Seasonal suitability of three rubber tree clonesto Calacarus heveae (Acari Eriophyidae)

Rodrigo Damasco Daud bull Reinaldo Jose Fazzio Feres bull

Fabio Akashi Hernandes

Received 1 March 2011 Accepted 11 September 2011 Published online 5 October 2011 Springer Science+Business Media BV 2011

Abstract The suitability of rubber tree clones to Calacarus heveae was inferred from the

life cycle reproduction and survivorship of this mite The assays were performed under

controlled conditions with leaflets detached from 6-year-old plants The development of 20

C heveae individuals on each of the clones GT 1 PB 235 and RRIM 600 was analysed

This experiment was performed four times during periods when C heveae was abundant in

the field (P1) NovemberndashDecember 2005 (P2) JanuaryndashFebruary (P3) MarchndashApril and

(P4) MayndashJune 2006 Accordingly the leaflets used in each assay represented the physi-

ological condition of the host plant during each period This approach allowed us to

evaluate the seasonal suitability of rubber tree clones to C heveae We observed seasonal

differences in the suitability of rubber tree clones to mite attack The mites reared on the

PB235 had a shorter development period the highest egg production and highest survi-

vorship This evidence showed that the PB 235 was the most suitable of those tested We

also observed that the leaflets used in the assays during periods P2 and P3 were the most

favourable for the development of C heveae This finding emphasises the seasonal suit-

ability of rubber tree leaflets On the other hand GT 1 showed higher resistance against

R D Daud (amp)Departamento de Ecologia Instituto de Ciencias Biologicas Universidade Federal de GoiasCampus Samambaia Caixa Postal 131 Goiania GO 74001-970 Brazile-mail rodrigodaudyahoocombr

R D Daud F A HernandesPrograma de Pos-graduacao em Biologia Animal UNESP Campus de SJ Rio Preto Sao Paulo Brazil

F A Hernandese-mail abakashigmailcom

R J F FeresDepartamento de Zoologia e Botanica Instituto de Biociencias Letras e Ciencias ExatasUNESPmdashUniversidade Estadual Paulista Rua Cristovao Colombo n2265Sao Jose do Rio Preto SP 15054-000 Brazile-mail reinaldoibilceunespbr

F A HernandesMontpellier Supagro CBGP-INRA Campus International de BaillarguetAv Campus Agropolis CS 30016 34988 Montferrier-sur-Lez France

123

Exp Appl Acarol (2012) 5657ndash68DOI 101007s10493-011-9494-9

C heveae than did RRIM 600 and PB 235 primarily during the period from November to

February This result indicated that use of the GT 1 clone to control the mite might

represent an alternative for growers

Keywords Biology Hevea brasiliensis Life cycle Phytophagous mite Resistance

Introduction

The concentration of mineral nutrients and secondary metabolites in plants as well as

morphological properties of leaves (eg toughness trichomes) are key factors in the sur-

vival reproduction and development of herbivorous arthropods (Awmack and Leather

2002) This factor may vary seasonally (Awmack and Leather 2002 Nukenine et al 2000

Rodriguez et al 1983) and between genotypes of a single plant species (Panizzi and Parra

2009 Resende et al 2008 Reinert et al 2004)

Several studies have revealed numerous factors that produce natural resistance against

herbivores in different cultivars of plants (eg Vieira et al 2009 Reinert et al 2008 Boina

et al 2005 Hennessey et al 1995 Erb et al 1994) Growing resistant cultivars on a com-

mercial scale has been regarded as a successful and low-cost measure for controlling pests

This approach reduces the populations of phytophagous arthropods below the economic

damage level and causes no pollution to the environment (Lara 1991 Cook and Smith 1988)

As hundreds of genotypes (clones) are currently produced and commercialised (Gon-

calves et al 2001) the rubber tree Hevea brasiliensis Muell Arg (Euphorbiaceae) has the

ideal characteristics for the application of that method of pest control However few

studies have sought to verify the susceptibility of different clones to the attack of her-

bivorous arthropods and no study to date has assessed the seasonal suitability of different

clones According to Feres (2000) some farmers have observed that the rubber tree clones

IAN 873 PB 235 and PB 260 were affected to a relatively great extent by the phytoph-

agous mite Calacarus heveae Feres (Acari Eriophyidae) Daud and Feres (2007) observed

heavy infestations of that species on PB 260 Similarly they have found heavy infestations

of Phyllocoptruta seringueirae Feres (Eriophyidae) and Tenuipalpus heveae Baker (Ten-

uipalpidae) also important mite pests of rubber trees on PB 235 and RRIM 600

respectively Using free-choice trials Lara and Tanzini (1997) verified that the clones GT 1

and IAN 873 are the most attractives to Leptopharsa heveae Drake and Poor (Hemiptera

Tingidae) Vieira et al (2009) identified eight rubber tree genotypes resistant to T heveaeand C heveae and Feres et al (2010) verified that the clone GT 1 is the least favourable

for the development and reproduction of T heveae

According to Awmack and Leather (2002) the oviposition also represents a critical

point in determining host acceptance by the mite because of the large amount of energy

required during its reproduction Accordingly we studied the development time the

fecundity and the population survival of C heveae reared on three commercial rubber tree

clones during four distinct seasons in order to verify their seasonal suitability for this

mites species C heveae has been considered to be the primary mite pest of rubber tree

crops in Sao Paulo and Mato Grosso states (Hernandes and Feres 2006 Vis et al 2006

Feres et al 2002 Ferla and Moraes 2002 Feres 2000 Vieira and Gomes 1999) It occurs

on the adaxial surface of leaflets According to Ferla and Moraes (2003) C heveaeindividuals reared on PB 260 clone spend about 3 days to reach the adulthood after

ecloding the adults longevity ranged from 40 to 84 days and females laid a average of

162 eggs during its lifetime Infestation by this mite occasionally leads to intense

58 Exp Appl Acarol (2012) 5657ndash68

123

defoliation (Vieira and Gomes 1999) and to a 30 reduction in latex yield according to

some growers (Feres 2000)

Materials and methods

The leaflets used in the experiments were collected from 6 year old rubber trees at the

experimental area of UNESP Sao Jose do Rio Preto SP Brazil The rubber trees used for

the assay were cultivated at the same locality near from each other assuring that all the

plants had the same soil (nutrients and water quantities) and weather conditions

For each experiment healthy leaflets (ie without observable damage) were taken from

the sixth to eighth gems of the same plant from each of the clones GT 1 PB 235 and

RRIM 600 Thus all leaflets used had the same age once the suitability to herbivorous

mites may vary according to the concentration of nutrients and defenses of the leaves in

different ages (Karban and Thaler 1999 Awmack and Leather 2002) The clones above

were chosen for the assays because of their economic importance being the most culti-

vated in the State of Sao Paulo Brazil (Goncalves et al 2001)

Stock population

The rearing arenas were made from leaflets of the above mentioned clones by using the

method described by Ferla and Moraes (2003) for the same mite The leaflets were washed

with distilled water and placed with the adaxial surface face up on 2 cm thick nylon foam

Distilled water was added daily in order to maintain the water saturation of the foam and

the desired humidity of the air Cotton strips were added to the borders of each leaflet to

prevent the mites from escaping Each arena was kept inside an aluminium tray of

5 9 17 9 25 cm above which a glass plate was placed in order to maintain a humid

microhabitat for the mites (Ferla and Moraes 2003) A 1 cm free space was left in both

sides of the glass to prevent water condensation

The mites used to start the stock population were collected from leaflets of RRIM 600

from the experimental area described above The leaflets were examined under a dissecting

microscope and the females were transferred to the rearing arenas using a fine brush At

least 50 females were placed in the arenas of each rubber tree clone The arenas were kept

in a rearing chamber at 28 plusmn 1C 80 plusmn 10 RH and a photoperiod of 1212 h (LD) for at

least 3 weeks before the assays were conducted

Life cycle reproduction and survivorship of Calacarus heveae

The arenas were prepared for this assay as described above However a thin layer of cotton

was put over the nylon foam above which the leaflets were placed Moreover each leaflet

was divided into 14 cm 9 14 cm squares using strips of tissue paper in order to define the

study units for the life cycle investigation The experiment was performed in a rearing

chamber at 80 plusmn 10 RH A photoperiod of 1410 h (LD) with temperatures of 28 plusmn 1C

in the light phase (20 W fluorescent tubes) and 25 plusmn 1C in the dark phase was used in

order to simulate the field conditions occurring during the peak of C heveae infestation

The rubber tree loses leaves each year at the peak of the dry season (JunendashAugust)

Consequently the mites (including C heveae) associated with its leaves also occur sea-

sonally and exhibit peaks of population fluctuation (Daud and Feres 2007 Hernandes and

Feres 2006)

Exp Appl Acarol (2012) 5657ndash68 59

123

C heveae than did RRIM 600 and PB 235 primarily during the period from November to

February This result indicated that use of the GT 1 clone to control the mite might

represent an alternative for growers

Keywords Biology Hevea brasiliensis Life cycle Phytophagous mite Resistance

Introduction

The concentration of mineral nutrients and secondary metabolites in plants as well as

morphological properties of leaves (eg toughness trichomes) are key factors in the sur-

vival reproduction and development of herbivorous arthropods (Awmack and Leather

2002) This factor may vary seasonally (Awmack and Leather 2002 Nukenine et al 2000

Rodriguez et al 1983) and between genotypes of a single plant species (Panizzi and Parra

2009 Resende et al 2008 Reinert et al 2004)

Several studies have revealed numerous factors that produce natural resistance against

herbivores in different cultivars of plants (eg Vieira et al 2009 Reinert et al 2008 Boina

et al 2005 Hennessey et al 1995 Erb et al 1994) Growing resistant cultivars on a com-

mercial scale has been regarded as a successful and low-cost measure for controlling pests

This approach reduces the populations of phytophagous arthropods below the economic

damage level and causes no pollution to the environment (Lara 1991 Cook and Smith 1988)

As hundreds of genotypes (clones) are currently produced and commercialised (Gon-

calves et al 2001) the rubber tree Hevea brasiliensis Muell Arg (Euphorbiaceae) has the

ideal characteristics for the application of that method of pest control However few

studies have sought to verify the susceptibility of different clones to the attack of her-

bivorous arthropods and no study to date has assessed the seasonal suitability of different

clones According to Feres (2000) some farmers have observed that the rubber tree clones

IAN 873 PB 235 and PB 260 were affected to a relatively great extent by the phytoph-

agous mite Calacarus heveae Feres (Acari Eriophyidae) Daud and Feres (2007) observed

heavy infestations of that species on PB 260 Similarly they have found heavy infestations

of Phyllocoptruta seringueirae Feres (Eriophyidae) and Tenuipalpus heveae Baker (Ten-

uipalpidae) also important mite pests of rubber trees on PB 235 and RRIM 600

respectively Using free-choice trials Lara and Tanzini (1997) verified that the clones GT 1

and IAN 873 are the most attractives to Leptopharsa heveae Drake and Poor (Hemiptera

Tingidae) Vieira et al (2009) identified eight rubber tree genotypes resistant to T heveaeand C heveae and Feres et al (2010) verified that the clone GT 1 is the least favourable

for the development and reproduction of T heveae

According to Awmack and Leather (2002) the oviposition also represents a critical

point in determining host acceptance by the mite because of the large amount of energy

required during its reproduction Accordingly we studied the development time the

fecundity and the population survival of C heveae reared on three commercial rubber tree

clones during four distinct seasons in order to verify their seasonal suitability for this

mites species C heveae has been considered to be the primary mite pest of rubber tree

crops in Sao Paulo and Mato Grosso states (Hernandes and Feres 2006 Vis et al 2006

Feres et al 2002 Ferla and Moraes 2002 Feres 2000 Vieira and Gomes 1999) It occurs

on the adaxial surface of leaflets According to Ferla and Moraes (2003) C heveaeindividuals reared on PB 260 clone spend about 3 days to reach the adulthood after

ecloding the adults longevity ranged from 40 to 84 days and females laid a average of

162 eggs during its lifetime Infestation by this mite occasionally leads to intense

58 Exp Appl Acarol (2012) 5657ndash68

123

defoliation (Vieira and Gomes 1999) and to a 30 reduction in latex yield according to

some growers (Feres 2000)

Materials and methods

The leaflets used in the experiments were collected from 6 year old rubber trees at the

experimental area of UNESP Sao Jose do Rio Preto SP Brazil The rubber trees used for

the assay were cultivated at the same locality near from each other assuring that all the

plants had the same soil (nutrients and water quantities) and weather conditions

For each experiment healthy leaflets (ie without observable damage) were taken from

the sixth to eighth gems of the same plant from each of the clones GT 1 PB 235 and

RRIM 600 Thus all leaflets used had the same age once the suitability to herbivorous

mites may vary according to the concentration of nutrients and defenses of the leaves in

different ages (Karban and Thaler 1999 Awmack and Leather 2002) The clones above

were chosen for the assays because of their economic importance being the most culti-

vated in the State of Sao Paulo Brazil (Goncalves et al 2001)

Stock population

The rearing arenas were made from leaflets of the above mentioned clones by using the

method described by Ferla and Moraes (2003) for the same mite The leaflets were washed

with distilled water and placed with the adaxial surface face up on 2 cm thick nylon foam

Distilled water was added daily in order to maintain the water saturation of the foam and

the desired humidity of the air Cotton strips were added to the borders of each leaflet to

prevent the mites from escaping Each arena was kept inside an aluminium tray of

5 9 17 9 25 cm above which a glass plate was placed in order to maintain a humid

microhabitat for the mites (Ferla and Moraes 2003) A 1 cm free space was left in both

sides of the glass to prevent water condensation

The mites used to start the stock population were collected from leaflets of RRIM 600

from the experimental area described above The leaflets were examined under a dissecting

microscope and the females were transferred to the rearing arenas using a fine brush At

least 50 females were placed in the arenas of each rubber tree clone The arenas were kept

in a rearing chamber at 28 plusmn 1C 80 plusmn 10 RH and a photoperiod of 1212 h (LD) for at

least 3 weeks before the assays were conducted

Life cycle reproduction and survivorship of Calacarus heveae

The arenas were prepared for this assay as described above However a thin layer of cotton

was put over the nylon foam above which the leaflets were placed Moreover each leaflet

was divided into 14 cm 9 14 cm squares using strips of tissue paper in order to define the

study units for the life cycle investigation The experiment was performed in a rearing

chamber at 80 plusmn 10 RH A photoperiod of 1410 h (LD) with temperatures of 28 plusmn 1C

in the light phase (20 W fluorescent tubes) and 25 plusmn 1C in the dark phase was used in

order to simulate the field conditions occurring during the peak of C heveae infestation

The rubber tree loses leaves each year at the peak of the dry season (JunendashAugust)

Consequently the mites (including C heveae) associated with its leaves also occur sea-

sonally and exhibit peaks of population fluctuation (Daud and Feres 2007 Hernandes and

Feres 2006)

Exp Appl Acarol (2012) 5657ndash68 59

123

defoliation (Vieira and Gomes 1999) and to a 30 reduction in latex yield according to

some growers (Feres 2000)

Materials and methods

The leaflets used in the experiments were collected from 6 year old rubber trees at the

experimental area of UNESP Sao Jose do Rio Preto SP Brazil The rubber trees used for

the assay were cultivated at the same locality near from each other assuring that all the

plants had the same soil (nutrients and water quantities) and weather conditions

For each experiment healthy leaflets (ie without observable damage) were taken from

the sixth to eighth gems of the same plant from each of the clones GT 1 PB 235 and

RRIM 600 Thus all leaflets used had the same age once the suitability to herbivorous

mites may vary according to the concentration of nutrients and defenses of the leaves in

different ages (Karban and Thaler 1999 Awmack and Leather 2002) The clones above

were chosen for the assays because of their economic importance being the most culti-

vated in the State of Sao Paulo Brazil (Goncalves et al 2001)

Stock population

The rearing arenas were made from leaflets of the above mentioned clones by using the

method described by Ferla and Moraes (2003) for the same mite The leaflets were washed

with distilled water and placed with the adaxial surface face up on 2 cm thick nylon foam

Distilled water was added daily in order to maintain the water saturation of the foam and

the desired humidity of the air Cotton strips were added to the borders of each leaflet to

prevent the mites from escaping Each arena was kept inside an aluminium tray of

5 9 17 9 25 cm above which a glass plate was placed in order to maintain a humid

microhabitat for the mites (Ferla and Moraes 2003) A 1 cm free space was left in both

sides of the glass to prevent water condensation

The mites used to start the stock population were collected from leaflets of RRIM 600

from the experimental area described above The leaflets were examined under a dissecting

microscope and the females were transferred to the rearing arenas using a fine brush At

least 50 females were placed in the arenas of each rubber tree clone The arenas were kept

in a rearing chamber at 28 plusmn 1C 80 plusmn 10 RH and a photoperiod of 1212 h (LD) for at

least 3 weeks before the assays were conducted

Life cycle reproduction and survivorship of Calacarus heveae

The arenas were prepared for this assay as described above However a thin layer of cotton

was put over the nylon foam above which the leaflets were placed Moreover each leaflet

was divided into 14 cm 9 14 cm squares using strips of tissue paper in order to define the

study units for the life cycle investigation The experiment was performed in a rearing

chamber at 80 plusmn 10 RH A photoperiod of 1410 h (LD) with temperatures of 28 plusmn 1C

in the light phase (20 W fluorescent tubes) and 25 plusmn 1C in the dark phase was used in

order to simulate the field conditions occurring during the peak of C heveae infestation

The rubber tree loses leaves each year at the peak of the dry season (JunendashAugust)

Consequently the mites (including C heveae) associated with its leaves also occur sea-

sonally and exhibit peaks of population fluctuation (Daud and Feres 2007 Hernandes and

Feres 2006)

Exp Appl Acarol (2012) 5657ndash68 59

123

Seven females were added to each study unit for the same clone in their rearing arena

After 12 h the females were removed retaining in each unit only one of the eggs they

laid This procedure was repeated until a total of 20 eggs for each cloneassay had been

achieved Each unit was observed daily at 8 am 1 and 6 pm to verify the develop-

mental stage of the mites During the adult stage a single observation was made daily at

2 pm in order to obtain data on fecundity and survivorship Males were not placed with

females in the arenas because the indirect sperm transfer in mites of this family (Lind-

quist et al 1996) would make successful fecundation uncertain Moreover C heveaereproduces by arrhenotokous parthenogenesis (Ferla and Moraes 2003) and oviposition

can therefore take place in the absence of males At the first symptom of leaflet dete-

rioration (about 2 weeks) the mites were transferred to new study units Eggs during

incubation time were transferred together with a piece of substrate in order to avoid

damage by handling

Mites found dead on the arenas were mounted on glass slides using Hoyer medium

(Moraes and Flechtmann 2008) for confirmation of sex and as voucher specimens in the

Acari Collection (DZSJRP)mdashhttpwwwsplinkcriaorgbr Department of Zoology and

Botany UNESP Sao Jose do Rio Preto SP Brazil

Experimental design and statistical analysis

The assays were performed using a completely randomised design We used 20 replicates

(individuals) for each rubber tree clone The assays were performed during four distinct

periods (20 replicatescloneperiod) Period 1 (P1) from November to December 2005 (P2)

from January to February (P3) from March to April (P4) from May to June 2006

Accordingly the leaflets used in each assay represented the physiological condition of the

host plant during each period This approach allowed us to evaluate the seasonal suitability

of rubber tree clones to C heveae The periods selected represented the natural seasonal

occurrence of this mite species in rubber tree crops in the state of Sao Paulo (Hernandes

and Feres 2006)

The development time of each stage the fecundity and the duration of reproductive

phases of mites reared on different clones and periods were compared using two-way

factorial ANOVA where the factors involved were the clone and the period In the cases

when individual ANOVA terms are statistically significant we followed a planned com-

parison approach according to Snedecor and Cochran (1980) Considering our expected

differences among treatments we first verified if GT 1 was different from the other clones

(considering that it is expected to be more resistent (according to results of pilots exper-

iments) and then compared PB235 to RRIM 600 In all cases where an interaction between

clone and period occurred we explore possible differences using a posteriori Tukey tests

(Zar 1999)

The survivorship curves were estimated independently for each period from the

cumulative proportion of surviving mites by using the KaplanndashMeier method The survi-

vorship curves were compared using the Peto and Peto generalised Wilcoxon test as

extended for comparisons of more than two samples (Hosmer and Lemeshow 1999) Dead

mites found on the paper tissue stripes or accidentally killed due to handling were treated

as censored data in the latter test Males were included in the analysis of survivorship but

excluded from all other statistical analyses because of the small number of males in the

samples

60 Exp Appl Acarol (2012) 5657ndash68

123

Results

Biological cycle of Calacarus heveae

There were significative interaction between clones and periods in average lengths of the

egg incubation and in female longevity No statistical interactions were observed for the

nymph 1 stage however there were detected differences between the clones for this life

stage (Table 1)

The shortest incubation time (53 days) was observed on the clone RRIM 600 during

P1 whereas the longest (62 days) occurred on GT 1 during P2 In general mites reared on

GT 1 had longer incubation times than those observed for the other clones P3 was the sole

exception The average duration of the egg stage did not differ significantly across treat-

ments for mites reared during P3 (Tables 1 2)

The duration of the nymph 1 stage were higher on GT 1 than on PB 235 and RRIM 600

clones (planned comparisons F = 76 df = 1 P 0001) while there was no differences

in this parameter between the two latter clones (F = 021 df = 1 P = 064) The nymph 2

did not differ among treatments (Tables 1 2)

All the females reared during P1 had shorter average longevity than those reared under

other treatments The shortest longevity (29 days) was observed on GT 1 The females

having the longest observed longevities were reared on the clones PB 235 during P2 and

GT 1 during P3 (Tables 1 2)

Reproductive parameters of females

We observed differences in the average lengths of the oviposition and postoviposition

periods and in the fecundity (total number of eggs per female) of females reared on

different clones (Tables 1 3)

The length of the preoviposition period (12ndash26 days) did not differ among treatments

(Table 1) The longest oviposition period was observed on PB 235 during P2 and on GT 1

during P3 whereas the postoviposition period of females during P2 was approximately 16

times shorter than that occurring during P3 (Table 3)

The highest values of fecundity were observed on PB 235 during P3 and P2 namely 38 and

329 eggsfemale respectively The lowest fecundity 86 eggsfemale was observed on GT 1

during P2 (Table 1 Fig 1) Females reared on RRIM 600 during P2 also had high fecundity

(243 eggsfemale) However females reared on RRIM 600 during P3 had lower fecundity

than did the females reared on PB 235 The values of fecundity for the females reared on GT 1

during P3 were similar to the values for females reared on RRIM 600 (Fig 1)

The data from P1 to P4 were excluded from statistical analysis owing to the small

number of replicates obtained for GT 1 and RRIM 600 Moreover the few females (n = 4)

that reached the adult stage on GT 1 did not lay any eggs during P1

Population survivorship

Significant variation in population survivorship among the three clones occurred only

during P2 (Wilcoxon v2 = 754 gl = 2 P = 002) During this period the highest value

of survivorship was obtained for the mites reared on PB 235 whereas the lowest value

occurred on GT 1 Mites survived on average 14ndash20 days on PB 235 whereas most mites

survived at most 16 days on GT 1 (Fig 2b)

Exp Appl Acarol (2012) 5657ndash68 61

123

Table 1 Factorial ANOVA examining the effects of different clones and periods on biological parametersof Calacarus heveae

Parameters Source of variation df MS F P

Egg incubation

Clonesa 2 221 725 00009

Perioda 3 180 580 00008

Clones 9 perioda 6 069 225 004

Error 153 030

Nymph 1 stage

Clonesa 2 048 384 002

Period 3 020 160 019

Clones 9 period 6 013 105 039

Error 118 012

Nymph 2 stage

Clones 2 040 264 007

Period 3 038 253 006

Clones 9 period 6 021 141 022

Error 92 015

Female longevity

Clones 2 890 057 057

Perioda 2 14257 922 00004

Clones 9 perioda 4 7239 468 0003

Error 45 1546

Pre-oviposition

Clones 2 140 088 042

Period 2 356 224 012

Clones 9 E period 4 117 074 057

Error 46 159

Oviposition

Clones 2 473 058 056

Period 1 406 050 048

Clones 9 perioda 2 10326 1268 00001

Error 30 814

Post-oviposition

Clones 2 294 247 010

Perioda 1 908 765 001

Clones 9 period 2 058 049 062

Error 26 119

Fecundity (eggsfemale)

Clones 2 21461 322 005

Perioda 1 31564 473 004

Clones 9 perioda 2 74287 1114 00002

Error 32 6666

P4 excluded from statistical analysis owing to insufficient replicates obtained from RRIM 600

P1 and P4 excluded from statistical analysis owing to insufficient replicates obtained from GT 1 and RRIM 600a Significant at probability level of 5

62 Exp Appl Acarol (2012) 5657ndash68

123

During the other periods survivorship did not differ significantly among mites reared on

the three clones (P1 v2 = 04 gl = 2 P = 082 P3 v2 = 24 gl = 2 P = 029 P4

v2 = 17 gl = 2 P = 042) The estimated curves exhibited similar inclination patterns

within each period (Fig 2a c and d) Most mites reared during P1 survived for a maximum

of 10 days whereas those reared during P3 survived from 8 to 16 days and those reared

during P4 survived from 5 to 135 days (Fig 2a c and d)

Discussion

According to our results we can infer that the rubber trees clones studied showed seasonal

differences in their suitability to C heveae From November to December (period P1) the

leaflets of the clones PB 235 and RRIM 600 were suitable for the development of this mite

as indicated by the presence of ovipositing females However these females had lower

survivorship and fecundity compared to the corresponding values for mites reared during

P2 and P3 Seasonal variation in the resistance of cultivars to phytophagous mites has been

noted by Kerguelen and Hoddle (2000) who detected differences in the susceptibility of

avocado (Persea americana Miller Lauraceae) to attack by Oligonychus perseae Tuttle

Baker amp Abbatiello (Tetranychidae) during the few months surveyed Likewise Nukenine

Table 2 Mean duration (plusmn SE) in days of Calacarus heveae life stages on three rubber tree clones duringfour periods

Periodclones Life stages

Egg incubation Nymph 1 Nymph 2 Female longevity

(P1) NovndashDec2005

GT 1 57 plusmn 02ab (14) 24 plusmn 02 (12) 20 plusmn 02 (9) 29 plusmn 05b (3)

PB 235 54 plusmn 02b (10) 20 plusmn 003 (6) 17 plusmn 03 (5) 56 plusmn 09b (3)

RRIM 600 53 01b (17) 21 plusmn 007 (16) 19 plusmn 01 (12) 52 plusmn 20b (6)

(P2) JanndashFeb2006

GT 1 62 plusmn 01a (16) 22 plusmn 01 (10) 21 plusmn 02 (8) 64 plusmn 15b (5)

PB 235 58 plusmn 01ab (12) 19 plusmn 006 (12) 18 plusmn 01 (11) 122 plusmn 18a (9)

RRIM 600 55 plusmn 02b (14) 20 plusmn 01 (13) 19 plusmn 007 (12) 108 plusmn 11a (10)

(P3) MarndashApr

GT 1 59 plusmn 01ab (19) 22 plusmn 008 (15) 20 plusmn 008 (10) 145 plusmn 26a (4)

PB 235 61 plusmn 01a (18) 19 plusmn 006 (12) 20 plusmn 006 (10) 65 plusmn 10b (7)

RRIM 600 59 plusmn 02ab (12) 20 plusmn 004 (11) 18 plusmn 01 (9) 117 plusmn 11a (7)

(P4) MayndashJun

GT 1 61 plusmn 02a (11) 19 plusmn 007 (8) 21 plusmn 007 (7) 91 plusmn 14 (5)

PB 235 54 plusmn 01b (11) 21 plusmn 007 (8) 19 plusmn 006 (7) 107 plusmn 22 (3)

RRIM 600 56 plusmn 02ab (11) 19 plusmn 02 (7) 25 plusmn 03 (4) 60 (1)

The number of mites analysed is shown in parentheses

Means followed by different letters are significantly different (Tukey test P 005)

Only differences between clones were significant (see text)

No significant differences in development time among the treatments

Exp Appl Acarol (2012) 5657ndash68 63

123

Table 1 Factorial ANOVA examining the effects of different clones and periods on biological parametersof Calacarus heveae

Parameters Source of variation df MS F P

Egg incubation

Clonesa 2 221 725 00009

Perioda 3 180 580 00008

Clones 9 perioda 6 069 225 004

Error 153 030

Nymph 1 stage

Clonesa 2 048 384 002

Period 3 020 160 019

Clones 9 period 6 013 105 039

Error 118 012

Nymph 2 stage

Clones 2 040 264 007

Period 3 038 253 006

Clones 9 period 6 021 141 022

Error 92 015

Female longevity

Clones 2 890 057 057

Perioda 2 14257 922 00004

Clones 9 perioda 4 7239 468 0003

Error 45 1546

Pre-oviposition

Clones 2 140 088 042

Period 2 356 224 012

Clones 9 E period 4 117 074 057

Error 46 159

Oviposition

Clones 2 473 058 056

Period 1 406 050 048

Clones 9 perioda 2 10326 1268 00001

Error 30 814

Post-oviposition

Clones 2 294 247 010

Perioda 1 908 765 001

Clones 9 period 2 058 049 062

Error 26 119

Fecundity (eggsfemale)

Clones 2 21461 322 005

Perioda 1 31564 473 004

Clones 9 perioda 2 74287 1114 00002

Error 32 6666

P4 excluded from statistical analysis owing to insufficient replicates obtained from RRIM 600

P1 and P4 excluded from statistical analysis owing to insufficient replicates obtained from GT 1 and RRIM 600a Significant at probability level of 5

62 Exp Appl Acarol (2012) 5657ndash68

123

During the other periods survivorship did not differ significantly among mites reared on

the three clones (P1 v2 = 04 gl = 2 P = 082 P3 v2 = 24 gl = 2 P = 029 P4

v2 = 17 gl = 2 P = 042) The estimated curves exhibited similar inclination patterns

within each period (Fig 2a c and d) Most mites reared during P1 survived for a maximum

of 10 days whereas those reared during P3 survived from 8 to 16 days and those reared

during P4 survived from 5 to 135 days (Fig 2a c and d)

Discussion

According to our results we can infer that the rubber trees clones studied showed seasonal

differences in their suitability to C heveae From November to December (period P1) the

leaflets of the clones PB 235 and RRIM 600 were suitable for the development of this mite

as indicated by the presence of ovipositing females However these females had lower

survivorship and fecundity compared to the corresponding values for mites reared during

P2 and P3 Seasonal variation in the resistance of cultivars to phytophagous mites has been

noted by Kerguelen and Hoddle (2000) who detected differences in the susceptibility of

avocado (Persea americana Miller Lauraceae) to attack by Oligonychus perseae Tuttle

Baker amp Abbatiello (Tetranychidae) during the few months surveyed Likewise Nukenine

Table 2 Mean duration (plusmn SE) in days of Calacarus heveae life stages on three rubber tree clones duringfour periods

Periodclones Life stages

Egg incubation Nymph 1 Nymph 2 Female longevity

(P1) NovndashDec2005

GT 1 57 plusmn 02ab (14) 24 plusmn 02 (12) 20 plusmn 02 (9) 29 plusmn 05b (3)

PB 235 54 plusmn 02b (10) 20 plusmn 003 (6) 17 plusmn 03 (5) 56 plusmn 09b (3)

RRIM 600 53 01b (17) 21 plusmn 007 (16) 19 plusmn 01 (12) 52 plusmn 20b (6)

(P2) JanndashFeb2006

GT 1 62 plusmn 01a (16) 22 plusmn 01 (10) 21 plusmn 02 (8) 64 plusmn 15b (5)

PB 235 58 plusmn 01ab (12) 19 plusmn 006 (12) 18 plusmn 01 (11) 122 plusmn 18a (9)

RRIM 600 55 plusmn 02b (14) 20 plusmn 01 (13) 19 plusmn 007 (12) 108 plusmn 11a (10)

(P3) MarndashApr

GT 1 59 plusmn 01ab (19) 22 plusmn 008 (15) 20 plusmn 008 (10) 145 plusmn 26a (4)

PB 235 61 plusmn 01a (18) 19 plusmn 006 (12) 20 plusmn 006 (10) 65 plusmn 10b (7)

RRIM 600 59 plusmn 02ab (12) 20 plusmn 004 (11) 18 plusmn 01 (9) 117 plusmn 11a (7)

(P4) MayndashJun

GT 1 61 plusmn 02a (11) 19 plusmn 007 (8) 21 plusmn 007 (7) 91 plusmn 14 (5)

PB 235 54 plusmn 01b (11) 21 plusmn 007 (8) 19 plusmn 006 (7) 107 plusmn 22 (3)

RRIM 600 56 plusmn 02ab (11) 19 plusmn 02 (7) 25 plusmn 03 (4) 60 (1)

The number of mites analysed is shown in parentheses

Means followed by different letters are significantly different (Tukey test P 005)

Only differences between clones were significant (see text)

No significant differences in development time among the treatments

Exp Appl Acarol (2012) 5657ndash68 63

123

During the other periods survivorship did not differ significantly among mites reared on

the three clones (P1 v2 = 04 gl = 2 P = 082 P3 v2 = 24 gl = 2 P = 029 P4

v2 = 17 gl = 2 P = 042) The estimated curves exhibited similar inclination patterns

within each period (Fig 2a c and d) Most mites reared during P1 survived for a maximum

of 10 days whereas those reared during P3 survived from 8 to 16 days and those reared

during P4 survived from 5 to 135 days (Fig 2a c and d)

Discussion

According to our results we can infer that the rubber trees clones studied showed seasonal

differences in their suitability to C heveae From November to December (period P1) the

leaflets of the clones PB 235 and RRIM 600 were suitable for the development of this mite

as indicated by the presence of ovipositing females However these females had lower

survivorship and fecundity compared to the corresponding values for mites reared during

P2 and P3 Seasonal variation in the resistance of cultivars to phytophagous mites has been

noted by Kerguelen and Hoddle (2000) who detected differences in the susceptibility of

avocado (Persea americana Miller Lauraceae) to attack by Oligonychus perseae Tuttle

Baker amp Abbatiello (Tetranychidae) during the few months surveyed Likewise Nukenine

Table 2 Mean duration (plusmn SE) in days of Calacarus heveae life stages on three rubber tree clones duringfour periods

Periodclones Life stages

Egg incubation Nymph 1 Nymph 2 Female longevity

(P1) NovndashDec2005

GT 1 57 plusmn 02ab (14) 24 plusmn 02 (12) 20 plusmn 02 (9) 29 plusmn 05b (3)

PB 235 54 plusmn 02b (10) 20 plusmn 003 (6) 17 plusmn 03 (5) 56 plusmn 09b (3)

RRIM 600 53 01b (17) 21 plusmn 007 (16) 19 plusmn 01 (12) 52 plusmn 20b (6)

(P2) JanndashFeb2006

GT 1 62 plusmn 01a (16) 22 plusmn 01 (10) 21 plusmn 02 (8) 64 plusmn 15b (5)

PB 235 58 plusmn 01ab (12) 19 plusmn 006 (12) 18 plusmn 01 (11) 122 plusmn 18a (9)

RRIM 600 55 plusmn 02b (14) 20 plusmn 01 (13) 19 plusmn 007 (12) 108 plusmn 11a (10)

(P3) MarndashApr

GT 1 59 plusmn 01ab (19) 22 plusmn 008 (15) 20 plusmn 008 (10) 145 plusmn 26a (4)

PB 235 61 plusmn 01a (18) 19 plusmn 006 (12) 20 plusmn 006 (10) 65 plusmn 10b (7)

RRIM 600 59 plusmn 02ab (12) 20 plusmn 004 (11) 18 plusmn 01 (9) 117 plusmn 11a (7)

(P4) MayndashJun

GT 1 61 plusmn 02a (11) 19 plusmn 007 (8) 21 plusmn 007 (7) 91 plusmn 14 (5)

PB 235 54 plusmn 01b (11) 21 plusmn 007 (8) 19 plusmn 006 (7) 107 plusmn 22 (3)

RRIM 600 56 plusmn 02ab (11) 19 plusmn 02 (7) 25 plusmn 03 (4) 60 (1)

The number of mites analysed is shown in parentheses

Means followed by different letters are significantly different (Tukey test P 005)

Only differences between clones were significant (see text)

No significant differences in development time among the treatments

Exp Appl Acarol (2012) 5657ndash68 63

123

et al (2000) have observed infestations of Mononychellus tanajoa Bondar (Tetranychidae)

associated with seasonal variations in the levels of nutrients in cassava leaves (Manihotesculenta Crantz Euphorbiaceae)

Table 3 Mean durations (plusmn SE) in days of Calacarus heveae female reproductive periods on three rubbertree clones during the four periods studied

Periodclones Female reproductive periods

Pre-oviposition Oviposition Post-oviposition

(P1) NovndashDec05a

GT 1 29 plusmn 05 (3) ndash ndash

PB 235 24 plusmn 07 (3) 18 plusmn 07 (3) 14 plusmn 04 (3)

RRIM 600 22 plusmn 05 (6) 56 plusmn 37 (3) ndash

(P2) JanndashFeb06

GT 1 12 plusmn 02 (5) 41 plusmn 14b (5) 14 plusmn 02 (4)

PB 235 17 plusmn 08 (8) 113 plusmn 10a (7) 26 plusmn 05 (6)

RRIM 600 15 plusmn 02 (10) 87 plusmn 08ab (9) 17 plusmn 04 (8)

(P3) MarndashApr

GT 1 16 plusmn 02 (6) 100 plusmn 24a (4) 30 plusmn 07 (4)

PB 235 26 plusmn 07 (7) 40 plusmn 04b (4) 37 plusmn 09 (3)

RRIM 600 12 plusmn 02 (7) 80 plusmn 10ab (7) 24 plusmn 02 (7)

(P4) MayndashJuna

GT 1 23 plusmn 11 (5) 65 plusmn 15 (4) 20 plusmn 04 (4)

PB 235 17 plusmn 03 (3) 60 plusmn 30 (3) 30 plusmn 10 (3)

RRIM 600 20 (1) 10 (1) 30 (1)

The number of mites analysed is shown in parentheses

No significant differences in mean duration for this stage

Means followed by different letters are significantly different (Tukey test P 005)

Differences between periods P2 and P3a Inadequate number of females for statistical analysis

Fig 1 Mean (SE) fecundity of females reared on leaflets of three rubber tree clones at four periods Meanscapped by different letters are significantly different (Tukey test P 005) Excluded from statisticaltesting owing to the small number of females reaching the adult phase

64 Exp Appl Acarol (2012) 5657ndash68

123

Mites reared during P2 and P3 had higher fecundity longer periods of oviposition and

higher survivorship on the three clones studied This result indicates that the rubber tree

leaflets collected from January to April furnished better conditions for the development of

C heveae These findings agree with field studies conducted in the state of Sao Paulo

These field studies have recorded heavy infestations of this species mostly from March to

April at the end of the rainy season (Demite and Feres 2005 Hernandes and Feres 2006

Vis et al 2006 Feres et al 2002 Vieira and Gomes 1999)

The mites reared on the clone GT 1 exhibited low performance during P1 During this

period C heveae had longer developmental stages did not reach the reproductive stage

and had low survivorship During P2 population survivorship and fecundity were lower on

GT 1 than on PB 235 or RRIM 600 These results suggest that the clone GT 1 furnishes the

least favourable conditions of any clone in this study for the development and survivorship

of C heveae This finding agrees with field observations of this species on GT 1 in

comparison with RRIM 600 (Daud and Feres 2007)

Of the three clones studied PB 235 was considered to be the most suitable to C heveaebecause females reared on that clone had higher fecundity during P2 and P3 because they

required shorter times to reach the adult stage and because they had the highest survi-

vorship during P2 RRIM 600 exhibited intermediate suitability to C heveae as indicated

by the analysis of survivorship and female oviposition at P2 and P3

Daud and Feres (2007) have found that in the field C heveae occurrence on PB 235 is

lower than that on GT 1 or RRIM 600 This finding suggests that the resistance of PB 235

to the mite is higher However like Furquim (1994) our results suggest the opposite

conclusion A possible explanation of these differences might be that the rubber trees

Fig 2 Survivorship curves estimated by the KaplanndashMeier cumulative proportion method for Calacarusheveae populations kept on leaflets of three rubber tree clones at four periods Legends a P1mdashNovemberndashDecember 2005 b P2mdashJanuaryndashFebruary c P3mdashMarchndashApril and d P4mdashMayndashJune 2006

Exp Appl Acarol (2012) 5657ndash68 65

123

Mites reared during P2 and P3 had higher fecundity longer periods of oviposition and

higher survivorship on the three clones studied This result indicates that the rubber tree

leaflets collected from January to April furnished better conditions for the development of

C heveae These findings agree with field studies conducted in the state of Sao Paulo

These field studies have recorded heavy infestations of this species mostly from March to

April at the end of the rainy season (Demite and Feres 2005 Hernandes and Feres 2006

Vis et al 2006 Feres et al 2002 Vieira and Gomes 1999)

The mites reared on the clone GT 1 exhibited low performance during P1 During this

period C heveae had longer developmental stages did not reach the reproductive stage

and had low survivorship During P2 population survivorship and fecundity were lower on

GT 1 than on PB 235 or RRIM 600 These results suggest that the clone GT 1 furnishes the

least favourable conditions of any clone in this study for the development and survivorship

of C heveae This finding agrees with field observations of this species on GT 1 in

comparison with RRIM 600 (Daud and Feres 2007)

Of the three clones studied PB 235 was considered to be the most suitable to C heveaebecause females reared on that clone had higher fecundity during P2 and P3 because they

required shorter times to reach the adult stage and because they had the highest survi-

vorship during P2 RRIM 600 exhibited intermediate suitability to C heveae as indicated

by the analysis of survivorship and female oviposition at P2 and P3

Daud and Feres (2007) have found that in the field C heveae occurrence on PB 235 is

lower than that on GT 1 or RRIM 600 This finding suggests that the resistance of PB 235

to the mite is higher However like Furquim (1994) our results suggest the opposite

conclusion A possible explanation of these differences might be that the rubber trees

Fig 2 Survivorship curves estimated by the KaplanndashMeier cumulative proportion method for Calacarusheveae populations kept on leaflets of three rubber tree clones at four periods Legends a P1mdashNovemberndashDecember 2005 b P2mdashJanuaryndashFebruary c P3mdashMarchndashApril and d P4mdashMayndashJune 2006

Exp Appl Acarol (2012) 5657ndash68 65

123

studied by Daud and Feres (2007) were 18 years old whereas the trees in the present

study were only 6 years old Previous studies have revealed that variation in susceptibility

of a cultivar might result from differences in the ages of the plants studied (Nukenine

et al 2000 Karban and Thaler 1999 Kearsley and Whitham 1989 Cook and Smith

1988) Another explanation of these variations in susceptibility might be that the plants

used in this study differed genetically from the plants studied by Daud and Feres (2007)

even though both supposedly belonged to the same clone Findings by Colombo et al

(2000) further support this hypothesis These authors have reported that PB 235 plants

from different localities were found to bear different genetic material Opit et al (2001)

also noted a similar discrepancy between their results and the results of other authors

regarding the susceptibility of cultivars of Pelargonium peltatum (L) LrsquoHex ex Ait

(Geraniaceae) to Tetranychus urticae Koch (Tetranychidae) They suggested that the

reason for this discrepancy was that the plants studied had originated from different

localities

Our results indicate that resistance to C heveae was highest for clone GT 1 and lower

for clones RRIM 600 and PB 235 and that this difference in resistance was primarily

expressed from November to February Therefore growing rubber trees of the former

clone might be an alternative means of reducing the population of this mite in the field

However other characteristics of this clone must to be considered including latex yield

and adaptations of the clone to soil and weather conditions More studies are needed to

identify the biological traits of the rubber trees (eg nutrients alkaloids) that are

responsible for the seasonal suitability to this mite observed in GT 1

Acknowledgments We thank lsquolsquoPlantacoes E Michelin Ltdarsquorsquo Itiquira MT and the institutions FAPERP(Fundacao de Apoio a Pesquisa e Extensao de Sao Jose do Rio Preto) and APABOR (Associacao Paulistados Produtores e Beneficiadores de Borracha) for their financial support CAPES (Coordenacao de Aper-feicoamento de Pessoal de Nıvel Superior) for a doctoral scholarship awarded to the senior author andRaquel G Kishimoto and Marcelo DelrsquoArco (UNESP Sao Jose do Rio Preto) for technical assistance withthe assays We also thank Paulo De Marco Junior (Universidade Federal de Goias Brazil) for criticallyreviewing the manuscript

References

Awmack CS Leather SR (2002) Host plant quality and fecundity in herbivorous insects Annu Rev Entomol47817ndash844

Boina D Prabhakar S Smith CM Starkey S Zhu L Boyko E Reese JC (2005) Categories of resistance tobiotype I greenbugs (Homoptera Aphididae) in wheat lines containing the greenbug resistance genesGbx and Gby J Kans Entomol Soc 78252ndash260

Colombo C Goncalves OS Maciel ACB Camargo A Favarin AC (2000) Identificacao de variacao geneticadentro de clones comerciais de seringueira alerta na heveicultura In Congresso Nacional de Genetica46 Aguas de Lindoia

Cook CA Smith CM (1988) Resistance plants as an alternative to chemical control of insects pitfalls toprogress Fla Entomol 71546ndash553

Daud RD Feres RJF (2007) Dinamica populacional de acaros fitofagos (Acari Eriophyidae Tenuipalpidae)em seis clones de seringueira no sul do Estado de Mato Grosso Rev Bras Entomol 51377ndash381 doi101590S0085-56262007000300016

Demite PR Feres RJF (2005) Influencia de vegetacao vizinha na distribuicao de acaros em seringal (Heveabrasiliensis Muell Arg Euphorbiaceae) em Sao Jose do Rio Preto SP Neotrop Entomol 34829ndash836doi101590S1519-566X2005000500016

Erb WA Lindiquist RK Flickinger NJ Casey ML (1994) Resistance of selected interspecific lycopersiconhybrids to greenhouse whitefly (Homoptera Aleurodidae) Fla Entomol 77104ndash116

66 Exp Appl Acarol (2012) 5657ndash68

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Feres RJF (2000) Levantamento e observacoes naturalısticas da acarofauna (Acari Arachnida) de se-ringueiras cultivadas (Hevea spp Euphorbiaceae) no Brasil Rev Bras Zool 17157ndash173 doi101590S0101-81752000000100011

Feres RJF de Rossa-Feres DC Daud RD Santos RS (2002) Diversidade de acaros em seringueiras (Heveabrasiliensis Muell Arg Euphorbiaceae) na regiao noroeste do estado de Sao Paulo Brasil Rev BrasZool 19137ndash144 doi101590S0101-81752002000100011

Feres RJF DelrsquoArco M Daud RD (2010) Biological cycle of Tenuipalpus heveae Baker (Acari Tenui-palpidae) on leaflets of three rubber tree clones Rev Bras Entomol 54298ndash303 doi101590S0085-56262010000200013

Ferla NJ Moraes GJ (2002) Acaros (Arachnida Acari) da seringueira (Hevea brasiliensis Muell Arg) noestado do Mato Grosso Brasil Rev Bras Zool 19867ndash888 doi101590S0101-81752002000300025

Ferla NJ Moraes GJ (2003) Ciclo biologico de Calacarus heveae Feres 1992 (Acari Eriophyidae) RevBras Entomol 47399ndash402 doi101590S0085-56262003000300006

Furquim GV (1994) Flutuacao populacional de acaros e caracterizacao de sintomas de Calacarus heveaeem clones de seringueira (Hevea brasiliensis Muell Arg) cultivados em Jaboticabal SP MonographUniversidade Estadual Paulista

Goncalves PS Bataglia OC Ortolani AA Fonseca FS (2001) Manual de heveicultura para o estado de SaoPaulo Boletim Tecnico IAC 18977p

Hennessey MK Knight RJ Schnell RJ (1995) Antibiosis to caribbean fruit fly (Diptera Tephritidae)immature stages in carambola germplasm Fla Entomol 78354ndash357

Hernandes FA Feres RJF (2006) Diversidade e sazonalidade de acaros (Acari) em seringal (Hevea bra-siliensis Muell Arg) no noroeste do Estado de Sao Paulo Neotrop Entomol 35523ndash535 doi101590S1519-566X2006000400016

Hosmer DW Jr Lemeshow S (1999) Applied survival analysis regression modeling of time to event dataWiley New York

Karban R Thaler JS (1999) Plant phase change and resistance to herbivory Ecology 80510ndash517 doi1018900012-9658(1999)080[0510PPCART]20CO2

Kearsley JC Whitham TG (1989) Development changes in resistance to herbivory implications for indi-viduals and populations Ecology 70422ndash434 doi1023071937547

Kerguelen V Hoddle MS (2000) Comparison of susceptibility of several cultivars of avocado to the perseamite Oligonychus perseae (Acari Tetranychidae) Sci Hortic 84101ndash114

Lara FM (1991) Princıpios de resistencia de plantas a insetos Icone Editora 2a edicao Sao PauloLara FM Tanzini MR (1997) Nonpreference of the lace bug Leptopharsa heveae Drake amp Poor (Het-

eroptera Tingidae) for rubber tree clones An Soc Entomol Bras 26429ndash434 doi101590S0301-80591997000300003

Lindquist EE Sabelis MW Bruin J (1996) Eriophyiods mites their biology natural enemies and controlElsevier Amsterdan

Moraes GJ de Flechtmann CHW (2008) Manual de Acarologia Acarologia basica e acaros de plantascultivadas no Brasil Holos editora Ribeirao Preto

Nukenine EN Hassan AT Dixon AGO (2000) Influence of variety on the within-plant distribution of cassavagreen spider mite (Acari Tetranychidae) and leaf anatomical characteristics and chemical componentsin relation to varietal resistance Int J Pest Manag 46177ndash186 doi101080096708700415508

Opit GP Jonas VM Willians KA Margolies DC Nechols JR (2001) Effects of cultivar and irrigationmanagement on population growth of the twospotted spider mite Tetranychus urticae on greenhouseivy geranium Exp Appl Acarol 25849ndash857 doi101023A102045311882

Panizzi AR Parra JRP (2009) Bioecologia e nutricao de insetos base para o manejo integrado de pragasEmbrapa Informacao Tecnologica Brasılia

Reinert JA Engelke MC Read JC (2004) Host resistance to insects and mites a review-a major IPMstrategy in turfgrass culture Acta Hort 661436ndash486

Reinert JA Taliaferro CM McAfee JA (2008) Susceptibility of bermudagrass (Cynodon) varieties tobermudagrass mite (Eriophyes cynodoniensis) Acta Hort 783519ndash528

Resende MTV Maluf WR Cardoso MG Faria MV Goncalves LD Nascimento IR (2008) Resistance oftomato genotypes with high level of acylsugars to Tetranychus evansi Baker amp Pritchard Sci Agric6531ndash35 doi101590S0103-90162008000100005

Rodriguez JG Reicosky DA Patterson CG (1983) Soybean and mite interaction effects of cultivar andplant growth stage J Kans Entomol Soc 56320ndash326

Snedecor GW Cochran WG (1980) Statistical methods The Iowa State University Press AmesVieira MR Gomes EC (1999) Sintomas desfolhamento e controle de Calacarus heveae Feres 1992 (Acari

Eriophyidae) em seringueira (Hevea brasiliensis Muell Arg) Cult Agron 853ndash71

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123

Vieira MR Silva HAS Cardoso MM Figueira JC (2009) Progenies de seringueira com potencial paraconferir resistencia a acaros (Calacarus heveae feres e Tenuipalpus heveae baker) Ciencia Rural391953ndash1959 doi101590S0103-84782009005000164

Vis MJ de Moraes GJ de Bellini MR (2006) Mites (Acari) of rubber trees (Hevea brasiliensis Muell ArgEuphorbiaceae) in Piracicaba State of Sao Paulo Brazil Neotrop Entomol 35112ndash120 doi101590S1519-566X2006000100015

Zar JH (1999) Biostatistical analysis 4th edn Prentice-Hall New Jersey

68 Exp Appl Acarol (2012) 5657ndash68

123