A Study on the Functional Responses of Gambusia affinis to Aedes albopictus Skuse

Research Article

A Study on the Functional Responses of Gambusia affinis to Aedes albopictus Skuse

Corresponding author: Dr. Lijuan Liu, Shandong Academy of Medical Sciences, Shandong Institute of Parasitic Diseases, Jining, 272033, China, Tel: +86 15866073249, Email: jj8liu@sina.com

Abstract

In this study, the predation of Gambusia affinis (Baird et Girard) to Aedes albopictus Skuse was studied in a laboratory. The results show that the functional response of G. affinis to Ae. albopictus qualifies as Holling’s type III. The model parameters for this group were estimated as follows: the search rate (a) of G. affinis (female and male) to Ae. albopictus were 0.0524, 0.0656. The experimental data can be described using Hassell’s equation and Wang Shize’s equation. The effect of different levels of hunger on the predation of G. affinis indicated that hunger could not change the functional response types but sim- ply affected the functional response parameters. The handling times for female G. affinis for 12 hours, 24 hours, 36 hours, and 48 hours of starvation were 0.1317, 0.1143, 0.0086, and 0.0830, respectively, and the handling times for male Gambusia affinis were 0.3784, 0.3902, 0.3447, and 0.1390, respectively. As the level of hunger increased, the handling times for female and male G. affinis reduced. When the spatial heterogeneity was complex, the functional response of female adult G. affinis specimens on Ae. albopictus showed the Holling III property and the functional response of male adult of G. affinis on Ae. albopictus showed the Holling I property.

Keywords: Gambusia affinis (Baird et Girard); Aedes albopictus Skuse; Functional response

Introduction

Gambusia affinis, a member of the family Poeciliidae of order Cyprinodontiformes [1], is a small ovoviviparous tropical fish native to the lowlands and ditches on the Atlantic coast of North America and is known to consume mosquito lar- vae. So far, G. affinis have been introduced throughout the world to control larval mosquito populations in aquatic en- vironments. Scientists in many countries have conducted detailed laboratory and field studies on G. affinis , demon- strating that G. affinis have the potential for biological con- trol of mosquitoes [2,3,4]. According to literature, G. affinis were introduced to Shanghai, China in 1927 from Manila, the Philippines. Relevant studies on their mosquito and malaria control have been reported domestically. However, most of the reports focused on experimental observations instead of detailed theoretical analysis. Ae. albopictus is a common spe- cies of mosquitoes in China and Southeast Asia that has long activity seasons, rapid population growth, and the habit of repeated bloodsucking, the mosquito is a primary medium for communicating dengue fever. Currently, one of the most

popular methods of mosquito control is through conven- tional insecticides, unfortunately, long-term extensive use of chemical pesticides has negatively affected the environ- ment and increased mosquitoes’ resistance to insecticides [5,6]. We have reexamined the studies and applications of biological control methods. We conducted an indoor study of

G. affinis to Ae. albopictus larvae and the effects of spatial het- erogeneity and levels of hunger on the functional responses of G. affinis to study the predation of G. affinis on Ae. albopic- tus larvae, scientifically evaluate the control of G. affinis over mosquitoes and determine strategies to better use G. affinis as a mosquito predator.

Materials and Methods

The experimental G. affinis subjects were caught from the pond of South China Agricultural University and fed on ar- tificial diet (Shandong Beisen fish feed Co., Ltd., China) in- doors for a year. Resulting small fish that were born in cap- tivity were fed until they reached sexual maturity. Subjects exhibiting agility were selected for the experiment. The ex-

perimental female G. affinis had an overall length of 3.0 cm, and the males had a length of 2.3 cm. The Ae. albopictus lar- vae were fed on a mix of pork liver powder and yeast powder

The relationship between the instantaneous attack rate a and the initial prey density Nt is:

at a temperature of 28 °C, a relative humidity of 70%~80%, and a photoperiod of 14L:10D. The fourth-instar larvae of

a  bNt

1 cNt

(2)

Ae. albopictus were used.

The experimental crispers were 290×200×115 mm3. Each

The new model of Holling’s type III functional response derived by Wang Shize et al. is:

crisper was filled with 1800 ml of tap water that had been left undistributed for 1 day. The experimental water tem- perature was 28 °C.

N Aexp( B )

Nt

a

(3)

The functional responses of Gambusia affinis to Aedes albopictus

The density of G. affinis predators was set at 1. The density of female per crisper Ae. albopictus larvae prey was set at 80, 100, 120, 140, 160, 180, and 200, totaling seven treatments with each treatment repeated four times. The density of male Ae. albopictus larvae prey was set at 15, 20, 25, 30, 40, 50, and 60, totaling seven treatments with each treatment repeated four times. The number of Ae. albopictus larvae were counted after twenty-four hours.

The effect of spatial heterogeneity on the predation of

Gambusia affinis

Stones (7×6×7 cm3) were used as barriers in the experiment. A stone was placed at each corner of the experimental crisp- ers with space left surrounding the stone to ensure the free movement of the G. affinis. All other variables were identical as outlined in 1.1.

The functional responses of Gambusia affinis at differ- ent levels of hunger to Ae. albopictus

G. affinis predators were set at a density of 1 and starved for 12 h, 24 h, 36 h, and 48 h. After the G. affinis were starved for 12 h, the density of female Ae. albopictus larvae was set at 30, 50, 80, 100, 120, 140, and 160, respectively (males: 30, 40, 50, 60, 70, and 80); after the G. affinis were starved for 36 h, the density of female Ae. albopictus larvae was set at 30, 50, 75, 100, 120, 140, and 160, respectively (males: 15, 20, 25, 30, 40, 50, and 60); after the G. affinis were starved for 48 h, the density of female Ae. albopictus larvae was set at 80, 100, 115, 130, 140, and 160, respectively (males: 35, 40, 50, 60, and 70). The experiment for a 24 h starvation period was conducted as outlined in 1.1.

The analysis method for functional responses

The functional response types of G. affinis to Ae. albopictus larvae were judged based on the scatter plot and the func- tional-response model derived by Real, and a reasonable Holling model was selected for fitting analysis.

The mathematical model of Holling’s type III functional response is [7]:

where Na is the number of prey consumed, Nt is the initial

prey density, T is the total time predators, and prey is ex- posed to each other (T =24 h), Th is handling time, a is the instantaneous attack rate, Pt is the predator density, A is the maximum number of prey consumed by a natural enemy, B is the optimal search density when a natural enemy’s den- sity is 1, and b and c are parameters.

Data processing

Data analysis was conducted on the statistical software IBM SPSS statistics [8].

Results

The functional responses of Gambusia affinis to Aedes albopictus larvae

According to the indoor measurements of G. affinis’ preda- tion at different prey densities, the functional responses of male and female G. affinis to Ae. albopictus larvae belonged to Holling’s type III. Figure 1 shows the relationship between the number of prey consumed and the prey density. In this paper, Hassell’s model (see Equations 1 and 2) and Wang Shize’s new model of functional response (see Equation 3) were used for fitting. The parameters and test results of the models are shown in Table 1. The analysis results of the data fitted by the two models are shown in Table 2. The relevant coefficients of the various equations were greater than 0.98. The F values of the F tests were greater than F=0.01, indi- cating that Hassell’s model and Wang Shize’s new model of functional response could appropriately describe the preda- tion of G. affinis on Ae. albopictus at different prey densities. The relevant coefficients of Hassell’s model were all greater than the relevant coefficients of Wang Shize’s new model of predation, and the mean square errors of Hassell’s model were smaller than those of Wang Shize’s new model of pre- dation. The data fitted by Hassell’s model were better than those fitted by Wang Shize’s new model of predation.

The effect of spatial heterogeneity on the functional response

In the presence of barriers, the functional response of female

G. affinis to Ae. albopictus still belonged to Holling’s type III, and the functional response of male G. affinis to Ae. albopic- tus changed to Holling’s type I. Table 3 shows the parameters and test results of the models. Figures 2 show the relation-

N =N [1- exp{- bNt Pt (T Th Na )}]

a t

1+cNt Pt

(1)

ship be tween the number of prey consumed and the prey

density.

Females (type III) Males (type III)
Wang Shize N =168exp(- 68 )

a N

N  61exp(- 27 )

a N

t t
(F=638.6 P<0.0001, R=0.9803) (F=419.04 P<0.0001, R=0.9712)
Hassel Na Nt [1 exp(0.00113Nt (24  0.1143Na ))]

(F=319.06 P<0.0001, R=0.9844)

Na Nt [1 exp(0.00171Nt (24  0.3902Na ))]

(F=116.72 P<0.0001, R=0.9903)

Table 1. The functional responses of G. affinis to Ae. Albopictus.

Hassel’s model Wang Shize’s model
Mean square error (MSE) R Mean square error (MSE) R
Females 105.1 0.9844 206.8 0.9803
Males 14.5613 0.9903 107.8 0.912

Table 2. Comparison of the analysis results of the two models.

Figure 1. The functional responses of G. affinis to Ae. Albopictus.

Females (type III) Males (type III)
Wang Shize N  172 exp(- 71)

a N

t

(F=1817.59 P<0.0001, R=0.9898)

Na=0.5857Nt-1.4643
Hassell Na Nt [1 exp(0.00136Nt (24  0.1538Na ))]

(F=409.54 P<0.0001, R=0.9927)

(F=69.65, P<0.0001, R=0.9945)

Table 3. The functional responses of G. affinis in the presence of barriers.

Figure 2. The functional responses of G. affinis in the presence of barriers.

The effect of hunger on the functional response of

Gambusia affinis

The functional responses of G. affinis at different levels of

hunger to Ae. albopictus larvae all belonged to Holling’s type

III. Table 4 shows the fitting results and primary model pa- rameters; it demonstrates that at different levels of hunger,

G. affinis had different search rates and handling times for Ae. albopictus larvae. The search rate decreased as the level of hunger increased.

G. affinis’s search rate was the highest after 12 h of starva- tion, being 0.0811. After 36 h of starvation, the search rate showed a slight increase. The maximum number of prey consumed by G. affinis A increased as the level of hunger in- creased, and the maximum number of prey consumed after 48 h of starvation was the greatest. Figures 1 and 3 show the relationship between the number of prey consumed and the prey density.

Time Wang Shize’s model Hassel’s model
A B F R a Th F R
12 h Females 156 60 931.30 0.9781 0.0704 0.1317 302.59 0.9902
Males 49 17 1440.88 0.9658 0.0689 0.3784 85.19 0.9840
24 h Females 168 68 638.66 0.9803 0.0524 0.1143 319.06 0.9844
Males 61 27 975.32 0.9712 0.0656 0.3902 116.72 0.9903
36 h Females 232 100 419.04 0.9389 0.0297 0.0086 235.60 0.9778
Males 65 27 849.84 0.9868 0.0606 0.3447 247.19 0.9788
48 h Females 298 134 1549.8 0.9704 0.0298 0.0830 346.84 0.9801
Males 81 47 544.55 0.9952 0.0245 0.1390 225.74 0.9956

Table 4. The parameters for the functional responses of G. affinis at different levels of hunger to Ae. Albopictus.

12 h ♀

The maximum number of prey consumed

36 h ♀

12 h ♂

36 h ♂

48 h ♀

The density of prey

48 h ♂

Figure 3. The functional responses of G. affin is at different levels of hunger to Ae. Albopictus larvae.

Conclusion

In addition to the characteristics of a natural enemy itself, pest density is one of the most important factors that affect the natural enemy’s predation. Holling [9] called the re- sponse of a natural enemy to the changes in the pest density in terms of the number of prey consumed a functional re- sponse, which is an ideal method for determining a preda- tor’s predation potential. A functional response not only reflects a predator’s search ability, handling efficiency, and the maximum amount of prey consumed for prey, it also contains the effects of a natural enemy’s predation dynamics and the behavior and density of pests on the natural enemy’s predation. The functional response of G. affinis to Ae. albopic- tus larvae belonged to Holling’s type III, which is consistent with the functional responses of vertebrates such as Phoe- nicopterus roseus [10], bonnetheads [11] and mice [12]. In this paper, Wang Shize’s new model of functional response and Hassell’s [7] model were used to fit the predation re- sults. Both models could appropriately describe the preda- tion of G. affinis at different prey densities on Ae. albopictus larvae. Hassell’s model could fit two biological factors, attack rate a and handling time Th, and are of great theoretical sig- nificance; Wang Shize’s new model of predation could fit the parameter of the optimal search density. Therefore, Hassell’s model and Wang Shize’s model can complement each other. For biological mosquito control, the optimal number of G. affinis released can be determined based on the density of mosquitoes in the environment.

The functional response of a natural enemy is significantly affected by space, the environment, and its level of hunger. Under this study’s experimental conditions, the level of hun- ger could not change the type of the functional response of G. affinis to Ae. albopictus larvae. However, as spatial com- plexity increased, the functional response of male G. affinis to Ae. albopictus larvae changed from type III to type I, which validated the conclusion drawn by Moustahfid [13]— that the functional response type will change as the environment changes.

Other studies have found that G. affinis also prey on tadpoles, fry, mayfly naiads, and aquatic plankton (primarily rotifers, cladocerans, and copepods) in addition to mosquitoes [14- 16]. Therefore, G. affinis has been reported to pose a threat to local species and is listed as one of the world’s 100 malig- nant alien invasive species. However, it has been found that when multiple species coexist, G. affinis first prey on mos- quito larvae and pupae. Meanwhile it had no effect on the numbers of all invertebrate predators [17,18]. In addition, the experiment in this paper was conducted in an indoor en- vironment where both the prey and the predator were in a controlled, simple closed system. Therefore, the experimen- tal results are different from the number of prey consumed in our natural environment, and the functional responses and mutual interference at natural states require further study.

Acknowledgments

This work is supported by the National Natural Science Foundation of China (Grant No. 30270279 ).

References
  1. Fernández-Delgado C. Life-history patterns of the mosqui- to-fish, Gambusia affinis, in the estuary of the Guadalquivir river of southwest Spain. Freshwater Biology. 1989, 22(3): 395-404.
  2. Billman EJ, Wagner EJ, Arndt RE. A comparison of mos- quito consumption and prey selection between least chub (Iotichthys phlegethontis) and western mosquitofish (Gam- busia affinis). Western North American Naturalist. 2007, 67(1): 71-78.
  3. Mulligan FS III, Farley DG, Caton JR, Schaefer CH. Survival and predatory efficiency of gambusia-affinis for control of mosquitos in underground drains. Mosquito News. 1983, 43(3): 318-321.
  4. Prasad H, Prasad RN, Haq S. Control of mosquito breed- ing through Gambusia affinis in rice fields. Indian J Malariol. 1993, 30(2): 57-65.
  5. Karunaratne SHPP, Weeraratne TC, Perera MDB, Suren- dran SN. Insecticide resistance and, the efficacy of space spraying and larviciding in the control of dengue vectors Aedes aegypti and Aedes albopictus in Sri Lanka. Pestic Bio- chem Physiol. 2013, 107(1): 98-105.
  6. Marcombe S, Farajollahi A, Healy SP, Clark GG, Fonseca DM. Insecticide resistance status of United States populations of Aedes albopictus and mechanisms involved. PLoS one. 2014, 9(7): 1-10.
  7. Hassell MP, Lawton JH, Beddington JR. Sigmoid functional responses by invertebrate predators and parasitoids. Jour- nal of Animal Ecology. 1977, 46(1): 249-262.
  8. Patil PB, Reddy BPN, Gorman K, Reddy KV, Barwale SR et al. Mating competitiveness and life-table comparisons be- tween transgenic and Indian wild-type Aedes aegypti L. Pest Manag Sci. 2015, 71(7): 957-965.
  9. Holling CS, Buckingham S. A behavioral model of predator- prey functional responses. Behavioral Science. 1976, 21(3): 183-195.
  10. Deville AS, Grémillet D, Gauthier-Clerc M, Guillemain M, Houwald FV et al. Non-linear feeding functional responses in the Greater Flamingo (Phoenicopterus roseus) predict im- mediate negative impact of wetland degradation on this flag- ship species. Ecology and evolution. 2013, 3(5): 1413-1425.
  11. Kroetz AM, Powers SP. Eating between the lines: func- tional feeding response of bonnetheads (Sphyrna tiburo). Environmental biology of fishes. 2015, 98(2): 655-661.
  12. Schauber EM, Ostfeld RS, Jones CG. Type 3 functional re- sponse of mice to gypsy moth pupae: is it stabilizing? Oikos. 2004, 107(3): 592-602.
  13. Moustahfid H, Tyrrell MC, Link JS, Nye JA, Smith BE et al. Functional feeding responses of piscivorous fishes from the northeast US continental shelf. Oecologia. 2010, 163(4): 1059-1067.
  14. Leyse KE, Lawler SP, Strange T. Effects of an alien fish, Gambusia affinis, on an endemic California fairy shrimp, Linderiella occidentalis: implications for conservation of diversity in fishless waters. Biological Conservation. 2004, 118(1): 57-65.
  15. Mansfield S, Mcardle BH. Dietary composition of Gambu- sia affinis (Family Poeciliidae) populations in the northern Waikato region of New Zealand. New Zealand Journal of Ma- rine and Freshwater Research. 1998, 32(3): 375-383.
  16. Rupp HR. Adverse assessments of Gambusia affinis: an alternate view for mosquito control practitioners. J Am Mosq Control Assoc. 1996, 12(2): 155-159.
  17. El SSH, Haridi AA, El RFM. The impact of the exotic fish Gambusia affinis (Baird and Girard) on some natural preda- tors of immature mosquitoes. J Trop Med Hyg. 1985, 88(2): 175-178.
  18. Mischke CC, Griffin MJ, Greenway TE, Wise D. Effects of Mosquitofish, Gambusia affinis, on Channel Catfish, Ictalurus puncatatus, Production Ponds. Journal of the World Aqua- culture Society. 2013, 44(2): 288-292.

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