Flat Mites: A Potential Threat to Turfgrasses ...

Published online October 19, 2017

RESEARCH

Flat Mites: A Potential Threat to Turfgrasses Worldwide, or Already Widespread? Owen D. Seeman, Hikaru Akamine, and Donald S. Loch*

ABSTRACT Two species of flat mites (Acari: Tenuipalpidae) from the genus Dolichotetranychus have recently been found to cause significant damage to Cynodon (bermudagrass) and Zoysia spp. turfgrasses. Despite records of D. australianus infesting bermudagrass throughout Africa, the Middle East, and Australia for more than 70 yr, most turf managers assume that any apparent mite damage is due to the widely publicized eriophyoid bermudagrass mite, Aceria cynodoniensis, rather than validating this under the microscope. To an experienced eye, the visual symptoms are distinctly different from those typically associated with A. cynodoniensis; but they are similar to the symptoms seen with the zoysiagrass mite, D. zoysiae, in Okinawa (Japan). The possibility that there may be further undescribed or misidentified Dolichotetranychus species affecting turfgrasses is discussed, together with examples and biosecurity implications. One such species that may prove to be more significant than hitherto suspected, if routine microscopic diagnosis were to be implemented, is D. summersi, which has been recorded five times from bermudagrass in the United States during the 1950s and 1960s but without any indication of the symptoms caused. The importance of making microscopic examinations of suspected mite infestations is emphasized.

O.D. Seeman, Queensland Museum, P.O. Box 3300, South Brisbane, QLD 4101, Australia; H. Akamine, Subtropical Field Science Center, Faculty of Agriculture, Univ. of the Ryukyus, Okinawa, Japan; D.S. Loch, School of Agriculture and Food Sciences, The Univ. of Queensland, St Lucia, QLD 4072, Australia. Received 1 Sept. 2016. Accepted 30 May 2017. *Corresponding author ([email protected]). Assigned to Associate Editor Douglas Richmond.

FLAT MITES AS PESTS The flat mites (Acari: Tenuipalpidae) comprise almost 1000 species, of which the vast majority are considered to be near-harmless leaf vagrants grazing on the phylloplane. A few, however, are pest species, the best known of which are several species of Brevipalpus, especially the B. phoenicis species complex, which vector citrus leprosis virus as well as damage leaves and fruit directly (Beard et al., 2015). The genus Dolichotetranychus comprises 25 described species found primarily on monocots (Table 1). Like other flat mites, a few are pest species, and many are probably host-specific. The best known is the pineapple flat mite, D. floridanus, which causes cracking of the leaf epidermis, damages the fruit, and allows entry of fungal and bacterial infections. Two of the known species are of documented significance to turfgrass production and management: D. australianus and D. zoysiae. Both of these species create distorted growths that become shelters for huge colonies of mites.

DOLICHOTETRANYCHUS AUSTRALIANUS— THE BERMUDAGRASS FLAT MITE This mite was first described by Womersley (1943) from an infestation of bermudagrass [Cynodon dactylon (L.) Pers.] in Queensland, Australia. Since its initial description, D. australianus has been reported sporadically throughout its likely native range in Africa Published in Int. Turfgrass Soc. Res. J. 13:497–501 (2017). doi: 10.2134/itsrj2016.09.0731 © International Turfgrass Society and ACSESS | 5585 Guilford Rd., Madison, WI 53711 USA All rights reserved.

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Table 1. Species of Dolichotetranychus, countries they are recorded from, and their host species and families. Dolichotetranychus species alpinus Collyer, 1973 ancistrus Baker and Pritchard, 1956 apaches Baker and Pritchard, 1956 australianus (Womersley, 1943)

babylonicus Al-Gboory, 1987 bakeri El-Enany and Soliman, 1987 carnea (Banks, 1906) cocos Flechtmann and Fernando, 2000 cracens Pritchard and Baker, 1958 cymosum Meyer, 1979 elatariae Mohanasundaram, 1983 floridanus (Banks, 1900) gramineus Mitrofanov and Strunkova, 1978 iranicus Safdarkhani et al. 2016 kermanicus Khanjani et al., 2011 macer Baker and Pritchard, 1956

Country

Host

Family

New Zealand New Zealand USA Australia, Egypt, Israel, Iran, Saudi Arabia, South Africa, Zimbabwe (Bangladesh? Kenya?) Iraq

Chionochloa sp. Hebe sp.† (koromiko) Tillandsia sp. (air plant) and unidentified bromeliads Cynodon dactylon (L.) Pers. (bermudagrass)

Poaceae Plantaginaceae Bromeliaceae Poaceae

Phragmites australis (Cav.) Trin. ex Steud. (common reed) unidentified desert plant Sporobolus sp. Cocos nucifera L. (coconut) Sporobolus cryptandrus (Torr.) A. Gray (sand dropseed) Helichrysum cymosum (L.) Less. (yellow-tipped straw-flower) Elettaria cardamomum (L.) Maton (cardamom) Ananas comosus (L.) Merr. (pineapple) undetermined cereal Phragmites australis (Cav.) Trin. ex Steud. (common reed)

Poaceae

Egypt Utah Sri Lanka USA South Africa India USA‡ Tajikistan Iran Iran South Africa

micidus Baker and Pritchard, 1956

USA

muhlenbergia Baker and Tuttle, 1972

USA

ramaniae Mallik and Paul, 1995 repenae Mohanasundaram, 1983 salinas Pritchard and Baker, 1952 summersi Pritchard and Baker, 1952 tenellae Mohanasundaram, 1983

India India USA USA India

vandergooti (Oudemans, 1927)

Indonesia, Philippines, Thailand

unknown Poaceae Arecaceae Poaceae Asteraceae Zingiberaceae Bromeliaceae Poaceae Poaceae

found on/in soil under citrus Stipagrostis namaquensis (Nees) De Winter (kalaharikweek) Muhlenbergia asperifolia (Nees & Meyen ex Trin.) Parodi (alkali muhly) Muhlenbergia torreyi (Kunth) Hitchc. ex Bush (ring muhly) Cocos nucifera L. (coconut) Panicum repens L. (creeping panic) Distichlis spicata (L.) Greene (saltgrass) Cynodon dactylon (L.) Pers. (bermudagrass) Eragrostis tenella (L.) P. Beauv. ex Roem. & Schult. (Japanese lovegrass) Dendrobium sp.

unknown Poaceae

Orchidaceae

Poaceae Poaceae Arecaceae Poaceae Poaceae Poaceae Poaceae

wiesei Meyer, 1979

South Africa

unknown grass

Poaceae

zoysiae Ehara, 2004

Japan

Zoysia matrella (L.) Merr., Z. pacifica (Goudswaard) M. Hotta & Kuroki (zoysiagrasses)

Poaceae

† Zhang and Fan (2004) showed the host was not Hebe salicifolia but another species of Hebe. ‡ Dolichotetranychus floridanus is known from many countries in the Americas, Africa, the Pacific, and SE Asia.

(Egypt, South Africa, and Zimbabwe) and the Middle East (Iran, Israel, and Saudi Arabia). In Australia prior to 2010, it was occasionally recorded as a pest, but generally damage was blamed on the eriophyoid bermudagrass mite, Aceria cynodoniensis, without checking which mite was responsible. Surveys and opportunistic field sampling over the past 7 yr, however, have shown the bermudagrass flat mite to be widespread in Australia and at least as important as the eriophyoid mite as a pest of bermudagrass (Seeman et al., 2016; McMaugh et al., 2016). Both the tenuipalpid and the eriophyoid bermudagrass mites cause distortion of growth, but each in a distinctive way; and, with practice and experience, the symptoms caused by the different mites can be distinguished accurately (Fig. 1).

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Witch’s brooms (rosetted growths at stolon nodes–see also Keifer et al., 1982) and poor stolon root development are typical of Aceria infestations, which tend to be concentrated more along the edges of a turfgrass stand rather than being spread across the area. At the same time, individual growths within an Aceria witch’s broom become shortened with leaves greatly reduced in length, thickened and flattened laterally to give a “pinetree” effect. Dolichotetranychus australianus, on the other hand, produces a characteristic thinning and weakening of the stand, usually concentrated in patches, but frequently spread across an infested area rather than being prevalent along the margins. There is markedly less proliferation of distorted growths at stolon nodes (i.e., no strong witch’s brooming), and these pinetree-like growths are slightly more thickened and rounded

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Fig. 1. Comparison of mite infestation symptoms for Aceria cynodoniensis (left), Dolichotetranychus australianus (center), and Dolichotetranychus zoysiae (right), showing vertically mite colonies under the leaf sheath (top), external symptoms in the field (middle) and close up images of mite galls (bottom).

with even shorter leaves than for Aceria. Dolichotetranychus australianus can also be found persisting in some quite old, half-dead, elongated pinetree-like growths, though not as prevalent as in younger growths. In the case of mixed Aceria-Dolichotetranychus populations, the external symptoms seen tend to follow the dominant species.

DOLICHOTETRANYCHUS ZOYSIAE— THE ZOYSIAGRASS FLAT MITE The tenuipalpid zoysiagrass mite was discovered much more recently, being collected by H. Akamine from Zoysia matrella and Z. pacifica (Akamine et al., 2005) and described by Ehara (2004). The symptoms caused by this mite are strikingly similar to those caused by the bermudagrass mite. Again, it produces thick, pinetree-like growths of short leaves, under the sheaths of which live colonies of these small orange–red mites (Fig. 1). Across the stand, there is also a thinning and weakening of growth, most typically in patches.

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Despite causing very similar symptoms, these two species do not seem to be closely related, with D. zoysiae lacking two important setae and males retaining a solenidion on tarsus II (Seeman et al., 2016). Examination of new specimens by the first author found that a seta noted to be lacking in Ehara’s (2004) excellent description–a femur III seta–is actually present. Curiously, D. zoysiae more closely resembles D. summersi, a mite collected on five occasions from bermudagrass in the United States, but only known from these original collections. Currently, D. zoysiae is known only from Okinawa Island and, considering that the extensive native range of Zoysia spp. through the western Pacific rim and Indian Ocean includes Okinawa, it is possible that D. zoysiae is endemic to that island. However, we expect that species of Dolichotetranychus, including D. zoysiae, could occur on zoysiagrasses elsewhere in the world, particularly in the extensive native areas of Zoysia spp. found in other parts of eastern and southern Asia. In the case of D. zoysiae,


Table 2. Species of Dolichotetranychus with alternative hosts. Countries and families in bold are different from records in Table 1. Dolichotetranychus alpinus, D. australianus and D. carnea probably represent new records of the same species, while Dolichotetranychus ancistrus and D. apaches, and some records of D. floridanus and D. vandergooti probably represent different (possibly undescribed) species. Dolichotetranychus alpinus

Country

Host

Family

Reference

New Zealand

Celmisia laricifolia Hook. f. (New Zealand daisy).

Asteraceae

Collyer (1973)

 Unlikely true host; sample of grass was contaminated with C. laricifolia. ancistrus USA Bouteloua gracilis (Kunth) Lag. ex Steud. Poaceae (blue grama)  This host record seems incongruous (different continent and host family) and the USA specimens need re-examination. apaches USA Aristida adscensionis L. (sixweeks threeawn), Cynodon Poaceae dactylon (L.) Pers. (bermudagrass), Distichlis stricta (Torr.) Rydb. (desert saltgrass), Hilaria jamesii (Torr.) Benth. (James’ galleta.), Sorghum halepense (L.) Pers. (Johnsongrass).  All of these records require re-examination; they may represent one or more additional species. australianus South Africa Cynodon incompletus Nees (blue couch) Poaceae  Second host plant for D. australianus Australia Pennisetum clandestinum Hochst. ex Chiov. (kikuyugrass)

 Not true host; no colonies found, only what were presumed to be migrating females. carnea USA Bouteloua (as Buchloe) dactyloides (Nutt.) Columbus (buffalograss), Distichlis sp., Muhlenbergia sp.

Baker and Tuttle (1972)

Baker and Tuttle (1972); Hennessey et al. (1986)

Meyer (1979)

Poaceae

McMaugh et al. (2016)

Poaceae

Baker and Pritchard (1956); Tuttle and Baker (1976)

Poaceae

Wafa et al. (1968/69)

 Possibly an oligophagous species as all hosts are Poaceae, but still warrant closer study. floridanus Egypt  Unlikely to be D. floridanus.

bamboo

Philippines Arundina sp. Orchidaceae Rimando (1962) Thailand Papilionanthe sp. Orchidaceae Charanasri et al. (1989)  Records in the Philippines and Thailand are very likely correctly identified as D. vandergooti. A mention of this species in Rimando (1962) from Panama has not been confirmed. India Cocos nucifera L. (coconut) Arecaceae Sathiamma (1985)  Unlikely to be the same species as those on Dendrobium; possibly a new species (or D. cocos Flechtmann and Fernando 2000)

vandergooti

our experience with mite infestations of bermudagrass in Australia has highlighted the fact that mite damage, particularly damage from flat mites, is often blamed on eriophyoid mites or other causes. In this context, the better known eriophyoid zoysia mite, A. zoysiae, is endemic to these parts of Asia and has also been introduced to North America (Baker et al., 1986). With respect to other species, we have recently discovered an undescribed species of Dolichotetranychus infesting Z. macrantha Desv. subsp. macrantha in native ecosystems along the northern New South Wales coastline in Australia, thus confirming our expectations. While more work is necessary to describe accurately the visual symptoms caused by this new mite, our initial impression is that infestations are associated with shoot proliferation but without the compression of internodes typical of both D. australianus and D. zoysiae.

ARE SPECIES OF DOLICHOTETRANYCHUS A BIOSECURITY RISK? Dolichotetranychus floridanus is the only species that could be considered to have a worldwide distribution, so all other species could pose a risk to biosecurity. Foremost of these 500

is D. australianus, which is unknown in the Americas, but also D. zoysiae, which could be more widespread than currently thought. Pathways to entry would not necessarily involve live plant material, which is prohibited for import, and Dolichotetranychus do not associate with seed. A more likely pathway for plant mites, especially those on turf grasses, would be on people’s clothing and their other belongings. A single mated female mite is capable of starting a new colony alone, and people, their lawns, and the mites that live on them in different countries are nowadays only separated by 1 d or less via international air travel. Other species of Dolichotetranychus may also pose a biosecurity risk, but what species these are is complicated. Several records of Dolichotetranychus from other host plants are probably misidentifications or, more likely, represent undescribed species (Tables 1 and 2); and some host plant identifications may also be doubtful [e.g., Eragrostis tenella (L.) P. Beauv. ex Roem. & Schult., a small weedy annual grass that invades C. dactylon and other turfgrass areas in the tropics]. However, we especially note that, in the United States, D. summersi has been recorded five times from bermudagrass during the 1950s and 1960s (Pritchard and Baker, 1952, 1958; Baker and Pritchard, 1956; Baker and Tuttle, 1964),

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but without any descriptions of the associated visual symptoms. In Canada, an undescribed species similar to D. carnea also infests grasses (Beaulieu and Knee 2014). Whether or not these mites cause damage similar to D. australianus and D. zoysiae is unknown, but we think it pertinent to consider each of these species as being of quarantine importance to other countries. Significantly also, Woods (2010) posted pictures of damage on bermudagrass in Bangladesh by an unknown mite species, in which the symptoms appear identical to damage typically caused by D. australianus. In conclusion, we would encourage all turfgrass managers to look closely at potential mite damage under a microscope. As our experience in Australia has demonstrated, flat mites are easily overlooked where damage is assumed to be caused by mites, especially eriophyoid mites, without proper microscopic examination.

Conflict of Interest Disclosure The authors declare that there is no conflict of interest. Acknowledgments Recent Australian studies cited in this paper were funded by Horticulture Innovation Australia (formerly Horticulture Australia Limited) with funds from the Australian Government and coinvestment from the Australian Racecourse Managers Association and Racing Queensland Limited as part of the project TU13021.

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