Diptera) in Hongneung Arboretum, Seoul, Korea

Journal of Asia-Paciﬁc Biodiversity xxx (2015) 1e6

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Original article Winter ﬂight of ﬂies (Diptera) in Hongneung Arboretum, Seoul, Korea

Tae-Sung Kwon a,*, Cheol Min Lee b, Ok Yeong Ji c a Division of Forest Insect Pests and Disease Division, Korea Forest Research Institute, Seoul, South Korea b Division of Forest Ecology, Korea Forest Research Institute, Seoul, South Korea c Korea Diptera Laboratory, Seoul, South Korea article info abstract

Article history: Winter phenology (diapause and activity) of insects is expected to change more significantly than that of Received 30 June 2015 other seasons, because temperature will increase more in winter than in other seasons in temperate Received in revised form regions. However, studies on winter phenology of insects are rare. It is expected that winter flights of flies 12 October 2015 (Diptera) will increase as climate warms. This study aims to find the relationship between flight of flies Accepted 13 October 2015 and temperature. The survey on flies and weather (temperature and rainfall) was carried out in the Available online xxx Hongneung Arboretum in Seoul, Korea. Flies were collected weekly from December 2012 to February 2013 using sweeping and Malaise trap. In the survey, 106 flies belonging to 28 morphospecies and 17 Keywords: fl Diptera families were collected. Richness and abundance of ies were positively correlated with temperature. Ó phenology Copyright 2015, National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA). temperature Production and hosting by Elsevier. This is an open access article under the CC BY-NC-ND license (http:// winter flight creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction published (Andrew et al 2012), it is evident that flies are suitable for investigating the impact of climate change. However, these studies Due to the use of fossil fuels and destruction of forests, the are usually focused on pests or disease vectors. average global temperature rose by w0.75C over the past 100 Although a few studies examined the seasonal occurrence of years (IPCC 2007), and the temperature of Korea rose by w1.5C flies in Korea, the studies were usually conducted between March (Kwon 2003). Such changes in temperature also change the and November (e.g. Gu et al 1965; Jo 1993), and even when parts of phenology of organisms (Walther et al 2002). In the case of insects, the winter season are included in the investigation period, it was whose body temperature is mainly determined by the air temper- reported that almost no flies were collected during that period (Jo ature, change of temperature has a huge impact on insect and Park 1992). Both the increase of average temperature and the phenology (Chon and Kwon 1985; Park et al 2003; Uvarov 1931). In effect of extreme climates are important to investigate the impact South Korea, two studies showed different results regarding the of climate change (Sinclair et al 2003). The increase in temperature influences of temperature increases on the phenologies of lepi- is different across seasons, and the increase of temperature is much dopteran species. In the case of Dendrolimus spectabilis, it was found higher in the winter season than in other seasons (Lee et al 2011). that rise in temperatures led to an increase in generation numbers Therefore, the increase in temperature may greatly increase winter (Choi et al 2011; Kwon et al 2002). In the case of butterflies, how- activities of insects. In temperate regions like Korea, insects usually ever, the time of flight of adults was not different between the late hibernate as eggs, larva, and pupa, while some species overwinter 1950s and the early 2000s, showing no influence of the rise of as adults, which remain almost inactive in winter. However, when temperature (Kwon et al 2008). Although flies are one of the most the temperature in winter was high, flying flies were observed. diverse insect groups, ecological studies on Korean flies are very Therefore, it is expected that the flight of flies in the winter season rare, excluding a few studies of taxonomy or pest species. As many is closely related to temperature. There are a few studies on the studies on flies related to global warming have recently been winter occurrence of flies in Europe and North America (Reisen et al 2010; Soszynska 2004), but there are none in Korea. However, it was exceptionally reported that adults of the Chionea sp. (Tipuli- dae) walked on snow in mountains (Lee 2011). The present study * þ þ Corresponding author. Tel.: 822 961 2662; fax: 822 961 2679. was carried out to identify the correlation between winter flight of E-mail address: [email protected] (T.-S. Kwon). flies and temperature. Peer review under responsibility of National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA). http://dx.doi.org/10.1016/j.japb.2015.10.006 pISSN2287-884X eISSN2287-9544/Copyright Ó 2015, National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA). Production and hosting by Elsevier. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Please cite this article in press as: Kwon T-S, et al., Winter flight of flies (Diptera) in Hongneung Arboretum, Seoul, Korea, Journal of Asia-Pacific Biodiversity (2015), http://dx.doi.org/10.1016/j.japb.2015.10.006 2 TS Kwon et al. / Journal of Asia-Pacific Biodiversity xxx (2015) 1e6

Table 1. Number of ﬂies collected in the Hongneung forest in Seoul from December 6, 2012 to February 29, 2013.

Species 2012 2013 Study method Study site (sweeping) Total

Dec Jan Feb Malaise trap Sweeping Forest gap Garden

Agromyzidae sp. 1 2 1 1 1 2 Anthomyiidae sp. 1 2 2 4 4 Aulacigastridae sp. 1 1 1 1 Calliphoridae sp. 1 1 1 1 Chironomidae sp. 1 1 1 2 1 1 2 Chloropidae sp. 1 1 1 1 1 Chloropidae sp. 2 1 1 1 1 Dolichopodidae sp. 1 1 1 1 Drosophilidae sp. 1 1 3 4 4 4 Drosophilidae sp. 2 1 1 1 Ephydridae sp. 1 1 1 1 1 Ephydridae sp. 2 1 1 1 3 2 1 3 Fanniidae sp. 1 7 10 28 22 23 6 17 45 Fanniidae sp. 2 3 1 3 1 1 4 Lauxaniidae sp. 1 3 3 2 1 3 Lauxaniidae sp. 2 1 1 1 1 1 2 Lauxaniidae sp. 3 2 2 2 2 Lonchaeidae sp. 1 1 1 1 3 2 1 3 Muscidae sp. 1 1 1 1 Muscidae sp. 2 2 2 2 Muscidae sp. 3 3 3 1 2 3 Mycetophilidae sp. 1 1 1 1 Mycetophilidae sp. 2 1 1 1 Mycetophilidae sp. 3 1 1 1 1 1 2 Phoridae sp. 1 4 2 4 8 2 2 10 Phoridae sp. 2 1 1 1 Sciaridae sp. 1 2 2 2 Sphaeroceridae sp. 1 2 2 2 2 Species richness 11 13 18 17 17 8 15 28 No. of individuals 25 27 54 52 54 17 37 106

Materials and methods using the identification key of Papp and Schumann (2000) and Triplehorn and Johnson (2005). The fly specimens used in this Survey of flies study are stored in the forest biospecimen room of the Korea Na- tional Arboretum. The fly survey was carried out at the Hongneung Arboretum located at the Korea Forest Research Institute, Seoul, Korea (North Data analysis 37.593546, East 127.044618). The Hongneung Arboretum was established in Korea in 1922, and is home to over 2000 species of The temperature data of the survey area used were obtained plants, as well as a variety of insects and birds (Kwon et al 2011; Lee from the automatic weather station (KWT1000, KL300) installed w et al 2012; Park et al 2014). The forest ( 40 ha) in the Hongneung at the Korea Forest Research Institute, and the precipitation data Arboretum is an urban forest within a city space and is currently were obtained from the Seoul meteorological measuring station being used as an experimental forest of the Korea Forest Research data (http://www.kma.go.kr/weather/climate/average_south.jsp, Institute. Details on the Hongneung Arboretum are available in the connected on March 23, 2015). Environmental factors that affect fl studies of Kwon et al (2011) and Cho et al (2014). The survey of ies the number of flies were analyzed using generalized linear was conducted in the garden located in front of the main building of the Korea Forest Research Institute and in a small (0.5 ha) forest gap located at the entrance of the experimental forest where shrubs and herbs grow. The survey was conducted every week from December 6, 2011 to February 28, 2012. Flies were collected using two methods: sweeping and Malaise trap. Sweeping was conducted using an insect net (diameter 38 cm, rod length 50 cm) while slowly walking along the survey site and sweeping 60 times on various vegetations such as trees, shrubs, and herbs. Everything collected was then placed in a vinyl bag and placed in a freezer for 24 hours to kill the flies. The survey was carried out on days with no rain or snowfall, and it was conducted around 2 PM when the temperature was highest during the day. The collected samples were observed under a stereoscopic microscope to sort flies; they were stored in 100% ethyl alcohol and were converted into dry specimens later. A survey using the Malaise trap was conducted on the same day as that of sweeping. Fly specimens collected using the Malaise trap were stored in 100% ethyl alcohol and were converted fi into dry specimens later. Fly specimens were identi ed to family Figure 1. Daily mean temperature and rainfall during the study period in the Hon- level and morphospecies. Family identification was conducted gneung Arboretum in Seoul.

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version 8.0 (Statsoft, Inc., Tulsa, OK, USA) was used for statistical analysis.

Results

Data of the temperature and precipitation at the survey site are shown in Table 1. The maximum temperature during the survey period was 11.4C and the minimum temperature was 18C, with an average temperature of 3.2C. The monthly average temperature was lowest in December (4.3C), and it was 3.6Cin January and 1.3CinFebruary(Figures 1 and 2). A total of 106 flies belonging to 28 species in 17 families were collected during the survey period (Table 1). Among the monthly abundance, it was lowest in December (25 individuals of 11 species) and January (27 individuals of 13 species), and highest in February (54 individuals of 18 species). Such monthly difference had a close relationship with the monthly average temperature, and so the number was highest in February when the temperature was highest and lowest in December when temperature was lowest (Figure 2). Numbers of individuals and species captured using the Malaise trap and sweeping were similar. However, considering that the samples was conducted at two sites and Malaise trapping at one site, it can be said that the number of flies collected using the latter method was about twice that collected with the former method. However, while the samples were collected for about 1 week using the Malaise trap, those were collected in just a few minutes with sweeping, so it is evident that sweeping is a very useful survey method for flies in winter. Comparing by the survey sites, the numbers of species collected in the garden site was over double Figure 2. Occurrence of flies collected by Malaise trap and sweeping. Dark area that collected in the forest gap site. The garden site faces south indicates the monthly mean temperature during the study period. and is near a building, while the forest gap site faces north and is within the forest and thus having lower temperature; therefore, analysis. For the Malaise trap data, four linear variables (such as such a difference is caused by differences in temperature of the temperatureddaily maximum, minimum, and average, and pre- survey sites. cipitation) and one category variable (month) were used as in- The number of species per family was 1e3, and the highest was dependent variables. For the analysis of the sweeping data, one three species in Lauxaniidae, Muscidae, and Mycetophilidae. The linear variable (daily maximum temperature) and one category most abundant species was Fanniidae sp. 1 (145 individuals), which variable (month) were used as independent variables. Regression accounted for about 42% of the total species occurred (Table 1). analysis was used for determining the relationship between Tables 2 and 3 show numbers of individuals of families in various number of flies and temperature. In the case of sweeping data, the temperature zones. When examining those collected in the Malaise maximum temperature of the day of survey was used as the in- trap, 20 of all the individuals (38%) were collected when the weekly dependent variable in the regression analysis, and for the data of average temperature was under 0C. In particular, one Lauxanidae the Malaise trap, the weekly average temperature was used as the was collected when the weekly average temperature was 5.2C. independent variable. As the number of flies collected was not By contrast, in the case of sweeping, only three flies were collected large, the regression analysis was not conducted at the family when the maximum temperature of the survey date was under 0C, level; instead, the number of individuals collected in various accounting for only 6% of the total. There was a very close rela- temperature ranges was represented in a table. STATISTICA tionship between the number of species of flies and the number of

Table 2. Number of ﬂies collected by Malaise trap in various temperature zones.

Family Temperature range (C) Total

6e5 5e4 4e3 3e2 2e1 1e00e11e22e3

Agromyzidae 11 Anthomyiidae 224 Aulacigastridae 11 Calliphoridae 1 1 Dolichopodidae 11 Drosophilidae 1 1 Fanniidae 7 7 11 25 Lauxaniidae 1 1 Muscidae 213 Mycetophilidae 33 Phoridae 2 2 2 3 9 Sciaridae 2 2 Total 1 0 0 2 17 0 11 0 21 52

Please cite this article in press as: Kwon T-S, et al., Winter flight of flies (Diptera) in Hongneung Arboretum, Seoul, Korea, Journal of Asia-Pacific Biodiversity (2015), http://dx.doi.org/10.1016/j.japb.2015.10.006 4 TS Kwon et al. / Journal of Asia-Pacific Biodiversity xxx (2015) 1e6

Table 3. Number of ﬂies collected by sweeping in various temperature zones.

Family Temperature range (C) Total

9e8 8e3 3e2 2e1 1e11e22e33e44e55e11 11e12

Agromyzidae 11 Chironomidae 11 2 Chloropidae 112 Drosophilidae 314 Ephydridae 1214 Fanniidae 1 1 1 12111 6 24 Lauxaniidae 2226 Lonchaeidae 11 1 3 Muscidae 123 Mycetophilidae 11 Phoridae 22 Sphaeroceridae 22 Total 101103832301454

individuals (Figure 3), so the number of species could be explained and month did not have a significant impact on the number of by the number of individuals with an accuracy exceeding 90%. Such individuals in both survey methods. The regression models using a high correlation is most likely due to the fact that there were not temperature as an independent variable were shown to be signif- many individuals per species (Table 1). In the generalized linear icant in cases of both Malaise trap and sweeping, and the explan- analysis, the weekly average and minimum temperatures had a atory power of the model was w38e43% (Figures 4 and 5). Thus, significant impact in the case of the Malaise trap, whereas the the observations and models indicate that the number of species maximum temperature on the day of survey had a significant and individuals increased with temperature. impact in the case of sweeping (Table 4). However, precipitation Discussion

In the present study, it was found that a relatively high number of flies were flying in the winter season and such activities were determined mainly by temperature. Therefore, it is predicted that if temperature increases, the number of in- dividualsandspeciesofflies flying in the winter season will also increase. Results of this study show that the higher the increase of temperature, the more the number of flies that will flyin winter. In the Malaise trap, because it was set up continuously for 1week,flies might be collected at relatively high temperatures in cold weeks, so a relatively higher number of flies were collected even at the below-zero weekly average temperature compared with sweeping. According to the results on occurrence of arthropods on snow in Poland, more than half of the individuals were flies (Soszynska 2004). Of the 16 families that occurred in the present study, and excluding Aulacigastridae, Dolichopodidae, and Lonchaeidae, 14 families also occurred in Poland. This shows that the families that appeared in the present study include species that overwinter in adult stage without hibernation. All species collected in this study are likely to be species that spend the winter as imago. This is because there is very little possibility for the flies to grow from larva or pupa into imago at the low temperatures (average 3.2C) of the study period. Hövemeyer (2000) identified 12 kinds of the

Table 4. Results of the generalized linear model for the inﬂuence of environmental factors on abundance of ﬂies.

Variable d.f. Sum of Mean Fp squares squares

Malaise trap Mean temperature (C) 1 209.8 209.8 10.21 0.019 Maximum temperature (C) 1 6.7 6.7 0.33 0.589 Minimum temperature (C) 1 136.4 136.4 6.64 0.042 Precipitation 1 4.4 4.4 0.21 0.659 Month 2 62.3 31.2 1.52 0.293 Sweeping Maximum temperature (C) 1 151.6 151.6 6.115 0.035 Month 2 13.3 6.6 0.268 0.771 Figure 3. Relationship between species richness (number of species) and abundance (number of individuals) of ﬂies collected by Malaise trap and sweeping. d.f. ¼ degrees of freedom.

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Figure 5. Characteristics of flies collected by sweeping: A, species richness (number of Figure 4. Characteristics of flies collected by Malaise trap: A, species richness (number species) versus daily maximum temperature; and B, abundance (number of fi of species) versus weekly mean temperature; and B, abundance (number of individuals) versus daily maximum temperature. The line in the gure indicates the individuals) versus weekly mean temperature. The line in the figure indicates the expected values from the regression model. expected values from the regression model. without any purpose, this would reduce their fitness (paradox of fly fly lifecycle, of which only one spends the winter as imago. This is winter flight). Since flying without any purpose may lead to un- the lifecycle of Tephritis bardanae (Tephritidae), in which flies are necessary consumption of energy and there is a possibility of in the eggs, larva, and pupa states from July to September, and freezing due to sudden temperature drops, it would be more ad- then spend their time as imago from September to June of the vantageous to hibernate as imago in the soil or among leaves than following year. However, when considering the results of the aimlessly flying in winter. However, if they are flying for repro- present study and that of Hövemeyer (2000) that species under a duction activities in winter, the flight in cold times may consume number of families spend the winter as imago, it is very likely that low energy and experience low chance with natural enemies there are flies with various lifecycles that spend the winter as (Aitchison 2001; Durska 2003). It is also expected that the imago are existent. competition for oviposition place is low in winter. These benefits The largest number of flies was collected in Poland in early may increase fitness of flies that fly in winter. Hence, more research December (Soszynska 2004), but in the present study, the fewest is needed on this issue. number of flies was collected in December and the most in While there is little difference in tolerance of high temperature February when the temperature was highest. In Germany, which among insects, there is a great difference in tolerance of low shares borders with Poland, the number of flies was highest in temperatures (Addo-Bediako et al 2000). Therefore, this is an December as well (reference in Soszynska 2004). In Poland, flies important factor in determining the distribution range of insects that are active on top of snow were investigated, so the surrounding (Kwon et al 2014b). If winter cold decreases in temperate areas environmental conditions were important; in addition, activities of such as Korea due to global warming, southern insects will in- flies had higher relations with humidity than with temperature crease in distribution, and the insect fauna would be expected to (Soszynska 2004). Activities of imagoes usually include mating, become richer and more diverse (Deutch et al 2008). However, spawning, eating, and defending their territory, but it seems un- according to the prediction on the change of distribution of ants, likely that imagoes perform such activities in winter. However, if spiders, and beetles, based on the recent national survey data, imagoes fly in relatively higher temperatures in the winter season there are more northern species than southern species in the

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