Tropical Biomedicine 27(3): 404–416 (2010)

Breeding patterns of the JE vector gelidus and its predators in rice cultivation areas of northern peninsular

Abu Hassan, A.1*, Hamady Dieng1, Tomomitsu Satho2, Michael Boots3 and Jameel S.L. Al Sariy1 1 School of Biological Sciences, Universiti Sains Malaysia, Penang 2 Faculty of Pharmaceutical Sciences, Fukuoka University, 3 Department of and Plant Sciences, University of Sheffield, UK * Corresponding author Email: [email protected] Received 7 May 2010; received in revised form 7 June 2010; accepted 12 June 2010

Abstract. (JE) virus activity is an important cause of viral encephalitis in Southeast Asia. In Malaysia, JEV activity has been first detected in Culex gelidus in 1976. Since then, no study has fully addressed the seasonal dynamics of this . As irrigated rice production expands, the incidence of JEV vectors, particularly Cx. gelidus is expected to increase. We surveyed Penang Island to determine the breeding patterns of Cx. gelidus and their potential insect predators, in relation to habitat/niche and rice growing period. Six rice fields proper (RFP) and related drainage canals (DC) were visited through three cultivation cycles (CCs) over 17 months. Weekly visits were performed to each of the 36 sites and mosquito larvae and aquatic were sampled from RFP and DCs using dippers. Culex gelidus was abundant in RFP and almost absent in DCs. Its densities usually were high during the first and 3rd CC and when the RFs were in Fp, Pp and Gp. In DCs, the mosquito was abundant during Mp, e.g., 2nd CC. Predators, especially those belonging to the families Corixidae, Coenagrionidae and Dytiscidae, were more present in RFP. Predator numbers usually were high during the first CC; in some cases predator abundance peaked during other CCs, e.g., corixids and dysticids. In RFP, neither corixids nor coenagrionids showed any positive correlation with densities of Cx. gelidus. However, dytiscids’ population peaked when the mosquito densities were on the rise. These observations suggest that Cx. gelidus is active during the period of rice cultivation. Operational vector control through bio-control or with insecticides near the end of the rice cultivation season in RFP may prove beneficial in reducing the density of Cx. gelidus, but also the amount of bio-agent or insecticide applied on riceland.

INTRODUCTION Several species of Culex that are potentially competent for JEV transmission Mosquito-borne diseases are a major threat (Yap & Ho, 1977; Vythilingam et al., 1994; to public health worldwide. Frequent Abu Hassan et al., 1998), are found in outbreaks of diseases such as dengue Malaysia, where rice is the third most (Rahman et al., 2002; Enserink, 2006) are important economic crop covering an area reminders of the continued threat of of about 209,300 hectares (Karim et al., diseases transmitted by insects, as does the 2004). The amount of land devoted to rice rise in cases of Japanese encephalitis virus cultivation by irrigation, and consequently (JEV) infection during the 2000s in Asia the incidence of related mosquito-borne (Ayukawa et al., 2004; Parida et al., 2006; diseases, are both expected to increase Wang et al., 2007). with the growing need for rice to feed the

404 expanding human population. With this negative effect (Chandler & Highton, 1975, expansion of irrigated rice production, JE 1976). The community of RF is a vectors most likely to increase in dynamic system in which each member has importance include Culex gelidus and a preference for a particular phase of rice Culex tritaeniorhynchus. In Malaysia, JEV field (RF) development (Takagi et al., 1996; activity has been detected in both species, Victor & Reuben, 2000). but is most common in the former species Efforts to combat rice field mosquito (Heathcote, 1970). Culex gelidus is found vectors still rely heavily on insecticides in many Southeast Asian countries (Lee et (Rose, 2001; Russell & Kay, 2008). al., 1989), where it is considered important However, the increased use of chemical as an important vector of Japanese insecticides has led to adverse effects on encephalitis (Williams et al., 2005). Native the environment, paddy ecology and to Southeast Asia, this species has proven human health (Pingali & Gerpacio, 1997). to be invasive. It has been reported as a Therefore, there is increasing emphasis voracious biter of humans, but also as on reducing the amount of insecticide having a preference for large domestic applied on agricultural land. The spatial (Whelan et al., 2000). In Malaysia, distribution of mosquitoes in RFs and Cx. gelidus is considered important in the related seasonal variations are central maintaining JE in pig-mosquito cycles. As to the successful application of an Malaysia is not that devoted to pig farming, insecticide-based control programme and it is possible for Cx. gelidus to acquire an have important environmental implications. increased human biting behavior, with Accurate information regarding the spatial respect to reduced number of pig host. distribution of the target has the potential Rice fields are inhabited by the to reduce the amount of product sprayed immature stages of mosquitoes including onto the crops. This information also is Cx. gelidus and Cx. tritaeniorhynchus in important for identifying reservoirs of addition to heterospecific insects that infectious agents. Surprisingly, the role of include mosquito predators (Sunahara et space as it affects population dynamics of al., 2002; Carlson et al., 2004). In fact, rice RF insects remains largely unexplored. growth creates microclimates that provide This study was set out to investigate a variety of habitats and niches conducive the breeding patterns of Cx. gelidus, and to a variety of organisms (Edirisinghe & coexisting aquatic insect predators in north Bambaradeniya, 2006). When irrigated, rice peninsular Malaysia, taking into account fields are connected to a network of habitat/niche and rice cultivation phase. irrigation and drainage canals (DCs). In addition to being the origin of most of the aquatic flora and fauna in rice fields MATERIALS AND METHODS (Fernando, 1993), these sub-habitats contiguous to the rice field proper (RFP) Study area and sampling sites also provide another environment for The survey was carried out in Penang, colonising insects (Amerasinghe et al., Malaysia within the rice growing areas of 1991; Edirisinghe & Bambaradeniya, 2006). Jalan Penanti and Seberang Perai from However, there has been relatively little February 2003 to October 2004. These research addressing the insect fauna of areas are mostly flat, and cover 8.75 these non-rice subhabitats. There has been hectares located 5.417ºN 100.417ºE (5º24’N a great deal of research regarding the 100º14’E). The area has a year-round effects of rice growth on the population equatorial climate, and is warm with high dynamics of insect communities. Overall, levels of sunshine. The average annual initial plant growth increases population rainfall is about 2600 mm, and the daily density of both mosquito and aquatic insect relative humidity varies from 60% to 96% (Chambers et al., 1979; Mogi & Miyagi, with ambient temperatures ranging from 1990), while later plant growth has a 23ºC to 35ºC (Ong, 1993; Ahmad et al.,

405 2006). The high levels of rainfall associated week from February 2003 to October 2004. with high relative humidity and the warm Metal dippers of 350 mL capacity fitted temperatures provide ideal conditions for with handles ca. 1.2 m long. At each mosquitoes. All rice fields (RFs) in the area sampling occasion, dips were taken along are irrigated by large irrigation canals the margin of RFP and DCs for 10 minutes from rivers and rainfall. The water is per site. Dips of water were strained received from a main reservoir and through a nylon bag (13 x 18 cm) and supplied to smaller canals present sampled insects brought to the laboratory. throughout RFs where two varieties of rice (MR219 and MR220) are cultivated. For the Data collection and analysis purpose of the survey, RFs were divided In the laboratory, some samples were into three stations, with two plots at each preserved in bottles with 75% ethanol, station, two replicates in each plot and separated by stages and counted. In some three sampling sites in each replicate. Plot cases, first and 2nd instar larval stages surface areas ranged from 0.76 to 1.89 were reared at room temperature hectares. All 36 sites were visited during (26ºC±1ºC, relative humidity 75%±10% and the rice growing season. In the year and photoperiod 13:10 h, 1 h dusk) until fourth half study period, typical cultivation stage and then identified to species under included a first cycle (February 2003 to a dissecting microscope (Olympus CX41; July 2003), a second cycle (August 2003 to Olympus, Tokyo, Japan). Aquatic insects April 2004) and a third cycle (April 2004 were identified morphologically to families, to October 2004). Except for the brief genera and species using appropriate drainage period during these cycles, RFs taxonomic keys (Usinger, 1956; Yano et al., were flooded continuously. As there were 1981; Mores et al., 1984). Mosquito no other ecotones in the vicinity, e.g. immature stages (larvae and pupae) were marshes, RFs proper (RFP) and drainage identified to subgenera or species using the canals (DCs) were the main breeding keys of Stojanovich & Scott (1966), Reid habitats for aquatic insects. The (1968) and Rattanarithikul & Panthusiri categorization of rice cultivation phases (1994). Density was defined as the number was adopted from Mogi & Miyagi (1990), of individuals per dip. This parameter was Abu Hassan (1994) and Che Salmah et al. determined for (i) Cx. gelidus collected (1999). RFs were classified into one of six from RFP and DC and (ii) corixids, phases of cultivation: plough phase (Pp), coenagrionids and dytiscids from RFP. To germination phase (Gp), young phase (Yp), assess temporal variations of population tiller phase (Tp), mature phase (Mp) and levels, densities were related to CCs. The fallow phase (Fp). All phases were present interactions of Cx. gelidus with the at the 36 sites. predators were examined in RFP when there were increased numbers of L1-L2 and Sampling of predators. Analyses were performed Since this study was aimed at only Cx. using Kendall’s tau-b correlation analysis gelidus, corixids, coenagrionids and from the statistical software package SPSS dytiscids, other aquatic insects were not for Windows v.11.0 (SPSS Software, Inc., enumerated thus following Das et al. New York, USA) (George & Mallery, 2003). (2006). During each rice cultivation cycle (CC), mosquito larvae and aquatic insects were sampled from RFP and DCs adopting RESULTS others (Chambers et al., 1979; Takahashi et al., 1982; Stewart et al., 1983; Service, Culex gelidus 1993; Abu Hassan, 1994). Sites for sampling A total of 20,913 individuals of mosquito were marked in both RFP and DCs using immature stages (L1-L2, L3-L4, and pupae) wooden stakes numbered according to the were collected, of which 99.9% were replications. Sampling was performed each collected from RFP and 0.1% were from DC.

406 All stages were found in RFP, but only the weeks. The density of the mosquito peaked two last were collected from DC. L3-L4 was during the 20th week (302.15 individuals per the most common stages, comprising more dip) and then decreased sharply thereafter. than 45.7% of the total. Its abundance was In DCs, this mosquito was not encountered higher in RFP than in DC (98.8% vs. 1.2%, (Figure 1C). respectively). During the first CC, the density of Cx. Insect predators gelidus in RFP was 4.48 individuals A total of 13,176 corixids were collected, (larvae + pupae) per dip during Gp. It of which 71.8% were collected from RFP. increased and remained almost constant They were most common during the first throughout the Yp with small peaks (11.32 and 2nd CCs, comprising 43% and 33% of and 9.71 individuals per dip) during the 3rd the total, respectively. A total of 1,508 and 6th weeks. The mosquito was almost coenagrionid larvae were collected, of absent (0-19 individuals per dip) when RFs which 64.6% were found in RFP. were in Tp and Mp. The density was high Coenagrionids were more abundant and almost constant during the Fp with a during the first and 2nd CCs, representing major peak (325.9 individuals per dip) 60.8% and 25% of the total, respectively. during the 17th week. In DCs, this species A total of 1,470 dytiscid larvae were was absent (Figure 1). collected, of which 64.6% were found in During the 2nd CC, the density of Cx. RF proper. Dytiscids were mostly gelidus was highest when RFP were in Pp encountered during the 2nd CC, comprising with a major peak (116.08 individuals per 46.3% of the total (Table 2). Other taxa dip) during the third week. It decreased encountered were Baetidae, Libellulidae, sharply during Yp and Tp. The mosquito Belostomatidae, Nepidae, Notonectidae, was almost absent (0-1.5 individuals per Pleidae, Hydrophilidae and Hydrochidae. dip) during the 11th and 13rd weeks, but reappeared at the end of Mp. Coenagrionid population dynamics and During Fp, the density of the mosquito interactions with Cx. gelidus increased from 21.49 and 32.99 individuals The genera encountered were per dip between the 17th and 19th weeks and Pseudagrion, Ischnura, Aciagrion and then decreased to its minimum (0 Cercion. The density of Coenagrionids was individuals per dip) during the 21st week. low during Gp and Yp. From the end of the From this week, the density of the mosquito latter phase, their density gradually increased to 91.57 individuals per dip increased attaining 3.9 larvae/dip at the during the 23rd week and then decreased 12th week and its maximum (7.3 larvae/dip) sharply in the 25th week. In DCs, Cx. at the beginning of Mp. It decreased to gelidus first appeared during the end of Tp less than three individuals thereafter. and the beginning of Mp with a small peak Coenagrionid larvae exhibited a significant during the 12th week. The mosquito was negative correlation (r = -0.344, P<0.05) absent the following 6 weeks. During Fp, with densities of Cx. gelidus especially the density of the mosquito increased to a during Fp. The peak in the population of the maximum at the 19th week and then mosquito coincided with a decrease in that decreased during the following week. The of the predator (Figure 2). mosquito exhibited a third peak during the 21st week and was absent thereafter Corixid population dynamics and (Figure 1B). During the 3rd CC, Cx. gelidus interactions with Cx. gelidus was almost absent (0-0.66 individuals per Only the genus Micronecta was found. The dip) during Gp, Yp, Tp and Mp. During Fp, densities of corixids were low throughout its density increased from 11.66 and 22.57 Gp and Yp. From the end of Yp, the density individuals per dip between the 15th and of this insect increased progressively and 16th weeks. The mosquito was not reached its major peak (95.8 indiv./dip) at encountered during from the 17th to the 19th the 9th week when rice field were in Tp. A

407 second but minor peak also was observed correlations between the population during this phase. The population densities of the two insects during the first decreased gradually during the next (r = -0.477, P<0.01) (Figure 3A) and the 2nd phases, but corixids tended to rebound at (r = -0. 367, P<0.05) (Figure 3B) CCs. The the end of Fp. There were strong negative peaks in the population of the mosquito

Figure 1. Seasonal densities of Cx. gelidus and aquatic insects at different rice growing phases during first (A), second (B) and third (C) cultivation cycles

408 Figure 2. Interactions of Cx. gelidus immatures stages with Coenagrionidae in rice fields proper (RFP) during the first rice cultivation cycle

Figure 3. Interactions of Cx. gelidus immatures stages with Corixidae in rice fields proper (RFP) during the first (A) and 2nd (B) rice cultivation cycles

409 Figure 4. Interactions of Cx. gelidus immatures stages with Dytiscidae in rice fields proper (RFP) during the 2nd rice cultivation cycle coincided with a decrease in that of the fields function. In general, the water from predator during both cycles. the main reservoir is supplied to the entire field uniformly through irrigation canals. Dytiscid population dynamics and Aquatic habitat insect productivity has interactions with Cx. gelidus often been associated with its degree of The genera encountered were Canthydrus, stability (Walker et al., 1991). Flooded Laccophilus and Hydrovatus. The density paddies have greater stability and the of dytiscids peaked during the first week feeding stages of insects may have (4.9 individuals/dip), decreased at the end abundant food resources as the water is of Pp and increased again to its maximum stagnant thereby allowing plankton (5.3 individuals/dip) at the beginning of Yp. development. After a certain period, the The population decreased gradually during stagnant water is discharged from the rice Tp and dytiscids were almost absent during fields through drainage canals and Mp. They rebounded and increased to a discarded (Johnson & Miller, 1973). major peak at the 19th week (5.74 Drainage canals hold water almost all individuals/dip) during Fp. Their density year round, contain more vegetation for remained high and nearly constant during longer period, and also provide refuge for the 4 next weeks, but decreased thereafter. aquatic predators when rice fields have Dytiscids exhibited a strong positive been artificially or naturally dried (Abu correlation with Cx. gelidus densities (r = Hassan, 1994). Drained water has high -0.396, P<0.01). The peak in the mosquito concentrations of nutrients and soluble population during Gp and the high and salts that can interfere with the uptake of constant densities during Fp corresponded other nutrients. These chemicals may to increased dytiscid density (Figure 4). inhibit microbial growth and consequently prevent larval growth in DCs. Water in DCs also has increased turbidity. According to DISCUSSION Paaijmans et al. (2008), there are many possible ways in which, water turbidity can Despite the close proximity of DCs and RFP, have effect on mosquitoes. For example, both Cx. gelidus and insect predators were suspended soil particles can increase water present in lower abundance in DCs. This temperatures at midday, thereby forcing was probably related to how irrigated rice near-surface dwellers such as Culex larvae

410 to remain submerged for long periods of rice plants <30 cm, almost entirely exposed time. There may also be direct interference to direct sunlight. These changes result in of soil particles with larval feeding that a vigorous vegetative aspect during Tp would slow the larval growth and decrease when the water surface is half-shaded by survival (Ye-Ebiyo et al., 2003). Culex the plants. This period is the time when gelidus was almost absent from DCs. Thus, most of the prey species have established a possible explanation of this absence is their populations, thus providing ample that this mosquito can discriminate habitats food supply for the predator species. for egg depositions that enhance success Vigorous vegetative growth may cause for its offspring. The observed low mechanical obstruction, thereby prevents prevalence in DCs is likely an adaptation oviposition (Forattini et al., 1994). The to prevent unsuccessful development. progressive shading of the water surface In RFP, L1 and L3 larvae of Cx. gelidus results in tiller fields. They further develop were highly present during the first cycle. to fallow fields characterized by a reduced The abundance of young instar larvae has vegetation cover and depressions filled been often correlated with increased with less clear water. This aspect of RFs oviposition. Mutero et al. (2004a) working water has been reported very attractive to in Kenyan rice fields observed increased gravid females, which may explain the high densities of young An. arabiensis larvae prevalence of Cx. gelidus during Fp. one week post-rice transplantation. They In rice fields, predator ability has been suggested that the increase in larval often related to the presence of alternative population level was the result of increased preys, because they can attract predators. egg-laying. In fact, mosquito oviposition Benfield & Minello (1996) and Luzier & behaviour is strongly influenced by visual Summerfelt (1997) observed that the stimuli. Evidence has been produced which foraging behaviour of some shrimp reduce demonstrates that synthetic fertilizers predator efficiency to detect and catch applied to RFs induce the disappearance of mosquito larvae. Chase et al. (2002) and water turbidity, thus creating a sharp visual Blaustein & Chase (2007) recorded reduced contrast that is very attractive to gravid predation responses by insect predators on mosquito females (Mutero et al., 2004b). rice field larval mosquitoes. They suggested Although fertilizer content was not that the reduction was a result of the measured in the current study, in general, presence of controphic species that served fertilizers are applied to nurseries, as alternative preys. In the present study, ploughed and newly transplanted fields in the predators encountered included highly most RFs of tropical Asia (Das et al., 2006). predaceous coenagrionids, which consume Indeed, the earlier cycle will tend to large numbers of larvae (McDonald & receive fertilizers first as it starts the rice Buchanan, 1981) and corixids. Although growing season. their predation ability was not specifically There was clearly a relationship analysed in the present study, the between the cultivation phase and the population level of the two predators densities of Cx. gelidus. Overall, the declined when Cx. gelidus densities plough/germination and fallow phases increased. This finding corroborates the provided better breeding conditions and the earlier reports that Culex larvae showed observed temporal abundance patterns positive correlation with predators (Victor could be explained on the basis of RFs & Reuben, 1999). Both insect predators evolution, well studied previously (Mogi & peaked in tiller phase. This period is Miyagi, 1990; Abu Hassan, 1994; Forattini earlier than the time of mosquito density et al., 1994, Che Salmah et al., 1999). In peak. Due to this time lag, a proportion of fact, after the start of flooding, ploughed/ the mosquito larval population escapes germinating fields exhibit gradual changes predation thus allowing them to develop. It in appearance with an initial “open/ is usually assumed that in rice fields, flooded” aspect turning to young fields with “predator pressure” is the major force other

411 than parasitism and pathogenic infection competition by having fewer individuals that reduces the abundance of larval JEV surviving to compete for food. These vector populations (Mogi et al., 1980; Miura individuals may benefit from a reduction in & Takahashi, 1988; Das et al., 2006). competition for food and emerge with a Therefore, the observed high densities of large body size. Thus, in this often the mosquito during Fp could be partly neglected sub-habitat, an increase in adult explained on the basis of feeding body size is possible and this could preference of the predator that play an potentially result in an increase in vector important role in prey survival. For capacity. In addition, due to its open aspect example, the ceonagrionid Pseudagrion and the permanence of water, DCs can be salisburyense prefers chironomid and an attractive habitat for ovipositing psychodid to other preys (Chutter, 1961), females. Therefore, the vigorous vegetative while corixids are preferred preys for Anax growth and the increased abundance of junius (Folsom, 1978). In contrast, predators during Tp may contribute to DCs dytiscids showed a strong positive colonization. The turbid aspect of DCs water correlation with Cx. gelidus densities. is also important in mosquito survival. An When dysticids reached their peak of increased turbidity can decrease the abundance during Gp and Fp, the chance of being preyed upon due to a lower population level of the mosquito declined, visibility (Paaijmans et al., 2008). In this but rebounded rapidly during the next regard, DCs should be considered for the cycle. control of JEV vectors. For example, due to To address the efficiency of insecticide- its small size, DCs may require only small based control of mosquito-borne diseases amounts of insecticides to achieve including JEV, Gu & Novak (2005) argued population control of Cx. gelidus and other for the need to identify and direct larval JEV vectors. control efforts to the most productive In aquatic habitats such as RFs, habitats. There is a close association predation is a major mortality factor between predation level and adult body and responsible for the maintenance of vector population sizes. Indeed, low predation density below a critical threshold where pressure will tend to produce larger bodied disease transmission could not occur. The adults and higher population density than results of this study indicated that Cx. high predation pressure (Agudelo-Silva & gelidus is present throughout the rice Spielman, 1984; Klowden et al., 1988; growing season with greater abundance Dieng et al., 2002). Large body size has a during the Fp. This period is the time when positive effect on vector capacity (Walker most predators appeared in small numbers. et al., 1998; Schneider et al., 2004). Clearly, this limited predation pressure will Several parameters come into play when tend to result in outbreaks of Cx. gelidus. the vectorial capacity of a mosquito for an For successfully controlling this JEV arbovirus is considered (Reisen, 1989). In vector, any operational control programme particular, population density plays a should consider larviciding just before and crucial role in the competence of a vector. during the Fp. Indeed the more individual vectors are present, the more likely they will be able Acknowledgements. Authors are grateful to to transmit a pathogen. Therefore, it is the staff of the Vector Control Research likely that RFP will produce adult Cx. Unit, School of Biological Sciences, Dr. gelidus at great number as it contains Abbas Al-karkhi, Mr. Hadzri, Mr. Kalimuthu, small numbers of weak predators during the staff of Mardi Station, and the personnel Fp, a period of increased mosquito density. of Bukit Merah Agricultural Experimental In DCs, partial predation could reduce Station.

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