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The potential for hyperparasitism to compromise biological control: Why don’t hyperparasitoids drive their primary parasitoid hosts extinct?
Biological Control 58 (2011) 167–173
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Perspective
The potential for hyperparasitism to compromise biological control: Why don’t hyperparasitoids drive their primary parasitoid hosts extinct? Shon S. Schooler a,⇑, Paul De Barro a, Anthony R. Ives b a b
CSIRO Ecosystem Sciences, Ecosciences Precinct, Brisbane, QLD, 4001, Australia Department of Zoology, University of Wisconsin, Madison, WI 53706, USA
a r t i c l e
i n f o
Article history: Received 21 March 2010 Accepted 27 May 2011 Available online 1 June 2011 Keywords: Biological control failure Population dynamics Establishment success Hyperparasitoid Predation Non-target effects
a b s t r a c t Predation or parasitism on species introduced as biological control agents is a common explanation for failure of biological control programs. Although there is clear evidence from some biological control programs that hyperparasitism can impact a parasitoid biological control agent, it is not clear whether hyperparasitoids have the potential to cause control failure. We performed glasshouse experiments using cages containing 48 plants to address whether the hyperparasitoid Asaphes suspensus can potentially eliminate a population of the primary parasitoid Aphidius ervi, a biological control agent of the pea aphid Acyrthosiphon pisum. Although As. suspensus has a low intrinsic rate of increase, only one-half that of A. ervi and one-third that of pea aphids, it was nonetheless capable of eliminating the A. ervi population within seven A. ervi generations. In contrast, in the absence of As. suspensus, A. ervi eliminated the pea aphid population. Field surveys, however, found that As. suspensus does not eliminate entire natural populations of A. ervi in lucerne crops, probably due to the high frequency of disturbance that favours high intrinsic rates of increase and short generation times. Nonetheless, the ability of As. suspensus to eliminate A. ervi in cages despite its low intrinsic rate of increase underscores the potential for hyperparasitism to disrupt biological control. Small populations are expected to be particularly susceptible to hyperparasitism, such as when releases of a new biological control agent are made. Crown Copyright Ó 2011 Published by Elsevier Inc. All rights reserved.
1. Introduction Classical biological programs select natural enemies from the native range of the target organism to control an introduced pest. The results of these introductions are often unpredictable, with some biological control agents exerting the desired level of control and others having little effect on target pest populations (Waterhouse and Sands, 2001). The three main reasons used to explain failure are climatic mismatches between the native and introduced range of the control agent (34.5%), predation or parasitism by native fauna on the control agent (20.3%), and lack of alternative hosts or food (16.9%) (Stiling, 1993). While climate is the most frequently cited cause for failure, it is also the one that can often be remedied (e.g., by releasing cold-tolerant populations of the biological control agent), whereas there is little that can be done to reduce the effects of native predators, parasitoids and hyperparasitoids (Stiling, 1993). Hyperparasitoids can be either obligate or facultative, and here we restrict our attention to obligate hyperparasitism. Furthermore, we do not consider heteronomous hyperparasitism in ⇑ Corresponding author. Address: CSIRO Ecosystem Sciences, EcoSciences Precinct, P.O. Box 2583, Brisbane, QLD 4001, Australia. Fax: +61 7 3833 5504. E-mail address: [email protected] (S.S. Schooler).
which female offspring develop as primary parasitoids and male offspring develop as hyperparasitoids. Parasitism and hyperparasitism may inhibit biological control programs targeting both invasive plants and insects. This is supported primarily by theoretical models (Beddington and Hammond, 1977; May and Hassell, 1981), although there are a small number of empirical case studies. For example, five species of native hymenopterous parasitoids were found to parasitise the tephritid gall fly, Procecidochares utilis Stone, that was introduced to control the weed Ageratina adenophorum (Spreng.) in Hawaii, and parasitism rates often exceeded 50% (Bess and Haramoto, 1959). An example of a negative effect in insect biological control caused by hyperparasitism is the control of the citrus psyllid (Diaphorina citri Kuwayama). In the native range of the psyllid, two parasitoids of the psyllid (Tamarixia radiata (Waterston) and Diaphorencyrtus aligarhensis (Shafee, Alam, and Agarwal)) are heavily hyperparasitised (up to 40%), whereas in introduced regions, where the hyperparasitoids are absent, the parasitoids provide good control (Waterhouse, 1998). Similarly, the Yugoslavian strain of Cotesia rubecula (Marshall) after initially establishing in Virginia in 1987 suffered an increase in hyperparasitism from an average of 37.9% in 1987 to a peak of 100% in August 1988; this was linked to the failure to recover the parasitoid in subsequent years (McDonald and Kok, 1991).
1049-9644/$ - see front matter Crown Copyright Ó 2011 Published by Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2011.05.018
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A review of hyperparasitism found several studies where hyperparasitism on a biological control agent reduced its efficacy in insect biological control programs, although no effect was found in other studies (Sullivan and Völkl, 1999). Other research suggests that, although hyperparasitism or predation rates on control agents may be high, it is the foraging behaviour of the biological control agents that primarily limits their effectiveness (Mackauer and Völkl, 1993). Mackauer and Völkl (1993) argue that the impact of hyperparasitoids is limited as a consequence of their relatively low lifetime fecundity and the limited storage capacity of their ovaries. Researchers in biological control have identified traits that are favourable for success of biological control agents. In particular, both ecological theory (Waage and Hassell, 1982; Murdoch, 1990) and biological control practice (Doutt and DeBach, 1964; Huffaker et al., 1977; Stiling, 1993) suggest that biological control agents with high intrinsic rates of increase are more likely to be effective. By the same logic, we might expect that hyperparasitoids with high intrinsic rates of increase relative to the control agent pose a greater threat to biological control. However, many hyperparasitoids have relatively low intrinsic rates of increase compared to the primary parasitoids that are often selected for control programs. This may contribute to the apparently few examples of hyperparasitoids compromising control programs using primary parasitoids. The evidence used to determine whether hyperparasitism can disrupt biological control programs generally consists of field assessments of hyperparasitism rates (e.g. McDonald and Kok, 1991). However, relatively few studies of post-release monitoring give sufficiently detailed information to quantify the impacts of hyperparasitism. Furthermore, hyperparasitism may be important when control agent populations are small and therefore difficult to assess, or hyperparasitism may be episodic yet still have a large impact on biological control success. Here, we take an alternative approach by conducting longterm population studies in a glasshouse to determine the potential impact of the hyperparasitoid Asaphes suspensus (Nees) (Pteromalidae: Asaphinae) on the primary parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae), a biological control agent of pea aphids (Acyrthosiphon pisum (Harris), Homoptera: Aphidae). To our knowledge, this is the only experimental cage study that examines the multi-generation population dynamics of a four trophic level insect system (plants, aphids, parasitoids and hyperparasitoids). While our study is not a substitute for detailed field assessments, it nonetheless addresses whether the hyperparasitoid has the biological capacity to disrupt biological control. The intrinsic rate of increase for As. suspensus is roughly half that of A. ervi, which by itself suggests that As. suspensus should not disrupt biological control by A. ervi. To compare with the glasshouse study, we also present detailed field assessments of hyperparasitism on A. ervi in lucerne crops over the course of a summer in Wisconsin, USA. 2. Methods 2.1. Study system The study system comprised four trophic levels; lucerne (Medicago sativa L., Fabaceae), the pea aphid (A. pisum), a parasitoid wasp (A. ervi), and a hyperparasitoid wasp (As. suspensus). Lucerne (alfalfa) is cultivated worldwide as a forage crop. The pea aphid is originally an Old World species that was accidentally introduced into North America in the 19th century (Hagen et al., 1976; Mackauer and Kambhampati, 1986). It feeds on a variety of legume crops. During the summer, reproduction is asexual (Blackman and Eastop, 1984). The parthenogenic females produce
as many as five nymphs per day, and nymphs go through four subadult instars (Hutchinson and Hogg, 1984, 1985; Thiboldeaux, 1986). The intrinsic rate of increase has been measured in a number of studies that give values between 0.241 (Siddiqui et al., 1973) and 0.562 (Hutchinson and Hogg, 1985) (depending on protocols and temperature). Sequiera and Mackauer (1988) report a value of 0.485, and we highlight this value because studies from the same lab have also measured the intrinsic rates of increase of A. ervi and As. suspensus. Pea aphids are attacked by A. ervi, which was introduced into the USA as a biocontrol agent in the 1960s and has now spread over much of North America (Gonzalez et al., 1978; Mackauer and Kambhampati, 1986; Thiboldeaux et al., 1987). A. ervi parasitises an aphid by laying a single egg through its exoskeleton (Stary, 1988), and the larva develops in the aphid, with a mummy forming in 6–10 days (Thiboldeaux, 1986). Larvae pupate within the mummy and emerge in 5–7 days. A. ervi principally attacks 2nd and 3rd instar aphids (Ives et al., 1999). While A. ervi attacks several genera of aphids (Stary, 1974; Mackauer and Finlayson, 1967), in Wisconsin, USA, the numerically most common host is the pea aphid (Thiboldeaux et al., 1987). Sequiera and Mackauer (1994) report its intrinsic rate of increase as 0.380. As. suspensus is a pupal hyperparasitoid that drills a hole in the aphid mummy with its ovipositor, injects venom into the immature parasitoid, and lays a single egg on the host’s ventral surface. The emergence time is approximately 16 days, the adult life span is approximately 14 days (Schooler et al., 1996), and females have a low average lifetime fecundity of 54 (Spencer, 1926). The reported host range of As. suspensus includes more than six genera of braconid parasitoids of aphids (Gibson and Vikberg, 1998), although A. ervi is likely its most common host in agricultural systems in temperate North America. As. suspensus has an intrinsic rate of increase of 0.172 (Mackauer and Völkl, 1993). 2.2. Glasshouse experiments The experiments took place in a glasshouse within two identical 75 150 50 cm cage arenas. The top and the two short sides consisted of a polyester screen while the long sides were composed of clear Mylar. The cages contained 48 lucerne plants. Pots 13 13 cm square and containing single plants (10–32 cm in ht.) were placed entirely within the cages. A plastic dish was placed around the base of each plant and the sides of the dish were coated with fluon, a slippery compound that prevents the aphids from leaving the dish. The glasshouse was environmentally controlled and supplemental light was provided by two 400 W high-pressure sodium bulbs suspended 1.5 m above the floor of the arena to produce a 16:8 L:D cycle. The two replicates took place sequentially, from 14 November 1994 to 25 February 1995 and from 17 April 1995 to 18 July 1995. The experiments were initiated by inoculating eight plants with four adult pea aphids (day 0). Five fertile female A. ervi adults were then added to each cage on days 7, 9, and 11, and four female adults were added on day 13. For the first experimental replicate, three fertile As. suspensus adult females were released in a randomly selected cage on day 14 (south cage, 28 November 1994) and during the sequential replicate three fertile As. suspensus adult females were released in the alternate cage (north cage, 6 May 1995) on day 22. Prior to introduction, females of A. ervi or As. suspensus were determined to be fertile by observing whether they oviposited into aphids or mummies, respectively. Every second day, measurements were made in each cage (number of aphids and number of mummies). In addition, plants were randomly assigned to eight groups (six per group) and mummies were collected from one of these groups, in sequential rotation, every two days. Mummies were then placed in covered Petri dishes and
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enclosed larvae were reared to adult in order to determine percent hyperparasitism. Plant condition was also examined and lucerne plants were replaced as they died. When plants were replaced, any remaining mummies were removed and placed back into the experimental cages. 2.3. Field surveys Surveys were conducted in two lucerne fields during 1998 at the University of Wisconsin Arlington Field Station, Arlington, Wisconsin. Twice per week at four (12 May–25 June) or two (29 June–1 September) stations in each field, 400 lucerne stems were sampled and all pea aphids and A. ervi mummies were counted (1600 or 800 total stems per field). Mummies were also collected in separate sampling, with numbers ranging from 2 to 386 depending on mummy densities in the field. Mummies were returned to the lab and allowed to emerge, with the emerging wasp identified as A. ervi or one of three hyperparasitoids: As. suspensus, Dendrocerus carpenteri (Curtis), or Pachyneuron altiscutum Cook. Not all mummies emerged, and therefore we report the percentage hyperparasitism determined by the numbers of emerging A. ervi and hyperparasitoids. One of the fields was established in 1997, whereas the other was planted in the spring of 1998. The previously established field was harvested in May, late June, and early August; the newly
A
planted field was harvested in late June and early August. For 1–2 weeks following harvesting (depending on the rate of lucerne regrowth), the sampling procedure described above could not be implemented, because plants were cut to stubble. Although we did not count aphids and mummies until lucerne regrowth reached roughly 10 cm, we did attempt to collect mummies for rearing and determination of percentage hyperparasitism. These data are part of a larger survey including records of aphid predators that was previously used in analyses of the importance of A. ervi parasitism and predation on pea aphid dynamics (Rauwald and Ives, 2001; Gross et al., 2005). 3. Results 3.1. Glasshouse cage studies When confined in glasshouse cages, hyperparasitoids had a large impact on the primary parasitoid, causing a breakdown in the ability of the primary parasitoid to suppress aphid densities. In the absence of the hyperparasitoid As. suspensus, aphid populations initially increased to high densities (max 965 and 2457 individuals in replicate 1 and 2, respectively) and thereafter the abundance of aphids declined to 0 and 211 aphids (Fig. 1A and 2A) at the end of the experiment. This reduction in hosts led to a reduction in parasitoids, from a maximum of 256 and 347 to 23
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Date Fig. 1. Results from the first cage experiment presenting the populations of aphids (A. pisum) and parasitoids (A. ervi) (total number of aphids and mummies in each cage) in a cage A) without and B) with hyperparasitoids (As. suspensus). Percent hyperparasitism is the number of As. suspensus relative to the number of parasitoids (number of As. suspensus divided by number of A. ervi plus As. suspensus) that later emerged from mummies collected from a subset of plants on a given date.
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Date Fig. 2. Results from the second cage experiment presenting the populations of aphids and parasitoids (A. ervi) (total number of aphids and mummies in each cage) in a cage (A) without and (B) with hyperparasitoids (As. suspensus). Percent hyperparasitism is the number of As. suspensus relative to the number of parasitoids (number of As. suspensus divided by number of A. ervi plus As. suspensus) that later emerged from mummies collected from a subset of plants on a given date.
and 160 mummies in cages one and two, respectively. In the presence of As. suspensus, mummies declined from a maximum of 340 to 19 (Fig. 1B) and 249 to 24 mummies (Fig. 2B). In contrast to the cages without hyperparasitoids, however, aphid densities remained high, with 1149 and 828 individuals at the end of the experiment in replicates one and two, respectively. Therefore, the decline in primary parasitoid mummies was not due to a decline in aphid numbers but instead was due to hyperparasitism. In both experiments, hyperparasitism reached 100% before the end of the experiment. 3.2. Field surveys In field surveys conducted in 1998, hyperparasitism generally increased through time as pea aphid and A. ervi mummy densities increased in fields up to the time of harvesting (Figs. 3 and 4). Percentage hyperparasitism often reached 20–40% by the time of harvesting, and hyperparasitism was sometimes even higher among those mummies found immediately following harvesting and before regular sampling of aphids and mummies could resume. The pattern for overall hyperparasitism was also shown for hyperparasitism by As. suspensus. Hyperparasitism showed a marked contrast with the pattern of A. ervi parasitism; in most harvesting cycles the increase in the number of mummies parallels the increase in the number of aphids (Figs. 3 and 4), and a detailed
analysis showed that percentage parasitism by A. ervi does not increase as aphid density increases over a harvesting cycle (Gross et al., 2005). 4. Discussion In this study we demonstrate the ability of the hyperparasitoid As. suspensus, under glasshouse conditions, to quickly drive the primary parasitoid A. ervi extinct. This time to extinction was roughly the same as the time to extinction of pea aphids caused by A. ervi when As. suspensus was absent. Why is there such a dramatic effect of As. suspensus on A. ervi populations, and what implication does this hold for biological control programs? The effect of hyperparasitism is amplified in cages in which A. ervi experiences mortality from two directions; directly from parasitism by As. suspensus and indirectly from the mortality of aphids that are carrying A. ervi larvae. The indirect mortality increases as the aphids approach the carrying capacity of the system. In the cage populations, A. ervi reaches high density quickly, at which point the per capita population growth rate becomes zero. Therefore, A. ervi cannot attain its intrinsic rate of increase. To eliminate A. ervi, As. suspensus only needs to maintain a per capita population growth rate exceeding zero. In this situation the potential A. ervi advantage in having a higher intrinsic rate of increase than As. suspensus is deceptive. Because
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populations are confined to a cage in which plants are replaced to maintain a relatively stable environment, populations of A. ervi approach their carrying capacity rapidly, at which point their population cannot out-grow the increasing hyperparasitoid population despite their higher intrinsic rate of increase. In contrast to the glasshouse experiments, the field data show that hyperparasitoids do not eliminate A. ervi. Although hyperparasitism rates are low when aphid and A. ervi populations begin to recover following harvesting, hyperparasitism rates reach 20–40% during the harvesting cycle. This demonstrates the densitydependent pattern that as A. ervi populations increase, the percent mortality caused by hyperparasitism also increases, and this may limit the ability of A. ervi to maintain pressure on out-breaking pea aphid populations. Arguing from the glasshouse experiments in which we experimentally removed disturbances, A. ervi populations in the field are only saved by disturbance events; e.g. crop harvesting. We found that disturbance events in field cropping systems decreased the ability of the hyperparasitoid to eliminate populations of the parasitoid species, whereas in the absence of disturbance, in laboratory mesocosms, presence of the hyperparasitoid caused extinction of the parasitoid. Although previous studies have not specifically examined the factors that facilitate coexistence in hyperparasitoid–parasitoid interactions, there is a rich literature on factors that promote coexistence in predator–prey systems. For example, a classic laboratory experiment by Huffaker (1958) found that complexity of the underlying resource (arrangement of oranges) facilitated long-term coexistence of herbivore (sixspotted mite: Eotetranuchus sexmaculatus) and predator (predatory mite: Typhlodromus occidentalis) populations. The effect of planthost complexity has also been demonstrated in a field experiment
where foraging efficiency of an ichneumonid parasitoid (Diadegma semiclausum) on the diamondback moth (Plutella xylostella) was reduced under more complex plant arrangements, which led to increased stability of parasitoid populations (Gols et al., 2005). In addition, complexity of herbivore communities (diversity of herbivore host species) can also promote stability of parasitoid populations (Vos et al., 2001). By extension, a possible explanation why hyperparasitoids do not cause the extinction of parasitoid populations in natural and cropping systems is habitat and host complexity. In general, even though obligate hyperparasitoids, or predators of biological control agents, may have low intrinsic rates of increase, they may still have the capacity to disrupt biological control. Theoretical studies that have explicitly addressed the impacts of hyperparasitism in biological control have generally considered only the case in which pests, control agents, and hyperparasitoids coexist at a stable equilibrium (e.g., Beddington and Hammond, 1977; May and Hassell, 1981); in this case, these studies show that high intrinsic rates of the hyperparasitoid are not needed to disrupt biological control. We know of no theoretical study of the effects of hyperparasitism in disturbed environments. Nonetheless, Schellhorn et al. (2002) compare the impacts of two primary parasitoids that differ in intrinsic rates of increase in disturbed and undisturbed environments, demonstrating that disturbance favours the primary parasitoid with the higher intrinsic rate of increase. Arguing from this, but at the hyperparasitism trophic level, disturbance should accentuate the importance of a hyperparasitoid’s intrinsic rate of increase for its ability to disrupt biological control. While the impact of hyperparasitoids on biological control success is seldom reported, the threat is implicitly considered in
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regards to the accidental introduction of hyperparasitoids along with the candidate agents. Prevention of accidental importation of hyperparasitoids is one of the reasons it is recommended that agents being imported for control are passed through at least one generation in quarantine. However, consideration of species as candidate biological control agents usually takes into account (a) potential efficacy and (b) potential for non-target attack, but there is little evidence to suggest that practitioners consider the threat to efficacy posed by hyperparasitoids already present in the recipient location. As McDonald and Kok (1991) showed, hyperparasitoids that are already present may have a marked negative influence on the capacity to establish and persist, and so may contribute to failure. Investigating the potential for resident hyperparasitoids to cause biological control failure, and considering this potential in the selection of candidate control agents, may lead to greater success of some biological control programs. In selecting candidate biological control agents, a second factor to consider is indirect non-target affects. The addition of a new species that is susceptible to attack by hyperparasitoids already present may result in an increase in the availability of food resources and so lead to an increase in hyperparasitoid abundance. In a review of indirect interactions in aphid–parasitoid communities, there was no mention of this type of interaction (Muller and Godfray, 1999). However, as some hyperparasitoids have more than one host, the question needs to be asked as to whether this increase in local abundance could result in increased hyperparasitism of non-target parasitoid species, thereby reducing the efficacy of these species resulting in disruption of control. Our glasshouse experiment shows that a hyperparasitoid with a low intrinsic rate of increase is nonetheless capable of locally
eliminating a biological control agent. While this does not occur in the field, it raises concern about the outcome of control agent releases at the initial stages of a control program, when control agent populations are small (sensu McDonald and Kok, 1991). Furthermore, we believe that the initial assumption should be that hyperparasitoids have the potential to disrupt biological control, and starting from this assumption, biological control practitioners should ask what factors might allow biological control agents to suppress pests despite this potential. A central question in basic ecological studies is why don’t predators drive their prey species locally extinct. We believe that the same question should be asked for biological control programs: why don’t hyperparasitoids drive their primary parasitoid hosts extinct? Acknowledgments Vic Jager and Arin Davis assisted in the glasshouse experiments and Kevin Gross led the field survey. We thank O. Edwards, J. Brodeur, and one anonymous reviewer for their constructive comments. S. Schooler was supported by a Holstrom Environmental Scholarship. References Blackman, R.L., Eastop, V.F., 1984. Aphids on the world’s crops: an identification and information guide. John Wiley & Sons, New York. Beddington, J.R., Hammond, P.S., 1977. On the dynamics of host–parasitehyperparasite interactions. Journal of Animal Ecology 46, 811–821. Bess, H.A., Haramoto, F.H., 1959. Biological control of pamakani, Eupatorium adenophorum, in Hawaii by a tephritid fly, Procecidochares utilis. Ecology 40, 244–249.
S.S. Schooler et al. / Biological Control 58 (2011) 167–173 Doutt, R.L., DeBach, P., 1964. Some biological control concepts and questions. In: DeBach, P. (Ed.), Biological control of insect pests and weeds. Van Nostrand, Princeton, NJ, pp. 118–142. Gibson, G.A.P., Vikberg, V., 1998. The species of Asaphes Walker from America north of Mexico, with remarks on extralimital distributions and taxa (Hymenoptera: Calcidoidea, Pteromalidae). Journal of Hymenoptera Research 7, 209–256. Gols, R., Bukovinszky, T., Hemerik, L., Harvey, J.A., Van Lenteren, J.C., Vet, L.E.M., 2005. Reduced foraging efficiency of a parasitoid under habitat complexity: implications for population stability and species coexistence. Journal of Animal Ecology 74, 1059–1068. Gonzalez, D., White, W., Hall, J., Dickson, R.C., 1978. Geographical distribution of Aphidiidae (Hym.) imported to California for biological control of Acyrthosiphon kondoi and Acyrthosiphon pisum (Hom: Aphididae). Entomophaga 23, 239–248. Gross, K., Ives, A.R., Nordheim, E.V., 2005. Estimating fluctuating vital rates from time-series data: A case study of aphid biocontrol. Ecology 86, 740–752. Hagen, K.S., Viktrorov, G.A., Yasumatsu, K., Schuster, M.F., 1976. Biological control of pests of range, forage, and grain crops. In: Huffaker, C.B., Messenger, P.S. (Eds.), Theory and Practice of Biological Control. Academic Press, New York, pp. 397– 442. Huffaker, C.B., 1958. Experimental studies on predation: Dispersion factors and predator-prey oscillations. Hilgardia 27, 343–383. Huffaker, C.B., Luck, R.F., Messenger, P.S., 1977. The ecological basis of biological control. In: Proceedings of the 15th International Congress of Entomology 19– 27 August 1976. Washington, DC, pp. 560–586. Hutchinson, W.D., Hogg, D.B., 1984. Demographic statistics for the pea aphid (Homoptera: Aphididae) in Wisconsin and a comparison with other populations. Environmental Entomology 13, 1173–1181. Hutchinson, W.D., Hogg, D.B., 1985. Time-specific life tables for the pea aphid, Acyrthosiphon pisum (Harris), on alfalfa. Researches on Population Ecology 27, 231–253. Ives, A.R., Schooler, S.S., Jagar, V.J., Knuteson, S.E., Grbic, M., Settle, W.H., 1999. Variability and parasitoid foraging efficiency: a case study of pea aphids and Aphidius ervi. American Naturalist 154, 652–673. McDonald, R.C., Kok, L.T., 1991. Hyperparasites attacking Cotesia glomerata (L.) and Cotesia rubecula (Marshall) (Hymenoptera: Braconidae) in Southwestern Virginia. Biological Control 1, 170–175. Mackauer, M., Finlayson, T., 1967. The hymenopterous parasites (Hymenoptera: Aphidiidae and Aphelinidae) of the pea aphid in eastern North America. Canadian Entomologist 99, 1051–1082. Mackauer, M., Kambhampati, S., 1986. Structural changes in the parasite guild attacking the pea aphid in North America. In: Hodek, I. (Ed.), Ecology of Aphidophaga. Academia, Prague, pp. 347–356. Mackauer, M., Völkl, W., 1993. Regulation of aphid populations by aphidiid wasps: does parasitoid foraging behaviour or hyperparasitism limit impact? Oecologia 94, 339–350. May, R.M., Hassell, M.P., 1981. The dynamics of multiparasitoid-host interactions. American Naturalist 117, 234–261. Muller, C.B., Godfray, H.C.J., 1999. Indirect interactions in aphid-parasitoid communities. Researches in Population Ecology 41, 93–106.
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Murdoch, W.W., 1990. The relevance of pest-enemy models to biological control. In: Mackauer, M., Ehler, L.E., Roland, J. (Eds.), Critical Issues in Biological Control. Intercept, Andover, Hants, UK, pp. 1–24. Rauwald, K.S., Ives, A.R., 2001. Biological control in disturbed agricultural systems and the rapid recovery of parasitoid populations. Ecological Applications 11, 1224–1234. Schellhorn, N.A., Kuhman, T.R., Olson, A.C., Ives, A.R., 2002. Competition between native and introduced parasitoids of aphids: Nontarget effects and biological control. Ecology 83, 2745–2757. Schooler, S.S., Ives, A.R., Harmon, J., 1996. Hyperparasitoid aggregation to variation in Aphidius ervi host density at three spatial scales. Ecological Entomology 21, 249–458. Sequeria, R., Mackauer, M., 1988. Effects of parasitism by Praon pequodorum on agespecific fecundity and population growth of the pea aphid, Acyrthosiphon pisum. Entomologia Experimentalis et Applicata 48, 179–185. Sequeria, R., Mackauer, M., 1994. Variation in selected life history parameters of the parasitoid wasp, Aphidius ervi: influence of host developmental stage. Entomologia Experimentalis et Applicata 71, 15–22. Siddiqui, W.H., Barlow, C.A., Randolph, P.A., 1973. Effects of some constant and alternating temperatures on populations growth of the pea aphid. Acyrthosiphum pisum (Homoptera: Aphididae) Canadian Entomologist 105, 145–156. Spencer, H., 1926. Biology of the parasites and hyperparasites of aphids. Annals of the Entomological Society of America 19, 119–157. Stary, P., 1974. Taxonomy, origin, and host range of Aphidius species (Hym., Aphidiidae) in relation to biological control of the pea aphid in Europe and North America. Zeitschrift fuer Angewandte Entomologie 77, 141–171. Stary, P., 1988. Natural enemies. In: Minks, A.K., Harrewijn, P. (Eds.), Aphids: their biology, natural enemies and control. Elsevier, Amsterdam, pp. 171–184. Stiling, P., 1993. Why do natural enemies fail in classical biological control programs? American Entomologist 39, 31–37. Sullivan, D.J., Völkl, W., 1999. Hyperparasitism: multitrophic ecology and behaviour. Annual Review of Entomology 44, 291–315. Thiboldeaux, R., 1986. The effect of temperature on population level interactions between the pea aphid, Acyrthosiphon pisum, and its primary parasitoid, Aphidius ervi. Master’s Thesis, University of Wisconsin, Madison, USA. Thiboldeaux, R.L., Hutchinson, W.D., Hogg, D.B., 1987. Species composition of pea aphid (Homoptera: Aphididae) primary and secondary parasitoids in Wisconsin. Canadian Entomologist 119, 1055–1057. Vos, M., Berrocal, F.K., Hemerik, L., Vet, L.E.M., 2001. Plant-mediated indirect effects and the persistence of parasitoid–herbivore communities. Ecology Letters 4, 38–45. Waage, J.K., Hassell, M.P., 1982. Parasitoids as biological control agents – a fundamental approach. Parasitology 84, 241–268. Waterhouse, D.F., 1998. Biological Control of Insect Pests: Southeast Asian Prospects. ACIAR Monograph No. 51, Canberra, Australia, ISBN 863202218. Waterhouse, D.F., Sands, D.P.A., 2001. Classical biological control of arthropods in Australia. ACIAR Monograph No. 77, Canberra, Australia, ISBN 642457093.
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Perspective
The potential for hyperparasitism to compromise biological control: Why don’t hyperparasitoids drive their primary parasitoid hosts extinct? Shon S. Schooler a,⇑, Paul De Barro a, Anthony R. Ives b a b
CSIRO Ecosystem Sciences, Ecosciences Precinct, Brisbane, QLD, 4001, Australia Department of Zoology, University of Wisconsin, Madison, WI 53706, USA
a r t i c l e
i n f o
Article history: Received 21 March 2010 Accepted 27 May 2011 Available online 1 June 2011 Keywords: Biological control failure Population dynamics Establishment success Hyperparasitoid Predation Non-target effects
a b s t r a c t Predation or parasitism on species introduced as biological control agents is a common explanation for failure of biological control programs. Although there is clear evidence from some biological control programs that hyperparasitism can impact a parasitoid biological control agent, it is not clear whether hyperparasitoids have the potential to cause control failure. We performed glasshouse experiments using cages containing 48 plants to address whether the hyperparasitoid Asaphes suspensus can potentially eliminate a population of the primary parasitoid Aphidius ervi, a biological control agent of the pea aphid Acyrthosiphon pisum. Although As. suspensus has a low intrinsic rate of increase, only one-half that of A. ervi and one-third that of pea aphids, it was nonetheless capable of eliminating the A. ervi population within seven A. ervi generations. In contrast, in the absence of As. suspensus, A. ervi eliminated the pea aphid population. Field surveys, however, found that As. suspensus does not eliminate entire natural populations of A. ervi in lucerne crops, probably due to the high frequency of disturbance that favours high intrinsic rates of increase and short generation times. Nonetheless, the ability of As. suspensus to eliminate A. ervi in cages despite its low intrinsic rate of increase underscores the potential for hyperparasitism to disrupt biological control. Small populations are expected to be particularly susceptible to hyperparasitism, such as when releases of a new biological control agent are made. Crown Copyright Ó 2011 Published by Elsevier Inc. All rights reserved.
1. Introduction Classical biological programs select natural enemies from the native range of the target organism to control an introduced pest. The results of these introductions are often unpredictable, with some biological control agents exerting the desired level of control and others having little effect on target pest populations (Waterhouse and Sands, 2001). The three main reasons used to explain failure are climatic mismatches between the native and introduced range of the control agent (34.5%), predation or parasitism by native fauna on the control agent (20.3%), and lack of alternative hosts or food (16.9%) (Stiling, 1993). While climate is the most frequently cited cause for failure, it is also the one that can often be remedied (e.g., by releasing cold-tolerant populations of the biological control agent), whereas there is little that can be done to reduce the effects of native predators, parasitoids and hyperparasitoids (Stiling, 1993). Hyperparasitoids can be either obligate or facultative, and here we restrict our attention to obligate hyperparasitism. Furthermore, we do not consider heteronomous hyperparasitism in ⇑ Corresponding author. Address: CSIRO Ecosystem Sciences, EcoSciences Precinct, P.O. Box 2583, Brisbane, QLD 4001, Australia. Fax: +61 7 3833 5504. E-mail address: [email protected] (S.S. Schooler).
which female offspring develop as primary parasitoids and male offspring develop as hyperparasitoids. Parasitism and hyperparasitism may inhibit biological control programs targeting both invasive plants and insects. This is supported primarily by theoretical models (Beddington and Hammond, 1977; May and Hassell, 1981), although there are a small number of empirical case studies. For example, five species of native hymenopterous parasitoids were found to parasitise the tephritid gall fly, Procecidochares utilis Stone, that was introduced to control the weed Ageratina adenophorum (Spreng.) in Hawaii, and parasitism rates often exceeded 50% (Bess and Haramoto, 1959). An example of a negative effect in insect biological control caused by hyperparasitism is the control of the citrus psyllid (Diaphorina citri Kuwayama). In the native range of the psyllid, two parasitoids of the psyllid (Tamarixia radiata (Waterston) and Diaphorencyrtus aligarhensis (Shafee, Alam, and Agarwal)) are heavily hyperparasitised (up to 40%), whereas in introduced regions, where the hyperparasitoids are absent, the parasitoids provide good control (Waterhouse, 1998). Similarly, the Yugoslavian strain of Cotesia rubecula (Marshall) after initially establishing in Virginia in 1987 suffered an increase in hyperparasitism from an average of 37.9% in 1987 to a peak of 100% in August 1988; this was linked to the failure to recover the parasitoid in subsequent years (McDonald and Kok, 1991).
1049-9644/$ - see front matter Crown Copyright Ó 2011 Published by Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2011.05.018
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A review of hyperparasitism found several studies where hyperparasitism on a biological control agent reduced its efficacy in insect biological control programs, although no effect was found in other studies (Sullivan and Völkl, 1999). Other research suggests that, although hyperparasitism or predation rates on control agents may be high, it is the foraging behaviour of the biological control agents that primarily limits their effectiveness (Mackauer and Völkl, 1993). Mackauer and Völkl (1993) argue that the impact of hyperparasitoids is limited as a consequence of their relatively low lifetime fecundity and the limited storage capacity of their ovaries. Researchers in biological control have identified traits that are favourable for success of biological control agents. In particular, both ecological theory (Waage and Hassell, 1982; Murdoch, 1990) and biological control practice (Doutt and DeBach, 1964; Huffaker et al., 1977; Stiling, 1993) suggest that biological control agents with high intrinsic rates of increase are more likely to be effective. By the same logic, we might expect that hyperparasitoids with high intrinsic rates of increase relative to the control agent pose a greater threat to biological control. However, many hyperparasitoids have relatively low intrinsic rates of increase compared to the primary parasitoids that are often selected for control programs. This may contribute to the apparently few examples of hyperparasitoids compromising control programs using primary parasitoids. The evidence used to determine whether hyperparasitism can disrupt biological control programs generally consists of field assessments of hyperparasitism rates (e.g. McDonald and Kok, 1991). However, relatively few studies of post-release monitoring give sufficiently detailed information to quantify the impacts of hyperparasitism. Furthermore, hyperparasitism may be important when control agent populations are small and therefore difficult to assess, or hyperparasitism may be episodic yet still have a large impact on biological control success. Here, we take an alternative approach by conducting longterm population studies in a glasshouse to determine the potential impact of the hyperparasitoid Asaphes suspensus (Nees) (Pteromalidae: Asaphinae) on the primary parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae), a biological control agent of pea aphids (Acyrthosiphon pisum (Harris), Homoptera: Aphidae). To our knowledge, this is the only experimental cage study that examines the multi-generation population dynamics of a four trophic level insect system (plants, aphids, parasitoids and hyperparasitoids). While our study is not a substitute for detailed field assessments, it nonetheless addresses whether the hyperparasitoid has the biological capacity to disrupt biological control. The intrinsic rate of increase for As. suspensus is roughly half that of A. ervi, which by itself suggests that As. suspensus should not disrupt biological control by A. ervi. To compare with the glasshouse study, we also present detailed field assessments of hyperparasitism on A. ervi in lucerne crops over the course of a summer in Wisconsin, USA. 2. Methods 2.1. Study system The study system comprised four trophic levels; lucerne (Medicago sativa L., Fabaceae), the pea aphid (A. pisum), a parasitoid wasp (A. ervi), and a hyperparasitoid wasp (As. suspensus). Lucerne (alfalfa) is cultivated worldwide as a forage crop. The pea aphid is originally an Old World species that was accidentally introduced into North America in the 19th century (Hagen et al., 1976; Mackauer and Kambhampati, 1986). It feeds on a variety of legume crops. During the summer, reproduction is asexual (Blackman and Eastop, 1984). The parthenogenic females produce
as many as five nymphs per day, and nymphs go through four subadult instars (Hutchinson and Hogg, 1984, 1985; Thiboldeaux, 1986). The intrinsic rate of increase has been measured in a number of studies that give values between 0.241 (Siddiqui et al., 1973) and 0.562 (Hutchinson and Hogg, 1985) (depending on protocols and temperature). Sequiera and Mackauer (1988) report a value of 0.485, and we highlight this value because studies from the same lab have also measured the intrinsic rates of increase of A. ervi and As. suspensus. Pea aphids are attacked by A. ervi, which was introduced into the USA as a biocontrol agent in the 1960s and has now spread over much of North America (Gonzalez et al., 1978; Mackauer and Kambhampati, 1986; Thiboldeaux et al., 1987). A. ervi parasitises an aphid by laying a single egg through its exoskeleton (Stary, 1988), and the larva develops in the aphid, with a mummy forming in 6–10 days (Thiboldeaux, 1986). Larvae pupate within the mummy and emerge in 5–7 days. A. ervi principally attacks 2nd and 3rd instar aphids (Ives et al., 1999). While A. ervi attacks several genera of aphids (Stary, 1974; Mackauer and Finlayson, 1967), in Wisconsin, USA, the numerically most common host is the pea aphid (Thiboldeaux et al., 1987). Sequiera and Mackauer (1994) report its intrinsic rate of increase as 0.380. As. suspensus is a pupal hyperparasitoid that drills a hole in the aphid mummy with its ovipositor, injects venom into the immature parasitoid, and lays a single egg on the host’s ventral surface. The emergence time is approximately 16 days, the adult life span is approximately 14 days (Schooler et al., 1996), and females have a low average lifetime fecundity of 54 (Spencer, 1926). The reported host range of As. suspensus includes more than six genera of braconid parasitoids of aphids (Gibson and Vikberg, 1998), although A. ervi is likely its most common host in agricultural systems in temperate North America. As. suspensus has an intrinsic rate of increase of 0.172 (Mackauer and Völkl, 1993). 2.2. Glasshouse experiments The experiments took place in a glasshouse within two identical 75 150 50 cm cage arenas. The top and the two short sides consisted of a polyester screen while the long sides were composed of clear Mylar. The cages contained 48 lucerne plants. Pots 13 13 cm square and containing single plants (10–32 cm in ht.) were placed entirely within the cages. A plastic dish was placed around the base of each plant and the sides of the dish were coated with fluon, a slippery compound that prevents the aphids from leaving the dish. The glasshouse was environmentally controlled and supplemental light was provided by two 400 W high-pressure sodium bulbs suspended 1.5 m above the floor of the arena to produce a 16:8 L:D cycle. The two replicates took place sequentially, from 14 November 1994 to 25 February 1995 and from 17 April 1995 to 18 July 1995. The experiments were initiated by inoculating eight plants with four adult pea aphids (day 0). Five fertile female A. ervi adults were then added to each cage on days 7, 9, and 11, and four female adults were added on day 13. For the first experimental replicate, three fertile As. suspensus adult females were released in a randomly selected cage on day 14 (south cage, 28 November 1994) and during the sequential replicate three fertile As. suspensus adult females were released in the alternate cage (north cage, 6 May 1995) on day 22. Prior to introduction, females of A. ervi or As. suspensus were determined to be fertile by observing whether they oviposited into aphids or mummies, respectively. Every second day, measurements were made in each cage (number of aphids and number of mummies). In addition, plants were randomly assigned to eight groups (six per group) and mummies were collected from one of these groups, in sequential rotation, every two days. Mummies were then placed in covered Petri dishes and
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enclosed larvae were reared to adult in order to determine percent hyperparasitism. Plant condition was also examined and lucerne plants were replaced as they died. When plants were replaced, any remaining mummies were removed and placed back into the experimental cages. 2.3. Field surveys Surveys were conducted in two lucerne fields during 1998 at the University of Wisconsin Arlington Field Station, Arlington, Wisconsin. Twice per week at four (12 May–25 June) or two (29 June–1 September) stations in each field, 400 lucerne stems were sampled and all pea aphids and A. ervi mummies were counted (1600 or 800 total stems per field). Mummies were also collected in separate sampling, with numbers ranging from 2 to 386 depending on mummy densities in the field. Mummies were returned to the lab and allowed to emerge, with the emerging wasp identified as A. ervi or one of three hyperparasitoids: As. suspensus, Dendrocerus carpenteri (Curtis), or Pachyneuron altiscutum Cook. Not all mummies emerged, and therefore we report the percentage hyperparasitism determined by the numbers of emerging A. ervi and hyperparasitoids. One of the fields was established in 1997, whereas the other was planted in the spring of 1998. The previously established field was harvested in May, late June, and early August; the newly
A
planted field was harvested in late June and early August. For 1–2 weeks following harvesting (depending on the rate of lucerne regrowth), the sampling procedure described above could not be implemented, because plants were cut to stubble. Although we did not count aphids and mummies until lucerne regrowth reached roughly 10 cm, we did attempt to collect mummies for rearing and determination of percentage hyperparasitism. These data are part of a larger survey including records of aphid predators that was previously used in analyses of the importance of A. ervi parasitism and predation on pea aphid dynamics (Rauwald and Ives, 2001; Gross et al., 2005). 3. Results 3.1. Glasshouse cage studies When confined in glasshouse cages, hyperparasitoids had a large impact on the primary parasitoid, causing a breakdown in the ability of the primary parasitoid to suppress aphid densities. In the absence of the hyperparasitoid As. suspensus, aphid populations initially increased to high densities (max 965 and 2457 individuals in replicate 1 and 2, respectively) and thereafter the abundance of aphids declined to 0 and 211 aphids (Fig. 1A and 2A) at the end of the experiment. This reduction in hosts led to a reduction in parasitoids, from a maximum of 256 and 347 to 23
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Date Fig. 1. Results from the first cage experiment presenting the populations of aphids (A. pisum) and parasitoids (A. ervi) (total number of aphids and mummies in each cage) in a cage A) without and B) with hyperparasitoids (As. suspensus). Percent hyperparasitism is the number of As. suspensus relative to the number of parasitoids (number of As. suspensus divided by number of A. ervi plus As. suspensus) that later emerged from mummies collected from a subset of plants on a given date.
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Date Fig. 2. Results from the second cage experiment presenting the populations of aphids and parasitoids (A. ervi) (total number of aphids and mummies in each cage) in a cage (A) without and (B) with hyperparasitoids (As. suspensus). Percent hyperparasitism is the number of As. suspensus relative to the number of parasitoids (number of As. suspensus divided by number of A. ervi plus As. suspensus) that later emerged from mummies collected from a subset of plants on a given date.
and 160 mummies in cages one and two, respectively. In the presence of As. suspensus, mummies declined from a maximum of 340 to 19 (Fig. 1B) and 249 to 24 mummies (Fig. 2B). In contrast to the cages without hyperparasitoids, however, aphid densities remained high, with 1149 and 828 individuals at the end of the experiment in replicates one and two, respectively. Therefore, the decline in primary parasitoid mummies was not due to a decline in aphid numbers but instead was due to hyperparasitism. In both experiments, hyperparasitism reached 100% before the end of the experiment. 3.2. Field surveys In field surveys conducted in 1998, hyperparasitism generally increased through time as pea aphid and A. ervi mummy densities increased in fields up to the time of harvesting (Figs. 3 and 4). Percentage hyperparasitism often reached 20–40% by the time of harvesting, and hyperparasitism was sometimes even higher among those mummies found immediately following harvesting and before regular sampling of aphids and mummies could resume. The pattern for overall hyperparasitism was also shown for hyperparasitism by As. suspensus. Hyperparasitism showed a marked contrast with the pattern of A. ervi parasitism; in most harvesting cycles the increase in the number of mummies parallels the increase in the number of aphids (Figs. 3 and 4), and a detailed
analysis showed that percentage parasitism by A. ervi does not increase as aphid density increases over a harvesting cycle (Gross et al., 2005). 4. Discussion In this study we demonstrate the ability of the hyperparasitoid As. suspensus, under glasshouse conditions, to quickly drive the primary parasitoid A. ervi extinct. This time to extinction was roughly the same as the time to extinction of pea aphids caused by A. ervi when As. suspensus was absent. Why is there such a dramatic effect of As. suspensus on A. ervi populations, and what implication does this hold for biological control programs? The effect of hyperparasitism is amplified in cages in which A. ervi experiences mortality from two directions; directly from parasitism by As. suspensus and indirectly from the mortality of aphids that are carrying A. ervi larvae. The indirect mortality increases as the aphids approach the carrying capacity of the system. In the cage populations, A. ervi reaches high density quickly, at which point the per capita population growth rate becomes zero. Therefore, A. ervi cannot attain its intrinsic rate of increase. To eliminate A. ervi, As. suspensus only needs to maintain a per capita population growth rate exceeding zero. In this situation the potential A. ervi advantage in having a higher intrinsic rate of increase than As. suspensus is deceptive. Because
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Date Fig. 3. (A) Densities (number per lucerne stem) of pea aphids and mummies and (B) percent hyperparasitism from As. suspensus and all hyperparasitoids (As. suspensus, D. carpenteri, and P. altiscutum) from a field in Wisconsin in 1998. Harvest days are shown by arrows. The field was planted with lucerne in the 1997.
populations are confined to a cage in which plants are replaced to maintain a relatively stable environment, populations of A. ervi approach their carrying capacity rapidly, at which point their population cannot out-grow the increasing hyperparasitoid population despite their higher intrinsic rate of increase. In contrast to the glasshouse experiments, the field data show that hyperparasitoids do not eliminate A. ervi. Although hyperparasitism rates are low when aphid and A. ervi populations begin to recover following harvesting, hyperparasitism rates reach 20–40% during the harvesting cycle. This demonstrates the densitydependent pattern that as A. ervi populations increase, the percent mortality caused by hyperparasitism also increases, and this may limit the ability of A. ervi to maintain pressure on out-breaking pea aphid populations. Arguing from the glasshouse experiments in which we experimentally removed disturbances, A. ervi populations in the field are only saved by disturbance events; e.g. crop harvesting. We found that disturbance events in field cropping systems decreased the ability of the hyperparasitoid to eliminate populations of the parasitoid species, whereas in the absence of disturbance, in laboratory mesocosms, presence of the hyperparasitoid caused extinction of the parasitoid. Although previous studies have not specifically examined the factors that facilitate coexistence in hyperparasitoid–parasitoid interactions, there is a rich literature on factors that promote coexistence in predator–prey systems. For example, a classic laboratory experiment by Huffaker (1958) found that complexity of the underlying resource (arrangement of oranges) facilitated long-term coexistence of herbivore (sixspotted mite: Eotetranuchus sexmaculatus) and predator (predatory mite: Typhlodromus occidentalis) populations. The effect of planthost complexity has also been demonstrated in a field experiment
where foraging efficiency of an ichneumonid parasitoid (Diadegma semiclausum) on the diamondback moth (Plutella xylostella) was reduced under more complex plant arrangements, which led to increased stability of parasitoid populations (Gols et al., 2005). In addition, complexity of herbivore communities (diversity of herbivore host species) can also promote stability of parasitoid populations (Vos et al., 2001). By extension, a possible explanation why hyperparasitoids do not cause the extinction of parasitoid populations in natural and cropping systems is habitat and host complexity. In general, even though obligate hyperparasitoids, or predators of biological control agents, may have low intrinsic rates of increase, they may still have the capacity to disrupt biological control. Theoretical studies that have explicitly addressed the impacts of hyperparasitism in biological control have generally considered only the case in which pests, control agents, and hyperparasitoids coexist at a stable equilibrium (e.g., Beddington and Hammond, 1977; May and Hassell, 1981); in this case, these studies show that high intrinsic rates of the hyperparasitoid are not needed to disrupt biological control. We know of no theoretical study of the effects of hyperparasitism in disturbed environments. Nonetheless, Schellhorn et al. (2002) compare the impacts of two primary parasitoids that differ in intrinsic rates of increase in disturbed and undisturbed environments, demonstrating that disturbance favours the primary parasitoid with the higher intrinsic rate of increase. Arguing from this, but at the hyperparasitism trophic level, disturbance should accentuate the importance of a hyperparasitoid’s intrinsic rate of increase for its ability to disrupt biological control. While the impact of hyperparasitoids on biological control success is seldom reported, the threat is implicitly considered in
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Date Fig. 4. (A) Densities (number per lucerne stem) of pea aphids and mummies and (B) percent hyperparasitism from As. suspensus and all hyperparasitoids (As. suspensus, D. carpenteri, and P. altiscutum) from a field in Wisconsin in 1998. Harvest days are shown by arrows. The field was planted in the spring of 1998.
regards to the accidental introduction of hyperparasitoids along with the candidate agents. Prevention of accidental importation of hyperparasitoids is one of the reasons it is recommended that agents being imported for control are passed through at least one generation in quarantine. However, consideration of species as candidate biological control agents usually takes into account (a) potential efficacy and (b) potential for non-target attack, but there is little evidence to suggest that practitioners consider the threat to efficacy posed by hyperparasitoids already present in the recipient location. As McDonald and Kok (1991) showed, hyperparasitoids that are already present may have a marked negative influence on the capacity to establish and persist, and so may contribute to failure. Investigating the potential for resident hyperparasitoids to cause biological control failure, and considering this potential in the selection of candidate control agents, may lead to greater success of some biological control programs. In selecting candidate biological control agents, a second factor to consider is indirect non-target affects. The addition of a new species that is susceptible to attack by hyperparasitoids already present may result in an increase in the availability of food resources and so lead to an increase in hyperparasitoid abundance. In a review of indirect interactions in aphid–parasitoid communities, there was no mention of this type of interaction (Muller and Godfray, 1999). However, as some hyperparasitoids have more than one host, the question needs to be asked as to whether this increase in local abundance could result in increased hyperparasitism of non-target parasitoid species, thereby reducing the efficacy of these species resulting in disruption of control. Our glasshouse experiment shows that a hyperparasitoid with a low intrinsic rate of increase is nonetheless capable of locally
eliminating a biological control agent. While this does not occur in the field, it raises concern about the outcome of control agent releases at the initial stages of a control program, when control agent populations are small (sensu McDonald and Kok, 1991). Furthermore, we believe that the initial assumption should be that hyperparasitoids have the potential to disrupt biological control, and starting from this assumption, biological control practitioners should ask what factors might allow biological control agents to suppress pests despite this potential. A central question in basic ecological studies is why don’t predators drive their prey species locally extinct. We believe that the same question should be asked for biological control programs: why don’t hyperparasitoids drive their primary parasitoid hosts extinct? Acknowledgments Vic Jager and Arin Davis assisted in the glasshouse experiments and Kevin Gross led the field survey. We thank O. Edwards, J. Brodeur, and one anonymous reviewer for their constructive comments. S. Schooler was supported by a Holstrom Environmental Scholarship. References Blackman, R.L., Eastop, V.F., 1984. Aphids on the world’s crops: an identification and information guide. John Wiley & Sons, New York. Beddington, J.R., Hammond, P.S., 1977. On the dynamics of host–parasitehyperparasite interactions. Journal of Animal Ecology 46, 811–821. Bess, H.A., Haramoto, F.H., 1959. Biological control of pamakani, Eupatorium adenophorum, in Hawaii by a tephritid fly, Procecidochares utilis. Ecology 40, 244–249.
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