Density Dependence and Environmental Factors Affect Population Stability of an Agricultural Pest and Its Specialist Parasitoid William H
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Density dependence and environmental factors affect population stability of an agricultural pest and its specialist parasitoid William H. Morgan, Elisa Thébault, Colleen L. Seymour, F. J. Frank van Veen To cite this version: William H. Morgan, Elisa Thébault, Colleen L. Seymour, F. J. Frank van Veen. Density depen- dence and environmental factors affect population stability of an agricultural pest and its specialist parasitoid. BioControl, Springer Verlag, 2016, 62 (2), pp.175-184. 10.1007/s10526-016-9777-5. hal- 01512928 HAL Id: hal-01512928 https://hal.sorbonne-universite.fr/hal-01512928 Submitted on 24 Apr 2017 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License BioControl (2017) 62:175–184 DOI 10.1007/s10526-016-9777-5 Density dependence and environmental factors affect population stability of an agricultural pest and its specialist parasitoid William H. Morgan . Elisa The´bault . Colleen L. Seymour . F. J. Frank van Veen Received: 14 March 2016 / Accepted: 7 November 2016 / Published online: 10 December 2016 Ó The Author(s) 2016. This article is published with open access at Springerlink.com Abstract Host–parasitoid dynamics are intrinsically found evidence for higher parasitism rates near natural unstable unless the risk of parasitism is sufficiently vegetation at the field scale, and inverse host-density heterogeneous among hosts. Spatial aggregation of dependent and density-independent parasitoid aggre- parasitoids can contribute to this heterogeneity, gation at both the leaf scale and field scale. Therefore, stabilising host–parasitoid population dynamics and we conclude that natural vegetation plays a role in thereby reducing pest outbreaks. We examined the promoting stabilising aggregation of parasitoids, pos- spatial distribution of mango gall fly (Procontarinia sibly through provision of non-host resources (nectar, matteiana, Kiefer and Cecconi), a non-native pest of pollen), in this system. South African mango orchards, which is controlled by a single parasitoid (Chrysonotomyia pulcherrima, Keywords Conservation biological control Á Kerrich). We assessed whether spatial aggregation of Integrated pest management Á Parasitoid aggregation Á parasitoids is associated with proximity to natural Natural enemies Á Pest control vegetation and/or to host density-dependent and host density-independent factors at three spatial scales. We Introduction Handling Editor: Josep Anton Jaques Miret In agricultural landscapes, natural vegetation has been W. H. Morgan Á F. J. F. van Veen (&) associated with improved pest control (Thies and Centre of Ecology and Conservation, College of Life and Tscharntke 1999; Thies et al. 2011). In understanding Environmental Sciences, University of Exeter, Penryn the mechanisms behind this control, much of the focus Campus, Penryn, Cornwall TR10 9EZ, UK e-mail: [email protected] has been on the role of natural vegetation in encour- aging greater abundance and diversity of natural C. L. Seymour enemies (Bianchi et al. 2006). A less explored idea South African National Biodiversity Institute, is the role of natural vegetation in promoting aggre- Kirstenbosch Gardens, PVT Bag X7, Claremont 7735, South Africa gation of parasitoids (but see Thomson and Hoffmann 2013) and stabilising host–parasitoid population E. The´bault dynamics by providing a host ‘‘refuge’’ deeper within Institute of Ecology and Environmental Sciences - Paris, the crop (Holt and Hassell 1993). Specialist para- UMR 7618 (UPMC, CNRS, IRD, INRA, UPEC, Paris Diderot), Universite´ Pierre et Marie Curie, 7 Quai St sitoids have been shown to exert important long-term Bernard, 75005 Paris, France suppression of their host species, so the role of 123 176 W. H. Morgan et al. parasitoids in biocontrol is particularly important the commercial mango-growing region of South (Snyder and Ives 2001, 2003). However, the dynamics Africa, P. matteiana is controlled by one specialised, of simple host–parasitoid interactions are inherently non-native parasitoid: Chrysonotomyia pulcherrima unstable and prone to diverging oscillations, resulting (Kerrich), which was identified by studying the in extinction of one or both species, and cycles of high seasonal occurrence of the gall fly and its natural host abundance (Hassell 2000). A stable pest popula- enemies (Grove´ et al. 2003, 2004). C. pulcherrima is tion maintained at a low level by a specialist parasitoid an ectoparasitoid that was not intentionally released may therefore be more desirable for successful and is not reared in insectaries in South Africa. To our biocontrol. Integrated pest management programs that knowledge its provenance is also not known, but it tolerate a level of pest infestation below the economic may have arrived with its host in larval form. threshold could help maintain environmental quality Generally very little is known about the parasitoids and reduce unnecessary management activities and associated with gall-inducing insects (Raman et al. costs (Cameron et al. 2001; El-Wakeil 2010). 2009), but C. pulcherrima has a phenology that is Theoretically, host populations will be stabilised if well-synchronised with that of the gall fly, which is its the distribution of searching parasitoids is sufficiently only host. This synchronicity was determined through heterogeneous (Hassell et al. 1991). This has been rearing the host and its parasitoid over a three year defined through the ‘‘CV2 [ 1 rule’’, where the period (Mahmood Ur Rehman et al. 2013). squared coefficient of the variation (CV2) of the The interaction between P. matteiana and C. distribution of searching parasitoids is [1 (Hassell pulcherrima is an example of a simple host–parasitoid et al. 1990). Any variation in parasitism of hosts system, so is expected to be unstable and prone to between patches reduces searching efficiency as diverging oscillations, resulting in the extinction of parasitoid density increases, and two important one or both species (Hassell 2000). Yet in this sources of this variation are host density-dependent instance, the host–parasitoid interaction appears to (HDD) parasitoid aggregation, and host density-inde- be stable, with both species being described in South pendent (HDI) parasitoid aggregation (Hassell et al. African mango orchards for over 25 years by the 1991; Pacala and Hassell 1991). If heterogeneity is the South African Mango Growers Association (Botha key to stability, one would expect that in a homoge- and Kotze´ 1987). Botha and Kotze´ (1987) first nous agricultural setting simple host–parasitoid inter- investigated the galls when it was thought that P. actions would be particularly prone to diverging matteiana may be a vector for bacterial black spot. It is oscillations. Therefore, heterogeneity of risk to hosts conceivable that some form of parasitoid aggregation due to aggregation of parasitoids is vital for the is providing the stability needed for the stable persis- persistence of a stable host–parasitoid interaction tence of these two species. South Africa’s commercial (Taylor 1993). mango-growing region is characterised by orchards The mango gall fly (Procontarinia matteiana, surrounded by large areas of natural ‘‘bushveld’’ Kiefer and Cecconi; Diptera: Cecidomyiidae) is a vegetation (Granite Lowveld; Mucina and Rutherford recognised pest of mangos (Mangifera indica) across 2006), and it may be that natural vegetation provides the world, from South Africa, where its impact has one source of parasitoid aggregation. While not a been recorded by commercial mango farmers (Louw source of C. pulcherrima, the natural vegetation may and Labuschagne 2011), to Pakistan and India where provide other benefits such as shade, shelter, and food recordings are widespread (Jhala et al. 1987; Mah- sources in the form of pollen and nectar (Bianchi et al. mood Ur Rehman et al. 2013). Adult females lay their 2006). Supplementing diet with sugar resources has eggs on the underside of young leaves, and the been shown to confer improved fitness for parasitoids, emerging larvae burrow into the leaf tissue where they resulting in increases to longevity and potential begin to feed (Augustyn et al. 2013). Heavy infesta- fecundity (Tylianakis et al. 2004; Protasov et al. tions can result in deformed leaves that drop prema- 2007). In fact, previous studies in South African turely, and even cause die-back of new growth (Grove´ mango farms of P. matteiana and its parasitoid C. et al. 2002). Differential susceptibility exists between pulcherrima suggest that rates of parasitism were different cultivars of mango owing to varying degrees higher closer to the natural vegetation than in the of antibiosis that they exhibit (Githure et al. 1998). In middle of mango orchards (Henri et al. 2015). A 123 Density dependence and environmental factors affect population 177 beneficial effect of proximate natural vegetation for by gall flies: Tommy Atkins, which is a susceptible, parasitoids could conceivably result in aggregation at true-gall forming cultivar;