HORTICULTURAL ENTOMOLOGY Overwintering Squash Bugs Harbor and Transmit the Causal Agent of Cucurbit Yellow Vine Disease

1 1 2 3 3 4 S. D. PAIR, B. D. BRUTON, F. MITCHELL, J. FLETCHER, A. WAYADANDE, AND U. MELCHER

USDAÐARS, South Central Agricultural Research Laboratory, P.O. Box 159, Hwy. 3 West, Lane, OK 74555

J. Econ. Entomol. 97(1): 74Ð78 (2004) ABSTRACT Since 1988, cucurbit crops, particularly watermelon, cantaloupe, and squash, grown in Oklahoma and Texas have experienced devastating losses from cucurbit yellow vine disease (CYVD), caused by the phloem-limited bacterium Serratia marcescens Bizio. Squash bug, Anasa tristis (De Geer), is a putative vector of the pathogen. In 2000Ð2001, overwintering populations of squash bug collected from DeLeon, TX, were tested for their ability to harbor and transmit the bacterium. Individual squash bugs (n ϭ 73) were caged serially for periods of up to7donatleast four squash seedlings. Two studies were conducted, one with insects collected in November 2000 placed on Þrst true leaf-stage seedlings and the second with insects from an April 2001 collection, placed on 3Ð5 true leaf-stage squash. Controls consisted of squash seedlings caged without insects. Squash bug trans- mission rates of the pathogen in studies I and II were 20 and 7.5%, respectively. Overall, 11.0% of the squash bugs harbored and successfully transmitted the bacterium to squash seedlings. All control plants tested negative for S. marcescens and did not exhibit CYVD. Female squash bugs killed a signiÞcantly greater proportion of young Þrst leaf-stage seedlings than males. Feeding on 3Ð5 leaf- stage squash resulted in no plant mortality regardless of squash bug gender. This study demonstrated that the squash bug harbors S. marcescens in its overwintering state. The squash bugÐS. marcescens overwintering relationship reported herein greatly elevates the pest status of squash bug and places more importance on development of integrated strategies for reducing potential overwintering and emerging squash bug populations.

KEY WORDS Anasa tristis, cucurbit yellow vine disease, Serratia marcescens, cucurbits, overwin- tering

CUCURBITS, PRIMARILY WATERMELON,(Citrullus lanatas 2001). The disease has also been conÞrmed in Arkan- (Thunb.) Matsum. & Nakai), cantaloupe, Cucumis sas, Colorado, Kansas, and Nebraska (B.D.B., unpub- melo variety cantaloupensis Naud., squash, and pump- lished data). CYVD-affected plants usually exhibit kin, Cucurbita pepo L., are important horticultural stunting, yellowing, and gradual decline beginning crops in the south central region of the United States Ϸ10 to14 d before harvest. Occasionally a rapid wilt that are affected by a variety of insect and disease occurs at the time of ßowering and/or fruit set, and complexes. Cucurbit yellow vine disease (CYVD) is a plants collapse within a single day without plant yel- newly described disease that affects cucurbits in lowing (Bruton et al. 1995a). Early-planted watermel- Texas, Oklahoma (Bruton et al. 1998), Tennessee ons targeted for the lucrative 4 July market generally (Bost et al. 1999), and Massachusetts (Wick et al. are impacted more severely than later plantings. The symptom most diagnostic and consistent with the dis- Mention of trade names or commercial products in this article is ease in all affected cucurbit species is a honey brown solely for the purpose of providing speciÞc information and does not discoloration of the phloem (Bruton et al. 1998). Dis- imply recommendation or endorsement by the U.S. Department of Agriculture. The article cited was prepared by a USDA employee as ease symptoms have been consistently associated with part of ofÞcial duties. Copyright protection under U.S. copyright law the presence of a walled bacterium, observed by elec- is not available for such works. Accordingly, there is no copyright to tron microscopy in phloem sieve tubes. Losses can transfer. The fact that the private publication in which the article range from Ͻ5 to 100% in affected Þelds of water- occurs is itself copyrighted does not affect the material of the U.S. Government, which can be freely reproduced by the public. melon, squash, pumpkin, and cantaloupe. Bruton et al. 1 E-mail: [email protected]. (2003) and Rascoe et al. (2003) detailed the known 2 Department of Entomology, Texas A&M University, Stephenville, biology and etiology of a strain of Serratia marcescens TX 76401. Bazio conÞrmed as the causal agent of CYVD in wa- 3 Department of Entomology and Plant Pathology, Oklahoma State University, Stillwater, OK 74078. termelon, squash, pumpkin, and cantaloupe. 4 Department of Biochemistry and Molecular Biology, Oklahoma Spatial distribution studies showed the disease to State University, Stillwater, OK 74078. have a patchy or clumped distribution within water- February 2004 PAIR ET AL.: OVERWINTERING SQUASH BUGS 75 melon Þelds (Duthie et al. 1993). That and other with seedling squash plants and held at Ϸ29ЊC and a evidence suggested that an insect-transmitted patho- photoperiod of 16:8 (L:D) h to induce cessation of gen causes CYVD (Bruton et al. 1995b, Bextine et al. diapause (Nechols 1987, 1988). After 2 wk, the squash 2001). Prominent among cucurbit insect pests is the bugs were observed feeding and mating. Seeds of squash bug, Anasa tristis (De Geer), long recognized yellow squash (ÔLemon DropÕ) were planted in 128- as a serious and pervasive problem of cucurbit crops cell trays (Speedling Inc., Sun City, FL) Þlled with throughout much of the United States (Quaintance Redi-Earth soil-less mix (Scotts Sierra Horticultural 1899, Beard 1940). Historically, squash bugs prefer Products Co., Marysville, OH) and maintained in the squash and pumpkin, Cucurbita spp., as hosts and have greenhouse at 22Ð35ЊC. Seedlings were then trans- been serious pests of these crops in Texas and Okla- planted, one per pot, into white plastic pots (15 cm in homa (Fargo et al. 1988, Stroup 1998). In contrast to diameter by 17 cm in height) containing sterilized previous reports, squash bugs have become an increas- sand. ing concern for growers of watermelon and canta- Study I. Twenty bugs (n ϭ 10 males and 10 females), loupe in Texas and Oklahoma (Pair 1997, Riley et al. selected from those that had terminated diapause, 1998, Edelson et al. 1999). Generally, infestations in were caged individually on Þrst true-leaf stage squash watermelon, cantaloupe, or cucumber are thought to seedlings. Plants were caged individually using clear result when preferred hosts are absent (Hoerner 1938, plastic Lexan (General Electric, Mt. Vernon, IN) cyl- Eichman 1945). Squash bugs damage cucurbits inders (8.5 cm in diameter by 30 cm in height) covered through feeding and withdrawal of plant sap, resulting with wire mesh. A single adult squash bug was intro- in plant wilting, delayed maturity, reduced yield, or duced into each cage and allowed to feed for7dor death. Sudden collapse of cucurbit plants following until the plant exhibited severe signs of stress or had squash bug feeding has been attributed to injected died as a consequence of squash bug feeding. At that toxins and was termed Anasa wilt (Robinson and Rich- point, the squash bug was transferred to another plant. ards 1931). However, toxins were never identiÞed and On the seventh day, each squash bug was transferred the wilting has since been ascribed to vascular block- to a new plant, regardless of the number of days on the age (Neal 1993). prior test plant. Thus, each individual squash bug was Recently, conclusive evidence revealed that the exposed to enough squash plants to obtain a minimum squash bug can transmit S. marcescens to several cu- of four different plants that were suitable for CYVD curbit crops under laboratory and Þeld conditions analysis. Squash plants (n ϭ 6) caged without squash (Pair et al. 2000, Bruton et al. 2003). However, squash bugs served as controls. bug infestations of cucumber, Cucumis sativus L., are Study II. In mid-April 2001, the DeLeon site was rare. Coincidentally, there are no reports of CYVD in revisited and squash bugs (n ϭ 56; sex ratio (1:1.9, cucumber, although low infection rates were obtained female:male) were collected from the overwintering from artiÞcial inoculation in the greenhouse (Bruton habitat. Insects from this collection fed readily, sug- et al. 2003). The implication of squash bug as a vector gesting that diapause had terminated. A second study of CYVD led to questions concerning the ability of was initiated using the surviving 19 female and 34 overwintering squash bug to successfully harbor S. males from this collection. Study II was conducted marcescens. Herein, we report overwintering of S. similarly to study I, except that 3Ð5 true-leaf stage marcescens in a feral population of A. tristis and sub- squash seedlings were used. No plant death due to sequent transmission of the bacterium to healthy test squash bug feeding was observed in study II; thus, each plants. insect was exposed to a total of four plants except in cases where the insect died. In study II, 35 squash plants were individually caged without insects as a Materials and Methods control. Hibernating squash bugs (n ϭ 208; sex ratio 1:1.6, In both studies, following the prescribed length of female:male) were collected in early November 2000 exposure to plants, cages and insects were removed, from overwintering habitat near in Comanche Co. and the treated and control plants were placed in a near DeLeon, TX, an area located in the Cross Timbers different greenhouse and fertilized weekly with a vegetational zone (Correll and Johnston 1979). Sub- 0.3% (wt:vol) solution of PeterÕs (Spectrum Group, stantial hectares of watermelon and cantaloupe are St. Louis, MO) fertilizer. After 4 wk, each plant was grown locally and are consistently affected to some removed from the pot, washed, and a thin cross section degree by CYVD. The insects were recovered from of the upper primary root was observed under a light hardwood leaf litter and dead tree bark in a well- microscope for the presence of phloem discoloration. drained area adjacent to an old home site in an area 5 A plant was considered positive for CYVD if phloem km from the nearest cucurbit crop. The site was Ͻ200 discoloration was observed. In addition, a plant tissue m2, and the entire area was examined for presence of sample was taken from the same area for bacterial squash bugs. The insects were transferred to environ- isolation and polymerase chain reaction (PCR) by mental chambers at Lane, OK, where they were main- using methods developed by Avila et al. (1998) and tained in a torpid state (12.5ЊC, photoperiod of 13:11 modiÞed by Melcher et al. (1999). Tissue samples (3 [L:D] h, Ϸ 60% RH) until used for transmission studies mm) for isolation were surface sterilized in 10% Clo- to plants. In mid-December, 30 male and 30 female rox solution for 30 s, placed on a paper towel, and squash bugs were transferred to 1-m3 screen cages sprayed with 80% ethanol; ground using a sterilized 76 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 97, no. 1

Table 1. CYVD incidence resulting from squash bugs collected did not survive even after the insect was removed, the at Deleon, TX, and feeding on healthy ‘Lemondrop’ squash actual percentage of transmission may have been un- seedlings derestimated. In each case, S. marcescens was reiso- Squash bug CYVDa lated from the symptomatic plants but not from Sex % No. plants % asymptomatic plants. Reisolated bacteria were con- n Transmitting exposedb Symptomatic Þrmed as S. marcescens by PCR. In study II, 7 of 185 (3.8%) test plants displayed Study Ic & 10 30.3 70 8.6 CYVD symptoms (Table 1). Transmission rates were ( 10 10.0 40 10.0 considerably lower than that observed in study I. All Summary 20 20.0 110 9.2 positive transmissions observed in study II resulted Study II from a single female and three males that were col- & 19 5.3 63 4.8 ( 34 8.8 122 3.3 lected on 15 April. Successful transmission of the bac- Summary 53 7.5 185 3.8 terium to healthy plants by positive insects ranged from 25 to 75%. None of the control plants (n ϭ 35) a Plants symptomatic for CYVD exhibited phoem discoloration exhibited symptoms characteristic of CYVD and all were PCR positive, and the bacterium was reisolated; asymptomatic test and control (study I ϭ 6; study II ϭ 35) plants were all negative. proved PCR negative for S. marcescens. As in study I, b Plants used in study I were Þrst true leaf-stage squash; those in reisolated bacteria were conÞrmed as S. marcescens by study II were 3Ð5 true-leaf stage. PCR. c Insects used in study I were collected November 2000; insects used in study II were collected in April 2001. Discussion mortar and pestle; and a 10-␮l pipetted subsample was In summary, 11% (8 of 73) of the squash bugs tested spread onto nutrient agar. After3dofgrowth at room from the DeLeon, TX, site transmitted the CYVD temperature, colonies with characteristics consistent bacterium to healthy plants. Of the insects exposed to with those of the CYVD strain of S. marcescens were at least four successive test plants, CYVD bacterial veriÞed by PCR. All plants that were killed had de- transmission ranged from 0 to 100%. Interestingly, teriorated to some degree. As a result, all dead plants more males were present in both the November 2000 were counted as asymptomatic even though infection and April 2001 collections (P2 ϭ 11.1, df ϭ 1, P Ͻ 0.01; may have occurred. P2 ϭ 5.8, df ϭ 1, P Ͻ 0.05), respectively). The dispro- Homogeneity of sex ratios from each collection of portionate numbers of males found may have been squash bugs from overwintering habitat was deter- due to sampling error or to other unknown factors. mined using chi-square; mortality of seedling squash as The lower percentage of insects transmitting S. a function of squash bug gender was analyzed using marcescens in study II may have been a function of the Mantel-Haenszel chi-square test (SAS Institute sampling, or likely the difference in test plant age, i.e., 2001). 1-leaf versus 3Ð5 leaf-stage squash. Recent studies have demonstrated that younger seedlings are more susceptible to infection by mechanical inoculation Results than those of more advanced age (Bruton et al. 2003). In study I, 4/20 (one male, three female) squash Certain strains of S. marcescens act as entomopatho- bugs transmitted S. marcescens to at least one test plant, gens (Rose et al. 1999). However, the effects of the resulting in phloem discoloration characteristic of CYVD strain of S. marcescens on insects in general or CYVD (Table 1). Of 110 plants exposed to squash bugs on overwintering squash bug mortality are unknown. in study I, 9.2% developed phloem discoloration. On The S. marcescensÐA. tristis relationship described average, 20% of the squash bugs collected in Novem- herein and elsewhere (Pair et al. 2000, Bruton et al. ber harbored and transmitted the bacterium. Trans- 2003, Rascoe et al. 2003) is, to our knowledge, the Þrst mission rates of CYVD-positive insects ranged from in which the squash bug has been identiÞed as a vector 11.1 to 100%. One male squash bug transmitted to all of a plant pathogen. No other coreids have been as- four squash plants, suggesting that the bacterium can sociated with a bacterial-induced plant disease be retained for at least 21 d after initial feeding. Num- (Mitchell 2000). Squash bugs, considered primary bers of plants exposed to individual squash bugs pests in squash and pumpkin, have decreasing pref- ranged from 4 to 12 and seedling death occurred more erence for and decreasing reproduction rates on wa- often when they were exposed to female squash bugs termelon, cantaloupe, and cucumber (Bonjour and than to males. In study I, in which young seedling Fargo 1989; Bonjour et al. 1990, 1991). However, they squash were used as test plants, all female insects have caused increasing concern in recent years among damaged the plants to the extent that one or more test watermelon and melon producers in Texas and Okla- plants had to be replaced. Numbers of plants that were homa. Margolies et al. (1998) noted that squash bugs replaced ranged from one to eight for individual fe- can overcome the antibiosis effects of host plant re- males. Overall, female squash bugs killed 30 of 70 sistance within Þve generations. Because early-season (42.8%) (Mantel-Haenszel P2 ϭ 10.0, df ϭ 1, P Ͻ 0.01) commercial summer squash production is limited in plants offered, whereas none (0/40) were killed by Oklahoma and central Texas, there may be a selection male squash bug feeding. Because the seedlings were pressure for increased squash bug feeding and surviv- only in the Þrst true-leaf stage, and many of the plants ability on watermelon. February 2004 PAIR ET AL.: OVERWINTERING SQUASH BUGS 77

Evidence presented from this study conÞrms not efforts will require a thorough knowledge of squash only that the squash bug can transmit S. marcescens, bug biology, including how they acquire and retain S. the CYVD causal bacterium, but also that overwin- marcescens, which is unknown. The mechanism of tering populations in central Texas harbor it. It is likely retention and acquisition of the bacterium and strat- that populations in other states where CYVD has been egies to reduce early- and late-season and diapausing reported are likewise capable of retaining the patho- squash bug populations are under investigation. gen over the winter and transmitting to cucurbits the following spring. Earlier reports have emphasized the need to clear crop residue and eliminate potential Acknowledgments overwintering populations of squash bug as a means to We appreciate the technical assistance provided by D. reduce losses the following season. This report places Baze, B. Anderson, S. Goodson, and R. Marble. Appreciation even more importance on development of integrated also is extended to J. V. Morgan and C. L. Bruton for collec- strategies aimed not only at reducing potential over- tion of squash bugs and to critical reviews by J. V. Edelson and wintering populations but also at early-season sup- A. Davis. pression of emerging populations. For example, Pair (1997) reported that the use of squash plants treated References Cited with carbofuran was a reliable tool to monitor squash bug emergence in Oklahoma. In addition, when sim- Avila, F. J., B. D. Bruton, J. Fletcher, J. L. Sherwood, S. D. ilarly treated squash trap plants were place in small Pair, and U. Melcher. 1998. Polymerase chain reaction Þelds of watermelon, cantaloupe, and squash, squash detection and phylogenetic characterization of an agent bug populations were concentrated and controlled in associated with yellow vine disease of cucurbits. Phyto- pathology 88: 428Ð436. the squash trap crop. The use of trap crops in large Beard, R. L. 1940. The biology of Anasa tristis De Geer. Þelds of watermelon has been reported effective in Conn. Agric. Exp. Stat. Bull. 440: 595Ð682. large Þeld situations in central Texas (Pair et al. 1998, Bextine, B., A. Wayadande, B. D. Bruton, S. D. Pair, F. Stroup 1998) for suppression of squash bug popula- Mitchell, and J. Fletcher. 2001. Effect of insect exclusion tions. Interplanting of squash with watermelon re- on the occurrence of yellow vine disease and of the duced the incidence of CYVD in small plots of wa- associated bacterium in squash. Plant Dis. 85: 875Ð878. termelon (unpublished data), and the technique is Bonjour, E. L., and W. S. Fargo. 1989. Host effects on the under investigation as a management tool in commer- survival and development of Anas tristis (Heteroptera: cial production systems. Coreidae). Environ. Entomol. 18: 1083Ð1085. Bonjour, E. L., W. S. Fargo, and P. E. Rensner. 1990. Ovi- Watermelon seedlings, as with other cucurbits, are positional preference of squash bugs (Heteroptera: Core- extremely vulnerable to squash bug feeding. In study idae) among cucurbits in Oklahoma. J. Econ. Entomol. 83: I, female squash bug feeding resulted in higher mor- 943Ð947. tality of seedling squash than males. However, sample Bonjour, E. L., W. S. Fargo, J. A. Webster, P. E. Richardson, sizes were too small to determine whether differential and G. H. Brusewitz. 1991. Probing behavior compari- transmission of CYVD is a function of gender. Beard sons of squash bugs (Heteroptera: Coreidae) on cucurbit (1940) observed that young squash seedlings were hosts. J. Environ. Entomol. 21: 143Ð149. extremely susceptible to squash bug feeding and that Bost, S. C., F. Mitchell, U. Melcher, S. D. Pair, J. Fletcher, A. a preference for stem feeding almost always resulted Wayadande, and B. D. Bruton. 1999. Yellow vine of wa- termelon and pumpkin in Tennessee. Plant Dis. 83: 587. in plant death. As the plants grew, leaf feeding became Bruton, B. D., S. D. Pair, and E. V. Wann. 1995a. Yellow vine more common, and the plant was able to tolerate disease of watermelon and cantaloupe in Central Texas additional feeding pressure. Bonjour and Fargo (1989) and Oklahoma, pp. 151Ð159. In G. E. Lester, and J. R. reported that female squash bugs are Ϸ25% larger than Dunlap [eds.], Cucurbitaceae Õ94. Gateway Printing, Ed- males, which may inßuence food resource require- inburg, TX. ments. Therefore, female feeding and subsequent in- Bruton, B. D., S. D. Pair, T. W. Popham, and B. O. Cart- creased mortality of young squash seedlings may be wright. 1995b. Occurrence of yellow vine, a new disease functions of greater pressure by females that would of squash and pumpkin, in relation to insect pests, likely increase plant vascular damage and, perhaps, mulches, and soil fumigation. Subtrop. Plant Sci. 47: 53Ð 58. heighten the probability that the bacterium would be Bruton, B. D., J. Fletcher, S. D. Pair., M. E. Shaw, and H. transferred. There is also the possibility that the fe- Sittertz-Bhatkar. 1998. The association of a phloem-lim- male squash bug, by virtue of greater body weight, ited bacterium with yellow vine disease in cucurbits. ingests and sustains a higher titer of the bacterium. Plant Dis. 82: 512Ð520. Edelson et al. (2002, 2003) determined that squash Bruton, B. D., F. Mitchell, J. Fletcher, S. D. Pair, A. Way- bug feeding severely impacts watermelon survival, adande, U. Melcher, J. Brady, B. Bextine, and T. H. Po- growth, and yield. Consequently, the association of pham. 2003. Serratia marcescens, a phloem-colonizing, squash bug and CYVD, and the overwintering of the squash bug-transmitted bacterium: causal agent of cu- bacterium in the squash bug, substantially elevates this curbit yellow vine disease. Plant Dis. 87: 937Ð944. Correll, D. S., and M. C. 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