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Larvicidal efficiency of aquatic predators: A perspective for mosquito biocontrol

Article (PDF Available) in Zoological studies 45(4):447-466 · October 2006 with 1,369 Reads

1st Ram Kumar
25.62 · Central University of Bihar
2nd Jiang-Shiou Hwang
40.44 · National Taiwan Ocean University

Abstract

Ram Kumar and Jiang-Shiou Hwang (2006) Larvicidal efficiency of aquatic predators: a perspective for mos- quito biocontrol. Zoological Studies 45(4): 447-466. Biological control of mosquito larvae with predators and other biocontrol agents would be a more-effective and eco-friendly approach, avoiding the use of synthetic chemicals and concomitant damage to the environment. Manipulating or introducing an auto-reproducing predator into the ecosystem may provide sustained biological control of pest populations. The selection of a biological control agent should be based on its self-replicating capacity, preference for the target pest popula- tion in the presence of alternate natural prey, adaptability to the introduced environment, and overall interaction with indigenous organisms. In order to achieve an acceptable range of control, a sound knowledge of various attributes of interactions between a pest population and the predator to be introduced is desirable. Herein, we qualitatively review a wide range of literature sources discussing the ability of different aquatic predators to con- trol mosquito larval populations in environments where mosquitoes naturally breed. Different predators of mos- quito larvae include amphibian tadpoles, fish, dragonfly larvae, aquatic bugs, mites, malacostracans, anostra- cans, cyclopoid copepods, and helminths. The most widely used biocontrol agents of mosquito populations are the western mosquito fish, Gambusia affinis, and the eastern mosquito fish, G. holbrooki. The effect of these fishes on native faunal composition and their inability to survive in small containers, tree holes etc., which are ideal breeding sites of vectorially important mosquitoes, make them inefficient in controlling mosquito popula- tions. On the basis of larvicidal efficiency, the ability to produce dormant eggs, the hatchability of dormant eggs after rehydration, faster developmental rates, and higher fecundity, various tadpole shrimp can be considered to

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Zoological Studies 45(4): 447-466 (2006)

447

*To whom correspondence and reprint requests should be addressed. Tel: 886-2-24622192 ext. 5304. Fax: 886-2-24629464.

E-mail:Jshwang@mail.ntou.edu.tw

Larvicidal Efficiency of Aquatic Predators: A Perspective for Mosquito

Biocontrol

Ram Kumar and Jiang-Shiou Hwang*

Institute of Marine Biology, National Taiwan Ocean University, 2 Pei- Ning Rd., Keelung, Taiwan 202, R.O.C.

(Accepted November 2, 2005)

CONTENTS

ABSTRACT ................................................................................................................................................447

INTRODUCTION ........................................................................................................................................448

Amphibian tadpoles ............................................................................................................................451

Larvivorous fish ..................................................................................................................................451

Predator escape mechanisms in mosquitoes ....................................................................................452

Aquatic insects ....................................................................................................................................454

Larvivorous psorophora ......................................................................................................................454

Odonate Iarvae ..................................................................................................................................454

Larvivorous organisms in temporary water bodies..............................................................................455

Cyclopoid copepods............................................................................................................................456

CONCLUSIONS ..........................................................................................................................................459

ACKNOWLEDGMENTS ..............................................................................................................................460

REFERENCES ............................................................................................................................................460

ABSTRACT

Ram Kumar and Jiang-Shiou Hwang (2006) Larvicidal efficiency of aquatic predators: a perspective for mos-

quito biocontrol. Zoological Studies 45(4): 447-466. Biological control of mosquito larvae with predators and

other biocontrol agents would be a more-effective and eco-friendly approach, avoiding the use of synthetic

chemicals and concomitant damage to the environment. Manipulating or introducing an auto-reproducing

predator into the ecosystem may provide sustained biological control of pest populations. The selection of a

biological control agent should be based on its self-replicating capacity, preference for the target pest popula-

tion in the presence of alternate natural prey, adaptability to the introduced environment, and overall interaction

with indigenous organisms. In order to achieve an acceptable range of control, a sound knowledge of various

attributes of interactions between a pest population and the predator to be introduced is desirable. Herein, we

qualitatively review a wide range of literature sources discussing the ability of different aquatic predators to con-

trol mosquito larval populations in environments where mosquitoes naturally breed. Different predators of mos-

quito larvae include amphibian tadpoles, fish, dragonfly larvae, aquatic bugs, mites, malacostracans, anostra-

cans, cyclopoid copepods, and helminths. The most widely used biocontrol agents of mosquito populations are

the western mosquito fish, Gambusia affinis, and the eastern mosquito fish, G. holbrooki. The effect of these

fishes on native faunal composition and their inability to survive in small containers, tree holes etc., which are

ideal breeding sites of vectorially important mosquitoes, make them inefficient in controlling mosquito popula-

tions. On the basis of larvicidal efficiency, the ability to produce dormant eggs, the hatchability of dormant eggs

after rehydration, faster developmental rates, and higher fecundity, various tadpole shrimp can be considered to

Review Article

Zoological Studies 45(4): 447-466 (2006)

448

INTRODUCTION

Mosquito-borne diseases have been a major

problem in almost all tropical and subtropical coun-

tries, and currently there are no successful vac-

cines against most such diseases. For years,

mankind has been exploring various methods to

combat threats from mosquito-borne diseases.

Many synthetic insecticides are widely used for

controlling adult and larval mosquito populations.

However, the harmful effects of chemicals on non-

target populations and the development of resis-

tance to these chemicals in mosquitoes along with

the recent resurgence of different mosquito-borne

diseases (Milam et al. 2000) have prompted us to

explore alternative, simple, sustainable methods of

mosquito control. The eradication of mosquito fly-

ing insect stocks using adulticides is not a prudent

strategy, as the adult stage occurs alongside

human habitation, and they can easily escape

remedial measures (Service 1983 1992).

Until recently, the ecological role of environ-

mental managers has been more concentrated on

preventing damage from pollution rather than

proposing sustainable solutions to different global

and local problems faced by human societies.

One of the multiple possibilities of applying ecolog-

ical theories for human welfare is the use of our

knowledge about the effects and mechanisms of

predation and competition within various kinds of

permanent and temporary aquatic habitats. By

manipulating particular trophic levels, desired

changes can be achieved in a system (He et al.

1994). Biotic interactions such as competition and

predation have been reported to be capable of reg-

ulating the number of mosquito populations by

reducing the number of larvae that survive through

larval development and by increasing the larval

and pupal duration times (Knight et al. 2004). It is

obvious that different pathogens and disease vec-

tors are part of the ecosystem, and anthropogenic

alterations of natural conditions provide an advan-

tage to some of these pathogens and disease vec-

tors. The recent resurgence of various mosquito-

borne diseases may have been an indirect result

of such altered conditions. Programs to decimate

mosquito populations by trying to kill the adult

stage frequently fail, because the adults reside

alongside human populations in their households,

and hiding places can often not be detected as

refuges for mosquitoes, thereby allowing them to

escape remedial measures. Even larval mosqui-

toes live in places where they are difficult to find

and kill: for instance, in old tires, trash, water

tanks, and basically any container that holds water

(Service 1983). Precautions also have to be taken

not to contaminate drinking water supplies and

water-transport containers with potentially harmful

chemicals. Additionally, mosquitoes have devel-

oped resistance to frequently used pesticides mak-

ing it even more difficult to control adult popula-

tions. Essentially, larval mosquito populations

should be the first target of all control measures

(Service 1992, Briegel 2003).

The potential for the use of genetics against

mosquito-borne infection has recently been con-

sidered in vector control programs. Recent tech-

niques to modify genes of mosquitoes are believed

to be an appropriate interventional remedy against

malaria and dengue fever. The main purpose is to

produce a genetically modified strain of mosquito

in the laboratory which does not serve as a carrier

of disease and which is competitively superior in

the natural habitat such that wild mosquitoes will

eventually be replaced after the release of geneti-

cally altered mosquitoes in nature. However, there

are several problems with this approach, and it is

taking some time to turn the prospects of this tech-

nology into practical tools (Stiling and Cornelissen

2005).

Therefore, the exploration of more-effective

and eco-friendly techniques to control mosquitoes

seems to be very promising. Various organisms,

known as natural biological control agents, can be

utilized to control mosquito populations, thus

avoiding the use of chemicals and harm to the

environment in the process. It is desirable to use

biological control agents that can adapt to mosqui-

be ideal control agents in temporary water bodies and rice paddy fields. Among various predators of mosquito

larvae, the cyclopoid copepods are efficient, found naturally, are safe for human beings, and are also economi-

cal in their application. The mosquito larval selectivity patterns of many cyclopoids, their adaptability to variable

aquatic environments which are ideal breeding sites for mosquitoes, their resistance to starvation, and their

day-night prey detection ability using hydromechanical signals make them an ideal biocontrol agent. Therefore,

there is a need to test the feasibility of cyclopoid copepods by putting them into operational use as ecocompati-

ble means of biocontrol. http://zoolstud.sinica.edu.tw/Journals/45.4/447.pdf

Key words: Mosquito predators, Larvivory, Copepod, Dragonfly larvae, Vector control.

Kumar and Hwang -- Aquatic Predators and Mosquito Biocontrol 449

to breeding habitats, are found naturally, and pose

no danger to people (Rishikesh et al. 1988,

Spielman et al. 1993). Biological control means

the use of different kinds of living things, and/or

their derivatives to eliminate pest populations.

Many biological control agents disperse by them-

selves enabling them to spread and build up viable

populations (Caltagirone 1981, Bellows 2001,

Headrick and Goeden 2001). In the field of

applied ecology, there have been many attempts

to achieve the biological control of pathogens or

vectors by introducing new effective natural ene-

mies to their natural habitats (Arthington and Lloyd

1989, Headrick and Goeden 2001, Denoth et al.

2002). The efficient selection of effective natural

enemies has become increasingly important for

the success of biological control programs.

Microbial larvicides such as Bacillus

thuringiensis israelensis (Bti) and Bacillus sphaeri-

cus (B. sphaericus) are gram-positive, aerobic

(facultative anaerobic) entomopathogenic soil bac-

teria (Johnson et al. 1995, de Maagd et al. 1999,

Bobrowski et al. 2002). Mosquito larvae ingest the

microbial product which is composed of a dormant

spore form of the bacterium and an associated

toxin (crystalline protein inclusion produced by Bti

during sporulation). The toxin acts as a stomach

poison by binding to receptor cells present in the

insect but not in mammals (Lacey and Undeen

1986, Neri-Barbosa et al. 1997, Bishop et al. 1999,

Batra et al. 2000). Interestingly, its application

destroys larval mosquitoes but spares predators if

present in the water (Ohana et al. 1987, Chansang

et al. 2004, Su and Mulla 2005). Very recently

non-larvicidal effects of Bacillus formulations have

also been recorded in various mosquitoes (Zahiri

and Mulla 2002). Relatively lower numbers of egg

rafts have been recorded in ovitraps treated with

Bti and B. sphaericus than in controls, and further-

more, an adverse relationship was found between

the Bacillus product concentration and oviposition

(Zahiri and Mulla 2005). Contrary to this, a liquid

formulation of Bti dispersed by ultra-low-volume

technology in laboratory and field experiments did

not affect the oviposition behavior of Aedes

albopictus females (Stoops 2005). The parasporal

proteinaceous toxin produced by Bti, however, is

photolabile and destroyed by sunlight (Bernhard

and Utz 1993, Cooping and Menn 2001). In mos-

quito breeding habitats, they are only effective for

1-4 wk after application (Jensen et al. 2000,

USEPA 2005). In a recent study in Taiwan, Teng

et al. (2005) recorded that the maximum duration

of effectiveness of Bti in reducing the larval num-

ber was 1 wk after application in rice paddy fields.

Essentially, frequent applications to each breeding

site are required, thereby making it more expen-

sive and rigorous (Amalraj et al. 2000). A fermen-

tation product called spinosad, produced by the

actinomycete, Sacchoropolyspora spinosa, is

another naturally derived larvicide (Williams et al.

2003). In a recent study in Antalya, Turkey, the

mosquito species Culex pipiens was eliminated

from septic tanks in 7 d after the application of

spinosad at a concentration of 100 active insects

(a.i.)/ha (Cetin et al. 2005). This has been shown

to be less toxic to birds and mammals (Bret et al.

1997, Breslin et al. 2000), and no adverse effects

were detected on predatory insects such as lady-

birds, lacewings, big-eyed bugs, or minute pirate

bugs (Cooping and Menn 2001, Williams et al.

2003). Its applicability has not been assessed in

nature. Many mosquito larvae have been reported

to ingest toxic and noxious algae (mostly

cyanobacteria) which inhibit larval development

and decrease survival (Marten 1986); however,

mosquito breeding sites are usually too dark for

algal growth.

The fungus Lagenidium giganteum has been

shown to have the ability to control mosquito popu-

lations through oospores that can resist drought

and which can readily be produced in bulk.

Oospores survive for many years in the soil, but

can reactivate within only about a month after

flooding. In practice, the spores are activated by

remaining in wet for 1-2 wk before being sprayed

on the surface of the site to be treated (Copping

and Menn 2001). The fungus infects and kills only

a portion of larval target mosquitoes, as well. The

level might not be sufficient to decrease the risk of

human infection. Very recently in rice paddy field

ecosystems in Taiwan, L. giganteum has been

found to be effective for only 1 wk in reducing the

number of larvae after application (Teng et al.

2005), thus necessitating frequent application of

this product.

The use of mosquito parasites, for instance,

protozoans and helminths, might be a possible

way (Sweeney and Becnel 1991, Santamarina et

al. 1999) to control mosquito populations. Oocysts

of Ascogregarina (a protozoan parasite) release

sporozoites that disrupt the gut wall of mosquito

larvae (Beier and Craig 1985). For instance,

Ascogregarina taiwanensis and As. culicis normal-

ly infect Ae. albopictus and Ae. aegypti respective-

ly (Munsterman 1990). The mermithid nematode,

Romanomermis iyengari Welch, is another mos-

quito larval parasite of Anopheles and Culex larvae

Zoological Studies 45(4): 447-466 (2006)

450

(Iyengar 1927) first reported in 1927 in the lower

Bengal delta, India. The biocontrol potential of R.

iyengari against Aedes, Anopheles, and Culex

mosquitoes has been evaluated in field and labo-

ratory experiments (Chandrahas and Rajagopalan

1979, Santamarina et al. 1996). Some recent

studies have demonstrated the effectiveness of

Romanomermis for mosquito control in Mexico

(Santamarina et al. 1999, Pérez et al. 2004). The

feasibility under field conditions has not been

established.

Biological control of mosquito larvae with bio-

logical agents like competitors and predators is

more convenient and alleviates the need for fre-

quent chemical applications. Biotic interactions of

larval mosquitoes with different predators and

competitors in aquatic ecosystems are schemati-

cally illustrated in figure 1.

The selection of biological control agents

should be based on their potential for unintended

impacts, self-replicating capacity, climatic compati-

bility, and their capability to maintain very close

interactions with target prey populations (Waage

and Greathead 1988). They eliminate certain prey

and sustain such environments (i.e., as when prey

is introduced, they eat the prey) for long periods

thereafter (Marten 1994a). However, this will only

be possible if the predator possesses extraordi-

nary search efficiency irrespective of the illumina-

tion situation in response to the emergence of

prey. It is important to have a sound general

knowledge of a predator,s prey selectivity patterns

and particularly of its mosquito larval selection in

the presence of alternate natural prey (Arthington

and Lloyd 1989, Arthington and Marshall 1999). In

addition, the predator,s adaptability to the intro-

duced environment and overall interaction with

indigenous organisms need to be considered prior

to introduction (Denoth et al. 2002, Carlson et al.

2004). This paper presents a brief account of dif-

ferent predators of mosquito larvae and possible

prey/predator interactions in aquatic ecosystems.

Fig. 1. Schematic representation of the interactions between mosquito larvae and their predators (diagram not to scale).

Only young ones are fed upon

Schematic representation of the prey-predator interactions (diagram not to scale)

Larvae Fish

Copepoda

Water

Cladocera

Fish fry are fed upon

Larvae

Pupa

Larvae

Adult

Air

Predation

Grow into

Mosquito

Adult

Dragonfly

Adult

Eggs laid

in water

Kumar and Hwang -- Aquatic Predators and Mosquito Biocontrol 451

Amphibian tadpoles

Omnivorous tadpoles are potential predators

of mosquito larvae (Spielman and Sullivan 1974,

Morgan and Buttemer 1996, Webb and Joss 1997,

Goodsell and Kats 1999, Komak and Crossland

2000) and exert significant impacts on freshwater

ecosystems (Blaustein and Kotler 1993, Blaustein

et al. 1996). Larvae of the giant Cuban tree frog

(Hyla septentrionalis) have been reported to

destroy aquatic insects and algae growing in water

containers (Morgan and Buttemer 1996, Webb and

Joss 1997, Goodsell and Kats 1999, Komak and

Crossland 2000). However, the dietary niche

breadth of larvivorous tadpoles includes other

predators of mosquito larvae as well, hence they

can efficiently predate on other co-occurring bio-

control agents of mosquito. Their efficiency in uti-

lizing mosquito larvae in the presence of alternate

prey has not been properly elucidated. It has been

reported that tadpoles of Rana tigrina are more-

efficient mosquito pupal predators (Marian et al.

1983) than others. However, in nature, tadpoles

are preyed upon by many predators, for example,

mosquitofish (Grubb 1972, Gamradt and Kats

1996, Carwood 1997, Komak and Crossland

2000), catfish, and dragonfly larvae (Woodward

1983, Travis et al. 1985, Wissinger 1989). These

predators prey on amphibian eggs and tadpoles,

and contribute to substantial anuran declines

(Baber and Babbitt 2003). Eklöv (2000) recorded

that larval dragonfly, Anax junius, can utilize bull-

frog (R. catesbeiana) larvae more efficiently than

the bluegill sunfish (Lepomis macrohirus). Of

course any introduction of amphibian tadpoles

beyond their natural range is difficult and requires

utmost caution. Tadpoles can rarely be accommo-

dated in small containers that hold less than sever-

al liters of water and seem to have small impacts

on larval populations of mosquitoes.

Larvivorous fish

One of the most widely distributed visually

feeding fish is the western mosquito fish,

Gambusia affinis (Baird and Girard), and the east-

ern mosquito fish, G. holbrooki (Giarard). During

the 20th century, several fish species were intro-

duced outside their natural habitats. Both, the

western and eastern mosquitofish were introduced

worldwide because of their reputation as mosquito-

control agents (Krumholz 1948, Courtenay and

Meffe 1989, Hammer et al. 2002). Both eastern

and western mosquitofish possess a wide dietary

niche breadth. Feeding strategy analyses sug-

gested high individual specialization, and thus an

opportunistic feeding strategy for mosquitofish in

both the juvenile and adult stages (Specziár 2004).

They exhibit remarkable spatial and temporal vari-

ations, as the diet composition changes with the

relative abundance of prey in the habitat (Cabral et

al. 1998, Arthington and Marshell 1999, Willems et

al. 2005). While mosquitofish have often been

released in highly disturbed or artificial habitats,

they have the potential to spread into pristine

water bodies (Arthington and Lloyd 1989,

Arthington 1991), where they severely impact

native fish, amphibians, and invertebrates

(Arthington 1991, Gamratt and Kats 1996, Howe et

al. 1997, Webb and Joss 1997, Goodsell and Kats

1999, Leyse et al. 2004). Chinese health authori-

ties have also used other fish species to exclude

Ae. aegypti mosquitoes from breeding in large cis-

terns or other containers of drinking water. Small

fish, such as Claris fuscus, Tilapia nilotica, and

Macropodus sp. have been used in many regions

to eliminate larvae in domestic water containers

with considerable success. The use of catfish

appears to be particularly effective (Neng et al.

1987). Larvivorous fish have been widely used as

biocontrol agents of mosquito larvae, but they

have their own limitations, for instance, such fish

are expensive to rear and do not survive for long in

small places (like containers, etc.).

Little is known about the ecology of larvivo-

rous fish (Hurlbert et al. 1972, Hurlbert and Mulla

1981, Meffe and Snelson 1989). Comparative

research on introduced and indigenous larvivorous

fish feeding is particularly scarce, although it is

crucial to determine the impacts of their introduc-

tion to ecosystems (Hoddle 2004). The mosqui-

tofish has invaded relatively lower stream sections,

mostly wetlands, shallow lakes, and almost all

ornamental pools in different parts of the world. It

has been shown that mosquitofish introduced in

1922 into southern California subsequently

reduced populations of native fish throughout the

state due to competition, predation, and hybridiza-

tion. It has now become a threat to native fishes

that share similar habitats, especially cyprinodon-

tids because of its ecological advantages related

to fast growth, early maturity, viviparity (Vargas

and Sostoa 1996, Barrier and Hicks 1994), and

food consumption, which can reach 83% of the

fish,s weight per day (Wurtsbaugh and Cech

1983). In addition to competition for resources,

species of Gambusia are aggressive and often

attack fish more than twice their own size and

Zoological Studies 45(4): 447-466 (2006)

452

mass (Gophen et al. 1998; Rowe 1998) which

results in damage to the fins and scales, leaving

the fish susceptible to disease. Considering its

nontarget effects and extraordinary ability to

spread in additional waters, ecologists have ques-

tioned the use of mosquitofish as biological control

agents, especially when introduced as exotics to

supplement native species (Moyle 1976, McKay

1984, Simberloff and Stiling 1996). The introduc-

tion of Gambusia into either riverine or large lake

systems (Kolar and Lodge 2000) or in temporary

and permanent wetlands (Leyse et al. 2004) can

cause rapid declines in a variety of invertebrates,

amphibians, and fish indigenous to those systems

(Gill et al. 1999, Knapp and Matthews 2000,

Hammer et al. 2002).

Some workers have used this species to test

pelagic trophic interactions (Hurlbert et al. 1972,

Lancaster and Drenner 1990), optimal foraging

theory (Bence and Murdoch 1986), and toxicant

bioaccumulation in wetlands. Some dietary stud-

ies have focused on its role in the control of

insects (Linden and Cech 1990, Walton et al.

1990, Su and Mulla 2001). In nature, a wide spec-

trum of different foods is available. The utilization

of target species by a predator depends upon its

prey selectivity patterns in the presence of alter-

nate natural prey co-occurring in the habitat with

the target organisms. However, few studies have

analyzed the dietary patterns of mosquitofish

(Crivelli and Boy 1987, Specziár 2004). Since the

beginning of the introductions, several studies

have pointed out negative effects of mosquitofish

on small indigenous fish species (Courtenay and

Meffe 1989, Howe et al. 1997, Ivantsoff and Aarn

1999), amphibians (Morgan and Buttemer 1996,

Webb and Joss 1997, Goodsell and Kats 1999,

Komak and Crossland 2000), and invertebrates

like zooplankton (Margaritora 1990), dragonfly lar-

vae (Rowe 1987), damselflies (Englund 1999), and

fairy shrimp (Leyse et al. 2004).

In natural habitats, many determinant factors

which affect prey preference and the dietary niche

breadth of Gambusia include the size of the water

body, availability of food, population density, the

invertebrate community, varieties of fish, primary

production, water temperature, oxygen content,

and the structure of sub-habitats (Mansfield and

McArdle 1998). Recently Specziár (2004) record-

ed 34% algae, 19% detritus, and remaining animal

prey in the gut content of G. holbrooki. In a study

by García-Berthou (1999), animal food included

11% rotifers, 28% dipterans, 19% ostracods, 19%

other insects, 18% copepods, and 5% cladocer-

ans. However, in another study on the eastern

mosquitofish, G. holbrooki, of Lake Banyoles,

Catalonia, Spain, it was observed that its diet was

based on littoral cladocerans, particularly

Chydorus sphaericus, Scapholeberis ramneri,

Ceriodaphnia reticulata, and Pleuroxus laevis, and

nematoceran (basically chironomid) adults. There

was a large variety of prey of terrestrial (collem-

bolans and ants) or aquatic neustonic origin (Sca.

ramneri and emerging nematoceran adults), show-

ing that the foraging range of microhabitats of the

mosquitofish is closely linked to the water surface.

Those studies, conducted in natural water bodies,

did not record a significant amount of larval mos-

quito in the diet of mosquitofish. Prey preference

by mosquitofish has not been found to be related

to fish density (García-Berthou 1999). Significant

differences in the extent of carnivory and efficiency

of utilizing dipteran larval prey have also been

reported between sexes. Sexual dimorphism and

size play a very important roles in feeding behavior

and differentially affect the utilization of food.

Females generally predate more intensively over a

wider range of items in response to their larger

size and reproductive needs, while males and

juveniles change their strategy to avoid competi-

tion and exploit resources (Specziár 2004). The

optimal temperature for Gambusia feeding rates

was 30-35°

C (Specziár 2004). Gambusia has a

voracious appetite, feeding at rates much higher

than those of most other similar-sized fish. At opti-

mal temperatures, maximum consumption rates

ranged from 0.75% to 1.1% of body weight per day

for fish ranging from 0.2 to 1.2 g (Cabral et al.

1998). Because of their ability to spread widely

and their negative impact on aquatic communities,

G. affinis and G. holbrooki have been designated

among 100 invasive species worldwide (ISSG

2000).

Predator escape mechanisms in mosquitoes

Different oviparous insects have been report-

ed to avoid aquatic sites where there is a high pre-

dation risk to their offspring. Mechanisms for

predator detection by insects may involve tactile,

visual, or chemical cues (Spencer et al. 2002).

The proximate mechanisms that mediate avoid-

ance behavior are certain chemical exudates

released by predators that are commonly called

kairomones. Chemically mediated avoidance is an

adaptation used by prey to detect and evade

predators. Kairomones or semiochemicals emitted

from predators (Nordlund 1981) are normally used

Kumar and Hwang -- Aquatic Predators and Mosquito Biocontrol 453

by prey to detect a predator,s presence in the

environment, and the prey can thereby minimize

such encounters (Kerfoot and Sih 1987, Kats and

Dill 1998). Common responses to chemicals from

predators include an increased use of refuges

(Kats et al. 1988), marked changes in the intensity

of movements (Mathis et al. 1993, Chivers et al.

1996, Huryn and Chivers 1999), reduced foraging

(Petranka and Hayes 1998), reduced courtship

behavior, predator avoidance (Flowers and Graves

1997), and increased growth rates (our own obser-

vations). Chivers and Smith (1998) and Kats and

Dill (1998) reviewed studies showing that fish,

amphibians, reptiles, mammals, a bird, and a

broad array of invertebrates have evolved

chemosensory mechanisms for detecting preda-

tors. Kats and Dill (1998) list 16 studies which

involved larvae of aquatic species that provide evi-

dence for chemically mediated detection of aquatic

predators by insects. Where chemical cues are

involved, responses to predators are often influ-

enced by the predator,s diet. For example, mayfly

and damselfly larvae are more likely to respond to

fish chemicals if the fish have recently consumed

conspecific prey (Chivers et al. 1996, Huryn and

Chivers 1999). Prey species are more likely to

evolve chemically mediated avoidance of preda-

tors when visual detection of predators is limited

(Kats and Dill 1998, Petranka and Hayes 1998). In

turn, prey must possess suitable behavior and

chemosensory mechanisms to detect and respond

to predators. Mosquitoes appear to meet most of

these requirements since many species are cre-

puscular or nocturnal and rely heavily on

chemosensory mechanisms when selecting ovipo-

sition sites. After mating and taking a blood meal,

a hemolymph-borne hormone triggers the female

to begin searching for a suitable oviposition site

and to become receptive to chemical signals from

the site (Klowden and Blackmer 1987). Gravid

females are known to spend some time flying

around a water body apparently evaluating it as an

oviposition site (Lester and Pike 2003). The main

criteria in such a selection process are the pres-

ence of competitors, predators, and/or kairomones

(Murdoch et al. 1984, Blaustein et al. 1995, Lester

and Pike 2003) and container size (Angelon and

Petranka 2002, Sunahara et al. 2002, Lester and

Pike, 2003). Females oviposit on mud or the

water,s surface (e.g., Culex spp.) after sampling

the chemical composition of the substrate using

receptors on the tarsi, antennae, and tips of the

proboscis (Davis 1976, Bentley and Day 1989).

Published evidence convincingly suggests that

mosquitoes use chemosensory information to

assess several parameters that reflect habitat

quality for the offspring, including the availability of

nutrients, the presence of competitors and preda-

tors, and the overall quality and permanence of the

water body (Davis 1976, Angerilli 1980, Chesson,

1984, Bentley and Day 1989, Edgerly et al. 1998).

It has been demonstrated that mosquitoes and

phantom midges greatly reduced ovipositing rates

in experimental pools that contained caged sunfish

(Lepomis) that were not visible to ovipositing

females. Grostal and Dicke (1999) demonstrated

a similar behavior in acarine mites, suggesting that

this phenomenon may occur across a diverse

array of arthropods. Recently it has been convinc-

ingly reported that adult mosquitoes have the abili-

ty to sense the presence of Gambusia, and that

mosquitoes reduce egg-laying rates in pools con-

taining the odor of mosquitofish (Angelon and

Petranka 2002). Those authors conducted an

experiment to determine whether mosquitoes

reduce oviposition rates in pools containing chemi-

cals of the mosquitofish (G. affinis). Their experi-

mental treatments consisted of outdoor pools that

contained known concentrations of fish chemicals

(low, medium, or high) or no fish chemicals (con-

trol). The mean number of larvae of the mosquito

species C. pipiens per pool significantly differed in

the experiment and was about 3 times larger in

control pools compared with those containing

medium and high concentrations of fish chemicals.

That study clearly demonstrated that ovipositing

female mosquitoes are able to make use of fish

kairomones to make behavioral decisions that

affect encounter rates of future offspring with

predators.

In nature, G. affinis inhabits temporary habi-

tats such as swamps, roadside puddles, and orna-

mental ponds, and forms schools that may contain

hundreds of individuals. Schooling behavior pro-

duces a patchy environment where predation risks

may vary locally, depending on the location of

schools. Female mosquitoes avoid Gambusia at

several spatial scales. For example, females can

use the strength of fish chemicals to avoid local

sites in ponds with dense schools. Alternatively,

females might strongly avoid ponds with Gambusia

and seek out ponds with fewer or no fish (Ritchie

and Laidlaw-Bell 1994).

Moreover, recent reviews have not supported

the effectiveness of the mosquitofish in controlling

mosquito populations or mosquito-borne diseases

(Arthington and Lloyd 1989, Courtenay and Meffe

1989, Rupp 1996). In some cases the mosqui-

Zoological Studies 45(4): 447-466 (2006)

454

tofish may even indirectly increase the survival

rate of mosquito larvae by feeding on their clado-

ceran competitors (Blaustein and Karban 1990).

Courtenay and Meffe (1989) concluded that

despite its reputation as being an effective preda-

tor of mosquitoes, Gambusia is generally ineffec-

tive as a biological control agent. For example,

Gambusia had a positive impact on controlling

mosquitoes in only four of 20 countries where it

was introduced for mosquito control or other pur-

poses. One explanation for the ineffectiveness of

Gambusia in controlling mosquitoes is that

ovipositing mosquitoes may seek out fish-free

habitats that adjoin large bodies of water contain-

ing Gambusia. The active avoidance of habitats

with a high predation risk to offspring may ultimate-

ly act to sustain high densities of mosquitoes near

areas stocked with Gambusia. Ritchie and

Laidlaw-Bell (1994) found that ovipositing Ae. tae-

niorhynchus strongly avoided sites with high densi-

ties of G. holbrooki and shifted to adjoining habi-

tats with few or no predatory fish. Similar results

were obtained by other workers (Stav et al. 2000).

Therefore, female mosquitoes often avoid oviposit-

ing in waters containing predatory fish (Chesson

1984, Blaustein et al. 1995, Blaustein 1998,

Angelon and Petranka 2002, Kiflawi et al. 2003a

b). The limitations of G. affinis and Poecilia reticu-

lata at controlling mosquito populations have been

further proven in a comparative study conducted

by Wang 1998, who revealed that the Taiwan

native larvivorous fish, Macropodus opercularis,

was better adapted to the breeding habitat and

could control larval populations 8 times more effi-

ciently than could G. affinis.

Therefore, recent studies suggest that the

effectiveness of Gambusia in controlling mosqui-

toes may be compromised if adult mosquitoes

respond to fish stocking by shifting to nearby

breeding sites that lack fish. The use of Gambusia

in biological control programs should be reconsid-

ered.

Aquatic insects

Some aquatic insects play important roles in

mosquito control (James 1966, Ellis and Borden

1970, Pandian et al. 1979). In general, almost all

aquatic insect predators prey on mosquito larvae

and pupae (Ellis and Borden 1970, Peckarsky

1984); the aquatic coleoptera (especially notonec-

tids and dysticids) and odonates have been

observed to ingest mosquito larvae as a

part of their natural food assemblages. The

backswimmer, Notonecta undulata (Hemiptera,

Notonectidae), has been shown to efficiently utilize

the second instar of mosquito larvae as prey (Ellis

and Borden 1970, Murdoch et al. 1984, Blaustein

et al. 1995, Blaustein 1998). The role of the back-

swimmer, Anisops assimilis, in controlling mosqui-

toes was recognized as early as 1939, when

Graham (1939) noted some stock troughs with A.

assimilis were free of mosquitoes, whereas pud-

dles in depressions surrounding the troughs con-

tained“energetic mosquito activity”. However, the

predation efficiency of backswimmers on mosquito

larvae was found to be container-specific (Lester

and Pike 2003). For instance, diving beetle

(Rhanthus pulverulosus) and damselfly larvae are

predators of mosquito larvae and show a prefer-

ence for larger container sizes (Sunahara et al.

2002). Furthermore, the presence of backswim-

mers within a water body has been demonstrated

to reduce oviposition rates by adult mosquitoes

(Chesson 1984, Blaustein et al. 1995).

Larvivorous psorophora

Toxorhynchites, a kind of mosquito with canni-

balistic larvae, has attracted much attention as

biological control agents. Certain kinds of

Toxorhynchites mosquitoes are good for the con-

trol of Ae. aegypti because they breed in the same

kinds of containers. However, it proved to be

unsuccessful in the field. Repeated release of

Toxorhynchites 1st instar larvae in waterlogged

places between bamboo trees had no effect on

mosquito populations in Indonesia (Annis et al.

1989 1990). Ironically it was recognized that it

increased prey density. This type of interfering

effect became evident when the prey was present

in excess (Hubbard et al. 1988). Subsequent tests

and trials have obtained similar results (Annis et al.

1989 1990).

Odonate larvae

The order Odonata includes insects like the

dragonfly and damselfly. They enjoy a wide distri-

bution and are particularly prominent around

aquatic ecosystems in tropical countries.

Invariably the adults mate near water bodies, and

the females lay eggs in water soon thereafter.

Aquatic larval instars are predators of mosquito

larvae. Dragonfly larvae, in particular, may be use-

ful for controlling mosquito larval populations. In

an experiment in Myanmar (Burma), 2 dragonfly

larvae were introduced in domestic containers

Kumar and Hwang -- Aquatic Predators and Mosquito Biocontrol 455

accommodating Ae. aegypti. The mosquito larvae

disappeared quite rapidly after dragonfly larva

introduction to each container, and the density of

target adults declined about 6 wk later. The drag-

onfly and damselfly are true enemies of mosqui-

toes as the larvae of these insects are able to uti-

lize mosquito larvae as food, and the adults are

efficient predators of airborne adult mosquitoes

(Fig. 1). However, they not only consume large

numbers of mosquitoes, in both larval and adult

forms, they also predate on different zooplankton

(gnats, midges, small moths, and little tadpoles;

Travis et al. 1985) beetles, and other insects

(Brendonck et al. 2002). Furthermore, Stav et al.

(2000) evaluated the overall consumptive and non-

consumptive (conditioned water) effect of the

nymph of Anax imperator (Aeshnidae: Odonata)

on populations of larval mosquitoes. They found

no difference in the oviposition of the mosquito,

Culiseta longiareolata. Still, the quantitative evalu-

ation of consumption of mosquito larvae by

odonate larvae in the presence of other prey is

warranted. Breene et al. (1990) observed no mos-

quito larvae in the gut of larvae of the damselfly

(Enallagma civile). Their analysis revealed that

the larvae preyed upon chironomid larvae, and

they also found corixids, cladocerans, ostracods,

and aquatic mites. No remains of mosquito larvae

were detected in any of the specimens, even

though mosquito larvae (Aedes, Culex, Culiseta,

Mansonia, and Psorophora) were observed in the

pond where the damselfly larvae were collected

(Breene et al. 1990).

Certain water bugs, e.g., Sphaerodema annu-

latum and S. rusticum (Heteroptera: Belosto-

matidae), are known to utilize mosquito larvae.

Recently it was found, however, that the consump-

tion of larvae by these bugs is dependent on the

density of larval prey in the medium, so a consider-

able amount of mosquito larvae is likely to be left

unconsumed (Pramanic and Raut 2003, Aditya et

al. 2004 2005). None of these agents has shown

any promise for mosquito control, as they have

been proven difficult to rear and store, as well as

being unstable or inefficient in the field. Their abili-

ty to aerially distribute themselves can be an

advantage, as the adults have access to most,

even tiny, water bodies where they lay their eggs.

Therefore, their larvae can be found in small water

tubs and tanks as well, ideal places where mosqui-

toes may breed. Further in-depth studies need to

be done to assess the role of aquatic insects and

their contribution to the control of mosquitoes.

Larvivorous organisms in temporary water

bodies

Temporary or ephemeral aquatic ecosystems

(pools, puddles, floodplains, etc.) are natural,

endorheic bodies of water, which experience a

recurrent dry phase of varying duration. In other

words, temporary aquatic systems are those in

which the entire habitat shifts from being available

to unavailable to aquatic organisms, for a duration

and/or frequency sufficient to affect the entire biota

(Williams 1987 1997). Generally, the hydroperiod

in ephemeral water bodies corresponds to the

breeding periods of mosquitoes, and such bodies

become ideal breeding sites for mosquitoes, par-

ticularly for the genera Aedes and Anopheles

(Laird 1988). In intermittent puddles, the even-

shorter permanence of the habitat makes it favor-

able to breed immature culicids as a consequence

of the rare exposure to predators (Laird 1988,

Sunahara et al. 2002). The composition and den-

sity of larval mosquito communities are strongly

influenced by the ephemeral or permanent nature

of the pools (Campos et al. 2004, Okogum et al.

2005). James (1961 1966) reported that immature

mosquitoes are less exposed to natural enemies in

temporary than in permanent ponds. The most

important suspected invertebrate predators in tem-

porary pools are turbellarians (Blaustein 1990,

Blaustein and Dumont 1990), notonectids, diving

beetles (Coleoptera), dragonfly larvae (Odonata)

(Wiggins et al. 1980, Williams 1987 1997,

Blaustein et al. 1995, Herwig and Schindler 1996,

Spencer et al. 1999), and crustaceans, e.g., tad-

pole shrimp (Su and Mulla 2001). Turbellarians

assume a particularly important position in

ephemeral ponds, as they have the ability to pro-

duce resting eggs which can survive dry periods

(Blaustein 1990). They are present and become

effective within the first few days after rains begin

to fall, while most other invertebrate predators

become effective only later in the hydroperiod of

individual pools or even at a later stage during the

rainy season. The most important flatworm preda-

tors are species of Mesostoma that occur in a wide

range of habitats (Blaustein and Dumont 1990).

These species display a wide variety of predation

mechanisms. Some species produce a kind of

mucus that functions as a toxic web to trap and kill

prey organisms (Dumont and Carels 1987). Other

species just wait to attack the approaching prey

(sit and wait or ambush predation). In addition,

Dumont and Carels (1987) showed that

Zoological Studies 45(4): 447-466 (2006)

456

Mesostoma cf. lingua produces chemicals that are

toxic to various prey organisms, e.g., Daphnia

magna. Turbellarians have been observed to kill

and utilize mosquito larvae as a food source

(Blaustein 1990, Brendonck et al. 2002). Some

species may also actively search for suitable prey

(Schwartz and Hebert 1982) or reveal prey selec-

tivity (Blaustein and Dumont 1990). Freshwater

crustaceans, tadpole shrimp, and some copepods

are adapted to temporary bodies particularly in arid

zones. Besides direct consumption, tadpole

shrimp have also been reported to enhance the

efficacy of some microbial control agents like Bti.

The digging activity and vertical foraging process

of the shrimp in the water column facilitates the

availability of Bti for larval feeding (Su and Mulla

2001). Basic quantitative data have not been

reported in relation to mosquito larval selectivity

patterns of these flatworms in the presence of

other natural prey types (Schwartz and Hebert

1982, Blaustein 1990, Brendonck et al. 2002).

Cyclopoid copepods

Cyclopoid copepods are abundant in eutroph-

ic water bodies and play important roles in their

trophodynamics. Like many predators in aquatic

environments, cyclopoid copepods are known to

strongly influence the structural and functional

organization of prey communities on which they

feed (Kerfoot and Sih 1987, Matsumura-Tundisi et

al. 1990, Irvine and Waya 1993, Plaβmann et al.

1997). Predominantly carnivorous but with an abil-

ity to utilize plants as well (Kumar and Rao 1999a

b), cyclopids have a wide spectrum of potential

food items available in their habitat, including

algae, ciliates, rotifers, cladocerans, and copepod

nauplii. The patterns of prey selection and feeding

rates in this group of invertebrate predators have

been the focus of considerable research (Greene

1983, Williamson 1986, Krylov 1988, Rao and

Kumar 2002).

Some cyclopoids have long been known to

have the ability to utilize mosquito larvae as food

(Hurlbut, 1938, Fryer 1957, Brown et al. 1991a b,

Marten 1990a b, Marten et al. 1994a b, Kay et al.

1992). Kumar and Rao (2003) conducted a series

of behavioral observations of the cyclopoid M.

thermocyclopoides handling and predating on

mosquito larvae. Figure 2 shows the cyclopoid, M.

thermocyclopoides, handling the larvae of Culex

quinquefasciatus. In the laboratory, many species

of Mesocyclops have been shown to prey upon

Ae. aegypti or Anopheles larvae (Marten et al.

1994a b, Brown et al. 1991a b, Kay 1996, Kay et

al. 1992, Mittal et al. 1997, Kumar and Rao 2003).

Furthermore, in many ponds and small water bod-

ies, a strong negative association has been report-

ed between Mesocyclops sp. and larvae of An.

albimanus (Marten et al. 1989, Zoppi De Roa et al.

2002). The ability of certain cyclopoid copepods to

destroy larval mosquitoes was first noted in 1938

by Hurlbut. These“water fleas”were seen prey-

ing on newly hatched larvae. Field experiments in

Rongaroa (French Polynesia) later demonstrated

that Mesocyclops sp. can be used in interventions

against Ae. aegypti (Rivière et al. 1987). Field tri-

als have been conducted to determine whether

copepods can usefully destroy larval Stegomyia

mosquitoes. Macrocyclops albidus was released

into each of about 200 tires arranged in 2 stacks of

about 100 discarded tires each located near New

Orleans (Marten 1990a b). A 3rd stack remained

untreated. Larval Ae. albopictus that had been

numerous in the treated tires at the beginning of

the experiment virtually disappeared within 2 mo.

Adults disappeared about 1 mo later and remained

scarce for at least another year (Marten 1990b,

Marten et al. 1994a b, Nam et al. 1998). These

predators, however, did not reduce the abundance

of the mosquito, Culex salinarius. Field trials are

currently being conducted in different parts of the

world to determine whether this is a good way of

preventing the transmission of diseases.

Preliminary results have been encouraging.

Fig. 2. Image of the cyclopoid copepod, Mesocyclops thermo-

cyclopoides handling mosquito larvae of Culex quinquefascia-

tus.

Kumar and Hwang -- Aquatic Predators and Mosquito Biocontrol 457

Cyclopoids now appear to offer high promise as

biological control agents for Ae. aegypti (Marten et

al. 1994b), An. stephensi (Kumar and Rao 2003),

and Ae. albopictus mosquitoes (Rey et al. 2004).

Malarial mosquito larvae were found to be absent

from aquatic habitats in Latin America (Marten et

al. 1989) that contained natural populations of M.

longisetus (Jennings et al. 1995, Nam et al. 1998,

Marten et al. 1994a b) and virtually disappeared

after M. longisetus and other species of

Mesocyclops were introduced to rice fields and

small marsh areas in Louisiana (Marten et al.

1994b). The technology using predatory cyclopi-

ods for controlling mosquitoes is“appropriate”at

modest costs. However, biological control using

cyclopoids as predators against mosquito larvae

has not received serious consideration in countries

affected by mosquito-borne diseases.

An additional advantage of cyclopoids over

other aquatic predators is that they are wasteful

killers with the capability to kill more mosquito lar-

vae than they actually ingest. If larvae are numer-

ous, they eat a small part of each larva, which

means that each copepod has the capacity to kill

30-40 larvae/d, far more than they actually eat

(Kumar and Rao 2003). In natural water bodies,

they are found in large numbers (Humes 1994).

However, only about 10% of places with water

where mosquitoes might breed contain natural

populations of cyclopoids which can drastically

reduce the survival of mosquito larvae (Brown et

al. 1991a b, Kumar and Rao 2003).

However, not all copepods destroy all mosqui-

toes. Differential selection by copepods is related

to mosquito larval species and instar stage (Fig.

3). Cyclopids show distinct prey selectivity behav-

ioral patterns and their prey selection patterns are

influenced by many attributes of the prey such as

morphology, behavior, and taste (Stemberger

1985, Rao and Kumar 2002, Kumar and Rao

2003). These are known to differ from species to

species (Kumar and Rao 2001, Kumar 2005).

Some species of cyclopoids usually select smaller

prey items from the available prey size spectrum

(Williamson 1980, Stemberger 1985, Kumar 2003),

while others may actively select the largest prey

they can capture (Krylov 1988, Janicki and

DeCosta 1990, Rao and Kumar 2002). The extent

of carnivory in omnivorous cyclopoids appears to

be directly related to their body size (Fryer 1957,

Adrian and Frost 1993). Animal prey selectivity of

omnivorous cyclopoids has been demonstrated to

be a function of their extent of dependence on an

algal diet; for instance, some animals (e.g.,

Mesocyclops thermocyclopoides) can complete

their entire life cycle exclusively on an animal diet,

whereas others (e.g., Cyclops vicinus) have a food

bottleneck in their life cycle (Adrian and Frost

1993, Kumar and Rao 1999b). The selectivity for

animal prey in those species that include algae in

their diet is also influenced by the extent of their

dependence on algae (Adrian and Frost 1993,

Kumar and Rao 1999b). In the laboratory, Kumar

and Rao (2003) studied the prey consumption

rates of the most abundant cyclopoid copepod in

tropical and subtropical water bodies, M. thermo-

cyclopoides on 1st and 4th instar larvae of 2

species of mosquito (An. stephensi and C. quin-

quefasciatus) in relation to their densities. Since

prey vulnerability is a product of prey encounter

rates with and ease of capture by the predator

(Pastorok 1981, Kumar 2005), certain morphologi-

cal and behavioral attributes of different prey

species that determine capturability (Williamson

1980 1983), and their relative proportions (which

Fig. 3. Daily per capita prey killing rates (mean ± SE) of

Mesocyclops thermocyclopoides in relation to the larval density

of the 2 mosquito species Anopheles stephensi (A. s) and

Culex quinquefasciatus (C. q), (A) Instar I and (B) instar IV

(Source: Kumar and Rao 2003).

Species

Prey Density

(A)

(B)

20010050

80402010

Prey Density

Species

No. Consumed No. Consumed

Zoological Studies 45(4): 447-466 (2006)

458

affect encounter rates) in the medium may be able

to explain observed differential larval selectivity

patterns in copepods. Considering this point,

Kumar and Rao (2003) also studied the prey

selectivity of M. thermocyclopoides towards mos-

quito larvae in the presence of alternate prey (the

cladocerans, Moina macrocopa and Ceriodaphnia

cornuta) in different proportions. That laboratory

study demonstrated that M. thermocyclopoides

had biocontrol potential against An. stephensi

even in the presence of alternative prey. However,

against C. quinquefasciatus, there was a signifi-

cant reduction in larval consumption in the pres-

ence of M. macrocopa, but not in the presence of

either D. similoides or C. cornuta. The predaceous

behavior of M. thermocyclopoides against mosqui-

to larvae was comparable to that of M. aspericor-

nis and other cyclopoid species reported earlier

(Brown et al. 1991b). When offered a combination

of instars I and IV, the cyclopoid actively selected

instar-I larvae, avoiding instar-IV larvae of both

mosquito species regardless of their relative pro-

portions in the medium, and with either instar I or

IV, the copepod selected An. stephensi over C.

quinquefasciatus (Fig. 3B; Kumar and Rao 2003).

When prey choice included a cladoceran as an

alternate prey, the copepod selected the cladocer-

an only when the other prey was instar-IV mosqui-

to larvae. Their results point to the potential of M.

thermocyclopoides as a biological agent for con-

trolling larval populations of mosquito species. It

should be noted that the surface area of the con-

tainer is one of the determinants of the predator,s

efficiency of controlling larval mosquitoes

(Sunahara et al. 2002, Lester and Pike 2003).

Therefore, further studies are required to assess

the role of M. thermocylopoides against mosquito

larvae breeding in containers and other small

water-collecting coolers, tires, etc.

It is further advantageous that mosquitoes do

not show habitat avoidance on the basis of info-

chemicals secreted by the copepod (Torres-

Estrada et al. 2001). Recently, those authors

demonstrated that gravid Ae. aegypti females were

significantly more attracted to ovitraps containing

copepods or to ovitraps containing copepod-condi-

tioned water than the controls. They concluded

that the copepod infochemicals may be responsi-

ble for attracting gravid Ae. aegypti females and

may increase the number of potential prey for the

copepod. Such attractants may play an important

role in the surveillance and control of mosquito

populations (Thavara et al. 2004). Additionally, the

cyclopoid can further be used in combination with

Bti to obtain better results (Tietze et al. 1994,

Chansang et al. 2004).

Although M. thermocyclopoides is dominant in

different lakes and ponds, its population is limited

at places where mosquitoes may breed.

Therefore, mass culture of cyclopoids should be

established, and active adult cyclopoids should be

introduced to different mosquito breeding habitats.

The life cycle of cyclopoid copepods and their abili-

ty to thrive on a wide spectrum of food organisms

make mass production easy and inexpensive; fur-

thermore, they are highly resilient and can function

in open containers of any size or shape. Females

are inseminated when entering adolescence, and

no further contact with males is required to pro-

duce 150-250 eggs/wk for their lifespan that can

last for several months (Kumar and Rao 1999a).

For start-up cultures, cyclopoids are collected from

local lakes or ponds (Kumar and Rao 1998), and

cultures can be established using ciliate or rotifer

diets. In an experiment with various diets,

Mesocyclops achieved the highest total fecundity

with mixed food including rotifers, cladocerans,

and algae (Kumar and Rao 1999a). Many species

of Mesocyclops with biocontrol potential against

mosquito larvae are relatively easy to culture, to

maintain, and to deliver to the target areas (Kumar

2003, Kumar and Rao 1998 1999a b, Marten et al.

1994b 2000, Rey et al. 2004). Some of the com-

mon container-dwelling mosquito species, such as

Ochlerotatus (formerly Aedes) notoscriptus, prefer

containers that are not exposed to direct sunlight,

and this is only rarely found in containers such as

stock troughs (Lee et al. 1982, Laird 1990 1995).

Cyclopoid copepods can survive in and colonize

such habitats whereas other predators are more

likely to find larger habitat patches (Washburn

1995).

Among non-copepod crustaceans, notostra-

can tadpole shrimp and malacostracan prawn are

predators of mosquito larvae. They constitute an

important group on many floodplains (Collins

1998). The larvivory efficiency of prawn

(Macrobrachium sp.) was first reported by Pruthi

(1928) followed by Jenkins (1964). Different mala-

costracan species show differential potentials for

predation on larval mosquitoes. For example,

Paratelphusa spinigera and Varuna litterata (Pruthi

1928, Jenkins 1964) are more-aggressive preda-

tors than Macrobrachium borelli and Mac. lamarrei

(Collins 1998). Malacostracan-imposed mortality

on larval mosquitoes recorded by Collins (1998)

was insufficient to consider these malacostrcans to

be potential biocontrol agents of mosquitoes in

Kumar and Hwang -- Aquatic Predators and Mosquito Biocontrol 459

nature (Collins 1998). Notostracan tadpole shrimp

have been considered to be potential predators

adapted to ephemeral aquatic habitats in arid

regions and rice paddy fields (Maffi 1962, Su and

Mulla 2002). Maffi (1962) demonstrated that

Triops granarius had the ability to decimate An.

gambiae larvae in temporary breeding sources

around huts in a village in Somalia. The biocontrol

potential of tadpole shrimp against mosquito larvae

was recently evaluated (Tietze and Mulla 1991,

Fry-O,Brien et al. 1994, Su and Mulla 2001 2005).

The larvicidal ability of tadpole shrimp combined

with their life history strategy (formation of resting

eggs in sediments, egg hatching success on dehy-

dration, faster developmental rates, and high

fecundity; Fry and Mulla 1992) indicates that they

may be a suitable candidate for mosquito larval

control in ephemeral habitats (Fry-O,Brien and

Mulla 1996, Su and Mulla 2002). Furthermore,

tadpole shrimp were demonstrated to have the

potential to enhance the efficacy of microbial con-

trol agents such as Bti for mosquito control as their

digging activity and vertical foraging process in the

water column facilitate the availability of Bti toxin

particles to mosquito larval feeding (Fry et al.

1994, Fry-O,Brien and Mulla 1996). Su and Mulla

(2001) collected useful information with respect to

colonization, stocking, introduction in mosquito

breeding habitats, and establishment of Triops

newberryi for the biocontrol of immature larvae in

ephemeral habitats. Furthermore, Su and Mulla

(2005) recorded negative effects of Bti, B. sphaeri-

cus, and larvicidal oil on the growth and survival of

tadpole shrimp; however, the effect was dependent

on the concentration.

Although highly promising, the practicality of

these biological agents in anti-mosquito programs

remains to be established. It has also been

recorded that native fish (Courtenay and Meffe

1989, Wang 1998, Willems et al. 2005) and

cyclopoid copepods (Marten 1994a b), including

those that mosquitofish affect in their natural habi-

tats, are better and more-efficient control agents.

Therefore, the use of native fish, cyclopoid

species, and tadpole shrimp (in temporary aquatic

habitats) needs to be promoted.

CONCLUSIONS

Interventions targeting vectors of diseases

are essentially the most effective strategies to con-

trol vector-borne diseases. Furthermore, a promis-

ing strategy would be to eliminate the aquatic juve-

nile or larval stages of vectors rather than the

infective adult stage. Much of the current efforts

directed at the development of new mosquito con-

trol tools are confined to the laboratory scale

(Spielman et al. 1993). This type of research lacks

good prospects for managing mosquito-borne dis-

eases in areas of intense transmission. The major

requirement of a program that will help stop the

transmission of mosquito-borne diseases is the

ability to adapt to various water bodies that are

scattered within and around human settlements

where vectorially important mosquitoes predomi-

nantly breed. As an example, a hidden automobile

tire or a broken or unused container in the bath-

room presents an obstacle to any effort in a soci-

ety that respects privacy. Only biological agents

carry the potential for overcoming such obstacles,

and the most likely agents are those represented

by closely related organisms. Toward this end, we

require a program of biological research aimed

towards understanding the factors that limit the

number of mosquitoes. The search efficiency of

the introduced predator and prey selectivity pat-

terns of larvivorous organisms need to be explored

by offering mosquito larvae in combination with

other alternate natural prey. Care needs to be

taken in case the introduced predator preys on or

alters populations of indigenous flora and fauna of

an ecosystem. Establishing a biocontrol agent

requires an understanding of the mechanisms by

which a predator directly or indirectly affects the

community composition. This is also important for

understanding under what set of environmental

conditions a predator will be effective in reducing

mosquito populations. Sometimes the presence of

predators may cause a relaxation of intra- and

interspecific competition. If the predator,s nega-

tive effect on the larval population via consumptive

effects of reduced intra- and interspecific competi-

tion is outweighed by its positive non-consumptive

effects of reduced competition, then the introduc-

tion of larval predators might result in more rather

than fewer mosquitoes. Nutrient regeneration

caused by larval predators is another positive non-

consumptive effect which may negate the con-

sumptive effects. The success in measuring the

efficacy of candidate agents depends on a multi-

tude of factors: (i) characterization of natural

enemy candidates including ecological, morpho-

logical, taxonomical, or genetic markers; (ii) selec-

tion of climatically matching candidates; (iii) evalu-

ation of semi-field or field cage conditions following

quarantine evaluations prior to proceeding with

natural release; (iv) assessment of unintended

Zoological Studies 45(4): 447-466 (2006)

460

impacts; and (v) the potential efficacy of existing

indigenous agents against larval populations.

A combination of life history, population

dynamics, production, and eco-ethological traits

(e.g., fast growth, reduced longevity, viviparity,

high productivity, an intermediate position within

the food chain, plasticity and adaptability in its food

use, and no particularly special habitat require-

ments for reproduction) show that Gambusia intro-

duced into different water bodies around the world

may certainly produce important impacts on the

structure and functioning of native biological com-

munities. It is extremely important to reinforce the

recommendations that Gambusia, the backbone of

biocontrol for 1/4 of a century, should not be intro-

duced into new areas. Mosquito larvae are rarely

found in permanent waters, the sort of habitat

where Gambusia flourishes. They are not likely to

find their way to common mosquito breeding

grounds such as tree holes, old tires, tin cans,

undrained swimming pools, and boats. These,

however, can be suitable habitats for invertebrate

predators like cyclopoids and aquatic insects.

Specific biological control agents for specific life

stages of the mosquito can be used to ensure bet-

ter and more-effective controls. Therefore, it is

recommended that biological control agents be

used that are effective even in such hidden places.

Those found naturally are safe for people and are

economic in their propagation. Turbellarians,

cyclopoid copepods, aquatic insects, and native

fish may prove to be more promising for controlling

mosquito populations. The relative efficiency of

various cyclopoid copepods in different ephemeral

and permanent mosquito breeding habitats, and

the introduction of larvivorous cyclopoids in combi-

nation with other entomopathogens such as Bti

need to be evaluated before being used for effec-

tive mosquito biocontrol.

Acknowledgments: We are thankful to Prof. T. R.

Rao, Univ. of Delhi, for constructive discussions

and particularly his expert help with the photogra-

phy of Mesocyclops thermocyclopoides capturing

mosquito larvae. We immensely benefited from

comments and suggestions made by Prof. H. U.

Dahms, and 5 anonymous reviewers on a previous

version of the manuscript. Thanks are due to

Priyanesh Prasad and Li-Chun Tseng for biblio-

graphic assistance. We acknowledge the National

Science Council, Taiwan for providing a postdoc-

toral fellowship (0940020949 Dt.2005/03/10) to

RK.

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- Approximately 3500 species of mosquitoes were reported from different parts of the world of whichCulex, Aedes, Anopheles, andOchlerotatus are very important genera (Service, 2012). Culex and Anopheles showed the most important public health significance because of their capability to transmit diseases such as malaria, filariasis and arboviral diseases to humans (Kumar & Hwang, 2006). Considering the incidence rate, mortality and morbidity, malaria is still the number one killer in more than 100 developing countries in tropical and subtropical areas.
Diversity and species composition of mosquitoes (Culicidae: Diptera) in Noor County, northern Iran
[Show abstract] [Hide abstract] ABSTRACT: Mosquitoes are highly important as public health problem due to their blood sucking habits and transmitting malaria, arboviruses and other diseases to humans. The present research was undertaken to determine the fauna, abundance, monthly distribution and activity of Culicidae mosquito larvae and adults in Noor County, northern Iran. This cross-sectional, descriptive study was conducted from August 2012 to November 2013 in the rural and urban outskirts of Noor. In each area, natural larval breeding places such as river beds, shallow wells, pits, sewer, marsh, small holes, tracks of animals as well as man-made breeding places like pools and rice paddy fields have been visited monthly for larval collection. To collect adult mosquitoes, human and animal dwellings including bedrooms, store rooms, toilets, barns, stables and pen were surveyed using WHO standard methods. A total of 844 larvae and 1484 adult mosquitoes were caught. Of the 665 Culicinae larvae, 501 were Cx. pipiens (75.3%), 108 Cx. mimeticus (16.2%) and 56 Cx. theileri (8.4%). Of the 179 Anophelinae larvae, 96 were An. hyrcanus (53.6%) and 83 An. maculipennis s.l. (46.4%). Among 889 adult Culicinae, 495 were Cx. pipiens (55.7%), 238 Cx. mimeticus (26.8%), 156 Cx. theileri (17.6%), and from 595 adult Anophelinae 371 were An. hyrcanus (62.4%) and 224 An. maculipennis (37.7%). Anopheles hyrcanus with 96 larvae (53.6%) and 371 adults (62.4%) and Cx. pipiens with 501 larvae (75.3%) and 495 adults (55.7%) showed the highest abundance and distribution in the county calling for more studies on their population, ecology, behavior and probable roles as vectors of various diseases.
Full-text · Article · Mar 2017
Fariborz YazdiSeyed Hassan NikookarMahmoud Fazeli-Dinan+1 more author...Hosseini S.A.
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- At present, biological control of vectors and continuous monitoring of the three systems studied are recommended . The options for controlling mosquitoes in these aquatic systems include maintaining ecological integrity, so that natural predators control mosquito populations, the introduction of larvivorous fish [26, 27] or other natural predators [28][29][30][31] and testing of target-specific bio- pesticides [32, 33]. At the same time, the general public should be encouraged to use mosquito nets and medical practitioners should be provided with facilities for screening immigrants coming from destinations where malaria is suspected to exist.
Species composition and population dynamics of malaria vectors in three previously ignored aquatic systems in Sri Lanka
[Show abstract] [Hide abstract] ABSTRACT: Background In 2015 alone there were an estimated 214 million new cases of malaria across the globe and 438,000 deaths were reported. Although indigenous malaria has not been reported in Sri Lanka since 2012, to date 247 imported cases of malaria have been identified. Knowledge of the locations, behaviour and vectorial capacity of potential malarial vectors is therefore needed to prevent future outbreaks. Attention is now being focused on some previously ignored habitats. Methods Active and abandoned granite and clay quarry pits, located in wet and intermediate zones, and agro wells located in the dry zone of Sri Lanka were mapped and sampled for 1 year, as potential mosquito breeding sites. Species composition and spatio-temporal variation in both malarial and other mosquito larvae were recorded. Results A total of 18 species of mosquito larvae were identified. Other than Anopheles culicifacies, the primary malaria vector, five species of potential malaria vectors (Anopheles vagus, Anopheles varuna, Anopheles nigerrimus, Anopheles peditaeniatus and Anopheles barbirostris) were found in all three aquatic systems. Additionally, Anopheles annularis was found in granite quarries and Anopheles subpictus and Anopheles pallidus in both types of quarry, but only during the initial sampling. Apart from potential malaria vectors, mosquito larvae such as Anopheles jamesii, Culex tritaeniorhynchus, Culex infula and Culex malayi were found in all three habitats at least once during the sampling period. Apart from potential malaria vectors and other mosquito larvae common to all three aquatic systems, Culex gelidus, Culex mimulus and Culex pseudo vishnui were detected in agro wells. Culex gelidus was also detected in granite quarry pits. Culex mimulus, Culex lutzia and Culex fuscocephala were detected in clay quarry pits. Accordingly, a total of 14, 13 and 15 mosquito species were identified in agro wells, granite and clay quarry pits, respectively. Conclusions Although zero occurrence of indigenous malaria has been achieved in Sri Lanka, the current study emphasizes the potential for future epidemics. The presence of native flora and fauna in abandoned granite and clay quarry pits and the need to extract drinking water from agro wells demand bio-sensitive control methods in these three aquatic systems.
Full-text · Article · Dec 2016
Achini FernandoSevvandi JayakodyW.M.H.K. Wijenayake+1 more author...Gawrie N L Galappaththy
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- (Ruderfußkrebse) zu nennen (Kumar & Hwang, 2006& Hwang, 2006).
Research into the Potential to Adapt and Establish of the invasive Asian Tiger Mosquito Aedes (Stegomyia) albopictus (SKUSE)
[Show abstract] [Hide abstract] ABSTRACT: There is general agreement that the former (breeding) macrohabitat of the Asian tiger mosquito, Aedes albopictus (synonym: Stegomyia albopicta) has been described as phytotelmata in the forested areas of Southeast Asia, however, this has changed in the last four decades as it has adapted to more urban areas and antrotelmata. Capable of producing eggs with a certain dry resistance as well as cold hardiness, populations of Ae. albopictus became distributed around the globe. The invasion of the Ae. albopictus across all over the world is thought to be the most rapid spread of any insect species in the last four decades in tropical, subtropical and temperate climate zones. In addition, Ae. albopictus is a potential vector for at least 27 viruses as well as for several parasites and plays a major role in the global transmission of dengue virus and chikungunya virus; and its contribution to the rapid spread of zika virus is currently under investigation. Therefore, this species is considered a serious threat to public health worldwide. This work broaches the issue of three investigations about the potential to adapt and establish stabile populations of the invasive Asian tiger mosquito Ae. albopictus. As a result of these investigations, a high potential for this species to become a threat to public health in many more countries, especially in temperate climatic zones, can be seen. Due to the fact on the one hand that Ae. albopictus can gain fitness advantages due to misapplied vector control measures and on the other hand of the high epigenetically adaptation potential, it is in summary recommended to focus further research on the development of vaccinations for viruses and other pathogens. By doing so, citizens will be protected without putting ecosystems and their services in danger and it is the even more economic solution.
Full-text · Thesis · Nov 2016 · Aquatic Sciences
Aljoscha Kreß
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- Overall, further research is needed to elucidate the effective potential of tadpoles in biocontrol programs against mosquito vectors. Furthermore, a number of omnivorous copepods, which are small aquatic cyclopoid crustaceans, can prey on immature mosquitoes, especially first-instar larvae, but rarely on later stages (Hurlbut, 1938; Marten et al., 1989; Williamson, 1999; Kumar and Hwang, 2006). Several species of copepods, such as Cyclops vernalis, Megacyclops formosanus , Mesocyclops aspericornis, Mesocyclops edax, Mesocyclops guangxiensis, Mesocyclops longisetus and Mesocyclops thermocyclopoides have been reported as active predators of mosquito young instars (Rawlins et al., 1991; ManriqueSaide et al., 1998; Schaper, 1999; Schreiber et al., 1993; Mahesh Kumar et al., 2012 Murugan et al., 2015b,c; Anbu et al., 2016).
Nanoparticles for mosquito control: Challenges and constraints
[Show abstract] [Hide abstract] ABSTRACT: Mosquito control programs are facing important and timely challenges, including the recent outbreaks of novel arbovirus, the development of resistance in several Culicidae species, and the rapid spreading of highly invasive mosquitoes worldwide. Current control tools mainly rely to the employ of (i) synthetic or microbial pesticides, (ii) insecticide-treated bed nets, (iii) adult repellents, (iv) biological control agents against mosquito young instars (mainly fishes, amphibians and copepods) (v) Sterile Insect Technique (SIT), (vi) “boosted SIT”, (vii) symbiont-based methods and (viii) transgenic mosquitoes. Currently, none of these single strategies is fully successful. Novel eco-friendly strategies to manage mosquito vectors are urgently needed. The plant-mediated fabrication of nanoparticles is advantageous over chemical and physical methods, since it is cheap, single-step, and does not require high pressure, energy, temperature, or the use of highly toxic chemicals. In the latest years, a growing number of plant-borne compounds have been proposed for efficient and rapid extracellular synthesis of metal nanoparticles effective against mosquitoes at very low doses (i.e. 1-30 ppm). In this review, we focused on the promising potential of green-fabricated nanoparticles as toxic agents against mosquito young instars, and as adult oviposition deterrents. Furthermore, we analyzed current evidences about non-target effects of these nanocomposites used for mosquito control, pointing out their moderate acute toxicity for non-target aquatic organisms, absence of genotoxicity at the doses tested against mosquitoes, and the possibility to boost the predation rates of biological control agents against mosquitoes treating the aquatic environment with ultra-low doses (e.g. 1 ppm) of green-synthesized nanoparticles, which reduce the motility of mosquito larvae. Challenges for future research should shed light on (i) the precise mechanism(s) of action of green-fabricated metal nanoparticles, (ii) their fate in the aquatic environment, (iii) the possible toxicity of residual silver ions in the aquatic ecosystems are urgently needed, (iv) the standardization of chemical composition of botanical products used as sources of reducing and capping metabolites, (v) the optimization of the green nanosynthetic routes, in order to develop large-scale production of eco-friendly nanomosquitocides.
Article · Aug 2016
Giovanni BenelliAlice CaselliAngelo Canale
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- and Aedes spp.) reduce their activity (Sih 1986; Ohba et al. 2012), and imagines appear to use kairomones of larval predators as a cue to avoid high-predation environments when searching for oviposition sites (Spencer et al. 2002; Ohba et al. 2012; Afify and Galizia 2015). A number of studies focused on predator–prey interactions between culicid mosquito larvae (including the genus Culex) and non-indigenous predators that have received attention as potential biological control agents against these vectors of human diseases (e.g., Krumholz 1948; Rosenheim et al. 1995; Kumar and Hwang 2006). For example, Offill and Walton (1999) compared a common native predator of Culex spp., the three-spined stickleback (Gasterosteus aculeatus Linnaeus) and Gambusia affinis (Baird and Girard), an introduced predator that is often used in mosquito control programs (Krumholz 1948), in terms of their efficiency of larval predation and found higher predation rates in G. affinis.
Adaptive growth reduction in response to fish kairomones allows mosquito larvae (Culex pipiens) to reduce predation risk
[Show abstract] [Hide abstract] ABSTRACT: Phenotypic plasticity is predicted to evolve when subsequent generations are likely to experience alternating selection pressures; e.g., piscine predation on mosquitoes (Culex pipiens) varies strongly depending on habitat type. A prey-choice experiment (exp. 1) detected a predilection of common mosquito predators (sticklebacks, Gasterosteus aculeatus) for large-bodied mosquito larvae, suggesting that larvae could benefit from suppressing growth under predation risk, and experiment 2 confirmed reduced pupa size and weight when we exposed larvae to stickleback kairomones. In experiment 3, we measured adult (imago) size instead to test if altered larval growth-patterns affect adult life-history traits. We further asked how specific life-history responses are, and thus, also used kairomones from introduced Eastern mosquitofish (Gambusia holbrooki), and from algivorous, non-native catfish (Ancistrus sp.). Adult body mass was equally reduced in all three kairomone treatments, suggesting that a non-specific anti-predator response (e.g., reduced activity) results in reduced food uptake. However, imagines were distinctly smaller only in the stickleback treatment, pointing towards a specific, adaptive life-history shift in response to the presence of a coevolved predator: mosquito larvae appear to suppress growth when exposed to their native predator, which presumably reduces predation risk, but also affects body size after pupation. Our study suggests that (a) not all antipredator responses are necessarily predator-specific, and (b) fluctuation in the cost-benefit ratio of suppressing larval growth has selected for phenotypic plasticity in C. pipiens larval life histories. This implies costs associated with suppressed growth, for example, in the form of lower lifetime reproductive success.
Full-text · Article · Apr 2016
Jonas JourdanJasmin BaierRüdiger Riesch+1 more author...Sven Klimpel
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- The entomopathogenic fungus most used in controlling mosquito infestations is Beauveria bassiana, which produces various active ingredients such as beauvericin [92]. The biological control of mosquito larvae with predators and other biological control agents could be a more effective and environmentally friendly strategy, thus avoiding the use of synthetic chemicals and the consequent environmental damage [93]. Among them, some insects and vertebrates such as fish, amphibians, and some mammals have the potential to control mosquito disease–vector populations.
Mosquito-Borne Diseases, Pesticides Used for Mosquito Control, and Development of Resistance to Insecticides
Chapter · Mar 2016 · Aquatic Sciences
Jaime A. Cuervo-ParraTeresa Romero CortésMario Ramirez-Lepe
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April 8, 2016

Goethe-Universität Frankfurt am Main

Kumar and Hwang did an exceptional work here. This review was a great knowledge base for me in order to gain a broad overview about the possibilities of biological vector control and especially mosquito control by predators and btw. as well by parasites and pathogens (not mentioned in the title).

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Larvicidal efficiency of aquatic predators: A perspective for mosquito biocontrol

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Research into the Potential to Adapt and Establish of the invasive Asian Tiger Mosquito Aedes (Stegomyia) albopictus (SKUSE)

Nanoparticles for mosquito control: Challenges and constraints

Adaptive growth reduction in response to fish kairomones allows mosquito larvae (Culex pipiens) to reduce predation risk

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