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This paper must be cited as:
[García-Martínez, F. O., Urbaneja, A., Ferragut, F., Beitia, F. J., & Pérez-Hedo, M. (2019).
Persimmon orchards harbor an abundant and well-established predatory mite fauna. Experimental and Applied Acarology, 77(2), 145-159.]
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1 Article type: Original research paper
1
To submit: Experimental and Applied Acarology 2
3 4
Persimmon-orchards harbor an abundant and well-established predatory mite fauna
56
F. Omar GARCÍA-MARTÍNEZ1, Alberto URBANEJA1; Francisco FERRAGUT2, Francisco J. BEITIA1, 7
Meritxell PÉREZ-HEDO1 8
1Instituto Valenciano de Investigaciones Agrarias (IVIA). Centro de Protección Vegetal y Biotecnología.
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CV-315, Km. 10,746113 Moncada, Valencia. Spain.
10
2Instituto Agroforestal Mediterráneo, Universitat Politècnica de València, Camino de Vera, s/n. 46022 11
Valencia, Spain.
12 13 14 15 16
* Correspondence Address:
17
Meritxell Pérez-Hedo 18
Unidad de Entomología. Centro de Protección Vegetal y Biotecnología 19
Instituto Valenciano de Investigaciones Agrarias (IVIA).
20
CV-315, Km. 10,746113 21
46113 Moncada, Valencia (SP) 22
Tel: +34 963424114; Fax: +34 963424001 23
E-mail: [email protected] 24
25
2 Abstract
26
Despite the fact that persimmon cultivation has been traditionally considered a minor crop in Spain, in 27
recent years this crop has experienced an important increase in both cultivated area and production. This 28
increase has been mainly attributed to the generalized adoption of a new postharvest treatment which allows 29
the considerable extension of the fruit commercialization period. The sudden expansion of this crop has not 30
allowed time to correctly develop an integrated pest management program (IPM). Consequently, chemical 31
treatments have become the main strategy to lessen the impact of pests. Given the importance of phytoseiids 32
in other Mediterranean fruit crops, where they are the basis of IPM, we sought to determine whether they 33
could be similarly employed in persimmon crops. For this, we studied the predatory mite complex, the 34
phytoseiid population dynamics and the potential prey for them during three consecutive seasons in four 35
persimmon orchards. Phytoseiids were abundant throughout the season, found on average at a density of 36
more than 1 predatory mite per leaf. The most abundant species was Euseius stipulatus (57.3%) followed 37
by Typhlodromus phialatus (24.8 %), Amblyseius andersoni (17.1 %) and Paraseiulus talbii (0.8 %).
38
Persimmon leaves provided diverse abundance of prey for predatory mites throughout the year, being 39
mealybugs, coccids, whiteflies and thrips the most common. The abundance of predatory mites was 40
significantly correlated to the abundance of potential prey available. From our results we anticipate that 41
phytoseiids will be key actors in the development of persimmon IPM. Their role and how to conserve their 42
populations in this crop are discussed in this research.
43
44
Keywords: Euseius stipulatus, Typhlodromus phialatus, Amblyseius andersoni, Paraseiulus talbii, IPM.
45
3 Introduction
46
During the last ten years, the cultivation of persimmon has gone from being a minor crop to a crop of great 47
importance for Spanish agriculture (Tena et al. 2015). Currently in Spain more than 17,000 ha are grown 48
with a production of 240,000 T, which is expected to increase to levels of 650,000 T in the year 2020 49
(Perucho 2016, personal communication). The main production area is concentrated in Eastern Spain (the 50
County of Valencia) with more than 50% of the Spanish production. The recent exponential increase in 51
persimmon crop land has been mainly attributed to the adoption of a new postharvest treatment consisting 52
of modified atmospheres at high CO2 concentrations (Arnal and Del Rio, 2003). This technique removes 53
the fruit astringency allowing its commercialization as solid flesh fruit. Thanks to this post-harvest 54
technique, the period of commercialization has increased considerably allowing the development of new 55
marketing channels which reach countries far from the production area such as Germany, Switzerland and 56
the United Kingdom (Perucho 2015). Spain has become the third greatest persimmon producing country in 57
the world; after China and Japan, and the largest persimmon exporter.
58
Before the widespread adoption of the elimination of the astringency in postharvest, the persimmon crop 59
had no important arthropod pest problems in Spain (Tena et al. 2015). At that time, the Mediterranean fruit 60
fly, Ceratitis capitata Wiedemann (Diptera: Tephritidae) was reported to be the main problem given that 61
the persimmon fruit matured on the tree. Apart from the medfly, there were only occasional reports of 62
Planococcus citri Risso (Hemiptera: Pseudoccidae) and Cryptoblabes gnidiella (Millière) (Lepidoptera:
63
Pyralidae)Nowadays, this situation has changed completely because fruit are harvested before they are 64
susceptible to the oviposition of Ceratitis capitata. Currently, mealybugs, honeydew moths and whiteflies 65
have become the main pests of this crop (García-Martínez et al. 2015; García-Martínez et al. 2016).
66
Integrated Pest Management (IPM) has not been correctly developed due to the haste with which the 67
persimmon industry has grown. Farmers have adopted the use of chemical treatments in an attempt to 68
manage mealybugs and honeydew moths. Unfortunately, in many cases these treatments (mainly 69
organophosphates and pyrethroids) have not controlled the pests, but rather have caused mealybugs and 70
honeydew moth populations to increase, probably due to the elimination of their natural enemies. It should 71
be noted that in recent years the incidence of whiteflies has increased; it is, again, highly probable that this 72
increase is associated with the impact chemicals have had on this pest´s natural enemies.
73
4 Predatory mites (Acari: Phytoseiidae) are key natural enemies in citrus and fruit trees in the Mediterranean 74
basin. In fact, pest management programs in several of these crops have been developed with phytoseiids 75
as the key natural enemies to be protected, maintained and promoted in the system. In Mediterranean citrus, 76
Euseius stipulatus (Athias-Henriot) (Acari: Phytoseiidae), is the most abundant predatory mite (Ferragut et 77
al. 1988; Abad et al. 2009). This phytoseiid is an omnivorous predator considered to be a key player in the 78
biological control of the citrus red mite Panonychus citri (McGregor) (Acari: Tetranychidae) (García-Marí 79
et al. 1983; García-Marí et al. 1986; Ferragut et al. 1988; Ferragut et al. 1992). In addition, this phytoseiid 80
can prey on small arthropods such as whiteflies and mealybug crawlers, so when E. stipulatus populations 81
are high, several citrus pests can be regulated by its action (Urbaneja et al. 2018). Similarly, Amblyseius 82
andersoni (Chant) (Acari: Phytoseiidae) and Neoseiulus californicus (McGregor) (Acari: Phytoseiidae) are 83
key natural enemies for the European red mite, Panonychus ulmi (Koch) (Acari: Tetranychidae) and other 84
small arthropods in apple and pear crops in the north and south of the Spanish Mediterranean coast, 85
respectively (Costa Comelles et al. 1990; MAGRAMA, 2014). Despite the importance that we think 86
phytoseiids may have in persimmon, at present there is no published research on the relative abundance of 87
predatory mites in this crop. To provide insights into the role played by indigenous predatory mites in 88
persimmon, the objective of the present study was aimed at cataloging the phytoseiids associated with 89
persimmon orchards and evaluating their relative abundance and population dynamics at four different 90
locations in the county of Valencia, the major persimmon-growing area of Spain. In addition, the presence 91
of potential prey for predatory mites in persimmon will be catalogued.
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Material and Methods 93
Study sites 94
Predatory mite populations were surveyed in four persimmon orchards (Diospyrus kaki. cv. Rojo Brillante 95
grafted on Diospyros lotus L) located in Almenara (39°45'09.0"N 0°15'50.5"W), in L’Alcudia 96
(39°11'23.3"N 0°32'30.9"W) and in Carlet (Carlet 1: 39°14'25.7"N 0°30'28.9"W and Carlet 2:
97
39°14'06.2"N 0°31'58.9"W). The climate of the region is classified as warm-temperate subtropical with an 98
annual mean temperature of 16.4◦C and rainfall of 458 mm (average data from 2000 to 2013) (STR, 2018).
99
The fields of Almenara (0.59 ha; 8 years old) (Conventional 1, hereinafter) and Carlet 1 (0.2 ha; 20 years 100
old) (Conventional 2, hereinafter) were managed conventionally, while the fields of L'Alcudia (0.12 ha; 30 101
years old) (Organic 1, hereinafter) and Carlet 2 (0.25 ha; 20 years old) (Organic 2, hereinafter) were 102
5 managed organically. In all organic fields, no insecticides were applied during the sampling period in the 103
sampling area. Growers in conventional orchards were convinced to stop treatments throughout the duration 104
of this study, however one chlorpyrifos methyl treatment in July 2016 and another one in September 2016 105
(marked with an arrow in Figure 1) were conducted in Almenara whereas a clorpyrifos-methyl treatment 106
was conducted in May 2015 in Carlet. Both conventional orchards had bare soil (following the application 107
of herbicides in spring, summer and fall) whereas in both organic orchards a spontaneous natural crop was 108
preserved (cover crop was mowed at the beginning of summer and fall). All the orchards were drip- 109
irrigated. Crops were at least nine years old and size and vigor was similar throughout the orchards. The 110
Conventional 1 orchard was surrounded completely by citrus and persimmon orchards with one side 111
bordering a semi-natural habitat, the conventional 2 orchard by pumpkins, citrus and peaches, the organic 112
1 orchard by kiwis, tomatoes, peppers and citrus and organic 2 orchard by peaches, citrus and persimmons.
113
Samplings of predatory mites and potential prey 114
Independently of the field surface area, twenty trees in an area of 0.1 ha in each orchard were sampled every 115
15 days from March 2014 until December 2016. From each tree, five leaves were sampled (100 leaves per 116
orchard). Leaves were taken randomly in all cases in the middle part of the tree canopy. Depending on the 117
tree physiological stage, leaves were young (March to May) or full size (May to December). Samples from 118
each tree were isolated and examined under binocular microscope. All specimens found on the leaves were 119
taxonomically identified to at least the family level and in most cases to the species level. Correlation 120
analyses were used to establish whether the abundance of predatory mite populations was correlated to the 121
abundance of each potential prey, as well as the sum of total prey. Total values per orchard and year were 122
calculated (n =12 pairs per correlation). Correlation analyses were performed SPSS 21.0 software was used 123
and Pearson’s coefficient was calculated.
124
Identification of predatory mites 125
A sample of mature individuals of each orchard and season (spring, summer, fall and winter) of 2014 and 126
2016 was mounted to identify the species. In 2015 the total number of phytoseiids was recorded, however, 127
the material destined to be mounted on slides (adult females) was lost due to an unexpected technical 128
problem with the samples. Collected individuals (after clearing in acid lactic) were mounted on microscope 129
slides with Hoyer’s medium to species identification by using a contrast phase microscope. The relative 130
abundance of each species per season and orchard was calculated, but only adult females were considered 131
6 for this purpose to assure a reliable identification to species. In some cases (winter samplings) there were 132
no leaves available because persimmons are deciduous trees.
133
Results 134
Activity-density patterns 135
Phytoseiid population dynamics are shown in Figure 1. A total of 17,570 phytoseiid individuals were 136
counted in the four orchards over three years of sampling. The population of phytoseiids in all orchards had 137
two main peaks, one of them at the end of spring/beginning of summer and the other one in the fall season.
138
In the spring and summer of 2015 the number of phytoseiids per leaf was lower than in the same period of 139
2014 and 2016; whereas in the fall season phytoseiid densities were similar. Mean maximum densities 140
varied from one to three phytoseiids per leaf; yet, in summer the density was lower than one phytoseiid per 141
leaf.
142
Species composition and relative abundance 143
From the total of 1,851 phytoseiids mounted, 4 species were identified: Euseius stipulatus (Athias-Henriot), 144
Typhlodromus phialatus Athias-Henriot, Amblyseius andersoni (Chant) and Paraseiulus talbii (Athias- 145
Henriot). The numbers of each species for each orchard are shown in Table 1.
146
The most abundant species was E. stipulatus (58.1% of the total), followed by T. phialatus (25.0%) and A.
147
andersoni (16.1%), although their relative abundance depended on the year and orchard; represented in 148
Figures 2 and 3. On the other hand, P. talbii was very scarce with only a 0.76% of relative abundance. In 149
both orchards under conventional management E. stipulatus and T. phialatus were almost the only species 150
found (Figure 2 and 3). In contrast, in both organic orchards, the species richness was higher, since the four 151
species were present (Figure 4 and 5). In all orchards the relative abundances were similar among years, 152
except in Organic 1 orchard where A. andersoni increased over time.
153
Potential prey 154
Mealybugs, were the most abundant arthropod pest, with 13,115 individuals captured, followed by coccids 155
(6,935), whiteflies (3,606) and thrips (1,997). Due to the low abundance of other arthropod pests identified 156
(e.g. lepidopterans and aphids), they were not included in the analysis. Mealybugs were equally abundant 157
in three out the four orchards sampled (the two conventional and organic 1) while their presence was scarce 158
7 in organic orchard 2 (Figure 3). Four species of mealybugs were identified Planococcus citri (De Risso), 159
Delottococcus aberiae (De Lotto), Pseudococcus longispinus (Targioni Tozzetti) and Pseudococcus 160
viburni (Signoret). Two species of coccids, Coccus hesperidium L. y Ceroplastes sinensis Del Guercio, 161
were identified and were present throughout the year (Figure 4). The conventional orchard 1 harbored less 162
coccids in comparison to the other three orchards. For the case of thrips, two species were identified, 163
Frankliniella occidentalis (Pergande) y Heliothrip haemorrhoidalis (Bouché) and a greater presence was 164
found in the conventional orchard 1 (Figure 6). Whiteflies were almost completely absent in conventional 165
1 and organic 2 (Figure 7). Two species of whitefly, Dialeurodes citri Ashmead and Paraleyrodes minei 166
Iaccarinowere found in fall of 2016 in conventional 2 and organic 1.
167
It was not possible to establish a clear relationship between the number of phytoseiids and the number of 168
mealybugs (Pearson’s r = 0.2962; n = 12; P = 0.3499), coccids (Pearson’s r = 0,4051; n= 12; P = 0.1914), 169
thrips (Pearson’s r = -0.1978; n = 12; P = 0.5378) or whiteflies (Pearson’s r = 0.3958; n = 12; P = 0.2029).
170
However, when the abundance of predatory mites was correlated to the total number of potential prey per 171
leaf and year, the relationship was significant (Pearson’s r = 0,6156; n = 12; P = 0.0331).
172
Discussion 173
Four species of phytoseiids were identified during the three years of this study. The four species have been 174
previously reported in fruit crops throughout the Mediterranean basin (Ferragut et al. 1988; Costa Comelles 175
et al. 1990; Ferragut et al. 1992; Abad et al. 2009). To the best of our knowledge, only two previous studies 176
cataloging predatory mites in persimmon are available. In Korea, Kawashima et al. (2008) reported four 177
phytoseiid species, Neoseiulus womersleyi (Schicha), Amblyseius eharai Amitai and Swirski, Phytoseius 178
(Dubininellus) rubii Xin, Liang and Ke and Typhlodromus (Anthoseius) vulgaris Ehara. In Turkey, Akyazi 179
et al. (2017) found seven species A. andersoni, Euseius finlandicus (Oudemans), Kampimodromus aberrans 180
(Oudemans), Neoseiulus umbraticus (Chant), Paraseiulus triporus (Chant and Shaul), Phytoseius finitimus 181
Ribaga, Transeius wainsteini (Gomelauri). Comparing these two surveys with our results, only one species, 182
A. andersoni, is common in Spain and Turkey. The rest of the species are unique for each of the 183
agroecosystems, although the genera are similar.
184
The predominance of E. stipulatus and T. phialatus found in our research is in agreement with McMurtry 185
(1977) and García-Marí et al (1986) who conclude that these two species are the most abundant phytoseiids 186
in the Mediterranean region. Despite the variability in relative abundance of phytoseiid species, E.
187
8 stipulatus is the predominant one in the orchards under conventional management which involves regular 188
application of pesticides. Some authors have commented on the greater resistance to pesticides in E.
189
stipulatus compared to other phytoseiid species (Jeppson et al. 1975; Argolo et al. 2014) and this fact can 190
explain the above mentioned situation as the sampled trees are located in the middle of orchards as islands 191
having been regularly treated with pesticides for years; in fact, the sampled trees themselves were regularly 192
sprayed with phytosanitary compounds before the beginning of this research. The pesticide regime could 193
also explain the lower species’ diversity in conventional orchards where E. stipulatus and T. phialatus are 194
nearly the only species found. In contrast, the two organic orchards contained the four phytoseiid species, 195
with two different predominant species: A. andersoni in Organic 1 and T. phialatus in Organic 2. It is worth 196
mentioning that A. andersoni was found at high levels in Organic 1 orchard, located in L’Alcudia at the 197
south of the Valencian province, which is quite interesting since A. andersoni had been usually found in 198
the North region of Spain (Garcia-Marí et al. 1991; Ferragut et al. 2010). The above mentioned 199
phytosanitary treatments had a clear effect on phytoseiid populations. In 2016, in Conventional 1 orchard, 200
after the first population peak, the number of phytoseiids per leaf was almost zero, probably associated with 201
the two chemical treatments conducted in week 28 and 38. Similarly, in 2015, in Conventional 2 orchard, 202
the unexpected phytosanitary treatment conducted in week 20 could have caused the low levels of 203
phytoseiids obtained until the end of summer.
204
During the three years of sampling in persimmon crops, phytoseiid populations began to increase after the 205
flush growth period in spring until fruit-set. At the beginning of that period, resources start to be available, 206
such as prey, honeydew and pollen, and environmental conditions become optimal. Each year, after their 207
first detection in the orchard, phytoseiids increased until they reach a population peak in late spring and 208
early summer then decreased throughout summer. Phytoseiid assemblages are sensitive to the high 209
temperatures and low relative humidity concentrations registered in summer in the Mediterranean region, 210
as reported by Ferragut et al. (1987) for E. stipulatus in the same area of this study. In the fall season, when 211
the environmental conditions were similar to those of spring, a second population peak was observed. The 212
population dynamics of the phytoseiids found during 2014 and 2016 were quite similar, showing two 213
distinct peaks, one in spring and the other in fall. However, in 2015 the trends were different, especially in 214
the spring peak where mean densities of phytoseiids were lower than 2014 and 2016 for the same period.
215
This can be explained by the climatic conditions of that year with a temperature peak on May 14th with a 216
maximum temperature of 42.64 °C and low RH of 7.02% (STR 2018). Additionally, spring and summer 217
9 average temperatures were higher in 2015 than in 2014 and 2016 (STR 2018). This fact might cause not 218
only lower population densities, but also a later appearance of phytoseiids in the system. However, the 219
phytoseiid populations in all the orchards in 2015 recovered in fall and reached a population density similar 220
to that of the other two years. On the contrary, Akyazi et al. (2016) observed an increase in the number of 221
phytoseiids per leaf obtained in persimmon in the region of Ordu (Turkey), in spring and remained more or 222
less constant until reaching a maximum in fall. This continuous growth was possible due to the high 223
humidity registered in Ordu, where the humidity averages are over 60% throughout the year, which is quite 224
different from the conditions found in our research.
225
As detailed in the introduction E. stipulatus and A. andersoni are key natural enemies for the citrus red mite 226
and the European red mite, respectively. In addition, they can effectively prey on small arthropods such as 227
crawlers of mealybug, coccids too (García-Marí et al. 1983; García-Marí et al. 1986; Ferragut et al. 1988;
228
Costa Comelles et al. 1990; Ferragut et al. 1992; MAGRAMA, 2014). Typhlodromus phialatus is reported 229
in Spanish citrus as a generalist predator that typically feeds on several species of mites and pollen (Ferragut 230
et al. 1987). However, its role in citrus is not entirely clear as it appears sporadically and in isolation. In 231
other Mediterranean crops, such as vineyards and in hazelnuts, its conservation is recommended because it 232
is key in the management of tetranichid mites (Villaronga and García-Mari, 1988; Barbar et al. 2007). The 233
high percentages of presence of T. phialatus found in persimmon suggest that this predatory mite is actively 234
preying on the phytophagous pest species found. The presence of P. talbii was sporadic in persimmon, 235
which corresponds to other studies reporting low abundance in citrus and fruit trees in Spain (Pérez-Moreno 236
1998; Vela et al. 2013).
237
In this work, we have determined how the four arthropod pests found, were overlapping their population 238
peaks throughout the cultivation cycle. It was not possible to find a significant relationship between the 239
phytoseid population levels and the population levels of the four pest species detected in this crop, 240
mealybugs, coccids, thrips and whiteflies. However, when the population of all four pest species was 241
considered, Phytoseiid populations were found to be correlated. The polyphagous nature of the four species 242
of predatory mites found in this crop could explain the lack of relationship with the individual pests 243
populations. The continuous availability of prey through the year could be one of the reasons for the high 244
number of phytoseiids found in these fields, in many occasions superior to one individual per leaf 245
throughout the year. In other crops, where the role of phytoseiids is key, this leaf density is not usually 246
reached (De la Iglesia et al. 2007; Praslika et al. 2009; Abad et al. 2010). This could lead us to think that 247
10 phytoseiids may be key in the regulation of phytophagous pests in this crop. In summary, this research has 248
established the first necessary step to initiate the development of an integrated pest management program 249
in persimmon and opens the door to further studies focused on the conservation of the phytoseiid complex 250
in persimmon and the assessment of its impact on pest populations on this crop.
251
Acknowledgments 252
The research leading to these results was funded by the Conselleria d’Agricultura, Pesca i Alimentació de 253
la Generalitat Valenciana. The authors thank Azucena Gallardo (IVIA) for their technical assistance. MP- 254
H was the recipient of a research fellowship from the INIA Spain (Subprogram DOC-INIA-CCAA) and 255
FOGM the recipient of a grant EU-FSE (Fondo Social Europeo).
256
257
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345 346 347
14 Table 1. Total number of predatory mites identified in four persimmon orchards in Eastern Spain.
348 349
Species
Conventional 1
Conventional 2
Organic 1
Organic 2
TOTAL
Euseius stipulatus 464 98 122 391 1,075
Typhlodromus phialatus 59 118 200 86 463
Amblyseius andersoni 1 13 285 0 299
Paraseiulus talbii 0 2 8 4 14
TOTAL 524 231 615 481 1,851
350 351
15 FIGURE CAPTIONS
352
Figure 1. Population dynamics of phytoseiids per year and orchard throughout the year. a) Conventional 1 353
b) Conventional 2, c) Organic 1 and d) Organic 2. n = number of total phytoseiids counted per orchard and 354
year. Chemical treatments are marked with an arrow (one chlorpyrifos methyl treatment in July 2016 and 355
another one in September 2016 in Conventional 1 orchard whereas a clorpyrifos-methyl treatment in May 356
2015 in Conventional 2 orchard).
357
Figure 2. Seasonal phytoseiid species relative abundances in 2014 in a) Conventional 1 orchard, b) 358
Conventional orchard 2, c) Organic 1 orchard and d) Organic 1 orchard.
359
Figure 3. Seasonal phytoseiid species relative abundances in 2016 in a) Conventional 1 orchard, b) 360
Conventional orchard 2, c) Organic 1 orchard and d) Organic 1 orchard.
361
Figure 4. Population dynamics of mealybugs per year and orchard throughout the year. a) Conventional 1 362
b) Conventional 2, c) Organic 1 and d) Organic 2. n = number of total mealybugs counted per orchard and 363
year. Chemical treatments are marked with an arrow (one chlorpyrifos methyl treatment in July 2016 and 364
another one in September 2016 in Conventional 1 orchard whereas a clorpyrifos-methyl treatment in May 365
2015 in Conventional 2 orchard).
366
Figure 5. Population dynamics of coccids per year and orchard throughout the year. a) Conventional 1 b) 367
Conventional 2, c) Organic 1 and d) Organic 2. n = number of total coccids counted per orchard and year.
368
Chemical treatments are marked with an arrow (one chlorpyrifos methyl treatment in July 2016 and another 369
one in September 2016 in Conventional 1 orchard whereas a clorpyrifos-methyl treatment in May 2015 in 370
Conventional 2 orchard).
371
Figure 6. Population dynamics of thrips per year and orchard throughout the year. a) Conventional 1 b) 372
Conventional 2, c) Organic 1 and d) Organic 2. n = number of total thrips counted per orchard and year.
373
Chemical treatments are marked with an arrow (one chlorpyrifos methyl treatment in July 2016 and another 374
one in September 2016 in Conventional 1 orchard whereas a clorpyrifos-methyl treatment in May 2015 in 375
Conventional 2 orchard).
376
Figure 7. Population dynamics of whiteflies per year and orchard throughout the year. a) Conventional 1 377
b) Conventional 2, c) Organic 1 and d) Organic 2. n = number of total whiteflies counted per orchard and 378
year. Chemical treatments are marked with an arrow (one chlorpyrifos methyl treatment in July 2016 and 379
another one in September 2016 in Conventional 1 orchard whereas a clorpyrifos-methyl treatment in May 380
2015 in Conventional 2 orchard).
381
16 Figure 1
382
Conventional 1
10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 0
1 2 3 4
2014 (n= 1,462)
2015 (n= 421) 2016 (n= 774)
Week
Number of phytoseiids per leaf
Conventional 2
10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 0
1 2 3 4
2014 (n= 1,761)
2015 (n= 1,093) 2016 (n= 1,917)
Week
Number of phytoseiids per leaf
Organic 2
10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 0
1 2 3 4
2014 (n= 1,864)
2015 (n= 1,653) 2016 (n= 2,990)
Week
Number of phytoseiids per leaf
Organic 1
10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 0
1 2 3 4
2014 (n= 1,056)
2015 (n= 815) 2016 (n= 1764)
Week
Number of phytoseiids per leaf
a)
d) c) b)
383 384
17 Figure 2
385
386 387
18 Figure 3
388
389 390
19 Figure 4
391
Conventional 1
10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 0
1 2 3 4 5
a) 2015 (n= 523)
2016 (n= 48)
2014 (n= 1029)
Week
# mealybugs / leaf
Conventional 2
10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 0
1 2 3 4 5
b)
2015 (n= 418) 2016 (n= 584)
2014 (n= 905)
Week
# mealybugs / leaf
Organic 1
10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 0
1 2 3 4 5
c)
2015 (n= 431) 2016 (n= 534)
2014 (n= 271)
Week
# mealybugs / leaf
Organic 2
10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 0
1 2 3 4 5
d)
2015 (n= 35) 2016 (n= 3)
2014 (n= 28)
Week
# mealybugs / leaf
392
20 Figure 5
393
Conventional 1
10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 0
1 2 3
a) 2015 (n= 53)
2016 (n= 117)
2014 (n= 332)
Week
# coccids / leaf
Conventional 2
10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 0
1 2 3 4 6 8
b) 2015 (n= 642
2016 (n= 145)
2014 (n= 879)
# coccids / leaf
Week
Organic 1
10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 0
1 2 3
c)
2015 (n= 1096) 2016 (n= 762)
2014 (n= 206)
# coccids / leaf
Week
Organic 2
10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 0
1 2 3
d)
2015 (n= 633) 2016 (n= 995)
2014 (n= 335)
# coccids / leaf
Week
394
21 Figure 6
395
Conventional 1
10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 0.0
0.1 0.2 0.3 0.4 0.5
a) 2015 (n= 100)
2016 (n= 71)
2014 (n= 215)
Week
# thrips / leaf
Conventional 2
10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 0.0
0.1 0.2 0.3 0.4 0.5
b) 2015 (n= 10
2016 (n= 48)
2014 (n= 10)
# thrips / leaf
Week
Organic 1
10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 0.0
0.1 0.2 0.3 0.4 0.5
c)
2015 (n= 35) 2016 (n= 26)
2014 (n= 41)
# thrips / leaf
Week
Organic 2
10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 0.0
0.1 0.2 0.3 0.4 0.5
d)
2015 (n= 73) 2016 (n= 133)
2014 (n= 18)
# thrips / leaf
Week
396
22 Figure 7
397
Conventional 1
10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 0.0
0.5 1.0 1.5 2.0
a) 2015 (n= 0)
2016 (n= 1)
2014 (n= 0)
Week
# whiteflies / leaf
Conventional 2
10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 0.0
0.5 1.0 1.5 2.0 5 10 15 20
b) 2015 (n= 12)
2016 (n= 1654)
2014 (n= 4)
# whiteflies / leaf
Week
Organic 1
10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 0.0
0.5 1.0 1.5 2.0
c)
2015 (n= 2) 2016 (n= 376)
2014 (n= 0)
# # whiteflies / leaf
Week
Organic 2
10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 0.0
0.5 1.0 1.5 2.0
d)
2015 (n= 4) 2016 (n= 27)
2014 (n= 1)
# whiteflies / leaf
Week
398
