Feeding habits of Carabidae (Coleoptera) associated with herbaceous plants and the phenology of coloured cotton

Hábito alimentar de Carabidae (Coleoptera) associado com plantas herbáceas e fenologia de algodão colorido

ABSTRACT.

The carabids (Coleoptera: Carabidae) are recognized as polyphagous predators and important natural enemies of insect pests. However, little is known about the feeding habits of these beetles. In this work, we determine the types of food content in the digestive tracts of nine species of Carabidae associated with herbaceous plants and different growth stages of coloured cotton. The food contents were evaluated for beetles associated with the coloured cotton cv. BRS verde, Gossypium hirsutum L. latifolium Hutch., adjacent to weed plants and the flowering herbaceous plants (FHPs) Lobularia maritima (L.), Tagetes erecta L., and Fagopyrum esculentum Moench. The digestive tract analysis indicated various types of diets and related arthropods for Abaris basistriata, Galerita brasiliensis, Scarites sp., Selenophorus alternans, Selenophorus discopunctatus and Tetracha brasiliensis. The carabids were considered to be polyphagous predators, feeding on different types of prey.

Keywords:
diet; habitat manipulation; conservative biological control; predator

RESUMO.

Os carabídeos (Coleoptera: Carabidae) são considerados predadores polífagos e importantes inimigos naturais de insetos pragas. No entanto, pouco se sabe sobre os hábitos alimentares destes besouros. Neste trabalho, determinamos o tipo de conteúdo alimentar no trato digestivo de nove espécies de Carabidae associados a plantas herbáceas e diferentes estágios de crescimento de algodão colorido. O conteúdo alimentar foi avaliado no cultivar de algodão colorido BRS Verde Gossypium hirsutum L. latifolium Hutch. e nas adjacencias da área com algodoeiro, foi inserido canteiros com plantas daninhas e plantas herbáceas floriferas (PHF) Lobularia maritima (L.), Tagetes erecta L. e Fagopyrum esculentum Moench. A análise trato digestivo indicaram vários tipos de dietas e artrópodes relacionados com Abaris basistriata, Galerita brasiliensis, Scarites sp., Selenophorus alternans, Selenophorus discopunctatus e Tetracha brasiliensis. Os carabídeos estudados foram considerados predadores polífagos, alimentando-se de diferentes tipos de presas.

Palavras-chave:
dieta; manipulação do habitat; controle biológico conservativo; predador

Introduction

The coleopteran Carabidae are recognized as ground beetles, with approximately 40,000 species described. In the Neotropical region, this family includes 203 genera and 1,132 species (Costa, Vanin, & Casari-Chen, 1988; Lövei & Sunderland, 1996). These beetles have emerged as important natural enemies of insect pests of various crops including cotton (Chocorosqui & Pasini, 2000; Wyckhuys & O'Neil, 2006). The diet of carabids includes Collembola, earthworms, nematodes, slugs, snails, aphids, eggs and larvae of Diptera and Coleoptera, Lepidoptera pupae and seeds of herbaceous plants (Kromp, 1999; Holland & Luff, 2000; Holland, 2002; Tooley & Brust, 2002).

The digestive system of insects reflects a major interaction between these organisms and the environment due to their great morphological and functional digestive diversity and the assimilation of nutrients from different food types (Terra, 1988). These variations in the digestive tracts of insects facilitate the feeding habits of each species and are correlated with factors such as phenology and the type of structure produced by floriferous plants (Caetano, 1984; Ribeiro, Ferreira, & Terra, 1990). Therefore, insects can be analysed based on food availability by classifying the diets according to the nutritional composition, namely whether the food items are of animal or vegetable origin (Dow, 1986).

Conservative biological control aims to increase and conserve natural enemy populations to increase the efficiency of pest control insects (Barbosa, 1998); therefore, the techniques used in this type of control are easily integrated into pest management programmes (Collins, Boatman, Wilcox, & Holland, 2003). The manipulation of habitat using flowering herbaceous plants increases natural biological control but requires information on the natural enemies involved (Jonsson, Wratten, Landis, Tompkins, & Cullen, 2010) and the floriferous plant species used, which should only attract natural enemies (Hogg, Bugg, & Daane, 2011). Carabids use refuge areas for shelter during adverse periods of the year (Bedford & Usher, 1994). Thus, refuge areas consisting of flowering plants increase the diversity of carabids and other insect predators, which maintains the biodiversity of agroecosystems and also their stability (Frank & Reichardt, 2004; Macleod, Wratten, Sotherton, & Thomas, 2004).

Although studies exist on the feeding habits of carabids in temperate regions, many gaps remain in the knowledge and understanding of the feeding habits of these beetles (Toft & Bilde, 2002). The analysis of the content of the digestive tract of carabids allows the evaluation of the types of food eaten in the field. These analyses can be conducted using optical microscopy (Walrant & Loreau, 1995, Holland, 2002), ELISA assays, DNA (PCR) and radioactive isotopes (Wallace, 2004; Sheppard & Harwood, 2005; Greenstone, Rowley, Weber, Payton, & Hawthorne, 2007; Ikeda, 2010; Eitzinger & Traugott, 2011). The study of the feeding habits of these beetles through dissection and analysis by optical microscopy is an important way to clarify the environmental aspects related to carabids, given the variety of foods that can be eaten by insects. This information may facilitate the advancement of techniques to rear these insects in the laboratory for use in biological control programmes against agricultural pests.

In this work, we determine the types of food content in the digestive tract of nine species of Carabidae associated with herbaceous plants and different growth stages of coloured cotton.

Material and methods

Experimental area

The study was conducted from August 2012 to July 2013 at Fazenda Experimental de Ensino, Pesquisa e Produção (21°15'32"S and 48°16'49"W) and in the Laboratório de Ecologia de Insetos (LECOL), Departamento de Fitossanidade, Faculdade de Ciências Agrárias e Veterinárias (FCAV), Universidade Estadual "Júlio de Mesquita Filho" (UNESP), Jaboticabal, São Paulo State, Brazil.

The coloured cotton cv. BRS verde, Gossypium hirsutum L. latifolium Hutch., was used. The seeds were sown in a 40-m-long by 40-m-wide area, for a total of 1600 m² (Figure 1), and the spacing adopted was 1 m between rows, with two plants occurring in holes spaced from 0.3 to 0.5 m.

Figure 1
Schematic representation of the experimental area with colored cotton cv. BRS verde Gossypium hirsutum subdivided into 48 traps associated with the borders of herbaceous flowering plants (PHF) and weeds. The black dots (•) indicate the locations of the traps.

Flowering herbaceous plants and weed plants were grown along the edges (1 × 10 m) of the cotton area (Figure 1). The following flowering herbaceous plants (FHPs) were included: sweet alyssum (Lobularia maritima (L.) (Brassicaceae)), marigold (Tagetes erecta L. (Asteraceae)), and buckwheat (Fagopyrum esculentum Moench (Polygonaceae)). One of the edges was formed by weed plants: Amaranthus retroflexus L., Alternanthera tenella Colla and Amaranthus spinosus L. (Amaranthaceae); Sida spinosa L. (Malvaceae); Digitaria insularis (L.), Eleusine indica (L.) Gaer and Cenchrus echinatus L. (Poaceae); Acanthospermum hispidum DC. (Asteraceae); Portulaca oleracea L. (Portulacaceae); Richardia brasiliensis Gomes (Rubiaceae); Euphorbia heterophylla L. and Chamaesyce hyssopifolia (L.) Small (Euphorbiaceae); Commelina benghalensis L. (Commelinaceae); Indigofera hirsuta L. (Fabaceae); and Ipomea grandifolia (Dammer) O'Donell (Convolvulaceae). The FHP species were planted using seedlings or seeds, and they were allowed to grow for a period of time to match the phase of flowering of these plants with the beginning of sampling of carabids on cotton.

The sampling of Carabidae

The carabid species studied were Abaris basistriata Chaudoir, Calosoma granulatum Perty, Galerita brasiliensis Dejean, Odontocheila nodicornis (Dejean), Scarites sp., Selenophorus alternans Dejean, Selenophorus discopunctatus Dejean, Selenophorus seriatoporus Putzeys and Tetracha brasiliensis (Kirby). These species were chosen because they are considered to be abundant in the north-eastern state of Sao Paulo (Cividanes, Barbosa, Ide, Perioto, & Lara, 2009).

In the coloured cotton area, 12 pitfall traps associated with each edge were installed, and the traps were spaced 4 m apart and 1 m from the edges of the FHPs and weeds (Figure 1). The traps were made with 8 cm plastic cups containing a water solution (48.6 mL water, 1.35 mL 36.5 to 38.0%

formaldehyde PA and 0.05 mL detergent). The samples were collected once every two weeks, and this procedure continued until no more carabids were captured in the traps, occurring between the period of 12/2012 to 05/2013. The species captured were separated and kept frozen for later dissection.

The Carabidae sampling was performed following the phenological periods of crops: (i) vegetative (V) (12/2012); (ii) reproductive (bud, blossom and boll) (R) (dates 12/2012 to 04/2013); and (iii) harvest (H) (dates 04/2013 to 05/2013).

The species were identified by Dr. George E. Ball, Department of Biological Sciences, University of Alberta, Edmonton, Canada.

Carabidae food content

For this study, individuals of each beetle species in each of the phenological periods were dissected under a stereoscopic microscope (Table 1). Using fine-point scissors, the dorsal region (tergum) and the ventral region (sternum) were separated. The digestive tract was then removed and placed in a Petri dish, sectioning the crop region and the proventriculus with a scalpel. The material was analysed in a saline solution (0.9 % sodium chloride) using an optical microscope (Barbosa, Cividanes, Andrade, & Santos-Cividanes, 2012). The classification of food content followed Holopainen and Helenius (1992), and these types were considered: (i) arthropod identifiable parts - AIP, (ii) chitinous residue of arthropods - CRA, (iii) amorphous mass - AM, (iv) vegetable material with typical cell structure - VMTCS, (v) fluid - F, and (vi) no food - NF.

Results and discussion

Vegetative stage of cotton (V)

None of the species studied showed the food content types AIP (arthropod identifiable parts) or VMTCS (vegetable material with typical cell structure) (Table 2). Barbosa et al. (2012) also reported that T. brasiliensis did not have vegetable material in their digestive tract. However, when associated with Tagetes erecta and weed plants, T. brasiliensis showed fragments of arthropod exoskeleton characterized as CRA (chitinous residue of arthropods), and Scarites sp. also showed CRA when associated with weed plants.

Table 1
Total number of specimens dissected of Carabidae species associated with Flowering Herbaceous Plants (FHP) during the phenological periods of cotton cv. BRS verde Gossypium hirsutum between 12/2012 to 05/2013, Jaboticabal, São Paulo State, Brazil.

• V = vegetative; R = reproductive; H = harvest; (-)not occurrence of Carabidae.

Table 2
Percentage of food contents present in Carabidae species associated with Flowering Herbaceous Plants (FHP) during the phenological periods of cotton cv. BRS verde Gossypium hirsutum between 12/2012 to 05/2013, Jaboticabal, São Paulo State, Brazil.

• AIP = Arthropods identifiable parts; CRA = Chitinous residue of arthropod, AM = Amorphous Mass; VMTCS = Vegetable material with typical cell structure; F fluid; NF = No food. T = total individuals.

A lower number of prey items was observed during the vegetative stage compared to the reproductive and harvest stages. According to Marur and Ruano (2003), during the vegetative stage, there is a low occurrence of pests in cotton compared to the reproductive and harvest stages, especially thrips, aphids and root borers. In this study, it was observed that in the vegetative stage, Scarites sp. and T. brasiliensis were active in the search for prey because fragments of arthropod exoskeletons were lodged in the digestive tract.

The food type F (fluid) was observed only when C. granulatum and Scarites sp. were associated with L. maritima and T. erecta, respectively (Table 2). Moreover, C. granulatum showed a higher frequency of AM (amorphous mass) food contents, indicating the predatory activity of this species when associated with F. esculentum, L. maritima and T. erecta. Tetracha brasiliensis showed this content in association with F. esculentum.

Reproductive stage of cotton (R)

Only T. brasiliensis did not show predatory activity during this stage (Table 2). At this developmental stage of the plant phenological stages, the occurrence of pest species is more intense, especially Lepidoptera larvae, Coleoptera (weevils), Hemiptera (bugs) and Acari (mites) (Marur & Ruano, 2003).

When associated with all FHPs, Galerita brasiliensis showed a higher frequency of individuals with arthropod identifiable parts (AIP), such as lepidopteran heads, legs and spiracles. This was not observed in the other studied species (Figure 2). This finding is indicative of the high level of predation shown by this carabid beetle when associated with flowering plants. In terms of Calosoma granulatum and Selenophorus alternans, AIP content was found only when these species were associated with L. maritima and T. erecta, respectively. In the predator C. granulatum, arrow fragments, antennae and mandibles of arthropods were found (Figure 2). These results are in accordance with those of Gidaspow (1963) and Pasini (1991), showing that C. granulatum is a potential predator associated with the velvetbean caterpillar, Anticarsia gemmatalis Hubner (Lepidoptera: Noctuidae), and other lepidopteran pests.

The presence of Collembola was observed in Selenophorus alternans (Figure 2). Similar results were reported by Penny (1966), who found spiders, collembolans, small flies, mites and worms in the digestive tract of Nebria brevicollis Fabricius. Hengeveld (1980) reported parts of Hymenoptera in the digestive tract of members of the Pterostichus genus.

When associated with FHPs, S. seriatoporus showed a high frequency of chitinous residue of arthropods (CRA), and we observed jaw and leg fragments (Figure 2), while in O. nodicornis and Scarites sp., CRA was found only when they were associated with Tagetes erecta and F. esculentum, respectively (Table 2). Sunderland (1975) analysed the gut contents of Loricera pilicornis Fabricius and reported the presence of residual unidentified arthropods.

Barbosa et al. (2012) noted that antennae were food contents in which antennomeres and arrows could be seen, which were not components observed in this study. In the study by Barbosa et al. (2012), this finding may possibly be related to soybean and corn, where these carabids were captured.

The presence of amorphous masses (AMs) was common in A. basistriata, Scarites sp., S. alternans, S. discopunctatus and S. seriatoporus associated with FHPs. In contrast, G. brasiliensis and O. nodicornis presented AM less frequently when associated with weed plants. Forsythe (1982) also detected the presence of amorphous content in the digestive tract of the carabid Abax parallelepipedus Mitterpacker and Piller.

The AM food contents may be related to the predation of arthropods because A. basistriata, C. granulatum, O. nodicornis, S. seriatoporus and T. brasiliensis contained identifiable parts of arthropods and chitinous residue of arthropods (Figure 2). This result coincides with the reports of Barbosa et al. (2012), who found the absence of plant material in the food content of A. basistriata, S. seriatoporus, T. brasiliensis, Scarites sp. 2 and Scarites sp. 3. In contrast, in S. alternans and S. discopunctatus, identifiable parts of arthropods (AIP), chitinous residue of arthropods (CRA) and vegetable material with typical cellular structure (VMTCS) were observed. In this case, the origin of the AM content is unclear due to the presence of both food contents related to the activity of other predatory arthropods, such as plant material (Figure 2).

The crops of all Scarites sp. individuals had the presence of rock fragments identified as AM content (Figure 2). The presence of these fragments in Scarites sp. suggests that members of this genus live in galleries on the ground and that when ingesting food, they also ingest this type of substrate. These fragments may also function as grinding aids for food that is indigestible or has a nutritional need for carabids, such as minerals, which are essential for development and reproduction (Nation, 2001).

When associated with FHPs, S. alternans and S. discopunctatus showed a higher frequency of VMTCS content, which was found less frequently in G. brasiliensis and Scarites sp. associated with weeds and in L. maritima, respectively. These results are in accordance with those of Honek, Martinkova, Saska, and Pekar (2007) and Hurka and Jarošík (2003), which showed that insects of the genus Selenophorus are known to feed on the seeds of herbaceous plants and small invertebrates. Insect seed predators can be studied in research on the biological control of weeds in agroecosystems (Tooley & Brust, 2002).

The species C. granulatum and Scarites sp. had type F contents when associated with FHP (Table 2). According to Valencia-Jiménez, Bustillo, Ossa, and Chrispeels. (2000), the presence of this type of food content is characterized by the rapid digestion of food by enzymatic action or lack of prey. We observed a low frequency of the food content type F in the other species.

Figure 2
Types of food content in Carabidae species associated with flowering herbaceous plants in phenological period of colored cotton cv. BRS verde Gossypium hirsutum. 12/2012 to 05/2013, Jaboticabal, São Paulo State Brazil. *Phenological period of cotton without the presence of Carabidae species. VS = vegetative stage, RS = reproductive stage, HS = harvest stage; AIP = Arthropods identifiable parts; CRA = Chitinous residue of arthropod, AM = Amorphous Mass; VMTCS = Vegetable material with typical cell structure; F = Fluid; NF = No food.

Harvest stage of cotton (H)

Abaris basistriata, G. brasiliensis and S. discopunctatus when associated with L. maritima, weed plants and F. esculentum, respectively, showed identifying parts of arthropods (AIP), such as those of spiders and collembolans as well as antennae, tarsi and arrow fragments (Figure 2). These results show that these species feed on a wide variety of prey, from Lepidoptera to Araneae (Figure 2).

Abaris basistriata, G. brasiliensis, S. discopunctatus and S. seriatoporus showed chitinous residue of arthropods (CRA), such as fragments of exoskeleton, when associated with weed plants. The food type MA was observed in A. basistriata and S. discopunctatus when associated with FHPs and in G. brasiliensis and S. alternans when associated with F. esculentum (Table 2).

Typical vegetable material with cellular structure (VMTCS), such as seeds and other plant structures, was observed in A. basistriata and S. alternans associated with F. esculentum, L. maritima and Tagetes erecta (Figure 2). The same result was found for Scarites sp. associated with L. maritima and in S. seriatoporus associated with weed plants. Johnson and Cameron (1969) observed vegetable material in the digestive tract of the carabid Amara cupreolata Putzeys, while Lindroth (1974) found plant material in the gut contents of Amara aulica Panzer.

Only A. basistriata and S. discopunctatus had type F food content when associated with Tagetes erecta (Table 2). A similar result was observed by Sunderland (1975), who reported the presence of only fluid substances in the digestive tract of A. dorsales.

When associated with FHPs, digestive tracts without food (NF) were more frequent in G. brasiliensis and S. alternans compared to A. basistriata, C. granulatum, S. discopunctatus and S. seriatoporus. Several authors (Davies, 1953; Hengeveld, 1980) also found no traces of food in the digestive tract of Pterostichus madidus (Fabricius) and Pterostichus oblongopunctatus (Fabricius).

The edge L. maritima presented the highest number of Carabidae in the vegetative and reproductive stages, and weed plants presented the greatest number in the harvest stage. During the vegetative stage, T. brasiliensis associated with Tagetes erecta and weed plants can be considered the most efficient predator. On the other hand, during the reproductive and harvest stages, G. brasiliensis can be considered the most efficient predator in association with all edges in the reproductive stage and associated with Tagetes erecta and weed plants in the harvest stage.

The analysis of ingested material can show the preferences and feeding habits of Carabidae. These predators are polyphagous, but we observed that they prefer prey that occurs during specific phenological periods of cotton crops. Therefore, studies about feeding habits using tests such as ELISA and DNA (PCR) that can identify genera or species are important in the development of rearing techniques for these predators and their future use in the biological control of pests.

Conclusion

In conclusion at flowering herbaceous plants F. esculentum, L. maritima, T. erecta and weeds plants promote the occurrence and abundance of species carabids, with emphasis Selenophorus discopunctatus. Galerita brasiliensis has behaved as the most efficient predator in different phenological periods, being observed in feeding habit, spiders, head, leg and spiracle of Lepidoptera and others unidentified taxon. Abaris basistriata, Scarites sp. and S. alternans it was more associated with vegetable material with typical cell structure. Finally, Scarites sp. only species to all individuals consumed soil and rock fragment.

Acknowledgements

The authors thank the Foundation for Research Support of the State of Sao Paulo (FAPESP) and the National Council for Scientific and Technological Development (CNPq), who provided grants to the first and second authors, respectively. Thanks also to Alex A. Ribeiro for his help in field work, to Dr. George E. Ball for the identification of Carabidae species, and to Dr. Victor F. Oliveira de Miranda and Nubia M. Correia for the identification of the weed plants.

References

• Barbosa, C. L., Cividanes, F. J., Andrade, D. J., & Santos-Cividanes, T. M. (2012). Effect of Diets on Biology of Abaris basistriata and Selenophorus seriatoporus (Coleoptera: Carabidae). Annals of the Entomological Society of America, 105(1), 54-59.
• Barbosa, P. (1998). Conservation biological control. San Diego, US: Academic Press.
• Bedford, S. E., & Usher, M. B. (1994). Distribution of arthropod species across the margins of farm woodlands. Agriculture Ecosystem and Environment, 48(3), 295-305.
• Caetano, F. H. (1984). Morfologia comparada do trato digestivo de formigas da subfamília Myrmicinae (Hymenoptera, Formicidae). Papéis Avulsos Zoologia, 35(1), 257-305.
• Cividanes, F. J., Barbosa, J. C., Ide, S., Perioto, N. W., & Lara, R. I. R. (2009). Faunistic analysis of Carabidae and Staphylinidae (Coleoptera) in five agroecosystems in northeastern Sao Paulo State, Brazil. Pesquisa Agropecuária Brasileira, 44(8), 954-958.
• Chocorosqui, V. R., & Pasini, A. (2000). Predação de pupas de Alabama argillacea (Hübner) (Lepidoptera: Noctuidae) por larvas e adultos de Calosoma granulatum Perty (Coleoptera: Carabidae) em Laboratório. Anais da Sociedade Entomologica Brasileira, 29(1), 65-70.
• Collins, K. L., Boatman, N. D., Wilcox, A., & Holland, J. M. (2003). Effects of different grass treatments used to create overwintering habitat for predatory arthropods on arable farmland. Agriculture Ecosystem and Environment, 96(1), 59-67.
• Costa, C., Vanin, S. A., & Casari-Chen, S. A. (1988). Larvas de Coleoptera do Brasil São Paulo, SP: Museu de Zoologia/USP.
• Davies, M. J. (1953). The contents of the crops of some British carabid beetles. The Entomologist’s Monthly Magazine, 89(1), 18-23.
• Dow, J. A. T. (1986). Insect midgut function. Advances in Insect Physiology, 19(1), 187-328.
• Eitzinger, B., & Traugott, M. (2011). Which prey sustains cold-adapted invertebrate generalist predators in arable land? Examining prey choices by molecular gut-content analysis. Journal Applied Ecology, 48(3), 591-599.
• Forsythe, T. G. (1982). Feeding mechanisms of certain ground beetles (Coleoptera: Carabidae). Coleopterist Bulletin, 36(1), 26-73.
• Frank, T., & Reichardt, B. (2004) Staphylinidae and Carabidae overwintering in wheat and sown wildflower areas of different age. Bulletin of Entomological Research, 94(3), 209-217.
• Gidaspow, T. (1963). The genus Calosoma in Central America, the Antilles, and South America (Coleoptera: Carabidae). Bulletin of the American Museum Natural History, 124(7), 275-314.
• Greenstone, M. H., Rowley, D. L., Weber, D. C., Payton, M. E., & Hawthorne, D. J. (2007). Feeding mode and prey detectability half-lives in molecular gut-content analysis: an example with two predators of the Colorado potato beetle. Bulletin Entomological Research, 97(2), 201-209.
• Hengeveld, R. (1980). Polyphagy, oligophagy and food specialization in ground beetles (Coleoptera, Carabidae). Netherlands Journal of Zoology, 30(4), 564-584.
• Hogg, B. N., Bugg, R. L., & Daane, K. M. (2011). Attractiveness of common insectary and harvestable floral resources to beneficial insects. Biological Control, 56(1), 76-84.
• Holland, J. M. (2002). The agroecology of carabid beetles Andover, MA: Intercept.
• Holland, J. M., & Luff, M. L. (2000). The effects of agricultural practices on Carabidae in temperate agroecosystems. Integrated Pest Management Review, 5(2), 109-129.
• Holopainen, J. K. & Helenius, J. (1992). Gut contents of ground beetles (Col., Carabidae), and activity of these and other epigeal predators during an outbreak of Rhopalosiphum padi (Hom, Aphididae). Acta Agriculture Scandinavica, 42(1), 57-61.
• Honek, A., Martinkova, Z., Saska, P., & Pekar, S. (2007). Size and taxonomic constraints determine the seed preferences of Carabidae (Coleoptera). Basic Applied of Ecology, 8(4), 343-353.
• Hurka, K., & Jarošík, V. (2003). Larval omnivory in Amara aenea (Coleoptera: Carabidae). European Journal of Entomology, 100(3), 329-335.
• Ikeda, H. (2010). Diverse diet compositions among harpaline ground beetle species revealed by mixing model analyses of stable isotope ratios. Ecological Entomology, 35(3), 307-316.
• Jonsson, M., Wratten, S. D., Landis, D. A., Tompkins, J. M. L., & Cullen, R. (2010). Habitat manipulation to mitigate the impacts of invasive. Biological Invasions, 12(9), 2933-2945.
• Johnson, N. E., & Cameron, R. S. (1969). Phytophagous ground beetles. An Entomological Society of America, 62(4), 909-914.
• Kromp, B. (1999). Carabid beetles in sustainable agriculture: a review on pest control efficacy, cultivation impacts and enhancement. Agriculture Ecosystem and Environment, 74(1), 187-228.
• Lindroth, C. H. (1974). Coleoptera, Carabidae. In Handbooks for the Identification of British Insects (Vol. 4, Part 2, p. 148). London, UK: Royal Entomological Society of London.
• Lövei, G. L., & Sunderland, K. D. (1996). Ecology and behavior of ground beetles (Coleoptera: Carabidae). Annual Review of Entomology, 41(1), 231-256.
• Macleod, A., Wratten, S. D., Sotherton, N. W., & Thomas, M. B. (2004). “Beetle banks” as refuges for beneficial arthropods in farmland: long-term changes in predator communities and habitat. Agricuçture and Forest Entomology, 6(2), 147-154.
• Marur, C. J., & Ruano, O. (2003). Escala do Algodão. Informe da Pesquisa, 105(1), 1-4.
• Nation, J. L. (2001). Insect Physiology and Biochemistry Boca Raton, FL: CRC Press.
• Penny, M. M. (1966). Studies on certain aspects of the ecology of Nebria brevicollis (F.). Journal of Animal Ecology, 35(1), 505-512.
• Ribeiro, A. F., Ferreira, C., & Terra, W. R. (1990). Morphological basis of insect digestion. In J. Mellinger (Ed.), Animal nutrition and transport processes 1. Nutrition in wild and domestic animals (Vol. 5, p. 96-105.). New York, NY: Karger.
• Sheppard, S. K., & Harwood, J. D. (2005). Advances in molecular ecology: tracking trophic links through predator-prey food webs. Functional Ecology, 19(5), 751-762.
• Sunderland, K. D. (1975). The diet of some predatory arthopods in cereal crops. Journal of Applied Ecology, 12(2), 507-515.
• Terra, W. R. (1988). Physiology and biochemistry of insect digestion: on evolutionary perspective. Brazilian Journal of Medical and Biological Research, 21(4), 675-734.
• Toft, S., & Bilde, T. (2002). Carabid diets and food value. In J. M. Holland. (Ed.), The agroecology of Carabid beetles (p. 81-110). Andover, MA: Intercept.
• Tooley, J., & Brust, G. E. (2002). Weed predation by carabid beetles. In J. M. Holland, (Ed.), The agroecology of Carabid beetles (p. 215-229). Andover, MA: Intercept .
• Valencia-Jiménez, A., Bustillo, A. E., Ossa, G. A., & Chrispeels, M. J. (2000). α-Amylases of the coffee berry borer (Hypothenemus hampei) and their inhibition by two plant amylase inhibitors. Insect Biochemistry and Molecular Biology, 30(3), 207-213.
• Walrant, A., & Loreau, M. (1995). Comparison of iso-enzime electrophoresis and gut content examination for determining the natural diet of the ground beetle species Abax ater (Coleoptera: Carabidae). Entomologia Generalis, 19(4), 253-259.
• Wyckhuys, K. A. G., & O’neil, R. J. (2006). Population dynamics of Spodoptera frugiperda Smith (Lepidoptera: Noctuidae) and associated arthropod natural enemies in Honduran subsistence maize. Crop Protection, 25(11), 1180-1190.

Publication Dates

• Publication in this collection
  June 2017

History

• Received
  06 July 2016
• Accepted
  29 Sept 2016