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Nutritional ecology of endoparasitic insects and their hosts: An overview
.I. Insect Physiol. Vol. 32,No. 4,pp.255-261,1986
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Copyright 0 1986Pergamon Press Ltd
NUTRITIONAL ECOLOGY OF ENDOPARASITIC AND THEIR HOSTS: AN OVERVIEW
INSECTS
FRANK SLANSKY JR Department
of Entomology
and Nematology, Institute of Food and Agricultural Florida, Gainesville, FL 32611, U.S.A.
Sciences,
University
of
Abstract-The impact of insect endoparasites (parasitoids) on the physiology and behaviour of their hosts is reviewed within the context of the nutritional ecology of the parasitoids and their hosts. Alterations in the consumption, utilization and allocation of food by parasitized hosts are common, as are internal changes in their metabolic physiology. Gregarious parasitoid species frequently increase feeding by their host larvae whereas solitary parasitoid species often reduce feeding and growth of their hosts. Many parasitoid-associated changes in host physiology and behaviour are interpreted to be of adaptive significance to parasitoids. Substantial circumstantial evidence suggests, and a few direct tests of such adaptive significance indicate, that parasitoids alter their hosts in ways beneficial to their own fitness. However, most of the changes in parasitized hosts are of unknown cause and undocumented significance to the parasitoids. Several relevant hypotheses are presented, and these require extensive evaluation (often requiring novel experimental approaches) before a thorough understanding of parasitoid nutritional ecology is established. Key Word Index:
Nutritional
ecology,
nutritional
INTRODUCTION Insect hosts provide food and living space for larval parasitoids (endoparasitic insects) and sometimes food for the adult parasitoid. Parasitoids represent potentially fatal intrusions into their hosts’ bodies, and insects manifest various “anti-parasitoid” tactics. For example, living within its food or within a webbed “nest”, and association with ants, may reduce an insect’s exposure to parasitoids (Price et al., 1980; Atsatt, 1981; Pierce and Mead, 1981; Stamp, 1984). Active defensive responses against parasitoids occur at both behavioural and physiological levels, and include head-thrashing, rapid wiggling, extrusion of fluid droplets directed at the attacking female parasitoid, and encapsulation and other immune responses against non-self substances (Vinson and Iwantsch, 1980a; Ratcliffe et al., 1984; Stamp, 1984). These responses must be overcome for successful parasitism and successful development within the host. Other host behaviour (e.g. continued intake of nutrients) may be favourable to, and often necessary for, successful development of the parasitoid; these must be allowed to continue and perhaps be enhanced by actions of the parasitoid. Thus, dominating characteristics of the nutritional ecology (Slansky, 1982) of insect parasitoids, as well as noninsect endoparasites (Thompson, 1983d; Moore, 1984), involve overcoming host defences while often simultaneously minimizing stressful impact on their hosts and influencing host physiology and behaviour to apparently benefit themselves (Vinson and Iwantsch, 1980a; 1980b). Within this context, three key questions, closely interrelated, must be answered to advance our understanding of parasitoid nutritional ecology: (1) To what extent are the variety of parasitoidassociated alterations in host physiology and behaviour of benefit to the parasitoids? (2) To what extent 255
physiology,
insect parasitism,
insect parasitoids
are these alterations actively influenced by parasitoids? and (3) In those cases where parasitoids actively influence host activities, what are the mechanisms by which parasitoids exert such control? In the present paper, I present hypotheses and discuss published data related primarily to the apparent adaptive nature of parasitoid-associated alterations in host physiology and behaviour, especially those related to consumption and utilization of food. Mechanisms of parasitoid control of their hosts are reviewed elsewhere (Vinson and Iwantsch, 1980b; see also Beckage and Riddiford, 1983b).
IMPACT OF PARASITOIDS ON PERFORMANCE OF THEIR HOSTS Once an insect larva is successfully parasitized by an insect parasitoid, it will die before reproducing [insects parasitized as adults ,may continue to reproduce but at a reduced rate (Shahjahan, 196811. Aspects of the larval host’s post-parasitization performance may involve continued defensive responses and stress-induced alterations in physiology and behaviour (Vinson and Iwantsch, 1980a, 1980b; Thompson, 1983d). However, because the genetic fitness of a parasitoid within a host is directly dependent on host activities, natural selection will undoubtedly commonly result in evolution of parasitoid-influenced changes in host physiology and behaviour that improve the parasitoid’s fitness. In many cases this may involve active “take-over” of control of host activities by parasitoids with input from both adult and larval stages of the parasitoid contributing to such take-over (Vinson and Iwantsch, 1980b). For example, in one of the few experimental studies assessing the apparent adaptive nature of parasitoid-associated alterations in host behaviour, Stamp (1981; see also Fritz, 1982) demonstrated that
FRANK SLANSKY JR
256
the behaviour of aposematically-coloured larvae of the checkerspot butterfly Euphydryas phaeton when parasitized by Apanteles euphydryidis, in crawling up out of dense vegetation to more exposed sites, benefits the parasitoids within them by reducing hyperparasitism. In cases where behaviour of a parasitized host benefits survival of its kin (such as hypothesized by Shapiro, 1976), then such behaviour may be adaptive to the host. Empirical documentation of this phenomenon is, however, required, and behaviour of parasitized hosts is considered here from the viewpoint of parasitoid fitness. Nonetheless, it must be emphasized that although many parasitoidassociated changes in host physiology and behaviour can be interpreted as adaptive to the parasitoids, experimental determinations of such adaptive benefit are few. Assessing the extent of such adaptive benefit is a major challenge for improving our understanding of parasitoid nutritional ecology. Effects of parasitoids include substantial impact on the consumption and utilization of food by their hosts, whereas host developmental time seems to be less frequently affected (summarized in Slansky and Scriber, 1985). Internal changes in host metabolism underlying these more overt alterations also occur (see below). If alterations in host physiology and behaviour are relevant to parasitoid fitness, then the extent of parasitoid influence on a host’s consumption and utilization of food should reflect the nutritional content of the host relative to the nutritional demands of the parasitoid(s). If sufficient nutrients for complete parasitoid development are lacking, then continued feeding by the host will be permitted and perhaps stimulated above the unparasitized level by the parasitoid.
MINIMIZING
IMPACT
ON THE HOST
Development of parasitoids frequently spans several host instars, apparently because there is selection to attack early host instars even though these provide an inadequate supply of nutrients for the parasitoid to complete its development (see below). Early instar parasitoids avoid substantial damage to host tissues, thereby minimizing their impact on early host development. Disruption of select host tissues may occur, however, apparently serving to reduce uptake of haemolymph nutrients by the host (Fisher, 1971; Smith and Smilowitz, 1976; Couchman and King, 1979). Parasitoids might evolve to exert less impact on the behaviour of “social” (i.e. gregarious) host species compared with solitary ones, because host individuals of the former acting “differently” from their neighbours may be more conspicuous and suffer increased mortality compared with those of the latter (Fritz, 1982). Parasitoids of web-inhabitating insects, however, might regulate their hosts to spend more time within the confines of the web, under the assumption of reduced susceptibility to predation and hyperparasitism within the web. Unfortunately, data needed to evaluate these hypotheses are apparently lacking.
STIMULATORY
EFFECTS
In addition to prolonged parasitoid development through several host instars, further support for the hypothesis that hosts may initially provide an insufficient supply of nutrients for parasitoids comes from the increased feeding exhibited by some parasitized hosts (summarized in Slansky and Scriber, 1985). In most of the cases where the amount of food and/or rate of feeding by a parasitized host is greater than that of an unparasitized host, the parasitoid involved is gregarious. These results suggest that the nutritional demands imposed by the several individuals of a gregarious parasitoid are greater than those of a single individual of a solitary parasitoid (Smith and Smilowitz, 1976). Supportive of this difference in nutritional demands between solitary and gregarious parasitoids is the finding that, although attacking the same early host instars, larvae of the solitary parasitoid Apanteles rubecula emerge during the fourth instar of the host (Pieris rapae) whereas larvae of the gregarious A. glomeratus (with about 30 larvae/host larva; Slansky, 1978) do not emerge until later in the fifth host instar (during which P. rapae larvae consume over 85% of their total food intake; Parker and Pinnell, 1973). The necessity for parasitoid survival of feeding by the host was elegantly demonstrated by Beckage and Riddiford (1983a). When newly ecdysed final-instar Manduca sexta larvae parasitized by Apanteles congrega tus are starved, parasitoid emergence is prevented; the longer host larvae are allowed to feed prior to starvation, the greater is the percentage emergence of the parasitoids. Increased density of parasitoids/host may also increase host feeding, such as in the aphid Acyrthosiphon pisum when parasitized by two larvae of Aphid&s smithi compared with aphids containing only one parasitoid (Cloutier and Mackauer, 1979, 1980; see also Fiihrer, 1981). Number of parasitoids/host larva is positively correlated with net weight of host carcass in the armyworm Leucaniu separata (Tagawa et al., 1982; Sato and Tanaka, 1984) and the sphingid M. sexta (Beckage and Riddiford, 1983a), indicating greater food consumption and/or food utilization efficiencies for more heavily parasitized larvae. Such apparent parasitoid regulation of host behaviour may be rather precise. For example, dry weight of emerging adult A. glomeratus is unaffected by density of its larvae within the host over a range of 9-47 parasitoids/host larva, suggesting that compensatory increases in host feeding occur as parasitoid density increases. However, once some limit of parasitoid density is exceeded, their body weight and survival may decline (Fiihrer and Keja, 1976; Slansky, 1978; Tagawa et al., 1982; Beckage and Riddiford, 1983a).
INHIBITORY
EFFECTS
In contrast with gregarious species, solitary parasitoids frequently inhibit host behaviour, causing various degrees of host paralysis and reduction in its food consumption (and consequently decreasing its growth). In general, species of ichneumonid parasitoids reduce growth rate of their hosts to a greater extent than do braconid species, and growth rates
Parasitoid nutritional ecology
are more severely reduced in later host instars (Thompson, 1982b). Several hypotheses concerning the apparent adaptive significance of such effects to parasitoids can be proposed. For example, a paralyzed host may exhibit reduced defensive capabilities and also reduced tissue uptake of haemolymph nutrients, thereby providing a greater supply of nutrients for the parasitoid (Vinson and Iwantsch, 1980a, 1980b). In addition, because movement associated with feeding and other behaviour may increase susceptibility of an insect to predation, host paralysis may reduce the host’s and thus the associated parasitoid’s chance of being killed before the parasitoid completes its development (Price et al., 1980; Fritz, 1982). Also, it is known that allelochemicals consumed by host larvae may negatively affect parasitoid performance (Campbell and Duffey, 1979; Barbosa et al., 1982); reducing or stopping the consumption of food by its host may therefore reduce a parasitoid’s exposure to potentially toxic allelochemicals. Some parasitoids, however, sequester allelochemicals from their hosts; whether these chemicals protect the parasitoids against their own enemies has apparently not yet been demonstrated; Benn et al., 1979). Unfortunately, rigorous experimental tests of these hypotheses are scarce. INTERNAL
CHANGES
IN HOST METABOLISM
Underlying the more overt parasitoid-associated changes in host activities discussed above are a variety of internal changes. Nutrient composition of host haemolymph (e.g. amino acids, proteins, carbohydrates and osmolality) and fat body (e.g. glycogen) are often altered after parasitization, as are host hormones and metabolic rate (Vinson and Iwantsch, 198Oa, 1980b; El-Sufty and Fiihrer: 1981; Thompson, 1982b, 1983d). Efficiency of nitrogen utilization and excretion of nitrogenous compounds may also be altered in parasitized hosts (Kahn et al., 1976; Slansky, 1978). These changes are undoubtedly related in complex ways to the presence of the parasitoids. Some of these alterations in host metabolic physiology are induced by the ovipositing adult parasitoid in Hymenoptera (but not Diptera; Mellini, 1983) or during the parasitoid’s egg stage. Other changes occur during the larval stage of the parasitoid, perhaps being induced by the parasitoid through chemical secretions or selective destruction of host tissues, as well as through consumption of haemolymph nutrients. Unravelling the causes and consequences of these complex interactions will require novel experimental approaches. For example, Thompson (1982a, 1982b, 1983a) manipulated food intake of unparasitized Trichoplusia ni through dietary dilution such that their relative consumption rate was reduced to a level similar to that of larvae parasitized by Hyposoter exiguae. This allowed distinction of the more direct effects of H. exiguae on host metabolic physiology (e.g. increased rate of food assimilation and haemolymph and fat body nutrient levels) from those effects resulting from reduced food consumption associated with parasitization (e.g. reduced growth rate).
NUTRITIONAL CONSTRAINTS PARASITOIDS
257 ON
As indicated above, parasitoids may overcome potential nutrient constraints on their performance through prolonged development spanning several host instars, through stimulatory effects on the consumption and utilization of food by their hosts, and through influences on host metabolism. Other data can also be interpreted within the context of nutritional constraints on parasitoid growth, including the following: (a) Slower parasitoid growth in early compared with later host instars (Sato, 1980). Examples of apparently “accelerated” parasitoid development when eggs are laid in later host instars (Beckage and Riddiford, 1978; Brewer and King, 1980, 1981) may actually be evidence of constrained parasitoid development in early host instars (Vinson and Barras, 1970; Smilowitz and Iwantsch, 1973). A number of factors influence growth and development of parasitoids (Thompson,,l981, 1983b, 1983~; Tauber et al., 1983), but the extent to which parasitoid larvae adaptively alter their growth rate depending on host age is poorly known (Fisher, 1971; Smilowitz and Iwantsch, 1973; Sato, 1980). (b) Reduced weight of parasitoids when emerging from heavily parasitized hosts (Tagawa et al., 1982; Beckage and Riddiford, 1983a). These results suggest that there is a limit to the extent of parasitoid-induced stimulation in food consumption and food utilization efficiencies by the host (Fiihrer, 1981). Once this limit is exceeded, the parasitoids apparently deplete their supply of food and subsequently starve. If, at this time, they exceed the critical weight for pupation (Sato, 1980; Angelo and Slansky, 1984), then they may survive to produce smaller than usual sized adults. In some cases of increased parasitoid density, duration of the parasitoid larval period may be shortened (Brewer and King, 1980; Parkman et al., 1983), whereas in others it may be lengthened (Beckage and Riddiford, 1978). Negative impact of reduced body size on parasitoid fitness (e.g. because of reduced fecundity) should select for avoidance of superparasitism (i.e. multiple ovipositions in the same host) such as through evolution of host-marking by parasitoids and of lethal interactions among parasitoid larvae that serve to reduce the number of parasitoids/host (for review see Vinson and Iwantsch, 1980a). Potential host species could evolve odours that mimic parasitoid host-marking odours thereby deterring female parasitoids (Slansky, 1978). (c) Reduced weight of parasitoids feeding in smallsized non-feeding host stages (Arthur and Wylie, 1959; Rojas-Rousse and Kalmes, 1978; Charnov and Skinner, 1984). Parasitoids of the egg or pupal stage lack the opportunity for increasing intake of food by the host and thus if the weight of the host is less than that required by the parasitoid to achieve its ideal body weight, then the resulting adult parasitoid may have a reduced body weight. For example, the parasitoid wasp Brachymeria intermedia attains its greatest dry body weight in gypsy moth pupae from larvae reared on red oak, whereas its body weight is reduced 30% in the smaller pupae from larvae reared on white oak or red maple (Greenblatt and Barbosa, 1981).
258
FRANK SLANSKY JR
Differences in nutritional and allelochemical content of hosts may override the benefits of their increased weight to parasitoids, resulting in parasitoids whose body weight is below that predicted by host weight (Greenblatt and Barbosa, 1980, 1981; Barbosa et al., 1982). Ovipositing females of some parasitoids and their hyperparasitoids may assess host size and bias the sex ratio of the eggs they lay toward the smaller sized sex (usually males) in smaller hosts (Kfir and Rosen, 198la, 198lb, 1981~) as well as alter the number of eggs they lay per host (Luck et al., 1982; Charnov and Skinner, 1984). PARASITIZATION
OF EARLY-INSTAR
HOSTS
Given the necessity for parasitoids to persist within their hosts through several host instars (especially when parasitization occurs during early host instars), and given the reduced probability of the host surviving through several instars (Price, 1972; Vinson and Iwantsch, 1980a), why should parasitoids attack early-instar hosts? Possible reasons include: (a) Ease of locating the more numerous earlyinstar host larvae compared with later instars (Price, 1972). (b) Overcoming host defences. For example, larger oral droplets emitted by later-instar Pieris brassicae are sufficient to drown or repel attacking females of the braconid wasp A. glomeratus whereas those of early-instar larvae are less efficacious (Johansson, 1950). The fully tanned cuticle of fifthinstar larvae of M. sexta is impenetrable to the ovipositor of A. congregatus (Beckage and Riddiford, 1978). Successful emergence of various parasitoids is highest when parasitization is initiated in particular host instars, probably due to age-related changes in internal defences (Vinson and Iwantsch, 1980a, 1980b). (c) Success in aggressive competition. The first parasitoid to become established in a host is often able to kill subsequent invaders (Vinson and Iwantsch, 1980a; Kfir and Rosen, 1981b; Godwin and Odell, 1984). FOOD UTILIZATION EFFICIENCIES OF PARASITOIDS
Parasitoids are hypothesized to exhibit high food utilization efficiencies because they consume food of seemingly high nutritional quality, because of their presumed relative inactivity within the host, and because of possible selection for efficient utilization of a limited food supply (Slansky and Scriber, 1985). Data for some 15 species of parasitoids indicate that they exhibit high assimilation efficiencies (55-94%, x = 68%) but net growth efficiencies (indicating the conversion of assimilated food into parasitoid biomass) range from a few low to mostly moderate values (11-62%, X = 37%; summarized in Slansky and Scriber, 1985). The only nitrogen utilization efficiency values apparently available for parasitoids (for two hymenopterous pupal parasitoids) tend to lie toward the low end of the range of values for insects in general when parasitizing gypsy moth pupae but toward the high end of the range when parasitizing wax moth pupae (Greenblatt et al., 1982). Net growth efhciencies may not be exceptionally high because of several reasons, including selection
for rapid rather than efficient parasitoid growth, the commonly exhibited inverse relationship between assimilation efficiency and net growth efficiency, and high metabolic activity of parasitoid larvae (e.g. because of active amino acid anabolism and catabolism, high detoxication enzyme activity, or rapid growth). At present, the data are too limited to critically evaluate these hypotheses. For example, apparently there are published relative growth rate values for only two parasitoid species (Thompson, 1982c, 1983~) and I have yet to find published relative consumption rate values for parasitoid larvae. Thus, it is not possible to compare adequately the quantitative performance of parasitoids with that of insects in other feeding guilds, although the limited data indicate relatively rapid growth of parasitoid larvae. Substantial technical difficulties involved in measuring consumption, metabolism and growth of parasitoid larvae within larval hosts that are also consuming food, metabolizing and growing have undoubtedly contributed to the lack of data (Slansky, 1978). Most of the efficiency values cited above were obtained from the relatively more easily studied situation of parasitoids feeding within non-feeding host pupae. The degree of “exploitation” of the host by parasitoid larvae can be calculated as the percentage of the host biomass consumed by the parasitoid, and as the percentage of host biomass converted to parasitoid biomass. Values for the former range from about 16 to 80% and for the latter from about 3 to 80% (Fisher, 1971; Rojas-Rousse and Kalmes, 1978; Slansky, 1978; Greenblatt et al., 1982). Most of these values are for pupal parasitoids, and thus using the biomass of unparasitized individuals to indicate the amount of host biomass potentially available to the parasitoid may be appropriate (i.e. there is probably little loss of pupal weight via respiration before the pupa is killed). However, because of the possibility of increased food utilization by parasitized larvae, it is not appropriate to use the biomass of unparasitized larvae in these calculations; instead, the amount of food assimilated by the parasitized host should be used to indicate the amount of food potentially available to the parasitoid. For example, it would appear that the braconid A. glomeratus converts about 77% of the dry weight of its larval host biomass to its own biomass (using the mean biomass of an unparasitized larva), whereas because of increased food consumption by parasitized larvae, it actually converts only about 35% of the food assimilated by its host to its own biomass (Slansky, 1978). Because of the scarcity of appropriately calculated values, whether gregarious parasitoids differ from solitary ones in their efficiency of host exploitation cannot at present be rigorously evaluated. However, Chlodny (1968) found that approx. 70% of a Pieris brassicae host pupa was consumed whether by a solitary larva of Pimpla instigator or by about 44 larvae of the gregarious Pteromalus puparum, suggesting relatively high exploitation efficiencies for solitary and gregarious parasitoids. Also, the data are too limited to determine whether specialized (monophagous) parasitoids tend to differ from more
Parasitoid nutritional ecology generalized (polyphagous) species in their efficiency of host exploitation. In one of the few studies avail-
able, Greenblatt et al. (1982) reported that the chalcid Brachymeria intermedia, a specialist on gypsy moth pupae, consumed from about 16 to 42% (depending on the host’s larval diet) of the nitrogen content of its host pupae whereas the more generalized ichneumonid Coccygomimus turionellae, which in nature does not attack gypsy moth pupae, consumed from about 62 to 80% of the nitrogen content of gypsy
moth pupae in the laboratory. CONCLUSION
Given the goal of understanding parasitoid-host interactions, it is evident that we must consider the nutritional ecology of parasitoids and their hosts. As indicated here, and in the other papers published in this issue, considerable data on parasitoid-host interactions are available, and we are clearly making progress toward the above stated goal. Some of this work is relevant to the use of parasitoids in biological control of insect pests. For example, the extent to which food consumption by parasitized hosts is altered will influence crop damage; solitary parasitoids that kill the host in an earlier instar may be preferred to gregarious parasitoids that allow the host to complete more of its development and perhaps even increase the amount of food consumed by the host. The influence of crop varieties exhibiting various degrees of resistance to insect pests on the suitability of these pests to their parasitoids should also be considered in herbivore pest management strategies (Campbell and Duffey, 1979; Hare, 1983; see also Hogarth and Diamond, 1984). In spite of some 70 years of quantitative studies (e.g. Tower, 1916) on parasitoid biology, however, we remain a long way from achieving the goal of understanding parasitoid-host interactions. As indicated here, there are many significant questions that cannot at present be answered because of lack of data. To what extent are the changes in physiology and behaviour of parasitized hosts due to active control by the parasitoids rather than to their mere presence and consumption of host tissue? What are the relative consumption, metabolic, and growth rates of parasitoid larvae, and how are these influenced by host age, food consumed by the host, parasitoid density, degree of parasitoid dietary specialization, and other factors? How does the ability of parasitoid larvae to survive to produce reproductively competent adults at reduced body sizes compare with other insects (Angelo and Slansky, 1984), and in particular, how do primary parasitoids compare in this regard with hyperparasitoids, in which individuals of the same species may be secondary, tertiary, or quarternary parasitoids (Kfir and Rosen, 1981a; 1981b; 1981c)? These are just a few of the many questions that remain unanswered. Development and use of artificial diets for parasitoids (Mellini, 1975; Thompson, 1981) is overcoming some of the technical difficulties of studying parasitoid nutrition and food utilization. Detailed studies on growth of parasitoids in vitro and in vivo, as carried out by Thompson and by Sato and colleagues are highly desirable. Most essential are studI.P. 32,4-B
259
ies in which various aspects of the host are manipulated by the experimenter and effects on performance of parasitoids are recorded. .The parasitized host starvation experiments and anti-juvenile hormoneinjection studies performed by Beckage and Riddiford, research on the impact of host diet on host quality and performance and subsequent parasitoid performance as carried out by Thompson and by Barbosa and colleagues, and Thompson’s in vitro dietary manipulation experiments, should serve as model studies for researchers in parasitoid-host interactions. It is only through such manipulation experiments that we will be able to evaluate hypotheses that allow us to advance beyond suggestive correlations and interesting speculations to achieve a true understanding of parasitoid-host relationships. Acknowledgements-I thank Drs N. E. Beckage and S. N. Thompson for inviting me to contribute this paper, and Dr S. N. Thompson and two reviewers for their comments on an early draft of this paper. Florida Agricultural Experiment Station Journal Series No. 6136.
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Hare J. D. (1983) Manipulation of host suitability for herbivore pest management. In Variable Plants and Herbiuores in Natural and Managed Systems (Ed. by Denno R. F. and McClure M. S.), pp. 655685. Academic Press, New York. Hogarth W. L. and Diamond P. (1984) Interspecific competition in larvae between entomophagous parasitoids. Am. Nat. 124, 552-560. Johansson A. S. (1950) Studies on the relation between Apanteles glomeratus L. (Hym., Braconidae) and Pieris brassicae (Lepid., Pieridae). Norsk. ent. Tidssk. 8, 145-186.
Kahn M. A. A., Vinson S. B. and Mitlin N. (1976) Effect of the parasitoid, Cardiochiles nigriceps, on the nitrogen excretion of its host, Heliothis virescens. J. Insect Physiol. 22, 51-56.
Kfir R. and Rosen D. (1981a) Biology of the hyperparasite Cheiloneurusparalia (Walker) (Hymenoptera: Encyrtidae) reared on MicroterysJlavus (Howard) in brown soft scale. J. ent. Sot. sth Afr. 44, 131-139. Kfir R. and Rosen D. (1981b) Biology of the hyperparasite Marietta javensis (Howard) (Hymenoptera: Aphelinidae) reared on MicroterysfEavus (Howard) in brown soft scale. J. ent. Sot. sth. Afr. 44, 141-150. Kfir R. and Rosen D. (1981~) Biology of the hyperparasite Pachyneuron concolor (Forster) (Hymenoptera:. Pteromalidae) reared on MicroterysJlauus (Howard) in brown soft scale. J. ent. Sot. sth Afr. 44, 151-163.
Luck R. F., Podoler H. and Kfir R. (1982) Host selection and egg allocation behaviour by Aphytis melinus and A. lingnanensis: comparison of two facultatively gregarious parasitoids. Ecol. Em. 7, 397-408. Mellini E. (1975) Possibilita di allevamento di Insetti entomofagi parassiti su diete artificiali. Boll. 1st. ent. Univ. Bologna 32, 257-290.
Mellini E. (1983) L’ipotesi della dominazione ormonale, esercitata dagli ospiti sui parassitoidi, alla lute delle recenti scoperte nella endocrinologia degli insetti. Boll. 1st. ent. Univ. Bologna 38, 135-166.
Moore J. (1984) Altered behavioral responses in intermediate hosts-an acanthocephalan parasite strategy. Am. Nat. 123, 572-577.
Parker F. D. and Pinnell R. E. (1973) Effect of food consumption of the imported cabbageworm when parasitized by two species of Apanteles. Envir. Ent. 2,216219. Parkman P., Jones W. A. Jr and Turnipseed S. G. (1983) Biology of Pediobius sp. near Facialis (Hymenoptera: Eulophidae), an imported pupal parasitoid of Pseudoplusia includens and Trichoplusia ni (Lepidoptera: Noctuidae). Envir. Ent. 12, 1669-1672. Pierce N. E. and Mead P. S. (1981) Parasitoids as selective agents in the symbiosis between lycaenid butterfly larvae and ants. Science 211, 1185-1187. Price P. W. (1972) Parasitoids utilizing the same host: adaptive nature of differences in size and form. Ecology 53, 19&195. Price P. W., Bouton C. E., Gross P., McPheron B. A., Thompson J. N. and Weis A. E. (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Ann. Rev. Ecol. Syst. 11, 41-65. Ratcliffe N. A., Leonard C. and Rowley A. F. (1984) Prophenoloxidase activation: nonself recognition and cell cooperation in insect immunity. Science 226, 557-559. Rojas-Rousse D. and Kalmes R. (1978) The development of male Diadromus pulchellus (Hymenoptera: Ichneumonidae) in the pupae of Acrolepiopsis assectella (Lepidoptera: Plutellidae): comparison of assimilation and energy losses under two temperature regimes. Envir. Ent. I, 469481.
Sato Y. (1980) Experimental studies on parasitization by Apanteles glomeratus V. Relationships between growth rate of parasitoid and host age at the time of oviposition. Entomophaga 25, 123-128.
Sato Y. and Tanaka T. (1984) Effect of the number of parasitoid (Apanteles kariyai) eggs (Hym.: Braconidae) on the growth of host (Leucania separata) larvae (Len.: Noctuidae). Entomophaga 29, 21-28. _ Shahiahan M. (1968) Suveroarasitization of the southern green stink bug by the-tadhinid parasite Tricopoda pennipes pilipes and its effect on the host and parasite survival. J. econ. Ent. 61, 1088-1091. Shapiro A. M. (1976) Beau geste? Am. Nat. 110, 900-902. Slansky F. Jr (1978) Utilization of energy and nitrogen by larvae of the imported cabbageworm, Pieris rapae, as affected by parasitism by Apanteles glomeratus. Envir. Ent. 7, 1799185. Slansky F. Jr (1982) Toward a nutritional ecology of insects. In Proc. 5th Int. Symp. Insect-Plant Relationships (Ed. by Visser J. H. and Minks A. K.), __ pp. 253-259. Pudoc, Wageningen. Slansky F. Jr and Scriber J. M. (1985) Food consumption and utilization. In Comprehensive Insect Physiology,- Biochemistry and Pharmacology (Ed. by Kerkut G. A. and Gilbert L. I.), Vol. 4, pp. 87-163. Pergamon Press, Oxford. Smilowitz Z. and Iwantsch G. F. (1973) Relationships between the parasitoid Hyposoter exiguae and the cabbage looper, Trichoplusia ni: effects of host age on developmental rate of the parasitoid. Envir. Ent. 2, 759-763.
Parasitoid nutritional ecology Smith C. L. and Smilowitz Z. (1976) Growth and development of Pieris rapae larvae parasitized by Apanteles glomeratus. Entomologia exp. appl. 19, 189-195.
Stamp N. E. (1981) Behavior of parasitized aposematic caterpillars: advantages to the parasitoid or the host? Am. Nat. 118, 715-725.
Stamp N. E. (1984) Interactions of parasitoids and checkerspot caterpillars Euphydryas spp. (Nymphalidae). J. Res. Lepid. 23, 2-18.
Tagawa J., Sato Y. and Tanaka T. (1982) Developmental interactions between the army worm Leucania separata (Lep.: Noctuidae) and its parasite Apanteles rujicrus (Hvm.: Braconidae). Entomoohaga 27, 447454. Tauber M. J., Tauber C. A., Nechols J. R. and Obrycki J. J. (1983) Seasonal activity of parasitoids: control by external, internal and genetic factors. In Diapause and Life CycZe Strategies in insects (Ed. by Brown V. K. and Hodek I.), pp. 87-108. Dr W. Junk, The Hague. Thompson S. N. (1981) Effects of dietary carbohydrate and lipid on nutrition and metabolism of metazoan parasites with special reference to parasitic Hymenoptera. In Current Topics in Insect Endocrinology and Nutrition (Ed. by Bhaskaran G., Friedman S. and Rodriguez J. G.), pp. 215-252. Plenum Press, New York. Thompson S. N. (1982a) Immediate effects of parasitization by the insect parasite, Hyposoter exiguae on the nutritional vhvsiologv of its host. Trichoplusia ni. J. Parasit. 68,936-9-41.
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Thompson S. N. (1982b) Effects of parasitization by the insect parasite Hyposoter exiguae on the growth,
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development and physiology of its host Trichoplusia ni. Parasitology 84, 491-510. Thompson S. N. (1982c) Exeristes roborator: Quantitative determination of in vitro larval growth rates in synthetic media with different glucose concentrations. Bxp. Parasit. 54, 229-234.
Thompson S. N. (1983a) The nutritional physiology of Trichoplusia ni parasitized by the insect parasite, Hyposoter exiguae, and the effects of parallel-feeding. Parasitology 87, 15-28.
Thompson S. N. (1983b) Larval growth of the insect varasite Brachvmeria Iasus reared in vitro. J. Parasit. 69, 425-427. . Thompson S. N. (1983c) Brachymeria lasus: Effects of nutrient level on in vitro larval growth of a chalcid insect parasite. Exp. Parasit. 55, 312-319. Thomuson S. N. (1983d) Biochemical and vhvsioloaical \ effects of metazoan endoparasites on their host species. I
*
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Comp. Biochem. Physiol. 74B, 183-211.
Tower D. G. (1916) Comparative study of the amount of food eaten by parasitized and nonparasitized larvae of Cirphis unipuncta. J. agric. Res. 6, 455458.
Vinson S. B. and Barras D. J. (1970) Effects of the parasitoid, Cardiochiles nigriceps, on the growth, development, and tissues of Heliothis virescens. J. Insect Physiol. 16, 1329-1338. Vinson S. B. and Iwantsch G. F. (1980a) Host suitability for insect parasitoids. A. Rev. Ent. 25, 397419. Vinson S. B. and Iwantsch G. F. (1980b) Host regulation by insect parasitoids. Q. Rev. Biol. 55, 143-165.
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NUTRITIONAL ECOLOGY OF ENDOPARASITIC AND THEIR HOSTS: AN OVERVIEW
INSECTS
FRANK SLANSKY JR Department
of Entomology
and Nematology, Institute of Food and Agricultural Florida, Gainesville, FL 32611, U.S.A.
Sciences,
University
of
Abstract-The impact of insect endoparasites (parasitoids) on the physiology and behaviour of their hosts is reviewed within the context of the nutritional ecology of the parasitoids and their hosts. Alterations in the consumption, utilization and allocation of food by parasitized hosts are common, as are internal changes in their metabolic physiology. Gregarious parasitoid species frequently increase feeding by their host larvae whereas solitary parasitoid species often reduce feeding and growth of their hosts. Many parasitoid-associated changes in host physiology and behaviour are interpreted to be of adaptive significance to parasitoids. Substantial circumstantial evidence suggests, and a few direct tests of such adaptive significance indicate, that parasitoids alter their hosts in ways beneficial to their own fitness. However, most of the changes in parasitized hosts are of unknown cause and undocumented significance to the parasitoids. Several relevant hypotheses are presented, and these require extensive evaluation (often requiring novel experimental approaches) before a thorough understanding of parasitoid nutritional ecology is established. Key Word Index:
Nutritional
ecology,
nutritional
INTRODUCTION Insect hosts provide food and living space for larval parasitoids (endoparasitic insects) and sometimes food for the adult parasitoid. Parasitoids represent potentially fatal intrusions into their hosts’ bodies, and insects manifest various “anti-parasitoid” tactics. For example, living within its food or within a webbed “nest”, and association with ants, may reduce an insect’s exposure to parasitoids (Price et al., 1980; Atsatt, 1981; Pierce and Mead, 1981; Stamp, 1984). Active defensive responses against parasitoids occur at both behavioural and physiological levels, and include head-thrashing, rapid wiggling, extrusion of fluid droplets directed at the attacking female parasitoid, and encapsulation and other immune responses against non-self substances (Vinson and Iwantsch, 1980a; Ratcliffe et al., 1984; Stamp, 1984). These responses must be overcome for successful parasitism and successful development within the host. Other host behaviour (e.g. continued intake of nutrients) may be favourable to, and often necessary for, successful development of the parasitoid; these must be allowed to continue and perhaps be enhanced by actions of the parasitoid. Thus, dominating characteristics of the nutritional ecology (Slansky, 1982) of insect parasitoids, as well as noninsect endoparasites (Thompson, 1983d; Moore, 1984), involve overcoming host defences while often simultaneously minimizing stressful impact on their hosts and influencing host physiology and behaviour to apparently benefit themselves (Vinson and Iwantsch, 1980a; 1980b). Within this context, three key questions, closely interrelated, must be answered to advance our understanding of parasitoid nutritional ecology: (1) To what extent are the variety of parasitoidassociated alterations in host physiology and behaviour of benefit to the parasitoids? (2) To what extent 255
physiology,
insect parasitism,
insect parasitoids
are these alterations actively influenced by parasitoids? and (3) In those cases where parasitoids actively influence host activities, what are the mechanisms by which parasitoids exert such control? In the present paper, I present hypotheses and discuss published data related primarily to the apparent adaptive nature of parasitoid-associated alterations in host physiology and behaviour, especially those related to consumption and utilization of food. Mechanisms of parasitoid control of their hosts are reviewed elsewhere (Vinson and Iwantsch, 1980b; see also Beckage and Riddiford, 1983b).
IMPACT OF PARASITOIDS ON PERFORMANCE OF THEIR HOSTS Once an insect larva is successfully parasitized by an insect parasitoid, it will die before reproducing [insects parasitized as adults ,may continue to reproduce but at a reduced rate (Shahjahan, 196811. Aspects of the larval host’s post-parasitization performance may involve continued defensive responses and stress-induced alterations in physiology and behaviour (Vinson and Iwantsch, 1980a, 1980b; Thompson, 1983d). However, because the genetic fitness of a parasitoid within a host is directly dependent on host activities, natural selection will undoubtedly commonly result in evolution of parasitoid-influenced changes in host physiology and behaviour that improve the parasitoid’s fitness. In many cases this may involve active “take-over” of control of host activities by parasitoids with input from both adult and larval stages of the parasitoid contributing to such take-over (Vinson and Iwantsch, 1980b). For example, in one of the few experimental studies assessing the apparent adaptive nature of parasitoid-associated alterations in host behaviour, Stamp (1981; see also Fritz, 1982) demonstrated that
FRANK SLANSKY JR
256
the behaviour of aposematically-coloured larvae of the checkerspot butterfly Euphydryas phaeton when parasitized by Apanteles euphydryidis, in crawling up out of dense vegetation to more exposed sites, benefits the parasitoids within them by reducing hyperparasitism. In cases where behaviour of a parasitized host benefits survival of its kin (such as hypothesized by Shapiro, 1976), then such behaviour may be adaptive to the host. Empirical documentation of this phenomenon is, however, required, and behaviour of parasitized hosts is considered here from the viewpoint of parasitoid fitness. Nonetheless, it must be emphasized that although many parasitoidassociated changes in host physiology and behaviour can be interpreted as adaptive to the parasitoids, experimental determinations of such adaptive benefit are few. Assessing the extent of such adaptive benefit is a major challenge for improving our understanding of parasitoid nutritional ecology. Effects of parasitoids include substantial impact on the consumption and utilization of food by their hosts, whereas host developmental time seems to be less frequently affected (summarized in Slansky and Scriber, 1985). Internal changes in host metabolism underlying these more overt alterations also occur (see below). If alterations in host physiology and behaviour are relevant to parasitoid fitness, then the extent of parasitoid influence on a host’s consumption and utilization of food should reflect the nutritional content of the host relative to the nutritional demands of the parasitoid(s). If sufficient nutrients for complete parasitoid development are lacking, then continued feeding by the host will be permitted and perhaps stimulated above the unparasitized level by the parasitoid.
MINIMIZING
IMPACT
ON THE HOST
Development of parasitoids frequently spans several host instars, apparently because there is selection to attack early host instars even though these provide an inadequate supply of nutrients for the parasitoid to complete its development (see below). Early instar parasitoids avoid substantial damage to host tissues, thereby minimizing their impact on early host development. Disruption of select host tissues may occur, however, apparently serving to reduce uptake of haemolymph nutrients by the host (Fisher, 1971; Smith and Smilowitz, 1976; Couchman and King, 1979). Parasitoids might evolve to exert less impact on the behaviour of “social” (i.e. gregarious) host species compared with solitary ones, because host individuals of the former acting “differently” from their neighbours may be more conspicuous and suffer increased mortality compared with those of the latter (Fritz, 1982). Parasitoids of web-inhabitating insects, however, might regulate their hosts to spend more time within the confines of the web, under the assumption of reduced susceptibility to predation and hyperparasitism within the web. Unfortunately, data needed to evaluate these hypotheses are apparently lacking.
STIMULATORY
EFFECTS
In addition to prolonged parasitoid development through several host instars, further support for the hypothesis that hosts may initially provide an insufficient supply of nutrients for parasitoids comes from the increased feeding exhibited by some parasitized hosts (summarized in Slansky and Scriber, 1985). In most of the cases where the amount of food and/or rate of feeding by a parasitized host is greater than that of an unparasitized host, the parasitoid involved is gregarious. These results suggest that the nutritional demands imposed by the several individuals of a gregarious parasitoid are greater than those of a single individual of a solitary parasitoid (Smith and Smilowitz, 1976). Supportive of this difference in nutritional demands between solitary and gregarious parasitoids is the finding that, although attacking the same early host instars, larvae of the solitary parasitoid Apanteles rubecula emerge during the fourth instar of the host (Pieris rapae) whereas larvae of the gregarious A. glomeratus (with about 30 larvae/host larva; Slansky, 1978) do not emerge until later in the fifth host instar (during which P. rapae larvae consume over 85% of their total food intake; Parker and Pinnell, 1973). The necessity for parasitoid survival of feeding by the host was elegantly demonstrated by Beckage and Riddiford (1983a). When newly ecdysed final-instar Manduca sexta larvae parasitized by Apanteles congrega tus are starved, parasitoid emergence is prevented; the longer host larvae are allowed to feed prior to starvation, the greater is the percentage emergence of the parasitoids. Increased density of parasitoids/host may also increase host feeding, such as in the aphid Acyrthosiphon pisum when parasitized by two larvae of Aphid&s smithi compared with aphids containing only one parasitoid (Cloutier and Mackauer, 1979, 1980; see also Fiihrer, 1981). Number of parasitoids/host larva is positively correlated with net weight of host carcass in the armyworm Leucaniu separata (Tagawa et al., 1982; Sato and Tanaka, 1984) and the sphingid M. sexta (Beckage and Riddiford, 1983a), indicating greater food consumption and/or food utilization efficiencies for more heavily parasitized larvae. Such apparent parasitoid regulation of host behaviour may be rather precise. For example, dry weight of emerging adult A. glomeratus is unaffected by density of its larvae within the host over a range of 9-47 parasitoids/host larva, suggesting that compensatory increases in host feeding occur as parasitoid density increases. However, once some limit of parasitoid density is exceeded, their body weight and survival may decline (Fiihrer and Keja, 1976; Slansky, 1978; Tagawa et al., 1982; Beckage and Riddiford, 1983a).
INHIBITORY
EFFECTS
In contrast with gregarious species, solitary parasitoids frequently inhibit host behaviour, causing various degrees of host paralysis and reduction in its food consumption (and consequently decreasing its growth). In general, species of ichneumonid parasitoids reduce growth rate of their hosts to a greater extent than do braconid species, and growth rates
Parasitoid nutritional ecology
are more severely reduced in later host instars (Thompson, 1982b). Several hypotheses concerning the apparent adaptive significance of such effects to parasitoids can be proposed. For example, a paralyzed host may exhibit reduced defensive capabilities and also reduced tissue uptake of haemolymph nutrients, thereby providing a greater supply of nutrients for the parasitoid (Vinson and Iwantsch, 1980a, 1980b). In addition, because movement associated with feeding and other behaviour may increase susceptibility of an insect to predation, host paralysis may reduce the host’s and thus the associated parasitoid’s chance of being killed before the parasitoid completes its development (Price et al., 1980; Fritz, 1982). Also, it is known that allelochemicals consumed by host larvae may negatively affect parasitoid performance (Campbell and Duffey, 1979; Barbosa et al., 1982); reducing or stopping the consumption of food by its host may therefore reduce a parasitoid’s exposure to potentially toxic allelochemicals. Some parasitoids, however, sequester allelochemicals from their hosts; whether these chemicals protect the parasitoids against their own enemies has apparently not yet been demonstrated; Benn et al., 1979). Unfortunately, rigorous experimental tests of these hypotheses are scarce. INTERNAL
CHANGES
IN HOST METABOLISM
Underlying the more overt parasitoid-associated changes in host activities discussed above are a variety of internal changes. Nutrient composition of host haemolymph (e.g. amino acids, proteins, carbohydrates and osmolality) and fat body (e.g. glycogen) are often altered after parasitization, as are host hormones and metabolic rate (Vinson and Iwantsch, 198Oa, 1980b; El-Sufty and Fiihrer: 1981; Thompson, 1982b, 1983d). Efficiency of nitrogen utilization and excretion of nitrogenous compounds may also be altered in parasitized hosts (Kahn et al., 1976; Slansky, 1978). These changes are undoubtedly related in complex ways to the presence of the parasitoids. Some of these alterations in host metabolic physiology are induced by the ovipositing adult parasitoid in Hymenoptera (but not Diptera; Mellini, 1983) or during the parasitoid’s egg stage. Other changes occur during the larval stage of the parasitoid, perhaps being induced by the parasitoid through chemical secretions or selective destruction of host tissues, as well as through consumption of haemolymph nutrients. Unravelling the causes and consequences of these complex interactions will require novel experimental approaches. For example, Thompson (1982a, 1982b, 1983a) manipulated food intake of unparasitized Trichoplusia ni through dietary dilution such that their relative consumption rate was reduced to a level similar to that of larvae parasitized by Hyposoter exiguae. This allowed distinction of the more direct effects of H. exiguae on host metabolic physiology (e.g. increased rate of food assimilation and haemolymph and fat body nutrient levels) from those effects resulting from reduced food consumption associated with parasitization (e.g. reduced growth rate).
NUTRITIONAL CONSTRAINTS PARASITOIDS
257 ON
As indicated above, parasitoids may overcome potential nutrient constraints on their performance through prolonged development spanning several host instars, through stimulatory effects on the consumption and utilization of food by their hosts, and through influences on host metabolism. Other data can also be interpreted within the context of nutritional constraints on parasitoid growth, including the following: (a) Slower parasitoid growth in early compared with later host instars (Sato, 1980). Examples of apparently “accelerated” parasitoid development when eggs are laid in later host instars (Beckage and Riddiford, 1978; Brewer and King, 1980, 1981) may actually be evidence of constrained parasitoid development in early host instars (Vinson and Barras, 1970; Smilowitz and Iwantsch, 1973). A number of factors influence growth and development of parasitoids (Thompson,,l981, 1983b, 1983~; Tauber et al., 1983), but the extent to which parasitoid larvae adaptively alter their growth rate depending on host age is poorly known (Fisher, 1971; Smilowitz and Iwantsch, 1973; Sato, 1980). (b) Reduced weight of parasitoids when emerging from heavily parasitized hosts (Tagawa et al., 1982; Beckage and Riddiford, 1983a). These results suggest that there is a limit to the extent of parasitoid-induced stimulation in food consumption and food utilization efficiencies by the host (Fiihrer, 1981). Once this limit is exceeded, the parasitoids apparently deplete their supply of food and subsequently starve. If, at this time, they exceed the critical weight for pupation (Sato, 1980; Angelo and Slansky, 1984), then they may survive to produce smaller than usual sized adults. In some cases of increased parasitoid density, duration of the parasitoid larval period may be shortened (Brewer and King, 1980; Parkman et al., 1983), whereas in others it may be lengthened (Beckage and Riddiford, 1978). Negative impact of reduced body size on parasitoid fitness (e.g. because of reduced fecundity) should select for avoidance of superparasitism (i.e. multiple ovipositions in the same host) such as through evolution of host-marking by parasitoids and of lethal interactions among parasitoid larvae that serve to reduce the number of parasitoids/host (for review see Vinson and Iwantsch, 1980a). Potential host species could evolve odours that mimic parasitoid host-marking odours thereby deterring female parasitoids (Slansky, 1978). (c) Reduced weight of parasitoids feeding in smallsized non-feeding host stages (Arthur and Wylie, 1959; Rojas-Rousse and Kalmes, 1978; Charnov and Skinner, 1984). Parasitoids of the egg or pupal stage lack the opportunity for increasing intake of food by the host and thus if the weight of the host is less than that required by the parasitoid to achieve its ideal body weight, then the resulting adult parasitoid may have a reduced body weight. For example, the parasitoid wasp Brachymeria intermedia attains its greatest dry body weight in gypsy moth pupae from larvae reared on red oak, whereas its body weight is reduced 30% in the smaller pupae from larvae reared on white oak or red maple (Greenblatt and Barbosa, 1981).
258
FRANK SLANSKY JR
Differences in nutritional and allelochemical content of hosts may override the benefits of their increased weight to parasitoids, resulting in parasitoids whose body weight is below that predicted by host weight (Greenblatt and Barbosa, 1980, 1981; Barbosa et al., 1982). Ovipositing females of some parasitoids and their hyperparasitoids may assess host size and bias the sex ratio of the eggs they lay toward the smaller sized sex (usually males) in smaller hosts (Kfir and Rosen, 198la, 198lb, 1981~) as well as alter the number of eggs they lay per host (Luck et al., 1982; Charnov and Skinner, 1984). PARASITIZATION
OF EARLY-INSTAR
HOSTS
Given the necessity for parasitoids to persist within their hosts through several host instars (especially when parasitization occurs during early host instars), and given the reduced probability of the host surviving through several instars (Price, 1972; Vinson and Iwantsch, 1980a), why should parasitoids attack early-instar hosts? Possible reasons include: (a) Ease of locating the more numerous earlyinstar host larvae compared with later instars (Price, 1972). (b) Overcoming host defences. For example, larger oral droplets emitted by later-instar Pieris brassicae are sufficient to drown or repel attacking females of the braconid wasp A. glomeratus whereas those of early-instar larvae are less efficacious (Johansson, 1950). The fully tanned cuticle of fifthinstar larvae of M. sexta is impenetrable to the ovipositor of A. congregatus (Beckage and Riddiford, 1978). Successful emergence of various parasitoids is highest when parasitization is initiated in particular host instars, probably due to age-related changes in internal defences (Vinson and Iwantsch, 1980a, 1980b). (c) Success in aggressive competition. The first parasitoid to become established in a host is often able to kill subsequent invaders (Vinson and Iwantsch, 1980a; Kfir and Rosen, 1981b; Godwin and Odell, 1984). FOOD UTILIZATION EFFICIENCIES OF PARASITOIDS
Parasitoids are hypothesized to exhibit high food utilization efficiencies because they consume food of seemingly high nutritional quality, because of their presumed relative inactivity within the host, and because of possible selection for efficient utilization of a limited food supply (Slansky and Scriber, 1985). Data for some 15 species of parasitoids indicate that they exhibit high assimilation efficiencies (55-94%, x = 68%) but net growth efficiencies (indicating the conversion of assimilated food into parasitoid biomass) range from a few low to mostly moderate values (11-62%, X = 37%; summarized in Slansky and Scriber, 1985). The only nitrogen utilization efficiency values apparently available for parasitoids (for two hymenopterous pupal parasitoids) tend to lie toward the low end of the range of values for insects in general when parasitizing gypsy moth pupae but toward the high end of the range when parasitizing wax moth pupae (Greenblatt et al., 1982). Net growth efhciencies may not be exceptionally high because of several reasons, including selection
for rapid rather than efficient parasitoid growth, the commonly exhibited inverse relationship between assimilation efficiency and net growth efficiency, and high metabolic activity of parasitoid larvae (e.g. because of active amino acid anabolism and catabolism, high detoxication enzyme activity, or rapid growth). At present, the data are too limited to critically evaluate these hypotheses. For example, apparently there are published relative growth rate values for only two parasitoid species (Thompson, 1982c, 1983~) and I have yet to find published relative consumption rate values for parasitoid larvae. Thus, it is not possible to compare adequately the quantitative performance of parasitoids with that of insects in other feeding guilds, although the limited data indicate relatively rapid growth of parasitoid larvae. Substantial technical difficulties involved in measuring consumption, metabolism and growth of parasitoid larvae within larval hosts that are also consuming food, metabolizing and growing have undoubtedly contributed to the lack of data (Slansky, 1978). Most of the efficiency values cited above were obtained from the relatively more easily studied situation of parasitoids feeding within non-feeding host pupae. The degree of “exploitation” of the host by parasitoid larvae can be calculated as the percentage of the host biomass consumed by the parasitoid, and as the percentage of host biomass converted to parasitoid biomass. Values for the former range from about 16 to 80% and for the latter from about 3 to 80% (Fisher, 1971; Rojas-Rousse and Kalmes, 1978; Slansky, 1978; Greenblatt et al., 1982). Most of these values are for pupal parasitoids, and thus using the biomass of unparasitized individuals to indicate the amount of host biomass potentially available to the parasitoid may be appropriate (i.e. there is probably little loss of pupal weight via respiration before the pupa is killed). However, because of the possibility of increased food utilization by parasitized larvae, it is not appropriate to use the biomass of unparasitized larvae in these calculations; instead, the amount of food assimilated by the parasitized host should be used to indicate the amount of food potentially available to the parasitoid. For example, it would appear that the braconid A. glomeratus converts about 77% of the dry weight of its larval host biomass to its own biomass (using the mean biomass of an unparasitized larva), whereas because of increased food consumption by parasitized larvae, it actually converts only about 35% of the food assimilated by its host to its own biomass (Slansky, 1978). Because of the scarcity of appropriately calculated values, whether gregarious parasitoids differ from solitary ones in their efficiency of host exploitation cannot at present be rigorously evaluated. However, Chlodny (1968) found that approx. 70% of a Pieris brassicae host pupa was consumed whether by a solitary larva of Pimpla instigator or by about 44 larvae of the gregarious Pteromalus puparum, suggesting relatively high exploitation efficiencies for solitary and gregarious parasitoids. Also, the data are too limited to determine whether specialized (monophagous) parasitoids tend to differ from more
Parasitoid nutritional ecology generalized (polyphagous) species in their efficiency of host exploitation. In one of the few studies avail-
able, Greenblatt et al. (1982) reported that the chalcid Brachymeria intermedia, a specialist on gypsy moth pupae, consumed from about 16 to 42% (depending on the host’s larval diet) of the nitrogen content of its host pupae whereas the more generalized ichneumonid Coccygomimus turionellae, which in nature does not attack gypsy moth pupae, consumed from about 62 to 80% of the nitrogen content of gypsy
moth pupae in the laboratory. CONCLUSION
Given the goal of understanding parasitoid-host interactions, it is evident that we must consider the nutritional ecology of parasitoids and their hosts. As indicated here, and in the other papers published in this issue, considerable data on parasitoid-host interactions are available, and we are clearly making progress toward the above stated goal. Some of this work is relevant to the use of parasitoids in biological control of insect pests. For example, the extent to which food consumption by parasitized hosts is altered will influence crop damage; solitary parasitoids that kill the host in an earlier instar may be preferred to gregarious parasitoids that allow the host to complete more of its development and perhaps even increase the amount of food consumed by the host. The influence of crop varieties exhibiting various degrees of resistance to insect pests on the suitability of these pests to their parasitoids should also be considered in herbivore pest management strategies (Campbell and Duffey, 1979; Hare, 1983; see also Hogarth and Diamond, 1984). In spite of some 70 years of quantitative studies (e.g. Tower, 1916) on parasitoid biology, however, we remain a long way from achieving the goal of understanding parasitoid-host interactions. As indicated here, there are many significant questions that cannot at present be answered because of lack of data. To what extent are the changes in physiology and behaviour of parasitized hosts due to active control by the parasitoids rather than to their mere presence and consumption of host tissue? What are the relative consumption, metabolic, and growth rates of parasitoid larvae, and how are these influenced by host age, food consumed by the host, parasitoid density, degree of parasitoid dietary specialization, and other factors? How does the ability of parasitoid larvae to survive to produce reproductively competent adults at reduced body sizes compare with other insects (Angelo and Slansky, 1984), and in particular, how do primary parasitoids compare in this regard with hyperparasitoids, in which individuals of the same species may be secondary, tertiary, or quarternary parasitoids (Kfir and Rosen, 1981a; 1981b; 1981c)? These are just a few of the many questions that remain unanswered. Development and use of artificial diets for parasitoids (Mellini, 1975; Thompson, 1981) is overcoming some of the technical difficulties of studying parasitoid nutrition and food utilization. Detailed studies on growth of parasitoids in vitro and in vivo, as carried out by Thompson and by Sato and colleagues are highly desirable. Most essential are studI.P. 32,4-B
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ies in which various aspects of the host are manipulated by the experimenter and effects on performance of parasitoids are recorded. .The parasitized host starvation experiments and anti-juvenile hormoneinjection studies performed by Beckage and Riddiford, research on the impact of host diet on host quality and performance and subsequent parasitoid performance as carried out by Thompson and by Barbosa and colleagues, and Thompson’s in vitro dietary manipulation experiments, should serve as model studies for researchers in parasitoid-host interactions. It is only through such manipulation experiments that we will be able to evaluate hypotheses that allow us to advance beyond suggestive correlations and interesting speculations to achieve a true understanding of parasitoid-host relationships. Acknowledgements-I thank Drs N. E. Beckage and S. N. Thompson for inviting me to contribute this paper, and Dr S. N. Thompson and two reviewers for their comments on an early draft of this paper. Florida Agricultural Experiment Station Journal Series No. 6136.
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