Ngubane-Ndhlovu, Nompumelelo P. ¹ ; Ochoa, Ronald ² ; Ueckermann, Edward A. ³ and Kapp, Caro ⁴

¹✉ Plant Health Diagnostic Services, Department of Agriculture, Land Reform and Rural Development (DALRRD), Private Bag X5015, Stellenbosch, 7599, South Africa.
²SEL, ARS, USDA, BARC-W, 10300 Baltimore Ave, Bldg 005, Room 137, Beltsville, Maryland 20705, USA.
³Unit for Environmental Sciences and Management, Potchefstroom Campus, North-West University, Private Bag X6001, Potchefstroom, 2520, South Africa.
⁴Department of Conservation Ecology and Entomology, Stellenbosch University, Private Bag X1, Matieland, 7602, South Africa.

2022 - Volume: 62 Issue: 2 pages: 332-339

Original research

Keywords

Abstract

Introduction

Bougainvillea are ornamental plants native to Brazil and belong to the family Nyctaginaceae. The family consist of approximately 30 genera worldwide. In South Africa, the genus Bougainvillea is represented by three important species, namely, B. spectabilis Willds, B. glabra Choisy and B. peruviana Bonpl. (Douglas and Spellenberg 2010; Struwig and Siebert 2010; Ghogar and Jiraungkoorskul 2017; Saika and Lama 2011).

Fruits and ornamental plants, the most common exported commodities, often host eriophyoid mites. Mite fauna on ornamental plants receive very little attention compared to other agricultural commodities of economic importance (Jeppson et al. 1975; Navia et al. 2010). In 1996, Smith Meyer reviewed nine genera with 24 eriophyoid species associated with ornamental flowering plants worldwide. During the same year, Castagnoli reported 15 genera of Phytoptidae and Eriophyidae as vagrants on ornamental coniferous trees. In addition, a project in Europe inventorying alien species reported 13 eriophyoid species, including the bougainvillea rust mite, Vittacus bougainvilleae (Keifer) (Navia et al. 2010).

Vittacus bougainvilleae was first described, as Phyllocoptes bougainvilleae Keifer, from leaves of Bougainvillea spectabilis Willd. (Nyctaginaceae) collected in Campinas, São Paulo, Brazil (Keifer 1959; Flechtmann and Berti-filho 1994). The bougainvillea rust mite causes upward leaf edge rolling to total leaf rolling from the underside of bougainvillea plants (Keifer 1959; Costa and Carvalho 1960). The mite was reported and redescribed in Kenya on B. glabra var. sandeina (Abou-awad and Elbanhawy 1991). In 1995 and 1998 it was intercepted in Florida and California (USA) from Egypt and Brazil respectively (Welbourn 1995, Navia et al. 2010, Ochoa personal communication). Ochoa and Amrine studied the 1995 and 1998 specimens using low-temperature scanning microscope (LTSEM) (Figure 1). Vittacus bougainvilleae was subsequently reported in Egypt infesting B. spectabilis Willd. B. glabra Choisy and B. luteoalba H. . K. (Nyctaginaceae) (Elhalawany 2018).

The family Tenuipalpidae has a worldwide distribution and all are phytophagous with several species of economic importance. (Welbourn et al. 2003; Mesa et al. 2009; Childers and Rodrigues 2011). Brevipalpus, the second largest genus in the family, has five species recorded in South Africa: B. yothersi Baker (1949), B. lewisi McGregor 1949, B. obovatus Donnadieu (1875), B. californicus (Banks, 1904) and B. ericae Meyer (1979) (Smith-Meyer 1979; Smith-Meyer and Craemer 1999; Saccaggi et al. 2017). Worldwide, three species of tenuipalpids have been reported from Bougainvillea; Brevipalpus phoenicis s.l. (Geijskes 1939) from a Bougainvillea sp. in Brazil and B. glabra in India; and B. californicus (Banks, 1904) and Tenuipalpus shanxiensis Qian et al., 1981 from B. glabra in India and China, respectively (Castro et al. 2021).

This study reports for the first time the presence of V. bougainvilleae in South Africa. It also presents for the first time bougainvillea as a host plant for B. yothersi in the world and for B. californicus in South Africa.

Material and methods

The Department of Agriculture, Land Reform and Rural Development (DALRRD) received a sample of bougainvillea plants from a nursery farm in Hopefield (33°02′45″S 18°20′51″E), Western Cape Province, South Africa, during summer, January 2020. The samples showed symptoms of stunted growth, rolled-up leaves as well as leaf and flower dropping. The plants were found to be infested with eriophyoid mites. To investigate the spread of infestation, samples were also collected from a household in Stellenbosch (33°56′05.7″S 18°50′10.1″E) in January 2020 and again in winter, June 2020. More samples were collected at two other households in Badplass (25°57′24.9″S 30°33′53.9″E) and Elukwatini (26°03′15.9″S 30°47′16.9″E) in Mpumalanga Province in winter, June 2020 and late spring, November 2020.

All mites were collected under a stereomicroscope at a minimum of 30X magnification. Eriophyoid mites were collected from the underside of the leaves into a drop of sorbitol-isopropyl solution, cleared in Keifer's booster and mounted in Keifer's F-medium for identification (Jeppson et al. 1975; Amrine and Manson 1996). Identification to genus level was done with ''The key to world eriophyoid genera'' by Amrine et al. (2003) and identification to species using Keifer (1959), Abou-Awad and Elbanhawy (1991), and Elhalawany (2018). Flat mites were collected from shoots and leaves into 70% alcohol. Mites were cleared in lactic acid and mounted on glass slides in polyvinyl alcohol (PVA) medium (Upton 1991; Evans 1992; Upton 1993). Slide-mounted specimens were identified to family using Krantz and Walter (2009) and further to species using Beard et al. (2012), Beard et al. (2015), Mesa et al. (2009) and Smith-Meyer (1979). Mounted specimens of Eriophyidae and Tenuipalpidae were studied and identified with a Leica DM4B compound microscope with phase contrast and DIC using 10X eyepieces and 100X oil immersion objectives. The microscope was fitted with a camera (Leica MC170 HD) used together with LAS V4.12 software for imaging and processing.

The voucher specimens were deposited in the National Collection of Arachnida – Mites (NCA–Mites) housed by Agricultural Research Council – Plant Health and Protection (ARC-PHP), Pretoria, and Department of Agriculture, Land Reform and Rural Development at Plant Quarantine Station in Stellenbosch, South Africa.

Results

Eriophyoid mites detected on bougainvillea plants from a nursery in Hopefield, were identified as V. bougainvilleae, the symptoms associated with the infestation were stunted growth, rolled-up leaves, as well as leaf and flower dropping (Figure 2). During the same season, specimens of V. bougainvilleae were detected from a Stellenbosch household from asymptomatic plants. However, no mites were detected on the same site during winter. In Mpumalanga, V. bougainvilleae was not found, but flat mites were detected at one site with no visible symptoms. Fifty specimens of V. bougainvilleae were collected in the Western Cape Province (Figures 3-4). Ten specimens of Brevipalpus species comprising B. yothersi and B. californicus were collected in Mpumalanga (Figures 5-6).

Discussion and Conclusion

Vittacus bougainvilleae induced symptoms on bougainvillea plants under controlled growth environment. These plants showed clear signs of curled up leaves, flower, and leaf drop, while no obvious symptoms were observed on infested plants under natural environment. Ngubane (2018) observed that high mite populations were encouraged by high temperatures of between 26°C and 33°C. In this case, high mite populations, which resulted in symptoms in the nursery, might be due to higher temperatures linking to what Ngubane (2018) observed. It is not clear why mites were detected in Western Cape and not in Mpumalanga Province but a possible explanation could be that the current distribution of these mites may be limited to Western Cape. Another reason could be that the mites were sampled out of season in Mpumalanga or other environmental factors. Vittacus bougainvilleae could not be detected in winter in Stellenbosch which is an indication that mites cannot withstand cold temperatures.

The population of Brevipalpus mites on bougainvillea was low, even though the presence of B. californicus and B. yothersi has been observed on different crops for a long time in South Africa (Smith-Meyer 1979). Brevipalpus californicus has been known to affect important crops such as citrus and cotton. For many years B. yothersi has been confused with B. phoenicis (Beard et al. 2015), and more recently it was collected and identified as B. yothersi on grapevine in South Africa (Saccaggi et al. 2017). According to Ulian and Oliveira (2002), B. spectabilis is not favourable to the development of B. phoenicis complex. Therefore, bougainvillea was recommended for use as hedges and/or windbreaks around citrus orchards in Brazil (Maia and Oliveira 2004). This is contrary to our findings where Brevipalpus species were collected on bougainvillea plants. Although the Brevipalpus species did not induce visible symptoms on bougainvillea, the risk associated with the presence of these species cannot be taken lightly, since B. californicus and B. yothersi may vector viruses which may lead to serious crop injuries (Childers and Rodrigues 2011; Rodrigues and Childers 2013).

Acknowledgement

Ms. Dhanani for mite collection and mounting and Dr. Saccaggi at Department of Agriculture, Land Reform and Rural Development for identifications of Tenuipalpidae. To Andrew Ulsamer (SEL-USDA) for his help with references and technical support. Special thanks to the late Eric Erbe and Chris Pooley (ECMU-USDA) for the LT-SEM photos. To the Smithsonian Natural History Museum and National Agricultural Library (NAL-USDA), SEL-USDA for assistance with specimens and references. National Research Foundation of South Africa (Grant Numbers 126938) for partial funding. Views and findings in here are those of the authors and not of the NRF. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA.

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