artropodos_olivar

Use of arthropods for the evaluation of the olive-orchardmanagement regimes

Francisca Ruano*, Carlos Lozano*, Pedro Garcia, Aranzazu Pena*, Alberto Tinaut, Felipe Pascualand Mercedes Campos*

*Department of Agroecology and Plant Protection, Estacion Experimental del Zaidn, CSIC, c/ Prof. Albareda 1, 18008 Granada, Spain,

Departments of yStatistic and O.I. and zAnimal Biology and Ecology, University of Granada, Granada, Spain

Abstract 1 The presence and abundance of arthropods were compared in three oliveorchards under organic, integrated and conventional management regimes. Ineach olive orchard, trees were sampled in the canopy by beating branches andsoil arthropods by placing pitfall traps. Contrary to expectations, the highestabundance of arthropods occurred in the integrated management orchard. Themost abundant groups were Formicidae and the species Euphyllura olivinae(Homoptera: Psyllidae).

2 Canopies and the soil under the tree canopy (interior soil) were selected as themost informative sites for sampling. The months with the strongest differenceswere May, June and July, especially June. In the canopy, Araneae, Coleoptera,Diptera, Heteroptera, Hymenoptera, Homoptera, Lepidoptera, Neuroptera andThysanoptera were the most abundant, and showed significant differences inabundance among orchards with different management regimes. Moreover, inthe canopies, Coleoptera and Lepidoptera showed a seasonal pattern of abund-ance and consistent significant differences between the organic orchard vs. theintegrated and conventional ones in both years of study. In the soil, 12 ordersshowed significant differences in abundance among management regimes atsome point of the sampling season.

3 In a search for biological indicators that could help to distinguish betweenmanagement regimes, a discriminant analysis applied to the data indicated thatonly the samples from the canopy were classified according to their manage-ment regime in a consistent way over time. The groups selected by the analysisto establish differences among management regimes were Coleoptera, Diptera,Heteroptera, Lepidoptera and Thysanoptera. The analysis applied to compareorganic vs. non-organic olive orchards, again identified Coleoptera and Lepi-doptera as suitable groups. The results suggest that these two orders arepotential bioindicators to distinguish, in a simple way, organic olive orchardsfrom non-organic ones.

Keywords Arthropods, bioindicators, IPM, olive, management, organic farm-ing, pesticides.

Introduction

Olives are one of the principal crops in theMediterranean area,

and, for years, pest management has reliedmostly on the use of

pesticides. However, in the last few decades, the negative envir-

onmental effects of the excessive use of these chemicals (Heim,

1985; Cirio, 1997; Civantos, 1999) has resulted in a tendency

towards agricultural strategies of low environmental impact,

such as integrated production and organic farming. There

is currently a heavy demand for products derived from these

agricultural methods. In this sense, governments have devel-

oped legislation to regulate and support olive orchardsCorrespondence: Dr Francisca Ruano. E-mail: francisca.ruano@

eez.csic.es

Agricultural and Forest Entomology (2004) 6, 111120

# 2004 The Royal Entomological Society

cultivated under these practices, by controlling the release and

the levels of certain chemicals (Malavolta et al., 2002). This has

created a need for reliable monitoring of these substances in

soil, plants and products. Conventional analytical techniques

(gas chromatography and mass spectophotometry) are being

applied for this purpose, which, although precise, are expensive

(Denninson & Turner, 1995).

A complementary technique may be based on the use of

biological indicators. The use of bioindicators to derive bio-

logical information on certain environmental variables has a

long tradition (Van Straalen & Verhoef, 1997). Specifically,

arthropods have been used as indicators of a range of envir-

onmental attributes since the beginning of the 20th century

(Cairns & Pratt, 1993; Brown, 1997). For example, in agro-

ecosystems, spiders have been recommended as indicators for

early detection of insecticide side-effects on predatory arthro-

pods (Everts et al., 1989), carabid beetles have been used as

bioindicators of crop management (Holland & Luff, 2000),

and ant species have been used as indicators of agroecosystem

and grassland conditions (Peck et al., 1998; New, 2000).

In the olive orchard, there is a large number of arthropod

species (Arambourg, 1986;DeAndres, 1991;Varela&Gonzalez,

1999; Campos & Civantos, 2000; Ruz & Montiel, 2000)

that might potentially be used as indicators to evaluate the

different types of olive management (Cairns & Pratt, 1993;

Brown, 1997). The arthropod community in olive orchards

includes mainly phytophagous (some of which are major

pests), parasitoid and predatory species. Parasitoid species

are the most abundant, consisting of approximately 300400

Hymenoptera species (Arambourg, 1986). Predators are repre-

sented by several groups, with spiders, beetles and ants being

the most diverse (Morris, 1997; Morris et al., 1999). Ants are

the most abundant and have been proposed as possible bio-

indicators of pesticide pollution by Redolfi et al. (1999).

The aim of the present study was to provide information

on the most appropriate sampling sites and date, as well as

the arthropod orders that can differentiate the various man-

agement regimes in olive orchards. Consequently, we ana-

lysed changes in arthropod fauna corresponding to different

sampling sites: (i) canopy; (ii) the soil under the tree canopy

(interior soil); and (iii) the soil not influenced by the shadow

of the tree (exterior soil), between March and October of

1999 and 2000, with respect to the different management

regimes (organic, integrated and conventional). With this

information, we sought to establish a method based on

bioindicators, using low sampling effort and easy taxo-

nomic identification, that can detect the absence of pesticide

application and crop sustainability.

Materials and methods

Study zones

The study was conducted in 1999 and 2000 in three com-

mercial olive orchards (Colomera, Arenales and Deifontes)

20 km north of Granada (southern Spain). These three sites

were in an area of large olive orchards ranging between 200

and 500 ha. They were some 4 km apart from each other,

located at similar altitudes and with similar environmental

characteristics, but were under different management regimes.

The Colomera orchard was under conventional intensive

management, Arenales was under integrated pest manage-

ment (IPM) and Deifontes was under organic management.

Colomera was drip irrigated every 15 days, frequently

ploughed deeply and, according to farmers information,

received three annual treatments of different insecticides

and herbicides.

First, in March or April, a dimethoate spray (150mL/ha

of the EC formulation at 40%) against the phylophagousgeneration of Prays oleae Bern., and a soil treatment with

the herbicide simazine (4L/ha of the formulation at 50%)were applied.

Second, in June, an alpha-cypermethrin spray (37.5mL/hL

of the SC formulation at 4%) against anthophagousgeneration of P. oleae was applied.

Finally, in October, a dimethoate spray against Bactrocera

oleae and a second treatment with simazine were applied.

In addition, the presence of these pesticides was moni-

tored during the years of study (Table 1).

Arenales, under IPM, was flood irrigated twice per sum-

mer and ploughed deeply from the end of May to the

beginning of June. Only one treatment with dimethoate,

was applied against the anthophagous generation of

P. oleae in June 2000 and, during both study years, two

soil treatments were made with simazine in March and in

Table 1 Pesticide residues (mg/g) determined in the conventional management (Colomera) and integrated management (Arenales) over thesampling periods: March 1999 to October 2000

1999 2000

Month 3 4 5 6 7 8 9 10 3 4 5 6 7 8 9 10

Colomera: conventional management

Dimethoate * 2.2 0.9 1.0 ND ND ND ND ND 0.5 0.1 2.7 0.7 0.5 0.1 14.2

acypermethrin ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND NDSimazine 0.5 0.3 * 0.2 0.1 0.1 < 0.1 ND 0.4 0.1 < 0.1 0.2 0.1 0.1 0.1 0.1

Arenales: integrated management

Dimethoate ND ND ND ND ND ND ND ND ND ND ND ND 3.5 1.8 1.0 0.1

acypermethrin ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND NDSimazine 0.4 0.3 * 0.1 < 0.1

September. Similarly to Colomera, residues of dimethoate

and simazine were also found in this orchard (Table 1).

Finally, Deifontes, the organic olive orchard, was drip

irrigated bi-weekly in the summer, ploughed only to a shal-

low depth (10 cm) from the end of May to the beginning of

June, and neither Bacilllus thuringiensis Berliner nor per-

mitted insecticides were applied during our study. No pesti-

cide residues were found during the study period.

Collection of arthropods

In each olive orchard, a plot with a total of 144 olive trees

(12 12) was randomly selected. Taking into account theexpected variability of the arthropod fauna, data from olive

orchards previously studied (Morris, 1997; Redolfi et al.,

1999) were then used to calculate the sampling size required

(Som, 1973). The result of this calculation comprised a

sampling size of 30 trees.

Thus, monthly from March to October in 1999, 30 trees

were chosen at random in each plot and sampled by beat-

ing, five times, four branches per tree (one per orientation),

also chosen at random, over an insect net of 50 cm in

diameter. Moreover, in 1999, two pitfall traps were placed

below each of these trees. As previously described byMorris

(1997), one trap was situated just below the tree (interior

soil) and the other one beyond the canopy of the tree, in a

northerly orientation (exterior soil). The pitfall traps con-

sisted of a 200-mL plastic glasses with a 7-cm opening, filled

half way with water and detergent. Traps were placed in

holes dug carefully with a minimum of soil and vegetation

disturbance so that the lip of the trap was even with the soil

surface. The traps were left in place for 24 h. In 2000, taking

into account the results from 1999, the required number of

samples was recalculated to 25 trees. A comparison with the

results for 1999 showed the absence of significant differ-

ences between samples of interior and exterior soil. Thus,

only the traps of the interior soil were analysed in 2000.

Samples from both the canopy and the soil were frozen

and, subsequently, the arthropods were separated from

vegetal and inorganic remains. Adults and juveniles were

identified to the taxonomic level of order and the total

number of each taxon recorded. Orders absent in more

than 80% of the samples, and representing less than 1% ofthe total individuals, were not considered in the statistical

analysis. The family Formicidae was separated from the

other Hymenoptera, and was considered as an independent

group due to its abundance. Thus, when we refer to other

Hymenoptera, we exclude Formicidae.

Statistical analysis

The abundance of the different orders captured was com-

pared among sampling sites (canopy, interior soil and exter-

ior soil), and among management regimes (conventional,

integrated and organic), by means of analysis of variance

(ANOVA), after checking the assumptions of the method

(normality, homoscedasticity using the Levene test, and

lack of correlation among variables) by means of the Durbin-

Watson test to evaluate the lack of correlation between

observations over time. Post hoc ANOVA multiple compari-

sons were performed using the Bonferroni test.

A discriminant analysis was performed using the groups

that showed significant differences in abundance to estab-

lish whether differences among management regimes would

arise. The discriminant analysis was performed in different

ways, either considering each month separately or grouping

them, and also grouping samples in different sizes (i.e. put-

ting together the samples in groups of 2 2, 3 3, etc).

Results

Arthropod abundance

The total number of specimens collected over the 2 years of

study in the conventional, integratedandorganic orchardswere

11 849, 77475 and 36095, respectively. The highest numbers

were captured in May and June, followed by July (Fig. 1).

The specimens were classified into 20 orders, each found in all

three olive orchards, although seven orders (Dermaptera,

Dictyoptera, Embioptera, Orthoptera, Scolopendromorpha,

0

20

40

60

80

100

120

140

160

3 4 5 6 7 8 9 10

ConventionalIntegratedOrganic

Mea

n of

indi

vidu

als

by tr

ap

Month

1999

0

50

100

150

200

250

3 4 5 6 7 8 9 10

2000

Mea

n of

indi

vidu

als

by tr

ap

Month

Figure 1 Seasonal evolution of the mean abundance of individuals

per sample in each management regime: conventional, integrated

and organic. Bars indicate the standard error.

Arthropods for the evaluation of olive management 113

# 2004 The Royal Entomological Society, Agricultural and Forest Entomology, 6, 111120

Thysanura and Trichoptera) were not considered in the statis-

tical analysis because of their scarcity. The 13 remaining orders

are listed in Tables 24. In the integrated and organic orchards,

the most abundant groups were Homoptera and Formicidae

(Hymenoptera), although the most abundant group in the

organic orchard was Diptera in the year 2000 (Tables 2 and

4). In the conventional orchardAcari, Collembola, Coleoptera,

Diptera, Formicidae (Hymenoptera) and Homoptera were the

most abundant groups (Table 3).

The abundance of Homoptera was a consequence of the

presence of the olive pest Euphyllura olivina Costa (Homo-

ptera: Psyllidae) in both sampling years. This species repre-

sented 95% of individuals of this order, being particularlyabundant in the integrated orchard. The presence of this

pest could be coincidental, and due to factors other than the

management regime. Therefore we did not consider this

order as a possible bioindicator, but rather sought more

stable groups in all three olive orchards.

Table 2 Total numbers of individuals, mean and standard deviation (SD), of each order of arthropod captured in each sampling site in Arenales,

orchard under integrated management

1999 2000

Canopy Interior soil Exterior soil Canopy Interior soil

Total Mean SD Mean SD Mean SD F2,>700 P Total Mean SD Mean SD F1,> 390 P

Acari 1597 0.03a 0.17 3.38b 10.43 3.29b 8.25 14.7 < 0.001 391 0.01a 0.10 1.96b 4.55 89.0 < 0.001

Araneae 593 1.44b 1.78 0.57a 1.06 0.49a 0.77 40.5 < 0.001 229 0.56a 0.83 0.59a 0.88 0.28 0.592

Collembola 1141 0.00a 0.00 1.34b 3.40 3.43c 5.68 48.7 < 0.001 379 0.02a 0.16 1.90b 3.61 150.1 < 0.001

Coleoptera 699 0.44a 0.71 1.59c 4.01 0.91b 1.36 12.8 < 0.001 244 0.63a 1.21 0.60a 1.00 1.8 0.183

Diptera 670 0.84a 1.77 1.27b 2.23 0.70a 1.13 6.8 0.001 3283 10.05b 15.84 6.43a 14.49 7.7 0.006

Formicidae 18730 0.59a 1.57 66.01c 230.00 12.27b 18.30 16.5 < 0.001 6023 0.24a 1.37 30.18b 145.28 20.0 < 0.001

Heteroptera 290 1.01b 2.00 0.11a 0.47 0.10a 0.48 43.7 < 0.001 1030 5.02b 12.82 0.14a 0.63 120.7 < 0.001

Hymenoptera 507 1.70b 2.52 0.26a 0.63 0.15a 0.42 77.3 < 0.001 507 0.70b 1.10 0.33a 0.97 18.1 < 0.001

Homoptera 15386 64.05b 66.01 0.49a 0.99 0.38a 0.78 221.4 < 0.001 24469 121.47b 139.64 0.89a 1.67 219.3 < 0.001

Isopoda 25 0.01a 0.09 0.09a 0.81 0.00a 0.06 2.6 0.07 7 0.00a 0.00 0.04b 0.19 31.4 < 0.001

Lepidoptera 146 0.42c 0.85 0.16b 0.41 0.04a 0.19 29.9 < 0.001 137 0.52b 1.16 0.17a 0.47 37.6 < 0.001

Neuroptera 256 1.06b 1.51 0.02a 0.16 0.00a 0.00 113.6 < 0.001 458 2.22b 3.94 0.08a 0.28 99.1 < 0.001

Psocoptera 118 0.11a 0.40 0.14a 0.47 0.24a 1.23 1.7 0.176 80 0.00a 0.07 0.40b 0.97 152.0 < 0.001

Thysanoptera 54 0.19b 0.62 0.03a 0.16 0.01a 0.11 16.2 < 0.001 26 0.11b 0.34 0.02a 0.14 51.1 < 0.001

40212 37263

Different letters indicate significant differences among sampling sites, for the same year, ANOVA test.

Table 3 Total numbers of individuals, mean and standard deviation, of each order of arthropod captured in each sampling site in Colomera,

orchard under conventional management

1999 2000


Total Mean SD Mean SD Mean SD F2,> 700 P Total Mean SD Mean SD F1,>390 P

Acari 839 0.07a 0.33 2.09b 8.08 1.35b 3.81 9.4 < 0.001 618 0.00a 0.00 3.14b 6.00 156.6 < 0.001

Araneae 384 0.92c 1.63 0.42b 0.69 0.27a 0.62 23.8 < 0.001 163 0.52b 1.05 0.30a 0.60 11.7 0.001

Collembola 1529 0.00a 0.00 2.05b 5.94 4.37c 7.01 40.4 < 0.001 1263 0.00a 0.00 6.41b 10.18 208.5 < 0.001

Coleoptera 891 0.57a 1.21 1.18b 2.33 1.98c 3.30 20.2 < 0.001 261 0.34a 0.66 0.98b 1.52 28.3 < 0.001

Diptera 265 0.38a 0.78 0.49b 0.99 0.24a 0.55 5.6 0.004 1834 2.88a 5.05 6.43b 12.68 37.7 < 0.001

Formicidae 1000 0.03a 0.19 3.48b 12.20 0.65a 2.77 15.6 < 0.001 423 0.04a 0.26 2.11b 7.00 31.3 < 0.001

Heteroptera 77 0.21b 0.45 0.06a 0.25 0.05a 0.23 17.7 < 0.001 37 0.17b 0.49 0.02a 0.14 73.4 < 0.001

Hymenoptera 147 0.46b 0.79 0.08a 0.33 0.07a 0.32 41.8 < 0.001 120 0.24a 0.51 0.37a 1.98 3.0 0.082

Homoptera 776 1.63b 2.12 0.66a 2.00 0.96a 2.00 9.2 < 0.001 487 2.18b 2.50 0.29a 0.87 108.7 < 0.001

Isopoda 7 0.00a 0.00 0.03a 0.23 0.00a 0.00 3.8 0.023 10 0.00a 0.00 0.05b 0.22 46.8 < 0.001

Lepidoptera 127 0.32b 0.88 0.11a 0.37 0.10a 0.35 10.8 < 0.001 37 0.10a 0.33 0.09a 0.32 0.8 0.368

Neuroptera 257 1.02b 1.42 0.05a 0.24 0.00a 0.06 114.1 < 0.001 156 0.72b 1.17 0.07a 0.26 158.8 < 0.001

Psocoptera 69 0.12a 0.39 0.05a 0.23 0.12a 0.37 2.7 0.065 5 0.03b 0.19 0.01a 0.10 4.1 0.044

Thysanoptera 64 0.23b 0.53 0.01a 0.11 0.03a 0.19 31.0 < 0.001 3 0.12b 0.39 0.02a 0.12 52.9 < 0.001

6432 5417

Different letters indicate significant differences among sampling sites, for the same year, ANOVA test.

114 F. Ruano et al.


Comparison between sampling sites: canopy vs. soil

In 1999, the comparison between interior and exterior soil

showed no significant differences in the three areas for

Coleoptera, Heteroptera, otherHymenoptera (without taking

into account the Family Formicidae), Homoptera, Neuro-

ptera and Thysanoptera. The other groups either did not

differ statistically or they were significantly more abundant

in the interior soil, depending on the management regime

considered (Tables 24). Collembola was the only order

significantly more abundant in the exterior soil compared

to the interior soil in the orchards under conventional and

integratedmanagement (Tables 2 and 3).However, Collembola

from the exterior soil did not differ among management

regimes. Therefore, the analysis of the 1999 sampling period

indicated that the orders found in the exterior soil did not

show significant differences for identifying the management

regimes (Tables 24).

Thus, the most abundant orders in both study years

(Tables 24), Araneae, Heteroptera, Homoptera, Lepidop-

tera, Neuroptera and Thysanoptera, were generally found

in higher numbers in the olive canopies than in the soil of

the three olive orchards, whereas Acari, Collembola and

Formicidae were mainly found in the soil. Other groups,

such as Coleoptera, Diptera, Hymenoptera, Isopoda and

Table 4 Total numbers of individuals, mean and standard deviation, of each order of arthropod captured in each sampling site in Deifontes,

orchard under organic management

1999 2000


Total Mean SD Mean SD Mean SD F2,>700 P Total Mean SD Mean SD F1,>390 P

Acari 1222 0.07a 0.67 3.38c 8.39 1.67b 4.21 22.2

Psocoptera, showed different patterns of abundance, being

equally or more abundant at one site or at the other,

depending on the management regime and year considered.

Thus, comparisons among management regimes were per-

formed for each sampling site separately, taking into account

the differences between canopy and soil found.

Comparison among management regimes:conventional, integrated and organic

In the canopy, the month in which greatest number of

orders was significantly affected by management regimes

was June (10 orders in 1999, eight orders in 2000), followed

by July (seven orders in 1999, eight orders in 2000) and May

(seven orders in 1999, five orders in 2000). In addition, eight

orders were significantly affected in March 1999, and seven

orders in September 2000 (Tables 5 and 6). In the interior

soil (Table 7), between April and October 1999, a similar

number of orders per month (six or seven orders) were

significantly different, except in August in which no order

was significantly affected by management regime. Never-

theless, in 2000, May (with differences in eight orders), June

(eight orders) and July (eight orders) had the greatest num-

ber of differences among management regimes (Table 8).

The abundance of all 10 orders presented in Tables 5 and

6 significantly differed at certain points during the sampling

periods. Araneae were more abundant in the organic orch-

ard in both years, differentiating the organic crop from the

other two in June of both years, and also in September of

1999, as well as July and August of 2000 (Tables 5 and 6).

Table 6 Results from the ANOVA test applied to samples obtained in the canopy during the year 2000. Comparisons were performed for each of

the orders of arthropods present in the three different types of management

Canopy 2000

March April May June July August September October

F2,87 P F2>86 P F2,87 P F2,87 P F2,>85 P F2,87 P F2,> 86 P F2,87 P

Araneae 6.18 c-io*** 3.60 NS 2.46 NS 4.70 o-ic* 9.61 o-ic*** 12.80 o-ic*** 5.46 o-i** 4.68 c-i*

Coleoptera 18.26 i-oc*** 2.37 NS 2.39 NS 9.30 o-ic*** 9.23 o-ic*** 9.09 o-ic*** 9.47 o-ic*** 2.63 NS

Diptera 11.34 i-oc*** 11.58 i-oc*** 7.85 c-io*** 20.18 c-io*** 1.06 NS 3.87 c-i* 0.51 NS 8.83 o-ic***

Formicidae 0.55 NS 2.19 NS 0.97 NS 8.01 o-ic*** 12.68 o-ic*** 1.78 NS 0.73 NS 10.99 o-ic***

Heteroptera 0.50 NS 4.29 i-oc* 18.90 i-oc*** 189.91 c-i-o*** 8.81 o-ic*** 9.26 o-ic*** 5.45 o-i*** 0.36 NS

Hymenopteraa 2.21 NS 13.39 i-oc*** 2.93 NS 3.36 NS 7.75 o-ic*** 2.10 NS 3.30 o-c* 3.11 NS

Homoptera 35.03 c-i-o*** 33.37 i-oc*** 79.62 i-oc*** 88.92 i-oc*** 48.93 i-oc*** 33.65 i-oc*** 47.82 i-oc*** 7.89 i-oc***

Lepidoptera 1.15 NS 4.98 o-c* 7.41 c-io*** 17.71 o-ic*** 3.60 o-c* 2.78 NS 6.58 i-oc*** 2.76 NS

Neuroptera 4.38 i-c* 2.28 NS 11.21 i-oc*** 2.18 NS 3.65 i-c* 10.64 i-oc*** 26.67 i-oc*** 26.57 i-oc***

Thysanoptera 2.25 NS 1.39 NS 1.41 NS 13.44 o-ic*** 2.08 NS 1.04 NS 1.00 NS

*0.05>P 0.01; **0.01>P 0.005; ***P< 0.005). Letters after P-values separated by a hyphen refer to the management regimes significantlydifferent for the corresponding order of arthropod; letters together do not show significant differences (post hoc multiple comparisons Bonferronitest) (c, conventional; I, integrated; o, organic management). aThis group includes only Hymenoptera other than Formicidae.

Table 7 Results from the ANOVA test applied to samples obtained in the interior soil during the year 1999. Comparisons were performed for each

of the orders of arthropods present in the three different types of management

Interior soil 1999


F2,87 P F2>86 P F2,87 P F2,87 P F2,> 85 P F2,87 P F2,> 86 P F2,87 P

Acari 0.83 NS 2.06 NS 2.20 NS 0.24 NS 0.10 NS 0.92 NS 5.22 o-i** 2.22 NS

Araneae 0.70 NS 0.7 NS 4.47 i-oc* 3.11 NS 2.62 NS 1.47 NS 6.01 c-io*** 4.14 o-i*

Collembola 14.64 o-ic*** 6.19 o-ic*** 5.90 o-ic*** 6.48 c-io*** 10.60 c-io*** 0.94 NS 0.48 NS 19.46 c-io***

Coleoptera 3.96 o-i* 3.03 NS 5.56 i-o** 3.09 NS 1.36 NS 0.70 NS 11.05 c-io*** 4.52 o-c*

Diptera 9.87 i-oc*** 11.70 c-io*** 2.24 NS 6.63 i-c*** 2.34 NS 3.02 NS 12.26 o-ic*** 2.46 NS

Formicidae 10.33 i-oc*** 12.29 i-oc*** 4.80 i-oc* 16.57 i-oc*** 4.30 i-c* 0.41 NS 2.17 NS 0.73 NS

Heteroptera 3.82 o-c* 2.23 NS 2.17 NS 0.82 NS 6.18 o-ic*** 2.84 NS 2.90 NS 4.46 o-ic*

Hymenopteraa 2.94 NS 1.70 NS 3.09 NS 12.96 o-ic*** 8.37 o-ic*** 2.67 NS 4.09 i-c* 0.57 NS

Homoptera 3.02 NS 6.47 i-c*** 5.38 o-ic** 7.30 o-ic*** 5.14 o-ic** 0.03 NS 4.82 i-oc* 12.05 c-io***

Isopoda 3.18 NS 7.39 o-ic*** 3.66 o-c* 0.43 NS 6.10 o-ic*** 2.09 NS 3.95 o-c* 8.37 o-ic***

Lepidoptera 3.22 NS 1.02 NS 1.70 NS 8.21 i-oc*** 0.98 NS 2.25 NS 0.07 NS 0.50 NS

Thysanoptera 2.07 NS 5.19 o-ic** 1.68 NS 3.26 o-c* 1.00 NS 1.01 NS 1.00 NS

*0.05>P 0.01; **0.01>P 0.005; ***P< 0.005. Letters after P-values separated by a hyphen refer to the management regimes significantlydifferent for the corresponding order of arthropod; letters together do not show significant differences (post hoc multiple comparisons Bonferronitest) (c, conventional; I, integrated; o, organic management). aThis group include only Hymenoptera other than Formicidae.

116 F. Ruano et al.


Diptera did not show a constant pattern in abundance over

the 2 years, being more abundant in 2000. Heteroptera did

not show a constant pattern in significant differences over

the 2 years, also being found in higher numbers in 2000 than

in 1999, and being more abundant under integrated and

organic management than under the conventional one,

especially in June. Heteroptera differentiated the conven-

tional orchard from the other two in March and June of

1999, and the three types of management regimes in June of

2000. Homoptera were most abundant in the integrated

orchard. In 1999, this order showed significant differences

in abundance among the three management systems

throughout May, July, August, September and October.

In 2000, the abundance of this order was significantly dif-

ferent in the integrated orchard and the other two regimes

throughout the sampling season, except in March, when

three management regimes all were significantly different.

Orders having a stable pattern of abundance over the

2 years of sampling were Coleoptera, Lepidoptera and Thy-

sanoptera (Fig. 2). The former two orders showed signifi-

cant differences between organic and non-organic

management (integrated and conventional) in a stable way

over the 2 years of sampling (Tables 5 and 6). Coleoptera

differed significantly between the organic orchard and the

non-organic management system in March, June, July,

August and September of both years, whereas Lepidoptera

differed only in June

In the soil, the 12 orders presented in Tables 7 and 8

showed significant differences in abundance in the three

olive orchards at some points during the sampling periods.

Collembola, Hymenoptera excluding Formicidae and Iso-

poda were in general more abundant in the organic orchard,

and Formicidae in the integrated one. The abundance of

Collembola in March and April of both years, and Isopoda

in April, July and October of 1999, as well as in March, and

from May to October in 2000 distinguished the organic

from the non-organic orchards. However, Collembola

were more abundant in the orchard under conventional

management in June and July than under both other

regimes. Formicidae were significantly more abundant in

the crop under integrated management between March and

June of 1999, and in April of 2000.

According to the results, Coleoptera, Lepidoptera and

Thysanoptera in the canopy, and Isopoda in the soil, were

significantly more abundant in the organic olive orchard,

but only the former three had a consistent pattern of abun-

dance (Fig. 2) whereas only Coleoptera and Lepidoptera

showed a consistent pattern of significant differences in

both study years. Homoptera in the canopy and Formicidae

in the soil were significantly more abundant in the inte-

grated olive orchard. In general, the different groups were

less abundant in the conventional orchard with respect to

either or both of the other two orchards.

Discriminant analysis

Using the mean number of specimens/trap for eachmonth, we

performed a discriminant analysis using the groups, Araneae,

Coleoptera, Diptera, Heteroptera, Lepidoptera and Thysa-

noptera. Homoptera was not taken into account as explained

previously. In relation to the soil, the groups used were

Collembola, Formicidae, other Hymenoptera and Isopoda.

The best results from the discriminant analysis, for both

canopy and soil took into account only the samples of June

in groups of 5 5. With this analysis, 88.9% and 100% ofthe samples from the canopy in 1999 and 2000, respectively,

were correctly classified according to their management

regime (Fig. 3) using only four groups, Coleoptera, Diptera,

Heteroptera and Thysanoptera. In addition, the coefficients

of the two canonical discriminant functions were coherent

in both years (Table 9), signifying that the results were

stable over time.

Table 8 Results from the ANOVA test applied to samples obtained in the interior soil during the year 2000. Comparisons were performed for each

of the orders of arthropods present in the three different types of management

Interior soil 2000


F2,87 P F2>86 P F2,87 P F2,87 P F2,>85 P F2,87 P F2,>86 P F2,87 P

Acari 1.64 NS 3.41 i-c* 8.08 i-oc*** 0.63 NS 3.13 NS 6.64 i-c*** 0.60 NS 3.36 o-c*

Araneae 2.80 NS 4.62 i-oc* 5.20 o-i** 3.80 i-o* 1.37 NS 2.24 NS 0.82 NS 9.43 c-io***

Collembola 7.66 o-ic*** 26.29 o-ic*** 6.32 c-i*** 17.53 c-io*** 34.81 c-io*** 2.50 NS 6.17 c-io*** 0.11 NS

Coleoptera 2.24 NS 1.72 NS 10.63 i-oc*** 14.66 o-ic*** 6.97 o-i*** 1.11 NS 0.10 NS 16.11 o-ic***

Diptera 0.06 NS 9.00 i-oc*** 23.87 o-ic*** 20.17 o-ic*** 8.43 o-i*** 3.09 NS 4.81 o-ic* 5.11 c-io**

Formicidae 4.08 i-c* 9.11 i-oc*** 1.19 NS 4.20 i-c* 14.04 o-ic*** 3.95 o-c* 3.30 NS 7.12 o-ic***

Heteroptera 0.95 NS 1.18 NS 6.97 i-oc*** 5.42 o-i** 5.15 o-ic** 0.50 NS 1.04 NS

Hymenopteraa 1.65 NS 10.89 i-oc*** 4.38 o-c* 2.24 NS 3.63 o-i* 0.52 NS 2.58 NS 1.44 NS

Homoptera 5.74 o-ic** 16.37 o-ic*** 9.18 o-c*** 4.48 o-c* 4.07 o-c* 2.11 NS 2.90 NS 2.23 NS

Isopoda 5.43 o-ic** 1.60 NS 17.24 o-ic*** 10.62 o-ic*** 13.07 o-ic*** 14.50 o-ic*** 11.09 o-ic*** 8.48 o-ic***

Lepidoptera 1.91 NS 0.96 NS 0.63 NS 0.02 NS 2.10 NS 1.20 NS 0.53 NS 2.25 NS

Thysanoptera 1.38 NS 1.70 NS 1.44 NS 2.80 NS 0.98 NS

*0.05>P 0.01; **0.01>P 0.005; ***P< 0.005. Letters after P-values separated by a hyphen refer to the management regimes significantlydifferent for the corresponding order of arthropod; letters together do not show significant differences (post hoc multiple comparisons Bonferronitest) (c: conventional, i: integrated, o: organic management). aThis group include only Hymenoptera other than Formicidae.



10/0

09/

008/

007/

006/

005/

004/

003/

00

10/9

99/

998/

997/

996/

995/

994/

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99

Mean

of C

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opt

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8

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Me

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hysa

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4

3

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4

3

2

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0

IntegratedConventionalOrganic

Figure 2 Mean of individuals per sample from the canopies.

Represented groups (Coleoptera, Lepidoptera and Thysanoptera)

are those that demonstrated a stable pattern of abundance

throughout the 2 years of sampling.

centroid of groupintegratedconventionalorganic

JUNE 1999

3

2

1

0

1

2

3

4

Fun

ctio

n2

3 2 1 0 1 2 3 4 5

6

4

2

0

2

4

6

8

Funct

ion

2

20 15 10 5 0 5 10 15 20 25 30

Function 1

JUNE 2000

Function1

Figure 3 Distribution of the samples of year 1999 and 2000, in

accordance with the values from the canonical discriminant function.

Table 9 Standardized coefficients for the orders of arthropods sel-

ected by the discriminant analysis performed, on the two canonical

axes, for the years 1999 and 2000

Function

1999 2000

1 2 1 2

Coleoptera 0.740 0.640 1.368 0.387Diptera 0.877 0.411 0.400 1.520Heteroptera 0.232 1.622 1.657 0.042Thysanoptera 0.547 1.689 0.427 1.089Percent of correct classification 89.9 100

The percentage of correct classification of the groups of samples isalso shown.

118 F. Ruano et al.


Organic and non-organic olive orchards were also com-

pared. Again, with June and samples of size five, 100% ofthe samples from the canopy in 1999 and 2000 were cor-

rectly classified. The analysis used only two groups, Coleop-

tera and Lepidoptera. The coefficients of the canonical

discriminant function were also similar in both years. This

result is in agreement with the previous ANOVA that indicates

differences in both groups between the organic and the

other two orchards (Fig. 3).

By contrast, in the soil, although it was possible to reach

high percentages of sample classification, the coefficients of

the discriminant functions were not constant in both years

for any of the groups.

Discussion

As expected, due to the negative effects of pesticides on

arthropod populations (Heim, 1985; Cirio, 1997), the lowest

number of arthropods were found in the conventional orch-

ard. Accordingly, it was also expected that the highest num-

ber of arthropods would occur in the organic orchard, where

the arthropod fauna was not exposed to chemical treatments.

However, the highest abundance corresponded to the orch-

ard under integrated management. This was probably due to

the abundance of some pests or opportunistic species. Never-

theless, the analyses of the different groups captured indi-

cated that the highest number of specimens occurred in the

integrated orchard as a result of the number of Homoptera

(mainly the olive pest E. olivina) and Formicidae (which

inhabits the soil and was less affected by the chemical treat-

ments). When both groups were disregarded, the number of

arthropods was greatest in the organic orchard.

In the interior soil, similar or higher numbers of individ-

uals were collected compared to the exterior soil. Thus, in

accordance with previously reported results (Morris et al.,

1999), sampling of the interior soil is sufficient to determine

the representative arthropod fauna from the soil.

May, June and July, the months in which the greatest

numbers of specimens were captured, also registered the

highest number of groups showing differences among man-

agement regimes. June was the month in which the highest

number of orders differed according to the management

regimes. Therefore, it is not surprising that a higher percent-

age of samples were classified when only data from this

month were included in the discriminant analysis.

A comparison among management regimes showed that

six groups differed in abundance in the canopy and five in the

soil from the orchards studied. Nevertheless, only the samples

from the canopy were classified according to orchard man-

agement in a consistent way over the 2 years. A basic pre-

requisite for any bioindicator system is that it does not show

random fluctuations unrelated to the factor to be indicated.

The community composition should be site-characteristic and

stable over time for as long as environmental conditions do not

change (Van Straalen, 1997). Therefore, the arthropod

community from the canopy was more reliable in reflecting

the impact of the different management regimes than the

community from the soil, possibly because insecticides were

applied to the canopy. Thus, the community of Coleoptera,

Diptera, Heteroptera, Lepidoptera and Thysanoptera in the

canopy could be defined as potential bioindicators of olive-

orchard management regimes and, specifically, Coleoptera

and Lepidoptera as bioindicators of organic olive orchards.

Certainly, the features of these groups agree with the criteria

for selecting bioindicators (Cilgi, 1994). They are widely dis-

tributed, permanent residents, relatively abundant, easily

sampled and identified, and are vulnerable to pesticides.

They are also important to the crop because many of them

are predators and parasites. Moreover, these groups have

already been indicated as bioindicators of sustainability in

other crops (Fauvel, 1999; Frouz, 1999; Iperti, 1999; Kevan,

1999). The differences provided by these groups have been

detected at a high taxonomic level (i.e. order), which offers

the advantage of easy identification. Several studies have

observed a similar response using different taxonomic levels

in marine studies (Gray et al., 1990; Ferraro & Cole, 1992;

Smith & Simpson, 1993). Wright et al. (1995) also detected a

similar pattern with different taxonomic levels, but the authors

note that their results became blurred when binary data were

used at the order level.

In conclusion, it is recommended that sampling in June,

in the canopy, and using the number of Coleoptera and

Lepidoptera, could indicate the management of the olive

orchard with a probability close to 99%. Because of thepossible seasonal variations among years, it would be advis-

able to extend the sampling period from May to July.

However, to ensure that this assertion is true, it is necessary

to confirm the trends shown in this study in other orchards,

in the same or other regions, in future years.

Acknowledgements

We thank Maria Ortega, Candido Fernandez and Herminia

Barroso for their technical assistance. D. Nesbitt revised the

English version of this manuscript. This work was supported

by the research project AMB98-0946 funded by CICYT.

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Accepted 20 January 2004

120 F. Ruano et al.


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