ZOBODAT - www.zobodat.at

Zoologisch-Botanische Datenbank/Zoological-Botanical Database

Digitale Literatur/Digital Literature

Zeitschrift/Journal: Denisia

Jahr/Year: 2006

Band/Volume: 0019

Autor(en)/Author(s): Mitchell Paula Levin

Artikel/Article: Polyphagy in True Bugs: A case study of phyllopus (L.) (, , ) 1117-1134 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

Polyphagy in True Bugs: A case study of (L.) (Hemiptera, Heteroptera, Coreidae)1

P.L. MITCHELL

Abstract: The polyphagous Leptoglossus phyllopus (L.) was examined with respect to host preference, tissue feeding specificity, seasonal dispersal among host , and life history. Mark-recap- ture, census, and rearing experiments demonstrated that this species exhibits true polyphagy, in that in- dividual bugs feed on plants from more than one family. Developmental parameters such as growth and survivorship did not differ among plants from several families, but did vary significantly with quality of host (e.g., wild vs. cultivated). Stadium duration, however, varied among wild host plant species in la- boratory experiments. Specialization on reproductive plant parts, coupled with sequential polyphagy and dispersal among a variety of seasonal host plants, allows multiple generations per year. Modes of fee- ding and preferred target tissues among coreids are discussed.

Key words: leaffooted bug, Leptoglossus phyllopus, polyphagy, stylet sheath, target tissue.

Introduction spp.), for example, employ a macerate-and- flush process, whereas an osmotic pump For phytophagous with piercing- mechanism is associated with coreids (MILES sucking mouthparts, feeding selectivity op- & TAYLOR 1994). However, some pentato- erates on two levels: preferred target tissue mids and lygaeids shift between salivary and host plant species. Tissue preference is sheath formation and lacerate-and-flush considered to be a conservative evolution- feeding (MILES 1972). ary character (TONKYN & WHITCOMB 1987); for example, specialization on xylem, Preference for a particular plant devel- phloem, or parenchyma is characteristic of opmental stage or structure (e.g., growing subfamilies or families in Auchenorrhyncha shoots, buds, ripe seeds), may also be associ- (PORT 1978). Phytophagous Heteroptera ated with specific groups. Pyrrhocoroidea have been extensively analyzed with respect feed predominantly on mature seeds, tingids to several factors associated with target tis- prefer mature leaves, while phytophagous sue preference: mouthpart morphology, sali- mirids concentrate on flowers, buds, and vary chemistry, preference for plant parts or new foliage (SCHUH & SLATER 1995). In structures, and mode of feeding (MILES some cases, however, such trends only be- 1972; COBBEN 1978; MILES & TAYLOR 1994; come evident at the tribal or even generic HORI 2000). The enzyme components of level. SCHAEFER & MITCHELL (1983) noted heteropteran saliva are considered to be a that an affinity for vegetative or reproduc- family-level character (MILES, cited in HORI tive structures is characteristic of tribes 2000), although induction of proteolytic en- within the Coreidae. Among Australian zymes has been demonstrated in a zoophy- coreids, KUMAR (1966) recognized two dif- tophagous mirid (ZENG & COHEN 2001). ferent types of feeding – exclusive sap feed- The mode of feeding may also be associated ing is found in some genera whereas others with particular taxa. Mirids (e.g., Lygus feed on both sap and fruit. However, such Denisia 19, zugleich Kataloge 1Dedicated affectionately to Ernst Heiss, my delightful colleague on the Executive Committee of the International der OÖ. Landesmuseen Heteropterists’ Society and heteropterist extraordinaire. Neue Serie 50 (2006), 1117–1134

1117 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

diversity of feeding was considered by phytophagous groups, he proposed that sap- COBBEN (1978) to indicate a “phase of un- feeding originated from polyphagous seed- balanced equilibrium.“ feeding, with the former mode of feeding tending toward a more restricted host range Even fewer generalizations may be made (COBBEN 1978). In Hemiptera in general, regarding host-plant specificity. Curiously, tissue-feeding specialization has been associ- the question of diet breadth in Heteroptera ated with host plant specificity (BERNAYS & has not been explored with the intense fer- CHAPMAN 1993), but this observation is vor devoted to -plant interactions in based primarily on the British fauna, and is Lepidoptera, Orthoptera, and other orders biased toward Sternorrhyncha and Auchen- of chewing insects. COBBEN (1978) charac- terized the Tingidae as monophagous while orrhyncha. Clearly, more information on suggesting that “polyphagy prevails“ among polyphagy in Heteroptera is needed. the phytophagous ; but he provided The objective of this research was to no comparable analysis for the Pentatomo- conduct a detailed study of polyphagous morpha. Nearly 30 years have passed since feeding behavior in a single coreid species, the publication of COBBEN’s (1978) monu- the leaffooted bug Leptoglossus phyllopus mental study of mouthparts and feeding (L.). Host range and dispersal, seasonal pat- strategies, but our understanding of het- terns of host plant use, preferred feeding eropteran-plant relationships remains limit- site, and target tissue were examined in or- ed. Neither facultative zoophagy nor the ex- der to characterize the factors influencing treme polyphagy associated with some het- host plant selection. Leptoglossus phyllopus eropterans is properly understood (ZENG & damages legumes, tomatoes, tree nuts, and COHEN 2001). WHEELER (2001) observes citrus in the southern and eastern United that despite an extensive literature on crop States (MITCHELL 2000), and is considered a injury, there are “large gaps in our knowl- minor economic pest. The primarily edge of mirid-plant interactions.“ Informa- Neotropical Leptoglossus GUERIN was tion for some heteropteran groups is lacking, selected for study because it includes species detailed ecological studies of bugs outside of exhibiting widely disparate feeding strate- agroecosystems are uncommon, and adult gies ranging from strict monophagy to ex- host plant records are not always reliable in- treme polyphagy, as well as a number of dicators of breeding hosts (SCHAEFER & species of economic importance. Several MITCHELL 1983). Leptoglossus species are presently expanding Polyphagy in Heteroptera is of great in- their ranges – and potential for economic terest from both an economic and an evolu- damage – geographically. The highly tionary standpoint. Many of the major agri- polyphagous L. zonatus (DALLAS), a pest of cultural pests (e.g., Nezara viridula (L.), Rip- many crops in and South America, tortus clavatus (THUNBERG), Leptoglossus has recently invaded the southeastern Unit- zonatus (DALLAS), Lygus lineolaris (PALISOT ed States to Florida (BUSS et al. 2005) and DE BEAUVOIS)) have a wide range of host has become a pest of Satsuma oranges in plants (SCHAEFER & PANIZZI 2000). Howev- , displacing L. phyllopus (HENNE et er, it is important to distinguish between al. 2003). Leptoglossus occidentalis HEIDE- generalist species composed of more special- MANN, once restricted to conifers in western ized populations and polyphagy at the indi- , has spread rapidly eastward vidual level (i.e., diet mixing) (FOX & MOR- across the continent to Ontario and New ROW 1981; BERNAYS & MINKENBERG 1997). England (RIDGE-O’CONNOR 2001). Acci- The evolution of omnivory has been shown dentally introduced into Italy in 1999 (TAY- to correlate with polyphagy in Heteroptera LOR et al. 2001), this species has now spread (EUBANKS et al. 2003), and these authors to Central Europe (RABITSCH & HEISS proposed that polyphagous, seed-feeding 2005). Thus, information on the feeding be- herbivores may be more likely to expand the havior of L. phyllopus may be applicable not diet to consume prey. COBBEN (1978, only in the southeastern , but 1979) considered polyphagous carnivory to to congeneric species of economic impor- be plesiomorphic within Heteroptera. For tance elsewhere.

1118 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

Materials and Methods Both L. phyllopus and another coreid, Eu- thochtha galeator (F.), were monitored. Num- Study site: Research was conducted pri- ber of adults, nymphs of all instars, and cop- marily at Brackenridge Field Laboratory ulations were counted. Location of bugs on (BFL), operated by The University of the plant was noted in greater detail than in at Austin. This field station is located inside earlier censuses, differentiating between the city limits of Austin, Texas, along the bud, stem, and leaf primordia as well as be- shores of the Colorado River, and comprises tween mature plant organs. The 1979 cen- 32 hectares of grassland, cedar-post oak sus covered the entire reproductive life span scrub and semi-deciduous woodland. of the host plant texanum BUCKL., Four study plots, each measuring 92.9 from bolting through seed set. 2 m , were established at BFL to investigate A plant census was conducted monthly seasonal activity of L. phyllopus and other in each study site in conjunction with the coreids. All plots were located in either ear- bug censuses in 1977 and 1978. Each plot ly successional or cultivated garden areas. was subdivided into 40 equal quadrats, and a Plot 1, on the river terrace, was dominated wire square measuring 930 cm2 was tossed by Johnsongrass, Sorghum halepense (L.) twice into each quadrat. This quadrat PERS., and various composite species. Plot 2, method was designed to eliminate the un- bordering an artificial pond, was composed equal representation of marginal areas fre- primarily of grasses and composites inter- quently associated with sampling by random spersed with prickly pear (Opuntia spp.) and toss (SOUTHWOOD 1966). After each throw, mesquite (Prosopis glandulosa TORR.). The presence or absence of plant species within remaining study plots were placed in the the wire sampler was noted, in order to com- cultivated garden area to ensure an adequate pute frequency of occurrence from a total of water supply during summer drought. Plot 3, 80 samples per study plot. Additionally, formerly under cultivation, had returned to counts were taken of number of stems, buds, native early successional vegetation two flowers, developing fruits, and mature fruits years before the commencement of research. of host plants within the confines of the Plot 4, the agricultural study plot, was plant- wire square. All counts were made visually ed each spring with (Lycopersicon es- in the field, and no plant material was re- culentum P. M ILL.), giant sunflower (He- moved from the study areas. All Leptoglossus lianthus annuus L.), and okra (Hibiscus host plants were identified to species. With [=Abelmoschus] esculentus L.). A sprinkler the exception of grasses, non-hosts were system provided water for both garden plots identified at least to genus. Within the twice weekly, and fertilizer was applied to Poaceae only S. halepense was distinguished; cultivated plants according to standard other grasses were lumped in a single cate- agronomic practices. gory. Plant family designations follow JUDD Field census: From July to November et al. (2002); species and describer names 1977, and February to November 1978, L. follow RADFORD et al. (1968) and CORRELL phyllopus individuals were visually counted in & JOHNSTON (1970). In 1979, only host each study plot at weekly intervals. All cen- plants were surveyed. Finer distinctions suses were taken within two hours of sunset, were used in the census of plant structural a time of maximal copulation and feeding ac- and reproductive organs, to correspond with the more detailed bug distribution studies. tivity. Field work was discontinued during the winter (mid-November through mid- For statistical analysis, plants were cate- February), as no bugs were active during this gorized as reproductive or non-reproductive, period. For each individual observed, the fol- and bug counts (log10 bug density for each lowing data were collected: location on plant non-zero census date) were correlated with (leaf, stem, bud, etc.), plant species and re- density of reproductive plants for C. tex- productive condition, instar (nymphs), and anum in Plot 1 and Heterotheca latifolia copulatory activity (adults). BUCKL. in Plots 2 and 3. From March to June 1979, a modified Mark-recapture: Mark-release-recap- bug census was conducted weekly in Plot 1. ture studies were carried out at BFL from

1119 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

Fig. 1: Leptoglossus phyllopus adults; June 1976 through November 1977. Adult bugs to emerge. The effect of prominent clockwise from upper left: aggregated on L. phyllopus were individually marked by white dorsal markings on bugs in the field is Cirsium sp., March, Brazos Co., Texas (Photo: W. O. Ree Jr.); in copula on Gaura painting the pronotum with typewriter cor- unknown, but this technique does not sig- parviflora, July, Burleson Co., Texas (Photo: rection fluid (Liquid Paper™) and number- nificantly alter survivorship or copulatory A. Calixto); aggregated with marked bug ing with india ink (Fig. 1). A total of 1,070 activity of individuals under laboratory con- on Helianthus annuus, August, Travis Co., Texas; feeding on Solidago sp., October, individuals was marked during the course of ditions (Mitchell unpubl. data). Mark-re- Brazos Co., Texas (Photo: W. O. Ree Jr.); the study. Bugs were collected in the field by lease-recapture studies were designed to ex- feeding on G. parviflora, July, dropping net bags over aggregations on host amine dispersal, host plant shifts, and length Burleson Co., Texas (Photo: A. Calixto). plants, and were returned to the laboratory of residency, rather than population size. for marking. With rare exceptions, each Consequently, initial marking was a discon- batch was completed and released on the tinuous process, although study areas were date of capture. Bags of marked individuals checked daily or twice daily for recaptures. were attached to a branch or stem of the Thirteen subsites (host plant patches) were original host plant and opened, allowing delineated in the mark-release-recapture

1120 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at study. Size of subsites was variable, being a Colony maintenance: Leptoglossus phyl- function of host plant density in a given lopus colonies were reared at 26 ± 2°C, and area, and ranged from a single Callicarpa a photoperiod of 16:8 [L:D], and were fed americana L. bush to a 30 m2 stand of H. lat- whole green beans, Phaseolus vulgaris L. and ifolia. Distance between subsites was meas- shelled organically grown sunflower (H. an- ured from center to center of each patch. nuus) seed. Adults were housed in screen Analysis of dispersal therefore did not ac- and Plexiglas™ cages (25 x 25 x 25 cm) pro- count for movement within the larger sub- vided with wooden applicator sticks for sites, and total movement may have been oviposition. Nymphs were maintained in slightly underestimated. Each subsite was smaller cages constructed from 300 ml plas- characterized by one dominant host plant tic drinking cups (cup cages) and provided species. with a constant source of water through cot- ton dental wicks. The following data were collected for each marked individual: sex, subsite, time of Rearing experiments: Conducted in collection, host plant species, absence of both laboratory and field, these experiments legs, presence (and position) of macrotype examined the ability of fifth-instar L. phyllo- tachinid eggs on exoskeleton, degree of scle- pus to develop on a variety of hosts from dif- rotization (teneral vs. mature) and wing ferent plant families at different stages of de- wear condition (tattered vs. whole). Begin- velopment. Three variables were used to ning in August 1976, bug length was meas- measure host plant suitability: duration of the fifth instar, growth increment during ured with calipers to the nearest 0.5 mm. At this period, and survivorship. Experimental each subsequent recapture original observa- bugs were derived from field collected par- tions were rechecked, with the exception of ents, and were reared in the laboratory. length measurement. Further information Rearing colony cages were checked nightly, collected for resighted individuals included at growth chamber sunset. All newly molted location on host plant and activity (e.g., sit- fifth instars were collected at this time, iso- ting, walking, probing, sucking, copulating). lated in screen-covered cups overnight, and Data from the pilot study (June to Sep- supplied with a green bean for moisture. tember 1976) and overwintering periods Distribution of nymphs among treatments (October to February of both years) were was completed within 24 hours. Assignment analyzed separately from the major mark-re- to treatment was randomized within the set lease-recapture project in 1977. Marking of of host plants in the appropriate develop- the overwintering generation proved unsuc- mental condition at a given point in time. cessful; no bugs marked in late fall of either Each nymph was measured with calipers year were ever sighted again the following to the nearest 0.5 mm before placement on spring. Pilot project data were analyzed by the experimental host plant. Cages were hand to determine host plant and subsite checked daily at sunset, and newly molted shifts by individual bugs. adults were re-measured. Growth increment The mark-release-recapture project in was calculated as the difference between 1977 involved a total of 543 individuals and these two length measurements. Instar dura- three complete generations of L. phyllopus. tion was defined as days elapsed between the Bugs were separated into four generational fifth instar and adult molts. Survivorship, categories (overwintering, spring, summer, assessed only in laboratory experiments, was fall) on the basis of wing wear and scleroti- calculated as number of surviving nymphs zation. Data were processed using the per cage. LONGPOP program (WATT et al. 1977, In the laboratory, detached fruits or seed 1979). This program applies the capture-re- heads of a single plant species were offered capture methods of JOLLY (1965) for calcula- as a food source. Each experimental cup tion of survivorship, and also tabulates dis- cage contained five bugs, individually persal and other population parameters. Sex marked with enamel dots on the tibial folia- ratios were tested using χ2 goodness-of-fit tion. Laboratory experiments involved six (ZAR 1999). treatments, consisting of laboratory diet

1121 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

control and five host plants: Callicarpa amer- Field data from mark-recapture studies icana L. var. lactea (Lamiaceae), Campsis were also analyzed to substantiate the exper- radicans (L.) SEEM. (Bignoniaceae), Gaura imental results for fifth instar growth incre- parviflora DOUGL. (Onagraceae), and ment. Adult length of L. phyllopus marked Solanum eleagnifolium CAV. (Solanaceae). as teneral individuals was compared among Each treatment consisted of four cages for a various host plants. Adult length of males total of 20 nymphs per treatment. and females was analyzed separately for these data, because sex ratios were not In field experiments, bugs were caged equivalent across treatments. individually on live host plants (n = 25). Tulle sleeves, measuring 45 by 25 cm, were Measurement data from both field and lowered around plant stems or branches, laboratory experiments were analyzed by t and fastened at the base with fine wire. Veg- tests or by one way analyses of variance etative portions of the plant, flower buds, or (ANOVA) followed by Fisher’s LSD. Loga- one or more developing seed heads (de- rithmic (base-10) transformation was used pending on the growth form of the plant) prior to ANOVA if needed to normalize da- were contained within each sleeve cage. Af- ta or correct for unequal variance (MINITAB ter addition of a nymph, each sleeve was 2000). Count data were analyzed by non- wired together at the top, enclosing both parametric tests, including Friedman two- bug and plant. Plants were maintained in way ANOVA, Kruskal-Wallis (MINITAB the bud stage by clipping flowers within the 2000), and non-parametric rank analog of cage as they opened, or moving the entire Tukey’s test (CONOVER 1971). cage to a new plant. Field experiments con- Laboratory choice tests: Choice exper- centrated mainly on species in the family iments were conducted in small cup cages. . Treatments included Baccharis Naive second instars were used in all tests. neglecta BRITT. (), C. texanum Field observations identified this instar as (), texana (DC) TORR. the first critical period of host plant selec- & GRAY (Astereae), H. annuus (He- tion, because the previous instar is a non- liantheae), H. latifolia (Astereae), Solidago feeding stage, and oviposition site does not altissima L. (Astereae), and G. parviflora necessarily reflect host plant preference (Onagraceae). The last four species were (MITCHELL & MITCHELL 1986). Nymphs tested in all three developmental stages; used in experiments were derived from field- other hosts listed were tested only in repro- collected adults, but reared from the egg ductive condition. stage in the laboratory. Prior to placement Field experiments were conducted from in testing cages, bugs received only green September to November of 1977, and May bean (a water source), and were not exposed through July of 1978, according to the phe- to laboratory diet. nology of host plants studied. Separating the Since early instar nymphs are normally influence of climatic variation from genuine gregarious, bugs were tested in groups of five treatment effects was therefore critical. A per cage. Preference between plant species series of controls was established, in order to was tested by offering seed heads of H. lati- monitor the combined effects of tempera- folia (Asteraceae) and G. parviflora (Ona- ture and daylength and also laboratory stock graceae) as alternative food choices; prefer- quality. In the laboratory control treatment, ence for plant parts was tested using buds bugs received standard rearing diet (beans, and immature seed heads of C. texanum. For sunflower seeds and distilled water), and each comparison, 36 replicates were con- were maintained in the growth chamber at ducted, using a total of 180 second instars. 16:8 [L:D] photoperiod conditions. Addi- Each testing cage contained one cut stalk tionally, tulle cages supplied with laboratory (ca. 8 cm) of each plant alternative, insert- diet were set up on the roof of the Zoology ed in separate water vials. Fresh plant cut- building on the University of Texas campus. tings for each experiment were collected One set of these “roof controls“ was con- daily at the field station. Following addition ducted in fall of 1977, and one in summer of of nymphs, cages were observed at 4-h inter- 1978. vals during the 16-h growth chamber day,

1122 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at and again at sunrise of the following day. Stylet tracks of L. phyllopus were exam- Stylet insertion was considered to represent ined on the wild host C. texanum, and also definitive choice. A single observation, that on cultivated green cherry tomato (L. escu- which involved the greatest number of feed- lentum), and green bean (P. vulgaris). In ad- ing individuals, was selected from each ex- dition, feeding by the coreid E. galeator on perimental data set. A sign test (ZAR 1999) C. texanum was investigated, as these two was performed on the resulting values. species coexist on thistle in the spring. Histology: Plant tissue exposed to het- Voucher specimens: Specimens of the eropteran feeding was sectioned and exam- dipteran parasitoid Trichopoda pennipes F. are ined under a light microscope. Field collect- deposited in the California Academy of Sci- ed plant material was supplemented by ences, Department of Entomology. Coreid caging bugs on potted plants and cuttings in specimens are in the insect collection at the laboratory. Sites of observed stylet inser- Texas A&M University, Department of En- tion were marked on the plant surface with tomology. an indelible pen. Marked plant tissue was cut with a single edge razor blade, allowing a margin of ca. 2 mm. around the point of Results insertion, and fixed in either Carnoys solu- Field census. Although a diverse array tion (0.5 hr) or formalin-acetic acid-alcohol of plants from seven families served as L. (FAA) (48 hrs). Material fixed in Carnoys phyllopus breeding hosts at BFL (Table 1), was dehydrated through a series of ethyl al- plant species were not used in direct propor- cohols to xylene, while FAA treated tissue tion to frequency of occurrence. One species was dehydrated with tertiary butyl alcohol, in each study plot was always colonized to a following the method of JOHANSEN (1940). greater extent than predicted on the basis of Although both procedures were satisfactory, abundance alone, and others (e.g., grasses) that of Johansen proved more consistently were never used as breeding hosts at all. reliable. Dehydrated tissue was embedded in Temporal patterns of bug distribution on Paraplast™ and sectioned at 15 microns on various wild and cultivated host plants are a rotary microtome. Serial sections obtained in this manner were rehydrated and stained shown in Figure 2. Small vertical arrows in- with a 1 % solution of safranin in 50 % dicate the beginning of plant reproductive ethanol, and counterstained with fast green activity. On thistle, tomato, sunflower and (0.2 % in 50 % ethanol). Best results were goldenrod, bug density increased dramati- obtained using a staining schedule of 2 h in cally following the transition from vegeta- safranin solution, followed by 1 min in fast tive to reproductive growth. Colonization green and 2 min in each of two 95 % alco- was concurrent with fruiting in the latter hol baths. Table 1: Nymphal host plants of L. phyllopus, Travis County, Texas, 1977-1979. Asterisk After staining and subsequent dehydra- indicates observations at locations other than Brackenridge Field Station. tion of sections, coverslips were mounted Plant family Plant species Common name with Permount™. Bug salivary sheaths stain Asteraceae Achillea millefolium L. yarrow bright pink with safranin. Xylem stains red Baccharis neglecta BRITT. desert willow Cirsium texanum BUCKL. Texas thistle in contrast to the fast green absorbed by Gutierrezia texana (DC) TORR. & GRAY broomweed parenchyma and other non-lignified plant Helianthus annuus L. sunflower tissues. Both stylet tracks and damaged Heterotheca latifolia BUCKL. camphor weed Solidago altissima L. goldenrod plant tissue were easily observed using this Bignoniaceae Campsis radicans (L.) SEEM. trumpet creeper* staining technique. As the plane of section- Cucurbitaceae Cucurbita pepo L. squash ing only rarely coincided with the path of Lamiaceae Callicarpa americana L. French mulberry insertion, seriality of sections was critical in Malvaceae Hibiscus (=Abelmoschus) esculentus L. okra determining the termination point of the Onagraceae Gaura parviflora DOUGL. lizard-tail stylet tracks. Rare sections bearing com- Orobanchaceae Agalinis heterophylla (NUTT.) SMALL EX BRITT. prairie false foxglove plete, parallel-cut salivary sheaths were pho- Agalinis strictifolia (BENTH.) PENNELL stiffleaf false foxglove tographed at 100x with a Nikon Eclipse Scrophulariaceae Verbascum thapsus L. woolly mullein* E600 microscope equipped with an Olympus Solanaceae Lycopersicon esculentum MILLER tomato DP10 digital camera. Solanum eleagnifolium CAV. silver-leaf nightshade

1123 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

hatched prior to flowering only in 1979, and buds were used temporarily as a food re- source until developing seed heads became available. Preference among plant reproductive structures is best documented by the de- tailed data for C. texanum in spring of 1979 (Fig. 3). Weekly plant censuses and biweek- ly bug counts covered the period from ap- pearance of the first bud primordia in April until seed set in early June. For each census date, numerical tallies were converted to percentages, to facilitate comparisons be- tween plant organ availability and bug uti- lization. Percent bug utilization was calcu- lated as number of bugs on a given plant structure (e.g. bud, flower, etc.) divided by total bugs observed on reproductive organs Fig. 2: Temporal patterns of L. phyllopus three species. Individuals dispersed between of that host plant species. Plant percentage distribution on various cultivated and wild host plants with overlapping life cycles, as values were determined in a similar manner. host plants based on 1978 census counts, Preference was indicated when bug percent- Travis Co., Texas. one host reached senescence and the next species began fruiting. Okra and H. latifolia age use exceeded plant percentage availabil- become reproductive several months before ity. Total daily bug counts during the census bug invasion, but were never colonized dur- ranged from 10 to 122; plant parts counted ing the vegetative stage. For a given plant in each census ranged from 40 at first ap- species, bug density corresponded closely pearance of primordia to 302 at peak with abundance of plants in reproductive growth. condition. The number of reproductive Early in the season, bugs concentrated plants was significantly correlated with the on primordia (Fig. 3a), areas of the plant ex- log of bug density in the study area for both hibiting rapid growth. As true buds ap- C. texanum (r = 0.927, n = 15, P < 0.01) and peared (Fig. 3b), abrupt switching behavior H. latifolia (r = 0.692, n = 44, P < 0.01); oth- was evident, leading to disproportionately er plant species were not numerous enough lower use of the still common primordia. for statistical analysis. Identical switching behavior accompanied Leaffooted bugs were active from early the first appearance of developing seed spring to late fall, and overwintered as heads (Fig. 3d), which continued as the pre- ferred feeding site for the remainder of the adults. Spring emergence varied from mid- season. Flowers (Fig. 3c), occurring during February to late March, depending on the the same time period as immature seed harshness of the winter. For 1976-1978, heads, were rarely used. Ripening of seed good correspondence was apparent between heads in mid-June was not accompanied by bug emergence and the condition of C. tex- an increased proportion of bugs on mature anum, the first breeding host. In early heads (Fig. 3e). spring, while thistles remained in the rosette stage, an occasional leaffooted bug could be Similar census data for 1978 (not pre- observed probing on B. neglecta, a woody, sented) also indicated an overwhelming late fall host. However, large aggregations of preference for immature fruit and develop- emerging adults did not appear in spring un- ing seed heads, and concomitant avoidance til thistles commenced bolting and pro- of open flowers and mature fruits and seeds; duced the first central bud primordia. Copu- this was observed for C. texanum, C. ameri- lation began 1-3 weeks after emergence cana, H. latifolia, and S. altissima consistent- from overwintering, and production of ly and for H. annuus in early season (June). nymphs coincided with flowering and seed Mature seed heads of the last species were development of C. texanum. Nymphs preferred in July, and all seed heads were

1124 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at used in proportion to abundance at the end of the season in August. A comparison of L. phyllopus distribu- tion with that of a less common coreid, E. galeator, on the same host plant shows a clear difference in utilization of plant parts of C. texanum (Fig. 4). Significantly higher numbers of L. phyllopus are found on repro- ductive structures (buds, flowers, and seed heads) compared with leaves or stems (T = 8.22, df = 2, P = 0.016), whereas signifi- cantly more E. galeator are found on stems (includes branches, petioles, and peduncles) than on leaves or reproductive parts (T = 9.39, df = 2, P < 0.01). Mark-recapture. Analysis of 1977 cap- ture-recapture data provided information on dispersal, longevity, copulatory activity, sex ratio, predation, and parasitism of adults, in addition to the primary objective of docu- menting individual host plant shifts. For males, 116 individuals were recaptured out of 300 marked (38.7 %); in total, 299 recap- ture events resulted in an average recapture frequency of 2.58. Of 243 females marked, 86 (35.4 %) were recaptured in 153 recap- ture events, for an average recapture fre- quency of 1.78. Females showed a greater tendency to disperse, although distance trav- eled was equivalent between the sexes; 31 fe- male dispersants (36 %) moved an average of 42.31 m, whereas for the 33 male dispersants (28.5 %), the mean distance moved by dis- persing individuals was 44.01 m. The majority of individuals recaptured (71.5 % of males, 63.9 % of females) re- mained in a single patch of host plants. Most dispersants were recorded moving be- tween separate patches of the same host plant species. However, multiple host shifts Marked bugs were also observed in cop- were documented. Teneral adults marked on Fig. 3: Floral and fruiting stages of Cirsium C. texanum were subsequently recaptured ula. Among male L. phyllopus, eight bugs texanum, Travis Co. Texas, April-June 1979, while feeding on H. annuus (n = 4) and L. were observed to be mating on two separate showing frequency of occurrence of each occasions. One marked individual engaged structure and distribution of L. phyllopus; esculentum (7). One mature, fully sclerotized squares connected by solid lines indicate in four copulations on different days. For fe- adult marked on G. parviflora was recap- percent occurrence of plant structure; tured feeding on H. annuus. Mature individ- males, three individuals were seen mating circles connected by dotted lines indicate uals marked on H. annuus were observed twice, and two engaged in copulations at percent bug distribution on a structure. feeding on H. latifolia (2), L. esculentum (1), least three times during the course of the and Zea mays L. (3). Marked individuals study. Since subsites were checked only from H. latifolia fed upon G. parviflora (1), briefly each day (ca. 10 minutes per site), and H. annuus (4), while those from L. es- these observations represent only a small culentum dispersed to feed upon H. annuus fraction of total copulatory activity. Caged (8). The maximal number of host shifts ob- bugs in the laboratory mated nearly every served was four per marked adult. evening. No individuals marked as teneral

1125 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

adults were observed in copula on C. tex- what more frequently than legs with simple anum, but four of the 11 dispersants sighted tibiae, this trend may indicate only that again on sunflower and tomato mated at predators preferentially approach from the least once on the adult host plant. After rear, or that the expanded leaf-feet present a bugs reached adulthood, average residence larger target for attack. Larger sample sizes time on the nymphal host plant (C. tex- would be required to verify a predator escape anum) was 3.8 + 2.1 days for males (n = 18), function for the tibial expansions. and 3.5 + 2.1 days for females (n = 11). A major natural enemy of L. phyllopus at Field longevity (e.g., residence rate) was BFL is the tachinid fly Trichopoda pennipes F. slightly higher for males, and the longest in- This parasitoid species (actually a complex terval between initial marking and final re- of cryptic species or biotypes) is an impor- capture was 51 days, as opposed to 42 for fe- tant natural enemy of the economic pest N. males. The recapture duration decay plot viridula (JONES 1988), and leaffooted bugs over time indicated a Type II survivorship serve as an alternative host in many crops in pattern for both sexes. For males, the regres- the southeastern United States (TILLMAN sion line may be expressed as y = 4.55 - 2006). Other coreid genera attacked include 0.0878x, where x = days in residence and y Acanthocephala, Anasa, Archimerus, Chelin- = ln number of individuals (F = 1728.3; df = idea, Euthochtha, Leptoglossus, and Narnia 1, 49; P < 0.005). For females, y = 3.94 - (ARNAUD 1978). At BFL, T. pennipes has 0.0985x (F = 803.1; df = 1,40; P < 0.005). been reared from Acanthocephala declivis SAY, A. femorata (F.), A. terminalis (DAL- Only the sex ratio of the overwintering LAS), vittiger UHLER, and Lep- Fig. 4: Distribution of Leptoglossus generation on C. texanum was significantly phyllopus (A) and Euthochtha galeator (B) toglossus oppositus (SAY) as well as L. phyllo- on leaves, stems, and reproductive parts of biased toward males (s.r. = 0.602, n = 103, pus (Mitchell unpublished). the host plant Cirsium texanum, Travis Co., χ2 = 4.28, df = 1, P < 0.05). Census data for Texas, April-May, 1979. Median value, first 1978 corroborated this result (s.r. = 0.597, n Intensity of parasitism was estimated as and third quartiles, and upper and lower = 613, χ2 = 23.1, df = 1, P < 0.01). For five the proportion of adult bugs bearing a ranges indicated by box and whisker plot. weeks following the initial colonization of macrotype egg (or eggs) on the exoskeleton. the first spring host, males predominated; af- Mark-recapture data indicated that high ter this time and throughout subsequent levels of parasitism were attained only in the generations, the ratio of males to females overwintering and first spring generations, did not differ significantly from 1:1. with 46 % and 27 % egg-bearing individu- als, respectively. Leptoglossus phyllopus is the The large hind leaf-feet of bugs in the first hemipteran species to reach appreciably coreine tribe Anisoscelini detach easily, and high densities in the spring, whereas alter- may operate as a predator escape mecha- nate hosts (e.g., A. femorata, Anasa tristis nism. The relative extent of predation in (DE GEER), various pentatomid species) be- different populations may be estimated by come common on garden crops somewhat frequency of leg loss, in much the same way later in the season. According to both mark- that tail break frequency is used to compare recapture and census data, <10 % of L. phyl- predation rates among lizard populations lopus in summer and fall populations bear ta- (e.g., PIANKA 1970). Leg loss data for indi- chinid eggs. viduals collected during the capture-recap- ture study showed that only the overwinter- Oviposition site on the bug exoskeleton ing generation on C. texanum exhibited a varies, but most eggs are placed on the head high rate of leg loss: 65 % of individuals re- of L. phyllopus. Of 142 eggs examined, dis- mained intact (n = 100). In all subsequent tribution on the body was as follows: head, generations, the percentage of undamaged 72.5 %; pronotum, 13.4 %; elsewhere on individuals was considerably higher, ranging thorax, 9.9 %; abdominal sternites, 2.1 %; from 87.0-90.3 % (n ≥ 93). Summation of abdominal tergites, 0.0 %; tibial foliation, hind, mid, and foreleg loss frequency over 0.7 %; wing, 1.4 %. The presence of a ta- the entire season yields 55 individuals lack- chinid egg on the exoskeleton does not ap- ing at least one hind leg, 41 lacking a mid- pear to deter an ovipositing T. pennipes. Oc- dle leg and 13 with a detached foreleg. Al- currence of supernumerary T. pennipes eggs, though the foliated hind legs are lost some- although infrequent in females, was com-

1126 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

Table 2: Development of fifth-instar L. phyllopus caged on various reproductive host plants in the field, Austin, Texas, Sept.-Nov. 1977 and May-July 1978. Plant Species Family Season n Growth incrementa (mm) n Stadium durationa (days) Baccharis neglecta Asteraceae 1977 10 4.15 ± 0.63a 10 15.10 ± 5.92a Gutierrezia texana Asteraceae 1977 13 4.00 ± 0.54a 13 14.69 ± 6.51a Heterotheca latifolia Asteraceae 1977 10 3.85 ± 1.16a 12 13.67 ± 7.57a Solidago altissima Asteraceae 1977 11 3.95 ± 0.65a 11 15.55 ± 6.39a controlb ——- 1977 6 4.33 ± 0.41a 10 11.20 ± 3.71a Cirsium texanum Asteraceae 1978 6 3.17 ± 1.13A 7 13.00 ± 3.61A Gaura parviflora Onagraceae 1978 10 3.45 ± 0.72A 10 13.30 ± 4.24A Helianthus annuus Asteraceae 1978 12 4.25 ± 0.75B 12 12.17 ± 2.85AB controlb ——- 1978 14 4.25 ± 0.85B 14 9.79 ± 2.04B amean ± standard deviation; within a season, means followed by the same letter do not differ significantly (ANOVA and Fisher’s LSD test, P > 0.05); 1977: growth, F = 0.51; df = 4, 49; P = 0.728; instar duration, F = 1.09; df = 4, 55; P = 0.373; 1978: growth, F = 4.00; df = 3,41; P = 0.014; in- star duration, F = 3.08; df = 3, 42; P = 0.039. bcontrol treatments were reared outdoors but received laboratory rearing diet

Table 3: Body length (mm) of teneral L. phyllopus collected from various nymphal host plants, Austin, Texas 1976-1977. Host plant Family Seasona n Malesb n Femalesb Baccharis neglecta Asteraceae F 14 15.86 ± 0.95a — ——- Gutierrezia texana Asteraceae F — ——- 11 16.77 ± 0.52a Heterotheca latifolia Asteraceae F 31 15.53 ± 0.87a 42 16.40 ± 0.76a Solidago altissima Asteraceae F 28 15.75 ± 0.65a 15 16.83 ± 0.67a Cirsium texanum Asteraceae S 58 15.55 ± 1.09A 46 17.23 ± 1.09A Helianthus annuus Asteraceae S 27 16.24 ± 1.20B 27 17.87 ± 1.24B Lycopersicon esculentum Solanaceae S 13 16.81 ± 1.07B 17 18.38 ± 1.15B aF = fall hosts; S = spring/summer hosts; plants with collection sample size <5 not included. bMean plus standard deviation. Within a season, values followed by the same letter do not differ significantly (ANOVA and Fisher’s LSD test; P > 0.05); fall: males, F = 0.97; df = 2, 72; P = 0.386; females, F = 2.62; df = 2, 67; P = 0.08; spring/summer: males, F = 8.31; df = 2, 97; P < 0.001; fe- males, F = 7.04; df = 2, 87; P = 0.001.

mon among males. Of 54 parasitized females outside surface of the net bags. Unwary ex- examined, only 5.6 % had more than a sin- perimental nymphs traversing the inside gle egg, whereas 37.5 % of parasitized males mesh surface were captured through the net- (n = 122) bore 2-8 eggs attached to the ting by these predators, and sucked dry. body. Percent parasitism in general is also Dead bugs were dismantled rapidly by scav- substantially higher in males. Total para- enging ants, so that condition of corpses sitism in the capture-recapture study was could not be used to distinguish death by 15.0 % for males (n = 300), and 8.6 % for fe- predation from actual treatment effects. males (n = 243). Despite the high incidence Therefore, survivorship was only analyzed in of attempted superparasitism, it should be the laboratory trials. noted that only one T. pennipes larva ulti- mately emerged from each L. phyllopus Survivorship on vegetative tissue of G. caged in the laboratory. However, four lar- parviflora, H. annuus, H. latifolia, and S. al- vae emerged from a single individual of A. tissima was zero. Individuals caged on buds femorata bearing 21 eggs. of these species fared marginally better, with overall survivorship of 4, 8, 8, and 20 %, re- Rearing experiments. Originally, only spectively, but insufficient data were gener- field rearing experiments were planned. ated for statistical comparisons, either However, both tulle cages and the enclosed among plant species or between plant devel- bugs were subject to severe depredations opmental stages. Bugs survived in adequate from biotic and abiotic factors. Plants bear- numbers for analysis only on reproductive ing cages collapsed during storms, drowning stage treatments in field (40-65 %) and lab- bugs in puddles, while high winds caused oratory (55-70 %) trials. tulle cages to catch on thorns and rip open. Although the fabric appeared to provide ad- Field cage experiments in 1977 showed equate protection from chewing predators, that fifth instars could develop equally well salticid spiders and reduviids stalked the on the various autumn host plants, all of

1127 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

Table 4: Development of fifth-instar L. phyllopus caged on detached fruits and seed heads of various host plants in the laboratory, Austin, Texas, August 1978. Plant species Family n Growth increment n Instar duration n No. of (mm)a (days) a surviving nymphsa Callicarpa americana Lamiaceae 13 3.00 ± 0.68b 13 15.00 ± 3.98b 4 3.25 ± 1.71a Campsis radicans Bignoniaceae 14 3.46 ± 1.01b 14 22.57 ± 5.64a 4 3.50 ± 1.29a Gaura parviflora Onagraceae 19 3.24 ± 0.87b 19 10.84 ± 2.16c 4 4.75 ± 0.50a Solanum eleagnifolium Solanaceae 11 3.36 ± 0.67b 11 12.82 ± 3.71bc 4 2.75 ± 2.06a control ——- 13 4.73 ± 0.67a 13 8.9 ± 0.76d 4 3.00 ± 1.41a amean ± standard deviation; entries in a column followed by the same letter do not differ significantly (ANOVA and Fisher’s LSD test or Kruskal- Wallis test; P > 0.05); Growth: F = 9.38; df = 4, 69; P < 0.001; instar duration: F = 27.26; df = 3, 56; P < 0.001; survivorship: H = 5.03, df = 4, P = 0.28) bcontrol treatment received laboratory rearing diet

which were in the family Asteraceae (Table layed significantly when pods of trumpet 2). Neither growth increment nor instar du- creeper were provided as food, although the ration differed among the four plant species growth achieved and the numbers of surviv- tested. However, some differences were not- ing bugs were similar to those on other ed among spring/summer host plants in plants tested. 1978 (Table 2). Bugs on thistle (Asteraceae) Laboratory choice tests. Experiments and lizard-tail (Onagraceae) did not differ in in which seed heads of two host plant developmental parameters, but both grew species were presented in a 1:1 ratio demon- significantly less than bugs provided labora- strated no significant differences in tory diet (sunflower seeds) or those caged on nymphal preference (sign test, n = 34, P > cultivated sunflowers (Asteraceae). A simi- 0.05). Second instars preferred H. latifolia in lar trend was found for stadium duration, 20 trials, G. parviflora in 14 trials, and ex- which was longer on wild hosts than on sun- hibited no preference in 2 trials. In contrast, flower seed. results of laboratory tests between buds and Mark-recapture data (see above) indi- immature seed heads of H. latifolia showed cated that dispersal to the adult host plant an overwhelming and highly significant was delayed until after the teneral stage; preference for seed heads (sign test, n = 30, therefore, collection site of incompletely P < 0.001), which were selected by second sclerotized adults is a reliable indicator of instars in 28 out of the 30 trials in which the nymphal host plant. Results of the field feeding occurred. rearing experiments were substantiated Histology. Stems, peduncles, and pedi- when length of teneral adults from different cels of tomato, thistle, and camphorweed, host plants was compared (Table 3). No dif- and immature reproductive structures of ferences were found among either males or beans and tomatoes, could be successfully females develaoping on three different preserved and sectioned; neither buds nor species of Asteraceae in autumn. Spring/ seedheads of Asteraceae were amenable to summer hosts again differed in food quality, histological technique. Typical tracks, or however; both males and females develop- stylet sheaths, of E. galeator and L. phyllopus ing on cultivated plants (tomato and sun- are shown in Figure 5. Irrespective of plant flower) were significantly larger than those part, both species produced sheath deposits maturing on the wild host (thistle). externally in addition to lining the full In laboratory rearing experiments (Table pathway of the stylets with gelling saliva. 4), neither survivorship nor growth incre- MILES (1958) showed that maxillary and ment differed across host plants from four mandibular stylets of Heteroptera move in families, although bugs on all wild hosts concert, so that (unlike some Auchenor- grew significantly less than those on the rhyncha) the termination of the stylet control diet of sunflower seed and green sheath in a feeding probe is indicative of the beans. Duration of the fifth stadium was ex- target tissue. Adults of E. galeator feeding on tremely variable, significantly extended on stem tissue (including peduncles and all wild hosts compared with the control, pedicels) typically produced branching and varying among and within host plant sheaths which caused massive destruction to treatments as well. The adult molt was de- the entire region of vascular tissue. Of 39 E.

1128 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

Fig. 5: Stylet tracks of coreids feeding on various hosts, photographed at 100x magnification, with horizontal bar indicating 100 µm; clockwise from upper left: Euthochtha galeator adult on peduncle of Cirsium texanum; Leptoglossus phyllopus adult on peduncle of C. texanum (partial track); L. phyllopus third instar on stem of Lycopersicon esculentum; L. phyllopus third instar on L. esculentum green fruit; L. phyllopus fifth instar on green pod of Phaseolus vulgaris; L. phyllopus adult on midvein of C. texanum leaflet.

1129 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

galeator stylet sheaths examined, 22 were peared to cross taxonomic lines between branched. Not all tracks could be followed plant species readily. The long adult life with certainty because of damage or loss of span of L. phyllopus (up to 51 days adult res- serial sections; however, 19 of 24 that were idence in the mark-recapture study) may ne- confirmed to reach the vascular tissue were cessitate dispersal among plants with over- branched. Although L. phyllopus adults did lapping life cycles (i.e., from a senescing occasionally insert their stylets into non-re- host plant to an alternate host in suitable productive tissue such as leaves, pedicels, condition); the same is true for teneral and peduncles, the target tissue in this case adults leaving the nymphal host. However, appeared to be primarily xylem, and the after the initial dispersal, the majority of re- tracks rarely branched (Fig. 5). Branched captured individuals remained in a single tracks occurred in fruit and bud tissue and patch of plants, or moved among patches of developing seeds (Fig. 5), but never to the a single host species. Therefore, the most extent observed with E. galeator. For L. phyl- appropriate description of L. phyllopus feed- lopus, 38 sheaths were located. In stems, on- ing behavior is sequential (rather than con- ly 1 sheath of 16 that reached vascular tissue current) polyphagy. Diet mixing did occur, was branched; 8 of these terminated in but it was infrequently observed. This ac- xylem and the remainder could not be de- cords with the conclusion of BERNAYS & finitively traced. In fruit and pods, most MINKENBERG (1997), who found that under stylet sheaths penetrated to developing experimental conditions, mixtures of avail- seed, although xylem was also targeted (Fig. able host plants offered no significant ad- 5). Penetration to pith was observed infre- vantage over single species for two quently in both species. polyphagous heteropterans, the pentatomid Thyanta custator (F.) and the mirid Lygus hes- Discussion perus KNIGHT. These authors argue that for Heteroptera, unlike Orthoptera, the advan- Leptoglossus phyllopus may be character- tage of a generalist feeding strategy is versa- ized as genuinely polyphagous, in the sense tility and greater resource availability rather that individuals are capable of using a vari- than nutritional enhancement or dilution of ety of host plant species. Not only is the allelochemicals. overall set of host plants extensive across In rearing experiments, fifth instars from the geographic range (MITCHELL 2000), but the same cohort developed equally well on bugs are local generalists as well. Fifteen different species of Asteraceae. Even across species from seven families were used as plant families (Onagraceae, Lamiaceae, breeding hosts at Brackenridge Field Sta- Bignoniaceae, Solanaceae), nymphal sur- tion. Asteraceae predominated among host vivorship and growth were equivalent, al- plants in the study, but this family is the sec- though stadium duration was significantly ond largest at the field site so the apparent extended on a few host species. The most preference may simply reflect availability. extreme differences in fifth instar develop- Host-switching, or dispersal to an alter- ment occurred not among plant families, nate host, may occur during three stages of but between cultivated and wild hosts, sug- bug development: nymph, teneral adult, or gesting that nutritional and host quality mature adult. Nymphal dispersal in the field considerations, rather than plant could not be examined through mark-re- (and associated plant secondary chemistry), lease studies. However, second instars (the ultimately determine host plant selection. stage that disperses from the egg mass to the The importance of nutrient availability is breeding host) showed no preference be- underscored by the failure of caged insects tween Onagraceae and Asteraceae in labo- to survive on vegetative hosts, and the sig- ratory choice tests. In field studies, marked nificantly lowered survivorship on buds teneral individuals dispersed from the compared with immature seed heads and nymphal breeding host to an adult host fruits. Preference experiments and distribu- plant belonging to a different family (e.g., tion of bugs in the field corroborated the Asteraceae to Solanaceae). Some post-ten- rearing experiments. Immature seed heads eral adults also moved among hosts and ap- and fruits were used far out of proportion to

1130 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at their availability; other plant parts were un- ized as “macerate and flush“ (or “lacerate and derused or avoided entirely. flush“ by earlier authors, before the role of salivary enzymes was fully appreciated) The close correspondence of plant re- (MILES & TAYLO R 1994; SHACKEL et al. production and L. phyllopus colonization in- 2005; ZENG & COHEN 2001). Pentatomo- dicates that patterns of host plant utilization morphan bugs produce stylet sheaths when are to a great extent determined by plant feeding on stem tissue, but exudation of phenology. Bugs disperse between host sheath material does not accompany the full plants with overlapping life cycles, as one length insertion of the stylets into seeds species reaches senescence and the next species begins fruiting. Generations are con- (MILES 1959). Thus, these insects were orig- tinuous throughout the season, with repro- inally described as either “lacerate and flush“ ductive diapause occurring only during the feeders (on seeds) or “stylet sheath“ feeders winter months. Thus, for L. phyllopus, de- (on growing plant tissues) (MILES 1972). pendence on relatively ephemeral plant Sheaths produced by milkweed bugs fruiting structures necessitates periodic dis- (MILES 1959) and chinch bugs (PAINTER persal. The risks entailed in such host 1928) feeding on stems are extensively switching are reduced as the range of ac- branched at the level of the phloem, resem- ceptable plant species increases. Polyphagy bling the feeding by E. galeator in this study. provides versatility and greater resource Squash bugs deposit gelling saliva in all stem availability (BERNAYS & MINKENBERG 1997) tissues, including collenchyma, parenchy- but is tied to specialization on nutrient-rich ma, phloem, and xylem (NEAL 1993). Wilt- reproductive tissue. ing has been attributed to extensive block- Clearly, L. phyllopus are specialists on age of xylem by saliva of A. tristis on squash plant structures, although not on plant and the pentatomid Palomena angulosa species or families. Analogous feeding pref- MOTSCHULSKY on potato (HORI et al. 1984, erences have been documented for two het- NEAL 1993). Palomena angulosa fed preferen- eropteran cotton pests. Bolls 7-27 days old tially on leaves and petioles and inserted the are damaged by Euschistus servus (SAY) to a stylets mainly to the phloem (HORI et al. significantly greater extent in the field than 1984), but nymphs also fed on buds, de- are other boll ages (WILLRICH SIEBERT et al. stroying the tapetum and consuming pollen. 2005) whereas cotton buds (squares) are In contrast, L. phyllopus feeding on stems used preferentially by adults and older and peduncles most frequently penetrate di- nymphs of the highly polyphagous L. hespe- rectly to xylem, with no branching and min- rus. In the case of these lygus bugs, the tar- imal destruction of vascular tissue. This be- get tissue is the anther sac; younger nymphs, havior, coupled with the failure of nymphs whose stylets cannot reach the anther sacs to develop on vegetative tissue, strongly of larger squares, are not economically dam- suggests that stem “feeding“ in this species is aging (ZINK & ROSENHEIM 2005). Lygus line- essentially drinking from xylem. Xylem olaris also primarily damages developing an- drinking by heteropterans was first noted by thers and staminal columns in cotton floral PAINTER (1928) in chinch bugs (Blissidae). buds (WILLIAMS III & TUGWELL 2000). These insects produce branching stylet tracks that pass intracellularly through leaf Selection by L. phyllopus of feeding sites tissue of sorghum to the phloem, and often at the plant organ and tissue level differs one branch terminates in xylem; PAINTER from feeding behavior of lygus bugs and that (1928) suggested that the xylem may pro- of most other pentatomomorphan species vide “an extra source of water...especially studied. Mirid feeding creates lesions con- during dry periods.“ WHEELER (2001) sum- sisting of areas of plant tissue from which cell marized observations of mirid stylet tracks in contents have been removed, sometimes dis- vascular tissue, and speculated that these in- tant from the termination point of the stylets sects may use xylem similarly. (MILES 1987). Mirids and other Cimicomor- pha do not produce a continuous stylet Actual feeding (i.e., nutrient ingestion) sheath; their extra-oral digestion via inject- in L. phyllopus occurs on reproductive tissue. ed salivary enzymes (pectinase) is character- In immature pods and fruit, a complete

1131 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

stylet sheath is produced through the wall to Acknowledgments the developing seed. This is similar to feed- I thank L.E. Gilbert for guidance and ing by other Leptoglossus species. Nymphs of John Crutchfield for logistical support in the (SAY) feed on nucellar field. J.C. Schaffner originally suggested tissue of pine ovules in conelets (DEBARR & Leptoglossus as a genus for study, and has en- KORMANIK 1975); Leptoglossus occidentalis couraged my heteropteran studies from the HEIDEMANN destroys the nucellus and disor- ganizes the female gametophyte of immature beginning. I am grateful to Bruce Tabashnik pine seeds (KRUGMAN & KOERBER 1969). and Ward Watt for the use of their LONG- Feeding by the latter species on developing POP program. I thank J.C. Schaffner for all and mature seeds of Douglas-fir causes de- coreid determinations, P.H. Arnaud, Jr. for pletion of protein and lipid reserves from determinations of tachinids, William O. storage parenchyma and reduces seedling Ree Jr. for the photographs of Leptoglossus emergence (BATES et al. 2000, 2001). Inter- on Solidago and Cirsium, and Alejandro Cal- estingly, examination of damaged seed and ixto for the photographs of Leptoglossus on insect saliva suggests that neither lacerate- Gaura. All field research was done at the and-flush nor osmotic pump mechanisms Brackenridge Field Station of The Universi- are involved, and a mirid-like pectinase ty of Texas, Austin. Financial support was mechanism is suggested (BATES et al. 2000). provided by a Sigma Xi Grant-In-Aid-of- Three species of Australian stem- or shoot- Research and a University of Texas Gradu- feeding coreids, Mictis profana (F.), Amblype- ate Fellowship. ta sp., and Amorbus sp., have been shown to produce salivary sucrases to osmotically Zusammenfassung draw parenchyma cell contents into inter- cellular spaces (“osmotic pump“). These in- Die polyphage Art Leptoglossus phyllopus sects typically made short, unbranched, (L.) wurde hinsichtlich ihrer Nahrungs- stylet sheaths (MILES 1987; MILES & TAYLOR pflanzenpräferenz, (Wirtspflanzen)Gewebe- 1994; TAYLOR & MILES 1994), unlike the spezifität, ihres saisonalen Wirtspflanzen- branched tracks of stem feeders described wechsels und ihrer Lebensgeschichte unter- previously, and they induce lesion formation sucht. Fang-Wiederfang, Zensus und Zucht- and wilting of shoots beyond the point of experimente zeigten, dass sich diese Art feeding. It appears that coreid feeding may polyphag ernährt, in dem Sinne, dass einzel- not fall neatly into a single category, but ne Tiere an Pflanzen unterschiedlicher Fa- could include osmotic pump, lacerate-and- milien saugen. Entwicklungsparameter wie flush, and macerate-and flush strategies in Körpergröße der Entwicklungsstadien und different species. Understanding the mode Überlebensrate unterscheiden sich nicht of feeding is important, because the extent zwischen Wirtspflanzen verschiedener Fa- to which tissue is damaged by feeding, and milien; signifikante Unterschiede wurden the secondary chemicals released by such jedoch zwischen unterschiedlichen Qualitä- damage, could in turn affect diet breadth. ten der Nahrungspflanzen (z.B. wild vs. kul- For example, cyanogenesis in cassava roots tiviert) festgestellt. Die Dauer der Entwick- is caused by cell wall rupture by the stylets of lungsstadien unterscheidet sich bei ver- a polyphagous cydnid, thereby deterring schiedenen Nahrungspflanzen im Experi- feeding (RIIS et al. 2003). The influence of ment. Eine Spezialisierung an bestimmte re- plant defensive chemicals on feeding behav- produktive Teile der Wirtspflanzen, gekop- ior of Heteroptera and other piercing-suck- pelt mit sequentieller Polyphagie und der ing insects deserves further study. Ausbreitung an bestimmte Wirtspflanzen über die Saison, erlaubt die Ausbildung mehrerer Generationen pro Jahr. Unter- schiedliche Möglichkeiten der Nahrungs- aufnahme und die Bevorzugung bestimmter Wirtspflanzengewebe bei Coreiden werden diskutiert.

1132 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

References Importance. CRC Press, Boca Raton, FL: xviii + 1-828. ARNAUD P.H. (1978): A host-parasite catalog of HORI K., KONDŌ Y. & K. KURAMOCHI (1984): Feeding North American Tachinidae (Diptera). — U.S. site of Palomena angulosa MOTSCHULSKY Dep. Agric. Misc. Publ. 1319: 1-860. (Hemiptera: Pentatomidae) on potato plants BATES S.L., BORDEN J.H., SAVOIE A., BLATT S.E., LAIT and injury caused by the feeding. — Appl. En- C.G., KERMODE A.R. & R.G. BENNETT (2000): Im- tomol. Zool. 19: 476-482. pact of feeding by Leptoglossus occidentalis JOHANSEN D.A. (1940): Plant Microtechnique. — (Hemiptera: Coreidae) on the major storage McGraw-Hill Book Co., New York, NY: 1-523. reserves of mature Douglas-fir (Pinaceae) seeds. — Can. Entomol. 132: 91-102. JOLLY G.M. (1965): Explicit estimates from capture- recapture data with both death and immigra- BATES S.L., LAIT C.G., BORDEN J.H. & A.R. KERMODE tion – stochastic model. — Biometrika 52: (2001): Effect of feeding by the western 225-247. conifer seed bug, Leptoglossus occidentalis, on the major storage reserves of developing JONES W.A. (1988): World review of the parasitoids seeds and on seedling vigor of Douglas-fir. — of the southern green stink bug, Nezara Tree Physiology 21: 481-487. viridula (L.) (Heteroptera: Pentatomidae). — Ann. Entomol. Soc. Amer. 81: 262-273. BERNAYS E.A. & R.F. CHAPMAN (1993): Host-plant Se- lection by Phytophagous Insects. — Chapman JUDD W.S., CAMPBELL C.S., KELLOGG E.A., STEVENS P.F. & & Hall, New York, NY: xiii + 1-312. M.J. DONOGHUE (2002): Plant Systematics: A Phylogenetic Approach. 2nd ed. —Sinauer BERNAYS E.A. & O.P.J.M. MINKENBERG (1997): Insect Assoc., Inc. Sunderland, MA: xvi + 1-576. herbivores: Different reasons for being a gen- eralist. — Ecology 78: 1157-1169. KRUGMAN S.L. & T.W. KOERBER (1969): Effect of cone feeding by Leptoglossus occidentalis on Pon- BUSS L.J., HALBERT S.E. & S.E. JOHNSON (2005): Lep- derosa pine seed development. — Forest Sci- toglossus zonatus – a new leaffooted bug in ence 15: 104-111. Florida. — Fla. Dept. Agric. & Consumer Serv. Div. Plant Industry Pest Alert: 1-3. KUMAR R. (1966): Studies on the biology, immature http://www.doacs.state.fl.us/pi/enpp/ento/l.zo stages and relative growth of some Aus- natus.html tralian bugs of the superfamily (Hemiptera: Heteroptera). — Austr. J. Zool. COBBEN R.H. (1978): Evolutionary trends in Het- 14: 895-991. eroptera. Part II. Mouth-part structures and feeding strategies. — Meded. Land- MILES P.W. (1958): The stylet movements of a bouwhogeschool Wageningen 78 (5): 1-407. plant-sucking bug, Oncopeltus fasciatus (DALL.) (Heteroptera: Lygaiedae). — Proc. R. COBBEN R.H. (1979): On the original feeding habits Entomol. Soc. London 33: 15-20. of the Hemiptera (Insecta): A reply to Merrill Sweet. — Ann. Entomol. Soc. Amer. 72: 711- MILES P.W. (1959): The salivary secretions of a 715. plant-sucking bug, Oncopeltus fasciatus (DALL.) (Heteroptera: Lygaeidae). — I. The CONOVER W.J. (1971): Practical Non-parametric Sta- types of feeding and their roles during feed- tistics. — John Wiley & Sons, Inc., New York, ing. — J. Ins. Physiol. 3: 243-255. NY: 1-462. MILES P.W. (1972): The saliva of Hemiptera. — Adv. CORRELL D.S. & M.C. JOHNSTON (1970): Manual of the Ins. Physiol. 9: 183-255. Vascular Plants of Texas. — Texas Research Foundation, Renner, TX: 1-1881. MILES P.W. (1987): Plant-sucking bugs can remove the contents of cells without mechanical DEBARR G.L. & P.P. KORMANIK (1975): Anatomical ba- damage. — Experientia 43: 937-939. sis for conelet abortion on Pinus echinata fol- lowing feeding by Leptoglossus corculus MILES P.W. & G.S. TAYLOR (1994): ‘Osmotic pump’ (Hemiptera: Coreidae). — Can. Entomol. 107: feeding by coreids. — Entomol. exp. Appl. 73: 81-86. 163-173.

EUBANKS M.D., STYRSKY J.D. & R.F. DENNO (2003): The MINITAB (2000): Minitab User’s Guide 2: Data evolution of omnivory in heteropteran in- Analysis and Quality Tools, Release 13 for sects. — Ecology 84: 2549-2556. Windows. — Minitab, Inc., State College, PA.

FOX L.R. & P.A. MORROW (1981): Specialization: MITCHELL P.L. (2000): Leaf-footed bugs (Coreidae) Species property or local phenomenon? — — In: SCHAEFER C.W. & A.R. PANIZZI (Eds), Het- Science 211: 887-893. eroptera of Economic Importance. CRC Press, Boca Raton, FL: xviii + 1-828. HENNE D.C., JOHNSON S.J. & W.J. BOURGEOIS (2003): Pest status of leaf-footed bugs (Heteroptera: MITCHELL P.L. & F.L. MITCHELL (1986): Parasitism and Coreidae) on citrus in Louisiana. — Proc. Fla. predation of leaffooted bug (Hemiptera: Het- State Hort. Soc. 116: 240-241. eroptera: Coreidae) eggs. — Ann. Entomol. Soc. Amer. 79: 854-860. HORI K. (2000): Possible causes of disease symp- toms resulting from the feeding of phy- NEAL J.J. (1993): Xylem transport interruption by tophagous Heteroptera. — In: SCHAEFER C.W. & Anasa tristis feeding causes Cucurbita pepo A.R. PANIZZI (Eds), Heteroptera of Economic to wilt. — Entomol. exp. Appl. 69: 195-200.

1133 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

PAINTER R.H. (1928): Notes on the injury to plant TONKYN D.W.& R.F. WHITCOMB (1987): Feeding cells by chinch bug feeding. — Ann. Entomol. strategies and the guild concept among vas- Soc. Amer. 21: 232-242. cular feeding insects and microorganisms. — In: HARRIS K.F. (Ed.), Current Topics in Vector PIANKA E.R. (1970): Comparative autecology of the lizard Cnemidophorus tigris in different parts Research. Vol. 4. Springer-Verlag, New York, of its geographic range. — Ecology 51: 703- NY: 179-199.

720. WATT W.B, CHEW F.S., SNYDER R.G., WATT A.G. & D.E.

PORT G.R. (1978): Studies on the feeding biology of ROTHSCHILD (1977): Population structure of Auchenorrhyncha: (Homoptera). Ph.D. thesis, pierid butterflies I. Numbers and movements University of London: 1-239. of some montane Colias species. — Oecologia 27: 1-22. RABITSCH W. & E. HEISS (2005): Leptoglossus occi- dentalis HEIDEMANN, 1910, eine amerikanische WATT W.B., HAN D. & B.E. TABASHNIK (1979): Popula- Adventivart auch in Österreich aufgefunden tion structure of pierid butterflies II. A “na- (Heteroptera: Coreidae). — Ber. nat.-med. tive“ population of Colias philodice eriphyle Verein Innsbruck 92: 131-135. in Colorado. — Oecologia 44: 44-52.

RADFORD A.E., AHLES H.E. & C.R. BELL (1968): Manu- WHEELER A.G. Jr. (2001): Biology of the Plant Bugs al of the Vascular Flora of the Carolinas. — (Hemiptera: Miridae) Pests, Predators, Oppor- Univ. North Carolina Press, Chapel Hill, NC: lxi tunists. — Cornell Univ. Press, Ithaca, NY: xv + + 1-1183. 1-507.

RIDGE-O’CONNOR G.E. (2001): Distribution of the WILLIAMS III L. & N.P. TUGWELL (2000): Histological , Leptoglossus occi- description of tarnished plant bug (Het- dentalis HEIDEMANN (Heteroptera: Coreidae) in eroptera: Miridae) feeding on small cotton Connecticut and parasitism by a tachinid fly, floral buds. — J. Entomol. Sci. 35: 187-195. Trichopoda pennipes (F.) Diptera: Tachinidae). — Proc. Entomol. Soc. Wash. 103: 364-366. WILLRICH SIEBERT M., LEONARD B.R., GABLE R.H. & L.R. LAMOTTE (2005): Cotton boll age influences RIIS L., BELLOTTI A.C., BONIERBALE M. & G.M. O’BRIEN feeding preference by brown stink bug (Het- (2003): Cyanogenic potential in cassava and eroptera: Pentatomidae). — J. Econ. Entomol. its influence on a generalist insect herbivore 98: 82-87. Cyrtomenus bergi (Hemiptera: Cyndidae). — J. Econ. Entomol. 96: 1905-1914. ZAR J.H. (1999): Biostatistical Analysis, 4th ed. — Pearson Education (Singapore) Pte. Ltd., Del- SCHAEFER C.W. & P.L. MITCHELL (1983): Food plants of the Coreoidea (Hemiptera: Heteroptera). — hi, India: xii + 1-663.

Ann. Entomol. Soc. Amer. 76: 591-615. ZENG F. & A.C. COHEN (2001): Induction of elastase

SCHAEFER C.W. & A.R. PANIZZI (Eds) (2000): Het- in a zoophytophagous heteropteran, Lygus eroptera of Economic Importance. — CRC hesperus (Hemiptera: Miridae). — Ann Ento- Press, Boca Raton, FL: xviii + 1-828. mol. Soc. Amer. 94: 146-151.

SCHUH R.T. & J.A. SLATER (1995): True Bugs of the ZINK A.G. & J.A. ROSENHEIM (2005): Stage-depend- World (Hemiptera: Heteroptera). Classifica- ent feeding behavior by western tarnished tion and Natural History. — Cornell Univ. plant bugs influences flower bud abscission in Press, Ithaca, NY: xii + 1-336. cotton. — Entomol. exp. Appl. 117: 235-242.

SHACKEL K.A., CELORIO-MANCERA M.P., AHMADI H., GREVE L.C., TEUBER L.R., BACKUS E.A. & J.M. LABAVITCH (2005): Micro-injection of Lygus sali- vary gland proteins to simulate feeding dam- age in alfalfa and cotton flowers. — Archiv. Ins. Biochem. Physiol. 58: 69-83.

SOUTHWOOD T.R.E. (1966): Ecological Methods, with Particular Reference to the Study of Insect Populations. — Methuen, London: xix + 1- 391.

TAYLOR G.S. & P.W. MILES (1994): Composition and variability of the saliva of coreids in relation to phytoxicoses and other aspects of the sali- vary physiology of phytophagous Het- eroptera. — Entomol. exp. Appl. 73: 265-277.

TAYLOR S.J., TESCARI G. & M. VILLA (2001): A Nearctic pest of Pinaceae accidentally introduced into Address of the Author: Europe: Leptoglossus occidentalis (Het- Dr. Paula Levin MITCHELL eroptera: Coreidae) in northern Italy. — Ento- Department of Biology mol. News 112: 101-103. Winthrop University TILLMAN P.G. (2006): Effect of selected insecticides on the leaffooted bug (Hemiptera: Coreidae). Rock Hill, SC 29733, U.S.A. — J. Entomol. Sci. 41: 184-186. E-Mail: [email protected]

1134