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Shorthouse, J. D. 2010. Galls Induced by Cynipid Wasps of the Genus Diplolepis (Hymenoptera: Cynipidae) on the Roses of Canada’s Grasslands. In Arthropods of Canadian Grasslands (Volume 1): Ecology and Interactions in Grassland Habitats. Edited by J. D. Shorthouse and K. D. Floate. Biological Survey of Canada. pp. 251-279. © 2010 Biological Survey of Canada. ISBN 978-0-9689321-4-8 doi:10.3752/9780968932148.ch12

Chapter 12Galls Induced by Cynipid Wasps of the

Genus Diplolepis (Hymenoptera: Cynipidae) on the Roses of Canada’s Grasslands

Joseph D. ShorthouseDepartment of Biology, Laurentian University

Sudbury, Ontario, Canada P3E 2C6

Abstract. Thirteen species of cynipid wasps of the genus Diplolepis induce structurally distinct galls on the three species of wild roses found on the grasslands of western Canada. Three species of Diplolepis gall the short rose, Rosa arkansana, in the Mixed Grassland and Moist Mixed Grassland ecoregions of southern Alberta and Saskatchewan, and eight species gall the common prairie rose, R. woodsii, throughout the prairie grasslands. Five species of Diplolepis gall the larger rose, R. acicularis, in more shaded regions such as the Aspen Parkland Ecoregion. This chapter outlines the life history strategy of Diplolepis and the manner by which these insects are well adapted to grassland conditions. Also described are the galls of each species, along with the component communities associated with them.

Résumé. Treize espèces de cynipidés du genre Diplolepis engendrent la formation de galles structurellement distinctes sur trois espèces de rosiers indigènes des prairies de l’ouest du Canada. Trois de ces espèces de guêpes produisent des galles sur le rosier des prairies (Rosa arkansana) dans les écorégions des prairies mixes et des prairies mixtes humides du sud de l’Alberta et de la Saskatchewan, et huit autres s’attaquent au rosier de Woods (R. woodsii) dans l’ensemble de la région des prairies. Cinq espèces de Diplolepis engendrent des galles sur le rosier aciculaire (R. acicularis) dans les régions plus ombragées comme l’écorégion de la forêt-parc à trembles. Ce chapitre décrit les stratégies de survie des Diplolepis et la façon donc ces insectes se sont adaptés aux conditions caractéristiques des prairies. Il décrit également les galles produites par chacune de ces espèces, ainsi que les communautés qui leur sont associées.

Introduction

Grasslands of the three prairie provinces and valleys of the southern mountain regions of British Columbia support a diverse assemblage of flora ranging from lichens and mosses to grasses, forbs, shrubs, and trees. All of the more advanced plants are fed upon by numerous species of insects and, as the plants become more structurally complex, the kinds of insects increase, along with the roles they play and the niches they occupy (Strong et al. 1984). Hence, forbs have more species of associated insects than do grasses, shrubs have more than forbs, and trees have more than shrubs (Leather 1986). As a result, the kinds of feeding relationships that phytophagous insects have with their host shrubs are more complex than the relationships they have with grasses and forbs. Studying insects on shrubs has many advantages over studying them on trees. Shrubs are usually smaller than trees and the entire canopy can be sampled, whereas one risks life and limb trying to sample insects in the upper canopy of trees.

Dozens of species of shrubs live in the grasslands of Canada’s prairies and British Columbia (Scoggan 1957; Looman and Best 1987; Moss and Packer 1983; Johnson et

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al. 1995; Brayshaw 1996; Harms 2003). The greatest diversity of shrubs on the prairies, especially in the Mixed Grassland Ecoregion in the south, occurs in areas with more moisture such as at the bottom of coulees; near creeks, potholes, and sloughs; and in the flood plains of rivers. Among the most common shrubs in the grasslands are wild roses. Three species of roses are found on the grasslands of the prairie provinces and one in the Okanagan grasslands. These species are host to insects in a variety of guilds, including leaf chewers, leaf miners, fluid feeders, stem borers, pollinators, and gall inducers (Shorthouse 2003).

Plant galls and the insects that induce them represent the most complex insect–plant relationship found on grassland shrubs. Galls are atypical plant growths stimulated by the feeding activities of a select group of insects and mites that are considered by many as the most specialized arthropods in the natural world (see references in Meyer and Maresquelle 1983; Meyer 1987; Shorthouse and Rohfritsch 1992). Rather than chewing on plant tissues externally or internally and walking or tunnelling to new sites when food at one site has been exhausted, gallers are sessile and manipulate the growth and physiology of their host plants such that food comes to them. Gallers stimulate their host plants into providing them with highly nutritious plant cells normally not found in the attacked organ (Bronner 1992). New nutritive cells are continually produced as the older cells are consumed. The immatures of gallers are surrounded by these unique cells that not only provide food, but also shelter that protects them from the elements and from predators (Stone and Schönrogge 2003).

Seven orders of insects have evolved the ability to induce galls. The most species-rich families of gallers are the Cecidomyiidae (midges) (Diptera) and the Cynipidae (cynipid wasps) (Hymenoptera) (Dreger-Jauffret and Shorthouse 1992). There are about 1,400 species of cynipids in the world (Csóka et al. 2005), with most found on oaks (Quercus spp.) and roses (Rosa spp.). All cynipid galls on roses are induced by wasps of the genus Diplolepis (= Rhodites of older literature) (Beutenmüller 1907). Amazingly, each species of cynipid induces distinct, anatomically complex galls (Stone and Cook 1998; Ronquist and Liljeblad 2001; Stone et al. 2002; Stone and Schönrogge 2003; Csóka et al. 2005) that develop from undifferentiated tissues of vegetative buds or immature stems. Galls are phenotypic and physiological extensions of the gall inducers (Dawkins 1982; Crespi and Worobey 1998; Stone and Cook 1998), with the insects, not the plants, in control of plant development.

An important aspect in the biology of cynipids is that their galls attract many other insects that feed either on the tissues of the gall or on the larvae of the inducers. Numerous species of parasitoids have discovered the defenceless larvae of inducers within galls and have become major mortality factors (Brooks and Shorthouse 1998; Csóka et al. 2005). In addition to parasitoids, most species of Diplolepis are also attacked by inquiline cynipids of the genus Periclistus that kill the inducers and then alter the anatomy of inhabited galls (Shorthouse 1998). Each species of Diplolepis appears to have a characteristic assemblage of inhabitants associated with its galls. The purpose of this chapter is to describe the life history strategy of cynipids found on wild roses of the grasslands of Canada, illustrate the differences in their galls, and compare the communities of insect inhabitants associated with them.

Roses of Canada’s Grasslands

Roses are perennial woody shrubs in the family Rosaceae and are among the most successful and widespread shrubs in the northern hemisphere. They have an important ecological role in most terrestrial ecosystems south of the treeline and influence the biology

Galls of cynipid wasps (Diplolepis) on grassland roses 253

of many animals, both invertebrates and vertebrates (Hatler 1972). The approximately 140 species of roses in the world form 10 taxonomic sections (Wissemann 2003). Wild roses are notoriously difficult to identify because of their variability and the ease with which they hybridize and yield fertile offspring (Lewis 1959). There are about 22 species of wild roses in North America (Erlanson MacFarlane 1966; Joly et al. 2006). Of the 12 species of endemic roses in Canada (Breitung 1952), only Rosa arkansana Porter, R. woodsii Lindley, and R. acicularis Lindley (section Cinnamomeae) (Wissemann 2003) occur on the grasslands of western Canada (Harms 1974; Moss and Packer 1983).

Fig. 1. Schematic drawing of a typical prairie wild rose. Note that the shoot to the left is several years old and has side branches. The middle shoot is a sucker shoot and the shoot to the right is an adventitious shoot. All shoots are joined by rhizomes.


Wild roses are deciduous woody shrubs with erect stems (Fig. 1). They are ephemeral and long-lived and have many branches arising from the main stem, giving them a bushy appearance. The roots of some roses extend downward for 2 m, making them well adapted to dry grasslands. The upper parts of the root system send out numerous underground stems called rhizomes (Fig. 1) from which adventitious shoots develop when the above-ground parts of the shrub are eaten or killed by fire (Calmes and Zasada 1982). Roses quickly regrow from the rhizomes, even if large herbivores remove all above-ground parts. Increased bushiness, which is an adaptation to herbivore damage (Paige and Whitham 1987),

Figs. 2–7. Wild roses of Canada’s grasslands and features of Diplolepis. Fig. 2. Rosa arkansana in early July near Coaldale, Alberta. Fig. 3. Rosa woodsii in early July in the Cypress Hills of southeastern Alberta. Fig. 4. Rosa acicularis at the forest edge in central Alberta. Fig. 5. Habitus of a female D. spinosa. Note the hypopygium extending from the ventral side of the abdomen. Fig. 6. Habitus of a male D. spinosa. Fig. 7. Full grown larva of D. spinosa. Photographs by the author.

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leads to rose patches altering their microhabitats. Bushiness reduces wind, which benefits Diplolepis adults searching for oviposition sites. In addition, blowing snow accumulates in bushy rose patches, providing abscised leaf gallers with the relative warmth of a subnivean habitat (Williams et al. 2002).

Stems that arise from seeds or underground rhizomes are called sucker shoots. Sucker shoots have no side branches (Fig. 1) and do not flower or branch for two to three years. The first new tissues on a wild rose to appear in the spring are vegetative buds. These buds occur near the distal ends of branches and are important oviposition sites for most species of Diplolepis (Shorthouse et al. 2005). Rose leaves are compound and odd-pinnate and each is composed of three, five, seven, or nine leaflets (Fig. 1).

Rosa arkansana PorterRosa arkansana is an erect shrub with thin, red-brown stems with little branching. The stems usually die down to the soil level annually (Harms 1974). This rose grows singly and not in clones as do R. woodsii and R. acicularis. Commonly called the wild prairie rose, R. arkansana is the shortest of the three prairie roses (Fig. 2) with erect stems up to 45 cm in height. It is common in the Mixed Grassland and Moist Mixed Grassland ecoregions of southern Alberta, Saskatchewan, and southwestern Manitoba on dry soil in disturbed sites such as along roadsides.

Rosa woodsii LindleyRosa woodsii is a much-branched shrub, 0.5–1 m high, with woody, brownish-red main stems (Fig. 3) (Harms 1974). Branches often turn grayish when the shrubs mature. They are armed to the apex of the floral branches with scattered prickles longer than 5 mm that are straight or slightly curved with enlarged bases. Commonly called Wood’s rose or the common wild rose, it is found throughout the grasslands of western Canada on open, dry, grassy prairies (Fig. 3); sand hills; and slopes of coulees and river valleys.

Rosa acicularis LindleyRosa acicularis commonly grows to 1 m or more in height. Its stems and branches are usually green, occasionally somewhat reddish, and covered with slender, straight prickles (Harms 1974). Commonly known as prickly rose, R. acicularis is the most widely distributed rose in the world. It is circumpolar and thrives in boreal forests in all Canadian provinces east of New Brunswick south of the treeline (Lewis 1959). This rose is also found in the northern part of the prairie grasslands in association with taller vegetation of the Aspen Parkland Ecoregion (Fig. 4).

Biology of Diplolepis and Their Galls and Inhabitants

Cynipids of the genus Diplolepis Geoffroy are Holarctic in distribution, but no single species is found naturally on both continents. Approximately 44 species occur worldwide, with 32 endemic species in North America (Burks 1979; Csóka et al. 2005). Thirteen species of Diplolepis induce galls on roses of the grasslands of Canada (Table 1). Each species of rose on the prairies (Moss and Packer 1983) and in British Columbia (Brayshaw 1996) is attacked by one or more species of Diplolepis (Table 1).

Adult Diplolepis are inconspicuous, poor-flying wasps best collected by harvesting their mature galls in the autumn or the spring and storing them in glass jars at room temperature. Adults are removed with a moistened brush when they exit the galls. These wasps are

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. Shorthouse

Table 1. Species of Diplolepis and their galls found on the wild roses of Canada’s grasslands.

Species Host Organ Attacked Chambers Season Gall Initiated

R. acicularis

R. woodsii

R. arkansana Leaves Stems Adventitious

Shoots Single Multi Spring Mid-Summer

Late Summer

D. polita (Ashmead) X X X X

D. bicolor (Harris) X X X X X

D. rosaefolii (Cockerell) X X X X X X X

D. nebulosa (Bassett) X X X X

D. ignota (Osten Sacken) X X X X X X

D. gracilis (Ashmead) X X X X X

D. bassetti (Beutenmuller) X X X X

D. variabilis (Bassett) X X X X X X

D. fusiformans (Ashmead) X X X X

D. nodulosa (Beutenmuller) X X X X

D. triforma Shorthouse and Ritchie

X X X X

D. spinosa (Ashmead) X X X X

D. radicum (Osten Sacken) X X X X X


distinguished from other Hymenoptera by their rather short and globular bodies (Figs. 5 and 6) that vary in length from 3 to 6 mm. The mesosoma (thorax and first segment of the abdomen) is short and strongly arched dorsally, giving Diplolepis a hunchbacked appearance in lateral view (Figs. 5 and 6). The metasoma is laterally compressed (gaster or abdomen of older literature), and sternites at the rear of the metasoma are fused to form a hypopygium shaped like a plow (Fig. 5; also see Fig. 8). The colouration of these wasps varies from entirely orange, to reddish-brown and black, to entirely black. Males are usually black.

Late-instar larvae of Diplolepis are hymenopteriform, apodous, cream-coloured, and have a weakly defined head (Fig. 7). Larvae of some species are comma-shaped and tapered toward the caudal end, whereas larvae of other species are more cylindrical. Comma-shaped larvae, common to leaf galls, wiggle actively when their chambers are opened, whereas the cylindrical larvae, common to stem galls, are nearly motionless.

Life CycleAll Diplolepis have one generation per year. Their entire life cycle, other than 10–15 days in the egg stage and about 5–12 days as an adult, is spent as immatures inside the chambers of their galls. The appearance of adults in the spring is synchronized with the availability of host tissues at a specific stage for oviposition and gall initiation.

Important events in the life cycle of Diplolepis are shown in Figs. 8–15. Adults chew an exit tunnel from their larval chambers to the outside in the spring or summer when bud or stem tissues are suitable for oviposition. Some species oviposit in the first vegetative buds to appear in the spring, whereas others lay eggs in axillary buds later in the season, in the sides of new current-year stems, or at the tips of adventitious shoots (Table 1). Females of several species sit in an inverted manner on young leaf buds (Fig. 8) and thrust their ovipositors between the developing leaflets to deposit eggs (Fig. 9). Eggs are attached to one or two plant cells by a tiny nipple at the tip of the egg (Bronner 1985; Shorthouse 1993, 1998; LeBlanc and Lacroix 2001). Proliferation of gall cells begins before the eggs hatch. Once the larvae start feeding, they are quickly surrounded by gall cells (Leggo and Shorthouse 2006; Sliva and Shorthouse 2006). As is the case with all cynipids, galls of Diplolepis undergo three phases of development known as initiation, growth, and maturation (Rohfritsch 1992; Brooks and Shorthouse 1998; Sliva and Shorthouse 2006).

Stem galls, such as those of D. spinosa (Ashmead), are first seen in the field when they are about twice the diameter of normal shoot tips (Fig. 10). Galls reach their maximum size by the end of the growth phase, which is near the end of June. Larvae are still small at this stage and eat little, but a thick layer of gall cells surrounds each chamber (Fig. 11). Galls enter the maturation phase near the middle of June and the larvae begin to feed and grow rapidly. All nutritive cells are consumed by the time the larvae are full grown (Fig. 12) and finish eating.

Both larvae and galls are mature by mid-August when the larvae enter an overwintering pre-pupa stage (Shorthouse and Leggo 2002). The pre-pupa is a transition stage between a larva and a pupa in which eyes (Fig. 13) and reproductive organs begin to form (Shorthouse and Leggo 2002). The pre-pupae turn into white pupae (Fig. 14) the following season. Pupae darken by early May (Fig. 15) when the temperatures rise above 12 °C. Adults chew exit tunnels from their chambers to the outside (Fig. 15) and fly off in search of mates or oviposition sites.

Gall Communities Galls induced by Diplolepis, like those of most other cynipids (Stone et al. 2002; Csóka et al. 2005), support species-rich communities of inhabitants. The sessile larval inducers


Figs. 8–15. Stages in the life history of Diplolepis. Fig. 8. Diplolepis bicolor ovipositing in a leaf bud of Rosa woodsii. Fig. 9. Eggs of D. spinosa deposited at the base of an apical meristem. Fig. 10. Early instar larvae of D. spinosa in an immature gall in the early growth phase. Fig. 11. Early instar larva of D. spinosa in an immature gall in the late growth phase. Fig. 12. Maturing larvae of D. spinosa in a mature gall in the late maturation phase. Fig. 13. Pre-pupa of D. spinosa in September in preparation for overwintering. Fig. 14. Pupal stage of D. spinosa in mid-May prior to darkening. Fig. 15. Pupa of D. spinosa (left) ready to emerge and an emerged adult (right) ready to chew an exit channel to the outside. Photographs by the author.

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within the chambers of grassland rose galls are attacked by 11 genera of parasitoids (Table 2), and numerous species have developed a close association with rose galls. Parasitoids have a lifestyle that is intermediate between that of predator and parasite (Hawkins and Goeden 1984; Waage and Greathead 1986; Godfray 1994). Whereas predacious insects kill their prey before consuming it and ingest several individuals over a lifetime, parasitoids eat only one host and often keep it alive long after they begin to feed (Godfray 1994).

Rose galls of all Diplolepis species, except those of D. triforma, are attacked by inquilines in the genus Periclistus. These inquilines are cynipid wasps that are unable to induce galls of their own and instead have larvae that make gall-like chambers within the galls of Diplolepis (Brooks and Shorthouse 1998; Shorthouse 1998). Periclistus are obligatorily dependent on Diplolepis and their galls for providing the gall tissues upon which they feed. Inquilines increase the insect biomass within galls and provide a food source for further trophic levels (Shorthouse 1973, 1993, 1998; Brooks and Shorthouse 1998).

Root (1973) designated all the members of a small part of an ecosystem, such as those associated with a tree or small pond, as compound communities. However, compound communities are often too complex to monitor the roles of all community members, and so smaller subunits, called component communities (Claridge 1987), have been identified. All inhabitants associated with a population of galls induced by the same species of Diplolepis in a given geographical region are considered a component community. Such communities have been the subject of many ecological studies (e.g., Askew 1984; Askew and Shaw 1986; Wiebies-Rijks and Shorthouse 1992; Stone et al. 2002; Price et al. 2004; Csóka et al. 2005). Gall communities can be monitored throughout the season by dissecting maturing galls in the laboratory and identifying and counting the larval inhabitants (Shorthouse 1973; Randolph 2005).

Most of the parasitoids associated with Diplolepis galls have short ovipositors and can reach the inducer’s chamber only when both the gall and the inducer larva are small. This

Table 2. Common inhabitants associated with galls of Diplolepis on wild roses.

Inducer Inquiline Parasitoids

Diplolepis Periclistus Eurytoma (Eurytomidae)

Orthopelma (Ichneumonidae)

Torymus (Torymidae)

Glyphomerus stigma (Torymidae)

Aprostocetus (Eulophidae)

Chrysocharis (Eulophidae)

Eupelmus vesicularis (Eupelmidae)

Pteromalus (Pteromalidae)

Tenuipetiolus (Eurytomidae)

Ormyrus rosae (Ormyridae)

Caenacis (Pteromalidae)


means that if the parasitoid killed an immature inducer, there would not be enough food for the parasitoid to mature. The solution is for the parasitoid to feed on the host for a period without inflicting serious damage, thereby allowing the parasitoid to continue feeding and the gall to grow.

Each species of gall inhabitant, excluding the inducers, has an optimum period for oviposition. The general pattern is for gall communities to become more complex as the season progresses until early fall when all inhabitants are mature and ready to overwinter. The complement of inhabitants within populations of galls by the beginning of winter is the assemblage present the following season (see Fig. 44 for examples) to re-establish the component community.

Most of the parasitoids associated with galls of Diplolepis are in the superfamily Chalcidoidea. Species attacking the inhabitants of rose galls in this superfamily belong to the families Eurytomidae, Torymidae, Eulophidae, Eupelmidae, Pteromalidae, and Ormyridae (Table 2). Orthopelma (family Ichneumonidae) are also associated with Diplolepis galls. Details of each family with drawings of typical adults are given in Gauld and Bolton (1988). Most parasitoids overwinter in the galls and the adults exit after current-season galls are initiated. Parasitoids oviposit in immature or maturing galls and remain in the larval stage all summer. Maturing larvae of each parasitoid have distinguishing features that allow them to be identified to genus (Shorthouse 1973; Randolph 2005). Larvae of some parasitoids, such as Eurytoma, Torymus, and Pteromalus, pupate and exit galls in the year of gall induction (Table 3). It is not known whether these inhabitants, called fall emergents, oviposit in galls of other Diplolepis that mature later in the summer or attack non-gall hosts.

Survey of Diplolepis Galls on Canada’s Grasslands

Diplolepis polita (Ashmead) (Figs. 16 and 17)Diplolepis polita was first described from galls collected in the United States by Ashmead (1890). This species is now known to occur from the coast of British Columbia north to central Alaska and the Yukon, east to western Quebec, and from central Ontario north to James Bay. It is common throughout the Aspen Parkland Ecoregion from Alberta to Manitoba on roses in partially shaded areas at the edge of forests (Fig. 4).

Table 3. Percentage of inhabitants associated with Diplolepis leaf galls found in south-central Saskatchewan exiting galls in the fall of the year of gall initiation.

Species Eurytoma Torymus Pteromalus

D. polita 47.2 43.9 2.8

D. bicolor 38.9 4.5 1.0

D. rosaefolii 31.2 1.0 55.2

D. nebulosa 16.6 26.4 0

D. ignota 1.9 0 0

D. gracilis 12.5 0 0


Mature galls are spherical, averaging 3.5–4.5 mm in diameter, clothed with weak spines, and found on the adaxial (upper) surface of leaves (Fig. 16). They are single-chambered (Fig. 17) with thin walls and usually grow in clusters, several galls per leaflet. Galls are found both on the sucker shoot and on multi-year roses. Galls always abscise in late summer. Immature galls in shaded areas are usually greenish-yellow, whereas those growing in areas open to the sun are often bright red. All turn light brown when dry.

Galls of D. polita are found only on R. acicularis east of the Rockies, never on R. woodsii growing in open areas of the southern prairies. However, they are found on R. woodsii in more shaded areas in the Okanagan in British Columbia. A large population was found on R. arkansana near the top of the Cypress Hills in Alberta (Shorthouse 1991).

A large population of galls from within Prince Albert National Park in Saskatchewan illustrates the composition of a typical component community (Fig. 44A). Only 4% of the inhabitants were inducers by fall, 29% were Periclistus, and the rest (67%) were parasitoids. Periclistus (average of 5.4 per gall; Table 4) were commonly found in about 70% of all maturing galls and 12% of mature galls (Table 5). The most common parasitoids were Eurytoma sp. and Pteromalus sp. (Fig. 44A). About half of the Eurytoma sp. and half of the Torymus sp. matured and exited galls by the end of the season (Table 3).

Diplolepis bicolor (Harris) (Figs. 18 and 19)Diplolepis bicolor was first described from galls collected at an unidentified locality in the northeastern United States (Harris 1841). It has a wider distribution in southern Canada than D. polita, being found from British Columbia to Nova Scotia but not in Newfoundland. Earlier workers have recorded the gall from Calgary (Weld 1926) to Alabama (Thompson 1915).

Mature galls are spherical, averaging 7.0–11.0 mm in diameter. They usually occur in dense clusters averaging eight galls per cluster and are clothed with sharp, stiff spines (Fig. 18). Galls are induced on the adaxial surface of leaflets but usually grow in a dense mass firmly attached to the shoots. Galls often remain on the shoots over the winter. They occur on all three species of prairie roses but are most common on R. woodsii.

Galls are single-chambered (Fig. 19) with walls much thicker than those of D. polita. Immature galls are either leaf green, yellow, or bright red. Most galls turn yellowish-brown as they mature, although some are bright red until they dry. Eggs are deposited in early May on the adaxial surface of immature leaflets (Shorthouse et al. 2005). Periclistus-modified galls are larger than inducer-inhabited galls.

Because populations of D. bicolor galls are usually widely scattered, it is difficult to obtain sufficient numbers to assess the community. However, a large population of galls found about 25 km east of Saskatoon, Saskatchewan, provided this information. The galls were heavily attacked by Periclistus (Fig. 44B), which is always the most abundant inhabitant. About 59% of the immature galls were inhabited by Periclistus and about 28% of the mature galls by the end of the season (Table 5). Inquiline-modified galls contained an average of 9.3 chambers (Table 4). By fall, only 5.5% of the inhabitants were inducers (Fig. 44B), which is typical throughout the range of this species. Parasitoids constituted about 32% of the remaining inhabitants (Fig. 44B), the most common being Eurytoma sp. and Pteromalus sp. About 39% of the Eurytoma sp. exited in the current year (Table 3), as did some of the Torymus and Pteromalus.

Diplolepis rosaefolii (Cockerell) (Figs. 20 and 21)Diplolepis rosaefolii was first described from galls collected in Colorado (Cockerell 1889).


It has the widest distribution of all Nearctic Diplolepis, being found from British Columbia to Newfoundland and from the Yukon and Alaska to Colorado. It is a common species on the prairies and in southern British Columbia.

Diplolepis rosaefolii is one of the smallest adults in the genus, along with D. fusiformans, averaging about 2 mm in length. Galls are lentil-shaped (Fig. 20), 2.0–2.5 mm thick, and 3.0–5.5 mm in diameter and protrude from both the adaxial and abaxial surface of leaflets. Galls usually occur scattered over the leaf, although sometimes they are densely packed and coalesced. They are usually the same colour as the host leaflet when immature but turn either pale yellow or bright red when mature. They are single-chambered with the larva lying parallel to the leaflet surface (Fig. 21). Immature galls appear from late spring to late summer, indicating the adults have a lengthy activity period.

This species appears to be the least host specific of all Diplolepis in Canada, being found on the three prairie species of Rosa. Galls are most common on short, bushy R. woodsii growing in dry sites in the Mixed Grassland Ecoregion. Most galled leaves abscise in mid-fall, but heavily galled leaves sometimes remain on the plants over the winter.

Galls of D. rosaefolii from coulees of the South Saskatchewan River near Langham, Saskatchewan (west of Saskatoon), illustrate the community typical for this species (Fig. 44C). Commonly, 50–75% of all inhabitants are inducers throughout the range of this species. Periclistus are also common, frequently accounting for 12–25% of all inhabitants. Eurytoma, Pteromalus, and Glyphomerus stigma are the most common parasitoids (Fig. 44C). The percentage of galls inhabited by Periclistus is high in mid-season but drops to less than 15% by the end of the season (Table 5). Fewer Periclistus larvae occur per gall than in the galls of other species (Table 4). About one-third of the Eurytoma exit galls in the year of induction, as do over half of the Pteromalus (Table 3).

Diplolepis nebulosa (Basset) (Figs. 22 and 23)Diplolepis nebulosa was first described from unknown localities in the northeastern United States (Bassett 1890). Beutenmüller (1907, 1914) recorded the species from Connecticut, New York City, and Ontario. It is found sporadically across the prairies but sometimes occurs in such large numbers that hundreds can be collected in an hour. Galls are most commonly found on roses growing in the Mixed Grassland Ecoregion of southern Alberta and Saskatchewan.

Table 4. Mean number of Periclistus larvae per modified Diplolepis leaf gall (without parasitoids) found in south-central Saskatchewan.

Species Number of Galls Mean Number of Larvae (± SD)

D. polita 350 5.4 (4.4)

D. bicolor 53 9.3 (4.3)

D. rosaefolii 47 1.4 (0.6)

D. nebulosa 31 3.3 (3.1)

D. ignota 31 2.9 (1.4)

D. gracilis 78 1.8 (1.0)


Galls are spherical, averaging 5.0–7.0 mm in diameter, spineless, and on the abaxial leaf surface (Fig. 22). They occur singly or in a row and sometimes coalesce. Galls are green when immature and light brown when mature. They are single-chambered (Fig. 23) and the walls of mature galls are thin and brittle. Mature galls often abscise before their host leaves do. Periclistus-modified galls are larger and much firmer than inducer-inhabited galls. Galls are initiated in mid-spring.

Beutenmüller (1907) recorded galls on R. blanda and R. carolina L. in eastern North America. On the prairies and in southern British Columbia, these galls are found on R.

Figs. 16–27. Habitus of leaf galls induced by Diplolepis polita, D. bicolor, D. rosaefolii, D. nebulosa, D. ignota, and D. gracilis. Fig. 16. Cluster of leaf galls of D. polita on the adaxial surface of leaflets of Rosa acicularis. Fig. 17. Single- chambered leaf galls of D. polita dissected to show mature larvae. Fig. 18. Cluster of leaf galls of D. bicolor on the adaxial surface of leaflets of R. blanda. Fig. 19. Single-chambered gall of D. bicolor dissected to show mature larva. Fig. 20. Coalesced cluster of single-chambered galls of D. rosaefolii on leaflets of R. woodsii. Fig. 21. Single-chambered gall of D. rosaefolii dissected to show mature larva. Fig. 22. Cluster of leaf galls of D. nebulosa on the abaxial surface of leaflets of R. woodsii. Fig. 23. Single-chambered leaf gall of D. nebulosa dissected to show mature larva. Fig. 24. Coalesced cluster of galls of D. ignota on abaxial surface of leaflets of R. arkansana. Fig. 25. Coalesced galls of D. ignota dissected to show mature larvae. Fig. 26. Cluster of galls of D. gracilis on the abaxial surface of leaflets of R. woodsii. Fig. 27. Single-chambered leaf gall of D. gracilis dissected to show mature larva. Photographs by the author.

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woodsii. The most common habitat for D. nebulosa is on short R. woodsii, averaging 0.75 m in height and growing on dry, exposed sites.

A large population of galls from the flood plain of the Oldman River northwest of Coaldale, Alberta, illustrates a typical community for this species (Fig. 44D). Inducers made up 8.8% of the inhabitants, whereas 32.1% were Periclistus. Parasitoids, mainly Orthopelma and Aprostocetus, formed 59.1% of the inhabitants. A higher percentage (66.6%) of galls were inhabited by Periclistus (average of 3.3 per gall; Table 4) in mid-season, which declined to 13.1% by the time galls were mature (Table 5). For Eurytoma and Torymus, 16.6% and 26.4%, respectively, of individuals exited galls by the fall (Table 3).

Diplolepis ignota (Osten Sacken) (Figs. 24 and 25)Diplolepis ignota was first described from galls collected at undisclosed locations in the eastern United States (Osten Sacken 1863). Beutenmüller (1907) and Kinsey (1920) provided descriptions of the adults. This species has been recorded in Minnesota (Olson 1964), the eastern United States (Beutenmüller 1907), and as far south as Florida (Thompson 1915). It is found in the Mixed Grassland Ecoregion across the driest regions of southern Alberta and Saskatchewan.

Galls are found on the abaxial surface of leaflets and are variable in shape and size. Single galls are spherical, but they usually coalesce to form irregularly rounded, often reniform masses (Fig. 24). Two or three masses commonly form in one large elongated cluster that causes host leaves to droop. Galls are single-chambered (Fig. 25), but when they coalesce, they appear multi-chambered. Single-chambered galls when mature average 6–9 mm in diameter. Reniform galls average 15–20 mm in length. Mature galls become hard and woody when they dry but are soft and spongy when wet. They have a smooth surface without spines or protuberances. Galls are initiated in early August. Mature galls are light tan and remain attached to their hosts.

Galls are found only on R. arkansana in Alberta and Saskatchewan, especially on those species growing sparsely on the flood plains in river valleys in areas without overgrowth or in open prairies without other shrubs. Beutenmüller (1907) and Kinsey (1920) reported galls on R. blanda, R. carolina, R. virginiana, and R. nitida in eastern North America.

Three populations of D. ignota galls are included here for an overview of the component communities. One population (Fig. 44E) was found on the flood plain of the Oldman

Table 5. Percentage of Diplolepis leaf galls found in central or southern Saskatchewan inhabited by Periclistus.

Species Mid-Season Maximum Mature Galls

D. polita 71.0 12.0

D. bicolor 58.8 28.1

D. rosaefolii 63.2 14.7

D. nebulosa 66.6 13.1

D. ignota 11.4 5.8

D. gracilis 20.0 19.1


River north of Coaldale, Alberta. Rosa arkansana here were growing among patches of R. woodsii on which galls of D. nebulosa and D. bassetti were common. The second site was a pure stand of R. arkansana about 2 km away on the level prairie above the flood plain (Fig. 44F) and was chosen to compare two communities near one another. The third site was an isolated patch of R. arkansana growing on native shortgrass prairie about 20 km north of Maple Creek, Saskatchewan. This circular patch of roses was about 50 m in diameter and most plants were galled. Galls at all three sites were collected in the spring and returned to the laboratory to emerge the adults.

Low numbers of inducers were present at the two Coaldale sites (Fig. 44E and F), but 23.5% of the inhabitants were inducers at the Maple Creek site (Fig. 44G). Few Periclistus were among the inhabitants at all three sites. Parasitoids constituted 75.8–92.5% of individuals recovered at each site. Aprostocetus was the most dominant parasitoid, followed by Eurytoma and Orthopelma. Communities at the two Oldman River sites were remarkably similar, whereas the Maple Creek site had more inducers. The reason for the differences could be that the Maple Creek site was more recently established and the parasitoids had yet to become established.

From a typical population of galls east of Saskatoon, Saskatchewan, 11.4% of galls in mid-season were inhabited by Periclistus and 5.8% by the end of the season (Table 5). The mean number of Periclistus larvae per gall was 2.9 (Table 4), with only 1.9% of the Eurytoma exiting in the year of gall induction (Table 3). Similar data were not obtained from the sites used for the communities summarized in Fig. 44.

Diplolepis gracilis (Ashmead) (Figs. 26 and 27)Diplolepis gracilis was first described from galls collected at an undisclosed site in the northeastern United States (Ashmead 1897). Little is known about the distribution of D. gracilis. However, it has been recorded from several northern states (Thompson 1915; Olson 1964; Burks 1979). On the prairies, galls are found on roses growing in shaded areas along the North Saskatchewan River in Edmonton, Alberta, eastward toward Prince Albert, Saskatchewan, and northward along the South Saskatchewan River from the Alberta–Saskatchewan border.

Mature galls are ellipsoid, averaging 4–6 mm in diameter, have blunt protuberances extending from the lateral circumference, and are on the abaxial surface of leaflets (Fig. 26). They are single-chambered (Fig. 27) with thin walls. Maturing galls are white and although they are usually found in rows, adjacent galls seldom coalesce. Mature galls turn light tan and fall with their host leaves in mid-September. Galls are initiated in late summer.

A large population of galls found near Douglas Provincial Park in Saskatchewan illustrates a typical community for this species (Fig. 44H), of which 12.7% were inducers and 21% were Periclistus. The most abundant parasitoids were Orthopelma (at 30.5%) and Aprostocetus (26.4%). Eurytoma were relatively low at 2.6%. Only about 20% of the immature galls sampled at another site in central Saskatchewan in mid-season had Periclistus and 19.1% by the time the galls matured (Table 5). The mean number of Periclistus per mature gall is also low (Table 4). No parasitoids mature and exit mature galls in the season of gall induction (Table 3).

Diplolepis bassetti (Beutenmüller) (Figs. 28 and 29)Diplolepis bassetti was first described from galls collected near Corvallis, Oregon (Beutenmüller 1918). However, the gall illustrated by Beutenmüller is that of the European multi-chambered gall of D. rosae, whereas galls of D. bassetti are single-chambered.


Figs. 28–43. Habitus of leaf galls induced by Diplolepis bassetti and D. variabilis and the stem gall induced by D. fusiformans, D. nodulosa, Periclistus-modified galls of D. nodulosa, D. triforma, D. spinosa, and D. radicum. Fig. 28. Coalesced galls of D. bassetti on adaxial surface of leaflets of Rosa woodsii. Fig. 29. Single-chambered gall of D. bassetti dissected to show mature larva. Fig. 30. Coalesced cluster of galls of D. variabilis on leaflets of R. woodsii. Fig. 31. Coalesced gall of D. variabilis dissected to show pre-pupa and pupa. Fig. 32. Rows of galls

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Because D. rosae is established in Oregon, this early report likely confused the two species. Kinsey (1922) provided a detailed description of the adults and recognized two subspecies. However, he also appears to have confused the galls of D. bassetti and D. rosae.

Diplolepis bassetti induces mossy, monothalamous galls (Figs. 28 and 29) on the adaxial surface of the leaflets of R. woodsii in open habitats in southern Alberta and Saskatchewan and in the Okanagan Valley of British Columbia. Diplolepis bassetti is also sparsely distributed across southern Alberta and southwestern Saskatchewan.

Galls are usually found in dense clusters. Their surface is covered with soft filamentous hairs (Fig. 29) that are green to red when immature, turning brown when mature. Galls are initiated in mid-summer. The chambers rarely coalesce and the individual galls can be easily separated. Galls average 4–5 mm in diameter. They commonly remain attached to the host plant throughout the winter.

Two large populations of mature galls collected in the spring were chosen to illustrate community composition. One collection was made on the flood plain of the Oldman River north of Coaldale at the same site as the D. ignota galls (Fig. 44E). The second was made from several large patches of roses from Kelowna to Osoyoos, British Columbia. No data were obtained on the seasonal changes of Periclistus attack, the number of Periclistus per modified gall, or the percentage of parasitoids exiting galls in the fall.

Inducers were by far the most abundant inhabitants (Fig. 44I) at the southern Alberta site. Galls here also had few Periclistus, representing 2.8% of the community. Only 19.6% of the remaining inhabitants were parasitoids, with the most abundant being Pteromalus (7.8%) and G. stigma (7.5%). In contrast, galls from southern British Columbia (Fig. 44J) had fewer inducers (16%) and Periclistus were much more abundant (28.4%). Parasitoids constituted 55.3% of the emergents, with the most abundant being Aprostocetus (46.9%) and Eurytoma (5.5%).

Diplolepis variabilis (Bassett) (Figs. 30 and 31)Diplolepis variabilis was first described from galls collected in North Dakota (Bassett 1890). Beutenmüller (1907) and Kinsey (1922) reported galls from Washington to Texas. In Canada, D. variabilis is found only west of the Rocky Mountains and is very common on tall R. woodsii from Kelowna to Osoyoos, British Columbia. Galls of D. variabilis are found on the leaves of the upper branches and are usually larger and denser than galls of D. ignota.

Galls are single-chambered and spherical and are found on the abaxial surface of leaflets. However, most galls coalesce to make clusters irregularly rounded and globular to ovate (Fig. 30). Single-chambered galls are about 8 mm in diameter, whereas coalesced galls are often 2 cm in diameter. They have a smooth surface and internally are pith-like with the consistency of packed sawdust. The chambers are located at the centre, deep

of D. fusiformans on tips of stems of R. woodsii. Fig. 33. Stem galls of D. fusiformans dissected to show mature larvae of the inducers to the left and mature larvae of Periclistus sp. to the upper right. Fig. 34. Single-chambered stem gall of D. nodulosa at tip of a stem of R. woodsii. Fig. 35. Gall of D. nodulosa dissected to show mature larva. Fig. 36. Periclistus-modified gall of D. nodulosa on a stem of R. woodsii. Fig. 37. Periclistus-modified gall of D. nodulosa dissected to show mature larvae. Fig. 38. Multi-chambered stem gall of D. triforma on R. woodsii. Fig. 39. Gall of D. triforma dissected to show mature larvae. Fig. 40. Multi-chambered stem galls of D. spinosa on R. woodsii. Fig. 41. Stem gall of D. spinosa dissected to show mature larvae. Fig. 42. Multi-chambered stem gall of D. radicum on R. woodsii. Fig. 43. Stem gall of D. radicum dissected to show mature larvae. Note one larva of Eurytoma sp. (arrow). Photographs by the author.


within the galls (Fig. 31). Galls are green when immature but turn tan to brown when mature. They are often so dense that branches droop with the combined weight of the galls. They remain on the host plants over winter. Galls are initiated in late summer.

Inhabitants were reared from a large population of galls collected in the fall near Oliver, British Columbia. Of recovered insects (Fig. 44K), 7.7% were inducers, 23.2% were Periclistus, and 69.3% were parasitoids. The most abundant parasitoids were Aprostocetus at 47.5% and Eurytoma at 17%.

Diplolepis fusiformans (Ashmead) (Figs. 32 and 33)Diplolepis fusiformans was first described from galls found in Colorado (Ashmead 1890). They have also been found in Ontario, Illinois, Nebraska, and Arizona (Beutenmüller 1907; Kinsey 1922; Burks 1979; Caouette and Price 1989). Diplolepis fusiformans is one of the smallest wasps in the genus, with females averaging 1.5–2.5 mm in length.

Galls of D. fusiformans are small, fusiform, and found along the terminal parts of the current-year stems (Fig. 32) of R. woodsii. Galls may be a gentle swelling or may be swollen to about twice the size of the host stem (Fig. 32). Galled stems are smooth and often have a split in the epidermis. The gall is multi-chambered with a series of chambers, usually about five in a row, along the length of the stems (Fig. 33). Galls are internally woody, soft, and porous and the chambers are inseparable. Chambers containing Periclistus are also found along the lengths of the stem (Fig. 33).

Adults of D. fusiformans exit their galls in late June and oviposit in new sucker shoots about 5 cm in length. In contrast to all other species of Diplolepis, D. fusiformans deposits its eggs on the exposed surface of the stems (Shorthouse et al. 2005). The galls form after the larvae enter the stem.

Galls are found throughout the grasslands of the prairie provinces and southern British Columbia on R. woodsii. They have not been reported on R. arkansana or R. acicularis. In Ontario, D. fusiformans forms galls on R. blanda but not on R. acicularis. No data on the component communities associated with this gall were obtained.

Diplolepis nodulosa (Beutenmüller) (Figs. 34–37)Diplolepis nodulosa was first described from galls collected in the northeastern United States (Beutenmüller 1909). A detailed description of adults was provided by Brooks and Shorthouse (1997). Galls of D. nodulosa are tiny swellings at the tips of stems of R. woodsii and are barely perceptible (Fig. 34).

Mature galls are single-chambered, fusiform, and spineless (Fig. 34). They average 3.1 mm in diameter and are commonly circumscribed by a series of stunted leaflets. Galls are green when immature but frequently turn red when mature. Larvae are usually found in a vertical position within their chambers (Fig. 35).

Periclistus greatly enlarge inhabited galls (Fig. 36), making them highly visible and indicating that D. nodulosa is in the area. Galls modified by Periclistus (Figs. 36 and 37) are multi-chambered, spherical structures averaging 12 cm in diameter, with some galls being 20 mm in diameter. Galls found near Sudbury, Ontario, contained an average of 17 Periclistus per gall (maximum of 146) (Brooks and Shorthouse 1997) and prairie galls are likely similar. Immature Periclistus-modified galls are initially green but turn mottled red-brown in the fall and are gray-tan by the following spring.

A closely related species, D. inconspicuous Dailey and Campbell, has been found in California on R. californica (Dailey and Campbell 1973). Its galls are identical to those of D. nodulosa, but the adults are morphologically distinct (Brooks and Shorthouse


1997). Diplolepis inconspicuous is apparently restricted to the west coast of the United States, whereas D. nodulosa is found throughout eastern and midwestern North America (Shorthouse and Ritchie 1984), east to the north shore of Prince Edward Island, and west to British Columbia. It is found on R. blanda in Ontario, R. virginiana on Prince Edward Island, and R. woodsii in British Columbia, Alberta, and Saskatchewan.

For a large population of galls near Sudbury, Ontario, Periclistus killed 65% of the inducers and parasitoids killed an additional 17%. Communities of prairie galls are likely similar (Brooks and Shorthouse 1997).

Diplolepis triforma Shorthouse and Ritchie (Figs. 38 and 39)Diplolepis triforma was first described from galls collected near Sudbury, Ontario (Shorthouse and Ritchie 1984). It was given this name because three types of galls can be induced by larvae from the same female. They are found on R. acicularis throughout the Aspen Parkland Ecoregion and R. woodsii on the prairies and in southern British Columbia. This species is found across southern Canada and the Yukon and is usually sparsely distributed.

Immature galls are green swellings at the base of the apical meristem and usually are covered with dense spines. Galls are initiated in the early spring. Mature galls are conspicuous, woody, and firmly attached to twigs. Most galls are pear-shaped without distal stem growth (Fig. 38). However, about one-quarter of the galls have some distal growth and a few are fusiform swellings of a twig distal to its base. The gall is multi-chambered and the chambers are close to the surface (Fig. 39). They remain on their hosts over the winter.

Wiebes-Rijks and Shorthouse (1992) provided data on the inhabitants associated with a large population of galls near Sudbury, Ontario, for which the most common parasitoids were Eurytoma spp, Pteromalus, Torymus sp., and Orthopelma sp. Periclistus are not associated with this gall.

Diplolepis spinosa (Ashmead) (Figs. 40 and 41)The first report of Diplolepis spinosa was in Florida (Ashmead 1897), where the species was named from the characteristics of the gall. Gillette (1890) provided the first description of D. spinosa females but under the name Rhodites multispinosus. Burks (1979) recognized R. multispinosus as a synonym of D. spinosa. Beutenmüller (1907) and Kinsey and Ayres (1922) provided a more detailed description (as D. multispinosus) and illustrated the galls, as did Shorthouse (1988, 1993).

Galls of D. spinosa are one of the most conspicuous galls on the grasslands. They are spherical or irregularly rounded and often the size of a golf ball (Fig. 40). They appear attached to the main stem but are formed from a leaf bud (Figs. 9–12). They are firmly attached to their hosts and often can be removed only with snips.

Galls of D. spinosa are found from eastern Ontario to the Okanagan Valley and northeastern British Columbia. They are found only on R. woodsii on the prairies and in British Columbia and only on R. blanda in Ontario. They are never found on R. acicularis. Galls are usually weakly spined to smooth on the spiny R. woodsii on the prairies but always heavily spined on the smooth-stemmed R. blanda in Ontario. They average about 23 mm in diameter in Ontario (Bagatto and Shorthouse 1994) and those on the prairies are similar.

Galls are multi-chambered (Fig. 41), with most chambers located in a cluster near the centre. Immature galls are yellowish-green, soft, and usually clothed with slender spines.


Mature galls are reddish-brown or dull purple, hard, and woody. Galls on wild roses from central Ontario have an average of 16.5 larval chambers per gall (Bagatto and Shorthouse 1994). Those on the prairies and in British Columbia are likely the same.

Galls collected in the spring from southern Saskatchewan in the Great Sand Hills are used here to illustrate a typical component community. Commonly, 20–30% of the inhabitants associated with populations of this gall are inducers (Fig. 46L). Periclistus sp. make up about 21.3% of all inhabitants, whereas parasitoids form about 50% of all inhabitants. The most abundant parasitoid was Eurytoma sp. at 47.1% of all inhabitants.

Diplolepis radicum (Osten Sacken) (Figs. 42 and 43)Diplolepis radicum was described from galls in the central United States (Osten Sacken 1863). Adult females are among the largest of the genus, averaging 3.0–4.0 mm in length. Kinsey (1922) and Shorthouse (1988) provided additional information on the adults.

Galls of D. radicum are by far the largest of all Diplolepis galls, ranging in size from 2.5 to 6.0 cm, with some 10 cm in diameter. They are found throughout the grasslands of the prairies and in southern British Columbia. However, they are difficult to locate, especially when partially buried in the ground or hidden by vegetation. They are formed at the tips of adventitious shoots (Fig. 1) just below the surface of the ground. Although galls of this species are commonly referred to as root galls because of their location, they are stem galls (Fig. 42).

Females crawl down cracks in the ground at the base of roses in early spring to locate adventitious shoots before they protrude above the surface. Large numbers of eggs, sometimes numbering 200–350, are laid within the shoot tips and the resulting larvae produce irregularly rounded, tomato-shaped, multi-chambered galls (Fig. 43) of variable size. Galls are soft and succulent when growing, with the larval chambers packed throughout the mass of the gall (Fig. 43). They always have a smooth surface and are reddish-brown throughout all stages of development.

Diplolepis radicum appears to be as widely distributed as D. spinosa. Diplolepis radicum has been recorded from Ontario to North Carolina on R. carolina and west to Colorado and north to Oregon and Washington State on R. nutkana and R. woodsii (Beutenmüller 1907, 1914; Weld 1926). Galls are found on R. woodsii across the prairies and appear to be most abundant where the soils are sandy. Galls are found on R. woodsii in southern British Columbia.

Less is known about the community of inhabitants associated with this gall than about those of other species. For inhabitants of 40 galls collected in the fall from the Great Sand Hills of Saskatchewan, 27.2% were inducers, 2.9% were Periclistus sp., and the rest were parasitoids. Eurytoma sp. and Pteromalus sp. were the most abundant parasitoids.

Conclusions

The findings reported in this chapter indicate the extent of the complexities associated with plant-feeding insects found in the grasslands of Canada. The chapter shows the intimate association that cynipids have with wild roses and provides some insight into why roses have been the ideal hosts for the radiation of the Diplolepis complex. Further, the specialized life history strategy of Diplolepis makes roses a good candidate for the insect most ideally adapted to the abiotic conditions of grasslands. On a small scale, Diplolepis can be considered “ecosystem engineers” (Wright and Jones 2006) because they provide habitats and resources for other insects in well-established component communities.


The significance of the unique feeding relations that Diplolepis have with their host plants can be understood by considering the three key hurdles that must be overcome by insects that exploit plants (Strong et al. 1984). These hurdles are desiccation, attachment, and food. Perhaps no other group of insects has met them as well as grassland Diplolepis. Whereas other insects feeding on the surface of leaves or stems have to contend with gusts of drying winds, Diplolepis larvae find themselves in chambers with high humidity. Vascular bundles within tissues of galls are joined to those of the host plant and serve as pipelines bringing water to cynipid larvae (Leggo and Shorthouse 2006). Gall cells, besides providing Diplolepis with food, encase the inducers within a sturdy structure that prevents them from falling off their host plants or being attacked by generalist predators. However, it is in their ability to obtain a complete diet, while restricted to feeding on one kind of cell, that Diplolepis surpass all other phytophagous insects. When cynipid larvae need food, they slice open a cell and suck up a liquid cocktail filled with all the nutrients necessary for their growth and development (Bronner 1992). In contrast, other plant-feeding insects have a problem obtaining enough amino acids because plant cells are composed predominantly of carbohydrates (Schoonhoven et al. 1998). Whereas other plant-feeding insects must move to new feeding sites when their source of food is exhausted, food “comes to” immature Diplolepis. Cynipid gallers have such intricate control over their hosts that the nutrient composition of cellular contents is altered as the contents are transported from other parts of the plant to the nutritive cells lining the surface of gall chambers. No other guild of plant-feeding insects on the grasslands has access to such cells.

Another factor in the success of Diplolepis has been their choice of host plant. Roses are widely distributed and readily found by Diplolepis. Roses are early successional species that do well in disturbed sites, providing opportunities for Diplolepis to disperse into new areas. The bushiness of roses provides protection for ovipositing female wasps and provides a deep snowpack for warmer rather than ambient overwintering sites. Roses are hardy and reliable shrubs able to tolerate the often dry and cold conditions of the prairies. Vegetative buds are produced early in the spring just as the warm temperatures return, providing clues for the adults to synchronize their appearance with tissues needed for oviposition. The ovipositors of Diplolepis are just the right length to reach the inside of vegetative buds and these ovipositors have the necessary receptors at their tips to detect individual cells on the surface of immature leaflets or procambium cells in immature vascular bundles (Bronner 1985; Sliva and Shorthouse 2006).

We can only guess at the events that were responsible for the radiation of extant species of Diplolepis. Several factors have been suggested for the radiation of other groups of cynipid gallers, such as competition for oviposition sites and pressures inflicted by parasitoids (see references in Stone et al. 2002; Csóka et al. 2005). Likewise, one can argue that as parasitoids, and possibly inquilines, began inflicting high levels of mortality on Diplolepis, the inducers were pressured to seek new oviposition sites, resulting in new types of galls that would provide them with protection. Such a strategy may have been successful for a period, but the enemy-free space did not last. Both parasitoids and inquilines successfully tracked the inducers no matter what type of new gall was developed and, as a result, all species of Diplolepis on the grasslands of Canada today have many parasitoids feeding on the inducers. However, even with high rates of mortality inflicted by both parasitoids and inquilines, grassland Diplolepis are thriving.

Perhaps Diplolepis evolved in the drier regions of central North America on early roses and then moved northward along with this host. Once present on the prairies, the ancestor of species such as D. polita, D. gracilis, and D. triforma may have moved onto R. acicularis


and become a separate species. Similarly, species such as D. bicolor, D. rosaefolii, and D. ignota may have radiated onto R. arkansana, with only D. ignota becoming restricted to this host. Once established on grassland roses, D. bicolor, D. spinosa, and D. nodulosa may have moved onto R. blanda in Ontario and D. bicolor and D. rosaefolii onto R. virginiana in the Atlantic provinces. If this scenario is correct, then understanding the biology of grassland Diplolepis is of great importance.

Of interest, 3 of the 13 species of prairie Diplolepis are found exclusively on R. acicularis, the species most common in the northern range of the grasslands (Table 1), whereas 6 are found exclusively on R. woodsii. Three species are found on R. arkansana, and one of these, D. ignota, is found only on this rose. Diplolepis bicolor is found on R. woodsii and R. arkansana, and D. rosaefolii is found on all three hosts. Only D. bicolor and D. radicum are found on two hosts, and D. rosaefolii is the only species found on all three roses. In the Okanagan Valley, 12 Diplolepis species (D. ignota is not found here) are found on R. woodsii.

Much remains to be learned about the host preferences of Diplolepis and their level of success on various hosts. Molecular studies of Diplolepis and their hosts, similar to those of Cook et al. (2002) who studied evolutionary shifts of cynipids between species of oaks, would be very revealing. Such a study might show that the occurrence of D. rosaefolii on all three species of prairie roses indicates its primitiveness compared with the other species, as was suggested by Plantard et al. (1998).

New species of Diplolepis possibly evolved on roses without geographical separation. Sympatric speciation by means of shifting hosts and organs is an important process in the evolution of phytophagous insects (Berlocher and Feder 2002), and the same process likely occurred for Diplolepis. Events leading to new species conceivably occurred by changes in oviposition sites (Shorthouse et al. 2005). New sites for gall initiation, in addition to slight changes in the messages imparted on the cells, could have led to new gall structures and the radiation of speciation on the same host.

Another aspect of Diplolepis ecology that contributes to their success is their ability to locate hosts when the window of opportunity for doing so is brief. Dispersal is an important ecological attribute for most insects and an important area of ecological research (Trakhtenbrot et al. 2005). Although poor fliers, Diplolepis somehow manage to locate even the most isolated shrubs. Isolated roses are commonly found with the galls of two or three species of Diplolepis. It is likely that Diplolepis are passively dispersed by wind and by chance land on host roses. Strong westerly winds are frequent on the prairies (Chapter 5) and probably contribute significantly to Diplolepis dispersal. Short-term turbulent gusts of wind have a profound influence on the aerial transport of many organisms (Nathan et al. 2005). Likewise, the presence of Periclistus and parasitoids in galls on isolated roses attests to their remarkable dispersal abilities. Not only must they find roses, but they must also find galls at the right stage of development for successful oviposition within a narrow window of opportunity.

Some species of Diplolepis have more restricted ranges than others. Galls of D. ignota, for example, are found only in the southern prairies. Those of D. variabilis are found only in the southern Okanagan. Diplolepis bassetti is peculiar because it appears to have the most restricted distribution of all prairie Diplolepis, being found only in southwestern Alberta. In contrast, its galls are common in the southern Okanagan and the main range of the species is possibly to the west of the Rockies. Populations of D. bassetti in southwestern Alberta may originate from adults blown east from populations in valleys of southeastern British Columbia. The southern Alberta community, with its high percentage of inducers


and low numbers of Periclistus and parasitoids (Fig. 46I), may be more recently established compared with the Okanagan communities (Fig. 46J). As was the case with galls of D. ignota, newly established gall populations appear to have a period in which they escape attack by inquilines and parasitoids.

Attack by inquilines and parasitoids exerts a strong effect on the survivorship of galling insects and are the principal cause of death of most cynipids (Washburn and Cornell 1981; Askew 1984; Fay and Samenus 1993; Ito and Hijii 2002; Stone et al. 2002). This finding suggests that refuge from enemy attack is a fitness component of importance to cynipids. Of interest, gall inducers as a group support richer parasitoid communities and suffer higher rates of parasitoid-induced mortality than do other groups of insect herbivores (Hawkins 1988; Price and Pschorn-Walcher 1988); as a consequence, no gall structure today provides an absolute refuge.

Parasitoids may be a major selective force on the diverse morphology of cynipid galls (Cornell 1983; Stone and Cook 1998; Stone and Schönrogge 2003). Morphological traits of galls, such as diameter and thickness of the walls of the chambers, affect the species composition of parasitoids and inquilines in galls of other cynipids (Schönrogge et al. 1994; Plantard et al. 1996; Ito and Hijii 2002) and the same likely occurs with galls of Diplolepis. Delays in growth of cynipids relative to growth of their galls also reduce the window of vulnerability (Plantard and Hockberg 1998).

Even though galls of Diplolepis are strikingly different and some, such as those of D. bicolor and D. spinosa, are spiny with thick, firm walls surrounding the chambers, many species of inquilines and parasitoids still find the means to successfully track them (Fig. 44). As a result, the sizes and shapes of rose galls we see today may be the “ghosts of competition past,” as suggested by Cornell (1980). Of interest, some cynipid populations are reported to have suffered local extirpations from natural enemies (Washburn and Cornell 1981), but similar events have not been observed on prairie or Okanagan roses. Species such as D. polita commonly suffer a 95% mortality rate or higher in some sites, but still persist from year to year (Shorthouse 1973). There is no question that populations of Diplolepis galls fluctuate widely from year to year on stable patches of roses and that populations may crash at some sites. However, such reductions are likely more related to harsh abiotic conditions such as cool, rainy weather at the time of oviposition than they are to parasitoids. High winds at the time of oviposition would also impede Diplolepis from finding their hosts, and prolonged freezing winter temperatures below −30 °C would be harmful (Williams et al. 2002).

Periclistus are important causes of mortality for Diplolepis, particularly for the inducers of leaf galls and some stem galls (Brooks and Shorthouse 1997). Over half the inducers of some galls are killed by Periclistus by mid-season (Table 5). At a study site near Edmonton, 88% of the galls of D. polita were inhabited by Periclistus by mid-June (Shorthouse 1973), meaning that only 12% could potentially contain an inducer. The number of leaf galls with Periclistus drops as the season advances (Table 5) because many are killed by parasitoids. Fewer galls of species that appear later in the season are attacked by Periclistus (Table 5).

The mean number of Periclistus chambers in galls without parasitoids is highest for galls of Diplolepis polita and D. bicolor (Table 4). Periclistus are dominant members of the communities by the end of the season for the galls of D. polita, D. bicolor, and D. nebulosa (Fig. 44). The reason that the final community within galls of D. rosaefolii is dominated by inducers (Fig. 44C) may be its lengthy emergence period, which results in later-appearing galls avoiding attack by Periclistus. The small size of D. rosaefolii larvae may also make them less attractive to parasitoids. In addition, in late-season galls such as


Fig. 44. Typical component communities associated with galls of nine species of Diplolepis found on the grasslands of western Canada. A. Galls of D. polita from Prince Albert National Park in Saskatchewan. B. Galls of D. bicolor from 25 km east of Saskatoon, Saskatchewan. C. Galls of D. rosaefolii from coulees of South Saskatchewan River


those of D. ignota and D. gracilis, usually less than 25% of their communities are composed of Periclistus. Galls of D. bassetti and D. variabilis in the Okanagan have more Periclistus than inducers. The coalesced nature of these two galls likely helps the Periclistus escape attack by parasitoids.

Interestingly, the communities associated with Diplolepis ignota galls at the two sites in southern Alberta (Fig. 44E and F) were similar, but galls at the site about 250 km to the east near Maple Creek had a different complement of inhabitants (Fig. 44G). Perhaps the Saskatchewan galls had fewer inquilines and parasitoids because the gall population was recently established. Roses are ephemeral shrubs, with populations disappearing and appearing at new sites over time. Diplolepis flying into new patches of roses, such as D. ignota flying into a new patch of roses near Maple Creek, would have a period of grace before Periclistus and parasitoids find them and then the community would stabilize.

Galls of Diplolepis gracilis are initiated in mid-summer and a high proportion of adults issuing from mature galls are inducers (Fig. 44H). Galls of D. bassetti are more common in the Okanagan Valley than they are on the prairies, and indeed, prairie populations of this gall are suspected to become established from adults that have blown over the Rockies. Inducers in prairie galls make up a high percentage of the inhabitants (Fig. 44I), which indicates newly established gall populations. In contrast, galls from the Okanagan appear to be more well-established, with a smaller percentage of their inhabitants being inducers and a high percentage of the inhabitants being Periclistus (Fig. 44J). Diplolepis variabilis is restricted to the Okanagan and its huge populations of galls throughout the valley appear to be well-established and stable from year to year. The presence of large populations of Periclistus (Fig. 44K) may indicate long-established populations of galls, as may also be the case with galls of D. polita and D. bicolor. Further, the large populations of Aprostocetus in galls of both D. bassetti (Fig. 44J) and D. variabilis (Fig. 44K) indicate the initiation of galls in mid-summer and the abundance of this parasitoid when galls are small. The spring-initiated, multi-chambered galls of D. spinosa on the prairies issue large numbers of both inducers and Periclistus (Fig. 44L) and large populations of either Torymus sp. or G. stigma. Both parasitoids have long ovipositors and attack maturing galls in mid-summer. Small species such as Aprostocetus must oviposit in the early spring when the galls are small.

Much remains to be learned about the component communities associated with galls of Diplolepis. Once they have been described, determining their host and gall specificity would be of interest. It is not known, for example, whether some species of Eurytoma are specific to leaf galls whereas other species attack stem galls, or whether species of parasitoids that attack early-season galls are the same as those that attack galls that appear later in the season. No studies have shown why parasitoids such as Aprostocetus sp. find galls of D. ignota (Fig. 44E–G), D. bassetti (Fig. 44J), and D. variabilis (Fig. 44K) so attractive, nor why some species of Eurytoma, Torymus, and Pteromalus pupate and exit their galls in the year of gall induction (Table 3).

near Langham, Saskatchewan. D. Galls of D. nebulosa from valley of Oldman River north of Coaldale, Alberta. E. Galls of D. ignota from valley of Oldman River north of Coaldale, Alberta. F. Galls of D. ignota from top of coulee above Oldman River north of Coaldale, Alberta. G. Galls of D. ignota from grassy plains north of Maple Creek, Saskatchewan. H. Galls of D. gracilis from Douglas Provincial Park north of Moose Jaw, Saskatchewan. I. Galls of D. bassetti from valley of Oldman River north of Coaldale, Alberta. J. Galls of D. bassetti from Osoyoos, British Columbia. K. Galls of D. variabilis from Oliver, British Columbia. L. Galls of D. spinosa from Great Sand Hills north of Maple Creek, Saskatchewan.


The application of molecular phylogenetic techniques has revolutionized studies of insect evolution, systematics, and community ecology and has been applied to several cynipid taxa (Stone and Cook 1998; Ronquist and Liljeblad 2001; Cook et al. 2002). For example, Plantard et al. (1998) undertook a preliminary study of the genetic differences between species of Diplolepis found in Europe and North America. Such techniques can provide much useful information. They would illustrate, for example, the similarity between species of Diplolepis, their Periclistus inquilines and parasitoids found in southern Saskatchewan, and those found in the boreal forests of northern Ontario. What would the patterns revealed by genetic differences and similarities tell us about the evolution of Diplolepis and the members of their associated component communities? The information presented in this chapter may encourage other researchers to investigate some of these intriguing issues.

Acknowledgements

Studies on grassland Diplolepis were funded by Discovery Grants from the Natural Sciences and Engineering Research Council of Canada and the Laurentian University Research Fund. I thank my wife Marilyn for her help in collecting galls in the rose patches on many expeditions across the prairies and in the Okanagan Valley of southern British Columbia. I also thank Bob Lalonde, Graham Stone, Saban Güçlü, and Rüstem Hayat for their suggestions on improving this chapter. I also thank Chris Blomme for the drawing of roses on page 253.

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