The effect of superparasitism on development of the solitary parasitoid wasp, Venturia canescens (Hymenoptera: Ichneumonidae)

Abstract.

• 1 The effects of superparasitism on the rate of development, adult size and mortality of Venturia canescens (Hymenoptera: Ichneumonidae) were investigated. Parasitoids were reared from third (L3) and fifth (L5) instars of one of its hosts, Plodia interpunctella (Lepidoptera: Pyralidae) containing one, two or four parasitoid eggs.
• 2 Superparasitism increased the development time of Venturia reared from both instars, but the developmental delay was more evident in wasps from L5 hosts.
• 3 The size of parasitoids from L3 hosts was unaffected by egg number, but wasps from both superparasitized L5 treatments were significantly smaller than those from singly parasitized hosts.
• 4 Parasitoid mortality was significantly higher in L5 than L3, but within instars did not differ significantly with egg number.
• 5 The results confirm that superparasitism may affect the fitness of both the adult female wasp and her progeny, and should therefore be incorporated into models of superparasitism as an adaptive foraging strategy.

     

Development of the solitary endoparasitoid Microplitis demolitor: host quality does not increase with host age and size

Abstract.  1. Many studies examining the relationship between host size, an index of host quality, and parasitoid fitness use development time and/or adult parasitoid size as currencies of fitness, while ignoring pre-adult mortality. Because the physiological suitability of the host may vary in different stages, sizes, or ages of hosts, a misleading picture of host quality may therefore be obtained in cases where fitness is based on only one or two developmental traits.
2. The development of the solitary koinobiont endoparasitoid Microplitis demolitor is examined in different larval age-classes of its host the soybean looper Pseudoplusia includens . Hosts were parasitised on days 1–8 after hatching from the egg, and development time, adult body size, and mortality of the parasitoid were compared.
3. A comparison of larval growth trajectories (using dry body mass) of M. demolitor revealed that parasitoid larvae attained over twice as much body mass in old hosts than in younger hosts. Similarly, adult parasitoid size at eclosion generally increased with host size, although parasitoids developing in smaller hosts lost a much lower proportion of mass between pupation and eclosion.
4. Overall egg-to-adult development was most rapid in intermediate-aged hosts, and longer in hosts at opposite ends of the age continuum. Moreover, parasitoid mortality varied non-linearly with host stage, and was generally higher in very young and older hosts.
5. Based on these results and other empirical data for koinobionts, it is argued that fitness functions in this group of parasitoids are not simply a positive function of host size or age, but instead may be distinctly dome-shaped, both patterns reflecting the degree of physiological and nutritional compatibility between the two organisms.     

Odour-mediated long-range avoidance of interspecific competition by a solitary endoparasitoid: a time-saving foraging strategy

1. In studies on optimal foraging strategies, long-range decisions in the pursuit of resource are rarely considered. This is also the case for sympatric parasitoids, which may be confronted with the decision to accept or reject host larvae that are already parasitized by a competing species. They can be expected to reject already parasitized hosts if it is likely that they will lose the resulting intrinsic competition. However, examples of such interspecific host discrimination are rare. 2. We propose that parasitoids that are not egg-limited should reject inferior hosts only if it saves them time, and that this will be achieved mainly when the parasitoids are able to detect competitors from a distance. We tested this hypothesis using the sympatric parasitoids Cotesia marginiventris (Cresson) and Campoletis sonorensis (Cameron). 3. C. sonorensis was found to be the superior intrinsic competitor but, upon contact with a host larva, both wasps readily accepted hosts that had already been parasitized by the other species. However, in an olfactometer experiment, C. marginiventris females were found to strongly avoid the odour of their superior competitor. 4. These results are in accordance with a time optimization scenario, whereby the inferior competitor accepts competition if it costs only an egg, but avoids competition if it may save time that can be allocated to the search for more profitable hosts. 5. Models on host discrimination strategies in parasitoids had not yet considered discrimination from a distance. Long-range foraging decisions can also be expected for other organisms that have to choose between resources of varying suitability and profitability.     

The effect of host nutrition on growth and development of the parasitoid waspVenturia canescens

We investigated the effect of host (Plodia interpunctella; Lepidoptera: Pyralidae) nutritional status on development of the solitary endoparasitoid,Venturia canescens (Hymenoptera: Ichneumonidae). Parasitoids from 3rd (L3) instars reared on a deficient diet during early parasitism took longer to develop and suffered higher mortality than those reared from hosts fedad libitum although there was not a significant difference in the size of eclosing wasps from the two groups. L5 hosts reared at high density produced smaller parasitoids, which developed more rapidly than those reared from hosts from low density containers, although mortality was higher in the latter. In a separate experiment we starved groups of 10–20 hosts (parasitized as L3) daily beginning on the 4th day after parasitism, to determine the host developmental stage required for successful parasitoid development to eclosion. Parasitoid survivorship increased with length of host access to food, while the egg-to-adult parasitoid development time increased throughout the experiment. Parasitoid size decreased with increasing periods of host starvation. The successful emergence ofVenturia depends uponPlodia reaching the size normally attained in the mid-5th instar, or 50–70% of the mass of healthy late 5th instars. Our results show that when earlier instars are parasitized, host growth is essential for successful parasitoid development to eclosion. Furthermore, they suggest that, for many koinobionts, host suitability may be greatly influenced by feeding rate and food quality.     

Interaction of a solitary larval endoparasitoid, Microplitis mediator, with its host, Mamestra brassicae: host acceptance and host suitability

Abstract:  Microplitis mediator (Haliday) (Hym., Braconidae) is an important parasitoid of early instar larvae of the European cabbage moth, Mamestra brassicae L. (Lep., Noctuidae). In the laboratory, we examined attack responses of female M. mediator to the first three larval instars of M. brassicae . Females were presented with M. brassicae larvae either one individual at a time in a no-choice experiment, or three individuals, one from each instar, simultaneously in a choice experiment. Whether or not there was choice, naïve female parasitoids attacked a high proportion of larvae and did not discriminate among instars. In the no-choice experiment, attacked larvae were reared, and parasitoid cocoons were produced from about 76% of larvae attacked as first and second instars, but from only 19% of larvae attacked as third instars. Dissections of attacked larvae from the choice experiment showed that about 79% of attacks on first and second instars resulted in oviposition compared with only 49% for third instars. When given choice, frequency and number of attacks on first instar larvae increased with increasing parasitoid experience. Our results suggest that first and second instar larvae of M. brassicae are suitable hosts for M. mediator , but that third instar larvae are suboptimal both because oviposition attempts were frequently unsuccessful and because immature parasitoids failed to complete development. Nevertheless, naïve attacking parasitoids exhibited minimal discrimination among instars, although experienced parasitoids most frequently attacked first instar larvae. The host selection behaviour of M. mediator is discussed in the context of optimal foraging theory and implications for biological control.     

Host behaviour and its influence on foraging and acceptance by the solitary parasitoid wasp,Venturia canescens (Hym: Ichneumonidae)

Behavioural interactions between the solitary koinobiont parasitoid,Venturia canescens, and two of its hosts,Plodia interpunctella andCorcyra cephalonica, were investigated. The response of both hosts to simulated antennation using a two-haired brush was examined over instars 3 (L3) to 5 (L5). YoungP. interpunctella larvae predominantly adopted escape tactics (writhe, trash) whereas L5P. interpunctella usually froze after the stimulus was applied. L3C. cephalonica larvae were more aggressive (headrear, flick) thanP. interpunctella in response to the application of the stimulus, but olderC. cephalonica responded less aggressively than in earlier instars. AlthoughV. canescens readily jabbed its ovipositor at both hosts after antennation,P. interpunctella was considerably more susceptible to parasitoid attack thanC. cephalonica, irrespective of size in the final (L5) instar.C. cephalonica, the larger, more aggressive host, actively resisted parasitism whereasP. interpunctella responded much more passively after parasitoid contact. Parasitoids examined and jabbed their ovipositors at dead hosts, but this behaviour was not sustained, implying that host movement stimulates parasitoid attack. On patches containingV. canescens, L5C. cephalonica andP. interpunctella, mostP. interpunctella larvae responded by freezing after parasitoid contact.P. interpunctella that froze usually avoided parasitism, whereas larvae that attempted to escape by crawling were pursued with vigour byV. canescens and usually parasitized. Irrespective of behaviour after parasitoid contact,C. cephalonia displayed more aggressive behaviour and had much greater success in warding off parasitoid attack. Host acceptance byV. canescens is clearly affected by the size and species of the host it attacks. The influence of host defensive behaviour is discussed in relation to the evolution of parasitoid counter-defences and oviposition strategies.     

Dynamic effects of parasitism by an endoparasitoid wasp on the development of two host species: implications for host quality and parasitoid fitness

1. The study reported here examined growth and developmental interactions between the gregarious larval koinobiont endoparasitoid Cotesia glomerata (Hymenoptera: Braconidae) and two of its hosts that vary considerably in growth potential: Pieris rapae and the larger P. brassicae (Lepidoptera: Pieridae). At pupation, healthy larvae of P. brassicae are over twice as large, in terms of fresh body mass, as those of P. rapae. 2. Clutch size of C. glomerata was manipulated artificially, and the relationship between parasitoid burden and the maximum weight of the parasitised host (= host–parasitoid complex) was measured. In both hosts, the maximum complex weight was correlated positively with parasitoid burden. Compared with unparasitised hosts, however, the growth of P. rapae was increased at significantly lower parasitoid burdens than in P. brassicae. Emerging wasp size was correlated negatively with parasitoid burden in both host species, whereas development time was less affected. 3. After larval parasitoid egress, the weight of the host carcass increased slightly, but not significantly, with parasitoid burden, although there was a strong correlation between the proportion of host mass consumed by C. glomerata larvae during development and parasitoid burden. 4. Clutch size was generally correlated positively with instar parasitised in both hosts, and greater in P. brassicae than in P. rapae. Sex ratios were much more female biased in L1 and L2 P. rapae than in all other host classes. Adult parasitoid size was correlated inversely with host instar at parasitism, and wasps emerging from P. brassicae were larger, and completed development faster, than conspecifics emerging from P. rapae. 5. The data reveal that parasitism by C. glomerata has profound species‐specific effects on the growth of both host species. Consequently, optimality models in which host quality is often based on host size at parasitism or unparasitised growth potential may have little utility in describing the development of gregarious koinobiont endoparasitoids. The results of this investigation are discussed in relation to the potential effectiveness of gregarious koinobionts in biological control programmes.     

Phenoloxidase in larvae of Plodia interpunctella (Lepidoptera: Pyralidae): molecular cloning of the proenzyme cDNA and enzyme activity in larvae paralyzed and parasitized by Habrobracon hebetor (Hymenoptera: Braconidae)

Phenoloxidase (PO) is a major component of the insect immune system. The enzyme is involved in encapsulation and melanization processes as well as wound healing and cuticle sclerotization. PO is present as an inactive proenzyme, prophenoloxidase (PPO), which is activated via a protease cascade. In this study, we have cloned a full-length PPO1 cDNA and a partial PPO2 cDNA from the Indianmeal moth, Plodia interpunctella (Hubner) (Lepidoptera: Pyralidae) and documented changes in PO activity in larvae paralyzed and parasitized by the ectoparasitoid Habrobracon hebetor (Say) (Hymenoptera: Braconidae). The cDNA for PPO1 is 2,748 bp and encodes a protein of 681 amino acids with a calculated molecular weight of 78,328 and pI of 6.41 containing a conserved proteolytic cleavage site found in other PPOs. P. interpunctella PPO1 ranges from 71-78% identical to other known lepidopteran PPO-1 sequences. Percent identity decreases as comparisons are made to PPO-1 of more divergent species in the orders Diptera (Aa-48; As-49; and Sb-60%) and Coleoptera (Tm-58; Hd-50%). Paralyzation of host larvae of P. interpunctella by the idiobiont H. hebetor results in an increase in phenoloxidase activity in host hemolymph, a process that may protect the host from microbial infection during self-provisioning by this wasp. Subsequent parasitization by H. hebetor larvae causes a decrease in hemolymph PO activity, which suggests that the larval parasitoid may be secreting an immunosuppressant into the host larva during feeding.     

Sex allocation and larval competition in a superparasitizing solitary egg parasitoid: competing strategies for an optimal sex ratio

1. Parasitic Hymenoptera reproduce by arrhenotokous parthenogenesis, and females of these species are able to control their progeny sex ratios. In structured populations of parasitic Hymenoptera, primary sex ratios are often highly biased toward females. However, sex ratio can be adjusted to the quality of encountered patches or hosts or be modified by differential developmental mortality.
2. In this paper, the effects were evaluated of the quality of encountered hosts and developmental mortality on the sex ratio in Anaphes victus , a solitary egg parasitoid whose first instar larvae present a sexual dimorphism and where superparasitism is regulated by larval fights between first instar larvae.
3. The results showed that a female-biased sex ratio is allocated to unparasitized hosts. In the presence of parasitized hosts, the second (superparasitizing) female produced a significantly higher sex ratio than the first female but the tertiary sex ratio (sex ratio at emergence) was not significantly different from the sex ratio produced with unparasitized hosts. The increase in the primary sex ratio produced by the second female was mostly compensated by the higher mortality of male larvae.     

Reduction of oviposition time and enhanced larval feeding: two potential benefits of aggregative oviposition for the viburnum leaf beetle

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Suitability of various stages of mealybug,Phenacoccus solenopsis (Homoptera: Pseudococcidae) for development and survival of the solitary endoparasitoid,Aenasius bambawalei (Hymenoptera: Encyrtidae)

Aenasius bambawalei has been recently reported as a solitary endoparasitoid of Phenacoccus solenopsis in India. Laboratory experiments were conducted comparing the parasitoid's preference for the three developmental stages of mealybug and its effect on parasitism, development, progeny fitness and sex ratio of A. bambawalei. The studies revealed third instar mealybugs as the most preferred stage for development of the parasitoid.     

How to become large quickly: quantitative genetics of growth and foraging in a flush feeding lepidopteran larva

Rapid larval growth in insects may be selected for by rapid ephemeral phenological changes in food resources modifying the structure of phenotypic and genetic (co)variation in and among individual traits. We studied the relative effects of three processes which can modify expression of additive genetic and nongenetic variation in traits. First, natural selection tends to erode genetic variation in fitness-related traits. Second, there may be high variance even in traits closely coupled with fitness, if these traits are themselves products of variable lower level traits. Third, traits may be canalized by developmental processes which reduce phenotypic variation. Moreover, we investigated the phenotypic and genetic role played by the underlying traits in attaining simultaneously both large size and short development time. We measured phenotypic and genetic (co)variation in several pre- and post-ingestive foraging traits, growth, development rate, development time and size, together forming a hierarchical network of traits, in the larvae of a flush feeding geometrid, Epirrita autumnata. Rapid larval growth rate and high pupal mass are closely related to fitness in E. autumnata. Traits closely associated with larval growth displayed low levels of additive genetic variation, indicating that genetic variability may have been exhausted by selection for rapid growth. The body size of E. autumnata, in spite of its close correlation with fitness, exhibited a significant additive genetic variation, possiblye because caterpillar size is the outcome of many underlying heritable traits. The low level traits in the hierarchical net, number (indicating larval movements) and size of feeding bouts in leaves, relative consumption rate and efficiency of conversion of ingested food, displayed high levels of residual variation. High residual variation in consumption and physiological ability to handle leaf material resulted from their flexibility which reduced variation in growth rate, i.e. growth rate was canalized. We did not detect a trade-off between development time and final size. On the contrary, large pupal masses were attained by short larval periods, and this relationship was strongly genetically determined, suggesting that both developmental time and final size are expressions of the same developmental process (vigorous growth) and the same genes (or linkage disequilibrium).     

Comparing the physiological effects and function of larval feeding in closely‐related endoparasitoids (Braconidae: Microgastrinae)

Abstract The larvae of most endoparasitoid wasps consume virtually all host tissues before pupation. However, in some clades, the parasitoid larvae primarily consume haemolymph and fat body and emerge through the side of the host, which remains alive and active for up to several days. The evolutionary significance of this host‐usage strategy has attracted attention in recent years. Recent empirical studies suggest that the surviving larva guards the parasitoid broods against natural enemies such as predators and hyperparasitoids. Known as the ‘usurpation hypothesis’, the surviving larvae bite, regurgitate fluids from the gut, and thrash the head capsule when disturbed. In the present study, the ‘usurpation hypothesis’ is tested in the association involving Manduca sexta, its parasitoid Cotesia congregata, and a secondary hyperparasitoid Lysibia nana. Percentage parasitoid survival is higher and hyperparasitism lower when cocoons of C. congregata are attached to the dorsum of M. sexta caterpillars. Fat body contents in several associations involving solitary and gregarious parasitoids feeding on haemolymph and fat body are also compared. The amount of fat body retained in parasitized caterpillars varies considerably from one association to another. In M. sexta and Pieris brassicae, considerable amounts of fat body remain after parasitoid emergence whereas, in Cotesia kariyai and Cotesia rufricus, virtually all of the fat body is consumed by the parsasitoid larvae. The length of post‐egression survival of parasitized caterpillars differs considerably in several tested associations. In Pseudeletia separata, most larvae die within a few hours of parasitoid emergence whereas, in M. sexta, parasitized larvae live up to 2 weeks after parasitoid emergence. Larvae in other associations parasitized by gregarious and solitary endoparasitoids live for intermediate periods. The results are discussed in relation to the adaptive significance of different feeding strategies of immature parasitoids and of the costs and benefits of retaining the parasitized caterpillar in close proximity with the parasitoid cocoons.     

Effects of cultivar on oviposition preference, larval feeding and development time of diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae), on some Brassica oleracea vegetables in Victoria

Abstract We studied oviposition preference of Plutella xylostella for four cultivars of cabbage, broccoli and cauliflower in the field. There were no differences in the number of eggs found on the various cultivars of broccoli or cauliflower. Significantly more eggs were laid on cultivar Savoy King than any of the other cabbage cultivars tested. We then compared the development time and feeding damage of larvae reared on Savoy King and Green Coronet cabbages. Larvae developed more rapidly and fed more and for longer on Green Coronet than Savoy King. Thus, while Savoy King is more attractive to oviposition in the field, net impacts on the crop may be lessened to some degree through lower feeding proficiency of the larvae on that cultivar.     

Facultative gregarious development in a solitary koinobiont parasitoid,Ephedrus californicus: implications of larval ecology and host constraints

In solitary parasitoids, the mandibulate first instars behave aggressively towards potential competitors so that generally only one larva survives per host. A ‘failure of competition’ may result in facultative gregarious development, however. We used Ephedrus californicus Baker (Hymenoptera: Braconidae: Aphidiinae), a solitary koinobiont parasitoid of aphids, to test two hypotheses in the laboratory that could explain facultative gregarious development. Gregarious development increased with the intensity of parasitism, with two (rarely three) parasitoids successfully developing in a single aphid. In heavily superparasitized hosts, interference between surviving larvae often caused abnormal pupation behaviour and inability to emerge from the mummy. The hypothesis that the survival of more than one larva per host is dependent on differences in larval age was not supported. The total body size in terms of dry mass of two males or two females developing together in the same host was higher than that of same‐sex counterparts developing singly. Females were larger than males with which they shared a host. Hypotheses about the evolutionary transition from a solitary to a gregarious lifestyle in parasitoid Hymenoptera have focused on lethal fighting between first instars but have ignored other constraints including immature mortality during later development and limiting host resources. Especially in species that pupate inside the dead host, specific requirements for pupation and emergence may determine whether one or several offspring per host can develop to adult.     

Effect of host deprivation on egg quality,egg load,and oviposition in a solitary parasitoid,Chetogena edwardsii (Diptera: Tachinidae)

Solitary parasitoids are limited to laying one egg per host because larvae compete within hosts. If host encounter rate is low, females should not increase the number of eggs/host in response. The tachinid fly, Chetogena edwardsii,was used to evaluate the effect of host deprivation on egg accumulation, oviposition behavior, and egg quality in a solitary parasitoid. Females deprived of hosts for 2– 7 days accumulate about 1 day's supply of eggs. Egg output of deprived females once hosts are restored does not differ from that of control females. Deprived females retain one egg in the uterus where it undergoes embryogenesis. Maggots emerging from retained eggs are more likely to survive in hosts molting in 40 h or less after receipt of an egg than are maggots emerging from eggs fertilized shortly before oviposition. Egg retention is a consequence of host deprivation that permits females to broaden the range of hosts they can exploit to include soon-to-molt hosts and possibly multiply parasitized hosts.     

The contribution of the facultative feeding period to echinoid larval development and size at metamorphosis: a comparative approach

Planktotrophic invertebrate larvae have two dissociable stages during development, a facultative feeding period, whose length is determined by the amount of maternal provisioning in the egg, and an obligate feeding period, whose length is determined by the quantity of exogenous energy needed to reach metamorphic competence. Here we set out to experimentally test the impact of feeding during the facultative feeding period at two food concentrations (limiting and nonlimiting) on larval development time and juvenile quality. We used two closely related subtropical sand dollar species that differ in the quantity of maternal investment for these comparisons: Leodia sexiesperforata (large egg, long facultative feeding period) and Mellita tenuis (small egg, short facultative feeding period). We found that feeding during the facultative period accelerates development to metamorphosis only in M. tenuis and only at the high food ration. Feeding during the facultative feeding period had no effect on development time for M. tenuis at a food limiting concentration and for L. sexiesperforata at either food concentration. Furthermore, we found feeding during the facultative period to significantly increase quantity of carbohydrates and lipids at metamorphosis only for M. tenuis in nonlimiting food concentration. Thus, our data reveal a two-fold benefit of the facultative feeding period for a poorly provisioned species under high food conditions but little effect on a well-provisioned species. We discuss our results in reference to McEdward's [McEdward, L.R., 1997. Reproductive strategies of marine benthic invertebrates revisited: facultative feeding by planktotrophic larvae. Am. Nat. 150, 48-72] facultative feeding model.     

Advantages and disadvantages of large colony size in a halictid bee: the queen's perspective

The size of the group of social species might influence basicaspects of productivity and social interactions. In many primitivelysocial insects, foundress queens are basically in control ofthe number of workers in their first brood. We examined factorsthat might influence the optimal number of workers a queen shouldproduce during the solitary founding phase in Lasioglossum malachurum(Hymenoptera, Halictidae). A priori, it seems plausible thatshe should produce as many workers as possible (1) to maximizecolony productivity and (2) to minimize the impact of broodparasitoids. However, there might also be unfavorable consequencesof a large colony size from the queen's perspective. First,the queen might incur disproportionately high costs that decreaseher potential for subsequent reproduction. Second, the queenmight not be able to suppress the development of ovaries ina large number of workers. As a clear advantage of a large colonysize, we found an increased production of sexuals. Contraryto our expectation, in the first worker phase, nests that wereparasitized by Sphecodes bees had more workers than did unparasitizednests. We found no evidence that the production of the firstworker brood entailed costs to the queen. However, the degreeof development of worker ovaries increased with colony size,and some degree of development was detectable with as few asfour workers. This study shows that the number of workers aqueen produces might depend on the interaction of several factors,some of which have not been considered in detail yet.     

Factors affecting the evolution of development strategies in parasitoid wasps: the importance of functional constraints and incorporating complexity

Parasitoid wasps have long been considered as model organisms for examining optimal resource allocation to different fitness functions, such as body size and development time. Unlike insect predators, which may need to consume many prey items to attain maturity, parasitoids generally rely on a limited amount of resources that are obtained from a single source (the host). This review discusses a range of ecophysiological constraints that affect host quality and concomitantly the evolution of development strategies in parasitoids. Two macroevolutionary differences in host usage strategies (idiobiosis, koinobiosis) are initially described. Over many years, particular attention has been paid in examining a range of quantitative host attributes such as size, age, or stage, as these affect idiobiont and koinobiont parasitoid development. Parasitoids and their hosts, however, constitute only a small part of an ecological community. Consequently, host quality may be affected by a broad range of factors that may operate over variable spatial and temporal scales. Intimate factors include aggressive competition with other parasitoids and pathogens for access to host resources, whereas less intimate factors include the effects of toxic plant compounds (allelochemicals) on parasitoid performance as mediated through primary and/or secondary hosts. It is suggested that future experiments should increase the levels of trophic complexity as these influence the evolution of life history and development strategies in parasitoids. This includes integration of a suite of direct and indirect mechanisms, including biological processes occurring in different ecological realms, such as above‐ground and below‐ground interactions.