arthropods associated with medicinal plants in coastal south carolina

© 2007 The Authors Insect Science (2007) 14, 519-524Journal compilation © Institute of Zoology, Chinese Academy of Sciences

Arthropods on medicinal plants 519

Abstract Arthropods were sampled from feverfew [Tanacetum parthenium (L.) Schultz-Bip], Echinacea purpurea (L.) Moench, Echinacea pallida (Nutt.) Nutt., Valeriana officinalisL., and St. John’s wort (Hypericum perforatum L.) during 1998-2001. In addition,arthropods were sampled on tansy (Tanacetum vulgare L.) from 2001-2004. In general,50-60 arthropod species where collected and identified among all of the medicinal plantspecies. Among the predators, Orius insidiosus (Say) (Hemiptera: Anthocoridae), Geocorispunctipes (Say) (Hemiptera: Lygaeidae) and spiders were most abundant from 1998-2004.The three-cornered alfalfa hopper, Spissistilus festinus (Say), was the most abundantherbivore found from 1998 to 2001. Orius insidiosus and G. punctipes were 3-4 times moreabundant on T. parthenium than on any other medicinal plant species. Based on the numbersof predatory arthropods found on T. parthenium, this crop could be suitable as a companionor “banker” plant to attract and maintain populations of predators, especially O. insidiosusand G. punctipes. Whitefly nymphs attacked by predators with piercing/sucking mouthpartsare easily identified using a microscope because of the general appearance of the carcass leftby the predators. Thus, populations of predators on T. parthenium suppressed Bemisia tabacipopulations on E. purpurea when these crops were planted as companion crops.

Key words companion plants, Geocoris punctipes, medicinal plants, Orius insidiosus,predatorsDOI 10.1111/j.1744-7917.2007.00181.x

www.blackwellpublishing.com/ins 519


Correspondence: B. Merle Shepard, Clemson University,Coastal Research and Education Center, 2700 Savannah Hwy.,Charleston, SC 29414, USA. Tel: +1 843 402 5393; fax: +1 843471 4654; email: [email protected]

Arthropods associated with medicinal plants in coastalSouth CarolinaROLANDO LOPEZ and B. MERLE SHEPARDClemson University, Department of Entomology, Soils and Plant Sciences, and Coastal Research and Education Center,Charleston, South Carolina, USA

Introduction

Although medicinal plants have been used for thousandsof years in every culture of the world, serious scientificresearch supporting their therapeutic value began onlyaround 1960. After that, scientists in the USA began aworldwide search and analysis of plants for treatment ofcancer and other diseases (Duke, 1997). The cancer screeningprogram eventually analyzed about 10% of the world’sknown plant species and provided an original data base:http://www.ars-grin.gov/duke/ (Duke, 1997). The World

Health Organization estimates that 75%-80% of people indeveloping countries, rely on plant-based medicines forprimary health care (WHO, 2005). Over 25% of ourcommon medicines contain at least some compounds iso-lated from plants. Approximately 10% of the major drugsin the USA have plant extracts as their active ingredient(Duke, 1997). In the USA alone from 1988 to 1998,medicinal herbs and supplements sales went from $200million to over $5 billion with many of them availablethrough pharmacy chains, grocery stores and via the internet(Graedon & Graedon, 2002; Dufault et al., 2000).

The higher demand for medicinal plants comes with anincreasing demand from a more educated public ready topay more for a more effective and safer product. It wasreported at the International Symposium on Medicinal andNutraceutical Plants (March 2007) that India, one of thecountries with a very high export of medicinal herbs


520 R. Lopez & B. M. Shepard

worldwide along with China, only has 15%-20% of themedicinal plants cultivated under organic conditions. It isexpected that as the demand for medicinal plants increasesthe demand for insecticide-free medicinal plants will alsobe required from the suppliers. However, information onpossible pests of medicinals and on ways to control thosepests organically is not available anywhere at present.

Except for a report of seasonal abundance of whiteflies(Bemisia tabaci) on E. purpurea in South Carolina, USA,(Simmons et al., 2000), we found no other reports ofarthropods associated with commercialized medicinal plants.The objective of this study was to determine the relativeabundance of insect herbivores and predatory arthropodson the six species: valerian (Valeriana officinalis L.), tansy[Tanacetum vulgare (L.)], feverfew [Tanacetum parthenium(L.) Schulz-Bip], coneflowers (Echinacea purpurea L.Moench), Echinacea pallida (Nutt.), and St. John’s wort(Hypericum perforatum L.) as a prerequisite to findingways for organic control of possible arthropod pests.

Materials and methods

1998-2001

Feverfew, coneflower (E. purpurea and E. pallida),valerian, tansy (T. vulgare) and St. John’s wort (H.perforatum) were established in field plots in 1998-2001at Clemson University’s Coastal Research and EducationCenter, Charleston, South Carolina, USA.

Seeds were grown every year in a greenhouse for 5 weeksbefore transplanting them into field plots in either the lastweek of April or the first week of May. Plots were com-posed of two rows of the same plant species 8 m long and4 m wide with each plot 3 m apart. The experiment wasarranged in a complete randomized design with fivereplications. Approximately 5 m of each row from thecentral part of every plot was sampled weekly using a D-Vac suction sampler (Dietrich, 1961) each year from Juneto September. Each sample was transferred to a Ziploc®

bag and taken to the laboratory where arthropods weresorted and specimens identified to species or family usinga microscope.　　　

2001-2004

In addition to D-Vac sampling, in 2002, we randomlyremoved six leaves from each E. purpurea plot and placedthem in individual Ziploc® bags to determine the numbersof whitefly nymphs, a major pest of E. purpurea (Simmonset al., 2000). Six flower heads were collected weekly fromboth E. purpurea and feverfew to determine the numbers of

Orius and Geocoris, the major predator genera. During the2001-2002 seasons, we replaced E. pallida with T. vulgare.

Data were analyzed using a one-way analysis of vari-ance to test for difference in abundance of the mainarthropod groups among the different species of medicinalplants. A Tukey HSD test was performed after the ANOVAto determine significant differences at P < 0.05.

Results and discussion

1998-2001

Arthropods were grouped into orders and families, ex-cept for G. punctipes and O. insidiosus, which were themost abundant predators. Other predatory Hemiptera in-cluded Nabis roseipennis Reuter, Podisus maculiventris(Say), Jalissus sp., Sinea spinnipes Herrich-Schäffer, andArilus cristatus (L). Coccinellids included Coccinellaseptempunctata L., Harmonia axyridis (Pallas) andColeomegilla maculata De Geer. Spiders in the familyLycosidae were mainly Schizocosa mcooki (Montgomery1904), within Oxyopidae. Peucetia viridans (Hentz) wasmost abundant and Phidippus sp. was most numerouswithin the Salticidae. Other spiders belonged to Clubionidaeand Linyphidae. All beneficial arthropods recorded weresignificantly more abundant in plots of feverfew (Table 1).The canopy of feverfew is lush, well-developed and mayafford a favorable habitat for both herbivores and benefi-cial species than did the other species of medicinal plants.

Seasonal average numbers are shown in Table 1. Para-sitic wasps belonged primarily in the families Chalcididae,Braconidae and Scelionidae. Plant feeders were mainly thepotato leafhopper, Empoasca fabae Harris, and the three-cornered alfalfa hopper, Spissistilus festinus (Say). Themajor aphid species were Myzus persicae (Sulzer) andMacrosiphum sp. Among the herbivores, S. festinus werehighest on feverfew with a mean number of 22.2 ± 3.7 persample during the season (Tables 1,2).

Adult Orius insidiosus were frequently encounteredwhile examining foliage but their numbers were low in D-Vac samples. Their small size and behavior may have keptthem from being adequately captured by this device, butthe actual reason for the low numbers using the D-Vacmachine is not known.

2001-2004

Relative abundance of arthropods on each of the medici-nal plants was about the same as previous years during theseason (Tables 1, 2). The most abundant beneficial groupswere spiders, G. punctipes, Solenopsis invicta and



coccinellids. The most abundant insect herbivores wereleafhoppers (e.g., E. fabae), whiteflies (e.g., B. tabaci),thrips, aphids and Lepidoptera such as Homeosomaelectellum, respectively. During this 3-year period the onlyimportant pest was B. tabaci which caused significantdamage to valerian. H. perforatum and valerian wereaffected by fungal diseases (Sclerotium rolfsii) due toexcessive rain during 2002 and a large number of plantsdied following these events (Keinath et al., 1999).

In 2001 plantings, there was an outbreak of Thripsnigropilosus Uzel (Thysanoptera: Thripidae) on T.parthenium early in the season on field plots during March-April 2001. Also on field plots during the same year,Condica sutor (Guenée) (Lepidoptera: Noctuidae) oc-

Table 1 Mean (± SE) numbers of major groups of insects onmedicinal plants, 1998-2001, Charlston, South Caroline, USA.

Arthropod groups Medicinal plant species Mean ± SE

Coccinellidae Valeriana officinalis 5.8 ± 1.0 a

Tanacetum parthenium 4.8 ± 0.7 a

Hypericum perforatum 3.2 ± 0.8 ab

Echinaceae purpurea 3.2 ± 0.5 ab

Echinaceae pallida 1.2 ± 0.2 b

Spiders Tanacetum parthenium 5.6 ± 0.8 a

Hypericum perforatum 3.2 ± 0.5 b

Valeriana officinalis 2.6 ± 0.6 b


Echinaceae purpurea 1.1 ± 0.3 b

Geocoris punctipes Tanacetum parthenium 33.0 ± 2.8 a

Hypericum perforatum 6.1 ± 0.8 c

Valeriana officinalis 3.1 ± 0.6 d



Predatory Heteroptera Tanacetum parthenium 4.1 ± 0.6 b





Parasitic wasps Tanacetum parthenium 6.2 ± 0.7 a

Valeriana officinalis 5.9 ± 1.2 ab

Echinaceae purpurea 3.3 ± 0.6 bc


Echinaceae pallida 1.3 ± 0.2 c

Miridae Tanacetum parthenium 4.6 ± 1.7 a





Leafhoppers Tanacetum parthenium 22.2 ± 3.8 b



Echinaceae pallida 3.0 ± 0.4 bc


Aphids Hypericum perforatum 4.1 ± 0.7 a

Echinaceae pallida 2.6 ± 0.5 ab


Valeriana officinalis 1.2 ± 0.3 bc

Tanacetum parthenium 0.7 ± 0.3 c

Predatory Heteroptera are those other than G. punctipes.Means with different letters (Tukey’s test) are significantlydifferent at P < 0.05. Each arthropod group numbers werestatistically analyzed independently from each other comparingits relevance for each medicinal plant species.

Table 2 Mean numbers (± SE) of the most abundant predatorson five species of medicinal plants 2001-2004, Charleston,South Carolina, USA.


Spiders Tanacetum parthenium 6.0 ± 0.8 aHypericum perforatum 2.5 ± 0.7 bTanacetum vulgare 1.8 ± 0.4 bEchinacea purpurea 1.3 ± 0.4 bValeriana officinalis 0.8 ± 0.1 b

Solenopsis sp. Tanacetum parthenium 5.0 ± 1.9 aTanacetum vulgare 2.3 ± 1.0 abHypericum perforatum 1.0 ± 0.2 bEchinacea purpurea 0.3 ± 0.1 bValeriana officinalis 0.1 ± 0.1 b

Geocoris punctipes Tanacetum parthenium 5.5 ± 1.8 aEchinacea purpurea 4.5 ± 1.2 abValeriana officinalis 3.3 ± 1.4 abcHypericum perforatum 0.8 ± 0.4 bcTanacetum vulgare 0.0 ± 0.0 c

Orius insidiosus Tanacetum parthenium 1.0 ± 0.3 aTanacetum vulgare 0.8 ± 0.4 abEchinacea purpurea 0.0 ± 0.0 bHypericum perforatum 0.0 ± 0.0 bValeriana officinalis 0.0 ± 0.0 b

Coccinellidae Valeriana officinalis 0.3 ± 0.2 aHypericum perforatum 0.2 ± 0.1 abEchinacea purpurea 0.0 ± 0.0 bTanacetum parthenium 0.0 ± 0.0 bTanacetum vulgare 0.0 ± 0.0 b

Parasitoids Echinacea purpurea 4.3 ± 0.6 aTanacetum parthenium 4.2 ± 1.0 aValeriana officinalis 3.3 ± 1.0 abHypericum perforatum 2.5 ± 0.7 abTanacetum vulgare 2.3 ± 0.6 b

Tukey’s studentized (HSD) test (P < 0.05).



originally obtained on feverfew in 1998-2001. FewEmpoasca sp. were found on T. parthenium from 2001-2004. During the 2002 season, whiteflies were concen-trated on H. perforatum during the summer (Table 3).Table 4 lists all insects that were collected on the medicinalplants from 1998 to 2004. Many of those insects werecollected only a few times, but in 2001, two insect pestsThrips nigropilosus and Condica sutor (Lepidoptera:Noctuidae) caused significant damage on feverfew.Homeosoma electellum (Lepidoptera: Noctuidae) has alsobeen causing some damage every year on coneflowerseeds. Dense populations of G. punctipes and O. insidiosusadults (between 5 and 10 adults of each species per plant,respectively) also were found overwintering under thecanopy of feverfew plants. Finding that feverfew harboredelevated populations of Orius and Geocoris, as well as anoverwintering site for these natural enemies, makes thisplant a possible candidate as a “banker plant” that may beplanted as a companion crop to attract and maintain preda-tors that move onto other plants that are susceptible toattack by insect pests. We are continuing to test feverfewplants in the laboratory with Orius and Geocoris to com-pare their fecundity and survival with or without preyversus two other unrelated plants. Whereas numerousspecies of spiders including many from the familiesLycosidae, Oxyopidae, Salticidae, Clubionidae, andLinyphiidae were always present in our plots, their impacton insect herbivores will require more study due to thecomplexity in the dynamics of spiders.

The consistent presence of the predatory heteropterans,O. insidiosus and G. punctipes, as well as the abundance ofpredators and parasitoids in our experimental plots offeverfew affords the development of a sustainable arthro-pod control strategy for medicinal plants. Feverfew attractsand maintains populations of arthropod predators. Thesepredators have been reported to feed on many insect andarthropod pests including thrips, whiteflies, two-spottedspider mites, and other pests, and also obtain some nutri-tion from plants to complement their carnivorous behavior(Coll & Robertson, 1998; Coll, 1998; Alomar &Wiedenmann, 1996; Crocker & Whitcomb, 1980; Cohen,1996). However, this is the first report, to our knowledge,that a plant species like T. parthenium has been shown tohave the attributes to attract and maintain O. insidiosus andG. punctipes all season long even when prey numbers arelow. The lush canopy structure of T. parthenium andperhaps its phytochemicals may provide a favorable envi-ronment and food for these beneficial species.

In summary, there are richer and more diverse communitiesof arthropods associated with T. parthenium than with anyother of the medicinal plant species observed in the coastalplain of South Carolina. The presence of this large and diverse

Table 3 Mean (± SE) number of plant-feeding arthropods onfive species of medicinal plants 2001-2004, Charleston, SouthCarolina, USA.


Leafhoppers Tanacetum parthenium 3.8 ± 0.7 aEchinacea purpurea 2.8 ± 0.3 abHypericum perforatum 2.3 ± 0.5 abTanacetum vulgare 2.3 ± 0.8 abValeriana officinalis 1.3 ± 0.3 b

Bemisia tabaci Hypericum perforatum 86.7 ± 18.1 aValeriana officinalis 13.0 ± 4.3 bEchinacea purpurea 6.3 ± 2.3 bTanacetum vulgare 4.7 ± 1.6 bTanacetum parthenium 1.3 ± 0.6 b

Aphids Hypericum perforatum 3.8 ± 0.6 aTanacetum parthenium 0.7 ± 0.3 abValeriana officinalis 0.3 ± 0.2 bTanacetum vulgare 0.0 ± 0.0 bEchinacea purpurea 0.0 ± 0.0 b

Thrips Tanacetum parthenium 0.2 ± 0.1 aEchinacea purpurea 0.0 ± 0.0 bValeriana officinalis 0.0 ± 0.0 bTanacetum vulgare 0.0 ± 0.0 bHypericum perforatum 0.0 ± 0.0 b

Lepidoptera Tanacetum parthenium 3.3 ± 1.4 aTanacetum vulgare 2.2 ± 0.5 abHypericum perforatum 1.0 ± 0.2 abEchinacea purpurea 0.7 ± 0.2 bValeriana officinalis 0.0 ± 0.0 b

Tukey’s studentized (HSD) test at P < 0.05.

curred in outbreak numbers on T. parthenium and manyplants were completely defoliated. This is the first report ofoutbreaks of these two pests on medicinal plants. Out-breaks have not occurred again at this location to date. Thesunflower moth, Homeosoma electellum (Hulst),(Lepidoptera: Pyralidae) also consistently caused damageto flower heads in both Echinacea species under fieldconditions.

Mean seasonal averages of each arthropod group for the2001-2004 seasons are shown in Tables 2 and 3. Therewere significantly higher numbers of spiders, red importedfire ant (Solenopsis invicta Buren) G. punctipes, O.insidiosus and Coccinellidae on T. parthenium comparedto these same groups of insects on the other medicinal plantspecies. Among the herbivores, numbers of S. festinuswere highest on feverfew with a mean number of 3.8 ± 0.7 per sample during the last three seasons. This 3.8 ± 0.7S. festinus mean number per sample from 2001-2004 wasa significant reduction from the 22.2 ± 3.7 per sample



Table 4 Arthropods collected from medicinal plants from 1998-2004, Charleston, South Carolina, USA.

†Outbreaks occurred only in 2001 on field plots.

group of predators on feverfew could make it an excellentcandidate for use in a system of companion or banker plantsthat offer a favorable habitat for build-up and maintenanceof indigenous arthropod predators. Thus, when Echinaceaesp. is severely attacked by whiteflies, these predators thenmove from T. parthenium onto Echinaceae spp., and mayprovide control of whiteflies and other arthropod pests.

Acknowledgments

We thank Dr. Brian Scholtens for identification of Candicasutor. This work was supported in part by a grant from theUSDA, CSREES. This publication is Technical contribu-tion number 5342 of the Clemson University ExperimentStation.

Order Family Species

Coleoptera Coccinellidae Hippodamia convergensGuérin-MénevilleColeomegilla maculata (DeGeer)Harmonia axyridis (Pallas)Coccinella septempunctata L.Coccinella novennotata HerbstScymus sp.

Cerambicidae sp.1Curculionidae sp.1Chrysomelidae Diabrotica undecimpuntata

howardii BarberPhyllotreta spp.

Elateridae sp.1Carabidae spp.Corylophidae Orthoperus sp.Staphilinidae Proteinus sp.

Coproporus sp.Oxyporus sp.

ScarabaeidaeThysanoptera Thripidae Frankliniella occidentalis

(Pergande)Thrips nigropilosus Uzel,1895†

Lepidoptera Noctuidae Condica sutor (Guenée)†

Tortricidae Homeosoma electellum (Hulst)Colias eurytheme Boisduval

Papilionidae Papilio polyxenes americus Kollar, 1850

Pieridae Pieris rapae (L.)Lycaenidae Parrhasius m-album

(Boisduval & LeConte)Atlides halesus (Cramer)

Dermaptera Forficulidae Labidura riparia (Pallas)Hemiptera Pentatomidae Perillus bioculatus (F.)

Miridae Nezara viridula (L.)Taylorilygus sp.Halticus bractatus (Say)

Coreidae Anasa tristis (DeGeer)Membracidae Spissistilus festinus (Say)

Leptoglossus spp.Alydadae Alydus eurinus (Say)

Order Family Species

Lygaeidae Geocoris punctipes (Say)Geocoris pallens StålLygus lineolaris(Palisot de Beauvois)Nysius raphanus HowardBlissus leucopterus (Say)

Antochoridae Orius insidiosus (Say)Berytidae Jalysus sp.Nabidae Nabis roseipennis ReuterReduviidae Arilus christatus (L.)

Sinea spinnipes(Herrich-Schaeffer)Sinea diadema (Fabricius)

Tingidae Corythucha sp.Stephanitis sp.

Homoptera Cicadellidae Homalodisca coagulata (Say)Homalodisca insolita (Walker)Empoasca fabae (Harris)

Aphididae Myzus persicae (Sulzer)Aleyrodidae Bemicia tabaco biotype B

(Gennadius)Aleyrodes sp.

Psyllidae Psylla sp.Orthoptera Acrididae Melanoplus sp.

Gryllidae Oecanthus celerinictusT. Walker 1963

Neuroptera Chrysopidae Chrysoperla rufilabris(Burmeister)Chrysopa sp.

Odonata Aeshnidae Erythemis simplicicolis (Say)Zigoptera Calopterix sp.

Diptera Syrphidae spp.Tipulidae spp.Culicidae Aedes albopictus (Skuse)

Hymenoptera Braconidae sp.Aphelinidae Eretmocerus sp.

Encarsia sp.Formicidae Solenopsis invicta Buren

Crematogaster sp.Lasius alienus (Foerster)



References

Alomar, O. and Wiedenmann, R.W. (1996) Zoophytophagousheteroptera: Implications for life history and integrated pestmanagement. Thomas Say Publications in Entomology:Proceedings. Entomological Society of America, Lanham,Maryland, USA. pp. 201.

Cohen, A.C. (1996) Plant feeding by predatory heteroptera:evolutionary and adaptational aspects of trophic switching.Predatory Heteroptera: Their Ecology and Use in BiologicalControl. (eds. M. Coll & J.R. Ruberson) Thomas Say Publica-tions in Entomology: Proceedings. Entomological Society ofAmerica Lanham. Maryland, USA. pp. 233.

Coll, M. (1998) Living and feeding on plants in predatoryheteroptera. Predatory Heteroptera: Their Ecology and Usein Biological Control (eds. M. Coll & J.R. Ruberson), pp. 89-129. Thomas Say Publications in Entomology: Proceedings.Entomological Society of America, Lanham, Maryland, USA.

Crocker, R.L. and Whitcomb, W.H. (1980) Feeding niches of thebig-eyed bugs Geocoris bullatus, G. punctipes and G. uliginosus(Hemiptera: Lygaeidae: Geocorinae). EnvironmentalEntomolology, 9, 508-513.

Dietrick, E.J. (1961) An improved backpack motor fan forsuction sampling of insect populations. Journal of EconomicEntomology, 54, 394-395.

Dufault, R.J., Hassell, R., Rushing, J.W., Shepard, M. andKeinath, A. (2000) Revival of herbalism and its roots inmedicine. Journal of Agromedicine, 7, 21-29.

Duke, J.A. (1997) The Green Pharmacy. St. Martin’s Paperbacks,USA. 617 pp.

Graedon, J. and Graedon, T. (2002) The People’s Pharmacy:Guide to Home and Herbal Remedies. St. Martin’s Paperbacks,USA. 603 pp.

Keinath, A.P., Rushing, J.W. and Dufault, R.J. (1999) First reportof southern blight caused by Sclerotium rolfsii on St.-John’s-wort. Plant Disease, 83, 696.

Naranjo, S.E. and Stimac, J.L. (1985) Development, survival andreproduction of Geocoris punctipes (Hemiptera: Lygaeidae):Effects of feeding on soybean and associated weeds. Environ-mental Entomology, 14, 523-530.

International Symposium on Medicinal and Nutraceutical Plants(2007) Proceedings. Fort Valley State University, Macon,Georgia, March 2007.

SAS Institute (2005) SAS Software Release 8.2 (TS02M0). Cary,NC, USA.

Simmons, A.M., McCutcheon, G.S., Default, R.J., Hassell, R.L.and Rushing, J.W. (2000) Bemisia argentifolii (Homoptera:Aleyrodidae) attacking species of medicinal herbal plants.Annals of the Entomological Society of America, 93, 856-861.

World Health Organization (2005) Regional consultation ondevelopment of traditional medicine in the South East AsiaRegion, Pyongyang, DPR Korea. www.searo.who.int/LinkFiles/Meetings_document17.pdf. (Accessed 5 October, 2007)

Accepted September 19, 2007

arthropods associated with medicinal plants in coastal south carolina

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