Rose rosette disease (RRD) has become established across much of the United States. The causal agent is Rose rosette virus (RRV) (genus Emaravirus) (Di Bello et al., 2015; Laney et al., 2011), with the main mode of natural transmission being the eriophyid mite, Phyllocoptes fructiphilus Keifer (Allington et al., 1968; Amrine et al., 1988; Bauchan et al., 2019; Gergerich and Kim, 1983), although the virus can be spread through grafting (Amrine et al., 1988; Gergerich and Kim, 1983) and movement of infected plant material. Eriophyid mites can use wind currents to disperse long distances to new locations (Galvao et al., 2012; Lindquist and Oldfield, 1996; Zhao and Amrine, 1997). The relationship between virus and vector and mode of virus transmission are unknown. However, more than just passive transport is suspected. Five other eriophyid mites are known to infest roses in the United States but are not known to transmit RRV: P. adalius, P. linegranulatus, P. chorites, Callyntrotus schlechtendali (Baker et al., 1996; Keifer, 1939a, 1939b, 1940, 1972; Otero-Colina et al., 2018; Styer, 1974), and Eriophyes eremus (Otero-Colina et al., 2018).
RRV is lethal to roses; and, like most other plant virus infection, there is no cure once roses are infected. Cultivated roses and many Rosa species are susceptible, including the noxious weed R. multiflora Thunb. (multiflora rose). Beds of ornamental roses and wild multiflora roses can serve as reservoirs of both the mite and the virus. Although control of multiflora rose is recommended, it is often difficult due to the numerous seeds produced annually, remote growing location, and regeneration of shoots from roots left in soil (Denight et al., 2008). Beds of landscape roses not frequently inspected for RRD symptomatic plants may serve as reservoirs for mites and virus.
RRD was first documented in Manitoba, Canada in 1940 (Conners, 1941). Shortly after, there were similar reports from Wyoming (in 1941) and California (in 1942) (Thomas and Scott, 1953). RRD has since spread to the south and east of the United States, and it is currently documented from 33 states, including: Alabama, Arkansas, California, Colorado, Connecticut, Delaware, Georgia, Illinois, Indiana, Iowa, Kansas, Kentucky, Louisiana, Maryland, Massachusetts, Michigan, Mississippi, Missouri, Nebraska, New Jersey, New York, North Carolina, Ohio, Oklahoma, Pennsylvania, South Carolina, Tennessee, Texas, Utah, Virginia, West Virginia, Wisconsin, and Wyoming (Amrine, 2002; Bauchan et al., 2019; Denight et al., 2008; Dobhal et al., 2016; Shires and Ong, 2018). Despite the wide incidence of RRD, the boundaries of the distribution are unknown, notably in the southeastern United States. With reports of RRD in the northern parts of Alabama, Georgia, and Mississippi (Shires and Ong, 2018) the southward extent of disease incidence in those states was unknown. There have been anecdotal reports of RRD infections as far south as Interstate I-20, a highway extending from Augusta through Atlanta, GA; Birmingham, AL; and Jackson, MS; but the absence of reports south (excepting reports from Florida discussed in the following) was intriguing.
Distribution of the vector, P. fructiphilus, has also not been clearly determined, though previously reported in North America (Hoy, 2013) and as “widely distributed” on both wild and ornamental roses (Amrine, 2002). Because the natural spread of RRV relies on P. fructiphilus, the distribution of RRV could correlate with the distribution of these mites. However, it is possible that the mite may be present in the absence of the disease, including on rose species not prone to infection (e.g., R. palustris).
The mite has so far not been reported from the southern halves of the U.S. Gulf States (Alabama, Georgia, and Mississippi) (Hoy, 2013). In Nov. 2013, a case of RRV-infected ‘Knock Out’ roses was discovered in Florida and confirmed using reverse transcription polymerase chain reaction (RT-PCR); but no eriophyid mites were recovered from the infected roses (Babu et al., 2014). This discovery suggests that infected roses were shipped into Florida. Following quarantine and destruction of the symptomatic roses that tested positive for RRV, no spread of the disease has been observed (Babu et al., 2014). Subsequently, three more cases were confirmed in Florida from 2014 to 2018 in symptomatic plants shipped from other states, but no eriophyid mites were found on the plants.
A better understanding of the distribution of the mite could identify the risk of spread of RRV, given that the mite is the primary vector, along with transport of infected plants to areas where the disease is unknown to occur. Therefore, more information on the incidence of P. fructiphilus can help in predicting potential for locations where natural spread of RRV can occur. Nursery growers, public and private gardens, and those overseeing natural areas with invasive and native wild roses in the Deep South (the southeastern region of the United States including Alabama, Georgia, and Mississippi) could benefit from more information when assessing the potential for impact the disease may have. This study surveyed this region by sampling for both RRV-infection and populations of eriophyid mites on cultivated roses. The objectives of this study were to determine if P. fructiphilus and RRD were present in this region in managed areas; if certain factors such as wind barriers, sun exposure levels, or plant size were associated with the presence of eriophyid mites in these sites; and if plant hardiness zones or latitude could be used to predict the prevalence of the P. fructiphilus or RRD in the region.
Allington, W.B., Staples, R. & Viehmeyer, G. 1968 Transmission of Rose Rosette Virus by the eriophid mite Phyllocoptes fructiphilus J. Econ. Entomol. 61 1137 1140
Amrine, J. Jr & Manson, D. 1996 Preparation, mounting and descriptive study of eriophyoid mites, p. 383–396. In: E. Lindquist, M. Sabelis, and J. Bruin (eds.). Eriophyoid mites—Their biology, natural enemies and control, vol. 6. Elsevier Science Publishing, Amsterdam, The Netherlands
Amrine, J.W. 1996a Phyllocoptes fructiphilus and biological control of multiflora rose, p. 741–749. In: E. Lindquist, M. Sabelis, and J. Bruin (eds.). Eriophyoid mites—Their biology, natural enemies and control, vol. 6. Elsevier Science Publishing, Amsterdam, The Netherlands
Amrine, J.W. 1996b Keys to the world genera of the Eriophyoidea. Indira Pub. House, West Bloomfield, MI
Amrine, J.W. Jr 2002 Multiflora rose, p. 265–292. In: R. Van Driesche, S. Lyon, B. Blossey, M. Hoddle, and R. Reardon (eds.). Biological control of invasive plants in the eastern United States, vol. FHTET-2002-04. USDA Forest Service Publication
Amrine, J.W. Jr, Hindal, D.F., Stasny, T.A., Williams, R.L. & Coffman, C.C. 1988 Transmission of the rose rosette disease agent to Rosa multiflora by Phyllocoptes fructiphilus (Acari: Eriophyidae) Entomol. News 99 239 252
Babu, B., Dankers, H., Newberry, E., Baker, C., Schubert, T., Knox, G. & Paret, M. 2014 First report of rose rosette virus associated with rose rosette disease infecting knockout roses in Florida Plant Dis. 98 1449
Baker, E.W., Kono, T., Amrine, J.W., Delfinado-Baker, M. & Stasny, T.A. 1996 Eriophyoid mites of the United States. Indira Pub House, West Bloomfield, MI
Bauchan, G., Otero-Colina, G., Hammond, J., Jordan, R. & Ochoa, R. 2019 Rose rosette disease: It all started with a small mite Acta Hort. 1232 227 232
Conners, I.L. 1941 Twentieth annual report of the Canadian Plant Disease Survey 1940, p. 97–98
Denight, M.L., Guertin, P.J., Gebhart, D.L. & Nelson, L. 2008 Invasive species biology, control, and research. Part 2, Multiflora rose (Rosa multiflora). In: R. Engineer (ed.). Environmental Laboratory, U.S. Army Engineer Research and Development Center, Vicksburg, MS
Di Bello, P.L., Ho, T. & Tzanetakis, I.E. 2015 The evolution of emaraviruses is becoming more complex: Seven segments identified in the causal agent of rose rosette disease Virus Res. 210 241 244
Dobhal, S., Olson, J.D., Arif, M., Garcia Suarez, J.A. & Ochoa-Corona, F.M. 2016 A simplified strategy for sensitive detection of Rose Rosette Virus compatible with three RT-PCR chemistries J. Virol. Methods 232 47 56
Druciarek, T. & Lewandowski, M. 2016 A new species of eriophyoid mite (Acari: Eriophyoidea) on Rosa sp. from Israel Zootaxa 4066 323 330
Galvao, A., Melo, J., Monteiro, V., Lima, D., Moraes, G. & Gondim, M. Jr 2012 Dispersal strategies of Aceria guerreronis (Acari: Eriophyidae), a coconut pest Exp. Appl. Acarol. 57 1 13
Gergerich, R. & Kim, K. 1983 A description of the causal agent of rose rosette disease. Arkansas Farm Research 32
Hoy, M. 2013 Common name: Eriophyid mite vector of rose rosette disease (RRD) scientific name: Phyllocoptes fructiphilus Keifer (Arachnida: Acari: Eriophyidae), p. EENY-558. In: J.L. Gillett-Kaufman (ed.). Featured creature. University of Florida, Gainsville, FL
Jesse, L.C., Moloney, K. & Obrycki, J. 2006 Abundance of arthropods on the branch tips of the invasive plant, Rosa multiflora (Rosaceae) Weed Biol. Manage. 6 204 211
Laney, A.G., Tzanetakis, I.E., Keller, K.E. & Martin, R.R. 2011 A discovery 70 years in the making: Characterization of the Rose Rosette Virus J. Gen. Virol. 92 1727 1732
Lindquist, E.E. & Amrine, J.W. 1996 Systematics, diagnoses for major taxa, and keys to families and genera with species on plants of economic importance, p. 33–87. In: E. Lindquist, M. Sabelis, and J. Bruin (eds.). Eriophyoid mites—Their biology, natural enemies and control, vol. 6. Elsevier Science Publishing, Amsterdam, The Netherlands
Lindquist, E. & Oldfield, G. 1996 Evolution of eriophyoid mites in relation to their host plants, p. 277–300. In: E. Lindquist, M. Sabelis, and J. Bruin (eds.). Eriophyoid mites—Their biology, natural enemies and control, vol. 6. Elsevier Science Publishing, Amsterdam, The Netherlands
Littell, R.C., Milliken, G.A., Stroup, W.W., Wolfinger, R.D. & Schabenberger, O. 2006 SAS for mixed models. 2nd ed. SAS Institute, Cary, NC
Otero-Colina, G., Ochoa, R., Amrine, J.W., Hammond, J., Jordan, R. & Bauchan, G.R. 2018 Eriophyoid mite found on healthy and rose rosette diseased roses in the United States J. Environ. Hort. 36 4 1288 1294
Shires, M. & Ong, K. 2018 Rose rosette distribution map. In: J. Laforest (ed.). 25 Mar. 2019. <https://roserosette.org/>
USDA-ARS 2012 Agricultural Research Service, Plant hardiness zone map 2012. 30 Mar. 2020. <https://planthardiness.ars.usda.gov/>