First report of Lema bilineata Germar (Coleoptera: Chrysomelidae) damaging Physalis peruviana (L.) in Brazil

Increased production of the Cape gooseberry (Physalis peruviana L.) in Brazil has given rise to interest in identifying the phytophagous species that might damage this crop to inform preventive control and integrated pest management strategies. In this study, we report the occurrence and describe the damage that larvae and adults of Lema bilineata Germar (Coleoptera: Chrysomelidae) cause in P. peruviana. The number of L. bilineata individuals, both larvae and adults, significantly affected the total consumption of P. peruviana leaves. We also report, for the first time, three natural enemies, including a fungus, a fly, and an ant, which are associated with this pest in Brazil and may play a role in biological control strategies.

The Cape gooseberry, Physalis peruviana L. (Solanaceae), is native to the Andean region and is commercially grown in Brazil (MUNIZ et al., 2014) due to its pharmacological and nutritional benefits (SANTOS et al., 2020). It has also become an attractive alternative for small farmers seeking to diversify their crops because of the high added value of its fruits and its low costs of cultivation (PUENTE et al., 2011).
In Argentina, Lema bilineata Germar (Chrysomelidae) has been identified as another arthropod pest attacking this crop (BADO et al., 2000). Lema bilineata is a defoliating insect that feeds on host plants of the Solanaceae family (MONTI et al., 2020). It causes considerable economic damage during its larval and adult phases to solanaceous crops such as tobacco Nicotiana tabacum L., in Argentina (ORMEÑO et al., 2002) and South Africa (BENNETT et al., 1999), and to Physalis viscosa L. in Australia (STEVENS et al., 2010), and P. peruviana in Argentina (BADO et al., 2000) and Italy (SERVIZIO FITOSANITARIO REGIONALE, 2017).
Species of the genus Lema have been reported in Brazil since the 1950s (cOSTA LIMA, 1955), where they were not initially considered pests. Later, insects of this genus were reported to cause damage to corn plants, Zea mays L., in the Federal District (LAUMANN et al., 2004) and Acnistus breviflorus Sendtn. (Solanaceae) plants in the state of Rio Grande do Sul (pINHEIRO & GRAZIA, 2013). This study documents, for the first time, the presence of L. bilineata in cultivated P. peruviana in Brazil, representing an extension of its geographical distribution. We examined the foliar consumption in larval and adult L. bilineata and observed the presence of three natural enemies associated with this species. These basic aspects are essential for controlling the incidence of this pest.
Between November 2018 and March 2019, field surveys in P. peruviana plantations in the municipalities of Curitiba (25º25'42''S, 49º16'24''W), Campo Largo (25º27'32''S, 49º31'55''W), and Pinhais (25º23'30''S, 49º07'30''W), all of which are located in the state of Paraná, southern Brazil, revealed that many plants had been attacked by larvae and adults of chrysomelids. Samples of ten specimens of these insects were collected and sent to the Department of Zoology of the Federal University of paraná (UFpR), curitiba, for identification. The specimens were identified by Dr. Germano Henrique Rosado-Neto as L. bilineata. Samples were deposited in the entomological collection of Pe. Jesus Santiago Moure Museum (DZUP), housed within the Zoology Department of UFPR. The collected insects were kept in the laboratory under controlled conditions (25 ± 2 ºC, 60 ± 10% RH, and 12:12 h [L:D] photoperiod) with leaves of P. peruviana for rearing.
We evaluated the herbivory of P. peruviana individuals using leaf blade consumption bioassays. The treatments used to measure leaf consumption were different numbers of third-instar larvae and nonsexed adults aged up to 48 h. Intact, pesticide residuefree leaves of P. peruviana were placed into 120 mL polypropylene containers after first being disinfected with 2% hypochlorite (one leaf per container). The treatments consisted of a variable number (one, three, or five) of third-instar larvae or adult L. bilineata individuals. Leaves were photographed before and after 48 h of exposure to the insects. Ten replicates per treatment were carried out. Defoliation estimates were expressed as total and individual consumption and as a percentage of leaf area loss calculated using Easy Leaf Area software (EASLOM & BLOOM, 2014). A one-way ANOVA was used to analyze total consumption and mean individual consumption data, with the number of L. bilineata individuals per leaf as a factor. Mean separation was carried out using a Tukey test. Normality (Shapiro-Wilk) and homogeneity of variances (Levene) tests were performed to check the ANOVA assumptions. Statistical analyses were completed in R version 3.5.2 (R cORE TEAM, 2019).
The duration of the life cycle (from egg to adult) of L. bilineata under the conditions of this study was 26.3 ± 3.7 days, which is consistent with findings by BADO et al. (2000). Oviposition of L. bilineata usually occurred on the abaxial side of the P. peruviana leaves in an isolated pattern. The eggs ( Figure 1A) are yellow and elliptical, measuring 0.51 x 0.22 mm; this stage lasted for 4.9 ± 0.3 days. The larval stage consisted of four instars, with a duration of 1.9, 1.6, 1.8, and 2.4 days, from the first to fourth instars. Larvae are dark yellow and approximately 6 mm in length at the fourth instar, with a dark brown to black cephalic capsule ( Figure 1B). The insects pupate in a matte white cocoon with approximately 6 mm in length ( Figure 1C). The pupa stage lasted for 12.6 ± 0.9 days, twice as long as reported by BADO et al. (2000). In adults, we observed that the coloration of the elytra consisted of alternating bright yellow and dark brown longitudinal lines extending from the base to the apex ( Figure 1D). The pronotum was dark in males and light brown in females ( Figure 1E). We also observed that the larvae have a fecal shield ( Figure 1B). This behavior is common in members of the Criocerinae subfamily, serving as camouflage and defense against predators such as ants and termites (SELMAN, 1988) and parasitoids (OLMSTEAD, 1994).
The leaf consumption bioassay indicated that larvae and adults from the group with the highest number of individuals showed the highest average total and mean individual consumption (Table 1). This increase in individual foliar consumption when peruviana could; therefore, compromise productivity ( Figure 1F) throughout the insect's life cycle. During the collection and evaluation of L. bilineata larvae, we observed the emergence of   (2008). The identified isolate was deposited in the Microbiological Collections of the Paraná Network (CMRP-Taxonline) as CMRP4485. We did not quantify the abundance of these natural enemies in the present study; however, they may represent alternatives for controlling this pest, highlighting the importance of managing agroecosystems by preserving the biodiversity of beneficial fauna.