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Phytoseiid mites (Acari: Mesostigmata) of Mohéli Island (Comoros Archipelago)

Mohéli is one of the four main islands constituting Comoros Archipelago, with Mayotte, Anjouan and Grande Comore Islands. It is the third Island closer from Madagascar after Mayotte and Anjouan. So far, no species of the mite family Phytoseiidae had been reported from this island. We report in this paper the results of a survey conducted at the end of 2018 in Mohéli Island, in which 18 species have been recorded.


Introduction
Mites of the family Phytoseiidae are all predatory species on phytophagous mites and small insects like thrips and whiteflies, on commercial plants and the wild vegetation. Several species are biological control agents for the control of pest organisms in both open and protected crops all around the world Croft 1997; McMurtry et al. 2013).
This family is widespread around the world, presents on all continents except Antarctica, and consists of 2,521 valid species in 94 genera belonging to three subfamilies (Demite et al. 2020).
Biodiversity surveys in poorly investigated areas is still urgently 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, b, c, 2020a, b, c, d; Kreiter and AboShnaf 2020a, b, Kreiter et al. 2021. In these perspectives, the more interesting area are probably those with a high level of biodiversity. Most of the Indian Ocean constitutes one of the highest world biodiversity area, those area being called hotspots, 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 agents (BCA) and future establishment of conservation programs.
Located in the Indian Ocean at around 1,000 km from the northern coast of Madagascar, 165 km from Mayotte and about only 70 km from Anjouan and Grande Comore Islands, Mohéli (Mwali in Shicomori language) Island is one of the four main islands constituting Comoros Archipelago, with Mayotte, Anjouan and Grande Comore. No phytoseiid species are known from this island.
The objective of this paper is to present the phytoseiid species reported in a survey conducted in early December 2018 in Mohéli Island.

Material and methods
The survey took place in Mohéli in the very beginning of December 2018. Plant inhabiting mites were collected from cultivated and wild plants in few locations mainly in the southern part of the island.
Mites were directly collected on leaves with a fine brush with or without a pocket lens or a stereoscopic microscope when available (large leaves 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 SaintGermaindu Plain, France). Collected mites were then transferred with a fine brush into small plastic vials containing 1.5 ml of 70% ethanol.
The mites were then all slidemounted in Hoyer's medium (Walter and Krantz 2009), the slides were dried at 4550 o C for at least two weeks and then all examined and identified using a phase and interferential contrast microscope (DMLB, Leica Microsystèmes SAS, Nanterre, France). 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 redescriptions 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 & YoshidaShaul (1989) for the dorsal surface and by Chant & YoshidaShaul (1991) for the ventral surface. Pore (= solenostome) and poroid (= lyrifissure) notations are that of AthiasHenriot (1975). Macrosetal notation (Sge = genual macroseta; Sti = tibial macroseta; St = tarsal macroseta) are that of Muma and Denmark (1970). Numbers of teeth on the fixed and movable cheliceral digits do not include the respective apical teeth. Setae not referred to in 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. Type of spermatheca or insemination apparatus are that of Denmark and Evans 2011. Only some species with only few measurements mentioned in the literature are provided in this paper. Classification of plants follows the APG IV classification of 2016 (ex. Byng et al. 2018). Specimens collected in fields in Mohéli Island within these surveys were all identified. Only very few single males or immatures collected during this study are not taken into account.
Specimens of each species are deposited in the mite collections of Montpellier SupAgro conserved in UMR CBGP INRA/IRD/CIRAD/SupAgro/University of Montpellier.
The following abbreviations are used in this paper for institutions: CBGP = Centre de Biologie pour la Gestion des Populations; CIRAD = Centre International de Recherche Agronomique pour le Développement; INRAE = Institut National de Recherche pour l ′ Agriculture, l ′ Alimentation et l ′ Environnement; INRAPE = Institut National de Recherche pour l ′ Agriculture, la Pêche et l'Environnement; IRD = Institut de Recherche pour le Développement; MSA = Montpellier SupAgro, France; UMR = Unité Mixte de Recherche; UR = Unité de Recherche.

Subfamily Amblyseiinae Muma
Neoseiulus teke belongs to the barkeri species group and the womersleyi species subgroup (Chant and McMurtry 2003a). This species is found in subSaharan Africa often associated with Mononychellus tanajoa (Bondar), the cassava green mite (CGM). It has been studied for its potential as BCA against the CGM. Nwilene and Nachman (1996) studied its reproduction characteristics on M. tanajoa. It was more efficient than I. degenerans, but seems not efficient enough in field conditions (Nwilene and Nachman 1996). Quilici et al. (2000) had collected this species before in La Réunion Island and it was recovered recently by Kreiter et al. (2020d).
Remarks: measurements of morphological characters of Neoseiulus teke female and male specimens from Mohéli Island are very close to measurements for specimens from neighbouring countries, especially from specimens from Mayotte ), La Réunion Island (Keiter et al. 2020d) and various countries in Africa, except for the holotype  and specimens from South Africa which are larger (van der Merwe 1965). Kampimodromini Kolodochka 1998: 59; Chant & McMurtry 2003b: 189, 2006: 137, 2007 33.
This species belongs to the orientalis species group (Chant and McMurtry 2003b). Our specimens with relatively shorter setae s4, Z4 and Z5, 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 Croft 1997; McMurtry et al. 2013). Navasero and Navasero (2016) had studied the life history of P. orientalis on the broad mite (Polyphagotarsonemus latus) (Banks) as prey and reported high predation rates on the eggs of P. latus, suggesting good potential for the control of this pest.
Remarks: morphological and morphometric characters and all measurements fit well measurements in Ferragut and Baumann (2019) and Kreiter et al. (2020d). This species was described from Asia (Narayanan et al. 1960) and presented also in Mauritius Baumann 2019; Kreiter et al. 2018a; Kreiter and AboShnaf 2020b), Mayotte , Vietnam , and in La Réunion Island (Kreiter et al. 2020d).  Chant & McMurtry 2004: 208, 2007 Like the previous species and for the same reasons, A. duplicesetus belongs to the largoensis species group and to the largoensis species subgroup (Chant andMcMurtry 2004a, 2007). First of all found only in Kenya (Moraes and McMurtry 1988; Zannou et al. 2007; ElBanhawy and Knapp 2011 and more recently in Sri Lanka (Moraes et al. 2004a), its biology is totally unknown. This is the second mention of that species in Indian Ocean Islands after Anjouan (Kreiter et al. 2021).
Amblyseius herbicolus is widespread in all tropical and subtropical regions of the world. It is the second most abundant phytoseiid mite on Coffea arabica L. in Brazil, associated with Brevipalpus phoenicis (Geijskes), vector of the coffee ring spot virus and it was found to be an efficient predator (Reis et al. 2007). Amblyseius herbicolus is also found associated with the broad mite, P. latus, in crops such as chili pepper (Capsicum annuum L.) in Brazil and has also a good potential for controlling the pest. RodriguezCruz et al. (2013) had studied biological, reproductive and life table parameters of A. herbicolus on three different diets: broad mites, castor bean pollen (Ricinus communis L.) and sun hemp pollen (Crotalaria juncea L.). The predator was able to develop and reproduce on all three these diets. However, its intrinsic growth rate was higher on broad mites and castor bean pollen. Feeding on alternative food such as pollen can facilitate the predator's mass rearing and maintain its population on crops when prey is absent or scarce. Many polyphagous generalist phytoseiid mites are important natural enemies because they can feed on plant provided pollen and various prey species, and thus persist in crops even in the absence of target pests (McMurtry et al. 2013). Hence, populations of these predators can be established in a crop by providing alternative food, thus increasing biological control. Alternative food affects P. latus control on chilli pepper plants by predatory mites (Duarte et al. 2015). Amblyseius herbicolus had high oviposition and population growth rates when fed with cattail pollen (Typha latifolia L.), chilli pepper pollen and beecollected pollen, and a low rate on the alternative prey (Tetranychus urticae Koch). Supplementing pepper plants with pollen resulted in better control of broad mite populations (Duarte et al. 2015). Release of A. herbicolus on young plants with weekly addition of honeybee pollen or cattail pollen until plants produce flowers seems a viable strategy to sustain populations of this predator (Duarte et al. 2015).  Remarks: morphological and morphometric characters and all measurements fit well measurements provided in Kreiter et al. (2018bKreiter et al. ( , 2020c. Amblyseius herbicolus was previously recorded in a lot of countries worldwide and especially in French West Indies (Moraes et al. 2000, Kreiter et al. 2006. It was first reported by Kreiter et al. (2018b) in the Comoros Archipelago in Grande Comore Island with two females collected. Amblyseius herbicolus was reported in the past from La Réunion Island from few specimens (Quilici et al. 1997(Quilici et al. , 2000 and more recently from a lot of specimens (Kreiter et al. 2020d). It is also reported recently from Vietnam (Kreiter et al. 2020c), Rodrigues and Maurice Islands (Kreiter and AboShnaf 2020a, b) but only from females.
The five male specimens of that species collected in this study will be redescribed in a following paper.  Gupta 1986).

Amblyseius largoensis (Muma)
Amblyseius largoensis belongs to the largoensis species group and to the largoensis species subgroup. It is widespread in all tropical and subtropical regions of the world and was the most abundant species collected by 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 Rodrigues Island by , from Mauritius Island by Ferragut and Baumann (2019) and Kreiter and AboShnaf (2020b) and from Mayotte by .
World distribution: this species is widely distributed in the tropical and subtropical regions of Africa, America, Asia and the Pacific Islands.

Euseius rhusi (van der Merwe)
Measurements of the single female (Table 3) fit well with the measurements from the literature (Ueckermann and Loots 1988; Moraes et al. 2006; ElBanhawy and Knapp 2011, with however some slightly shorter dimensions, especially for Z5, and some longer dimensions, especially of j3. Table 1 Character measurements of adult females of Euseius baetae collected in this study compared to those obtained in previous studies (localities followed by the number of specimens measured between brackets).

Sub-tribe Typhlodromalina Chant & McMurtry
Typhlodromalus spinosus was collected from Eastern, Western, but mainly Southern Africa and La Réunion (Demite et al. 2020). The rapid multiplication of this species on the western flower thrips (WFT), Frankliniella occidentalis Pergande, was confirmed and clear evidence that T. spinosus predates on WFT under laboratory and field conditions, but not on T. urticae (Mwangi et al. 2015). It seems abundant in low vegetation as it was found in high populations in a study of companion plants in a citrus orchard (Le Bellec et al. unpub. data).
This species have never been record from Guadeloupe or Martinique in similar studies, but it is interesting to notice that in those islands, another Typhlodromalus was collected, T. peregrinus (Muma) (Mailloux et al. 2010; Kreiter et al. 2013, 2018c. Typhlodromalus spinosus was recorded from La Réunion by Quilici et al. (2000) and was then find in quite Table 2 Character measurements of the adult male of Euseius baetae collected in this study with those obtained from previous studies (localities followed by the number of specimens measured between brackets).

Characters
Mohéli (1)  Remarks: morphological and morphometric characters and all measurements of our specimens fit well measurements in Kreiter et al. (2020d). This species was described from Mozambique (Meyer and Rodrigues 1966), then mentioned in the Indian Ocean from la Réunion (Quilici et al. 2000; Kreiter et al. 2020d, Mauritius (Kreiter and AboShnaf 2020b) and more recently from Anjouan (Kreiter et al. 2021).
Remarks: morphological and morphometric characters and all measurements of our specimens (Table 4) fit well measurements in Moraes et al. (2006) for specimens from Africa and above all that of Kreiter et al. (submitted) for specimens from Anjouan. But specimens from Mohéli have shorter setae j4, j5, j6, R1, s4, S2, z2, z4, z5, SgeII, SgeIII and smaller ventrianal shield and cheliceral digits but have longer macrosetae StIV compared to specimens from Africa. Above all, our specimens have pointed macrosetae or slightly rounded macrosetae on leg IV and the original description ) mentioned three evidently knobbed macrosetae. As it is the only main difference, we consider this difference as a variation of the character and not enough for considering that our specimens belong to a new species. The male of U. eastafricae was unknown until our collection. The single male collected will be described in a following paper. Phytoseiini Berlese 1913: 3; Phytoseiinae Vitzthum 1941 Genus Phytoseius Ribaga Phytoseius Ribaga 1904: 177. Table 4 Character measurements of adult females of Ueckermannseius eastafricae collected in this study with those obtained from previous studies (localities followed by the number of specimens measured between brackets).

Characters
Mohéli ( This species belongs to the plumifer species group (Chant and McMurtry 1994) as setae R1 and J2 are present. This species was described from specimens collected on Heterosmilax gaudichaudiana (Kunth) Maximovich (Smilacaceae), and Urena lobata L. (Malvaceae) in Victoria Mount Forest, Hong Kong Island, Hong Kong. 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 species belongs to the contiguus species group (Chant and McMurtry 1994) and its biology remains totally unknown.
World distribution: China, HongKong, Japan, Madagascar, Philippines, Singapore.  Ueckermann et al. 2008: 48. This species belongs to the singularis species group as setae JV3 are absent and dorsal shield setae are short (Chant and McMurtry 1994). The biology of that species is totally unknown. It was mentioned only from Kenya (Ueckermann et al. 2008)  Remarks: the species was mentioned only once from Kenya and described from only one female specimen (Ueckermann et al. 2008). Morphological and morphometric characters and all measurements of our specimens (Table 5) fit well measurements of the original description of Zannou, Moraes & Oliveira in Ueckermann et al. (2008) and with measurements of specimens from Mayotte Island  Typhlodromus (Anthoseius) hartlandrowei Evans Typhlodromus (Typhlodromus) hartlandrowei Evans, 1958: 580581; Chant 1959: 60. Clavidromus hartlandrowei, Muma, 1961. Typhlodromus (Neoseiulus) hartlandrowei, Pritchard & Baker, 1962: 222. Typhlodromus (Anthoseius) hartlandrowei, Moraes et al. 2004b: 328; Chant & McMurtry, 2007: 155; Ueckermann et al. 2008 This species belongs to the bergi species group (Chant and McMurtry 1994). The biology of that species is totally unknown. This is the first mention of that species outside the African continent.
World distribution: Democratic Republic of Congo, Nigeria, Uganda. Specimens examined: two specimens (2 ♀) collected during this study. Remarks: morphological and morphometric characters and all measurements of our specimens (Table 6) fit well with measurements of the original description given by Evans (1958), those given by Ueckermann et al. (2008) concerning specimens from Africa and those of specimens from Anjouan Island (Kreiter et al. 2021).
World distribution: Ghana, Mauritius Island, Mayotte Island, Rodrigues Island. Table 5 Character measurements of adult females of Typhlodromus (Anthoseius) grewiae collected in this study compared to those obtained in previous studies (localities followed by the number of specimens measured between brackets).
Remarks: morphological and morphometric characters and all measurements of our specimens fit well with measurements of the original description by Zannou, Moraes and Oliveira in Ueckermann et al. (2008) concerning specimens from Ghana, Western Africa. And with measurements of specimens from Rodrigues (Kreiter and AboShnaf 2020a), Mauritius (Kreiter and AboShnaf 2020b), Mayotte  and Anjouan (Kreiter et al. 2021). This species seems rather common in the Indian Ocean Islands, except in La Réunion Island.
World distribution: La Réunion Island. Specimens examined: three specimens (3 ♀♀) collected during this study. BandarEs Table 6 Character measurements of adult females of Typhlodromus (Anthoseius) hartlandrowei collected in this study compared to those in previous studies (localities followed by the number of specimens measured between brackets).
Salam, Les Abous Inn (23 m aasl, 12°17 ′ 37 ″ S, 43°45 ′ 27 ″ E), 1 ♀ on Punica granatum L. (Lythraceae), 4/XII/2018/ Remarks: several species are found both in La Réunion Island (in the Indian Ocean) and in the West Indies, probably because of reciprocal introductions certainly a long time ago with slavetrade and commercial exchanges between the two areas or because of introduction of plants from Antilles into La Réunion coming from the same African countries than slaves. The measurements and description of the specimens collected fit very well those given by Kreiter et al. (2002) for the original description and measurements of specimens from La Réunion (Kreiter et al. 2020d) and Rodrigues Islands (Kreiter and AboShnaf 2020a).

Conclusion
The results of a survey carried out in 2018 in Mohéli Island is presented in this paper. A total of 18 new records, 16 of which being documented in this paper: Two new species (Paragigagnathus sp. and Typhlodromalus sp.) found in several islands will be described in a next paper Among the 18 recorded species, at least five species (P. orientalis, A. largoensis, A. herbicolus, T. spinosus and T. [A.] transvaalensis) are already 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 Mohéli Island is of great agricultural, commercial and strategic interests for the country.