Evolution of starvation resistance in an invasive insect species,Aethina tumida (Coleoptera: Nitidulidae)

Starvation resistance, or the ability to survive periods without food, can shed light on selection pressure imposed by food scarcity, including chances to invade new regions as a result of human transport. Surprisingly, little information is known about starvation resistance for invasive insect species. Given that native and invasive populations differ in starvation resistance, this would suggest different selection scenarios and adaptive shifts fostering invasion success. Here, we show striking differences in starvation resistance of adult small hive beetles Aethina tumida (SHB) between native and invasive populations. In the laboratory, starvation resistance of freshly emerged laboratory‐reared and field‐collected adult females and males was evaluated in the beetle's native African range and in their invasive North American range. SHB in their native African range survived longer than SHB in their invasive North American range. Across ranges, females survived longer than males. Field‐collected SHB survived in Africa longer than freshly emerged ones, but not in the invasive range. This suggests no selection for starvation resistance in the invasive range, possibly due to differences between African and European‐derived honey bee hosts facilitating a trade‐off scenario between reproduction and starvation resistance. The ability of adult females to survive up to two months without food appears to be one factor contributing to the invasion success of this species. Assuming food availability is usually high in the invasive ranges, and trade‐offs between starvation resistance and fecundity/reproduction are common, it seems as if selection for starvation resistance during transport could set up potential trade‐offs that enhance reproduction after invasion. It would be interesting to see if this is a possible general pattern for invasive insect species.     

Global warming promotes biological invasion of a honey bee pest

Climate change and biological invasions are two major global environmental challenges. Both may interact, e.g. via altered impact and distribution of invasive alien species. Even though invasive species play a key role for compromising the health of honey bees, the impact of climate change on the severity of such species is still unknown. The small hive beetle (SHB, Aethina tumida, Murray) is a parasite of honey bee colonies. It is endemic to sub‐Saharan Africa and has established populations on all continents except Antarctica. Since SHBs pupate in soil, pupation performance is governed foremost by two abiotic factors, soil temperature and moisture, which will be affected by climate change. Here, we investigated SHB invasion risk globally under current and future climate scenarios. We modelled survival and development time during pupation (=pupal performance) in response to soil temperature and soil moisture using published and novel experimental data. Presence data on SHB distribution were used for model validation. We then linked the model with global soil data in order to classify areas (resolution: 10 arcmin; i.e. 18.6 km at the equator) as unsuitable, marginal and suitable for SHB pupation performance. Under the current climate, the results show that many areas globally yet uninvaded are actually suitable, suggesting considerable SHB invasion risk. Future scenarios of global warming project a vehement increase in climatic suitability for SHB and corresponding potential for invasion, especially in the temperate regions of the Northern hemisphere, thereby creating demand for enhanced and adapted mitigation and management. Our analysis shows, for the first time, effects of global warming on a honey bee pest and will help areas at risk to prepare adequately. In conclusion, this is a clear case for global warming promoting biological invasion of a pest species with severe potential to harm important pollinator species globally.     

Olfactory responses of Aethina tumida murray (Coleoptera: Nitidulidae) to some major volatile compounds from hive materials and workers of Apis mellifera

The small hive beetle (Aethina tumida Murray) is an invasive pest affecting honey bee colonies. The beetles are known to be attracted to volatiles from hive products and honey bees like Apis mellifera L. Previously we reported the presence of five major compounds from the volatile extracts of hive materials; ethyl linolenate and ethyl palmitate from pollen dough, oleamide and tetracosane in fermenting honey, and oleamide and 5-methyl-2-phenyl-1H-indole from A. mellifera worker bees. This study tested the attractiveness of the aforementioned five volatile organic compounds to small hive beetles (SHB) by Y-tube olfactometric bioassay. Ethyl linolenate was highly attractive to both male and female adults of SHB. Ethyl palmitate was attractive to SHB only at higher concentration (0.01–01 mg/ml). Interestingly, tetracosane, 5-methyl-2-phenyl-1H-indole and oleamide were repellent for SHB of both sexes, but ethyl linolenate and ethyl palmitate as components of honey bee brood pheromone attracted SHB. The results highlight that SHB differentially utilizes volatile chemicals from hive materials and honey bees as cues to locate honey bee hives.     

Alien flora of the Korean Peninsula

The Korean Peninsula has been divided into the countries of North and South Korea since 1948. This adoption of different political and socio-economic regimes has significantly changed economic activity and international exchange by those nations, thus affecting the introduction of alien plants. Our study objective was to provide a comprehensive, up-to-date inventory of the alien flora on the Korean Peninsula and to analyse how the partitioning between North and South Korea has influenced the numbers and status of those alien plants. We identified pre-1876 aliens that were brought to the Korean Peninsula before 1876, when Korea opened up to foreign countries, and also determined the post-1876 aliens that were introduced after 1876. Plants in the latter group were further classified into those that arrived before the outbreak of the Korean War in 1950 (1876–1950 aliens) and those introduced since then (post-1950 aliens). We investigated the regions of origin, family compositions, and invasion status of those alien taxa. In total, 504 alien taxa were identified, with 102 taxa being pre-1876 and 117 being 1876–1950 aliens. After the Korean War, the number of alien plants in South Korea more than doubled (276 taxa), whereas the number reported for North Korea was considerably lower (33 taxa). This might be due to enhanced economic activity and a larger human population in South Korea. Climatic differences as well as variations in the recording intensity for alien flora between North and South Korea may also have contributed to the large contrast in numbers of new alien species recorded during the last decades. Coordinated measures between the two nations are necessary if the spread of invasive alien plants onto the Korean Peninsula is to be reduced.     

Genetic diversity and genetic structure of the endangered Manchurian trout, <Emphasis Type="Italic">Brachymystax lenok tsinlingensis</Emphasis>, at its southern range margin: conservation implications for future restoration

The Manchurian trout, Brachymystax lenok tsinlingensis (family: Salmonidae), is a cold freshwater fish endemic to Northeast Asia. South Korean populations of this species, which comprise its southern range limit, have recently decreased markedly in size and are now becoming critically endangered. We assessed the current population status of this species in South Korea by estimating the levels of genetic diversity and genetic structure of five natural and four restored populations using mitochondrial DNA (mtDNA) control region sequences and eight nuclear microsatellite loci. Levels of within-population genetic diversity were low, suggesting that past effective population sizes (N _e) have been small. Each population had one or a maximum of two mtDNA haplotypes. Microsatellite allelic richness (AR) was significantly higher for natural populations (mean AR?=?3.51; 95% confidence interval, 3.00–4.03) than for restored populations (mean AR?=?2.61; 2.38–2.98). South Korean populations were significantly genetically isolated from one another, with private mtDNA haplotypes and microsatellite alleles, suggesting that limited gene flow has been occurring among populations. A mtDNA phylogeny revealed that South Korean lineages were more closely related to those of China than to those of North Korea and Russia. Overall, we suggest that future restoration efforts aimed at South Korean populations should consider the genetic characteristics reported here, which should help to fulfil effective conservation strategies for this highly cherished species. Our results will inform other conservation efforts, including assisted migration of freshwater fish populations at the equatorial end of the geographical range limit of the species.     

我国入侵害虫西部喙缘蝽的溯源分析

本文对我国外来入侵物种西部喙缘蝽Leptoglossus occidentalis Heidemann, 1910进行了溯源分析,依据对国内种群的观察和标本简要描述了其形态特征和生活习性。通过野外采集国内种群标本,提取扩增COI基因序列,结合原产地和国外其他入侵种群的公共序列,构建西部喙缘蝽COI基因数据集,以中国入境口岸对木材的检疫情况为参考,分析西部喙缘蝽的入侵来源。全世界目前已知10种单倍型,中国存在4种。山东青岛种群有H＿8、H＿9和H＿10三种单倍型,其中H＿8与韩国共享,H＿9和H＿10为中国特有单倍型,青岛种群可能部分来自韩国;山东烟台两个采集点的种群都属于H＿2,可能来自北美东部,与青岛种群的入侵来源不同。以上分析表明,我国西部喙缘蝽种群可能来源于多次独立入侵事件,同时在国内发生了小范围的扩散迁移。本研究首次对我国入侵害虫西部喙缘蝽做了溯源分析,为更好地制定规制措施,开展检疫防治工作提供了科学依据。     

Genetic diversity and structure analyses on the natural populations of diploids and triploids of tiger lily, <Emphasis Type="Italic">Lilium lancifolium</Emphasis> Thunb., from Korea,China, and Japan

Tiger lily, Lilium lancifolium Thumb. is an endemic species in Korea. Genetic structure and diversity of diploid and triploid tiger lily accessions were analyzed using SSRP and IRAP molecular markers. All genetic indices analyzed showed that the diploids hold higher genetic variations compared to the triploids which were collected from Korea, China, and Japan. All variations found in triploids were also found in diploids to support the autotriploidy of L. lancifolium. It was also revealed that the triploid populations have experienced population regrowth from small population after population bottleneck. The population and phylogenetic analyses showed that analyzed tiger lilies were partitioned into three populations, Pop 1 from West Sea of Korean Peninsula, Pop 2 from South Sea of Korean Peninsula and Pop 3 of triploids in which many accessions of West Sea and South Sea were admixed in each partitioned group. Although the level of population differentiation is not extensive, F_ST analysis revealed some level of differentiation among the three populations. The analyses of genetic structure and phylogenetic dendrogram revealed admixture in some accessions among populations. All the results obtained in our analyses imply that autotriploid tiger lilies were originated from a small number of accessions of diploid L. lancifolium.     

Behavioral responses of the small hive beetle,Aethina tumida,to odors of three meliponine bee species and honey bees,Apis mellifera scutellata

Recent studies have shown that honey bees, bumble bees, and some meliponine bee species of the genera Trigona, Meliponula, and Dactylurina are hosts of the small hive beetle (SHB) Aethina tumidaMurray (Coleoptera: Nitidulidae), a pest of honey bee colonies in various regions of the world. Olfaction has been implicated in SHB infestations of honey bee and bumble bee colonies. We used olfactometer bioassays to investigate responses of adult male and female SHBs to odors from intact colonies and separate hive components (pot honey, pot pollen, cerumen, and propolis) of three African meliponine bee species, Meliponula ferruginea (Lepeletier) (black morphospecies), M. ferruginea (reddish brown morphospecies), and Meliponula bocandei (Spinola) (Hymenoptera: Apidae). Although both sexes of the beetle strongly preferred intact colony, pot honey, and pot pollen odors, there was no evidence of attraction to propolis and cerumen odors from the three meliponine bee species. Both sexes of SHB also strongly preferred odors from honey bees, Apis mellifera L. (Hymenoptera: Apidae), over odors from the three meliponine bee species. Our results provide substantial evidence of the host potential of African meliponine bees for the SHB, and we discuss this complex association of the SHB with species within the Apidae family.     

Genetic status of Asiatic black bear (Ursus thibetanus) reintroduced into South Korea based on mitochondrial DNA and microsatellite loci analysis

The Asiatic black bear is one of the most endangered mammals in South Korea owing to population declines resulting from human exploitation and habitat fragmentation. To restore the black bear population in South Korea, 27 bear cubs from North Korea and Russian Far East (Primorsky Krai) were imported and released into Jirisan National Park, a reservoir of the largest wild population in South Korea, in 2004. To monitor the success of this reintroduction, the genetic diversity and population structure of the reintroduced black bears were measured using both mitochondrial and nuclear DNA markers. Mitochondrial D-loop region DNA sequences (615 bp) of 43 Japanese black bears from previous study and 14 Southeast Asian black bears in this study were employed to obtain phylogenetic inference of the reintroduced black bears. The mitochondrial phylogeny indicated Asiatic black bear populations from Russian Far East and North Korea form a single evolutionary unit distinct from populations from Japan and Southeast Asia. Mean expected heterozygosity (H(E)) across 16 microsatellite loci was 0.648 for Russian and 0.676 for North Korean populations. There was a moderate but significant level of microsatellite differentiation (F(ST) = 0.063) between black bears from the 2 source areas. In addition, genetic evidences revealed that 2 populations are represented as diverging groups, with lingering genetic admixture among individuals of 2 source populations. Relatedness analysis based on genetic markers indicated several discrepancies with the pedigree records. Implication of the phylogenetic and genetic evidences on long-term management of Asiatic black bears in South Korea is discussed.     

Susceptibility of small honey bee colonies to invasion by the small hive beetle,Aethina tumida (Coleoptera,Nitidulidae)

Weak and small honey bee colonies are supposed to be more susceptible to infestations by the small hive beetle [Aethina tumida, small hive beetle (SHB)]. To test this, we established 24 nucleus colonies [12 with and 12 without previous SHB removal (= screening)]. Four weeks later, we compared beetle numbers and the occurrence of SHB reproduction to the corresponding full‐sized colonies. Full‐sized colonies with no screening were infested with significantly more SHBs than all other groups (mean ± standard deviation = 46.9 ± 26.7). Regardless of this, none of the full‐sized colonies showed damage or evidence of SHB reproduction. In contrast, five nucleus colonies collapsed and SHB larvae were found in an additional seven colonies. Our study demonstrates that SHB infestation levels which are harmless to full‐sized colonies may have a negative impact on small nucleus colonies.     

Origin and dispersal of bluegill sunfish, Lepomis macrochirus, in Japan and Korea

The bluegill sunfish, Lepomis macrochirus, is a notorious exotic species in many freshwater ecosystems, currently expanding its distribution worldwide. In 1960, a small group of bluegills captured in the Mississippi River at Guttenberg in Iowa were imported to Japan as a gift from the mayor of Chicago to the Japanese government. The offspring of these fish were released into the wild in Japan and also in Korea. Over 40 years after this first introduction, L. macrochirus now occupies all the freshwater ecosystems of both countries. We compared invading populations of L. macrochirus in Japan and Korea with native populations in the USA, using PCR-RFLP (polymerase chain reaction-restricted fragment length polymorphism) analyses of mitochondrial DNA, to estimate the origin and dispersal of L. macrochirus in Japan and Korea. Five haplotypes of mitochondrial DNA detected in Japanese and Korean populations completely coincided with the haplotypes of the Guttenberg population. Haplotype diversity of invading populations was shown to be highest in populations established in the 1960s, while genetic variability was lower in more recently established populations. Our results suggest that all L. macrochirus in Japan and Korea have originated from the 15 fish first introduced in 1960. Low haplotype diversity in newly established populations is probably due to genetic drift arising from repeated population bottlenecks, while the high similarity of haplotypes among neighbouring populations is considered to reflect the history of transplantation by humans.     

Molecular phylogeny and biogeography of the Korean woodroaches Cryptocercus spp

Phylogenetic relationships and biogeography of Northeast Asian Cryptocercus were inferred based on the DNA sequences of mitochondrial COII and 16S rRNA genes and nuclear 18S rRNA gene. The results suggest that two clades exist in Korean populations. The southwestern population (Cryptocercus from Jiri-san) was more closely related to the populations from Northeast China and eastern Russia than to all the other Korean Cryptocercus. According to molecular-based estimated divergence times, the divergence event occurred between Cryptocercus in Jiri-san, Northeast China and eastern Russia and those in the remaining South Korea during the Miocene (7.5-17.4Myr ago), and then the divergence event between Cryptocercus in Jiri-san and those in Northeast China and eastern Russia occurred 0.8-1.9Myr ago. In the Korean Peninsula, Jiri-san is located in the most southwestern region among the high mountains surveyed. The location is the farthest from Northeast China and eastern Russia among sampling localities in South Korea. Thus, it was unexpected that the southwestern populations are more closely related to those from Northeast China and eastern Russia rather than to the other Korean Cryptocercus. Based on Korean topography and estimated divergence times, possible scenarios are proposed for the current geographical distribution of Korean Cryptocercus.     

Genetic divergence between the South Korean and Mongolian populations of the dung beetle,Gymnopleurus mopsus (Coleoptera: Scarabaeidae) based on mitochondrial cytochrome c oxidase subunit I (COI) gene sequences

The locally extinct dung beetle, Gymnopleurus mopsus Pallas, 1781 (Coleoptera: Scarabaeidae), has not been found in South Korea since the 1970s. This research was conducted to understand the genetic divergence between the South Korean and Mongolian populations of G. mopsus as a part of its reintroduction program in South Korea. The genetic distance and diversity were determined using the mitochondrial cytochrome c oxidase subunit I (COI) gene sequence (658 bp ) corresponding to the DNA barcode region. The mitochondrial COI gene sequences of 64 individuals of G. mopsus collected in South Korea (7 individuals) and Mongolia (57 individuals) showed a relatively high level of genetic diversity (nucleotide diversity, 0.0078 ± 0.0007; Haplotype diversity, 0.965 ± 0.017). The genetic distances between the South Korean and Mongolian populations lay within the intraspecific level and the phylogenetic reconstruction using the neighbor‐joining (NJ) method showed that all individuals belonged to a single clade. This result indicates that the current Mongolian population of G. mopsus is a good candidate source population to restore the locally extinct population of the species in South Korea.     

Two genetic lineages of sea slaters, Ligia (Crustacea: Isopoda) in South Korea: a population genetic approach

In this study, the species composition and population genetic properties of the sea slater, Ligia, in South Korea were investigated using mitochondrial and nuclear gene sequences. Two groups of sea slaters, genetically isolated from each other, a Western Group (WG) and an Eastern Group (EG) were identified. These groups exhibited considerable genetic divergence from Ligia exotica, previously recorded as a species inhabiting this country. These results indicate that there may be two species of Ligia in South Korea, but there is a small probability that both groups are L. exotica. A comparison of their genetic properties indicates that WG has a higher effective population size than EG, and that EG may have experienced a recent expansion, implying that it has a shorter history in South Korea than WG. These findings suggest that the South Korean sea slater populations may have been established as a result of several colonization events that can be traced on a continental scale by phylogeographic studies of sea slaters.     

Uncovering the spatial pattern of invasion of the honeybee pest small hive beetle,Aethina tumida,in Italy

The fast tracking of invasion spatial patterns of alien species is crucial for the implementation of preventive and management strategies of those species. Recently, a honeybee pest, the small hive beetle Aethina tumida (hereafter SHB), has been reported in Italy, where it colonized more than 50 apiaries in an area of about 300 km². SHB is a nest parasite and scavenger of honeybee colonies native of Sub-Saharian Africa. Likely being helped by the globalization of apiculture, SHB underwent several invasions in the last twenty years, causing locally relevant economic impact. While many features of its biology have been addressed, an important knowledge gap concerns the spatial invasion dynamics in invaded areas. In this paper we coupled two spatial analysis techniques (geographic profiling and a density-based spatial clustering algorithm) to uncover the possible invasion pattern of SHB in Italy. We identified the port town of Gioia Tauro as the most likely point from which SHB may have spread and suggested the possible successive axes of diffusion. These putative diffusion paths suggest that the SHB spread in south Italy might have been due to a mix of natural dispersal between close apiaries and longer distance movement through faster, likely human-mediated, communication routes.     

Higher genetic diversity in introduced than in native populations of the mussel Mytella charruana: evidence of population admixture at introduction sites

Aim  Levels of genetic diversity can be used to determine haplotype frequency, population size and patterns of invasive species distribution. In this study, we sought to investigate the genetic structure of the invasive marine mussel Mytella charruana and compare variation from invasive populations with variation found within three native populations.
Location  Invaded areas in the USA (Florida, Georgia); native areas in Ecuador, Colombia and Brazil.
Methods  We sequenced 722 bp of the mitochondrial COI gene from 83 M. charruana samples from four invasive populations (USA) and 71 samples from two natural populations (Ecuador, Columbia). In addition, we sequenced 31 individuals of a congeneric species, Mytella guyanensis , from Salvador, Brazil. We constructed the phylogenetic relationship among all haplotypes and compared diversity measures among all populations.
Results  We found significantly higher levels of nucleotide diversity in invasive populations than in native populations, although the number of haplotypes was greater in the native populations. Moreover, mismatch distribution analyses resulted in a pattern indicative of population admixture for the invasive populations. Conversely, mismatch distributions of native populations resulted in a pattern indicative of populations in static equilibrium.
Main conclusion  Our data present compelling evidence that the M. charruana invasion resulted from admixture of at least two populations, which combined to form higher levels of genetic diversity in invasive populations. Moreover, our data suggest that one of these populations originated from the Caribbean coast of South America. Overall, this study provides an analysis of genetic diversity within invasive populations and explores how that diversity may be influenced by the genetic structure of native populations and how mass dispersal may lead to invasion success.     

Tracing the origin of US brown marmorated stink bugs, Halyomorpha halys

Identifying the origin of a biological invasion has important applications to the effective control of the invaders. This is more critical for invasive agricultural pests that cause severe economic losses. The brown marmorated stink bug, Halyomorpha halys, originally from East Asia, has become a principal agricultural pest in the US since its first detection in Pennsylvania in 1996. This species is responsible for crop failures on many mid-Atlantic farms and current control efforts rely on heavy insecticide applications because no other options are available. To examine the genetic diversity and identify the source region of the US introductions, we sequenced portions of the mitochondrial cytochrome c oxidase subunit II gene, 12S ribosomal RNA gene and control region in populations from the US, China, South Korea and Japan. We detected high genetic divergence among native populations and traced the origin of US H. halys to the Beijing area in China. We observed much lower genetic diversity in exotic compared to native populations—two mitochondrial haplotypes in 55 US specimens versus 43 haplotypes in 77 native specimens. A single introduction of small propagule size matches the invasion history in the US. For the effective control of the US population, we suggest that surveys on egg parasitoids and insecticide resistance in natives should focus on the Beijing area in China.     

Inferring the invasion history of coral berry Ardisia crenata from China to the USA using molecular markers

Genetic comparisons between native and invasive populations of a species can provide insights into its invasion history information, which is useful for guiding management and control strategies. The coral berry Ardisia crenata was introduced to Florida last century as a cultivated ornament plant, and has since spread widely throughout the southern regions of the USA. Previously, the genetic variation among 20 natural populations of A. crenata across its distribution center in southern China was quantified using seven microsatellite markers. Here we expand on that work by additionally sampling individuals from four other native populations in Taiwan and Japan, and from five invasive populations in the USA. We also examined the results from one chloroplast intergenic spacer region (trnF-trnL) in all 29 populations. Our aim is to identify the invasion source and subsequent history of the species?? spread throughout the southern USA. We observed lower genetic diversity in the invasive populations based on both microsatellite and chloroplast markers. Our data show that the invasive populations can be clustered with native populations in southeastern China, inferring this region as the geographic origin of A. crenata cultivars invading the USA. We further classified invasive individuals into invasive I and invasive II clusters. Nantou in Taiwan and Xihu in mainland China are the most closely related populations to those, which identify the former as potential sources for host-specific control agents. Our results, combined with the known introduction records, suggest that A. crenata was first multiply introduced into Florida and then secondarily colonized Louisiana and Texas from Florida.     

DNA data and morphology suggest an occurrence of Dendrolimus sibiricus Tschetverikov, 1908 (Lepidoptera: Lasiocampidae) instead of D. superans Butler, 1877, in South Korea

In the present study, specimens of Dendrolimus superans collected from South Korea suggest the presence of D. sibiricus, instead of D. superans. Comparisons of the wing morphology, female and male genitalia, 3′‐end region of the cytochrome c oxidase I (COI) gene sequence, and internal transcribed spacer (ITS) 2 sequence of the Korean specimens with those of the D. superans specimens from Japan consistently supported the presence of D. sibiricus in South Korea. Phylogenetic analyses of the concatenated sequences of COI and ITS2 from the available sequence types of D. sibiricus and D. superans, along with South Korean specimens, were conducted using the Bayesian inference (BI) and maximum likelihood (ML) methods. These phylogenetic analyses placed the South Korean specimens with the Russian D. sibiricus as an inclusive group, excluding the Japanese D. superans, indicating the distribution of D. sibiricus in South Korea. Nevertheless, D. superans formed a distinct group only by BI analysis (Bayesian posterior probabilities = 0.89), whereas D. sibiricus, including the South Korean samples, formed a distinct group only by the ML analysis (99%), suggesting a low genetic divergence between the two species.