Occurrence and Population Dynamics of Chironomids in the Early Rice Field

1,2 1 2 2 2 LI Zhi-Yu , YANG Hong , LAI Feng-Xiang , FU Qiang , HU Yang (1Institute of Entomology, Guizhou University/The Provincial Key Laboratory for Agricultural Pest Management of Mountainous Region, Guiyang 550025; 2China National Rice Research Institute, Hangzhou 310006)

Abstract: The Chironomid is one of world wide distribution insects and normally occurs in a great abundance among many kinds of water bodies. In rice field, Chironomids are very abundant. Currently, our knowledge about Chironomid in rice field is limited on the species survey. The rice field living Chironomids is considered as a group insect at the family level, e.g., termed as a kind of the neutral insects. By using the special designed emergence traps, the species richness and occurrence of Chironomids in rice field were studied throughout the early rice season in Fuyang, Zhejiang province, China. There were four species, namely, Tanytarsus formosanus, Chironomus sinicus, Polypedilum nubifer and Tanypus punctipennis of Chironomids collected from rice fields. All of them are widely distributed species. T. formosanus and C. sinicus were the most dominant species in rice field. The succession of Chironomids in the early rice season could be divided into two phases, namely the early and late phases. The abundance of Chironomid was higher in the early phase than that in the late phase. It was estimated that there were around 3 million individuals of Chironomids emerged from the 667 m2 rice field throughout the early rice season. It was also found that the sex ratio of T. formosanus was female biased during the early phase, whereas male biased during the late phase. In contrast, the sex ratio of C. sinicus was male biased throughout the entire field season. Key words: rice field; Chironomids; dynamic; sex ratio

Chironomids, also called the non-biting midges, ecosystem, as well as in the paddy ecosystem. are worldwide distributed Diptera species. There are The ecological roles of chironomids living in the more than 5 000 species of Chironomids identified paddy ecosystem are not only about substances and occurred in almost all types of aquatic ecosystems. releasing and absorbing, but also the yield loss of rice The abundance of Chironomids is extensively high. In and the pest management. Some species of many aquatic ecosystems, the Chironomids consist Chironomid larvae can consume the endosperm and 50% or more of the total macroinvertebrate abundance even completely destroy the embryo of rice seeds, and the biomass could account for 70%–80% of the attack the developing root systems of aerially sown amount of aquatic invertebrates (Armitage et al, 1995; rice, eat the newly sown seeds, which lead the vigor of Zhang and Jin, 1995). Most kinds of Chironomid rice seedlings largely reduced and the seedlings liable larvae can directly use the organic particles. They are to wind damage (Plant Protection Institute, Hubei able to consume the great amount of organic mass, Academy of Agricultural Sciences, 1978). For thus effectively purifying the water quality especially example, Cricotopus and Chironomus larvae damaged for the eutrophic waterbodies. In addition, the root of rice plants resulting in poor crop Chironomid larvae can promote the sediments to establishment were reported in Italy and Australia release nitrogen and phosphorus elements (Chen and respectively (Ferrarses, 1992; Steven et al, 2006). Liu, 1995). These released nitrogen and phosphorus Chironomids affected the rice production. In some elements can be directly absorbed by plants, thus areas of China, Polypedilum nubifer larvae also feed Chironomids also play an important role for on the rice roots leading a heavy economic loss (Wang, mineralization process in the water body. Therefore, 2000). the Chironomids play a vital role in the aquatic At present, researches about Chironomids in China focus on taxonomy and distribution areas Received: 8 November 2010; Accepted: 18 January 2011 survey (Wang, 1998) and about its role as the neutral Corresponding author: HU Yang ([email protected] ) Rice Science, Vol. 18, No. 2, 2011 insects (Wu et al, 1994; Guo et al, 1995; Hu et al, variety was planted into a single experimental field. 1998; Xu and Wu, 1999; Liu and Gu, 2002; Zheng et The acreage of a single experimental field was al, 2006). The term of the neutral insect refers to the 16.7 m×80 m. Each field was divided into six plots insects neither the natural enemy nor the pest in rice (13.3 m×16.7 m for each plot) and one emergence trap ecosystem. The term emphasizes the role of a given was randomly placed within each plot. Thus, there arthropod related to the rice product directly. All of were six replications for each variety. No insecticide those studies reported that there were plenty of was used during the trial. Chironomids occurred in paddy fields, especially in Sampling method the early rice season. The number of Chironomids consists of more than half of arthropod in rice fields The special designed traps, called the emergence (Hu et al, 1998; Liu and Gu, 2002). Since trap made of stainless steel pipe (2 cm in diameter) Chironomids can be the prey of the predatory natural and covered with the black mesh, were used to collect enemies, the growth of predatory natural enemies can the newly emerged Chironomid adults. Each trap be largely promoted (Xu and Wu, 1999). covered 0.5 m×0.5 m area. The height of the Consequently, pests in paddy ecosystem can be greatly emergence trap was 1.5 m, and the upper section (80 controlled by thus promoted predators, especially cm from soil surface) of trap was narrowed gradually during the late rice season (Zheng et al, 2006). with a 2.5 cm diameter opening, which allows adults Nevertheless, these researches regarded all to pass through. A specially designed collecting Chironomids as one species group. To the best of our receiver was placed above the opening to keep adults knowledge, there is no study in China about the past the opening of the emergence trap. The Chironomids in paddy field conducted systemically. collecting receiver with adults collected was replaced The basic information such as how many species with an empty receiver. The traps were relocated Chironomids occurred as well as their dynamic pattern randomly after each collection event. in the paddy field remains unknown. The first collection was took place at the 9th day Our goals were aimed to investigate species after transplanting. There were 14 collections and the richness, abundance and population dynamics of intervals of collections were varied at 2, 4, or 6 days Chironomids in the paddy field of China National according to the adults collected. For example, if there Rice Research Institute (CNRRI). We also aimed to were a large number of Chironomid adults collected, investigate the dynamic patterns of major Chironomid the interval between two collections was two days species occurred in our examined fields. Such basic only. If there were a small number of Chironomid information of Chironomids would be useful for the adults collected, the interval was 6 days. The last further research. harvesting of the adults was taken on July 12. The receiver of each trap was replaced in field. MATERIALS AND METHODS The replaced receivers were brought back to the laboratory. In laboratory, the collected adults were put Trial site, rice variety, plot arrangement into 75% alcohol for preservation and examined under a microscope to identify the species and count the Trial site was at the China National Rice number of each species. Research Institute (CNRRI) experimental station in Fuyang, Zhejiang province, China, where is a typical Analytical method rice area in Yangzi Delta, also well known as the The species name and number of each species Hangjiahu Plain rice area. were input to EXCEL. The DPS software (Tang and Two early rice varieties, Zhongzao 22 and Jinzao Feng, 2007) was used for the statistic analysis. 47, were planted for our experiments. Both varieties were sown on April 1, 2009 and transplanted on May 4. Both rice fields were harvested on July 21. Each LI Zhi-Yu, et al. Occurrence and Population Dynamics of Chironomids in the Early Rice Field

RESULTS

Species richness and dominance

Four species of Chironomids collected belong to four genera and two subfamilies: Tanytarsus formosanus, Chironomus sinicus and Polypedilum nubifer belong to the subfamily Chironominae; Tanypus punctipennis fall under the subfamily Tanypodinae. In total, there were 7 801 adults collected from Zhongzao 22 field and 6 293 adults from Jinzao 47 field over the field trail. Among four species, the most Fig. 1. Occurrence and succession of Chironomids community in dominant species was T. formosanus in both fields. the early rice season in Fuyang, Zhejiang province, China 2009. The actual dominant indices were 0.6623 in Zhongzao 22 field and 0.6404 in Jinzao 47 field, respectively. 30 till the harvest, the occurrence of Chironomids was The second most dominant species was C. sinicus, relatively lower than in the early phase. Also, with dominant indices of 0.2227 in Zhongzao 22 field Chironomids fluctuated at the low level. For instance, and 0.2482 in Jinzao 47 field, respectively (Table 1). from May 30 to June 4, there were only about 2 Succession of Chironomids in the early rice field individual/(d·trap) collected in both fields. Moreover, there was no significant difference (P=0.2534) As Fig. 1 shown, the succession of Chironomids detected on the amount of Chironomids collected from in the early rice field could be divided into the early two fields over the whole season. and the late phases. The period was about one month for the early phase, one and a half month for the late Population dynamics of dominant Chironomid phase. The abundance of Chironomids was much species higher in the early phase than in the late phase. From Dynamic patterns of T. formosanus, the most May 4 (transplanting date) to May 30, the collected dominant species, were similar to each other in both Chironomids adults were 60–80 individual/(d·trap) rice fields (Fig, 2-A). Similar to the succession of and fluctuated at this level throughout the early phase. Chironomids community, the dynamic pattern of T. For instance, from May 20 to May 22 in Zhongzao 22 formosanus also could be divided into the early and field, the collected Chironomids adults were 92 the late phases, with the same time periods as the individual/(d·trap). In addition, collected adults were Chironmids community. The early phase was also 80 individual/(d·trap) in Jinzao 47 field. After May from May 4 (transplanting date) to May 30. During 25, the amount of collected Chironomids fell down this phase, the population density of T. formosanus quickly. Then, the succession of Chironomids entered raised about 3 fold higher than the initial dates in into the late phase. During the late phase, from May

Table 1. Species, quantity and dominance of chironomids collected in early rice fields Fuyang, China 2009. Paddy field Taxon Zhongzao22 Jinzao47 Quantity Dominance Quantity Dominance Tanytarsus formosanus 4690 0.6623 4030 0.6404 Chironomus sinicus 1577 0.2227 1562 0.2482 Tanypus punctipennis 722 0.102 651 0.1034 Polypedilum nubifer 92 0.013 50 0.008 Total 7081 1 6293 1

Dominance (D), D=NMAX/NT, where NMAX is the quantity of a given species, NT is the total quantity of all species. Rice Science, Vol. 18, No. 2, 2011

Fig. 2. Dynamic of Tanytarsus formosanus (A) and Chironomus sinicus (B) in the early rice season in Fuyang, Zhejiang province, China 2009.

Zhongzao 22 field and about 2 folds in Jinzao 47 field. the density. The later phase also ranged from May 30 to the Sex ratios of dominant species harvesting, and population densities decreased largely as compared to the early phase. For example, from In General, the sex ratio of T. formosanus, the May 30 to June 4, the averages of collected adults of most dominant species, was reversed during the early both species were only two individual/(d·trap). In and late phases. The sex ratio of T. formosanus was general, in the early phase, T. formosanus occurred at female biased during the early phase in both fields. a large quantity and fluctuated at a relatively larger The female/male ratio of adults collected from range, whereas occurred at a small quantity and Zhongzao 22 field was 1:0.69 during the early phase fluctuated at a small range in the late phase. and that from Jinzao 47 field was 1:0.84. By contrast, As Fig. 2-B shown, the second dominant species the sex ratio was strongly male biased during the late was C. sinicus. The population dynamic patterns were phase in both fields. The female/male ratio of T. also similar to each other in both rice fields. Dynamic formosanus was 1:2.67 in Zhongzao 22 and 1:1.166 in pattern of C. sinicus population could be divided into Jinzao 47 field (Fig. 3-A, B). In addition, from the the early and the late phases. Additionally, the occurred individuals of T. formosanus, the number of fluctuation pattern was also similar to T. formosanus. females was significantly different from that of males The difference between these two species was about in Zhongzao 22 field (p=0.0378). However, it was not

Fig. 3. Comparison of collected females and males of Tanytarsus formosanus in Zhongzao22 (A) and Jinzao47 (B) fields in Fuyang, Zhejiang province, China 2009. LI Zhi-Yu, et al. Occurrence and Population Dynamics of Chironomids in the Early Rice Field the case in Jinzao 47 rice field, Southeast Asia, such as in Malaysia (Al-Shami et al, The sex ratio of second dominant Chironomid 2006). P. nubifer is a worldwide distributed species, C. sinicus, was male biased in both fields Chironomid species that can occur in a large number throughout the entire season (Fig. 4-A, B). The especially in eutrophia waterbody. Sometimes, adults numbers of males collected in two rice fields were of P. nubifer can cause a serious nuisance problem for more than that of females at the sampling dates, with human activity (Wang, 2000). In the early rice season, the female/male ratios of 1:2.07 and 1:1.15 in the abundance of P. nubifer was not very high, which Zhongzao 22 and Jinzao 47 field, respectively. In might be due to the lack of organic substances during Zhongzao 22 field, the collected numbers of females the early rice season and that rice field is not and males were significantly different (P<0.01). constantly lagged by water, in comparison to the eutrophia lakes. DISCUSSION It was estimated that there were 2.8 million (in Jinzao 47 field) and 3.2 million (in Zhongzao 22) 2 Wang (1998) recorded that there were 3 Chironomid adults emerged from every 667 m field subfamiles, 13 genera, and 19 species of Chironomids over the entire rice season. In addition, 81% and 77% in Chinese rice ecosystem. In his report, these of Chironomids were collected during the early phase, Chironomids were distributed across 12 provinces in respectively. Since the pest community, e.g., rice China, and there were only 1 subfamily and 6 species planthoppers, is still in a low abundance, the large in Zhejiang province alone. In our trial, there were 2 number of Chironomids provides a rich food source subfamiles, 4 genera, and 4 species collected. Among for predators. Thus, the predators can be effectively these species, T. formosanus, P. nubifer and T. promoted. Consequently the predators may have a punctipennis have been recorded in his survey already, greater controlling effect on the pests during the late but not C. sinicus.. Indeed, C. sinicus was previously rice season (Wu et al, 1994; Guo et al, 1995). named as C. plumosus before 2005(Kiknadze et al, Moreover, in the late phase, largely declined 2005), which is a kind of widely distributed abundance of Chironomids allows predators to center Chironomids. Overall, 4 Chironomid species reported on pests. Thereby, the occurrence patterns of in our study are widely distributed species. For Chironomids may play a very positive role in terms of instance, the distribution of T. punctipennis ranges controlling rice pests, especially for the biocontrol from the Northwest China, Ningxia Hui Autonomous effect on rice planthoppes. Region, the Northeast China, and Liaoning province Two dominant Chironomids, T. formosanus and (Wang et al, 2000). It is also commonly found in the C. sinicus, showed different sex ratio patterns over the

Fig. 4. Comparison of collected females and males of Chironomus sinicus in Zhongzao22 (A) and Jinzao47 (B) fields in Fuyang, Zhejiang province, China 2009. Rice Science, Vol. 18, No. 2, 2011 entire rice season. During the early phase, there are identification. This work was supported by the more females than males in T. formosanus. During the National Transgenic Crops Program, China (Grant No. late phase, it became male biased. By contrast, it was 2008ZX08012-004), the Startup Grant for Returned male biased in C. sinicus throughout the entire rice Oversee Scholar of China National Rice Research season. Since we do not know the biological Institute (Grant No. 2008001). characters of these two species, including other Chironomids collected from rice field, we suppose it REFERENCES is about the differences of their developmental periods and possibly about the protandry, like some other Armitage P D, Cranston P S, Pinder L C V. 1995. The insects. 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