1 Title: Population studies of arthropods present on Melia azedarach, with special
2 reference to Eutetranychus orientalis (Acari: Tetranychidae) and its natural enemies.
3 Authors: González-Zamora J.E., López C., Avilla C.
4
5 Corresponding author: J. E. González-Zamora
7 8 Published version: http://dx.doi.org/10.1007/s10493-011-9476-y 9
10
1
11 Abstract
12 Eutetranychus orientalis has become an important pest of the ornamental tree Melia
13 azedarach in the city of Seville. These trees suffer a total defoliation at the end of summer.
14 Studies were conducted in 2008 (in two zones, A and B) and 2009 (in one zone, A) to
15 determine the arthropod populations present on the trees, with particular interest in the
16 possible natural enemies of E. orientalis. Eutetranychus orientalis accounted for 98.3% of the
17 arthropods found in the leaflets. Two species of phytoseiids were found, Euseius scutalis and
18 Euseius stipulatus, but they only represented 0.2% of the population. The most abundant
19 insect was the predator thrips Scolothrips longicornis, which accounted for 0.9% of the
20 population. The population of E. orientalis reached two peaks in 2008, 325 individuals per
21 leaflet in August, and 100 individuals per leaflet in November. The S. longicornis population
22 closely followed the E. orientalis population, showing a clear predator-prey response in both
23 years. The phytoseiid population did not show such a response to the E. orientalis population.
24 Eutetranychus orientalis was more abundant in the exterior plots of zone A (p=0.019). No
25 differences were found between the different orientations (p>0.251) in zone A, although the
26 rows in this zone showed statistically significant differences between populations (p=0.04).
27 In general, the phytoseiid and S. longicornis populations did not show differences between
28 the plots in zone A. The E. orientalis population was very aggregative (b=1.62) and the S.
29 longicornis population was less aggregative (b=1.37), whereas the phytoseiid population
30 showed a random distribution (b=1.03).
31
32 Keywords: Melia azedarach, Eutetranychus orientalis, Euseius scutalis, Scolothrips
33 longicornis, population dynamics, aggregation parameters.
34
2
35 Introduction
36
37 Eutetranychus orientalis (Klein), known as the oriental red mite and the citrus brown mite, is
38 considered as an important pest of citrus in many countries of Africa, Asia, and certain
39 regions of Oceania, but it has also been recorded in a wide range of other plants (Migeon and
40 Dorkeld 2009; EPPO 2010). The first mention of E. orientalis in Spain occurred in Málaga
41 (south of Spain) in 2001 on citrus, and since then it has spread throughout most of southern
42 Spain, attacking mainly citrus but also other crops such as mango and avocado and other trees
43 as well (García et al. 2003). Eutetranychus orientalis was first detected in the city of Seville
44 (southern Spain) in the summer of 2003, and since then it has become a serious problem in
45 the ornamental tree Melia azedarach L., causing a premature fall of leaves in the middle of
46 summer. Melia azadarach is planted in many parts of Spain to provide shade and to
47 embellish parks, gardens, streets and avenues, as is the case in Seville. The loss of its leaves
48 in summer produces a negative visual impact, together with a lack of shade, which is
49 important in a city like Seville with high levels of insolation and temperatures during this
50 season.
51 The Eutetranychus orientalis mite also attacks the Seville orange Citrus aurantium L.,
52 but the damage caused here is not so important. It has spread throughout citrus groves of the
53 region, together with the very similar species Eutetranychus banksi (McGregor), resulting in
54 degrees of damage of variable importance (García et al. 2003).
55 The chinaberry or paraiso tree, M. azedarach, is native to India, south-east Asia and
56 Australia and it has many different uses, although it is mainly used for timber due its good
57 quality. Melia azedarach is of interest for other reasons. Components related to azadirachtin
58 have been extracted from its seeds and investigated for pest control purposes (Charleston et
59 al. 2006; Hammad and McAuslane 2006; Nathan et al. 2006; El-sawi 2008).
3
60 Although the distribution of M. azedarach extends throughout many parts of the
61 world, there are scarce studies of the arthropod fauna present on this plant, which mainly
62 concerns acari (Song et al. 2006; Song et al. 2008; Migeon and Dorkeld 2009). The presence
63 of pathogens has also been recorded on this tree (Arneodo et al. 2007).
64 The objectives of this study were to determine the arthropod fauna present on M.
65 azedarach in the area of study (the city of Seville), the evolution of populations of the most
66 important arthropods present in the tree (with a special interest in their possible natural
67 enemies), their distribution, and other ecological parameters that could be of interest for
68 developing an integrated pest management plan.
69
70 Material and methods
71 This study was carried out in two areas of the city of Seville (Spain) (37º 23’ 19.22’’ N and
72 5º 59’ 40.02’’ W). The first area was a regular plantation of 12,680 m2 with around 200 trees
73 of M. azedarach planted in rows and columns, located in the Miraflores Park (37º 24’ 21.09’’
74 N and 5º 57’ 50.59’’ W). This area was called the A zone. The second area was about 2700
75 m2 with around 20 dispersed M. azedarach trees. This area was called the B zone, and it was
76 adjacent to the A zone. Sampling started in May 2008 and finished in September 2009, with
77 24 and 19 sampling dates in the A zone (during 2008 and 2009) and the B zone (only 2008),
78 respectively.
79 The A zone in the Miraflores Park was divided up by using a grid with four rows
80 (from A to D) and four columns (from 1 to 4). This produced 16 plots, in which two to three
81 leaves per plot were cut from different trees on each sampling date (with the help of pruning
82 pole to reach the higher branches), amounting to 34 leaves per sampling date. Ten leaves
83 were cut in the B zone from different trees on each sampling date using the same procedure,
84 and all leaves were taken to the laboratory. Since the leaves of M. azedarach are two to three
4
85 times compound leaves and can reach lengths of around 50 cm or more, a basal leaflet was
86 selected from each leaf and closely observed under a stereomicroscope at × 7-45. All
87 arthropods present were recorded and those of particular interest were collected and placed
88 into an alcoholic solution of 70% to determine the species afterwards.
89 Comparisons between zones A and B were made with the Student’s t-test, using the
90 mean population values of the sampling dates. Comparisons between interior vs. exterior
91 plots in the zone A were made with the Student’s t-test, using the mean population values of
92 the plots. Comparisons of mean population values of the plots in zone A were made between
93 orientations (north-south vs. east-west) using a factorial analysis of variance with
94 interactions. Comparisons of mean population values of the plots in zone A were also made
95 between rows and columns using a factorial analysis of variance. If the treatments were
96 significant at p < 0.05, then the differences between the means were determined using
97 Tukey’s HDS test at a 95% confidence level. All data used in each analysis were Ln
98 transformed. All analyses were performed using the Statgraphics package (Statistical
99 Graphics Corporation 2000).
100 Taylor’s power law (s2=amb) (Taylor 1961) was used to study the aggregation of the
101 most significant arthropods found on M. azedarach leaflets. Natural logarithms were applied
102 to the Taylor’s power law to calculate the regression parameters a and b.
103
104 Results
105 Species distribution
106 Acari represented the main group of arthropods observed on the M. azedarach leaves, which
107 accounted for 98.7% of the individuals observed (Table 1). The most important species of
108 acari was E. orientalis, which made up 98.3% of the individuals observed. Stage distribution
5
109 was clearly biased towards eggs, followed by immature stages and females, with males the
110 least abundant.
111 Another phytophagous species present in the leaves was T. urticae, with a very low
112 importance (0.2% of the total population) but with a similar population distribution to E.
113 orientalis. Acari of the families Tenuipalpidae (the species identified was Brevipalpus
114 phoenicis (Geijskes)) and Tideidae were also found, but again with very low numbers,
115 representing less than 0.1% of the total arthropods observed. Phytoseiids were present on the
116 leaves although at low numbers, representing only 0.2% of the arthropod population. Two
117 species of phytoseiids were identified, Euseius scutalis (Athias-Henriot) and Euseius
118 stipulatus (Athias-Henriot), and their population distribution was very different to the
119 phytophagous species, with a greater presence of mobile instars than eggs.
120 Insects were the other group of arthropods observed on M. azedarach leaves (Table
121 1), but they only represented 1.3% of the total population of arthropods. The thrips
122 Scolothrips longicornis Priesner was the most abundant (0.9% of the total population),
123 followed by the scale insect Aonidiella aurantii (Maskell) (0.2% of the total population).
124 Eggs of Chrysopidae were also observed, but at low numbers (less than 0.1% of the total
125 population). Other insects observed included Psocopterans, coccinelllidae larvae and different
126 coccids.
127
128 Population dynamics
129 The evolution of arthropod population dynamics was studied over two years, 2008 and 2009
130 (Fig. 1). Although the vegetative period of M. azedarach was only completed in 2008, the
131 partial evolution of the arthropod populations in 2009 showed a similar pattern.
132 Eutetranychus orientalis increased its population in the middle of summer, reaching a peak of
133 around 325 individuals per leaflet in August 2008. This population quickly decreased at the
6
134 end of August, but increased again in autumn, with the population being maintained at around
135 100 individuals per leaflet in November until December, when the trees lost their leaves near
136 winter. The few data available from 2009 showed a similar pattern: the first observation of E.
137 orientalis was at the end of July 2009, and the next sampling date in September showed an
138 increment in its population, but not as high as in 2008.
139 The main damage caused by E. orientalis to M. azedarach was the loss of leaves,
140 where the trees were left without leaves as soon as the end of August 2008. In October 2008,
141 the trees started to sprout leaves again, but with little vigour. In the year 2009 the trees lost
142 their leaves in lower quantities and much later, around the end of September.
143 Scolothrips longicornis was the principal insect which appeared on M. azedarach
144 leaves during the two-year sampling period. This insect is a known predator of tetranychids,
145 and its population evolution followed closely that of the E. orientalis population in summer,
146 both in 2008 and 2009, reaching 5 and 3 individuals per leaflet, respectively (Fig. 1). Our
147 observations confirmed that larvae (and adults) of this thrips were located on leaflets with E.
148 orientalis, and they were also observed feeding on the eggs and immature stages of the mite.
149 Thrips population was almost nonexistent in autumn 2008.
150 The other arthropods of particular interest observed on the M. azedarach leaves were
151 phytoseiids (Fig. 1). The most important predators of tetranychids used to be phytoseiids, but
152 in the evolution pattern observed in Figure 1 there is no response of the phytoseiids
153 population to the phytophagous mite population. Phytoseiids maintained a population of
154 around 0.2 individuals per leaflet throughout the entire period of sampling, both in 2008 and
155 2009, regardless of the supposed prey population. On no occasion was a phytoseiid observed
156 feeding on any stage of Eutetranychus during manipulation of the leaflets under the
157 stereomicroscope.
158
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159 Distribution and aggregation
160 The populations of E. orientalis, the phytoseiids and S. longicornis were not significantly
161 different between zones A and B, with values of p = 0.367, p = 0.246 and p = 0.133,
162 respectively. The population of E. orientalis was clearly higher in the exterior plots of the A
163 zone (89.2 ± 14.4 individuals per leaflet) compared to the interior plots (37.4 ± 4.7
164 individuals per leaflet), with p = 0.019. There were no significant differences in phytoseiids
165 and S. longicornis populations between the exterior and interior plots, with p = 0.769, and p =
166 0.785, respectively.
167 No significant differences were found between north-south and east-west orientations
168 for E. orientalis and S. longicornis populations, with p values between p = 0.251 and p =
169 0.685. There was a difference in the phytoseiids population in the east-west comparison, with
170 p = 0.045, but the populations were very low. Interactions between north-south and east-west
171 orientations were not significant in any case, with the p values always being higher than
172 0.543.
173 There were differences in the populations of E. orientalis in the analysis of rows (p =
174 0.040), but not in the case of columns (p = 0.777). Row B, with 33.9 ± 3.0 individuals per
175 leaflet, was different from row D, with 103.9 ± 17.3 individuals per leaflet. Populations of
176 phytoseiids and S. longicornis were not statistically different between the rows and the
177 columns, with p values between p = 0.067 and p = 0.732. It was not possible to evaluate the
178 interactions between rows and columns due the lack of degrees of freedom.
179 The mite E. orientalis showed a high aggregation in all of the stages considered
180 (Table 2), with a global value of b = 1.62. Females had a lower b value (1.53), whereas the
181 mobile stages had a higher b value (1.69). The phytoseiids showed a b value near 1 (b =1.03),
182 whereas S. longicornis had a value of b = 1.37.
183
8
184 Discussion
185 Melia azedarach is a common tree in parks, avenues and streets of the city of Seville,
186 although very little information was found on the arthropod fauna of this species (Song et al.
187 2008; Migeon and Dorkeld 2009). After the monitoring program developed in 2008 and
188 partially in 2009, the predominance of the mite E. orientalis over the rest of the arthropods
189 found in this tree was clear. This species of tree has been planted throughout Seville largely
190 because of its lack of significant pest problems, at least until 2003. The rest of the Acari
191 fauna observed on M. azedarach presented very little numerical importance. The other
192 phytophagous mites found were T. urticae and few individuals of the families Tenuipalpidae
193 and Tideidae. Predator mites were represented by the family Phytoseiidae, although also at
194 very low numbers, with two species being found: E. scutalis and E. stipulatus. Euseius
195 scutalis seemed to be more abundant, accounting for 73.3% of the adult females identified.
196 Both species have been previously described in Spain, although it is not very common to see
197 them together due their different ecological preferences (Ferragut and Escudero 1997).
198 The population distribution of E. orientalis was very similar to other phytophagous
199 tetranychids, such as T. urticae and Panonychus ulmi (García-Marí et al. 1991), with a
200 predominance of eggs, followed by immature instars, females and males. This was also the
201 case for T. urticae found on M. azedarach. The phytoseiids presented the opposite case, with
202 mobile stages predominating over the eggs, which represented only 19.4% of the population.
203 The group of insects found was very limited, only representing 1.3% of the arthropods
204 found on M. azedarach. The most important insect species was the thrips S. longicornis,
205 which alone accounted for 71.2% of the insect group. This species is known as a good
206 predator of tetranychids (Gerlach and Sengonça 1985; Oatman et al. 1985). Chrysopidae eggs
207 were found (in some of them only the corion), although no larvae were seen in the samples.
9
208 The most important phytophagous insect species found on the leaflets of M. azedarach was
209 the California red scale, A. aurantii.
210 The population dynamics of E. orientalis on M. azedarach trees in Seville was
211 relatively similar to those found in other countries on different plants, where one or two peaks
212 of its population were found throughout one year (Tanigoshi et al. 1990; KapurGhai and
213 Mandeep 2003; Rabindra et al. 2006; Zhou et al. 2006), although the time of these peaks
214 varied in the different references. The optimal development temperature for E. orientalis is
215 between 25-30 ºC on Albizia lebbek (L.) Benth (Imani and Shishehbor 2009) and between 21-
216 27 ºC on citrus trees (Bodenheimer 1951, quoted in EPPO 2010), and the summer
217 temperatures in Seville (mean temperature around 27-28 ºC in July-August both in 2008 and
218 2009) did not seem to be a problem to its populations, which reached a peak of 350
219 individuals per leaflet in August 2008.
220 Phytoseiids are considered as the main predators of tetranychids, and one of the most
221 promising species is E. scutalis, which can adequately develop feeding on E. orientalis
222 nymphs, with high rm values (between 0.175 and 0.257) (Momen and AbdelKhalek 2008;
223 AlShammery 2010) that are similar or superior to the few rm values (range from 0.094 to
224 0.144) obtained for E. orientalis at different temperatures (Imani and Shishehbor 2009).
225 Euseius scutalis was reported to control E. orientalis populations at non-economical densities
226 in the Jordan valley (Tanigoshi et al. 1990). However, the E. scutalis population found on the
227 M. azedarach leaves in Seville did not seem to respond to the E. orientalis population at all.
228 Furthermore, it seemed to keep a regular level throughout the period of sampling,
229 independently of the supposed prey. Research into phytoseiids able to control E. orientalis
230 populations is very extensive (Fouly 1997; Momen and El-Borolossy 1999; Rasmy et al.
231 2003; Ibrahim et al. 2005; Romeih et al. 2005) but there have been no clear practical results.
232 A promising phytoseiid species is Thyphlodromips (Amblyseius) swirskii (Athias-Henriot),
10
233 which can also adequately develop feeding on E. orientalis (Ali and Zaher 2007; Zaher et al.
234 2007), and it is commercially produced and extensively used in greenhouses of southern
235 Spain to control different pests (Calvo et al. 2009).
236 The most important predator observed during the sampling period was the thrips S.
237 longicornis, with high populations in both years which followed closely the E. orientalis
238 population. Other species of Scolothrips have been cited as feeding on E. orientalis, such as
239 S. indicus Priesner in India (Walter et al. 1995), and different species of Scolothrips are
240 generally considered to be important predators of tetranychids (Gerlach and Sengonça 1985;
241 Oatman et al. 1985; García-Marí and González-Zamora 1999).
242 The mite E. orientalis was most abundant in the exterior part of the M. azedarach
243 plantation of zone A. There were also differences between populations depending on the row
244 considered, with higher populations in the exterior rows, but no differences were observed
245 regarding columns or orientation. Phytoseiids and S. longicornis populations did not show
246 clear differences between the different parts of zone A. This pattern suggests that E.
247 orientalis colonizes an area from the exterior, depending on the row situation, whereas the
248 other two groups of arthropods (phytoseiids and especially thrips) are not conditioned by this
249 aspect.
250 Eutetranychus orientalis populations are very aggregative on the leaflets of M.
251 azedarach (with b values which ranged between 1.52 and 1.69), as occurs with many other
252 tetranychids in different crops (Jones 1990a; García-Marí et al. 1991). On the contrary, the
253 phytoseiids found on M. azedarach had a random distribution (b = 1.03), which in some way
254 reflects a weak association of the phytoseiids with the mite population. This b value differs
255 largely from other b values found for different phytoseiid species which normally feed on
256 tetranychids, where the b values were higher, ranging between 1.23 and 1.59 (Cross 1984;
11
257 Wilson et al. 1984; Jones 1990b; García-Marí et al. 1991). Instead, the thrips S. longicornis
258 showed a relatively high aggregation (b = 1.36), conditioned by the presence of its prey.
259 The problem of E. orientalis in Seville city mainly arises from the visual effect of
260 defoliated trees at the end of summer. An integrated management of this problem should take
261 into account predators of the pest population, improvements in the knowledge of the biology
262 of the arthropods of interest, and should consider a possible joint use of pesticides and
263 substances able to limit mite populations whilst at the same time respecting the natural pest
264 enemies and the environment where they are to be used. Augmentation of predators, via
265 inoculative releases, could be of interest and deserves further study, especially regarding
266 some phytoseiids such as T. swirskii.
267
12
268 Acknowledgements
269 The authors wish to thank Carmen Lora, director of the Miraflores Park of Seville city, for
270 her support and for allowing us the use of the facilities in the park to carry out this work. We
271 also thank Pedro Torrent, from the Servicio de Parques y Jardines of Seville town council, for
272 his help in finding the sampling zones and throughout the period of study. Species of acari
273 were determined and/or confirmed by Francisco Ferragut, from the Universidad Politécnica
274 de Valencia (Spain).
275
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376 Silvae Sinicae 42:89-93
377
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378 379 Table 1 Arthropods found on Melia azedarach leaflets in 2008 and 2009 in the city of 380 Seville (Spain). 381 Number Proportion 382 (%) 383 TOTAL ARTHROPODS 69,516 384 1 Acari 68,627 98.7 385 Tetranychidae 386 Eutetranychus orientalis 68,347 98.3 387 2 388 Eggs 63.5 389 Inmatures 28.4 390 Males 3.2 391 Females 4.9 392 Tetranychus urticae 114 0.2 393 Eggs 63.5 394 395 Mobile instars 36.5 396 Phytoseiidae 143 0.2 397 Eggs 19.4 398 Mobile instars 80.6 399 Euseius scutalis 73.33 400 3 Euseius stipulatus 26.7 401 Others 23 <0.1 402 403 Tenuipalpidae 30.4 404 (Brevipalpus phoenicis) 405 Tydeidae 52.2 406 Others 17.4 407 Insects 889 1.3 408 Scolothrips longicornis 633 0.9 409 (Thysanoptera,Thripidae) 410 411 Neuroptera, Chrysopidae 48 <0.1 412 (eggs) 413 Aonidiella aurantii 170 0.2 414 (Hemiptera, Diaspididae) 415 Others 38 <0.1
416 417 418 419 Arthropods found on 964 leaflets. 420 1Numbers in bold represent proportion re€fered to Total Arthropods. 421 2 Numbers in italics represent proportion within species or group. 422 3 Proportion obtained from 15 females. 423 424 425
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426 Table 2 Agreggation parameters of different arthropods found on Melia azedarach 427 leaflets during 2008 and 2009 in the city of Seville (Spain). 428 No. of Intercept Slope Species and life stage C.I. b R2 observations Ln a ± s.e. b Eutetranychus orientalis Eggs 30 2.23±0.25 1.63 1.49-1.76 0.955 Inmatures+males 29 2.25±0.17 1.67 1.56-1.79 0.970 Females 30 1.55±0.13 1.53 1.40-1.67 0.948 Mobile stages 30 2.09±0.17 1.69 1.57-1.80 0.969 All stages 30 2.40±0.24 1.62 1.50-1.74 0.962 Phytoseiids All stages 30 0.15±0.16 1.03 0.88-1.18 0.868 Scolothrips longicornis All stages 20 1.17±0.15 1.37 1.21-1.52 0.949 429 430 The parameters obtained come from the regression line Ln s2= Ln a+b Ln m, where s2 is the variance and m is the 431 mean of the population. 432 433 434
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435 Figure captions
436
437 Fig. 1 Evolution of Eutetranychus orientalis, Scolothrips longicornis, and phytoseiids
438 on Melia azedarach leaflets during 2008 and 2009 in the city of Seville (Spain). Vertical bars
439 represent the standard error.
440
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2008 2009
441 450 450 442 400 400 443 350 350 444 300 300 445 250 250 200 200 446 150 150
447 100 100 E. orientalis/leaflet 448 50 E. orientalis/leaflet 50 449 0 0 ♦ ♦ ♦ 450 May Jun. Jul. Aug. Sept. Oct. Nov. Dec. May Jun. Jul. Aug. Sept. Oct. Nov. Dec.
451 7 7 452 6 6 453 5 5 454 4 4 3 455 3 2 2 456 1 1
♦ ♦ ♦ S. longicornis/leaflet 457 S. longicornis/leaflet 0 0 458 May Jun. Jul. Aug. Sept. Oct. Nov. Dec. May Jun. Jul. Aug. Sept. Oct. Nov. Dec.
459 0,8 0,8 460 0,6 0,6 461 462 0,4 0,4 463 0,2 0,2
0 0 Phytoseiids/leaflet
May Jun. Jul. Aug. Sept. Oct. Nov. Dec. Phytoseiids/leaflet May Jun. Jul. Aug. Sept. Oct. Nov. Dec.
22