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Parasitoids associated with the black scale Saissetia oleae (Olivier) (Hemiptera: Coccidae) in olive trees in Minas Gerais State, Brazil/Parasitoides associados a cochonilha-preta Saissetia oleae (Olivier) (Hemiptera: Coccidae) em oliveira no Estado de Minas Gerais, Brasil.

Introduction

Black scale, Saissetia oleae (Olivier), is native to South Africa and presently found throughout the world (PRINSLOO, 1997; VIGGIANI, 1978). This scale is considered a major pest in many economic cultures and particularly in olive trees. As a world economic pest, black scale has been the target of numerous biological control programs with relatively successful results (DAANE et al., 1991), and parasitoid introduction and release have been the main utilized strategy. In California, classical biological control programs against this pest by introducing natural enemies from different parts of the world, such as South America, dates from the late 19th century (DAANE et al., 1991). The occurrence of black scale in Brazil was reported in 1898 (COMPERE, 1939), and this organism colonizes a large number of hosts (SILVA et al., 1968). New plantings of commercial olives are increasing in Brazil, and this insect appears to be the main threat to the culture (PRADO; SILVA, 2006). Currently, no biological control program has been implemented in Brazil; therefore, the parasitoids that are reared from the black scale are either autochthonously or accidentally introduced with the pest or closely related insects.

Before the establishment of any biocontrol strategy, it is necessary to know the complex of natural enemies acting upon a pest under local conditions. The damage and importance of black scale is variable depending on climatic conditions, the host, and the impact of natural enemies; therefore, regional differences can be expected (PANIS, 1977). Studies of black scale parasitoids are abundant in the literature, but these studies have not been performed in Brazil.

Sixteen parasitoid wasps were recorded to be associated with this scale in Brazil (Table 1). However, some of these wasps have only been reported at the genus level, namely Moranila sp. (as Tomocera sp.), Metaphycus sp. (as Euaphycus sp.), Eupelmus sp., Eurytoma sp., (COMPERE, 1939), and Moranila sp. (as Moranita sp. "sic") (SILVA et al., 1968).

The aim of this study was to determine the parasitoid complex that was associated with the black scale of olive trees, their relative abundance, and the rate of parasitism in an insecticide-free orchard that was located southeast of Brazil.

Material and methods

Sampling

Infested olive branches were sampled from an insecticide-free orchard located in Maria da Fe (22[degrees]17' 46"S, 45[degrees]23'5"W), which was south of the State of Minas Gerais, Brazil, during the period of September 2009 to February 2012.

Recovery

Infested olive twigs were kept inside a parasitoid emergence container, which was a modified, transparent plastic, gaseous bottle that was covered with aluminum foil. A glass tube was attached to the neck of the bottle so parasitoids would be attracted to the light. Emerging parasitoids were checked daily for 45 days, and their relative abundance was calculated based on the total number of recovered individuals.

Parasitism

A bouquet of olive branches was kept in a water container inside a cage (Flanders battery). After one month, 100 scales were examined for parasitoid presence or evidence, and the parasitism level was estimated. Parasitoids were identified by the first author (E.P.).

Results and discussion

Parasitism caused by the parasitoid complex ranged from 3 to 31% (Figure 1), which was a rather low value within the large range of parasitism that has been obtained for this insect (PEREIRA et al., 1998; TENA et al., 2008). This level of parasitism failed to maintain the black scale under the damage level and resulted in high infestation and the presence of sooty mold.

Sixteen species of wasp parasitoids belonging to the following families were collected: Aphelinidae (1), Pteromalidae (1), Eupelmidae (5), Encyrtidae (6), and Eulophidae (3). However, some species (not determined) could have been hyperparasitoids. The species that were recovered in this survey are listed in Table 2.

[FIGURE 1 OMITTED]

Mesopeltita truncatipennis (Pteromalidae: Eunotinae) (Figures 2 and 3A).

[FIGURE 2 OMITTED]

The members of this subfamily are mainly egg predators but may also act as scale parasitoids. This species is cosmopolitan (DAANE et al., 1991; MURUA; FIDALGO, 2001; TENA et al., 2008), was initially reported in Brazil in 2012 (PRADO et al., 2012), and was the most abundant parasitoid that was collected in our survey. This species is very similar to and is easily confounded with another species of Eunotinae, Scutellista caerulea (Fonscolombe), which is one of the most frequent species associated with black scale in the world and has a similar feeding behavior (PRADO et al., 2003). However, members of Eunotinae were not recovered during this survey.

Coccophagus caridei (Aphelinidae)

This parasitoid is native to South America and is associated with many coccids of the genera Pulvinaria, Saissetia, Coccus, Eulecanium, Ceroplastes Pseudococcus, and Ischnaspis (DE SANTIS, 1980; MURUA; FIDALGO, 2001; PRADO et al., 2003). The date of the first occurrence of this wasp in Brazil is unknown, but the literature reports that it was introduced in California from Brazil and Argentina in 1935 (COMPERE, 1939; DAANE et al., 1991). In this study, this parasitoid ranked second in abundance but was present at a low density and frequency. C. caridei was collected mainly in December 2009, and only a few specimens were found on other dates. Another species, C. fallax, appeared to be the most numerous and commonly found during other studies (COMPERE, 1939); however, it was absent in this survey.

Diversinervus elegans (Encyrtidae) (Figure 3B)

This parasitoid is non-specific for scales (Coccidae), particularly of nymphs and adults (PRINSLOO, 1985). The female has the peculiarity of ovipositing inside the hind intestine of its host through the aperture of the anus (COMPERE, 1931a). This organism has attracted great interest in biological control programs, and it has been introduced from Africa to other countries for controlling S. oleae (BARTLETT; MEDVED, 1966; COMPERE, 1931b; DAANE et al., 1991). However, its efficacy has been questioned due to the encapsulation of its eggs (VIGGIANI, 1978). Only a few of these specimens were reared from the black scale.

Metaphycus spp. (Encyrtidae) (Figure 3C)

Only two specimens of different species of Metaphycus (unidentifiable due to the poor condition of the specimens) were collected in our survey. Species of this genus have been reported as effective against the black scale, particularly M. helvolus (Compere) and M. lounsburyi (Howard) (ARGOV; ROSSLER, 1993; VIGGIANI, 1978; STRATOPOULOU; KAPATOS, 1998), and five species belonging to this genus have been recorded in Brazil, but only M. flavus (Howard) has been associated with black scale (NOYES, 2013).

[FIGURE 3 OMITTED]

Lecaniobius utilis (Eupelmidae) (Figure 3D)

This parasitoid is an egg predator of S. oleae and other soft scales such as Ceroplastes and Lecanium, and it was described in Vicosa, Minas Gerais, Brazil and posteriorly recorded from the states of Bahia, Mato Grosso, Minas Gerais, Sao Paulo and Rio de Janeiro (COMPERE, 1939; DE SANTIS, 1980; MYARTSEVA et al., 2010).

L. utilis was successfully introduced from Brazil and Argentina to California in 1935 for controlling S. oleae and Saissetia nigra (Nietner) (DAANE et al., 1991), and it has been considered an efficient parasitoid but sometimes also considered of low value (MURUA; FIDALGO, 2001; MYARTSEVA et al., 2010) depending on local conditions. Only one specimen from this group was found in our survey of samples from October 2009.

The remaining parasitoid species were only sporadically collected and comprised several species of Eupelmidae, Eulophidae, and Encyrtidae.

Despite the number of parasitoids that were found, the contribution of parasitoid wasps seemed to be rather poor and had a low capacity for regulating the black scale population. The presence of these organisms was irregular between years, and few parasitoids were recovered during 2012. S. caerulea and species of the genus Metaphycus and Coccophagus are predominant in black scale around the world, and their absence and that of other important parasitoids with high potential as biological control agents opens the opportunity to improve the parasitoid complex by importing and releasing new natural enemies. It appears that the efficiency of each species of black scale parasitoid is highly dependent on local conditions, and a large number of wasp species should be desirable for introduction. The parasitoid wasp composition from this study showed a substantial difference from similar studies that were carried out in neighboring countries such as Argentina and Chile (MURUA; FIDALGO, 2001; PRADO et al., 2003).

Conclusion

At least 16 species of parasitoids were associated with S. oleae, and four were most common. Among these species, M. truncatipennis was the most abundant and frequent.

A low level of parasitism, which ranked from 3 to 31% throughout the years, was found.

Doi: 10.4025/actasciagron.v37i4.19743

Acknowledgements

The authors wish to thank Fapemig for financial support and a fellowship that was awarded to the third author and to two anonymous referees for their valuable contribution to improve this manuscript.

References

ARGOV, Y.; ROSSLER, Y. Biological control of the Mediterranean black scale, Saissetia oleae (Hom.: Coccidae) in Israel. Entomophaga, v. 38, n. 1, p. 89-100, 1993.

BARTLETT, B. R.; MEDVED, R. A. The biology and effectiveness of Diversinervus elegans (Encyrtidae: Hymenoptera), an imported parasite of Lecaniine Scale Insects in California. Annals of the Entomological Society of America, v. 59, n. 5, p. 974-976, 1966.

COMPERE, H. A revision of the genus Diversinervus Silvestri, encyrtids parasites of coccids (Hymenoptera). University of California Publications in Entomology. v. 5, p. 233-245, 1931a.

COMPERE, H. A discussion of the parasites of Saissetia oleae (Bern.) collected in Eritrea. University of California Publications in Entomology. v. 5, p. 247-255, 1931b.

COMPERE, H. The insect enemies of the black scale, Saissetia oleae (Bern.) in South America. University of California Publications in Entomology. v. 7, p. 75-90, 1939.

DAANE, K. M.; BARZMAN, M. S.; KENNETT, C. E.; CALTAGIRONE, L. E. Parasitoids of black scale in California: establishment of Prococcophagus probus Annecke; Mynhardt and Coccophagus rusti Compere (Hymenoptera: Aphelinidae) in olive orchards. Pan-Pacific Entomologist, v. 67, n. 2, p. 99-106, 1991.

DE SANTIS, L. Catalogo de los himenopteros calcidoideos de America al sur de los Estados Unidos. Buenos Aires: Publicacion Especial Comision de Investigaciones Cientificas Provincia de Buenos Aires, 1979.

DE SANTIS, L. Catalogo de los himenopteros brasilenos de la serie Parasitica incluyendo Bethyloidea. Curitiba: UFP, 1980.

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MYARTSEVA, S. N.; RUIZ-CANCINO, E.; CORONADO-BLANCO, J. M. Especies neotropicales de Lecaniobius Ashmead (Hymenoptera: Chalcidoidea: Eupelmidae): clave y descripcion de dos especies nuevas. Acta Zoologica Mexicana, v. 26, n. 3, p. 669-683, 2010.

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PANIS, A. Contribucion al conocimiento de la biologia de la "cochinilla negra de los agrios" (Saissetia oleae Olivier). Boletin de Sanidad Vegetal Plagas, v. 3, n. 1, p. 199-205, 1977.

PEREIRA, J.; TORRES, L.; CABANAS, J.; BENTO, A. Parasitismo associado a Saissetia oleae (Oliv.) em Tras-os-Montes. Revista de Ciencias Agrarias, v. 21, n. 1-4, p. 237-244, 1998.

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PRADO, E.; SANTA-CECILIA, L. V. C.; ALVARENGA, T. M. Pragas da oliveira: bioecologia, inimigos naturais e manejo. In: Oliveira no Brasil: tecnologias de producao. Belo Horizonte: Epamig, 2012. p. 497-515.

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PRINSLOO, G. L. On the southern African species of Diversinervus [Hymenoptera: Encyrtidae], with descriptions of two new species. Biological Control, v. 30, n. 2, p. 133-142, 1985.

PRINSLOO, G. L. Encyrtidae. In: BEN-DOV, Y.; HODGSON, C. J. (Ed.). Soft scale insects--Their Biology, natural enemies and control. Amsterdam: Elsevier Science B.V., 1997. p. 69-109.

SILVA, A. G. A.; GONCALVES, C. R.; GALVAO, D. M.; GONCALVES, A. J. L.; GOMES, J.; SILVA, M. N.; SIMON, L. Quarto catalogo dos insetos que vivem nas plantas do Brasil, seus parasitos e predadores. Parte 2, Tomo 1, insetos, hospedeiros e inimigos naturais. Rio de Janeiro: Ministerio de Agricultura, 1968.

STRATOPOULOU, E. T.; KAPATOS, E. T. Key factors and regulation of population of Saissetia oleae (Hom., Coccidae) on olive trees in the region of Magnesia, Greece. Journal of Applied Entomology, v. 122, n. 1-5, p. 501-507, 1998.

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Received on February 4, 2013.

Accepted on July 4, 2013.

Ernesto Prado (1) *, Thiago Marinho Alvarenga (2) and Lenira Viana Costa Santa-Cecilia (1)

Empresa de Pesquisa Agropecuaria de Minas Gerais, Cx. Postal 176, 37200-000, Lavras, Minas Gerais, Brazil. departamento de Entomologia, Universidade Federal de Lavras, Lavras, Minas Gerais, Brazil. * Author for correspondence. E-mail: epradoster@gmail.com
Table 1. Parasitoids that were previously recorded
to be associated with the black scale in Brazil.

Species                                   Family           Biology

Diversinervus elegans                   Encyrtidae       Parasitoid
  Silvestri, 1915
Aloencyrtus saissetiae                  Encyrtidae       Parasitoid
  (Compere, 1939)
Coccophagus basalis                     Aphelinidae      Parasitoid
  Compere, 1939
Coccophagus brasiliensis                Aphelinidae      Parasitoid
  (Compere, 1936)
  Coccophagus brethesi
De Santis, 1967                         Aphelinidae      Parasitoid
  (= C. lecanii Brethes, 1913)
Coccophagus caridei (Brethes, 1918)     Aphelinidae      Parasitoid
Coccophagus fallax Compere, 1939        Aphelinidae      Parasitoid
Coccophagus lycimnia (Walker, 1839)     Aphelinidae      Parasitoid
Coccophagus oculatipennis               Aphelinidae      Parasitoid
  (Girault, 1916)
Coccophaguspauidiceps                   Aphelinidae      Parasitoid
  (Compere, 1939)
Chartocerus niger (Ashmead, 1900)      Signiphoridae   Hyperparasitoid
Mesopeltita truncatipennis             Pteromalidae     Egg predator
  (Waterston, 1917)                                    and parasitoid
Scutellista caerulea                   Pteromalidae     Egg predator
  (Fonscolombe, 1832)                                  and parasitoid
Lecaniobius utilis Compere, 1939        Eupelmidae       Parasitoid
Eupelmus coccidivorus Gahan, 1924       Eupelmidae     Hyperparasitoid
Gahaniella saissetiae                   Encyrtidae     Hyperparasitoid
  Timberlake, 1926

Species                                    Reference

Diversinervus elegans                   De Santis, 1979
  Silvestri, 1915
Aloencyrtus saissetiae                 Silva et al., 1968
  (Compere, 1939)
Coccophagus basalis                      Compere, 1939
  Compere, 1939
Coccophagus brasiliensis                 Compere, 1939
  (Compere, 1936)
  Coccophagus brethesi
De Santis, 1967                        Silva et al., 1968
  (= C. lecanii Brethes, 1913)
Coccophagus caridei (Brethes, 1918)      Compere, 1939
Coccophagus fallax Compere, 1939         Compere, 1939
Coccophagus lycimnia (Walker, 1839)      Compere, 1939
Coccophagus oculatipennis                Compere, 1939
  (Girault, 1916)
Coccophaguspauidiceps                    Compere, 1939
  (Compere, 1939)
Chartocerus niger (Ashmead, 1900)      Silva et al., 1968
Mesopeltita truncatipennis             Prado et al., 2012
  (Waterston, 1917)
Scutellista caerulea                     Compere, 1939
  (Fonscolombe, 1832)
Lecaniobius utilis Compere, 1939         Compere, 1939
Eupelmus coccidivorus Gahan, 1924        Compere, 1939
Gahaniella saissetiae                    Compere, 1939
  Timberlake, 1926

Table 2. Result of analysis of variance of six
characteristics of high heritability (0.55-0.80) obtained
by simulation and evaluated in thirteen populations.

FV          DF    [Y.sub.H55]   [Y.sub.H60]   [Y.sub.H65]

Treatment   12     .8261 **      1.058 **      .3925 **
Residue     637      .1398         .1201         .1265
Mean                100.28        100.30        100.25
CV(%)                0.37          0.34          0.35

FV          [Y.sub.H70]   [Y.sub.H75]   [Y.sub.H80]

Treatment    .7643 **      .7101 **      1.996 **
Residue        .1059         .0696         .0550
Mean          100.38        100.18        100.58
CV(%)          0.32          0.26          0.23

** and * significant at 1% and 5% levels, respectively,
according to an F-test.
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Author:Prado, Ernesto; Alvarenga, Thiago Marinho; Santa-Cecilia, Lenira Viana Costa
Publication:Acta Scientiarum. Agronomy (UEM)
Date:Oct 1, 2015
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