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Ann. Zool. Fennici 54: 83–95 ISSN 0003-455X (print), ISSN 1797-2450 (online) Helsinki 15 May 2017 © Finnish Zoological and Botanical Publishing Board 2017 Ilkka Hanski: The legacy of a multifaceted ecologist The roles of trophic interactions, competition and landscape in determining metacommunity structure of a seed-feeding weevil and its parasitoids Marko Nieminen1,2 & Saskya van Nouhuys1,3 1) Department of Biosciences, P.O. Box 65, FI-00014 University of Helsinki, Finland 2) Centre for Biodiversity Genomics, Biodiversity Institute of Ontario, University of Guelph, Guelph, ON, N1G 2W1, Canada 3) Department of Entomology, Cornell University, Ithaca, NY 14850, USA Received 13 Feb. 2017, final version received 12 Apr. 2017, accepted 11 Apr. 2017 Nieminen, M. & van Nouhuys, S. 2017: The roles of trophic interactions, competition and land- scape in determining metacommunity structure of a seed-feeding weevil and its parasitoids. — Ann. Zool. Fennici 54: 83–95. Community composition is determined by attributes of the environment, individual spe- cies, and interactions among species. We studied the distributions of a seed weevil and its parasitoid and hyperparasitoid wasps in a fragmented landscape. The occurrence of the weevil was independent of the measured attributes of the landscape (patch connectivity and resource availability). However, between habitat-patch networks, weevil density decreased with increasing parasitism, suggesting top-down control, especially in the north. Parasitism was mostly due to a specialist and a generalist that appeared to compete strongly. This competitive interaction was strongest at high patch-connectivity, perhaps due to a trade-off of local competitive ability and dispersal. Finally, the abundance of the generalist hyperparasitoid was unrelated to landscape or host-species abundance. The snapshot presented by these data can best be explained by top-down effects, interactions among species, host ranges, and patch configuration in the landscape, but not by local host-plant abundance. Introduction landscape are considered a metacommunity, then the spatial structure and heterogeneity of the Communities are made up of species living in landscape can contribute to the complexity of the a shared habitat. Which species are present, metacommunity (Holt 2002, Amarasekare 2008). their abundances and the complexity of the food To understand the structure of a community, as web can depend on attributes of the habitat and well as its dynamics and resilience, we must the surrounding landscape. Many species in a determine the roles of both spatial factors and community also interact so their persistence and biotic interactions (Leibold et al. 2004). This is prevalences are interdependent. This is espe- most tractable for species with narrow resource cially true for strongly interacting species such requirements and strong interactions with other as those competing for a shared resource, or species (van Nouhuys & Hanski 2005). those in predator–prey relationships (Cornell & A community made up of host plants, their Lawton 1992). Finally, when species inhabiting a insect herbivores, parasitoids and hyperparasit- 84 Nieminen & van Nouhuys • ANN. ZOOL. FENNICI Vol. 54 oids provides such a scenario. There are several landscape and local host plant abundance. The studies of plant–herbivore–parasitoid commu- species interactions were rates of parasitism and nities that highlight specific attributes of the hyperparasitism. Out of the many possible out- system in determining the species abundances, comes, we expected that the weevil abundance such as local plant density (Hambäck & Englund would be positively associated with the local P. 2005), host-plant quality (Price & Hunter 2015, lanceolata abundance due to resource concen- Riolo et al. 2015), and higher trophic level tration in terms of apparency (Root 1973) and interactions (Cronin 2007). Only a handful of availability (Rand et al. 2014), and that weevil studies were on a scale appropriate to address abundance would also increase with habitat patch the role of spatial configuration of the habitat connectivity because highly connected patches in determining community or metacommunity provide a large stable resource over time (Hanski structure (e.g. Amarasekare 2000, Harrison et 1998). The same argument can be made for the al. 2005, Laszlo & Tothmeresz 2013, Cronin parasitoids, in which case we would expect a & Reeve 2014, Riolo et al. 2015). Both land- high rate of parasitism where the plant and host scape structure and local species interactions are weevil are abundant. On the other hand, parasit- clearly important in determining the composition oids can cause host population size to decrease, and dynamics of some communities, such as the which would diminish the association of weevil Glanville fritillary butterfly and its parasitoids population size with plant abundance (Jones et al. and hyperparasitoids in the Åland Islands, Fin- 1994, Walker et al. 2008), and could increase the land (van Nouhuys & Hanski 2005). But the rel- association of patch connectivity with host and ative importance of these intrinsic and extrinsic parasitoid population sizes (Hassell 2000). We factors must vary depending on attributes of the would also expect competing parasitoids to be landscape such as structure and primary produc- negatively associated (Hassell & Waage 1984), tivity; attributes of the species such as resource and to have contrasting distributions in the land- breadth, mobility, and size; as well as food web scape if, for example, there is a trade-off between complexity, and the spatial scale of the study. dispersal ability and local competitive ability The monophagous weevil Mecinus pascuo- (Calcagno et al. 2006). Going up one trophic rum (Coleoptera: Curculionidae) feeds on the level, we expected hyperparasitoids to influence developing seeds of Plantago lanceolata (Plan- the overall rate of parasitism and the competitive taginaceae). In the Åland Islands, the weevil is relationship between host parasitoids (Sullivan part of the community of herbivores inhabiting & Völkl 1999, van Nouhuys & Hanski 2000), P. lanceolata in dry meadows, pastures and dis- the effects of which can depend on landscape turbed areas, where it is host to a community of connectivity (Holt & Hoopes 2005). Lastly, we parasitoids (Vikberg & Nieminen 2012, Niemi- expected the interactions among species to be nen & Vikberg 2015). The meadows are char- weaker with wider resource breadth or host range acterized as the setting for the long-term study (van Nouhuys 2005). These types of patterns of the metapopulation biology of the Glanville are predicted theoretically, and are important to fritillary butterfly Melitaea cinxia (Lepidoptera: understanding biodiversity as well as biological Nymphalidae) (Nieminen et al. 2004, Hanski control of insect pests (Holt 2002, Frago 2016, 2011, Ojanen et al. 2013, Fountain et al. 2016) Kaser & Ode 2016). There are many empirical and its parasitoids (Lei et al. 1997, van Nouhuys examples of subsets of them but they are seldom & Hanski 2005, Nair et al. 2016). addressed simultaneously on a large scale in a We studied the association of environmental natural system. factors and species interactions, with the abun- dance of the weevil M. pascuorum and its associ- ated parasitoids, using a sample of 6170 individu- Material and methods als collected from 18 patch networks in the Åland Islands in 2009. These data are described in Study species Nieminen and Vikberg (2015). The environmen- tal factors were latitude, patch connectivity in the Mecinus pascuorum is a monophagous seed- ANN. ZOOL. FENNICI Vol. 54 • Metacommunity structure of a seed-feeding weevil and its parasitoids 85 feeder of P. lanceolata. Females lay one egg the habitat in the landscape. The habitat patches per developing seed capsule, each larva usually are open meadows, pastures and disturbed areas consumes two seed capsules, and pupation takes where P. lanceolata grows. In total, we sampled place within the seed capsule (Dickason 1968, 643 habitat patches (size range 0.002–5.5 ha; Mohd Norowi et al. 1999). In the Åland Islands, see Table 1) between 29 July and 8 August adult emergence peaks around early August. 2009. Plantago lanceolata patches are naturally They overwinter as adults, and are most active in clustered in the landscape. These clusters were late May and June (Nieminen & Vikberg 2015). delineated into semi-independent patch networks Mesopolobus incultus (Hymenoptera: Ptero- (SINs) using the software SPOMSIM (Moilanen malidae) is a solitary primary parasitoid of M. 2004). The number of patches, their areas and pascuorum (e.g. Norowi et al. 2000). It is appar- distribution differed among SINs; for thorough ently a specialist on M. pascuorum in the Åland descriptions of the study sites see Nieminen et Islands, though there are records of other host al. (2004) and Ojanen et al. (2013). We collected weevils as well as Apion species feeding on samples from each patch in 18 SINs spread over Trifolium (see e.g. Baur et al. 2007). For further the Åland Islands (Fig. 1). The landscape struc- discussion see Nieminen and Vikberg (2015). ture was characterized based on the population Eupelmus vesicularis (Hymenoptera: Eupel- biology of the butterfly M. cinxia. However, it is mi dae) is a highly generalist species that, accord- relevant for any species dependent on P. lance- ing the literature acts as both a primary and a olata. For instance, the dynamics and evolution secondary parasitoid (Gibson

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