Life History Effects of Prey Choice by Copepods: Implicattons for Btocontrol of Vector Mosquitoes

Home , Cyclopidae, Macrocyclops, Macrocyclops albidus, Mesocyclops pehpeiensis

Journal of the American Mosquito Control Association, 19(l):67-'13,2OO3 Copyright O 2003 by the American Mosquito Control Associarion, Inc.

LIFE HISTORY EFFECTS OF PREY CHOICE BY COPEPODS: IMPLICATTONS FOR BTOCONTROL OF VECTOR MOSQUITOES

HAMADY DIENG,' MICHAEL BOOTS,' NOBUKO TUNO,T YOSHIO TSUDAT aNo MASAHIRO TAKAGI'

ABSTRACT, Macrocyclops distinctus, Megacyclops viridis, and Mesocyclops pehpeiensis, which are common in rice fields during the summer season in Nagasaki, Japan, showed variable potentialities as biological control agents of lawal Aedes albopictus, Culex tritaeniorhynchus, and Anopheles minimus in the laboratory. Macro- cyclops distinctus and M. viridis. the largest copepod species, had fewer eggs within an egg clutch in nature than the smallest species, M. pehpeiensis, which also had a lower developmental time for sexual maturation (based on the appearance of the lst clutch). Longevity as well as fecundity were influenced by nutritionat conditions and varied significantly between the species. All species had shorter life spans when starved, but resistance to starvation was more pronounced in the larger species. AII the species had lower clutch production when starved. Also, although the frequency of clutch production was high in M. pehpeiensis (M. pehpeiensis produced a clutch every 2 days, whereas M. distinctus and M. viridis took on average almost 3 days), total clutch production was far higher in the larger species. The copepods fed readily on mosquito larvae, with M. distinctus and M. viridis killing fewer Ae. albopictus than M. pehpeiensis, which, however, killed fewer An. minimus. These copepods exhibited a similar and limited predation against Cx. titaeniorhynchas. Results of our study support the contention that these copepods have the potential to be used as biological control agents of immature mosquitoes. Also, our results give useful information on colony maintenance and field introduction. In particular, releasing copepods with Paramecium as food could increase their survival in the habitat of the targeted pest.

KEY WORDS Mosquito, immature, copepod, predation, reproduction

INTRODUCTION reproductive biology of the candidate copepods, which is clearly directly related to their survival Cyclopoid copepods are distributed almost uni- and ease of mass production in field applications. versally in aquatic habitats and may occur at high It has been reported that habitat desiccation (Zhen densities in areas that produce mosquito larvae et al. 1994) and loss (Marten et al. 1994) have been (Nasci et al. 1987, Brown et al. 1991). Although reported to influence the populations of most spe- their interactions with mosquito larvae still are not cies, including copepods. Disappearance of habitat fully understood, they have been demonstrated to was particularly noted when ecologically different serve as obligate hosts for fungi (Whistler et al. species were mixed to improve control efficiency 1974, Fredeici (Andread- 1980) and microsporidia (Marten et al. 1994). Indeed, population loss is the is et al. 1985, Sweeney et al. 1985, Vossbrinck et most important factor limiting their use. Recently, al. 1998) to which mosquitoes are vulnerable. In Kay et al. (2O02) reported desiccation resistance of addition, copepods have become a focus of large eggs in the genus Mesocyclops. Therefore, a pop- number of studies focused on their use for biocon- ulation ecological approach, especially one that in- trol (Riviere and Thirel 1981, Marten 1984, Nasci cludes the study of reproductive biology, should be et al. 1987, Marten 1990, Marten et al. 1994, Zhen involved in evaluating copepods as biological con- et al. 1994, Schreiber et al. 1996). Copepods have trol agents. been shown to be very useful in controlling mos- In cyclopoid copepods, female reproduction is quitoes (Aedes sp.) in large containers (Nam et al. always sexual (Wyngaard and Chinnapa 1982, Gil- 2000, Kay et al. 2OO2) and in subterranean habitats bert and Williamson 1983) and ovigerous females (Russell et al. 1996, Kay et al.2OO2). Presently, carry their eggs in 2 sacs attached ventrolaterally copepods are one of the most promising biological to the genital segment of the urosome. When ma- control agents. ture, the sacs drop and subsequently hatch within Consideration of predatory efficiency, reproduc- the medium (Gilbert and Williamson 1983). Fe- tive potential, ease of mass production, and survival males have 4 recognizable reproductive phases: is the lst step of evaluating a candidate biocontrol ovigerous, bearing egg sacs; gravid, oviducts full agent. However, most of the evaluations of cope- of visible darkened matures oocytes; both oviger- pods as candidates for mosquito control have con- ous and gravid; and neither ovigerous nor gravid sidered only their predatory efficiency on 1st-stage (Williams and Butler 1987). Females are able to larvae. No evaluation has taken into account the store sperm, which enables the fertilization of many oocytes from 1 insemination (Hill and Cooker 1930, Williams and Butler I Department of Vector Ecology and Environment, In- 1987, Maier 1992). stitute of Tiopical Medicine, Sakamoto l-12-4, Nagasaki These alternative reproductive states depend largely 852-8523, Japan. on environmental factors, that is, food in particular 2 Department of Biological Sciences, Stirling Universi- (Williams and Butler 1987). Thus, diagnosis of the ty, Stirling, Scotland. reproductive state is useful during a field trial. 68 JounNll oF THE AMERICANMoseurro Conrnol Assocterror Vor. 19. No. I

In this study, we evaluated 3 copepods (Macro- tions: daily supply of 5 ml of Paramecium infusion cyclops distinctus, Megacyclops viridis, and Meso- (7-day-old); daily supply of live mosquito larvae; cyclops pehpeiensis) against 3 mosquito species and starvation, given only tap water. The reproduc- (Aedes from 3 genera albopictus (Skuse), Culex tri- tive phase of each individual was recorded by daily taeniorhynchas Giles, and Anopheles minimus observation under a lamp. In case of egg hatch, the Theobald) by examining the reproductive output experimental vial was washed with hot water to with reference to nutritional factors including star- prevent an additional feeding source, because co- vation, mosquito prey, and the coexistence of Par- pepods are reported to feed upon their own nauplii amecium. (Maier 1995). Predation on dffirent mo.squito lar-vae: The 3 MATERIALS AND METHODS copepod species were evaluated separately against lst-stage larvae of Ae. albopictus, Laboratory colonization, systematics, and basic Cx. tritaeniorhynchus, and An. minimus in features of copepods: The species used in this small vials with 5 ml study were collected fiom rice fields near Isahaya of well water and 1 adult copepod that had been City, Nagasaki Prefecture, in southern Japan. Sam- starved for 24 h. Larvae were given at a ratio of pled specimens were allowed to acclimate to the 50 larvae/copepod. Containers with the same num- laboratory where they were maintained under con- ber of larvae but without copepods served as con- trolfed tempeftture (23-25'C) and light conditions trols. For each copepod, the predation trial against and relarive humidity (60-8OEo). Lighting was pro- each mosquito was replicated 15 times. vided by 2 fluorescent tubes (80 W) with a l2:1O Data collectir.rn.' Following the method of Hop- h light: dark photoperiod. From these samples, kins (1977), we measured the body size and the gravid f-emales were introduced singly in trays and number of eggs contained in the 2 egg sacs fed a mixture of Paramecium-Chilomonas infusion (:clutch size) in laboratory-eclosed specimens. and boiled lettuce, following the methods of Suarez The distance from the nauplii eye to the end of the et al. (1992), to establish a monospecies culture. caudal rami, excluding setae, was used to represent Copepod food was cultivated in plastic bottles and body size. Clutch size was recorded after detaching fed with wheat seeds. Cultures were renewed ap- both egg sacs and carefully dissecting the sacs by proximately weekly. Subsamples were made from removing a protective membrane. In a predation ex- laboratory-eclosed specimens for species identifi- periment, mangled mosquito larvae were consid- cation, body size measurement, and counting of eggs. ered killed by copepods. The number of surviving larvae was counted after I Mosquitoes: A colony of Ae. albopicras was ini- day. The difference between the initial tiated from eggs collected in Nagasaki, whereas and final larval numbers was taken colonies of Cx. tritaeniorhynchus and An. minimus as the numbers killed per female per day. Repro- were initiated from larvae collected. resoectivelv. ductive parameters such as the time for the lst lrom Nishi Arita and Ishigaki. sourhein Japan. clutch to appear (:sexual maturation time), the Mosquitoes were maintained under the same envi- number of clutches produced, the interclutch peri- ronmental conditions as the copepods. Larvae were od, and the age at death were monitored for each reared in trays, and fed daily with a mixture of liver specimen. We calculated developmental time for powder and brewer's yeast. Adults were held in sexual maturity as the time from maternal egg hatch cages, provided with 107o sucrose solution, and to the appearance of the lst clutch for each speci- bloodfed on mice at approximately 4-5 days after men. The interclutch period was the time between emergence. 2 clutches. Longevity was the time from maternal Reproductive characteristics.. From the colonies, clutch hatch to death. Resistance to starvation was l0 egg sac-bearing f'emales of each species were taken as the time from hatch to death in treatment placed in 250-ml vials filled wirh water and fed without food. daily with 5 ml of a 7-day-old Paramecium infu- Statistical analysis: The computer program Sys- sion (-15.102 cells, based on rhe method used by tat (Wilkinson 1996) was used to perform statistical Enright and Hennessey [1987]). After egg hatch, analysis. A 2-way analysis of variance was applied parents were removed and nauplii were fed daily to compare the basic features, developmental time, with 5 ml of mixed food (Paramecium: Chilomonas longevity, and resistance to starvation 2.5:2.5 ml). One week later, 2-3 progenies of each of the different copepod species that hatched on the same day were mixed species as well as the number of to increase the chances of successful and viable mosquito larvae they killed. We analyzed fecundity mating. and the effects of nutritional conditions on this pa- Newly ovigerous females (with lst clutch) were rameter by comparing the numbers of clutches pro- transferred individually into small vials under the duced and the interclutch period (Paramecium same feeding conditions as their parents for fecun- treatment). The Tukey-test was applied for the com- dity and longevity studies. Fifteen to 18 of these parison between copepod species in each of these females were assigned to I of 3 nutritional condi- parameters. Mrrcu 2003 Pnpy CnorcE By CopEpoDs 69

Table 1. Mean (+ SE) body size (in mm) and clutch size in various copepod species.l

Body size Clutch size

Species Mean Range Range Macrocyclops dis tinctus 1.57+0.08a (n:25) 1.47-t.75 26.O4+ 1.3a 2r) t4-37 Megacyclops viridis 1.53+ 0.07a (n: 25) 1.37-1.67 65.92+ 4.6b 13) 33-l0l M esocyc lops pehpeiensis 1.28+ O.O"7b (n: 16) l. 1- l .40 100.60+ 4.9 c 1s) 64-r30 rBy analysis of vriance, values in the same column and with the sme lowercase letter do not show a significant difference (P ) 0.05); n, number of replicates.

RESULTS (Table 2). Life spans were different between the species for each nutritional condition (P***,"" ( Body and clutch sizes 0.0001, P,.,,""< 0.0001, P"*"^nu*: 0.0159). In all These 3 species are significantly different in treatments, M. pehpeiensis had the shortest life span body (P < 0.001) and in clutch (P < 0.001) sizes. and M. viridis had the longest life span (Table 3). Mesocyclops pehpeiensis is smaller than M. dis- Adult females of all species lived longer when tinctus, which in turn is smaller than M. viridis (Ta- supplied with either Paramecium or mosquito lar- ble 1). Mesocyclops pehpeiensis had more eggs vae than when starved (Pr.o,nr,n^: 0.0003, Pu.vtitis within its sacs than M. distinctus. Macrocyclops : 0.0087, Pu.nenpep,"t:0.0001). Resistance to star- distinctus had the smallest clutch size (Table 1). vation was much higher in M. viridis and M. distinctus. Mesocyclops pehpeiensis had the same longevity when unfed or fed with mosquito larvae Development and sexual maturation ffable 3). This parameter differed significantly between species (P < 0.0001). Mesocyclops pehpeiensis had Fecundity the shortest time to mating and extruding of the 1st clutch. It was followed by M. distinctus, whereas A significant difference was found in egg sac M. viridis had the longest time (Fig. l). production among the nutritional conditions (Table 2). In the starvation treatment, no significant difference was found in the number of clutches pro- Longevity and resistance to starvation duced (P.,..,",,.": 0.1559) between the species (Ta- Both species and nutritional condition as well as ble 4). In copepods supplied with mosquito larvae, their interactions significantly affected longevity reproduction differed significantly between the species (P,,."".: 0.0002; Table 4). ln the Paramecium 35 treatment, although no significant difference was found in clutch production (Pr.,.,,",.,,,,,:O.l33l), M. viridis laid numerically more clutches than the other 2 species, in which the numbers of clutches pro- gJU duced were similar (Table 4). Females of all 3 species produced the most clutches when fed (Pr. : 0.0002, Pr.,,,,0,, : €=f< u,n,,,"u" 0.0001, Pu penptiensi:< 0.0001; Table 4). Mesocyclops C! pehpeiensis did not produce a single clutch in the '.1 absence of food, whereas M. distinctus and M. vir- o;)n idis females did produce clutches (Table 4). When .=9 : food was supplied, all species reproduced, with M. o- distinctus and M. viridis prodtcing the most clutches when supplied with mosquito larvae (Table 4). The timing of clutch production (when using only O data from treatment with supply of Paramecium) was significantly different between species (P : Macro Mega Meso 0.0055). Mesocyclops pehpeiensis had the shortest interclutch period (Table 5). Copepod species

Fig. 1. Developmental time (in days) for sexual mat- Predation uration of newly hatched nauplii of difl'erent copepod species when fed with a mixed Paramecium-Chilomonas in- Larval mortality in containers with copepods was fusion (Macro : Macrocyclops distinctus, Mega : significantly different from that observed in control Megacyclops viridis, and Meso : Mesocyclops pehpeien- containers for each mosquito species (Po".ro",r,^ < .sr.s). pcx. pon. o.oool, trtaenL,rhrnch,,.< 0.0001, ^r,^^ 1 Jounxal or rne Awnnrcar Moseuno CoNrnor AssoclATIoN VoL. 19, No. I

Table 2. Results of analysis of variance for effects of speciesand nutritional conditions on longevity and egg production in various copepod species.

Longevity Egg production Source variables df F-value F-value

Species z 39.48* 11.47* Starvation vs, larvae ys. Paramecium 2 l'1.17* 36.33* Species X stafvation vs. larvae vs. Paramecium 4 3.10** 4.39*** *P < 0.0001,**P < 0.05.xx*P < 0.01.

0.0001) and between species (P < 0.0001). No sig- Development and sexual maturation nificant difference was found in number of larval Mate limitation has been shown to be unimpor- Aedes, Culex, and Anopheles killed by M. distinctus tant for cyclopoid copepods (Smyly 1970, White- (p : 0.12281' Table 6). However, larvae of Ae. al- house and Lewis 1973, Wyngaard and Chinnapa bopictus were preyed upon most by M. pehpeiensis 1982), except when male densities are low (Watras (P : O.O4O2)and M. viridis (P < 0.0001; Table 6). and Haney 1980). Williamson and Butler (1987), Mesocyclops pehpeiensis killed more Ae. albopic- when studying Diaptomus pallidus (a copepod re- tus than did M. viridis, which in turn killed more lated to those studied here), found no Ae. albopicrus than did M. distinctus (P < 0.0001; egg sac--car- rying females in the absence of males and deter- Table 6). When Cx. tritaeniorhynchus was exposed mined that high densities of males were associated to copepods, no significant difference was found in with high mating success. In the present study, number of larvae killed between the copepod spe- all 3 species produced a lst clutch, indicating that cies (P : O.5334; Table 6). When An. minimus was at least 1 mating event occurred in each case. The exposed, M. distinctus and M. viridis killed similar shortest period for 1st numbers of larvae (P : 0.9997). Their predation reproduction that was recorded for M. pehpeiensis is most on this mosquito was higher than that of M. peh- likely because it has a larger number of eggs. peiensis (P : 0.0041; Table 6). Regardless of egg and larval mortality, this species is likely to have more offspring compared to both M. distinctus and M. DISCUSSION viridis. In this study, progenies were mixed, another mechanism that Collection and systematics could increase mating chances in M. pehpeiensis. This may increase population size Macrocyclops distinctus, M. viridis, and M. peh- and thus allow higher encounter rates between the peiensis were collected from rice fields in Naga- both sexes in this species. saki, Kyushu Island, Japan, where they are common during the early summer. T}:re 2latter species were Fecundity and longevity more abundant in our samples and were easier to cultivate. The lst species was very rare and was The term reproduction in copepods has been recorded only from Yamagata Prefecture in Japan, used differently by various investigators. Hopkins although it is widespread throughout the world (1977) defined reproduction as clutch size, whereas (Guo 2000). The 2nd species has been recorded Hopp et al. (1997) considered it as the cumulative from various localities in Japan but not in Kvushu number of clutches produced in adult life. Environ- (Guo 2OO0). The 3rd species formerly was identi- mental factors have been shown to influence repro- fied as Mesocyclops leuckarti. It is rare, and is duction by affecting either clutch size or the found in Europe and Central Asia, but not in East frequency with which clutches are produced (Wil- Asia. This species was recorded as Mesocyclops liamson and Butler 1987). In our study, we found ruttneri from Miyazaki Prefecture (Hueda et al. that the small M. pehpeiensis was more productive 1997). Recently, Guo (2000) reidentified M. peh- in term of absolute number of eggs per clutch, peiensis and concluded that M. ruttneri is a syno- whereas in the long term, the larger species were nym of M. pehpeiensis. more productive in all treatments, including when

Table 3. Mean 1+ SE) longevity (in days) of various copepod species under different nutritional conditions.'

Starvation Mosquito larvae Paramecium Species Mean Range Range Range Macrocyclops distinctus 29.1 + 2.OAa 25-38 67.8 + 6.2 Ba 39-84 53.0t 5.6 Ba 40-:72 Megacyclops viridis 46.'7+ 2.5 Ab 42-64 78.6 + 4.'l Ba 49-93 71.8t I1.6 Ba 33-120 Mesocyclops pehpeiens is 21.2 + O.3Ac 20-22 23.5 + 0.9 Ab 21-27 34.3 + 1.0Ba 3l-3'7 'By analysis of vriance, values in the same column with the sme lowercase letter do not show a significant difference (P > 0.05) Those in the same row with the same capital letter do not show a significant difference (,P > 0.05). Mencn 2003 Pnev Cnorce BY CoPEPoDs 71

Table 4. Mean (t SE) number of clutches produced by various copepod species under different nutritional conditions.r

Starvation Mosquito larvae Paramecium

Species Range Range Mean Range 'l-11 Macrocyclops distinctus 1.5 + 0.2 Aa 1a l3.l ! 2.2 Ba 4-19 8.6 + 0.6 Ba Megacyclops viridis 1.4 + 0.2 Aa 1) l7.O + 1.4Ba 9-23 14.7+ 3.6 Ba 3-28 Mesocyc lops pe hpeie ns is 1.0 + 0.0 Aa 0-1 4.50 + 0.2 Bb 4-5 8.6 + 0.5 Ca 6-10

'By analysis of vmiance, values in the same column with the same lowercase letter do not show a significant difference (P > 0.05). Those in the same row with the same capital letter do not show a significant difference (P > 0.0-5).

there was less productivity under starvation condi- duction and increases the proportion of females that tions. Clearly, body size and larval feeding history do not bear eggs in copepod populations. are likely to affect egg production. Possibly, M. vir- Mesocyclops pehpeiensis did not reproduce at all idis and M. distinctus, which are larger that M. peh- in the absence of food, whereas M. distinctus and peiensis, store more nutrients for reproduction be- M. viridis did reproduce. In addition, M. pehpeien- cause evidence exists that small adult female sis had the same longevity whether unfed or reared copepods generally carry fewer eggs than do large with food. This demonstrates the high resistance to individuals (Hopkins 1977). starvation in this species. However, resistance to Size has been considered as an important trait for starvation was much higher in M. viridis and M. screening a predator copepod because larger spe- distinctus; this is likely to be related to their ability cies are better predators (Fryer 1957, Marten et al. to accumulate more energetic reserves and nutrients 1994). Therefore, if size is associated with a small compared to the small M. pehpeiensis. clutch size, as is the case with M. distinctus, the In these experiments, the females were kept potential for population increase may be poor. The without males but they produced eggs when food lower presence of M. distinctus compared M. peh- was available. This shows an ability of female co- peiensis and M. viridis in our samples in April 2000 pepods to store sperm and confirrns previous results and 2001, and the difficulties in cultivating M. dis- that argued that cyclopoid copepods do not need to tinctus in the laboratory, seem to confirm the poor remate to fertilize their eggs (Gilbert and William- population growth potential of this species (Dieng, son 1983, Williams and Butler 1987,Maier 1992). unpublished data). The females tested here produced fewer egg sacs when unfed and lived for a shorter period than Predation on mosquitoes those fed with either protozoans or mosquito lar- All 3 species were observed to feed on the dif- vae. This suggests that egg production depends on ferent mosquito larvae, with M. distinctus and M. food type and quantity, as already has been dem- viridis kllling fewer Ae. albopictus than M. peh- onstrated in other copepods (Hutchinson 1951, peiensis, which, however, killed fewer An. minimus. Checkley 1980, Hansen and Santer 1995, Hopp et According to Marten et al. (1994), a good copepod al. 1997). Such a loss of reproductive potential be- predator should kill more than 20 mosquito larvae cause of food has been well studied in copepods. daily. Thus, all 3 species are effective predators on Marshall and Orr (1955) postulated that under un- Ae. albopictus, but only M. distintus and M. viridis favorable conditions, copepod females could delay should be considered good predators on An. mini- egg laying or resorb egg material into the body. mus. Based on the performances of Mesocyclops Corkett and Mclaren (1969) reported that after a longis etus, M acrocyclops albidus, M egacyc lops la- period of starvation, copepod females lose their tipes, and Acanthocyclops vernalis against Culex ability to reproduce. Gilbert and Williamson (1983) quinquefoscialas Say (Marten et al. 1994, Marten indicated that scarcity of food retards oocyte pro- et al. 2000), the 3 species in the present study should be considered to be effective predators on Cx. tritaeniorhynchus. Table 5. Mean (+ interclutch period (in days) of SE) Differences clearly existed between the preferred various copepod speciesfed with Pararneciuminfusion.r prey of the different species, which are likely to be Number of due to both predator and prey characteristics. We clutches studied 3 copepod genera and 3 mosquito genera Species Mean pooled with different morphological features, as well as Macrocyclops distinctus 2.54 + 1.6a 46 different behaviors. Copepods are capable ofjudg- Megacyclops viridis 2.88+ 1.4a 95 ing prey speed (Kerfoot 1978) and attack only Me socyclops pehpeie nsis 2.O4+ 1.3b 4'7 moving prey (Williamson 1981, DeMott and Wat-

rBy analysis of vmiance, values in the same colum with the son 1991), indicating that their ability to detect prey sme letter do not show a significant difference (P > 0.05). depends on their activity but also on the prey char- 't2 JounNnr- oF THE AMERICAN MoseurTo CoNrnol Assocr,qnon Vor-.19, No. 1

Table 6. Mean (+ SE) numbersof lst-stage larvae of various mosquito speciesfound dead in containerswithout copepods(controls) and in containerswith copepods.l

Copepod species Aedes albopictus Culex tritaeniorhynchus Anopheles minimus Macrocyc lops distinc tus 20.8 + 1.4Aa 18.1+ 1.5Aa 23.2+ 1.9Aa Megacyclops viridis 27.3+ 1.7Ab 20.6+ 1.6Aa 23.1+ 2.1Aa Mesocyclops pehpe iensis 34.9 + 1.7Ac 2l.O + 2.7Aa 14.8+ 1.7Ab Control (no copepod) o.94 + O.2d 1.6+ 0.4b 9.6 + 0.8 b rBy malysis of varimce, values in the same column and with the sme lowercase letter do not show a significant difference (p > 0.05). Those in the sme row md with the same capital letter do not show a significant difference (P > 0.05). Lowercase letters are for the compaisons between control and treated containers, whereas capital letters re for the compuisons between copepod species.

acteristics (Kerfoot 1978). Mesocyclops sp. have umu Saita, Hu Xi-min, Junko Sakemoto, and Gi- been reported to have a high activity level with a thuto Joyce Nyambura for their moral and technical average swimming speed of 1.0-1.5 mm/sec (Wil- support. liamson 1981). Laboratory observations showed that M. pehpeiensis is more active than M. viridis, REFERENCES CITED whereas M. distinctus is a less powerful swimmer (Dieng, unpublished data). Andreadis TD. 1985. Experimental transmission of a mi- Larval Ae. albopictus were the most vulnerable crosporidian pathogen tiom mosquitoes to an alternate copepod to copepod predation, especially by M. pehpeiensis. host. Proc Natl Acad Sci USA 85:5574-5577. Brown MD, Kay BH, Hendrikz JK. 1991. Evaluation Analysis of larval movement with high-speed pho- of Austrafian Mesocyclops (Cyclopoida: Copepoda) for tography has shown that Aedes species are very ac- mosquito control. J Med Entomol 28:618-623. tive (Natchigall 1965). This behavior may increase Checkley DM Jr. 1980. The egg production of a marine the amount of water disturbance and hence the sig- pfanktonic copepod in relation to its food supply. Lim- nal to the attacking copepods. In a related study, nol Oceanogr 25 :430-436. Sih (1986) showed that when a single predarory Corkett CJ, Mclaren lA. 1969. Egg production and oil Notonecta was present, larval Culex pipiens (L.) storage by the copepod Pseudocalanus in the labora- reduced their movementby 79.5Vo and their occu- Iory. J Exp Mar Biol Ecol 3:9O-105. DeMott pancy of the center by 85.l%o (the corresponding WR, Watson MD. 1991. Remote detection of algae by copepods: responses to algal size, odors reductions for Aedes aegypti (L.), which is related and motility. J Plankton Res 13:1203-1222. to Ae. albopictus, were 15.5Vo and l8.3%o,respec- Enright WJ, Hennessey TN. 1987. Growth of paramecium tively). Culex pilosus (Dyar and Knab), another tetraurelia in bacterized, monoxenic cultures. J proto- species related to Cx. tritaeniorhynchus, moves in- zool 34:.137-142. frequently (Strickman 1989). Low motilitv may re- Frederici BA. 1980. Production of the mosquito-parasitic duce predation by minimizing detectability and this fungts Coelomyces dodgei through synchronized infec- factor may explain why Aedes was the most vul- tion and growth of the intermediate copepod host Acan- nerable in these studies. The inefficiency against thocyc lops vernalis. Entomophaga 25:2O9-217 . Fryer G. 1957. The food Cx. tritaeniorhynchus also could be due to the bris- of some freshwater cyclopoid copepods and its ecological tles on larval Culex, which may significance. J Anim Ecol increase the ap- 26:263-286. parent size of the larvae and therefore prevent their Gilbert JJ, Williamson CE. 1983. Sexual dimorphism in consumption (Marten et al. 1994). Low locomotion zooplankton (Copepoda. Cladocera, and Rotifera). and surface-dwelling behaviors of Anopheles sp. Annu Rev Ecol Syst 14:1-33. (Jones 1954, Strickman 1989) may minimize en- Guo X. 2000. A redescription of Mesocyclops pehpeiensis counter frequency with copepods, aiding greatly to Hu, 1943 and notes on Mesocyclops ruttneri Kiefer, their escape efficiency and reducing the efficacy of 1981 (Copepoda, Cyclopidae). Hydrobiologia 418:33- copepods as biocontrol agents on these species. 43. Hansen AM, Santer B. This work suggests the importance of an ecolog- 1995. The influence of food re- sources on the development, survival and reproduction ical approach to the study of potential biological of the two cyclopoid copepods: Cyclops vicinus and control agents, especially study of their reproduc- Mesocyclops leuckarti (Claus). J Plankton Res l7:631- tive potential, a key factor for survival in prey hab- 646. itats. Hill LL, Coker RE. 1930. Observation on mating habits of Cycktps. J Elisha Mitchell Soc. 45:2O6-22O. Hopkins CCE. 1977. The relationship between maternal ACKNOWLEDGMENTS body size and clutch size, development time and egg We thank Gerald Gerry Marten, Greg Thompson, mortality in Euchaeta norvegica (Copepoda: Calanoida) from Loch Etive, Scotland. Mar (JK Janet Reid, Hiroshi Hueda, and Steven Juliano for J Assoc 57:723- I J-)- their helpful suggestions and advice. We also thank Hopp U, Maier G, Bleher R. 1997. Reproduction and lon- Mayumi Koura Dieng, Niamey Dia, Hio Dieng, gevity of five species of planktonic cyclopoid copepods Masako Ota, Takesue Atsuhide, Ronald Morales, reared on different diets: a comparative studv. Fresy'r- Emiko Urakawa, Maiko Hasegawa (Gakkai), Sus- water Biol 38:289-300. '73 MencH 2003 Pnsv Cnotcg gy Copspoos

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