Lima bean (Phaseolus lunatus L. (Fabaceae) is an important legume species for human consumption in tropical regions (Bitocchi et al. 2017). Its seeds are important sources of protein for the populations of South America, Africa, and Mexico (Araújo et al. 2015). There are few studies on phytophagous insects related to P. lunatus in Brazil. Generally, in South America insect pests are a limiting factor adversely affecting the agricultural production of Fabaceae, especially in genus Phaseolus. For example, Aphis craccivora Koch (Hemiptera: Aphididae), as well as the phytophagous mites Eutetranychus banksi (McGregor) (Acari: Tetranychidae) and Tetranychus urticae Koch (Acari: Tetranychidae) (Coceano et al. 1998; Mendonça et al. 2011) have been reported to severely affect the production of several bean species.

A number of studies on natural enemies associated with phytophagous pests of P. lunatus have been reported in the world literature; examples include the predatory mites Phytoseiulus persimilis (Acari: Phytoseiidae) in the USA and Neoseiulus pseudolongispinosus (Xin, Liang and Ke) (Acari: Phytoseiidae) in China (Bancroft & Margolies 1999; Sarwar 2014), the predatory stink bug Podisus maculiventris (Say) (Hemiptera: Pentatomidae) and a eulophid wasp, Pediobius foveolatus (Crawford) (Hymenoptera: Eulophidae) (Nottingham et al. 2016), in the USA. Currently, there is little biological information on the occurrence of natural enemies associated with phytophagous insect pests on lima beans from South America. Here we report on our efforts to document the parasites and predators on this agronomic crop in the state of Piauí, in northeastern Brazil, as well as providing information on their bioecology and trophic interactions.

Weekly leaf samples were collected during May through Sep 2016 in experimental lima bean fields located at the Department of Plant Science, Agricultural Sciences Center, Federal University of Piauí (Socopo campus), Teresina, Piauí. A total of 200 plants were sampled for the entire study (10 leaves per sample). Mites, thrips, syrphids, and coccinellids were collected from excised leaves; when thrips were observed in the fields, a 30-min manual sample effort was performed. In addition, lima bean plants were sampled in an infested greenhouse. Parasitized aphids (mummies) were removed from leaves using a probe and placed individually in Petri dishes for the emergence of parasitoids. Predatory mites were mounted on microscope slides using Hoyer's medium and identified using the morphological identification keys of Chant and McMurtry (2007), Moraes et al. (1986), and Moraes et al. (2004) using a phase contrast microscope (400×) (Brand Olympus Model BX41, St. Louis, Missouri, USA). Once parasitoids emerged, they were placed in 70% alcohol and sent for identification by Dr. Marcus Vinicius Sampaio (Federal University of Uberlândia, Uberlândia, Minas Gerais, Brazil). Syrphidae larvae were removed with a brush, placed in flat bottom tubes, 8.5 cm H × 2.5 cm, and reared at 25 ± 1 °C, relative humidity of 70 ± 10%, and 12:12 h (L:D) photoperiod. Nymphs of the aphid Aphis craccivora Koch (Hemiptera: Aphididae) were offered ad libitum to larvae of the predator until they reached the pupal stage. Adult syrphids were stored in alcohol at 70% and sent for identification by Gil Felipe Gonçalves Miranda (Laboratory of Systematic, Urban and Forensic Entomology, National Institute of Amazonian Research, Manaus, Amazonas, Brazil).

Table 1.

Natural enemies collected with phytophagous insects on lima bean (Phaseolus lunatus) in northeastern Brazil.

The following predatory arthropods were recovered from leaf samples: Scymnus (Pullus) rubicundus Erichson (Coccinellidae: Scymninae), Pseudodorus clavatus (F.) (Diptera: Syrphidae: Syrphinae), as well as their prey, A. craccivora. Aphelinus sp. (Hymenoptera: Aphelinidae) was reared from the aphid A. craccivora. Franklinothrips vespiformis (Crawford) (Thysanoptera: Aeolothripidae) was reared from Tetranychus neocaledonicus André (Acari: Tetranychidae) and Caliothrips phaseoli (Hood) (Thysanoptera: Thripidae) (Table 1).

Fig. 1.

(A) Proctolaelaps bickleyi; (B) Amblyseius tamatavensi male, highlight for the long arrows; (C–D) Franklinothrips vespiformis; (E) emergence of Aphelinus sp. parasitizing Aphis craccivora; (F) Aphelinus sp. adult; (G) Pseudodorus clavatus larva; (H) Scymnus (Pullus) rubicundus egg; (I) S. rubicundus larva at different instars; (J) larva feeding on A. craccivora; (K) S. rubicundus adult.

Franklinothrips vespiformis, and its prey C. phaseoli, were collected from lima bean plants. The occurrence of both species on P. lunatus provides new information regarding their ecological association in this habitat. It is also the first report of this predator on lima bean since thrips surveys were conducted by Lima and Zucchi (2016) on fabaceous plants and weeds in northeastern Brazil. Earlier, Sampaio et al. (2009) had reported that F. vespiformis was collected from P. vulgaris (common beans). On the other hand, C. phaseoli is widely distributed in Brazil, and can be found on Macroptilium lathyroides (L.) Urb (Fabaceae) (Lima & Zucchi 2016), common beans (Jesus et al. 2010), and soybeans (Link et al. 1981).

In our study, the presence of Pseudodorus clavatus (F.) (Diptera: Syrpidae) feeding on A. craccivora on bean plants also was observed. Larvae of P. clavatus have a high efficiency in the predation of A. craccivora, besides being considered the most abundant and important syrphid predator in South America (Auad 2003). This predator occurs in several agronomic crops, such as citrus, cabbage, cucumber, and wheat, and may be associated with other aphid pests, e.g., Toxoptera citricidus (Kirkaldy), Brevicoryne brassicae (L.) (Hemiptera: Aphididae), Aphis gossypi (Glover) (Hemiptera: Aphididae), A. spiraecola (Patch) (Hemiptera: Aphididae), Myzus persicae (Sulzer) (Hemiptera: Aphididae), and B. brassicae (L.) (Hemiptera: Aphididae) (Auad & Trevizani 2005; Bächtold & Del-Claro 2013; De La Pava & Sepulveda-Cano 2015).

The predatory mites Euseius concordis (Chant) (Acari: Phytoseiidae), Amblyseius tamatavensis Blommer (Acari: Phytoseiidae), and Proctolaelaps bickleyi Bram (Acari: Ascidae) were collected together feeding on T. neocaledonicus (Fig. 1). Amblyseius tamatavensis proved to be the most abundant mite in our collections. This is the first report in Brazil of the natural occurrence of these 3 mite species on lima beans.

In summary, there is potential for natural enemies to be used in the management of phytophagous pests in lima bean production in Brazil. Further research on the ecological relationships of these various predators, parasites, with phytophagous pests found on P. lunatus is needed including, but not limited to, characterizing their bionomic attributes, preferences, and ultimate effectiveness in the field at reducing crop damage.

The authors thank the Coordination for the Improvement of Higher Education Personnel for the scholarship granted; to the scientific initiation fellow Clovyedson da Silva Pereira for the help in obtaining the images of the mites; to Lúcia Massutti de Almeida (Department of Zoology, Federal University of Paraná) for identification of predatory beetles, and to Marcus Vinicius Sampaio (Federal University of Uberlândia) for identification of Hymenoptera parasitoids.