The Common Asparagus Beetle, Crioceris Asparagi (Linnaeus), and the Twelve-Spotted Asparagus Beetle, Crioceris Duodecimpunctata (Linnaeus) (Coleoptera: Chrysomelidae)

PROC. ENTOMOL. SOC. WASH. 110(3), 2008, pp. 602–621

INTRODUCED LEAF BEETLES OF THE MARITIME PROVINCES, 6: THE COMMON ASPARAGUS BEETLE, CRIOCERIS ASPARAGI (LINNAEUS), AND THE TWELVE-SPOTTED ASPARAGUS BEETLE, CRIOCERIS DUODECIMPUNCTATA (LINNAEUS) (COLEOPTERA: CHRYSOMELIDAE)

LAURENT LESAGE,ERHARD JOHN DOBESBERGER, AND CHRISTOPHER G. MAJKA

(LL) Agriculture and Agri-Food Canada, ECORC, K.W. Neatby Bldg., 960 Carling Avenue, Ottawa, ON, Canada K1A 0C6 (e-mail: [email protected]); (EJD) Science Advice Division, Canadian Food Inspection Agency, Plant Health Risk Assessment Unit, 3851 Fallowfield Rd., Ottawa, ON, Canada K2H 8P9 (e-mail: [email protected]); (CGM) Nova Scotia Museum, 1747 Summer Street, Halifax, NS, Canada B3H 3A6 (e-mail: [email protected])

Abstract.—The common asparagus beetle, Crioceris asparagi (Linnaeus) and the twelve-spotted asparagus beetle, Crioceris duodecimpunctata (Linnaeus) are introduced Palearctic leaf beetles that feed exclusively on asparagus. The introduction history of these species in North America is reviewed and their dispersal to and distribution in the Maritime Provinces of Canada are described. Both species were first reported in Canada in 1899 in asparagus production areas in Queenston, Ontario, and other parts of the Niagara Peninsula where they caused serious crop damage. However, we discovered that both species were already found around Que´bec City 22 years earlier. Populations now established in the Maritime Provinces of Canada probably originated from southwestern Ontario where most commercial asparagus production in Canada began and now occurs. Crioceris asparagi and C. duodecimpunctata spread steadily throughout eastern Canada by adult flight dispersal abetted by wind, by the dissemination of seeds by birds, and by commercial movement of root crowns and spears of asparagus. Asparagus escaped from cultivation, growing along transportation corridors (such as railway tracks, power utility right-of-ways and roads) and in vacant lands, which facilitated the spread and establishment of C. asparagi and C. duodecimpunctata throughout North America. Now, both these adventive pest species occur wherever asparagus is grown. Both C. asparagi and C. duodecimpunctata are confirmed to occur in New Brunswick and Nova Scotia, but not Newfoundland and Labrador. However, C. duodecimpunctata is newly recorded from Prince Edward Island. These introduced beetles are not regulated by Canada or by the U.S.A., and they are readily controlled at economically acceptable damage thresholds. Key Words: Coleoptera, Chrysomelidae, Criocerinae, Crioceris asparagi, Crioceris duodecimpunctata, asparagus beetle, twelve-spotted asparagus beetle, Canada, Maritime Provinces, adventive species, pest distribution, quarantine pest, invasive alien species VOLUME 110, NUMBER 3 603

The common asparagus beetle, Crio- nada are not included here but most of ceris asparagi (Linnaeus, 1758) and the them are found in Beirne (1971). Various twelve-spotted asparagus beetle, Crio- United States government documents ceris duodecimpunctata (Linnaeus, 1758) have provided useful data as well. In are chrysomelid beetles introduced to this analysis, we provide new verified North America that are monophagous information obtained directly from on asparagus (Clark et al. 2004). They voucher specimens of older records, or generally occur wherever asparagus from new data not previously published. grows, either cultivated or escaped from cultivation, and both beetles originate HISTORICAL REVIEW from the Mediterranean Sea region Asparagus (Asparagus officinalis Lin- (Monro and Small 1997, Fara 2007). naeus) and its many varieties, is a Crioceris asparagi and C. duodecimpunc- vegetable delicacy known to ancient tata co-exist throughout North America Egyptians, Romans, and Greeks more wherever asparagus is grown because of than two thousand years ago. In his De adaptive differences in their phenological Agricultura, Cato the Elder (234–149 development which enable both to ex- B.C.) described techniques of production ploit the same single plant species and cultivation which are still in use (Capinera 1976, 2001). The major differ- today (Dalby 1998, Hutchinson et al. ences are found during the larval stages. 2006). Asparagus has been used for heart While the larvae of C. asparagi feed only trouble, dropsy, liver and jaundice com- on foliage, those of C. duodecimpunctata plaints, bee stings, poor eyesight, and develop one month later in the berries sciatica. Asparagus has been marketed as (Capinera 2001). Damage can be severe, a good source of folic acid, vitamin C, particularly to cold-stressed plants. This thiamin, vitamin B6, potassium, and is uncommon now because of effective many micronutrients such as glutathione pesticides and quick harvesting of spears which is thought to protect against upon which beetles normally feed, there- cancer, and rutin which strengthens by reducing resource availability. Eulo- blood vessels (Borris and Brunke 2006). phid parasitoids such as Tetrastichus Asparagus was brought to North coeruleus Nees (5 T. asparagi Crawford) America by early colonists from Europe. are a significant population control in C. According to Lescarbot (1612), aspara- asparagi, but not for C. duodecimpunc- gus was grown at Port Royal (Nova tata (Capinera 2001). Other biological Scotia). The earliest archaeological evi- mortality agents and seed scarcity prob- dence found by Erskine (1975) was from ably limit C. duodecimpunctata popula- 1770 in surficial remains at the Minas tions (Campbell et al. 1989, Capinera settlement (Nova Scotia). In their survey 2001). of the colonial garden plants, Favretti Most of the available information on and DeWolf (1971) cited Parkinson C. asparagi and C. duodecimpunctata in (1629) who recommended asparagus as Canada has consisted of reports in a delicacy which was also good for Canadian agricultural pest surveys or treatment of urinary and kidney prob- reports by Canadian entomological soci- lems. Boucher (1664) mentioned that, eties, either at the provincial or federal like parsnip (Pastinaca sativa L.), it had government level. Primarily notes, re- escaped from cultivation and was found ports, or articles on asparagus beetles wild on islands around Hochelaga (Mon- from eastern Canada (Ontario, Que´bec, tre´al Island). It was reported to thrive and the Maritime Provinces) were con- well in Massachusetts in 1672 and was sidered. References from western Ca- growing in every colony along the 604 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

Atlantic Coast by 1776 (Haughton asparagus spears for consumption orig- 1978). During his travels in North inating in Japan (USDA 1984), and in America in 1750, the Finn, Pehr Kalm, Massachusetts and New York in 1981 noticed that some asparagus grew wild originating in Italy and the former on the shores of the Hudson River Yugoslavia (USDA 1982). (Benson 1966, Rousseau et al. 1977), Even though Crioceris asparagi and C. which means that the plant must have duodecimpunctata co-occur, they were been grown in gardens for many years detected in the U.S.A. about 25 years previously. apart. Crioceris duodecimpunctata was The establishment of the asparagus first found near Baltimore, Maryland beetle, C. asparagi, and the twelve- about 1881 (Chittenden 1908, 1917). spotted asparagus beetle, C. duodecim- Both beetles caused severe damage in punctata, came much later. Fitch (1862) asparagus crops and were established was the first entomologist to report C. several years prior to their detection at asparagi in North America from Albany outbreak population levels. Fortunately, (New York). Three years later, he a primary parasitoid of C. asparagi, T. mentioned that a Mr. John Quin had coeruleus Nees, was found in asparagus already noticed C. asparagi at Astoria, beetle populations about 1863 (Walsh New York, in 1859 (Fitch 1865). Chit- and Riley 1868; Johnston 1915; Capinera tenden (1908) believed that the beetle and Lilly 1975a, 1975b). was introduced there about 1856 but he Crioceris asparagi spread steadily did not explain on what he based his throughout eastern U.S.A. at an estimat- assumption. In a footnote, he added: ed rate of 32 km/year, primarily by ‘‘The capture of this species was recorded human-mediated pathways such as early in the past century in Pennsylvania movement of root crowns of asparagus, – presumably near Hanover – and again or by ‘‘hitch-hiking’’ accidentally along in the vicinity of Chicago and Rock transportation corridors (road, train, Island, Illinois, about ten years after the boat, etc.), but also by water along discovery on Long Island; but, as the various waterways (Chittenden 1917). insect did not obtain a permanent Crioceris duodecimpunctata probably foothold, but died out in these localities, spread similarly after its detection in these importations can not be considered Baltimore, Maryland in 1881 (Chitten- introductions.’’ den 1917). Escaped plants from cultivat- Beetles probably entered the USA ed asparagus beds facilitated the spread during the commercial production of and establishment of C. asparagi and C. that period as adults or pupae in root duodecimpunctata throughout North crowns or with soil (Chittenden 1917, America, and both these species now Caesar 1938). However, there were prob- occur wherever asparagus is grown ably sporadic introductions earlier that commercially or as a volunteer crop were never noticed because of low (White 1993, Capinera 2001). By 1898, numbers or failure to establish due to C. asparagi was reported to occur in winter mortality or asynchronous host Buffalo, New York, and Berrien County, conditions. Various life stages, most Michigan (Chittenden 1898b), and along likely including eggs, may have been parts of the Niagara River just across transported with the movement of spears from Canada (Kilman 1899). or asparagus stems. A few such cases Both C. asparagi and C. duodecim- have been documented, but without clear punctata are usually considered to have reference to the life stage. Crioceris sp. been officially recognized as present in was intercepted in Hawaii in 1983 on Canada for the first time in 1899, with VOLUME 110, NUMBER 3 605 both species causing serious damage in For some reason, pest activity for both asparagus production areas in Queen- species remained unreported for many ston and other parts of the Niagara years in Canada during the period of Peninsula in Ontario (Fletcher 1900a, both World Wars. In 1948, C. duodecim- 1900b; Webster 1900; Chittenden 1907a, punctata was first reported in Morden, 1917). However, Provancher (1877) had Manitoba, and it was found to be already collected C. asparagi from the numerous in Winnipeg in the summer Que´bec City area 22 years before, but of 1954, but caused little damage (Mac- this occurrence has been overlooked by Nay 1955, Beirne 1971). many authors. Crioceris asparagi was first recorded in By the end of 1899 both asparagus the Maritimes in 1950 in Truro, Nova beetles had reached St. Catharines, Scotia and subsequently in 1952 from Lincoln, and Welland Counties in On- Fredericton, New Brunswick (Pond tario (Lochhead 1900). By 1900 they 1953). Its incursion into the Maritimes were near Hamilton, and by 1901 both coincided with outbreak population lev- beetles had reached Guelph where it was els in southern Ontario, and moderate noted that C. duodecimpunctata was damage levels in Montre´al and Que´bec more damaging (Fletcher 1902, 1904). City in 1952. Crioceris duodecimpunctata By 1902 this species was first recorded was also first recorded in the Maritimes from London (Balkwill 1903). Mean- in 1950 in Truro, Nova Scotia. Both while, C. asparagi had spread further species were present in low numbers in east to Bracondale near Toronto (Fletch- Truro and Kentville, Nova Scotia, in er 1904). In 1904 it continued to do some 1952, and shortly thereafter, in 1953, C. damage in the Niagara and St. Cathar- duodecimpunctata was also found on ines districts (Fletcher 1905). It was Prince Edward Island (Fox and Neary reported in large numbers in western 1953). Que´bec in 1903 (Kilman 1904). Beirne In Western Canada, C. duodecimpunc- (1971) stated that the asparagus beetle tata was first detected in British Colum- was found in Que´bec City in 1917, and in bia in 1962 (Beirne 1971, Capinera 2001). British Columbia in 1962. Crioceris asparagi was reported to be Crioceris asparagi was known to occur mainly a pest in the Lower Fraser Valley, in Ottawa in 1906, whereas C. duodecim- and sporadic on Vancouver Island and in punctata was not detected in Ottawa until the southern Okanagan (Banham and 1915 (Gibson 1916). Ross and Curran Arrand 1978). (1917) reported that the egg parasitoid T. Both asparagus beetle species are now coeruleus satisfactorily held in check the widespread across southern Canada, but beetle at Vineland Station of Agriculture neither is yet reported from Newfound- Canada. In his preliminary list of the land and Labrador (LeSage 1991). insects of Que´bec, Chagnon (1917) reported both species from the Island of METHODS AND CONVENTIONS Montre´al, Iˆle-Je´sus, and Saint-Jean-sur- Codens of collections (following Even- Richelieu. Twenty years later he stated huis 2007) referred to in the text are: that they both were common on asparagus without additional information on ACNS Agriculture and Agri-Food their distribution (Chagnon 1937). Canada, Kentville, Nova Sco- Crioceris asparagi and C. duodecim- tia, Canada punctata are characterized by intermit- ACPE Agriculture and Agri-Food Ca- tent periods of several years during nada, Charlottetown, Prince which populations may go undetected. Edward Island, Canada 606 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

CNC Canadian National Collection Linnaeus, 1758 as the type species (ICZN of Insects, Arachnids, and 1970, Opinion 908). Nematodes, Ottawa, Ontario At the beginning of the nineties, I. M. DHWC David H. Webster Collection, Kerzhner resubmitted the case of Geof- Kentville, Nova Scotia, Ca- froy’s work to the Commission (Case nada 2292), but this time for the conservation JOC Jeffrey Ogden Collection, of most of the genera published by this Truro, Nova Scotia, Canada author (Kerzhner 1991, Tubbs 1992). NSAC Nova Scotia Agricultural Col- With respect to the leaf beetle genera lege, Bible Hill, Nova Scotia, Altica, Crioceris, Cryptocephalus, and Canada Galeruca created by Geoffroy, the Com- NSMC Nova Scotia Museum Collec- mission reverted to the ruling of 1954 tion, Halifax, Nova Scotia, and recognized his Histoire abre´ge´e as Canada valid for nomenclatorial purposes, and NSNR Nova Scotia Department of also recognized the authorship of Geof- Natural Resources, Shubena- froy for many of the genera created in his cadie, Nova Scotia, Canada original work, including the four leaf UMNB Universite´ de Moncton, Mon- beetle genera mentioned above (ICZN cton, New Brunswick, Canada 1994, Opinion 1754). Recently, Schmitt (2005) proposed an The number of specimens is indicated official correction of the gender of in parentheses together with the collec- Crioceris Geoffroy to feminine (it was tion codens. recognized as masculine before, ICZN 1954). The case has not yet been ruled by NOMENCLATURE the Commission but the correction will In an application to the International very likely be accepted. Commission of Zoological Nomencla- There are distinct color variations in ture for a decision regarding the status C. asparagi and C. duodecimpunctata of the generic name Corixa Geoffroy with the result that over thirty varieties, (1762), H.B. Hungerford (1947) raised aberrations, or forms for each species the much broader question of the valid- were named by authors. These color ity for nomenclatorial purposes of the differences have no taxonomic signifi- whole work of this author, Histoire cance (White 1993, Riley et al. 2003). abre´ge´e des insectes qui se trouvent aux environs de Paris. In a first decision, the IDENTIFICATION Commission placed Geoffroy’s entire Within the family Chrysomelidae, the work in the Official Index of Rejected leaf beetles, members of the subfamily and Invalid Works in Zoological No- Criocerinae are easily recognizable by menclature (ICZN 1954, Opinion 228). lateral slopes of the pronotum that are In the late sixties, B. J. Selman and R. rounded without a marginal bead, and F. Smith appealed to the Commission in by their elytral punctures arranged into order to clarify the generic status of regular rows (Figs. 1–2). Within the Crioceris Mu¨ller, 1764, and Lema Fabri- subfamily Criocerinae Crioceris Geof- cius, 1798 (Selman and Smith 1967, froy, 1762 is characterized by tarsal 1968). Three years later, the Commission claws that are broadly divergent from ruled that Crioceris Mu¨ller was a mas- the base and by a pronotum that is not culine genus and designated under the markedly constricted in the middle, as in plenary powers Chrysomela asparagi Lilioceris Reitter, 1912. VOLUME 110, NUMBER 3 607

Fig. 1. Habitus of Crioceris asparagi (dorsal view). 608 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

Fig. 2. Habitus of Crioceris duodecimpunctata (dorsal view). VOLUME 110, NUMBER 3 609

Both species are very easy to recognize Chittenden (1896). Larvae of both spe- since their color pattern is unique among cies can be keyed out using the key of the Canadian leaf beetle fauna. Crioceris Sailsbury (1943). The egg bursters are asparagi is multicoloured (Fig. 1). In present on a heavily sclerotized tubercle most specimens of eastern Canada the dorsal to the spiracle on abdominal appendages are black, the elytra also are segment I in the first instar larva (Cox black but with metallic bluish reflections. 1994). A photograph of a live mature In addition, the elytra bear three pairs of larva is given by Metcalf and Flint (1939, white spots of variable size and the 1962) and by Howard et al. (1994), a lateral margins vary from yellow to lateral view in Drake and Harris (1932) reddish, often with an enlargement at and Hutchinson et al. (2005). the apex. The pronotum is reddish with a Chittenden (1896, 1908) illustrated the more or less poorly defined dark spot on ventral view of the pupa of C. asparagi. the disc. C. duodecimpunctata (Fig. 2) is Fink (1913) gave photographs of the largely bright reddish orange with black ventral and dorsal views of the pupa antennae, black apex of the femora, and of C. duodecimpunctata. Unfortunately, six pairs of small round black spots on these illustrations do not allow for the the elytra. Both species are treated in recognition of species and detailed de- Chagnon (1937, 1940), Chagnon and scriptions of both are still needed. Robert (1962), Swan and Papp (1972), The complete mitochondrial DNA White (1993), Howard et al. (1994), and sequence of C. duodecimpunctata is Downie and Arnett (1996). A field key is known (Stewart and Beckenbach 2003). found in Metcalf and Flint (1939, 1962). Compositions of the mitochondrial ge- The eggs of C. asparagi were sketched nome were reported to be similar to by Walsh and Riley (1868), Wickham other insects in general. Distinct features (1896), Chittenden (1896, 1908, 1917), of this genome included the substitution Balachowsky and Mesnil (1936), Drake of UCU for GCU as the anticodon for and Harris (1932), and Parrott and tRNASer, an unusual T psi C loop for Huckett (1944), and a photograph of the tRNAIle gene, and the identification eggs on spears was provided by Metcalf of a putative ATT start codon for cox1 and Flint (1939, 1962) and by Howard et (Stewart and Beckenbach 2003). al. (1994). The eggs of C. duodecimpunctata were illustrated by Chittenden BIOLOGY (1898a, 1907b) and Drake and Harris The asparagus beetles pass the winter (1932). However, the fine structure of the in the adult stage, hibernating under egg chorion of both species is still sticks, stones, litter, bark, rubbish, or unknown. any other suitable shelter. They also may Habitus of Crioceris larvae and illus- be found in numbers inside the cavity of trations of the head, mouthparts and legs asparagus stems or other plants (Drake are found in Chittenden (1908), Bøving and Harris 1932). Adults of C. asparagi and Craighead (1931), Sailsbury (1943), emerge from hibernation in late April or Peterson (1951), and Lawson (1991). The early May when asparagus sprouts start head is dark brown, the labrum narrowly to emerge from the soil. They feed for a notched and the body tan in C. asparagi, few days before mating and ovipositing. whereas the head is light brown, the Feeding damage and eggs laid on spears labrum broadly notched and the body make the spears unmarketable (Hutch- off-white in C. duodecimpunctata (Law- inson et al. 2005). The eggs are cylindri- son 1991). A lateral view of the second cal, greenish grey to brownish, and about abdominal segment was provided by 1–2 mm long; they are always deposited 610 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON endwise upon the spears or on the foliage black coloration is avoided by predators either separately or in up to 7 (Chit- and stridulating may protect them by tenden 1908), or 11 eggs per row startling the predator and causing it to (Balachowsky and Mesnil 1936). Eggs release its hold (Haskell 1961, Retten- hatch after about twelve days, the time meyer 1970). needed largely depending on local tem- According to Campbell et al. (1989), peratures. Larval development passes referring to populations in Canada, C. through four instars and takes 2–3 weeks asparagi is trivoltine with egg-laying to be completed. According to Taylor peaks in June, early July, and early and Harcourt (1978), the optimum tem- August. Adults of the third generation peratures for eggs and larval instars I overwinter in dead stalks of asparagus, and II is 32uC, but 30uC for the larval in the ground litter, or any other instars III and IV and the pupa. convenient shelter. No information is The larvae are eruciform, their body available on the exact number of gener- grayish, the head and appendages black. ations in the Maritimes, but there are Each abdominal segment is provided probably two complete generations and with a pair of tubercles which, with the a partial third one as in Massachusetts aid of the anal prolegs, help in crawling (Capinera and Lilly 1975a). Chittenden and climbing the plants. Hutt (1900) (1917) estimated the time needed from observed that when approached the the egg to the emergence of the adult at larvae had the peculiar habit of raising Long Island, New York as 30 days. The their heads and excreting a dark viscid development time for C. asparagi should fluid. When mature, the larvae drop to be of this order in the Maritime Prov- the ground. They build a pupal cell by inces. packing and mixing soil particles with The biology of C. duodecimpunctata their saliva. Only the inside of the cell is was described by Fink (1913) in New covered with a silken secretion. Conse- York State and by Beaulne (1935) in the quently, the pupal cells are not exactly province of Que´bec. Fink (1913) stated ‘‘cocoons spun by the larvae’’ as stated that both asparagus beetle species by Armand (1949). The pupa is yellow. emerged in early spring at almost the Adults emerge from the pupal cells in same time, but Beaulne (1935) men- 7–10 days. tioned that C. duodecimpunctata emerged The bright coloration of adult C. from hibernation a week later. Accord- asparagi is aposematic, and the beetles ing to our own observations, both are commonly avoided by predators species have been collected together in (Jones 1932). Lutz (1908) found that, the spring in eastern Canada. when a normal C. asparagi with three In contrast to C. asparagi, the ovipo- yellow spots on blue-black elytra was sition of C. duodecimpunctata occurs crossed with a variety where the upper much later, not before the berries have spot was united with the middle one, the begun to form by the middle of June or normal form was dominant. According later (Chittenden 1898a, Fink 1913). to Capinera (1976), the first defensive Meanwhile, adults attack the sprouting behavior of C. asparagi adults is to shoots in the same manner as do those of dodge to the opposite side of stems. C. asparagi. Later, when the shoots have With persistent stimulation, beetles will begun to branch out, they feed mainly on feign death or run to another part of the stalks and branches, gnawing out large plant. Crioceris duodecimpunctata adults pieces of their epidermis. They will respond quite differently to stimuli, by extend their feeding to flowers and taking flight and stridulating; their red- berries when these appear. Eggs are not VOLUME 110, NUMBER 3 611 laid in conspicuous rows as in C. similar number is expected for the asparagi but instead singly, on the side, Maritimes. The adults of the first new and hidden among narrow branches, generation emerge in late July while preferably those with berries. Their those of the second generation appear incubation lasts 7–12 days. After hatch- in September (Armand 1949). ing, the young larvae wander about the stems until they find a berry. As soon as PREDATORS one is located, the larvae will bore into it References to avian predation on between the two sepals of the calyx. asparagus beetles are few. House spar- Although up to four berries will be rows (Passer domesticus (Linnaeus)), and utilized throughout their development eastern kingbirds (Tyrannus tyrannus until they mature, Fink (1913) never (Linnaeus)) were reported by Beal observed more than one larva per berry. (1912) to consume adults, but Capinera The larvae have the ability to discrimi- (1976) stated that North American birds nate between occupied and unoccupied were probably accidental predators. Ac- berries which accounts for their consis- cording to Drake and Harris (1932), tent singular distribution amongst aspar- chickens and ducks destroy asparagus agus berries (Alphen and Boer 1980). beetles and may be used under favorable Females of C. duodecimpunctata do not conditions. oviposit on or in the asparagus berries in The coccinellid beetles, Coleomegilla which the larvae feed, and therefore this maculata (De Geer, 1775) and Hippoda- distribution of a single larva in each mia convergens (Gue´rin-Me´neville, 1842), berry cannot be the result of ovipositing are efficient predators of eggs and larvae females (Alphen and Boer 1980). The (Chittenden 1896, 1898a, 1908, 1917; larvae spend several days inside the Watts 1938). Capinera and Lilly (1975a) berries, eating only the soft juicy pulp. interpreted the decrease of C. asparagi Before leaving for a second berry, the eggs during the increase of coccinellid larva molts and the cast skin is found populations as a response of the latter to inside the discarded berry. After the the diminishing numbers of aphids, their second molt a larva can eat an entire larvae being forced to feed on whatever berry in less than a day. Berries are food is available. Large carabids such as mildly poisonous to humans (Plants for a Poecilus lucublandus Say, 1823, Pterosti- Future 2007). chus melanarius Illiger, 1798, Harpalus There are four larval instars as in C. pennsylvanicus De Geer, 1774, and Har- asparagi, although Fink (1913) and palus erraticus Say, 1823 are presumed to Beaulne (1935) erroneously reported consume mature larvae when these drop only three. The larvae mature in 3– to the ground to pupate (Capinera and 4 weeks, and, like those of C. asparagi, Lilly 1975a). The melyrid beetle, Collops drop to the ground where they make quadrimaculatus (Fabricius, 1798), fed silken cells in which they pupate. Pupa- freely on eggs and larvae of Crioceris in tion lasts 12–20 days in Ithaca, New confinement (Chittenden 1898a). York (Fink 1913). Adults overwinter in Chittenden (1896, 1907b, 1917) report- plant debris or other suitable shelters ed that the stink bugs (Pentatomidae) (Banham and Arrand 1978), and like Podisus maculiventris (Say, 1832) and those of C. asparagi can stridulate by Stiretrus anchorago (Fabricius, 1775) rubbing the tip of the abdomen against devoured the larvae of C. asparagi, but the elytra (Dingler 1932, Schmitt 1994). the latter does not occur in Canada According to Caesar (1938) there are two (Maw et al. 2000). Drake and Harris generations per year in Ontario, and a (1932) gave a photograph of P. maculi- 612 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON ventris piercing the body of an adult C. develops no further because by this asparagi. The nabid bug, Nabis rufuscu- time it has been completely devoured lus Reuter, 1872, was commonly ob- by the parasitic larvae which will pupate served to prey on larvae earlier in the within the host pupal cell and later season, whereas the reduviid bug, Sinea emerge as an adult (Capinera and Lilly diadema (Fabricius, 1776), was an occa- 1975b). sional predator (Capinera and Lilly The level of egg parasitism or feeding 1975a). can be very high. The parasitoid females The vespid wasp, Polistes fuscatus are avid feeders on the beetle eggs and (Fabricius, 1793), hovers over infested may consume a greater number of eggs plants, pounces upon larvae, and carries than they parasitize. Johnston (1915) them away (Chittenden 1917). found that of 2,097 eggs counted, Chittenden (1898a) noticed the dam- 71.3% had been destroyed by the feeding selfly, Ischnura positum (Hagen, 1861), by the parasitoid females. According to flying about infested asparagus, seize Capinera and Lilly (1975a), 50% of the small larvae and fly off with them. eggs of C. asparagi were destroyed by Ischnura species are peculiarly adept at this parasitoid through feeding, and picking small insects from foliage (West- nearly 50% of those not fed upon were fall and May 2006). parasitized. At L’Assomption, Que´bec, The neuropteran chrysopid, Chrysopa Hendrickson et al. (1991) observed oculata Say, 1839, is an occasional 39.1% of parasitism in the first genera- predator of the larvae (Capinera and tion and 49.2% in the second during the Lilly 1975a). years 1980 to 1987. Tetrastichus coeruleus is a monophagous parasitoid of PARASITES C. asparagi and does not accept The European hymenopteran eulo- C. duodecimpunctata as a host, whereas phid, T. coeruleus (Nees, 1834), usually T. crioceridis (Graham 1983) feeds reported in North America as T. aspar- and parasitizes exclusively the eggs of agi was placed in synonymy by Graham C. duodecimpunctata. This parasitoid has (1961, 1991). The ‘‘black parasite fly not yet been recorded in North America. Chalcis or Proctotrupes’’ reported by The hymenopteran ichneumonid, Le- Walsh and Riley (1868) corresponds to mophagus crioceritor Aubert, 1986, is T. coeruleus. The parasitoid was formally probably established in Canada and identified for the first time in Canada in favored by cooler latitudes. A parasitism 1915 at the Agriculture Canada Vineland level of 8.9% was measured at L’As- Research Station, Ontario, by Ross somption, Que´bec, and 15.7–24.8% at (1915). the Cambridge Research Station of the The parasitoid female pierces the egg University of Guelph, Ontario, where the of the beetle with its ovipositor and parasitoid was released in 1987 (Hen- deposits therein 3–9 eggs (Beaulne 1935, drickson et al. 1991). Harmer et al. Van Alphen 1980). She is also able to (1990), also at Guelph, estimated the discriminate between unparasitized and annual rate of parasitism at 19.5%; that parasitized eggs after checking with is, 15.7% for the first generation and antennae or probing with the ovipositor 24.8% for the second. (Van Alphen 1980). The egg of the In 1939, 9,500 puparia and 17,825 host asparagus beetle host is not visibly larvae from France parasitized by the affected, hatches and develops into tachinid fly, Meigenia mutabilis (Falle´n, normal larval stages, but when the larva 1810), were introduced into the United falls to the ground for pupation it States of America and released at several VOLUME 110, NUMBER 3 613 infestation points in New Jersey. The flowers are dioecious with both male and parasite failed, however, to establish female plants. Generally, female plants either because it could not survive produce larger spears than the male through the winter or because of the plants (Hutchinson et al. 2006). The lack of a suitable alternate host (Clausen flowers are small, greenish yellow, and 1956, 1978). Another tachinid fly, Myio- fixed on jointed pedicels. Honeybees are pharus (Paralispe) infernalis (Townsend, not needed for pollination in asparagus, 1919), a native species, has been reared but they are very common when the from larvae of C. asparagi, but it is an plants are flowering in mid- to late uncommon parasitoid (Watts 1938, Ca- summer (Hutchinson et al. 2005). Of pinera and Lilly 1975b). It produced only interest for the production of an exclu- 2.1% parasitism at the Beneficial Insects sively male plant is the indirect impact Research Laboratory, in Saint-Bruno- for control of the larvae of C. duodecim- de-Mortarville, Que´bec (Hendrickson et punctata since these develop in berries al. 1991). (produced only by female plants). The Impudentia crioceris Vujanovic is a filiform so-called ‘‘leaves’’ are actually newly discovered dematiaceous hypho- branchlets, functioning as leaves, clus- mycetous fungus that is found on C. tered in the axils of little scales which are asparagi and C. duodecimpunctata from the true leaves (Fernald 1970). The fruits asparagus fields in Quebec, Canada are red round berries produced only by (Vujanovic et al. 2003). female plants. The propagation of asparagus can be done by seeds or roots. HOST PLANT Asparagus which has escaped from Asparagus is a perennial salt-tolerant cultivation is spread by seeds dissemi- herbaceous plant that has both wild and nated by birds (Haughton 1978). Culti- domesticated forms. It is believed to be vated plants are usually duplicated by native to the region east of the Mediter- splitting older root crowns into smaller ranean Sea and the Middle East (Fara bundles. Ornamental varieties are pro- 2007). In Canada, the domesticated form duced in the same manner. Commercial escaped from cultivation and can be asparagus plantations can be established found as a naturalized plant across either by traditional crown planting or southern regions of the country, except by transplanting seedlings (Hutchinson Saskatchewan (Monro and Small 1997). et al. 2006). A well established asparagus It is also found in the waste steppes of bed can be profitable for 15–20 years. southern Poland and Russia (Ohioline The new shoots are sold fresh, frozen, or 2007). Volunteer plants from seeds serve canned. as a reservoir for asparagus insects and Crioceris asparagi and C. duodecim- asparagus rust during harvest, after all punctata are both monophagous in other asparagus plant material is re- North America since they feed exclusive- moved from commercial fields (Hutch- ly on A. officinalis, but are oligophagous inson et al. (2005). in the Old World because they develop Asparagus consists of thick matted on other species and varieties as well (see rootstocks from which emerge branched extended bibliography in Clark et al. stems, 1–2 m tall, which are produced 2004). annually (Hutchinson et al. 2006). The edible parts are the succulent shoots, or DISTRIBUTION spears, as they issue from the crown and The distribution of C. asparagi and C. emerge above the ground. The later duodecimpunctata in the Maritime Prov- shoots develop into large bushes. The inces of Canada is shown in Fig. 3. Both 614 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

Fig. 3. Distribution of Crioceris asparagi (open circles) and C. duodecimpunctata (closed circles) in the Maritime Provinces of Canada. species are newly recorded in Nova Kentville, 11.VI.1995, D.H. Webster, Scotia and C. duodecimpunctata is newly (1, DHWC). recorded on Prince Edward Island since Crioceris duodecimpunctata.—A total publication of the latest checklist of the of 117 specimens were examined. beetles of Canada (LeSage 1991). NEW BRUNSWICK: Sunbury Co.: Crioceris asparagi.—A total of 32 Hoyt, 4.VI.1987, host Asparagus, D.B. specimens were examined. Finnamore, (1, CNC); York Co.: Fre- NEW BRUNSWICK: Gloucester Co.: dericton, 4–30.VII.1955, ex goldenrods Tracadie, 2.VIII.1978, S. Poirier, (1, with Macrosiphum ambrosiae Thomas, UMNB). B.C. Smith (8, CNC). NOVA SCOTIA: Antigonish Co.: NOVA SCOTIA: Colchester Co.: Shu- Antigonish, 15.VI.2006, M. Workman, benacadie, 8.VII.2002, J. Ogden, (1, (3, NSNR); Colchester Co.: Bible Hill, NSNR); Truro, 1.VII.1950, V.R. Vickery, 28.V.1998, T.D. Smith, (12, NSAC); (3, NSAC); Truro, 18.VII.1950, V.R. Truro, 18.VII.1950, V.R. Vickery, (2, Vickery, (16, NSAC); Truro, 11.VIII. NSAC); Truro, 11.VIII.1950, V.R. Vick- 1950, V.R. Vickery, (1, NSAC); Truro, ery, (9, NSAC); Kings Co.: Wolfville, 11.IX.1975, A.M. Bubar, (1, NSAC); 28.VI.1996, D. de Geus, (1, ACNS); Cumberland Co.: Oxford, 2.VIII.1990, J. VOLUME 110, NUMBER 3 615

Ogden, (1, JOC); Nappan, 19.XI.1975, the North Atlantic States through the D.A. Smith, (2, NSAC); Halifax Co.: open gateway into the interior of the Dartmouth, 24.VIII.1988, K. McKay, (7, continent past lakes Ontario and Erie. NSMC); Dartmouth, 16.VI.1991, R. Sir- Clearly, both asparagus beetles were able com, (3, NSMC); Kings Co.: Kentville, to acclimatize to cold temperatures 26.VII.1961, C.J.S. Fox, (4, ACNS); encountered in North America com- Kentville, 5.IX.1961, R.L. Horsbourgh, pared to their native range. Thus, they (71, NSAC); Kentville, 6.IX.1961, R.L. have been able to survive and spread Horsbourgh, (6, NSAC); Kentville, successfully throughout their new conti- 3.VII.1973, D.H. Webster, (1, DHWC). nental environment. PRINCE EDWARD ISLAND: Queens Another possibility is that both species Co.: Charlottetown, 10.VII.1953, F.M. of asparagus beetles survived for decades Cannon, (1, ACPE). unnoticed until they could survive the winters in greater numbers. The commer- DISCUSSION cial production initiated soon after 1860 Although both species of Crioceris helped in building larger populations. were reported as occurring in Nova Such pattern of appearance, apparent Scotia by Fox and Neary (1953) and disappearance, and reappearance in num- MacNay (1955), this information was bers is known for the lily leaf beetle overlooked by LeSage (1991); thus, the (Lilioceris lilii Scopoli, 1763). This beetle present paper confirms their presence in almost disappeared for forty years prior this province. However, C. duodecim- to spreading rapidly from Montre´al punctata is newly recorded as occurring where it was first discovered in 1943 on Prince Edward Island from a speci- (LeSage 1983). According to Provancher men collected in 1953. Since both species (1877), C. asparagi was present at Cap- feed exclusively on asparagus, their Rouge near Que´bec City that year. We distribution in the region is limited to have examined the voucher specimens places where asparagus is cultivated, or preserved in his collection housed at the where it has escaped and has been Universite´ Laval, in Que´bec. Although naturalized, primarily in agricultural not mentioned by Provancher (1877), areas of the region. None of the two specimens of C. duodecimpunctata were beetle species has yet been found in also preserved in his collection. Conse- Newfoundland, although asparagus is quently, it is evident that both species cultivated there in gardens (D. Larson, were thriving 22 years before the official S. Pardy, and J. Coombes, personal date of introduction into Canada (1889) communication). The earliest document- in a location completely separate from the ed date of introduction known for C. known infested areas of the United States. asparagi in Astoria, New York is 1859 We don’t know, however, if these early (Fitch 1865), although Chittenden (1908) populations disappeared or survived long estimated that it was already present enough to merge with those originating there by 1856. from southern Ontario and which even- Both asparagus beetles were probably tually spread northeastwards. The two repeatedly introduced for more than two asparagus beetle species were rediscov- centuries but did not survive or could not ered in Que´bec City in 1917 (Chittenden establish before the sixties of the nine- 1917, Beirne 1971), and Kilman (1904) teenth century. As Webster (1902) has reported the occurrence of C. asparagi in shown, one of the main lines of migra- abundance in Que´bec in 1903. tion and spread of insects in North It is well known that a large number of America has been from New York or adventive insect and plant species were 616 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON introduced to North America in ships’ ACKNOWLEDGMENTS ballast (Lindroth 1957, Sheffield 1990, Thanks are extended to Susan Westby Buckland et al. 1995). This is true for soil and Cory Sheffield (Agriculture and dwelling insects but not likely for adults Agri-Food Canada, Kentville, NS), or larvae of asparagus beetles which Christine Noronha and Mary Smith thrive on plants. The first vegetables to (Agriculture and Agri-Food Canada, become of importance in the new colo- Charlottetown, PE), Jean-Pierre Le nies appeared to have been the roots. Blanc (Nova Scotia Agricultural Col- Numerous cargo lists included ‘‘roots,’’ lege), Jeffrey Ogden (Nova Scotia De- and in addition to root-crops commonly partment of Natural Resources), Pauline found in gardens, settlers were experi- Duerr (Universite´ de Moncton), Jean- menting with asparagus and other vege- Marie Perron (Universite´ Laval, Que´bec) tables. Asparagus root crowns were and David H. Webster (private collec- probably used regularly because they tion) for making specimens and records were easy to dig out (in Europe), available. We also acknowledge the transport by ship, and replant in a new generous assistance of Pierre Moriset environment (in North America). Vege- (Universite´ Laval, Que´bec City). We tative propagation produces new spears thank Klaus Bolte (Agriculture and quickly and is much faster than starting Agri-Food Canada, ECORC Ottawa) production from seeds. Asparagus beetle for executing the habitus photographs adults may have been hiding in the root and Heather Auld and Kristina Verhu- crowns, and could have crossed the fen (Agriculture and Agri-Food Canada, ocean by means of this pathway. Cer- ECORC, Ottawa) for assistance with the tainly eggs or other life stages attached to literature search. C.G. Majka thanks transported spears could have been David Christianson, Calum Ewing, An- introduced in this way, but interceptions drew Hebda, and the Board of Gover- are not well documented. The European nors of the Nova Scotia Museum for obligate endoparasite T. coeruleus was ongoing support. We would like to thank found in 1863, only a few years after the D.E. Watler, J.A. Garland and E.A. discovery of the asparagus beetles. Its Snyder (Plant Health Risk Assessment presence in North America can be Unit, Canadian Food Inspection Agen- explained only by the (unintentional) cy, Ottawa) for review of earlier drafts of introduction of parasitized eggs. The this manuscript. Shawn M. Clarke read a early introduction of T. coeruleus which previous version of the manuscript and established successfully in Canada prob- made many constructive suggestions. We ably significantly controlled C. asparagi also thank Dave Larson (Maple Creek, populations, as commercial asparagus SK), Shelly Pardy (Corner Brook, NL) farms were being developed in the New and Janet Coombes (Agriculture and World. Now, pesticides with little resid- Agri-Food Canada, St. John’s, NL) for ual toxicity levels are used to prevent information with respect to the status of adult egg laying on spears which are both asparagus beetles and their host in harvested daily (Capinera 2001, Wold- Newfoundland. Burkness et al. 2007). Neither C. asparagi nor C. duodecim- LITERATURE CITED punctata are regulated by Canada or by Alphen, J. J. M. van. and H. Boer. 1980. the U.S.A., and they are readily con- Avoidance of scramble competition between trolled at economically acceptable dam- larvae of the spotted asparagus beetle, Crio- age thresholds. ceris duodecimpunctata L. (Chrysomelidae) by VOLUME 110, NUMBER 3 617

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