Biological control of Rumex species in Europe: opportunities and constraints
P.E. Hatcher,1 L.O. Brandsaeter,2 G. Davies,3 A. Lüscher,4 H.L. Hinz,5 R. Eschen5 and U. Schaffner5
Summary The increasing problems caused by dock infestations (especially Rumex obtusifolius L., R. crispus L., and R. longifolius DC.) to organic agriculture in Great Britain, Norway and Switzerland are discussed. Inadequate, costly, or time-consuming non-chemical control options for Rumex are among the major barriers for farmers converting to organic production. Potential biological control agents for Rumex in Europe are discussed. We conclude that the chrysomelid beetle Gastrophysa viridula Degeer and the rust fungus Uromyces rumicis (Schum.) Wint. remain the most promising of the researched indig- enous species and that G. viridula can be combined with other non-chemical control methods. How- ever, there is a need for biological control agents that target dock roots; we suggest that Pyropteron chrysidiformis (Esper), one of several sesiid moth species present in Europe which attack dock roots, has good potential for Rumex spp. biological control and merits further study within Europe.
Keywords: dock, organic farming, Rumex crispus, Rumex longifolius, Rumex obtusifolius.
Introduction we examine this problem as well as recent and ongo- ing research into it in three European countries—Great Docks, especially Rumex obtusifolius L. and R. crispus Britain, Switzerland and Norway. We discuss possible L., have been recognized as problem weeds in conven- biological control methods (none of which are current- tional agriculture for centuries (Foster, 1989; Zaller, ly used in Europe) and our recommendations for the 2004). These species grow rapidly, are resilient to cut- way ahead in Europe. Of course, this paper only gives a ting (being able to quickly regrow from their root stock, snapshot of the situation in three countries and there is and replenish carbohydrates used in regrowing within much work also taking place in other European coun- two to three weeks), are long-lived and are able to pro- tries—for example, Germany (Zaller, 2004), the Czech duce up to 80,000 seeds per plant per year (Cavers and Republic (Martinková and Honĕk, 2004) and Austria Harper, 1964). These seeds form a long-lasting soil seed (Hann and Kromp, 2003). Also, as we do not intend to bank with seeds surviving for possibly up to 80 years review the voluminous work on non-chemical control (Cavers and Harper, 1964). More recently, docks have of Rumex spp., readers are referred to Foster (1989), been recognized as a serious problem for organic agri- Hatcher and Melander (2003), Zaller (2004) and Bond culture and an important limiting factor in the conver- et al. (2006) for this. sion from conventional to organic farming is thought to be the worry of many farmers over their ability to con- The problems trol docks without chemical herbicides. In this paper, Great Britain In January 2005, a total of 690,269 ha of agricul- 1 School of Biological Sciences, The University of Reading, Reading, tural land in the UK was registered as organic or in UK. 2 Bioforsk, Norway. conversion to organic; just over 4% of all agricultural 3 HDRA, Ryton Organic Gardens, Coventry, UK. land (FiBL, 2006). Of this, 92% was fully organic and 4 Agroscope Reckenholz-Tänikon, Research Station ART, Zurich, the retail market for organic products in the UK was Switzerland. worth GBP 1.213 billion in 2006. The problem caused 5 CABI Europe-Delémont, Switzerland. Corresponding author: P.E. Hatcher
470 Biological control of Rumex species in Europe: opportunities and constraints
(DEFRA)-funded research programme into the man- sward density and prevent gaps are successful against agement of weeds in organic production systems, car- the new establishment of dock plants, and root competi ried out by the Henry Doubleday Research Association tion was much more important than shoot competition (HDRA) (Turner et al., 2004, 2007). Of those farmers [this has also been shown for R. longifolius in Norway surveyed, 92% listed Rumex spp. as one of their main (Haugland, 1993)]. Such cultural control methods must problem weed species. Farmers had a clear understand- be part of a holistic management strategy if the weed is ing of what encouraged docks in their systems (e.g. to be controlled (LBL Bericht, 2001; Niggli, 2005) and poaching, inappropriate or untimely cultivation) and should focus on preventing the establishment of new many thought that their dock problems were historical dock plants (Dierauer et al., 2007). Due to the restric- and had persisted due to poor weed management prior tions on control methods in organic farming, biologi- to organic conversion. The general approach to control cal control is a logical tool to be integrated into such was to prevent dock seeding and to reduce their vigour a strategy. by harvesting crops before docks seeded, keeping mar- gins clean, planning control periods into rotations and the use of grazing stock. Direct action included various Norway integrated topping and grazing strategies, with many Organic farming started in Norway in the 1930s, but farmers using topping machinery. Sheep were used to there were few such farms until the 1970s. A national intensively graze young seedlings, and goats to strip organic certification procedure was adopted in 1986, mature plants. Manual removal was also used at times, with 19 farms being certified originally, and since then and periods of summer fallow were used to cultivate the number of organic farms has increased steadily. In the land, cutting roots below 10 cm and exposing the 1996 there were 946 farms of 7900 ha total (0.8% to- roots on the surface to desiccate (to prevent regrowth). tal agricultural land) (Johnsen and Mohr, 2000), while Raking off these roots and burning them was effective. by 2006 there were 2500 farms of 38,798 ha (3.8% of agricultural land) (Debio, 2006). At 13 ha, the average organic farm size is slightly larger than that of conven- Switzerland tional farms, and almost all are run as family farms. Switzerland was one of the pioneers in organic The current national ‘plan of action’ aims for 15% farming, and there were already 500–1000 such farms of agricultural land to be organically farmed by 2015 in the 1960s (Niggli, 2005). From the 1940s there was (www.regjeringen.no). a steady increase in conversion to organic farming and Over 80% of organic agricultural land in Norway is since the 1990s this conversion has increased rapidly: in under grassland, meadows or green manure, 15% under 1990 there were 803 organic farms totalling 10,000 ha; cereals, with little organic horticulture (Debio, 2006). by 2005 there were 6462 of 112,000 ha comprising Thus, grassland weeds are a major problem. A report roughly 10% of farms and cultivated land in the country from Sweden (Andersson, 2005) states that many farm- (Niggli, 2005). These farms are typically small, with an ers feel powerless to control their Rumex problem, and average size of 14 ha in 1998. Farmers in Switzerland some organically motivated farmers are prevented have identified R. obtusifolius and other dock species from converting to organic production because of this. (e.g. R. crispus, R. alpinus L.) as a major limitation to This applies also to Norway. Along with R. crispus and plant production on existing organic farms and a seri- R. obtusifolius, R. longifolius DC is also present in Nor- ous obstacle to conversion to this type of production way. It is the most widespread weedy Rumex species (LBL Bericht, 2001). Organic farmers are typically (Fykse, 1986) and is one of the most troublesome di- prepared to put considerable time into weed control cot species in Norwegian grasslands (Haugland, 1993). with some devoting over 1000 man-hours per year to R. longifolius can grow up to 1250 m above sea level; dock control alone (Grossrieder and Keary, 2004) but it develops much faster in the spring and forms twice as this amount of effort is not feasible for all farms and is many shoots from root fragments but regrows slower obviously limited by economics. Large-scale physical after defoliation than R. crispus and R. obtusifolius control using machines was not suitable as it causes (Fykse, 1986). A major Norwegian study has started to soil disturbance and this promotes dock seedling estab- investigate the natural enemies and control options for lishment. Variation in cultural control methods, such R. longifolius and other Rumex spp. in Norwegian or- as cutting height and frequency, grass species sown, ganic agriculture (Brandsæter and Haugland, 2007). and added nutrients have all been found to have only limited effects on dock populations. A review of these grassland experiments (Lüscher et al., 2001) demon- Biological control strated that all these management options did not sig- nificantly reduce the competitive ability of established Insects R. obtusifolius plants. Dock seedlings, however, have Grossrieder and Keary (2004) have reviewed recent a much weaker competitive ability than most sown studies on potential insect biological control agents for grasses. Consequently, all measures that increase grass Rumex spp. Much of the research reported here was
471 XII International Symposium on Biological Control of Weeds carried out on European species of potential for Rumex Gastrophysa viridula is the most-studied dock in- and Emex biocontrol in Australia, and has concentrated sect. It has up to four generations a year in Europe, on agents with a southern European, or Mediterranean overwintering as an adult in the surface layers of the distribution, to match that of Australia. It is unlikely soil, and passing through a generation in six weeks in that these species will be suitable for biological control favourable conditions throughout the spring to autumn. in the three central and northern European countries The species can show a large population increase dur- considered here, ruling out species such as Lixus crib- ing the year; with females able to lay over 1000 eggs ricollis Boheman (Col., Curculionidae) and Synans- each. Outbreaks of this insect have been reported, phecia doryliformis (Ochsenheimer) (Lep., Sesiidae). stripping Rumex plants of leaf material. Although Mar- Nor is it likely that introducing non-indigenous bio- tinková and Honĕk (2004) report that it will feed upon logical control agents will be feasible in Europe within nine other plant families, it can only complete its life- the near future, due to the current regulatory climate. cycle on Rumex spp. and prefers R. obtusifolius to other There is only one species in this category that might be docks (Bentley and Whittaker, 1979). Dispersal of the worth investigating at present: Gastrophysa atrocyanea beetle is limited; it has been rarely observed to fly and Motschulsky (Col., Chrysomelidae) from Japan, which tends to occur in discrete patches. Martinková and is probably the most promising insect for classical bio- Honĕk (2004) suggest that the beetle has become more logical control of R. obtusifolius. widespread in central Europe during the 20th century, Within Europe, we need to concentrate on those in- with a recent expansion since 1950 with the spread of sect species that can cope with the current management weedy docks in lowlands during the formation of large regimes used against docks (e.g. cutting, ploughing, farms. G. viridula can cause up to 50% reduction in dry removal before flowering) and this eliminates further weight of R. obtusifolius during the first year of growth species. For example, several species of Apion wee- (Hatcher et al., 1997), up to 80% shoot and 65% root vils are found on Rumex. These mainly bore into the reduction of R. crispus and R. obtusifolius first-year flowering stem as larvae, and adults emerge in July to overwintering plants (Hatcher, 1996), and can cause up August, after flowering. However, no organic farmer is to 70% reduction of dry mass and 65% reduction in likely to leave a flowering Rumex in their fields if they seed production in the first four years ofR. obtusifolius can help it, although this could be considered in uncul- growth in the field (Hatcher, unpublished data). tivated areas. Biocontrol agents should also be easy to Several species of clearwing moth may be suitable rear or culture for potential inundative releases. biological control agents. While Synasphecia dory- Brachycaudus rumexicolens (Patch) (Hom., Aphi- liformis has a Mediterranean distribution, the closely didae) is recommended for further study by Grossrie- related Pyropteron chrysidiformis Esper (Lep., Sesii- der and Keary (2004). First discovered in the US in dae) is native throughout western Europe and southern the early 20th century, this species is confined mainly England, but has not been recorded from Scandinavia to the Polygonaceae (Scott and Yeoh, 1998), especially (Spatenka et al., 1999). As in the case of S. dorylifor- Rumex and Emex, although it can also attack Lupinus mis, the species is univoltine and the larvae feed in the albus L. and Triticum aestivum L. and it may also be roots of various Rumex spp. (Spatenka et al., 1999). a virus vector. Nevertheless, the aphid was considered Synasphecia doryliformis, which was mass-released sufficiently safe to be used in a programme aimed at the into Australia in the early to mid-1990s as a biologi- biological control of Emex australis Steinh. in Australia cal control agent against docks (Fogliani and Strick- (Scott and Yeoh, 1998). This sap-feeding insect caused land, 2000), reduced dock densities there by up to 90% widespread death and stunting of Emex, reducing indi- within five years of release (Faithful, 2000). Scott and vidual achene weight by 41% (Scott and Shivas, 1998), Sagliocco (1991a, b) considered P. chrysidiformis to be and has a high intrinsic rate of increase [rm alatae = as effective a biological control agent as S. doryliformis, 0.32, apterae = 0.43 at 24oC (Scott and Yeoh, 1999)] but attempts to adjust its life cycle to southern hemi- even for an aphid. Scott and Yeoh (1999) carried out sphere conditions failed and therefore their work on temperature studies and bionomic modelling on B. ru- P. chrysidiformis was discontinued. Preliminary stud- mexicolens and showed that it should be able to survive ies have been initiated at CABI Europe-Switzerland, in northern Europe. It has already been recorded from aiming to further study the biology of P. chrysidiformis most of Europe, including the UK and Norway (e.g. and to develop rearing protocols. Mass-rearing and re- Ossiannilsson, 1962). lease methods have been developed in Australia for S. Hyperia rumicis L., a leaf-feeding weevil (Col., doryliformis (Fisher, 1992), using pieces of dock root Curculionidae), and Pegomya nigritarsis (Zetterstedt) for larval rearing, and gluing eggs to swizzle sticks by (Dipt., Anthomyiidae), a leaf miner, can both occasion- machine and inserting them directly into cut flower- ally cause extensive damage to docks (Grossrieder and ing dock stems. We believe that these methods could Keary, 2004) but seem to have few advantages over easily be adapted to rearing P. chrysidiformis. In the the leaf beetle Gastrophysa viridula Degeer (Col., UK, P. chrysidiformis occurs on R. crispus only in a Chrysomelidae). couple of sea-cliff and shingle beach sites in Kent, SE
472 Biological control of Rumex species in Europe: opportunities and constraints
England, and is protected by law as an endangered spe- this is likely to be easy or not. It also occurs early, grows cies under Schedule 5 of the Wildlife and Countryside throughout the year on dock, and can cause almost total Act (1981). Thus, working with this species in the UK defoliation—including younger leaves—during severe will be especially challenging, but the combination of outbreaks (Hatcher, personal observation). This fungus insect conservation and weed biological control, if suc- is very common on R. longifolius in Norway. Hüber- cessful, would be particularly rewarding. Meinicke et al. (1989) found that infection by this fun- Two other sesiids, P. minianiforme Freyer and gus reduced shoot weight of R. obtusifolius by 58% S. triannuliformis Freyer coexist on Rumex spp., espe- after 11 weeks, and root weight by up to 48%. cially R. crispus in SE Europe, with the latter species Venturia rumicis (Desm.) Wint. also occurs on extending into north and central Europe (Grossrieder R. crispus and R. obtusifolius. This hemibiotrophic and Keary, 2004). The biological control potential of ascomycete is the least common of these three patho- both should also be considered. gens in the UK and usually causes damage in late sum- mer and autumn, although low levels can be present throughout the year. It is unclear whether this fungus Fungi can be cultured in vitro and no work has yet been at- Three species of pathogenic fungi commonly infect tempted on using it as a biological control agent. weedy Rumex spp. throughout Europe, and have poten- tial for their biological control. The way forward The rust Uromyces rumicis (Schum.) Wint. is the most studied fungus on Rumex spp., and was considered Along with meeting all the usual criteria for biologi- in the 1960s as a potential biological control agent for cal control agents, agents selected for dock biological R. crispus in the USA (Inman, 1970). However, work control in organic agriculture must also be able to cope was discontinued when it was impossible to confirm the with the cultural control methods already being prac- alternate hosts of the fungus [in Europe the fungus is ticed by organic growers until and unless they can be almost entirely spread through uredospores and teleu- demonstrated to be superior to these. Thus, the interac- tospores, but rarely forms spermogonia and aecidia on tions among and between insect and fungus species be- Ranunculus ficaria L. as an alternate host (Schubiger come important, and also the effects of cutting, grazing et al., 1985)]. U. rumicis can cause up to 35% reduc- and other control methods on the population dynamics tion in dry weight of R. obtusifolius during the first year of the insects and pathogens need to be studied in situ, of growth (Hatcher et al., 1997), up to 60% shoot and under a range of conditions. For example, P. chrysidi- 52% root reduction of R. crispus first-year overwinter- formis oviposits on dry dock stalks, so any attempt to ing plants (Hatcher, 1996), and can cause up to 40% re- ‘clean’ dock-infested pastures by cutting the dry stalks duction of dry mass in the first four years of R. obtusi- may seriously hamper the population buildup of this folius growth in the field (Hatcher, unpublished data.). moth. U. rumicis damage is not normally apparent in the field Recent reviews of potential dock biological control until late in the year, after dock has flowered, and thus agents (Grossrieder and Keary, 2004; Zaller, 2004; it usually has little effect on seed production. It also Bond et al., 2006) suggest that of the indigenous spe- cannot infect young developing dock leaves and as it is cies, Gastrophysa viridula and Uromyces rumicis still non-systemic, the plant is able to outgrow fungal dam- show the greatest promise for inundative biological age (Hatcher et al., 1995). However, while U. rumicis control at the moment, but that Ramularia rubella and is not promising as a sole biological control agent for Brachycaudus rumexicolens need further investigation Rumex spp., it combines well with G. viridula. The rust to determine their potential. infects the older leaves, causing the beetles to move to One way forward is to engage organic growers in the younger leaves; thus an additive amount of damage enhancing or conserving the herbivores and pathogens is consistently produced by combined beetle and rust they already have on Rumex. This has started in the UK attack (Hatcher, 1996; Hatcher et al., 1997; Hatcher with the HDRA-managed project mentioned above. A and Paul, 2001). Artificial inoculation with the rust questionnaire about G. viridula received 34 replies: early in the year is possible, and in cool, moist climates 23 respondents had seen the beetle, and 18 said that it is likely to persist over much of the summer. It is easy occurred every year and noted that it caused signifi- to produce large numbers of uredospores for artificial cant damage to the plant, although this could be patchy. inoculation from R. obtusifolius plants in the laboratory Ideas for encouraging the beetle in field margins at the or glasshouse (Hatcher et al., 1994; Hatcher, 1996). start of the growing season by covering plants with The necrotrophic fungus Ramularia rubella (Bon.) fleece or simple polytunnels, for example, were put for- Nannf. also shows promise as a dock biological control ward. It is easy to rear the beetle in bulk, either in plas- agent. Unlike U. rumicis, this fungus can be cultured on tic boxes on detached dock leaves (the beetle pupates agar and thus might be bulked up in the laboratory but under several layers of absorbent paper at the bottom there has been insufficient work to ascertain whether of the box) or on plants grown in pots and sleeved with
473 XII International Symposium on Biological Control of Weeds perforated plastic bags. Both methods have been used Bentley, S. and Whittaker, J.B. (1979) Effects of grazing by a for many years at the University of Reading, UK, and chrysomelid beetle, Gastrophysa viridula, on competition can produce many thousands of gravid female beetles between Rumex obtusifolius and Rumex crispus. Journal (thought to be the best stage for release). This has en- of Ecology 67, 79–90. abled populations to be introduced into new areas of Bond, W., Davies, G. and Turner, R.J. (2006) The biology and non-chemical control of broad-leaved dock (Rumex southern England, which have established after intro- obtusifolius L.) and curled dock (R. crispus L.). Available duction (Hatcher, personal observation). Such methods at: http://www.gardenorganic.org.uk/organicweeds (ac- could easily be adopted by farmers and thus inundative cessed 14 April 2007). and conservation biological control could be practised Brandsaeter, L.O. and Haugland, E. (2007) Kontroll av høy- with this insect. mole (Rumex spp.) i økologiske og konvensjonelle dyrk- As mentioned above, the beetle can be combined ingssystem. Bioforsk FOKUS 2(7), 55–58. with other biocontrol agents, and a combination of G. Cavers, P.B. and Harper, J.L. (1964) Biological flora of the viridula and U. rumicis with early re-sowing of Lo- British Isles, Rumex obtusifolius L. and R. crispus L. lium perenne L. can control the flush of emerging R. Journal of Ecology 52, 737–766. obtusifolius seedlings after a pasture seed-bed is pre- Debio (2006) Organic plant production in Norway, statistics http://debio.no pared (Keary and Hatcher, 2004). It is possible that 2006. (accessed 14 April 2007). Dierauer, H., Hermle, M., Lüscher, A., Schaller, A. and Thal- regular cutting of dock-infested grassland may inhib- mann, H. (2007) Blackenregulierung: Vorbeugende Mass- it G. viridula, for example if it occurs during a peak nahmen ausschöpfen. Merkblatt, Forschungsinstitut für egg-laying period. However, natural populations of biologischen Landbau (FiBL) und Arbeitsgemeinschaft the beetle are rarely synchronized and the beetle has zur Förderung des Futterbaues (AGFF), Binkert Druck, persisted throughout a ten-year experiment at the Uni- Laufenberg, pp. 1–16. versity of Reading, UK, in a field which is mown at FiBL (2006) Organic farming in the United Kingdom. Avail- least four times a year without regard for the beetle able at: http://www.organic-europe.net/country_reports/ (Hatcher, personal observation). It is also possible to great_britain/default.asp (accessed 14 April 2007). modify mowing regimes to accommodate the beetle. Faithful, I. (2000) Distribution of dock moth in Victoria. Un- In Austria, Hann and Kromp (2003) found that ‘beetle- der Control 12, 9–10. friendly’ mowing (mowing twice per year rather than Fisher, K. (1992) Clearwing moths are key to dock control. Western Australia Journal of Agriculture 33, 152–155. the three times used in conventional management, and Fogliani, R.G. and Strickland, G.R. (2000) Biological Con- each mow timed to coincide with the period the bee- trol of Dock: Enhanced Distribution of the Dock Moth. tle was in the soil as a pupa) had a positive effect on Research Report, Meat Research Corporation, Sydney, G. viridula density and feeding damage, compared to a Australia. conventional regime of three cuts per year. The beetles Foster, L. (1989) The biology and non-chemical control of were able to spread over the site, and unmown sites had dock species Rumex obtusifolius and R. crispus. Biologi- greater numbers of overwintering adults than the mown cal Agriculture and Horticulture 6, 11–25. ones. Thus, unmown refuges at the edge of fields could Fykse, H. (1986) Experiments with Rumex species. Growth be useful for the beetle. and regeneration. Scientific Reports of the Agricultural However, as we noted above, Rumex spp. are resil- University of Norway 65 (25), 11 p. ient to defoliation and have fast regrowth rates due to Grossrieder, M. and Keary, I.P. (2004) The potential for the biological control of Rumex obtusifolius and Rumex cris- tap-root reserves that are rapidly replenished after re- pus using insects in organic farming, with particular ref- growth of leaves. Hence, successful control strategies erence to Switzerland. Biocontrol News and Information should include organisms that target other parts of the 25/3, 65N–79N. plant than the foliage, in particular the below-ground Hann, P. and Kromp, B. (2003) Der Ampferkäfer (Gastro- storage organs. 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