Population Dynamics of Spalgis Epius (Lepidoptera: Lycaenidae), a Candidate Biocontrol Agent of Mealybugs and Its Interaction with Mealybug- Attendant Ants

Biocontrol Science and Technology

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Population dynamics of Spalgis epius (Lepidoptera: Lycaenidae), a candidate biocontrol agent of mealybugs and its interaction with mealybug- attendant ants

Anegunda S. Dinesha & Melally G. Venkatesha

To cite this article: Anegunda S. Dinesha & Melally G. Venkatesha (2016) Population dynamics of Spalgis epius (Lepidoptera: Lycaenidae), a candidate biocontrol agent of mealybugs and its interaction with mealybug-attendant ants, Biocontrol Science and Technology, 26:3, 337-350, DOI: 10.1080/09583157.2015.1115823

To link to this article: http://dx.doi.org/10.1080/09583157.2015.1115823

Accepted author version posted online: 04 Nov 2015. Published online: 11 Jan 2016.

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Download by: [Bangalore University] Date: 01 July 2016, At: 23:23 BIOCONTROL SCIENCE AND TECHNOLOGY, 2016 VOL. 26, NO. 3, 337–350 http://dx.doi.org/10.1080/09583157.2015.1115823

RESEARCH ARTICLE Population dynamics of Spalgis epius (Lepidoptera: Lycaenidae), a candidate biocontrol agent of mealybugs and its interaction with mealybug-attendant ants Anegunda S. Dinesha and Melally G. Venkatesha Insect Science Laboratory, Department of Zoology, Bangalore University, Bengaluru, Karnataka, India

ABSTRACT ARTICLE HISTORY Spalgis epius is an economically important hemipterophagous Received 12 February 2015 butterfly. Detailed information on the population dynamics, Revised 10 October 2015 natural enemies, and prey range of S. epius and its association Accepted 26 October 2015 with mealybug-attendant ant species is lacking. Three years of fi KEYWORDS eld studies conducted at Bangalore University campus, Spalgis epius; mealybugs; Bengaluru, India on these aspects indicated that the population population dynamics; prey density of S. epius was greatest from June to December and least range; mealybug-attendant from February to May in the low land region. S. epius survived on ants; predators eight prey species, which were present in different months, of which Phenacoccus indicus was recorded as a prey of S. epius for the first time. Different prey species occurred on 12 species of host plants. The occurrence of S. epius was negatively correlated with temperature and positively correlated with relative humidity and prey populations. Six mealybug-attendant ant species were associated with the larvae of S. epius. The seven general predators of S. epius adults were recorded. Knowledge on the population dynamics and a prey range of S. epius and its interaction with mealybug-attendant ant species could be helpful to using this predator as a major biocontrol agent of various species of mealybugs. This study contributed to our understanding of the population dynamics of a hemipterophagous butterfly.

Downloaded by [Bangalore University] at 23:23 01 July 2016 1. Introduction Natural enemies can have a major impact on the control of hemipteran pests of ﬁeld and orchard crops (Buckley, 1987). Information on spatio-temporal population dynamics of ants, mealybugs, and their natural enemies could be used to develop Integrated Pest Man- agement strategies that conserve natural enemies (i.e. parasitoids and predators) and therefore enhance their role as biological control agents (Thomson, Sharley, & Hoffmann, 2007). The number of host species used by an insect population is an important part of niche breadth. Undoubtedly, the successful conservation of rare Lepidoptera requires a detailed understanding of their natural history and ecology (Hochberg, Thomas, & Elmes, 1992). The Lycaenidae comprises almost a quarter of the ca. 17,000 species of known butterﬂies,

CONTACT Melally G. Venkatesha [email protected] Insect Science Laboratory, Department of Zoology, Bangalore University, Bengaluru, 560056, Karnataka, India © 2016 Taylor & Francis 338 A. S. DINESHA AND M. G. VENKATESHA

and the larvae of at least half of the species are associated with ants (Fiedler, 1991). Full or partial life histories have been recorded for about 20% of these species, and of those whose full life histories are known, about 75% associate with ants. These interactions range from parasitism to mutualism. Even when lycaenids are not myrmecophilous, they may be protected against ant aggression by a suite of ant-associated adaptations. The Lycaenidae are additionally characterised by a striking life history diversity. Herbivorous species consume an unusually wide array of different plant families, and a small number of lycaenids are parasitic or predatory. The behavioural and ecological diversity of the Lycaenidae makes this group particularly amenable to comparative studies of life history evolution (Pierce et al., 2002). Like other Lepidoptera, the great majority of lycaenid larvae feed exclusively on living plant tissue. However, some use insect-derived food resources during all or part of their development. These include ant eggs, larvae and pupae, ant regurgitations, Hemiptera, hemipteran honeydew, and other lycaenid larvae (Pierce et al., 2002). Some hemipterophagous lycaenids are myrmecophilous and can thwart an attack by their natural enemies with the help of hemipteran-attendant ant species. A number of features of the life histories of myrmecophilous lycaenids show that mutualism with ant species has a strong impact on population structure (Jordano, Rodriguez, Thomas, & Haeger, 1992). Various species of mealybugs (Hemiptera: Pseudococcidae) are major pests of economically important crops, that is, coffee, citrus, cocoa, guava, grapes, papaya, cotton, mango, mulberry, vegetable crops, and ornamental plants worldwide (Browning, 1992; Franco, Gross, Carvalho, Blumberg, & Mendel, 2001). Some of the economically important species are Planococcus citri (Risso), Planococcus lilacinus (Cockerell), Phenacoccus solenopsis Tinsley, Paracoccus marginatus Williams and Granara de Willink, Ferrisia virgata (Cockerell), and Maconellicoccus hirsutus (Green) (Hemiptera: Pseudococcidae) (Browning, 1992; Franco et al., 2001; Le Pelley, 1968; Williams & Willink, 1992). Biological control of mealybugs using parasitoids and predators is the most important control method as chemical control is less effective and environmentally undesirable (Bentley, 2002). The apeﬂy Spalgis epius (Westwood) (Lepidoptera: Lycaenidae) is an economically important butterﬂy as it is a potential predator of different species of mealybugs (Dinesh & Venkatesha, 2011a, 2011b). S. epius occurs in India, Burma, Sri Lanka, Philip-

Downloaded by [Bangalore University] at 23:23 01 July 2016 pines, Java, Bangladesh, Thailand, and Krakatau Island (Indonesia) (see Dinesh & Venka- tesha, 2011a). Studies on the biology, mating and oviposition behaviour, feeding potential, mass rearing, effects of temperature on the life cycle and inter- and intraspeciﬁc interactions of S. epius have been conducted (Dinesh & Venkatesha, 2011a, 2011b, 2012, 2013a, 2013b, 2014; Dinesh, Venkatesha, & Ramakrishna, 2010; Venkatesha, 2005; Ven- katesha & Dinesh, 2011; Venkatesha & Shashikumar, 2006; Venkatesha, Shashikumar, & Gayathri Devi, 2004). Knowledge on the population dynamics can help to determine the population pattern, population structure, and limiting factors of a species (Ehrlich & Murphy, 1987; Turchin & Taylor, 1992). Understanding of a population cycle provides a basis for predicting population changes (Turchin & Taylor, 1992). Although S. epius is a potential predator of various species of mealybugs, investigations on its population dynamics with relation to climatic factors are incomplete. Moreover, detailed information on the alternative prey species of S. epius in different seasons and their host plants, various species of BIOCONTROL SCIENCE AND TECHNOLOGY 339

mealybug-attendant ants and their association with S. epius and natural enemies of S. epius is lacking. The goal of our study is to understand the population dynamics of S. epius in relation to the environmental factors in an effort to use this predator more effectively as a biological control agent of mealybugs.

2. Materials and methods 2.1. Study area The study was carried out in the Bangalore University campus, Bengaluru, India (latitude 12° 58′N, longitude 77° 35′E, elevation 921 masl, total area 450 ha). The campus in the low land region has several vegetation patches containing weeds, shrubs, scrubs, herbs, papaya (Carica papaya L.), and ornamental plants.

2.2. Population dynamics of S. epius and its prey species The population density of S. epius was assessed during January 2009–December 2011 at eight selected sites in the study area (each site was about 30 m2 in size) where the occurrence of mealybug species was common. Observations were made in each study site for the infestation of mealybugs on herbs, weeds, shrubs, papaya, and ornamental plants. On finding a mealybug infestation, with the aid of magnifying lens (20×) the species were identified and number of larvae and pupae of S. epius as well as adults of prey species present on the plants was recorded once a month. The density of mealybug species was assessed by counting only adult females, which are sedentary and conspicuous. S. epius density was assessed by counting the second, third, and fourth instar larvae and pupae. The first instar larvae of S. epius were not counted as they hide deep in the mass of mealybugs. Different sampling methods were adopted for assessing the population density of mealybug species and S. epius based on the height of the host plants. Mealybug infested plants, which were less than one metre tall were searched 15–20 minutes, counting adult mealybugs and S. epius stages. Mealybug infested plants, which were more than one metre tall were divided into three sections (i.e. upper, middle, and lower parts). Each section was searched 15–20 minutes, counting adult mealybugs and S. epius

Downloaded by [Bangalore University] at 23:23 01 July 2016 stages. A destructive sampling method was used to count mealybugs and S. epius stages in papaya plants. Eight leaves were collected from the upper four quadrants (i.e. two leaves/quadrant) of papaya plants. The collected leaves were brought to the laboratory where adult mealybugs and S. epius stages were counted. Weather factors, that is, temperature, humidity, and precipitation were recorded daily in the study area using a thermo-hygrometer (Temp.Tec: Ao9Q32) and a rain gauge (Model: 380).

2.3. Record of host plants, mealybug-attendant ant species and predators Infestation of different mealybug species on various host plant species were recorded once a month. Different mealybug-attendant ant species and S. epius predators in the ﬁeld were recorded once a fortnight and observations were made on their interactions with S. epius by ad libitum method. Different species of ants and predators (spiders) were identiﬁed fol- lowing keys by Bolton (1994) and Sebastian and Peter (2009), respectively. 340 A. S. DINESHA AND M. G. VENKATESHA

2.4. Data analysis Prior to analysis, data were checked for homoscedasticity and normality, and data were transformed as needed. Data were pooled by month and prey species to show variations in S. epius and its prey populations. To assess the abundance of S. epius and its prey species in different months as well as in each year, a repeated measure analysis of variances (RM- ANOVA) was used. For each year, months represented replications (12) and sites (8) as treatments. To assess the difference in abundance among various species of mealybug, the abundance of S. epius on each mealybug species and S. epius incidence on different prey species were subjected to ANOVA. When ANOVA was significant at the P < .05 level, differences were determined by post-hoc Tukey’s honestly significant difference (HSD) multiple range test (P < .05) (SPSS Inc., 2008). Pearson correlation was utilised to analyse the influence of climatic factors on the population of S. epius (SPSS Inc., 2008).

3. Results 3.1. Population dynamics of S. epius and its prey species The population density of S. epius differed significantly between different months (RM- ANOVA: F11, 22 = 32.482, P < .05). The prey populations of S. epius increased from May onwards and reached its peak in July, and again in October, and fluctuated significantly until January (F11, 22 = 211.233, P < .05). Prey populations started declining from February and reached their lowest level during March–April (Figure 1). The highest population density of S. epius was observed from June to December and lowest from February to May (Figure 1). The population density of S. epius steadily increased from April and Downloaded by [Bangalore University] at 23:23 01 July 2016

Figure 1. Mean (±SE) population sizes of S. epius and its prey species in different months. Vertical lines indicate the SE of the mean S. epius population. BIOCONTROL SCIENCE AND TECHNOLOGY 341

reached its peak in August, and then fluctuated slightly until January (Figure 1). A minimum S. epius population density was recorded during March–May (Figure 1). fi There was no signi cant difference in the density of S. epius between years (F2, 22 = 0.676, P = .519). Similarly, there was no significant difference in its prey density between the years (F2,22 = 1.247, P = .307). Among different prey species, the abundance of P. mariginatus, P. solenopsis and Phe- nacoccus indicus (Avasthi and Shafee) (Hemiptera: Pseudococcidae) was significantly greater than that of other prey species in the study area (F7, 16 = 758.651, P < .05) (Figure 2). The abundance of S. epius on different prey species was significantly different (F7, 16 = 176.834, P < .05; Figure 2)(F7, 16 = 252.010, P < .05; Figure 2). Both S. epius and its prey populations increased during the months of minimum temperature and maximum humidity and vice versa (Figure 3). The number of an S. epius population was negatively correlated with temperature and positively correlated with humidity (% relative humidity) and number of prey, but it was not significantly correlated with precipitation (Figure 3; Table 1). The density of prey was negatively correlated with temperature, and positively correlated with relative humidity and precipitation (Table 1).

3.2. Record of host plants, mealybug-attendant ant species and predators The occurrence of eight mealybug prey species (Figure 4(a)–(h)) of S. epius in different months and their host plants are given in Table 2. S. epius fed on eight prey species, includ- ing the ﬁrst record for P. indicus (Figure 2). Two species of mealybug from January to April, eight mealybug species from May to October, and three species of mealybug during November–December (Table 2). Downloaded by [Bangalore University] at 23:23 01 July 2016

Figure 2. Mean (±SE) incidence of different prey species and S. epius. Means with different lower and upper case letters indicate signiﬁcant differences in S. epius and prey populations, respectively (ANOVA; Tukey HSD test P < .05). Vertical lines indicate the SE of the mean mealybug/S. epius population. 342 A. S. DINESHA AND M. G. VENKATESHA Downloaded by [Bangalore University] at 23:23 01 July 2016

Figure 3. Population ﬂuctuations of S. epius and prey species in relation to temperature, humidity and precipitation in different months.

Six mealybug-attendant ant species i.e. Tapinoma melanocephalum (Fabricius), Oeco- phylla smaragdina (Fabricius), Camponotus compressus (Fabricius), Camponotus variegatus (Smith), Crematogaster hodgsoni Forel, and Monomorium latinode Mayr (Hymenoptera: Formicidae) were associated with S. epius larvae (Figure 5(a)–(f)). Of BIOCONTROL SCIENCE AND TECHNOLOGY 343

Table 1. Relationship between S. epius/prey population and climatic factors. Correlation coefficient Species Year Rainfall Temperature Humidity Prey S. epius 2011 0.035 −0.716** 0.768** 0.501* 2010 0.199 −0.680* 0.852** 0.653* 2009 0.240 −0.751** 0.678* 0.666* Prey 2011 0.768** −0.530* 0.817** 2010 0.631* −0.640* 0.791** 2009 522* −0.510* 0.729** *Significant at 0.05 level. **Significant at 0.01 level. Downloaded by [Bangalore University] at 23:23 01 July 2016

Figure 4. (Colour online) Prey species of S. epius. (a) M. hirsutus, (b) P. citri, (c) P. indicus, (d) Coccido- hystrix insolita, (e) P. marginatus, (f) F. virgata, (g) P. solenopsis and (h) Rastrococcus iceryoides. 344 A. S. DINESHA AND M. G. VENKATESHA

Table 2. Prey range of S. epius and their host plants in different months. Month Prey species Host plant January–April P. marginatus Williams and Codiaeum sp. (Malpighiales : Euphorbiaceae) Granara de Willink C. papaya L. (Brassicales: Caricaceae) P. citri (Risso) Codiaeum sp. May–August P. marginatus C. papaya Manihot esculenta Crantz (Malpighiales: Euphorbiaceae) Codiaeum sp. Hibiscus sp. (Malvales: Malvaceae) Eupatorium perfoliatum L. (Asterales: Asteraceae) P. solenopsis Tinsley Parthenium hysterophorus L. (Asterales: Asteraceae) Sida sp. (Malvales: Malvaceae) E. perfoliatum F. virgata (Cockerell) Psidium sp.(Myrtales: Myrtaceae) Annona squamosa L. (Magnoliales: Annonaceae) P. indicus (Avasthi and Shafee) P. cineraria (L.) (Fabales: Fabaceae)

Coccidohystrix insolita (Green) Achyranthus aspera L. (Caryophyllales: Amaranthaceae) Ratrococcus iceryoides (Green) Phyllanthus reticulatus Poiret (Malpighiales: Phyllanthaceae) M. hirsutus (Green) Hibiscus sp. September–October P. solenopsis Parthenium hysterophorus L. (Asterales: Asteraceae) Sida sp., E. perfoliatum P. citri Codiaeum sp., A. squamosa P. indicus P. cineraria C. insolita A. aspera R. iceryoides P. reticulatus M. hirsutus Hibiscus sp. November–December P. citri Codiaeum sp. P. indicus P. cineraria P. marginatus C. papaya

these mealybug-attendant ant species, only O. smaragdina major workers were observed attacking S. epius larvae and rarely carrying them to their nest (Figure 6(a)). Major workers of O. smaragdina rarely attacked ovipositing females of S. epius (Figure 6(b)). Other species of mealybug-attendant ants were observed drumming S. epius larvae with their antennae and sometimes hitchhiking on the larvae. Six species of jumping spiders, that is, Epocilla aurantiaca (Simon) (Figure 6(c)) and Oxyopes javanus (Thorell) (Oxypidae); Hyllus semicupreus Koch, Myrmarachne plataleoides Cambridge (Figure 6(d) and (e)) and Ptocasius yashodharae Tikader (Salticidae) (Figure 6(f)); Amyciaea forticeps Cambridge (Thomisidae); and the praying mantis Hier-

Downloaded by [Bangalore University] at 23:23 01 July 2016 odula patellifera Serville (Mantodea: Mantidae) were rarely found attacking newly emerged S. epius adults in the ﬁeld.

4. Discussion The greater abundance of S. epius from August to January could be because of favourable environmental factors as well as high prey availability in the low land study area. In the month of May pre-monsoon showers in the study area induced the growth of small weeds, herbs and shrubs, which were hosts of various species of mealybug. From January onwards, a decreasing S. epius population may be owing to increasing temperature and lower humidity as well as fewer prey. Wilting of host plants during March–May reduced the build-up of prey populations, which in turn may have affected the S. epius population. A similar population trend of S. epius was observed in a cotton growing BIOCONTROL SCIENCE AND TECHNOLOGY 345

Figure 5. (Colour online) Mealybug-attendant ants. (a) T. melanocephalum, (b) O. smaragdina, (c) C. compressus, (d) C. variegatus, (e) M. latinode and (f) C. hodgsoni.

Downloaded by [Bangalore University] at 23:23 01 July 2016 region (Jothi et al., 2009). However, S. epius is known to occur abundantly from January to May and to be absent from June to December in coffee plantations (Vinod Kumar, Vasudev, Seetharama, Irulandi, & Sreedharan, 2007) which could be due to severe monsoon rains (4000–6000 mm) (Dolia, Devy, Aravind, & Kumar, 2008) and the absence of prey species in hilly plantation areas. A severe monsoon is unfavourable for the growth of mealybugs and only two species of mealybug P. citri and P. lilacinus occur in coffee plantations (Chacko, Krishnamoorthy Bhat, & Ramanarayan, 1977), which may inﬂuence the abundance of S. epius populations. Further, Arve, Patel, Chavan, and Vidhate (2011) reported the occurrence of S. epius from October to Decem- ber and its absence from January to September on P. solenopsis. These observations indicated that the abundance of S. epius in different periods in various regions is governed by climatic factors and availability of prey. In the present low land study area, moderate rains (850 mm) (Shankar, Balasubramanya, & Maruthesha Reddy, 2008) and the occurrence of 346 A. S. DINESHA AND M. G. VENKATESHA

Figure 6. (Colour online) Some of the predators of S. epius. (a) O. smaragdina carrying S. epius larvae, (b) O. smaragdina carrying S. epius adult, (c) E. aurantiaca caught S. epius adult, (d) H. semicupreus caught S. epius adult, (e) M. plataleoides and (f) P. yashodharae carrying S. epius larvae. Downloaded by [Bangalore University] at 23:23 01 July 2016 eight prey species helped to maintain the S. epius population for a long duration. Although environmental factors were favourable for mealybugs during August–September, the reduction of mealybug populations during this period could be due to the maximum incidence of S. epius population in the ﬁeld, which consumed a greater number of mealybugs. The abundant populations of prey species, that is, P. marginatus, P. solenopsis and P. indicus may be due to the occurrence of their host plants. Two species of mealybug P. marginatus and P. solenopsis survived on ﬁve and three species of host plants, respectively. The more abundant weed Prosopis cineraria (L.) (Fabales: Fabaceae) was the only host for the mealybug P. indicus in the study area, which was one of the major prey species for S. epius from May to December. Although the abundance of S. epius on various prey species was different, its incidence was dependant on the density of prey BIOCONTROL SCIENCE AND TECHNOLOGY 347

species which suggest that S. epius attacked all prey species based on their density and thus, found to be a successful density-dependent predator. As a result, an S. epius population was positively correlated with prey populations. However, the minimum incidence of S. epius on F. virgata compared to other prey species may be because F. virgata occurred sparsely and sporadically in the study area. Moreover, this species is well protected by long wax body threads (Hanchinal et al., 2011), which may deter the attack of S. epius larvae. Butterflies are particularly sensitive and conspicuous indicators of climatic and environmental changes (Dennis, 1993). Butterfly phenology is known to be sensitive to climatic changes; emergence dates, flight periods and number of broods have all been related to trends in warming (Roy & Sparks, 2000; Stefanescu, Peñuelas, & Filella, 2003). A significant negative correlation between an S. epius population and temperature suggests that an S. epius population decreases with increasing temperature as reported by Dinesh and Venkatesha (2012). However, Vinod Kumar et al. (2007) reported that an S. epius population was positively correlated with rising temperature. Many studies docu- mented that the growth rate of lepidopteran larvae increased with rising temperature to some extent, but at maximum temperatures, growth rate decreased or larvae died (Rawlins & Lederhouse, 1981). Larvae of S. epius put mealybug debris on their back and mimic mealybugs (Dinesh et al., 2010), and thus generally escape attacks by mealybug-attendant ants (Venkatesha et al., 2004). Ant species T. melanocephalum, C. compressus, C. variegatus, C. hodgsoni and M. latinode were not hostile to S. epius larvae as reported for Anoplolepis longipes (Jerd.) (Venkatesha, 2005; Vinod Kumar, Vasudev, Seetharama, Irulandi, & Sreedharan, 2008). However, O. smaragdina ants rarely attacked S. epius larvae likely because of scar- city of mealybug honeydew in a sparse mealybug population and hence, attacked non- honeydew secreting S. epius larvae as reported by Venkatesha (2005) and Vinod Kumar et al. (2008). However, the hemipterophagous S. epius has evolved as an amyrmecophilous type and ants derive no benefit from the predatory larvae (Venkatesha, 2005). Unlike other lycaenids, S. epius larvae do not have dorsal nectary gland, and some ant species visiting honey-secreting hemipterans are hostile to these larvae (Venkatesha, 2005). As several hemipteran-attendant ant species hinder the activities of parasitoids and insect predators of mealybugs (Fraser, Axén, & Pierce, 2001; Pierce et al., 2002), S. epius may be an

Downloaded by [Bangalore University] at 23:23 01 July 2016 effective natural enemy of mealybugs as it can co-exist with mealybug-attendant ants in the field as reported by Dinesh and Venkatesha (2013a). Although a few general predators attacked fresh adults of S. epius occasionally, they were not found interfering with the oviposition activity of females and thus do not seem to affect the biological control activity of S. epius. The results of our study indicate that S. epius can survive successfully on various prey species in a range of fluctuating environmental factors. Moreover, unlike many other parasitoids and insect predators of mealybugs, S. epius can co-exist with different species of mealybug-attendant ants and attack prey. There are no known specific predators or parasitoids known to attack S. epius. However the use of S. epius as a biocontrol agent may be compromised by the build-up of alternative prey species on weeds/shrubs/herbs in the vicinity that pull this predator away from the target pest. Future studies need to investigate how non-crop vegetation and associated mealybugs interact with S. epius in an adjacent cropping system. 348 A. S. DINESHA AND M. G. VENKATESHA

Disclosure statement No potential conﬂict of interest was reported by the authors.

Funding This work was supported by University Grants Commission (UGC), New Delhi, India under grant number [F. No. 33-344/2007 (SR)]; and Council of Scientiﬁc and Industrial Research (CSIR), New Delhi, India [09/039(0100)/2011 EMR-I].

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