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Diversity and Host Specificity of Psylloidea

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Diversity and Host Specificity of Psylloidea bs_bs_banner Austral Entomology (2014) ••, ••–•• Diversity and host specificity of Psylloidea (Hemiptera) inhabiting box mistletoe, Amyema miquelii (Loranthaceae) and three of its host Eucalyptus species Anna E Burns,1*GarySTaylor,2 David M Watson1 and Saul A Cunningham3 1School of Environmental Sciences and Institute for Land, Water and Society, Charles Sturt University, PO Box 789, Albury, NSW 2640, Australia. 2Australian Centre for Evolutionary Biology and Biodiversity, School of Earth and Environmental Sciences, The University of Adelaide, Adelaide, SA 5005, Australia. 3CSIRO Ecosystem Sciences, Black Mountain, ACT 2601, Australia. Abstract This study is the first direct comparison of the diversity of phytophagous insects associated with a parasitic plant and its host plants. Specifically, we compared the species composition, density and host specificity of psylloids or jumping plant lice (Hemiptera: Psylloidea), inhabiting hemiparasitic box mistletoe Amyema miquelii, and three of its host Eucalyptus species: Eucalyptus blakelyi, Eucalyptus melliodora and Euca- lyptus polyanthemos. Insects were sampled by restricted canopy fogging in remnant Eucalyptus woodlands in an agricultural region of temperate south-eastern Australia. Although most psylloids are understood to be mono- or oligophagous, most species in our survey were found on the foliage of both mistletoes and eucalypts. Nevertheless, analysis of density patterns and reference to previous work on psylloids supports the high degree of host specificity for psylloids, leading to distinct assemblages on these two intimately associated plants. We show that (1) there were two mistletoe-associated species of psylloid and 18 eucalypt- associated species; (2) there were a large number of tourist species, as indicated by known psylloid/plant host associations; and (3) psylloid density was higher on eucalypt than mistletoe leaves. The different psylloid assemblages found on box mistletoes compared with their host plants are likely to be due to differences in the foliar properties implicated in host specificity and host selection by phytophagous insects. Further research is required to understand the ecological dynamics and evolutionary origins of these arbo- real assemblages. Key words arboreal, assemblage similarity, community composition, Psyllidae, tourist species. INTRODUCTION mistletoe to be a nested subset of the assemblage on the host plant. However, mistletoes and their host plants usually belong Studies of host specialisation of insects inform our understand- to different orders and clades. The association between mis- ing of species richness and turnover among host plants and tletoe and host plant offers an opportunity to explore factors locations and, thus, species diversity at different scales that influence the host specificity, composition and distribution (Ødegaard et al. 2000; Dyer et al. 2007; Novotny et al. 2007). of arboreal arthropod assemblages in tree canopies. Variation in community composition among insect assem- Although interactions between mistletoes and vertebrates blages is strongly influenced by host plant identity or plant have been well studied (as reviewed by Watson 2001; Watson species composition, particularly for phytophagous insects & Herring 2012), much less is known about invertebrate (Frenzel & Brandl 2001; Ødegaard et al. 2005). Mistletoes are assemblages associated with mistletoes. Species-specific parasitic plants that are physiologically linked with their host studies have shown that ecological interactions between mis- plants, and thereby strongly spatially associated, such that tletoes and insects include herbivory, frugivory, pollination mistletoes and host plants share the same physical environ- and tri-trophic relationships (Penfield et al. 1976; Atsatt 1981; ment and may appear to be one plant canopy (especially in De Baar 1985; Braby 2000, 2005; French 2004; Robertson cases of leaf mimicry by mistletoes, see Mathiasen et al. et al. 2005). However, we are unaware of any direct compara- 2008). If plant chemistry and evolutionary history were not tive studies of arthropod assemblages on mistletoes and their important, one would expect the assemblage of insects on host plants, apart from our own research (Burns 2009; Burns et al.2011),andoneindirectinvestigationofafoodplantshift of a lepidopteran between a dwarf mistletoe and host conifers *[email protected] (Mooney 2003). © 2014 Australian Entomological Society doi:10.1111/aen.12123 2 A E Burns et al. The mistletoe form has evolved five times in different fami- Table 1 Details of the sampling design, including the number of lies within the Santalales (Vidal-Russell & Nickrent 2008) and samples (n) collected from individual box mistletoe (Amyema mistletoe species vary in their degree of host specificity miquelii) plants and Eucalyptus trees, and the number of solo and (Barlow 1996; Downey 1998). Australian mistletoes, of which duplicate mistletoe samples (i.e. solo = no sample collected from there are 91 species, belong to the families Loranthaceae (in 12 the host tree; duplicate = two mistletoe samples collected in the same tree) genera, Gondwanan origin), Viscaceae (in 3 genera, Laurasian origin) and Santalaceae (1 genus/species) and constitute Site Mistletoe Eucalypt Eucalyptus species (n) Solo Duplicate approximately 6% of nearly 1600 species worldwide (Barlow No. n n mistletoe mistletoe 1984; Downey 1998; Downey & Wilson 2004; Nickrent 2011; samples samples Watson 2011). Our study species, the box mistletoe, Amyema 1 4 3 RB(3) 0 1 miquelii (Loranthaceae), is distributed throughout mainland 2 6 5 RB(2), YB(2), BR(1) 1 0 Australia and has been recorded parasitising 125 host plant 3 5 3 RB(2), YB(1) 0 2 species, primarily in Eucalyptus (Myrtaceae; Downey 1998; 4 10 6 RB(3), YB(1), BR(2) 3 1 5 5 2 RB(2) 2 1 Watson 2011). It was the most common mistletoe species in Totals 30 19 RB(12), YB(4), BR(3) 6 5 the study area. The three Eucalyptus species included in this study (see Materials and Methods) are widely distributed in RB: red box, E. polyanthemos; YB: yellow box, E. melliodora; BR: Blakely’s red gum, E. blakelyi. south-eastern Australia, in woodlands and open forest (Chippendale 1988). Psylloidea (Hemiptera) were the most abundant group of November 2005 at five sites of remnant grassy box wood- insects collected in a previous study of the arthropod assem- land, 4–18 hectares in size and located 2–23 km apart (i.e. blages inhabiting mistletoes and eucalypts (Burns et al. 2011). sites 1–5 in Burns et al. 2011). These sites were surrounded Here, we examine the diversity and distribution of psylloids by grazed pastures or crops on privately owned land. The from that survey. Psylloidea are particularly diverse and abun- remnant woodlands were dominated by Eucalyptus dant in Australia, where the 382 described species (and >100 polyanthemos (red box), which is the primary host of species not yet described) constitute more than 10% of the A. miquelii in the region. At least 40 individual A. miquelii world fauna (Hollis 2004; and recent taxonomic descriptions, occurred at each site. including Taylor et al. 2010, 2013; Taylor & Kent 2013; Insects were collected using a restricted canopy fogging Taylor & Moir 2014). Currently, three described species of technique (after Basset 1990), from plants of A. miquelii psylloids have been collected from Australian mistletoes (n = 30) and three of its host tree species: E. polyanthemos (listed as ‘Amyema pendulum’, ‘probably A. miquelii’ and (red box, n = 12), Eucalyptus melliodora (yellow box, n = 4) ‘unidentified species’; see Taylor 1999) and many species and Eucalyptus blakelyi (Blakely’s red gum, n = 3) using a from Eucalyptus (Hollis 2004). However, few community- trailer-mounted hydraulic bucket hoist (maximum height: level studies have described the assemblages of psylloids on 12 m above ground). Sampling was constrained by the tree particular host plant species (Hodkinson et al. 1979; Jäger & species mix of each remnant patch and the access permitted Topp 2002; Moir et al. 2005, 2011; Powell 2011; Powell et al. by the hoist; therefore, it was not possible to collect the same 2012), including only one for a Eucalyptus species (Barton number of samples from each Eucalyptus species. The greater et al. 2013) and none for mistletoes. Therefore, our aim was to number of samples collected from box mistletoe than the investigate the diversity and host specificity of psylloids inhab- eucalypts occurred for two reasons: in some cases, mistletoe iting box mistletoe and a subset of its host plants. Given that foliage was accessible but the tree foliage was out of reach most psylloid species are either monophagous or (six trees); or, two mistletoe plants were sampled in the oligophagous, i.e. feeding and completing their life cycle on a same tree (five trees, see Table 1). At each site, sampled single host plant species or a group of congeneric or trees were between 5 and 500 m apart. Psylloids were confamilial species (Hodkinson 1974; Hollis 2004), we pre- sampled from eucalypt foliage within approximately 3 m dicted low similarity in species composition between box mis- of a mistletoe plant that was sampled in the same tree, at a tletoe and the eucalypts, despite the close physical association similar height above ground and depth in the canopy (3 m of these plants. was within the reach of the boom arm of the bucket hoist without moving its base). Psylloids were collected from one sample of foliage per mistletoe plant or eucalypt tree. The dimensions of the
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