Phytoseiid mites of Rodrigues Island (Acari: Mesostigmata)

Rodrigues is one of the three main islands constituting Mascareignes Archipelago, with La Réunion and Mauritius. It belongs to the state of Mauritius. So far, no mite species of the family Phytoseiidae have been reported from this Island. We report in this paper the results of a survey conducted in November 2018 on Rodrigues Island, during which 18 species have been recorded.


Introduction
Mites of the family Phytoseiidae are known for their predatory habits on phytophagous mites and small insects on cultivated plants and wild vegetation. Several of them are used for the control of pest organisms in agricultural open fields and protected crops all around the world (McMurtry and Croft 1997;McMurtry et al. 2013). This family is widespread around the Globe, presents on all continents except Antarctica and consists presently of 2,521 valid species of 94 genera belonging to three sub-families (Demite et al. 2020).
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. 2020a, b, c).
Most of the Indian Ocean constitutes one of the world's biodiversity hotspots. The concept of biodiversity hotspot was defined by Myers (1988) in order to identify the most immediately important areas for biodiversity conservation. These hotspots 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 areas may contribute to future establishment of conservation programs.
Located in the Indian Ocean at 1,740 km from the eastern coast of Madagascar, at 617 km from Mauritius, and 836 km from La Réunion, Rodrigues is one of the three main islands constituting Mascareignes Archipelago, together with La Réunion and Mauritius.
No phytoseiid species have been recorded until now from this island. The objective of this paper is to present the phytoseiid species recorded as a new survey conducted in November 2018 on Rodrigues Island.
This species belongs to the barkeri species group of the genus Neoseiulus, as the spermathecal atrium is large and forked at junction with major duct. It belongs to the barkeri species subgroup as the calyx is not markedly constricted at junction with the atrium, the atrium is deeply forked at the junction with major duct without vacuolated area, and the major duct, atrium and calyx are of approximately the same width (Chant and McMurtry 2003a).
Various studies had 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 control of broad mite, Polyphagotarsonemus latus (Banks), on peppers. Neoseiulus barkeri constitutes a potential Biological Control Agents (BCA) for several crops especially in vegetables greenhouses. This species had been mentioned by Quilici et al. (2000) and Kreiter et al. (2020c) on La Réunion Island.
Specimens examined: A single ♀ collected during this study. Port-Mathurin, City Center (11 m aasl, lat. 19°40 ′ 53 ″ S, long. 63°25 ′ 17 ″ E), 1 ♀ on Litchi chinensis Sonnerat (Sapindaceae), 14/XI/2018. Remarks: measurements of characters of the female from Rodrigues are only slightly different from female specimens from other countries, especially La Réunion Island. Comparisons with N. barkeri measurements of female and male specimens of various origins in Beaulieu and Beard (2018) show shorter dimensions of all characters of Rodrigues specimens. These authors mentioned shorter dorsal setae of African female and male specimens (lower part of observed ranges) compared to their own measurements (Beaulieu and Beard 2018 Kreiter et al. 2020c). Neoseiulus barreti Kreiter in Furtado et al. 2005: 135 (synonymy according to Kreiter et al. 2020c).
This species belongs to the cucumeris species group of Neoseiulus. It was collected and described in 1987 on Vigna unguiculata (L.) Walp. in Queensland, Australia (Schicha 1987) and described long time after under two different species names, N. recifensis Gondim Jr and Moraes and N. barreti Kreiter. Kreiter et al. (2020c) Kreiter et al. 2020c. This species was described from Australia, but presented also in Brazil and was firstly mentioned in the Indian Ocean from La Réunion Island, an Island distant of 836 km from Rodrigues. Several species are shared by the two Islands and probably by many others.
This species is distributed in many countries of the world, mainly in tropical areas (Moraes et al. 2000;Mailloux et al. 2010;Kreiter et al. 2013Kreiter et al. , 2018Demite et al. 2020). It was found in low numbers in Guadeloupe, Martinique and La Réunion except for studies on companion plants in citrus orchards (Mailloux et al. 2010;Kreiter et al. 2013Kreiter et al. , 2018cLe Bellec et al., unpub. data). This species seems to be more common on weeds with populations of tetranychid mites. Neoseiulus longispinosus, a type II phytoseiid predatory mite, as is N. californicus (McMurtry et al. 2013), had received increasing attention in Asia for the control of different spider mites (of Eutetranychus, Oligonychus, and Tetranychus) since 2010 (Nusartlert et al. 2011). The feeding, development, predation, cannibalism, intra-guild predation and behaviour had thus been extensively studied by several authors (e.g., Luong et al. 2017) for pest control purposes. Neoseiulus longispinosus is well-known as a BCA sell in several countries in the world for the management of spider mites. The recent results of Huyen et al. (2017) showed at least in controlled laboratory conditions, N. longispinosus is a potential biological control agent against the citrus red mite, Panonychus citri (McGregor).
World distribution: This species is distributed in many countries of the world, mainly in tropical areas. Remarks: measurements of specimens of Rodrigues females and males overlap with those obtained for populations of various countries, especially for specimens from La Réunion Island (Kreiter et al. 2020c). Kampimodromini Kolodochka 1998: 59;Chant & McMurtry 2003b: 189, 2006b: 137, 2007 33.
Remarks: morphological and morphometric characters and all measurements fit well with measurements in Kreiter et al. 2020b, c. This species was described from Africa (Pritchard & Baker 1962), but distributed also in Vietnam (Kreiter et al. 2020b) and was firstly mentioned in the Indian Ocean from la Réunion Island, an Island distant of 836 km from Rodrigues. Several species are shared by the two Islands and probably by many others.
Phytoseiulus persimilis is a Mediterranean / subtropical predatory mite that is a type I species, i.e., a specialist predator of the urticae species group of the genus Tetranychus (McMurtry and Croft 1997;McMurtry et al. 2013). Considerable research had been conducted on this predator-prey interaction (see review by Kostiainen and Hoy 1996), and numerous biological control programs had used P. persimilis against T. urticae on a wide range of ornamental and vegetable crops. Phytoseiulus persimilis was the first greenhouse biological control agent available commercially and is one of the most successful biological control agents. It can also be used in temperate climates on open-field crops such as strawberries. Optimum conditions are 20-27°C and relative humidity of 60-90%. Cooler or warmer temperatures may have a negative effect on reproduction, development and efficiency of this predatory mite. This species is present on Rodrigues probably because of its commercial introduction and uses in vegetable and ornamental greenhouses, dispersion of some specimens released and establishment in the environment. This species was reared and sold on La Réunion and commercialized in Mascareignes since a long time (Quilici, personal communication).
World distribution: widely distributed in Africa, Australia, Europe, especially Mediterranean countries, South America, and Asia, probably after largely distributed commercial uses in the world, dispersion in the environment in at least some locations and establishments of this species.
Remarks: measurements of adult females collected in this work agree very well with measurements in the literature, especially those of Ueckermann et al. (2007).

Amblyseius herbicolus
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 vase-shaped. 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 and McMurtry 2004).
It 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. Rodriguez-Cruz 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 bee-collected pollen, and a low rate on the alternative prey T. urticae. 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 recorded recently in Comoros archipelago (Kreiter et al. 2018b) and in La Réunion (Quilici et al. 1997(Quilici et al. , 2000Kreiter et al. 2020c Ueckermann & Loots 1988). Amblyseius amtalaensis Gupta 1977: 53 (Synonymy according to Gupta 1986).
This species belongs to the largoensis species group, and the largoensis species subgroup for the same reasons.
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.
Using morphometric analyses of 36 characters, molecular analyses and crossing tests, Navia et al. (2014) studied specimens collected from 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.
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 fit well with measurement values given by Zannou et al. (2007) for specimens from Africa, Navia et al. (2014) for specimens from Brazil, La Réunion and Trinidad and Tobago an,d Ferragut and Baumann (2019) for specimens from Mauritius. This is of the three more numerous species collected during this study and probably one of the more common species on the island, with A. passiflorae and E. ovaloides.
This species was only known from the type series (five females and one male) (Blommers 1974). The original description was rather complete, providing comprehensive information on female and male morphology, and Ferragut and Baumann (2019) had added information on dorsal adenotaxy and poroidotaxy. This species was collected for the latter authors and thus already recorded from Mauritius, but of course not from Rodrigues. Remarks: this species was reported before by Ferragut and Baumann (2019). Morphological and morphometric characters and all measurements of our specimens fit well with measurements in Blommers (1974) and Ferragut and Baumann (2019). This is one of the three more numerous species collected during this study and probably one of the more common species in the island, together with A. largoensis and Euseius ovaloides.  Denmark & Muma 1989).

Amblyseius tamatavensis Blommers
This species belongs to the obtusus species group as setae J2 and Z1 are present, setae z4 are minute and the female ventrianal shield is not vase-shaped or divided. It belongs to the aerialis species subgroup (46 species) as the calyx of the spermatheca is tubular (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. (2013). Cavalcante et al. (2017) reported this species as a promising natural enemy of B. tabaci. Experimental releases of this predator on caged plants in a screenhouse caused the reduction of the density of B. tabaci on pepper plants by up to 60-80% (Massaro and Moraes 2019). It can be easily produced in large numbers (Massaro et al. 2018) when fed with astigmatine mites, which could allow the mass production for augmentative biological control. This species is reported from tropical areas from over 20 countries around the world (Africa, Asia, America and Oceania). It was recorded in La Réunion (Quilici et al. 2000).
World distribution: this species was described from Madagascar, but is actually widely distributed in several countries of tropical and subtropical regions of Africa, America, Asia and the Pacific Islands.
This species belongs to the belizensis species group as genu I have no macrosetae. As the spermatheca of that species has a short calyx, cup-shaped, it belongs to the asetus species subgroup (Chant and McMurtry 2005a).
This species is known from all Islands of French West Indies (Kreiter and Moraes 1997;Moraes et al. 2000;Kreiter et al. 2006Kreiter et al. , 2018cMailloux et al. 2010), but it was found only in very large numbers during a previous study on companion plants in Guadeloupe (Mailloux et al. 2010) and in a study on La Réunion (Le Bellec, unpub. data). This species seems to be very abundant on weeds in the lower vegetation. Phytoseiid mites of the genus Proprioseiopsis had been found mainly in ground surface, humus, litter, soil, moss or on grass (Muma and Denmark 1970;McMurtry et al. 2015).
Proprioseiopsis mexicanus population increased when fed T. urticae eggs (Megevand et al. 1993) and seems to be a good predator of thrips (Kreiter, unpub. data). It is one of the prevailing phytoseiid species on citrus orchards in Alabama (Fadamiro et al. 2009). Denmark and Evans (2011) mentioned that the species can be reared on T. urticae and Oligonychus pratensis (Banks) and is associated with Bryobia praetiosa Koch, Bryobia spp. and P. ulmi. It was also found in association with Tetranychus evansi Baker and Pritchard (Furtado et al. 2014), but mentioned as a poor predator of that species. The biology of this species is however almost unknown.
Proprioseiopsis mexicanus was already recorded in the Indian Ocean by Quilici et al. (2000) and Kreiter et al. (2020c).
World distribution: This species is distributed in many countries of the world, mainly in tropical areas.
Remarks: measurement values of female specimens from Rodrigues fit well with all those indicated in Kreiter et al. (2018cKreiter et al. ( , 2020c

Subfamily Phytoseiinae Berlese
This species belongs to the horridus species group as setae J2 and R1 are absent (Chant and McMurtry 1994).
This species was described from Hong-Kong by Swirski and Shechter (1961) collected on a wide range of plants and very common on citrus. 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.
Remarks: this species was reported before by Ferragut and Baumann (2019) from Mauritius, but it was already reported by Quilici et al. (2000) from Mascareignes Archipelago in La Réunion Island where Kreiter et al. (2020c) have recently recovered the species. Morphological and morphometric characters and all measurements of our specimens fit well with measurements in Kreiter et al. (2020c).

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). It was abundant on lower 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 despite this observation that has to be confirmed, the biology of this species remains totally unknown.  Ferragut and Baumann (2019). Morphological and morphometric characters and all measurements of our specimens fit well with measurements of the original description by Kreiter et al. (2002) concerning specimens from La Réunion Island, Ferragut and Baumann (2019) for specimens from Mauritius and Kreiter et al. (2020c) for additional specimens from La Réunion Island.
The biology of this species remains totally unknown. This is the most numerous species of Phytoseius in this study. This species belongs to the large rhenanus species group (Chant and McMurtry 1994). The biology of that species is totally unknown. 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.
World distribution: Guadeloupe, La Réunion Island. Remarks: several species are found both on La Réunion Island (in the Indian Ocean) and in the West Indies, probably because of reciprocal introductions certainly long time ago with slave 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 description of the specimens collected fit very well with those given by Kreiter et al. (2002).

Conclusion
The results of an additional survey made in 2018 on Rodrigues Island is presented in this paper. A total of 18 records, 11 Amblyseiinae, 4 Phytoseiinae and 3 Typhlodrominae, have been obtained. The fauna of Rodrigues after our study is composed of this 18 species, namely: Neoseiulus barkeri, N. houstoni, N. longispinosus Among the 18 recorded species, at least seven species are known as biological control agents (BCA). 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 Rodrigues is of great agricultural, commercial and strategical interests for the country.