# Distribution and biological features of Typhlodromus (Anthoseius) recki (Acari: Phytoseiidae) on Tetranychus urticae, T. evansi (Acari: Tetranychidae) and Aculops lycopersici (Acari: Eriophyidae)

Marie-Stéphane Tixier, Martial Douin, Oliva Rocio, Lucia Gonzalez, Benjamin Pount, Serge Kreiter

► To cite this version:

Marie-Stéphane Tixier, Martial Douin, Oliva Rocio, Lucia Gonzalez, Benjamin Pount, et al.. Distribution and biological features of Typhlodromus (Anthoseius) recki (Acari: Phytoseiidae) on Tetranychus urticae, T. evansi (Acari: Tetranychidae) and Aculops lycopersici (Acari: Eriophyidae). Acarologia, 2020, 60 (4), pp.684-697. 10.24349/acarologia/20204396. hal-02953980

HAL Id: hal-02953980

https://hal.science/hal-02953980

Submitted on 1 Jul 2021

HAL is a multi-disciplinary open access
archive for the deposit and dissemination of sci-
entific research documents, whether they are pub-
lished or not. The documents may come from
teaching and research institutions in France or
abroad, or from public or private research centers.

L'archive ouverte pluridisciplinaire HAL, est
destinée au dépôt et à la diffusion de documents
scientifiques de niveau recherche, publiés ou non,
émanant des établissements d'enseignement et de
recherche français ou étrangers, des laboratoires
publics ou privés.

<figure><img src="image_1.png" /></figure>

Distributed under a Creative Commons Attribution 4.0 International License
<figure><img src="image_2.png" /></figure>

Acarologia
Open Science in Acarology

<figure><img src="image_3.png" /></figure>

Acarologia

A quarterly journal of acarology, since 1959
Publishing on all aspects of the Acari

All information:
http://www1.montpellier.inra.fr/CBGP/acarologia/
acarologia-contact@supagro.fr

<figure><img src="image_4.png" /></figure>

OPEN ACCESS

Acarologia is proudly non-profit,
with no page charges and free open access

Please help us maintain this system by
encouraging your institutes to subscribe to the print version of the journal
and by sending us your high quality research on the Acari.

Subscriptions: Year 2021 (Volume 61): 450 €
http://www1.montpellier.inra.fr/CBGP/acarologia/subscribe.php

Previous volumes (2010-2020): 250 € / year (4 issues)
Acarologia, CBGP, CS 30016, 34988 MONTFERRIER-sur-LEZ Cedex, France
ISSN 0044-586X (print), ISSN 2107-7207 (electronic)

The digitalization of Acarologia papers prior to 2000 was supported by Agropolis Fondation under the reference ID 1500-024 through the « Investissements d'avenir » programme
(Labex Agro: ANR-10-LABX-0001-01)

<figure><img src="image_5.png" /></figure>

<figure><img src="image_6.png" /></figure>

Acarologia is under **free license** and distributed under the terms of the
Creative Commons-BY.
Acarologia

Open Science
in Acarology

# Distribution and biological features of *Typhlodromus (Anthoseius) recki* (Acari: Phytoseiidae) on *Tetranychus urticae*, *T. evansi* (Acari: Tetranychidae) and *Aculops lycopersici* (Acari: Eriophyidae)

Marie Stephane Tixier IDª, Martial Douinª, Oliva Rocioᵇ, Lucia Gonzalezª, Benjamin Pountª, Serge Kreiter IDª

## Original research

### ABSTRACT

The mite family Phytoseiidae contains predatory species used in biological control. However, among the 2,521 valid species, only a few are presently considered for pest management. The study focuses on a species, frequently observed in agrosystems, but whose biology is almost totally unknown: *Typhlodromus (Anthoseius) recki*. The objectives were to assess its distribution and to determine under laboratory conditions: (i) the development of three populations fed on three tomato pests (*Tetranychus urticae*, *T. evansi*, *Aculops lycopersici*), (ii) the dispersion along the tomato stem, and (iii) the dispersion from mint to infested tomato leaf discs. Based on its distribution, this species seems to be adapted to Mediterranean climate, and is preferentially found on Boraginaceae, Solanaceae, Asteraceae and Lamiaceae. Results show that *T. (A.) recki* is a generalist predator, with good performance regarding the number of prey consumed. Differences were observed between the populations considered; one population out of the three tested shows even a higher mean consumption of *T. urticae* than that recorded for *Neoseiulus californicus* and *N. cucumeris*. It is attracted by food source and is able to walk along the tomato stem. These results are encouraging enough to consider *T. (A.) recki* as a good natural enemy candidate for biological control (especially based on biodiversity conservation). Further experiments should be developed to test the predatory ability of this species at larger scale (entire tomato plants and tomato fields or greenhouses).

**Keywords** feeding habits; predator; biological control; tomato; distribution

### Introduction

Mites of the family Phytoseiidae are predators, and some species are used for controlling pest mites and small insects, in various crops all over the world (Gerson *et al.* 2003; McMurtry *et al.* 2013). This family contains 2,521 valid species (Demite *et al.* 2020) but only a few are presently used in biological control, probably because of little knowledge on the biological features of most species. We thus hypothesise that much more species than the 20-30 species presently known for their predatory efficiency could be exploited for biological control issues (Van Lenteren 2012; Van Lenteren *et al.* 2017). Phytoseiidae mites are naturally occurring in crops and uncultivated areas (Moraes *et al.* 1986). Most Phytoseiidae species are generalist predators (McMurtry & Croft 1997; McMurtry *et al.* 2013); they feed on prey and also on pollen,

Received 20 May 2020
Accepted 28 September 2020
Published 30 September 2020

Corresponding author
Marie Stephane Tixier ID:
marie-stephane.tixier@supagro.fr

Academic editor
Tsolakis, Haralabos

DOI
10.24349/acarologia/20204396

ISSN 0044-586X (print)
ISSN 2107-7207 (electronic)

Copyright
Tixier M. S. et al.

Distributed under
Creative Commons CC-BY 4.0

OPEN ACCESS

<footnote>ªCBGP, Institut Agro, INRA, CIRAD, IRD, Univ. Montpellier, France, 755 Avenue du Campus Agropolis, CS 30016, 34988 Montferrier-sur-Lez cedex, France.</footnote>

<footnote>ᵇUniversidad de Almería, Carretera Sacramento s/n, 04120 La Cañada de San Urbano, Almería, Spain.</footnote>
plant exudates, sometimes plant tissues, fungi, etc. Their occurrence and diversity are strongly affected by plant phylloplane features (Karban et al. 1995; Kreiter et al. 2002; Schmidt 2004; Tixier 2018). Tomato plants have specific morphological and chemical characteristics that can act as a selective filter on Phytoseiidae communities. Trichomes on tomato leaves and stems hinder mite dispersal and development, Phytoseiidae get stuck on the sticky trichomes and die (Kennedy 2003; Simmons and Gurr 2005; Sato et al. 2011; Van Houten et al. 2013a, b). Alkaloids contained in tomato and ingested by prey adapted to this plant, can also be toxic for non-adapted predators (Koller et al. 2007; Ferrero et al. 2014a, b). However, some studies report the presence of Phytoseiidae on tomatoes (i.e. Moraes et al. 1986; Tixier et al. 2020). Studies on *Phytoseiulus longipes* Evans show that strains of this species collected on Solanaceae in Argentina and Brazil are adapted to tomato and can control both *Tetranychus urticae* (Koch) and *T. evansi* Baker & Pritchard on this crop (Furtado et al. 2007; Ferrero et al. 2014a, b). However, as *P. longipes* is endemic to the Neotropical region, the introduction of this species in Europe is confronted with regulatory and environmental problems. In a recent study, we showed that *Typhlodromus (Anthoseius) recki* Wainstein is one of the species most frequently reported on Solanaceae in Europe (Tixier et al. 2020). It is also observed on plants with high trichome density, or presenting spiny and sticky trichomes (especially on plants of the families Lamiaceae and Boraginaceae) (Moraes et al. 1986; Swirski and Amitai 1997; Tixier et al. 2020). Little is known on the biology of *T. (A.) recki*; it has been reported on tomatoes, feeding on mites and thrips, in Turkey and Iran (Hajizadeh et al. 2006; Kumral and Cobanoglu 2015a, b). In the present study, a series of experiments was carried out to characterise the feeding and dispersal habits of *T. (A.) recki*. Furthermore, its current distribution was also analysed.

# Materials and methods

## Distribution of *Typhlodromus (Anthoseius) recki*

Information on the geographic distribution and plant occurrence was retrieved from 59 publications (from 1958 to 2018) reporting *T. (A.) recki* occurrence (database available on request).

## Plant Nomenclature

We followed the Angiosperm Phylogeny Group III's nomenclature (2009) for family, genus and species names.

## Feeding habits of *Typhlodromus (Anthoseius) recki* in the laboratory

The aim was to characterise the ability of *T. (A.) recki* to feed on three prey species. Three populations of *T. (A.) recki* collected in France on Solanaceae and Lamiaceae were considered (Table 1). Two "control" species, commonly used in biological control (Knapp et al. 2018), both collected on Solanaceae in France (Table 1), were also studied: *Neoseiulus californicus* (McGregor) and *N. cucumeris* (Oudemans). The predatory mites were maintained in rearing units, as described by McMurtry and Scriven (1965). Pollen of *Typha* sp. was added daily as food source.

Feeding ability was assessed on three prey species: (i) *T. evansi* collected on tomato, *Solanum lycopersicum* L., in a greenhouse at Saint-Jeannet (Alpes-Maritimes, South-East France) in October 2007 and then reared in the laboratory on *Solanum nigrum* L., (ii) *T. urticae* collected in Montpellier in 2010 and maintained since then on *Phaseolus vulgaris* L. (var. Contender) in a greenhouse and (iii) *Aculops lycopersici* (Tryon) sent by Koppert BV (Netherlands) in 2017 and then reared on entire plants of *S. nigrum* in the laboratory.

Three treatments were tested: (i) *T. urticae* on bean leaf discs, (ii) *T. evansi* on *S. nigrum* leaf discs and (iii) *A. lycopersici* on *S. nigrum* leaf discs. As *T. urticae* does not develop well on
S. nigrum, it was impossible to carry out the tests on this latter plant. Three tetranychid females (T. evansi or T. urticae) were placed on a leaf disc (2.5 cm in diameter) of S. nigrum or P. vulgaris var. Contender, disposed on humid cotton in a Petri dish (10 cm in diameter) to avoid mite escape. After two days, the Tetranychidae females were removed, the number of eggs laid was counted and a predatory female (young gravid female issued from the rearing units) introduced in the experimental arena. The experimental conditions were 25 °C, 70% relative humidity and 16D: 8N photoperiod. The number of prey and predator eggs was counted each day during four days as a rapid test to screen the predator efficiency.

For *A. lycopersici* experiments, *S. nigrum* leaf discs (2.5 cm in diameter), highly infested with this pest, were placed on humid cotton in a Petri dish (10 cm in diameter). One predatory female (young gravid female issued from the rearing units) was introduced and the number of eggs laid by the predator was counted daily during four days. The experimental conditions were the same as for the Tetranychidae experiments. For each prey and predator population / species treatment, 15 replicates were performed.

Analysis of variance (ANOVA) followed by mean comparison tests (Newman-Keuls) were carried out to compare the mean daily fecundity and mean daily egg consumption of the populations / species considered for each food treatment. The analyses were performed using Statistica (Statsoft France, 2010).

## Dispersal abilities of *Typhlodromus (Anthoseius) recki* in the laboratory

The experiment aims at determining "in vitro" conditions how *T. (A.) recki* disperses along tomato stems. The population of *T. (A.) recki* used was that collected in Saint-Guilhem-le-Désert (Hérault, South of France) on *Mentha suaveolens* Ehrhart (Table 1). This population was chosen because of its higher fecundity compared to the other strains, when fed on *A. lycopersici*. The experimental design consisted of a detached tomato stem (var. Marmande) (10 cm in length) placed in a vertical position within a box filled with agar (Figure 1). Agar was maintained moistened (wet cotton strips placed around the agar layer) to avoid mite escape and keep the leaf discs and the stem turgescent. A leaf tomato disc with pollen or *A. lycopersici* was placed at one extremity of the stem, whereas a tomato leaf disc without food was placed at the other extremity. Shelters (wool yarns and cardboard) were disposed on the leaf discs, as nests where Phytoseiidae use to lay eggs. The boxes were turned each day to avoid phototropism effects. Fifteen replicates were carried out for each treatment (pollen or *A. lycopersici*). For each replication, one young gravid female of *T. (A.) recki* (issued from rearing units) was placed in the middle of the stem. The position of the female, the number of eggs and immatures on each leaf disc was counted for seven days. Student t-tests were carried out to compare the mean number of eggs laid on leaf discs with and without food.

## Assessment of the ability of *T. (A.) recki* to disperse from mint to tomato under laboratory conditions

In a recent survey, high densities of *T. (A.) recki* were observed on *M. suaveolens* (Tixier et al. 2020). Thus, we wondered about the use of this plant as a reservoir (banker plant) for *T. (A.)*

<table><caption>**Table 1** Locations and plants where the populations of *T. (A.) recki*, *N. californicus* and *N. cucumeris* were collected.</caption><thead><tr><td>Species</td><td>Locality</td><td>Geographic coordinates</td><td>Host plant</td></tr></thead><tbody><tr><td>Typhlodromus (Anthoseius) recki</td><td>Saint Guilhem-Le-Désert, France</td><td>43°44'1.68"N, 3°32'59.46"E</td><td>Mentha suaveolens (Labiaceae)</td></tr><tr><td>Typhlodromus (Anthoseius) recki</td><td>Carnon, France</td><td>43°32'46.32"N, 3°58'58.8"E</td><td>Datura stramonium (Solanaceae)</td></tr><tr><td>Typhlodromus (Anthoseius) recki</td><td>Tarascon, France</td><td>43°48'28.03"N, 4°40'47.19"E</td><td>Solanum lycopersicum (Solanaceae)</td></tr><tr><td>Neoseiulus californicus</td><td>Miomo - Corsica, France</td><td>42°4437.85"N, 9°27'39.81"E</td><td>Solanum nigrum (Solanaceae)</td></tr><tr><td>Neoseiulus cucumeris</td><td>Juvignac, France</td><td>43°36'50.682"N, 3°48'36.592"E</td><td>Solanum boraniense (Solanaceae)</td></tr></tbody></table>
<figure><img src="image_7.png" /><figcaption>**Figure 1** Experimental design used to characterise the dispersal of *T. (A.) recki* along tomato stem "in vitro" conditions.</figcaption></figure>

*recki*. This experiment aims at determining under laboratory conditions if *T. (A.) recki* would disperse from mint to tomato. The population used was the same as that considered for the stem dispersal experiment (Saint Guilhem-Le-Désert). The mint leaves were collected at Saint Guilhem-Le-Désert. Five females of *T. evansi* were deposited for three days on a tomato leaf disc (var. Marmande, 2.5 cm in diameter). The tomato leaf disc was cut into two equal parts. Each tomato half-disc was placed adjacently to a half-leaf disc of mint (same dimension as the tomato half-disc) containing two females of *T. (A.) recki*. The mint leaf discs were checked to avoid prey presence. The number of *T. evansi* (females, eggs and immatures) and the number of Phytoseiidae (females, eggs and immatures) on each half-disc were daily counted during 7 days and 15 replications were performed. Student t-tests were carried out to compare the number of *T. evansi* and *T. (A.) recki* on the two half discs through the time. A Chi2 test was carried out to compare the percentages of females, eggs and eggs+immatures on each half-disc, through the time. The analyses were performed using Statistica (Statsoft France 2010).

**Results and discussion**

**Distribution of Typhlodromus (Anthoseius) recki**

*Typhlodromus (A.) recki* is reported from 22 countries, mainly in the Southern West-Palearctic region (Figure 2) under Mediterranean climate. It is reported 421 times on 213 plant species, belonging to 138 genera and 51 families. It is recorded less than 5 times on 37 plant families, and the highest record rates were observed on six plant families (56% of reports): Asteraceae (61 reports), Lamiaceae (50 reports), Rosaceae (40 reports), Boraginaceae (36 reports), Fabaceae (26 reports) and Solanaceae (25 reports). This might suggest close relationships between this species and those plants. However, because of no close phylogenetic relationship among these plant families, such occurrence seems not related to evolutionary aspects, as also stated by Tixier (2018) and Tixier *et al.* (2020). *Typhlodromus (A.) recki* is reported less than 5 times on 123 plant genera. The highest number of reports (19% of total reports) is observed on species of the genera *Solanum* (19 reports), *Echium* (17 reports), *Vitis* (14 reports), *Prunus* (12 reports) and *Salvia* (11 reports). Again, these genera are not phylogenetically close, and *T. (A.) recki* occurrence seems not related to plant support evolution. Those data provide elements on the “probability” to retrieve *T. (A.) recki* on some plant species, although we are aware that the recorded occurrences do not exactly reflect the real distribution.
<figure><img src="image_8.png" /><figcaption>**Figure 2** Map showing the present distribution of *T. (A.) recki*.</figcaption></figure>

Feeding habits of *Typhlodromus (Anthoseius) recki* in the laboratory

Tetranychus urticae and bean

The average number of eggs laid over 4 days by females of *T. (A.) recki*, *N. cucumeris* and *N. californicus* was significantly different (*P* = 0.0008) (Table 2). This was due to the significantly higher fecundity of *N. californicus* (1.4 eggs/ day/ female) as no difference was observed between the three populations of *T. (A.) recki* and *N. cucumeris*. Those differences were not significant at days 1 (*P*=0.07) and 2 (*P*=0.06) but were significant at days 3 (*P*<0.001) and 4 (*P*=0.001) (Table 4, Figure 3a). For days 3 and 4, the fecundity of *N. californicus* was significantly higher than that of *N. cucumeris* and *T. (A.) recki*. Differences in fecundity through the time were only observed for *N. californicus*, a higher fecundity being observed at days 3 and 4 than at days 1 and 2 (Table 4). Even if not significant, we can note that among the *T. (A.) recki* populations, the highest daily fecundity was observed for the population collected on *Datura stramonium* L. (0.95 eggs/ day/ female) and the lowest for the population collected on *S. lycopersicum* L. (0.57 eggs/ day/ female) (Table 2).

The number of *T. urticae* eggs consumed by the populations/species was significantly different (*P* = 0.02) (Table 3). The highest mean consumption was observed for *T. (A.) recki* collected on *S. lycopersicum* (18.47 eggs consumed / day) and the lowest for *N. californicus* (10.67 eggs consumed / day) and *T. (A.) recki* collected on *M. suaveolens* (11.69 eggs consumed / day). The numbers of eggs consumed were significantly different at day 1 (*P*<0.001), day 3 (*P*=0.05) and day 4 (*P*<0.001) (Table 4). At day 1, *T. (A.) recki* from *S. lycopersicum* showed the highest consumption (40.5 eggs consumed) and *N. californicus* the lowest (6.0
<figure><img src="image_9.png" /><figcaption>N° eggs laid/female feeding on *T. evansi*</figcaption></figure>

<figure><img src="image_10.png" /><figcaption>N° eggs consumed /female feeding on *T. urticae*</figcaption></figure>

<figure><img src="image_11.png" /><figcaption>N° eggs consumed /female feeding on *T. evansi*</figcaption></figure>

<figure><img src="image_12.png" /><figcaption>N° eggs laid/female feeding on *A. lycopersici*</figcaption></figure>

<figure><img src="image_13.png" /></figure>

**Figure 3** Cumulated number of eggs laid through the time by *T. (A.) recki* (D: collected on *Datura stramonium*, S: collected on *Solanum lycopersicum*, M: collected on *Mentha suaveolens*), *N. californicus* and *N. cucumeris* when fed with (a) *T. urticae*, (b) *T. evansi* and (e) *A. lycopersici*. Number of prey eggs consumed by *T. (A.) recki*, *N. californicus* and *N. cucumeris* when fed with (c) *T. urticae* and (d) *T. evansi*.
eggs consumed). At day 3 and 4, the highest values were observed for *N. californicus* (Table 4). Egg consumption significantly decreased from day 1 to day 4, except for *N. californicus* for which they increased (Table 4). The mean number of eggs consumed during 4 days was the highest (73.9) for *T. (A.) recki* from *S. lycopersicum*. For the other populations of *T. (A.) recki*, this consumption was about 50 eggs (Figure 3c).

There are no data on biological features of *T. (A.) recki* in literature. Differences between the three populations were observed but they were relatively low, except for the population collected on *S. lycopersicum* that consumed significantly more *T. urticae* eggs than the two others. Globally, *T. (A.) recki* has low transformation rates: many eggs of *T. urticae* need to be consumed to produce one Phytoseiidae egg (especially for the population collected on *S. lycopersicum*). These results are in accordance with biological features (observed in experimental conditions comparable to the present ones: 18 °C-25°C, 65%-75% HR and 16D:8N - 18D:6N) of other generalist Phytoseiidae species. For instance, Kasap (2010) showed for *Kampimodromus aberrans* (Oudemans), a low consumption rate (2.85 eggs / day) of *T. urticae* and a mean fecundity of one egg per day. Zemek (1993) indicated a low fecundity for *Typhlodromus (Typhlodromus) pyri* Scheuten when fed with *T. urticae* (0.72 eggs / day). Basheer *et al.* (2014) observed for *Typhlodromus (Typhlodromus) athiasae* Porath & Swirski, a daily consumption of 10 *T. urticae* eggs and a mean fecundity of 1.42 eggs/day. The consumption and oviposition rates reported in the literature for *N. californicus* are variable depending on the populations considered and the environmental conditions. Globally, the mean fecundity is about 2 eggs/female/day (Gotoh *et al.* 2004; Lebdi-Grissa *et al.* 2005; Canlas *et al.* 2006; Rhamani *et al.* 2009; Marafeli *et al.* 2014), but lower values were observed by Hatherly *et al.* (2005) (0.62 eggs/day) and Castagnoli *et al.* (2001) (1.46 eggs / day). The fecundity here observed (1.61 eggs/day) show an intermediary value; such differences might be due to strain effects (Castagnoli *et al.* 2001). Regarding *T. urticae* egg consumption, the present results (10.7 eggs consumed/ female/ day) are similar to those obtained for several strains of *N. californicus* by Castagnoli *et al.* (2001) (9.09 - 11.41) and a bit lower than the data obtained by Canlas *et al.* (2006). For *N. cucumeris*, the fecundity here observed is much lower than that reported by Al-Azzazy *et al.* (2018). The daily *T. urticae* egg consumption (14.52) is in accordance with values obtained by Li & Zhang (2016) and Zheng *et al.* (2017) and higher than those reported by Al-Azzazy *et al.* (2018).

## Tetranychus evansi on Solanum nigrum

The number of eggs laid by the three populations of *T. (A.) recki*, *N. cucumeris* and *N. californicus* was significantly different (*P* = 0.016) (Table 2). The highest fecundity was observed for *T. (A.) recki* from *D. stramonium* L. (0.3 eggs / female/ day) and the lowest for

<table><caption>**Table 2** Mean daily fecundity (± standard error) of populations *T. (A.) recki* (D: collected on *Datura stramonium*, S: collected on *Solanum lycopersicum*, M: collected on *Mentha suaveolens*), *N. californicus* and *N. cucumeris* when the females are feeding on eggs of *T. urticae* (on bean leaf discs), of *T. evansi* (on *S. nigrum* leaf discs) and all stages of *A. lycopersicum* (on *S. nigrum* leaf discs).</caption><thead><tr><th rowspan="2"></th><th colspan="2">Daily fecundity per female</th><th colspan="2">Daily fecundity per female</th><th colspan="2">Daily fecundity per female</th><th rowspan="2">P value</th></tr><tr><th>Bean/T. urticae</th><th></th><th>S. nigrum / T. evansi</th><th></th><th>S. nigrum / A. lycopersici</th><th></th></tr></thead><tbody><tr><td><i>N. californicus</i></td><td>1.40 ± 1.41</td><td>a</td><td>A</td><td>0.05 ± 0.22</td><td>b</td><td>C</td><td>0.83 ± 0.79</td><td>B 0.0001</td></tr><tr><td><i>N. cucumeris</i></td><td>0.92 ± 0.76</td><td>b</td><td>A</td><td>0.18 ± 0.39</td><td>ab</td><td>B</td><td>0.89 ± 0.78</td><td>A 0.00001</td></tr><tr><td><i>T. (A.) recki</i> D</td><td>0.95 ± 0.90</td><td>b</td><td>A</td><td>0.30 ± 0.46</td><td>a</td><td>B</td><td>0.35 ± 0.49</td><td>A 0.00001</td></tr><tr><td><i>T. (A.) recki</i> S</td><td>0.57 ± 0.50</td><td>b</td><td>A</td><td>0.07 ± 0.26</td><td>ab</td><td>B</td><td>0.56 ± 0.81</td><td>A 0.00002</td></tr><tr><td><i>T. (A.) recki</i> M</td><td>0.75 ± 0.73</td><td>b</td><td>A</td><td>0.25 ± 0.52</td><td>ab</td><td>B</td><td>1.00 ± 0.81</td><td>A 0.00002</td></tr><tr><td>P value</td><td colspan="2">0.0008</td><td colspan="2">0.016</td><td colspan="2">0.055</td><td colspan="2"></td></tr></tbody></table>

<footnote>* Small different letters correspond to significant differences between the populations / species considered (Newman & Keuls, P < 0.05).</footnote>

<footnote>* Capital different letters correspond to significant differences between food sources for a same population/species (Newman & Keuls, P < 0.05).</footnote>
<table><caption>**Table 3** Mean daily consumption (± standard error) of eggs of *T. urticae* (on bean leaf discs) and of *T. evansi* (on *S. nigrum* leaf discs) by females of populations *T. (A.) recki* (D: collected on *Datura stramonium*, S: collected on *Solanum lycopersicum*, M: collected on *Mentha suaveolens*), *N. californicus* and *N. cucumeris*.</caption><thead><tr><th rowspan="2"></th><th colspan="2">Daily consumption per female</th><th colspan="2">Daily consumption per female</th><th rowspan="2">P value</th></tr><tr><th>Bean/T. urticae</th><th>S. nigrum / T. evansi</th><th></th><th></th></tr></thead><tbody><tr><td><i>N. californicus</i></td><td>10.67 ± 5.85</td><td>b</td><td>1.60 ± 1.33</td><td>b</td><td>0.0001</td></tr><tr><td><i>N. cucumeris</i></td><td>14.52 ± 10.82</td><td>ab</td><td>4.23 ± 4.30</td><td>a</td><td>0.0001</td></tr><tr><td><i>T. (A.) recki</i> D</td><td>12.55 ± 9.42</td><td>b</td><td>4.52 ± 6.11</td><td>a</td><td>0.00002</td></tr><tr><td><i>T. (A.) recki</i> S</td><td>18.47 ± 16.54</td><td>a</td><td>4.00 ± 3.94</td><td>a</td><td>0.00001</td></tr><tr><td><i>T. (A.) recki</i> M</td><td>11.69 ± 12.23</td><td>b</td><td>3.11 ± 2.40</td><td>ab</td><td>0.0005</td></tr><tr><td>P value</td><td colspan="2">0.02</td><td colspan="2">0.01</td><td></td></tr></tbody></table>

*N. californicus* (0.05 eggs / female/ day) (Table 2). Significant differences were only observed at day 1 (*P*=0.01) (Table 4, figure 3b), where the highest fecundity was observed for *T. (A.) recki* from *D. stramonium* and *N. cucumeris* and the lowest for *N. californicus*. For all the species, the mean fecundity decreases through the time (Table 4). The mean number of *T. evansi* eggs consumed per day was significantly different (*P*=0.01). The highest values were observed for *T. (A.) recki* collected on *D. stramonium*, *T. (A.) recki* collected on *S. lycopersicum* and *N. cucumeris*, and the lowest for *N. californicus* (Table 3). No significant difference was observed at each day (Table 4). For all species, the daily consumption significantly decreased through the time (Table 4). The cumulated number of eggs consumed during four days ranged from 6.4 (*N. californicus*) to 18.1 (*T. [A] recki* from *D. stramonium*) (Figure 3d). These results, as in Escudero and Ferragut (2005), Moraes & McMurtry (1985) and Koller *et al.* (2007), show the low mean fecundity of *N. californicus* when fed on *T. evansi*, even lower than the values obtained in these publications (0.79 eggs/ female/ day, 0.5 eggs/ female/ day and 0.56 eggs/female/day, respectively). The low mean fecundity observed for *N. cucumeris* and the three populations of *T. (A.) recki* are in accordance with the results obtained for eight Phytoseiidae species by Moraes and McMurtry (1985). For *T. evansi* egg consumption, data in literature are scarce. Moraes and McMurtry (1986) reported a lower mean consumption by *Phytoseiulus persimilis* Athias-Henriot (1.4 - 1.7 eggs/ female/day) than the one here obtained for *N. cucumeris* and *T. (A.) recki* (3.11 - 4.52 eggs/female/day).

## Aculops lycopersici on Solanum nigrum

The mean fecundity of the populations / species was not significantly different (*P* = 0.055) (Table 2), but we can note that the highest fecundity for *T. (A.) recki* collected on *M. suaveolens* (1.00 eggs/ female) and the lowest for *T. (A.) recki* collected on *D. stramonium* (0.35 eggs/ female). Significant differences were only significant at day 1 (*P*=0.02) (Table 4, Figure 3e). The values obtained were much lower than the ones reported for *N. cucumeris* when fed with *A. lycopersici* by Al-Azzazy *et al.* (2018) (2.12 eggs/ female/ day), for *Euseius concordis* (Chant) by Moraes and Lima (1983) (1.7 eggs/ female/ day), *Amblydromalus limonicus* Garman & McGregor (Van Houten *et al.* 2013a, b) (3.6 eggs/ female/ day) and *Amblyseius swirskii* Athias-Henriot (Momen and Abdel-Khalek 2008; Park *et al.* 2010; Van Houten *et al.* 2013a, b) (2.00, 1.7 and 2.4 eggs/ female/ day, respectively). Castagnoli *et al.* (2003) reported a decreasing *rm* from F1 to F3 generations (0.21 to 0.08) for *N. californicus* feeding on *A. lycopersici*. Some preliminary measurements (data not shown) indicate a consumption of 50 eriophyids mites / day by *T. (A.) recki* (population from *M. suaveolens*). This value is much higher than the one reported by Al-Azzizy *et al.* (2018) for *N. cucumeris* (consumption ranging from 12.82 to

<footnote>* Different letters correspond to significant differences between the populations / species considered (Newman & Keuls, P < 0.05).</footnote>
21.69 *A. lycopersici* per day).

Considering each predator separately, *T. evansi* was the less favourable food source. However, no distinction between the populations/species was observed when the prey was *T. urticae* or *A. lycopersici*. Only, a higher fecundity was observed for *N. californicus* fed on *T. urticae* than on *A. lycopersici* (Table 2).

## Dispersal abilities of *Typhlodromus (Anthoseius) recki* along tomato stem in laboratory studies

Females dispersed along the stem bridge whatever the food source (pollen or *A. lycopersici*). A low proportion was observed on the stem. They essentially moved during the first day (Figure 4). Afterwards, their movement was less frequent. The females were preferentially found on the discs with food, both for pollen and *A. lycopersici* treatments (Table 5). The number of eggs

<table><caption>**Table 4** Mean fecundity and mean number of eggs consumed each day (± standard error) for the populations *T. (A.) recki* (D: collected on *Datura stramonium*, S: collected on *Solanum lycopersicum*, M: collected on *Mentha suaveolens*), *N. californicus* and *N. cucumeris* when the females are feeding on eggs of *T. urticae* (on bean leaf discs), of *T. evansi* (on *S. nigrum* leaf discs) and all stages of *A. lycopersicum* (on *S. nigrum* leaf discs).</caption><thead><tr><th colspan="8">Tetranychus urticae on bean leaves</th></tr><tr><th colspan="8">Number of eggs laid</th></tr><tr><th></th><th>T. (A.) recki D</th><th>T. (A.) recki S</th><th>T. (A.) recki M</th><th>N. californicus</th><th>N. cucumeris</th><th>P value</th></tr></thead><tbody><tr><td>Day 1</td><td>1.00 ± 0.81</td><td>0.60 ± 0.51</td><td>0.66 ± 0.70</td><td>0.2 ± 0.42</td><td>0.72 ± 0.59</td><td>0.07</td></tr><tr><td>Day 2</td><td>1.10 ± 0.99</td><td>0.50 ± 0.52</td><td>0.88 ± 0.60</td><td>0.8 ± 1.03</td><td>0.86 ± 0.83</td><td>0.06</td></tr><tr><td>Day 3</td><td>0.70 ± 0.82</td><td>B</td><td>0.60 ± 0.51</td><td>B</td><td>0.50 ± 0.72</td><td>B</td><td>2.2 ± 1.32</td><td>a A</td><td>1.11 ± 0.64</td><td>B</td><td>&lt; 0.001</td></tr><tr><td>Day 4</td><td>1.00 ± 1.05</td><td>B</td><td>0.60 ± 0.51</td><td>B</td><td>0.88 ± 0.92</td><td>B</td><td>2.4 ± 1.35</td><td>a A</td><td>1.04 ± 0.94</td><td>B</td><td>0.001</td></tr><tr><td>P value</td><td>0.75</td><td>0.89</td><td>0.76</td><td colspan="4">&lt; 0.0001</td><td colspan="4">0.06</td></tr><tr><th colspan="8">Tetranychus urticae on bean leaves</th></tr><tr><th colspan="8">Number of eggs consumed</th></tr><tr><th></th><th>T. (A.) recki D</th><th>T. (A.) recki S</th><th>T. (A.) recki M</th><th>N. californicus</th><th>N. cucumeris</th><th>P value</th></tr><tr><td>Day 1</td><td>18.60 ± 12.40</td><td>a B</td><td>40.50 ± 19.04</td><td>a A</td><td>21.77 ± 19.84</td><td>a B</td><td>6.00 ± 3.01</td><td>c C</td><td>25.31 ± 11.64</td><td>a B</td><td>&lt; 0.001</td></tr><tr><td>Day 2</td><td>16.70 ± 8.12</td><td>a</td><td>12.70 ± 7.10</td><td>b</td><td>11.67 ± 8.20</td><td>ab</td><td>8.60 ± 4.27</td><td>bc</td><td>15.65 ± 8.49</td><td>b</td><td>0.08</td></tr><tr><td>Day 3</td><td>7.25 ± 4.71</td><td>b AB</td><td>9.20 ± 2.69</td><td>b AB</td><td>6.22 ± 2.90</td><td>b B</td><td>12.60 ± 5.54</td><td>ab A</td><td>10.15 ± 5.95</td><td>c AB</td><td>0.05</td></tr><tr><td>Day 4</td><td>7.60 ± 5.01</td><td>b B</td><td>11.50 ± 6.32</td><td>b AB</td><td>7.11 ± 3.65</td><td>b B</td><td>15.50 ± 5.62</td><td>a A</td><td>6.11 ± 4.11</td><td>c B</td><td>&lt; 0.001</td></tr><tr><td>P value</td><td>0.0007</td><td colspan="4">&lt; 0.0001</td><td colspan="4">0.004</td><td colspan="4">&lt; 0.0001</td></tr><tr><th colspan="8">Tetranychus evansi on S. nigrum leaves</th></tr><tr><th colspan="8">Number of eggs laid</th></tr><tr><th></th><th>T. (A.) recki D</th><th>T. (A.) recki S</th><th>T. (A.) recki M</th><th>N. californicus</th><th>N. cucumeris</th><th>P value</th></tr><tr><td>Day 1</td><td>0.60 ± 0.51</td><td>a A</td><td>0.10 ± 0.31</td><td>AB</td><td>0.42 ± 0.78</td><td>AB</td><td>0.00 ± 0.00</td><td>B</td><td>0.60 ± 0.51</td><td>a A</td><td>0.01</td></tr><tr><td>Day 2</td><td>0.30 ± 0.48</td><td>b</td><td>0.20 ± 0.42</td><td></td><td>0.14 ± 0.37</td><td></td><td>0.10 ± 0.31</td><td></td><td>0.10 ± 0.31</td><td>b</td><td>0.76</td></tr><tr><td>Day 3</td><td>0.10 ± 0.31</td><td>b</td><td>0.00 ± 0.00</td><td></td><td>0.14 ± 0.37</td><td></td><td>0.00 ± 0.00</td><td></td><td>0.00 ± 0.00</td><td>b</td><td>0.45</td></tr><tr><td>Day 4</td><td>0.20 ± 0.42</td><td>b</td><td>0.00 ± 0.00</td><td></td><td>0.28 ± 0.48</td><td></td><td>0.10 ± 0.31</td><td></td><td>0.00 ± 0.00</td><td>b</td><td>0.28</td></tr><tr><td>P value</td><td>0.031</td><td colspan="4">0.19</td><td colspan="4">0.64</td><td colspan="4">0.53</td></tr><tr><th colspan="8">Tetranychus evansi on S. nigrum leaves</th></tr><tr><th colspan="8">Number of eggs consumed</th></tr><tr><th></th><th>T. (A.) recki D</th><th>T. (A.) recki S</th><th>T. (A.) recki M</th><th>N. californicus</th><th>N. cucumeris</th><th>P value</th></tr><tr><td>Day 1</td><td>9.80 ± 9.62</td><td>a</td><td>6.70 ± 5.77</td><td>a</td><td>3.14 ± 2.34</td><td></td><td>2.50 ± 1.26</td><td>a</td><td>7.80 ± 6.03</td><td>a</td><td>0.06</td></tr><tr><td>Day 2</td><td>3.00 ± 4.52</td><td>b</td><td>3.30 ± 3.09</td><td>b</td><td>1.57 ± 2.29</td><td></td><td>1.10 ± 1.10</td><td>b</td><td>2.70 ± 3.12</td><td>b</td><td>0.47</td></tr><tr><td>Day 3</td><td>2.70 ± 2.36</td><td>b</td><td>3.10 ± 2.84</td><td>b</td><td>4.28 ± 2.92</td><td></td><td>1.80 ± 1.31</td><td>ab</td><td>2.90 ± 1.91</td><td>b</td><td>0.31</td></tr><tr><td>Day 4</td><td>2.60 ± 1.35</td><td>b</td><td>2.90 ± 2.37</td><td>b</td><td>3.42 ± 1.51</td><td></td><td>1.00 ± 1.24</td><td>b</td><td>3.37 ± 3.02</td><td>b</td><td>0.07</td></tr><tr><td>P value</td><td>0.009</td><td colspan="4">0.036</td><td colspan="4">0.39</td><td colspan="4">0.028</td></tr><tr><th colspan="8">Aculops lycopersici on Solanum nigrum leaves</th></tr><tr><th colspan="8">Number of eggs laid</th></tr><tr><th></th><th>T. (A.) recki D</th><th>T. (A.) recki S</th><th>T. (A.) recki M</th><th>N. californicus</th><th>N. cucumeris</th><th>P value</th></tr><tr><td>Day 1</td><td>0.16 ± 0.40</td><td>B</td><td>0.60 ± 0.89</td><td>AB</td><td>1.20 ± 0.91</td><td>a A</td><td>1.00 ± 0.75</td><td>AB</td><td>0.53 ± 0.57</td><td>AB</td><td>0.02</td></tr><tr><td>Day 2</td><td>0.25 ± 0.50</td><td></td><td>0.75 ± 0.95</td><td></td><td>1.33 ± 0.70</td><td>a</td><td>0.87 ± 0.83</td><td></td><td>1.07 ± 0.72</td><td></td><td>0.17</td></tr><tr><td>Day 3</td><td>1.00 ± 0.00</td><td></td><td>0.75 ± 0.95</td><td></td><td>0.88 ± 0.78</td><td>b</td><td>1.00 ± 0.75</td><td></td><td>1.29 ± 0.85</td><td></td><td>0.60</td></tr><tr><td>Day 4</td><td>0.50 ± 0.70</td><td></td><td>0.00 ± 0.00</td><td></td><td>0.56 ± 0.72</td><td>b</td><td>0.33 ± 0.81</td><td></td><td>0.70 ± 0.80</td><td></td><td>0.59</td></tr><tr><td>P value</td><td>0.14</td><td colspan="4">0.45</td><td colspan="4">0.04</td><td colspan="4">0.21</td></tr></tbody></table>

<footnote>* Small different letters correspond to significant differences between days for each population/species considered (Newman & Keuls, P < 0.05).</footnote>

<footnote>* Capital different letters correspond to significant differences between the population/species for a same day (Newman & Keuls, P < 0.05).</footnote>
<figure><img src="image_14.png" /><figcaption>**Figure 4** Percentage *T. (A.) recki* females that moved along the tomato stem in the two treatments during four days (D1–D4), when the food provided was *Typha* sp. pollen or *A. lycopersici*.</figcaption></figure>

laid on the leaf disc with food was significantly higher than those laid on the leaf disc without food (*P* < 0.0001 - pollen disc : 1.50 eggs/female/day, disc without pollen: 0.25 eggs/female/day; *P* = 0.03 - disc with *A. lycopersici* : 1.09 eggs/female/day, disc without *A. lycopersici*: 0.40 eggs/female/day). No significant difference in fecundity was observed for leaf discs with *A. lycopersici* and pollen (*P* = 0.13). For a same replicate, eggs were sometimes observed on both leaf discs suggesting that the female was able to re-cross the stem bridge. Even if those results are encouraging, cut tomato stem have different physical and chemical properties than not-cut ones. Thus, further experiments on entire plants are needed to conclude on the ability *T. (A.) recki* to disperse along the stem, as shown for other Phytoseiidae species (*P. longipes* and *Phytoseiulus macropilis* (Banks)) by Sato *et al.* (2011).

**Assessment of the ability of *T. (A.) recki* to move from mint to tomato leaves under laboratory conditions**

One day after the beginning of the experiments, females of *T. (A.) recki* dispersed to the tomato half-disc infested with *T. evansi* (Table 6). Overall, the number of females and the percentage of occupation of each half-disc (mint vs. tomato) were not significantly different. However, at days 3 and 6, the number of females of the tomato half-disc was higher than on the mint half-disc and the percentage of females on tomato half-disc was higher than on mint at days 2,

<table><caption>**Table 5** Position (%) of *T. (A.) recki* females and eggs on the stem and leaf discs with and without food (pollen or *A. lycopersici*).</caption><thead><tr><th rowspan="2"></th><th colspan="3">% of position of females</th></tr><tr><th>Leaf with food</th><th>Stem</th><th>Leaf without food</th></tr></thead><tbody><tr><td>Pollen</td><td>84.2</td><td>3.5</td><td>12.3</td></tr><tr><td><i>A. lycopersici</i></td><td>59.4</td><td>13.5</td><td>27.0</td></tr></tbody><tbody><tr><th rowspan="2"></th><th colspan="3">% of position of eggs</th></tr><tr><th>Leaf with food</th><th>Stem</th><th>Leaf without food</th></tr><tr><td>Pollen</td><td>83.3</td><td>3.3</td><td>13.3</td></tr><tr><td><i>A. lycopersici</i></td><td>84.6</td><td></td><td>15.4</td></tr></tbody></table>
<figure><img src="image_15.png" /><figcaption>**Figure 5** a – Percentage of females of *T. (A.) recki* on the tomato and mint leaf half-disc through the time; b – percentage of eggs of *T. (A.) recki* on the tomato and mint leaf half-discs through the time and (c) percentage of eggs + immatures of *T. (A.) recki* on the tomato and mint leaf half-discs through the time. A star (*) indicates significant differences after Chi2 test.</figcaption></figure>

3 and 6 (Figure 5).

The number of eggs+ immatures of *T. (A.) recki* was significantly greater on the mint half-disc at day 1 and day 2. At day 3, no significant difference was observed between the two treatments, whereas at days 6 and 7, the number of eggs + immatures were much greater on the tomato half-disc (Table 6). At day 7, all the eggs of *T. (A.) recki* were laid on the tomato disc.
<table><caption>**Table 6** Mean number (± standard error) of *T. (A.) recki* females, immatures+eggs on mint and tomato half-discs through the time and mean number of *T. evansi* females and eggs+immatures on tomato half-discs through the time.</caption><thead><tr><th></th><th>Number of females of T. (A.) recki on mint half-discs</th><th>Number of females of T. (A.) recki on tomato half-discs</th><th>P value</th><th>Number of eggs + immatures of T. (A.) recki on mint half-discs</th><th>Number of eggs + immatures of T. (A.) recki on tomato half-discs</th><th>P Value</th><th>Number of T. evansi females on tomato half-discs</th><th>Number of eggs + immatures of T. evansi on tomato half-discs</th></tr></thead><tbody><tr><td>D1</td><td>1.33 ± 1.33</td><td>0.87 ± 0.91</td><td>0.25</td><td>0.87 ± 0.91</td><td>0.20 ± 0.56</td><td>b 0.02</td><td>3.20 ± 1.32</td><td>a 10.00 ± 7.62</td></tr><tr><td>D2</td><td>0.80 ± 0.77</td><td>1.26 ± 0.79</td><td>0.14</td><td>1.47 ± 1.25</td><td>0.27 ± 0.59</td><td>b 0.002</td><td>2.26 ± 1.43</td><td>ab 12.00 ± 12.96</td></tr><tr><td>D3</td><td>0.93 ± 0.96</td><td>1.06 ± 0.96</td><td>0.74</td><td>1.20 ± 1.20</td><td>0.67 ± 1.04</td><td>b 0.19</td><td>1.60 ± 1.35</td><td>b 16.06 ± 16.91</td></tr><tr><td>D6</td><td>0.64 ± 0.63</td><td>1.07 ± 0.82</td><td>0.19</td><td>1.07 ± 0.99</td><td>2.07 ± 1.26</td><td>a 0.03</td><td>1.64 ± 1.15</td><td>b 12.57 ± 11.74</td></tr><tr><td>D7</td><td>0.90 ± 0.70</td><td>0.63 ± 0.67</td><td>0.41</td><td>0.36 ± 0.92</td><td>1.81 ± 1.60</td><td>a 0.01</td><td>1.72 ± 1.35</td><td>b 6.18 ± 5.70</td></tr><tr><td>P value</td><td>0.26</td><td>0.41</td><td></td><td>0.11</td><td>&lt; 0.0001</td><td></td><td>0.007</td><td>0.32</td></tr></tbody></table>

The percentage of eggs+immatures was significantly higher on mint half-discs at day 1 and 2, whereas it was significantly higher on tomato half-discs at day 7 (Figure 5).

The number of *T. evansi* females decreased significantly through time (from 5 females / leaf disc at day 0 to 1.72 at day 7). Several hypotheses can explain this observation: (i) female escaped (but this is unlikely as they would be observed on moistened cotton), (ii) female were predated even if predation usually occur on eggs and immature stages and/or (iii) female died (but cadavers were not retrieved). The number of eggs and immatures of *T. evansi* increased until the day 3 and then decreased but no significant difference was observed through the time (P=0.32) (Table 6).

## Conclusion

This study presents first data on the biology of *T. (A.) recki*. It confirms that this species is a generalist predator, with biological features close to those of other efficient generalist predators as *K. aberrans* and *T. (T.) pyri*. Its mean consumption of *T. urticae* is similar to *N. californicus*, which is considered as an efficient predator of spider mites (i.e. Knapp *et al.* 2018). Furthermore, it seems to perform better on *T. evansi* than the generalist species already tested. It is similarly attracted by prey and pollen, confirming its generalist statute. It is the first time that this species is tested on *A. lycopersici*, one of the most important pests in tomato crops (Trottin-Caudal *et al.* 2003; Duso *et al.* 2009). These preliminary results are encouraging considering both biological features and dispersal abilities. However, as laboratory observations do not entirely reflect real situations, trials on entire plants are required. Furthermore, because of the biological characteristics of this generalist predator, such as for *K. aberrans* and *T. (T.) pyri*, biodiversity conservation biological control should be favoured, in line with the banker plant strategy already tried in tomato greenhouses to control white flies (i.e. Frank 2010). Several characteristics of *T. (A.) recki* (endemic species of Europe, current distribution, its occurrence on Solanaceae and the fact that it is attracted by prey) constitute elements to further investigate its predation ability at plant and crop level.

## Acknowledgements

We thank the French national program (Ecophyto – Project ACAROSOL) that granted in part the surveys carried out. We are also grateful to the two anonymous reviewers for their accurate and relevant comments.

## References

Al-Azzazy M., Suloiman M., Al-Rehiayani M., Nagdy F. A. 2018. Life tables of the predatory mite *Neoseiulus cucumeris* (Acari: Phytoseiidae) on two pest mites as prey, *Aculops lycopersici* and *Tetranychus urticae*. Archives of Phytopathology and Plant Protection 51 (11-12): 637-648.
doi:10.1080/03235408.2018.1507013
Basheer A., Saker I., Dahiah H., Mofjeh M. 2014. Life Table Parameters of *Typhlodromus (Typhlodromus) athiasae* Porath and Swirski (Gamasida: Phytoseiidae), Predator of the Two-Spotted Spider Mite, *Tetranychus urticae* (Koch) (Actinedida: Tetranychidae). Egyptian Journal of Pest Control, 24(2): 373-377.

Castagnoli M., Simoni S., Liguori M. 2003. Evaluation of *Neoseiulus californicus* (McGregor) (Acari: Phytoseiidae) as a candidate for the control of *Aculops lycopersici* (Tyron) (Acari Eriophyoidea): a preliminary study. Redia, 86: 97-100.

Castagnoli M., Simoni S., Nachman G. 2001. Short-term changes in consumption and oviposition rates of *Neoseiulus californicus* strains (Acari: Phytoseiidae) after a diet shift. Exp. Appl. Acarol., 25: 969-983. doi:10.1023/A:1020639301898

Canlas L.J., Mamano H., Ochiai M., Takeda M. 2006. Biology and predation of the strain Japanese of *Neoseiulus californicus* (McGregor) (Acari: Phytoseiidae). Syst. Appl. Acarol., 11 (2): 141-157. doi:10.11158/saa.11.2.2

Demite P.R., Moraes G.J. de, McMurtry J.A., Denmark H.A., Castilho R.C. 2020. Phytoseiidae Database. Available from: www.lea.esalq.usp.br/phytoseiidae (accessed 15/IV/2020)

Duso C., Castagnoli M., Simoni S., Angeli G. 2009. The impact of eriophyoids on crops: Recent issues on *Aculus schlechtendali*, *Calepitrimerus vitis* and *Aculops lycopersici*. Exp. Appl. Acarol., 51(1-3): 151-68. doi:10.1007/978-90-481-9562-6_8

Escudero L.A., Ferragut F. 2005. Life-history of predatory mites *Neoseiulus californicus* and *Phytoseiulus persimilis* (Acari: Phytoseiidae) on four spider mite species as prey, with special reference to *Tetranychus evansi* (Acari: Tetranychidae). Biol Control, 32(3): 378-384. doi:10.1016/j.biocontrol.2004.12.010

Ferrero M., Tixier M.-S., Kreiter S. 2014a. From specificity to specialisation. I. Comparative life histories of three populations of *Phytoseiulus longipes* Evans (Acari, Mesostigmata, Phytoseiidae) depending on prey species and plant supports. Exp. Appl. Acarol., 62: 313-324. doi:10.1007/s10493-013-9745-z

Ferrero M., Tixier M.-S., Kreiter S. 2014b. From specificity to specialization. II. Choice tests and attractiveness of different prey species, prey stages and plant supports for two populations of *Phytoseiulus longipes* Evans [Acari, Mesostigmata, Phytoseiidae]. Exp. Appl. Acarol., 62: 325-335. doi:10.1007/s10493-013-9746-y

Frank S.D. 2010. Biological control of arthropod pests using banker plant systems: Past progress and future directions. Biol. Contr., 52 : 8-16 doi:10.1016/j.biocontrol.2009.09.011

Furtado I.P., Moraes G.J.de, Kreiter S., Tixier M.-S., Knapp M. 2007.Potential of a Brazilian population of the predatory mite *Phytoseiulus longipes* as a biological control agent of *Tetranychus evansi* (Acari: Phytoseiidae, Tetranychidae). Biol. Control, 42: 139-147. doi:10.1016/j.biocontrol.2007.04.016

Gerson U., Smiley R.L., Ochoa T. 2003. *Mites (Acari) for Pest Control*. Blackwell Science, Oxford, UK, 539pp. doi:10.1002/9780470750995

Gotoh T., Yamaguchi K., Mori K. 2004. Effect of temperature on life history of the predatory mite *Amblyseius (Neoseiulus) californicus* (Acari: Phytoseiidae). Exp. Appl. Acarol., 32(1-2):15-30. doi:10.1023/B:APPA.0000018192.91930.49

Hajizadeh H., Kamali K., Faraji F. 2006. Predatory mite fauna of Phytoseiidae of northwest Iran (Acari: Mesostigmata). Turk. J. Zool., 34(4): 497-508.

Hatherly I., Bale J. S., Walters K.F.A. 2005. Intraguild predation and feeding preferences in three species of phytoseiid mite used for biological control. Exp. Appl. Acarol., 37(1-2): 43-55. doi:10.1007/s10493-005-0358-z

Karban R., English-Loeb G., Walker M.A., Thaler J. 1995. Abundance of phytoseiid mites on *Vitis* species: effects of leaf hairs, domatia, prey abundance and plant phylogeny. Exp. Appl. Acarol., 19(4): 189-197. doi:10.1007/BF00130822

Kasap I. 2010. Prey-stage preference and population increase of the predaceous mite *Kampimodromus aberrans* (Oudemans) (Acari: Phytoseiidae) on *Tetranychus urticae* Koch (Acari: Tetranychidae) under laboratory conditions. Int. J. Acarol., 36 (6): 473-481. doi:10.1080/01647950903575341

Kennedy G.G. 2003. Tomato, pest, parasitoids, and predators: tritrophic interactions involving the genus *Lycopersicon*. Ann. Rev. Entomol., 48: 51-72. doi:10.1146/annurev.ento.48.091801.112733

Knapp M., Van Houten Y., Van Baal E., Grout T. 2018. Use of predatory mites in commercial biocontrol: current status and future prospects. Acarologia, 58: 72-82. doi:10.24349/acarologia/20184275

Koller M., Knapp M., Schausberger P. 2007. Direct and indirect adverse effects of tomato on the predatory mite *Neoseiulus californicus* feeding on the spider mite *Tetranychus evansi*. Entomol. Experim. Appl., 125: 297-305. doi:10.1111/j.1570-7458.2007.00625.x

Kreiter S., Tixier M.-S., Croft B.A., Auger P., Barret D. 2002. Plants and leaf characteristics influencing the predaceous mite *Kampimodromus aberrans* (Acari: Phytoseiidae) in habitats surrounding vineyards. Environ. Entomol., 31: 648-660. doi:10.1603/0046-225X-31.4.648

Kumral N.A., Cobanoglu S. 2015a. The potential of the nightshade plants (Solanaceae) as reservoir plants for pest and predatory mites. Turk. J. Entomol., 39(1): 91-108. doi:10.16970/ted.55042

Kumral N.A., Cobanoglu S. 2015b. A reservoir weed for mites: *Datura stramonium* L. (Solanaceae) in the vicinity of cultivated solanaceous plants in Turkey. Int. J. Acarol., 41: 563-573. doi: 10.1080/01647954.2015.1084043

Lebdi-Grissa K., Van Impe G., Lebrun P. 2005. Paramètres biologiques et démographiques de *Neoseiulus californicus* (acari : phytoseiidae) à différentes temperatures. Acarologia, 45 (1): 13-22.

Li G.Y., Zhang Z.K. 2016. Some factors affecting the development, survival and prey consumption of *Neoseiulus cucumeris* (Acari: Phytoseiidae) feeding on *Tetranychus urticae* eggs (Acari: Tetranychidae) Syst. Appl. Acarol., 21(5): 555-566. doi:10.11158/saa.21.5.1

Marafeli P.P., Reis P.R., Silveira E.C., Souza-Pimentel G.C., Toledo M.A. 2014. Life history of *Neoseiulus californicus* (McGregor, 1954) (Acari: Phytoseiidae) fed with castor bean (*Ricinus communis* L.) pollen in laboratory conditions. Braz. J. Biol., 74(3): 691-697. doi:10.1590/bjb.2014.0079
McMurtry J.A., Croft B.A. 1997. Life-styles of phytoseiid mites and their roles in biological control. Annu. Rev. Entomol., 42: 291-321. doi:10.1146/annurev.ento.42.1.291

McMurtry J.A., Moraes G.J. De, Sourassou N.F. 2013. Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Syst. Appl. Acarol., 18(4): 297-320. doi:10.11158/saa.18.4.1

McMurtry J.A., Scriven G.T. 1965. Insectary production of phytoseiid mites. J. Econ. Entomol., 58(2): 282-284. doi:10.1093/jee/58.2.282

Momen F.M., Abdel-Khalek A. 2008. Effect of the tomato russet mite *Aculops lycopersici* (Acari: Eriophyidae) on the development and reproduction of three predatory phytoseiid mites. Int. J. Trop. Insect Sci., 28: 53-57. doi:10.1017/S1742758408942594

Moraes G.J., Lima H.C. 1983. Biology of *Euseius concordis* (Chant) (Acarina: Phytoseiidae) a predator of the tomato russet mite. Acarologia, 24: 251-255.

Moraes G.J. de, McMurtry J.A. 1985. Comparison of *Tetranychus evansi* and *T. urticae* (Acari: Tetranychidae) as prey for eight species of phytoseiid mites. Entomophaga, 30(4): 393-397. doi:10.1007/BF02372345

Moraes G.J.de, McMurtry J.A. 1986.Suitability of the spider mite *Tetranychus evansi* as prey for *Phytoseiulus persimilis*. Entomol. Exp. Appl. 40: 109-115. doi:10.1111/j.1570-7458.1986.tb00490.x

Moraes G.J. de, McMurtry J.A., Denmark H.A. 1986. A catalog of the mite family Phytoseiidae. References to taxonomy, synonymy, distribution and habitat-EMBRAPA - DDT, 353 pp.

Park H.H., Shipp L., Buitenhuis R. 2010. Predation, development, and oviposition by the predatory mite *Amblyseius swirskii* (Acari: Phytoseiidae) on tomato russet mite (Acari: Eriophyidae). J. Econ. Entomol., 103: 563-569. doi:10.1603/EC09161

Rahmani H., Fathipour Y. Kamali K. 2009. Life history and population growth parameters of *Neoseiulus californicus* (Acari: Phytoseiidae) fed on *Thrips tabaci* (Thysanoptera: Thripidae) in laboratory conditions. Syst. Appl. Acarol., 14: 91-100. doi:10.11158/saa.14.2.2

Schmidt R.A. 2014. Leaf structures affect predatory mites (Acari: Phytoseiidae) and biological control: a review. Exp. Appl. Acarol., 62: 1-17. doi:10.1007/s10493-013-9730-6

Sato M.M., Moraes G.J., Haddad M.L., Weseka V.W. 2011. Effect of trichomes on the predation of *Tetranychus urticae* (Acari: Tetranychidae) by *Phytoseiulus macropilis* (Acari: Phytoseiidae) on tomato, and the interference of webbing. Exp. Appl. Acarol., 54: 21-32. doi:10.1007/s10493-011-9426-8

Simmons A.T., Gurr G.M. 2005. Trichomes of *Lycopersicon* species and their hybrids: effects on pests and natural enemies. Agric. Forest Entomol., 7: 265-276. doi:10.1111/j.1461-9555.2005.00271.x

StatSoft France 2010. STATISTICA (logiciel d'analyse des données), version 9.1. http://www.statsoft.fr.

Swirski E., Amitai S. 1997. Annotated list of phytoseiid mites (Mesostigmata: Phytoseiidae) in Israel. Isr. J. Entomol., 31: 21-46.

The Angiosperm Phylogeny Group. 2009. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Botan. J. Linn. Soc., 161, 105-121. doi:10.1111/j.1095-8339.2009.00996.x

Tixier M.-S. 2018. Predatory mites (Acari: Phytoseiidae) in agro-ecosystems and conservation biological control: a review and explorative approach for forecasting plant-predatory mite interactions and mite dispersal. Front. Ecol. Evol. 6: 192. doi:10.3389/fevo.2018.00192

Tixier M.-S., Kreiter S., Douin M. 2020. Phytoseiidae (Acari: Mesostigmata) on plants of the family Solanaceae: results of a survey in South of France and a review of world biodiversity. Exp. Appl. Acarol. In press. doi:10.1007/s10493-020-00507-0

Trottin-Caudal Y., Fournier C., Leyre J.-M. 2003. Biological control of *Aculops lycopersici* (Massee) using the predatory mites *Neoseiulus californicus* McGregor and *Neoseiulus cucumeris* (Oudemans) on tomato greenhouse crops. In: Proceedings, international symposium on Greenhouse Tomato: integrated crop protection and organic production, 17-19 September 2003. Avignon, France: 153-157.

Van Houten Y., Glas J.J., Hoogerbrugge H., Rothe J., Bolckmans K., Simoni S., van Arkel J., Alba J.M., Kant M.J., Sabelis M.W. 2013a. Herbivory-associated degradation of tomato trichomes and its impact on biological control of *Aculops lycopersici*. Exp. Appl. Acarol., 60: 127-138. doi:10.1007/s10493-012-9638-6

Van Houten Y., Knapp M., Hoogerbrugge H., Bolckmans K. 2013b. The potential of *Amblyseius swirskii* as biocontrol agent for *Aculops lycopersici* on tomatoes. IOBC-WPRS Bulletin, 93: 51-57.

Van Lenteren J.C. 2012. The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl, 57:1-20. DOI 10.1007/s10526-011-9395-1 doi:10.1007/s10526-011-9395-1

Van Lenteren J.C., Bolckmans K., Köhl J., Ravensberg W.J., Urbaneja A. 2017. Biological control using invertebrates and microorganisms: plenty of new opportunities. BioControl, 63 : 39-59 (2018). doi:10.1007/s10526-017-9801-4

Zemek R. 1993. Characteristics of development and reproduction in *Typhlodromus pyri* on *Tetranychus urticae* and *Cecidophopsis ribis*. II. Progeny of overwintered females. Exp. Appl. Acarol., 17(11): 847-858. doi:10.1007/BF00225858

Zheng Y., De Clercq P., Song Z.-W., Li D.-S., Zhang B.-X. 2017. Functional response of two *Neoseiulus* species preying on *Tetranychus urticae* Koch. Syst. Appl. Acarol., 22(7): 1059-1068. doi:10.11158/saa.22.7.13