Pollinator Rarity As a Threat to a Plant with a Specialized Pollination System
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Erschienen in: Botanical Journal of the Linnean Society ; 179 (2015), 3. - S. 511-525 https://dx.doi.org/10.1111/boj.12336 Pollinator rarity as a threat to a plant with a specialized pollination system RYAN D. PHILLIPS1,2,3*, ROD PEAKALL1, BRYONY A. RETTER2,3, KIRKE MONTGOMERY2, MYLES H. M. MENZ4, BELINDA J. DAVIS2,3, CHRISTINE HAYES1, GRAHAM R. BROWN5,6, NIGEL D. SWARTS7,8 and KINGSLEY W. DIXON2,9 1Evolution, Ecology and Genetics, Research School of Biology, The Australian National University, Canberra, ACT 0200, Australia 2Kings Park and Botanic Garden, The Botanic Gardens and Parks Authority, Fraser Avenue, West Perth, WA 6005, Australia 3School of Plant Biology, The University of Western Australia, Crawley, WA 6009, Australia 4Institute of Ecology and Evolution, University of Bern, Baltzerstrasse 6, 3012 Bern, Switzerland 5Museum and Art Gallery of Northern Territory, GPO Box 4646, Darwin, NT 0801, Australia 6Research institute for Environment and Livelihoods, Charles Darwin University, Darwin, NT 0909, Australia 7Royal Tasmanian Botanic Gardens, Queens Domain, Hobart, TAS 7000, Australia 8Tasmanian Institute of Agriculture, University of Tasmania, Private Bag 98, Hobart, TAS 7000, Australia 9Department of Agriculture and Environment, Curtin University, WA 6102, Australia An increasing diversity of highly specialized pollination systems are being discovered, many of which are likely to be vulnerable to anthropogenic landscape modification. Here, we investigate if a specialized pollination system limits the persistence of Caladenia huegelii (Orchidaceae), an endangered species pollinated by sexual deception of thynnine wasps. Once locally common in part of its geographical range, C. huegelii is now largely restricted to small habitat remnants in urban areas. Pollinator surveys coupled with DNA barcoding detected a single pollinator taxon, a small form of Macrothynnus insignis. Phylogenetic analysis revealed that small M. insignis from within the range of C. huegelii are strongly divergent from other wasp populations, suggesting that some reproductive isolation may exist. Although common in intact landscapes outside the range of C. huegelli, small M. insignis individuals were recorded at only 4% of sites in suitable C. huegelii habitat. Accordingly, reproductive success in C. huegelii was low compared with related Caladenia spp., with 33–60% of populations failing to set fruit in any given year. As such, populations are likely to now persist primarily through individual plant longevity rather than reproduction. Due to the low reproductive success of C. huegelii, ongoing human intervention will almost certainly be needed to sustain the species. Future research will need to focus on optimizing hand pollination to maintain reproduction and high seed fitness. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 179, 511–525. ADDITIONAL KEYWORDS: habitat fragmentation – orchid – sexual deception. INTRODUCTION pollinated plants are specialized on a subset of the available pollinator community (Fenster et al., 2004; Although pollination by multiple animal species pro- Rosas-Guerrero et al., 2014). Further, there is vides greater reproductive assurance, most animal- increasing recognition that there is a wide range of specialized pollination systems, with plants being *Corresponding author. E-mail: [email protected] reliant on just one or a few species of pollinators 511 Konstanzer Online-Publikations-System (KOPS) URL: http://nbn-resolving.de/urn:nbn:de:bsz:352-2-ctuy3kdcag0q3 512 (Johnson, 2010). In these systems, specialization can analysis in south-western Australia (Phillips et al., be mediated through a diversity of processes includ- 2011). Further, a detailed investigation of correlates ing exaggerated morphology for which only one polli- of rarity in the sexually deceptive genus Drakaea nator species can reach the nectar (Nilsson et al., Lindl. suggested that rarity was most likely caused by 1987), unusual rewards of interest to a small portion the absence of pollinators from otherwise suitable of the pollinator community (Houston et al., 1993; orchid habitat, rather than low levels of reproductive Pauw & Bond, 2011) or chemical attractants that success within existing populations (Phillips et al., exploit sensory biases of a particular pollinator 2014a). However, meta-analyses have shown that in (Schiestl et al., 2003; Brodmann et al., 2008; Bohman other genera sexually deceptive species tend to have et al., 2014). As a consequence of relying on just a few lower levels of fruit set than related orchids with pollinator species for sexual reproduction, low density more generalized pollination strategies (Phillips or narrow geographical range of the pollinator can et al., 2009b; Gaskett, 2011), suggesting low fruit set contribute to rarity of the plant (Phillips et al., could cause rarity in some sexually deceptive species. 2014a). Further, should a pollinator species undergo a Caladenia R.Br. is a diverse genus of terrestrial decline following anthropogenic landscape modifica- orchids (>375 taxa) with centres of diversity in south- tion, plant populations are also likely to decline western and south-eastern Australia (Phillips et al., (Anderson et al., 2011; Pauw & Hawkins, 2011; 2009a), two regions with extensive habitat removal. Geerts & Pauw, 2012). In extreme scenarios, local Although many Caladenia taxa are pollinated by extinctions of pollinators can leave plant populations nectar-foraging insects (Faast et al., 2009; Phillips entirely reliant on clonal reproduction. This situation et al., 2009b), and a small portion are self-pollinating is exemplified by the oil-producing orchids pollinated (Jones, 2006), > 100 species representing three subgen- by the bee Rediviva peringueyi, with local extinction era are believed to be pollinated by sexual deception of of the bees leading to local extinctions of the orchids, thynnine wasps (Stoutamire, 1983; Bower, 2001; and the less clonal species suffering extinction more Phillips et al., 2009b). Caladenia contains > 70 taxa rapidly (Pauw & Hawkins, 2011). that are currently federally listed as threatened or Orchidaceae are characterized by a high incidence endangered (Department of the Environment, 2015), of specialized pollination strategies, with many over half of which are believed to be pollinated via orchid species reliant on only one or few pollinator sexual deception. This trend raises the question of species (Tremblay, 1992; Schiestl & Schluter, 2009). whether pollination by sexual deception is contribut- Of these strategies, one of the most diverse and ing to rarity either through intrinsic rarity of some geographically widespread is pollination by sexual wasp species or vulnerability of specialized pollination deception (Gaskett, 2011; Phillips et al., 2014b). In systems to landscape modification. Given the diversity this pollination strategy, long-range attraction of pol- of the genus, understanding causes of rarity in sexu- linators occurs through mimicry of the sex phero- ally deceptive Caladenia may yield useful information mone of female insects, with pollination achieved by for the management of a large number of threatened the male during attempted courtship or copulation taxa. with the flower (Schiestl et al., 1999, 2003; Bohman Caladenia huegelii Rchb.f. is a rare species endemic et al., 2014). As a by-product of mimicking the spe- to south-western Australia (Hoffman & Brown, 2011) cific sex pheromones of insects, sexually deceptive (Fig. 1). It is currently known only from the Swan orchids often have only a single known pollinator Coastal Plain between Perth and Busselton (Fig. 2), species (Paulus & Gack, 1990; Phillips et al., 2009b; preferring areas of banksia woodland on the Bassen- Peakall et al., 2010; Gaskett, 2011). However, studies dean dune system (Hoffman & Brown, 2011). Once investigating populations of sexually deceptive locally common in at least part of its range (Hopper & orchids over a broad geographical range are increas- Brown, 2001), C. huegelii has undergone an extensive ingly revealing geographical variation in pollinator decline associated with the large scale habitat species (Breitkopf et al., 2013; Menz et al., 2015b; destruction for agriculture, housing and light Phillips et al., 2015). Furthermore, DNA barcoding industrial areas, which has continued in recent has demonstrated that some groups of sexually decades (Brown, Thomson-Dans & Marchant, 1998; deceived pollinators contain morphologically cryptic Department of Environment and Conservation, 2008). taxa (Griffiths et al., 2011; Menz et al., 2015b), poten- Of the 48 known populations, no plants were recorded tially obscuring the exact number of species actually at 21 of them during the last major surveys involved in pollination. (Department of Environment and Conservation, Due to their high pollinator specificity, lineages of 2008). Further, 17 of the surviving populations con- sexually deceptive orchids may show higher levels of tained less than five flowering plants (Department of intrinsic rarity than other pollination strategies, a Environment and Conservation, 2008). Due to the prediction that has been supported by a regional small and isolated nature of the remaining popula- 513 Figure 1. Macrothynnus insignis s.l. (A), the pollinator of the sexually deceptive orchid Caladenia huegelii (B). Panel (A) illustrates specimens of the large and small forms of M. insignis s.l. Only the small form is responsible for pollination of C. huegelii. Photographs