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Linking parasitoid nectar feeding and dispersal in conservation biological control
Biological Control 132 (2019) 36–41
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Linking parasitoid nectar feeding and dispersal in conservation biological control
T
George E. Heimpel Department of Entomology, University of Minnesota, 1980 Folwell Ave, St. Paul, MN 55108, USA
A R T I C LE I N FO
A B S T R A C T
Keywords: Superparasitism Hyperparasitoids Risk-spreading Inbreeding Complementary sex determination Anagrus
The nectar provision hypothesis posits that biological control by parasitoids can be enhanced by providing supplemental nectar in the vicinity of cropland. The rationale for this hypothesis is that parasitoid longevity and fecundity can be greatly enhanced by sugar meals and that many agricultural areas are devoid of naturally occurring sugar sources. While some experimental field studies have produced results supporting the nectar provision hypotheses, many others have failed to show that supplemental nectar can improve biological control by parasitoids. I propose that some parasitoids may engage in medium- or long-range dispersal upon feeding on nectar and thus not contribute to local parasitism adjacent to flower plantings. If true, this could help to explain some of the negative results of nectar supplementation experiments. I further propose that certain conditions favor nectar-induced dispersal and discuss four of these here: (i) the risk of self-superparasitism, (ii) the risk of density-dependent hyperparasitism, (iii) benefits of ‘spreading the risk’ of catastrophic mortality and (iv) the risk of inbreeding among parasitoid offspring.
1. Introduction A particularly appealing hypothesis in conservation biological control is that polycultures decrease pest pressure by providing nectar for parasitoids. This hypothesis has been called the ‘parasitoid nectar provision hypothesis’ (Heimpel and Jervis, 2005), and it is attractive for three main reasons. First, many monocultures are thought to be relatively devoid of sugar sources such as floral or extrafloral nectar. Second, numerous laboratory studies have shown that parasitoids live far longer and can attack many more hosts when they are fed sugar than when they are sugar-starved. Typical lifespans range between one and five days for starved parasitoids and between 2 and 8 weeks for sugarfed parasitoids (e.g. Heimpel et al., 1997; Olson et al., 2000; Lee et al., 2004; Wyckhuys et al., 2008). Third, many parasitoid species utilize nectar under natural conditions (e.g. Wolcott, 1942; Jervis et al., 1993; Gilbert and Jervis, 1998; Jervis, 1998; Casas et al., 2003; Lavandero et al., 2005; Lee et al., 2006; Winkler et al., 2009). These considerations have combined to produce an expectation that biological control can be improved by the incorporation of flowering cover crops or other means of delivering sugar to parasitoids in the field (Landis et al., 2000; Lu et al., 2014). A few field studies have indeed produced results that support the parasitoid nectar provision hypothesis (English-Loeb et al., 2003; Tylianakis et al., 2004; Irvin et al., 2006; Gurr et al., 2016). These cases
are important in demonstrating one or more important aspects of the hypothesis, including sugar limitation by parasitoids, the use of supplemental nectar, increased parasitism rates in the presences of supplemental nectar, and improved biological control of pest arthropods (Heimpel and Jervis, 2005; Tena et al., 2015; Heimpel and Mills, 2017). It is also important to note that insects with a predatory larval stage and nectar-feeding adult stage are subject to similar life-history constraints as parasitoids are and some of these have also provided cases of successful nectar provisioning (e.g. Hickman and Wratten, 1996; Pineda and Marcos-Garcia, 2008). However, these inspiring cases of success have been the exception rather than the rule in tests of the parasitoid nectar provision hypothesis with many provisioning studies not leading to improved biological control (Heimpel and Jervis, 2005; Lee and Heimpel, 2005a). There does not seem to be a single correct explanation for failure of nectar supplementation to improve biological control. Proposed reasons for the failure of the parasitoid nectar provision hypothesis have ranged from a lack of sugar limitation on the part of parasitoids (e.g. Lee et al., 2006) to scenarios in which pest insects utilize supplemented nectar to greater effect than their parasitoids do (e.g. Baggen and Gurr, 1998). Broadly speaking, the inconsistency of supplemental nectar in improving biological control, along with some the postulated ecological explanations for cases of failure, can be seen as a microcosm of some of the five hypotheses for the failure of natural habitat to enhance natural
E-mail address: [email protected]. https://doi.org/10.1016/j.biocontrol.2019.01.012 Received 31 October 2018; Received in revised form 23 January 2019; Accepted 25 January 2019 Available online 28 January 2019 1049-9644/ © 2019 Elsevier Inc. All rights reserved.
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Under these circumstances, dispersal away from host patches prior to reproduction may be a more logical response to nectar feeding than retention in host patches. It follows that supplemental nectar provisions may fail to improve local biological control services by parasitoids, although overall or more distant parasitism rates may be improved. It is also important to note that dispersal away from sugar sources could improve local parasitism rates if it is very limited in distance, as noted above in the case of A. rhopalosiphi (Tylianakis et al., 2004). Thus the spatial scale of dispersal is a critical determinant of how parasitoid dispersal behavior affects biological control under conditions of habitat diversification in general, and nectar supplementation in particular (Corbett, 1998).
biological control that Tscharntke et al. (2016) outlined. It is also consistent with a recent worldwide meta-analysis of habitat manipulation for the purpose of biological control (Karp et al., 2018) that revealed a lack of consistency of diversified habitats in improving biological control services. These patterns are a clear reminder that the discipline of conservation biological control is still searching for the ‘right forms of biodiversity’ that need to be implemented to consistently and predictably improve biological control (Heimpel and Mills, 2017). I outline here a hypothesis that I believe was first articulated by Lee and Heimpel (2005b) to explain at least a subset of some of the failures of nectar supplementation to improve biological control of insect pests by parasitoids in experimental or farm-based settings. This hypothesis posits that sugar feeding can induce parasitoid dispersal away from nectar sources. It contradicts an implicit (and sometimes explicit) assumption of the parasitoid nectar provision hypothesis that parasitoids are retained in the local area by nectar-feeding and that they attack more hosts adjacent to nectar sources as a result (Wäckers and Lewis, 1994; Lewis et al., 1998). What is the support for the hypothesis of retention of parasitoids by nectar? Some evidence comes from studies of the tachinid Lixophaga sphenophori, which is attracted and retained by flowering plants at the edges of sugarcane fields, where more hosts are attacked (Leeper, 1974; Topham and Beardsley, 1975). Also, some elegant small-plot field studies showed that the braconid Microplitis croceipes will stay in the local area to attack hosts longer in the presence of sugar meals (Takasu and Lewis, 1995; Stapel et al., 1997). And Lavandero et al. (2005) reported higher levels of parasitism adjacent to flowering buckwheat by the parasitoid Diadegma semiclausum despite the fact that these parasitoids are highly mobile. In all of these systems, it does appear that sugar feeding led to some degree of parasitoid retention. A number of studies have shown that sugar-fed parasitoids respond to host-related cues in laboratory studies (e.g. Lewis and Takasu, 1990; Takasu and Lewis, 1993, 1996; Wäckers, 1994; Jacob and Evans, 2000), but it does not necessarily follow from these studies that sugar feeding leads to local retention in field settings. I argue here that an alternative hypothesis – that sugar-feeding induces parasitoid dispersal, not retention – is worth considering. A number of studies from the literature are consistent with such a reaction to sugar feeding. First, Wäckers (1994) found that sugar – fed Cotesia rubecula engaged in more flight behavior than starved individuals did in a wind tunnel setting. Similar results were found for the parasitoids Trichogramma minutum and Tetrastichus planipennisi (Forsse et al., 1992; Fahrner et al., 2014). Second, in a field study in which nectar sources were marked with the trace element Rubidium, Freeman Long et al. (1998) captured more marked Hyposoter sp. parasitoids 75 m from the marked plants than 6 m or less from the marked plants. Short-range dispersal may also be responsible for ‘surprisingly’ low parasitism levels by the aphid parasitoid Aphidius rhopalosiphi directly adjacent to a flowering strip in the very careful studies done by Tylianakis et al. (2004). But why would parasitoids disperse after feeding on sugar? The answer to this question must lie at least in part in the dynamics of adaptive foraging behavior by parasitoids, and in particular, whether there is an advantage to be gained by spreading eggs out over a series of host patches. Although it may at first seem that all or most hosts in a patch should be used before leaving one host patch in search of another in order to minimize opportunity costs and mortality during dispersal, this may not necessarily be the case. Montovan et al. (2015) discussed a number of reasons for early patch leaving and I focus on four here that can favor leaving patches before their quality declines due to depletion: (i) avoidance of self-superparasitism (Rosenheim and Mangel, 1994), (ii) avoidance of density-dependent hyperparasitism (Ayal and Green, 1993; Mackauer and Völkl, 1993), (iii) ‘spreading the risk’ of catastrophic mortality in a single patch (Cronin and Strong, 1993a), and (iv) reduction in the risk that one’s offspring engage in inbreeding. If any of these (or other) dynamics lead to selection for early patch leaving, sugar-feeding (or more generally, high energy reserves) may provide the resources necessary for successful dispersal to another host patch.
2. Hypotheses for adaptive patch-leaving in parasitoids with implications for sugar-fueled dispersal 2.1. Risk of self-superparasitism The term superparasitism is used to describe the act of parasitizing hosts that already contain conspecific eggs or larvae. This behavior can be adaptive if the previously parasitized host was attacked by a different female (van Alphen and Visser, 1990; Mangel, 1992) but is almost always considered maladaptive if the previously parasitized host was attacked by the foraging female herself (Rosenheim and Mangel, 1994; Desneux et al., 2009; but see van Alphen and Visser, 1990 for cases in which this can be adaptive). This latter behavior is known as ‘self-superparasitsm’, and if parasitoid females cannot discriminate between hosts that they themselves have parasitized and healthy hosts, they run the risk of such self-superparasitism, and thus incurring costs associated with egg and time wastage as well as exposing their offspring to competition against each other. Rosenheim and Mangel (1994) used two separate modeling approaches to show that parasitoids with poor discrimination abilities were selected to leave patches after only a very small fraction of the hosts had been used, solely to avoid self-superparasitism. Another way to view this result is that diminishing returns of foraging are reached earlier during patch visitation for parasitoids that have poor rather than good discriminatory abilities (Montovan et al., 2015). Patch leaving was favored in Rosenheim and Mangel’s (1994) models by other factors as well, including low mortality during travel between patches, area-restricted search coupled with poor discrimination, and a high risk of egg limitation (Rosenheim and Mangel, 1994). One of these latter hypotheses was confirmed in a study on an egg parasitoid of planthoppers that utilized a higher proportion of patches after long dispersal events (Cronin and Strong, 1999). This suggests that female parasitoids were more willing to risk self-superparasitism when the risk of mortality during travel between patches was greater. The issue of spatial scale was not explicitly addressed in these models and it was assumed that the risk of self-superparasitism was zero in new host patches. Whether the dynamics identified by these patchleaving rules will affect the dynamics linking parasitoid sugar feeding and biological control will depend on issues of scale – particularly whether different host patches are found in the same general vicinity (e.g. on the same plant) and can thus be found by trivial dispersal events or whether long-distance dispersal is needed to locate host patches that sufficiently decrease the chance of self-superparasitism. In any case, the outcomes of the models developed by Rosenheim and Mangel (1994) suggest that parasitoids with poor discriminatory abilities should have more to gain by using sugar meals to fuel travel among patches of hosts than parasitoids with high discriminatory ability. I therefore predict a higher chance of success in improving parasitism rates by using supplemental sugar for parasitoid species with good rather than poor discrimination abilities. This hypothesis has not been explicitly tested, but a comparison among some mymarid species with divergent discrimination abilities may be able to provide insights into an important recent conservation 37
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biological control success. Detailed field studies of the mymarid parasitoid Anagrus delicatus attacking patches of planthopper eggs embedded within Marsh grass tissue revealed extremely low levels of proportional patch use, with an average of only 18% of possible hosts used per patch under normal conditions (Cronin and Strong, 1993a). In a separate study, however, Cronin and Strong (1993b) showed that A. delicatus has very poor discrimination ability and thus suffers from a very high risk of self superparsitism (see also Bouskila et al. (1995) for a complementary explanation involving host quality). In fact, it was these data as well as information on potential egg limitation that were used to parameterize Rosenheim and Mangel’s (1994) models and thus led to the insights outlined above. By themselves, these insights do not go far in addressing our hypothesis linking host-patch use, parasitoid dispersal and conservation biological control. But interestingly, some other species of mymarids exhibit much higher levels of discrimination of parasitized hosts, allowing the avoidance of self-superparasitsm, and these species (as expected) utilize a much higher proportion of host patches (Hasan, 1982, 1984; Rosenheim and Mangel, 1994) and thus presumably engage in less dispersal between patches. And one of these species, A. obtibalis, has recently been shown to respond positively to nectar supplementation in a very successful conservation biological control intervention in South-East Asia and China (Gurr et al., 2016; Zhu et al., 2018). While nectar feeding has not been demonstrated for A. obtibalis in the field, laboratory studies show the potential for this (Zhu et al., 2013), and the field data that have been presented are consistent with a nectar subsidy improving biological control of rice brown planthoppers, the main host of A. obtilis. And pursuant to our hypothesis, the fact that this parasitoid species has high discrimination abilities may aid the effectiveness of nectar subsidies by facilitating the retention of parasitoids in the vicinity of the floral plantings. A different study demonstrated higher levels of parasitism of by one or more unidentified species of Anagrus of eggs of pest leafhoppers in vineyards adjacent to floral plantings as well (English-Loeb et al., 2003) but discrimination and patch-use behaviors of this species are not known as far as I am aware.
maximal patch use. Montovan et al. (2015) concluded that the risk of density-dependent hyperparasitism contributed to the pattern of submaximal patch use and dispersal among patches found for this parasitoid. Based on the considerations presented here I propose the following hypotheses with respect to hyperparasitism and sugar supplementation. First, parasitoids that are subject to density-dependent hyperparasitism at the local scale will be selected to engage in early patch leaving and thus will be more likely to engage in relatively long-distance dispersal under conditions of enhanced sugar availability than parasitoids not subject to density-dependent hyperparasitism. Thus, density-dependent hyperparasitism will translate into lower effectiveness of nectar supplementation as a biological control strategy. While these hypotheses have not been tested per se, a link between hyperparasitism and the dispersal of primary parasitoids was established by Holler et al. (1994), who showed that the aphid parasitoid Aphidius uzbekistanicus actively dispersed away from arenas that contained adult hyperparasitoids or their traces. Also, Lee and Heimpel (2005a) found strong density-dependent hyperparasitism of the parasitoid Diadegma insulare by the chalcidid Conura side in a field study. Interestingly, this same study showed that supplemental nectar did not enhance parasitism by D. insulare, consistent with the predictions articulated above. The main hypothesis explaining the lack of an effect of nectar supplementation on biological control in these studies was an absence of sugar limitation for D. insulare (Lee et al., 2006; Lee and Heimpel, 2008) but a response to density-dependent hyperparasitism should be added as a potential determinant as well. 2.3. Risk spreading If there is a non-trivial chance of complete patch failure after parasitism and before parasitoid eclosion (e.g. from factors such as vertebrate herbivory or plant senescence for herbivorous hosts), it may be possible that spreading eggs over many patches (and therefore, early patch leaving) is selected for. This is the explanation that Cronin and Strong (1993a) gave for early patch leaving in A. delicatus that was discussed above. This explanation – known as spatial risk spreading (or bet-hedging) – has intuitive appeal, but conditions favoring it are stringent. These conditions include very small populations, and temporal variation in mortality risk (Godfray, 1994; Hopper, 1999; Hopper et al., 2003). I am not currently aware of host-parasitoid systems that are subject to these conditions – particularly ones that involve targets of conservation biological control. In the event that such conditions are discovered, I predict that parasitoids that engage in a risk-spreading strategy would be at risk of using supplementary sugar meals to enhance dispersal and thus not be retained near supplementary nectar sources.
2.2. Density-dependent hyperparasitism If the risk of parasitoid mortality increases with the parasitism rate, it pays to keep per-patch rates of primary parasitism low. In principle, this applies to all sources of mortality to immature parasitoids, but since most predators that would have such an effect are likely intraguild predators and would thus more likely respond to host rather than parasitoid density, this hypothesis applies primarily to hyperparasitoids. Having said this, density dependent intraguild predation could translate to a higher mortality risk for immature parasitoids as well (e.g. Chacón and Heimpel, 2010; Frago, 2016). For simplicity though, I focus on the case of hyperparasitoids here. Under conditions of density-dependent hyperparasitism, early patch leaving may be optimal (Ayal and Green, 1993; Mackauer and Völkl, 1993; Weisser et al., 1994). As discussed above, optimal patch leaving under this hypothesis will be modified by factors such as the risk of mortality during inter-patch movement and egg limitation. Also – the relevance of these dynamics for conservation biological control will depend upon the spatial scale at which they operate. Density-dependent hyperparasitism has been found in some studies (Horn, 1988 [Cited by Weisser et al. (1994)]; Lee and Heimpel, 2005a; Montovan et al., 2015) but not others (Muller and Godfray, 1998; van Veen et al., 2002) although the response can be complex, depending on spatial scale and other factors (Schooler et al., 2011; Chow, 2000; van Veen et al., 2002; Lee and Heimpel, 2005a). Montovan et al. (2015) demonstrated strong positive density dependent parasitism of the ichneumonid Hyposoter horticola in natural settings in Finland and determined that per-patch fitness gains peaked at 70% parasitism due to the dangers of density dependent hyperparasitism. While this does not indicate particularly strong early patch leaving, it illustrates sub-
2.4. Inbreeding Spreading eggs out over a series of patches could decrease the risk that one’s offspring engage in inbreeding. While some parasitoid taxa appear to be relatively tolerant of inbreeding, others show strong inbreeding depression (Henter, 2003). In particular, many parasitic Hymenoptera suffer from a severe form of inbreeding depression known as complementary sex determination (CSD). Under CSD, sex is determined by one or more highly polymorphic ‘sex loci’. Sex locus heterozygotes develop as females, and sex locus homozygotes develop as diploid males (unfertilized hemizygotes develop as haploid males as per standard haplo-diploidy) (Heimpel and de Boer, 2008). Diploid males are inviable in some species and in other species can effectively sterilize females that accept them as mates (Stouthamer et al., 1992; Harpur et al., 2012; de Boer et al., 2007). Among the parasitic hymenoptera, CSD is only known in the superfamily Ichneumonoidea with members of other superfamilies exhibiting greater tolerance to inbreeding (Heimpel and Lundgren, 2000; Asplen et al., 2009). And CSD is only 38
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Acknowledgements
partly expressed within the Ichneumonoidea, with some taxa exhibiting it and others not (Asplen et al., 2009). Also – the details of CSD expression vary among species that have it, and this results in variability in the strength of inbreeding depression. Thus, in at least one parasitoid species with CSD diploid males are almost completely viable and can sire diploid daughters (Elias et al., 2009), and in others sex is determined at two or more loci in a way that requires much more extreme inbreeding to produce diploid males (De Boer et al., 2008, 2012, 2015; Carabajal Paladino et al., 2015; Weis et al., 2017). And finally, the mating system of parasitoids with CSD is usually based on outbreeding strategies (including dispersal) as a means of avoiding diploid male production (Antolin and Strand, 1992; Ode et al., 1995, 1998; Heimpel, 1997). Given these considerations, I hypothesize that female parasitoids with single-locus CSD (or other forms of inbreeding depression) engage in early patch leaving as a means of decreasing the likelihood that their offspring mate with one another and producing sterile diploid males or suffer other consequences of inbreeding. I further hypothesize that such females will be more likely to utilize sugar meals to engage in mediumto long-distance dispersal than females of parasitoid species that do not suffer inbreeding depression. I therefore predict a higher likelihood of successful biological control improvement from nectar supplementation targeting parasitoid species with low rather than high risk of inbreeding depression. While this hypothesis would seem to be relatively easy to test using comparative data, in my estimation the data base is still too small to conduct a proper comparative test. What would be needed are more studies of nectar supplementation targeting parasitoids with known inbreeding biologies, including both the magnitude of inbreeding depression itself and the ability of the parasitoids to avoid inbreeding.
I thank the organizers of this special feature, Lessandro Gontijo and William Snyder, for the invitation to submit a contribution and the comments of three anonymous reviewers for advice on the ms. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.biocontrol.2019.01.012. References Antolin, M.F., Strand, M.R., 1992. Mating system of Bracon hebetor (Hymenoptera: Braconidae). Ecol. Entomol. 17, 1–7. Asplen, M.K., 2018. Dispersal strategies in terrestrial insects. Curr. Opin. Insect Sci. 27, 16–20. Asplen, M.K., Whitfield, J.B., De Boer, J.G., Heimpel, G.E., 2009. Is single-locus complementary sex determination the ancestral mechanism for hymenopteran haplodiploidy? J. Evol. Biol. 22, 1762–1769. Ayal, Y., Green, R.F., 1993. Optimal egg distribution among host patches for parasitoids subject to attack by hyperparasitoids. Am. Nat. 141, 120–138. Baggen, L.R., Gurr, G.M., 1998. 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3. Conclusions The over-arching hypothesis that I have posed here is that the females of some parasitoid species may be selected to engage in mediumor long-distance dispersal upon feeding on nectar and that this behavior could compromise the successful deployment of supplemental nectar to improve biological control at the local scale. I further suggest that this dispersal behavior is likely to vary among species based on optimal patch-use and dispersal behavior in a predictable way that is based upon the dynamics of early patch leaving behavior. The dynamics that I focused on were (i) the ability to avoid self-superparasitism (but note that similar arguments could be made for superparaitism in general; Montovan et al. (2015)), (ii) the risk of density-dependent hyperparasitism, (iii) the advantage of spatial risk-spreading in terms of oviposition, and (iv) risks associated with inbreeding. In each case, early patch leaving is expected if fitness reductions occur before patch depletion dynamics would dictate patch leaving (see Wajnberg, 2006). In my estimation there is inadequate biological knowledge of the parasitoid species that have been subjected to nectar supplementation experiments to perform meaningful comparative tests of the hypotheses that I have presented at the time of this writing. However, some directed laboratory studies of parasitoids have already shown that sugarfeeding can enhance the tendency to disperse (e.g. Wackers, 1994; Fahrner et al., 2014). A next step could be to take this approach into the field. Indeed, a number of authors have argued for the importance of understanding the dynamics of dispersal in parasitoids (Corbett and Plant, 1993; Corbett, 1998; Cronin and Reeve, 2005; Heimpel and Asplen, 2011; Schellhorn et al., 2014; Asplen, 2018) and I would suggest investigating in particular the effects of sugar feeding on parasitoid dispersal behavior to gain more insights into the potential effects of nectar supplementation strategies in conservation biological control. 4. Author statement GEH conceived of all ideas presented in this ms. 39
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Linking parasitoid nectar feeding and dispersal in conservation biological control
T
George E. Heimpel Department of Entomology, University of Minnesota, 1980 Folwell Ave, St. Paul, MN 55108, USA
A R T I C LE I N FO
A B S T R A C T
Keywords: Superparasitism Hyperparasitoids Risk-spreading Inbreeding Complementary sex determination Anagrus
The nectar provision hypothesis posits that biological control by parasitoids can be enhanced by providing supplemental nectar in the vicinity of cropland. The rationale for this hypothesis is that parasitoid longevity and fecundity can be greatly enhanced by sugar meals and that many agricultural areas are devoid of naturally occurring sugar sources. While some experimental field studies have produced results supporting the nectar provision hypotheses, many others have failed to show that supplemental nectar can improve biological control by parasitoids. I propose that some parasitoids may engage in medium- or long-range dispersal upon feeding on nectar and thus not contribute to local parasitism adjacent to flower plantings. If true, this could help to explain some of the negative results of nectar supplementation experiments. I further propose that certain conditions favor nectar-induced dispersal and discuss four of these here: (i) the risk of self-superparasitism, (ii) the risk of density-dependent hyperparasitism, (iii) benefits of ‘spreading the risk’ of catastrophic mortality and (iv) the risk of inbreeding among parasitoid offspring.
1. Introduction A particularly appealing hypothesis in conservation biological control is that polycultures decrease pest pressure by providing nectar for parasitoids. This hypothesis has been called the ‘parasitoid nectar provision hypothesis’ (Heimpel and Jervis, 2005), and it is attractive for three main reasons. First, many monocultures are thought to be relatively devoid of sugar sources such as floral or extrafloral nectar. Second, numerous laboratory studies have shown that parasitoids live far longer and can attack many more hosts when they are fed sugar than when they are sugar-starved. Typical lifespans range between one and five days for starved parasitoids and between 2 and 8 weeks for sugarfed parasitoids (e.g. Heimpel et al., 1997; Olson et al., 2000; Lee et al., 2004; Wyckhuys et al., 2008). Third, many parasitoid species utilize nectar under natural conditions (e.g. Wolcott, 1942; Jervis et al., 1993; Gilbert and Jervis, 1998; Jervis, 1998; Casas et al., 2003; Lavandero et al., 2005; Lee et al., 2006; Winkler et al., 2009). These considerations have combined to produce an expectation that biological control can be improved by the incorporation of flowering cover crops or other means of delivering sugar to parasitoids in the field (Landis et al., 2000; Lu et al., 2014). A few field studies have indeed produced results that support the parasitoid nectar provision hypothesis (English-Loeb et al., 2003; Tylianakis et al., 2004; Irvin et al., 2006; Gurr et al., 2016). These cases
are important in demonstrating one or more important aspects of the hypothesis, including sugar limitation by parasitoids, the use of supplemental nectar, increased parasitism rates in the presences of supplemental nectar, and improved biological control of pest arthropods (Heimpel and Jervis, 2005; Tena et al., 2015; Heimpel and Mills, 2017). It is also important to note that insects with a predatory larval stage and nectar-feeding adult stage are subject to similar life-history constraints as parasitoids are and some of these have also provided cases of successful nectar provisioning (e.g. Hickman and Wratten, 1996; Pineda and Marcos-Garcia, 2008). However, these inspiring cases of success have been the exception rather than the rule in tests of the parasitoid nectar provision hypothesis with many provisioning studies not leading to improved biological control (Heimpel and Jervis, 2005; Lee and Heimpel, 2005a). There does not seem to be a single correct explanation for failure of nectar supplementation to improve biological control. Proposed reasons for the failure of the parasitoid nectar provision hypothesis have ranged from a lack of sugar limitation on the part of parasitoids (e.g. Lee et al., 2006) to scenarios in which pest insects utilize supplemented nectar to greater effect than their parasitoids do (e.g. Baggen and Gurr, 1998). Broadly speaking, the inconsistency of supplemental nectar in improving biological control, along with some the postulated ecological explanations for cases of failure, can be seen as a microcosm of some of the five hypotheses for the failure of natural habitat to enhance natural
E-mail address: [email protected]. https://doi.org/10.1016/j.biocontrol.2019.01.012 Received 31 October 2018; Received in revised form 23 January 2019; Accepted 25 January 2019 Available online 28 January 2019 1049-9644/ © 2019 Elsevier Inc. All rights reserved.
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Under these circumstances, dispersal away from host patches prior to reproduction may be a more logical response to nectar feeding than retention in host patches. It follows that supplemental nectar provisions may fail to improve local biological control services by parasitoids, although overall or more distant parasitism rates may be improved. It is also important to note that dispersal away from sugar sources could improve local parasitism rates if it is very limited in distance, as noted above in the case of A. rhopalosiphi (Tylianakis et al., 2004). Thus the spatial scale of dispersal is a critical determinant of how parasitoid dispersal behavior affects biological control under conditions of habitat diversification in general, and nectar supplementation in particular (Corbett, 1998).
biological control that Tscharntke et al. (2016) outlined. It is also consistent with a recent worldwide meta-analysis of habitat manipulation for the purpose of biological control (Karp et al., 2018) that revealed a lack of consistency of diversified habitats in improving biological control services. These patterns are a clear reminder that the discipline of conservation biological control is still searching for the ‘right forms of biodiversity’ that need to be implemented to consistently and predictably improve biological control (Heimpel and Mills, 2017). I outline here a hypothesis that I believe was first articulated by Lee and Heimpel (2005b) to explain at least a subset of some of the failures of nectar supplementation to improve biological control of insect pests by parasitoids in experimental or farm-based settings. This hypothesis posits that sugar feeding can induce parasitoid dispersal away from nectar sources. It contradicts an implicit (and sometimes explicit) assumption of the parasitoid nectar provision hypothesis that parasitoids are retained in the local area by nectar-feeding and that they attack more hosts adjacent to nectar sources as a result (Wäckers and Lewis, 1994; Lewis et al., 1998). What is the support for the hypothesis of retention of parasitoids by nectar? Some evidence comes from studies of the tachinid Lixophaga sphenophori, which is attracted and retained by flowering plants at the edges of sugarcane fields, where more hosts are attacked (Leeper, 1974; Topham and Beardsley, 1975). Also, some elegant small-plot field studies showed that the braconid Microplitis croceipes will stay in the local area to attack hosts longer in the presence of sugar meals (Takasu and Lewis, 1995; Stapel et al., 1997). And Lavandero et al. (2005) reported higher levels of parasitism adjacent to flowering buckwheat by the parasitoid Diadegma semiclausum despite the fact that these parasitoids are highly mobile. In all of these systems, it does appear that sugar feeding led to some degree of parasitoid retention. A number of studies have shown that sugar-fed parasitoids respond to host-related cues in laboratory studies (e.g. Lewis and Takasu, 1990; Takasu and Lewis, 1993, 1996; Wäckers, 1994; Jacob and Evans, 2000), but it does not necessarily follow from these studies that sugar feeding leads to local retention in field settings. I argue here that an alternative hypothesis – that sugar-feeding induces parasitoid dispersal, not retention – is worth considering. A number of studies from the literature are consistent with such a reaction to sugar feeding. First, Wäckers (1994) found that sugar – fed Cotesia rubecula engaged in more flight behavior than starved individuals did in a wind tunnel setting. Similar results were found for the parasitoids Trichogramma minutum and Tetrastichus planipennisi (Forsse et al., 1992; Fahrner et al., 2014). Second, in a field study in which nectar sources were marked with the trace element Rubidium, Freeman Long et al. (1998) captured more marked Hyposoter sp. parasitoids 75 m from the marked plants than 6 m or less from the marked plants. Short-range dispersal may also be responsible for ‘surprisingly’ low parasitism levels by the aphid parasitoid Aphidius rhopalosiphi directly adjacent to a flowering strip in the very careful studies done by Tylianakis et al. (2004). But why would parasitoids disperse after feeding on sugar? The answer to this question must lie at least in part in the dynamics of adaptive foraging behavior by parasitoids, and in particular, whether there is an advantage to be gained by spreading eggs out over a series of host patches. Although it may at first seem that all or most hosts in a patch should be used before leaving one host patch in search of another in order to minimize opportunity costs and mortality during dispersal, this may not necessarily be the case. Montovan et al. (2015) discussed a number of reasons for early patch leaving and I focus on four here that can favor leaving patches before their quality declines due to depletion: (i) avoidance of self-superparasitism (Rosenheim and Mangel, 1994), (ii) avoidance of density-dependent hyperparasitism (Ayal and Green, 1993; Mackauer and Völkl, 1993), (iii) ‘spreading the risk’ of catastrophic mortality in a single patch (Cronin and Strong, 1993a), and (iv) reduction in the risk that one’s offspring engage in inbreeding. If any of these (or other) dynamics lead to selection for early patch leaving, sugar-feeding (or more generally, high energy reserves) may provide the resources necessary for successful dispersal to another host patch.
2. Hypotheses for adaptive patch-leaving in parasitoids with implications for sugar-fueled dispersal 2.1. Risk of self-superparasitism The term superparasitism is used to describe the act of parasitizing hosts that already contain conspecific eggs or larvae. This behavior can be adaptive if the previously parasitized host was attacked by a different female (van Alphen and Visser, 1990; Mangel, 1992) but is almost always considered maladaptive if the previously parasitized host was attacked by the foraging female herself (Rosenheim and Mangel, 1994; Desneux et al., 2009; but see van Alphen and Visser, 1990 for cases in which this can be adaptive). This latter behavior is known as ‘self-superparasitsm’, and if parasitoid females cannot discriminate between hosts that they themselves have parasitized and healthy hosts, they run the risk of such self-superparasitism, and thus incurring costs associated with egg and time wastage as well as exposing their offspring to competition against each other. Rosenheim and Mangel (1994) used two separate modeling approaches to show that parasitoids with poor discrimination abilities were selected to leave patches after only a very small fraction of the hosts had been used, solely to avoid self-superparasitism. Another way to view this result is that diminishing returns of foraging are reached earlier during patch visitation for parasitoids that have poor rather than good discriminatory abilities (Montovan et al., 2015). Patch leaving was favored in Rosenheim and Mangel’s (1994) models by other factors as well, including low mortality during travel between patches, area-restricted search coupled with poor discrimination, and a high risk of egg limitation (Rosenheim and Mangel, 1994). One of these latter hypotheses was confirmed in a study on an egg parasitoid of planthoppers that utilized a higher proportion of patches after long dispersal events (Cronin and Strong, 1999). This suggests that female parasitoids were more willing to risk self-superparasitism when the risk of mortality during travel between patches was greater. The issue of spatial scale was not explicitly addressed in these models and it was assumed that the risk of self-superparasitism was zero in new host patches. Whether the dynamics identified by these patchleaving rules will affect the dynamics linking parasitoid sugar feeding and biological control will depend on issues of scale – particularly whether different host patches are found in the same general vicinity (e.g. on the same plant) and can thus be found by trivial dispersal events or whether long-distance dispersal is needed to locate host patches that sufficiently decrease the chance of self-superparasitism. In any case, the outcomes of the models developed by Rosenheim and Mangel (1994) suggest that parasitoids with poor discriminatory abilities should have more to gain by using sugar meals to fuel travel among patches of hosts than parasitoids with high discriminatory ability. I therefore predict a higher chance of success in improving parasitism rates by using supplemental sugar for parasitoid species with good rather than poor discrimination abilities. This hypothesis has not been explicitly tested, but a comparison among some mymarid species with divergent discrimination abilities may be able to provide insights into an important recent conservation 37
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biological control success. Detailed field studies of the mymarid parasitoid Anagrus delicatus attacking patches of planthopper eggs embedded within Marsh grass tissue revealed extremely low levels of proportional patch use, with an average of only 18% of possible hosts used per patch under normal conditions (Cronin and Strong, 1993a). In a separate study, however, Cronin and Strong (1993b) showed that A. delicatus has very poor discrimination ability and thus suffers from a very high risk of self superparsitism (see also Bouskila et al. (1995) for a complementary explanation involving host quality). In fact, it was these data as well as information on potential egg limitation that were used to parameterize Rosenheim and Mangel’s (1994) models and thus led to the insights outlined above. By themselves, these insights do not go far in addressing our hypothesis linking host-patch use, parasitoid dispersal and conservation biological control. But interestingly, some other species of mymarids exhibit much higher levels of discrimination of parasitized hosts, allowing the avoidance of self-superparasitsm, and these species (as expected) utilize a much higher proportion of host patches (Hasan, 1982, 1984; Rosenheim and Mangel, 1994) and thus presumably engage in less dispersal between patches. And one of these species, A. obtibalis, has recently been shown to respond positively to nectar supplementation in a very successful conservation biological control intervention in South-East Asia and China (Gurr et al., 2016; Zhu et al., 2018). While nectar feeding has not been demonstrated for A. obtibalis in the field, laboratory studies show the potential for this (Zhu et al., 2013), and the field data that have been presented are consistent with a nectar subsidy improving biological control of rice brown planthoppers, the main host of A. obtilis. And pursuant to our hypothesis, the fact that this parasitoid species has high discrimination abilities may aid the effectiveness of nectar subsidies by facilitating the retention of parasitoids in the vicinity of the floral plantings. A different study demonstrated higher levels of parasitism of by one or more unidentified species of Anagrus of eggs of pest leafhoppers in vineyards adjacent to floral plantings as well (English-Loeb et al., 2003) but discrimination and patch-use behaviors of this species are not known as far as I am aware.
maximal patch use. Montovan et al. (2015) concluded that the risk of density-dependent hyperparasitism contributed to the pattern of submaximal patch use and dispersal among patches found for this parasitoid. Based on the considerations presented here I propose the following hypotheses with respect to hyperparasitism and sugar supplementation. First, parasitoids that are subject to density-dependent hyperparasitism at the local scale will be selected to engage in early patch leaving and thus will be more likely to engage in relatively long-distance dispersal under conditions of enhanced sugar availability than parasitoids not subject to density-dependent hyperparasitism. Thus, density-dependent hyperparasitism will translate into lower effectiveness of nectar supplementation as a biological control strategy. While these hypotheses have not been tested per se, a link between hyperparasitism and the dispersal of primary parasitoids was established by Holler et al. (1994), who showed that the aphid parasitoid Aphidius uzbekistanicus actively dispersed away from arenas that contained adult hyperparasitoids or their traces. Also, Lee and Heimpel (2005a) found strong density-dependent hyperparasitism of the parasitoid Diadegma insulare by the chalcidid Conura side in a field study. Interestingly, this same study showed that supplemental nectar did not enhance parasitism by D. insulare, consistent with the predictions articulated above. The main hypothesis explaining the lack of an effect of nectar supplementation on biological control in these studies was an absence of sugar limitation for D. insulare (Lee et al., 2006; Lee and Heimpel, 2008) but a response to density-dependent hyperparasitism should be added as a potential determinant as well. 2.3. Risk spreading If there is a non-trivial chance of complete patch failure after parasitism and before parasitoid eclosion (e.g. from factors such as vertebrate herbivory or plant senescence for herbivorous hosts), it may be possible that spreading eggs over many patches (and therefore, early patch leaving) is selected for. This is the explanation that Cronin and Strong (1993a) gave for early patch leaving in A. delicatus that was discussed above. This explanation – known as spatial risk spreading (or bet-hedging) – has intuitive appeal, but conditions favoring it are stringent. These conditions include very small populations, and temporal variation in mortality risk (Godfray, 1994; Hopper, 1999; Hopper et al., 2003). I am not currently aware of host-parasitoid systems that are subject to these conditions – particularly ones that involve targets of conservation biological control. In the event that such conditions are discovered, I predict that parasitoids that engage in a risk-spreading strategy would be at risk of using supplementary sugar meals to enhance dispersal and thus not be retained near supplementary nectar sources.
2.2. Density-dependent hyperparasitism If the risk of parasitoid mortality increases with the parasitism rate, it pays to keep per-patch rates of primary parasitism low. In principle, this applies to all sources of mortality to immature parasitoids, but since most predators that would have such an effect are likely intraguild predators and would thus more likely respond to host rather than parasitoid density, this hypothesis applies primarily to hyperparasitoids. Having said this, density dependent intraguild predation could translate to a higher mortality risk for immature parasitoids as well (e.g. Chacón and Heimpel, 2010; Frago, 2016). For simplicity though, I focus on the case of hyperparasitoids here. Under conditions of density-dependent hyperparasitism, early patch leaving may be optimal (Ayal and Green, 1993; Mackauer and Völkl, 1993; Weisser et al., 1994). As discussed above, optimal patch leaving under this hypothesis will be modified by factors such as the risk of mortality during inter-patch movement and egg limitation. Also – the relevance of these dynamics for conservation biological control will depend upon the spatial scale at which they operate. Density-dependent hyperparasitism has been found in some studies (Horn, 1988 [Cited by Weisser et al. (1994)]; Lee and Heimpel, 2005a; Montovan et al., 2015) but not others (Muller and Godfray, 1998; van Veen et al., 2002) although the response can be complex, depending on spatial scale and other factors (Schooler et al., 2011; Chow, 2000; van Veen et al., 2002; Lee and Heimpel, 2005a). Montovan et al. (2015) demonstrated strong positive density dependent parasitism of the ichneumonid Hyposoter horticola in natural settings in Finland and determined that per-patch fitness gains peaked at 70% parasitism due to the dangers of density dependent hyperparasitism. While this does not indicate particularly strong early patch leaving, it illustrates sub-
2.4. Inbreeding Spreading eggs out over a series of patches could decrease the risk that one’s offspring engage in inbreeding. While some parasitoid taxa appear to be relatively tolerant of inbreeding, others show strong inbreeding depression (Henter, 2003). In particular, many parasitic Hymenoptera suffer from a severe form of inbreeding depression known as complementary sex determination (CSD). Under CSD, sex is determined by one or more highly polymorphic ‘sex loci’. Sex locus heterozygotes develop as females, and sex locus homozygotes develop as diploid males (unfertilized hemizygotes develop as haploid males as per standard haplo-diploidy) (Heimpel and de Boer, 2008). Diploid males are inviable in some species and in other species can effectively sterilize females that accept them as mates (Stouthamer et al., 1992; Harpur et al., 2012; de Boer et al., 2007). Among the parasitic hymenoptera, CSD is only known in the superfamily Ichneumonoidea with members of other superfamilies exhibiting greater tolerance to inbreeding (Heimpel and Lundgren, 2000; Asplen et al., 2009). And CSD is only 38
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Acknowledgements
partly expressed within the Ichneumonoidea, with some taxa exhibiting it and others not (Asplen et al., 2009). Also – the details of CSD expression vary among species that have it, and this results in variability in the strength of inbreeding depression. Thus, in at least one parasitoid species with CSD diploid males are almost completely viable and can sire diploid daughters (Elias et al., 2009), and in others sex is determined at two or more loci in a way that requires much more extreme inbreeding to produce diploid males (De Boer et al., 2008, 2012, 2015; Carabajal Paladino et al., 2015; Weis et al., 2017). And finally, the mating system of parasitoids with CSD is usually based on outbreeding strategies (including dispersal) as a means of avoiding diploid male production (Antolin and Strand, 1992; Ode et al., 1995, 1998; Heimpel, 1997). Given these considerations, I hypothesize that female parasitoids with single-locus CSD (or other forms of inbreeding depression) engage in early patch leaving as a means of decreasing the likelihood that their offspring mate with one another and producing sterile diploid males or suffer other consequences of inbreeding. I further hypothesize that such females will be more likely to utilize sugar meals to engage in mediumto long-distance dispersal than females of parasitoid species that do not suffer inbreeding depression. I therefore predict a higher likelihood of successful biological control improvement from nectar supplementation targeting parasitoid species with low rather than high risk of inbreeding depression. While this hypothesis would seem to be relatively easy to test using comparative data, in my estimation the data base is still too small to conduct a proper comparative test. What would be needed are more studies of nectar supplementation targeting parasitoids with known inbreeding biologies, including both the magnitude of inbreeding depression itself and the ability of the parasitoids to avoid inbreeding.
I thank the organizers of this special feature, Lessandro Gontijo and William Snyder, for the invitation to submit a contribution and the comments of three anonymous reviewers for advice on the ms. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.biocontrol.2019.01.012. References Antolin, M.F., Strand, M.R., 1992. Mating system of Bracon hebetor (Hymenoptera: Braconidae). Ecol. Entomol. 17, 1–7. Asplen, M.K., 2018. Dispersal strategies in terrestrial insects. Curr. Opin. Insect Sci. 27, 16–20. Asplen, M.K., Whitfield, J.B., De Boer, J.G., Heimpel, G.E., 2009. Is single-locus complementary sex determination the ancestral mechanism for hymenopteran haplodiploidy? J. Evol. Biol. 22, 1762–1769. Ayal, Y., Green, R.F., 1993. Optimal egg distribution among host patches for parasitoids subject to attack by hyperparasitoids. Am. Nat. 141, 120–138. Baggen, L.R., Gurr, G.M., 1998. 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3. Conclusions The over-arching hypothesis that I have posed here is that the females of some parasitoid species may be selected to engage in mediumor long-distance dispersal upon feeding on nectar and that this behavior could compromise the successful deployment of supplemental nectar to improve biological control at the local scale. I further suggest that this dispersal behavior is likely to vary among species based on optimal patch-use and dispersal behavior in a predictable way that is based upon the dynamics of early patch leaving behavior. The dynamics that I focused on were (i) the ability to avoid self-superparasitism (but note that similar arguments could be made for superparaitism in general; Montovan et al. (2015)), (ii) the risk of density-dependent hyperparasitism, (iii) the advantage of spatial risk-spreading in terms of oviposition, and (iv) risks associated with inbreeding. In each case, early patch leaving is expected if fitness reductions occur before patch depletion dynamics would dictate patch leaving (see Wajnberg, 2006). In my estimation there is inadequate biological knowledge of the parasitoid species that have been subjected to nectar supplementation experiments to perform meaningful comparative tests of the hypotheses that I have presented at the time of this writing. However, some directed laboratory studies of parasitoids have already shown that sugarfeeding can enhance the tendency to disperse (e.g. Wackers, 1994; Fahrner et al., 2014). A next step could be to take this approach into the field. Indeed, a number of authors have argued for the importance of understanding the dynamics of dispersal in parasitoids (Corbett and Plant, 1993; Corbett, 1998; Cronin and Reeve, 2005; Heimpel and Asplen, 2011; Schellhorn et al., 2014; Asplen, 2018) and I would suggest investigating in particular the effects of sugar feeding on parasitoid dispersal behavior to gain more insights into the potential effects of nectar supplementation strategies in conservation biological control. 4. Author statement GEH conceived of all ideas presented in this ms. 39
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