Insect Science (2005) 12, 381JPUR

Functional response of Ganaspidium utilis

381

Functional response of a parasitoid Ganaspidium utilis (Hymenoptera: Eucoilidae) on the leafminer Liriomyza trifolii (Diptera: Agromyzidae)
L E K H N AT H K A F L E 1 , P O - Y U N G L A I 1 a n d Y I N - F U C H A N G 2
1

Department of Tropical Agriculture and International Cooperation, National Pingtung University of Science and Technology, Pingtung Hsien and 2Asian Vegetable Research and Development Center, Shanhua, Tainan, Taiwan, China Abstract Functional response of a solitary, larval-pupal endoparasitoid of Liriomyza leafminers, Ganaspidium utilis Beardsley, was estimated on Liriomyza trifolii Burgess at three temperatures (17 , 25 , 29 ) and host densities. A type II random parasitoid equation (RPE) was used to estimate instantaneous search rate and handling time. The instantaneous search rate increased as temperature increased. All of the RPE regressions obtained for functional response of G. utilis at different temperatures were significant (P < 0.01). The slope of RPE regression lines was lower across the temperatures. At 29 2 , the maximum number of larvae parasitized was 7.8 per day. It decreased to 7.2 larvae parasitized at 25 2 . At 17 2 , no significant increment of parasitization was observed due to the host density increments. The estimated handling time was lowest at 17 2 and highest at 25 2 , respectively. The ability of G. utilis to find and parasitize L. trifolii over a wide range of temperatures makes them a good candidate for biological control of Liriomyza leafminers. Key words functional response, Ganaspidium utilis, host density, Liriomyza trifolii, random parasitoid equation, temperature DOI 10.1111/j.1744-7917.2005.00047.x

Introduction Liriomyza trifolii Burgess, L. bryoniae Kaltenbach and L. sativae Blanchard have caused serious damage to ornamentals and vegetables from 1984 to 1995 in Taiwan (Chien, 1997). Chien and Ku (1996) reported that in Taiwan the most favorable temperature for survival of L. trifolii ranges from 15 to 25 . The Liriomyza species has been known to be regulated by many natural enemies in their native ranges (Murphy & LaSalle, 1999). For example, in Taiwan, Hemiptarsenus varicornis Girault,

Correspondence: Lekhnath Kafle, Department of Tropical Agriculture and International Cooperation, National Pingtung University of Science and Technology, 1 Hsuen Fu Road, Neipu Hsiang, Pingtung Hsien, Taiwan, China. Tel: +886 95 339 5546; fax: +886 87 740 446; e-mail: kafleln@rediffmail.com

Neochrysocharis formosa Westwood, Chrysocharis pentheus Walker and Chrysonotomyia okazakii Kamijo were reported as native parasitoid species of L. trifolii (Chien & Ku, 2001). Ganaspidium utilis Beardsley (Hymenoptera: Eucoilidae) is a solitary, larva-pupal endoparasitoid that was introduced into Hawaii from the Weslaco area of Texas for the control of L. trifolii and L. sativae (Nakao & Funasaki, 1979). It was successfully established in Hawaii, Marianas, Tonga and Guam and became an important biological control agent of Liriomyza spp. (Lai & Funasaki, 1986; Greathead & Greathead, 1992; Johnson, 1993). In 2003, G. utilis was introduced to Taiwan from Hawaii for control of L. trifolii, L. bryoniae and L. sativae. The functional response of a parasitoid is a key factor regulating the population dynamics of parasitoid-host systems (Pervez & Omkar, 2005). The number of hosts attacked per parasitoid is used as the experimental measure
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of the functional response (Mills & Getz, 1996; Lynch, 1998). The assumptions made are that the parasitoid search is random and the host population is distributed at random and is homogenous. The functional response can determine the efficiency of a parasitoid in regulating host populations (Murdoch & Oaten, 1975). The general form of the functional response has been categorized into three types, according to the shape of the response curve (Holling, 1959, 1965). The functional response curves can be differentiated by evaluating the parameters, namely coefficient of instantaneous search rate and handling time. The coefficient of instantaneous search rate estimates the steepness of the increase in parasitization with increasing host density, and handling time helps estimate the satiation threshold (Pervez & Omkar, 2005). Previous studies described the biology (Petcharat & Johnson, 1988), cost-effective method for mass production (Rathman et al., 1991), pesticide susceptibility (Rathman et al., 1995) and demographic study of G. utilis by Omer et al. (1996). There have been no reports on the functional responses of G. utilis parasitizing L. trifolii. Therefore, this study describes the functional response of G. utilis on L. trifolii larvae at different temperatures.

leaves were cut at the base and kept in closed plastic containers to allow L. trifolii larvae to pupate. Leafminer puparia were collected and held in a Petri dish (9 cm diameter) until G. utilis adults emerged. Parasitoid adults were returned to oviposition cages for either culture maintenance or used in subsequent studies. Rearing of the G. utilis population was carried out in a laboratory at 25 2 , 50% 10% RH and a photoperiod of 14:10 (L: D). Functional response test To quantify how many L. trifolii larvae can be parasitized by one G. utilis female at different host densities in a period of 24 hours, a functional response test was conducted. For this test, eight host densities per cage (0.008 m3) at 10, 20, 30, 40, 50, 60, 70 and 80, late 2nd or early 3rd instar leafminer larvae were tested. To determine the minimum host density for functional response test, a preliminary study on the parasitization rate of G. utilis was conducted. The results of the preliminary study showed that the host parasitization rate was lower than 10 L. trifolii larvae per day across the temperatures (17 2 , 25 2 and 29 2 ). The leafminer larvae in each plant were counted and plants were arranged in order to obtain the proper leafminer density required for each experimental density. Plants infested with the exact number of leafminer larvae for each density were placed separately in a cage, where one pair of newly emerged parasitoid adults was introduced. Honey-water solution (25%) was sprayed on the lima bean leaves as food supplement source for the parasitoid adults. Leafminer larvae on infested plants at each host density were exposed to the parasitoids for parasitization for 24 hours. After exposing to the parasitoids for 24 hours, the plants were removed from the cylinder and pupae were collected at each host density and placed separately in a Petri dish (9 cm diameter). Data on the number of L. trifolii and G. utilis adults emerging daily were recorded. A type II random parasitoid equation (RPE) (Royama, 1971) was used to estimate instantaneous search rate and handling time for each temperature, using a nonlinear procedure (SAS, 2003): Na = Nt { 1Jexp ( J aTPt/1 + aThNt )} , (1)

Materials and methods Leafminer Late second or early third instar L. trifolii larvae were used as host insects. Six pairs of Phaseolus Henderson lima bean plants (2 leaves each) were placed for 6 hours in a screen cage containing 50J60 L. trifolii adults. After 6 hours, bean plants were removed from the cage and held for 5 days to allow L. trifolii eggs to hatch and develop until they reached the late 2nd or early 3rd instar. This work was carried out in a laboratory at 25 2 , 50% 10% RH and a photoperiod of 14:10 (L: D). Rearing of G. utilis G. utilis parasitoids used in this study were obtained from a laboratory culture using L. trifolii as the host insect. The L. trifolii colony was maintained in the laboratory using the methods described by Rathman et al. (1991). G. utilis was reared by using the methods as described by Petcharat and Johnson (1988). Stems of L. trifolii-infested bean plants (2 leaves each) were cut immediately above the roots and placed in a 200 mL flask filled with water. A honey-water solution (25%) was sprayed on lima bean leaves as a food source for adult parasitoids. Plants were exposed to G. utilis for 24 hours and then removed. The

where, Na is the number of hosts parasitized, Nt is the number of hosts available, a is the instantaneous search rate, T is the duration of the experiment in days, Pt is the number of parasitoids and Th is the parasitoid handling time. The instantaneous search rate and parasitoid handling time was analyzed based on 14 hours (0.58 day) assuming
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that activity of G. utilis occurred only during the daylight. To evaluate the parasitism of G. utilis across the densities, the numbers of G. utilis adults emerged from L. trifolii pupae were counted and means were analyzed by using the SNK test of SAS (2003). This study was replicated 10 times and carried out in a laboratory at 17 2 , 25 2 and 29 2 , 50 10% RH and a photoperiod of 14:10 (L: D).

Table 1 Estimates of instantaneous search rate and handling time for Royama (1971) type II disk equation for G. utilis. Temperature 17 2 25 2 29 2

a† 0.0128 0.0220 0.0237

Th‡ 0.049 0.056 0.053

T/ Th§ 20.40 17.85 18.86

r2 36.2 36.9 58.6

Results The differences in the mean number of L. trifolii parasitized by an individual G. utilis female on 30, 40, 50, 60, 70 and 80 L. trifolii larvae density were significant (P < 0.05) across temperatures. However, the mean number of L. trifolii parasitized by an individual G. utilis female on 30, 40, 50, 60, 70 and 80 L. trifolii larvae per cage were not significant (P < 0.05) at 29 2 and 25 2 . In addition, the differences in the mean number of L. trifolii larvae parasitized by an individual G. utilis female on 10 and 20 L. trifolii larvae per cage were not significant (P < 0.05) across temperatures. The trend obtained from graphical plotting of mean number hosts parasitized by a G. utilis female at 29 2 and 25 2 showed a higher slope than the curve obtained at 17 2 (Fig. 1). It was revealed that the estimated instantaneous search rate of G. utilis was increased with increasing temperatures (Table 1). The estimated handling time was lower when the temperature was higher or lower than 25 2 . The handling time was highest at 25 2 and lowest at 17 2 (Table 1). Values for the instaneous search rate and handling time were obtained by employing the type II RPE (Royama,

Instantaneous search expressed as per day at different temperatures; ‡handling time expressed as day/s at different temperatures; §estimated maximum numbers of L. trifolii larvae parasitized by one G. utilis female per day.

1971). The analyses of the mortality factor across temperatures were done separately and the type II functional response curve was obtained (Fig. 1). In this type of functional response curve, the number of L. trifolii attacked and parasitized by a G. utilis females increased at a decreasing rate until reaching an upper plateau with the increase of the number of L. trifolii provided for parasitization for 24 hours. The upper plateau was fixed by the handling times, which were 44.4, 46.8 and 41.2 minutes across temperatures, respectively for the parasitic action. Similarly, the estimated maximum numbers of L. trifolii larvae that can be parasitized by a G. utilis female were 20.4, 17.85 and 18.86 at 17 2 , 25 2 and 29 2 , respectively (Table 1). Following the RPE (1971), the number of L. trifolii parasitized by an individual G. utilis female on different densities of L. trifolii for 24 hours was calculated as equation 2, 3 and 4 for 29 2 , 25 2 and 17 2 , respectively. Na = Nt {1Jexp (J 0.0237 / 1 + 0.0012561 Nt)} , Na = Nt {1Jexp (J 0.022 / 1 + 0.001232 Nt)} , Na = Nt {1Jexp (J 0.0128 / 1 + 0.0006272 Nt)} . (2) (3) (4)

Discussion At all tested temperatures, the number of L. trifolii parasitized increased in a decreasing rate as the density increased, following the type II functional response curve proposed by Royama (1971) (Fig. 1). However, the decreasing rates were lower at 17 2 than other temperatures. This type II functional responses has been reported previously for a number of parasitoids in laboratory experiments (Patel et al., 2003; Menon et al., 2002). Because of the decelerating increase of the number of L. trifolii parasitized as its density increases, the mortality rate decreases exponentially as the L. trifolii density increases. As the number of L. trifolii per container increases to more than 20.4 (17 2 ), 17.86 (25 2 ),

Fig. 1 Type II curve for functional responses of G. utilis. Prediction of the number of L. trifolii parasitized by an individual G. utilis female as provided with different densities of L. trifolii larvae for 24 hours for parasitization at different temperatures.

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and 18.87 (29 2 ) as shown in T/Th (Table 1), the parasitic action of an individual G. utilis female does not represent an important mortality factor for L. trifolii. Therefore, an individual parasitoid female does not exert an efficient control of L. trifolii. As a result, the population of L. trifolii escapes the suppression pressure by G. utilis. To avoid L. trifolii escaping from the suppression pressure of G. utilis, an increase in the number of G. utilis females based on the temperature of the infested area and leafminer density per plant is required. Before releasing the parasitoid in the infested area, estimation of the population of leafminers per unit of area or per crop unit is necessary (e.g., number of L. trifolii per leaf) because habitat parameters as well as host density and distribution play an important role in host-parasitoid interactions (Meiners & Obermaier, 2004). This study demonstrated that when the L. trifolii larvae density per plant reached 30, depending upon the temperature, seven (25 2 and 29 2 ) or 13 (17 2 ) G. utilis females were able to regulate the L. trifolii infestation within 14 hours in the lab conditions. However, the mutual interference among parasitoids searching for hosts is another factor that affects the numbers of parasitoids needing to be released to control the specific number of hosts, and this also should be considered before the release. The RPE was fitted separately for each temperature in order to compare the search rate and handling times across different temperatures (Table 1). The instantaneous search rate increased as temperature increased (Table 1), and increased with increasing host density (Fig. 1). This might be due to the higher chances of an encounter by G. utilis females with hosts when host density increased. G. utilis female s activeness increased as the temperature increased, resulting in an incremental chances of encountering hosts. All of the RPE regressions obtained for functional response of G. utilis at different temperatures were significant (P < 0.01). The slope of RPE regression lines was low across the temperatures. At 29 2 , the maximum number of larvae parasitized was 6.4 in a 24-hour period. This decreased to a maximum of six larvae parasitized at 25 2 . At 17 2 , there was no significant increment of parasitization due to the host density increments. A short handling time increases the time available for search and hence the likelihood of finding additional hosts. The estimated handling time was lowest at 17 2 and highest at 25 2 (Table 1). An unavoidably long handling time can be compensated for by a long searching period (Menon et al., 2002). In conclusion, the ability of G. utilis to find and parasitize L. trifolii over a wide range of temperatures in laboratory conditions, makes them good candidates for natural control of Liriomyza leafminers in areas where temperature

fluctuations are 17

2

to 29

2

.

Acknowledgments The authors would like to express their thanks to Dr Ethel M. Vilalobos and Dr Larry Nakahara for donating and hand-carrying the parasitoids to Taiwan from Hawaii. Thanks are also due to the National Pingtung University of Science and Technology for offering scholarship and other supportive facilitates for this study.

References
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Meiners, T. and Obermaier, E. (2004) Hide and seek on two spatial scales-vegetation structure effects herbivore oviposi tion and egg parasitism. Basic and Applied Ecology, 5, 87J94. Mills, N.J. and Getz, W.M. (1996) Modelling the biological control of insect pests: a review of host-parasitoid models. Ecological Modelling, 92, 121J143. Murdoch, W.W. and Oaten, A. (1975) Predation and population stability. Advances in Ecological Research, 9, 1J131. Murphy, S.T. and LaSalle, J. (1999) Balancing biological control strategies in the IPM of new world invasive Liriomyza leafminers in field vegetable crops. Biocontrol News and Information, 20, 91J104. Nakao, H.K. and Funasaki, G.Y. (1979) Introductions for biological control in Hawaii-1975 and 1976. Proceeding of the Hawaiian Entomological Society, 23, 125J128. Omer, A.D., Johnson, M.W. and Tabashnik, B.E. (1996) Demography of the leafminer parasitoid Ganaspidium utilis Beardsley (Hymenoptera: Eucoilidae) at different temperatures. Biological Control, 6, 29J34. Patel, K.J., Chustere, D.J.S. and Smerage, G.H. (2003) Density dependent parasitism and host-killing of Liriomyza trifolii (Diptera: Agromyzidae) by Diglyphus intermedius (Hymenoptera: eulophidae). Florida Entomologist, 86, 8J14.

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Accepted June 30, 2005

Insect Science 12, 381J385

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