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Steneotarsonemus ananas (Acari: Tarsonemidae): a complementary description from Australian pineapples and a new pest on Neoregelia spp. (Bromeliaceae) in Costa Rica

Aguilar-Piedra, Hugo 1 ; Solano-Guevara, Ana María 2 ; Seeman, Owen D. 3 and Ochoa, Ronald 4

1✉ Laboratorio de Acarología, Centro de Investigación en Protección de Cultivos (CIPROC), Escuela de Agronomía, Facultad de Ciencias Agroalimentarias, Universidad de Costa Rica, PO Box 2060, San José, Costa Rica.
2Laboratorio de Acarología, Centro de Investigación en Protección de Cultivos (CIPROC), Escuela de Agronomía, Facultad de Ciencias Agroalimentarias, Universidad de Costa Rica, PO Box 2060, San José, Costa Rica.
3Queensland Museum, PO Box 3300, South Brisbane 4101, Australia.
4SEL, ARS, USDA, BARC-W, 10300 Baltimore Ave, Bldg 005, Room 137, Beltsville, Maryland 20705, USA.

2021 - Volume: 61 Issue: 4 pages: 802-823

https://doi.org/10.24349/7u12-OKqx

Original research

Keywords

Steneotarsonemus ananas Tarsonemidae mites Neoregelia Aechmea Bromeliaceae Australia Colombia Costa Rica Guatemala USA (California, Hawaii)

Abstract

The pineapple tarsonemid mite Steneotarsonemus ananas (Tryon), 1898 is associated with pineapple around the world, including Costa Rica. Here, we report its association with Neoregelia sp. (Bromeliaceae) for the first time. These mites damaged the plantlets considerably, affecting the esthetic quality of the product and thus causing economic losses to the local growers. This discovery prompted us to redescribe the adult females and males from the type host and locality (pineapple in Queensland, Australia) and compare it with the original description, subsequent descriptions, and material collected from the USA, Costa Rica, and Colombia on pineapple, Neoregelia, and an unidentified bromeliad. Further specimens from pineapple in Guatemala were identified as the same species and represent the first record for this country. We concur with previous observations that the original description by Tryon is not the same species in subsequent descriptions. We tentatively consider all specimens examined the same as those described as S. ananas in succeeding descriptions, i.e., Steneotarsonemus ananas Tryon sensu Beer.


Introduction

Several phytophagous mite species are associated with pineapple (Ananas comosus [L.] Merr., 1917) including two significant pest species, the red-pineapple mite Dolichotetranychus floridanus (Banks, 1900) (Tenuipalpidae) and the pineapple blister mite Phyllocoptruta sakimurae Keifer, 1966 (Eriophyidae). Additionally, six species of Tarsonemidae are reported: three species of Tarsonemus (T. bilobatus Suski, 1965, T. buchelerei Smiley, 1967, and T. merus Lin & Zhang, 2002) and three species of Steneotarsonemus (S. ananas (Tryon, 1898), S. perezi Cromroy, 1958, and S. comosus Ochoa, 1991 (Ochoa et al., 1991a, 1991b, 1994; Lin and Zhang 2002). Of these species, the best known species of Steneotarsonemus is the pineapple tarsonemid mite, or leathery pocket mite, S. ananas.

Steneotarsonemus ananas was described by Tryon (1898) associated with pineapple fruit in Australia. Since then, it has been collected from Brazil, Costa Rica, Cote d'Ivoire, Ecuador, India, Netherlands, Peru, Philippines, Poland, South Africa, and USA (Hawaii) (e.g., Illingworth 1931; Beer 1954; Jeppson et al., 1975; Mourichon et al., 1987; Mourichon and Sarah 1993; Rohrbach and Johnson 2003; Corpuz-Raros 2005; Petty et al., 2006; De Moraes and Flechtmann 2007, 2008; Pijnakker and Ramakers 2009; Aguilar and Murillo 2012; Joy et al., 2016; Kolicka et al., 2016; Bazan 2018). The species is often linked with leathery pocket disease in pineapple (e.g., Petty 1989; Mourichon 1997). Furthermore, Pijnakker and Ramakers (2009) recorded this species from ornamental bromeliads, and Kolicka et al. (2016) found it associated with the bromeliaceous genera Tillandsia sp. and Aechmea sp. Thus, these mites are associated with several genera in the family Bromeliaceae.

Costa Rica exports a great number of ornamental plants of commercial interest to different markets around the world, including bromeliads in the genera Bromelia and Neoregelia. Although mites often associate with Bromeliaceae (e.g., Nesbitt 1985; Guerra et al., 2012), including S. ananas from pineapples in Costa Rica (Ochoa et al., 1991), no mite species were reported as pests of Bromelia and Neoregelia in Costa Rica. Here, we provide the first record of S. ananas found associated with the ornamental bromeliad Neoregelia spp. Its discovery raised questions about the identity of the species on both pineapple and the new host plant, leading us to redescribe S. ananas from pineapple so that it could be reliably compared to other material. We also describe the symptoms induced by this tarsonemid mite on Neoregelia.

Material and methods

Like many bromeliad genera, Neoregelia is native to the South American rainforests, specifically from southeastern Brazil (Royal Botanic Garden, Kew Science, n.d.), as are pineapples (Coppens d´Eeckenbrugge and Leal 2003), but the first Neoregelia cuttings were brought to Costa Rica from Europe more than 20 years ago and now mother plants are all produced in Pococí, Limón, Costa Rica. Some of the cuttings are developed to the seedling stage on another farm located in the province of Alajuela (810 masl). When they are ready for production, they are transported to the province of Limón to continue their growth. Mother plants are also produced on the farm in Limón, consequently materials from both places are mixed and grown together. Farm workers are responsible for the selection of mature plants and packing them in boxes for shipment to the different markets around the world.

A commercial plantation in Costa Rica, comprising many different bromeliad plant species, was visited on February 2018 because numerous plants were attacked by a small mite, causing visible symptoms. The damage was negatively affecting the quality of the product for export, particularly bromeliads in the genus Neoregelia. Plants for export should lack any injury and foliage must be free of spots, deformations, or any other visible damage.

The plantation, which utilized a black shade cloth (Saran) system, is located in the canton of Pococí, province of Limón, at 467 m above sea level. This zone is known for having high temperatures (24 to 30 oC throughout the year) and humidity (90-100% during the year), as well as considerable annual precipitation mostly through the rainy season. Eighteen samples, consisting of whole plants, were collected in plastic bags and placed into a cooler. The samples were transported to the Laboratory of Acarology at the University of Costa Rica and processed according to the laboratory protocols.

The samples were observed under a stereoscope-microscope, individual leaves were detached manually; then, the symptoms and mite behavior were recorded. The mites were collected in a Syracuse dish with 70% ethanol and mounted on slides in Hoyer´s medium (Krantz and Walter 2009). The slides were processed in an oven at 50oC for three days or until the mites were completely clarified.

Once the mites were ready, the slides were sealed with glossy polyurethane varnish and examined with the help of Olympus BX 51 and Zeiss Axio Imager D1 microscopes, both with phase contrast and DIC (Differential interference contrast), as well as an Axio Imager D1 with DIC.

For the material from Costa Rica, five slides were deposited in the mite collection of the Laboratory of Acarology (CIPROC), University of Costa Rica and two slides with male and female specimens, as well as two larvae, at the Smithsonian (NMNH), National Insect and Mite Collection, Washington DC. Additionally, three larvae, two females and one male from Costa Rica were later prepared and deposited in the Queensland Museum (QM). The Australian material of S. ananas was found as an unidentified tarsonemid mite species in the Queensland Agriculture collection housed at the Queensland Museum (QM). This material, from pineapple in southeast Queensland (the type locality), was examined with phase contrast (Leica DMLB) and DIC (Leica DM2500). Other material examined is housed in the NMNH. A photograph of the first record in the USA of S. ananas on Aechmea (Figure 1) is provided. Morphological terminology follows Lindquist (1986).

Figure 1. First record of Steneotarsonemus ananas (Tryon) 1898 (Tarsonemidae) on Aechmea fasciata (Lindl.) Baker 1879 (Bromeliaceae).

Results

Steneotarsonemus Beer

Steneotarsonemus Beer, 1954: 1229. Type-species Steneotarsonemus hyaleos Beer, 1954, by original designation.

Parasteneotarsonemus Beer & Nucifora, 1965: 40, Lindquist, 1986: 274.

Neosteneotarsonemus Tseng & Lo, 1980: 127; Lindquist, 1986: 274.

Steneotarsonemus are characterized for having: females with stigmata close to setae v1, body elongate-slender, sejugal and poststernal apodemes reduced; males often with round lobes on femorogenu IV; both genders with small pharynx and subcircular to subquadrate gnathosoma (Beer 1954; Lindquist 1986). A full description is provided by Lindquist (1986).

Steneotarsonemus (Steneotarsonemus) ananas (Tryon, 1898)

Tarsonemus ananas Tryon, 1898: 458.

Steneotarsonemus ananas (Tryon), Beer, 1954: 1276.

Diagnosis

All life stages: femur II with three setae; tarsi II-III elongate, longer than wide, setae tc′ on tarsus I distinctly proximal to tc″. Female (Figure 2). Posterior margin of prodorsal plate medially concave and crenate; seta v1 positioned at anterolateral corner of prodorsal plate, anterior of stigmata; bothridial seta sc1 capitate, its head obovate; seta c2 positioned far anterior of seta c1; pore ia positioned far anterior of seta d; setae c1, d, e, f slender to slightly thickened, stiff; seta h thickened; c2 about twice as long as c1 and filiform; setae e and h with minute barbs. Paired remnants of sejugal apodeme each highly curved, boomerang-like; apodemes 3 reaching level of seta 3a; apodemes 4 well developed, almost reaching mid-line; seta 2a positioned on or slightly behind apodeme 2; seta 3a short, not reaching trochanter III; leg IV moderately long, extending to or just beyond idiosomal margin; femur I seta d lanceolate, l′ and l′′ thickened; femur II seta l′ thick; genu II seta l′ thick; seta G v′ IV not reaching base of seta Ti v′ IV. Male (Figure 3). Prodorsum with four pairs of setae; seta sc1 at least three times as long as seta sc2; seta c2 not reaching base of c1; seta c1 not reaching base of seta d; coxisternal plates smooth; apodeme 5 well-developed, forked; femur, genu, tibia II–III without sexually-dimorphic spine-like setae l′, v′; leg IV with small abaxial femorogenual flange and large, semi-circular adaxial flange; seta v′ Ti 30‒54 long, thick. Larva. Setae v1 short, tips not overlapping; setae h1 long, about twice length of h2.

Figure 2. Steneotarsonemus ananas (Tryon). Female, dorsal view.

Figure 3. Steneotarsonemus ananas (Tryon). Male, dorsal view.

Differential diagnosis

Seeman et al. (2016) brought together the two existing subgeneric classifications of Steneotarsonemus, recognizing six subgenera. Steneotarsonemus ananas is best placed in nominate subgenus Steneotarsonemus. However, it does not match this subgenus perfectly as the small abaxial flange on the male femorogenu IV is present in S. ananas and Parasteneotarsonemus. However, this feature is easily missed, and may be present elsewhere in Steneotarsonemus.

Many descriptions of Steneotarsonemus are rudimentary and sometimes lack even basic illustrations of females (e.g., Cromroy 1958) which are essential for classification. Thus, our proposed diagnostic features are tentative. Nevertheless, Steneotarsonemus ananas is unique in Steneotarsonemus by having females with a crenate posterior margin of the prodorsal plate. However, the crenate prodorsal margin does occur in some females of Tarsonemus such as T. stammeri Schaarschmidt, 1959, as well as on Deleonia aguilari Goldarazena & Ochoa, 2002 (Goldarazena et al., 2002).

The two other species of Steneotarsonemus found on pineapple are S. comosus and S. perezi. Steneotarsonemus ananas is differentiated from S. comosus by having females with setae c2 about twice the length of c1 (c1 and c2 subequal in S. comosus) and coxal setae 3a and 3b subequal (3a about twice as long as 3b in S. comosus); and a male with leg IV with a large rounded flange (versus a narrower rectangular flange in S. comosus). Steneotarsonemus perezi is distinguished from S. ananas and S. comosus by having males with setae v1 much longer than v2 (versus v1 shorter than v2).

Description

Female (Figures 4‒7). Measurements are given in Table 1. Idiosoma elongate. Gnathosoma rounded. Dorsal gnathosomal setae ch finely pilose, longer than ventral setae su. Palpi approximate, small, directed anteriorly. Cheliceral stylets short, strongly curved, with basal levers conspicuous. Pharynx short, with muscular, thinly sclerotized walls.

Figure 4. Steneotarsonemus ananas (Tryon). Female, ventral view. Idiosoma and legs III and IV.

Figure 5. Steneotarsonemus ananas (Tryon). Female, ventral view. A – phase contrast; B – differential interference contrast.

Dorsum. Prodorsal plate truncated anteriorly, not projected beyond basal part of gnathosoma, posterior edge concave, crenated with 7 to 8 fine lobes (Figure 6A). Stigmata on anterior margin of prodorsal plate, situated closely posterolaterad of setae v1; main tracheal trunks with small, fine sclerotized atria, each atrium divided into two elongate halves. Setae v1 filiform, finely pilose; setae sc2 long, filiform, about twice the length of v1. Bases of sc2 posterolaterad setae sc1. Bothridial setae sc1, capitate, finely pilose. Setae c1, filiform, shorter than setae c2, also filiform. Bases of c2 located anterolaterad c1. Cupules ia anterolaterad setae d. Setae d, e and f simple, finely barbed, similar in length, setae e slightly thicker than setae d and f. Tergite EF with base of setae e located anterolaterad setae f. Cupules im anteromedial of setae e. Setae h stout, barbed, slightly longer than v1.

Figure 6. Steneotarsonemus ananas (Tryon). Female. A – Propodosoma, dorsal view (crenulation); B – Leg IV, and apodemes III and IV.

Venter. Apodemes I short, united with prosternal apodeme; apodemes II conspicuous and curved, not united with prosternal apodeme. Prosternal apodeme not extending posteriad of apodemes II, with a bifurcated ending. Sejugal apodeme reduced to two lateral highly-curved, boomerang-like fragments. Apodemes III slender, conspicuous, curving posteromedially near setae 3a. Apodemes IV slender (Figure 6B), extending anteriorly about ¾ distance to 3a. Poststernal apodeme absent. Setae 1a, 2a, 3a, 3b slender, similar in length, 3a, 3b longest. Tegula 3-4 times longer than wide, truncated apically. Pseudanal setae slender, slightly longer than v1.

Legs (Figure 7). Leg III longer than legs I, II and IV. Leg IV cylindrical; terminal seta tc″ filiform, about three times longer than subterminal seta v′Ti; subterminal setae stout, finely pilose; femorogenu with genual seta v′G slightly shorter than seta v′F.

Figure 7. Steneotarsonemus ananas (Tryon). Female. A – tibiotarsus I; B – tarsus II.

Setal counts for legs I‒III (femur to tarsus): leg I (Fe-Ta) 4-4-6(+2φ)+8(+ω), 3-3-4-6(+ω), 1+3-4-5. Setae smooth, slender, unless otherwise mentioned. Leg I: femur I, d lanceolate, barbed, 7‒8, l′ thickened, weakly barbed, 6‒7, l″ narrowly lanceolate, weakly barbed, 7‒8, v″ 10‒12; genu I, l′ shortest, 5, l″ longest, 10‒12; tibiotarsus I, d longest, 23‒28, ϕ1 5, ϕ 3‒4, k 5, p′ 10‒11, p″ 12‒14, tc′ 15‒16, tc″ 16‒18, s with weakly bifid tip, 3, ω 6‒7. Leg II: femur II, d thickened, 4‒5, l′ narrowly lanceolate, barbed, 6‒8, v″ 5‒8; genu II, l′ narrowly lanceolate, 6‒7, l″ weakly barbed, v′ 4‒5; tibia II l′ shortest, 8‒9, d, v′, v″ 18‒23; tarsus II, seta pl′ thick, thorn-like, 4, tc″ longest, 20‒26, u′ with weakly bifid tip, 3, ω 4‒5. Leg III: femorogenu III Fv′, Gv′, Gv″ short, 3‒5, Fl′ longer, 11‒14; tibia III, d shortest, 4‒6, v′, v″ longest, 15‒21; tarsus III, tc″ longest, 26‒32, u′ with weakly bifid tip, 3‒4. Leg IV with seta Ti v′ barbed, thick (measurements in Table 1).

Table 1. Morphometric data (presented as ranges, in μm) for females of Steneotarsonemus ananas collected from Australia (ex pineapple), Costa Rica (ex Neoregelia), Colombia (ex unidentified bromeliad), and USA (ex Aechmea fasciata).

Male (Figures 8‒10) (n = 5 from Neoregelia; n = 2 from Queensland pineapple). Measurements are given in Table 2. Idiosoma broadest near level of c2, body length variable in Costa Rican population (ca. 20% length variation versus 2.5% width variation). Gnathosoma oval rounded. Dorsal gnathosomal setae finely barbed basally, ventral gnathosomal setae smooth. Cheliceral stylets moderately short, straight. Pharynx small, same as female, with muscular, thinly sclerotized walls.

Figure 8. Steneotarsonemus ananas (Tryon). Male. Ventral view. Idiosoma.

Figure 9. Steneotarsonemus ananas (Tryon). Male. Ventral view. A – phase contrast; B – differential interference contrast.

Dorsal plates unornamented (Figure 10A). Prodorsal plate weakly sclerotized, subtriangular. Vertical setae v1, slender, slightly barbed, shorter than v2. Scapular setae sc1 simple, slightly pilose, longer and thicker than sc2. Base of sc2 aligned with v2-sc1.

Figure 10. Steneotarsonemus ananas (Tryon). Male. A – Dorsal view of propodosoma; B – Ventral view of leg IV (detailed).

Plate CD with setae c2, filiform, two times longer than c1. Setae c1 and d stout, barbed. Plate EF with setae f, stout, pilose. Setal lengths vary between populations: Australian specimens with much shorter setae compared with Costa Rican and Colombian populations, USA intermediate (Table 2). Genital capsule as long as wide, with accessory copulatory structures ps1 spinelike, pointed apically.

Venter. Apodemes I short, united with prosternal apodemes; apodemes II conspicuous and distally curved, weakly united with prosternal apodemes. Prosternal apodemes not reaching posterior podosomal margin. Sejugal apodemes absent. Apodemes III, IV, poststernal apodeme united; apodemes V separate, joining poststernal apodeme.

Legs. Legs I-II, IV subequal in length; leg III longer than leg IV. Leg IV with large adaxial rounded flange and narrow distal abaxial flange (Figure 10B).

Leg setation for legs I-III same as female except for addition of small ft″ on tarsus I. Setal form similar except for: femur I, all setae smooth, slender or only slightly thickened, d 5‒ 7, l′ 4‒5, l″ 6‒7, v″ 7‒8; genu I setae 8‒14, l′ not obviously shorter than other setae; femur II setae smooth, slender or only slightly thickened; genu II setae smooth, slender; femur III setae v′, l′ similar length, 13‒17; tibia III seta d long, 16‒22. Measurements from Australian specimens; males from Costa Rica with longer setae (Table 2).

Table 2. Morphometric data (presented as ranges, in μm) for males of Steneotarsonemus ananas collected from Australia (ex pineapple), Costa Rica (ex Neoregelia), Colombia (ex unidentified bromeliad), and USA (ex Aechmea fasciata).

Larva (from Neoregelia spp. material) (Figures 11-13). Idiosoma length 170‒270, width 95‒115. Gnathosoma rounded, length 32‒33, width 32‒33; setae ch 13‒14, su 7‒8.

Figure 11. Steneotarsonemus ananas (Tryon). Larva. Dorsal view.

Figure 12. Steneotarsonemus ananas (Tryon). Larva. Ventral view.

Figure 13. Steneotarsonemus ananas (Tryon). Larva. A – Dorsal view; B – Idiosoma; C – Prosoma; D – Hysterosoma.

Prodorsal plate with setae v1 4–8, sc1 6‒8, sc2 22‒26; opisthosoma with setae c1 5‒9, c2 8‒10, setae c2 usually longer than c1; d 6‒9; e 11‒13, f 10‒12; caudal setae h1 22-25, about twice as long as h2 11-13, setae ps1 and ps2 4‒5. All idiosomal setae slightly thickened and minutely pilose, setae sc2, c1, d, e, f thicker than other setae, their tips blunt; setae ps1-2 fine, smooth.

Ventral apodemes ap1, ap2 and appr distinct, ap2 not reaching appr; sejugal apodeme not apparent; ap 3 indistinct. Setae 1a, 2a small, slender, length 3; setae 3a, 3b longer, length 4‒6.

Legs. Leg setation for legs I-III similar to female except lacking ϕ2 on tibia I, proral setae on tarsus I and pv′ on tarsi II-III. Form of setae similar to female except for: femur I seta d only slightly thickened, peg-like, 2‒3, other setae slender, smooth; genu II seta l′ not shorter than other setae; femur II, genu II setae slender, smooth; tibia III with short, thick thorn-like seta l′, 3.

Material examined. 56 females, 35 males, 2 pharate males, 6 larvae as follows. Australia: 6 females, 2 males, 1 pharate male, Cooroy, Queensland, 4 Apr. 1968, C. Dodson, ex pineapple (mount by J.J. Davis, in Hoyers), deposited in QM. Colombia: 12 females, 9 males, 1 pharate male, Fusagasuga, Cundinamarca, 13 Dec. 1997, D. Navia, ex Bromeliaceae (cup), deposited in NMNH, Smithsonian, USA. Costa Rica: 17 females, 11 males, 5 larvae, Pococí Limón, 28 Feb. 2018, H. Aguilar, ex Neoregelia spp. (8 females, 3 males, 2 larvae, deposited in NMNH; 9 females, 8 males, deposited in the Laboratory of Acarology, Univ. of Costa Rica; 2 females, 1 male, 3 larvae deposited in QM); 10 females, 3 males, 1 larva, Venecia, San Carlos, Alajuela, 25 Feb. 2009, A. Obando, pineapple, deposited in the Acarology Lab., Univ. of Costa Rica; 1 female, 1 male, interception, Philadelphia, PA, from Costa Rica 28 Nov. 1994, F. Salantri, ex Ananas comosus, deposited in NMNH; 2 females, 1 male, interception Philadelphia CBP, PA, from Costa Rica 14 Mar. 2016, G. Evans, ex Ananas comosus, deposited in NMNH. Guatemala: 2 females, 2 males (poor condition), interception Wilmington CBP, DE, from Guatemala, 2 Aug. 2016, E. McDonald, ex. Ananas comosus, deposited in NMNH. United States: 4 females, 5 males, Brea, CA, 18 Mar. 1966, R. Smiley, ex Aechmea fasciata, deposited in NMNH.

Discussion

Tryon (1898) described S. ananas from mites collected on pineapples showing severe symptoms of fruitlet core rot, which is caused by Fusarium fungi and linked to the feeding of S. ananas by Tryon (1898) and later by several studies (e.g., Petty et al., 2006).

Unfortunately, Tryon (1898) did not mention the specimens on which the species is based: they are merely an undisclosed number of mites from pineapples in southern Queensland. Ewing (1939) did not examine type specimens, instead relying on Tryon's manuscript and female and larval material from Hawaii. Beer (1954) considered the whereabouts of Tryon's material ''unknown″, again relying upon Ewing´s material from Hawaii. In the past decade or so, several unsuccessful efforts were made to locate these type specimens at the Queensland Department of Agriculture collection, the Queensland Museum, and the Australian National Insect Collection.

Tryon's drawings and descriptions are, not surprisingly for their time, rudimentary, however, we doubt that the species described by Tryon (1898) is the same species later called S. ananas by subsequent authors. Tryon (1898) provided ventral views of each sex. The male shows a few significant differences from later descriptions (Beer 1954; Jeppson et al., 1975). First, the flange on leg IV is absent in Tryon (1898), but with a low-powered microscope, it is unlikely but possible that the flange was misinterpreted as a spine-like process. Second, in his original description the male is widest just anterior to seta c1, whereas in subsequent descriptions of the male, it is widest just anterior to seta c2. Third, Tryon (1898) also shows an undivided apodeme 5, but male S. ananas have a posteriorly forked apodeme 5. The female presents further significant differences that are incongruous not only with S. ananas in subsequent descriptions (Ewing 1939; Beer 1954; Jeppson et al., 1975) but also with Steneotarsonemus. Instead of an elongate body as in Steneotarsonemus, it is ovate; rather than short setae h, they are long; contrary to separate apodemes 3, they are joined; instead of lacking a post-sternal apodeme, it is present; rather than separate apodemes 4, they join the post-sternal apodeme. Therefore, the mite described by Tryon is not S. ananas as currently defined. It is not Steneotarsonemus. A similar conclusion is reached in Kolicka et al. (2016), who doubted that S. ananas (Tryon, 1898) was the same species described by later authors as S. ananas.

What is S. ananas (Tryon, 1898)? We are unaware of any species of tarsonemid that matches his original description. The only tarsonemid mites described from Bromeliaceae are the six species known from pineapple and records of S. ananas from other bromeliad hosts (Lin and Zhang 2002; Kolicka et al., 2016). Thus, as Tarsonemus is the only other tarsonemid genus known from Bromeliaceae, perhaps Tryon (1898) described a species of Tarsonemus rather than Steneotarsonemus. This genus at least has females with an ovate body and more complete apodemes. Unfortunately, the three species of Tarsonemus recorded on pineapples (T. bilobatus, T. buchelerei, and T. merus (Suski 1965; Smiley 1967; Flechtmann 1971; Lin & Zhang 2002)) bear no great similarity with S. ananas sensu Tryon (1898). Until material matching Tryon's description is found, the true identity of S. ananas will remain a mystery.

Ewing (1939) provided the first description of S. ananas after Tryon (1898). While he copied the description of the male from Tryon, his description of the female was new. However, the specimens examined, two females and a larva (''nymph″), were poorly and incompletely described making the description unsuitable for identification purposes or comparison with Tryon (1898). Thus, the first complete description is that of Beer (1954), who also provided the first description of the male, and we thus consider the species Steneotarsonemus ananas (Tryon, 1898) sensu Beer (1954). Unfortunately, the specimens of Ewing (1939) have not been located, and Beer´s (1954) material in the University of Kansas is not available.

The specimens from Australia, described here, are from the type locality and host for S. ananas, but are clearly not the same species described by Tryon (1898) and instead match S. ananas sensu Beer. Comparisons between females from Queensland pineapple, Costa Rican Neoregelia and pineapple, Colombian bromeliad and Californian (USA) ornamental bromeliad demonstrated not only concordance with diagnostic features but also measurements (Table 1). However, males were less similar (Table 2). While they all agree in general diagnostic features, some setal lengths differ considerably in size with males from Queensland pineapple having much shorter setae than those found on Costa Rican Neoregelia and Colombian bromeliads. As intraspecific variation in males is known in Tarsonemidae (e.g., Tarsonemus waitei Banks, Lindquist (1978)) and other collections from USA pineapples were intermediate in size, we tentatively consider these differences as intraspecific. Thus, they are all S. ananas sensu Beer (1954), pending further studies into the identity of Steneotarsonemus species on pineapple throughout the world.

Description of symptoms on Neoregelia spp. (Bromeliaceae)

Mites were observed grouped in the interior of the plant, especially hidden on the underside of the leaves, near the axils of the younger foliage. The leaves also form rosettes, which compose microreservoirs in the axils, beneath the main phytotelmata of the plant. This provides a good habitat for many organisms, including tarsonemid species, which require warm temperatures, high humidity and low light intensity to develop (Jeppson et al., 1975). The feeding damage shows a light brown color, mostly in the middle of the young leaf surface (Figures 14A and 14B), while the apex remains green and the base of the leaf white in color, which serves as a depository camouflaging a high concentration of wandering mites and eggs.

Figure 14. A – Damage caused by Steneotarsonemus ananas on Neoregelia spp., Limón, Costa Rica; B – Symptoms provoked by S. ananas on Neoregelia spp. Limón, Costa Rica; C- Old damage caused by S. ananas on Neoregelia spp. Limón, Costa Rica.

When the leaves develop and become more coriaceous, red spots of different diameters appear along the leaves upper side. These spots are the remnants of the earlier feeding damage by S. ananas. The dimensions of the brownish discolorations could be associated with the population density at the time of feeding (Figure 14C).

It is at this point in the plant's development, when the mites are no longer present, that these symptoms are most likely to be noticed by farm personnel in charge of monitoring the plants. Plants exhibiting such damage are not commercially acceptable for export.

The damage caused by S. ananas on pineapple occurs on growing plants during the development of the inflorescence, fruit and crown (Jeppson et al., 1975; Py et al., 1987; Rohrbach and Johnson 2003), which is similar to the symptoms caused by this organism on Neoregelia. As noted, the pineapple tarsonemid mite has also been associated with Fusarium and also in the pathogenesis of Penicillium funiculosum Thom, (1910) (Rohrbach et al., 1981). Another important factor is the presence of an entomopathogenic fungus, Hirsutella spp. (Umaña et al., 1990; Zoebisch et al., 1992; Quesada-Sojo and Rivera-Mendez 2016), associated with soil and bromeliads in Costa Rica; species of this fungus genus could be used for the control of phytophagous mites like S. ananas that live in concealed places on their host plants. Further studies on the biology of the mite are required for effective monitoring, focused on the plant phenology, as well as control measures, both chemical and biological.

In conclusion, we consider Steneotarsonemus ananas sensu Beer (1954) to be the species found on pineapple and several other bromeliaceous plants world-wide, where it causes damage through both its feeding and association with pathogenic fungi. Its taxonomy remains difficult, in part due to the lack of types, and that at least two species are involved: the species originally described by Tryon (1898) and that described by Beer (1954), Jeppson et al. (1975), and also probably by Ewing (1939). However, the presence of other species of Steneotarsonemus on pineapple, and the intraspecific variation in males noted here, suggest the problem requires a much larger revision involving fresh samples from numerous hosts and countries, combining both morphology and molecular methods.

Acknowledgements

To Debra Creel, Michele Touchet and Andrew Ulsamer (SEL-USDA), Peter Touhey, Mary Joyce and Eric McDonald (APHIS-USDA), Sara Cascante-Gamboa (Biblioteca de Ciencias Agroalimentarias, UCR), for their assistance with references, collection material and helpful suggestions. We are also grateful for the careful work reviewing the manuscript of José Marcos Rezende (Escola Estadual Tiradentes, Iturama; Sistema COC - Colégio FAMA-MG, Brazil), and Wojciech Magowski (Faculty of Biology, University of Poznań-Poland). Dr. Magowski generously shared information on Australian S. ananas, as well. Similarly, to Drs Jurgen Otto and Ross Rickard (DAWE) for helping us navigate the idiosyncrasies of importing museum specimens into Australia. Special thanks to Jenny Beard (Queensland Museum, South Brisbane, Australia) and Denise Navia (previously on EMBRAPA-Brazil; today on INRAE, UMR, GBGP, Montpellier, France) for the help with information on Australian pineapple tarsonemid specimens and bromeliad tarsonemid specimens from Colombia; and also, to Bruce Halliday (ANIC, Canberra, Australia) for valuable advice and literature. To Adriana Matamoros (San José, Costa Rica) for her labor on design, and other details related to the artworks. To the Smithsonian National Museum of Natural History (NMNH), National Agricultural Library (NAL), Systematic Entomology Laboratory (SEL-USDA), Centro de Investigación en Protección de Cultivos (CIPROC), Escuela de Agronomía, Facultad de Ciencias Agroalimentarias, Universidad de Costa Rica (UCR) for their support with materials, references and equipment. The 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, CIPROC and UCR; USDA is an equal opportunity provider and employer.



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Date received:
2021-04-04
Date accepted:
2021-09-29
Date published:
2021-10-11

Edited by:
Auger, Philippe

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2021 Aguilar-Piedra, Hugo; Solano-Guevara, Ana María; Seeman, Owen D. and Ochoa, Ronald

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