Ecological limitations on aquatic mosquito predator colonization in the urban environment

December, 2004 Journal of Vector Ecology 331

Ecological limitations on aquatic mosquito predator colonizationin the urban environment

John Carlson, Joseph Keating1, Charles M. Mbogo2, Samuel Kahindi2, and John C. Beier1

Department of Tropical Medicine, Tulane University, 1430 Tulane Avenue SL-17, New Orleans, LA 70112,U.S.A.

1Department of Epidemiology and Public Health, University of Miami School of Medicine, South Campus,12500 SW 152nd Street, Building B, Miami, Florida 33177, U.S.A.

2 Kenya Medical Research Institute (KEMRI), Centre for Geographic Medicine Research-Coast, P.O. Box 428,Kilifi, Kenya

Received April 5, 2004; Accepted 3 June 2004

ABSTRACT: Urban malaria cases are becoming common in Africa as more people move into cities andindustrialization proceeds. While many species of Anopheles mosquitoes vector malaria in rural areas, only a feware found within cities. The success of anthropophilic species in cities, such as members of the An. gambiaecomplex, may be explained by limitations on colonization by predator species in urban environments. Habitats thatare temporal or structurally simple have lower predator survivorship in a variety of ecosystems, but these have notbeen investigated previously in an urban area. Areas within and around the Kenyan coastal town of Malindi werepreviously sampled for the presence of standing water using a geographic sampling strategy with probabilityproportional to size sampling of planned well-drained, unplanned poorly-drained, planned poorly-drained, unplannedwell-drained, and peri-urban locations. Standing aquatic habitats in these areas were reassessed. During monthlysampling, presence/absence of mosquitoes and predator taxa were noted, as were ecological habitat variables:structural complexity and presence of water. Lambda statistics were calculated to associate predator guilds, habitattypes, location variables, and ecological variables. All predator guilds found in habitats were strongly associatedwith habitat type, as were the structural complexity and temporal nature of the habitats. Types of habitat wereheterogeneously distributed throughout Malindi, with swimming pools as a common habitat type in planned urbanareas and tire track pools a common habitat type in peri-urban areas of Malindi. Predator colonization of aquatichabitats in Malindi was strongly influenced by habitat type, and not associated with location characteristics. Ecologicalvariables were affected by the type of habitats, which are co-associated with planning and drainage in Malindi.While habitat types are distributed heterogeneously within Malindi, habitats with low predation pressure are availablefor mosquito colonization in both urban and peri-urban areas. The temporal, peri-urban tire track pools and thestructural simplicity of urban swimming pools may discourage predator colonization, thereby increasing theprobability of malaria vectors in these areas of Malindi. Future studies should evaluate habitats for use in malariasurveillance and experimentally test the effects of structural complexity and temporal nature of urban habitats onthe densities of mosquito larvae and their aquatic predators. Journal of Vector Ecology 29 (2): 331-339. 2004.

Keyword Index: Anopheles gambiae, predation, urban, Malindi.

INTRODUCTION

In Africa, where 90% of malaria cases are diagnosed,malaria parasites have followed the movements ofhumans into the industrializing cities (WHO 2000). Theendemic malaria transmission documented in Africancities requires the year-round presence of competentvector species, all of which belong to the mosquito genusAnopheles. There are more species of malaria vectorsfound in rural areas than in African cities. The factors

that limit the colonization of cities by some rural malariavectors may also present an obstacle to colonization ofcities by mosquito predators. In rural areas there is atremendous diversity of predators that prey on the aquaticmosquito larvae, reducing mosquito survivorship (Andisand Meek 1985). Thus, mosquitoes able to inhabit urbanenvironments may benefit from diminished predationpressure in cities.

Little is known about the ecology of urbanmosquitoes or the aquatic predators that help regulate

332 Journal of Vector Ecology December, 2004

larval population levels in urban areas of Africa.Mosquito larvae have been found in a variety of aquaticurban environments, including wells and other sourcesof drinking water, stagnant drainage systems, and otherdepressions resulting from human activities (Welch etal. 1989, Ijumba and Lindsay 2001, Marten et al. 1994,Marten et al. 2000, Robert et al. 1998). There are manyfactors that might limit predator colonization of the urbanenvironment, but these have yet to be explored.Documented insecticide resistance in mosquito speciesraises the concern that pesticide use leads to the selectiveremoval of mosquito predators from mosquito larvalhabitats, causing an increase in potential vectorpopulations (Roberts and Andre 1994, Oloo et al. 1996).A variety of toxic substances, such as lead, may lead toa similar phenomenon. However, human perturbationwithin the urban environment may also influence theecology of mosquitoes and their predators in more subtleways.

The structural complexity (amount of vegetation ordebris) in habitats and the age of temporal habitats(recurring, temporary habitats) have been shown toinfluence arthropod populations in a variety of naturaland agricultural environments (Finke and Denno 2002,Clark and Messina 1998, Rypstra et al. 1999, Yanoviak2001a, Yanoviak 2001b). A reduction in the structuralcomplexity of a habitat leads to an increase in intraguildpredation (predator-predator antagonism), therebydiminishing the predation pressure on prey species.Similarly, the frequency of drying out in aquatic temporalhabitats prevents progression of biological succession,thereby maintaining fewer predators in the habitat.Variations in the structural complexity of availablehabitats and the number of habitats that are temporalmay affect mosquito larvae densities and the distributionsof their aquatic predators in urban environments as well.“Sanitation” measures in urban sites decrease structuralcomplexity through removal of vegetation and debrisfrom ditches and water storage structures. Patterns ofwater use in cities promote temporal habitats bypromoting periodic drainage of aquatic habitats. Urbanpollutants may prohibit aquatic predator colonizationdirectly, or by eliminating plant life, thereby reducingstructural complexity. Once the ecological influences onpredator colonization in urban environments have beenidentified, informed policies can be developed for betterurban vector control.

Previous studies in Malindi, Kenya, by members ofour team (Keating et al. 2003) found that 93% ofAnopheles larval habitats were human-made. Theyfurther identified two potential variables associated withincreased larval habitats in urban environments: lack ofurban planning and the absence of drainage systems.

Additionally, peri-urban areas of Malindi were found tobe ecological extensions of the unplanned and poorly-drained urban areas, with numerous mosquito habitatsin these locations as well.

The specifics of how city planning and drainageaffect the ecology of mosquitoes are uncertain. Changesin planning and drainage may influence the structuralcomplexity and/or the temporal patterns of water sources,which can alter the ability of aquatic predators to colonizeand suppress urban mosquito larvae populations.Alternatively, urban planning and drainage may be co-associated with other variables (such as the types ofhabitat available) that are responsible for the spatial ortemporal distribution of Anopheles larvae within aquatichabitats. To test these alternate hypotheses,characteristics of the aquatic habitats were tested forassociation with the distribution of mosquito larvae andtheir aquatic predators.

MATERIALS AND METHODS

Study siteThe Kenyan coastal town of Malindi has been

described elsewhere (Macintyre et al. 2002, Keating etal. 2003). In 2001, major roadways, waterways, andlandmarks within Malindi were mapped. A series of 270meter by 270 meter grid cells overlaid on the map servedas the sampling frame. Grid cells were stratified intoplanned well-drained, planned poorly-drained,unplanned well-drained, unplanned poorly-drained, andperi-urban areas (Keating at al. 2003). A grid cell wasclassified as well-drained if engineered drainage systems,clear of debris or vegetation, were present; no standingwater was visible; or if located on a slope. Poorly-drainedgrid cells had no functional drainage systems or werelocated in depressions or valleys. The level of planningwas based on house spacing, road types and networks,community water sources, and access to utilities.Information contained in the 1999 census and DistrictDevelopment Report, as well as environmentaldescriptions from the field and topographical maps wereused to assist with the stratification process. Probabilityproportional-to-size sampling (PPS), based on thenumber of grid cells within each stratum, was used torandomly select 28 grid cells for entomological samplingand water body characterization.

Sampling and habitat characterizationUrban habitats were evaluated monthly for six mo

(June 2002- September 2002, January-March 2003).During each evaluation, habitats were scored ascontaining water or being dry. For those containingwater, vertebrates and invertebrates were captured by


aquatic net and by dipping. Specimens were identifiedas precisely as possible under field conditions: VertebrataOrders, Odonata Suborders, Hemiptera and ColeopteraFamilies, and Culicidae (Diptera) genera (Merritt andCummins 1996, Huang 2001). Only presence/absencedata were collected due to the logistical difficulties incalculating densities in the variety of urban habitats.When possible, the insect predators were furthercategorized into guilds based upon locomotion: striders(surface skating predators), divers (submerged,swimming predators), and crawlers (submerged, crawlingpredators)(Merritt and Cummins 1996). Habitats weredefined as structurally complex if they containedvegetation and/or debris throughout, and structurallysimple if vegetation and/or debris was absent or only atthe margins of the habitat. Habitats were assumed to bepermanent unless they did not contain water during atleast one of the six observations.

Data analysisData management and calculations were performed

using SPSS 11.0 (SPSS Inc, Chicago, IL). Uponcompletion of data collection, habitats were scored basedon presence or absence of individual taxa and guildsduring the entire course of the study. Lambda values weregenerated to test a series of asymmetric nominal-by-nominal associations with defined independent anddependent variables. Tests were performed forassociations among habitat characteristics (type,structural complexity, and temporal vs. permanent),habitat location (urban vs. peri-urban location, presenceof urban planning, quality of drainage), and the presenceof predator taxa or guilds (striders, divers, crawlers).Lambda values and asymptotic standard errors were usedto generate approximate T-values for purposes ofdetermining statistical significance with a 95%confidence level.

RESULTS

Habitat typesThere were 29 different stagnant aquatic habitats

falling into eight specific types that were evaluated inand around Malindi (Table 1). All but one of the habitats(a stream pool present only once) were human-made(96.6%). Of the human-made habitats, twelve (42.9%)were luxury-related habitats (i.e., swimming pools,ornamental pools, and ornamental pots), six (21.4%) hadon-going functions (i.e., drainage ditches, waterreservoirs), and ten (35.7%) were due to poormaintenance (i.e., tire track pools in unpaved roads,abandoned tires). Habitats ranged from being presentonly once throughout the course of the investigation (i.e.,

a stream pool in peri-urban Malindi) to being presentduring each of the investigations (i.e., swimming pools).There was a statistically significant, very strongassociation between the type of habitat and whether itwas permanent or temporal (Lambda = 0.929, P < 0.001),and a strong, but statistically insignificant associationbetween type of habitat and whether the habitat wasstructurally simple or complex (Lambda = 0.667, P =0.087).

Permanent habitatsOf the 29 habitats evaluated, 14 (48.3%) were

permanent. Of these, 78.6% were structurally simple.All of the seven swimming pools had low structuralcomplexity due to periodic cleanings for use by tourists.Drinking water reservoirs were both deep and covered,which prevented the growth of vegetation. Oneornamental pool was a fishpond, and contained novegetation due to daily disturbances by domesticatedgeese and large fish. However, two of the ornamentalpools (one aquatic garden and an abandoned bathtub)and one group of ornamental pots contained highamounts of vegetation due to deliberate cultivation ofvegetation.

Temporal habitatsThere were 15 temporal habitats, of which 12

(80.0%) were structurally simple. Seven groups of tiretrack pools (depressions caused by vehicles on unpavedroads that filled with rain) were evaluated. The regulardisturbance of these habitats by vehicles prevented thegrowth of vegetation within them. The water withingroups of discarded tires contained no vegetation, withsome habitats possessing minimal amounts of detritus.A group of ornamental containers in an enclosedbackyard periodically filled with rainwater and did notcontain vegetation or debris. A single stream pool waspresent only once throughout the period of investigationand did not contain vegetation or debris. Three drainageditches (i.e., one road-side ditch, one slaughter housedrainage ditch, and one drainage ditch next to a house)were the only three temporal habitats with structuralcomplexity, consisting of terrestrial grasses. Theslaughter house drainage ditch was filled by water usedin the operation of the slaughter house and was manuallyemptied periodically as a public health measure. Theremaining two habitats filled with rainwater and emptiedover time without human intervention.

Biota of habitatsDuring this investigation, mosquitoes belonging to

four genera were found: Anopheles, Culex, Aedes, andToxorhynchites. While Culex and Aedes larvae were


Tabl

e 1.

Dis

tribu

tion,

cha

ract

eris

tics,

and

biot

a of

hab

itat t

ypes

in M

alin

di, K

enya

.

Mos

quito

es

Stri

ders

C

raw

lers

D

iver

s O

ther

s

Hab

itat t

ype

Urb

an

plan

ning

Num

ber

of

habi

tats

Tem

pora

l vs.

Perm

anen

t St

ruct

ural

co

mpl

exity

Anopheles

Aedes

Culex

Toxorhynchites

Gerrid

Hydrometrid

Veliid

Damselfly

Dragonfly

Naucorid

Beetle

Notonectid

Pleid

Frog

Tadpole

Fish

Crab

Swim

min

g po

ols

Plan

ned

7 Pe

rman

ent

Sim

ple

+ +

+

+ +

+ +

+ +

+ +

+ +

+

Wat

er r

eser

voir

s Pl

anne

d 3

Perm

anen

t Si

mpl

e

+ +

+

+

Plan

ned

1 Pe

rman

ent

Sim

ple

+

O

rnam

enta

l poo

ls Pl

anne

d 2

Perm

anen

t C

ompl

ex

+

+

+

+

+

Plan

ned

1 Pe

rman

ent

Com

plex

+ +

Orn

amen

tal p

ots

Plan

ned

1 Te

mpo

ral

Sim

ple

+

Dra

inag

e di

tche

s U

npla

nned

3

Tem

pora

l C

ompl

ex

+

+

+ +

+ +

+

+ +

+

+

Unp

lann

ed

1 Te

mpo

ral

Sim

ple

+

Ti

res

Peri-

urba

n 2

Tem

pora

l Si

mpl

e

+

+

Plan

ned

2 Te

mpo

ral

Sim

ple

+

+

Ti

re tr

acks

Pe

ri-ur

ban

5 Te

mpo

ral

Sim

ple

+

+ +

+

+ +

+

+

Stre

am p

ool

Peri-

urba

n 1

Tem

pora

l Si

mpl

e

+


collected on numerous occasions in multiple habitattypes, Anopheles larvae were found only in four habitats:in two different swimming pools, a drainage ditch, and agroup of tire track pools. Toxorhynchites larvae werealso rare, being found only twice in a single domesticwater reservoir. All Anopheles larvae found belongedto the An. gambiae complex.

The surface predators found in Malindi belongedto three Heteropteran families: Gerridae (waterstriders),Hydrometridae (watermeasurers), and Veliidae (broad-shouldered waterstriders). Gerrids were present in allseven (100%) of the swimming pools, hydrometrids insix (85.7%), and veliids were present in three (42.9%).Surface predators were present in five of the seven groupsof tire track pools (71.4%): three occupied by gerrids,one by gerrids and hydrometrids, and one by veliids.Veliids were found in all three drinking water reservoirsand an ornamental ground pool. Aside from this, nosurface predators were present in ornamental habitats ortires. Predictions of the presence of surface striders couldbe improved by knowing habitat type (Lambda = 0.571,P = 0.031; Table 2).

Crawling predators present in Malindi were nymphalOdonata (damselflies and dragonflies) and theNaucoridae (Heteroptera). Damselflies were found in oneswimming pool and a drainage ditch. Dragonflies werepresent in all seven swimming pools, the drainage ditchof the slaughter house, and two of the three ornamentalpools. Naucorids were only found in two swimmingpools. Predictions of the presence of crawling predators

could be improved by knowing habitat type (Lambda =0.800, P = 0.004; Table 2).

Diving predators belonged to the heteropteranfamilies Notonectidae and Pleidae, and the coleopteranfamily Dytiscidae. Dytiscids were present in six of theseven groups of tire track pools (85.7%), as either larvaeor adults, all seven (100%) of the swimming pools, theslaughter house drainage, one roadside ditch, (66.7% ofdrainage ditches), and one tire (33.3% of tire groups).Pleids were found in one tire track pool (14.3%) andthree swimming pools (42.9%). Notonectids were foundin three tire track pools (42.9%), all seven swimmingpools (100%), and one roadside ditch (33.3%).Predictions of the presence of diving predators could beimproved by knowing habitat type (Lambda = 0.833, P= 0.001; Table 2).

While adult frogs were found in only two (28.6%)of the swimming pools, tadpoles were found in the streampool (100%), three tire tracks (42.9%), one swimmingpool (14.3%), one ornamental pool (33.3%), and oneroadside ditch (33.3%). Crabs were found once, in aroadside ditch following heavy rains. Fish were foundonly in a single ornamental pool, where they were presentduring each evaluation.

Distribution of habitat types in MalindiHabitat types were heterogeneously distributed

throughout Malindi (Table 3). For example, six of theswimming pools (85.7%) and three of the ornamentalhabitats (60.0%) were in planned, well-drained areas of

Table 2. Associations of predator taxa and guilds (dependent variable) with aquatic habitat type (independent variable) in Malindi.

Predator Lambda Asymptotic St Error a Approx. T b Approx. P-value

Strider guild 0.571 0.187 2.154 0.031 d Gerrids 0.636 0.145 3.038 0.002 d Hydrometrids 0.625 0.203 2.018 0.044 d Veliids 0.125 0.203 0.581 0.561 . Diver guild 0.833 0.118 3.420 0.001 d Pleids 0.000 0.000 c c Notonectids 0.636 0.145 3.038 0.002 d Dytiscid 0.833 0.118 3.420 0.001 d Crawler guild 0.800 0.141 2.866 0.004 d Dragonfly larvae 0.800 0.141 2.866 0.004 d Damselfly larvae 0.000 0.000 c c Naucorids 0.000 0.000 c c

a) Not assuming the null hypothesis. b) Using the asymptotic standard error assuming the null hypothesis. c) Cannot be computed because the asymptotic standard error equals zero. d) Significant at 0.05 level.


Malindi. In contrast, peri-urban areas contained fivegroups of tire track pools (71.4%) and two groups ofabandoned tires (66.7%). Habitat type was moreassociated with the stratum within which it was located(Lambda = 0.409, P = 0.005) than with any individualcomponent of the stratum: planning (Lambda = 0.318, P= 0.022), drainage (Lambda = 0.273, P = 0.043), or urbanlocation (Lambda = 0.227, P = 0.080).

Association of predator guild presence with locationcharacteristics

Habitat type had a large, statistically significantassociation with presence of predator guilds whileurbanization, planning, drainage, or stratum (a compositeof urbanization, planning, and drainage) did not (Table4). Although not statistically significant, the position ofan aquatic habitat within an individual city stratum(planned, well-drained urban area, planned, poorly-drained urban area, unplanned well-drained urban area,unplanned poorly-drained urban area, or peri-urban area)had a large impact on the presence of striders (Lambda= 0.429, P = 0.118) and crawlers (Lambda = 0.500, P =0.116), while divers were not affected (Lambda = 0.250,P = 0.246).

Association of ecological variables with locationcharacteristics

The temporal nature of a habitat had a strongerassociation with habitat type (Lambda = 0.929, P <0.001) than with strata (Lambda = 0.786, P = 0.002), or

any component location variable. Likewise, habitatcomplexity was more associated with habitat type(Lambda = 0.667, P = 0.087) than with strata (Lambda= 0.333, P = 0.143) or any component location variable(Table 5).

DISCUSSION

Limitations on predator colonization in the urbanenvironment

The results of our study indicate that there areecological limitations on the colonization of the urbanenvironment by aquatic predators. Distribution ofpredators is heterogeneous due to the heterogeneousdistribution of habitat types available. Habitat typepredicts colonization by diving predators and crawlingpredators over 80% of the time, with strider colonizationpredicted 57% of the time. Avoidance of certain habitattypes may apply to all predators (i.e., no predators foundin ornamental containers, thereby limiting colonizationin planned urban areas), guild-specific (i.e., crawlersabsent from tire track pools, thereby limiting colonizationof habitats in the peri-urban areas), or taxon-specific (i.e.,pleids absent from drainage ditches, thereby limitingcolonization in unplanned urban areas).

Earlier work in Malindi found an effect, albeitstatistically insignificant, of urban planning and thequality of drainage on the abundance of larvalhabitats(Keating et al. 2003). The results of this studysuggest that these variables do not affect the distribution

Table 3. Habitat types, mosquito genera, and predator taxa present within areas of Malindi stratified by urban planning, quality of drainage, and urbanization.

Location characteristics

# of aquatic habitats

Types of habitat Mosquitoes present

# of predator taxa present

Swimming pools (6) An, Cx, Ae 11 Tire tracks (1) 0 1 (dytiscids) Water reservoir (1) Ae, Cx, Tx 2 (Tx, veliids)

Well-drained 11

Ornamental pools/ containers (3) Ae, Cx 2 (veliids, dytiscids) Swimming pools (1) An, Cx 6 Water reservoir (2) Ae 1 (veliids) Ornamental pools/ containers (2) Ae 1 (fish)

Planned

Poorly-drained 6

Tire tracks (1) 0 2 (dytiscids, notonectids)

Well-drained 1 Tires (1) Ae 0

Slaughter house drainage (1) Cx 5 Unplanned

Poorly-drained 2 Road ditch (1) An 5

Tire tracks (5 groups) An 7 Tires (2 locations) Ae 1 (dytiscids) House drainage (1) 0 0 Peri-urban 9

Steam pool (1) 0 1 (tadpoles) An= Anopheles larvae, Cx= Culex larvae, Ae= Aedes larvae, Tx= Toxorhynchites larvae.


Table 4. Association of predator guild presence with habitat type and location characteristics within Malindi, Kenya.

Habitat variable (independent)

Predator guild (dependent) Lambda Asymptotic SE a Approximate T b P-value

Striders 0.571 0.187 2.154 0.031 d Divers 0.833 0.118 3.420 0.001 d Habitat type Crawlers 0.800 0.141 2.866 0.004 d Striders 0.214 0.190 1.018 0.309 . Divers 0.000 0.000 c c Urban Crawlers 0.000 0.000 c c Striders 0.214 0.190 1.018 0.309 . Divers 0.000 0.000 c c Planning Crawlers 0.100 0.391 0.243 0.808 . Striders 0.214 0.261 0.734 0.463 . Divers 0.000 0.236 0.000 1.000 . Drainage Crawlers 0.400 0.268 1.182 0.237 . Striders 0.429 0.216 1.562 0.118 . Divers 0.250 0.191 1.160 0.246 . Strata Crawlers 0.500 0.235 1.570 0.116 .

a Not assuming the null hypothesis. b Using the asymptotic standard error assuming the null hypothesis. c Cannot be computed because the asymptotic standard error equals zero. d) Significant at 0.05 level.

Table 5. Association of temporal nature and structural complexity of habitats (dependent variables) with habitat type and characteristics of habitat location (independent variables) in Malindi, Kenya.

Habitat ecology variable

Habitat description variable Lambda Asymptotic SE a Approximate T b P-value

Urban strata 0.786 0.136 3.071 0.002 d Planning 0.786 0.136 3.071 0.002 d Drainage 0.571 0.162 2.556 0.011 d Urban/peri-urban 0.571 0.209 1.897 0.058 d

Temporal nature

Habitat type 0.929 0.069 4.854 0.000 d Urban strata 0.333 0.192 1.466 0.143 Planning 0.167 0.264 0.581 0.561 Drainage 0.000 0.000 c c

Urban/peri-urban 0.000 0.000 c c Structural complexity

Habitat type 0.667 0.236 1.714 0.087 a Not assuming the null hypothesis. b Using the asymptotic standard error assuming the null hypothesis. c Cannot be computed because the asymptotic standard error equals zero. d) Significant at 0.05 level.


of aquatic predators directly. Instead, a large proportionof the differential colonization of habitat types isprobably due to variation in the underlying ecology ofdifferent habitats. Anopheles larvae were scarce duringthe course of this study, preventing the analysis ofvariable effects on malaria vector distribution. Whilelocation characteristics predicted habitat types, theyfailed to predict predator distribution. In contrast, giventhe habitat type, the temporal nature of the habitat ispredictable 93% of the time and structural complexity ispredictable 67% of the time.

Evaluating the effect of temporal nature andstructural complexity on predator guild colonization wasdifficult due to the extreme differences in habitats. Forexample, both swimming pools and domestic waterreservoirs were permanent, structurally simple habitats.However, the sheltering of the reservoirs led tocolonization by only two predator taxa: veliids andToxorhynchites larvae, while the larger, unshelteredswimming pools contained numerous predator taxa.Similarly, tire track pools and water-filled tires are bothstructurally simple, temporal habitats, yet difficult tocompare due to the confounding differences in size,substrate, and shading. Comparisons between structurallysimple and structurally complex habitats were also madedifficult due to a paucity of structurally complex habitatsavailable for study. In Malindi, structurally complexhabitats are rare, which is in contrast to the numeroussimple habitats. Similarly, large temporal habitats arepresent in high numbers, especially tire track pools inperi-urban areas that are present after heavy rains.Despite these limitations, the strong association of habitattype with structural complexity and temporal nature, andthe inability to explain distribution with locationcharacteristics, suggest that these ecological variablesare of importance in determining distribution of urbanaquatic habitats.

Impact of habitat type on malaria vectorsPrevious studies have found Anopheles larvae in a

wide variety of urban habitat types, including most ofthe habitat types evaluated in this study (Welch et al.1989, Ijumba and Lindsay 2001, Marten et al. 1994,Marten et al. 2000, Robert et al. 1998). Therefore, thevariables that effect predator distribution described inthis study are likely pertinent to understanding thedistribution of mosquito larvae.

Swimming pools, although permanent sources ofwater, are cleaned often enough in Malindi that theyremain clear of significant vegetation and are structurallysimple most of the year, even when abandoned duringnon-tourist seasons. The large size of swimming poolsand their permanent water promotes colonization by all

predator guilds, but it is probable that the predatordensities are smaller than structurally complex naturalhabitats due to suppression of smaller specialist predatorsby a few large top predators as is the case in other systems(Clark and Messina 1998, Finke and Denno 2002,Rypstra et al.1999). Densities of predators were notmeasured during this study due to the logisticaldifficulties involved. Studies with experimentalmanipulation of structural complexity will be needed inthe future to verify these preliminary findings.

Temporal habitats were also heterogeneouslydistributed, dominated by drainage ditches in unplannedurban areas and tire track pools in peri-urban areas. Aswith swimming pools, the densities of predator taxa wasprobably low in temporal habitats due to the early levelof biological succession in these young habitats(Yanoviak 2001a, Yanoviak 2001b). The temporalpatterns of man-made water storage systems may providethe ideal habitat for mosquito larvae by failing to providethe lengthy development time required by many largepredators. In the case of the numerous tire track pools,a low structural complexity coupled with their temporalexistence could make large outbreaks of malariafollowing heavy rains possible.The World HealthOrganization has made development of surveillancenetworks a priority for predicting malaria epidemics(WHO 2001). Further studies on surveillance systemsshould more thoroughly evaluate these structurallysimple, temporal habitats as sentinel locations formonitoring larval populations of malaria vectors.

Implications for control of malaria vectorsAquatic predators are important in regulating the

populations of mosquito larvae in rural areas (Sunaharaet al. 2002), suggesting that the survivorship ofanthropophilic mosquitoes is aided by limitations oncolonization of the urban environment. Because temporalhabitats and habitats that are structurally simple limitpredator colonization, vector control efforts should targetthese habitats. In peri-urban areas, source reduction inthe form of filling tire track pools is an important step ineliminating this Anopheles larval habitat. Chemicalcontrol of mosquito larvae in swimming pools in theplanned areas of Malindi may be necessary to preventthe possibility of year-round use of these habitats bymalaria vectors for larval development. Additionally,water-management systems should evaluate thepracticalities of decreasing the number of structurallysimple, temporal habitats and increasing the number ofstructurally complex permanent habitats to encouragepredator colonization in cities. Encouraging naturalpopulation regulation is a form of biological control withincreasing popularity (Lacey and Orr 1994). Further


investigations into the ecology of urban mosquitoes willprovide more insight into limitations on predatordistribution and increase the opportunities for lessexpensive, more effective control measures.

Acknowledgments

We are grateful for the assistance provided by thescientific and technical staff at the Center for GeographicMedicine Research-Coast, KEMRI. The authors alsowish to acknowledge the technical advice provided byWanja Kinuthia at the National Museums of Kenya andtheoretical perspectives provided by John Githure at theInternational Center for Insect Physiology and Ecology.Two anonymous reviewers provided important feedbackon this manuscript that was of considerable help.Additionally, financial support was provided by NIHICIDR grant U19 AI45511 and CDC fellowship providedto JC through CCT 622308-02. This paper is publishedwith the permission of the Director of the Kenya MedicalResearch Institute.

REFERENCES CITED

Andis, M.D. and C.L. Meek. 1985. Mortality andsurvival patterns for the immature stages ofPsorophora columbiae. J. Am. Mosq. Contr. Assoc.1: 357-362.

Clark, T. and F. Messina. 1998. Foraging Behavior ofLacewing Larvae (Neuroptera: Chrysopidae) onPlants with Divergent Architectures. J. InsectBehavior 11: 303-317.

Finke, D. and R. Denno. 2002. Intraguild PredationDiminished in Complex-Structured Vegetation:Implications for Prey Suppression. Ecol. 83: 643-652.

Huang, Y.-M. 2001. A pictorial key for the identificationof the subfamilies of Culicidae, genera of Culicinae,and subgenera of Aedes mosquitoes of theAfrotropical region (Diptera: Culicidae). Proc.Entomol. Soc. Wash. 103: l-53.

Ijumba, J.N. and S.W. Lindsay. 2001. Impact of irrigationon malaria in Africa: paddies paradox. Med. Vet.Entomol. 15: 1-11.

Keating, J., K. Macintyre, C. Mbogo, A. Githeko, J.L.Regens, C. Swalm, B. Ndenga, L.J. Steinberg, L.Kibe, J.I. Githure, and J.C. Beier. 2003. Ageographic sampling strategy for studyingrelationships between human activity and malariavectors in urban Africa. Am. J. Trop. Med. Hyg. 68:357-365.

Lacey, L.A. and B.K. Orr. 1994. The role of biologicalcontrol of mosquitoes in integrated vector control.

Am. J. Trop. Med. Hyg. 50: 97-115.Macintyre, K., J. Keating, S. Sosler, L. Kibe, C.M.

Mbogo, A.K. Githeko, and J.C. Beier. 2002.Examining the determinants of mosquito-avoidancepractices in two Kenyan cities. Malar. J. 1: 14.

Marten, G.G., G. Borjas, M. Cush, E. Fernandez, andJ.W. Reid. 1994. Control of larval Aedes aegypti(Diptera: Culicidae) by cyclopoid copepods inperidomestic breeding containers. J. Med. Entomol.31: 36-44.

Marten, G.G., M. Nguyen, B.J. Mason, and G. Ngo. 2000.Natural control of Culex quinquefasciatus larvae inresidential ditches by the copepod Macrocyclopsalbidus. J. Vector Ecol. 25: 7-15.

Merritt, R. and K. Cummins. 1996. An introduction tothe aquatic insects of North America. Kendall/HuntPublishing Company: Dubuque, IA. 862 pp.

Oloo, A.J., J.M. Vulule, and D.K. Koech. 1996. Someemerging issues on the malaria problem in Kenya.East Afr. Med. J. 73: 50-53.

Robert, V., H.P. Awono-Ambene, and J. Thioulouse.1998. Ecology of larval mosquitoes, with specialreference to Anopheles arabiensis (Diptera:Culicidae) in market-garden wells in urban Dakar,Senegal. J. Med. Entomol. 35: 948-955.

Roberts, D.R. and R.G. Andre. 1994. Insecticideresistance issues in vector-borne disease control.Am. J. Trop. Med. Hyg. 50: 21-34.

Rypstra, A., P.E. Carter, R.A. Balfour, and S.D. Marshal.1999. Architectural features of agricultural habitatsand their impact on the spider inhabitants. J.Arachnol. 27: 371-377.

Sunahara, T., K. Ishizaka, and M. Mogi. 2002. Habitatsize: a factor determining the opportunity forencounters between mosquito larvae and aquaticpredators. J. Vector Ecol. 27: 8-20.

Welch, J.B., J.K. Olson, W.G. Hart, S.G. Ingle, and M.R.Davis. 1989. Use of aerial color infraredphotography as a survey technique for Psorophoracolumbiae oviposition habitats in Texas ricelands.J. Am. Mosq. Contr. Assoc. 5: 147-160.

World Health Organization. 2000. WHO ExpertCommittee on Malaria. WHO Tech Rep Ser 892: i-v, 1-74.

World Health Organization. 2001. Malaria early warningsystems, a framework for field research in Africa:concepts, indicators and patterns. World HealthOrganization: Geneva. 80 pp.

Yanoviak, S. 2001a. Predation, resource availability, andcommunity structure in Neotropical water-filled treeholes. Oecologia 126: 125-133.

Yanoviak, S. 2001b. The macrofauna of water-filled treeholes on Barro Colorado Island, Panama. Biotropica33: 110-120.

Ecological limitations on aquatic mosquito predator colonization in the urban environment

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