Danos causados por Conotrachelus psidii (Coleoptera: Curculionidae) en frutos de feijoa (Acca sellowiana).
Palabras clave: Frutos danados. Interaccion insecto-planta. Taxonomia. Gorgojo.
Abstract: The feijoa, Acca sellowiana, is a native fruit species from Southern Brazil. In this work, we study the occurrence and damage caused by a weevil species to the fruits of feijoa. The study was conducted during two seasons in orchards and the natural forests of A. sellowiana at two locations in the States of Santa Catarina (SC) and Rio Grande do Sul, Brazil. In the feijoa orchard in Lages, SC, fruits were sampled to typify the injury. The fruit size, incidence, and severity of damage to the fruits were measured. Fifteen plants were randomly selected in which 30 fruits were measured weekly and the number of weevil injuries per fruit was counted. The taxonomic expertise confirmed the species as Conotrachelus psidii (Coleoptera: Curculionidae). The incidence and severity of weevil damage was higher on fruits from monoculture orchards than on fruits from native forests. Both unripe and ripe fruits were damaged by weevils through epidermis disruption resulting in blackened holes. The larvae damage the pulp and seeds, there by causing rotten fruits. Weevils are able to damage the feijoa fruits immediately after the onset of fruiting. In feijoa monoculture, 100% of the fruits evaluated until harvest were damaged by C. psidii. The severity of the weevil damage increased proportionately to the increase of fruit size.
Keywords: Damaged fruits. Insect-plant interaction. Taxonomy. Weevils.
Damage caused by Conotrachelus psidii (Coleoptera: Curculionidae) to the fruits of feijoa (Acca sellowiana)
The feijoa (Acca sellowiana (Berg) Burret) or pineapple guava in English is a fruit tree that belongs to the family Myrtaceae. It is distributed throughout the Brazilian Southern Plateau, from Parana to Rio Grande do Sul States, and in North-Eastern Uruguay, occurring in Araucaria forests and natural grasslands (Mattos 1990). It is commonly known in Brazil as "goiaba serrana", "goiabeira-da-serra"or "feijoa"(Mattos 1990).
Ducroquet et al. (2000) pointed out that their fruits have a distinctive flavor and aroma and contain bioactive components that, according to Weston (2010), may be sold as nutraceutical products. The anti-oxidant and immunological properties of feijoa fruits are attributed to bioflavonoids/polyphenols such as catequins, leucoantocianins, proantocianidins, and-naftoquinones (Ebrahimzadeh et al. 2008). According to Quintero (2012), the processed fruits are used in more than 15 commercial products such as juice, brandy, icecream, and jam. In New Zealand, the fruit pulp is used to make juices, wines, liqueurs, and chocolates among other products (Thorp and Bieleski 2002).
The species A. sellowiana has been considered, by the Brazilian Ministry of Environment, as a high promising domesticated plant for the future, suitable for small family farm production systems in Brazil (MMA 2007). Although it is cultivated in Southern Brazil, feijoa is also commercially cultivated in several regions of the United States, Colombia, New Zealand, and Australia among others (Thorp and Bieleski 2002). In China, it was introduced as an ornamental plant and nowadays it is cultivated in orchards for fruit production (Zhang et al. 2010).
The success of cultivating feijoa on a commercial scale depends on the domestication process by natural selection within productive populations and on their breeding without losing their rusticity and natural resistance to diseases and pest. According to Hickel and Ducroquet (1994), the first record of feijoa cropping in Brazil dates from the beginning of 90's. Two major insects' infestations were observed, the fruit fly, Anastrepha spp. and an unusual weevil of the genus Conotrachelus.
Belonging to the Coleopteran order the Conotrachelus Dejean is one of the largest genera in the world. According to O'Brien and Couturier (1995), there are more than 1,100 Conotrachelus species that are concentrated in the Neotropical region and they report two new species Conotrachelus eugeniae O'Brienand C. dubiae O'Brien that are economically important due to their attack on commercially and grown fruits in the Amazonian basin. In the Peruvian Amazon, the species C. eugeniae was found damaging fruits of Eugenia stipitata Me Vaughn (Myrtaceae), and C. dubiae on Myrciaria dubia Mark Vaughn (Myrtaceae) fruits (O'Brien and Couturier 1995; Couturier et al. 1996; Delgado and Couturier 2004). In addition, Delgado and Couturier (2014) studied the major pests of cashew (Anacardium occidentale L.) in the Peruvian Amazon and found that Conotrachelus sp. was one of the five insect species that causes significant pseudo fruit damage. On the other hand, the species Conotrachelus psidii Marshall, 1922 is reported mostly due to its damaging "guava fruits" Psidium guajava L. (Myrtaceae). This species in which the larva feeds on the pulp and seeds of guava is present in Bolivia, Brazil, Paraguay, and Venezuela (Costa Lima 1956, Couturier et al. 1996; Vasquez and Delgado 2002; Bailez et al. 2003, Delgado and Couturier 2004; Salas-Araiza and Romero-Napoles 2012).
In southern Brazil, weevils of the Conotrachelus were observed causing damage to feijoa (A. sellowiana) fruits in high lands, whereas fruit fly was more frequent at low altitude (Ducroquet et al. 2000, Hickel and Ducroquet 2006). According to Ducroquet et al. (2007: 2008) most of the work done for breeding feijoa was to improve yield and fruit quality. Thereby the control of insect pests is dependent on the use of synthetic chemical products. Moreover, regarding the regional condition in the Santa Catarina State, we observed that the improvement of the crop system has not taken into account the sustainable management strategies of major pests occurring in feijoa.
The few farmers in South Brazil who already started growing feijoa adopted conventional systems that include the use of pesticides that are recommended for apple orchards but are not registered for feijoa cultivation. This brings us to legal problems and, besides that, growers need information about the level of damage caused by the feijoa weevil and what the restrictions are in order to avoid Conotrachelus infestations (Luckmann et al. 2009). It was also argued that in case no chemicals were registered for the cultivated species, it would be better to select a plant from natural feijoa populations that occur in natural ecosystems. Cultivation under ecological principles was also claimed by organic farming that can use home-made preparations to protect the crop.
The objectives of this study were to identify the species of Conotrachelus weevil occurring in feijoa orchards in Southern Brazil, to characterize fruit injuries, and to evaluate the intensity of the damage caused by this insect. The description of the injury and the infestation by Conotrachelus will show basic information that will help to design a suitable program for sustainable management of the weevil in feijoa orchards. This native fruit species has high potential as commercial crop in Southern Brazil.
Material and methods
The study was carried out from November 2008 until April 2010 in the regions of "Planalto Serrano Catarinense", in Santa Catarina State and "Campos de Cima da Serra" in Rio Grande do Sul State, both in Southern Brazil. The samples of insects were collected in native feijoa plants in Araucaria forest ecosystem and in orchards of feijoa.
Species identification. Samples of adult weevils were collected from feijoa plants. A white cloth was stretched out on the canopy projection and the stirring of the branches was performed. Immediately after collection, the weevils were killed in mortal glass containing ethyl acetate. Then, the insects were assembled and placed in an oven at 38 degrees for 48 hours for drying, labeled, and sent to a specialist. The taxonomic identification of the specimens was confirmed by the weevil specialist Dr. Germano Henrique Rosado-Neto, Federal University of Parana (UFPR), by means of dichotomous keys and by comparison with insects of the entomological collection at UFPR. The identified specimens were deposited in the collections of the Museum of Entomology of UDESC/CAV, Lages, SC and the Pe. J. S. Moure Entomology Collection of Zoology Department at UFPR, PR, Brazil.
Characterization of weevil's injuries on feijoa fruits. Fruits of feijoa were collected in trees of the Municipalities of Capao Alto (27[degrees]57'S 50[degrees]00'W), Painel (27[degrees]53'S 50[degrees]06'W), and Vacaria (28[degrees]29'S 50[degrees]58'W). The fruits were put into thermo-box and brought to Laboratory of Homeopathy and Plant Health at EPAGRI Experimental Station, Lages, SC. The typical weevil damages were characterized through the description of external and internal symptoms of the fruits. Cuts in the fruit pericarp were done to observe the oviposition site, as well the disposition of eggs. Then, destructive analysis was done by a transverse cut in the equatorial region of the fruit for description of internal damage and larvae characterization.
Incidence and severity of weevil on feijoa fruits. The study was conducted from the end of flowering (November 2009) until the fruit maturation (April 2010). Fruits were collected from orchards located at EPAGRI Experimental Station located in Lages, SC (27[degrees]48'S 50[degrees]19'W) 904 m high. According to Koeppen, the climate of this region is subtropical Cfb, humid and summer. Wintertime is cool with an annual temperature average of approx. 16[degrees]C (Peel et al. 2007; Epagri/Ciram 2011). The orchard from where the fruits were collected had 1.5 ha, under ecological management, with spacing of 1 m among plants and 5 m among rows. The orchard was surrounded by native pastures, conifer plantation and a segment of Araucaria forest belonging to Atlantic biome. Thirty fruits at the height of 1.5 to 2.0 m in each 15 randomized plants were labeled. Every week, the number of typical weevil holes per fruit was counted and the diameter of each fruit was measured. The incidence of damage was considered as the proportion of fruits that had at least one typical hole caused by C. psidii in relation to the total fruits. The severity was estimated by counting the number of holes per fruit. Pearson's correlation analysis was done to study the relation between incidence (proportion of damaged fruits) and severity (number of holes per fruit) with fruit diameter through SAS[R] statistical program version 9.2.
Results and discussion
Species identification and damage characterization of the feijoa weevil. The sampled weevils were all identified as Conotrachelus psidii (Curculionidae: Molytinae). This insect in its adult form is a small beetle about six mm long by four mm wide, dark-brown, with mouthparts shaped snout and elongated shape. Their elytra show longitudinal striai covered by yellow and white thinner and short setae which corroborates with Monroy and Insuasty (2006). Salas-Araiza and Romero-Napoles (2012) report that adults of C. psidii presents mesosternum plane between the middle coxae, the metastemum has the surface densely covered with coarse and deep punctures, the carina in the interval five disappears in the basal third and the humeri are rounded.
It was observed that C. psidii caused damage on unripe, as well as, on ripe feijoa fruits. The damaged fruit showed deformation and presented dry black spots hollow and pierced with many holes and the small ones ([+ or -] 2 cm in diameter) drop soon after the weevil attack. The holes in the feijoa fruits were made by the mouthparts (placed at the distal end of the long and thin snout) due to feeding and oviposition behaviors. In both cases, the mandibles allow epidermis scraping and perforations of fruit bark (Fig. 1A). Boscan de Martinez and Casares (1980) reported that the adults and larvae of C. psidii can also feed from flower buds and small fruits of P. guajava distributed in the Neotropical Region.
The C. psidii eggs (1 mm long) are deposited about 3-4 mm beneath the fruit epidermis only one egg per hole, however it was found more than one oviposition site per fruit (Fig. 1B) and consequently it was found more than one larvae in a fruit as was observed by Monroy and Insuasty (2006) in P. guajava fruits. Our observations contrast with those of Rodriguez and Casares (2003) that found three eggs of Conotrachelus sp. per hole in fruits of Manilkara achras L. (Sapotaceae). The fruit tissue around the oviposition hole died and became dark and hardened, causing fruit deformation (Fig. 1C). According to Souza et al. (2003) if fruits of feijoa are superficially damaged by C. psidii they present physiological disturbance showing abnormal and anticipated maturation and are considered unsuitable for natural consumption and industrialization. Monroy and Insuasty (2006) also observed that P. guajava fruits damaged by C. psidii lose their commercial value. Ducroquet et al. (2000) reported that perforations done by the weevil on feijoa fruits also facilitate the infection of pathogenic diseases such as anthracnose (Colletotrichum sp.).
The larvae of C. psidii hatch in approximately four days following the oviposition with white color and feed of the inner fruit part, building galleries throughout pulp and eventually reaching the seeds. The fruit pulp became dark and rotten (Fig. 1D), which anticipate the fruit drop. These observations are similar those reported by Bailez et al. (2003) about damage and biological cycle of C. psidii on fruits of P. guajava, a related species to feijoa.
According to Bailez et al. (2003) and Valente and Benassi (2014) the life cycle of C. psidii on P. guajava in the laboratory conditions is about 360 [+ or -] 144 and 302,59 days, respectively. However Monroy and Insuasty (2006) working at natural conditions observed that the total C. psidii life cycle lasted 199 days. The daily annual average of temperature in the area where C. psidii was sampled is 16[degrees]C and the wintertime is relatively cold with minimum temperatures reaching -10[degrees]C. This temperature is probably not optimal for the development of C. psidii, but the presence of feijoa could facilitate the establishment of this insect (Ducroquet 2000).
Fruit infestation by Conotrachelus psidii. Mature fruits harvested from native growing feijoa trees exhibited less infestation (40, 55 and 64% of the total fruits) and reduced number of holes per fruit (2.1, 6.1, and 1.35 holes/ fruit) than those collected from conventional orchard (75% of fruit infestation and 11.2 holes/fruit) (Table 1). According to Sa and Silva (2011) fruit sampling from the feijoa plants is considered a suitable method to assess the level of infestation of weevil in the orchards. This method is also recommended for larval control of weevil on P. guajava. Sa and Silva (2011) reported that a high infestation of C. psidii occurred in monoculture where there was a high density of guava plants in comparison to diversified areas where plants were dispersed. It seems that higher food availability attracts more insects for oviposition and increase reproductive rate. In agreement with that, Luckmann et al. (2009) observed the fruits of feijoa from the monoculture system but managed under ecological principle presented more damage from weevil than fruits sampled from plant natural growing in the forest. According to Altieri (2003) diversified crop systems mislead insect to found the proper host plant. At the same time gives the stability of low population density due to the greater food availability and the presence of phytophagous insects will provide a smooth fluctuation of pest enemies.
Size of fruits and infestation of weevil. The diameter of fruit was positively correlated with the number of fruits damaged (incidence) by weevil in every plant (r = 0.80, P [less than or equal to] 0.001) (Fig. 2).
The injury by breaking the epidermis and attempting to make holes throughout cork feijoa fruit cause deformation in the early stage of fruit development. Ferreira et al. (2003) in studying the infestation of the weevil Conotrachelus dubiae on the fruits of Myrciaria dubia under Amazon conditions found positive correlation between fruit damage and fruit ripeness. In fact, injuries on fruits stimulate ethylene production, which speeds up fruit maturation (Kluge et al. 2002).
Bailez et al. (2003) reported the studies of C. psidii on P. guajava and found larvae damaging fruits from the size of 4 cm diameter. These species grow in warmer conditions than feijoa and a single hole per fruit is enough to start putrefaction. In most studies, the losses are estimated by counting the damaged fruits regardless the number of holes per fruit (Moore 1983; Haji et al. 1995). In our study, 20% of feijoa fruits at 0.5 cm diameter showed perforations and at 3.0 cm diameter all fruit were damaged by the weevil. Luckmann et al. (2009) verified that fruits from monoculture orchard located at Lages reached 98% of damage by Conotrachelus sp. (probably C. psidii). In Venezuela, C. psidii could affect more than 60% of the fruits of P. guajava (Boscan de Martinez and Casares 1980).
Injury severity of C. psidii on fruits of feijoa. The number of holes per fruit are correlated with the diameter of the fruit (r = 0.83, P [less than or equal to] 0.001) (Fig. 3). Fruits with more than 3.0 cm diameter had an average of 15 holes per fruit.
Conotrachelus psidii occurs in feijoa orchards before the late flowering time. The high frequency of fruit infestation and damage severity by C. psidii justify the development of sustainable management in feijoa orchards. In Theobroma grandiflorum ("cupuacu"), according to Aguilar and Gasparotto (1999), the success of chemical control of Conotrachelus sp. is difficult due to development of the larval stage inside the fruits. The pupae develop in the soil. Bagging fruits would be a good option to get high quality fruits, free of insect damage (Teixeira et al. 2011). This practice was already suggested by Hickel and Ducroquet (1994) to manage fruit fly on feijoa. For that insect, the authors recommended to bag fruits until 22 mm diameter and before 45 days of harvest. Because the weevil can damage the early stage of fruit development, it is necessary to start fruit bagging at the beginning of the feijoa fruit formation.
Additionally, Silva-Filho et al. (2012) found an attractive effect of feijoa bud flowers and weevil excrement on the adults of other weevils. The sugary and fleshy characteristics of feijoa flower petals match the taste and feeding of weevil (Sazima and Sazima 2007). This could be used as traps to manage weevil populations in the feijoa orchards.
In conclusion, the weevil species that occur in native plants and orchards of Acca sellowiana in the Southern Brazil region is Conotrachelus psidii (Coleoptera: Curculionidae). The damage caused by the feijoa weevil can start from the beginning of fruit formation. Injuries of feijoa weevil on fruits cause deformation and anticipate maturation and make it unsuitable for consumption. High infestation and losses are more expected under monoculture conditions.
The authors would like to thank CNPq (Conselho Nacional de Desenvolvimento Cientifico e Tecnologico) and FAPESC (Fundacao de Apoio a Pesquisa Cientifica e Tecnologica do Estado de Santa Catarina) for providing financial support for this research through the Guarani-Serra Geral Consortium Network, Project FAPEU/FAPESC n. 16261/10-2 and the Project Nucleo de Agroecologia e Saude Ambiental TO TR2012000363. They are also grateful to the farmers and technicians from EPAGRI for their valuable help during the study. We also appreciate the comments made by the reviewers of this paper. The second author is a PQ-CNPq researcher.
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Received: 26-Jun-2014 * Accepted: 9-Mar-2015
JOMAN MACHADO DA ROSA (1,2), MARI INES CARISSIMI BOFF (1,3), MARCELO ZANELATO NUNES (1,2), LENITA AGOSTINETTO (1,4) and PEDRO BOFF (5)
(1) University of Santa Catarina State, Agronomy Department, 88520-000 Lages, SC, Brazil. (2) M. Sc. Laboratory of Entomology, email@example.com. Corresponding author. (3) Ph. D. Laboratory of Entomology. (4) Dr. Laboratory of Phytopathology. (5) Ph. D. Laboratory of Plant Health and Homeopathy, Lages Experimental Station of EPAGRI, 88.502-970 Lages, SC, Brazil.
Table 1. Intensity of damages by weevil Conotrachelus psidii on feijoa fruits, according to location of growing trees (orchard and native forests). Crop cycle 2009/2010. Incidence Location No. of fruits (% of injured fruits) Lages, SC (1) 40 75 Painel, SC (2) 40 55 Vacaria, RS (2) 40 40 Capao Alto SC (2) 40 64 V.C (%) -- -- Severity Location (No. of holes per fruit [+ or -] SE) (1) Lages, SC (1) 11.2 [+ or -] 1.22 (a) Painel, SC (2) 6.1 [+ or -] 1.19 (b) Vacaria, RS (2) 2.1 [+ or -] 0.53 (c) Capao Alto SC (2) 1.35 [+ or -] 0.23 (c) V.C (%) 51.5 (1) Experimental orchard of feijoa managed without chemicals. (2) Native forests. SC: Santa Catarina State; RS: Rio Grande doSul State; (3) SE: Standard error of mean. Means followed by the same letters in the column do not differ by Tukey's test (P < 0.05).