https://orcid.org/0000-0002-1412-1554
Figures
Abstract
Predatory mites in the family Phytoseiidae (Acari: Mesostigmata) are of great importance as biological control agents of pest mites and other arthropods. Correct identification of species is crucial to implement effective biological control of target pests. Here, we provide re-descriptions of seven phytoseiid mite species collected from citrus orchards in Florida. The several important morphological features including dorsal setae lengths, dorsal solenostomes, shape of calyx of spermatheca, chelicera dentition, measurements, and shape of macrosetae on legs currently used to discriminate phytoseiid species were missing in the original descriptions and re-descriptions of these species. Additionally, we observed the presence of a previously unnoted taxonomically important character on Proprioseius meridionalis Chant. Therefore, the re-description was essential for further diagnosis of this species. Accordingly, the validity of the presence/absence of this structure as a diagnostic character to separate species groups in the genus Proprioseius should be re-considered. Furthermore, Typhlodromalus peregrinus, a species for which a series of morphological variations are reported in previous descriptions, is re-described and illustrated from Clermont, Florida, a location very close (10 km) to its type location (Minneola), and the leaves of type host citrus. The macrosetae StIV was knobbed apically in all our specimens of T. peregrinus indicating invalidity of sharp-pointed or knobbed StIV to separate this species from a closely related species, T. aripo De Leon. These re-descriptions and species are important to utilizing authentic and promising candidates for biological control.
Citation: Demard EP, Döker I, Qureshi JA (2021) Re-description of seven predatory mite species of family Phytoseiidae (Acari: Mesostigmata) sourced from Florida citrus groves. PLoS ONE 16(8): e0255455. https://doi.org/10.1371/journal.pone.0255455
Editor: Michael Schubert, Laboratoire de Biologie du Développement de Villefranche-sur-Mer, FRANCE
Received: August 20, 2020; Accepted: July 16, 2021; Published: August 20, 2021
Copyright: © 2021 Demard et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All data is made available in the manuscript.
Funding: This research work is based upon work that is supported by the National Institute of Food and Agriculture, U.S. Department of Agriculture (https://nifa.usda.gov/), under award number 2018-70016-27387, awarded to A. Schumann, J. Qureshi, A. Singerman, P. Rolshausen, and R. Ferrarezi. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Predatory mites in the family Phytoseiidae (Acari: Mesostigmata) are important biological control agents of many pest species that include spider mites, thrips, and whiteflies [1, 2]. They may also attack the relatively recently introduced Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), responsible for vectoring the causal pathogens of huanglongbing or citrus greening disease that is currently spreading across Florida and other states [3, 4]. The phytoseiid species such as Amblydromalus limonicus (Garman & McGregor), Amblyseius andersoni (Chant), A. swirskii Athias-Henriot, Neoseiulus barkeri Hughes, N. californicus (McGregor), N. cucumeris (Oudemans), N. fallacis (Garman), Transeius montdorensis (Schicha) and Phytoseiulus persimilis Athias-Henriot are currently reared on a commercial scale and utilized to control several pests all over the world [5]. Determination of the identity of native populations of predatory mites is of considerable importance for achieving effective local pest control. Indigenous populations or species can often provide greater control success in the specific region and environmental conditions to which they are adapted [6].
Phytoseiid mite fauna in the United States has been well documented with about 370 species [7–11]. A total of 140 species, including synonyms, have been reported from Florida [1, 11, 12]. Studies on phytoseiid taxonomy from Florida date back to the mid-1950s with a series of new species being described between 1955 to 2011 [1, 13–17]. However, most of these descriptions or re-descriptions did not include many crucial taxonomical characters which are currently used to discriminate phytoseiid species such as dorsal setae lengths, dorsal solenostomes, shape of calyx of spermatheca, chelicera dentition, and measurements and shape of macrosetae on legs. The inadequate descriptions and re-descriptions or the absence of re-descriptions for some phytoseiid species have made accurate species identifications a challenge. This situation has often resulted in misidentifications and overall confusion among taxonomists.
We have been collecting predatory mites from multiple citrus groves in Florida, to find and identify species for biological control in citrus crops. The older descriptions or re-descriptions of some species lacked some important morphological features for species identification. Those did not include the necessary details for species separation, and therefore do not meet the current standards. We provide the re-description of seven phytoseiid mite species collected from multiple locations in Florida and important for biological control.
Materials and methods
Mite species and locations of collection
Permission was sought and granted from the orchard owners prior to undertaking all field collecting for this study. Information on the species, their habitat, and the location of the collection are provided in Table 1.
Extraction of mites from samples
The ground cover and canopy leaf samples were washed in a jar filled with 250 ml of 80% ethanol. The jar was shaken for about 30 seconds to dislodge the mites. The vegetative material from the jars was then retrieved using forcep and discarded. Leaf litter samples were collected in a four-gallon plastic bag and then processed through the Berlese funnel (Collapsible Berlese funnel, BioQuip, CA, USA) and stored in 80% ethanol. The mites were kept in 60% lactic acid for 24 hours at 55°C.
Mounting and examination of the specimens
Specimens were mounted on microscope slides using Hoyer’s medium and dried on a slide warmer at 50°C (Premiere® XH-2004) for five days. Further examinations were conducted using an Olympus® CX-41 microscope. Pictures of type specimens were taken with a Leica® DMC2900 camera mounted on a Leica® DM1000 LED microscope and a Zeiss AxioCam ICc5 camera mounted on a Zeiss Axio Imager D1 microscope. The taxonomic system is based on that proposed by Chant & McMurtry [18]. The dorsal and ventral setal pattern notations follow Chant & Yoshida-Shaul [19–21]. Other terminologies follow Athias-Henriot [22, 23] for organotaxy, and Evans [24], and Evans & Till [25] for the ventral pores and leg chaetotaxy. The species redescribed were assigned consecutive numbers and arranged according to the commonly used taxonomic system worldwide [18]. After a species’ scientific name, the numbers in the parenthesis refer to the article and follow with the page number containing previously reported information on a particular species. Illustrations were prepared using an Olympus U-Da drawing attachment camera Lucida. Measurements are given in micrometers as mean followed by the range in parenthesis. Examined specimens were deposited into the mite collection of the Acarology Laboratory, Department of Plant Protection, Çukurova University, Adana, Turkey, and the Indian River Research Center, University of Florida, Fort Pierce, Florida, USA.
Results and discussion
Family Phytoseiidae Berlese, subfamily Amblyseiinae Muma Tribe Neoseiulini Chant & McMurtry, genus Neoseiulus Hughes
1. Neoseiulus marinellus (Muma).
Cydnodromus marinellus [14]: 8.
Neoseiulus marinellus (Muma) [26]: 101; [27]: 667; [28]: 35; [1]: 147.
Female (n = 5).
Dorsum (Fig 1A). Dorsal setal pattern 10A:9B (r3 and R1 off shield). Dorsal shield oval with a slight waist at the level of Z1, smooth except for a few anterolateral striations. Bearing five pairs of rounded solenostomes (gd1, gd2, gd4, gd6, and gd9). Muscle-marks (sigilla) visible on podosoma, length of dorsal shield 313 (293–325), width (distance between bases of s4) 143 (133–148), width (distance between bases of S2) 151 (141–155). All dorsal setae smooth. Measurements of dorsal setae as follows: j1 13 (10–14), j3 16 (12–18), j4 15 (14–16), j5 15 (15–16), j6 16 (15–17), J2 18 (17–20), J5 11 (11–12), z2 15 (14–16), z4 17 (16–17), z5 15 (14–16), Z1 16 (15–18), Z4 23 (22–24), Z5 24 (21–26), s4 16 (14–17), S2 19 (18–20), S4 18 (17–19), S5 16 (15–17), r3 15 (14–16), and R1 13 (11–15).
Neoseiulus marinellus (Muma)–Female (A–E): A. Dorsal shield, B. Ventral idiosoma, C. Chelicera, D. Spermatheca, E. Leg IV. Scale bars = 100 μm for A, B; 30 μm for C, D; 60 μm for E (Photo credit: Ismail Döker).
Peritreme. Long, extends beyond setae j1.
Venter (Fig 1B). Ventral setal pattern 14:JV–3:ZV. Sternal shield smooth, lightly sclerotized with three pairs of setae (ST1, ST2, ST3), two pairs of poroids (pst1 and pst2). Distance (ST1–ST3) 59 (58–61), width (ST2–ST2) 61 (60–63). Metasternal setae ST4 and a pair of pores (pst3) on metasternal shields. Genital shield smooth; width at level of genital setae (ST5) 58 (55–62). Ventrianal shield reticulated, bearing three pairs of pre-anal setae (JV1, JV2, and ZV2), a pair of para-anal (Pa) and a post-anal seta (Pst), and with a pair of small rounded solenostomes (gv3) posteromedian to JV2; distance gv3–gv3 33 (31–34). Length of ventrianal shield 103 (99–108), width at level of ZV2 83 (78–87), width at level of anus 68 (65–71). Setae JV4, JV5, ZV1, ZV3, and four pairs of poroids on integument surrounding ventrianal shield. Two pairs of metapodal plates, primary 20 (19–20), and secondary 11 (10–11) in length. Setae JV5 smooth, 27 (26–28) in length.
Chelicera (Fig 1C). Fixed digit 29 long with five teeth, with pilus dentilis; movable digit 30 long with one tooth.
Spermatheca (Fig 1D). Calyx trumpet-like, elongated, flaring distally, 33 (31–34) in length; atrium nodular, enlarged, broadly joined to the calyx; major duct broad.
Legs (Fig 1E). Length of legs (base of coxae to base of claws) as follows: leg I 285 (280–290), leg II 213 (210–215), leg III 200 (195–205), leg IV 270 (265–275). Genua II, III, and IV each with seven setae. No macrosetae present on legs.
Remarks. Neoseiulus marinellus description by Muma [14] was based on the material collected from leaf litter under Citrus sp. in Minneola, Florida. Many morphological details including measurements of dorsal setae were missing in the original description and subsequent re-descriptions [26, 27]. Here, we provide a complementary description of this species for the first time from specimens collected from citrus leaf litter from three locations in Florida. Morphological characters of the current specimens examined in this study are in agreement with those of type materials (Fig 2).
2. Neoseiulus planatus (Muma).
Cydnodromus planatus [14]: 9.
Neoseiulus planatus (Muma); [26]: 104; [27]: 667; [28]: 37; [1]: 152.
Female (n = 1).
Dorsum (Fig 3A). Dorsal setal pattern 10A:9B (r3 and R1 off shield). Dorsal shield oval with a slight waist at level of Z1, smooth. Bearing five pairs of rounded solenostomes (gd1, gd2, gd4, gd6, and gd9). Muscle-marks (sigilla) visible mostly on podosoma, length of dorsal shield 333, width (distance between bases of s4) 178, width (distance between bases of S2) 188. All dorsal setae smooth. Measurements of dorsal setae as follows: j1 15, j3 18, j4 17, j5 16, j6 17, J2 17, J5 14, z2 15, z4 18, z5 18, Z1 21, Z4 30, Z5 35, s4 23, S2 25, S4 21, S5 20, r3 18, and R1 17.
Neoseiulus planatus (Muma)–Female (A–E): A. Dorsal shield, B. Ventral idiosoma, C. Chelicera, D. Spermatheca, E. Leg IV. Scale bars = 100 μm for A, B; 30 μm for C, D; 60 μm for E (Photo credit: Ismail Döker).
Peritreme. Long, extending beyond setae j1.
Venter (Fig 3B). Ventral setal pattern 14:JV–3:ZV. Sternal shield smooth except few anterior striations, sclerotized with three pairs of setae (ST1, ST2, ST3), two pairs of poroids (pst1 and pst2). Distance (ST1–ST3) 60, width (ST2–ST2) 60. Metasternal setae ST4 and a pair of pores (pst3) on metasternal shields. Genital shield smooth; width at level of genital setae (ST5) 58. Ventrianal shield reticulated, bearing three pairs of pre-anal setae (JV1, JV2, and ZV2), a pair of para-anal (Pa), and a post-anal seta (Pst), and with a pair of small rounded solenostomes (gv3) posteromedian to JV2; distance gv3–gv3 25. Length of ventrianal shield 115, width at level of ZV2 90, width at level of anus 75. Setae JV4, JV5, ZV1, ZV3, and six pairs of poroids on integument surrounding ventrianal shield. Setae JV5 smooth, much longer than other ventral setae, 33 in length.
Chelicera (Fig 3C). Fixed digit 30 long with three apical teeth, with pilus dentilis; movable digit 30 long with one tooth.
Spermatheca (Fig 3D). Calyx saccular, elongated, flaring distally, 20 in length; atrium broad and forked at the juncture with major duct, slightly narrowing where it joins to the calyx; major duct very broad.
Legs (Fig 3E). Length of legs (base of coxae to base of claws) as follows: leg I 318, leg II 233, leg III 215, leg IV 313. Genua II, III, and IV each with seven setae. A short and sharp-pointed macrosetae is present on leg IV, StIV 33 in length.
Remarks. Neoseiulus planatus described by Muma [14], came from the material collected from leaf litter under Citrus sp. in Avon Park, Florida. Many morphological details of this species including measurements of dorsal setae were missing in the original description. The subsequent re-description by Muma & Denmark [26] contained relatively detailed drawings but was still missing the dorsal setae measurements. Most likely due to the inadequate descriptions, this species was treated as “uncertain species” in barkeri species group and barkeri species subgroup in the most recent revision of the genus by Chant & McMurtry [29]. Denmark & Evans [1] included several measurements such as j3 (20), z2 (20), z4 (20), Z4 (36), Z5 (53), and calyx of spermatheca (21) in an identification key for the genus Neoseiulus found in North America and Hawaii. Their measurements match with those of the current specimen that we report except for Z5 (35 vs 53). We consider this difference as intraspecific variation because the current specimen was collected approximately 100 km east of its type location. After examination of the spermatheca from a specimen identified by Muma in 1961, we found no differences with our specimen. Indeed, the calyx length between the specimens was the same (20 μm) (Fig 4). We also measured and found no difference in dorsal, ventral, and ventrianal setae between specimens. Unfortunately, the spermatheca was not obvious in the pictures sent by Dr. Ronald Ochoa to confirm it with the holotype.
Tribe Kampimodromini Kolodochka, genus Proprioseius Chant
3. Proprioseius meridionalis Chant.
Proprioseius meridionalis [15]: 358; [30]: 111; [31]: 259; [26]: 25; [32]: 206; [1]: 229.
Female (n = 5).
Dorsum (Fig 5A, 5F). Dorsal setal pattern 10A:6E (r3 and R1 off shield). Dorsal shield oval with a slight waist at level of R1, strongly sculptured. Bearing three pairs of solenostomes (gd2, gd6, and gd9). Some muscle-marks (sigilla) visible on podosoma, a subcylindrical erect structure is located posterior to setae j6, length of dorsal shield 279 (273–285), width at level of s4 143 (138–150), width at level of Z4 147 (145–150). Dorsal setae j1, j3, z2, Z4, Z5, s4, S5, and r3 are strongly serrated, and arises on tubercules. Other setae are simple, setae z4, z5, Z1, J5 and R1 also arise on tubercules. Measurements of dorsal setae as follows: j1 23 (20–25), j3 26 (25–28), j4 12 (10–13), j5 10, j6 13 (13–15), J5 12 (10–13), z2 23 (23–25), z4 18 (18–20), z5 10 (8–13), Z1 19 (18–20), Z4 63 (63–65), Z5 68 (65–70), s4 51 (50–53), S5 18 (15–20), r3 23(20–25), and R1 17 (15–18).
Proprioseius meridionalis Chant–Female (A–F): A. Dorsal shield, B. Ventral idiosoma, C. Chelicera, D. Spermatheca, E. Leg IV, F. Sub-cylindrical erect structure on dorsal shield. Scale bars = 100 μm for A, B; 30 μm for C, D, F; 60 μm for E (Photo credit: Ismail Döker).
Peritreme. Long, extending to level setae j1.
Venter (Fig 5B). Ventral setal pattern 14:JV–3:ZV. Sternal shield smooth except few anterior striations, sclerotized with three pairs of setae (ST1, ST2, ST3), two pairs of poroids (pst1 and pst2). Distance (ST1–ST3) 54 (53–55), width (ST2–ST2) 55 (53–58). Metasternal setae ST4 and a pair of pores (pst3) on metasternal shields. Genital shield smooth; width at level of genital setae (ST5) 53 (50–55). Ventrianal shield smooth, elongated, much longer than wide, bearing three pairs of pre-anal setae (JV1, JV2, and ZV2), a pair of para-anal (Pa) and a post-anal seta (Pst), and with a pair of small rounded solenostomes (gv3) posteromedian to JV2; distance gv3–gv3 25. Length of ventrianal shield 95 (90–100), width at level of ZV2 49 (45–55), width at level of anus 48 (45–53). Setae JV4, JV5, ZV1, ZV3, and four pairs of poroids on integument surrounding ventrianal shield. Two pairs of metapodal plates, primary 23 (21–25), and secondary 11 (10–11) in length. Setae JV5 serrated and arise on tubercules, much longer than other ventral setae, 53 (50–55) in length.
Chelicera (Fig 5C). Fixed digit 23 (23–25) long with nine strong teeth, with pilus dentilis; movable digit 26 (25–28) long with two teeth.
Spermatheca (Fig 5D). Calyx cup or dish-shaped, flaring distally at the base of vesicle, 8 (8–10) in length; atrium slightly nodular; major duct long.
Legs (Fig 5E). Length of legs (base of coxae to base of claws) as follows: leg I 265 (260–270), leg II 208 (200–215), leg III 202 (200–205), leg IV 292 (285–300). Genua II, III, and IV with eight, seven, and seven setae, respectively. A short and sharp-poined macrosetae that is noticeably thicker than other setae on the same segment, StIV 19 (18–20) in length.
Remarks. Proprioseius meridionalis described by Chant [15] came from the material collected from Psychotria bahamensis (Rubiaceae) in Homestead, Florida. In their revision of the tribe, Kampimodromini Kolodochka, Chant & McMurtry [32] divided genus Proprioseius into three species groups based on the relative length of lateral dorsal setae and presence/absence of subcylindrical, erect structure posterior to setae j6. They characterized meridionalis species group with the absence of this erect structure. However, we observed this erect structure in all specimens that we examined in our study. To ensure that the structure identified by Chant & McMurtry [32] was the one we observed in our samples, a specimen was also mounted laterally. As a result, we confirmed the presence of the erect structure. Finally, because all other morphological characters including setae measurements concurred with the original and the re-descriptions, we consider current specimens as P. meridionalis [15, 31]. We believe that this structure might have been overlooked in previous descriptions, probably due to ornamentations on the dorsal shield and poor optic material used at that time. Indeed, the presence of this structure in the type material was confirmed through communication with Dr. Ronald Ochoa based on the photos (Fig 6). Accordingly, the presence/absence of this structure in all other species known in the genus should be confirmed to determine whether it can be used as a valid diagnostic character to separate species groups in the genus.
Tribe Amblyseiini Muma, genus Amblyseius Berlese
4. Amblyseius aerialis (Muma).
Amblyseiopsis aerialis [13]: 264.
Amblyseius aerialis (Muma); [33]: 91; [34]: 71; [35]: 15; [36]: 377; [37]: 238; [38]: 203; [39]: 3; [40]: 3; [41]: 609; [42]: 1136.
Typhlodromus (Amblyseius) aerialis [30]: 88.
Female (n = 5).
Dorsum (Fig 7A). Dorsal setal pattern 10A:9B (r3 and R1 off shield in all specimen except, illustrated specimen where r3 folded on the dorsal shield). Dorsal shield oval with a slight waist at level of Z1, smooth. Bearing seven pairs of rounded solenostomes (gd1, gd2, gd4, gd5, gd6, gd8, and gd9). Length of dorsal shield 419 (400–430), width (distance at level of s4) 271 (263–288), width (distance at level of S2) 321 (305–330). All dorsal setae smooth except Z4 and Z5 which have very little barbs. Measurements of dorsal setae as follows: j1 35 (33–37), j3 53 (49–55), j4 5, j5 5, j6 7 (6–8), J2 8 (8–9), J5 8 (8–9), z2 11 (10–12), z4 9 (8–9), z5 5 (5–6), Z1 9 (8–10), Z4 119 (110–125), Z5 291 (280–297), s4 105 (100–108), S2 10 (9–11), S4 12 (11–13), S5 13 (12–13), r3 13 (12–13), and R1 12 (11–13).
Amblyseius aerialis (Muma)–Female (A–E): A. Dorsal shield, B. Ventral idiosoma, C. Chelicera, D. Spermatheca, E. Leg IV. Scale bars = 100 μm for A, B; 30 μm for C, D; 60 μm for E (Photo credit: Ismail Döker).
Peritreme. Long, extending beyond setae j1.
Venter (Fig 7B). Ventral setal pattern 14:JV–3:ZV. Sternal shield smooth except for a few anterior striations, lightly sclerotized with three pairs of setae (ST1, ST2, ST3), two pairs of poroids (pst1 and pst2). Distance (ST1–ST3) 70 (68–71), width (ST2–ST2) 84 (78–87). Metasternal setae ST4 and a pair of pores (pst3) on metasternal shields. Genital shield smooth; width at level of genital setae (ST5) 89 (83–93). Ventrianal shield smooth, bearing three pairs of pre-anal setae (JV1, JV2, and ZV2), a pair of para-anal (Pa) and a post-anal seta (Pst), and with a pair of crescentic solenostomes (gv3) posteromedian to JV2; distance gv3–gv3 26 (25–27). Length of ventrianal shield 127 (125–130), width at level of ZV2 90 (88–90), width at level of anus 87 (83–89) (widest level). Setae JV4, JV5, ZV1, ZV3, and four pairs of poroids on integument surrounding ventrianal shield. Two pairs of metapodal plates, primary 25 (23–25), and secondary 19 (18–21) in length. Setae JV5 smooth, much longer than other ventral setae 83 (78–89) in length.
Chelicera (Fig 7C). Fixed digit 38 (36–40) long with 14 teeth, with pilus dentilis; movable digit 41 (40–42) long with four teeth.
Spermatheca (Fig 7D). Calyx tubular, 16 (15–17) in length; atrium bulbous larger than calyx and incorporated in the base of calyx, major duct long.
Legs (Fig 7E). Length of legs (base of coxae to base of claws) as follows: leg I 411 (375–425), leg II 337 (330–340), leg III 343 (335–350), leg IV 444 (435–450). Genua II, III, and IV each with seven setae. Macrosetae present in all legs. Measurements of macrosetae as follows: SgeI 47 (45–49), SgeII 43 (41–45), SgeIII 63 (60–68), StiIII 42 (40–44), StIII 34 (32–35), SgeIV 136 (133–138) StiIV 91 (86–94) and StIV 79 (75–81).
Remarks. Amblyseius aerialis description of Muma [13] was based on the material collected from leaves of Citrus sp. in Lucerne Park, Florida. Many morphological characters including setae measurements were not included in that original description. These measurements were provided for the specimens of different populations collected from many South American countries such as Argentina [39], Brazil [40], Colombia [34], Dominican Republic [41], Guadeloupe [36], Guyana [33], and Peru [42], but illustrations are absent in most papers except some partial drawings in De Leon [33] and Muma [13]. In addition, a full set of illustrations is available in Muma & Denmark [26] and Denmark & Muma [35]. However, the bulbous (enlarged) atrium of spermatheca is not clearly illustrated in the available literature [26, 33, 35, 43]. Therefore, we re-described this species based on the specimens collected from its type host Citrus sp. in Fort Pierce, Vero Beach, and Clermont, all close to its type location in Lucerne Park, Florida (170, 133, and 64 km, respectively) to provide evidence for additional diagnosis including a detailed illustration with drawings of the spermatheca and other characters. Some morphological characters and measurements of the specimens that we observed are very close to those provided by others [33, 35, 36, 40], nevertheless, there were several noticeable variations. For example, Muma [13] mentioned a smooth movable digit in the original description. However, our observation on the type materials confirmed four teeth on that cheliceral digit as mentioned in other redescriptions. The shape of the calyx of spermatheca also fits well with that of the holotype specimen (Fig 8).
5. Amblyseius curiosus (Chant & Baker).
Iphiseius curiosus [44]: 11. 5.
Amblyseius curiosus (Chant & Baker); [45]: 202; [26]: 64; [38]: 201.
Amblyseius (Amblyseius) curiosus (Chant & Baker); [35]: 35; [1]: 65.
Female (n = 5).
Dorsum (Fig 9A). Dorsal setal pattern 10A:9B (r3 and R1 off shield). Dorsal shield oval with a slight waist at level of Z1, smooth. Bearing seven pairs of rounded solenostomes (gd1, gd2, gd4, gd5, gd6, gd8 and gd9). Muscle-marks (sigilla) visible mostly on podosoma, length of dorsal shield 361 (320–388), width (distance at level of s4) 236 (220–250), width (distance at level of S2) 258 (250–265). All dorsal setae smooth. Measurements of dorsal setae as follows: j1 27 (26–29), j3 33 (32–34), j4 5 (4–5), j5 5 (4–5), j6 5 (4–5), J2 8 (7–8), J5 8 (7–8), z2 11 (10–13), z4 6 (5–8), z5 6 (5–8), Z1 6 (5–8), Z4 142 (140–145), Z5 304 (265–325), s4 131 (115–145), S2 6 (5–8), S4 6 (5–8), S5 11 (9–14), r3 10 (10–11), and R1 9 (8–10).
Amblyseius curiosus (Chant & Baker)–Female (A–E): A. Dorsal shield, B. Ventral idiosoma, C. Chelicera, D. Spermatheca, E. Leg IV. Scale bars = 100 μm for A, B; 30 μm for C, D; 60 μm for E (Photo credit: Ismail Döker).
Peritreme. Long, extending to level of setae j1.
Venter (Fig 9B). Ventral setal pattern 14:JV–3:ZV. Sternal shield smooth, lightly sclerotized with three pairs of setae (ST1, ST2, ST3), two pairs of poroids (pst1 and pst2). Distance (ST1–ST3) 65 (64–65), width (ST2–ST2) 79 (78–80). Metasternal setae ST4 and a pair of pores (pst3) on metasternal shields. Genital shield smooth; width at level of genital setae (ST5) 79 (70–85). Ventrianal shield reticulated anteriorly, bearing three pairs of pre-anal setae (JV1, JV2, and ZV2), a pair of para-anal (Pa) and a post-anal seta (Pst), and with a pair of crescentic solenostomes (gv3) posterior to JV2; distance gv3–gv3 22 (20–23). Length of ventrianal shield 117 (103–127), width at level of ZV2 94 (88–98), width at level of anus 75 (73–78) (widest level). Setae JV4, JV5, ZV1, ZV3, and five pairs of poroids on integument surrounding ventrianal shield. Setae JV5 smooth, much longer than other ventral setae 78 (65–83) in length.
Chelicera (Fig 9C). Fixed digit 29 (27–30) long with 15 teeth, with pilus dentilis; movable digit 32 (29–33) long with four teeth.
Spermatheca (Fig 9D). Calyx saccular flaring distally, 23 (22–23) in length; atrium incorporated in the base of calyx, a very small fork is visible in some specimens, major duct long and narrow.
Legs (Fig 9E). Length of legs (base of coxae to base of claws) as follows: leg I 393 (380–405), leg II 308 (303–315), leg III 306 (295–315), leg IV 388 (370–405). Genua II, III, and IV each with seven setae. Macrosetae present in all legs. Measurements of macrosetae as follows: SgeI 46 (45–48), SgeII 39 (35–42), SgeIII 65 (58–70), StiIII 43 (38–46), StIII 25 (24–26), SgeIV 151 (130–162) StiIV 96 (80–108) and StIV 71 (58–75).
Remarks. Amblyseius curiosus was described from Costa Rica based on the material collected from an unknown host shrub by Chant & Baker [44]. No measurements were provided in the original and the subsequent re-descriptions [26, 44] even though the original description presents clear drawings [44]. Denmark & Muma [35] provided a re-description based on a single specimen without measurements of some leg macrosetae. Therefore, we provided a complementary description. Morphological characters of the specimens examined in our study are in agreement with those of type materials. We noticed four teeth through examination of the photographs of the type specimens (Fig 10). Three are obvious in the photograph and the fourth next to the junction between the fixed and movable digit.
Tribe Amblyseiini Muma, genus Proprioseiopsis Berlese
6. Proprioseiopsis carolinianus (Muma, Metz & Farrier).
Amblyseius carolinianus [45]: 199.
Proprioseiopsis carolinianus (Muma, Metz & Farrier); [46]: 13; [1]: 197.
Female (n = 14).
Dorsum (Fig 11A). Dorsal setal pattern 10A:8E (r3 and R1 off shield). Dorsal shield oval with a slight waist at level of Z1, smooth. Bearing seven pairs of rounded solenostomes (gd1, gd2, gd4, gd5, gd6, gd8 and gd9). Muscle-marks (sigilla) visible on podosoma, length of dorsal shield 334 (300–360), width (distance at level of s4) 247 (195–268), width (distance at level of S2) 265 (230–280). All dorsal setae smooth. Measurements of dorsal setae as follows: j1 26 (20–30), j3 26 (23–28), j4 6 (5–8), j5 7 (5–8), j6 7 (5–8), J5 7 (5–8), z2 16 (10–18), z4 6 (5–8), z5 6 (5–8), Z1 6 (5–8), Z4 178 (165–187), Z5 254 (220–278), s4 149 (133–163), S2 6 (5–8), S4 6 (5–8), S5 13 (10–15), r3 9 (8–11), and R1 6 (5–8).
Proprioseiopsis carolinianus (Muma, Metz & Farrier)–Female (A–E): A. Dorsal shield, B. Ventral idiosoma, C. Chelicera, D. Spermatheca, E. Leg IV. Scale bars = 100 μm for A, B; 30 μm for C, D; 60 μm for E (Photo credit: Ismail Döker).
Peritreme. Long, extending to level setae j1.
Venter (Fig 11B). Ventral setal pattern 14:JV–3:ZV. Sternal shield smooth, lightly sclerotized with three pairs of setae (ST1, ST2, ST3), two pairs of poroids (pst1 and pst2). Distance (ST1–ST3) 57 (53–59), width (ST2–ST2) 66 (63–69). Metasternal setae ST4 and a pair of pores (pst3) on metasternal shields. Genital shield smooth; width at level of genital setae (ST5) 77 (70–82). Ventrianal shield reticulated, bearing three pairs of pre-anal setae (JV1, JV2, and ZV2), a pair of para-anal (Pa) and a post-anal seta (Pst), and with a pair of small rounded solenostomes (gv3) posterior to JV2; distance gv3–gv3 52 (48–55). Length of ventrianal shield 96 (85–101), width at level of ZV2 95 (83–100), width at level of anus 80 (68–85) (widest level). Setae JV4, JV5, ZV1, ZV3, and four pairs of poroids on integument surrounding ventrianal shield. Two pairs of metapodal plates, primary 22 (19–23), and secondary 8 (7–9) in length, Setae JV5 smooth, much longer than other ventral setae 74 (65–84) in length.
Chelicera (Fig 11C). Fixed digit 28 (23–29) long with 13 teeth, with pilus dentilis; movable digit 29 (28–30) long with two teeth.
Spermatheca (Fig 11D). Calyx cup-shaped, slightly flaring distally, 5 (4–6) in length; atrium has a very small fork, major duct long.
Legs (Fig 11E). Length of legs (base of coxae to base of claws) as follows: leg I 345 (320–358), leg II 265 (245–280), leg III 266 (240–280), leg IV 343 (313–360). Genua II, III, and IV with eight, seven, and seven setae, respectively. Macrosetae present in all legs. Measurements of macrosetae as follows: SgeI 33 (30–36), SgeII 32 (27–35), SgeIII 47 (34–53), StiIII 28 (25–30), StIII 24 (20–26), SgeIV 119 (100–128) StiIV 70 (63–79) and StIV 60 (53–68).
Remarks. Proprioseiopsis carolinianus was described based on two specimens collected from pine and oak litter from North Carolina by Muma et al. [45]. This original description is not well defined and there is no re-description available. Denmark & Evans [1] reported this species from Missouri, and they separated it from their new species, P. paracarolinianus Denmark & Evans based on some setae of single specimens of both species. Their measurements of s4, Z4, Z5, and SgeIV are 126, 151, 210, and 83 in P. carolinianus as opposed to 160, 176, 271, and 125 in P. paracarolinianus, respectively. Here, we provided a re-description based on 14 specimens all collected from the same habitat (leaf litter) and nearby the type location of P. paracarolinianus. A wide range of variation (the maximum values are 15–28% longer than the minimum values) in the aforementioned setae measurements is reported among the specimens examined in this study. When we compared our measurements with those provided by Denmark & Evans [1], our specimens were closer to P. carolinianus based on the minimum values and similar to P. paracarolinianus considering maximum values. Denmark & Evans [1] also mentioned that leg I is longer than leg IV in P. carolinianus while it is shorter than leg IV in P. paracarolinianus. In our specimens, measurements of these legs are subequal in length suggesting that setae measurements and relative length of leg I and leg IV provided by Denmark & Evans [1] may be invalid to separate P. carolinianus and P. paracarolinianus. Moreover, in the original description of P. paracarolinianus, three teeth on the movable digit of chelicerae were reported whereas all specimens that we examined have two teeth on that cheliceral digit. We were unable to confirm the presence of three teeth on the type material provided as chelicera were closed (Fig 12). However, a recent molecular study confirmed movable digit dentition as a diagnostic character in Kampimodromus [47], another genus in the subfamily Amblyseiinae. Based on our investigation and evidence we consider current specimens as P. carolinianus, which may be more common than P. paracarolinianus.
Tribe Euseiini Chant & McMurtry, genus Typhlodromalus Muma
7. Typhlodromalus peregrinus (Muma).
Typhlodromus peregrinus [13]: 270.
Typhlodromus (Amblyseius) peregrinus Muma; [30]: 97.
Amblyseius peregrinus (Muma); [48]: 60; [49]: 255; [34]: 73.
Typhlodromalus peregrinus (Muma); [50]: 221; [46]: 199; [39]: 15; [42]: 25; [51]: 42; [52]: 386.
Female (n = 5).
Dorsum (Fig 13A). Dorsal setal pattern 10A:9B (r3 and R1 off shield). Dorsal shield oval with a waist at level of Z1, rugose ornamentations are visible. Margin of dorsal shield indented at level of setae S5 giving the posterior margin of the shield in a trilobate shape. Bearing seven pairs of rounded solenostomes (gd1, gd2, gd4, gd5, gd6, gd8, and gd9). Muscle-marks (sigilla) visible mostly on podosoma, length of dorsal shield 339 (325–347), width (distance at level of s4) 190 (170–222), width (distance at level of S2) 193 (182–210). Dorsal setae smooth except Z4 and Z5 which are strongly serrated. Dorsal setae somewhat stout. Measurements of dorsal setae as follows: j1 26 (24–28), j3 33 (30–35), j4 11 (10–13), j5 11 (10–12), j6 13 (12–14), J2 14 (13–16), J5 10 (9–11), z2 22 (20–24), z4 24 (21–26), z5 11 (10–12), Z1 16 (15–17), Z4 43 (40–45), Z5 73 (65–80), s4 37 (35–40), S2 28 (25–32), S4 21 (18–24), S5 13 (12–14), r3 19 (17–21), and R1 17 (15–18).
Typhlodromalus peregrinus (Muma)–Female (A–E): A. Dorsal shield, B. Ventral idiosoma, C. Chelicera, D. Spermatheca, E. Leg IV. Scale bars = 100 μm for A, B; 30 μm for C, D; 60 μm for E (Photo credit: Ismail Döker).
Peritreme. Long, extending to level of setae j1.
Venter (Fig 13B). Ventral setal pattern 14:JV–3:ZV. Sternal shield smooth, lightly sclerotized with three pairs of setae (ST1, ST2, ST3), two pairs of poroids (pst1 and pst2), prominent posterior projection is present. Distance (ST1–ST3) 66 (64–69), width (ST2–ST2) 64 (60–68). Metasternal setae ST4 and a pair of pores (pst3) on metasternal shields. Genital shield smooth; markedly wider than ventrianal shield; width at level of genital setae (ST5) 74 (72–80). Ventrianal shield vase-shaped; smooth, with a strong waist at level of JV2; Setae JV2 and ZV2 have migrated forwards to the prenal area; margins at level of anus covered with muscle marks; bearing three pairs of pre-anal setae (JV1, JV2, and ZV2), a pair of para-anal (Pa) and a post-anal seta (Pst), and with a pair of crescentic solenostomes (gv3) posteriomedian to JV2; distance gv3–gv3 27 (24–32). Length of ventrianal shield 111 (101–120), width at level of ZV2 62 (57–65), width at level of anus 67 (59–74) (widest level). Setae JV4, JV5, ZV1, ZV3, and five pairs of poroids on integument surrounding ventrianal shield. Setae JV5 smooth, much longer than other ventral setae 50 (45–56) in length.
Chelicera (Fig 13C). Fixed digit 32 (28–34) long with nine teeth, with pilus dentilis; movable digit 32 (30–34) long with three teeth.
Spermatheca (Fig 13D). Calyx saccular flaring distally, 16 (15–18) in length; atrium nodular attached to the calyx without neck, major duct broad.
Legs (Fig 13E). Length of legs (base of coxae to base of claws) as follows: leg I 321 (315–330), leg II 275 (265–312), leg III 274 (255–300), leg IV 370 (345–390). Genua II, III, and IV each with seven setae. Macrosetae present in all legs. Measurements of macrosetae as follows: SgeI 18 (15–20), SgeII 20 (18–22), SgeIII 26 (24–31), StiIII 18 (16–19), StIII 20, SgeIV 40 (38–42) StiIV 26 (25–28) and StIV 69 (62–82). Setae SgeII, SgeIII, SgeIV, and StIV are knobbed apically.
Remarks. Tyhlodromalus peregrinus was described from Minneola, Florida, based on the material collected from orange leaves by Muma [13]. While setae measurements are absent in the original description, these measurements were provided for specimens of different populations collected from South American countries such as Argentina, Brazil, Colombia, Dominican Republic, Martinique, Guadeloupe, Guatemala, and Peru, as well as for type materials [52]. Typhlodromalus aripo De Leon [53] described from Trinidad and also reported from many South American countries shows a close affinity to T. peregrinus. Moraes & Mesa [34] pointed out that setae z2 is 50% shorter than z4 in T. aripo while it is only 20% shorter than z4 in T. peregrinus. Furthermore, they also reported macrosetae StIV as setaceous and knobbed or blunt in T. peregrinus and T. aripo, respectively [34]. The StIV was also depicted as sharp-pointed in T. peregrinus by Chant & McMurtry [46]. Here, we provided for the first time a complementary description of T. peregrinus based on the materials collected from Clermont, a location very close (10 km) to its type location. As stated by Moraes & Mesa [34], we observed setae z2 is 20% shorter than z4 in most or both setae at subequal length. However, all specimens examined in this study have macrosetae StIV knobbed apically. Kreiter et al. [52] examined type materials of both T. peregrinus and T. aripo and suspected T. aripo as a junior synonym of T. peregrinus. The lengths of setae z2 and z4 are listed among the apomorphic characters for some genus (e.g. Amblyseius, Transeius) in the subfamily Amblyseiinae [38]. Hence, we believe that further molecular studies or crossbreeding experiments are essential to conclude whether these species are conspecific.
Implications for biological control
We re-described seven species of predatory mites from the family Phytoseiidae, which lacked the use of important morphological features or information in the previous descriptions or re-descriptions.
There is a lack of knowledge regarding the food habits and predation efficiency of a large number of phytoseiid species. Little is known about the biology, ecology, behavior, food habits, and predation of the species redescribed here, except for T. peregrinus and A. aerialis. Typhlodromalus peregrinus is a prevalent species in citrus tree canopy and ground cover plants in Florida citrus orchards [54]. According to McMurtry et al. [55], it is a generalist predator with type III feeding habit. It has the ability to feed on a wide range of food sources including mites such as Tetranychus urticae Koch and Panonychus citri (McGregor) (Acari: Tetranychidae) and can be artificially reared using pollen of plant species such as Malephora crocea (Jaquin) (Family: Aizoaceae), Quercus virginiana Miller (Family: Fagaceae), and Typha latifolia (L.) (Family: Typhaceae) [56]. Peña [57] reported that T. peregrinus also feeds on the citrus rust mite, Phyllocoptruta oleivora (Ashmead) (Acari: Eriophyidae) but prefers the broad mite, Polyphagotarsonemus latus (Banks) (Acari: Tarsenomidae) in laboratory and glasshouse trials when both species are offered. Typhlodromalus peregrinus was reported as a dominant phytoseiid species in Alabama citrus orchards, but densities were too low to provide effective control of P. citri [58, 59].
Amblyseius aerialis is also a generalist predator with Type-III feeding habit [60]. It was first collected feeding on six-spotted spider mite, Eotetranychus sexmaculatus, and has since been found in citrus orchards from Guadeloupe, Dominican Republic, Florida, and Brazil [51, 54, 61, 62]. Studies showed that it can feed and reproduce on T. urticae [63, 64]. The oviposition rate of A. aerialis was shown to be high on Raoiella indica Hirst (Acari: Tenuipalpidae) and cattail pollen, Typha dominguensis [62, 64], as well as on African oil palm pollen (Elaeis guineensis), and coconut pollen (Cocos nucifera) (both Arecaceae) [62], and low on Calacarus heveae Feres (Acari: Eriophyidae) and T. urticae [64].
The other five species considered here were mainly collected from ground cover and leaf litter. Amblyseius curiosus and P. carolinianus could be classified as type III-e generalist predators [2], as they were mainly found in leaf litter. Neoseiulus marinellus and N. planatus are also generalist predators living in confined spaces on monocotyledonous plants [2], as most of the specimens were collected from mixed ground cover including grasses from the family Poaceae. There is no information on the feeding habits and other biological parameters (development time, reproduction, or survivorship) of these species. Therefore, research is needed to assess the potential of phytoseiids found in these specific microhabitats as biological control agents. Neoseiulus baraki and N. paspalivorus which are also generalist predators found in monocotyledonous plants have been found in association with the coconut mite, Aceria guerreronis (Eriophyidae) [2]. These species were able to feed and reproduce on their prey in laboratory conditions [65, 66]. Moreover, N. cucumeris a commercially available predatory mite extensively used in the past decade is a species originally found in the soil/litter habitats [2]. Therefore, it is likely that the provision of refugees and augmentative releases of N. marinellus and N. planatus may help to enhance their potential to target Eriophyidae species in citrus groves.
Acknowledgments
We are grateful to Dr. Samuel Bolton (Division of Plant Industry, Florida Department of Agriculture and Consumer Services, FL, USA) for lending us the type specimen of P. carolinianus; Dr. Ronald Ochoa, Dr. Debra Creel and Dr. Gregory Evans (United States Department of Agriculture, Agricultural Research Service, Beltsville, MD, USA) to discuss and provide photos of the type materials from Smithsonian National Museum of Natural History collection.
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