Biocontrol Science and Technology

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Research article: life history and host range of Prochoerodes onustaria, an unsuitable classical biological control agent of Brazilian peppertree

E. Jones & G. S. Wheeler

To cite this article: E. Jones & G. S. Wheeler (2017) Research article: life history and host range of Prochoerodes onustaria, an unsuitable classical biological control agent of Brazilian peppertree, Biocontrol Science and Technology, 27:4, 565-580, DOI: 10.1080/09583157.2017.1325837 To link to this article: http://dx.doi.org/10.1080/09583157.2017.1325837

Published online: 16 May 2017.

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Download by: [University of Florida] Date: 13 July 2017, At: 08:24 BIOCONTROL SCIENCE AND TECHNOLOGY, 2017 VOL. 27, NO. 4, 565–580 https://doi.org/10.1080/09583157.2017.1325837

Research article: life history and host range of Prochoerodes onustaria, an unsuitable classical biological control agent of Brazilian peppertree E. Jonesa,b and G. S. Wheelera aUSDA/ARS Invasive Research Laboratory, Ft Lauderdale, FL, USA; bSCA/AmeriCorps, Ft Lauderdale, FL, USA

ABSTRACT ARTICLE HISTORY The life history and host range of the South American defoliator Received 13 January 2017 Prochoerodes onustaria (: Geometridae) were examined Accepted 26 April 2017 to determine its suitability as a classical biological control agent of KEYWORDS the invasive weed Brazilian Peppertree, Schinus terebinthifolia,in Schinus terebinthifolia; the U.S.A. Larvae were collected feeding on S. terebinthifolia in ; Geometridae; Brazil and were colonised and tested in quarantine. Life history invasive weeds; observations indicated that 54% (n = 63) of larvae reared on consumption; specific leaf S. terebinthifolia leaves survived to adulthood and 65% of adults area (n = 34) required five instars. Development time from eclosion to adult did not differ by sex: males required 42.9 ± 1.1 days and females required 41.1 ± 0.9 days. No-choice host range tests were conducted on 11 species in two families (Anacardiaceae and

Sapindaceae), including U.S.A. native, commercial, and ornamental species. Larvae completed development on all species, although survival differed significantly among them. Larvae fed Anacardium occidentale, Cotinus coggygria, Dodonaea viscosa, and Mangifera indica demonstrated higher survival than those on S. terebinthifolia, whereas survival was reduced among larvae fed toxiferum and dodonaea. Consumption was significantly greater on M. toxiferum than on the other species. The results presented here suggest that P. onustaria is highly polyphagous, feeding and completing development on members of two related plant families, and is not suitable for biological control of Brazilian peppertree in the U.S.A.

1. Introduction Valued for its vibrant red fruit and evergreen foliage, Schinus terebinthifolia Raddi (Sapin- dales: Anacardiaceae) was introduced to over 20 countries in the Americas, Europe, Africa, and Asia as an ornamental in the nineteenth century (Ewel, Ojima, Karl, & DeBusk, 1982; Morton, 1978; Pell, Mitchell, Miller, & Lobova, 2011). Today, S. terebinthifolia is an inva- sive weed in many regions of the world, including the states of Florida, California, Texas, and Hawai’i in the U.S.A (CABI, 2016; USDA/NRCS, 2016). In Florida, where it is com- monly known as ‘Brazilian peppertree,’ S. terebinthifolia is a state-designated noxious

CONTACT G. S. Wheeler [email protected] USDA/ARS Invasive Plant Research Laboratory, Ft Lauderdale, FL, USA © 2017 Informa UK Limited, trading as Taylor & Francis Group 566 E. JONES AND G. S. WHEELER weed and prohibited plant and is listed as a Category I Invasive Exotic by the Florida Exotic Pest Plant Council (FLEPPC, 2015). Schinus terebinthifolia (hereafter Schinus) is native to the east coast of Brazil, northern Argentina, and Paraguay (Barkley, 1944; JBRJ, 2015; Mukherjee et al., 2012). In the U.S.A, Schinus occurs as a multi-stemmed, drooping capable of colonising a wide range of habitats, including areas of high moisture (Ewe & Sternberg, 2002), salinity (Mytinger & Williamson, 1987), and shade (Ewel et al., 1982). A vigorous grower prone to producing monocultures in areas disturbed by human activity, such as roadsides and canal banks, Schinus is also highly capable of invading largely undisturbed hammocks, pinelands, man- grove forests, and wetlands, including areas of Everglades National Park (Ewel et al., 1982; Rodgers, Pernas, & Hill, 2014). Its aggressive intrusion threatens the biodiversity of native habitats, which support native imperiled species, such as the state-threatened gopher tor- toise (Gopherus polyphemus Daudin) (Doren & Jones, 1997) and the federally endangered Florida panther (Puma concolor coryi Bangs) (Maffei, 1997). Schinus was recently esti- mated to occupy more than 280,000 hectares in peninsular Florida alone (Ferriter, 1997; Schmitz, Simberloff, Hofstetter, Haller, & Sutton, 1997). The abundant drupe production by Schinus between October and December each year provides a plentiful food source for birds and mammals when many native have completed their reproduction cycle, resulting in ingestion and widespread dispersal (Ewel et al., 1982). Despite this apparent benefit for native frugivores, the drupes can have paralysing effects on birds (Campello & Marsaioli, 1974; Kinde et al., 2012), and con- sumption of plant material is reported to cause illness in livestock and horses (Morton, 1978). A cardanol produced by Schinus drupes causes an itchy, blistering rash on human skin, and a similar rash is reported to result from contact with the weed’s sap (Morton, 1978; Stahl, Keller, & Blinn, 1983). Some individuals also experience respiratory irritation when the plant is in bloom (Morton, 1978). In addition, Schinus is known to produce allelopathic compounds that can inhibit the growth of native plant species (Don- nelly, Green, & Walters, 2008; Morgan & Overholt, 2005). As a member of the Anacardiaceae, Schinus is closely related to several Florida natives and is also confamilial with Mangifera indica L. (mango) and Pistacia vera L. (pistachio nut), two food crops that are produced commercially in the Schinus-invaded range (Pell et al., 2011; Perez & Ferreira, 2016; USDA/NASS, 2016). Schinus serves as an alternate host of several agricultural pests known to attack these and other commercial species: namely, red-banded thrips (Selenothrips rubrocinctus Giard) (Thysanoptera: Thripidae) (Cassani, 1986; Morton, 1978; Mossler & Crane, 2002), black vine thrips (Retithrips syria- cus Mayet) (Thysanoptera: Thripidae) (Wheeler unpublished data), and the root weevil Diaprepes abbreviates (L.) (Coleoptera: Curculionidae) – a major pest of the citrus indus- try in Florida (Hall et al., 2001; McCoy, Stuart, & Nigg, 2003). Efforts to control Schinus mechanically are complicated by the weed’s tendency to sprout shoots from cut stumps and branches, often requiring application of chemical her- bicides to prevent vegetative regrowth (Ferriter, 1997; Langeland, 2002). Though the plant often forms monocultures, Schinus thickets also contain native plant species, making clear cutting or widespread herbicide application problematic (Ewel et al., 1982). In 2011, the South Florida Water Management District reported fiscal year spending on Schinus removal (including mechanical and chemical methods) totalled $1795k – greater than that spent controlling the highly invasive Melaleuca quinquenervia (Cav.) S.T. Blake BIOCONTROL SCIENCE AND TECHNOLOGY 567

(Rodgers, Bodle, Black, & Laroche, 2012). For these reasons, and because many areas infested by Schinus are remote and inaccessible, classical biological control is being con- sidered to complement other methods of management. Field surveys and literature reviews were conducted to assess the diversity of associated with Schinus in its native range (Bennett & Habeck, 1991; Mc Kay et al., 2009; Silva et al., 1968). Using data collected with these methods, it was estimated that more than 150 phytophagous species consume Schinus in Brazil (Bennett & Habeck, 1991). Several of these species have been released as biological controls on Schinus in the Hawaiian Islands. The leaf-tying/defoliating caterpillar E. unguiculus (=utilis) Zim- merman (Lepidoptera: Tortricidae), the gall forming caterpillar Crasimorpha infuscata Hodges (Lepidoptera: Gelechiidae), and the seed feeding beetle Lithraeus atronotatus (Pic) (Coleoptera: Bruchidae) were released in the 1950s and 1960s, although their com- bined effect on Schinus has been negligible (Hight, Cuda, & Medal, 2002; Krauss, 1962; Yoshioka & Markin, 1991). Several species of the families Coleoptera and Lepidoptera were recently tested and found to be unsuitable for biological control of Schinus in the U.S.A. (Wheeler et al., 2016). The sawfly Heteroperreyia hubrichi Malaise (Hymenoptera: Pergidae) was rec- ommended for release on the mainland (Medal et al., 1999), but was not considered safe for release in Hawai’i (Hight, Horiuchi, Vitorino, Wikler, & Pedrosa-Macedo, 2003). Two insects, the thrips Pseudophilothrips ichini (Hood) (Thysanoptera: Phlaeothri- pidae) and the psyllid Calophya latiforceps Burckhardt (Hemiptera: Calophyidae), were recently recommended for release in the U.S.A. by the United States Department of Agri- culture (USDA)/ and Plant Health Inspection Service Technical Advisory Group for Biological Control (Diaz et al., 2015; Wheeler, Manrique, Overholt, Mc Kay, & Dyer, 2017). Additional surveys in the native range of Schinus produced an undescribed Paectes species (Lepidoptera: Euteliidae); preliminary testing indicates it may be suitable for release (Jones & Wheeler unpublished data). These surveys also identified another species: the defoliator Prochoerodes onustaria (Hübner) (Lepidoptera: Geometridae). The objective of this research was to describe the life history of this South American species and determine its laboratory host range using larval no-choice tests in order to esti- mate its suitability for biological control of Schinus.

2. Materials and methods 2.1. Plants All plant species were grown in outdoor groves or in screenhouses in 4- or 12-l pots under drip irrigation. All plants were fertilised with Peters® Professional Water Soluble Fertilizer (20-20-20, Scotts-Sierra Horticultural Products Company, Marysville, OH, U.S.A.) and Multicote 4® (15-7-15 + MgO + Micronutrients, Haifa, Altamonte Springs, FL, U.S.A.) and supplemented with vitamin solution Superthrive® (Vitamin Institute, North Holly- wood, CA, U.S.A.), prepared and applied according to label directions. An application of the insecticide acephate (9.4%, Bonide Systemic Control®, Oriskany, NY, U.S.A.) was occasionally required to control infestations of S. rubrocinctus and R. syriacus; however, no pesticide was applied to test plants within four weeks of host range testing. 568 E. JONES AND G. S. WHEELER

2.2. Insect field collection Larvae of P. onustaria were collected in Ouro Preto, Minas Gerais, Brazil (S20.4209; W43.55287; 1320 m elevation) and in Rio Grande do Sul, Brazil (S29.39690; W50.89867; 823 m elevation) during a February 2014 survey of herbivores feeding on Schinus. Identifi- cation and DNA barcode analysis of specimens were conducted by Dr Axel Hausmann (Zoologische Staatssammlung München, Munich, Germany; GenBank accession No. KT3530150).

2.3. Insects – laboratory rearing A colony of P. onustaria was maintained under USDA Agricultural Research Service Inva- sive Plant Research Laboratory quarantine from February 2014 to March 2017. Tempera- ture and relative humidity were maintained at approximately 24 ± 2°C and 65%, respectively, under a 12:12 light:dark photoperiod. Larvae were reared individually or in groups of 2–10 in Ziploc® food storage containers (591 ml, SC Johnson, Racine, WI, U.S.A.) (11 × 11 × 6.5 cm) or Glad® food storage containers (1890 ml, The Glad Products Company, Oakland, CA, U.S.A.) (17.5 × 12 × 9.5 cm) with lids vented with fine plastic mesh (7.5 × 7 cm and 9 × 9 cm, respectively). This technique was later modified and larvae were reared en masse in acrylic cages (40.5 cm3). The top and bottom of each cage were solid acrylic; the front held a hinged door lined with weather stripping, and fine plastic mesh was glued to the open back to allow air circulation. Each side of the cage had a single circular hole; one hole was fitted with plastic sheeting to reduce airflow, the other with a fabric sleeve to allow hand access. The floors of cages used for rearing, pupation, and mating were lined with paper towels (Make-a-Size Two-Ply Strength, up & up® Target Brands, Inc. Minneapolis, MN, U.S.A.) and misted with tap water to increase interior humidity. Plant material supplied for larval feeding was pruned from an outdoor grove consisting of three Schinus haplotypes; however, plant haplotype was disregarded when selecting foliage. Larvae in food storage containers were supplied excised Schinus leaves: young, tender tips for early instars and mature leaves for later instars. Larvae in acrylic cages were supplied with Schinus ‘bouquets’ consisting of 1–3 stems, 20–40 cm in height, placed in a 185 ml vial (No. 55-50, Thornton Plastic Co., Salt Lake City, UT, U.S.A.) filled with tap water and sealed with Parafilm ‘M’® Laboratory Film (Pechiney Plastic Packaging, Chicago, IL, U.S.A.). Plant material was replaced and frass was removed as needed, generally every 1–3 days. Upon prepupation, evident by the shrunken appearance of larvae and the preparation of cocoons using towels or leaves, larvae were moved to Glad® containers for the two days required for pupation. Once pupae sclerotised (generally 1 day), the genital pore position of each individual was examined under a microscope (Leica® MZ12 5, Leica Microsystems Ltd., Heerbrugg, Switzerland) to determine its sex, using a technique described by Oleiro, Mc Kay, and Wheeler (2011). Pupae were returned to acrylic cages for adult emergence and mating. Adult were supplied honey water (1:5) solution or Gatorade® (Lemon-Lime flavour in powered form, prepared according to label instructions [The Gatorade Company, Chicago, IL, U.S.A.]) in 30 ml cups (Solo® Plastic Soufflés, Solo Cup BIOCONTROL SCIENCE AND TECHNOLOGY 569

Company, Lake Forest, IL, U.S.A.) with dental wicks (#2 medium cotton rolls, non-sterile, Primo® Dental Products, New York, NY, U.S.A.) inserted through the lids for feeding. New solution was supplied every 2–4 days to prevent mould growth. Schinus bouquets were provided as an egg-laying substrate, and every 1–3 days, eggs were collected and placed in Ziploc® containers for hatching. After eclosion, neonates were supplied newly expanded Schinus tips and were returned to clean acrylic cages.

2.4. Life history A life history study of P. onustaria was conducted between July and October 2014. In total, 63 individual eggs were set up under the conditions and using the methods described above. Larval containers were misted daily with tap water and larvae were supplied fresh Schinus tips every 1–2 days. Moulting and survival data were collected daily. Instars were determined by counting moulted head capsules, which were located using a microscope (Leica® MZ12 5), col- lected using a paintbrush, and stored in 95% ethanol for later measurement using a Keyence VHX-600® digital microscope (Keyence Corporation of America, Atlanta, GA, U.S.A.). Pupae were sexed and weighed (Ohaus Explorer® E10640 d = 0.1 mg, Ohaus Corporation, Pine Brook, NJ, U.S.A.) on the third day after pupation to allow time for sclerotisation. The date of adult emergence was recorded and moths were returned to cages for mating. To determine the length of the adult life stage, 10 male and 10 female pupae from the colony were paired (male–female) in Glad® containers lined with paper towels. Emerged adults were supplied with dental wicks soaked in Gatorade® placed in a 15 ml cup (Dart® Conex Complements® Clear Portion Containers, Dart Container Corporation, Mason, MI, U.S.A.) for nectaring. Towels and wicks were replaced every 3 days to prevent mould growth, and emergence and death dates were recorded daily.

2.5. Host range The host range of P. onustaria was determined using larval no-choice survival tests under the conditions described above. All testing was conducted between October 2014 and November 2015. Eleven species in the families Anacardiaceae and Sapindaceae were tested as potential hosts (Table 1). Test plants were chosen based on taxonomic relatedness to Schinus and ease of procurement, except for the Florida native Dodonaea viscosa (Sapindaceae), which was chosen because it elicited a small amount of feeding in the potential biological control agent P. ichini (Wheeler et al., 2017). Within 24 hours of eclosion, unfed neonates were placed in individual Ziploc® contain- ers where they were supplied newly expanded leaves from Schinus or 1 of the 11 non-target species. The number of replicates tested at a given time varied depending on plant quality and young leaflet production, but each test always included a Schinus replicate. Frass was removed and the container was misted daily. Plant material was changed every 1–3 days, depending on level of consumption or wilt, and data on survival were recorded daily. When prepupation began, the remaining plant material was removed. Pupae were weighed and sexed on the fifth day following pupation, and the date of adult emergence was recorded. 570 E. JONES AND G. S. WHEELER

Table 1. Plant species used in no-choice larval host range tests to determine laboratory host range of P. onustaria.a Family, , and species Common name Plant status U.S.A. distribution Anacardiaceae S. terebinthifolia Raddi Brazilian peppertree Target weed introduced to FL FL, CA, TX, HI, PR Rhus copallina L. Winged Native to FL E, MW R. sandwicensis A. Gray Neneleau Native not present in FL HI (L.) Kuntze Poison ivy Native to FL E, MW, SW (L.) Krug & Urb Poisonwood Native to FL FL, PR (L.) Urb Poison ash Native not present in FL PR, VI M. indica L. Mangob Agricultural present in FLc FL, PR, HI P. vera L. Pistachio Agricultural not present in FLd CAd Cotinus coggygria Scop. European smoketree Introduced not present in FL E, MW, UT Anacardium occidentale L. Introduced not present in FL PR, VI Spondias purpurea L. Purple mombin Introduced present in FL FL, PR, VI Sapindaceae D. viscosa (L.) Jacq.e Florida hopbush Native to FL FL, PR, VI, CA, AZ, HI aPlant names, status and distribution follow USDA/NRCS (2016). bCarrie, Ice Cream, Jehangar, Juicy Peach, and Haden varieties. U.S.A. region abbreviations: E (East), MW (Midwest), SW (Southwest), PR (Puerto Rico), VI (Virgin Islands). cData from USDA NASS Quick Stats. dData from Perez and Ferreira (2016). eSapindaceae.

2.6. Consumption Because most consumption and growth occurs during the final instar in many Lepidop- teran species (Scriber & Slansky, 1981; Soo Hoo & Fraenkel, 1966), consumption data were collected during this stage on each test species. The final instar was identified by the moult of penultimate head capsule, easily recognisable due to its cream and brown, mask-like colouration. Upon moulting of the penultimate instar, all plant material and frass were removed from the larval container. Fresh leaves were scanned (Epson® Perfection 3590 Photo, Epson America, Inc., Long Beach, CA, U.S.A.) alongside a ruler. Images were imported into Adobe® Photoshop® CS4 Extended (Adobe Systems Incor- porated, San Jose, CA, U.S.A.), where leaf area (cm2) was determined by converting pixels to centimetres as measured on the ruler in the image. The scanned leaves were then supplied to larvae for feeding. Every 1–3 days, depending on level of consump- tion, wilt, or decomposition, leaves were removed from larval containers and scanned again to determine the area eaten (cm2). C. dodonaea was excluded from these measurements because its spinose leaves did not readily flatten during scanning and leached dermatitis-causing sap when cut or torn (Gross, Baer, & Fales, 1975; Pell et al., 2011). To estimate dry weight consumption gravimetrically, a specific leaf area (SLA) was cal- culated for each plant species [dry leaf weight (mg)/area (cm2)]. Ten leaves of each species, of size and shape similar to those fed to larvae, were scanned, dried at 50°C for 72 hours (Precision™ Model 6524, Thermo Fisher Scientific, Marietta, OH, U.S.A.), allowed to cool to room temperature, and weighed. Leaf area was calculated in Photoshop® and the dry weight of each leaf was divided by its area to determine an SLA. This value, different for each plant species, was multiplied by the area consumed by each larva to estimate dry weight consumption. BIOCONTROL SCIENCE AND TECHNOLOGY 571

2.7. Data analysis Prior to statistical analysis, all data were checked for agreement with the assumptions of analysis of variance (ANOVA) and transformed (log + 1) as appropriate. Data were ana- lysed with SAS® 9.3 (SAS Institute Inc., Cary, NC, U.S.A.). To determine if insect sex influ- enced life history results, a one-way ANOVA was conducted on development time and pupal weights. Larval survival data for host range tests were compared using a chi- square test. Larval pupal weights, development time, and leaf consumption for host range tests were analysed with a two-way ANOVA and means were compared with a Tukey’s honestly significant difference (HSD; P = .05). All data are reported untrans- formed as means ± SE.

3. Results 3.1. Life history Adult females appeared to preferentially oviposit on the undersides of paper towels lining cage floors, although eggs were also laid in the folds of the fabric sleeves and on Schinus leaflet margins, petioles, and auxiliary buds – singly and in clusters. Eggs were smooth and ovoid, with mean dimensions of 0.74 × 0.59 mm (n = 20). Viable eggs were bluish-green at oviposition and turned bright red, then mahogany, before eclosion, which occurred after 7.4 ± 0.1 days (n = 59; Figure 1(a)). All instars were looping, defoliating caterpillars (Figure 1(b)). Larvae changed slightly in appearance with maturation, altering in colour and texture. In first through third instars, the larval epidermis appeared slick and dark with a milky subdorsal stripe. During instars four through six, dark blemishes and irregular lateral lines appeared on the epidermis, giving it the appearance of bark. In the fourth instar, a pair of fleshy

Figure 1. Life stages of P. onustaria fed S. terebinthifolia leaves with corresponding developmental intervals in days (d) ± SE. (a) Eggs at various stages of maturation. (b) Fourth instar larva on the target weed. (c) Pupa near eclosion. (d) Pinned female specimen. (e) and (f) Ventral surfaces of adult male and female, respectively, for comparison of abdomen shape. 572 E. JONES AND G. S. WHEELER protuberances or ‘hips’ appeared on the dorsal lower third of the body and remained through the final instar. Similar protuberances are described for congener P. truxaliata (Guenée) (Palmer & Tilden, 1987). Behaviourally, neonates were highly mobile and dispersed rapidly upon eclosion. First and second instars often rested in midair, hanging by strands of silk several centimetres below the surface to which they were attached. Later instars frequently assumed a stick- like posture, attaching a silk thread to the substrate and stretching away from it at approxi- mately 45°. Early instars left small windows in young leaflets, while later instars consumed entire leaves, except for petioles. Most larvae required five instars to complete development, but of those that required a sixth (35%, n = 34), there was an apparent sex bias: three males to eight females (one indi- vidual was deformed and not sexed). In both sexes, each successive head capsule increased in width by 1.5× on average, which is in general agreement with Dyar’s rule (Dyar, 1890) (Table 2). Larval development time from eclosion to adult did not differ significantly between sexes (F1,32 = 1.67, P = .2061). Pupae of P. onustaria were obtect and tan with dark brown anal segments (Figure 1(c)). As pupae matured, the pupal cases softened and darkened. Development time from pupa to adult differed significantly by sex: females required fewer days for pupation than males (F1,32 = 19.90, P < .0001) (Table 2). Pupal dry weights also differed significantly by sex: females were heavier (F1,32 = 25.46, P < .0001) (Table 2). Slightly more than half (54%; n =63)oflarvaerearedonSchinus survived to adult- hood. Adult longevity averaged 22.9 ± 1.4 days and did not differ significantly by sex (F1, 18 =1.03, P = .3228) (Table 2). Adults of both sexes were predominately tan, with downy bodies, spotted legs, and simple filiform antennae (Figure 1(d)). Little sexual dimorphism was apparent, except in shape of the abdomen: male abdomens were slender with pointed apices, whereas female abdomens were rotund with blunt apices (Figure 1(e) and 1(f)). On all adults, wings were marked lightly with dark transverse striations (Figure 1(d)). A set of three postmedial lines was distinctive on the wings of adult P. onustaria, extending diagonally from the apex of the forewing to the middle inner margin of the hindwing. Often, a purple iridescence shone above this line, although it was not visible on all moths (Figure 1(d)). Also notable was a small brown tail protruding from each

Table 2. Results of life history observations on P. onustaria larvae fed S. terebinthifolia leaves. Males Females Instar N Days SE Width (mm) SE N Days SE Width (mm) SE I 16 6.4 0.7 0.4 0.01 17 5.4 0.4 0.4 0 II 14 3.6 0.3 0.6 0.01 16 3.6 0.2 0.6 0.01 III 14 3.3 0.2 0.9a 0.02 17 4 0.3 0.9b 0.02 IV 15 5.3 0.2 1.5 0.06 18 4.5 0.3 1.4 0.04 V 14 8.6 0.7 2.5 0.13 18 7.6 0.6 2.3 0.12 VI 3 11.3 1.9 2.6 0.07 8 9.6 0.5 2.9 0.11 Pupa 16 13.4 0.4 . . 18 11.7 0.2 . . Adult 10 21.5 2.4 . . 10 24.3 1.35 . . Pupal weight 16 . . 76.1 mg 2.9 18 . . 95.1 mg 2.5 Note: Mean ± SE development time by stage (days), larval head capsule widths (mm), and pupal dry weights (mg) of males and females. aN = 16. bN = 18. BIOCONTROL SCIENCE AND TECHNOLOGY 573 hindwing margin at M3, striped with cream-coloured scales. Similar colouration patterns and wing shapes, including postmedial lines and hindwing tails, are described for the con- gener P. tetragonata tetragonata (Guenée, [1858]) (Pitkin, 2002).

3.2. Host range Larvae of P. onustaria developed to adulthood on Schinus and all non-target species, 2 although survival differed significantly among plant species (X1,11 = 44.5, P < .0001) (Figure 2(a)). Percent survival to adulthood among larvae reared on A. occidentale, C. coggygria, M. indica, D. viscosa, and P. vera ranged from 70% to 78% (n values ranged from 20 to 35), compared with 37% (n = 79) for those fed with Schinus,and 15–25% (n =20)amongthosefed C. dodonaea and M. toxiferum (Figure 2(a)). Pupal weights were influenced by species and by sex (females were heavier), but not by their interaction (Table 3). Pupae reared on A. occidentale and P. vera were significantly heavier than those reared on S. purpurea, although none differed significantly from those reared on Schinus (Figure 2(a)). Development time to adult also was influenced significantly by species, but not by sex or their interaction (Table 3). Larvae reared on A. occidentale, M. indica,andP. vera developed to adulthood significantly faster than those on Schinus, C. dodonaea,andD. viscosa (Figure 2(b)).

3.3. Consumption

SLAs differed significantly among species (F10,99 = 79.49, P < .0001) (Figure 2(c)). Leaves of M. toxiferum had the highest SLA (21.5 mg/cm2), whereas C. coggygria and T. radicans had the lowest (4.0 mg/cm2). The SLA of Schinus (10.2 mg/cm2) did not differ significantly from that of A. occidentale, D. viscosa,orP. vera (Figure 2(c)). Dry weight consumption also differed significantly by species and sex but not by their interaction (Table 3). Larvae fed M. toxiferum consumed significantly more leaf material than larvae on any other species, yet exhibited lower survival than those fed Schinus and most other species (Figure 2(a) and 2(c)). Larvae fed Schinus consumed significantly more leaf material than larvae fed C. coggygria and D. viscosa, although larvae on the latter two species exhibited greater survival (Figure 2(a) and 2(c)). Although larval survival on A. occidentale and M. indica was greater than on Schinus, consumption levels did not differ significantly among these species (Figure 2(a) and 2(c)).

4. Discussion The laboratory no-choice results presented here demonstrate that P. onustaria consumed and survived on the target weed Schinus and all non-target species, although significant differences were found in larval performance, survival, and consumption. These data also indicate that, although larvae were collected on the target weed in two distinct regions of its native range, Schinus may not be the optimal host of P. onustaria; larval sur- vival was greater and development time was shorter among larvae fed A. occidentale, M. indica, and P. vera. Additionally, consumption was significantly higher on the Florida native M. toxiferum than on any other species, whereas survival to adulthood was among the lowest – suggesting that this species was a poor-quality host, requiring 574 E. JONES AND G. S. WHEELER

Figure 2. Mean ± SE results of no-choice tests of P. onustaria larvae on 11 test plant species and the target weed S. terebinthifolia. (a) Dry pupal weight of P. onustaria and percent survival of neonates to adult. (b) Development time in days (d) from neonate to adult. (c) SLA [dry leaf wt (mg)/area (cm2)] for each species and dry weight of material consumed by larvae (mg). The black bar within each panel represents the target weed. Numbers within bars represent the number surviving for each metric: (a) to pupal stage, (b) to adult, and (c) to prepupal stage. Within panels, bars and data points topped with the same letter were not significantly different according to Tukey’s HSD multiple com- parison test (P = .05). BIOCONTROL SCIENCE AND TECHNOLOGY 575

Table 3. Results of two-way ANOVA depicting effects of no-choice test species (Spp), insect sex, and their interaction on pupal weight, development time, and consumption by P. onustaria larvae during host range testing. Spp Sex Spp × sex Variable df FPdf FPdf FP Pupal weight 11 3.2 .0006 1 39.37 <.0001 11 1.26 .2538 Development time 11 13.08 <.0001 1 0.99 .3223 11 0.69 .7484 Consumption 10 43.83 <.0001 1 13.01 .0004 10 0.8 .6276 larvae to modify their feeding behaviour. Despite the increased consumption on M. toxiferum, neither pupal weight nor development time of larvae fed this species differed significantly from those fed most other species. The leaves of M. toxiferum had a significantly higher SLA than those of any other test species. The high SLA indicates that leaves of this species contained higher amounts of dry matter, which potentially diluted the nutrient content. High dry matter content also reduces the digestibility of plant material, and low digestibility and low nutrient content can induce compensatory feeding in larvae, ultimately resulting in higher consumption (Behmer, 2009; Soo Hoo & Fraenkel, 1966). Thus, the significantly higher consumption of M. toxiferum witnessed among larvae may have been the result of compensatory feeding, induced in response to a nutrient-dilute, poor-quality host. While SLA is useful to explain the high consumption M. toxiferum in particular, SLA is only one factor potentially affecting feeding behaviour and cannot be used to explain con- sumption levels on all species. Many test plants had significantly different SLAs, but did not induce significantly different levels of consumption among larvae. Possibly, increased consumption of M. toxiferum was induced in response to a dearth of an essential nutrient in this species – such as nitrogen – rather than to a high SLA. Low foliar nitrogen content is known to limit larval performance and induce compensatory feeding in several species (Mattson, 1980; Slansky & Feeny, 1977; Wheeler, Van, & Center, 1998; Zalucki, Clarke, & Malcolm, 2002). However, a hypothesis that low nitrogen content is solely responsible for high consumption of M. toxiferum is not supported by previous work. Wheeler, Chawner, and Williams (2014) demonstrated that the foliar nitrogen content of this species, grown under the same conditions as plants in this study, was not significantly different than that of Schinus, R. copallina,orT. radicans – all species on which P. onustaria larvae consumed significantly less foliage. There was a discrepancy between the survival of P. onustaria larvae fed Schinus in the life history observations (54%; n = 63) and those fed Schinus the host range testing (37%; n = 79). This difference could be influenced by several factors, among them the quality of leaves collected during different Schinus phenological stages, which are highly synchro- nous (Ewel et al., 1982). Schinus leaf flushing peaks during the summer months in South Florida, particularly in August. Life history observations, conducted between July and October, included leaves grown during this period, and the relatively high larval sur- vival suggests they were high quality. In contrast, host range testing was conducted from mid-September through mid-April – a period during which Schinus is reproductive; peak flowering season occurs in October in South Florida, and drupes are produced from December to February (Ewel et al., 1982). Reproduction has a physiological cost for plants, often requiring the reallocation of resources typically used for growth (Bazzaz, 576 E. JONES AND G. S. WHEELER

Chiariello, Coley, & Pitelka, 1987; de Jong & Kinkhamer, 2005; Lovett Doust & Lovett Doust, 1988). As Schinus flowered and fruited, access to new, readily expanding leaves was notably limited, and the P. onustaria larvae fed available mature leaves during this time exhibited reduced survival. The geometrid genus Prochoerodes consists of 24 described species distributed throughout the Americas, with highest biodiversity in the Neotropics (Pitkin, 2002; Scobel & Hausmann, 2007). Of these species, field host records are established for two: P. pilosa Warren in Ecuador and P. lineola (=transversata) (Goeze) in the U.S.A. Both species were shown to be polyphagous (Bodner, Brehm, Homeier, Strutzen- berger, & Fiedler, 2010; Wagner, 2005). Prior to this research, laboratory life history and host range were established for only one member of the genus, P. truxaliata (Guenée). Under laboratory conditions, P. truxaliata demonstrated a host range sufficiently narrow to be recommended as a biological control agent for Baccharis hamilifolia (L.) (Asteraceae) in Australia (Palmer & Tilden, 1987). This assessment, and others indicating the success of geometrids as biological control agents (Adair & Edwards, 1996; Heard et al., 2010), engendered confidence in this investigation of P. onustaria as a potential biological control agent for Schinus. However, the results presented here indicate that P. onustaria exhibits a broad host range similar to other geometrids tested on Schinus, namely Oxydia vesulia transpeneus (Cramer) (Fung & Wheeler, 2016), Hymenomima nr. memor (Broggi, Dyer, & Wheeler, 2016), and Oospila pallidaria Schaus (Chawner & Wheeler, unpublished data). Like these species, P. onustaria larvae were polyphagous in laboratory tests, consuming and developing on non-target species of ecological and commercial value found in many states and territories in the U.S.A. Therefore, P. onustaria will not be pursued as a biological control agent of Schinus in this region of the world.

Acknowledgements We thank J. Fung (AmeriCorps/SCA), K. Dyer, and E. Broggi (USDA-ARS-IPRL) for help with colony maintenance and advice; W. Pierre and A. Sanchez (USDA-ARS-IPRL) for maintaining healthy test plants; and two anonymous reviewers for their thoughtful comments. Identification and DNA barcode analysis (GenBank accession No. KT353015) were generously conducted by A. Hausmann (Zoologische Staatssammlung Munchen, Munich, Germany). Voucher specimens were deposited in the Smithsonian Institution, Washington, D.C. and Florida Department of Agri- culture and Consumer Services. Insect collections and exportations were authorised by Instituto Brasiliero do Meio Ambiente (Permit No.14BR004731/DF). The importation permit to the U.S.A. was issued by USDA/APHIS to G.W. (Permit No. P526P-07-06609).

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

Funding This project was partially funded by Florida Fish and Wildlife Conservation Commission (#08250, TA:088), South Florida Water Management District, and USDA/ARS. BIOCONTROL SCIENCE AND TECHNOLOGY 577

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