Two species of adventive weevil (Coleoptera: Curculionidae) from Europe, hitherto unrecorded from New Zealand

Abstract

Two curculionid weevils, Orthochaetes setiger (Beck, 1817) and Exomias pellucidus (Boheman, 1834) are recorded in New Zealand for the first time. The former has a wide distribution through the eastern South Island, while the latter has so far only been located in a single suburban garden in Dunedin. Both species are polyphagous and flightless. Although neither is expected to cause notable economic damage, their potential to invade native ecosystems makes them worthy of further investigation.

Keywords:

• first record
• identification
• invasive species
• New Zealand
• parthenogenesis
• weevils

Introduction

Invasive species threaten biodiversity and economic values in New Zealand and globally (Simberloff 2005; Brockerhoff et al. 2010). Increasing global trade and commerce have made the establishment of alien organisms a regular occurrence despite diligent biosecurity in New Zealand (Kriticos et al. 2005). Some invasions have significant economic impacts (e.g. Didymo, Pseudomonas syringae pv. actinidiae (Psa), tomato potato psyllid, clover root weevil); however, invasive species also have the potential to threaten New Zealand's unique biodiversity (Snyder & Evans 2006; Brockerhoff et al. 2010). While economic consequences are well recognised, non-economic environmental impacts of invasive species attract less attention (Simberloff 2005; Brockerhoff et al. 2010).

Within the invertebrates, the weevils (Coleoptera: Curculionoidea) are a group that is particularly invasive. In New Zealand, over 60 species have become established (Kuschel 1972; Macfarlane et al. 2011), with some species (e.g. clover root weevil [Sitona obsoletus (Gmelin)], lucerne weevil [Sitona discoideus Gyllenhal], Argentine stem weevil [Listronotus bonariensis (Kuschel)], eucalyptus weevil [Gonipterus platensis Marelli], and vine weevils [Otiorhynchus Germar spp.]) harming New Zealand's primary industries (Bain 1977; Prestidge et al. 1991; Eerens et al. 2005). Identifying recently arrived species is a critical first step towards evaluating and responding to them (Phillips & Barratt 2004). Here, we provide the first reports of two European weevils in New Zealand.

Exomias pellucidus (Boheman, 1837) (until recently placed in the genus Barypeithes Jacquelin du Val, see Löbl & Smetana 2013) is commonly known as the juniper root weevil, hairy broad-nosed weevil or hairy spider weevil and is classified in the tribe Sciapithini, subfamily Entiminae (Alonso-Zarazaga & Lyal 1999). Originally from Europe, it is a pest in North America in forestry nurseries and horticultural crops, where it is distributed across the continent between latitudes 34°N and 60°N (Coyle et al. 2008). The genus Exomias Bedel, 1883 has 35 described species in Europe and Asia (Löbl & Smetana 2013), and was most recently revised (as Barypeithes) by Fremuth (1971).

Orthochaetes setiger (Beck 1817) is in the tribe Styphlini, subfamily Curculioninae (Alonso-Zarazaga & Lyal 1999). Orthochaetes Germar 1824 contains 15 described species distributed throughout Europe and North Africa. Most species of Orthochaetes are locally distributed in southwestern Europe and North Africa, but O. setiger and Orthochaetes insignis Aubé 1863 have wider distributions through Europe and into the British Isles. The most recent revision of the genus was published by Gonzalez (1967), who provided a key to the known species of Orthochaetes.

Exomias pellucidus

Discovery

Specimens of E. pellucidus were found by pitfall trapping during a survey of biodiversity in 55 Dunedin domestic gardens in mid to late November 2009. The invertebrate survey was part of a larger study carried out by researchers in the Departments of Geography, Zoology and Botany, University of Otago, Dunedin (Barratt et al. 2015). Pitfall traps were set for a 10-day period with three to five traps set in each garden, depending upon garden area, and were positioned in areas of lawn, shrubs and open flower/vegetable beds. Only three E. pellucidus specimens were found, all from the same property. After the Ministry of Primary Industries was alerted to this discovery, one larva was found from around ivy roots by Ministry of Primary Industries response officers and was confirmed as E. pellucidus through DNA sequencing. Since the initial discovery, little effort has gone into locating further specimens, so it remains uncertain if this species is established.

New Zealand specimens were determined by BIPB using keys in Morris (1997) and Fremuth (1971), and the identity was confirmed by RS Anderson (Canadian Museum of Nature, Ottawa, Canada; pers. comm.). The length and curvature of the aedeagus match the illustrations provided by Fremuth (1971) and Dieckmann (1980). DNA sequencing for confirming the identity of the larva was done through EcoGene (Auckland, New Zealand), and involved sequencing 386 base pairs of the cytochrome c oxidase subunit 2 (COII) gene using the primers C2-J-3400 and TK-N-3785 (Simon et al. 1994) (D Jones pers. comm.). Sequences from an adult and a larva matched each other, and had a 91% identity to E. pellucidus sequences from GenBank (GU182497–GU182499; Hirsch et al. 2010). Sequences for nine other species of Exomias (as Barypeithes) are also available (DQ836068–DQ836076, Lackowska et al. unpub. data), with identities to these sequences ranging between 83% and 87%. This identity is low for absolute confidence in the identity of these specimens, as other studies of COII in weevils show intraspecific distances in the region of 0.7%–7.7% (Emerson et al. 2000; Machado 2008); however E. pellucidus has a wide range through Europe and is known to have infraspecific morphological variation. The sequence from the adult specimen has been deposited in GenBank (KM359706).

Specimens of E. pellucidus were deposited in the Ministry of Primary Industries synoptic collection (Christchurch; two males), and the Invermay Agricultural Research Collection (Mosgiel, Dunedin; one male).

Identification

Exomias pellucidus (Fig. 1A, C) can be distinguished from all other entimine weevil species present in New Zealand by the combination of its smaller size (2.9–4.0 mm); the small, dorsally situated eyes; shiny castaneous elytra clothed with sparse, long hairs; connate tarsal claws; and a tooth on each trochanter (RG Oberprieler pers. comm.). Similar species in New Zealand include Otiorhynchus ovatus Linnaeus, from which E. pellucidus can be distinguished by the long hairs on the elytra, the lack of teeth on the femora, and its castaneous elytra with lighter legs. The aedeagus was illustrated by Dieckmann (1980) and the pupa was described and illustrated by Gosik & Sprick (2013).

Figure 1 Habitus photographs of introduced weevils. A, Exomias pellucidus, dorsal; B, Orthochaetes setiger, dorsal; C, E. pellucidus, lateral; D. O. setiger, lateral.

In Kuschel's (1972) key to introduced Curculionoidea, E. pellucidus keys out to O. ovatus, from which it differs in the characters given above. Confusion may be encountered at couplet 64, where E. pellucidus shares with Maleuterpes spinipes Blackburn connate claws, but differs by having the pronotum not humped, and by having long, silky hairs on the dorsum.

Biology

Exomias pellucidus is polyphagous, with records coming from a wide range of plant species and families (Table 1). It is not of major economic importance, but has been recorded as a pest in horticultural nurseries (Morris 1997) and strawberries (Borg 1981; Bomford & Vernon 2005). In Canada, E. pellucidus occurs in forestry nurseries and vineyards (Brandt et al. 1996; Bouchard et al. 2005), and in the Great Lakes region it is one of a complex of nine European weevils that is threatening indigenous hardwood forests where it can reach densities of over 100 adults/m/day at peak emergence (Coyle et al. 2012). Outbreaks and aggregations have been recorded (Petherbridge 1915); however, the cause of these aggregations is not known.

Table 1 Host plants recorded for Exomias pellucidus.

Host plant	Geographical location	Reference
Acer saccharum, Aceraceae (Sugar maple)	Michigan, USA	Coyle et al. (2012)
Ostrya virginiana, Betulaceae (Ironwood)
Rubus sp., Rosaceae (Raspberry)
Fragaria × ananassa, Rosaceae (Strawberry)	Sweden	Borg (1981)
Vitis sp., Vitaceae (Grape)	Quebec, Canada	Bouchard et al. (2005)
Picea pungens, Pinaceae (Colorado spruce)	Ontario, Canada	Brandt et al. (1996)
Aster divaricatus, Asteraceae (White wood aster)	Ohio, USA	Galford (1987)
Aster lowrieanus, Asteraceae (Lowrie's aster)
Circiumarvense, Asteraceae (Canada thistle)
Crataegus sp., Rosaceae (Hawthorn)
Potentilla sp., Rosaceae (Cinefoil)
Prunus serotina, Rosaceae (Black cherry)
Quercus rubra, Fagaceae (Northern red oak)
Rhus radicans, Anacardiaceae (Poison ivy)
Rosa sp., Rosaceae (Wild rose)
Senecio sp., Asteraceae (Ragwort)
Taraxacum officinale, Asteraceae (Dandelion)
Ulmus americana, Ulmaceae (American elm)
Acer negundo, Aceraceae (Box elder)	Cambridgeshire, UK	Petherbridge (1915)
Brassica oleracea fruticosa, Brassicaceae (Kale)
Brasica oleracea gongylodes, Brassicaceae (Kohlrabi)
Collinsia heterophylla, Plantaginaceae (Innocence)
Iberis sp., Brassicaceae (Candytuft)
Nemophila menziesii insignis, Boraginaceae (Baby blue-eyes)
Papaver somniferum, Papaveraceae (Poppy)
Hedera helix, Araliaceae (Ivy)	UK	Metcalfe (2005)
Alopecurus pratensis, Poaceae (Meadow foxtail)	Germany	Gosik & Sprick (2013)
Bergenia crassifolia ‘Admiral’, Saxifragaceae(Elephant's ears)
Fragaria vesca, Rosaceae (Wild strawberry)
Acer pseudoplatanus, Aceraceae (Sycamore)	Germany	Dieckmann (1980)
Alchemilla vulgaris, Rosaceae (Lady's mantle)
Artemisia vulgaris, Asteraceae (Mugwort)
Brassica napus, Brassicaceae (Rape)
Corylus avellana, Corylaceae (Hazel)
Fragaria × ananassa, Rosaceae (Strawberry)
Fragaria viridis, Rosaceae (Wild strawberry)
Iris pseudacorus, Iridaceae (Yellow flag)
Lotus corniculatus, Fabaceae (Birdsfoot trefoil)
Lysimachia nummularia, Primulaceae (Creeping Jenny)
Populusnigra, Salicaceae (Black poplar)
Taraxacum officinale, Asteraceae (Dandelion)

Larvae of E. pellucidus are root-feeders, and are usually found in the top 10–30 cm of the soil (Brandt et al. 1996; Coyle et al. 2011). The species overwinters as larvae, and the nocturnal adults emerge in early summer (Brandt et al. 1996; Coyle et al. 2011, 2012) when they can be found on the ground or low vegetation (Morris 1997). It reproduces sexually, with males and females present in roughly equal proportions (Morris 1997). In western Ukraine, E. pellucidus is associated with moist and warm environments, including deciduous and mixed forest as well as other managed and modified environments (Mazur 2002). It is often found in ruderal plant communities, associated with herbaceous plants (Mazur 2002). Exomias pellucidus is capable of sustained movement, and is a strong climber (Bomford & Vernon 2005), but its dispersal is limited by it being flightless (Morris 1997).

Orthochaetes setiger

Discovery

The first specimens to be recognised were collected by SDJB at Lake Evelyn in the Lake Coleridge area on 11 December 2010. Specimens were shown in January 2011 to G Kuschel, who was also unfamiliar with the species. When dissections of a number of specimens showed them all to be female, the possibility that the specimens represented a previously unrecognised exotic parthenogenetic species became a consideration. After consulting Morris (2002), it became likely that these specimens were Orthochaetes setiger, an identity confirmed by SDJB by referring to the available literature and comparing specimens with those in the Natural History Museum; London, UK).

After this initial discovery, O. setiger has been widely collected east of the main divide of the South Island (Fig. 2). However, it is generally found in low numbers, and had therefore escaped notice by researchers sampling weevil pests in pasture (CB Phillips, pers. comm.). Historical specimens have been found in unsorted weevil collections from Canterbury and Central Otago tussock grassland, with the earliest found so far being two specimens collected from Broadfield, Canterbury on 5 January 1996.

Figure 2 Currently known distribution of Orthochaetes setiger and Exomias pellucidus within New Zealand.

New Zealand specimens were determined as Orthochaetes setiger by the combination of costate odd-numbered interstriae, apically inserted antennae, unarmed fore femora, simple tarsal claws, six funicle segments, oval elytra, and erect elytral setae (Gonzalez 1967; Morris 2002; Caldara et al. 2014). The length of the arms of the eighth sternite and stout spermatheca are also consistent with O. setiger (Davidian & Savitsky 2000).

Sequences were obtained from a single specimen collected in Sutton (CO, Crosby et al. 1998) for the 28S ribosomal DNA and cytochrome c oxidase I (COI) regions and deposited in GenBank (28S: KM359704, COI: KM359705). 28S was amplified using the primers S3660/28SFF (Sequeira et al. 2000; Gómez-Zurita et al. 2005), and COI using primers TY-J-1460/TL2-N-3014 (Simon et al. 1994). COI showed no close matches (i.e. identity over 90%) when searched for in GenBank or BOLD.

Specimens of O. setiger were deposited in the New Zealand Arthropod Collection (Manaaki Whenua Landcare Research, Tamaki, Auckland), Ministry of Primary Industries synoptic collection (Tamaki, Auckland and Christchurch), Museum of New Zealand Te Papa Tongarewa (Wellington), the Lincoln University Entomology Research Museum (Lincoln, Christchurch), and the Natural History Museum (London, UK).

Identification

Orthochaetes setiger (Fig. 1B, D) can be distinguished from all other weevil species in New Zealand by a combination of its small size (2.3–2.9 mm), grey coloration, oval outline, having six funicle segments, a heavily pitted metasternum, and costate elytra with numerous erect scales. Similar species in New Zealand include Listronotus bonariensis (Kuschel), and species within Baeosomus Broun, Microcryptorhynchus Lea, and Notacalles Kuschel. It differs from Listronotus bonariensis and Baeosomus by having costate elytra with erect scales. It differs from Microcryptorhynchus and Notacalles by not having a prosternal canal. In Kuschel (1972), O. setiger keys out to Sitophilus Schoenherr (couplet 21), from which it differs by being grey, having clubbed upright scales on the elytra, in the form of the antennal club, and by not being found in stored products.

Biology

Orthochaetes setiger is polyphagous, but has an apparent preference for members of the Asteraceae (Table 2). It has negligible economic impact, but has been noted as causing aesthetic damage to ornamental plants (Halstead 1977).

Table 2 Host plants recorded for Orthochaetes setiger.

Host plant	Geographical location	Reference
Aposeris spp., Asteraceae (False dandelion)	Germany	Dieckmann (1986)
Aster spp., Asteraceae (Michaelmas daisy)
Bellis spp., Asteraceae (Daisy)
Centaurea spp., Asteraceae (Knapweed)
Chondrilla spp. Asteraceae (Chondrilla)
Cicerbita spp., Asteraceae (Sow thistle)
Cichorium spp., Asteraceae (Chicory)
Crepis praemorsa, Asteraceae (Hawksbeard)
Hieracium spp., Asteraceae (Hawkweed)
Hypochoeris spp., Asteraceae (Catsear)
Lactuca spp., Asteraceae (Lettuce)
Lapsana spp., Asteraceae (Nipplewort)
Leontodon hispidus, Asteracaeae (Hawkbit)
Myosotis spp., Boraginaceae (Forget-me-not)
Picris spp., Asteraceae (Ox-tongue)
Plantago spp., Plantaginaceae (Plantain)
Ranunculus spp., Ranunculaceae (Buttercup)
Scorzonera hispanica, Asteraceae (Viper's grass)
Solidago spp., Asteraceae (Golden-rod)
Sonchus spp., Asteraceae (Sow thistle)
Taraxacum spp., Asteraceae (Dandelion)
Clematis vitalba, Ranunculaceae (Old man's beard)	Netherlands	Osella & Zuppa (1993)
Fragaria collina, Rosaceae (Wild strawberry)	Austria
Ajuga spp., Lamiaceae (Bugle)	England	Halstead (1977)
Centaurea spp., Asteraceae (Knapweed)
Cyclamen hederifolium, Primulaceae (Sowbread)
Cyclamen persicum, Primulaceae (Cyclamen)
Hieracium spp., Asteraceae (Hawkweed)
Lactuca spp., Asteraceae (Lettuce)
Myosotis spp., Boraginaceae (Forget-me-not)
Plantago spp., Plantaginaceae (Plantain)
Sonchus spp., Asteraceae (Sow thistle)
Taraxacum spp., Asteraceae (Dandelion)

All eight specimens of O. setiger that were dissected were female. Hence the population in New Zealand is probably parthenogenetic, as is the case throughout most of northern Europe and Britain (Gonzalez 1967). Orthochaetes setiger and O. insignis are the only species in the subfamily Curculioninae that are known to be parthenogenetic (Caldara et al. 2014); though parthenogenesis is also known in the subfamilies Brachycerinae, Cyclominae and Entiminae (Marvaldi et al. 2014; Oberprieler 2014).

Larvae of O. setiger are leaf miners, with mines appearing as pale-brown, irregularly shaped blotches (Halstead 1977). Larvae develop over about 2 months in spring (Halstead 1977). Pupation occurs in the soil, and takes about 3 weeks. The species apparently overwinters as adults. It is assumed to be univoltine, though this has not been investigated in detail. In Europe, O. setiger has a wide ecological tolerance, being found in xerophytic habitats as well as cooler humid environments (Dieckmann 1986). It has a broad altitudinal distribution and is found up to 2100 m in Switzerland (Dieckmann 1986). A preference for drier habitats is consistent with its known distribution through the eastern South Island of New Zealand (Fig. 2). The inherent dispersal capacity of O. setiger is very low, due to this species being flightless (Morris 2002) and particularly slow moving.

Discussion

These weevils are two of a number of adventive weevils that have been accidentally introduced to New Zealand over the past 50 years. While some of these weevils pose little threat to the economy or environment of New Zealand, several have caused substantial economic losses, particularly within the agricultural sector. It is also notable that species such as Sitona obsoletus and Listronotus bonariensis have reached a greater level of severity as pests in New Zealand compared with other regions where they have invaded and established. This might be a reflection of the relatively low level of species diversity, and hence natural enemy complex, in New Zealand agricultural systems compared with larger continental land masses (Tylianakis & Romo 2010; Goldson et al. 2014), combined with New Zealand's heavy reliance on ryegrass and white clover as forage crops. Hence predicting impacts of invasive species in New Zealand can be challenging.

Discoveries such as those reported here are reminders that regular collecting post-border, with follow-up identification and reporting of specimens that are suspected of being new to New Zealand, is important in the rapid detection of invasive species.

The discovery of O. setiger in remote localities such as Lake Coleridge and Sedgemere suggests that it is readily dispersed, despite its apparently poor capacity for dispersal. This was probably achieved through movement of soil or plant matter, especially stock feed. Its behaviour makes it unlikely to have been dispersed through hitch-hiking on vehicles, as has been implicated in the spread of Sitona obsoletus (CB Phillips pers. comm.). The presence of O. setiger in areas with high native plant diversity, including native species of genera that are known to be attacked as hosts (such as Myosotis and Ranunculus), makes it a potential conservation concern.

Further research into the genetic diversity of O. setiger may offer insight into the origin of the New Zealand population, and potential pathways for its invasion.

The ability of E. pellucidus to invade indigenous hardwood forest in North America (Coyle et al. 2012) makes this species also worthy of monitoring. In the first instance, a survey to verify its establishment and determine its distribution in New Zealand needs to be carried out. The composition of New Zealand forests is quite different from those in North America, so they may not be at risk from E. pellucidus; however, trees in amenity areas might be damaged.

Acknowledgements

Thanks to Rolf Oberprieler (Australian National Insect Collection, CSIRO, Canberra, Australia) for useful discussion of key characters. Birgit Rhode (Landcare Research, Tamaki, Auckland) provided photographs of E. pellucidus. Basemap of Figure 2 courtesy of Geographx. Joana Cristovao (NHM) translated Gonzalez's key to Orthochaetes. Diane Jones (Ministry of Primary Industries, Tamaki, Auckland) provided details of the molecular identification of the E. pellucidus larva. Craig Phillips (AgResearch, Lincoln) made helpful comments on the manuscript. This research was funded by Lincoln University, the Miss EL Hellaby Indigenous Grasslands Research Trust and AgResearch (MSI contract LINX0304, Ecosystems Bioprotection), as part of SDJB's doctoral programme. SDJB's trip to the NHM was funded by the Spragg Agricultural Research and Development Award. BIPB was supported by AgResearch as part of the Better Border Biosecurity (B3, www.b3nz.org) collaborative research programme, and a University of Otago Research Grant.

Associate Editor: Dr Rob Cruickshank.