Influência da temperatura no desenvolvimento de Euborellia annulipes (Lucas) (Dermaptera: Anisolabididae), predador do bicudo-do-algodoeiro

Age-Dependent Fecundity and Life-Fertility Tables for Euborellia annulipes (Lucas) (Dermaptera: Anisolabididae) a Cotton Boll Weevil Predator in Laboratory Studies with an Artificial Diet Author(s): W. P. Lemos, F. S. Ramalho, and J. C. Zanuncio Source: Environmental Entomology, 32(3):592-601. Published By: Entomological Society of America DOI: http://dx.doi.org/10.1603/0046-225X-32.3.592 URL: http://www.bioone.org/doi/full/10.1603/0046-225X-32.3.592

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BIOLOGICAL CONTROLÑPARASITOIDS AND PREDATORS

Age-Dependent Fecundity and Life-Fertility Tables for Euborellia annulipes (Lucas) (Dermaptera: Anisolabididae) a Cotton Boll Weevil Predator in Laboratory Studies with an Artificial Diet W. P. LEMOS,1, 2 F. S. RAMALHO,1

AND

J. C. ZANUNCIO2

Environ. Entomol. 32(3): 592Ð601 (2003)

ABSTRACT Little information regarding the biology and ecology of dermapteran predators has been reported. For possible use of Euborellia annulipes (Lucas) (Anisolabididae) in biological control programs against the cotton boll weevil Anthonomus grandis grandis Boheman (Curculionidae), it is important to know the effect of temperature on reproduction in this predator. Our objective was to evaluate the reproductive potential and the longevity of females of E. annulipes under laboratory conditions using an artiÞcial diet, at 25 and 30⬚C, and to estimate life-fertility tables and growth rates. Fecundity began to decline on day 84 at 25⬚C and on day 74 at 30⬚C of adult age and ended with the death of the females at both temperatures. Females of E. annulipes oviposited an average of 206 and 306 eggs, and had a mean longevity of 198 and 149 d at 25 and 30⬚C, respectively. The gross reproductive rates were 89.2 at 25⬚C and 91.4 at 30⬚C; the net reproductive rates were 65.3 at 25⬚C and 40.3 at 30⬚C; the generation times were 195.2 d at 25⬚C and 142.9 d at 30⬚C; the doubling time was 33.0 d at 25⬚C and 26.7 d at 30⬚C; the intrinsic rates of increase were 0.02 at 25⬚C and 0.03 at 30⬚C, and the Þnite rates of increase were 1.02 at 25⬚C and 1.03 at 30⬚C. The predator population increased by 52 at 25⬚C and 20 at 30⬚C adult progeny per female per generation in the laboratory. The best age for inoculative releases of E. annulipes against cotton boll weevil populations is the age with the highest age-speciÞc reproductive values, that is, newly emerged females at 25 or 30⬚C. KEY WORDS Insecta, ring-legged earwig, fecundity, life table, cotton boll weevil

THE COTTON BOLL WEEVIL, Anthonomus grandis grandis Boheman (Curculionidae), is the most important pest of cotton in several countries that produce this crop (Ramalho 1994). The most common method used by cotton farmers to control populations of A. grandis grandis is intense and continuous applications of insecticides. However, the utilization of insecticides results in negative impacts on agroecosystems, especially on beneÞcial fauna (Van Den Bosch and Stern 1962, Ramalho 1994). Thus, it is important to implement biological control to help reduce pesticide use. Dermapterans are organisms with high predatory capacity (Klostermeyer 1942, Langston and Powell 1975, Ramamurthi and Solayappan 1980, Mourier 1986, Reis et al. 1988, Bueno and Berti Filho 1991). They are voracious, have high attack capacity, and have been important in the control of several insect pests, particularly, immature lepidopterans (Klostermeyer 1942, Gould 1948, Painter 1955, Reis et al. 1988), homopterans (Schlinger et al. 1959, Buxton and Madge 1976, Madge and Buxton 1976), coleopterans (Klos1 Unidade de Controle Biolo ´ gico (UCB)/Embrapa Algoda˜o, Caixa Postal 174, 58107Ð720, Campina Grande, Paraõ´ba, Brazil. 2 Departamento de Biologia Animal, Universidade Federal de Vic¸ osa, Vic¸ osa, Minas Gerais, Brazil.

termeyer 1942, Ramalho and Wanderley 1996, Lemos et al. 1998), and dipterans (Mourier 1986, Guimara˜es et al. 1992). The diversity of species and habitats of dermapterans, their generalist habits, and various reports in the literature (Klostermeyer 1942, Bharadwaj 1966, Knabke and Grigarick 1971, Buxton and Madge 1976, Madge and Buxton 1976, Mourier 1986, Guimara˜es et al. 1992, Koppenho¨ fer 1995, Rankin et al. 1995, Ramalho and Wanderley 1996, Lemos et al. 1998) show the importance and potential of these predators in programs of integrated pest management. The ringlegged earwig Euborellia annulipes (Lucas) has been reported as an efÞcient natural enemy of Cosmopolites sordidus German (Curculionidae) and some pest insects of stored grains (Klostermeyer 1942), as well as lepidopterous pests in sugar-cane ecosystems in the United States and Japan (Klostermeyer 1942, Gould 1948, Hensley 1971). Recently, studies conducted by Ramalho and Wanderley (1996), and Lemos et al. (1998, 1999) reported the possibility of using E. annulipes as a predator of larvae and pupae of the cotton boll weevil in the northeast region of Brazil. Although the biology of only a few representatives of the order Dermaptera has been studied, primarily because most species are native to tropical areas

0046-225X/03/0592Ð0601$04.00/0 䉷 2003 Entomological Society of America

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LEMOS ET AL.: FECUNDITY AND LIFE-FERTILITY OF Euborellia annulipes

where resources required for research are quite limited, E. annulipes has been the subject of several investigations in different parts of the world. Studies on the life history and bionomics of North American populations of this species have been conducted by Klostermeyer (1942), Neiswander (1944), Bohart (1947), Bharadwaj (1966), and Rankin et al. (1995) and comparative notes with E. cincticollis (Gerstaecker) in California were added by Knabke and Grigarick (1971). In Brazil, during the last few years there has been an increase in the knowledge on this predator, especially its biology and rearing techniques (Lemos 1997), impact of temperature on development (Lemos et al. 1998), and thermal requirements (Lemos et al. 1999). Melamed-Madjar (1971) and Koppenho¨ fer (1995) also studied the bionomic aspects of populations of E. annulipes in Israel and Kenya, respectively. The life history of other species of the genus Euborellia has also been studied, among them E. stali (Dohrn) (Easwaramoorthy and Nandagopal 1984), E. pallipes Shiraki (Yang 1985), and E. annulata (F.) (Situmorang and Gabriel 1988). Life tables are of great importance in understanding the population dynamics of an insect. They allow us to condense the essential biological data of a population into deÞnable terms of mortality rate, survival (Silveira Neto et al. 1976), longevity, reproduction and life expectancy (Coppel and Mertins 1977). This research was designed to evaluate the reproductive potential and the longevity of females of E. annulipes under laboratory conditions using an artiÞcial diet at 25 and 30⬚C, and to estimate life-fertility tables and growth rates. Materials and Methods The research was conducted at the Unidade de Controle Biolo´ gico (UCB)ÑEmbrapa Algoda˜o, Campina Grande, Paraõ´ba, Brazil. The predator was maintained in growth chambers, type BOD, at 25 and 30⬚C, relative humidity of 60 ⫾ 10%, and photoperiod of 14:10 (L:D) h. The E. annulipes studied were from a colony (12th generation) maintained at UCB, as described by Lemos (1997). Juvenile Development and Mortality. Twentyfour h before the initiation of the experiment, clutches of eggs of E. annulipes in an advanced development stage were collected. Egg masses of E. annulipes were maintained in Petri dishes (9.0 cm ⫻ l.5 cm) with a piece of absorbent paper inside (11.5 ⫻ l0.0 cm). This paper was folded in four similar parts for protection of the predator. One milliliter of water was put on the paper the Þrst day and 0.3 ml each of the following days to maintain constant humidity. Each Petri dish was sealed with l9-mm wide adhesive tape to reduce humidity loss. After this, Petri dishes were maintained in growth chambers at 25 and 30⬚C. Daily observations were made to determine incubation period and egg viability for E. annulipes. After emergence, 25 (at 25⬚C) and 35 (at 30⬚C) nymphs of E. annulipes were placed in Petri dishes (9.0 ⫻ 1.5 cm), containing artiÞcial diet and a piece of absorbent paper bent in four

593

parts of the same size and properly humidiÞed. The development time of the predator was monitored at 25 and 30⬚C until the emergence of adults. The number of instars of E. annulipes was measured by observing and registering the occurrence of ecdysis or change in nymph coloration. Newly emerged nymphs of E. annulipes show a brilliant black coloration. The differentiation between newly emerged adults and nymphs of the penultimate instar (Þfth or sixth) can be distinguished from the adults owing to the fact that the nymphs have 10 abdominal segments, whereas the adult female has only eight; and the adult male with 10 abdominal segments has characteristic forceps, in which the branch of the forceps turns sharply inward near the tip. Development time of each instar of E. annulipes, at each of the tested temperatures, was obtained and measured in days between molts. Survival was calculated as the inverse of nymph mortality during each instar. Sex ratio was determined at a late time, by counting the number of newly eclosed adults in the above mentioned experiment at both temperatures. Oviposition Periods and Fecundity. A total of 20 (at 25⬚C) and 18 (at 30⬚C) newly emerged pairs of adult E. annulipes were selected for each temperature and conÞned in Petri dishes (9.0 ⫻ 1.5 cm) until the death of the females. Males which died before their female partners were replaced. Each Petri dish had a container (3.5 ⫻ 0.5 cm) with 460 mg of artiÞcial diet (Lemos et al. 1998), which was changed every 2 d. Half of the top and bottom and sides of the Petri dishes were covered with black paper providing light and dark environments. This was done because dermapterans are nocturnal, and light conditions are important for mating activity of these insects (Shepard et al. 1973). Two pieces of absorbent paper (11.5 ⫻ 10.0 cm) bent in four identical parts, creating a speciÞc site for oviposition of E. annulipes, were placed in the dark areas of each Petri dish, alongside 1 ml of distilled water. Whenever necessary, an additional 0.3 ml of water was added to each dish to maintain constant humidity. Every 10 d, the paper inside the Petri dishes was changed and 1 ml of distilled water was added. Number of dead adults were counted daily, as were the number of clutches deposited per female, number of eggs per clutch per female, and number of eggs per female. The following parameters were analyzed: interval between clutches, preoviposition, oviposition and postoviposition periods; longevity of females, sex ratio of emerging adults and percentage of egg hatch. Each clutch stayed with the respective female until nymphs hatched, because eggs of this predator require care by females to prevent infestation of mites or fungi (Lemos et al. 1998). Statistical means and standard errors of the reproductive variables studied including survival and longevity of females of E. annulipes were calculated for 20 pairs at 25⬚C and 18 pairs at 30⬚C. Differences in observations between the individuals or different temperatures were compared by the Student-NewmanKeulÕs test (P ⫽ 0.05) (SAS Institute 2000). To study

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Table 1. Survivorship (%) and mean development time of the egg stage and instars of Euborellia annulipes at 25 and 30°C, 60 ⴞ 10% RH, and photoperiod of 14:10 (L:D) h Temperature (⬚C) 25

Male ⫽ 25 Female ⫽ 23 30

Male ⫽ 17 Female ⫽ 16

Stage Egg First instar Second instar Third instar Fourth instar Fifth instar Egg First instar Second instar Third instar Fourth instar Fifth instar

Development time (mean ⫾ SE) Male (day)

Female (day)

11.34 ⫾ 0.04 12.70 ⫾ 0.36 12.05 ⫾ 0.44 13.90 ⫾ 0.35 16.58 ⫾ 0.49 22.45 ⫾ 0.66 6.88 ⫾ 0.06 8.00 ⫾ 1.68 7.50 ⫾ 0.29 8.00 ⫾ 0.41 9.00 ⫾ 0.58 13.75 ⫾ 0.75

11.34 ⫾ 0.04 12.30 ⫾ 0.43ns 11.35 ⫾ 0.22ns 13.65 ⫾ 0.31ns 15.67 ⫾ 0.53ns 20.30 ⫾ 0.69* 6.88 ⫾ 0.06 7.88 ⫾ 0.43ns 7.00 ⫾ 0.27ns 7.94 ⫾ 0.25ns 9.13 ⫾ 0.60ns 10.00 ⫾ 0.62*

Survivorship (%)

Number of individuals

85.50 98.00 97.96 100.00 100.00 100.00 78.10 86.00 95.30 100.00 97.50 82.50

59 50 49 48 48 48 64 50 43 41 41 40

* F test (P ⫽ 0.05) for development time between male and female. Not signiÞcant F test (P ⫽ 0.05) for development time between male and female.

ns

age-dependent fecundity of E. annulipes, the data obtained by the method described above were divided in 21-d age classes. Means and standard errors of eggs per female per day were calculated for every age class. Life and Fertility Tables. Life and fertility table parameters were calculated for adult predators using data obtained from the study described above. The death and survival rates (qx and sx) observed each day were recorded for all immature stages and adult ages. The probability of surviving from birth to age x (lx) for every immature stage and adult age was also calculated. From these data the following statistics were calculated as described by Morales-Ramos and Cate (1992): intrinsic rate of population increase (rm), gross reproductive rate (GRR), net reproductive rate (R0), Þnite rate of increase (␭), mean generation time (GT), doubling time (DT), and age-speciÞc reproductive values (RVx). Voucher specimens from this study were identiÞed by Dr. S. Sakay, Daito Bunka University, Tokyo, Japan and are maintained at the Unidade de Controle Biolo´ gico (UCB), at the Centro Nacional de Pesquisa de Algoda˜o, Campina Grande, Paraõ´ba, Brazil. Results and Discussion Juvenile Development and Mortality. Incubation period of eggs of E. annulipes at 25⬚C was 1.6 times longer than at 30⬚C, although survival at 30⬚C was slightly lower (Table 1). Similar results were obtained by Melamed-Madjar (1971) with higher number of nymphs eclosing at 20 than at 32⬚C, a Þnding that agrees with the higher survival rate found at the lower temperature in this study. Koppenho¨ fer (1995) at 25⬚C and Rankin et al. (1995) at 28⬚C reported an egg incubation period around 8 d for E. annulipes. This duration can be between 6 and 17 d when this insect develops at temperatures between 20 and 29⬚C (Bharadwaj 1966), as was conÞrmed by Knabke and Grigarick (1971). Survival rate of eggs of E. annulipes was 78% at 28⬚C (Rankin et al. 1995), which was similar to those observed in our study with insects reared at

30⬚C. This indicates that E. annulipes shows similar egg viability in this temperature range (28 Ð30⬚C). Development time of E. annulipes differs with instar, sex, and temperature (Table 1), but development time of each successive instar of E. annulipes tended to increase at both temperatures for both sexes (Table 1). This fact was also observed by Rankin et al. (1995). Even though individuals of our population showed variation in development time compared with those of Bharadwaj (1966) and Koppenho¨ fer (1995) the relative development time of instars was comparable with shorter duration for Þrst and second instars and longer for the last (Þfth) instar, independent of sex and temperature. Similar duration was observed by Rankin et al. (1995). Differences observed between these various studies could be because of a variation in diet (Neiswander 1944, Jones et al. 1988), temperature (Rankin et al. 1995), and experimental conditions. Differences in development time between males and females were signiÞcative (Fˆ-test; P ⫽ 0.05) only for Þfth instar with males showing longer development than females (Table 1). Total development time to the adult decreased with higher temperature and was slightly longer for males than for females: 89 d at 25⬚C to 53 d at 30⬚C for males and 85 d at 25⬚C to 49 d at 30⬚C for females (Table 1). Survival of E. annulipes during all instars was high and varied from 82.5 (Þfth instar: 30⬚C) to 100% (third instar at 25 and 30⬚C; fourth and Þfth instars at 25⬚C) (Table 1). Higher mortality was observed at both temperatures especially during the egg stage. Uvarov (1931) deÞned the optimum temperature for development as the point where the highest number of individuals develop in the shortest time. In our study, E. annulipes had higher survival at 25⬚C (Table 1), suggesting that the optimal temperature for development of this species is close to 25⬚C. The sex ratio (females/(males⫹females)) of E. annulipes was similar at both temperatures, being in favor of males, with 0.48 ⫾ 0.01 at 25⬚C and 0.49 ⫾ 0.02 at 30⬚C. Koppenho¨ fer (1995) found in the laboratory at 25⬚C, a sex ratio of 0.50 for this predator, a ratio very

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Table 2. Influence of temperature on reproductive attributes and on longevity (mean ⴞ SE) of predator Euborellia annulipes femalesa at 25 and 30°C, 60 ⴞ 10% RH, and photoperiod of 14:10 (L:D) h Temperature Pre-oviposition (d) Oviposition (d) Post-oviposition (d) No. clutch/female No. egg/female No. egg/clutch No. clutch/female/day No. egg/female/day Clutch interval (d) Longevity (d)

25⬚C

30⬚C

21.9 ⫾ 1.2 152.7 ⫾ 16.1 22.2 ⫾ 3.7 7.7 ⫾ 0.7 206.2 ⫾ 20.3 25.7 ⫾ 1.6 0.04 ⫾ 0.1 1.0 ⫾ 0.1 21.0 ⫾ 0.6 198.4 ⫾ 15.6

11.3 ⫾ 0.4* 138.7 ⫾ 1.0ns 15.3 ⫾ 2.1ns 9.4 ⫾ 0.6ns 306.0 ⫾ 22.3* 32.0 ⫾ 1.0* 0.06 ⫾ 0.1* 2.1 ⫾ 0.2* 14.6 ⫾ 0.3* 149.1 ⫾ 14.5*

a

Number of individuals, 20 at 25⬚C, 18 at 30⬚C. * F test (P ⫽ 0.05). Not signiÞcant F test (P ⫽ 0.05).

ns

similar to that found in our study. A higher proportion of female progeny of E. annulipes was found by Lemos et al. (1998) at 20⬚C (1.0 male:2.2 females) and at 28⬚C (1.0 male:1.3 females). Other studies have demonstrated that the sex ratio of insects (Lemos et al. 1998, Medeiros et al. 1998) and mites (Ydergaard et al. 1997) can vary with temperature and type of prey offered to predators (Enkegaard et al. 1995). Oviposition Period. Females of E. annulipes reared at 30⬚C had a mean preoviposition period almost two times lower than those reared at 25⬚C (Table 2). Studies conducted by other workers have likewise shown that the preoviposition period of E. annulipes varies with temperature. Thus, E. annulipes completed its preoviposition in 10 Ð12 d at 24⬚C (Neiswander 1944). Bharadwaj (1966) showed that this period varies from 1 to 23 d, when E. annulipes was reared between 20 and 29⬚C; and at 28⬚C, females of E. annulipes typically began ovipositing 17.8 d after adult eclosion (Rankin et al. 1995). This indicates that the values obtained in our research for the preoviposition period are similar to those reported by other researchers for E. annulipes. Oviposition and postoviposition periods did not differ signiÞcantly at these two temperatures (Table 2). During the winter of 1937Ð1938, Neiswander (1944) reported an oviposition period for E. annulipes of approximately 90 d, which was lower than that obtained in the current study. This may indicate that diet inßuences the oviposition period of E. annulipes. Bharadwaj (1966) reported that this predator was able to oviposit throughout the year, at 20 Ð29⬚C. There is no information in the literature on the postoviposition period of E. annulipes. However, Easwaramoorthy and Nandagopal (1984) reported that the congener E. stali has a postoviposition period of 47.6 d at 27⬚C, a period longer than we found for E. annulipes. Temperature signiÞcantly affected the mean longevity of E. annulipes females. Longevity of E. annulipes at 25⬚C was almost 1.5 times longer than at 30⬚C (Table 2). Koppenho¨ fer (1995) reported that females of this species, when reared at 25⬚C, showed a longevity of 154 d, a shorter period than that found in our

595

study. Klostermeyer (1942) and Rankin et al. (1995) reported that individuals of E. annulipes live ⬍210 d in the adult stage. According to Knabke and Grigarick (1971), Þeld-collected adults of E. cincticollis survived as long as 240 d in the laboratory. Similar results were found by Yang (1985) with E. pallipes. According to this author the predator earwig has one generation per year, and the life span of adults is 0.5Ð1.0 yr or longer. All of these results demonstrate that E. annulipes has a shorter longevity when compared with other Euborellia species. Bueno and Berti Filho (1987) reported that the longevity of dermapterous species varies with sex, type of food, and humidity. Survival during the adult stage of E. annulipes was affected by temperature in diferent ways (Fig. 1). Females of E. annulipes reared at 25⬚C showed a survival rate 1.5 times higher during the Þrst 84 d of life than those reared at 30⬚C. Survival of females of E. annulipes showed a continuous decrease up to their death from this age on (Fig. 1). The shape of these survival curves are similar to PriceÕs (1998) type III classiÞcation. Fecundity. There was a signiÞcant effect of temperature on the number of eggs per female and the number of eggs per female per day produced by E. annulipes during their life span. Egg production was almost 1.5 times higher at 30⬚C than at 25⬚C (Table 2). Fecundity of E. annulipes reported by other researchers varies with temperature and the values found are lower in relation to those obtained in our study. Thus, Neiswander (1944) and Koppenho¨ fer (1995) reported a lifetime fecundity of E. annulipes of 186 and 91.4 eggs, respectively. According to Melamed-Madjar (1971), there was a signiÞcant difference between the number of eggs oviposited by E. annulipes at low temperatures (10 Ð20⬚C) and high temperatures (24 Ð34⬚C), with the most eggs being laid at temperatures between 24 and 30⬚C. The mean number of eggs laid by E. annulipes was 90. Most females (85%) laid between 0 Ð150 eggs, and only a few laid higher numbers, up to 250 eggs (Melamed-Madjar 1971). Knabke and Grigarick (1971) reported that the total number of eggs produced by E. cincticollis was also affected by temperature, and ranged from 47.2 at 26.7Ð29.4⬚C to 83.7 eggs at 22.2Ð26.7⬚C. However, the earwig E. annulata showed higher fecundity when compared with other species of the same genus, depositing an average of 321 eggs during its life span (Situmorang and Gabriel 1988). Females reared at 30⬚C, had signiÞcantly higher numbers of eggs per clutch and numbers of clutches per female per day than females studied at 25⬚C (Table 2). The intervals between clutches of E. annulipes were signiÞcantly higher when the predator was reared at 25⬚C (Table 2). The mean number of eggs per clutch of E. annulipes reported by Neiswander (1944) and Koppenho¨ fer (1995) are similar to those obtained in our research at 25 and 30⬚C with 32.0 eggs per clutch at 25⬚C and 35.1 eggs per clutch at 30⬚C. However, Bharadwaj (1966) and Rankin et al. (1995) found a mean number of eggs per clutch of 52.7 and 62.8, respectively, which are two times higher than

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Vol. 32, no. 3

Fig. 1. Survivorship (lx) of E. annulipes at 25 and 30⬚C. Observations from adult females (N ⫽ 20 at 25⬚C and 18 at 30⬚C). Age class ⫽ 21 d. Survivorship (lx) is the survival rate from age class 0 to the beginning of age x.

those observed in our study. Neiswander (1944) reported that the number of eggs per clutch of E. annulipes was higher in the beginning of its oviposition period and tended to decrease in later clutches. Females of E. annulipes at 28⬚C oviposited multiple clutches typically at 20 d intervals (Rankin et al. 1995), which agrees with results obtained in our study at 25⬚C. The number of clutches per female of E. annulipes did not differ signiÞcantly at 25 and 30⬚C (Table 2). According to Neiswander (1944), the number of clutches deposited by E. annulipes vary from 2 to 7 with an average of 3.9 clutches per female. Bharadwaj (1966) found similar results showing that females of this species deposit four clutches during their life span. Knabke and Grigarick (1971) stated that adults of E. annulipes only produce one or two clutches in the laboratory, whereas adults of E. cincticollis produce one to eight clutches. Recently, Koppenho¨ fer (1995) and Rankin et al. (1995) obtained a mean number of 2.6 and 4.5 clutches per female of E. annulipes, respectively. These values obtained by other workers were lower than those found in our study (Table 2), demonstrating that variables other than temperature, such as geographic origin of the predator, rearing conditions, and diet may inßuence some reproductive parameters of this organism, especially the numbers of eggs per clutch and clutches per female. Although studies of effects of diet on reproduction are not reported for E. annulipes, Jones et al. (1988) showed that diet affected the number of eggs per clutch for the dermapteran predator Doru taeniatum (Dorhn). The highest cohort fecundity (mx) was observed when the adult predators were 84 d of adult age (at 25⬚C) and 21 d of adult age (at 30⬚C), with mx values of 19.3 and 15.9, respectively (Figs. 2 and 3). There-

fore, it was veriÞed in this research that at both temperatures studied, females of E. annulipes produce the highest numbers of eggs and of female progeny per female in the same age classes (Figs. 2 and 3), suggesting that the highest number of female progeny generated per females of E. annulipes occurs at the age at which they deposit the highest number of eggs, that is, 84 and 21 d of adult age, at 25 and 30⬚C, respectively. These Þndings will be useful in determining the impact of age on fecundity of E. annulipes and in determining the best age to release the predators in cotton Þelds. Studies of this nature correlating the number of eggs per female, number of female progeny per female and adult age are nonexistent in the literature for the order Dermaptera. These rates declined with age of females of E. annulipes from this time on. Duration of reproductive period (mx) of E. annulipes at 25⬚C was longer (335 d) than that observed at 30⬚C (251 d) (Figs. 2 and 3). Highest egg production per female of E. annulipes was registered at 30⬚C in the third week of their adult life, demonstrating that temperature signiÞcantly inßuences fecundity of this predator. Neiswander (1944) reported that the fecundity of this predator was higher in the Þrst clutches and tended to decrease with each succeeding one. These results corroborate the Þndings of Knabke and Grigarick (1971), which revealed that sucessive clutches of E. cincticollis gradually declined in number of eggs. Differences found on E. annulipes fecundity are associated with a variety of factors, including temperature, that affect population growth of predators (Southwood 1978) and food quality that may also affect the progeny and survival of E. annulipes. Conßicting results among studies in the literature using the same temperature or diet may reßect differences in the studied strains or in their adaptation to the diet

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597

Fig. 2. Age-dependent fecundity and natality (mx) of E. annulipes at 25⬚C. Observations from 20 adult females. Vertical bars signify standard error. Age class (21 d). Natality (mx) is the mean number of female progeny per female of age class x.

provided in the laboratory. According to Rankin et al. (1995) descriptions of clutch size and number of clutches (lifetime fecundity) vary widely among studies and may be caused in part by diet quality, varying temperatures and photoperiods, or differences among experimental populations. Studies demonstrating the effects of temperature on fecundity of dermapteran species are rare in the lit-

erature. Bharadwaj (1966) found that most of the eggs of ring-legged earwig were laid in ⬇165 d in laboratory conditions between the middle of September and the end of February; after that, oviposition declined and was sporadic. When reared at 25⬚C, females of E. annulipes laid 1.7 eggs per female per day (Koppenho¨ fer 1995), which is close to the values obtained in the current study. Melamed-Madjar (1971) reported that

Fig. 3. Age-dependent fecundity and natality (mx) of E. annulipes at 30⬚C. Observations from 18 adult females. Vertical bars signify standard error. Age class (21 d). Natality (mx) is the mean number of female progeny per female of age class x.

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the highest number of eggs was laid by Anisolabis annulipes Lucas (⫽E. annulipes) at 24Ð30⬚C, at 14⬚C few eggs were laid, and none were laid at 10⬚C. The number of hatched nymphs was almost 1.5 times higher at 30⬚C (243.3) than at 25⬚C (172.7). Studies on impacts of temperature on egg mortality in E. annulipes are few in the literature. Melamed-Madjar (1971) showed that there was a signiÞcant effect of temperature on egg hatching of E. annulipes. According to this author, eggs do not develop at 10 and 14⬚C; however, a high proportion of eggs hatch at 20⬚C (73.6%) and 32⬚C (85.4%). Lemos et al. (1998) reported that this predator had egg survival of 85.5% (at 25⬚C) and 78.1% (at 30⬚C), which are similar to the survival rates obtained in this research. These rates varied greatly as a function of the age of females at both temperatures. As the data on E. annulipes survival and reproduction become available, a population growth model can be constructed. A simulation model developed in such a manner can be coupled with prey population dynamic models to develop boll weevil management strategies involving biological control programs for cotton. Life and Fertility Tables. Mean generation times (GT) were 195.2 and 142.9 d, gross reproductive rates were 89.2 and 91.4 eggs per female, and the net reproductive rates (R0) were 65.3 and 40.3 female progeny per adult female, at 25 and 30⬚C, respectively. The values obtained for generation time indicate that 1.9 and 2.6 generations of E. annulipes per year can be obtained at 25 and 30⬚C, respectively. The positive values of R0 indicate population growth of E. annulipes at the two studied temperatures. When reared at 25⬚C, the population of E. annulipes increased 1.4 times per generation over that at 30⬚C. The intrinsic rate of population increase (rm), mean generation (GT), and doubling time (DT) are useful indices of population growth under a given set of growing conditions (Tsai 1998). The rm and ␭ values, at 25⬚C, were respectively, 0.02 per day and 1.02. However, when reared at 30⬚C, these values were 0.03 per day and 1.03. The doubling times were 33.0 d, at 25⬚C, and 26.7 d at 30⬚C. The proportions of individuals surviving through all immature stages and reaching adulthood (lx) were 0.8 at 25⬚C and 0.5 at 30⬚C. Thus, under optimal conditions, an increase of 52.2 at 25⬚C and 20.5 at 30⬚C adult progeny per female per generation (lx ⫻ R0) could be expected. E. annulipes reared at 30⬚C showed higher intrinsic rate of increase resulting from faster development, higher survival, and higher reproductive rate. The age-speciÞc reproductive values (RVx) provide information that can be useful in determining the best age for releasing E. annulipes in the cotton ecosystems to reduce the cotton boll weevil populations. The higher value of RVx (81.6) at 25⬚C corresponds to newly-emerged adults. However, the maximum value of RVx (78.3) at 30⬚C also corresponds to newlyemerged adults. Therefore, the ideal age for inoculative releases of E. annulipes would be the age with the highest RVx values, that is, newly emerged females at

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25⬚C (RV6 ⫽ 81.6) and 30⬚C (RV4 ⫽ 78.3). In programs of biological control of cotton boll weevil by propagation and release of predators, the major strategy that should be followed is inoculative release. Population Models. The relationship between agespeciÞc fecundity and age was described by a model composed of a linear function for the increase in fecundity at early ages combined with a exponential function for the subsequent decrease in egg laying at older ages. This relationship was described by f(x) ⫽ ␣x exp(Ð␤x). In the model f(x) is the daily age-speciÞc fecundity rate (eggs/female/d), x is the age in days (age class), and ␣ and ␤ are constants. For age class 1 (0 Ð20 d as adults), the model was Þtted to the data by the nonÐlinear least square technique (SAS Institute 2000), weighted by the number of females contributing to the means giving the curves in Fig. 4. The parameters ␣ (⫾SE) and ␤ (⫾SE), respectively, were estimated to be 1.60 ⫾ 0.26 and 0.36 ⫾ 0.03 at 25⬚C, and 3.23 ⫾ 0.58 and 0.42 ⫾ 0.04 at 30⬚C. The model described 78.8% and 74.8% of the variation at 25 and 30⬚C, respectively. The pattern in age-speciÞc fecundity was the same at both temperatures. A similar pattern in age-speciÞc fecundity was seen when Macrolophus caliginosus Wagner (Heteroptera: Miridae) was fed on various stages of Tetranychus urticae Koch (Acari: Tetranychidae) (Hansen et al. 1999). As temperature increased, the time required to reach the maximum rate of oviposition decreased, and the highest fecundity rate was predicted to be attained at 30⬚C. Artificial Diet. In our study the predator was maintained on artiÞcial diet comprised of powder milk, beer yeast, chicken food, and bran (Lemos et al. 1998). Neiswander (1944) and Bharadwaj (1966) fed this predator on a combination of animal and vegetable foods. It remains to be investigated whether newly emerged adults of E. annulipes when released in the Þeld to control cotton boll weevil populations maintain or even increase their rates of survival and/or reproductive capacity once they feed on their natural prey. Several authors (De Clercq and Degheele 1993a, 1993b; Saavedra et al. 1997; Chocorosqui and De Clercq 1999; Cohen 2000) have reported that some predator species (Heteroptera: Pentatomidae) maintained several generations on artiÞcial diets or unnatural prey in laboratory environments maintained their feeding habits as indicated by search time, handling time, quantity of food extracted, and extraction rates. According to Chocorosqui and De Clercq (1999), predation rates of P. maculiventris (Say) reared on artiÞcial diet were similar or somewhat higher than those of predators reared on live prey. These results corroborate the Þndings of Saavedra et al. (1997). In their research, nymphs and adults of Podisus nigrispinus (Say) reared for three and four generations, respectively, on artiÞcial diet were able to prey on Anticarsia gemmatalis (Hu¨ bner) (Noctuidae) both under laboratory and greenhouse conditions. De Clercq and Degheele (1993a) also found that prolonged rearing (⬎15 generations) on artiÞcial diet did not affect the predation efÞciency of nymphs and adults of P. maculiventris and P. nigrispinus. Similarly, after prolonged

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599

Fig. 4. Observed (dots) and predicted (solid line model) age-speciÞc fecundity (eggs/female/d) of E. annulipes fed on artiÞcial diet as a function of female adult age. Age class 1 (0Ð20 d as adults).

maintenance of Geocoris punctipes Say bugs on artiÞcial diet, their predation ability was identical to that of Þeld-collected individuals (Hagler and Cohen 1991, Cohen 2000). It is expected that the weight, reproductive capacity, and predation ability of adults of E. annulipes from nymphs reared on artiÞcial should be similar to those fed on natural prey and that under Þeld conditions these predators should have the same efÞciency against populations of A. grandis grandis. Thus, the availability of an artiÞcial diet that supports growth and reproduction of E. annulipes provides a means for a mass rearing procedure of this predator for use in integrated management programs of cotton boll weevil. Sex Ratio in the Laboratory Versus the Field. Concern about quality of natural enemies reared in the laboratory is relatively recent, and it has increased in the last few years (Prezotti and Parra 2002). Our results demonstrated for two temperatures the resulting sex ratio favors males of E. annulipes. This can indicate inadequate rearing (Prezotti and Parra 2002) or unfavorable experimental conditions. Because the predators used were reared in the laboratory and maintained during this research on artiÞcial diet, it is possible that this type of food is not adequate for the nutritional requirements of E. annulipes. According to

Van Driesche and Bellows (1996), it should be expected that diet may progressively affect a number of important natural enemy characteristic in colonies reared for several generations. Nutritional, as opposed to genetic, basis should be suspected if altering diet or host species causes rapid improvement. Females of these insects are nutritionally more demanding than males because they need higher quantities of nutritional reserves for reproduction. For this reason it is likely that females will be the Þrst to suffer from poor quality food offered in the laboratory. However, it is possible that this tendency will change in favor of females under Þeld conditions where they can start feeding on their natural prey (A. grandis grandis larvae), which is nutritionally more suitable for their development. These females will also be able to feed on complementary vegetable substrates (leaves, nectar, or polen) such as observed by Ruberson et al. (1986) and Valicente and OÕNeil (1992, 1995) for P. maculiventris, Zanuncio et al. (2000) for Brontocoris tabidus (Signoret) (Heteroptera: Pentatomidae) and Lemos et al. (2001) for P. nigrispinus. Feeding in the Þeld increases reproduction and longevity of these insects and could therefore improve production of female progeny by females of E. annulipes once released for biological control.

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ENVIRONMENTAL ENTOMOLOGY Acknowledgments

We thank Randy Luttrell (Department of Entomology/ University of Arkansas) for his helpful comments on earlier drafts of this manuscript and two anonymous reviewers for their comments and suggestions. We also express our appreciation to the personnel at the Biological Control Unit/Embrapa Algoda˜o. Research was supported by funds from the CNPq, Common Fund for Commodities/International Cotton Advisory Committee, and Fundac¸ a˜o Banco do Brasil.

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