorpha longicaudata, Doryctobracon crawfordi, Opius hirtus and Utetes anastrephae), allocate resources acquired during the larval stage towards adult reproduction. Parasitoid larvae developed in a single host species reared on four different substrates that differed in quality. We measured parasitoid egg load at the moment of emergence and at 24 h, egg numbers over time, egg size, and also adult size. We predicted that across species the most specialized would have a lower capacity to respond to changes in host substrate quality than wasps with a broad host range, and that within species, females that emerged from hosts that developed in better quality substrates would have the most resources to invest in reproduction. Consistent with our predictions, the more specialized parasitoids were less plastic in some responses to host diet than the more generalist. However, patterns of egg load and size were variable across species. In general, there was a remarkable degree of reproductive effort-allocation constancy within parasitoid species. This may reflect more “time-limited” rather than “egg-limited” foraging strategies where the most expensive component of reproductive success is to locate and handle patchily-distributed and fruit-sequestered hosts. If so, egg costs, independent of degree of specialization, are relatively trivial and sufficient resources are available in fly larvae stemming from all of the substrates tested.     

Evaluating biological control of fire ants using phorid flies: effects on competitive interactions

The effects of the parasitic phorid fly, Pseudacteon tricuspis Borgmeier, on the competitive interactions between the red imported fire ant, Solenopsis invicta Buren, and a native North American ant, Forelius pruinosus (Roger), were investigated in the laboratory. P. tricuspis is a highly host-specific endoparasitoid of S. invicta workers that is currently being reared and released as a biological control agent of S. invicta in the US. We tested the effect of P. tricuspis on the colony growth rate of S. invicta when S. invicta was forced to compete with F. pruinosus for a protein resource (freeze-killed crickets) in laboratory competition arenas. In addition to colony growth rate, we quantified the effect of the phorid flies on the foraging rate of S. invicta. Though S. invicta significantly reduced its foraging rate in the presence of the phorid flies, we did not detect an effect of the flies on colony growth rate. Possible explanations for these results include behavioral compensation by S. invicta for the presence of the flies. We present these laboratory results in light of a literature search indicating that laboratory tests of biological control agent efficacy are good predictors of field efficacy. We conclude that P. tricuspis alone is unlikely to suppress S. invicta populations in the field by reducing their competitive ability.     

Rock-scissors-paper game in a chaotic flow: the effect of dispersion on the cyclic competition of microorganisms

Laboratory experiments and numerical simulations have shown that the outcome of cyclic competition is significantly affected by the spatial distribution of the competitors. Short-range interaction and limited dispersion allows for coexistence of competing species that cannot coexist in a well-mixed environment. In order to elucidate the mechanisms that destroy species diversity we study the intermediate situation of imperfect mixing, typical in aquatic media, in a model of cyclic competition between toxin producing, sensitive and resistant phenotypes. It is found, that chaotic mixing, by changing the character of the spatial distribution, induces coherent oscillations in the populations. The magnitude of the oscillations increases with the strength of mixing, leading to the extinction of some species beyond a critical mixing rate. When mixing is non-uniform in space, coexistence can be sustained at much stronger mixing by the formation of partially isolated regions, that prevent global extinction. The heterogeneity of mixing may enable toxin producing and sensitive strains to coexist for very long time at strong mixing.     

Herbivory below ground and biological weed control: life history of a root-boring weevil on purple loosestrife

The life history of the root-boring weevil Hylobius transversovittatus was studied in north and central Europe. The weevil develops on Lythrum salicaria, a perennial marshland plant that has become a problem weed in North America. It was found in all habitats of its host plant with the exception of permanently flooded sites. It also attacked L. salicaria in an early successional stage, devastating large parts of the storage tissue. The beetle was found in two-thirds of the field populations examined with a mean attack rate of 76.3%. Larvae developed according to a 1- or 2-year generation cycle depending on the time of oviposition. Adult beetles developing within 1 year emerged between July and October, whereas beetles with a 2-year larval period emerged within 3 weeks in July and August. Adults were long-lived and could hibernate several times. Beetles of the new generation mated right on the spot and some oviposited prior to overwintering. Hibernated females had an oviposition period from May to early September and produced 3–4 eggs/day during the peak oviposition period. Specific mortality factors were scarce. Dispersal flights ensure the regular occurrence of H. transversovittatus in scattered L. salicaria populations. The severe impact of the weevil is expected to reduce the competitive ability of its host plant after introduction into North America.     

Testing a new version of the size-advantage hypothesis for sex change: sperm competition and size-skew effects in the bucktooth parrotfish, Sparisoma radians

A variety of field studies suggest that sex change in animalsmay be more complicated than originally depicted by the size-advantagehypothesis. A modification of the size-advantage hypothesis,the expected reproductive success threshold model, proposesthat sperm competition and size-fecundity skew can stronglyaffect reproductive pay-offs. Size-fecundity skew occurs ifa large female's fecundity is markedly higher than the aggregateof the other members of her social group and, together withpaternity dilution from sperm competition, can produce situationsin which large females benefit by deferring sex change to smallerfemales. Deferral by large females can create sex-size distributionscharacterized by the presence of large females and small sex-changedmales, and it is precisely these distributions that the traditionalsize-advantage model cannot explain. We tested the predictionsof the new model with the bucktooth parrotfish, Sparisoma radians,on coral reefs in St. Croix, U.S. Virgin Islands. Collectionsand spawning observations determined that the local environmentalregime of S. radians is characterized by pervasive sperm competition(accompanying 30% of spawns) and factors that can produce substantialsize-fecundity skew in social groups. Dominant male removalexperiments demonstrate that the largest females in social groupsoften do not change sex when provided an opportunity. Instead,smaller, lower-ranking females change sex when a harem vacancyarises. This pattern of sex change is in contrast to virtuallyall previous studies of social control of sex change in fishes,but provides strong support for the general predictions of theexpected reproductive success threshold model.     

The parasitoid guild of larvae of Chrysophtharta agricola Chapuis (Coleoptera: Chrysomelidae) in Tasmania, with notes on biology and a description of a new genus and species of tachinid fly

Abstract  The taxonomic status of the parasitoid guild associated with the larvae of Southern Eucalypt Beetle ( Chrysophtharta agricola Chapuis) in Tasmania is discussed. The primary larval parasitoid complex comprised the tachinid flies Balde striatum gen. n., sp. n. and Paropsivora australis (Macquart) (Diptera: Tachinidae: Goniinae: Blondeliini), and Eadya paropsidis Huddleston & Short (Hymenoptera: Braconidae), while the hymenopteran hyperparasitoids included Perilampus tasmanicus (Cameron) (Perilampidae), Mesochorus sp. (Ichneumonidae) and possibly Meteorus sp. (Braconidae). Keys are provided to the three adult primary parasitoids and two adult hyperparasitoids, and to the pupae of primary parasitoids. Balde striatum gen. n., sp. n. is described, and P. australis is redescribed. Brief notes on biology are included.     

The influence of light and moisture gradients on the attack rate of parasitoids foraging for hosts in a laboratory arena (Hymenoptera: Pteromalidae)

Microhabitat preferences of four parasitoids (Hymenoptera: Pteromalidae) of house fly pupae were measured in a two-dimensional arena containing perpendicular light and moisture gradients. Parasitism by Muscidifurax raptorand Nasonia vitripenniswas greatest in dry substrates, with the latter preferring bright illumination and the former tending to prefer dark. Urolepis rufipesselected bright illumination and moist substrates, attacking the most hosts at bright-moist and dim-moist microhabitats. Spalangia cameroniexhibited no main-effect preference for light intensity or moisture, although parasitism was highest at dim-moist, dark-wet, and dark-moist microhabitats. These results demonstrate that simple abiotic attributes, such as light intensity and substrate moisture concentration, are important in defining some dimensions of the niches of these parasitoids.     

Effect of Air Humidity on the Egg Viability of Predatory Mites (Acari: Phytoseiidae, Stigmaeidae) Common on Rubber Trees in Brazil

Rubber pest mites, Calacarus heveae and Tenuipalpus heveae, reach economic damage levels at the end of the rainy season and the beginning of the dry season in Brazil. Therefore, low humidity adaptation might be an important characteristic for predatory mites to successfully control pest organisms. This study determined the effect of the relative humidity (RH) levels of 30–100% on the hatching of larvae of Amblyseius acalyphus, Euseius citrifolius, Iphiseiodes zuluagai, Metaseiulus camelliae, Agistemus floridanus and Zetzellia malvinae at 25 ± 0.5 °C. These predatory mites are common on rubber trees in the state of São Paulo and might be used for introduction in the major rubber tree production regions in the state of Mato Grosso. At 70% RH or higher, viability was 70% or higher for all species, indicating that their performance might be higher during the rainy season than during the dry season. Eggs of E. citrifolius and M. camelliae presented higher viability at the lower relative humidity levels than those of other species, indicating that these species might have higher chance to persist in the dry season. It is suggested that M. camelliae should be further evaluated for introduction in the state of Mato Grosso, considering that this mite is not yet present in that area.     

Effect of nectar-robbing birds on fruit set of Fuchsia magellanica in Tierra Del Fuego: a disrupted mutualism

1. This paper investigates spatial habitat variation in flower visitation by avian pollinators (mainly Hummingbirds) and nectar robbers to Fuchsia magellanica at the southern limit of its range, Tierra del Fuego, and their effects on plant reproductive success.
2. The plant-pollination mutualism appears to be disrupted as Hummingbirds ( Sephanoides galeritus) are rare at this high latitude and the frequencies of a nectar-robbing bird ( Phrygilus patagonicus) are high, especially in open areas where F. magellanica is most abundant.
3. Nectar robbery by P. patagonicus reduced fruit set about 20%, mainly because this fringillid can damage the ovary when piercing a flower. This bird was more abundant in open areas than inside the forest and, as expected, flower piercing was also more frequent in the former habitat.
4. Spatial variation was also found in the frequency of flower visitation by Hummingbirds; these birds foraged chiefly in the forest presumably because of the greater probability of finding intact (non-robbed) flowers there. This suggests that cross-pollinations in this self-compatible plant are more likely to occur in the forest. Nectar robbers therefore may influence not only the quantity of seeds produced but also, indirectly, their quality.
5. Fuchsia magellanica is polymorphic in flower colour. Robbery was significantly lower in the pale than in the normal (red) morph, although fruit set was similar between morphs.     

Studies on the rust,Maravalia cryptostegiae,a potential biological control agent of rubber-vine weed,Cryptostegia grandiflora (Asclepiadaceae: Periplocoideae), in Australia,II: Infection

The parameters which govern infection of rubber-vine weed by the rustMaravalia cryptostegiae were investigated. The infection process, from appressorial formation to sporulation, is described and illustrated. Uredinioid teliospores have an optimum temperature range for germination at 22–27 °C, both in vitro and in vivo. However, germination on the rubber-vine leaf was more than double (81–92%) that in the absence of the host, and appressoria were formed only in vivo. An optimum temperature of 20–22°C and a dew period of 12 hours or more gave the highest level of infection as measured by sporulation density. The latent period from inoculation to pustule formation decreased with increasing temperature; the shortest period (8–11 days) being recorded at 25–27°C. At the lower temperatures (18°C), this was significantly extended (19–21 days). Four successive inoculations significantly reduced plant height and dry weight, although a compensatory growth flush occurred after the third inoculation. The addition of cryoprotectants had a negative affect on spore viability and subsequent infectivity. Cooling dry spores to –196°C at the rate of 10°C min^–1 gave the best results, with high germination (93–65%) up to 8 days after thawing.     

Preliminary observation on the role of conditioning and mechanical Interference with egg masses and Juveniles in the competitive relationships Between Helisoma Durvi (Wetherby) and the Intermediate host of Schistosoma Mansoni Sambon: Biomphalaria Camerunensis (Boettger).

Biological control of the intermediate hosts of schistosomiasis by means of the introduction oa a competitor snail Helisoma duryi has been suggested. The effect of conditioning by Biomphalaria camerunensis and H. duryi respectively on growth and egg laying capacity of B. camerunensis and on the hatchability of B. camerunensis egg masses was compared. No differences were found besides an indication of a growth promoting effect of B. camerunensis conditioning.B. camerunensis egg masses were found to be much more sensitive to mechanical interference from snails than were H. duryi egg masses. Both juvenile and adult H. duryi caused a great reduction in the number of B. camerunensis egg masses and adult B. camerunensis showed a great tendency to destroy its own egg masses. Newly hatched B. camerunensis appeared to be destroyed to a greater extent by adult H. duryi than by adult B. camerunensis.