Journal of the American Contol Association, 12(3):414_420,1996 Copyright O 1996 by the American Association,Inc.

EVALUATION OF ASPERICORNIS (: ) AND TOXORHYN C H ITE S SP EC I O SUSAS INTEGRATED PREDATORS OF MOSQUITOES IN TIRE HABITATS IN QUEENSLAND

MICHAEL D. BROWN,I JOAN K. I{ENDRIKZ,' JACK G. GREENWOODT aNn BRIAN H. KAY'

ABSTRACT, This study addressed biological control of peridomestic Aedes notoscriptas, known to be a highly effective colonizer of tire habitats and a possible vector of Ross River virus. A laboratory trial of the compatibility of the predators Mesocyclops aspericomi,s and Toxorhynchites speciosus in small container habitats showed that 4th-instar Tx. speciosus did not significantly affect M. aspericornis rnor- tality. Introduced M. aspericornis and naturally occuring Tx. speciosus were found to form a compatible predator pair for reduction of larval Ae. notoscriptus and populations in tire habitats. Over 22 months of field survey, 97Vo of tires without predators contained mosquito larvae, at a median density of 43 larvae/liter. By companson, Sl%o of tires containing both predator held mosquito larvae at a median density of 4 larvae/liter. Predation by Tx. speciosu.s persisted for the duration of the study. The inability of the Lake Kurwongbah strain of M. aspericornis to tolerate temperatures of <10"C, which are prevalent in Brisbane during winter, resulted in a failure to deliver persistent reduction of mosquitoes in tires. The temperature-dependent population characteristics of M. aspericomis emphasize the long-recognized importance of matching a biological control candidate's physiological requirements to the environment in which control is sousht.

INTRODUCTION poid in tires has also been noted by Riviere (1985), Riviere et al. (1986), and Marten In Australia, as in much of the world, dis- (1990a). These carded tires are a threat to public health. Exotic observations are encouraging, as practice, vectors of disease such as (Linn.) in field the degree of control achieved (Frank 1981, Barker-Hudson et al. 1988), and by Toxorhynchites spp. alone has been disap- Aedes albopicrus (Skuse) (Hawley 1988) are be- pointingly low (Mogi et al. 1985, Pillai 1985, coming increasingly prevalent in tires despite Annis et al. 1989). warnings from public health authorities. A population of Much research has been aimed at utilizing the (Daday) from Lake Kurwongbah (27"15'5, inherent predatory behavior of cyclopoid cope- 152'58'E) in northeastern Australia was found pods and Toxorhynchites mosquitoes for the bi- to be more effective than 6 other species of na- ological control of insect vectors inhabiting con- tive Mesocyclops for killing Ae. aegypti and Cu- tainer habitats (Laird 1988). In the field, various lex quinquefasciatus Say in artiflcial containers species of cyclopoids have produced a high level (Brown et al. 1991). It was also the most fecund of control of Aedes mosquitoes, in a variety of Mesocyclops species evaluated, and survived at natural and artificial containers (Riviere et al. water temperatures similar to a subtropical Aus- 1987; Marten 1990a, 1990b). In New Orleans, tralian winter. Therefore, this warranted M ac ro cy c lo p s al b idu s (Jurine) and M es o cy c lop s investigation in subtropical northeastern Austra- longisetus (Thiebaud) were the most effective lia as a biological control agent for mosquitoes predators of Ae. albopictus in discarded tires breeding and developing in tire habitats. over a l-year period (Marten 1990a). In Brisbane (27"28'5, 153'Ol'E), Aedes no- In a study of habitats in which mosquitoes and toscriptus (Skuse) (a suspected vector of Ross copepods naturally coexist, Toxorhynchites ru- River virus causing epidemic polyarthritis [Wat- (Dyar tilus septentrionalis and Knab) was found son, Ritchie, and Kay, unpublished datal) and with number in association a of cyclopoid spe- Cx. quinquefasciatus (a proven filaria vector cies in tires (Nasci et al. 1987). The cohabitation [Boreham and Marks 1986]), commonly inhabit and compatibility of Toxorhynchites with cyclo- discarded tires. Larvae of the large larvivorous and nonhematophagous Toxorhynchites specio- 'Queensland Institute of Medical Research, Royal sas (Skuse) are also not uncommon in this hab- Brisbane Hospital P. O., Brisbane, QLD 4029, Austra- itat type (Marks 1982). This naturally occurring lia. 2 assemblage of mosquito species provided an ide- Faculty of Science, University of Queensland, St. al opportunity to study both the efficiency with Lucia, Brisbane, QLD 4067, Australia. 3 Department of Zoology, University of Queensland, which M. aspericornis reduces Aedes and Culex St. Lucia, Brisbane, QLD 4067, Australia. larvae in tires, and the compatibility of the co- Serrrunen 1996 MEsocycLops AND ToxoRHyNcHffES: IN-TEcRATEDPneo,qtons 415 pepod with Toxorhynchites larvae as integrated 0l) from which combinations of these categories control agents. for prey (Ae. notoscriptus and Cx. quinquefos' Accordingly, a small-scale trial was initiated ciatus) and predators (M. aspericornis and Tx. in which populations of each species were mon- speciosus) were derived. Chi-square tests of itored over 22 months, and the control efficacy Fisher's exact test (in the case of small expected of the 2 predators was gauged according to sea- frequencies) were applied to cross-classification son. The goal of this study was the delivery of tables involving these combinations and any a long-term, self-sustaining, inexpensive method 2-group factors of interest. The primary cate- of control. In addition to field assessments, a gories of interest in the hypotheses were tires laboratory compatibility trial of M. aspericornis where there were no mosquitoes (none) com- and 4th-instar Tx. speciosus in small container pared with tires where mosquitoes were present; habitats was conducted. and tires where there were no predators (none) compared with tires where predators were pres- ent. MATERIALS AND METHODS 2) For those tires where mosquitoes were Study sile: The study was conducted in a present, mosquito prey counts were analyzed wooded undisturbed section of the Queensland with respect to any 2-group factors of interest, Institute of Medical Research grounds, Brisbane. using the Wilcoxon-Mann-Whitney U-test. This Nine standard car tires, selected for inoculation test is independent of the fact that the distribu- with M. aspericornis, were iuranged into 3 tions are J-shaped and only assumes that types groups of 3. Two groups of 3 tires, to be used of probability distributions are similar. The test as untreated controls, were placed approximately statistic involves rank transformation of counts 5 m apart, and lO m from the treated tire group. and evaluates the probability distributions of the Four liters of tap water and a sediment of leaves groups and whether the 2-group factors have and twigs were introduced into each tire. The similar locations (I/n) or different locations (I1,). tires were left undisturbed for 2 wk prior to in- As the distribution was J-shaped, median counts oculation, thus allowing time for colonization by were used in place of averages. the indigenous mosquito fauna and the break- The data were divided into 3 summer and 2 down of chlorine to levels nontoxic to M. as- winter seasons and analyzed on the basis of wa- pericornis (Brown et al. 1994). ter temperature groupings as follows: summer Inoculation and sampling.' In January 1990, was defined as having water temperatures 5 gravid M. aspericornis were introduced into >15'C, and winter, temperatures s15"C. Anal- each tire via 20-ml plastic tubes to give a dosage ysis of copepod predation efficacy above and be- of 1.25 copepodsniter. The inoculum was col- low l5'C was of interest as this is the temper- lected from a 2,0ooliter culture tank. Oviposi- ature at which Brown et al. (1991) found M. tion in the tires by naturally occurring Tx. spe- aspericornis to exhibit reduced activity. Month- ciosus made artificial introduction and manipu- ly averages were expressed as means (range) lation of this predator unnecessary. Every 14 and seasonal averages were expressed as medi- days, copepods and mosquitoes in each tire were ans. Statistical Analysis System software (SAS sampled, and water temperature recorded for 22 Institute 1988) was used for all computations. months. A lliter sample was taken from the Laboratory trial of M. aspericornis and Tx. bottom of each tire by sweeping a 5 X lO-cm- speciosus compatibility.' The compatibility of aperture net of lo0-pm mesh a distance of ap- large predacious 4th-instar Toxorhynchites lar- proximately 2O cm. The contents of each sample vae and M. aspericornis at 2 and lO individuals were emptied into a white tray for counting and per liter, respectively, was studied in three 3-liter mosquitoes identified according to Marks tin cans. Three cans containing 10 copepods/liter (1982). Once counted, the sample was returned without Tx. speciosus were used as controls. The to the tire, and distilled water added to return trial was run for 72 h. with the numbers of sur- the volume to 4 liters. Copepod identity was pe- viving copepods and mosquitoes counted every riodically verified according to Van de Velde 12 h. (1984). All sampling was completed between In order to approximate field conditions where 0800 and l20O h. alternative food sources are available. 40O ml of Analyses of data: The probability distribu- Chlorella suspension and 200 ml of protozoan tions of all species sampled were J-shaped (an culture were provided in each can. The proto- index of homogeneity or relative diversity [Pie- zoan culture consisted of a mixed Euglena, Par- lou 19661). In light of these distributions, 2 ap- amecium, and rotifer fauna. Harper's powdered proaches to analyses were used: dog food (5 pg/can) was added as larval mos- l) Analysis of binary variables consisting of quito food. Distilled water was added to main- 2 classes (absent [count : 0]; present [count ) tain the volume at 2 liters. A lid was fitted to 416 JounNnl oR rrm AvenrcaN Moseurro CoNTRoL AssoclATroN VoL. 12, No. 3

cover 8O7o of the top to simulate an enclosed and a mean density of 1.5 larvae/liter in the sec- container habitat, and the trial was conducted at ond winter. 25"C, a common summer temperature of con- Prey mosquito population density character- tainer habitats in southeastem Queensland (Jen- istics: l) Aedes notoscriptus: This was the first nings et al. 1994). of the prey species to colonize the tires. Two Differences in survival of M. aspericornis in weeks after the tires had been filled with watel the To xo r hy nc hit es and,M es o cy c lop s containers, and on the day M. aspericornis was introduced and the Mesocyclops only (control) containers, into the selected tires, Ae. notoscriptus numbers were compared using Kaplan-Meir survival had reached a density of 4 (range O-9) and 3l curves and the log-rank test statistic (Kalbfleisch (range 7-27O) larvae/liter in the treatment and and Prentice 1980). control tires, respectively (Fig. l). From Febru- ary to May 1990 in the treated tires, larval den- (range RESULTS sities varied between 2 1-3) and 2 (range O-4) larvaetiter, and the median density in this Predator population density characteristics: first summer season was 2 larvae/liter. During l) Mesocyclops aspericornis.. During the first l2 this period, densities varied between 47 (range months (1990), the number of copepods present 12-l9O) and 5 (range l-74) larvaetiter in the in the treated tires was closely related to tem- untreated tires, with a median of 30 larvae/liter. perature (Fig. l). Following introduction into the The 2 medians were significantly different (P < tires, the numbers of copepods increased expo- 0.0001). In July, at a temperature of l4oC, when nentially, reaching a mean density of 24 (range copepod numbers were reduced to a mean den- 8-76) copepods/liter after 4 wk. From February sity of 2 (range 0-4) copepods/liter, 13 (range to May, when temperatures were above l5oC, an 5-33) larvaefliter was recorded in the treated equilibrium density of approximately 18 (range tires. After 12 months of study, densities of 3 6-35) copepods/liter was maintained. At tem- (range 0-9) and 19 (8-60) larvaefliter were re- peratures below l5'C (May-August), a copepod corded in the treated and untreated tires, respec- density of approximately 2 (range 0-3) cope- tively. At the conclusion of the study, 7 (range pods/liter was maintained. With increased tem- 1-13) and 79 (range 35-100) larvae/liter were perature from August 1990 to March 1991, co- sampled from the treated and untreated tires, re- pepod densities varied between 23 (range 18- spectively (Fig. l). Consistently, the median 28) and lO (range 3-28) copepods/liter, respec- densities (seasonal averages expressed as medi- tively. ans) in the treated tires were significantly lower The median densities were 9, 2, and 23 co- than in the control tires (P < 0.005), with overall pepods/liter during the first 3 seasons. The in- medians of 9.5 larvae/liter in the treated tires crease in density between the first and second and 3l larvae/liter in the control tires. summer seasonswas significant (P : 0.02). The 2) Culex quinquefosciatus: Culex quinquefas- numbers then decreased with temperature to O ciatus was first sampled 2.5 months after the copepods/liter by May 1991. From May ro No- study was initiated, at a density of I (range 0- vember, no copepods were recovered. At the 2) larva/liter. Larval numbers then oscillated in- conclusion of the study, 2 of these tires con- dependently of temperature in both the treated tarned M. aspericornis at densities of 1 and 6 and untreated tires for the remainder of the copepods/liter. study. A maximum density of 25 larvaetiter was 2) Toxorhynchites speciostrs.. Maximum den- recorded in August and September l99O in the sities of 3 (range 1-5) and 4 (range 2-6) Tx. untreated tires, when treated densities were 6 speciosus larvae/liter were recorded in May and (range O-12) larvae/liter. For the last 2 months February 1990, for treated and untreated tires, of the study, no Culex were sampled from either respectively (Fig. l). From August to November the treated or untreated tires. In terms of mos- in both 1990 and 1991, numbers were reduced. quito prey species composition in the tires dur- The percentage of tires containing only Toxo- ing the 22 months of study, 5O.9Voof the sam- rhynchites larvae reached a maximum at 427o in ples contained only Ae. notoscriptus, 4.5Vo only the second winter, by which time M. aspericor- Cx. quinquefasciatus, and 23.6Vo both species. nis had disappeared. The percentage of tires con- Analysis of control efficacy: During the first taining only Tx. speciosus differed significantly summer, 68Vo of the tires in which the only con- over the 5 seasons (P < 0.04). Using a chi- tained predator was M. aspericomis also con- square goodness-of-fit test, and adjusting for the tained mosquito larvae (Table l). In these tires, number of tires and their location, total Toxo- the mosquito prey (both Aedes and Culex spe- rhynchites larval counts also varied significantly cies) were sampled at a low median density of over the seasons (P : O.O2),with a mean density 3 larvae/liter. In tires in which the only predator of 2.5 Toxorhynchiteslltter in the first summer, was Zr. speciosus, 6'7Vo contained mosquito lar- Sep,reNasrn1996 M nsocvc to ps x.to ToxonnvNcn rrps: INTEGRATEDPnEonrons 417

TREATEDTIRES UNTREATEDTIRES

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Fig. 1. Number of Mesocyclops aspericomis and larval mosquitoes in treated and untreated tires during 22 months of field study. Points for copepods and mosquitoes shown as mean of 9 and 6 tires for treated and untreated studies, respectively. vae, and these occurred at a median density of vaefliter, which was significantly different from 17.5 larvae/liter. In tires where both predators the above (P < 0.05). occurred, 49Vo contained mosquito larvae at a The second summer of the study was the last median density of 2 larvaetiter. In the absence period in which M. aspericornis exerted any of predators, 92Vo of tires contained mosquito mosquito control (Table l). Toxorhynchites spe- larvae at a higher median density of 45 lar- ciosus preyed on mosquito larvae (both Aedes 418 JounNel or rss AvnnrceN Mosqurro CoNrnol AssocrerroN VoL. 12,No.3

Table l. Summary of the effectiveness of Mesocyclops aspericornis and Toxorhynchites speciosus control of mosquitoes in tires over a Z}-month period. The presence of predators is compared with no predators in statistical tests.

Percentage of tires with prey mosquitoes and median mosquito numbers (n)' Jan.-Mav 1990 June-Aug. 1990 Sept. 1990-May l99l No predators 92Vo& 45 (23) 89Vo& 31 (25) 98Vo& 37 (60) Predators M. aspericornis 68Vo*& 3** (15) 75Vo& r4.5 (12) g4Vo**& 7** (3) Tx. speciosus 67Vo*& 17.5** (26) 89Vo& 12.5 (16) glVo** & l3** (46) Both predators 497o** & 2** (24) 94Vo& 7** (6) 3l,o** * ,.5** (12) rLevels of significance denoted as follows: * P < 0.05; ** P < 0.001, blank is nonsisnificant.

and Culex) for the duration of the study, and the Kurwongbah (Brisbane) and French Polynesia median numbers ranged between 12.5 and 22.5 died at 10'C. The low morning temperatures larvae/liter. recorded during the 1991 winter (12 -+ 2'C) Of the tires treated with M. aspericornis, only may have proved limiting. 67o contained copepods after 22 months of study Aedes notoscriptus was proven to be an op- (Table 2). With reduced numbers of M. asperi- portunistic colonizer of tire habitats. The speed cornis over time, and the oscillating density of with which this mosquito species invaded the Tx. speciosus, the percentage of tires containing tires, and the high larval densities that were predators decreased from 98Vo in the first sum- maintained throughout the summer and winter mer to 23Vo in the third summer (Table 2). seasons,indicate why this mosquito has so suc- Analysis showed that where M. aspericornis cessfully adapted to the peridomestic environ- was the only predator, 66Vo of tires had l0o7o ment in southern Queensland and New South elimination of Ae. notoscriptus, and this oc- Wales (Russell et al. 1984). The Tx. speciosus curred at copepod densities of >4 M. aspericor- larvae were if anything more common during nis[iter (Fig. 2). In contrast, with 7x. speciosus the cooler winter months and were entirely de- only, 6l%o of tires displayed 1007o elimination pendent on Ae. notoscriptus and Cx. quinque- of the prey, and these contained at least 2 Tx. fasciatus larval populations. As a consequence speciosusAiter. of their slow development time and greater Analysis of laboratory trial: There was no ev- food demands (May and Anderson 1979), they idence to suggest that the survival rates of M. never exceeded a mean density of4 larvae/liter. aspericornis were different in the presence or This study indicated that tire habitats, rather absence of 4th-instar Tx. speciosus (Xt : O.O, I than rainwater tanks (Lardeux 1992, Brown et df, P = 0.99) (Fie. 3). al. 1994), are suitable for M. aspericornis colo-

DISCUSSION Table 2. Percentage occurrence of predators The temperature-dependent population char- in tires treated with Mesocyclops aspericornis acteristics of M. aspericornis duing this study over a 22-month period. emphasize the importance of matching the Percentage of tires with physiological requirements of biocontrol can- predators for summers didates with the environment in which control (Sl-S3) and winters is sought. Although the M. aspericornis popu- (Wl and W2) lation was derived from a large south Queens- land lake, it seems that water temperatures in Predator sl wl s2 w2 s3 tires are subject to greater extremes because of M. aspericornis the smaller water volume. After an expected only 26 19 24 decline in copepod numbers during the second Toxorhynchites winter, the population failed to redevelop with speciosus only 392048r7 increased summer temperatures (Fig. l). In a Both predators 69252762 study of Mesocyclops population growth in re- Total percentage 98 53 7r 54 23 lation to temperature, Brown et al. (1991) No. of observations 83 46 ll9 54 45 found that M. aspericornis from both Lake Snrrerragln1996 M EsocvcLops AND ToxoRHyNcHITES: INtncRAreo Pneonrons

Table 1. Extended.

Percentage of tires with prey mosquitoes and median mosquito numbers (n)' Iune-Sept. l99l Sept.-Nov. 1991 All data rNVo & 44 (49) IOOVo& @ (60) 97Vo& 43 (217)

jgqo** * 7x* (60) 6gv"** u t2.5xx (26) 5OVo*& 22.5** (6) 73Vo** U 14** (12O) 5l7o** & 4** (55)

nization. In contrast to the lack of persistence of in tire habitats, their long-term performance, as copepods in rainwater tanks, M. aspericornis evidenced in this study, could be considered a maintained median densities of 9 and 23 cope- failure, as Ross River virus transmission is still pods/liter for 2 consecutive summers in tire hab- possible even with low mosquito numbers (Kay itats. The comparative levels of contained or- and Aaskov 1989). When the results of this ganic nutrients may provide an explanation for study are extrapolated theoretically to a large tire the contrasting results. Low food levels are a dump, with 5lVo of tires containing a median of major factor limiting Mesocyclops population 4 mosquito larvae (all data considered, Table l), growth in rainwater tanks (Jennings et al. 1994). significant adult mosquito production will still The thick substrate of leaves and organic matter occur. The continued abundance of Ae. notos- present in the bottom of the tires during this criptus through winter and the presence of Ross study would have provided a readily available River transmission (Hargreaves and Hall 1992) source of energy for primary (bacteria and fun- in the absence of known major vectors suggest gi), secondary (protozoa, rotifers), and tertiary that Ae, notoscriptus could be involved in urban (dipterous larvae) food production (Riviere transmission. Furthermore, less than total pre- 1985). Although we added detritus to our tires dation may increase adult mosquito fitness as a artificially, the levels were realistic in view of consequence of decreased intraspecific compe- field observations. tition for limited resources durine the larval Although M. aspericornis and Lr. speciosus stages (Ho et al. 1989). appear to be a compatible predator pair for use

(r) -^ Qt* ir .-_. CONTROL (M- ASPERICOFNIS ONLY) ge0 P < 0.0001 Q,n ^---^ TX. SPECIOSUSAND M, ASPERICOBNIS c q- o80 n =687 o |I o P70 ._. M.ASPERICOBNIS <30 o 5 zm f....f TX. SPECIOSUS u- v20

E E,o J tr F'o a,30 E. o Lo-N t. a ""'\g'-=..-...a-- s0 trul 10 o122436486072 tro T-...... HOURS bS Fig. 3. Percentage mortality of Mesocyclops as- '72 PREDATORS/ LITER pericomis from laboratory trials over h, at Toxo- rhynchites speciosus and Mesocyclops aspericornis Fig. 2. Optimal densities of Mesocyclops asperi, densities of 2 larvae and l0 copepods/liteq respective- cornis and, Toxorhynchites speciosuslliter for elimina- ly. Points for copepod mortality are shown as mean t tion of Aedes notoscriptus in tire habitats. SD of 3 replicates. l

JounNnLop rnE AusnrcAN Moseurro Covrnol AssocteloN Vol. 12.No. 3

ACKNOWLEDGMENTS mature Culicidae, pp. 466-484. In: M. Laird (ed.). The natural history of larval mosquito habitats. Ac- We thank L. Muir (Queensland Institute of ademic Press, New York. Medical Research IQIMRI) for manuscripr re- Lardeux, E J. R. 1992. Biological control ofculicidae view. T, Watson, P Ryan, and C. D. Jennings with the copepod Mesocyclops aspericornis and lar- (QIMR) contributed useful discussion and ad- vivorous fish (Poeciliidae) in a village of French vice. M. Shee (Zoology Department, University Polynesia. Med. Vet. Entomol. 6:9-15. Marks, E. N. 1982. An atlas of common of Queensland), K. Marshall, I. Fanning, and P Queensland mosquitoes. Institute of Medical Re- Gyte (QIMR) provided technical assistance. This Queensland search. Herston. Australia. study was funded by the National Health and Marten, G. G. l99oa. Evaluation of cyclopoid cope- Medical Research Council. Canberra. Australia. pods for Aedes albopicrus control in tires. J. Am. Mosq. Control Assoc. 6:681-688. Marten, G. C. 1990b. Elimination REf,'ERENCES CITED of Aedes albopictus from tire piles by introducing albidus Annis, B. J., K. A. Santijo, A. Soerto and S. Pranoto. (Copepoda, Cyclopidae). J. Am. Mosq. Control As- 1989. Suppression of larval Aedes aegypti popula- soc. 6:689-693. tions in household containers in Jakarta. Indonesia. May, R. M. and R. M. Anderson. 1979. Population through release of first-instar Toxorhynchites splen- biology of infectious diseases. Part 3. Nature 280: dens larvae. J. Am. Mosq. Control Assoc. 5:235- 455-46r. 238. Mogi, M., M. Horio, I. Miyagi and B. D. Cabrera. Barker-Hudson, P R., R. Jones and B. H. Kay. 1988. 1985. Succession, distribution, overcrowding and Categorization of domestic breeding habitats ofAe- predation in the aquatic community in aroid axils, des aegypti (Diptera: Culicidae) in north Queens- with special reference to mosquitoes, pp. 95-119. land, Australia. J. Med. Entomol. 25:178-182. In: L. P. Lounibos, J. R. 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