238

TAXON 57 (1) bull February 2008 238ndash242Inbar bull Aphids and Pistacia classification

INTRODUCTION

hellip aphids could probably be much more utilized in decision-making in systematic botany

(D Hille Ris Lambers 1979)

The pistachio tree Pistacia vera L (Anacardiaceae) was first cultivated in Central Asia (Iran Afghanistan) then spread to the Middle East and eventually to other parts of the world (Hormaza amp al 1994) The grow-ing interest in pistachio cultivation stresses the need for vigorous rootstocks based on related wild Pistacia spe-cies Therefore identification and conservation of wild Pistacia species and their hybrids have become highly important and germplasm collections have been estab-lished (Sheiban 1995 Golan-Goldhirsh amp Kostiukovsky 1998) Due to misnaming polymorphism and the exis-tence of hybrids the classification of the genus Pistacia is not fully clear Since the seminal monograph by Zohary (1952) several methods have been used to identify Pista-cia species and construct their phylogenetic relationships The methods employed include morphological anatomi-cal cytological palynological physiological and molecu-lar analyses (Zohary 1952 Grundwag amp Werker 1976 Parfitt amp Badenes 1997 Kafkas amp al 2002 Katsiotis amp al 2003 Golan-Goldhirsh amp al 2004 Ahmad amp al 2005) But some confusion and disagreements on Pistacia classification still exist at all levels

Based on morphological characters Zohary (1952) divided the genus Pistacia into four sections Lentiscella (New World species) Lentiscus (evergreens) Butmela (P

atlantica Desf) and Terebinthus (P chinensis Bunge P khinjuk Stocks P palaestina Bois P terebinthus L P vera L) The latter section is composed of deciduous trees with unwinged leaf rachis and sclerified drupes Because of its winged leaf rachis P atlantica was placed in the separate Butmela section (Zohary 1952) This early char-acterization by Zohary has been challenged by modern molecular analyses Parfitt amp Badenes (1997) recognized two sections ldquoLentiscusrdquo (P lentiscus L P mexicana Kunth P texana Swingle P weinmannifolia Poisson) and a monophyletic group (ldquoTerebinthusrdquo) composed of all other species Golan-Goldhirsh amp al (2004) placed P atlantica in a separated still questionable position Kafkas amp Perl-Treves (2002) came out with two differ-ent subdivisions One includes the big single-trunk trees (P atlantica P eurycarpa P integerrima P khinjuk P vera) and the other group is composed of the shrubs and small trees (P lentiscus P mexicana P palaestina P texana P terebinthus)

Pistacia spp are the obligate host for specialized gall-forming aphids (Homoptera Fordinae) Gall-form-ing insects have very close relationships with their host plants The galling process involves intimate crosstalk between the plant and the insect genotypes The insects are obligated to a specific host plant species organ and tissue (Weis amp al 1988) Indeed several studies have used gall-forming insects as a tool in plant systemat-ics (Meeuse 1973 Aguilar amp Boecklen 1992 Floate amp Whitham 1995 Floate amp al 1996 Abrahamson amp al 1998 Burckhardt amp Basset 2000) About thirty spe-cies of gall-forming aphids belonging to the subfamily Fordinae (Pemphigidae) are associated with the genus

Systematics of Pistacia Insights from specialist parasitic aphids

Moshe Inbar

Department of Evolutionary amp Environmental Biology University of Haifa Haifa 31905 Israel minbarresearchhaifaacil

Clarifying the systematics of the genus Pistacia (Anacardiaceae) has been a challenging task The use of sev-eral classical and modern classification tools resulted in disagreements Pistacia spp are the obligate hosts of highly specialized gall-forming aphids (Homoptera Fordinae) It is well known that closely related species of insects may utilize closely related plants A complete linkage cluster analysis of Pistacia species based on presenceabsence of thirteen aphid genera is presented Aphids recognized between evergreen and New World Pistacia species Other Pistacia species are clustered into two groups ldquoVerardquo (P vera P atlantica P mutica) and ldquoKhinjukrdquo (P khinjuk P chinensis P integerrima P palaestina P terebinthus) Fordinae contribution to Pistacia taxonomy at the species and hybrid levels is discussed The close association between insect herbivores and their hosts deserves to be used more often by plant taxonomists

KEYWORDS aphids cluster analysis gall Pistacia taxonomy

239

Inbar bull Aphids and Pistacia classificationTAXON 57 (1) bull February 2008 238ndash242

Pistacia (Blackman amp Eastop 1994) Most species are found in Central Asia and in Mediterranean-type habi-tats in Asia Europe and North Africa (Bodenheimer amp Swirski 1957 Koach amp Wool 1977) The galls are highly divergent in shape and size (Koach amp Wool 1977 Inbar amp al 2004) Usually each aphid species makes a specific gall on specific Pistacia species in which they feed on the phloem sap (Inbar amp Wool 1995 Inbar amp al 1995) The complex life cycle of the aphids includes sexual and asexual reproduction and regular alternation between the primary Pistacia host and roots of non-specific second-ary hosts The basic life cycle (which may have a few modifications) is as follows In early spring the galls are formed by the first instar nymphs (fundatrices) hatching from overwintering eggs Within each gall two to three additional aphid generations are produced parthenogeneti-cally In fall winged aphids (fall migrants) disperse from the galls and the subsequent generations develop on the secondary hosts The next spring another winged morph (sexuparae) migrates back to the Pistacia and gives birth to the sexual stage (males and females) After mating the fertilized eggs remain on the tree until the fundatrices hatch the following year (Bodenheimer amp Swirski 1957 Wool 1984)

The aim of this paper was to use the gall-forming aphids as zoologically-based method for identifying spe-cies inbreeds and relatedness among Pistacia species

MATERIALS AND METHODSAphidsrsquo taxonomy might also be problematic due

to the wide distribution of aphids and plants and the morphological plasticity within species at different gen-erations and stages which cause misidentifications and consequently misinterpretations In order to eliminate some of the confusion this analysis was restricted to the more consensus genus level The taxonomic literature was thoroughly reviewed (see references in Table 1) Once the list of aphid genera was completed (literature review personal information) a cluster analysis was conducted based on presenceabsence of the aphid genera on each Pistacia using the complete linkage model with Pearsonrsquos r distances of the Statistica software package (StatSoft Inc Tulsa OK USA)

RESULTS AND DISCUSSIONThirteen aphid genera were recognized in the current

analysis (Table 1) This list is slightly different from the one complied by Blackman amp Eastop (1994) For example they listed Smynthurodes betae from P terebinthus and the aphid genus Forda on P lentiscus According to the current survey and personal observations these are most probably mistakes Blackman amp Eastop (1994) also noted

Table 1 List of gall-forming aphids (genera) and Pistacia hosts recognized in this study See text for discrepancies with Blackman amp Eastop (1994)

Aphid genus Pistacia species ReferencesAloephagous aethiopica Blackman amp Eastop 1994Aploneura lentiscus Koach amp Wool 1977Asiphonella chinensis khinjuk palaestina Remaudiegravere amp Tao 1957 Davatchi 1958 Koach amp

Wool 1977Baizongia chinensis integerrima khinjuk palaestina

terebinthusDavatchi 1958 Zhang 1995 Chakrabarti 1998 Peacuterez Hidalgo amp Nieto Nafriacutea 2003

Chaetogeoica chinensis Remaudiegravere amp Tao 1957Forda atlantica chinensis integerrima khinjuk mutica

palaestina terebinthus vera Davatchi 1958 Blackman amp Eastop 1994 Chakra-barti 1998 Peacuterez Hidalgo amp Nieto Nafriacutea 2003

Fordini a atlantica Koach amp Wool 1977 Wool amp Manheim (pers comm)Geoica atlantica integerrima khinjuk mutica palaestina

terebinthusDavatchi 1958 Brown amp Blackman 1994 Chakrabarti 1998

Geopemohigus mexicana texana Muntildeoz-Viveros amp Remaudiegravere 1999Paracletus khinjuk palaestina terebinthus Davatchi 1958 Blackman amp Eastop 1994Rectinasus khinjuk palaestina Davatchi 1958 Koach amp Wool 1977Slavum atlantica mutica vera Davatchi 1958 Koach amp Wool 1977Smynthurodes atlantica mutica Davatchi 1958 Koach amp Wool 1977Note No galls are known from P saportaaAccording to D Wool O Manheim (submitted MS) and G Remaudiegravere (pers comm) the Fordini spp listed in Koach amp Wool (1977) belong to a new genus

240

TAXON 57 (1) bull February 2008 238ndash242Inbar bull Aphids and Pistacia classification

that P vera bears three aphid genera (Baizongia Geoica Paracletus) that were not mentioned in the thorough study of the Iranian fauna on Pistacia (Davatchi 1958) Because P vera is cultivated and different studies might be in-fluenced by its variety two sets of cluster analyses were conducted with and without the three above-mentioned genera on this tree Nevertheless adding these aphid gen-era to the analysis resulted in similar clustering (Fig 1)

Division into sections mdash The aphid-based associa-tion found P lentiscus P aethiopica and the two indistin-guishable New World species (P mexicana P texana) in a clear distinct position from all other species They each host exclusive aphid fauna and therefore the aphids can-not provide useful information about their phylogenetic relationships with other Pistacia species It is important to note that the New World Pistacia regardless of their similarity to other species has a very little chance to be infested by the Old World aphids

Other Pistacia species were clustered into two clades (Fig 1) The first hereinafter the ldquoVerardquo group includes P vera P atlantica and P mutica This places P atlan-tica closely related to P vera The second hereinafter the ldquoKhinjukrdquo group includes P chinensis P integerrima P khinjuk P palaestina and P terebinthus Slavum is an aphid genus associated with the ldquoVerardquo group while Baizongia is typically found on the ldquoKhinjukrdquo group (Table 1) The aphid genera Forda and Geoica are wide spread within the two Pistacia groups indicating frequent host shiftes (Inbar amp al 2004) The fact that Forda and Geoica do not form galls on P lentiscus despite its partial distribution overlap with other Old World Pistacia spe-cies (around the Mediterranean) places this evergreen shrub in an evidently distinct position (section) as was suggested before by Golan-Goldhirsh amp al (2004) and Zohary (1952) Furthermore according to the aphids plac-ing P lentiscus in a section together with parts of the ldquoVerardquo or ldquoKhinjukrdquo members (Kafkas amp Perl-Treves 2002 Parfitt amp Badenes 1997) might not be justified

During the process of host plant selection and suc-cessful gall formation the aphids should assess plant chemical anatomical physiological and structural aspects (Hille Ris Lambers 1979 Weis amp al 1988) Mismatches usually end up with low fitness or death Thus host shifts among specific phytophagous insects take place accord-ing to chemical similarities between the original and the new plants (Becerra 1997 Mitter amp al 1991) closely re-lated insect taxa will usually feed on closely related plant species The aphid genera Geoica and Forda found on Pistacia species from both ldquoVerardquo and ldquoKhinjukrdquo indicate that these groups are close enough to facilitate repeated successful host shifts of aphids between them

Perhaps one of the most surprising results is the simi-larity between aphid genera (not species) which was found on P palaestina and P khinjuk It should be stressed that

previous morphological and molecular analyses found P vera and P khinjuk closely related (Zohary 1952 Parfitt amp Badenes 1997 Kafkas amp Perl-Treves 2002 Golan-Goldhirsh amp al 2004) Due to its wide distribu-tion its tendency to form hybrids and its local misnaming (Browicz 1988 Kafkas amp Perl-Treves 2002) some ento-mologists might have mistakenly recognized P khinjuk as the host of the aphids However even if some mistakes have occurred this cannot change the close relationships between P khinjuk and P palaestina (and P terebinthus) which share several aphid genera (Table 1) A reasonable speculation would be that P khinjuk diverted directly from P vera (Zohary 1952 Parfitt amp Badenes 1997 Kafkas amp Perl-Treves 2002 Golan-Goldhirsh amp al 2004) but soon established association with new aphid genera such as Baizongia and Paracletus

Fig 1 Cluster analysis of Pistacia species based upon presenceabsence of gall-forming aphidrsquos (Fordinae) gen-era The dendrogram was generated using the complete linkage (Pearson) model Note that the lower branch can-not suggest any phylogenetic relationships between the New World species (P mexicana P texana) and the ever-green species P aethiopica and P lentiscus because they do not share any aphid genus

241

Inbar bull Aphids and Pistacia classificationTAXON 57 (1) bull February 2008 238ndash242

Closely related Pistacia species mdash In agree-ment with the previous morphological and molecular analyses the aphid-plant association clearly revealed the close similarities between P texana and P mexicana P atlantica and P mutica and P palaestina and P tere-binthus (Parfitt amp Badenes 1997 Kafkas amp Perl-Treves 2002 Golan-Goldhirsh amp al 2004) The European P terebinthus has similar aphid species fauna (excluding Geoica) as that of the P palaestina This indicates that regarding the aphid species P terebinthus and P pa-laestina are highly similar host plants as determined by plant systematics

Identification of hybrids mdash Hille Ris Lambers (1979) suggested that aphids could be utilized in decision-making in systematic botany even on the hybrid level Especially gall-forming insects were found to be sensitive enough to discriminate between plant hybrids (Floate amp Whitham 1995 Skuhravyacute amp al 1997) Natural inter-specific hybrids of Pistacia species are quite common (Kafkas amp Perl-Treves 2001) Trees that according to leaf morphology are presumably hybrids of P atlantica times P palaestina are scattered in Mediterranean-type habitats in Israel These trees bear galls of Smynthurodes betae that are only associated with P atlantica and galls of Baizongia pistaciae and Forda formicaria that are as-sociated with P palaestina (Inbar amp al 2004 Koach amp Wool 1977 pers obs) Interestingly P saporta a hybrid between P lentiscus and P terebinthus (and P palaes-tina) which belong to different sections (Werner amp al 2001) created a new genotype that is resistant to gall-forming aphids

The Fordinae may further assist in Pistacia systemat-ics at the hybrids morphs and possibly population levels A special effort should be devoted to analyses based on the species of the aphids on order to construct a deeper phylogenic picture For example full understanding of the aphid genus Geoica (Brown amp Blackman 1994) may provide useful information on relationships within and between the ldquoVerardquo and ldquoKhinjukrdquo groups Recently we have described a new aphid species G swirskii which is restricted to certain P atlantica populations (Remaudiegravere amp al 2004)

The sensitivity and specificity of the Fordinae may serve as field tool for rapid screening of Pistacia geno-types that will promote germplasm collection and natural conservation which are important for the pistachio nut production

ACKNOWLEDGMENTSI thank S Lev-Yadun and anonymous referees for their

helpful comments

LITERATURE CITEDAbrahamson WG Melika G Scrafford R amp Csoacuteka

G 1998 Gall-inducing insects provide insights into plant systematic relationships Amer J Bot 85 1159ndash1165

Aguilar JM amp Boecklen WJ 1992 Patterns of herbivory in the Quercus grisea times Quercus gambelii species complex Oikos 64 498ndash504

Ahmad R Ferguson L amp Southwick SM 2005 Molec-ular marker analyses of pistachio rootstocks by Simple Sequence Repeats and Sequence-Related Amplified Poly-morphisms J Hort Sci Biotechnol 80 382ndash386

Becerra JX 1997 Insects on plants macroevolutionary chem-ical trends in host use Science 276 253ndash256

Blackman RL amp Eastop VF 1994 Aphids on the Worldrsquos Trees Cambridge University Press Cambridge

Bodenheimer FS amp Swirski E 1957 The Aphidoidea of the Middle East The Weizmann Science Press of Israel Jerusalem

Browicz K 1988 Chorology of Trees and Shrubs in South-west Asia and Adjacent Regions vol 6 Polish Scientific Publishers Warsaw

Brown PA amp Blackman RL 1994 Morphometric variation in the Geoica utricularia (Homoptera Aphididae) species group on Pistacia (Anacardiaceae) with descriptions of new species and a key to emigrant alatae Syst Entomol 19 119ndash132

Burckhardt D amp Basset Y 2000 The jumping plant-lice (Hemiptera Psylloidea) associated with Schinus (Ana-cardiaceae) systematics biogeography and host plant re-lationships J Nat Hist 34 57ndash155

Chakrabarti S 1998 Biology of gall forming aphids in west-ern and northern Himalaya India Pp 147ndash152 in Nieto Nafriacutea JM amp Dixon AFG (eds) Aphids in Natural and Managed Ecosystems Universidad de Leoacuten Secretariado de Publicaciones Leoacuten

Davatchi GA 1958 Eacutetude biologique de la faune entomolo-gique des Pistacia sauvages et cultiveacutes Rev Pathol Veacuteg Entomol Agric Fr 37 3ndash166

Floate KD Fernandes GW amp Nilsson JA 1996 Dis-tinguishing intra populational categories by their insect faunas gall on rabbitbrush Oecologia 105 221ndash229

Floate KD amp Whitham TG 1995 Insects as traits in plant systematics their use in discriminating hybrid cotton woods Canad J Bot 73 1ndash13

Golan-Goldhirsh A Barazani O Wang ZS Khadka DK Saunders JA Kostiukovsky V amp Rowland LJ 2004 Genetic relationships among Mediterranean Pistacia species evaluated by RAPD and AFLP markers Pl Syst Evol 246 9ndash18

Golan-Goldhirsh A amp Kostiukovsky V 1998 The Mediter-ranean Pistacia genus germplasm collection at Sede Boker Israel Acta Hort 470 131ndash137

Grundwag M amp Werker E 1976 Comparative wood anat-omy as an aid to identification of Pistacia L species Israel J Bot 25 152ndash167

Hille Ris Lambers D 1979 Aphids as botanists Symb Bot Upsal 22 114ndash119

Hormaza JI Dollo L amp Polito VS 1994 Determination of relatedness and geographical movements of Pistacia vera (Pistachio Anacardiaceae) germplasm by RAPD analysis Econ Bot 48 349ndash358

239

Inbar bull Aphids and Pistacia classificationTAXON 57 (1) bull February 2008 238ndash242

Pistacia (Blackman amp Eastop 1994) Most species are found in Central Asia and in Mediterranean-type habi-tats in Asia Europe and North Africa (Bodenheimer amp Swirski 1957 Koach amp Wool 1977) The galls are highly divergent in shape and size (Koach amp Wool 1977 Inbar amp al 2004) Usually each aphid species makes a specific gall on specific Pistacia species in which they feed on the phloem sap (Inbar amp Wool 1995 Inbar amp al 1995) The complex life cycle of the aphids includes sexual and asexual reproduction and regular alternation between the primary Pistacia host and roots of non-specific second-ary hosts The basic life cycle (which may have a few modifications) is as follows In early spring the galls are formed by the first instar nymphs (fundatrices) hatching from overwintering eggs Within each gall two to three additional aphid generations are produced parthenogeneti-cally In fall winged aphids (fall migrants) disperse from the galls and the subsequent generations develop on the secondary hosts The next spring another winged morph (sexuparae) migrates back to the Pistacia and gives birth to the sexual stage (males and females) After mating the fertilized eggs remain on the tree until the fundatrices hatch the following year (Bodenheimer amp Swirski 1957 Wool 1984)

The aim of this paper was to use the gall-forming aphids as zoologically-based method for identifying spe-cies inbreeds and relatedness among Pistacia species

MATERIALS AND METHODSAphidsrsquo taxonomy might also be problematic due

to the wide distribution of aphids and plants and the morphological plasticity within species at different gen-erations and stages which cause misidentifications and consequently misinterpretations In order to eliminate some of the confusion this analysis was restricted to the more consensus genus level The taxonomic literature was thoroughly reviewed (see references in Table 1) Once the list of aphid genera was completed (literature review personal information) a cluster analysis was conducted based on presenceabsence of the aphid genera on each Pistacia using the complete linkage model with Pearsonrsquos r distances of the Statistica software package (StatSoft Inc Tulsa OK USA)

RESULTS AND DISCUSSIONThirteen aphid genera were recognized in the current

analysis (Table 1) This list is slightly different from the one complied by Blackman amp Eastop (1994) For example they listed Smynthurodes betae from P terebinthus and the aphid genus Forda on P lentiscus According to the current survey and personal observations these are most probably mistakes Blackman amp Eastop (1994) also noted

Table 1 List of gall-forming aphids (genera) and Pistacia hosts recognized in this study See text for discrepancies with Blackman amp Eastop (1994)

Aphid genus Pistacia species ReferencesAloephagous aethiopica Blackman amp Eastop 1994Aploneura lentiscus Koach amp Wool 1977Asiphonella chinensis khinjuk palaestina Remaudiegravere amp Tao 1957 Davatchi 1958 Koach amp

Wool 1977Baizongia chinensis integerrima khinjuk palaestina

terebinthusDavatchi 1958 Zhang 1995 Chakrabarti 1998 Peacuterez Hidalgo amp Nieto Nafriacutea 2003

Chaetogeoica chinensis Remaudiegravere amp Tao 1957Forda atlantica chinensis integerrima khinjuk mutica

palaestina terebinthus vera Davatchi 1958 Blackman amp Eastop 1994 Chakra-barti 1998 Peacuterez Hidalgo amp Nieto Nafriacutea 2003

Fordini a atlantica Koach amp Wool 1977 Wool amp Manheim (pers comm)Geoica atlantica integerrima khinjuk mutica palaestina

terebinthusDavatchi 1958 Brown amp Blackman 1994 Chakrabarti 1998

Geopemohigus mexicana texana Muntildeoz-Viveros amp Remaudiegravere 1999Paracletus khinjuk palaestina terebinthus Davatchi 1958 Blackman amp Eastop 1994Rectinasus khinjuk palaestina Davatchi 1958 Koach amp Wool 1977Slavum atlantica mutica vera Davatchi 1958 Koach amp Wool 1977Smynthurodes atlantica mutica Davatchi 1958 Koach amp Wool 1977Note No galls are known from P saportaaAccording to D Wool O Manheim (submitted MS) and G Remaudiegravere (pers comm) the Fordini spp listed in Koach amp Wool (1977) belong to a new genus

240

TAXON 57 (1) bull February 2008 238ndash242Inbar bull Aphids and Pistacia classification

that P vera bears three aphid genera (Baizongia Geoica Paracletus) that were not mentioned in the thorough study of the Iranian fauna on Pistacia (Davatchi 1958) Because P vera is cultivated and different studies might be in-fluenced by its variety two sets of cluster analyses were conducted with and without the three above-mentioned genera on this tree Nevertheless adding these aphid gen-era to the analysis resulted in similar clustering (Fig 1)

Division into sections mdash The aphid-based associa-tion found P lentiscus P aethiopica and the two indistin-guishable New World species (P mexicana P texana) in a clear distinct position from all other species They each host exclusive aphid fauna and therefore the aphids can-not provide useful information about their phylogenetic relationships with other Pistacia species It is important to note that the New World Pistacia regardless of their similarity to other species has a very little chance to be infested by the Old World aphids

Other Pistacia species were clustered into two clades (Fig 1) The first hereinafter the ldquoVerardquo group includes P vera P atlantica and P mutica This places P atlan-tica closely related to P vera The second hereinafter the ldquoKhinjukrdquo group includes P chinensis P integerrima P khinjuk P palaestina and P terebinthus Slavum is an aphid genus associated with the ldquoVerardquo group while Baizongia is typically found on the ldquoKhinjukrdquo group (Table 1) The aphid genera Forda and Geoica are wide spread within the two Pistacia groups indicating frequent host shiftes (Inbar amp al 2004) The fact that Forda and Geoica do not form galls on P lentiscus despite its partial distribution overlap with other Old World Pistacia spe-cies (around the Mediterranean) places this evergreen shrub in an evidently distinct position (section) as was suggested before by Golan-Goldhirsh amp al (2004) and Zohary (1952) Furthermore according to the aphids plac-ing P lentiscus in a section together with parts of the ldquoVerardquo or ldquoKhinjukrdquo members (Kafkas amp Perl-Treves 2002 Parfitt amp Badenes 1997) might not be justified

During the process of host plant selection and suc-cessful gall formation the aphids should assess plant chemical anatomical physiological and structural aspects (Hille Ris Lambers 1979 Weis amp al 1988) Mismatches usually end up with low fitness or death Thus host shifts among specific phytophagous insects take place accord-ing to chemical similarities between the original and the new plants (Becerra 1997 Mitter amp al 1991) closely re-lated insect taxa will usually feed on closely related plant species The aphid genera Geoica and Forda found on Pistacia species from both ldquoVerardquo and ldquoKhinjukrdquo indicate that these groups are close enough to facilitate repeated successful host shifts of aphids between them

Perhaps one of the most surprising results is the simi-larity between aphid genera (not species) which was found on P palaestina and P khinjuk It should be stressed that

previous morphological and molecular analyses found P vera and P khinjuk closely related (Zohary 1952 Parfitt amp Badenes 1997 Kafkas amp Perl-Treves 2002 Golan-Goldhirsh amp al 2004) Due to its wide distribu-tion its tendency to form hybrids and its local misnaming (Browicz 1988 Kafkas amp Perl-Treves 2002) some ento-mologists might have mistakenly recognized P khinjuk as the host of the aphids However even if some mistakes have occurred this cannot change the close relationships between P khinjuk and P palaestina (and P terebinthus) which share several aphid genera (Table 1) A reasonable speculation would be that P khinjuk diverted directly from P vera (Zohary 1952 Parfitt amp Badenes 1997 Kafkas amp Perl-Treves 2002 Golan-Goldhirsh amp al 2004) but soon established association with new aphid genera such as Baizongia and Paracletus

Fig 1 Cluster analysis of Pistacia species based upon presenceabsence of gall-forming aphidrsquos (Fordinae) gen-era The dendrogram was generated using the complete linkage (Pearson) model Note that the lower branch can-not suggest any phylogenetic relationships between the New World species (P mexicana P texana) and the ever-green species P aethiopica and P lentiscus because they do not share any aphid genus

241

Inbar bull Aphids and Pistacia classificationTAXON 57 (1) bull February 2008 238ndash242

Closely related Pistacia species mdash In agree-ment with the previous morphological and molecular analyses the aphid-plant association clearly revealed the close similarities between P texana and P mexicana P atlantica and P mutica and P palaestina and P tere-binthus (Parfitt amp Badenes 1997 Kafkas amp Perl-Treves 2002 Golan-Goldhirsh amp al 2004) The European P terebinthus has similar aphid species fauna (excluding Geoica) as that of the P palaestina This indicates that regarding the aphid species P terebinthus and P pa-laestina are highly similar host plants as determined by plant systematics

Identification of hybrids mdash Hille Ris Lambers (1979) suggested that aphids could be utilized in decision-making in systematic botany even on the hybrid level Especially gall-forming insects were found to be sensitive enough to discriminate between plant hybrids (Floate amp Whitham 1995 Skuhravyacute amp al 1997) Natural inter-specific hybrids of Pistacia species are quite common (Kafkas amp Perl-Treves 2001) Trees that according to leaf morphology are presumably hybrids of P atlantica times P palaestina are scattered in Mediterranean-type habitats in Israel These trees bear galls of Smynthurodes betae that are only associated with P atlantica and galls of Baizongia pistaciae and Forda formicaria that are as-sociated with P palaestina (Inbar amp al 2004 Koach amp Wool 1977 pers obs) Interestingly P saporta a hybrid between P lentiscus and P terebinthus (and P palaes-tina) which belong to different sections (Werner amp al 2001) created a new genotype that is resistant to gall-forming aphids

The Fordinae may further assist in Pistacia systemat-ics at the hybrids morphs and possibly population levels A special effort should be devoted to analyses based on the species of the aphids on order to construct a deeper phylogenic picture For example full understanding of the aphid genus Geoica (Brown amp Blackman 1994) may provide useful information on relationships within and between the ldquoVerardquo and ldquoKhinjukrdquo groups Recently we have described a new aphid species G swirskii which is restricted to certain P atlantica populations (Remaudiegravere amp al 2004)

The sensitivity and specificity of the Fordinae may serve as field tool for rapid screening of Pistacia geno-types that will promote germplasm collection and natural conservation which are important for the pistachio nut production

ACKNOWLEDGMENTSI thank S Lev-Yadun and anonymous referees for their

helpful comments

LITERATURE CITEDAbrahamson WG Melika G Scrafford R amp Csoacuteka

G 1998 Gall-inducing insects provide insights into plant systematic relationships Amer J Bot 85 1159ndash1165

Aguilar JM amp Boecklen WJ 1992 Patterns of herbivory in the Quercus grisea times Quercus gambelii species complex Oikos 64 498ndash504

Ahmad R Ferguson L amp Southwick SM 2005 Molec-ular marker analyses of pistachio rootstocks by Simple Sequence Repeats and Sequence-Related Amplified Poly-morphisms J Hort Sci Biotechnol 80 382ndash386

Becerra JX 1997 Insects on plants macroevolutionary chem-ical trends in host use Science 276 253ndash256

Blackman RL amp Eastop VF 1994 Aphids on the Worldrsquos Trees Cambridge University Press Cambridge

Bodenheimer FS amp Swirski E 1957 The Aphidoidea of the Middle East The Weizmann Science Press of Israel Jerusalem

Browicz K 1988 Chorology of Trees and Shrubs in South-west Asia and Adjacent Regions vol 6 Polish Scientific Publishers Warsaw

Brown PA amp Blackman RL 1994 Morphometric variation in the Geoica utricularia (Homoptera Aphididae) species group on Pistacia (Anacardiaceae) with descriptions of new species and a key to emigrant alatae Syst Entomol 19 119ndash132

Burckhardt D amp Basset Y 2000 The jumping plant-lice (Hemiptera Psylloidea) associated with Schinus (Ana-cardiaceae) systematics biogeography and host plant re-lationships J Nat Hist 34 57ndash155

Chakrabarti S 1998 Biology of gall forming aphids in west-ern and northern Himalaya India Pp 147ndash152 in Nieto Nafriacutea JM amp Dixon AFG (eds) Aphids in Natural and Managed Ecosystems Universidad de Leoacuten Secretariado de Publicaciones Leoacuten

Davatchi GA 1958 Eacutetude biologique de la faune entomolo-gique des Pistacia sauvages et cultiveacutes Rev Pathol Veacuteg Entomol Agric Fr 37 3ndash166

Floate KD Fernandes GW amp Nilsson JA 1996 Dis-tinguishing intra populational categories by their insect faunas gall on rabbitbrush Oecologia 105 221ndash229

Floate KD amp Whitham TG 1995 Insects as traits in plant systematics their use in discriminating hybrid cotton woods Canad J Bot 73 1ndash13

Golan-Goldhirsh A Barazani O Wang ZS Khadka DK Saunders JA Kostiukovsky V amp Rowland LJ 2004 Genetic relationships among Mediterranean Pistacia species evaluated by RAPD and AFLP markers Pl Syst Evol 246 9ndash18

Golan-Goldhirsh A amp Kostiukovsky V 1998 The Mediter-ranean Pistacia genus germplasm collection at Sede Boker Israel Acta Hort 470 131ndash137

Grundwag M amp Werker E 1976 Comparative wood anat-omy as an aid to identification of Pistacia L species Israel J Bot 25 152ndash167

Hille Ris Lambers D 1979 Aphids as botanists Symb Bot Upsal 22 114ndash119

Hormaza JI Dollo L amp Polito VS 1994 Determination of relatedness and geographical movements of Pistacia vera (Pistachio Anacardiaceae) germplasm by RAPD analysis Econ Bot 48 349ndash358

240

TAXON 57 (1) bull February 2008 238ndash242Inbar bull Aphids and Pistacia classification

that P vera bears three aphid genera (Baizongia Geoica Paracletus) that were not mentioned in the thorough study of the Iranian fauna on Pistacia (Davatchi 1958) Because P vera is cultivated and different studies might be in-fluenced by its variety two sets of cluster analyses were conducted with and without the three above-mentioned genera on this tree Nevertheless adding these aphid gen-era to the analysis resulted in similar clustering (Fig 1)

Division into sections mdash The aphid-based associa-tion found P lentiscus P aethiopica and the two indistin-guishable New World species (P mexicana P texana) in a clear distinct position from all other species They each host exclusive aphid fauna and therefore the aphids can-not provide useful information about their phylogenetic relationships with other Pistacia species It is important to note that the New World Pistacia regardless of their similarity to other species has a very little chance to be infested by the Old World aphids

Other Pistacia species were clustered into two clades (Fig 1) The first hereinafter the ldquoVerardquo group includes P vera P atlantica and P mutica This places P atlan-tica closely related to P vera The second hereinafter the ldquoKhinjukrdquo group includes P chinensis P integerrima P khinjuk P palaestina and P terebinthus Slavum is an aphid genus associated with the ldquoVerardquo group while Baizongia is typically found on the ldquoKhinjukrdquo group (Table 1) The aphid genera Forda and Geoica are wide spread within the two Pistacia groups indicating frequent host shiftes (Inbar amp al 2004) The fact that Forda and Geoica do not form galls on P lentiscus despite its partial distribution overlap with other Old World Pistacia spe-cies (around the Mediterranean) places this evergreen shrub in an evidently distinct position (section) as was suggested before by Golan-Goldhirsh amp al (2004) and Zohary (1952) Furthermore according to the aphids plac-ing P lentiscus in a section together with parts of the ldquoVerardquo or ldquoKhinjukrdquo members (Kafkas amp Perl-Treves 2002 Parfitt amp Badenes 1997) might not be justified

During the process of host plant selection and suc-cessful gall formation the aphids should assess plant chemical anatomical physiological and structural aspects (Hille Ris Lambers 1979 Weis amp al 1988) Mismatches usually end up with low fitness or death Thus host shifts among specific phytophagous insects take place accord-ing to chemical similarities between the original and the new plants (Becerra 1997 Mitter amp al 1991) closely re-lated insect taxa will usually feed on closely related plant species The aphid genera Geoica and Forda found on Pistacia species from both ldquoVerardquo and ldquoKhinjukrdquo indicate that these groups are close enough to facilitate repeated successful host shifts of aphids between them

Perhaps one of the most surprising results is the simi-larity between aphid genera (not species) which was found on P palaestina and P khinjuk It should be stressed that

previous morphological and molecular analyses found P vera and P khinjuk closely related (Zohary 1952 Parfitt amp Badenes 1997 Kafkas amp Perl-Treves 2002 Golan-Goldhirsh amp al 2004) Due to its wide distribu-tion its tendency to form hybrids and its local misnaming (Browicz 1988 Kafkas amp Perl-Treves 2002) some ento-mologists might have mistakenly recognized P khinjuk as the host of the aphids However even if some mistakes have occurred this cannot change the close relationships between P khinjuk and P palaestina (and P terebinthus) which share several aphid genera (Table 1) A reasonable speculation would be that P khinjuk diverted directly from P vera (Zohary 1952 Parfitt amp Badenes 1997 Kafkas amp Perl-Treves 2002 Golan-Goldhirsh amp al 2004) but soon established association with new aphid genera such as Baizongia and Paracletus

Fig 1 Cluster analysis of Pistacia species based upon presenceabsence of gall-forming aphidrsquos (Fordinae) gen-era The dendrogram was generated using the complete linkage (Pearson) model Note that the lower branch can-not suggest any phylogenetic relationships between the New World species (P mexicana P texana) and the ever-green species P aethiopica and P lentiscus because they do not share any aphid genus

241

Inbar bull Aphids and Pistacia classificationTAXON 57 (1) bull February 2008 238ndash242

Closely related Pistacia species mdash In agree-ment with the previous morphological and molecular analyses the aphid-plant association clearly revealed the close similarities between P texana and P mexicana P atlantica and P mutica and P palaestina and P tere-binthus (Parfitt amp Badenes 1997 Kafkas amp Perl-Treves 2002 Golan-Goldhirsh amp al 2004) The European P terebinthus has similar aphid species fauna (excluding Geoica) as that of the P palaestina This indicates that regarding the aphid species P terebinthus and P pa-laestina are highly similar host plants as determined by plant systematics

Identification of hybrids mdash Hille Ris Lambers (1979) suggested that aphids could be utilized in decision-making in systematic botany even on the hybrid level Especially gall-forming insects were found to be sensitive enough to discriminate between plant hybrids (Floate amp Whitham 1995 Skuhravyacute amp al 1997) Natural inter-specific hybrids of Pistacia species are quite common (Kafkas amp Perl-Treves 2001) Trees that according to leaf morphology are presumably hybrids of P atlantica times P palaestina are scattered in Mediterranean-type habitats in Israel These trees bear galls of Smynthurodes betae that are only associated with P atlantica and galls of Baizongia pistaciae and Forda formicaria that are as-sociated with P palaestina (Inbar amp al 2004 Koach amp Wool 1977 pers obs) Interestingly P saporta a hybrid between P lentiscus and P terebinthus (and P palaes-tina) which belong to different sections (Werner amp al 2001) created a new genotype that is resistant to gall-forming aphids

The Fordinae may further assist in Pistacia systemat-ics at the hybrids morphs and possibly population levels A special effort should be devoted to analyses based on the species of the aphids on order to construct a deeper phylogenic picture For example full understanding of the aphid genus Geoica (Brown amp Blackman 1994) may provide useful information on relationships within and between the ldquoVerardquo and ldquoKhinjukrdquo groups Recently we have described a new aphid species G swirskii which is restricted to certain P atlantica populations (Remaudiegravere amp al 2004)

The sensitivity and specificity of the Fordinae may serve as field tool for rapid screening of Pistacia geno-types that will promote germplasm collection and natural conservation which are important for the pistachio nut production

ACKNOWLEDGMENTSI thank S Lev-Yadun and anonymous referees for their

helpful comments

LITERATURE CITEDAbrahamson WG Melika G Scrafford R amp Csoacuteka

G 1998 Gall-inducing insects provide insights into plant systematic relationships Amer J Bot 85 1159ndash1165

Aguilar JM amp Boecklen WJ 1992 Patterns of herbivory in the Quercus grisea times Quercus gambelii species complex Oikos 64 498ndash504

Ahmad R Ferguson L amp Southwick SM 2005 Molec-ular marker analyses of pistachio rootstocks by Simple Sequence Repeats and Sequence-Related Amplified Poly-morphisms J Hort Sci Biotechnol 80 382ndash386

Becerra JX 1997 Insects on plants macroevolutionary chem-ical trends in host use Science 276 253ndash256

Blackman RL amp Eastop VF 1994 Aphids on the Worldrsquos Trees Cambridge University Press Cambridge

Bodenheimer FS amp Swirski E 1957 The Aphidoidea of the Middle East The Weizmann Science Press of Israel Jerusalem

Browicz K 1988 Chorology of Trees and Shrubs in South-west Asia and Adjacent Regions vol 6 Polish Scientific Publishers Warsaw

Brown PA amp Blackman RL 1994 Morphometric variation in the Geoica utricularia (Homoptera Aphididae) species group on Pistacia (Anacardiaceae) with descriptions of new species and a key to emigrant alatae Syst Entomol 19 119ndash132

Burckhardt D amp Basset Y 2000 The jumping plant-lice (Hemiptera Psylloidea) associated with Schinus (Ana-cardiaceae) systematics biogeography and host plant re-lationships J Nat Hist 34 57ndash155

Chakrabarti S 1998 Biology of gall forming aphids in west-ern and northern Himalaya India Pp 147ndash152 in Nieto Nafriacutea JM amp Dixon AFG (eds) Aphids in Natural and Managed Ecosystems Universidad de Leoacuten Secretariado de Publicaciones Leoacuten

Davatchi GA 1958 Eacutetude biologique de la faune entomolo-gique des Pistacia sauvages et cultiveacutes Rev Pathol Veacuteg Entomol Agric Fr 37 3ndash166

Floate KD Fernandes GW amp Nilsson JA 1996 Dis-tinguishing intra populational categories by their insect faunas gall on rabbitbrush Oecologia 105 221ndash229

Floate KD amp Whitham TG 1995 Insects as traits in plant systematics their use in discriminating hybrid cotton woods Canad J Bot 73 1ndash13

Golan-Goldhirsh A Barazani O Wang ZS Khadka DK Saunders JA Kostiukovsky V amp Rowland LJ 2004 Genetic relationships among Mediterranean Pistacia species evaluated by RAPD and AFLP markers Pl Syst Evol 246 9ndash18

Golan-Goldhirsh A amp Kostiukovsky V 1998 The Mediter-ranean Pistacia genus germplasm collection at Sede Boker Israel Acta Hort 470 131ndash137

Grundwag M amp Werker E 1976 Comparative wood anat-omy as an aid to identification of Pistacia L species Israel J Bot 25 152ndash167

Hille Ris Lambers D 1979 Aphids as botanists Symb Bot Upsal 22 114ndash119

Hormaza JI Dollo L amp Polito VS 1994 Determination of relatedness and geographical movements of Pistacia vera (Pistachio Anacardiaceae) germplasm by RAPD analysis Econ Bot 48 349ndash358

241

Inbar bull Aphids and Pistacia classificationTAXON 57 (1) bull February 2008 238ndash242

Closely related Pistacia species mdash In agree-ment with the previous morphological and molecular analyses the aphid-plant association clearly revealed the close similarities between P texana and P mexicana P atlantica and P mutica and P palaestina and P tere-binthus (Parfitt amp Badenes 1997 Kafkas amp Perl-Treves 2002 Golan-Goldhirsh amp al 2004) The European P terebinthus has similar aphid species fauna (excluding Geoica) as that of the P palaestina This indicates that regarding the aphid species P terebinthus and P pa-laestina are highly similar host plants as determined by plant systematics

Identification of hybrids mdash Hille Ris Lambers (1979) suggested that aphids could be utilized in decision-making in systematic botany even on the hybrid level Especially gall-forming insects were found to be sensitive enough to discriminate between plant hybrids (Floate amp Whitham 1995 Skuhravyacute amp al 1997) Natural inter-specific hybrids of Pistacia species are quite common (Kafkas amp Perl-Treves 2001) Trees that according to leaf morphology are presumably hybrids of P atlantica times P palaestina are scattered in Mediterranean-type habitats in Israel These trees bear galls of Smynthurodes betae that are only associated with P atlantica and galls of Baizongia pistaciae and Forda formicaria that are as-sociated with P palaestina (Inbar amp al 2004 Koach amp Wool 1977 pers obs) Interestingly P saporta a hybrid between P lentiscus and P terebinthus (and P palaes-tina) which belong to different sections (Werner amp al 2001) created a new genotype that is resistant to gall-forming aphids

The Fordinae may further assist in Pistacia systemat-ics at the hybrids morphs and possibly population levels A special effort should be devoted to analyses based on the species of the aphids on order to construct a deeper phylogenic picture For example full understanding of the aphid genus Geoica (Brown amp Blackman 1994) may provide useful information on relationships within and between the ldquoVerardquo and ldquoKhinjukrdquo groups Recently we have described a new aphid species G swirskii which is restricted to certain P atlantica populations (Remaudiegravere amp al 2004)

The sensitivity and specificity of the Fordinae may serve as field tool for rapid screening of Pistacia geno-types that will promote germplasm collection and natural conservation which are important for the pistachio nut production

ACKNOWLEDGMENTSI thank S Lev-Yadun and anonymous referees for their

helpful comments

LITERATURE CITEDAbrahamson WG Melika G Scrafford R amp Csoacuteka

G 1998 Gall-inducing insects provide insights into plant systematic relationships Amer J Bot 85 1159ndash1165

Aguilar JM amp Boecklen WJ 1992 Patterns of herbivory in the Quercus grisea times Quercus gambelii species complex Oikos 64 498ndash504

Ahmad R Ferguson L amp Southwick SM 2005 Molec-ular marker analyses of pistachio rootstocks by Simple Sequence Repeats and Sequence-Related Amplified Poly-morphisms J Hort Sci Biotechnol 80 382ndash386

Becerra JX 1997 Insects on plants macroevolutionary chem-ical trends in host use Science 276 253ndash256

Blackman RL amp Eastop VF 1994 Aphids on the Worldrsquos Trees Cambridge University Press Cambridge

Bodenheimer FS amp Swirski E 1957 The Aphidoidea of the Middle East The Weizmann Science Press of Israel Jerusalem

Browicz K 1988 Chorology of Trees and Shrubs in South-west Asia and Adjacent Regions vol 6 Polish Scientific Publishers Warsaw

Brown PA amp Blackman RL 1994 Morphometric variation in the Geoica utricularia (Homoptera Aphididae) species group on Pistacia (Anacardiaceae) with descriptions of new species and a key to emigrant alatae Syst Entomol 19 119ndash132

Burckhardt D amp Basset Y 2000 The jumping plant-lice (Hemiptera Psylloidea) associated with Schinus (Ana-cardiaceae) systematics biogeography and host plant re-lationships J Nat Hist 34 57ndash155

Chakrabarti S 1998 Biology of gall forming aphids in west-ern and northern Himalaya India Pp 147ndash152 in Nieto Nafriacutea JM amp Dixon AFG (eds) Aphids in Natural and Managed Ecosystems Universidad de Leoacuten Secretariado de Publicaciones Leoacuten

Davatchi GA 1958 Eacutetude biologique de la faune entomolo-gique des Pistacia sauvages et cultiveacutes Rev Pathol Veacuteg Entomol Agric Fr 37 3ndash166

Floate KD Fernandes GW amp Nilsson JA 1996 Dis-tinguishing intra populational categories by their insect faunas gall on rabbitbrush Oecologia 105 221ndash229

Floate KD amp Whitham TG 1995 Insects as traits in plant systematics their use in discriminating hybrid cotton woods Canad J Bot 73 1ndash13

Golan-Goldhirsh A Barazani O Wang ZS Khadka DK Saunders JA Kostiukovsky V amp Rowland LJ 2004 Genetic relationships among Mediterranean Pistacia species evaluated by RAPD and AFLP markers Pl Syst Evol 246 9ndash18

Golan-Goldhirsh A amp Kostiukovsky V 1998 The Mediter-ranean Pistacia genus germplasm collection at Sede Boker Israel Acta Hort 470 131ndash137

Grundwag M amp Werker E 1976 Comparative wood anat-omy as an aid to identification of Pistacia L species Israel J Bot 25 152ndash167

Hille Ris Lambers D 1979 Aphids as botanists Symb Bot Upsal 22 114ndash119

Hormaza JI Dollo L amp Polito VS 1994 Determination of relatedness and geographical movements of Pistacia vera (Pistachio Anacardiaceae) germplasm by RAPD analysis Econ Bot 48 349ndash358

242

TAXON 57 (1) bull February 2008 238ndash242Inbar bull Aphids and Pistacia classification

Inbar M Eshel A amp Wool D 1995 Interspecific competi-tion among phloem-feeding insects mediated by induced host plant sinks Ecology 76 1506ndash1515

Inbar M Wink M amp Wool D 2004 The evolution of host plant manipulation by insects molecular and ecological evidence from gall-forming aphids on Pistacia Molec Phylog Evol 32 504ndash511

Inbar M amp Wool D 1995 Phloem-feeding specialists shar-ing a host tree resource partitioning minimizes interfer-ence competition among galling aphid species Oikos 73 109ndash119

Kafkas S Kafkas E amp Perl-Treves R 2002 Morpho-logical diversity and a germplasm survey of three wild Pistacia species in Turkey Genet Resources Crop Evol 49 261ndash270

Kafkas S amp Perl-Treves R 2002 Interspecific relationships in Pistacia based on RAPD fingerprinting Hortscience 37 168ndash171

Katsiotis A Hagidimitriou M Drossou A Pontikis C amp Loukas M 2003 Genetic relationships among spe-cies and cultivars of Pistacia using RAPDs and AFLPs Euphytica 132 279ndash286

Koach J amp Wool D 1977 Geographic distribution and host specificity of gall forming aphids (Homoptera Fordinae) on Pistacia trees in Israel Marcellia 40 207ndash216

Meeuse ADJ 1973 Co evolution of plant hosts and their parasites as a taxonomic tool Pp 189ndash200 in Heywood VH (ed) Taxonomy and Ecology Academic Press Lon-don

Mitter C Farrel B amp Futuyma DJ 1991 Phylogenetic studies of insect-plant interactions insight into the genesis of diversity Trends Ecol Evol 9 290ndash293

Muntildeoz-Viveros AL amp Remaudiere G 1999 Les eacutespegraveces de Geopemphigus gallicoles sur Pistacia mexicana Rev Fr Entomol 21 35ndash48

Parfitt DA amp Badenes ML 1997 Phylogeny of the genus

Pistacia as determined from analysis of the chloroplast genome Proc Natl Acad Sci USA 94 7987ndash7992

Peacuterez Hidalgo N amp Nieto Nafriacutea JM 2003 Check-list of Eriosomatinae (Hemiptera Sternorrhyncha Aphididae) of the Iberian Peninsula and Balearic islands Acta Entomol Ibeacuterica Macaroneacutesica 1 67ndash73

Remaudiegravere G Inbar M Menier JJ amp Shmida A 2004 Un nouveau Geoica gallicole sur Pistacia atlantica en jor-danie (Hemiptera Aphididae Eriosomatinae Fordini) Rev Fr Entomol 26 37ndash42

Remaudiegravere G amp Tao CC 1957 Les Fordinae (Hom Aphi-doidea) du Pistacia sinensis Rev Pathol Veacuteg Entomol Agric Fr 36 223ndash236

Sheiban A 1995 Distribution use and conservation of pista-chio in Iran Pp 51ndash56 in Padulosi S Caruso T amp Bar-one E (eds) Taxonomy Distribution Conservation and Uses of Pistacia Genetic Resources IPGRI Palermo

Skuhravyacute V Skuhravaacute N amp Brewer JW 1997 Gall midge (Dipt Cecidomyiidae) associated with Populus tremula P tremuloides and their hybrid (Salicaceae) J Appl En-tomol 121 315ndash320

Weis AE Walton R amp Crego CL 1988 Reactive plant tis-sue sites and the population biology of gall makers Annu Rev Entomol 33 467ndash486

Werner O Saacutenchez-Goacutemez P Guerra J amp Martiacutenez JF 2001 Identification of Pistacia times saporta Burnat (Anacar-diacea) by RAPD analysis and morphological characters Sci Hort 91 179ndash186

Wool D 1984 Gall forming aphids Pp 11ndash58 in Anan-thakrishnan TN (ed) Biology of Gall Insects Oxford amp IBH New Delhi

Zhang G 1995 A study on Baizongia Rondani 1848 with descriptions of a new subgenus and two new species (Homoptera Pemphigidae) Entomol Sinica 2 291ndash299

Zohary M 1952 A monographical study of the genus Pistacia Palestine J Bot Jerusalem Ser 5 187ndash228