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

Anjouan is one of the four main islands constituting Comoros Archipelago, with Mayotte, Mohéli and Grande Comore Islands. It is the second Island closer from Madagascar after Mayotte. So far, no species of the mite family Phytoseiidae (Acari: Mesostigmata) had been reported from this island. In this paper, 18 species are recorded from a survey conducted at the end of 2018 in Anjouan Island.


Introduction
Mites of the family Phytoseiidae are all predatory species on phytophagous mites and small insects such as thrips and whiteflies, on commercial plants and the wild vegetation. Several of them are biological control agents for control of pest organisms in both open and protected crops all around the world (McMurtry and Croft 1997; McMurtry et al. 2013; Knapp et al. 2018). This family is widespread around the world, presents on all continents except Antarctica, and consists of about 2,500 valid species in 94 genera and three subfamilies (Demite et al. 2020).
Biodiversity survey in poorly investigated areas is still an urgent need 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 2020. 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 are 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 and future establishment of conservation programs.
Located in the Indian Ocean at around 460 km from the northern coast of Madagascar, Anjouan Island (Ndzuwani or Nzwani in Shikomori) is one of the four main islands constituting Comoros Archipelago, with Mayotte, Mohéli and Grande Comore. No phytoseiid species are known from this island.
The objective of this paper is consequently to present the phytoseiid species found in a survey conducted in November 2018 in Anjouan Island.

Material and Methods
The samplings took place in Anjouan at the end of November and beginning of December 2018. Plant inhabiting mites were collected from cultivated and wild plants in few locations mainly in the western part of the island.
Mites were directly collected on large leaves and herbaceous plants with a fine brush using either a hand magnifier or a stereoscopic microscope, or on shrubs and trees by beating the plants with very small or spiny leaves. The mites were kept in a black plastic rectangular saucer 45 x 30 cm (Ref. STR 45, BHR, 71370 SaintGermainduPlain, France). The phytoseiid mites were then transferred using a fine brush into small plastic vials containing 1.5 ml of 70% ethanol.
Mites were mounted on slides in Hoyer's medium, and all examined 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 as well as 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 (1992) for the dorsum and by Chant & YoshidaShaul (1991) for the venter. The notation for solenostomes and poroids is based on AthiasHenriot (1975). Numbers of teeth on the fixed and movable cheliceral digits do not include the respective apical hook. Setae not referred 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. 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 (see for example Byng et al. 2018).
Specimens of each species are deposited in the mite collections of Montpellier SupAgro conserved in UMR CBGP INRA/IRD/CIRAD/SupAgro/University of Montpellier.
Remarks: the measurements of the single female of N. lula (Table 1) fit well with the type materials from Central Africa (Schicha 1981b) and those of specimens from Africa ) as well as from La Réunion (Kreiter et al. 2020d). When compared to other specimens from subSaharan Africa studied by Zannou et al. (2006), our specimen has shorter Z4 and relatively longer ventrianal shield. Specimens from South Africa and Madagascar (van der Merwe 1968; Ueckermann andLoots 1988) have in general greater dimensions than those obtained for specimens from La Réunion (Kreiter et al. 2020d) and Anjouan Islands. Kampimodromini Kolodochka 1998: 59; Chant & McMurtry 2003b: 189, 2006: 137, 2007 33.
Our specimens of Paraphytoseius should be placed the orientalis species group by the absence of setae S5 (Chant and McMurtry 2003b). As suggested by Chant and McMurtry (2003b) and Moraes et al. (2007), we consider that P. horrifer and P. orientalis are different valid species. All our specimens have long setae s4, Z4, Z5, and no distinctly short, thick, spatulate macroseta on genu I. They all belong consequently to the former species. This species is widely distributed in SubSaharan Africa and Madagascar. The biology of P. horrifer remains totally unknown. It was mentioned recently for the first time from several countries: La Réunion (Kreiter et al. 2020d), Mauritius (Kreiter and AboShnaf 2020b), Rodrigues (Kreiter and AboShnaf 2020a) Islands and Vietnam (Kreiter et al. 2020c Remarks: morphological and morphometric characters and all measurements fit well with those mentioned by Kreiter et al. (2020c, d). This species described from Africa (Pritchard & Baker 1962) was first mention in the Indian Ocean from La Réunion Island (Kreiter et al. 2020d) but seems to be present in Rodrigues, Mauritius and Mayotte AboShnaf 2020a, b; Kreiter et al. 2020a) and actually in at least one island of Comoros Archipelago. This is the most abundant species in Anjouan Island but all specimens were collected only in one sample site. Amblyseius duplicesetus belongs to the largoensis species group and to the largoensis species subgroup (Chant andMcMurtry 2004a, 2007). It was found in Kenya (Moraes and McMurtry 1988; Zannou et al. 2007; ElBanhawy and Knapp 2011 and in Sri Lanka (Moraes et al. 2004a). Its biology is totally unknown. This is the first mention of that species in Indian Ocean Islands.

Amblyseius herbicolus (Chant)
Amblyseius herbicolus is widespread in all tropical and subtropical regions of the world. It is the second most abundant phytoseiid mites 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 Table 3 Character measurements of adult males of Amblyseius duplicesetus collected in this study with those obtained from previous studies (localities followed by the number of specimens measured between brackets).

Characters
Anjouan ( ) and sun hemp pollen (Crotalaria juncea L.). The predator was able to develop and reproduce on all these three 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 maintains 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).
Amblyseius herbicolus was previously recorded in a lot of countries of the world and especially in French West Indies (Moraes et al. 2000, Kreiter et al. 2006) and in Comoros Archipelago in Grande Comore Island (Kreiter et al. 2018b Kreiter et al. (2018b) in the Grande Comore Island of the Comoros Archipelago in the Indian Ocean based on two females. This is interesting to notice that no male were collected, just like in La Réunion Island (Kreiter et al. 2020c) and also on Citrus in Black Sea Region of Turkey (Doker et al. 2020). 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. Morphological and morphometric characters and all measurements fit well with those measurements provided in Kreiter et al. (2018bKreiter et al. ( , 2020c Gupta 1986).
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 Mauritius Island by Ferragut and Baumann (2019) and Kreiter and AboShnaf (2020b), from Rodrigues Island by Kreiter and AboShnaf (2020a) and from Mayotte by Kreiter et al. (2020a) based on males and females records.
World distribution: this species is widely distributed in the tropical and subtropical regions of Africa, America, Asia and the Pacific Islands.
Remarks: morphological and morphometric characters and all measurements of the Anjouan specimen fit well with those given in Zannou et al. (2007) for specimens from Africa, Navia et al.. (2014) for specimens from Brazil, La Réunion and Trinidad & Tobago, by Ferragut and Baumann (2019) and Kreiter and AboShnaf (2020b) for specimens from Mauritius Island, by Kreiter and AboShnaf (2020a) for specimens from Rodrigues Island and by Kreiter et al. (2020a) for specimens from Mayotte Island. Schicha (1981c) has given a detailed description of A. herbicolus (under the name A. deleoni Muma and Denmark). He states that, whereas the male of A. deleoni has been described from Florida by Muma and Denmark (1970), it has not been found on leaf samples taken regularly over 5 years from citrus trees on the central coast of New South Wales (Schicha 1981c). Similarly, Blommers (1976) failed to observe males in the mass rearing of this species in Madagascar. Ferragut and Baumann (2019), Kreiter et al. (2020d) and Kreiter and AboShnaf (2020b) never recorded a single male among several hundred specimens collected in La Réunion and Mauritius, respectively. Occurrence of males in natural populations of A. herbicolus, a thelytokous species after several author, is questioned. Amblyseius largoensis is a species also very common in the Islands of Indian Ocean very often recorded in several Islands AboShnaf 2020a, b; Kreiter et al. 2020a, b). We consequently consider that the single specimen collected in Anjouan which setae length is in accordance with description of the male of that species, is a male of A. largoensis. But as females were not collected in the same time, a doubt is still existing on the occurrence of that species, which must be confirmed in further more surveys in more locations.
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 to be abundant in low vegetation as it was found in high populations in a study of companion plants in citrus orchard (Le Bellec et al. unpub. data).
This species have never been recorded 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 high numbers by Kreiter et al. (2020d) and in few numbers from Mauritius Island (Kreiter and AboShnaf 2020b).

Characters
Anjouan (2)  As the previous species, this species belongs also to the horridus species group (Chant and McMurtry 1994). It was recorded in several countries of Asia, in Burundi, Madagascar (Demite et al. 2020) and La Réunion (Quilici et al. 2000). Its biology remains totally unknown. It was recently recorded in Mauritius Island by Ferragut and Baumann (2019).

Subfamily Typhlodrominae Wainstein
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. Specimens examined: 11 specimens (10 ♀♀ and 1 ♂) collected during this study. Remarks: morphological and morphometric characters our specimens fit well with those of numerous descriptions and redescriptions available in the literature, especially those by Blommers (1976) for specimens from Madagascar. This species was reported only from SouthEast Asia and Madagascar. This is the second report of this species in the Indian Ocean outside Madagascar after Mayotte Island (Kreiter et al. 2020a).  20; Karg 1982: 194; Chant & McMurtry 1994: 250, 2007

Typhlodromus (Anthoseius) grewiae Zannou, Moraes & Oliveira
Typhlodromus (Anthoseius) grewiae Zannou, Moraes & Oliveira in 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) based on single female.

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). Its biology is totally unknown. Remarks: morphological and morphometric characters of our specimens fit well with those of the original description based on the specimens collected from Ghana, Western Africa by Ueckermann et al. (2008) and with those of specimens from Rodrigues (Kreiter and AboShnaf 2020a), Mauritius (Kreiter and AboShnaf 2020b) and Mayotte (Kreiter et al. 2020a). 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 of our specimens fit well with those of specimens from South Africa in van der Merwe (1968) and Ueckermann et al. (2008) and those of specimens from Mayotte Island (Kreiter et al. 2020a).

Typhlodromus (Anthoseius) moraesi Kreiter & Ueckermann
Typhlodromus (Anthoseius) moraesi Kreiter & Ueckermann in Kreiter et al. 2002: 338. The biology of this species found in La Réunion Island by Kreiter et al. (2002) on various host plants (Kreiter et al. 2002) and then in French Caribbean Islands (Mailloux et al. 2010; Kreiter et al. 2013) remains unknown. 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 long time ago with slaves markets and commercial exchanges between the two areas or because of introduction of plants in Antilles and La Réunion coming from the same African area than Slaves. The measurements and characteristics of the specimens collected fit very well with those given by Kreiter et al. (2002) and with measurements of specimens from Rodrigues Island (Kreiter and AboShnaf 2020a).
This species has elongate serrated dorsal setae, setae Z1 and JV3 absent, an elongate calyx of the spermatheca, leg IV with 3 macrosetae and few teeth on chelicerae. It belongs to the transvaalensis species group of the subgenus Anthoseius of the genus Typhlodromus (Chant and McMurtry 1994).
According to McMurtry et al. (2013), T. (A.) transvaalensis is a type III phytoseiid and a generalist predator that feeds on mites, insects and pollen. It completed its life cycle when fed on the eriophyid mites Eriophyes dioscoridis Soliman and AbouAwad and Eriophyes olive Zaher and AbouAwad, eggs of the scale insect Parlatoria zizyphus (Lucas) and pollen of Ricinus communis L. in experimental conditions. The percentage of individuals attaining maturity was less than 20% when nymphs of the tetranychid mite, T. urticae Koch, were provided. The development was faster and reproduction was higher when T. (A.) transvaalensis fed on eriophyid mites. T. urticae was an unsuitable feeding for reproduction of the phytoseiid. The daily reproduction was as low as 0.4 and 0.8 egg/ female/ day when females were maintained on pollen grains of R. communis and eggs of P. zizyphus. The adult female daily consumed 126, 97 and 6 individuals of E. olivi, E. dioscoridis and T. urticae, respectively (Momen and Hussein 1999). Adult female T. (A.) transvaalensis were more efficient at predating all stages of P. latus (Banks) than Tetranychus bastosi Tuttle, Baker and Sales. The T. (A.) transvaalensis life cycle was shorter with diets including R. communis pollen, but Zea mays L. pollen was also suitable for reproduction. The results indicate that T. (A.) transvaalensis is a generalist predator with high potential for controlling P. latus in Jatropha curcas L. plantations and that the presence of R. communis and Z. mays crops boosts its development and reproduction (Cañarte et al. 2017). This species is widely distributed all over the world (Demite et al. 2020). It was recorded from La Réunion Island in the Indian Ocean (Quilici et al. 2000, Kreiter et al. 2020d. Specimens examined: 25 specimens (13 ♀♀, 9 ♂♂ and 3 imm.) collected during this study.  (Kreiter et al. 2020d), Kenya and South Africa (Ueckermann et al. 2008).

Conclusion
The result of a survey conducted in 2018 in Anjouan Island is presented in this paper. A total of 18 species belonging to three subfamilies: Amblyseiinae (9), Phytoseiinae (2) and Typhlo drominae (7)   Among the 18 recorded species, at least four species [A. largoensis, A. herbicolus, T. spinosus and T. (A.) transvaalensis] are already known as biological control agents. 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 Comoros is of great agricultural, commercial and strategic interests for the country.