Activity-density of Pardosa cribata in Spanish citrus orchards and its predatory capacity on Ceratitis capitata and Myzus persicae

Activity-density of Pardosa cribata in Spanish citrusorchards and its predatory capacity on Ceratitis capitataand Myzus persicae

Cesar Monzo Æ Oscar Molla Æ Pedro Castanera ÆAlberto Urbaneja

Received: 19 March 2008 / Accepted: 10 November 2008 / Published online: 26 November 2008

� International Organization for Biological Control (IOBC) 2008

Abstract The wolf spider Pardosa cribata Simon is

the most abundant ground-dwelling spider inhabiting

citrus orchards in eastern Spain. However, little is

known about its activity-density and its predatory role

in the citrus agrosystem. Here we report on the activity-

density of P. cribata monitored by pitfall traps, and on

its capacity to prey on two citrus pests that appear both

in the citrus canopy and the ground cover, Ceratitis

capitata (Wiedemman) and Myzus persicae (Sulzer),

respectively. Pardosa cribata was present in citrus

orchards throughout the year, with a peak in spring and

a higher peak in summer. Pardosa cribata preyed on

adults and third-instar larvae but not on pupae of

C. capitata. A type II functional response was obtained

for teneral-like adults, with an estimated attack rate (a0)of 0.771 ± 0.213 days-1 and a handling time (Th) of

0.051 ± 0.013 days. Pardosa cribata also preyed

efficiently on M. persicae, giving a type II functional

response with an estimated attack rate and han-

dling time of 2.833 ± 0.578 days-1 and 0.031 ±

0.001 days, respectively. The data reported here indi-

cate that this wolf spider could play an important role in

regulating both these pests, and therefore might

contribute to developing conservation biological con-

trol strategies for citrus pests.

Keywords Mediterranean fruit fly �Green-peach aphid � Functional response �Generalist predator � Population dynamics

Introduction

The citrus agrosystem is known to support a great

number of pests and natural enemies. Many of these

predators inhabit both the soil and the aerial parts of

the crop. There is a great deal of information about

the arthropod predators in the canopy, some of which

display different polyphagous habits and play an

important role in regulating their prey (Jacas et al.

2006). Conservation biological control with ento-

mophagous species can be advantageous for pest

control, helping to increase food production by

reducing crop losses caused by arthropods. When

successful, predators also reduce the need for insec-

ticides and thereby help create more sustainable

agriculture and a safer food supply (Pimentel 2008).

In this context, information is needed regarding the

Handling Editor: Arne Jenssen.

C. Monzo � O. Molla � A. Urbaneja (&)

Centro de Proteccion Vegetal y Biotecnologıa, Instituto

Valenciano de Investigaciones Agrarias (IVIA),

Ctra. Moncada-Naquera Km. 4.5, 46113 Moncada,

Valencia, SP, Spain

e-mail: [email protected]; [email protected]

C. Monzo � P. Castanera

Departamento Biologıa de Plantas, Centro de

Investigaciones Biologicas (CIB), del Consejo Superior de

Investigaciones Cientıficas (CSIC), C/Ramiro de Maeztu,

9, 28040 Madrid, SP, Spain

123

BioControl (2009) 54:393–402

DOI 10.1007/s10526-008-9199-0

ground-dwelling predator arthropods in citrus agro-

system in Spain.

Many ground-dwelling predators have been

recorded in citrus orchards located in the province

of Valencia (Spain) (Monzo et al. 2007). In the

aforementioned study, rove beetles (Coleoptera:

Staphylinidae) were the most abundant-active group

monitored by pitfall traps representing about 38.6%

of the total number of predators collected, followed

by spiders (Arachnida: Araneae) (28.9%), earwigs

(Dermaptera) (18.0%), ground beetles (Coleoptera:

Carabidae) (12.7%) and tiger beetles (Coleoptera:

Cicindelidae) (1.8%). Nevertheless, it is as yet

unknown whether these predators could play a role

in regulating citrus pests.

Spiders are important predators in agricultural

habitats, but their effects on regulating pest popula-

tions are poorly known (Hagen et al. 1999). Over 50

species of spiders have been found in Spanish citrus

orchards (Monzo et al. 2007). Of these, the generalist

predator Pardosa cribata Simon (Araneae: Lycosidae)

was the most common species, representing about

19.3% followed by Zodarion pusio (Simon) (Araneae:

Zodariidae) (14.1%) and Trachyzelotes fuscipes

(Koch) (Araneae: Gnaphosidae) (9.9%). Most spiders

are generalist predators, although there are a few

exceptions (Nentwig 1986).

One of the major Spanish pests of citrus, the

Mediterranean fruit fly (medfly), Ceratitis capitata

(Wiedemann) (Diptera: Tephritidae) spends part of its

lifecycle in the ground. There are three stages that can

be found there: late third-instar larva, pupae and teneral

adults, which climb up to the soil surface and remain on

the soil until they are able to fly. Therefore, spiders

might contribute to reducing medfly populations, and

hence increase the effectiveness of other control

methods. In recent years, emphasis has been placed

on implementing more environmentally friendly mea-

sures to control medfly in Spain (Castanera 2003). One

of them involves identification and conservation of

polyphagous predators of the medfly (Urbaneja et al.

2006). Recently, PCR-based methods used to detect

C. capitata DNA within predators have revealed that

P. cribata is able to prey on C. capitata both in

laboratory and field conditions (Monzo et al. 2007).

We report here on the activity-density of the wolf

spider, P. cribata, monitored by pitfall traps in two

citrus orchards over a three year period in Valencia,

Spain. Because pitfall traps do not sample true

abundance and are an inefficient sampling method

for P. cribata, the values presented are referred to as

activity-density. Secondly, selected predatory charac-

teristics of P. cribata, such as prey suitability,

consumption rate and functional response were inves-

tigated for C. capitata. Similarly, we have estimated

the predatory response of this spider to another citrus

pest, which spends a part of its lifecycle on cover crops

in citrus and weeds, the green peach aphid, Myzus

persicae (Sulzer) (Hemiptera: Aphididae), which

could also be a potential prey of this spider.

Materials and methods

Sampling sites

Two 1 ha citrus orchards located in Naquera (UTM

X722427 Y4385216; Z110 m altitude) and Betera

(UTM X722106 Y4388610; Z30 m altitude) (Eastern

Spain) were used for the P. cribata survey. The first

orchard had no soil cover whereas in the other a natural

cover crop was maintained. Both orchards were drip-

irrigated and surrounded by other citrus orchards. In

the orchard without cover, glyphosate herbicide was

applied in the spring, summer and fall for weed control.

In Betera a spontaneous natural cover crop was

preserved and it was mowed at the end of spring and

the beginning of fall.

Sampling of P. cribata

Twelve pitfall traps were regularly distributed diago-

nally across each orchard to monitor the abundance-

activity of P. cribata. Each trap consisted of a plastic

jar (12.5 cm diameter and 12 cm depth), with a

plastic funnel fitted to the upper edge of the jar. A

plastic 150 ml container half filled with a 3:1 mixture

of water and ethanol, and 0.1% detergent, was placed

inside the plastic cup. Sampling was performed from

April 2004 until April 2007 and August 2003 until

August 2006 for Naquera and Betera, respectively.

Traps were changed every 15 days and all individuals

collected were recorded.

Predation capacity on C. capitata stages

All the P. cribata individuals used in assays were

collected from citrus fields close to the Instituto

394 C. Monzo et al.

123

Valenciano de Investigaciones Agrarias (IVIA). All

individuals were in sub-adult or adult stage with a

sex ratio of approximately 1:1. Subsequently, they

were individually placed in 100 ml plastic containers

and starved for 7 days at 25 ± 2�C and 16:8 (L:D)

photoperiod. Water-soaked cotton wool was supplied

as a source of water. The predatory capacity of

P. cribata was evaluated in terms of their capacity to

feed on the two selected prey in a no-choice

laboratory test. All assays were performed under

the previously described environmental conditions.

The sex ratio of the predators used in these assays

was 1:1 to maintain the sex ratio found under field

conditions.

Ceratitis capitata individuals were obtained from a

laboratory colony, maintained at the IVIA (Valencia,

Spain) since 2002. This colony has periodically been

supplemented by introducing wild flies from naturally

occurring infested fruit during summer and fall. Eggs

less than 24 h-old were sown on plastic trays

containing an artificial diet consisting of 400 g of

wheat bran, 112 g of sugar, 58 g of brewer’s yeast,

4.5 g of methyl paraben, 4.5 g of propyl paraben, 4 g

of benzoic acid, and 900 ml water, with a density of

4 eggs g-1 diet (Alonso et al. 2005). The trays were

placed on shelves and covered with aluminum foil to

prevent contamination by Drosophila spp. Wet sand

was placed on the shelves. Larvae developed on the

diet and, 16 days later, they jumped out of the trays

and buried themselves in the sand to pupate. Fifteen-

days-old larvae and one-day-old pupae were used for

the corresponding assays. To obtain a cohort of adults,

approximately 1,000 pupae of less than 24 h were

collected and maintained in perspex cages

(20 9 20 9 20 cm) with sterilized wet sand until

adult emergence. Less than three-days-old adults were

used in all assays. Flies were given water and a diet

consisting of a mixture of enzymatic autolyzed

brewer’s yeast and sugar (1:4, w:w) until assays

started.

Spiders were individually transferred to plastic

cages (15 9 7 9 10 cm depth), with a lid with a hole

(12 9 18 cm) that was covered with mesh for

ventilation. Water was supplied as described above.

In each arena, five third-instar larvae, pupae or adults

were offered daily for five days. A control treatment

without spiders was also included for each medfly

stage studied. Twelve replicates were conducted for

the adult and pupae treatments, and 11 for the larvae

treatment. The number of individuals consumed or

killed was counted daily.

Functional response on C. capitata adults

Different densities of three-days-old C. capitata

adults (2, 4, 6, 8 12, 20, and 40) were exposed to

starved standardized P. cribata in eight replicates per

density, in an arena consisting of a plastic Petri dish

(14 cm in diameter and 1.6 cm high). This experi-

mental arena was selected to simulate teneral-like

adult behavior, in which the medfly could not escape

by flying away from the predator. Two control

treatments each with eight replicates and a density

of 20 medflies were carried out to assess mortality

rates due to anti-predator behavior and to natural

mortality factors. In the first control treatment, a Petri

dish (diameter 4 cm) containing one spider was

placed inside a larger Petri dish (14 cm). In this way,

the caged spider was not able to prey on teneral-like

adults, but both the spider and medflies could see

each other. The second control treatment was without

spiders inside the small Petri dish. Differences in

mortality rates between both control treatments

would point at extra mortality due to anti-predator

behavior, for example because prey would try to

escape and crash against the walls of the arena. In all

treatments a water-soaked piece of cotton wool was

supplied as water source and adult medfly food

consisting of a mixture of sugar and hydrolyzed yeast

(4:1; w/w) was provided. After 24 h the predators

were removed from the arenas and the number of

dead medflies (either killed and consumed or crashed

against the walls) was evaluated. Prey were not

replaced during the experiment.

Functional response on M. persicae

Starved standardized spiders were exposed individu-

ally to one of the following M. persicae adult

densities: 2, 4, 6, 10, 20, 40, 80,120, and 160, reared

on broad-bean leaves (Vicia faba L.; Leguminosae)

kept inside Petri dishes (14 cm in diameter). Broad

beans were free of insecticides and were grown under

glass at the IVIA. The petiole of each leaf was placed

inside an Eppendorf tube containing a nutritive

solution to keep leaf turgidity during the experiments

(Moutous 1973). The leaf petiole was sealed to the

Eppendorf with plasticine (Plastilina Jovi� JOVI,

Activity-density and predatory capacity of P. cribata 395

123

S.A. Barcelona, SP). Water supply as explained

above, was provided in each arena. A control

treatment with eight replicates and without spiders

at a density of 20 aphids was also carried out in order

to know their natural mortality rate. For each density

and for the control, eight replicates were performed.

After 24 h, predators were removed from the arenas

and preyed aphids were counted. Prey were not

replaced during the experiment.

Data analysis

Values are expressed as mean ± standard error of the

mean. Sampling data obtained for both orchards were

submitted to two-way ANOVA to explain variability

in captures throughout the sampling period and

among years (SPSS 1999). An LSD test was applied

for mean separation at P \ 0.05.

In the medfly-stage predation experiment, data

obtained were subjected to a one-way ANOVA

analysis to analyze the differences observed among

stages (SPSS 1999). In the functional response expe-

riment with C. capitata adults, data of both control

treatments were submitted to t-test to compare means

to detect effects of anti-predator behavior on prey

mortality. To know possible significant differences

between the number of prey killed and consumed when

prey density was increased, the proportion of prey

consumed (consumed/killed) was subjected to a

Generalized Linear Model in which the variable was

assumed to be binomial distributed. Contrasting of

successive levels of density were obtained to detect the

prey density at which differences appear.

In the functional response experiments, in order to

discriminate between Type II and Type III functional

responses, a logistic regression of the relative

proportion of prey killed was performed (Trexler

et al. 1988; Juliano 2001). The data were fitted to a

polynomial function with intercept, linear and qua-

dratic coefficients using the maximum likelihood

method (SPSS 1999). A positive linear coefficient

and a negative quadratic coefficient imply that the

data fit a type III functional response whereas a

negative linear coefficient means a better adjustment

to type II. Once this analysis was performed, data

were fitted to the corresponding functional response

equation. Because prey was not replaced, we used the

‘‘random-predator’’ equation (Rogers 1972; Royama

1971) for a type II functional response equation, for

those densities in which not all prey were killed or

consumed before the end of the assay. Therefore, the

densities 2 and 4 for C. capitata and 2, 4 and 6 for

M. persicae were excluded from the analysis. The data

were fitted through a non-linear least-squares regres-

sion by means of the Levenberg–Marquardt iterative

estimation procedure (SPSS 1999). The functional

response parameters, attack rate (a0) and handling time

(Th), were extracted from this regression.

Results

Dynamics of P. cribata

A total of 1,030 individuals of P. cribata were

collected in the two orchards during the three-years

study. A large number of individuals (n = 778) were

captured in Betera, where a spontaneous natural

cover crop was maintained, whereas 252 individuals

were captured in the bare-soil citrus orchard in

Naquera. In general, P. cribata was present through-

out the year in both orchards. In Betera, P. cribata

showed a significantly higher activity during spring

and summer (F3,143 = 15.01; P \ 0.001) than during

autumn and winter. Moreover, the number of captures

was significantly higher during the third year of

sampling (F2,143 = 9.69; P \ 0.001) (Fig. 1). In

Naquera, the seasonal activity of P. cribata was

significantly higher during summer than in other

seasons (F3,143 = 10.70; P \ 0.001) whereas no

differences were found among years of sampling

(F2,143 = 0.48; P = 0.6197) (Fig. 2).

Predation capacity on C. capitata stages

Spiders were able to prey on medfly adults and third

instar larvae, but not on pupae. The number of adults

killed by P. cribata (2.32 ± 0.16) was significantly

higher than the number of third-instar larvae killed

(1.22 ± 0.17) (F1,22 = 20.60; P \ 0.001). However,

there were no significant differences between the mean

number of adults and the mean number of third instar-

larvae consumed (1.45 ± 0.13, and 1.12 ± 0.17,

respectively) (F1,22 = 1.58; P = 0.222). The number

of adults killed (2.32 ± 0.16) was significantly higher

than the number of adults consumed (1.45 ± 0.13)

(F1,23 = 15.84; P \ 0.001). Hence, P. cribata kills

more adult medfly than it consumes. On the contrary,

396 C. Monzo et al.

123

there were no significant differences between the mean

number of larvae killed (1.22 ± 0.17) and the mean

number of larvae consumed (1.12 ± 0.17) (F1,23 =

0.041; P = 0.842) (Table 1).

Functional response on C. capitata adults

Control mortality was 1.3 and 1.9% for the control with

and without spiders, respectively. No differences were

found between both treatments (t = 0.509; df = 14;

P = 0.6186). P. cribata killed more flies than it

consumed (Table 2). Differences were found between

the number of medfly adults killed and consumed

when prey density was increased (F6,49 = 10.95; P \0.0001). This differences appeared at density 20

(t = 3.36; df = 49; P = 0.0015 at 12 vs. 20 contrast)

and significantly increased at density 40 (t = 2.50;

df = 49; P = 0.0156 at 20 vs. 40 contrast). The linear

and quadratic coefficients of the logistic regression of

the proportion of medfly killed were -0.165 ± 0.036

A)

B)

2003-2004

0.0

0.1

0.2

0.3

0.4

0.5

0.6

Aug

-03

Oct

-03

Nov

-03

Jan-

04

Feb

-04

Apr

-04

Jun-

04

Jul-0

4

Indi

vid.

trap

ped

day

–1

2004-2005

0.0

0.1

0.2

0.3

0.4

0.5

0.6

Aug

-04

Oct

-04

Nov

-04

Jan-

05

Mar

-05

Apr

-05

Jun-

05

Aug

-05

Indi

vid.

trap

ped

day

–1

C) 2005-2006

0.0

0.1

0.2

0.3

0.4

0.5

0.6

Sep

-05

Oct

-05

Dec

-05

Feb

-06

Mar

-06

May

-06

Jul-0

6

Indi

vid.

trap

ped

day

–1

Fig. 1 Mean number of

Pardosa cribata(individuals trapped

day-1 ± SE) collected in

pitfall traps during

three years (2004–2007) in

a citrus orchard with natural

cover-crop management

(Betera)

Activity-density and predatory capacity of P. cribata 397

123

and 0.0025 ± 0.0007, respectively. Both parameters

were significant (df = 45; linear: v2 = 22.38, P \0.001; quadratic: v2 = 13.35; P \ 0.001). A type II

functional response was obtained from the logistic

regression because estimation of the linear coefficient

was negative and the quadratic coefficient was

positive. The estimated attack-rate coefficient was

0.771 ± 0.213 days-1 (95% confidence interval

0.178–1.36) and the estimated handling time was

0.051 ± 0.013 days (95% confidence interval 0.015–

0.088) (Fig. 3).

Functional response on M. persicae

Control mortality was 0.63% and the number of

aphids killed differed significantly with aphid density

(F8,85 = 69.87; P \ 0.0001) (Table 3). The linear

and quadratic coefficients of the logistic regression of

the proportion of M. persicae preyed on by P. cribata

were -0.030 ± 0.004 and 0.0001 ± 0.00002, respec-

tively. Both parameters were significant (df = 54;

linear: v2 = 71.80, P \ 0.0001; quadratic: v2 =

19.97; P \ 0.0001). A type II functional response

A)

B) 2005-2006

0.0

0.1

0.2

0.3

0.4

0.5

0.6

Apr

-05

Jun-

05

Aug

-05

Sep

-05

Nov

-05

Jan-

06

Feb

-06

Apr

-06

Indi

vid.

trap

ped

day

–1

2004-2005

0.0

0.1

0.2

0.3

0.4

0.5

0.6

Apr

-04

Jun-

04

Jul-0

4

Sep

-04

Nov

-04

Dec

-04

Feb

-05

Apr

-05

Indi

vid.

trap

ped

day

–1

C) 2006-2007

0.0

0.1

0.2

0.3

0.4

0.5

0.6

May

-06

Jun-

06

Aug

-06

Sep

-06

Nov

-06

Jan-

07

Feb

-07

Apr

-07

Indi

vid.

trap

ped

day

–1

Fig. 2 Mean number of

Pardosa cribata(individuals trapped

day-1 ± SE) collected in

pitfall traps during three

years (2003–2006) in a

citrus orchard with bare-soil

management (Naquera)

398 C. Monzo et al.

123

was obtained from the logistic regression because

estimation of the linear coefficient was negative and

the quadratic coefficient was positive. The estimated

attack rate coefficient was 2.833 ± 0.578 days-1

(95% confidence interval 1.347–4.319) and the esti-

mated handling time was 0.031 ± 0.001 days (95%

confidence interval 0.030–0.033) (Fig. 4).

Discussion

The wolf spider, P. cribata was the most abundant

species recorded in a citrus orchard with vegetation

covering the soil and a citrus orchard without soil

cover. Populations of the spider increased during

spring and peaked in summer when aphids were also

more abundant in citrus orchards conditions (Herm-

oso de Mendoza et al. 2006). Furthermore, teneral

adults emerged during the spring and early summer

from pupae that overwinter in the citrus ground

(Urbaneja et al. 2006; Aleixandre 2007). The fact that

the highest abundance-activity was recorded in

Betera, the orchard with vegetation covering the soil,

suggests that this could be due to the diversity of

plant species, which can house a broad range of

alternative prey on which P. cribata may feed.

Indeed, semi-natural habitats with host-plant diver-

sity and, therefore, prey availability, have proven an

important factor for the conservation and enhance-

ment of spider species (Bogya and Marko 1999;

Pfiffner and Luka 2003; Schmidt et al. 2005).

Little is known about the efficacy of spiders in

agroecosystems, although a number of studies

express high expectations that spiders can play a

significant role in regulating pest species (Riechert

and Lockley 1984; Hagen et al. 1999). Our results

show that P. cribata prey on two of the three stages of

C. capitata (adults and third-instar larvae), which can

be found in the soil of citrus orchards. No predation

was observed when pupae were offered. Neverthe-

less, Urbaneja et al (2006) observed predation of

pupae by P. cribata, but in very low numbers.

The predation rate obtained in the functional

response assay with teneral-like adults was higher

Table 1 Mean predation (±SE) of Ceratitis capitata larvae,

pupae and adults per day by P. cribata in a no-choice labora-

tory assays

Killed Consumed

Third instar larvae 1.22 ± 0.17 Ab 1.12 ± 0.17 Aa

Pupae 0.00 ± 0.00 0.00 ± 0.00

Adults 2.32 ± 0.16 Aa 1.45 ± 0.13 Ba

Five prey were offered to each spider

Within each column, mean values followed by a different lower

case character and mean values followed by a different

upper character within each row are significantly different

(P \ 0.05)

Table 2 Medfly adults killed and consumed (mean ± SE) at

different prey densities by Pardosa cribata in laboratory assays

Prey density Killed adults Consumed adults

2 1.50 ± 0.19 1.25 ± 0.16

4 2.75 ± 0.37 2.25 ± 0.37

6 4.50 ± 0.60 4.13 ± 0.64

8 4.00 ± 0.65 3.13 ± 0.44

12 6.25 ± 1.16 5.13 ± 1.20

20 6.38 ± 1.21 3.13 ± 0.67

40 11.25 ± 2.41 3.13 ± 0.79

0

5

10

15

20

25

30

0 10 20 30 40

Initial medfly adults offered

N°

adul

ts k

illed

Fig. 3 Observed number

of C. capitata killed and the

functional response curve

(Type II) fit by non-linear

least square

Activity-density and predatory capacity of P. cribata 399

123

than that obtained when medfly adults were able to

escape by flying away in the predation capacity

experiment. Movement triggers spiders to attack, so

logically killing rate would be lower when adults

have limited mobility. However, similar movement

trends for medflies were observed between both

assays, thus the predatory behavior of P. cribata was

not affected, so the differences obtained could be

attributed mainly to their ability to fly away.

The number of medfly adults consumed seemed to

level off around 4–5 adults. This plateau represents

the prey consumption level at which the predators

were satiated. Over-killing of adult medflies was

observed and is described in other spider species

(Riechert and Lockley 1984; Mansour et al. 1980;

Mansour and Heimbach 1993; Pekar 2005).

Pardosa hortensis Thorell also presented a type II

functional response preying on another fruit fly,

Drosophila melanogaster Meigen (Diptera: Tephriti-

dae) (Samu and Biro 1993). In the aforementioned

work, the attack rate was not calculated, but

P. hortensis exhibited a handling time slightly lower

than our results.

Aphids generally represent low-quality food for

spiders (Toft and Wise 1999a, b). Furthermore,

different feeding experiments with wolf spiders have

revealed that they begin to reject cereal aphids after

continuous exposure to them (Toft 1997; Oelbermann

and Scheu 2002). Nevertheless, because spiders are

adapted to living in a state of semi-starvation, they

demonstrate hardly any preference when capturing

their prey (Anderson 1974; Riechert 1992; Bilde and

Toft 1998). Therefore, aphids certainly form part of

the spider’s diet and contribute to sustain spider

populations (Chiverton 1987; Sunderland et al. 1987).

Mansour and Heimbach (1993) using Pardosa agrestis

(Westring) and Oelbermann and Scheu (2002) with

Pardosa lugubris (Walckenaer) observed that both

Pardosa species killed more Rhopalosiphum padi (L.)

than they actually ate. In contrast, we found that all the

aphids killed were eaten. When comparing the

estimated attack-rate coefficient obtained for P. cribata

on M. persicae (2.773 ± 0.606 days-1) with different

specialist aphid-feeding coccinelid species [Coccinella

septempunctata (Linnaeus), 1.2 days-1 (Mao-Lin and

Fang-Hao 2004); Cheilomenes sexmaculata (Fabricius),

0.9 days-1; Propilea dissecta (Mulsant), 0.7 days-1;

and Coccinella transversalis Fabricius, 0.9 days-1

(Pervez 2005)] we could conclude that P. cribata has

a great potential to control M. persicae. However,

handling time was between 3 and 10 times higher than in

aphid-feeding specialists, suggesting they are less well

adapted to feeding on this prey probably due to its

generalist prey behavior. However, there are other traits

inherent to generalist predators that should be taken into

account when comparing them to specialist predators

Table 3 Mean predation (±SE) of Myzus persicae adults by

Pardosa cribata at different densities in laboratory assays

Prey density Number of adults killed and eaten

2 1.62 ± 0.74

4 3.50 ± 0.76

6 5.12 ± 1.35

10 7.50 ± 2.37

20 13.12 ± 1.27

40 25.00 ± 2.47

80 27.06 ± 4.13

120 28.50 ± 3.74

160 29.75 ± 4.26

0

10

20

30

40

50

60

0 40 80 120 160

Initial aphids offered

N°

aphi

ds k

illed

Fig. 4 Observed number

of M. persicae eaten and the

functional response curve

(Type II) fit by non-linear

least square

400 C. Monzo et al.

123

(Symondson et al. 2002). These predators can maintain

their populations when the pest populations decline or

even disappear due to their opportunistic feeding habits,

which enable them to survive on a wide range of prey.

Indeed, at relative high predator densities, theoretical

studies suggest that generalist predators may be able to

stabilize fluctuations in their prey if predator densities

are unrelated to prey densities and if their functional

response shows some density-dependent predation

(Hanski et al. 1991).

The functional response parameters obtained in

this work will be helpful when comparing with other

ground-dwelling predators abundant also throughout

the year in the Spanish citrus orchards, which can

also prey on these two pests. This could be the case of

the carabaid, Pseudophonus rufipes De Geer or the

earwig Forficula auricularia L, which are currently

under evaluation for the same preys (data not shown).

Other behavioral parameters, such as the numerical

response, are certainly involved in these predator–

prey systems and should also be studied in depth to

clarify the role of these predators as biocontrol agents

in citrus orchards. However, such studies are difficult

to assay on generalist ground-dwelling predators, and

especially on spiders under real conditions (Riechert

1974).

Altogether, the data presented here reveal that

P. cribata is the most abundant generalist predator

present in citrus orchard in Valencia throughout the

year. Furthermore, it is an efficient predator on both

Medfly and green-peach aphid. In addition, PCR-based

methods have recently revealed that P. cribata is also

able to prey on C. capitata under field conditions (data

not shown). These findings suggest that P. cribata

could play an important role in regulating medfly and

green-peach aphid populations. A challenge for future

studies will be to enhance their populations, for

example by means of cover-crop management, and

consequently to incorporate P. cribata in conservation

biological control strategies.

Acknowledgments This work was funded by FEOGA

COOPERACION, the Conselleria d’Agricultura, Pesca i

Alimentacio de la Generalitat Valenciana and INIA (RTA03-

103-C6-01). The authors wish to thank Tomas Cabello

(Universidad de Almerıa, Spain) for his help in the functional

response analysis and Martın Llavador for the agronomic

cooperation in this work. We are also grateful to A. Melic

(Araneae, Sociedad Entomologica Aragonesa, Zaragoza SP) for

taxonomical advice and to H. Monton, T. Pina, P. Vanaclocha

and D. Tortosa (IVIA) for their time in field sampling and

technical assistance. C.M. was recipient of a grant from the

CSIC.

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