Spittlebugs associated with actinorhizal hostplants1,2

Vinton Thompson

Abstract: Actinorhizal plants are major hosts for many spittlebugs, particularly species of the genera Clastoptera andAphrophora. World host records indicate that at least 20 spittlebug species have primary associations with at least 17actinorhizal hosts in the genera Alnus, Casuarina, Ceanothus, Comptonia, Elaeagnus, and Myrica. The highlypolyphagic spittlebug, Philaenus spumarius (L.), has also been observed in association with Hippophaë and Coriaria.Several other spittlebugs have minor associations with actinorhizal hosts.

Key words: actinorhizal plant, spittlebug, host, nitrogen-fixing.

Résumé : Les plantes actinorhiziennes constituent des hôtes majeurs pour plusieurs insectes cracheurs (spittelebugs), enparticulier des espèces des genres Clastoptera et Aphrophora. Le registre mondial des hôtes indique qu’au moins 20espèces d’insectes cracheurs ont une association primaire avec au moins 17 hôtes actinorhiziens des genres Alnus,Casuarina, Ceanothus, Comptonia, Elaeagnus et Myrica. L’insecte cracheur fortement polyphagique, le Philaenusspumarius, a aussi été observé en association avec des espèces d’Hippophaë et de Coriaria. Plusieurs autres insectescracheurs ont des association mineures avec des hôtes actinorhiziens.

Mots clés : plante actinorhizienne, insecte cracheur (spittlebug), hôte, fixation de l’azote.

[Traduit par la Rédaction] Thompson 1390

Introduction

Spittlebugs (Homoptera: Cercopoidea) are common suck-ing insects that live on xylem sap. Many exhibit a preferencefor nitrogen-fixing host plants, probably because these hostsprovide a relatively abundant and reliable supply of xylem-borne organic nitrogen compounds (Thompson 1994). Actin-orhizal plants (Baker and Mullin 1992), which fix nitrogenthrough association with the root nodule symbiont Frankia,fit this pattern. Several actinorhizal spittlebug hosts, includ-ing species of Alnus, Casuarina, Ceanothus, Comptonia,Coriaria, Myrica, and Hippophaë, transport fixed nitrogenfrom root to shoot as organic nitrogen compounds (refer-ences in Baker and Parsons 1997; Thompson 1994). InMyrica gale L., for example, asparagine and glutamine dom-inate the xylem stream, with at least a dozen other amino ac-ids present, and total xylem amino acid concentration dropswhen nitrogen fixation is repressed by in situ oxygenation ofroot nodules (Baker et al. 1997).

At least one spittlebug, Philaenus spumarius (L.), keys onamino acids as a feeding cue and a xylem-feeding cousin,the leafhopper Homalodisca coagulata (Say), chooses hosts

with high xylem amino acid concentrations (references inThompson 1994). Perhaps not surprisingly then, a prelimi-nary study suggested that actinorhizal plants are dispropor-tionately common among spittlebug hosts and particularlysusceptible to spittlebugs of the genus Clastoptera (Thomp-son 1994). Thorough examination of the large and scatteredworld spittlebug host literature has confirmed this patternand revealed additional actinorhizal hosts. In this note I re-port all known spittlebug actinorhizal hosts and briefly char-acterize major patterns of association.

Spittlebugs on actinorhizal plants

Important spittlebug associates live on six of the 25 rec-ognized genera of actinorhizal plants: Alnus, Casuarina,Ceanothus, Comptonia, Elaeagnus, and Myrica (Table 1).Allowing for ambiguities of identification in both bugs andplants, at least 20 different spittlebug species have majoractinorhizal hosts and at least 17 species of actinorhizalplants have important spittlebug associates (primarily of thegenera Aphrophora and Clastoptera). These host associa-tions are not exclusive. Spittlebugs are typically polyphagicor oligophagic and most of the spittlebugs listed have alter-native hosts that are not actinorhizal. Nevertheless, the predi-lection for actinorhizal plants is striking, given the relativelysmall number of actinorhizal taxa available for colonization(Thompson 1994).

Spittlebugs of actinorhizal plants rarely pose economicproblems. There are two documented exceptions. Clasto-ptera undulata Uhler defoliated some Casuarina plantings inBermuda in the early 1960s (Bennett and Hughes 1963),perhaps a consequence of release from predators, since theinsects as well as the trees were apparently introduced ontothe island. In eastern North America, adult Aphrophora sara-

Can. J. Bot. 77: 1387–1390 (1999) © 1999 NRC Canada

1387

Received August 15, 1998.

V. Thompson. School of Science and Technology, RooseveltUniversity, 430 South Michigan Avenue, Chicago, IL 60605,U.S.A. e-mail: vthompso@roosevelt.edu

1This paper was presented at the 11th InternationalConference on Frankia and Actinorhizal Plants, June 7–11,1998, University of Illinois at Urbana–Champaign.

2This version of the manuscript was revised by the author inMay 1999 to accommodate new information appearing in aseries of papers by Komatsu (1997a, 1997b, 1997c) onJapanese species of the genus Aphrophora.

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togensis (Fitch) spittlebugs are a serious pest of Pinus resin-osa Aiton and Pinus banksiana Lamb. Although Aphrophorasaratogensis nymphs live on several dozen understory plants(none of them pines), they prefer the actinorhizal hostComptonia peregrina (L.) J.M. Coult., and the percentage of

Comptonia peregrina ground cover is a good predictor ofspittlebug damage (Wilson 1987).

The casuarinas are particularly interesting hosts. Whilethese trees are all native to tropical Asia, Australia, andneighboring islands (Bond 1983), most casuarina spittlebugs

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Actinorhizal host plant Spittlebug associate Geographical area Reference

Alnus firma Siebold & Zucc. Aphrophora obliqua Uhlera Japan Komatsu 1997bAlnus glutinosa (L.) Gaertn. Aphrophora alni (Fallén)a Sweden Ossiannilsson 1950

Aphrophora alnia North Americab Hamilton 1982Alnus incana (L.) Moench. Aphrophora alnia Finland Nuorteva 1952Alnus japonica (Thunb.) Steud. Aphrophora major Ulhera Japan Komatsu 1997c

Aphrophora rugosa Matsumuraa Japan Komatsu 1997cAlnus rugosa (Du Roi) Spreng. Clastoptera obtusa (Say) North America Hamilton 1982

Aphrophora alnia Michigan Wheeler 1992Alnus serrulata (Aiton) Willd. Clastoptera obtusa North Carolina Thompson and Mohd-Saleh 1995Alnus tenuifolia Nutt. Clastoptera obtusa North America Johnson and Lyon 1991Alnus sp. Aphrophora ishidae Matsumuraa Japan Matsumura 1904

Clastoptera elongata Doeringa Colorado Smithsonian recordCasuarina cunninghamiana Miq. Clastoptera laenata Fowler Costa Ricab Thompson and Mohd-Saleh 1995

Clastoptera undulata Uhler Bermudab Bennett and Hughes 1963Clastoptera undulata Floridab Mead and Bennett 1987

Casuarina equisetifolia L. Clastoptera funesta Stål Jamaicab Bennett and Hughes 1963C. nr. paradoxa (2 spp.) Trinidadb Bennett 1965Clastoptera undulata Bermudab Bennett and Hughes 1963Clastoptera undulata Cubab Bennett and Hughes 1963Clastoptera undulata Floridab Mead and Bennett 1987Clastoptera sp. Hondurasb V. Thompson (unpublished data)Clovia quadridens (Walker) India William and Ananthasubramanian 1991

Casuarina glauca Sieber ex Spreng. Clastoptera undulata Floridab Mead and Bennett 1987Casuarina stricta Miq. Clastoptera undulata Bermudab Bennett and Hughes 1963

Clastoptera undulata Cubab Brunner et al. 1945Clastoptera undulata Floridab Mead and Bennett 1987

Casuarina sp. Clastoptera flavidorsa Metcalf& Bruner

Jamaicab Bennett and Hughes 1963

Clastoptera undulata Trinidadb Urich 1913Philagra parva Donovan Australia Evans 1966

Ceanothus griseus (Trel.) McMinn Clastoptera sp. North America Fasoranti 1984Ceanothus sanguineous Pursh Clastoptera ovata Doering North America Hamilton 1982Ceanothus velutinus Douglas ex Hook. Clastoptera ovata North America Hamilton 1982Comptonia peregrina (L.) J.M. Coult. Aphrophora saratogensis (Fitch)c North America Wilson 1987Elaeagnus sp. Aphrophora ishidaea Japan Komatsu 1997c

Aphrophora majora Japan Komatsu 1997cMyrica gale L. Aphrophora alnid Great Britain Lyle 1919

Aphrophora alnid Ireland Halbert 1935Aphrophora alnid Norway Holgersen 1944Aphrophora major Great Britain Dolling 1991Clastoptera obtusa North America Hamilton 1982Clastoptera saintcyri Provancher North America Hamilton 1982Lepyronia coleoptrata (L.)d Finland Halkka et al. 1977Philaenus spumarius (L.)d Ireland Nixon et al. 1975

Note: The table includes only cases in which the host plant is the preferred host or one of a few preferred hosts for the spittlebug associate. Forgeographic areas with multiple possible citations per spittlebug species (e.g., Aphrophora alni in continental Europe) a single representative citation hasbeen chosen. With the exception of Aphrophora alni in North America (and probably Clastoptera undulata in Bermuda) the spittlebugs are native to theareas given. This table supersedes Table 2 of Thompson (1994).

aOnly adult spittlebugs are recorded on the host (there are no nymphal host records for Aphrophora obliqua, Aphrophora obtusa, or Clastopteraelongata).

bHost plant is introduced.cOnly nymphal spittlebugs live on the host.dPolyphage with occasional actinorhizal host preference (nymphs only for Aphrophora alni).

Table 1. Actinorhizal host plants with spittlebug associates.

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belong to the exclusively New World genus Clastoptera(Table 1). Clastoptera species occur widely on casuarinas inCentral America, Bermuda, Florida, and many Caribbean is-lands. The attraction is so strong that several of these abun-dant Clastoptera species are known only from casuarinas.They have no recorded native hosts. Something in Casua-rina physiology exerts a powerful draw, probably root nod-ule nitrogen fixation accompanied by xylem transport oforganic nitrogen compounds.

Other spittlebug species live on actinorhizal plants sporad-ically or as one of many hosts. For example, the highlypolyphagic north temperate spittlebug Philaenus spumariusprefers dicot herbs, particularly forage legumes, but occurson hundreds of hosts including several actinorhizal plants.In Illinois, Philaenus spumarius adults have been observedfeeding on Alnus rugosa (Du Roi) Spreng. leaves adjacentto Clastoptera obtusa (Say) nymphs (V. Thompson, unpub-lished data). In Europe, Philaenus spumarius feeds on Alnusincana (L.) Moench, Alnus glutinosa (L.) Gaertn., andM. gale (Ossiannilsson 1950; Halkka et al. 1967, 1977). Atone Irish site, M. gale is the primary Philaenus spumariushost (Nixon et al. 1975). At another European site it hasbeen observed “in truly immense numbers” on Hippophaërhamnoides L. (Frey-Gessner 1865). In New Zealand, wherePhilaenus spumarius is a recent introduction, a Coriariaspecies (Hamilton and Morales 1992) may represent the onlynative host recorded among a number of Eurasian exotics.

Aphrophora quadrinotata (Say), an eastern North Ameri-can polyphage, has been taken on Alnus rugosa (Hamilton1982) and Ceanothus (Froeschner 1946). Alders are its mostcommon host among Michigan trees (Hanna 1970). In Ja-pan, adults of the polyphagic species Aphrophora intermediaUlher, Aphrophora obtusa Matsumura, and Aphrophora vit-tata Matsumara have been taken on Alnus japonica (Thunb.)Steud. (Komatsu 1997a, 1997b). Clastoptera lineatocollisStål, which generally feeds on Compositae (Hamilton 1982),also feeds on alders in California (Wheeler 1952). In Hondu-ras, Aeneolamia postica (Walker), a native pest spittlebuglimited almost exclusively to grasses (V. Thompson, unpub-lished data), has been taken once in a Casuarina nursery,one of only eight cases in which it has been associated witha nonmonocot host of any kind (V. Thompson, unpublisheddata). In Britain, Cercopis vulnerata Rossi adults have beentaken on alders (Imms 1951), one of many adult hosts.

The abundance of spittlebugs on several actinorhizal hostssuggests that continued reconnaissance of actinorhizal plantswill engender novel spittlebug host records. Conversely, afew spittlebug hosts may prove to be hitherto unrecognizedactinorhizal plants.

Note added in proof: Krivolutskaya (1997, Table 3) re-ports that alders, species unspecified, are major hosts oftwo additional spittlebugs in the Kuril Islands north of Ja-pan: Aphrophora similis Lethierry and Sinophora submaculaMetcalf & Horton.

Acknowledgments

L.L. Deitz facilitated access to the Metcalf Archive atNorth Carolina State University, an invaluable resource forhistorical Homoptera host studies. An anonymous reviewermade helpful comments.

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