Phytoseiidae of Vietnam (Acari: Mesostigmata) with description of a new species

Vietnam is a large country of Southeast Asia and a globally recognized hotspot of biodiversity. Until recently, only limited surveys had been carried out on the resident Phytoseiidae fauna and presence of 12 species had been documented, with 11 belonging to the sub-family Amblyseiinae and 1 to the sub-family Typhlodrominae. Here, we present results from 2017 field surveys and add a total of 8 new country records, one of which a newly-described species. At least 5 species (i.e., Neoseiulus longispinosus, Paraphytoseius cracentis, P. orientalis, Amblyseius cinctus and A. herbicolus) are well-known biological control agents (BCA), while two species (Euseius ovaloides and Gynaeseius liturivorus) carries ample potential as BCA agents but necessitates further study. In addition to the intrinsic value of phytoseiid mite biodiversity in tropical environments, demonstration of the natural occurrence of efficient BCAs in Southeast Asian countries such as Vietnam is of great agricultural and commercial interest.


Introduction
The Phytoseiidae family is widespread all over the world and consists of about 2,500 valid species dispatched in three sub-families and 94 genera (Demite et al. 2014(Demite et al. , 2020. Several species in the family are important natural enemies of phytophagous mites, insect eggs and small (or immature) insects in natural habitats, arable field crops and protected crops globally (McMurtry and Croft 1997;McMurtry et al. 2013). Despite the extensive faunistic surveys carried out for more than 70 years worldwide, the fauna of certain countries and ecosystems remains little explored (Tixier and Kreiter, 2009;Kreiter et al. 2020a). Consequently, it is important to conduct surveys in these poorly-investigated areas and gain more information on resident biodiversity, especially in hotspots of biodiversity. Furthermore, in-country surveys of Phytoseiidae can signal local presence of known biological control agents (BCA) and introduce new potential BCAs, especially in the context of international and country regulations including the Nagoya Protocol on Access and Benefit Sharing (Mason et al. 2018).
Most areas of Southeast Asia constitute globally-important hotspots of biodiversity (Myers, 1988). These geographical entities are of immediate importance to biodiversity conservation, regularly hold high endemism and have been subject to considerable loss of natural habitats ZV2 level and at paranal setae level; Dist. solen. vas = distance between solenostomes on the ventrianal shield; scl = total spermatheca length (calyx + neck or cervix + atrium); scw = calyx width; FD = fixed digit; Fdl = fixed digit length; MD = movable digit; Mdl = movable digit length; No teeth Fd = number of teeth on the fixed digit; No teeth Md = number of teeth on the movable digit; Shaft = length of the shaft of spermatodactyl; BCA = Biological control agents; FCI = French Caribbean Islands; VCW: various countries in the world; im. = immature. The following abbreviations are used in this paper for institution: CBGP = Centre de Biologie pour la Gestion des Populations; CIRAD = Centre International de Recherche Agronomique pour le Développement; INRA = Institut National de la Recherche Agronomique; IRD = Institut de Recherche pour le Développement; MSA = Montpellier SupAgro, France; UMR = Unité Mixte de Recherche.

Results and Discussion
A total of 14 species were found: 11 belonging to Amblyseiinae and to genera Amblyseius, Euseius, Graminaseius, Gynaeseius, Neoseiulus, Paraphytoseius and Scapulaseius; Three species are belonging to Phytoseiinae and to genus Phytoseius. No species of the sub-family Typhlodrominae has been found.

Characters
This species was already known from Vietnam and reported as a local BCA in earlier survey work (Nguyen et al. 2016) though no measurements were given. Measurements of female specimens collected during this study are given in table 1 and compared with measurements obtained from specimens collected in other countries of Asia and Islands of the Indian Ocean. Measurements match with most of the previous measurements, especially with those obtained on specimens from La Réunion Island. The setal lengths of the present females are longer than those obtained from the holotype, which are in the lower part of the range of data obtained for each seta (probably measurements were obtained from a very small size female). Remarks: the predatory mite P. cracentis is a natural enemy of thrips found on vegetables such as green bean, cucumber, green squash, eggplant, and pepper in the Red River Delta in Vietnam. Paraphytoseius cracentis is feeding on Frankliniella occidentalis Pergande (Thysanoptera: Thripidae) and Carpoglyphus lactis (L.) (Acari: Acaridae) (Nguyen and De Clercq 2018, paper in which this species was mentioned for the first time for Vietnam. The intrinsic rate of natural increase of P. cracentis fed on C. lactis (0.215 female/ female/ day) was however significantly higher than that of mites fed on thrips (0.189). Nguyen and De Clercq (2018) conclude that P. cracentis can sustain and increase its population when fed on Table 2 Character measurements of adult females and males of Paraphytoseius cracentis collected in this study and those reported in previous studies (localities followed by the number of specimens measured). 6 (5 -7) 6 (6 -7) 6 6 minute 7 (5 -9) 7 (5 -8) 2 -4 -6 6 (6 -7) J5 5 4 (4 -5) 5 2 minute 5 (4 -6) 4 (3 -5) 2 -4 -4 3 r3 45 ( 10 (9 -11) 10 (9 -10) 10 8 -12 minute 10 (8 -13) 10 (8 -11) 8 -9 10 (10 -11) z4 9 (8 -10) 9 10 8 -12 minute 9 (8 -12) 9 (8 -10) 8 -8 10 (9 -11) z5 5 5 4 4 minute 5 (4 -5) 3 (3 -4) 2 -4 -5 5 Z1 8 (6 -8) 7 9 7 -8 minute 7 (6 -9) 7 (5 -8) 8 -6 6 (6 -7) Z4 75 ( F. occidentalis, and that C. lactis can be used for mass-rearing of this predatory mite in the perspective to use it in biological control. This species was already known from Vietnam and reported locally as a BCA from earlier survey work (Nguyen and De Clercq 2018) though no measurements were provided. Measurements are given here in table 2 for females and males and compared with those obtained from specimens collected in other countries of Asia.
All measurements collected during this study match well with most of the previous measurements, especially with measurements of specimens from Thailand.
Paraphytoseius horrifer (Pritchard & Baker) Amblyseius (Ptenoseius) horrifer Pritchard & Baker, 1962: 295 This is the first record of this species from Vietnam and from Asia. Measurements are given in the table 3 for females and males and compared with those obtained from specimens collected in other countries of Africa and Indian Ocean. Measurements obtained during this study agree well with most of the previous measurements obtained, especially with measurements of specimens from La Réunion Island.
Amblyseius herbicolus (Chant)   Remarks: Amblyseius herbicolus is widespread in all tropical and subtropical regions of the world. It is the second most abundant phytoseiid mite on Coffea arabica in Brazil, and is deemed to be an efficient predator of Brevipalpus phoenicis (Geijskes), vector of the coffee ring spot virus (Reis et al. 2007). Amblyseius herbicolus is also found in association with the broad mite, Polyphagotarsonemus latus Banks in crops such as chili pepper (Capsicum annuum) in Brazil and has good potential for controlling the latter. Rodriguez-Cruz et al. (2013) have demonstrated that A. herbicolus was able to develop on broad mites, castor bean pollen (Ricinus communis) and sunn hemp pollen (Crotalaria juncea). Provision of pollen can enhance populations of this predator and increase biological control (Duarte et al. 2015), Table 7 Character measurements of adult females of Amblyseius cinctus collected in this study and those reported in previous studies (localities followed by the number of specimens measured).   Amblyseius herbicolus was collected recently in Comoros archipelago (Kreiter et al. 2018b). This is the first record of that species in Vietnam. Measurements of the single specimen collected during this study are provided in table 8 and compared with measurements obtained from specimens collected in other countries of Africa, Asia and Indian Ocean. These measurements match with those obtained previously. The dorsal shield width is less important in the single Vietnam specimen than all order widths of the table, probably because the single female was a small one, all other dimensions being quite similar.
The biology of G. polisensis remains totally unknown and even the life type of this species and of species of Graminaseius are unknown. Table 9 Character measurements of one adult female and one adult male of Graminaseius polisensis collected in this study and those reported in previous studies (localities followed by the number of specimens measured). This species was already known from Vietnam from a previous survey (Nguyen et al. 2016). Details of locations were provided in this paper though no measurements were provided on the collected specimens. Measurements of specimens collected in this study are provided in table 9 for the single female and the single male and compared with measurements obtained from specimens collected in the Philippines, i.e., country of the original description. Measurements obtained for Vietnamese specimens (both damaged) collected during this study agree well with most obtained from female and male type material from Philippines, most of the setae being shorter in Vietnamese specimens.
Remarks -This species was found on Manihot esculenta in Vietnam. It is a type-III predator and is considered of interest for thrips control on grape infested with Scirtothrips dorsalis Hood (Shibao et al. 2004) and on various plants with Frankliniella occidentalis (Pergande) and Thrips palmi Karny (Mochizuki 2009). Gynaeseius liturivorus fed on the larvae of these thrips species. Females consumed an average of 7.4 -19.4 first-stadium larvae of these 74 (
thrips within the first 24 hrs and laid an average number of 1.6 -6.8 eggs within 24-48 hrs. These data suggest that G. liturivorus would be a promising BCA against thrips (Mochizuki 2009). All measurements obtained on female specimens collected during this study (Table 10) agree well with measurements obtained from female specimens collected in other countries, especially with type specimens from Japan and Thailand. Specimens of Taiwan have shorter setae while specimens of Indonesia and Papua New Guinea have longer setae.
It is interesting to notice that in deutonymph specimens some setae are longer than those of female specimens, especially j1, j3, Z5, SgeII, SgeIV, StIV, shorter peritremes and chelicerae and a lower number of teeth than female specimens on both digits of chelicerae.

Characters Characters
Sources of measurements -Guadeloupe: Moraes et al. (2000); Remarks: All measurements obtained on the single female specimen collected during this study agree well with measurements obtained from female specimens collected in other countries.
Euseius ovaloides was described by Blommers (1974) from specimens collected on Citrus hystrix and Persea americana in Madagascar. Like all Euseius species, this species belongs to the type IV (polliniphagous generalist predators) of McMurtry and Croft (1997) and McMurtry et al. (2013). The species has been occasionally recorded from Madagascar (Blommers, 1974), Papua-New Guinea (Schicha and Gutierrez 1985), Seychelles (Schicha, 1987), Reunion Island, (Quilici et al., 1997(Quilici et al., , 2000, Guadeloupe, Martinique and Marie-Galante (Moraes et al., 2000;Kreiter et al., 2006) on various plants, though its biology remains unknown. It is suspected to be a poor predator of tetranychid mites (Gutierrez and Etienne, 1986) but can be considered as a potentially good predator of thrips and of whiteflies. This is one of the more common species on La Réunion Island. This is the first mention of that species in Vietnam. Measurements of the single female specimen collected during this study are provided in table 11 and compared with measurements obtained from specimens collected in other countries of Indian Ocean and the Caribbean. Phytoseiini Berlese 1913: 3;Phytoseiinae, Vitzthum 1941: 768. Genus Phytoseius Ribaga Phytoseius Ribaga, 1904: 177.

Phytoseius coheni Swirski & Shechter
Phytoseius (Dubininellus) macropilis coheni Swirski & Shechter 1961: 104. Phytoseius (Phytoseius) macropilis coheni, Ehara 1966: 26. Phytoseius (Dubininellus) coheni, Swirski & Golan 1967: 226;Wu 1997: 153. Phytoseius (Phytoseius) coheni, Moraes et al. 1986: 219. Phytoseius coheni, Moraes et al. 2004a: 235;Chant & McMurtry 2007: 129. Phytoseius hawaiiensis Prasad 1968: 1460(synonymy according to Denmark & Evans 2011. Phytoseius huangi Ehara 1970: 62 (synonymy according to Ehara 2002. Phytoseius jianfengensis Chen, Chu & Zhou 1980: 15 (synonymy according to Wu 1997. Although species of the genus Phytoseius are considered to belong to the type III (polyphagous generalist predators) of McMurtry and Croft (1997) and McMurtry et al. (2013), its specific biology is totally unknown. This is the first mention of that species in Vietnam. Measurements of specimens collected during this study are provided in table 12 and compared with measurements obtained from specimens collected in other countries of Asia and Indian Ocean. Measurements obtained during this study agree well with most obtained from female specimens collected in other countries.  (1997) and McMurtry et al. (2013), its specific biology is totally unknown. This is the first mention of that species in Vietnam. Measurements of specimens collected during this study are provided in table 13 for females and males and compared with measurements obtained from specimens collected in other countries of Asia and Africa.
Measurements obtained agree well with most of those obtained previously, with slightly shorter dimensions, especially in male specimens.
Spermatheca - (Fig. 5a) Spermatheca with calyx pocular (Denmark and Evans 2011), 10 long and 5 wide, and a small atrium. Ductus minor not visible but large ductus major well visible in all specimens.
Legs - (Fig. 5b) Four macrosetae on leg IV, all spatulate: SgeIV 10, StiIV 39 (38 -  the knowledge of mites and especially to the taxonomy of Phytoseiidae and her great assistance with this paper. Remarks -Measurements of specimens collected during this study are provided in table 14 for females and for the single male and compared with measurements obtained from specimens of the closest described species. Females of Phytoseius tixierae Kreiter n. sp. (Table 14) resembles that of P. huaxiensis Xin, Liang and Ke but differs in having s6 only slightly serrated, shorter s4, s6, Z4, Z5 and JV5. It also resembles P. indicus Bhattacharyya but differs in having s6 only slightly serrated, shorter s4, s6, Z4, JV5, Z4 not serrated but z4 serrated and longer. It is also related to P. kazusanus Ehara but differs in having s6 only slightly serrated, z4 serrated, longer Z5, JV5 and StIV and Z4 not serrated. It is also very close to P. longchuanensis Wu but differs from this species by having longer setae except s4 and Z4, s6 only slightly serrated, z4 serrated, longer JV5 and 4 macrosetae on the leg IV instead of zero. It is also very similar to P. rimandoi Corpuz but differs from this species in having shorter s6, Z4 smooth. Finally, the closest species is P. nudus Wu and Li but the new species differs from this species in having z4 strongly serrated (only slightly serrated in the former), and the dorsal shield rugose (smooth in the former).
Males of Phytoseius tixierae Kreiter n. sp. (Table 14) also resembles to the males of P. huaxiensis and P. kazusanus that are the only species for which males have been described. But males of the new species differ from males of the former species in having s6 only slightly Table 14 Character measurements of adult females and one adult male of Phytoseius tixierae Kreiter n. sp. collected in this study and close species reported in previous studies (localities followed by the number of specimens measured).

Conclusion
The fauna of Phytoseiidae of Vietnam is now composed of 20 species, 12 already known from previous studies and 8 added in this paper. As this number of species is still far below the anticipated real number of phytoseiid species present in this tropical biodiversity hotspot, follow-up survey work is urgently needed.