Phytoseiid mites of Mayotte Island (Acari: Mesostigmata)

Mayotte is one of the four main islands constituting Comoros Archipelago, with Anjouan, Mohéli and Grande Comore. Among them, it is the closest island to Madagascar. So far, only one species of the mite family Phytoseiidae (Acari: Mesostigmata) had been reported from this island in an early study. In addition, only five species were recently collected from Grande Comore. In this paper, we report the results of a survey conducted at the end of 2018 in Mayotte Island, in which 18 species are reported for the first time for the Mayotte Island.


Introduction
Mites of the family Phytoseiidae (Acari: Mesostigmata) are well-known for their predatory behaviour on phytophagous mites and small insects on cultivated plants and wild vegetation. Some of them are used to control pest organisms especially in protected crops and to some extent in open fields all around the world (McMurtry and Croft 1997;McMurtry et al. 2013). This family is widespread around the world, presents on all continents (except Antarctica). It presently consists of more than 2,500 valid species belonging to 94 genera and three subfamilies (Demite et al. 2020). Biodiversity surveys in poorly investigated areas is still an urgent needed and might result in the discovery of additional species potentially useful for biological control as well as having more information on the biodiversity of these areas (Kreiter et al. 2018a(Kreiter et al. , b, c, 2020a. The more interesting area are probably those with a high level of biodiversity. Most of the Indian Ocean constitutes one of the world biodiversity hotspots, a concept defined by Myers (1988) in order to identify the most immediately important areas for biodiversity conservation. The common characteristics of these hotspots is that they hold high endemism levels and have lost at least 70% of their original natural vegetation (Myers et al. 2000). Knowledge of the phytoseiid diversity in these high interest areas in the context of global climate changes may contribute to identify potential biological control agent (BCA) and future establishment of conservation programs. Located in the Indian Ocean at 300 km from the northern coast of Madagascar, Mayotte Island (Maore in Shikomori language) is one of the four main islands constituting Comoros Archipelago, with Anjouan (Ndzuwani or Nzwani in Shikomori, and Johanna or Anjouane in Arabic), Mohéli (Mwali in Shikomori) and Grande Comore (Ngazidja in Shikomori). Only one phytoseiid species had been reported from this island long time ago, namely Phytoseius mayottae Schicha (Schicha 1984). The objective of this paper is to report the phytoseiid species found in a new survey conducted in November 2018 in Mayotte Island.

Material and methods
The survey took place in Mayotte in the second half of November 2018. Plant inhabiting mites were collected from cultivated and uncultivated plants in few locations in the centre of the island. Mites were directly collected on leaves with a fine brush with or without a pocket lens or a stereo-microscope when available (large leaf and herbaceous plants) or by beating the plants (mainly shrubs and trees with very small or spiny leaves) and collecting the mites in a black plastic rectangular saucer 45 x 30 cm (Ref. STR 45, BHR, 71370 Saint-Germain-du-Plain, France). The mites were then transferred with a fine brush into small plastic vials containing 1.5 ml of 70% ethanol. All mites were mounted on slides using Hoyer's medium and they were identified using a phase and interferential contrast microscope (DMLB, Leica Microsystèmes SAS, Nanterre, France). Morphological characters of specimens were measured using a graded eyepiece (Leica, see above). Chant andMcMurtry's (1994, 2007) concepts of the taxonomy of the family Phytoseiidae for identification and the world catalogue database of Demite et al. (2014Demite et al. ( , 2020 for distribution and information on descriptions and re-descriptions were used. The setal nomenclature system adopted was that of Lindquist & Evans (1965) and Lindquist (1994) as adapted by Rowell et al. (1978), and Chant & Yoshida-Shaul (1992) for the dorsum and by Chant & Yoshida-Shaul (1991) for the venter. The notation for solenostomes and poroids is based on Athias-Henriot (1975). Numbers of teeth on the fixed and movable cheliceral digits do not include the respective apical teeth on apical hook. Setae not referred to in the results section should be considered as absent. All measurements are given in micrometres (µm) and presented with the mean in bold followed by the range in parenthesis.
Specimens of each species are deposited in the mite collections of Montpellier SupAgro conserved in UMR CBGP INRAE/IRD/CIRAD/SupAgro/University of Montpellier. Specimens collected in fields in Mayotte within these surveys were all identified. Only few single males or immatures collected during this study are not taken into account. The following abbreviations are used in this paper for morphological characters: dsl = dorsal shield length just above j1 to just below J5; dsw = dorsal shield width at the level of s4; Z4 ser., Z5 ser. = Z4, Z5 serrated (if Z4 and Z5 without ser. = not serrated); gensl = genital shield length; gensw post. cor. = genital shield width posteriorly; lisl = Largest inguinal sigilla (= "metapodal plate") length; lisw = Largest inguinal sigilla (= "metapodal plate") width; sisl = smallest inguinal sigilla (= "metapodal plate") length; sisw = smallest inguinal sigilla (= "metapodal plate") width; vsl = ventrianal shield length; gv3 -gv3 = distance between solenostomes gv3 on the ventrianal shield; vsw ZV2 & vsw anus = ventrianal shield width at ZV2 level and at paranal setae level; scl: calyx length; scw = calyx widest width; Fdl = fixed digit length; 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; toe = length of the toe; BCA = Biological control agent; aasl = altitude above sea level. The following abbreviations are used in this paper for institutions: CBGP = Centre de Biologie pour la Gestion des Populations;
This species belongs to the barkeri species group of the genus Neoseiulus and to the barkeri species subgroup (Chant and McMurtry 2003a). Neoseiulus barkeri has a worldwide distribution (Moraes et al. 2004;Demite et al. 2020). Various studies have shown its ability to control Frankliniella occidentalis Pergande (Rodriguez-Reina et al. 1992), Thrips tabaci (Lindeman) (Broodsgaard and Stengaard Hansen 1992) and Tetranychus urticae Koch on cucumbers (Fan and Petitt 1994b). Fan and Petitt (1994a) showed that augmentative releases of N. barkeri provided also control of the broad mite, Polyphagotarsonemus latus (Banks), on peppers. Neoseiulus barkeri constitutes a potential BCA for several crops, especially in vegetables greenhouses. This species has been mentioned by Quilici et al. (2000) and Kreiter et al. (2020c) in La Réunion Island and more recently from Rodrigues by Kreiter and Abo-Shnaf (2020a).
World distribution: it has a worldwide distribution in all continents, in more than 50 countries (Demite et al. 2020).
Remarks: morphological and morphometric characters and all measurements fit well with those provided by Kreiter et al. (2020b, c). This species described from Africa (Pritchard and Baker 1962) was first mentioned in the Indian Ocean from La Réunion Island (Kreiter et al. 2020c), but seems to be present in several other investigated islands (Kreiter and Abo-Shnaf 2020a, b).
Paraphytoseius orientalis (Narayanan, Kaur & Ghai) Matthysse & Denmark 1981in Denmark et al. 1999. Paraphytoseius narayanani Ehara 1967: 67 (synonymy according to Chant & McMurtry 2003b). Table 2 Character measurements of an adult male of Neoseiulus teke collected in this study with those in previous studies (localities followed by the number of specimens measured between brackets).

South Africa
(2) Characters La Réunion (2) This species belongs to the orientalis species group (Chant and McMurtry 2003b), but according to these authors and Moraes et al. (2007), specimens with shorter setae s4, Z4 and Z5, and having a distinctly short, thick, spatulate macroseta on genu I belong to the species P. orientalis. This species is widely distributed in tropical and subtropical areas in South America, Africa and Asia. It belongs to a genus included in the large polyphagous generalist group named type III phytoseiid mites (McMurtry and Croft 1997;McMurtry et al. 2013). Navasero and Navasero (2016) studied the life history of P. orientalis on the broad mite (P. latus) as prey and reported high predation rates when eggs of P. latus were offered as food, suggesting good potential for the control of this pest. This species was also collected in Mauritius (Kreiter et al. 2018a; Ferragut and Baumann 2019; Kreiter and Abo-Shnaf 2020b), La Réunion (Kreiter et al. 2020c) and Vietnam   Kreiter et al. (2018a and by Ferragut and Baumann (2019) from various places. Morphological and morphometric characters and all measurements fit well with those given by Ferragut and Baumann (2019) and Kreiter et al. (2020b, c). It is described from Asia (Narayanan et al. 1960) and present in Vietnam . Paraphytoseius orientalis seems to be more common than P. horrifer in Mauritius Island (Kreiter and Abo-Shnaf 2020b), whereas the latter is more abundant in Mayotte Island.  Moraes et al. 1986Moraes et al. : 147, 2004Chant & McMurtry 2005c: 327, 2007 Typhlodromips ivoloinae (Blommers 1974): 146 (synonymy according to Ueckermann & Loots 1988).

Tribe Typhlodromipsini Chant & McMurtry
This species belongs to the culmulus species group of the genus Typhlodromips with nine other species. It was described under the name ivoloinae by Blommers (1974) from Madagascar on Citrus lemon (L.) Burman (Rutaceae). Mayotte Island is approximately 340 km away from Madagascar coasts and it is not surprising to find this species on a close island. The species was not reported from Mascareignes Archipelago. Its biology is totally unknown.
Remarks: morphological and morphometric characters and all measurements fit well with those provided in the literature as indicated in (Table 3). This species recorded in several countries of Africa and is also present in Madagascar. Mayotte is consequently the second island of Indian Ocean known for hosting this species.  Gupta 1986).

Tribe Amblyseiini Muma
Amblyseius largoensis belongs to the largoensis species group and the largoensis species subgroup. It is widespread in all tropical and subtropical regions of the world and was the Table 3 Character measurements of adult females of Typhlodromips shi collected in this study with those in previous studies (localities followed by the number of specimens measured between brackets).

Mayotte (1)
Mayotte ( Moraes et al. (2000) in French Caribbean Islands and as a potential BCA of Raoiella indica Hirst in La Réunion Island (Moraes et al. 2012). Using morphometric analyses of 36 characters, molecular analyses and crossing tests, Navia et al. (2014) studied specimens collected in Brazil, La Réunion Island and Trinidad and Tobago to determine whether A. largoensis populations from different geographic origins belong to the same taxonomic entity. Though differences in the lengths of some setae were observed, molecular analyses and crossing experiments indicated that populations from Indian Ocean and America were conspecific. This species was previously recorded from Mauritius Island by Ferragut and Baumann (2019) and Kreiter and Abo-Shnaf (2020b), and Rodrigues Island by Kreiter and Abo-Shnaf (2020a).  (2019) for specimens from Mauritius. This is the third more common species of our samplings.

Amblyseius parasundi Blommers
Amblyseius (Proprioseiopsis) parasundi Blommers 1974: 144. Amblyseius parasundi, Moraes et al. 1986Moraes et al. : 27, 2004. Amblyseius (Amblyseius) parasundi, Denmark & Muma 1989: 19. This species have no setae Z1 and consequently belongs to the sundi species group and having the spermatheca elongate, tub-like, belongs to the sundi species subgroup. Despite its high population on fruit trees in Madagascar and preying on tetranychid mites (Blommers and Gutierrez 1975), its biology is totally unknown.  (Table 4) fit quite well with few measurements from the other studies (Table 4) except some setae which are 10-20% longer (Z5, JV5, SgeIV, StiIV and StIV ) or 10-40% shorter (j3, r3) in Mayotte specimens. This is the second more common species of our samplings. Amblyseius sundi is reported by Blommers (1974) as being a thelytokous species in mass-rearing and field collected specimens and similar information is also mentioned by Denmark and Muma (1989). Four males were however collected during our study.

Amblyseius tamatavensis Blommers
Amblyseius tamatavensis Blommers 1974: 144;Moraes et al. 1986Moraes et al. : 31, 2004Denmark & Muma 1989: 13;Chant & McMurtry 2004: 203, 2007 Amblyseius tamatavensis belongs to the obtusus species group and the aerialis species subgroup which contains 46 species (Chant and McMurtry 2004). It seems to fit the functional type III-b (generalist predators living on glabrous leaves) group defined by McMurtry et al.  Table 4 Character measurements of adult females of Amblyseius parasundi collected in this study with those in previous studies (localities followed by the number of specimens measured between brackets).
with astigmatine mites, which could allow the mass production for augmentative biological control. This species is reported in tropical areas from over 20 countries around the world (Africa, Asia, America and Oceania). It was recorded from La Réunion Island (Quilici et al. 2000;Kreiter et al. 2020c), from Rodrigues Island (Kreiter and Abo-Shnaf 2020a) and from Mauritius Island (Ferragut and Baumann 2019;Kreiter and Abo-Shnaf 2020b). World distribution: this species was described from Madagascar, but is actually widely distributed in the tropical and subtropical regions of Africa, America, Asia and the Pacific Islands.

Proprioseiopsis antonelli Congdon 2002: 15 (synonymy according to Denmark & Evans 2011).
Proprioseiopsis ovatus belongs to the belizensis species group as genu I have no macrosetae. As the spermatheca of that species is saccular, it belongs to the belizensis species subgroup (Chant and McMurtry 2005a). This species is known from Guadeloupe, Marie-Galante and Martinique (Kreiter and Moraes 1997;Moraes et al. 2000;Mailloux et al. 2010;Kreiter et al. 2018c). It was found in very large number only during a previous study on companion plant in Guadeloupe (Mailloux et al. 2010) and in a recent study in La Réunion (Le Bellec, unpub. data). In other habitats, it seems to be rare. Similar to P. mexicanus (Garman), P. ovatus seems to be abundant on weeds in the lower vegetation. Denmark and Evans (2011) indicated that this species is associated with Oligonychus pratensis (Banks) and Brevipalpus spp. It was also found in association with Tetranychus evansi Baker and Pritchard (Furtado et al. 2014), but mentioned as poor predator of that species. Despite this information, the biology of P. ovatus remains unknown. Remarks: morphological and morphometric characters and all measurements of our single specimen in perfect shape fit well measurements of Kreiter et al. (2020c) and other measurements of the literature mentioned by these authors for specimens from La Réunion and other parts of the world.  Moraes et al. 1986: 46, 2001: 46, 2004: 78. Moraeseius papayana, Chant & McMurtry 2005b: 216, 2007 Moraeseius papayana was first placed in the genus Amblyseius, then assigned to the genus Euseius before being erected as a new genus, Moraeseius by Chant and McMurtry (2005b). It was described from Nelspruit, Transvaal, South Africa on Carica papaya L. This is the first record of this species outside the African continent. The biology of this species is totally unknown.
Euseius ovaloides was described by Blommers (1974) from specimens collected on Citrus hystrix de Candolle (Rutaceae) and Persea americana Miller (Lauraceae) 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 had been occasionally recorded from Madagascar (Blommers 1974), Papua-New Guinea (Schicha and Gutierrez 1985), Seychelles (Schicha 1987), La Réunion Island, (Quilici et al. 1997, Kreiter et al. 2020c, 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 potential predator of thrips and whiteflies. This is one of the most common species on La Réunion Island (Kreiter et al. 2020c).
Specimens examined: 4 ♀♀ specimens in total. L'Abattoir, City Center (15 m aasl, 12°47 ′ 18 ″ S, 45°16 ′ 21 ″ E), 4 ♀♀ Carica papaya L. (Caricaceae), 27/XI/2018. Remarks: this species was recently reported from Vietnam ). Morphological and morphometric characters and all measurements of our specimens fit well with measurements in . This species was the second more collected species in our study concerning Mauritius (Kreiter & abo-Shnaf 2020b) Phytoseiidae after A. herbicolus and it was also very common in La Réunion (Kreiter et al. 2020c), but less common in Mayotte Island. Table 5 Character measurements of adult females of Moraeseius papayana collected in this study with those in previous studies (localities followed by the number of specimens measured between brackets).

Phytoseius haroldi Ueckermann & Kreiter
Phytoseius haroldi Ueckermann & Kreiter in Kreiter et al. 2002: 339;Chant & McMurtry 2007: 129. This species belongs to the horridus species group as setae J2 and R1 are absent (Chant and McMurtry 1994). This species was described by Ueckermann and Kreiter in Kreiter et al. (2002) from La Réunion Island. It was abundant in low vegetation in a study of companion plants in citrus orchard in La Réunion Island (Kreiter et al. 2020c). It seems that this species prefers low plants, but this observation has to be confirmed in further studies. The biology of this species remains also totally unknown. This species was recently reported in Mauritius (Ferragut and Baumann 2019;Kreiter and Abo-Shnaf 2020b) and in Rodrigues Island (Kreiter and Abo-Shnaf 2020a).

Subfamily Typhlodrominae Wainstein
This species belongs to the contiguus species group (Chant & McMurtry 1994) and its biology remains totally unknown.
World distribution: China, Hong-Kong, Japan, Madagascar, Philippines, Singapore. Specimens examined: 59 specimens in total, 51 ♀♀, 7 ♂♂ and 1 im. Coconi, Maison de L'Office National des Forêts (156 m aasl, 12°50 ′ 1 ″ S, 45°8 ′ 5 ″ E), 2 ♀♀ on Cinnamomum verum J. Presl (Lauraceae), 2 ♀♀ on Barleria lupulina Lindley (Acanthaceae), 2 ♀♀ on Stachytarpheta jamaicensis (L.) Vahl (Verbenaceae), 1 ♀ and 1 ♂ on Terminalia catappa L. Remarks: morphological and morphometric characters and all measurements of our specimens fit well with measurements in numerous description and redescriptions available in the literature, especially those of Blommers (1976) for specimens from Madagascar. This is the most abundant species in our samplings. Mentioned only from South-East Asia and Madagascar, this is the first report of this species outside this main island.  Ueckermann et al. 2008: 48. This species belongs to the singularis species group as setae JV3 are absent on the female and as specimens have shorter dorsal shield setae (Chant and McMurtry 1994). The biology of that species is totally unknown. It was reported only from Kenya (Ueckermann et al. 2008) based on a single female specimen. Remarks: the species was mentioned only once from Kenya and described based on a single female specimen. Morphological and morphometric characters and all measurements of our specimens (Table 6) fit well those of the original description by Ueckermann et al. (2008).

Typhlodromus (Anthoseius) lobatus Zannou, Moraes & Oliveira
Typhlodromus (Anthoseius) lobatus Zannou, Moraes & Oliveira in Ueckermann et al. 2008: 59. This species belongs to the rhenanus species group (Chant and McMurtry 1994). The biology of that species is totally unknown. It was recently recorded from Rodrigues Island (Kreiter and Abo-Shnaf 2020a) and from Mauritius (Kreiter and Abo-Shnaf 2020b). Remarks: morphological and morphometric characters and all measurements of our specimens fit well with measurements of the original description by Ueckermann et al. (2008) concerning specimens from Ghana, in Western Africa and measurements of specimens from Rodrigues and Mauritius, respectively (Kreiter and Abo-Shnaf 2020a, b). Table 6 Character measurements of adult females of Typhlodromus (Anthoseius) grewiae collected in this study (localities followed by the number of specimens measured between brackets).
Remarks: morphological and morphometric characters and all measurements of our specimens fit well those of specimens from South Africa in van der Merwe (1968) and Ueckermann et al. (2008).
The fauna of Mayotte after our study is composed of 19 species: 13 Amblyseiinae, 2 Phytoseiinae and 4 Typhlodrominae. Unfortunately, we have not recovered the unique species known before our study, Phytoseius mayottae Schicha. Among the 18 newly recorded species, at least four species (N. barkeri, A. largoensis, A. tamatavensis, and E. ovaloides) are known as biological control agents (BCAs). In addition to the intrinsic value of phytoseiid mite biodiversity in tropical environments, demonstration of the natural occurrence of efficient BCAs in a developing country such as Mauritius is of great agricultural, commercial and strategic interests for the country.