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First records of Phytoseiidae (Acari: Mesostigmata) from one island of the Comoros archipelago

Kreiter, Serge1; Payet, Rose-My2; Fillâtre, Jacques3 and Azali, Hamza Abdou4

1✉ CBGP, Montpellier SupAgro, INRA, CIRAD, IRD, Univ Montpellier, Montpellier, France.
2CIRAD, UPR Hortsys, Station de Bassin-Plat, 97410, Saint-Pierre, Réunion, France.
3Armeflhor, 1 Chemin de l’IRFA, 97410 Saint-Pierre, Réunion, France.
4INRAPE, Moroni, Grande Comore, Union des Comores.

2018 - Volume: 58 Issue: 3 pages: 529-545

DOI: 10.24349/acarologia/20184256
ZooBank LSID: BABDD080-D2D0-46F6-8172-442298192D42

Keywords

Survey collection taxonomy systematics Grande Comore

Abstract

The Comoros Archipelago is constituted of four islands. These islands are located in the North Mozambique Channel in the Indian Ocean, one of the world’s hotspots of biodiversity. Despite this status of hotspot, only one species of Phytoseiidae was known from this Archipelago, from Mayotte: Phytoseius mayottae. No species were recorded from the three other islands. We report in this paper the results of a preliminary survey in Great Comoro or “Grande Comore” Island also called Ngazidja in the Comorian language (= Shikomori) with five species recorded.

Introduction

Several species in the family Phytoseiidae are important natural enemies controlling phytophagous mite and small insects in natural areas and crops all around the world (McMurtry and Croft 1997; McMurtry et al. 2013).

This family is widespread all over the world and consists of 2,479 valid species dispatched in three sub-families and 94 genera (Demite et al. 2017).Most of areas of the Indian Ocean constitute one of the world’s hotspots of biodiversity. The hotspot of biodiversity concept was defined by Myers (1988) in order to identify the most immediately important areas for conservation of biodiversity. These hotspots hold high endemism levels and have lost at least 70% of their original natural vegetation (Myers et al. 2000). The characterization of the phytoseiid mite diversity in these areas is thus contributing to this general topic of conservation.

Located in the Indian Ocean in the North of Mozambique Channel, Comoros Archipelago is constitutes of four islands: “Grande Comore” called also Ngazidja in Comorian language (= Shikomori), Moheli called also Mweli, Anjouan called also Nzouani, and Mayotte called also Maoré. The climate of the Comoros Archipelago, south of the Equator, is tropical, with a hot and rainy season from December to April, and a relatively cool and dry season from May to November. The average daily temperature goes from around 27°C in the warmest period (January to April), to around 23°C in the coolest months (July, August and September). The two smaller islands (Mohéli and Anjouan) are covered by hills in the interior, while Grande Comore has the volcano Karthala, 2,360 meters high. This main island is the rainiest. On Mount Karthala, even 5,000 mm of rain / year fall, while the capital Moroni, which is located on the windward side receives 2,700 mm of rain / year. On the Comoros there are numerous tropical ecosystems that are primarily dependent on the altitude. Many kinds of tropical plants can be found, large numbers of which are endemic. Like most islands, the diversity of the local flora suffers from two pressures, on one hand the reduction of available space caused by the reduction of biotopes due to the invasion of humans in wildest areas and on the other hand, the invasion of exotic plant species such as guava trees.

Presently, only one species of Phytoseiidae is known from this part of the world, from Mayotte: Phytoseius mayottae Schicha. This species was collected by Jean Gutierrez and described by Schicha (1984). No species are recorded from the three other islands.

We report in this paper result of a preliminary survey in Grande Comore Island (Ngazidja).

Material and methods

The survey took place in “Grande Comore” (or Ngazidja) in February 2017. Plant inhabiting mites were collected for this preliminary survey only from various crops in two locations. Mites were directly collected from leaves with a fine brush and then transferred into small plastic vials containing 70% and 98% ethanol. Plant species were identified by Jacques Fillâtre (Armeflhor).

Mites in vials with 70% ethanol were then all mounted on slides using Hoyer’s medium and all identified using a phase and interferential contrast microscope (Leica DMLB, Leica Microsystèmes SAS, Nanterre, France). Mites in vials with 98% ethanol will be used for barcoding (in progress).

Morphological characters were measured using a graduate eyepiece (Leica, see above). Chant and McMurtry’s (1994, 2007) concepts of the taxonomy for the family Phytoseiidae and the world catalogue database of Demite et al. (2017) were used for faunistical and biogeographical aspects. The chaetotaxy terminologies used in this paper followed those proposed by Lindquist and Evans (1965) as adapted by Rowell et al. (1978) for Phytoseiidae for dorsal and by Chant and Yoshida-Shaul (1991) for ventral idiosomal setae, respectively. Adenotaxy and poroidotaxy terminologies are those proposed by Athias-Henriot (1975).

Numbers of teeth on the fixed and movable cheliceral digits do not include the respective apical teeth. Setae not referred to in the Results section should be considered as absent.

All measurements are given in micrometers (μm) and presented as the mean in bold followed by the range in parenthesis. All individuals collected were measured.

Specimens of each species are deposited in the mite collections of Montpellier SupAgro conserved in UMR CBGP INRA/IRD/CIRAD/SupAgro.

The following abbreviations are used in this paper for morphological characters: dsl = dorsal shield length; dsw = dorsal shield width; lisl = Largest inguinal sigilla (= “metapodal plate”) length; lisw = Largest inguinal sigilla (= “metapodal plate”) width; sisl = smallest inguinal sigilla(= “metapodal plate”) length; vsl = ventrianal shield length (or ventral shield length for Iphiseisus degenerans); asl = anal shield length; vsw ZV2 and vsw anus = ventrianal shield width at ZV2 level and at anus level; scl = spermatheca cervix length; scw = spermatheca cervix width; fdl = fixed digit length; mdl = movable digit length.

The following abbreviations are used in this paper for institutions: Armeflhor = Association Réunionnaise pour la Modernisation de l’Economie Fruitière, Légumière et HORticole; CBGP = Centre de Biologie pour la Gestion des Populations; CIRAD = Centre International de Recherche Agronomique pour le Développement; INRA = Institut National de la Recherche Agronomique; 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; UPR = Unité Propre de Recherche.

Results and discussion

A total of five species have been collected and identified, four species of the sub-family Amblyseiinae and one species of the sub-family Phytoseiinae. Three of them are biological control agents, may have great interest for agriculture of this part of the world and some data from the literature are provided here.

Subfamily Amblyseiinae Muma

Amblyseiinae Muma, 1961: 273.

Tribe Amblyseiini Muma

Amblyseiini, Muma, 1961: 68.

Subtribe Amblyseiina Muma

Amblyseiina Muma, 1961: 69.

Genus Amblyseius Berlese

Amblyseius Berlese, 1914: 143.

Amblyseius herbicolus (Chant)

Typhlodromus (Amblyseius) herbicolus Chant, 1959: 84;

Amblyseius (Amblyseius) herbicolus, Muma 1961: 287;

Typhlodromus herbicolus, Hirschmann, 1962: 23;

Amblyseius herbicolus, Moraes et al., 1986: 14; 1989: 79; 2004: 27; Chant & McMurtry, 2004: 209; 2007: 78;

Amblyseius deleoni Muma & Denmark, 1970: 68 (synonymy according to Daneshvar & Denmark, 1982; Denmark & Muma 1989);

Amblyseius giganticus Gupta, 1981: 33 (synonymy according to Gupta, 1986);

Amblyseius impactus Chaudhri, 1968, 553 (synonymy according to Daneshvar & Denmark, 1982; Denmark & Muma, 1989);

Amblyseius (Amblyseialus) thermophilus Karg, 1991: 12 (synonymy according to El-Banhawy & Knapp, 2011 and to Demite et al., 2017);

Typhlodromus (Amblyseius) amitae Bhattacharyya, 1968: 677 (synonymy according to Denmark & Muma, 1989).

Amblyseius herbicolus (Chant) is the second most abundant phytoseiid mites on coffee plants (Coffea arabica L.) in Brazil, associated with Brevipalpus phoenicis (Geijskes) (Acari: Tenuipalpidae), vector of the coffee ring spot virus. Amblyseius herbicolus was found to be an efficient predator of the coffee ring spot mite (Reis et al. 2007).

Amblyseius herbicolus is also found associated with the broad mite, Polyphagotarsonemus latus Banks in crops such as chili pepper (Capsicum annuum L.) in Brazil. This species has also a good potential for controlling P. latus. RodrÍguez-Cruz et al. (2013) have studied biological, reproductive and life table parameters of A. herbicolus on three different diets: broad mites, castor bean pollen (Ricinus communis L.) and sunn 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 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).

Specimens examined — Moroni, Adoudja (long. 11°41′S, lat. 43°15′E, alt. 100 m), 1 ♀ + 1 immature on Alocasia macrorrhiza (L.) G. Don (Araceae), 2-02-2017; 1 ♀ + 2 immatures on Morinda citrifolia L. (Rubiaceae), 2-02-2017.

Previous record — Large distribution worldwide. This species is mentioned from Mozambique, La Réunion Island, Kenya, Tanzania for the closest places.

Remarks (Table 1) — Measurements of the two females collected fit very well with the measurements reported literature, except for greater dimension of the ventrianal shield and a longer spermatheca for specimens from Grande Comore.

Table 1. Comparisons of character measurements of female specimens of Amblyseius herbicolus collected in different locations (Localities followed by the number of specimens measured between brackets)
Tribe Euseiini Chant and McMurtry

Euseiini Chant & McMurtry, 2005b: 191.

Subtribe Euseiina Chant and McMurtry

Euseiina Chant & McMurtry, 2005b: 209.

Genus Euseius Wainstein

Amblyseius (Amblyseius) section Euseius, Wainstein, 1962: 15; Euseius De Leon, 1967: 86.

Euseius baetae (Meyer & Rodrigues)

Amblyseius baetae (Meyer & Rodrigues, 1966): 28;

Euseius baetae (Meyer & Rodrigues), Moraes et al., 2001a: 11; Moraes et al., 1986: 37; 2004: 62; Chant & McMurtry 2005b: 215; 2007: 120; El Banhawy & Knapp, 2011: 36;

Euseius kangwanensis Ueckermann & Loots , 1988: 85 (synonym according to Ueckermann & Loots, 1988; Moraes et al., 2001b; El-Banhawy & Knapp, 2011).

The 200 species of the genus Euseius are considered as Type IV species, polliniphagous generalists (McMurtry and Croft 1997; McMurtry et al. 2013) and Euseius baetae is supposed to belong to that Type IV. The biology of E. baetae is however totally unknown.

Specimens examined — Mdé, INRAPE (long. 11°41′S, lat. 43°14′E, alt. 50 m), 1 ♀ on Manihot esculenta Crantz (Euphorbiaceae), 2-02-2017; Moroni, Adoudja (long. 11°41′S, lat. 43°15′E, alt. 100 m), 2 ♀♀ on Plectranthus scutellarioides (L.) R.Br. (Lamiaceae), 2-02-2017; 1 ♀ on Alocasia macrorrhizos (L.) G.Don (Araceae), 2-02-2017.

Previous record — Congo, Kenya, Malawi, Mozambique, South Africa.

Remarks (Table 2) — Measurements of the 4 ♀♀ fit well with the measurements from the literature with slightly shorter dimensions in general.

Table 2. Comparisons of character measurements of female specimens of Euseius baetae collected in different locations (Localities followed by the number of specimens measured between brackets)
Genus Iphiseius Berlese

Iphiseius Berlese, 1916: 33; Chant & McMurtry, 2005b: 217; 2007: 123.

Iphiseius degenerans (Berlese)

Seius degenerans (Berlese, 1889): 9;

Amblyseius (Iphiseius) degenerans, Muma, 1961: 288;

Typhlodromus degenerans, Hirschmann, 1962: 2;

Iphiseius (Iphiseius) degenerans, Pritchard & Baker 1962: 299;

Amblyseius degenerans, Zaher, 1986: 99; Northcraft, 1987: 521; Papadoulis & Emmanouel, 1991: 36;

Iphiseius degenerans, Berlese, 1921: 95; Evans, 1954: 518; Moraes et al., 1986: 61; 2004: 92; Chant & McMurtry, 2005b: 215; 2007: 125;

Iphiseius martigellus El-Badry, 1968: 325 (synonymy according to Chant & McMurtry, 2005; El-Banhawy & Knapp, 2011).

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 type-III 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 nec (Klein) in the Mediterranean region (Fantinou et al. 2012).

Iphiseius degenerans preys on Oligonychus perseae Tuttle, Baker & Abbatiello outside the webbed nests. Although I. degenerans contribution to O. perseae biocontrol can be limited, it needs to be assessed, also taking into account the importance of alternative food source (e.g. Castor oil pollen) for predator population growth (Zappala et al. 2015).

Specimens examined — Mdé, INRAPE (long. 11°41′S, lat. 43°14′E, alt. 50 m), 7 ♀♀ + 4 ♂♂ on Ricinus communis L. (Euphorbiaceae), 2-02-2017.

Previous record — Numerous countries in Northern and Southern Africa (Demite et al. 2017), in Mediterranean area (Cyprus, Greece, Italy, Portugal), in Near East or Middle East (Egypt, Israel, Lebanon, Saudi Arabia, Syria, Turkey, Yemen), in Europe (Georgia), in South America (Brazil) and in North America (USA in California, Florida, Georgia, New Hampshire).

Remarks (Tables 3 and 4) — Measurements of the 7 ♀♀ + 4 ♂♂ fit well with measurements of specimens reported in the literature for closest countries, except width of the ventral and the anal shields of the female and JV5 which is more than 40 % longer.

Table 3. Comparisons of character measurements of female specimens of Iphiseius degenerans collected in different locations (Localities followed by the number of specimens measured between brackets)

Table 4. Comparisons of character measurements of male specimens of Iphiseius degenerans collected in different locations (Localities followed by the number of specimens measured between brackets)
Tribe Neoseiulini Chant and McMurtry

Neoseiulini Chant & McMurtry, 2003a: 6.

Genus Neoseiulus Hughes

Neoseiulus Hughes, 1948: 141.

Neoseiulus longispinosus (Evans)

Typhlodromus longispinosus Evans, 1952: 413; Evans, 1953: 465; Womersley, 1954: 177; Ehara, 1958: 55;

Typhlodromus (Amblyseius) longispinosus, Chant, 1959: 74;

Amblyseius longispinosus, Corpuz and Rimando, 1966: 129; Schicha, 1975: 103;

Neoseiulus longispinosus, Moraes et al., 1986: 85; 2000: 245; 2004: 129; Chant & McMurtry 2003a: 37; 2007: 29.

This species is distributed in many countries of the world, mainly in tropical areas, especially in Guadeloupe and other Islands of the French Antilles (Moraes et al. 2000; Mailloux et al. 2010; Kreiter et al. 2013; Kreiter et al. in press).

Neoseiulus longispinosus, a type II phytoseiid predatory mite (McMurtry et al. 2013), has received increasing attention in Asia for the control of spider mites since 2010 (Nusartlert et al. 2011). It can develop on different tetranychid species of the genera Eutetranychus, Oligonychus, and Tetranychus (Nusartlert et al. 2011). Several studies demonstrated the potential of the predatory mite to control spider mite outbreaks including Oligonychus coffeae (Nietner) on tea (Rahman et al. 2013), Stigmaeopsis nanjingensis (Ma & Yuan) on bamboo in China (Zhang et al. 1999) or Eotetranychus cendanai Rimando in greenhouse crops (Thongtab et al. 2001). In addition, N. longispinosus was also found to have a great potential for practical applications due to its resistance or tolerance to agricultural chemicals (Zhang et al. 1996).

Thus, the biology of this species has been studied mostly for pest control purposes including side effects of miticides (Bin Ibrahim and Tan 2000). The activity, feeding, development, predation, cannibalism, intra-guild predation and behaviour have been extensively studied by several authors (Croft et al. 1999a, b; Schausberger and Croft 1999a, b; 2000a, b; Blackwood et al. 2001). It was found very rarely in Mascareignes area except in a study on companion plants in citrus orchards in La Réunion (Le Bellec, unpublished data). This species seems to be more common on grasses of the lower vegetation, especially Fabaceae with populations of tetranychid mites. However, the recent results of Huyen et al. (2017) show that at least in controlled laboratory conditions the predatory mite N. longispinosus is a potential biological control agent against the citrus red spider mite P. citri.

Previous Records — Australia, China (Fujian, Guangdong, Guangxi, Hainan, Yunnan), Cuba, Dominican Republic, Guadeloupe, Egypt, Hawaii, Hong-Kong, India, Indonesia, Japan, Les Saintes, Malaysia, Marie-Galante, Martinique, New Zealand, Nicaragua, Pakistan, Papua New Guinea, Philippines, Russia, South Korea, Sri Lanka, Taiwan, Thailand, USA (Florida), Vietnam.

Specimens examined — Moroni, Adoudja (long. 11°41′S, lat. 43°15′E, alt. 100 m), 1 ♀ on Plectranthus scutellarioides (L.) R. Br. (Lamiaceae), 2-02-2017.

Remarks (Table 5) — Measurements of the single female collected show that most of the setae lengths are 7 to 15 % longer, except j6, J2, J5, and Z4. All ventral, spermathecal and cheliceral dimensions agree well except ventrianal shield length and width at the level of anus and JV5 which are longer.

Table 5. Comparisons of character measurements of female specimens of Neoseiulus longispinosus collected in different locations (Localities followed by the number of specimens measured between brackets)
Subfamily Phytoseiinae Berlese

Phytoseiini Berlese, 1913: 3; Phytoseiinae, Vitzthum, 1941: 768.

Genus Phytoseius Ribaga

Phytoseius Ribaga, 1904: 177.

Phytoseius amba Pritchard & Baker

Phytoseius (Pennaseius) amba Pritchard & Baker 1962: 224; Blommers, 1976: 85;

Phytoseius (Phytoseius) amba, Denmark, 1966: 49;

Typhlodromus (Pizytoseius) amba, Van der Merwe, 1968: 101;

Phytoseius amba, Swirski & Ragusa, 1978: 408;

Pennaseius amba, Matthysse & Denmark, 1981: 352;

Phytoseius amba, Moraes et al., 1986: 210; 2004: 232; Chant & McMurtry, 2007: 129.

Species of the genus Phytoseius are supposed to belong to the Type III species (McMurtry and Croft 1997; McMurtry et al. 2013), i.e. a polyphagous generalist predator. However, the biology of Phytoseius amba remains totally unknown.

Specimens examined — Mdé, INRAPE (long. 11°41′S, lat. 43°14′E, alt. 50 m), 1 ♀ on Annona muricata L. (Annonaceae), 2-02-2017.

Previous Records — Benin, Burundi, Cameroon, Cape Verde, DR Congo, Kenya, Madagascar Island, Malawi, Mozambique, Nigeria, Reunion Island, Rwanda, Senegal, South Africa, Zambia, Zimbabwe.

Remarks (Table 6) — The setae lengths seem very variable in this species following data of the literature. Measurements of the single adult female (Table 6) 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 the exception of longer j3 and z3, shorter st5-st5, ventrianal shield length and width at the level of anus and macrosetae of the basitarsus and telotarsus.

Table 6. Comparisons of character measurements of female specimens of Phytoseius amba collected in different locations (Localities followed by the number of specimens measured between brackets)
Conclusion

Only one species was known before 2017 from the Comoros Archipelago (Schicha 1984). After this preliminary survey conducted in only two locations, the number of species known from Comoros Islands is now of six; four Amblyseiinae: Amblyseius herbicolus, Euseius baetae, Iphiseius degenerans, Neoseiulus longispinosus; and two Phytoseiinae: Phytoseius amba and Phytoseius mayottae. No Typhlodrominae were found until now. This is still a low number of species and from a tropical island, one could have expected a higher number, even from only two locations. The low number of species could be explained by the fact that samplings were made in crops more or less disturbed and not in wild areas.

Some of the species collected during this survey have interesting potential for biological control, especially A. herbicolus, I. degenerans and N. longispinosus.This must be underlined as new regulations on importation of macro-organisms are proposed in a lot of countries and specifically for over-sea territories for countries like France that have very far tropical territories. Therefore it is impossible to import and of course to sell and use exotic species if they are not indigenous in the territory. An importation permit must be requested, but it is expensive and chances to obtain are generally very low (Kreiter et al. 2016). The knowledge of the biodiversity, especially of efficient biological control agents from oversea territories, not only for conversation purposes but also for agricultural and economical ones, is so of a considerable importance.

Acknowledgements

Thanks are due to Mr. Hadji MOUIGNI (from INRAPE) who has helped Jacques Fillâtre (Armeflhor) to collect mites in Grande Comore Island and the two anonymous reviewers for improvement of the paper.

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2017-11-28
Date accepted:
2018-01-10
Date published:
2018-06-01

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Tixier, Marie-Stéphane

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© 2018 Kreiter, Serge; Payet, Rose-My; Fillâtre, Jacques and Azali, Hamza Abdou

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