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
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
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
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
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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
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123
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
Exp Appl Acarol (2012) 5657ndash68 67
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
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
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
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
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
123
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
Exp Appl Acarol (2012) 5657ndash68 67
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
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
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
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
123
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
Exp Appl Acarol (2012) 5657ndash68 67
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
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
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
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
123
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
Exp Appl Acarol (2012) 5657ndash68 67
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
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
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
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
123
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
Exp Appl Acarol (2012) 5657ndash68 67
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
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
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
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
123
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
Exp Appl Acarol (2012) 5657ndash68 67
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
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
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
123
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
Exp Appl Acarol (2012) 5657ndash68 67
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
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
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
123
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
Exp Appl Acarol (2012) 5657ndash68 67
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
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
123
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
Exp Appl Acarol (2012) 5657ndash68 67
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
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
123
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
Exp Appl Acarol (2012) 5657ndash68 67
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
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
Exp Appl Acarol (2012) 5657ndash68 67
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
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
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