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Winter flight of flies (Diptera) in Hongneung Arboretum, Seoul, Korea
Journal of Asia-Pacific Biodiversity xxx (2015) 1e6
H O S T E D BY
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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 Division of Forest Ecology, Korea Forest Research Institute, Seoul, South Korea c Korea Diptera Laboratory, Seoul, South Korea b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 30 June 2015 Received in revised form 12 October 2015 Accepted 13 October 2015 Available online xxx
Winter phenology (diapause and activity) of insects is expected to change more significantly than that of other seasons, because temperature will increase more in winter than in other seasons in temperate regions. However, studies on winter phenology of insects are rare. It is expected that winter flights of flies (Diptera) will increase as climate warms. This study aims to find the relationship between flight of flies and temperature. The survey on flies and weather (temperature and rainfall) was carried out in the 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 families were collected. Richness and abundance of flies were positively correlated with temperature. 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/).
Keywords: Diptera phenology temperature winter flight
Introduction Due to the use of fossil fuels and destruction of forests, the average global temperature rose by w0.75 C over the past 100 years (IPCC 2007), and the temperature of Korea rose by w1.5 C (Kwon 2003). Such changes in temperature also change the phenology of organisms (Walther et al 2002). In the case of insects, whose body temperature is mainly determined by the air temperature, change of temperature has a huge impact on insect phenology (Chon and Kwon 1985; Park et al 2003; Uvarov 1931). In South Korea, two studies showed different results regarding the influences of temperature increases on the phenologies of lepidopteran species. In the case of Dendrolimus spectabilis, it was found that rise in temperatures led to an increase in generation numbers (Choi et al 2011; Kwon et al 2002). In the case of butterflies, however, the time of flight of adults was not different between the late 1950s and the early 2000s, showing no influence of the rise of temperature (Kwon et al 2008). Although flies are one of the most diverse insect groups, ecological studies on Korean flies are very rare, excluding a few studies of taxonomy or pest species. As many studies on flies related to global warming have recently been
* Corresponding author. Tel.: þ822 961 2662; fax: þ822 961 2679. E-mail address: [email protected] (T.-S. Kwon). Peer review under responsibility of National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA).
published (Andrew et al 2012), it is evident that flies are suitable for investigating the impact of climate change. However, these studies are usually focused on pests or disease vectors. Although a few studies examined the seasonal occurrence of flies in Korea, the studies were usually conducted between March and November (e.g. Gu et al 1965; Jo 1993), and even when parts of the winter season are included in the investigation period, it was reported that almost no flies were collected during that period (Jo and Park 1992). Both the increase of average temperature and the effect of extreme climates are important to investigate the impact of climate change (Sinclair et al 2003). The increase in temperature is different across seasons, and the increase of temperature is much higher in the winter season than in other seasons (Lee et al 2011). Therefore, the increase in temperature may greatly increase winter activities of insects. In temperate regions like Korea, insects usually hibernate as eggs, larva, and pupa, while some species overwinter as adults, which remain almost inactive in winter. However, when the temperature in winter was high, flying flies were observed. Therefore, it is expected that the flight of flies in the winter season is closely related to temperature. There are a few studies on the 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. (Tipulidae) walked on snow in mountains (Lee 2011). The present study was carried out to identify the correlation between winter flight of flies and temperature.
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
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Table 1. Number of flies collected in the Hongneung forest in Seoul from December 6, 2012 to February 29, 2013. Species
Agromyzidae sp. 1 Anthomyiidae sp. 1 Aulacigastridae sp. 1 Calliphoridae sp. 1 Chironomidae sp. 1 Chloropidae sp. 1 Chloropidae sp. 2 Dolichopodidae sp. 1 Drosophilidae sp. 1 Drosophilidae sp. 2 Ephydridae sp. 1 Ephydridae sp. 2 Fanniidae sp. 1 Fanniidae sp. 2 Lauxaniidae sp. 1 Lauxaniidae sp. 2 Lauxaniidae sp. 3 Lonchaeidae sp. 1 Muscidae sp. 1 Muscidae sp. 2 Muscidae sp. 3 Mycetophilidae sp. 1 Mycetophilidae sp. 2 Mycetophilidae sp. 3 Phoridae sp. 1 Phoridae sp. 2 Sciaridae sp. 1 Sphaeroceridae sp. 1 Species richness No. of individuals
2012
2013
Dec
Jan
Study method Feb
2 2
2 1
1 1 1 1 1 1
1
1 4 1 1
1
Total Garden 1
1 1
1 1
4
4
1 1 10
1 2 1
1 1 28 1 3 1 1 1
22 3 1
2
3 1 1 1 4 1
2 13 27
1 3 23 1 3 1 2 3
2 18 54
2 6 2
1 1 17 1 1 1
2 2
1
1
2
1 2
3
11 25
Forest gap
1
2 1 1
3
2
1 4
Study site (sweeping) Sweeping
1
1 1 7 3
Malaise trap
1 1 1 8 1 2 17 52
Materials and methods Survey of flies The fly survey was carried out at the Hongneung Arboretum located at the Korea Forest Research Institute, Seoul, Korea (North 37.593546 , East 127.044618 ). The Hongneung Arboretum was established in Korea in 1922, and is home to over 2000 species of plants, as well as a variety of insects and birds (Kwon et al 2011; Lee et al 2012; Park et al 2014). The forest (w40 ha) in the Hongneung Arboretum is an urban forest within a city space and is currently being used as an experimental forest of the Korea Forest Research Institute. Details on the Hongneung Arboretum are available in the studies of Kwon et al (2011) and Cho et al (2014). The survey of flies 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 into dry specimens later. Fly specimens were identified to family level and morphospecies. Family identification was conducted
1 2
2 17 54
1 2
8 17
2 15 37
2 4 1 1 2 1 1 1 4 1 1 3 45 4 3 2 2 3 1 2 3 1 1 2 10 1 2 2 28 106
using the identification key of Papp and Schumann (2000) and Triplehorn and Johnson (2005). The fly specimens used in this study are stored in the forest biospecimen room of the Korea National Arboretum. Data analysis The temperature data of the survey area used were obtained from the automatic weather station (KWT1000, KL300) installed at the Korea Forest Research Institute, and the precipitation data were obtained from the Seoul meteorological measuring station data (http://www.kma.go.kr/weather/climate/average_south.jsp, connected on March 23, 2015). Environmental factors that affect the number of flies were analyzed using generalized linear
Figure 1. Daily mean temperature and rainfall during the study period in the Hongneung Arboretum in Seoul.
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
TS Kwon et al. / Journal of Asia-Pacific Biodiversity xxx (2015) 1e6
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version 8.0 (Statsoft, Inc., Tulsa, OK, USA) was used for statistical analysis. Results
Figure 2. Occurrence of flies collected by Malaise trap and sweeping. Dark area indicates the monthly mean temperature during the study period.
analysis. For the Malaise trap data, four linear variables (such as temperatureddaily maximum, minimum, and average, and precipitation) and one category variable (month) were used as independent variables. For the analysis of the sweeping data, one linear variable (daily maximum temperature) and one category variable (month) were used as independent variables. Regression analysis was used for determining the relationship between number of flies and temperature. In the case of sweeping data, the maximum temperature of the day of survey was used as the independent variable in the regression analysis, and for the data of the Malaise trap, the weekly average temperature was used as the independent variable. As the number of flies collected was not large, the regression analysis was not conducted at the family level; instead, the number of individuals collected in various temperature ranges was represented in a table. STATISTICA
Data of the temperature and precipitation at the survey site are shown in Table 1. The maximum temperature during the survey period was 11.4 C and the minimum temperature was 18 C, with an average temperature of 3.2 C. The monthly average temperature was lowest in December (4.3 C), and it was 3.6 C in January and 1.3 C in February (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 that collected in the forest gap site. The garden site faces south and is near a building, while the forest gap site faces north and is within the forest and thus having lower temperature; therefore, such a difference is caused by differences in temperature of the survey sites. The number of species per family was 1e3, and the highest was three species in Lauxaniidae, Muscidae, and Mycetophilidae. The most abundant species was Fanniidae sp. 1 (145 individuals), which accounted for about 42% of the total species occurred (Table 1). Tables 2 and 3 show numbers of individuals of families in various temperature zones. When examining those collected in the Malaise trap, 20 of all the individuals (38%) were collected when the weekly average temperature was under 0 C. In particular, one Lauxanidae was collected when the weekly average temperature was 5.2 C. By contrast, in the case of sweeping, only three flies were collected when the maximum temperature of the survey date was under 0 C, accounting for only 6% of the total. There was a very close relationship 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) 6e5
Agromyzidae Anthomyiidae Aulacigastridae Calliphoridae Dolichopodidae Drosophilidae Fanniidae Lauxaniidae Muscidae Mycetophilidae Phoridae Sciaridae Total
5e4
Total 4e3
3e2
2e1
1e0
0e1
1e2
2e3
1 2
2 1
1 1 1 7
7
11
2
1 3 3
1 2 2 1
0
0
2
2 2 17
0
11
0
21
1 4 1 1 1 1 25 1 3 3 9 2 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
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Table 3. Number of flies collected by sweeping in various temperature zones. Family
Temperature range ( C) 9e8
Agromyzidae Chironomidae Chloropidae Drosophilidae Ephydridae Fanniidae Lauxaniidae Lonchaeidae Muscidae Mycetophilidae Phoridae Sphaeroceridae Total
8e3
Total 3e2
2e1
1e1
1e2
2e3
3e4
1 1
1
4e5
5e11
11e12 1
1
1
1 1
1
2 2 1 1
1 1 1 6 2
3 2 11 2 1
1 1
1 2 2 4 4 24 6 3 3 1 2 2 54
2
1
1
0
1
1
0
individuals (Figure 3), so the number of species could be explained by the number of individuals with an accuracy exceeding 90%. Such a high correlation is most likely due to the fact that there were not many individuals per species (Table 1). In the generalized linear analysis, the weekly average and minimum temperatures had a significant impact in the case of the Malaise trap, whereas the maximum temperature on the day of survey had a significant impact in the case of sweeping (Table 4). However, precipitation
3
8
2 2 23
3
0
14
and month did not have a significant impact on the number of individuals in both survey methods. The regression models using temperature as an independent variable were shown to be significant in cases of both Malaise trap and sweeping, and the explanatory power of the model was w38e43% (Figures 4 and 5). Thus, the observations and models indicate that the number of species and individuals increased with temperature. 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 individuals and species of flies 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 fly in winter. In the Malaise trap, because it was set up continuously for 1 week, 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 3.2 C) 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
Figure 3. Relationship between species richness (number of species) and abundance (number of individuals) of flies collected by Malaise trap and sweeping.
Malaise trap Mean temperature ( C) Maximum temperature ( C) Minimum temperature ( C) Precipitation Month Sweeping Maximum temperature ( C) Month
d.f.
Sum of squares
Mean squares
F
p
1 1 1 1 2
209.8 6.7 136.4 4.4 62.3
209.8 6.7 136.4 4.4 31.2
10.21 0.33 6.64 0.21 1.52
0.019 0.589 0.042 0.659 0.293
1 2
151.6 13.3
151.6 6.6
6.115 0.268
0.035 0.771
d.f. ¼ degrees of freedom.
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
TS Kwon et al. / Journal of Asia-Pacific Biodiversity xxx (2015) 1e6
Figure 4. Characteristics of flies collected by Malaise trap: A, species richness (number of species) versus weekly mean temperature; and B, abundance (number of individuals) versus weekly mean temperature. The line in the figure indicates the expected values from the regression model.
fly lifecycle, of which only one spends the winter as imago. This is the lifecycle of Tephritis bardanae (Tephritidae), in which flies are in the eggs, larva, and pupa states from July to September, and then spend their time as imago from September to June of the following year. However, when considering the results of the present study and that of Hövemeyer (2000) that species under a number of families spend the winter as imago, it is very likely that there are flies with various lifecycles that spend the winter as imago are existent. The largest number of flies was collected in Poland in early December (Soszynska 2004), but in the present study, the fewest number of flies was collected in December and the most in February when the temperature was highest. In Germany, which shares borders with Poland, the number of flies was highest in December as well (reference in Soszynska 2004). In Poland, flies that are active on top of snow were investigated, so the surrounding environmental conditions were important; in addition, activities of flies had higher relations with humidity than with temperature (Soszynska 2004). Activities of imagoes usually include mating, spawning, eating, and defending their territory, but it seems unlikely that imagoes perform such activities in winter. However, if imagoes fly in relatively higher temperatures in the winter season
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Figure 5. Characteristics of flies collected by sweeping: A, species richness (number of species) versus daily maximum temperature; and B, abundance (number of individuals) versus daily maximum temperature. The line in the figure indicates the expected values from the regression model.
without any purpose, this would reduce their fitness (paradox of fly winter flight). Since flying without any purpose may lead to unnecessary consumption of energy and there is a possibility of freezing due to sudden temperature drops, it would be more advantageous to hibernate as imago in the soil or among leaves than aimlessly flying in winter. However, if they are flying for reproduction activities in winter, the flight in cold times may consume low energy and experience low chance with natural enemies (Aitchison 2001; Durska 2003). It is also expected that the competition for oviposition place is low in winter. These benefits may increase fitness of flies that fly in winter. Hence, more research is needed on this issue. While there is little difference in tolerance of high temperature among insects, there is a great difference in tolerance of low temperatures (Addo-Bediako et al 2000). Therefore, this is an important factor in determining the distribution range of insects (Kwon et al 2014b). If winter cold decreases in temperate areas such as Korea due to global warming, southern insects will increase in distribution, and the insect fauna would be expected to become richer and more diverse (Deutch et al 2008). However, according to the prediction on the change of distribution of ants, spiders, and beetles, based on the recent national survey data, there are more northern species than southern species in the
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
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Korean peninsula; the habitable range of most species will decrease as temperature rises, but the inflow of southern species will be inhibited due to the separation by southern sea, resulting in a decrease of the overall diversity (Kwon and Lee 2015). Especially in the case of flies, the abundance (number of individuals) is expected to decrease for most families (living in the forest ground) projected. This is due to the fact that more species of most families are northern species of which the main distributional range is located further north than the Korean peninsula. Such prediction is against our intuition (general expectation of more flies in warmer climate). Studies on the change of phenology associated with climate change, with analysis of the change of first occurrence in the early spring season, were most common, followed by studies on autumn phenology or hibernation, and on the change of generation number or number of individuals within activity season between spring and autumn (Walther et al 2002); however, studies on the increase of activities in the winter season are rare. However, survival or activities in the winter season are very important for the survival of individuals. Especially in Korea, where harsh winter climate conditions have decisive impact on the survival of insects, the importance of such research increases. Pseudozizeeria maha could not overwinter in the central region of Korea; however, this phenomenon has become feasible recently, and thus, the number of individuals is on the rise (Kwon et al 2014a). In the case of Lycorma delicatula that has recently migrated from China to Korea causing heavy damages to orchards nationwide, it has been reported that the winter season temperature plays a decisive role for its survival (Lee et al 2011). From the analysis of the distribution of ants in Korea, it is proposed that the winter season temperature also plays a decisive role in the distribution of species (Kwon et al 2014b). In Korea, the increase of winter season temperature is more than that in other seasons (Kwon 2003), so the impact of such rapid climate change in winter on insects requires more in-depth research on diverse taxonomical groups as well as flies (e.g. physiological reaction and tolerance against low temperature, phenology change, behavioral ecological study in low temperatures, interspecific interaction, etc.). Acknowledgments We appreciate Dr Myeong-Soo Won and Mr Yoo-Seung Kim for providing meteorological data. This study was carried out as a part of a research project of the Korea Forest Research Institute (Effect of Climate Change on Forest Ecosystem and Adaptation of Forest Ecosystem; project number FE 0100-2009-01). References Addo-Bediako AA, Chown SL, Gaston KJ. 2000. Thermal tolerance, climatic variability and latitude. Proceedings of the Royal Society of London. Series B: Biological Sciences 267:739e745. Aitchison CW. 2001. The effect of snow cover on small animals. In: Jones HG, Pmeroy JW, Walker DA, Hohem RW, editors. Snow ecology. Cambridge University Press. pp. 229e265. Andrew NR, Hill SJ, Binns M, et al. 2012. Assessing insect responses to climate change: what are we testing for? Where should we be heading? PeerJ; 2012. http://dx.doi.org/10.7717/peerj.11. I:e11.
Cho JH, Park CY, Kim SG. 2014. Story telling of the Hongneung forest. Forest Short Report 11e02. GeoBuk, Seoul: Korea Forest Research Institute. [In Korean]. Choi WI, Park Y-K, Park Y-S, et al. 2011. Changes in voltinism in a pine moth Dendrolimus spectabilis (Lepidoptera: Lasiocampidae) population: implications of climate change. Applied Entomology and Zoology 46:319e325. Chon TS, Kwon TS. 1985. Construction of a temperature-dependent simulation model to predict population growth of the German cockroach, Blattella germanica. The Korean Journal of Ecology 8:179e196. Deutch CA, Tewsbury JJ, Huey RB, et al. 2008. Impacts of climate warming on terrestrial ectotherms across latitude. Proceeding of the National Academy of Science of the United States 105:6668e6672. Durska E. 2003. The phenology of Triphlera Rondani species (Diptera: Phoridae) in moist pine forests in the Bialowe z Forest. Entomologica Fennica 14:177e182. Gu SH, Shim DB, Ahn HH. 1965. Seasonal change of the fly fauna in Seoul city. Journal of Public Health 2:53e57. Hövemeyer K. 2000. Ecology of Diptera. In: Papp L, Darvas B, editors. Contributions to a manual of Palaearctic Diptera, Vol. 1. Budapest: Science Herald. pp. 437e490. IPCC. 2007. Climate change 2007: the physical science basis. Contribution of Working Group I to the fourth assessment report of the International Panel on Climate Change. United Kingdom and New York, NY, USA: Cambridge University Press. p. 999. Jo TH. 1993. On the flies collected from Mts. Gumo, Palgong and Kaya, Korea and their seasonal prevalences. Journal of Science Education 19:87e147. Jo TH, Park SH. 1992. On the flies collected in the Choseokpark, Chinju city and their seasonal prevalence. Journal of Science Education 18:5e19. Kwon TS, Byun BK, Kang SH, et al. 2008. Analysis on changes, and problems in phenology of butterflies in Gwangneung forest. Korean Journal of Applied Entomology 47:209e216. Kwon TS, Kim SS, Lee CM. 2014a. Local change of butterfly species in response to global warming and reforestation in Korea. Zoological Studies 52:47e54. Kwon TS, Kim SS, Chun JH. 2014b. Pattern of ant diversity in Korea: an empirical test of Rapoport’s altitudinal rule. Journal of Asia-Pacific Entomology 17:161e167. Kwon TS, Lee CM. 2015. Prediction of abundance of ants according to climate change scenario RCP 4.5 and 8.5 in South Korea. Journal of Asia-Pacific Biodiversity 8:49e65. Kwon TS, Lee CM, Chun JH, et al. 2011. Ants in the Hongneung forest. Research Note 412. Seoul: Korea Forest Research Institute [In Korean]. Kwon TS, Park YK, Oh KS, et al. 2002. Increase in the number of generations in Dendrolimus spectabilis (Butler) (Lepidoptera: Lasiocampidae) in Korea. Journal of Korean Forest Society 91:149e155. Kwon WT. 2003. Changes of Korean climate of last 100 years and future prospects. Korean Meteorology Administration Newsletter 2:1e8. Lee CM, Kwon TS, Kim SS, et al. 2012. Butterflies in the Hongneung forest. Research Note 453. Seoul: Korea Forest Research Institute [In Korean]. Lee JH. 2011. Insect walking over snow, spider tipuloid fly (Chionea). Nature and Ecology; 2011:8e23. Lee JS, Kim IK, Koh SH, et al. 2011. Impact of minimum winter temperature on Lycorma delicatula (Hemiptera: Fulgoridae) egg mortality. Journal of Asia-Pacific Entomology 14:123e125. Papp L, Schumann H. 2000. Key to familiesdadults. In: , Papp L, Darvas B, editors. Contributions to a manual of Palaearctic Diptera, Vol. 1. Budapest: Science Herald. pp. 163e200. Park CY, Choi GH, Gang WM, et al. 2014. Birds stay in the Hongneung forest. Research Note 570. Seoul: Korea Forest Research Institute [In Korean]. Park YS, Kwon TS, Kim JK, et al. 2003. Effect of temperatures on the development of the stick insect, Baculum elongatus (Phasmida: Phasmidae) and the life cycle. Journal of Korean Forest Society 92:62e70. Reisen WK, Thiemann T, Barker CM, et al. 2010. Effects of warm winter temperature on the abundance and gonotropic activity of Culex (Diptera: Culicidae) in California. Journal of Medical Entomology 47:230e237. Sinclair BJ, Vernon P, Klok CJ, et al. 2003. Insects at low temperature: an ecological perspective. Trends in Ecology and Evolution 18:257e262. Soszynska A. 2004. The influence of environmental factors on the supranivean activity of flies (Diptera) in Central Poland. European Journal of Entomology 191: 481e489. Triplehorn CA, Johnson NF. 2005. Borror and Delong’s introduction to the study of insects. 7th ed. Belmont: Brooks/Cole. Uvarov BP. 1931. Insects and climate. Transactions of the Entomological Society of London 79:1e232. Walther GR, Post E, Convey P, et al. 2002. Ecological responses to recent climate change. Nature 416:389e395.
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
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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 Division of Forest Ecology, Korea Forest Research Institute, Seoul, South Korea c Korea Diptera Laboratory, Seoul, South Korea b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 30 June 2015 Received in revised form 12 October 2015 Accepted 13 October 2015 Available online xxx
Winter phenology (diapause and activity) of insects is expected to change more significantly than that of other seasons, because temperature will increase more in winter than in other seasons in temperate regions. However, studies on winter phenology of insects are rare. It is expected that winter flights of flies (Diptera) will increase as climate warms. This study aims to find the relationship between flight of flies and temperature. The survey on flies and weather (temperature and rainfall) was carried out in the 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 families were collected. Richness and abundance of flies were positively correlated with temperature. 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/).
Keywords: Diptera phenology temperature winter flight
Introduction Due to the use of fossil fuels and destruction of forests, the average global temperature rose by w0.75 C over the past 100 years (IPCC 2007), and the temperature of Korea rose by w1.5 C (Kwon 2003). Such changes in temperature also change the phenology of organisms (Walther et al 2002). In the case of insects, whose body temperature is mainly determined by the air temperature, change of temperature has a huge impact on insect phenology (Chon and Kwon 1985; Park et al 2003; Uvarov 1931). In South Korea, two studies showed different results regarding the influences of temperature increases on the phenologies of lepidopteran species. In the case of Dendrolimus spectabilis, it was found that rise in temperatures led to an increase in generation numbers (Choi et al 2011; Kwon et al 2002). In the case of butterflies, however, the time of flight of adults was not different between the late 1950s and the early 2000s, showing no influence of the rise of temperature (Kwon et al 2008). Although flies are one of the most diverse insect groups, ecological studies on Korean flies are very rare, excluding a few studies of taxonomy or pest species. As many studies on flies related to global warming have recently been
* Corresponding author. Tel.: þ822 961 2662; fax: þ822 961 2679. E-mail address: [email protected] (T.-S. Kwon). Peer review under responsibility of National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA).
published (Andrew et al 2012), it is evident that flies are suitable for investigating the impact of climate change. However, these studies are usually focused on pests or disease vectors. Although a few studies examined the seasonal occurrence of flies in Korea, the studies were usually conducted between March and November (e.g. Gu et al 1965; Jo 1993), and even when parts of the winter season are included in the investigation period, it was reported that almost no flies were collected during that period (Jo and Park 1992). Both the increase of average temperature and the effect of extreme climates are important to investigate the impact of climate change (Sinclair et al 2003). The increase in temperature is different across seasons, and the increase of temperature is much higher in the winter season than in other seasons (Lee et al 2011). Therefore, the increase in temperature may greatly increase winter activities of insects. In temperate regions like Korea, insects usually hibernate as eggs, larva, and pupa, while some species overwinter as adults, which remain almost inactive in winter. However, when the temperature in winter was high, flying flies were observed. Therefore, it is expected that the flight of flies in the winter season is closely related to temperature. There are a few studies on the 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. (Tipulidae) walked on snow in mountains (Lee 2011). The present study was carried out to identify the correlation between winter flight of flies and temperature.
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
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Table 1. Number of flies collected in the Hongneung forest in Seoul from December 6, 2012 to February 29, 2013. Species
Agromyzidae sp. 1 Anthomyiidae sp. 1 Aulacigastridae sp. 1 Calliphoridae sp. 1 Chironomidae sp. 1 Chloropidae sp. 1 Chloropidae sp. 2 Dolichopodidae sp. 1 Drosophilidae sp. 1 Drosophilidae sp. 2 Ephydridae sp. 1 Ephydridae sp. 2 Fanniidae sp. 1 Fanniidae sp. 2 Lauxaniidae sp. 1 Lauxaniidae sp. 2 Lauxaniidae sp. 3 Lonchaeidae sp. 1 Muscidae sp. 1 Muscidae sp. 2 Muscidae sp. 3 Mycetophilidae sp. 1 Mycetophilidae sp. 2 Mycetophilidae sp. 3 Phoridae sp. 1 Phoridae sp. 2 Sciaridae sp. 1 Sphaeroceridae sp. 1 Species richness No. of individuals
2012
2013
Dec
Jan
Study method Feb
2 2
2 1
1 1 1 1 1 1
1
1 4 1 1
1
Total Garden 1
1 1
1 1
4
4
1 1 10
1 2 1
1 1 28 1 3 1 1 1
22 3 1
2
3 1 1 1 4 1
2 13 27
1 3 23 1 3 1 2 3
2 18 54
2 6 2
1 1 17 1 1 1
2 2
1
1
2
1 2
3
11 25
Forest gap
1
2 1 1
3
2
1 4
Study site (sweeping) Sweeping
1
1 1 7 3
Malaise trap
1 1 1 8 1 2 17 52
Materials and methods Survey of flies The fly survey was carried out at the Hongneung Arboretum located at the Korea Forest Research Institute, Seoul, Korea (North 37.593546 , East 127.044618 ). The Hongneung Arboretum was established in Korea in 1922, and is home to over 2000 species of plants, as well as a variety of insects and birds (Kwon et al 2011; Lee et al 2012; Park et al 2014). The forest (w40 ha) in the Hongneung Arboretum is an urban forest within a city space and is currently being used as an experimental forest of the Korea Forest Research Institute. Details on the Hongneung Arboretum are available in the studies of Kwon et al (2011) and Cho et al (2014). The survey of flies 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 into dry specimens later. Fly specimens were identified to family level and morphospecies. Family identification was conducted
1 2
2 17 54
1 2
8 17
2 15 37
2 4 1 1 2 1 1 1 4 1 1 3 45 4 3 2 2 3 1 2 3 1 1 2 10 1 2 2 28 106
using the identification key of Papp and Schumann (2000) and Triplehorn and Johnson (2005). The fly specimens used in this study are stored in the forest biospecimen room of the Korea National Arboretum. Data analysis The temperature data of the survey area used were obtained from the automatic weather station (KWT1000, KL300) installed at the Korea Forest Research Institute, and the precipitation data were obtained from the Seoul meteorological measuring station data (http://www.kma.go.kr/weather/climate/average_south.jsp, connected on March 23, 2015). Environmental factors that affect the number of flies were analyzed using generalized linear
Figure 1. Daily mean temperature and rainfall during the study period in the Hongneung Arboretum in Seoul.
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
TS Kwon et al. / Journal of Asia-Pacific Biodiversity xxx (2015) 1e6
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version 8.0 (Statsoft, Inc., Tulsa, OK, USA) was used for statistical analysis. Results
Figure 2. Occurrence of flies collected by Malaise trap and sweeping. Dark area indicates the monthly mean temperature during the study period.
analysis. For the Malaise trap data, four linear variables (such as temperatureddaily maximum, minimum, and average, and precipitation) and one category variable (month) were used as independent variables. For the analysis of the sweeping data, one linear variable (daily maximum temperature) and one category variable (month) were used as independent variables. Regression analysis was used for determining the relationship between number of flies and temperature. In the case of sweeping data, the maximum temperature of the day of survey was used as the independent variable in the regression analysis, and for the data of the Malaise trap, the weekly average temperature was used as the independent variable. As the number of flies collected was not large, the regression analysis was not conducted at the family level; instead, the number of individuals collected in various temperature ranges was represented in a table. STATISTICA
Data of the temperature and precipitation at the survey site are shown in Table 1. The maximum temperature during the survey period was 11.4 C and the minimum temperature was 18 C, with an average temperature of 3.2 C. The monthly average temperature was lowest in December (4.3 C), and it was 3.6 C in January and 1.3 C in February (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 that collected in the forest gap site. The garden site faces south and is near a building, while the forest gap site faces north and is within the forest and thus having lower temperature; therefore, such a difference is caused by differences in temperature of the survey sites. The number of species per family was 1e3, and the highest was three species in Lauxaniidae, Muscidae, and Mycetophilidae. The most abundant species was Fanniidae sp. 1 (145 individuals), which accounted for about 42% of the total species occurred (Table 1). Tables 2 and 3 show numbers of individuals of families in various temperature zones. When examining those collected in the Malaise trap, 20 of all the individuals (38%) were collected when the weekly average temperature was under 0 C. In particular, one Lauxanidae was collected when the weekly average temperature was 5.2 C. By contrast, in the case of sweeping, only three flies were collected when the maximum temperature of the survey date was under 0 C, accounting for only 6% of the total. There was a very close relationship 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) 6e5
Agromyzidae Anthomyiidae Aulacigastridae Calliphoridae Dolichopodidae Drosophilidae Fanniidae Lauxaniidae Muscidae Mycetophilidae Phoridae Sciaridae Total
5e4
Total 4e3
3e2
2e1
1e0
0e1
1e2
2e3
1 2
2 1
1 1 1 7
7
11
2
1 3 3
1 2 2 1
0
0
2
2 2 17
0
11
0
21
1 4 1 1 1 1 25 1 3 3 9 2 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
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Table 3. Number of flies collected by sweeping in various temperature zones. Family
Temperature range ( C) 9e8
Agromyzidae Chironomidae Chloropidae Drosophilidae Ephydridae Fanniidae Lauxaniidae Lonchaeidae Muscidae Mycetophilidae Phoridae Sphaeroceridae Total
8e3
Total 3e2
2e1
1e1
1e2
2e3
3e4
1 1
1
4e5
5e11
11e12 1
1
1
1 1
1
2 2 1 1
1 1 1 6 2
3 2 11 2 1
1 1
1 2 2 4 4 24 6 3 3 1 2 2 54
2
1
1
0
1
1
0
individuals (Figure 3), so the number of species could be explained by the number of individuals with an accuracy exceeding 90%. Such a high correlation is most likely due to the fact that there were not many individuals per species (Table 1). In the generalized linear analysis, the weekly average and minimum temperatures had a significant impact in the case of the Malaise trap, whereas the maximum temperature on the day of survey had a significant impact in the case of sweeping (Table 4). However, precipitation
3
8
2 2 23
3
0
14
and month did not have a significant impact on the number of individuals in both survey methods. The regression models using temperature as an independent variable were shown to be significant in cases of both Malaise trap and sweeping, and the explanatory power of the model was w38e43% (Figures 4 and 5). Thus, the observations and models indicate that the number of species and individuals increased with temperature. 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 individuals and species of flies 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 fly in winter. In the Malaise trap, because it was set up continuously for 1 week, 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 3.2 C) 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
Figure 3. Relationship between species richness (number of species) and abundance (number of individuals) of flies collected by Malaise trap and sweeping.
Malaise trap Mean temperature ( C) Maximum temperature ( C) Minimum temperature ( C) Precipitation Month Sweeping Maximum temperature ( C) Month
d.f.
Sum of squares
Mean squares
F
p
1 1 1 1 2
209.8 6.7 136.4 4.4 62.3
209.8 6.7 136.4 4.4 31.2
10.21 0.33 6.64 0.21 1.52
0.019 0.589 0.042 0.659 0.293
1 2
151.6 13.3
151.6 6.6
6.115 0.268
0.035 0.771
d.f. ¼ degrees of freedom.
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
TS Kwon et al. / Journal of Asia-Pacific Biodiversity xxx (2015) 1e6
Figure 4. Characteristics of flies collected by Malaise trap: A, species richness (number of species) versus weekly mean temperature; and B, abundance (number of individuals) versus weekly mean temperature. The line in the figure indicates the expected values from the regression model.
fly lifecycle, of which only one spends the winter as imago. This is the lifecycle of Tephritis bardanae (Tephritidae), in which flies are in the eggs, larva, and pupa states from July to September, and then spend their time as imago from September to June of the following year. However, when considering the results of the present study and that of Hövemeyer (2000) that species under a number of families spend the winter as imago, it is very likely that there are flies with various lifecycles that spend the winter as imago are existent. The largest number of flies was collected in Poland in early December (Soszynska 2004), but in the present study, the fewest number of flies was collected in December and the most in February when the temperature was highest. In Germany, which shares borders with Poland, the number of flies was highest in December as well (reference in Soszynska 2004). In Poland, flies that are active on top of snow were investigated, so the surrounding environmental conditions were important; in addition, activities of flies had higher relations with humidity than with temperature (Soszynska 2004). Activities of imagoes usually include mating, spawning, eating, and defending their territory, but it seems unlikely that imagoes perform such activities in winter. However, if imagoes fly in relatively higher temperatures in the winter season
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Figure 5. Characteristics of flies collected by sweeping: A, species richness (number of species) versus daily maximum temperature; and B, abundance (number of individuals) versus daily maximum temperature. The line in the figure indicates the expected values from the regression model.
without any purpose, this would reduce their fitness (paradox of fly winter flight). Since flying without any purpose may lead to unnecessary consumption of energy and there is a possibility of freezing due to sudden temperature drops, it would be more advantageous to hibernate as imago in the soil or among leaves than aimlessly flying in winter. However, if they are flying for reproduction activities in winter, the flight in cold times may consume low energy and experience low chance with natural enemies (Aitchison 2001; Durska 2003). It is also expected that the competition for oviposition place is low in winter. These benefits may increase fitness of flies that fly in winter. Hence, more research is needed on this issue. While there is little difference in tolerance of high temperature among insects, there is a great difference in tolerance of low temperatures (Addo-Bediako et al 2000). Therefore, this is an important factor in determining the distribution range of insects (Kwon et al 2014b). If winter cold decreases in temperate areas such as Korea due to global warming, southern insects will increase in distribution, and the insect fauna would be expected to become richer and more diverse (Deutch et al 2008). However, according to the prediction on the change of distribution of ants, spiders, and beetles, based on the recent national survey data, there are more northern species than southern species in the
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Korean peninsula; the habitable range of most species will decrease as temperature rises, but the inflow of southern species will be inhibited due to the separation by southern sea, resulting in a decrease of the overall diversity (Kwon and Lee 2015). Especially in the case of flies, the abundance (number of individuals) is expected to decrease for most families (living in the forest ground) projected. This is due to the fact that more species of most families are northern species of which the main distributional range is located further north than the Korean peninsula. Such prediction is against our intuition (general expectation of more flies in warmer climate). Studies on the change of phenology associated with climate change, with analysis of the change of first occurrence in the early spring season, were most common, followed by studies on autumn phenology or hibernation, and on the change of generation number or number of individuals within activity season between spring and autumn (Walther et al 2002); however, studies on the increase of activities in the winter season are rare. However, survival or activities in the winter season are very important for the survival of individuals. Especially in Korea, where harsh winter climate conditions have decisive impact on the survival of insects, the importance of such research increases. Pseudozizeeria maha could not overwinter in the central region of Korea; however, this phenomenon has become feasible recently, and thus, the number of individuals is on the rise (Kwon et al 2014a). In the case of Lycorma delicatula that has recently migrated from China to Korea causing heavy damages to orchards nationwide, it has been reported that the winter season temperature plays a decisive role for its survival (Lee et al 2011). From the analysis of the distribution of ants in Korea, it is proposed that the winter season temperature also plays a decisive role in the distribution of species (Kwon et al 2014b). In Korea, the increase of winter season temperature is more than that in other seasons (Kwon 2003), so the impact of such rapid climate change in winter on insects requires more in-depth research on diverse taxonomical groups as well as flies (e.g. physiological reaction and tolerance against low temperature, phenology change, behavioral ecological study in low temperatures, interspecific interaction, etc.). Acknowledgments We appreciate Dr Myeong-Soo Won and Mr Yoo-Seung Kim for providing meteorological data. This study was carried out as a part of a research project of the Korea Forest Research Institute (Effect of Climate Change on Forest Ecosystem and Adaptation of Forest Ecosystem; project number FE 0100-2009-01). References Addo-Bediako AA, Chown SL, Gaston KJ. 2000. Thermal tolerance, climatic variability and latitude. Proceedings of the Royal Society of London. Series B: Biological Sciences 267:739e745. Aitchison CW. 2001. The effect of snow cover on small animals. In: Jones HG, Pmeroy JW, Walker DA, Hohem RW, editors. Snow ecology. Cambridge University Press. pp. 229e265. Andrew NR, Hill SJ, Binns M, et al. 2012. Assessing insect responses to climate change: what are we testing for? Where should we be heading? PeerJ; 2012. http://dx.doi.org/10.7717/peerj.11. I:e11.
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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