the outer epidermal cell walls (Kaufman et al. 1971) and possible toxic ..... of horsetail insects: Brian Brown, Shawn Clark, Andy Ham- ilton, Pierre Jolivet, Andrei ...
Insect Herbivores of
Horsetaıls Bionomics, Dispersal, and Co-evolution GEORGE POINAR, JR.
KEY WORDS: Tortricidae, Chrysomelidae, Curculionidae, Tenthridinidae
he genus Equisetum L. (Equisetales: Equisetaceae), which is the sole remaining genus of the previously diverse order Equisetales, is native to all regions of the world except Australia, New Zealand, and Antarctica. The genus has been divided into the subgenus Equisetum L., or horsetails proper, and the subgenus Hippochaete (Milde) Baker, better known as scouring rushes (Hauke 1963, 1974). Since all reports of insect herbivory on Equisetum except one are thus far restricted to the eight species in the subgenus Equisetum (E. arvense L., E. bogotense H.B. K., E. diffusum D. Don, E. fluviatile L., E. palustre L., E. pratense Ehrh., E. sylvaticum L., and E. telmateia Ehrh.), further discussion will be limited to members of this group. Species in the subgenus Equisetum have separate vegetative (sterile) (Fig. 1) and reproductive (fertile) plants and all cases of insect herbivory appear to
American Entomologist • Volume 60, Number 4
be limited to the vegetative shoots or rhizomes (tubers) of the sterile plants. The Equisetales date back to the Upper Devonian, apparently arising as an offshoot from giant arborescent Calamites that reached 30 m in height, formed an understory in Carboniferous coal swamps, and became extinct in the Lower Permian (Stewart and Rothwell, 1993). Various equisetal fossils are known, but the earliest lineages that can be assigned to Equisetum appear in the Triassic and have been described under the generic name Equisetites. One of the earliest species placed in this genus was the Upper Triassic E. munsteri Sternberg, 1853. While it was originally described from Germany (Andrews 1970), ABOVE: Fig. 1. A colony of Equisetum arvense growing along the edge of a coastal forest in Oregon. 235
Fig. 2. Second-stage larva of Dolerus napaeus feeding on E. telmateia in Oregon. Bar = 1.0 mm.
this species is known from additional Triassic localities in Europe and Greenland (Andrews 1970; Harris 1931; Taylor and Taylor 1993). The most studied and nearly cosmopolitan species of Equisetum is the field horsetail, E. arvense, which has adapted to a range of habitats outside its preference for damp, acidic soils. Once the underground rhizomes become established, the plants can be quite difficult to eradicate because they are resistant to many herbicides. This is why New Zealand and Australia are interested in controlling introduced field horsetail with biological agents and Paynter and Barton (2008) have made a survey of insects and fungi attacking E. arvense. Equisetum species are avoided by most insects, probably because of the abrasive silicates associated with the outer epidermal cell walls (Kaufman et al. 1971) and possible toxic compounds within the cell sap. However, some insects have formed obligate host associations with horsetails, while other insects are occasional feeders. A synopsis of these herbivores, with observations on their occurrence in Oregon, is presented below.
occasionally drier areas with undisturbed sod. In North America, at least four species feed on Equisetum arvense, namely D. similis (Norton), D. aprilis (Norton), D. napaeus (MacGillivray) and D. apricus (Norton). Of the 40 some European species in the genus, D. aericeps, D. bimaculatus, D. eversmanni, D. germanicus, D. gessneri, D. gilvipes, D. nicaeus, D. palustris, D. pratensis, D. pratorum, D. vestigialis, and D. yukonensis develop on Equisetum arvense, E. palustre, E. sylvaticum, and E. pratense (Ross 1931; Paynter and Barton 2008). In Western Oregon, D. napaeus, a species confined to the Pacific coast of North America, occurs on E. arvense and E. telmateia. Females captured on these species and maintained in captivity deposited eggs in the branches and stems with their saw-like ovipositor. The larvae fed externally, initially clasping the lateral edges of the branches and eating small holes (Fig. 2 ), then climbing to the tips of the branches and devouring them completely while working back toward the stem. The larvae are quite fragile and many died in captivity before completing their development. Pupation occurred in earthen compartments but the larvae did not form cocoons. The black adults of D. napaeus (Fig. 3) apparently sustain themselves on flower nectar and tree sap (Ross, 1931).
Horsetail Weevils: Grypus spp. (=Grypius) (Coleoptera: Curculionidae) (Fig. 4) As far as known, all members of this genus feed on horsetails. In Oregon, Grypus equiseti Fab. is the most common
Materials and Methods Various populations of Equisetum arvense and E. telmateia were examined in western Oregon over the past five years. Insects recovered from the vegetative plants were removed and maintained in deep Petri dishes in the laboratory with a daily supply of fresh horsetail plants until they matured or died. Photographs of the horsetail weevil and horsetail leaf beetle were taken from specimens in the Hatch Pacific Northwest Beetle Collection, now deposited in the Arthropod Collection at Oregon State University. All photographs were taken by the author with a Nikon SMZ-10 stereoscopic microscope.
Results Horsetail sawflies: Dolerus spp. (Hymenoptera: Tenthridinidae) Dolerus is a Holoarctic genus whose larvae typically develop on grasses, sedges, and rushes. Their favorite habitat is low, semi-swampy areas, wet prairies, and 236
Fig. 3. Adult Dolerus napaeus. Bar = 2.5 mm. American Entomologist • Winter 2014
Horsetail Leaf Beetle: Hippuriphila Foudras 1860 spp. (Coleoptera: Chrysomelidae)
Fig. 4. Horsetail weevil, Grypus equiseti from Oregon Bar = 1.9 mm.
species feeding on E. arvense. It is a medium-sized weevil, 5-8 mm in length, and covered with brown, white, and yellowish scales. There are five elongate tubercles capped with longish setae on the elytra. This weevil has a Holarctic distribution extending from the UK to Central Europe through Siberia into North America (Cawthra 1957a, b). In North America, its range extends from Canada down to New York and across the nation to the Pacific northwest, then down through California. It shares its territory with the Holarctic species G. brunnirostris. The five additional species of Grypus are G. mannerheimi Faust in Japan and Siberia, G. rugicollis Voss in China, G. kaschmirensis Voss in India, and G. leechi Cawthra in North America (Cawthra 1957b). Cawthra (1957a) studied Scottish populations of the weevil on E. arvense and since he could not induce the adults to fly, concluded that they mostly travel by walking. However, the elytra are not fused and the wings are well developed (Andrei Legalov, personal correspondence), so the adults can probably fly. The eggs are deposited in holes made in the stems by females with strongly pointed mandibles. After oviposition, the larvae develop inside the stems, eventually moving downwards as they feed. The final instars occur in the rhizomes, the pupae are formed in the soil, and the emerging adults feed on the horsetail stems, producing characteristic feeding scars. Grypus equiseti was recorded from field populations of both E. arvense and E. palustre in Scotland and could be induced to feed on E. pratense and feed and oviposit on E. sylvaticum in the laboratory (Cawthra 1957a, 1957b). It is interesting that a second weevil genus, also in the subfamily Erirhininae, contains at least one representative that develops on horsetails. The Eurasian Garous lutulentus (Gyllenhal) develops in the stems of water horsetail, E. fluviatile, in Poland (Gosik 2009). The other two hundred or so species of Garous Germar apparently feed on sedges (Cyperaceae), water lilies (Nymphaceae), and other aquatic plants (Gosik 2009). American Entomologist • Volume 60, Number 4
Three species of this small genus of leaf beetles occur in North America, Hippuriphila equiseti Beller and Hatch, H. mancula LeConte, and H. canadensis Brown. All of these appear to be restricted to E. arvense; however, the Palearctic species, H. modeeri (L.), feeds on both E. arvense and E. palustre. The two former species occur in Oregon, with H. equiseti (Fig. 5) being the most common (Hatch 1971). Other species occur around the world, with H. babai Chûjô (= H. ohnoi L. N. Medvedev) in Japan and Eastern Russia, and Hippuriphila catharinae (Jacoby) in Brazil. The adults of this genus range from 2–2.6 mm in length and tend to be shiny bronze-brown, with a smooth dorsum covered with minute punctures. The undersides are clothed with fairly long setae lying more or less flat. The males have the first protarsal segment enlarged for grasping the female (Hatch, 1971). The larvae develop inside stems of the sterile plants. Details on the various developmental stages were presented by Brown (1942). While very few observations have been made on their food plants, Brown (1942) felt that all species of Hippuriphila are probably dependent on horsetails for their survival.
Fig. 5. Horsetail leaf beetle, Hippuriphila equiseti from Washington. Bar = 0.8 mm. 237
Fig. 6. Larva of Sparganothis senecionana developing on E.arvense in Oregon. Bar = 3.2 mm.
Fig. 7. Adult Sparganothis senecionana reared from the larva in Fig. 6. Bar = 2.9 mm.
Horsetail Agromyzid Flies. Liriomyza spp. (Diptera: Agromyzidae)
range (Powell and Opler 2009 )(Fig. 7). The caterpillars webbed together adjacent branches of E. arvense and lived within the constructed cavity (Fig. 6). The pupa is also formed within the shelter and the newly emerged adult moth (Fig. 7) may rest on the branches for a few hours before dispersing. The Palearctic tortricid Loxoterma tiedemanniana (Zeller) develops in the stems of Equisetum (Paynter and Barton 2008). The European Rosy Rustic noctuid, Hydraecia micacea (Esper) develops on the tubers of Equisetum arvense and has a number of other unrelated host plants such as Rumex, Iris, and Plantago (Thompson and Nelson 2003). Paynter and Barton (2008) provide a list of additional polyphagous insects that have been found on Equisetum arvense, including the Asian flea beetle, Liprus punctatostriatus Motschulsky (Coleoptera: Chrysomelidae); the European noctuid, Xylena vetusta (Hübner); the Asian and European Hepialids, Endoclita excrescens (Butler) and Triodia sylvina (L.), respectively; the Palearctic sawfly, Ametastegia equiseti, (Fallén); the European cicadellids, Ophiolix paludosa (Boheman) and Notus flavipennis (Zetterstedt); and the widespread pink hisbiscus mealybug, Maconellicoccus hirsutus Green (Pseudococcidae).
Four species of Liriomyza are reported to mine the stems of E. arvense throughout the world. These include the European L. occipitalis Hendel and L. virgula Frey and the Holarctic L. virgo (Zetterstedt) and L. equiseti de Meijere, the latter being recently found in California (Lonsdale 2011; Robbins 1991; Meijere 1924). Liriomyza virgo also develops in E. fluviatile (Paynter and Barton 2008). The larvae mine the branches and stems, often causing them to blacken. Pupation occurs in the soil and there appears to be a single generation per year (Spencer 1972). There is no evidence that the above species that feed on Equisetum are specific to that plant genus, as most species of Liriomyza develop in angiosperms (Lonsdale 2011).
Horsetail Hemiptera. Several hemipterans have been observed feeding on Equisetum spp. These include the Nearctic leafhopper Macrosteles borealis (Dorst) in the Yukon feeding on Equisetum spp. and the Palearctic species M. frontalis feeding on E. palustre (Hamilton 1997; Nickel and Remane 2002). The aphid Macrosiphon ( =Sitobion) equiseti (Holman), considered a European species introduced into Canada, Aphis equiseticola Ossiannilsson (1964), and Anoecia equiseti Halbert (Jensen and Holman 2000; Halbert 1991) appear to be monophagous on horsetails. The latter species was recovered from the rhizomes of Equisetum laevigatum. The respectively Nearctic and Palaearctic planthoppers Paraliburnia kilmani (Van Duzee) and Javesella stali (Metcalf) have also been recovered from horsetails (Wilson et al. 1994; Nickel and Remane 2002).
Polyphagous insects occasionally developing on Equisetum. While most of the aforementioned insects are considered to be specialists on horsetail, some polyphagous insects can also complete their development on Equisetum. A tortricid moth larva of the genus Sparganothis was collected from E. arvense in Oregon (Fig. 6). The adults resemble S. senecionana (Walsingham 1879) (Lepidoptera: Tortricidae), which is a Nearctic species with a wide host 238
Discussion The herbivores of horsetails include monophagous species dependent on Equisetum spp. for their survival and polyphagous species that occasionally develop on these plants. The former group includes species of Coleoptera (Curculionidae, Chrysomelidae), Hymenoptera (sawflies), Hemiptera (Delphacidae, Cicadellidae, Aphidoidea) and Diptera (Agromyzidae). Based on the fossil record, it is reasonable to assume that the subgenus Equisetum evolved sometime in the Late Triassic (230 mya) in the northern portion of Pangaea, now roughly equivalent to the Holarctic region, when the land masses of North America, Europe and Asia north of the Himalayas were adjacent (Smith et al. 1994)(Fig. 8). The climate was warm and temperate at that time (Boucot et al. 2013). This lineage slowly spread further and eventually speciated into E. arvense, E. fluviatile, E. palustre, E. pratense, and E. sylvaticum, all of American Entomologist • Winter 2014
and Palaearctic could have simultaneously occurred in the Late Cretaceous when a western connection sporadically opened (Beringia) connecting Asia with North America. Dispersal could have continued during the Paleocene and Eocene over the De Geer and Thulean land bridges connecting Europe with Eastern North America (Lillegraven et al. 1979). The subgenus Equisetum did not reach Africa, suggesting that the southward migration from the north occurred Fig. 8. Putative positions of the continents in the Fig. 9. Putative positions of the continents in after Africa had separated Triassic (~230 mya), when the subgenus Equithe Jurassic (~160 mya), when the subgenus from South America (Smith setum (grey area on map) evolved and started Equisetum (grey area) spread southward and et al 1994)(Fig. 10). However, to disperse through the northern continents that entered South America. Map modified from later would become North America (NA) and Smith et al 1994. (NA= North America; EA the presence of Equisetum Eurasia (EA). Map modified from Smith et al = Eurasia; SA= South America; A = Africa; bogotense in South Ameri1994. (NA= North America; EA = Eurasia; SA= Au-Nz-etc.= Australia, New Zealand and other ca shows that the genus did South America; A = Africa; Au-Nz-etc.= Australia, Pacific lands) enter that continent, probaNew Zealand and other Pacific lands) bly during the Early Cretawhich presently have a Holarctic distribution. ceous, yet Grypus never reached Central or South America The southern movement of the subgenus from what (Blackwelder 1982), indicating that the weevils arrived would be the Holarctic region must have occurred some- only after Gondwana separated from Laurasia (Fig. 10). time in the mid-Jurassic (160 mya) before South AmeriThe presence of G. mannerheimi and G. equiseti in ca separated from North America, but after or while the Siberia suggests that Grypus may have dispersed over Australian plate was separating from South America the Bering Strait to reach Asia, where Equisetum tel(Fig. 9), which explains why Australia and New Zealand mateia could have served as host (Lillegraven et al. have no native Equisetum (only introduced species). In 1979). Equisetum telmateia is the only member of the South America, the subgenus Equisetum produced E. subgenus that occurs on three separate continents bogotense. In the northern hemisphere, dispersal eastward into Asia resulted in E. telmateia in the Middle East and E. diffusum in the Himalayas. It is possible that some of the monophagous Equisetum–insect associations noted above are ancient, dating back to the Jurassic soon after the appearance of Equisetum. One such association could have been with an early lineage of Grypus weevils. While weevils as a group date from the Jurassic, the family Curculionidae was already established by the Early Cretaceous (Legalov 2012). It is interesting that the dispersal of Equisetum throughout the North American–Eurasian land mass parallels the spread of Grypus (Fig. 10). Holarctic lineages of Grypus equiseti and G. brunnirostris, which are restricted to Fig. 10. Putative positions of the continents Fig. 11. Putative positions of the continents in hosts of the subgenus Equisetum, proba- in the Early Cretaceous (~120 mya), when lin- the Late Miocene (~10 mya), showing essenbly co-evolved as herbivores of one of the eages of the weevil Grypus (black) dispersed tially the present distribution of the subgenus over populations of the subgenus Equisetum Equisetum (grey) and the weevil genus Grypus host plants, especially E. arvense. After the separation of North Amer- (grey). Map modified from Smith et al 1994. (black). Map modified from Smith et al 1994. (NA= North America; EA = Eurasia; SA= South (NA= North America; EA = Eurasia; SA= South ica from Eurasia, interchange of both America; A = Africa; Au-Nz-etc.= Australia, New America; A = Africa; Au= Australia) plants and weevils between the Nearctic Zealand and other Pacific islands) American Entomologist • Volume 60, Number 4
(North America, Europe, and Asia). It could have served as a host plant to G. mannerheimi in Japan and Siberia, to G. rugicollis Voss that reached China, and to G. kaschmirensis Voss in Kashmir (Fig. 11). Dispersal into Kashmir is presumed to have occurred after India made contact with Eurasia sometime in the Eocene. A similar dispersal scenario could have occurred with species of the monophagous Holoarctic herbivores Dolerus and Hippuriphila. It is interesting that the separation of the genus Equisetum into the subgenera Equisetum and Hippochaete (Hauke 1963, 1974), which had in the past been regarded as separate genera by some, is recognized by all of the monophagous insect herbivores that feed on the above-ground portion of the sterile plants in the subgenus Equisetum. Only one insect, the aphid Anoecia equiseti, develops on a member of the subgenus Hippochaete (E. laevigatum), but it feeds on the rhizomes (Halbert 1991).
Acknowledgements The author would like to thank Roberta Poinar and Art Boucot for reviewing the manuscript and the following scientists for supplying information on the identification of horsetail insects: Brian Brown, Shawn Clark, Andy Hamilton, Pierre Jolivet, Andrei Legalov, Christopher Marshall, Gary Parsons, David Smith and David J. Voegtlin.
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