Preferred name: Margarodes capensis
Authority: Giard
Taxonomic position: Animalia: Arthropoda: Hexapoda: Insecta: Hemiptera: Sternorrhyncha: Margarodidae
Common names in English: ground pearls, vine margarodes
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Notes on taxonomy and nomenclature EU Categorization: A1 Quarantine pest (Annex II A)
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EPPO Code: MARGCA

Margarodes capensis has only been recorded on the roots of grapevine (Vitis vinifera) and on roots of Rumex acetosella subsp. pyrenaicus (synonym: Rumex angiocarpus, Polygonaceae), an introduced weed growing in vineyards (Brain, 1915; de Klerk, 1978). Grapevines would be the host at risk in the EPPO region. It is by no means certain that grapevine is the only cultivated crop that this ground pearl could infest. The indigenous host plants of this ground pearl have not been identified yet.

Host list: Rumex acetosella subsp. pyrenaicus, Vitis vinifera

Margarodes capensis has been recorded only from South Africa, where it occurs in Western Cape province in the areas around Malmesbury (Jakubski, 1965; de Klerk et al., 1982), Worcester and Stellenbosch (Jakubski, 1965).

Africa: South Africa

Margarodes capensis is parthenogenetic, with one generation per year (Jakubski, 1965; de Klerk, 1978; de Klerk et al., 1980). The biology of M. capensis was studied under laboratory and field conditions by De Klerk (1978). The females are most abundant in soil at a depth of 16-75 cm, while cysts occur mostly at a depth of 46-60 cm, the zone of greatest root abundance, but they can occur as deep as 120 cm. Only 3-10% of cysts collected in the field developed into adult females annually, emerging between the end of November and the beginning of March with the peak in late January to mid-February. In a single sample of cysts collected from the field, adult females emerged in four successive years and, after the fourth year, 19% of the remaining cysts were still alive. Under laboratory conditions, emergence of adult females from cysts mostly occurred at 20-30˚C, whereas at 40˚C there was 100% mortality. The adult female lives 24 days on average, 11 days of which are spent in oviposition; after about 9 days in vitro an average of 251 eggs per female were deposited in a string with wax filaments, but in the field clusters of eggs are laid in the soil close to grapevine roots, in pockets lined with secreted wax filaments; the eggs hatch 34-43 days later. Newly hatched nymphs disperse through the soil and attach by their mouthparts to rootlets 0.5-1.2 m below the soil surface, to feed; they then become sessile. After about two months they moult to the legless second-instar nymphal cyst stage, which lasts for more than a year and has two phases: an initial feeding and growing phase, followed by secretion of a protective waxy covering and multiple moults to form a pearl-like, dormant non-feeding cyst resistant to unfavourable conditions. Cysts remain attached to the roots by the long mouthparts (de Klerk, 2017) and can remain viable in the soil for several years; their maximum longevity is not known. Nor is it known precisely what triggers, or can prevent, cyst formation. De Klerk (1978) found that the vertical distribution of M. capensis cysts was directly related to the vertical distribution of grapevine roots; very dry and very wet soil conditions inhibited the occurrence of cysts, but cyst distribution was not affected by the percentage of clay in the soil.

Symptoms

Infestations of vineyards by species of Margarodes, including M. capensis, are usually patchy. Over several years the patches increase in size, presumably because of the gradual subterranean dispersal of the first-instar nymphs and adult females. Infested vines exhibit gradual loss of vigour, shoots become thinner and shorter, and the leaves become smaller (Annecke & Moran, 1982) and tend to point downwards (de Klerk, 2017). One or more of the branches may die, followed in severe infestations by the eventual death of the whole plant within five or six years; the duration of this process varies but happens much faster if the vines are stressed by either too much or too little water (de Klerk, 2017). Ground pearl infestation symptoms resemble those caused by grapevine phylloxera (Daktulosphaira vitifoliae (Fitch), Hemiptera: Aphidomorpha: Phylloxeridae), but in the case of M. capensis no root or leaf galls are formed.

Morphology

Eggs

Newly laid eggs are each 0.43-0.60 mm long, smooth, glossy-white, elongated, with one end more rounded than the other (de Klerk, 1978; de Klerk et al., 1982). 

Nymphs

First-instar nymphs are creamy white, elongate, 0.84-0.91 mm long, with antennae and legs clearly visible under the dissection microscope (Jakubski, 1965; de Klerk, 1978, de Klerk et al., 1982). The second-instar cysts (ground pearls) are approximately spherical, 3.5-6.3 mm diameter, dull, light to dark brown, thick-walled and very hard, with a bark-like surface texture (Jakubski 1965; de Klerk, 1978; de Klerk et al., 1982). When the hard outer layers are removed, the insect within is yellow. The slide-mounted cyst has 7 pairs of abdominal spiracles, and fewer than 10 cicatrices (sometimes arranged in pairs) between the anus and the last pair of abdominal spiracles (Jakubski, 1965; de Klerk et al., 1982).

Adults

According to de Klerk (1978) and de Klerk et al. (1982), the ovoid, dirty white to yellowish adult females of M. capensis vary considerably in size (from 3.8–7.5 mm long and 3.1-6.0 mm wide), with bodies sparsely covered with short hair-like setae and segmentation clearly visible; they have characteristic enlarged fossorial (digging) forelegs with heavily sclerotised dark-brown claws. According to Jakubski (1965), the slide-mounted adult female has 7 pairs of abdominal spiracles, the posterior end of abdomen without bulbous spines, ventral setae short (less than 200 μm long), multilocular pores restricted to the metathorax and head, and short blunt subcylindrical spines present on margins and mid-venter of the thorax and abdomen; medial areas of the dorsum are entirely without spines. The prothoracic pleurites are covered with delicate, flexible hairs but lack spines. For detailed morphological descriptions of the immature and adult female stages, see Jakubski (1965) and de Klerk et al. (1982). Being parthenogenetic, this species does not produce any males.

Authoritative identification requires detailed microscopic study of the cysts and/or adult females by a scale insect specialist. Prior to identification, specimens may be preserved in 70% ethanol. De Klerk et al. (1983) and Watson (2022) provide morphological keys to live cysts, slide-mounted cysts and adult females, of ten South African Margarodes spp. including the five species that infest grapevine roots (M. capensis, M. greeni, M. prieskaensis, M. trimeni and M. vredendalensis). The adult female of the South American species, M. vitis, is described by Jakubski (1965) but there is no key provided to identify the species so it is very difficult to use for identification purposes. Foldi & Soria (1989) provide descriptions and illustrations of the adult female and cyst stage of M. vitis but no identification key.

Detection and inspection methods

In vineyards, patches of possible infestation can be detected visually. Symptoms Infestations of vineyards by species of Margarodes, including M. capensis, are usually patchy. Over several years the patches increase in size, presumably because of the gradual subterranean dispersal of the first-instar nymphs and adult females. Infested vines exhibit gradual loss of vigour, shoots become thinner and shorter, and the leaves become smaller (Annecke & Moran, 1982) and tend to point downwards (de Klerk, 2017). One or more of the branches may die, followed in severe infestations by the eventual death of the whole plant within five or six years; the duration of this process varies but happens much faster if the vines are stressed by either too much or too little water (de Klerk, 2017). Ground pearl infestation symptoms resemble those caused by grapevine phylloxera (Daktulosphaira vitifoliae (Fitch), Hemiptera: Aphidomorpha: Phylloxeridae), but in the case of M. capensis no root or leaf galls are formed. 

Natural dispersal of M. capensis is extremely limited due to the subterranean habit of the insect; the first-instar crawlers and adult females within the soil are the only natural dispersal stages. However, infestation can be spread within and between vineyards or blocks of vines within a vineyard on soil cultivation implements (de Klerk, 2017). All the developmental stages may be transported over long distances from infested areas via human-assisted spread on grapevine plants for planting (when moved with roots and soil attached) and / or in soil.

Economic impact

There is no data available on the actual economic impact of M. capensis. Ground pearls devitalize the host directly by sap and nutrient depletion, and vines sometimes die within five or six years (de Klerk, 2017). Infestation of vines stressed by drought or nematode infestation can result in them dying in patches. The pest is difficult to control due to its subterranean habit and even after an interval of several years, vineyards replanted in infested soils are readily reinfested. Once infested, land may become unsuitable for commercial vineyard cultivation indefinitely (de Klerk, 1978, 2017). 

Control

Although many European and American varieties of Vitis vinifera have been tested, no resistant cultivars have been found; nor have any natural enemies of M. capensis have been documented. Consequently, the only possible control has been with insecticides, which presents technical problems because the target insects live 0.5-1.2 m underground. Soil drenches of systemic insecticides applied to control Planococcus ficus mealybugs shortly after harvest (in autumn), when the annual population of new cysts starts feeding and translocation in vines is still active, can reduce ground pearl infestations. As cysts can survive in the soil for years without feeding and only a certain percentage of cysts annually develop into adult females (de Klerk, 1978), follow-up treatments in successive years are essential. Fumigation for nematodes before planting could reduce numbers of females if done at the time when the females are active (but this method is not officially registered). After first treatments, annual re-evaluation of pest presence is necessary to decide on the need for any follow-up treatments (de Klerk, 2017).

Where an infestation of M. capensis has resulted in removal of the vines, the pest might be eliminated eventually by growing a series of annual crops over four or more years, because the cyst stage lasts longer than one year (de Klerk, 2017). However, since the native hosts of M. capensis are not known, there is uncertainty as to what type of annual crops would not serve as hosts for the ground pearls.

As M. capensis is a parthenogenetic species, there is no sex pheromone to exploit to monitor population levels by trapping males. 

Phytosanitary risk

There are no Margarodes species occurring in the EPPO region on grapevine, nor any grapevine pest with similar biology. Accordingly, ground pearl species recorded on grapevine in South Africa and South America present a serious phytosanitary risk to vineyards in the EPPO region. Non-European ground pearl species recorded feeding on grapevine roots are: M. capensis, M. greeni, M. prieskaensis, M. trimeni and M. vredendalensis from South Africa; and Dimargarodes meridionalis Morrison from California and the closely related Eurhizococcus brasiliensis (Hempel in Wille) from Brazil; however, the ground pearl species most damaging to grapevines is M. vitis in South America. 

Margarodes capensis occurs in South Africa in the Western Cape province, in winter rainfall areas around Malmesbury, Stellenbosch and Worcester where the climate varies with altitude between warm, dry temperate (Köppen-Geiger climate types Csa and Csb) and cold, arid steppe (Bsk). Across the EPPO region a variety of soil types and climates occur, and grapevines are widely cultivated, so it is assumed that M. capensis would be able to establish in the EPPO region (EFSA, 2019), particularly in drier Mediterranean areas. M. capensis can remain dormant as cysts in the soil for many years, making it extremely difficult to eradicate, so it is important to exclude it from the EPPO region.

A number of EPPO countries already ban the import of Vitis plants for planting (other than seeds) (e.g. EU countries: Annex VI, point 10 of Regulation/2072 (EU, 2019)) and prohibit the import of soil. Other appropriate phytosanitary measures to regulate import of Vitis (other than seeds) with roots into the EPPO region could require that these plants are produced in a pest-free area (including for the whole country) or in a pest-free place/site of production for M. capensis, established according to EPPO Standard PM 5/8 Guidelines on the phytosanitary measure ‘Plants grown under physical isolation’ (EPPO, 2016). Rooted grapevine plant material destined for export from South Africa are reported to be treated with both hot water and insecticide before shipment, to reduce the risk of infestation, and additional treatments are sometimes required on arrival in the country of destination. Host plants for planting could also be imported using post-entry quarantine (in the framework of a bilateral agreement).

Annecke DP & Moran VC (1982) Insects and mites of cultivated plants in South Africa, 382 pp. Butterworths, Durban (ZA).

Brain CK (1915) The Coccidae of South Africa. Transactions of the Royal Society of South Africa. Cape Town 5, 65-194.

EFSA (2019) Pest categorisation of non-EU Margarodidae. EFSA Journal 17(4), 5672, 1-42. Available at: https://efsa.onlinelibrary.wiley.com/doi/epdf/10.2903/j.efsa.2019.5672 (accessed 12 February 2022).

EPPO (2007) PM 7/82 (1) Margarodes prieskaensis, Margarodes vitis, Margarodes vredendalensis. EPPO Bulletin 37, 560–570. Available at: https://gd.eppo.int/download/standard/206/pm7-082-1-en.pdf (accessed 12 February 2022).

EPPO (2016) EPPO Standard PM 5/8 (1) Guidelines on the phytosanitary measure ‘Plants grown under physical isolation’. EPPO Bulletin 46, 421-442. Available at: https://onlinelibrary.wiley.com/doi/epdf/10.1111/epp.12340 (accessed 12 February 2022).

EPPO (2018) PM 3/85 (1) Inspection of places of production – Vitis plants for planting. EPPO Bulletin 48(3), 330-349. Available at: https://gd.eppo.int/download/standard/738/pm3-085-1-en.pdf (accessed 12 February 2022).

EU (2019) Commission Implementing Regulation 2019/2072 of 28 November 2019 establishing uniform conditions for the implementation of Regulation (EU) 2016/2031 of the European Parliament and the Council, as regards protective measures against pests of plants, and repealing Commission Regulation (EC) No 690/2008 and amending Commission Implementing Regulation (EU) 2018/2019. Annex VI, points 10. Available at: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A32019R2072

de Klerk CA (1978) Morphology and taxonomy of the South African species of the genus Margarodes (Hemiptera: Margarodidae), with detailed studies on the biology of two vine infesting species. PhD thesis, Stellenbosch University, South Africa. 

de Klerk CA (1985) Occurrence of South African species of Margarodes Guilding (Homoptera: Coccoidea: Margarodidae) with special reference to vine infesting species. Phytophylactica 17, 215-216.

de Klerk CA (2017) Identification, control and management of grapevine Margarodes. Viticulture research, Winetech Technical. Available at: https://www.wineland.co.za/identification-control-management-grapevine-margarodes/ (accessed 3 March 2022).

de Klerk CA, Ben-Dov Y & Giliomee JH (1980) Biology of Margarodes capensis Giard (Homoptera; Coccoidea: Margarodidae) under laboratory and controlled conditions in South Africa. Phytophylactica 12, 147-156.

de Klerk CA, Ben-Dov Y & Giliomee JH (1982) Redescriptions of four vine infesting species of Margarodes Guilding (Homoptera: Coccoidea: Margarodidae) from South Africa. Phytophylactica 14, 61-76.

de Klerk CA, Ben-Dov Y & Giliomee JH (1983) General morphology of South African species of Margarodes Guilding (Homoptera: Coccoidea: Margarodidae) with keys to nymphs and adult females. Phytophylactica 15, 133-144.

Foldi I & Soria SJ (1989) Les cochenilles nuisibles à la vigne en Amérique du Sud (Homoptera: Coccoidea). Annales de la Société entomologique de France (N.S.) 25(4), 411-430.

Jakubski AW (1965) A critical revision of the families Margarodidae and Termitococcidae (Hemiptera, Coccoidea), 187 pp Trustees of the British Museum (Natural History) London (GB).

Watson GW (2022) Towards identification of the scale insects (Hemiptera: Coccomorpha) of continental Africa: 2. Checklists and keys to six archaeococcoid families. Zootaxa 5105(3), 301-356.

This datasheet was prepared in 2022 by Gillian W. Watson, Natural History Museum, London, UK, and Elleunorah Allsopp, ARC Infruitec-Nietvoorbij Fruit, Vine and Wine Institute, South Africa. Their valuable contribution is gratefully acknowledged.

EPPO (2024) Margarodes capensis. EPPO datasheets on pests recommended for regulation. https://gd.eppo.int (accessed 2024-11-21)

This datasheet was first published online in 2022. It is maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.