High Degree of Polyphagy in a Seed-Eating Bark Beetle

High Degree of Polyphagy in a Seed-Eating Bark Beetle

ISSN : 0917-415X DOI:10.3759/tropics.MS18-07 TROPICS Vol. 27 (3) 59-66 Issued December 1, 2018 ORIGINAL ARTICLE High degree of polyphagy in a seed-eating bark beetle, Coccotrypes gedeanus (Coleoptera: Curculionidae: Scolytinae), during a community-wide fruiting event in a Bornean tropical rainforest Asano Iku1*, Takao Itioka1, Atsushi Kawakita2, 3, Hideaki Goto4, Akira Ueda4, Usun Shimizu-kaya1, 5 and Paulus Meleng6 1 Graduate School of Human and Environmental Studies, Kyoto University, Kyoto, Japan 2 Center for Ecological Research, Kyoto University, Otsu, Japan 3 The Botanical Gardens, Graduate School of Science, The University of Tokyo, Tokyo, Japan 4 Kyushu Research Center, Forestry and Forest Products Research Institute, Kumamoto, Japan 5 Faculty of Life and Environmental Science, Shimane University, Matsue, Japan 6 Research Development and Innovation Division, Forest Department Sarawak, Kuching, Malaysia * Corresponding author: [email protected] Received: October 14, 2018 Accepted: November 9, 2018 ABSTRACT A bark beetle Coccotrypes gedeanus Eggers (Coleoptera: Curculionidae: Scolytinae) is a dominant insect seed predator of dipterocarp fruits in the lowland tropical rainforests of Southeast Asia. In this study, the host preference and host range of C. gedeanus was determined by sampling 22,216 fruits from 137 species of 59 genera belonging to 24 families in a primary lowland mixed dipterocarp forest in Borneo. Coccotrypes gedeanus adults were found in the fruits of 51 species from 19 genera belonging to 13 families, and were observed to settle in the fruits of 34 species of 11 genera belonging to 6 families to initiate breeding. Except one plant species, the rest of the 34 plant species were confirmed to bear“ nut” or“ drupe” type fruit. These results suggested that a population of C. gedeanus utilize seeds of various plant species simultaneously. The polyphagy of the bark beetle might be adaptive for survival in the Bornean tropical rain forests where the density of each plant species is low, and most plants produce fruits at unpredictably long intervals. Our results also suggested that the characteristics of fruit might affect the host plant preference of C. gedeanus adults and/or the growth performance of C. gedeanus larvae. Key words: Dipterocarpaceae, general flowering, masting, predator satiation hypothesis, Southeast Asian tropical rainforests INTRODUCTION of dipterocarp reproduction. However, limited biological information on C. gedeanus is available. In the lowland tropical rainforests of Southeast Asia, Many Coccotrypes species breed in small hard seeds Dipterocarpaceae is a dominant family that includes many (Kirkendall et al. 2015), most are considered to have wide canopy tree species (Ashton 2004; Ghazoul 2016). Most host ranges (Wood & Bright 1992), and some can use seeds dipterocarp species in the region produce large fruit at as well as bark, leafstalks, and other plant tissues as their irregular intervals of 2‒10 years, synchronously with many breeding spaces (Jordal et al. 2002, Kirkendall et al. 2015). other tree species at the community level (Appanah 1985; Although several studies have reported that C. gedeanus Ashton et al. 1988; Sakai et al. 1999, 2006). Such uses the seeds and leafstalks of multiple plant families as reproduction periods are termed“ community-wide host plants (Beaver 1979a; Wood & Bright 1992; Jordal et synchronized reproduction” (CSR), and start with al. 2002, Nakagawa et al. 2003), most studies have been community-wide flowering, which was originally termed based on fragmentary records and have included insufficient “general flowering”. Coccotrypes gedeanus Eggers seed samples obtained by routine sampling from a site. (Coleoptera: Curculionidae: Scolytinae) is a bark beetle and Thus, to date, the host preference and host range of C. one of the most dominant insect predators of dipterocarp gedeanus at the population level have not been sufficiently seeds. This beetle reproduces during CSR periods in a elucidated. Bornean lowland tropical rainforest (Nakagawa et al. 2003; In this study, to determine the host preference and host Iku et al. 2018), and is thus predicted to affect the success range of C. gedeanus, we repeatedly sampled fruits of 60 TROPICS Vol. 27 (3) Asano Iku, Takao Itioka et al. Fig. 1. Lateral view of a Coccotrypes gedeanus adult female (a), and a C. gedeanus adult female with several eggs inside a Dipterocarpus globosus seed (b). The latter photo shows that the female has settled into the seed. Photograph (b) captured by Makoto Yokotsuka. various tree species and collected bark beetles from the Coccotrypes gedeanus sampled fruits during a CSR period in a Bornean tropical rainforest. Coccotrypes gedeanus is a bark beetle species and a seed predator in a wide area of Southeast Asia (Fig. 1a) (Wood & Bright 1992). One or a few female adults burrow MATERIALS AND METHODS into a post-dispersal fruit of the host species, excavate tunnels and galleries inside the fruit, including the seed Study site part, and lay multiple eggs in the galleries. The larvae feed mainly on seed parts of the host fruit and pupate within the The study site was a primary lowland mixed dipterocarp galleries (Fig. 1b) (Hulcr et al. 2007; Iku et al. 2018). After forest in Lambir Hills National Park, Sarawak, Malaysia sib-mating, the new female adults disperse from the host (4°20′N, 113°50′E; altitude, 50‒250 m). The mean annual fruit (Jordal et al. 2002). Usually, more than 15 new adults temperature and precipitation were 26℃and 2,600 mm, appear from a host fruit, which has lost its germination respectively (Kume et al. 2011). The forest at the study site capacity. is composed of more than 1,100 tree species belonging to Wood & Bright (1992) reported that the beetle used approximately 80 families (Lee et al. 2002), more than seeds of plants belonging to Anacardiaceae, Burseraceae, 20 % of which reproduce during CSR periods (Sakai et al. Dipterocarpaceae, and Moraceae as its food resources, 2006). Most plant species that reproduce during CSR although it is unclear whether the predation occurred during periods, including most of the dipterocarp species in that CSR periods. In the study site, the beetle was confirmed to region, produce seeds only during CSR periods. prey on seeds of plants belonging to mainly Dipterocarpaceae, The field survey was conducted in two research plots but also Celastraceae, Moraceae, and Myrtaceae during a (an 8 ha plot: 200×400 m and a 4 ha plot: 200×200 m) and CSR period (Nakagawa et al. 2003). The beetle usually three belt transects along sightseeing trails (approximately utilizes plant seeds as its food resources; however, in some 10 m×1 km, 10 m×1 km, 10 m×2 km, respectively). cases, such as an absence of plant seeds around its habitats, Almost all trees over 10 cm DBH in the research plots, it apparently also uses leafstalks (Beaver 1979a). consisting of approximately 6,100 and 2,800 trees in the 8 and 4 ha plots, respectively, were identified at the species level. Although most trees in the belt transects were not Sample collection identified, the species composition of the trees was similar to that within the two research plots. Fruit was collected in the study site over 9 months in a long CSR period from August 2013 to October 2014 (see Iku et al. 2017 for details). We repeatedly collected the fallen fruits of various plant species within the two research High degree of polyphagy in a bark beetle Coccotrypes gedeanus 61 plots and the three belt transects, mainly targeting canopy GenBank (accession number AF375310). If a sampled tree species, at intervals of 1‒3 weeks during the CSR beetle shared 99 % identity with the registered sequence, period. Fifty fruits were collected from each species per the sampled beetle was identified as C. gedeanus. sampling event. When the total number of fallen fruits was less than 50, we collected as many as possible. We dissected the sampled fruits to detect any bark beetles inside. We also RESULTS recorded the presence or absence of bark beetle eggs or larvae in a small fraction of sampled fruits per plant species. In total, we collected 22,216 fruits from 137 species of The plant species where at least one C. gedeanus adult was 59 genera belonging to 24 families (Table 1). The total found with their eggs or larvae in a fruit, we considered that number of adult bark beetles obtained from the collected the bark beetle could have settled in the fruit of the plant fruit was 3,710. Of these, 1,791 were C. gedeanus, which species and started breeding. All sampled bark beetles were were collected from 51 species belonging to 19 genera of preserved in 99.5 % ethanol soon after sampling. 13 plant families (Table 1). There were no inconsistencies between identification based on morphological charac- teristics and that based on sequences of the COI gene. In Identification of the collected bark beetles each of 34 species belonging to 11 genera of six families, at least one C. gedeanus adult settled in fruits to begin We sorted C. gedeanus from all collected bark beetles breeding (Table 1). Except Allantospermum borneense based on their morphological characteristics. Bark beetle (Irvingiaceae), all plant species were confirmed to bear nut- species belonging to Coccotrypes are often difficult to or drupe-type fruit (Table 1). distinguish based on morphological characteristics alone Bark beetles other than C. gedeanus accounted for (Jordal et al. 2002; Hulcr et al. 2015); therefore, we also approximately 51.7 % of those obtained from fruits. All used DNA barcoding (Hebert et al. 2003) to confirm the belonged to Coccotrypes, comprising at least six species; identification based on morphological characteristics. however, they could not be identified at the species level. Identification via DNA barcoding is based on the sequences of the mitochondrial cytochrome oxidase subunit I (COI) gene, which is a standard marker used to detect within- and DISCUSSION among-species variations in bark beetles (Jordal et al.

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