Biology of Two Members of the Euwallacea Fornicatus Species
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Agricultural and Forest Entomology (2016), 18, 223–237 DOI: 10.1111/afe.12155 Biology of two members of the Euwallacea fornicatus species complex (Coleoptera: Curculionidae: Scolytinae), recently invasive in the U.S.A., reared on an ambrosia beetle artificial diet ∗ † ‡ ∗∗ Miriam F. Cooperband , Richard Stouthamer , Daniel Carrillo , Akif Eskalen§, Tim Thibault¶, Allard A. Cossé , Louela A. Castrillo††,JohnD.Vandenberg‡‡ and Paul F. Rugman-Jones† ∗Otis Laboratory, USDA-APHIS-PPQ-CPHST, 1398 W. Truck Road, Buzzards Bay, MA 02542, U.S.A., †Department of Entomology, 900 University Ave., University of California, Riverside, CA 92521, U.S.A., ‡Tropical Research and Education Center, University of Florida–IFAS, 18905 SW 280 ST, Homestead, FL 33031, U.S.A., §Department of Plant Pathology and Microbiology, 3401 Watkins Ave., University of California, Riverside, CA 92521, U.S.A., ¶Huntington Library, Art Collections, and Botanical Gardens, 1151 Oxford Rd., San Marino, CA 91108, U.S.A., ∗∗USDA-ARS-NCAUR, 1815 N. University St., Peoria, IL 61604, U.S.A., ††Department of Entomology, Cornell University, 129 Garden Ave., Ithaca, NY 14853, U.S.A. and ‡‡USDA, Agricultural Research Service, Robert W. Holley Center for Agriculture and Health, 538 Tower Rd., Ithaca, NY 14853, U.S.A. Abstract 1 Recent molecular studies have found that the ambrosia beetle Euwallacea fornicatus Eichhoff (Coleoptera: Curculionidae: Scolytinae) is a complex of cryptic species, each carrying a different species of symbiotic fungus, in the genus Fusarium, which they farm within galleries inside woody hosts. Several of these beetle species have become invasive pests around the world for attacking and infecting healthy trees with their phytopathogenic fungal symbionts. 2 Diet and rearing protocols were developed for two members of the E. fornicatus species complex, polyphagous shot hole borer (PSHB) and tea shot hole borer (TSHB), using sawdust from host trees, allowing collection of data on beetle biology, phenology and sex ratios. Adults developed within 22 days at 24 ∘C. Single PSHB or TSHB foundresses averaged 32.4 and 24.7 adult female offspring, respectively, and up to 57 and 68 female adults within 6–7 weeks. A strong predictor of the number of offspring in a colony was the number of entry holes. Average sex ratios (% male) for PSHB and TSHB, respectively, were 7.4% and 7.2%. 3 Being haplodiploid, virgin PSHB foundresses were able to produce and mate with male offspring, then subsequently produce female offspring, confirming that they have arrhenotokous reproduction. 4 A cold tolerance study found significant mortality rates among PSHB colonies exposed to −5∘ or −1 ∘C but not colonies exposed to 0∘,1∘ or 5 ∘C. 5 Given Hamilton’s local mate competition (LMC) theory, a number of LMC predictions were violated. PSHB sex ratios were not affected by the number of foundresses; approximately 14% of broods did not contain males; males did not usually eclose before females but eclosed around the same time (22–23 days); and PSHB males were found walking outside of their natal galleries on the trunk of a heavily infested tree in the field. Alternatives to LMC are considered, such as early forms of sociality (maternal care, cooperative brood care), local resource enhancement and kin selection. Keywords Artificial rearing, cold tolerance, Fusarium dieback, insect diet, local mate competition, polyphagous shot hole borer, sex ratio, tea shot hole borer. Introduction 1868). Long considered the most serious pest of tea in Sri Lanka (Gadd, 1941; Walgama & Pallemulla, 2005), this pest species Euwallacea fornicatus Eichhoff (Coleoptera: Curculionidae: originates from southeast Asia, occurring in countries from Sri Scolytinae), the tea shot hole borer (TSHB), was first described from Sri Lanka in 1868 (as Xyleborus fornicatus) (Eichhoff, Lanka to Taiwan, and is known for its broad host range and dis- tribution, as well as numerous invasions around the world, such Correspondence: Miriam F. Cooperband. Tel.: +1 508 563 0934; fax: as Hawaii, California, Florida, Israel, Australia, Africa, Vanuatu, +1 508 563 0903; e-mail: [email protected] Panama, Costa Rica and many more (Danthanarayana, 1968; Published 2016. This article is a U.S. Government work and is in the public domain in the USA. 224 M. F. Cooperband et al. Rabaglia et al., 2006; Kirkendall & Ødegaard, 2007; Mitchell The TSHB was detected in Florida in 2002 but with minor & Maddox, 2010). However, its status as a single species has initial impact (Rabaglia et al., 2008), and was found in avocado recently been questioned based on molecular data. Eskalen et al. groves in south Florida in 2012 where levels started out low, (2013) were the first to draw attention to large levels of genetic although damage and abundance are increasing (Carrillo et al., differences between invasive populations of shot hole borers 2012, 2015). The PSHB was first discovered in 2003 and 2005 from Florida and California, both of which matched the mor- (although it was misidentified as TSHB), in Los Angeles County phological description of E. fornicatus, suggesting that they and Israel, respectively (Rabaglia et al., 2006; Mendel et al., were different species, and coining the common name for the 2012). The Israeli avocado industry sustained major loss as a polyphagous shot hole borer (PSHB) in California. O’Donnell result of Fusarium dieback, a serious plant disease associated et al. (2015) subsequently conducted DNA-based phylogenetic with PSHB (Eskalen et al., 2012; Mendel et al., 2012; Freeman analyses on beetles matching the morphological description of et al., 2013b), and the California avocado industry has started TSHB from invasive populations around the world, including to experience similar losses (Eskalen et al., 2012). Additionally, beetles from Sri Lanka (where E. fornicatus was first described). thousands of other landscape and forest trees have been killed Their findings suggested that E. fornicatus was a complex of at and removed in southern California as a result of Fusarium least five morphologically indistinguishable species (O’Donnell dieback. Eskalen et al. (2013) reported that, of 335 plant species et al., 2015). Invasive populations in both Israel and the greater observed, PSHB attacked 207 species of healthy trees in 58 Los Angeles region of southern California were genetically iden- plant families, and Fusarium was established and recovered in tical (which they referred to as Euwallacea sp. #1) but dif- more than half of those species. At the time of their study, fered genetically from the invasive population in Miami-Dade Eskalen et al. (2013) reported 19 species as reproductive hosts County, Florida (Euwallacea sp. #2), and both differed from in which attacks resulted in the establishment of Fusarium and a more recently discovered invasive population in San Diego colonies with offspring. Subsequently, the list of attacked tree County, southern California (Euwallacea sp. #5). Furthermore, species has increased to 342 taxa in 63 families (T. Thibault and all three of these beetles differed genetically from those in Sri A. Eskalen, unpublished data). Of these, 39 species in 16 families Lanka (Euwallacea sp. #4, potentially the true E. fornicatus) are known reproductive hosts, 13 of which are species native and Australia (Euwallacea sp. #3). Molecular data suggest that to California (Table 1) (Eskalen et al., 2013; Eskalen, 2016; Euwallacea sp. #1 (PSHB) most likely originated from Viet- http://eskalenlab.ucr.edu/avocado.html). Less is known about the nam (R. Stouthamer, unpublished data; Lynch et al., 2016). The full host range of TSHB, although its range is also likely to genetic differences found between beetle populations were mir- be extensive because E. fornicatus has been recorded attacking rored in the species of Fusarium symbionts that they each carry, at least 100 different plant species, in 35 families, in India, and were sufficiently great for the the beetles to be considered Java, Malaysia and Sri Lanka, with at least 21 of those being as separate species (O’Donnell et al., 2015). Fusarium euwal- reproductive hosts (Danthanarayana, 1968). The Euwallacea sp. laceae is the principal and obligate symbiont for PSHB (Eskalen #5 population in San Diego has been found attacking commercial et al., 2012, 2013; Freeman et al., 2013a; O’Donnell et al., 2015), avocado groves and other hosts similar to those of PSHB although, recently, two additional fungal associates, Graphium (Eskalen, 2016; http://eskalenlab.ucr.edu/avocado.html). euwallaceae and Paracremonium pembeum, were identified One of the economically important reproductive hosts of all from PSHB mycangia (Lynch et al., 2016). The fungal associate three species in the U.S.A. is avocado, which, in California G. euwallaceae is capable of sustaining offspring development alone, is an industry worth about $400 million annually whereas the role of P. pembeum is not known (Sharon et al., (California Avocado Commission, 2015). Mexico is the 2015). However, infection by a complex of fungal associates may world’s top producer and exporter of avocados, exceeding impart an increased risk to the host plant (Lynch et al., 2016). the avocado production of any other nation by more than The E. fornicatus species complex is in need of thorough taxo- four-fold, and is followed by Indonesia, Dominican Repub- nomic revision and, as such, the application of scientific names to lic, U.S.A., Columbia, Peru, Kenya, Chile, Brazil, Rwanda, the constituent member species would