Insect Conservation and Diversity (2018) 11, 58–71 doi: 10.1111/icad.12241 Species traits explain long-term population trends of Finnish cuckoo wasps (Hymenoptera: Chrysididae) 1 € 2 2 JUHO PAUKKUNEN, JUHA POYRY and MIKKO KUUSSAARI 1Finnish Museum of Natural History, Zoology Unit, University of Helsinki, Helsinki, Finland and 2Finnish Environment Institute (SYKE), Natural Environment Centre, Helsinki, Finland Abstract. 1. Kleptoparasitic and parasitoid insects are expected to be particu- larly sensitive to changes in habitat availability due to their high trophic posi- tion and small population sizes compared with their hosts, but there are only few quantitative studies on their population changes. 2. Here, we studied the distribution and abundance of 48 kleptoparasitic and parasitoid species of cuckoo wasps (Chrysididae) and eight selected host species recorded in Finland from 1840 to 2015 based on an extensive survey of entomologi- cal collections. Population trends were assessed by studying changes in occupancy in 10 9 10 km grid squares between two study periods, 1840–1967 and 1968–2015. 3. Statistically significant decreases in occurrence were found for 11 cuckoo wasp species and one host species, while significant increases were not observed for any species. Trends of cuckoo wasps and their hosts were positively corre- lated, and changes were generally stronger in cuckoo wasps than in their hosts. 4. In a comparative analysis of species traits, abundance, body size and nest- ing type of host were related to occurrence changes of cuckoo wasps. Scarce and small species that use above ground-nesting hosts declined more than abun- dant and large species that use ground-nesting hosts. 5. Cuckoo wasp species dependent on dead wood are more vulnerable to changes in the environment than species associated with open sandy habitats. While both groups of species have probably suffered from habitat loss, the emergence of secondary habitats may have benefitted species living in sandy areas and compensated for the negative impact of habitat destruction. Key words. Declining trend, distribution, host, host–parasitoid dynamics, klep- toparasite, museum collections, occurrence, parasitoid, sun-exposed dead wood, threatened species, vulnerability of high trophic level. Introduction structure of woodlands and agricultural landscapes (Stoate et al., 2009; Paillet et al., 2010). Forests have Major changes in land use have profoundly altered become more homogeneous and closed with less large landscapes and habitats in large parts of the world trees and dead wood (Kouki et al., 2001), while over the last two centuries. In Europe, particularly the flower-rich meadows and pastures have disappeared introduction of large-scale industrial forestry and agri- from agricultural areas (Cousins et al., 2015). These culture during the 20th century, including efficient pre- changes, in combination with climatic factors, have vention of forest fires and abandonment of traditional benefitted some organisms, while others have suffered animal husbandry, has dramatically transformed the and even become threatened. In northern Europe, especially species dependent on natural forests (Hyvarinen€ et al., 2006; Tikkanen et al., 2006) and Correspondence: Juho Paukkunen, Finnish Museum of Natural semi-natural grasslands (Kuussaari et al., 2007) have History, Zoology Unit, University of Helsinki, P.O. Box 17, Hel- been negatively affected. sinki FI-00014, Finland. E-mail: juho.paukkunen@helsinki.fi 58 Ó 2017 The Royal Entomological Society Population trends of cuckoo wasps 59 While population trends of species are often linked to regionally extinct (Paukkunen, 2010; Table S2). According their habitat requirements, also other ecological and life- to such evaluations, the main threat for cuckoo wasps is history traits can affect responses to environmental habitat loss, and especially the decrease of sparsely vege- changes. Niche breadth and dispersal ability can deter- tated dry meadows and biotopes with sun-exposed dead mine insect species’ responses to human-induced changes, wood. so that a narrow niche breadth (i.e. a specialised diet) and Despite Red List assessments indicating severe declines a poor dispersal ability are predicted to make species in cuckoo wasps, quantitative studies on long-term popu- more vulnerable (e.g. Kotiaho et al., 2005; Bommarco lation trends have not been carried out previously in this et al., 2010; Ockinger€ et al., 2010). Declining trends or group. The probable main reasons are the difficulties of increased vulnerability have also been associated with sampling large amounts of cuckoo wasps and that their other life-history traits, such as large body size (Bar- identification always requires an experienced expert. tomeus et al., 2013), nest site location (Potts et al., 2005; Therefore, in contrast to some other insect groups with Steffan-Dewenter et al., 2006; Williams et al., 2010) and citizen science type of monitoring (Poyry€ et al., 2009), solitary or social lifestyle (Steffan-Dewenter et al., 2006; documenting population trends of cuckoo wasps is only Williams et al., 2010). Kleptoparasitic and parasitoid spe- possible by examining existing museum and amateur col- cies, which require viable host populations, are more vul- lections of pinned individuals. Being difficult to identify nerable to habitat loss than species at lower trophic levels can also be seen as an advantage in cuckoo wasps. This is (e.g. Komonen et al., 2000; Roslin et al., 2013), but quan- because the pinned individuals in collections are likely to titative studies covering entire insect groups are virtually be much closer to a representative random sample from lacking (Hochberg, 2000; Shaw & Hochberg, 2001). nature than pinned individuals of some easily identifiable Cuckoo wasps (Hymenoptera, Chrysididae) are a group insects in which museum collections may be heavily biased of wasps, which develop during their larval stage as klep- to rare species (see Kuussaari et al., 2007). toparasites or parasitoids of mainly other hymenopterans Assessing long-term population trends and distribu- (Kimsey & Bohart, 1991). While parasitoids feed directly on tional changes on the basis of natural history collections the host larva or pupa, kleptoparasites (or brood parasites) can also be difficult due to several other reasons, such as mainly utilise the food items stored in the host brood cell changes in sampling effort, changes in the spatial coverage (O’Neill, 2001). Both modes of development practically of sampling and changes in collection methods over time always result in the death of the host. When occasionally (Jeppsson et al., 2010; Scheper et al., 2014). Numerous more than one host brood cell is destroyed, the kleptopara- methods have been proposed in literature for taking these site can be also considered to be a predator. Although klep- potential sources of bias into account in trend assessments toparasites mostly feed on the same food as their hosts and (Isaac et al., 2014). The most commonly used methods may thus be considered as inter-specific competitors (cf. employ data filtering or statistical correction procedures. Iyengar, 2008), they share several characteristics in their life- Here, we employ the method of data filtering to examine style with species belonging to a higher trophic rank, as they population trends of cuckoo wasps. are totally dependent on their hosts and therefore compara- Our study has four aims. First, we explore the general ble with parasitoids. Most North-European species of the patterns of distribution and abundance of the cuckoo subfamily Chrysidinae are kleptoparasites of solitary wasps wasps recorded in Finland. Second, we investigate how of the families Vespidae and Crabronidae, whereas a few the occurrence and distribution cuckoo wasps have chan- species are ectoparasitoids of solitary bees of the family ged during a period of 170 years. Based on observed Megachilidae. Species of the subfamily Cleptinae are changes in the occupancy of selected well-studied ectoparasitoids of sawfly prepupae of the families Tenthre- 10 9 10 km grid squares, we assess population trends for dinidae and Diprionidae (Paukkunen et al., 2014, 2015). As each species. Third, we analyse using comparative meth- the hosts of most cuckoo wasps themselves are highly spe- ods how species traits, specifically host specificity, body cialised predators or pollen feeders, which require specific size, nesting type of host, abundance and size of distribu- nesting sites and nest building material, cuckoo wasps as tion, are related to the observed trends. Fourth, we inves- their natural enemies are expected to be particularly vulnera- tigate how changes in the occurrence of specialist cuckoo ble to environmental changes. Many cuckoo wasp species wasps are correlated with changes in the occurrence of are also highly specialised in their host selection (Parn€ et al., their hosts and test the prediction that changes in cuckoo 2014) and probably have poor dispersal abilities due to their wasps are more pronounced than changes in their hosts small size (Greenleaf et al., 2007; Gunton & Poyry,€ 2016). because they are positioned at a higher trophic level. The sensitivity of cuckoo wasps for environmental changes has become evident in the latest North-European Red List assessments. The proportion of Red-Listed Materials and methods cuckoo wasp species is exceptionally high in all Nordic countries (Paukkunen, 2010; Larsson, 2015; Ødegaard Data collection et al., 2015). For example, nearly half