The Roles of Trophic Interactions, Competition and Landscape in Determining Metacommunity Structure of a Seed-Feeding Weevil and Its Parasitoids

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 landscape 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 species, 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 abundance of the weevil M. pascuorum and its associated 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 environmental 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 midae) 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 1995, Noyes 2013). of the phytopathogen Podosphaera plantaginis Females are brachypterous which limits their dis- that infects P. lanceolata are in part determined persal ability, but Gibson (1995) suggests that on by the same spatial landscape structure (Laine & a local scale the wasp is a superior competitor Hanski 2006). over other parasitoid species due to its wide host We collected P. lanceolata spikes from all range that includes primary parasitoids as hosts. parts of each patch. The number of spikes sam- Eupelmus vesicularis has been presumed to attack pled from each patch was proportional to the both M. incultus and M. pascuorum, but see the abundance of P. lanceolata in it. Each spike section ‘Comparison of Mesopolobus incultus and was collected from a different plant. When the Eupelmus vesicularis adults’ below. number of spikes in a patch was very low, we Baryscapus endemus (Hymenoptera: Eulo collected at most 10% of them. This proce- phidae) is a hyperparasitoid (Graham 1991) dure resulted in a sample of 1–161 spikes per which attacks parasitoid wasps from the family patch (30.7 on average). We aimed to collect Pteromalidae (Noyes 2013). In this community, spikes with ripe seeds only. Spikes were placed it is highly likely to be a parasitoid of M. incul- individually in plastic tubes in the laboratory, tus but not E. vesicularis (Nieminen & Vikberg and emerged insect individuals were transferred 2015). into coded Eppendorf tubes after about a month for identification by experts. Mortality during rearing was not scored, but based on our earlier Landscape, sampling and rearing experience it was likely low and unbiased due to uniform laboratory conditions. Details of sam- We studied factors determining metacommunity pling and rearing can be found in Nieminen and structure of the seed-feeding weevil M. pascuo- Vikberg (2015). rum and its associated parasitoids by systemati- cally collecting naturally infested P. lanceolata seed spikes from habitat patches in a well char- Comparison of Mesopolobus incultus acterized landscape in the Åland Islands, Fin- and Eupelmus vesicularis adults land. We kept the spikes under laboratory conditions until weevils and parasitoids emerged and We compared the sizes of adult M. incultus and then analyzed the occurrence of the species with E. vesicularis wasps to infer whether the latter respect to each other, and to the configuration of species might have been a primary parasitoid of 86 Nieminen & van Nouhuys • ANN. ZOOL. FENNICI Vol. 54 M. . NA 0.82 0.74 0.81 0.82 0.82 0.84 0.90 0.81 0.74 0.76 1.0 0.73 0 0.84 0.85 1.0 0.91 of Rate of pascuorum parasitism 4 1 1 1 4 3 0 0 0 0 3 18 21 59 19 50 23 142 reared No. of B. endemus

5 5 4 1 1 4 92 No. of E. vesicularis

11 29 22 55 13 25 302 reared incultus No. of M.

8 3 6 0 0 1 0 0 1 3 13 26 73 37 86 21 64 29 124 402 156 109 189 121 121 357 181 266 784 446 275 688 103 158 237 164 reared No. of M.

M. pascuorum 8 6 4 2 0 3 9 1 1 1 41 15 33 26 13 39 19 13 pascuorum No. of patches occupied by

) in 2 46.0 48.0 14.5 92.1 50.7 90.4 82.1 NA NA NA 2008 148.5 244.8 255.6 348.6 315.5 213.9 108.5 (m 3308.6 coverage Sum of PL 3.38 0.15 8.17 2.97 3.25 5.22 1.67 4.85 3.65 0.62 1.13 0.61 2.85 1.61 3.51 Mean connectivity 0.38 5.85 6.10 2.31 0.88 2.01 3.44 1.79 2.14 1.24 4.99 1.91 6.76 3.10 8.54 (ha) area Total 12.3 39.8 12.3 25.9 10.8 habitat 80 332 808 189 19.0 300 149 243 275 108 891 441 100 1121 1321 1045 no. of patches spikes in occupied Corrected 369 814 546 139 662 27 194 297 509 627 298 213 1103 5565 690 1616 1780 1546 1222 1004 No. of spikes sampled 8 11 11 20 57 53 30 70 33 64 14 34 14 23 32 17 No. of patches sampled 11 11 21 68 61 83 89 39 73 19 34 19 22 37 18 12 43 112 172 109 no. of Current patches

27 9 Table 1. Summary of the characteristics patch networks. Table SIN 2

57 36 37 40 47 50 11 63 106 75 108 111 116 117 123 ANN. ZOOL. FENNICI Vol. 54 • Metacommunity structure of a seed-feeding weevil and its parasitoids 87

Fig. 1. Map of the Åland Islands showing the sampled patch networks (SINs) shaded in pink (high weevil occurrence) and blue (low weevil occurrence). Each gray dot represents a Plan- tago lanceolata patch. The number associated with each SIN is the ID number.

M. pascuorum, in which case most E. vesicularis Statistical analyses individuals would be relatively large, or if it was both a primary parasitoid as well as a hyperpara We used unweighted least-squares linear regres- sitoid of M. incultus. If that were the case then sion (Statistix 10.0, Analytical Software, Tal- there would be two size classes of E. vesicularis, lahassee, FL) to model associations of weevil one of which being smaller than M. incultus. abundance and parasitism rates of each wasp We randomly selected one storage box of reared species with various variables. We modeled the point-mounted individuals, and measured the mean abundance of weevils per spike (log-trans- length of each under a stereomicroscope with an formed) as a function of average connectiv- ocular scale (0.05 mm accuracy). All individuals ity of SINs, latitude, abundance of host plants missing some body part(s) or glued in a curved (log-transformed), total parasitism rate (number position were excluded. The size measure was of parasitoid individuals/[number of parasitoid the body length from the front of the head to individuals + number of weevil individuals]) the end of abdomen (excl. ovipositor). A total of and their first-order interactions. The mean per- 346 female and 232 male E. vesicularis, and 66 spike weevil abundance was calculated for the female and 59 male M. incultus were measured. occupied habitat patches within each SIN. The Many parasitoids, including facultative total number of spikes sampled from several hyperparasitoids can use host species of two patches was not recorded (missing values: SIN sizes by using large hosts for female offspring IDs 11, 27, 37, 40, 75 and 116 one patch; SINs and small hosts for male offspring (Macedo et 36 and 47 two patches; SIN 57 six patches). For al. 2014). To test whether E. vesicularis might be these missing values we used the median of the doing this we compared the SIN level sex ratio recorded values from the SIN the patch was in. of E. vesicularis associated with rate of parasit- The total weevil abundance in a SIN was defined ism (E. vesicularis/all parasitized and unpara- as the sum of both weevils and parasitoids that sitized weevils) or potential hyperparasitism (E. emerged in the rearing. Abundance of host plants vesicularis/[M. incultus + E. vesicularis]). was the sum of P. lanceolata coverage per SIN 88 Nieminen & van Nouhuys • ANN. ZOOL. FENNICI Vol. 54 in 2008. Host-plant coverage was not estimated Results for SINs 2, 75 and 106 in 2008. We estimated the host-plant coverage for these SINs by multi- The weevil M. pascuorum was present in 17 of plying the mean coverage (5.745) of all patches the 18 patch networks sampled. However, its in this study by the number of patches in the distribution at the landscape scale was strongly SIN. The spatial structure of the landscape can bimodal. In eight mostly northern SINs weevils be quantified in several ways. We used average were found in less than 9% of the patches, and connectivity of patches within a SIN because in 10 SINs more than 39% of the patches were it incorporates total area of habitat, patch size occupied (Table 1 and Fig. 2A–B). The reason and distance between patches, which are all for this spatially correlated bimodality (Fig. 1) is strongly correlated. The average connectivity not explained by the effects of sampling effort, was determined by first calculating the connec- the total habitat area, average connectivity of tivity (sensu Moilanen & Nieminen 2002) of patch networks, latitude or the abundance of the each patch based on its proximity to all other host plant (Figs. 2 and 3C). P. lanceolata patches, and the sizes of those Within occupied habitat patches within SINs, patches, with mean dispersal distance of 0.25 km the mean number of weevils per spike was 0.80 (dispersal kernel α = 0.025), and then averaging (SD = 0.63), with at most 2.1 per spike. The the connectivities of the patches within each SIN density of weevils was unrelated to latitude, (Table 1). We incorporated latitude to account habitat patch connectivity in the patch network, for the apparent north–south gradient in weevil and local density of P. lanceolata. However, abundance (see Fig. 1). there was a strong negative association between We modeled rates of parasitism (the frac- weevil density and the rate of parasitism (Fig. 3A tion of hosts parasitized) by the parasitoids E. and Table 2; t = –4.89, p = 0.002). vesicularis and M. incultus as a function of The primary parasitoid M. incultus was pres- average connectivity, latitude, total host weevil ent in all but one of the patch networks occupied abundance (log-transformed), parasitism rate by by the weevil, parasitizing 45%–100% of the the other primary parasitoid species and their weevils sampled (mean rate = 0.65, SD = 0.16). first-order interactions. For M. incultus we also The rate of parasitism by M. incultus was low used the parasitism rate by the hyperparasit- where the rate of parasitism by E. vesicularis oid B. endemus. We modeled the parasitism was high (Fig. 3B and Table 2; t = –3.14, p = rate (the fraction of hosts parasitized) of the 0.009). Once the strong positive association with hyperparasitoid B. endemus as a function of latitude was taken into account by using the average connectivity, latitude, total host abun- residuals of the regression of M. incultus para- dance (logn + 1-transformed), total abundance of sitism rate vs. latitude as the dependent variable,

E. vesicularis (logn + 1-transformed) and their rate of parasitism was found to be related land- first-order interactions. In the analysis of M. scape connectivity and competition. Specifically, incultus parasitism rate, there were several pos- where patch connectivity was high (patches clus- sible best statistical models because the vari- tered together) the rate of parasitism by M. ables latitude and weevil abundance were highly incultus tended to be low (Table 2; t = –2.23, p = correlated. Therefore, as a post-hoc analysis, 0.047). we used residuals of the linear regression of The parasitoid E. vesicularis was present the parasitism rate of M. incultus as a function in all but two of the patch networks occupied of latitude as the dependent variable in order to by the weevil host, parasitizing 5% to 29% of remove the strong effect of latitude. To compare the weevils sampled (mean rate = 0.18, SD = the sizes of the parasitoids M. incultus and E. 0.09). The rate of parasitism by E. vesicularis vesicularis we used an unpaired two-sample was unrelated to habitat patch connectivity, lat- t-test. Finally, we tested the associations of SIN itude and host abundance (Fig. 3D). However, level sex ratio of E. vesicularis with the rate of it decreased with the rate of parasitism by M. parasitism and potential hyperparasitism with incultus (Fig. 3B and Table 2; t = –5.63, p = Spearman’s rank-order correlation. 0.0001). In order to determine the probable tro- ANN. ZOOL. FENNICI Vol. 54 • Metacommunity structure of a seed-feeding weevil and its parasitoids 89 phic level of E. vesicularis, we compared its size p 0.0002 0.0002 0.0001 0.0001 with M. incultus. In both wasp species, females 0.0004 0.009 0 0.553 0 0.171 0 (E. vesicularis: mean length = 1.80 mm, SD = 0.27; M. incultus: mean length = 1.76 mm, SD =

0.25) were significantly longer than males (E. t vesicularis: mean length = 1.32 mm, SD = 0.21; 4.59 0.61 1.46 –4.89 –5.63 M. incultus: mean length = 1.21 mm, SD = 0.18) –3.14 –2.23 0.047 0

(t-test: E. vesicularis: t577 = 23.83, p < 0.0001;

M. incultus: t124 = 13.83, p < 0.0001). There was

no difference in length between the two species F 23.95 31.71 21.07 (t-test: females: t411 = 1.173, p = 0.5; males: t292 = 4.04, p = 0.5). The sex ratio of E. vesicularis among SINs was marginally female-biased

(average female:male ratio: 0.54, SD = 0.14). No df 1,13 1,14 correlations were found between the SIN level 1,14 sex ratio of E. vesicularis and the rate of parasitism (Spearman’s correlation: rS = –0.325, n = 13, p = 0.280) or the potential rate of hyperparasitism (rS = –0.289, n = 13, p = 0.334). The hyperparasitoid B. endemus was present in all but two of the habitat-patch networks occu- parasitism rate pied by its wasp host M. incultus. It parasitized the wasp in two to 26% of the weevils sampled (mean rate = 0.09, SD = 0.07). The rate of hyperparasitism was unrelated to any of the factors parasitism rate ¥ E. vesicularis measured. Total parasitism rate Total M. incultus parasitism rate Predictor variable(s) Discussion E. vesicularis Connectivity Log(total weevil abundance)

The weevil

The biotic factors that influence population dynamics of a species can be resource limitation (bottom-up) and predators, parasites and dis- eases (top-down) interactions (Hunter & Price 1992). Classically, to observe top-down control we should detect delayed density dependence over time in the relationship between a predator and prey (Hunter et al. 1997) or conduct a predator exclusion experiment (Harrison & Cappuc- cino 1995, Kasparson 2016). At the scale of this M. incultus parasitism rate vs . latitude study, there was no association of habitat connectivity or resource availability with density of M. pascuorum. Habitat patch connectivity may not be important because the patches are rela- parasitism rate tively stable, and large, and the weevil is very small (2–3 mm) so it may not be very mobile. Further, the vast majority of P. lanceolata seeds E. vesicularis Residuals of the regression Table 2. Results of the unweighted least-squares linear regression analysis weevil abundance and rates parasitism. Table Dependent variable Log(mean weevil abundance per spike) were left uneaten so we expected that the resi- Connectivity 90 Nieminen & van Nouhuys • ANN. ZOOL. FENNICI Vol. 54

40 A B

N 500

30 e

50 20 Weevil abundanc

10 5 Number of occupied patches per SI

0 1

20 40 60 80 100 0 2 468 Number of patches sampled per SIN Average connectivity per SIN

40 C D 2000 N 30

500

20 a coverage 200 P. lanceolat 10 50 Total habitat area (ha) per SI

20 0

02468 0 10 20 30 40 Average connectivity per SIN Total habitat area (ha) per SIN Fig. 2. Associations between (A) the number of patches in a semi-independent patch network (SIN) and the number of patches occupied by the weevil Mecinus pascuorum, (B) average patch connectivity in a SIN and abundance of Mecinus pascuorum, (C) average patch connectivity and the total habitat area of SINs, and (D) the total habitat area in a SIN and the total coverage of Plantago lanceolata. Each circle represents one SIN. Filled circles represent SINs with > 0.39 and circles SINs with < 0.09 occupancy rate.

dent populations of beetles were not on average and E. vesicularis (Table 1) apparently led to the resource limited. One explanation of why the association of weevil abundance with latitude weevil may not be resource limited is that it is (Fig. 3C), suggesting that on a large spatial scale on average parasitized at a very high rate. The the parasitoids may determine the distribution of data presented here are a snapshot in time, but by the weevil. This local (SIN level) and regional comparing semi-independent habitat-patch net- (Åland Island level) associations with parasit- works that differ in weevil host-density we see a ism, along with the stability of the plant popula- negative association of host density with the rate tions suggest that parasitoids play a considerable of parasitism. Additionally, extremely high par- role in the dynamics of the weevil, which may be asitism in the northern SINs (Fig. 1) due to the controlled from the top down. combined effects of the parasitoids M. incultus ANN. ZOOL. FENNICI Vol. 54 • Metacommunity structure of a seed-feeding weevil and its parasitoids 91

2.00 A 0.30 B

0.25

0.50 0.20 y 0.20 0.15 parasitism rate

Weevil densit 0.10 0.05

E. vesicularis 0.05

0.01 0

0.70 0.75 0.80 0.85 0.90 0.95 1.00 0.4 0.5 0.6 0.70.8 0.91.0 Total parasitism rate M. incultus parasitism rate

60.4 C D

500 60.3 e

50 60.2 Latitude (° ) Weevil abundanc 60.1 5

60.0 1

155 0 500 0 0.2 0.4 0.60.8 1.0 Weevil abundance E. vesicularis parasitism rate Fig. 3. Associations within each SIN (excluding SINs with no occurrence of the species) of (A) weevil density and the rate of parasitism, (B) rate of parasitism by Eupelmus vesicularis and Mesopolobus incultus, (C) latitude of the SIN midpoint and weevil abundance, and (D) weevil abundance and rate of parasitism by Eupelmus vesicularis.

The parasitoids M. incultus and E. known, but it is a generalist, and has been con- vesicularis sidered both a parasitoid of M. pascuorum and a hyperparasitoid of M. incultus (Bouček 1977, On average 80% of the weevils were parasitized Noyes 2013). An immature hyperparasitoid is which is a very high rate of parasitism (Hawkins restricted to feeding on a single host individual 1994). Mesopolobus incultus made up most of and cannot have perfect conversion efficiency this, however, E. vesicularis was also abun- so it will be significantly smaller than its host dant, and there was a strong negative association (Sullivan & Völkl 1999, Hatton et al. 2015). between the two parasitoids (Fig. 3B). This pat- In our sample, M. incultus and E. vesicularis tern could occur if there were direct competition individuals were of the same length, though between parasitoids, or if one parasitoid were E. vesicularis was slightly slenderer. Eupelmus a hyperparasitoid of the other. The natural his- vesicularis individuals that developed as hyper- tory of the parasitoid E. vesicularis is not well parasitoids of M. incultus should be noticeably 92 Nieminen & van Nouhuys • ANN. ZOOL. FENNICI Vol. 54 smaller than M. incultus and much smaller than that when using pupae of the parasitoid Cote- those developing in M. pascuorum. However, sia glomerata, the hyperparasitoid Gelis agilis we found only one size class of E. vesicularis. develops to 90% its host mass, and Lysibia nana Finally, if E. vesicularis used both hosts but lay reaches 95% host mass. If this were the case male eggs in M. incultus we would expect a male in the weevil parasitoid community then the bias where the ratio of E. vesicularis to M. incul- negative association between the two wasps can tus was high because male eggs would be laid be partly due to strong variation of the rate of in smaller hosts. We found instead that the sex hyperparasitism (from 7 to 40% of M. incultus), ratio was equal in the different patch networks. which is strongest at high connectivity due to Based on these three factors, the length of E. low mobility of E. vesicularis. vesicularis, the single size class and the consis- tent sex ratio, we think it is most plausible that E. vesicularis acts merely as a primary parasitoid The hyperparasitoid Baryscapus in this system. It follows from that, that the neg- endemus ative association of the two parasitoids is due to competition for hosts (Teder et al. 2012). The hyperparasitoid B. endemus is relatively Competing parasitoids can coexist if they common, parasitizing up to 26% of M. incultus. have different resource needs or strategies for However, we found no association of the hyper- host use. In a landscape context this might occur, parasitoid with factors that we measured. This for example, if a superior local competitor is an suggests that the population size of B. endemus inferior disperser, allowing the other parasitoid is independent of that of the host M. incultus, to persist as a fugitive (Amarasekare 2003, Bon- presumably because it has other hosts in the sall et al. 2004, van Nouhuys & Punju 2010); landscape, including several other parasitoids in our case, the specialist parasitoid M. incultus of the family Pteromalidae, even within the P. parasitizes at the highest rates at low patch-con- lanceolata weevil metacommunity (Nieminen nectivity and high host-abundance (Table 2). Had & Vikberg 2015). Though we found no direct E. vesicularis shown the opposite trend we might association between B. endemus and its host M. have concluded that E. vesicularis is the superior incultus, the hyperparasitoid can still influence local competitor and inferior disperser. Indeed, the competitive relationship between the two it probably persists well locally because it does primary parasitoids of the weevil by decreasing not depend on a single host species. It is also a the population size of M. incultus. poor disperser because females are brachypterous (Nieminen & Vikberg 2015). Furthermore, the negative association of the two parasitoids is Dynamics of the community strongest at high connectivity (Table 2), which suggests that dispersal limitation may constrain At the base of this community is an abundant E. vesicularis to well-connected patches of suit- host plant, P. lanceolata, associated with a few able habitat. While the idea of co-existence due generalist and a few specialized herbivores, one to a trade-off between local competitive ability of which is the specialist seed predator weevil M. and dispersal ability is a compelling scenario, pascuorum (Nieminen & Vikberg 2015). As in and has rarely if ever been shown to occur in most insect communities (Hawkins 1994) there insect communities (Amarasekare 2003, 2007, are many species of parasitoids associated with van Nouhuys & Punju 2010), it is worthy of fur- the weevil, however all but three are relatively ther study in this system. rare (Nieminen & Vikberg 2015). The special- Though hyperparasitoids are generally much ist parasitoid M. incultus parasitizes the largest smaller than their parasitoid hosts (Sullivan & fraction of hosts and is hyperparasitized by B. Völkl 1999, Hatton et al. 2015), a hyperparasit- endemus. The generalist parasitoid E. vesicularis oid will be nearly the size of its host if it devel- which could be both a primary or hyperparasit- ops extremely efficiently. Harvey et al. (2006) oid probably acts mostly as a primary parasitoid found such an exceptional case. They showed in this community. ANN. ZOOL. 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