New records of phytoseiid mites (Acari: Mesostigmata) of Grande Comore Island (Comoros Archipelago)

Grande Comore is the larger Island of the four main islands constituting Comoros Archipelago. It is the fourth Island starting from Madagascar after Mayotte, Anjouan and Mohéli and closer to the African coast (Mozambique and Tanzania). So far, only five 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 Grande Comore Island, in which 29 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 (McMurtry and Croft 1997; McMurtry et al. 2013; Knapp et al. 2018. This family is widespread around the world, present on all continents except Antarctica, and consists of about 2,500 valid species in 94 genera and three subfamilies (Demite et al. 2021).
Biodiversity surveys 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, 2021a, b, c; Kreiter and AboShnaf 2020a. In these perspectives, the more interesting areas are probably those with a high level of biodiversity. Most of the Indian Ocean constitutes one of the highest world biodiversity areas, those areas 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 about 1,000 km from the northern coast of Madagascar, about only 70 km from Mohéli Islands and 300 kms from Mozambique coast in the Africa continent, Grande Comore (Ngazidja in Shicomori language) Island is one of the four main islands constituting Comoros Archipelago, with Mayotte, Anjouan and Mohéli and the largest of the four with more than 1,000 km².
The objective of this paper is to present the phytoseiid species reported in a survey conducted in December 2018 in Grande Comore Island.

Material and methods
The survey took place in Grande Comore from 6 to 11 th of December, 2018. Plant inhabiting mites were collected from cultivated and wild plants in few locations mainly in the eastern and southern parts 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. ( , 2021 for distribution and information on descriptions and redescriptions were used. World distribution indicated for each species is the world distribution prior to tthis study. 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 of each species are deposited in the mite collections of Montpellier SupAgro conserved in UMR CBGP INRA/IRD/CIRAD/SupAgro/University of Montpellier.

Characters
China ( , c, d, Kreiter et al. 2021a). This species described from Africa (Pritchard and Baker 1962) was first mentioned in the Indian Ocean from La Réunion Island (Kreiter et al. 2020d) but is also present in Rodrigues, Mauritius, Mayotte and Anjouan Islands , b, Kreiter et al. 2020a, Kreiter et al. 2021a. It was the more abundant species in Anjouan Island (Kreiter et al. 2021a).

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 the Madagascar coast and it is not surprising to find this species on a close by island. But Grand Comore is further from Madagascar but closer to Mozambique than Mayotte. The species was not reported from Mascareignes Archipelago. Its biology is totally unknown.  (Tables 3  and 4) fit well with those provided in the literature, except for s4 and Z4 for females which are longer in specimens from Grande Comore and s4, Z4 and macrosetae of leg IV which are also longer in specimens collected during this study. The presence of this species on Madagascar and Mayotte Island ) makes Grande Comore the third island of the Indian Ocean known for hosting this species.  Chant & McMurtry 2004a: 208, 2007 This species belongs to the largoensis species group as setae J2 and Z1 are present, setae s4 are minute and the ventrianal shield of the female is vaseshaped. It belongs to the largoensis species subgroup as setae Z4 are long, spermatheca has the calyx elongate and the female ventrianal shield is entire (Chant andMcMurtry 2004, 2007).

Tribe Amblyseiini Muma
It was described from Kenya (Moraes and McMurtry 1988; Zannou et al. 2007; ElBanhawy and Knapp 2011) and more recently reported from Sri Lanka (Moraes et al. 2004a), its biology is totally unknown. This is the third mention of that species in Indian Ocean Islands after Anjouan and Mohéli Islands (Kreiter et al. 2021a, b).
Remarks: this is the more abundant species found in several sites. All measurement values fit well those already published on this species with only very slight variations (Moraes and McMurtry 1988; Moraes et al. 2004a; Zannou et al. 2007; ElBanhawy and Knapp 2011; Kreiter et al. 2021a. Measurement values of female specimens of Grande Comore are very similar to values for specimens from Kenya and Sri Lanka, however with some shorter setae in specimens of Anjouan and Mohéli Islands (Kreiter et al. 2021a, b). The male of that species will be redescribed in a following paper.
Like the previous species, A. largoensis belongs to the largoensis species group and to the largoensis species subgroup (Chant and McMurtry 2004).
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 . 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 Caribean were conspecific. This species was previously recorded from Mauritius Island by Ferragut and Baumann (2019) and Kreiter and AboShnaf (2020b), from Rodrigues Island by , from Mayotte Island by  and Anjouan and Mohéli Islands (Kreiter et al. 2021a; Kreiter et al., 2021b. World distribution: this species is widely distributed in the tropical and subtropical regions of Africa, Americas, Asia and the Pacific Islands. It is also present in several Islands of the Indian Ocean (Rodrigues Island, Mauritius Island, Mayotte Island, Anjouan Island and Mohéli Island).
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 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 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 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 a 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 with measurements provided in Kreiter et al. (2018bKreiter et al. ( , 2020cKreiter et al. ( , d, 2021a and Kreiter and AboShnaf (2020a, b). Amblyseius herbicolus was previously recorded in many countries of the world 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 with only few specimens (Quilici et al. 1997(Quilici et al. , 2000 and more recently many 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. Males were however found among several females in Mohéli and will be redescribed in a following paper.

Subtribe Proprioseiopsina Chant & McMurtry
Proprioseiopsis ovatus belongs to the belizensis species group as genu I has 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, MarieGalante and Martinique (Kreiter and Moraes 1997; Moraes et al. 2000; Mailloux et al. 2010; Kreiter et al. 2018c. It was found in very high numbers 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). Proprioseiopsis mexicanus, and P. ovatus seems to be abundant on weeds in the lower vegetation (Mailloux et al. 2010; Kreiter et al. 2018c). 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 an ineffective predator of that species. Despite this information, the biology of P. ovatus remains unknown. Remarks measurements of the 5 ♀♀ and of the single male (tables 4 and 5) fit well with the measurements from the literature with slightly shorter dimensions in general and measurements from specimens of a previous record in Grande Comore (Kreiter et al. 2018b).
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 (pollenophagous generalist predators) of McMurtry and Croft (1997) and McMurtry et al. (2013). The species had been occasionally recorded from Madagascar (Blommers 1974), PapuaNew Guinea (Schicha and Gutierrez 1985), Seychelles (Schicha 1987), La Réunion Island, (Quilici et al. 1997, Kreiter et al. 2020c, Guadeloupe, Martinique and MarieGalante (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  ) and from Vietnam . Morphological and morphometric characters and all measurements of our specimens fit well with measurements in Kreiter et al. (2020d). This species was the second most collected species in our study comparing with A. herbicolus on Mauritius (Kreiter & AboShnaf 2020b) and it was also very common in La Réunion (Kreiter et al. 2020c Zaher 1986: 99, Northcraft 1987: 521, Papadoulis & Emmanouel 1991: 36. Iphiseius degenerans, Berlese 1921: 95, Evans 1954: 518, Moraes et al. 1986: 61, 2004b: 92, Chant & McMurtry 2005b: 215, 2007: 125. Iphiseius martigellus ElBadry 1968: 325 (synonymy according to Chant & McMurtry 2005b. The biological characteristics of this Ethiopian species have been well documented because of its use in controlling thrips on various cultivated plants in greenhouses. Iphiseius degenerans is a commercially available biological control agent of thrips and spider mites in greenhouse crops. It is able to feed on a variety of foods, but thrips' larvae and sweet pepper pollen are unfavourable food for immature development. This could compromise the establishment of this biological control agent when used against thrips in sweet pepper crops. According to the classification by McMurtry et al. (2013), I. degenerans is a typeIII generalist predator. It is one of the most common native phytoseiid mite species on cassava in southern Africa (Zannou et al. 2005) and feeds on Mononychellus tanajoa (Bondar) (Nwilene and Nachman 1996), a widely distributed neotropical mite pest of cassava in Africa, insect larvae and pollen of many plants (Vantornhout et al. 2005). Another study concluded that I. degenerans can be considered a suitable biological control candidate based on its preference for Eutetranychus orientalis (Klein) in the Mediterranean region (Fantinou et al. 2012). Remarks: measurements of the 3 ♀♀ + 1 ♂ fit well with measurements of specimens reported in the literature, but especially with those specimens previously collected in Grande Comore at Moroni (Kreiter et al. 2018b).
• concerning males (Table 6), setae S2 and z2 which shorter in specimens from Grande Comore Island and seta r3 and length and width of ventrianal shield which are longer in specimens from Grande Comore Island. However, males collected in Grande Comore Island and in Kenya were very few (2 for both). According to Tixier (2012) this number of males are lower than the minimum number of specimens needed to determine intraspecific variations.
This is the first mention of that species for the Indian Ocean and outside the Africa continent.

Typhlodromalus spinosus (Meyer & Rodrigues)
Amblyseius spinosus Meyer & Rodrigues 1966: 30, Moraes et al. 1986: 31. Kampimodromus spinosus, Quilici et al. 2000 Typhlodromalus spinosus, Moraes et al. 2004b: 204, Chant & McMurtry 2005b: 199, 2007 This species also belongs to the athiasae species group as setae J1 and S5 are absent (Chant andMcMurtry 2005b, Moraes et al. 2006). The rapid multiplication of this species on the western flower thrips (WFT), Frankliniella occidentalis Pergande, was confirmed under laboratory and field conditions, but it was not effective against 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 citrus orchards (Le Bellec et al. unpub. data Remarks: morphological and morphometric characters and all measurements of our specimens fit well with measurements in Kreiter et al. (2020d). This species was described from Mozambique (Meyer and Rodrigues 1966) and then reported from Indian Ocean from La Réunion Island (Quilici et al. 2000; Kreiter et al. 2020d, Mauritius (Kreiter and AboShnaf 2020b) and more recently from Anjouan (Kreiter et al. 2021a) and Mohéli Islands (Kreiter et al. 2021b) in the Comoros Archipelago.  Moraes et al. 1986: 210, 2004b: 232, Chant & McMurtry 2007 This species belongs to the horridus species group (Chant and McMurtry 1994) as setae R1 and J2 are present. Species of the genus Phytoseius are supposed to belong to the Type III species Croft 1997; McMurtry et al. 2013), i.e., a polyphagous generalist predator. However, the biology of Phytoseius amba remains totally unknown.

Subfamily Phytoseiinae Berlese
World distribution: Anjouan Island, Benin, Burundi, Cameroon, Cape Verde, DR Congo, Grande Comore Island, Kenya, Madagascar Island, Malawi, Mozambique, Nigeria, Reunion Table 5 Character measurements of adult females of Typhlodromalus athiasae collected in this study with those obtained from previous studies (localities followed by the number of specimens measured between brackets).
Remarks: measurements of the specimens collected during this study agree well with measurements of the literature, especially with those of Ueckermann et al. (2007) obtained with a great number of specimens (29) from various countries in Africa, with those of Kreiter et al. (2020d) for specimens from La Réunion, with those of Kreiter et al. (2018b) for specimens from Grande Comore and with those of Kreiter et al. (2021a) for specimens from Anjouan Island.
World distribution: Anjouan Island, Burundi, China, Hong Kong, India, Indonesia, Japan, Madagascar Island, Mauritius Island, Philippines, Réunion Island, Rodrigues Island, Singapore, Table 6 Character measurements of adult males of Typhlodromalus athiasae collected in this study with those obtained from previous studies (localities followed by the number of specimens measured between brackets).

Taiwan.
Specimens examined: 2 ♀♀ in total. Moroni (51 m aasl, lat. 11°41 ′ 01 ″ S, long. 43°15 ′ 55 ″ E), 2 ♀♀ on Passiflora edulis Sims (Passifloraceae), 9/XII/2018; Remarks: morphological and morphometric characters and all measurements of our specimens fit well with measurements in Kreiter et al. (2020d) for specimens of La Réunion Island. This species was recorded in several countries of Asia, in Burundi, Madagascar (Demite et al. 2021) and La Réunion (Quilici et al. 2000). It was recently recorded in Mauritius Island by Ferragut and Baumann (2019) and in Anjouan Island by Kreiter et al. (2021a). It was however previously reported by Quilici et al. (2000) in the Indian Ocean from Mascareignes Archipelago in La Réunion Island where Kreiter et al. (2020d) have recovered the species in larger numbers.

Subfamily Typhlodrominae Wainstein
This species belongs to the contiguus species group (Chant and McMurtry 1994) and its biology remains totally unknown.  Remarks: morphological and morphometric characters and all measurements of our specimens fit well with measurements in the many descriptions and redescriptions available in the literature, especially those of Blommers (1976) for specimens from Madagascar. Mentioned only from SouthEast Asia and Madagascar, this species seems quite common in Comoros Table 7 Character measurements of adult females of Phytoseius duplus collected in this study and those reported in previous studies (localities followed by the number of specimens measured between brackets).

Characters Mauritius (4) South Africa
(2) Archipelago , Kreiter et al. 2021a. This is the second most abundant species collected during this study. 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 unknown. It was mentioned only from Kenya (Ueckermann et al. 2008)  Remarks: morphological and morphometric characters and all measurements of our specimens (Table 8) fit well with measurements of the original description of Zannou, Moraes and Oliveira in Ueckermann et al. (2008) and with measurements of specimens from Mayotte Island , Anjouan Island (Kreiter et al. 2021a) and Mohéli Island (Kreiter et al. 2021b 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 this species is unknown. This is the first mention of this species outside the African continent. The male was unknown until our study but one male has been collected and will be described in a following paper. Remarks: morphological and morphometric characters and all measurements of our specimens (Table 9) fit well with measurements of the original description given by Evans Table 8 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).

Mayotte Island
(2) This species belongs to the large rhenanus species group (Chant and McMurtry 1994). The biology of that species is unknown. Remarks: morphological and morphometric characters and all measurements of our specimens fit well with measurements of the original description in Ueckermann et al. (2008) concerning specimens from Ghana, Western Africa. They fit well with measurements of specimens from Rodrigues (Kreiter and AboShnaf 2020a), Mauritius (Kreiter and AboShnaf 2020b), Mayotte , Anjouan (Kreiter et al. 2021a) and Mohéli Islands (Kreiter et al. 2021a). This species seems rather common in the Indian Ocean Islands, except in La Réunion Island. As the previous species, this one also belongs to the large rhenanus species group (Chant and McMurtry 1994). It has been collected only once in Philippines on Dysoxylum cumingianum (De Candolle) Harms, a common Meliaceae in this area. This is the first mention of its occurrence outside Philippines. Its biology is unknown.

Typhlodromus (Anthoseius) quadratus Wu & Liu
Typhlodromus quadratus Wu & Liu 1997: 150151. Typhlodromus (Anthoseius) quadratus, Moraes et al. 2004b: 344, Chant & McMurtry 2007: 155, Wu et al. 2010 This species also belongs to the rhenanus species group (Chant and McMurtry 1994). It has been collected only once in China on unknown host plants. So this the first report of this species outside China. Its biology is unknown. Table 9 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).
World distribution: China. Specimens examined: A single female collected during this study. Djoumoichongo (230 m aasl, lat. 11°48 ′ 34 ″ S, long. 43°17 ′ 37 ″ E), 1 ♀ on Cyathea sp. (Cyatheaceae), 10/XII/2018. Remarks: description by Wu and Liu (1997) is quite poor, with many details lacking and very small drawings, making difficult comparisons and diagnose. Morphological and morphometric characters and all measurements of our specimen (Table 11) fit however very well with measurements of the original description given by those authors. Only slight differences exist in the length of setae. The most important difference between the Chinese specimens and the present specimen is seta Z4 which is serrated in our specimen but smooth in the original description.

Conclusion
The results of the survey carried out in 2018 in Grande Comore Island is presented in this paper. Of a total of 29 records, 25 are documented in this paper: 16 Amblyseiinae, 3 Phytoseiinae Table 10 Character measurements of an adult female of Typhlodromus (A.) luzonensis collected in this study compared to those in previous studies (localities followed by the number of specimens measured between brackets).
Only one species not recovered during this study [Neoseiulus longispinosus (Evans) in Kreiter et al. 2018a], 28 species are now recorded from this Island.
Among the 25 recorded species during this study, at least seven species (N. teke, P. orientalis, A. largoensis, A. herbicolus, E. ovaloides, I. degenerans, and T. spinosus) are already known as biological control agents (BCAs), some having been evaluated and some others commercially reared in other parts of the world. With N. longispinosus, not recovered this time but reported previously (Kreiter et al. 2018a) and which is also a effective BCA in many parts of the world, it represents eight species of interest for Grande Comore. Table 11 Character measurements of an adult female of Typhlodromus (A.) quadratus collected in this study compared to those in previous studies (localities followed by the number of specimens measured between brackets).

Characters
Grande Comore Island (1) (this study) China ( 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 Grande Comore Island is of great agricultural, commercial and strategic interests for the country.