Competition between Catolaccus grandis (Hymenoptera: Pteromalidae) and Bracon vulgaris (Hymenoptera: Braconidae), parasitoids of the Boll Weevil

AGRICULTURE, AGRIBUSINESS AND BIOTECHNOLOGY

Competition between Catolaccus grandis (Hymenoptera: Pteromalidae) and Bracon vulgaris (Hymenoptera: Braconidae), parasitoids of the Boll Weevil

Francisco de Sousa RamalhoI, ^*; Ana Maria Camêlo da Silva^II; José Cola Zanuncio^III; José Eduardo Serrão^III

^IEmbrapa Algodão; Unidade de Controle Biológico; C. P. 174; 58107-720; Campina Grande - PB - Brasil

^IIUniversidade Estadual da Paraíba; Departamento de Biologia; Campina Grande - PB - Brasil

^IIIDepartamento de Biologia Geral; Universidade Federal de Viçosa; Campus Universitário; Viçosa - MG - Brasil

ABSTRACT

The competition between populations of the parasitoids C. grandis and B. vulgaris was studied using larvae of Euscepes postfasciatus (Fairmaire) as an alternative host. A series of biological parameters was observed and related to the competitive abilities of both parasitoid species. They were capable of colonizing and maintaining their populations regardless of host location. The population growth of C. grandis and B. vulgaris, based on fecundity was not affected by the competition. The parasitism and survivorship to the adult stage were affected by competition, except when the host was located at the bottom of the rearing cage. C. grandis performed better than B. vulgaris independently of the competition and host location, but it did not exclude the other species.

Key words: Biological control, Anthonomus grandis, competition between parasitoids

RESUMO

Catolaccus grandis (Burks) e Bracon vulgaris Ashmead são os principais parasitóides do bicudo-do-algodoeiro Anthonomus grandis Boheman no Nordeste do Brasil. É importante que se determinem as interações entre esses parasitóides e o seu efeito em programas de controle biológico dessa praga com os mesmos. A competição entre os parasitóides C. grandis e B. vulgaris foi estudada, utilizando-se larvas de Euscepes postfasciatus Fairmaire como hospedeiro alternativo. A fecundidade de C. grandis e B. vulgaris baseada na produção de ovos, não foi afetada pela competição, mas o parasitismo e a produção de adultos desses parasitóides foram afetados pela competição, exceto quando o hospedeiro se encontrava na base da caixa de criação. Independentemente da competição e da localização do hospedeiro, C. grandis apresentou melhor desempenho que B. vulgaris, mas não excluiu as populações da outra espécie de parasitóide.

INTRODUCTION

The family Braconidae presents many parasitoid species of key-pests of agriculture and stored grains (Wanderley, 1998). Species of the genus Bracon are among the main parasitoids of Anthonomus grandis Boheman in the United States (Cross and Chesnut, 1971; Cross 1973), where larval parasitization can reach 94 to 100% (Meinken and Slosser, 1982).

There are many ectoparasitoids attacking the boll weevil in Brazil (Ramalho and Wanderley, 1996), but Bracon vulgaris Ashmead (Hymenoptera: Braconidae) and Catolaccus grandis (Burks) (Hymenoptera: Pteromalidae) are considered the major parasitoids of this pest in many areas where cotton is cultivated in the State of Paraíba, Brazil (Ramalho et al., 1993; Ramalho et al., 1996; Ramalho et al., 2000).

Although both parasitoids exploit the same host, they are somewhat isolated because they prefer to attack hosts at different stages of development. C. grandis prefers to parasitize the host after the cotton squares have fallen to the ground (Morales-Ramos and Cate, 1992), while B. vulgaris preferably attacks the host infesting cotton bolls while still in the upper part of cotton plants (Ramalho and Wanderley, 1996). This behavior shows the possibility of having a high parasitism rate in biological control programs of A. grandis through releases of both parasitoids due to the exploitation of different ecological niches. However, it is important to verify if competition between these parasitoids may exist, and if it could impair the parasitization of A. grandis through biological control programs seeking for the release of both natural enemies. Therefore, the objective of this work was to study the competitive abilities of the parasitoids C. grandis and B. vulgaris and to determine their impact on the population growth of these species through survival of their immature stages.

MATERIAL AND METHODS

This work was carried out in an acclimatized room at 26 ± 1ºC, relative humidity of 60 ± 10%, and a photoperiod of 16 h. C. grandis and B. vulgaris were obtained from the colonies of the "UCB-Embrapa Algodão" where they were reared with the alternative host Euscepes postfasciatus (Fairmaire) according to Ramalho and Dias (2003). Host larvae were obtained on Ipomoea potato which were replaced every 24 h, and those containing eggs of E. postfasciatus were placed into plastic trays or paper bags and kept under controlled conditions (28 ± 1°C and relative humidity of 80 ± 10%) to allow for the immature development. Fifth instar larvae of this host were supplied to the parasitoids. Host larvae were collected through a double sieving process. The first sieve had a mesh of 4.0 mm and allowed insects and small pieces of roots to pass through retaining large pieces of the root. The second sieve, with a 2.0 mm mesh separated the larvae from small roots fragments of I. potato and dust. Larvae of E. postfasciatus collected from the roots were disinfected in a 10% sodium hypochlorite solution during 10 minutes prior to parasitization.

Larvae of E. postfasciatus were encapsulated using the procedure of Cate (1987) with modifications of Wanderley and Ramalho (1996). The effect of competition between populations of C. grandis and B. vulgaris were determined with individual and combined populations of these parasitoids in acrylic transparent cages (40 x 40 x 25 cm) similar to those described by Wanderley and Ramalho (1996).

The experiment was done in a randomized complete-block design with six treatments: (1) three males and six females of C. grandis + 40 encapsulated larvae of the host at the base of the cage; (2) three males and six females of C. grandis + 40 encapsulated larvae of E. postfasciatus at the top of the cage; (3) three males and six females of B. vulgaris + 40 encapsulated larvae of this host at the base of the cage; (4) three males and six females of B. vulgaris + 40 encapsulated larvae of the host at the top of the cage; (5) three males and six females of C. grandis + three males and six females of B. vulgaris + 40 encapsulated larvae of the host at the base of the cage and (6) three males and six females of C. grandis + three males and six females of B. vulgaris + 40 encapsulated larvae of this host at the top of the cage. A total of four replicates were used for each treatment.

Each experimental unit was composed of an acrylic cage with 0-24 h-old adults of C. grandis and B. vulgaris. Two glass tubes with distilled water and covered with a cotton wad were put in the upper part of each cage to keep humidity inside it and to supply water to the parasitoids. Parasitoids were fed with droplets of honey of Apis mellifera Linné distributed in the cage's walls with a disposable syringe. Parafilm sheets with 40 or 80 encapsulated larvae of E. postfasciatus were daily offered for each experimental unit. The number of eggs deposited and larvae parasitized were quantified with a stereomicroscope, and parasitized larvae were transferred to 500 ml plastic cups and the number of adults of C. grandis and/or B. vulgaris were quantified immediately after their emergence. Data of each replicate was taken daily, during 80 days.

Data obtained were analyzed with the procedure of PROC GLM and average compared using the test of Student-Newman-Keuls (P= 0.05) (Sas Institute, 2003).

RESULTS AND DISCUSSION

The populations of C. grandis, maintained alone, tended to produce more eggs, to parasitize a larger number of larvae and to produce a larger number of descendants than those of B. vulgaris with hosts located either at the base or at the top of the cages. Both parasitoid species showed relatively population growth at the end of the study (Figs. 1-3).

Populations of B. vulgaris were affected by competition with C. grandis with a decrease in the population levels in a relatively short period (Figs. 1-3). However, populations of C. grandis were not affected by competition with B. vulgaris. Populations of C. grandis alone, or in competition with the other parasitoid presented higher densities and longer growth period. C. grandis competes with B. vulgaris during host searching.

The egg production of C. grandis [host at the base: alone vs competition (F=0.24, df=1;3, P=0.6573) and host at the top: alone vs competition (F=0.22, df=1;3, P=0.6719)] and B. vulgaris [host at the base: alone vs competition (F=2.15, df=1;3, P=0.2390) and host at the top: alone vs competition (F=6.45, df=1;3, P=0.0847)] was not affected by competition; though parasitism (C. grandis: F=85.02, df=1;3, P=0.0027 and B. vulgaris: F=18.97, df=1;3, P=0.0224), and adult emergence of both parasitoids were affected by competition when the host was located at the top of the cages (C. grandis: F=80.99, df=1;3, P=0.0029 and B. vulgaris: F=240.54, df=1;3, P=0.0078).

C. grandis, independent of host location (base vs top: F=1.85, df=1;3, P=0.2670) deposited a larger number of eggs and consequently a larger number of E. postfasciatus larvae was parasitized (base vs top: F=0.10, df=1;3, P=0.7719); however, independently of host location (base vs top: F=3.13, df=1;3, P=0.1750), the emergence of adults was relatively low. This could be attributed to the cannibalistic behavior of the larvae of C. grandis. The C. grandis larvae could also destroy B. vulgaris larvae because its females did not discriminate parasitized hosts. These results suggested that females of C. grandis possibly deposited their eggs in parasitized larvae of A. grandis by B. vulgaris in cotton plants. The presence of females of one parasitoid did not inhibit oviposition by the other and they did not discriminate parasitized hosts. Female parasitoids with good strategy effectiveness to locate the host might have a competitive advantage and this was particularly important when densities of the host were low (Godfray, 1994).

The populations of B. vulgaris maintained alone, or in competition deposited higher number of eggs (top vs base: F=80.17, df=1;3, P=0.0029 and top vs base; F=15.08, df=1;3, P=0.0303, respectively) and produced higher number of parasitized larvae (top vs base: F=86.38, df=1;3, P=0.0026 and top vs base: F=15.41, df=1;3, P=0.0294, respectively) and adults (top vs base: F=32.61, df=1;3, P=0.0107 and top vs base: F=47.69, df=1;3, P=0.0062, respectively) with the host at the top than at the base of the cages; however, this behavior was not verified in C. grandis populations (eggs: alone: top vs base: F=4.42, df=1;3, P=0.1262 and competition: top vs base: F=1.85, df=1;3, P=0.2670, parasitized larvae: alone: top vs base: F=4.75, df=1;3, P=0.1174 and competition: top vs base: F=0.10, df=1;3, P=0.7719, and adults: alone: F=7.86, df=1;3, P=0.1071 e competition: top vs base: F=3.13, df=1;3, P=0.1750).

The behavior of B. vulgaris females to produce higher population levels when the host was located at the top of the cages was similar to host searching behavior of this parasitoid in field conditions (Ramalho and Wanderley, 1996). Similar results were reported for B. mellitor (Adams et al. 1969). On the other hand, population densities of C. grandis were similar with the host at the top, or at the base of the cages what differs from its behavior under field conditions (Johnson et al., 1973; Ramalho and Wanderley, 1996; Ramalho et al., 2000). It was possible that the height of the cages had a more accentuated impact on C. grandis than on B. vulgaris and that it was not enough to affect population dynamics of this parasitoid.

B. vulgaris and C. grandis produced a larger number of descendants independent of the host location at the base, or at the top of the cages. These results indicated that possibly both species could colonize and maintain their populations in cotton fields with A. grandis larvae in cotton squares on the soil or in bolls and/or squares in the superior part of cotton plants.

The populations of B. vulgaris alone and competing for the host at the top of the cages produced approximately five and two fold more individuals, than those with the host at the base of the cages; while C. grandis produced similar number of descendants independently of host location, respectively. These results showed that C. grandis could not drive populations of B. vulgaris to extinction even being the dominant species in situations of competition (host at the base or at the top of the cages). These data differed from those observed for C. grandis, which took populations of B. mellitor towards extinction when competing with the latter species independent of host location (O'Neil and Cate, 1985). However, competition between parasitoids is a complex interaction and it is necessary to identify relevant variables of this process under field conditions. High mortality rates of A. grandis could be obtained in programs of biological control with periodical releases of C. grandis and B. vulgaris because surviving populations of the latter species would have a complementary action to that of C. grandis. The impact of this behavior will be more relevant when cotton bolls attacked by A. grandis start to appear because the synchronization of B. vulgaris with this host occurs in this period.

C. grandis prefers to parasitize A. grandis larvae in abscised squares in the cotton agroecosystem (Ramalho, 1994; Ramalho and Wanderley, 1996). However, in this study, C. grandis, independent of competition, was effective against this host on the base and in the top of the cages. This was also reported on a competition study between populations of B. mellitor and C. grandis but the impact of this last natural enemy was not affected by host location (O'Neil and Cate, 1985). These results suggested that probably C. grandis could maintain its populations in the cotton field, parasitizing A. grandis larvae in bolls if squares infested by this pest were not present on the ground.

The interaction between C. grandis and B. vulgaris on biological control programs of A. grandis is important because these species compete for the same nutritional resource (Berberet and Bisges, 1998). C. grandis showed better performance than B. vulgaris independent of competition or host location but it did not drive the latter species to extinction (Fig. 3). However, O'Neil and Cate (1985) reported that C. grandis led populations of B. mellitor to extinction when competing for the host independent of its location. Probably, the competition between parasitoids is function of the species.

Probably B. vulgaris has a complementary action to that of C. grandis under natural conditions during the production of squares in cotton plants. This would provide a higher parasitism rate of A. grandis than that of a single species with a primary action during this period. However, competition intensity in the dynamic cotton ecosystem might differ from that observed in the laboratory. Therefore, it is recommended to study if interactions between populations of C. grandis and B. vulgaris are complementary in controlling A. grandis in cotton fields.

ACKNOWLEDGEMENTS

We thank to the "Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)" and to "Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG)" for financial grant.

Received: June 06, 2005;

Revised: March 08, 2006;

Accepted: March 12, 2007.

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*

Author for correspondence

Publication Dates

• Publication in this collection
  31 Aug 2007
• Date of issue
  May 2007

History

• Accepted
  12 Mar 2007
• Received
  06 June 2005
• Reviewed
  08 Mar 2006