The Evolution of Toxic Phenolic Compounds in a Group of Anacardiaceae Genera

Author(s): Carlos J. Aguilar-Ortigoza and Victoria Sosa

Source: Taxon, Vol. 53, No. 2 (May, 2004), pp. 357-364
Published by: International Association for Plant Taxonomy (IAPT)
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TAXON 53 (2) * May 2004: 357-364 Aguilar-Ortigoza& Sosa * Compounds in Anacardiaceae

The evolution of toxic phenolic compounds in a group of Anacardiaceae gen-

era
Carlos J. Aguilar-Ortigozal,2 & Victoria Sosal

SInstituto de Ecologia, A.C., Apartado Postal 63, 91000 Xalapa, Veracruz, MWxico.victoria@ecologia.edu.mx
(author for correspondence)
2Facultad de Ciencias, Universidad Autdnoma del Estado de MWxico, Toluca, Mixico. aguilarc@
ecologia.edu.mx

Anacardiaceae are largely tropical trees, shrubs and lianas of the order Sapindales, characterized by production
of three types of toxic phenols: biflavonoids, alkylcatechols and alkylresorcinols. Anatomical, morphological
and rbcL sequence data were used to reconstruct the phylogeny of a group of Anacardiaceae and address ques-
tions about the origin and evolution of these toxic phenolic compounds. Their evolutionary patterns are dis-
cussed in relation to the group of Hemipteran insects that feed on Anacardiaceae. Our study included 22 taxa
of Anacardiaceaeand the results supportpreviousphylogenetic studies in thattwo clades are detected:a basal
clade, with Spondias and related genera that do not produce toxic phenolic compounds, and a second clade
with the remaining genera, i.e., those that produce biflavonoids, as do species of Burseraceae. The evolution-
ary patterns of alkylcatechols and alkylresorcinols are not straightforward; these substances are produced in
unrelatedgroupsof genera.We suggest, however,thatHemipteraninsects do not feed on taxa of Anacardiaceae
that produce alkylcatechols.

KEYWORDS: alkylcatechol, alkylresorcinol, Anacardiaceae, associated herbivores, biflavonoid, phylogenet-

ics, evolution.

In Anacardiaceaetoxic phenolsare likely a defense

E INTRODUCTION againstpests,becausetheyare capableof restrictingthe
Anacardiaceae are an angiospermfamilyknownto growthof pathogenicfungisuchasAlternaria(Cojocaru
produceallergenicsubstancesin the resincanalsof pri- & al., 1986;Harbome,1999).It has alsobeensuggested
maryandsecondaryphloemassociatedwiththeveins of thattoxic phenolsare a defenseagainstinsectsandver-
leaves and other parenchymatous tissues (Metcalf & tebrates(Joel, 1980; Mitchell, 1990; Farrel& al., 1991).
Chalk,1950).Toxicchemicalsarephenolsof threetypes: Occurrenceof toxicphenolsin Anacardiaceae andrelat-
alkylcatechols, alkylresorcinols and biflavonoids. ed groupshave createdinterestingplant-insectinterac-
Urushiol,the mostallergenicandcommonof these,is a tions. For example,Bursera,a groupclosely relatedto
mixtureof saturatedand unsaturatedpentadecyl-and Anacardiaceae,producesterpenes against Coleoptera
foundin a numberof taxa,suchas
heptadecylcatechols, such as Blepharida (Furth & Young, 1988; Becerra,
poison ivy (Toxicodendron radicans; Eggers, 1974; 1997).It has also beenreportedthatBlepharidafeed on
Gross & al., 1975; Baer & al., 1980; Adawadkar& severalspecies of Rhus (Anacardiaceae) in which the
EISohly,1983;Du & al., 1984;Gambaro& al., 1986; toxic phenolsthat have been detectedwere flavonoids
Rivero-Cruz& al., 1997). Cardol,anotherallergenic (Furth & Young, 1988; Becerra, 1997). Calophya, a
phenolic compound that is characteristicof some monophagousgenus of Hemiptera,feeds on speciesof
Anacardiaceae, found in the
is a pentadecylresorcinol Burseraceae,Anacardiaceaeand Rutaceae(Hodkinson,
fruit of the cashew nut (Anacardiumoccidentale; Tyman 1989). Coevolutionaryhypothesesof the relationship
& Morris,1967;Evans& Schmidt,1980).Heptadecyl- betweenCalophyaand some species of Anacardiaceae
resorcinolis foundin themangofruit(Mangiferaindica) have recently been proposed(Burckhardt& Basset,
(Cojocaru& al., 1986). Biflavonoidsare commonin 2000).
most groups of Anacardiaceaebut absent from the Fifty-twospeciesof 27 of the approximately
80 gen-
Spondiasgroupof genera(Young,1976;Wannan& al., era of Anacardiaceaecontaintoxic phenols (Mitchell,
1985; Young& Aist, 1987; Wannan& Quinn, 1988; Yuh- 1990; Aguilar-Ortigoza & al., 2003). The majorityof
Meei & al., 1989). Biflavonoids are also common in the thesetoxic speciesaremembersof tribeRhoeae.
gymnosperms (Smith, 1976) and in Burseraceae Engler (1883) divided Anacardiaceaeinto five
(Wannan& al., 1985). tribes:Anacardieae,Spondiadeae,Rhoeae,Semecarpeae
357

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Aguilar-Ortigoza& Sosa * Compounds in Anacardiaceae
and Dobineae,basedon morphologicalcharacterssuch
as carpelandlocule numberat anthesisandfruit,stylar
morphology,insertionof ovule, and leaf morphology.
However,studiesbased on anatomical,morphological,
andmolecularevidenceindicatethatthereareonly two
lineageswithinthe family,one formedby the generaof
Spondiadeae witha few generaof Rhoeae,anda second
with the remaininggenera(Wannan& Quinn, 1991;
Terrazas, 1994; Terrazas& Chase, 1996; Pell &
Urbatsch,2001).
We used anatomical, morphological and rbcL
sequencedatato reconstructthephylogenyof a groupof
generabelongingto Spondiadeaeandotherspreviously
consideredin Anacardieaeand Rhoeae,and to address
questionsabout the origin and evolutionof phenolic
toxiccompoundssuchas alkylcatechols,alkylresorcinols
and biflavonoids.We discussthese compoundsin rela-
tion to the group of Hemipteraninsects that feed on
Anacardiaceae.
E pairsof primersdescribedin Savolainen& al. (2000a).
AND METHODS
MATERIALS
Plant material. - Our study includes only repre-
sentatives of 22 out of the 80 genera of the family.
However, our sampling strategy for the phylogenetic
analysis was to include differentspecies of currentlyrec-
ognized groups in Anacardiaceaeas well as species hav-
ing any of the three toxic phenolic compounds consid-
ered in this study.Currentmolecularphylogeneticevi-
dence indicates that Anacardiaceaeare sister to
Burseraceae and that Sapindaceae, Rutaceae and
Meliaceaeare closely related(Savolainen& al., 2000a,
b; Soltis & al., 2000). Therefore,as an outgroup,four
species belonging to Burseraceae, Sapindaceae,
Rutaceaeand Meliaceae, were considered.Vouchersand
DNA GenBank accession numbers are given in
Appendix 1 (see online version of Taxon).
Morphological characters. - The 88 morpho-
logical charactersused in the presentanalysis were com-
piled from our own observations of herbariummaterial
and supplementedwith data in the literature.The charac-
ters are essentially those used by Aguilar & al. (2004)
OH OH
(CH2)7CH=CH(CH2)7CH3
(CHz2)14CH3
(1) A 3-Pentadecylcatechol (2) A 3-Heptadecylcatechol
Fig. 1. Toxic chemicals in Anacardiaceae.
358
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TAXON 53 (2) * May 2004: 357-364
and represent aspects of morphology and anatomy of
leaf, inflorescence,flower,fruit,seed and wood (Table
1;.the morphological andanatomicaldatamatrixis pro-
vided in Appendix 2 and the examinedherbariumspeci-
mens in Appendix 3 (both available online).
Chemical characters. - Occurrenceof alkylcat-
echols, alkylresorcinols and biflavonoids in different
parts of the plants was taken for most species from the
compilation of Aguilar-Ortigoza& al. (2003) (Fig. 1;
Appendix 1). For some other species the same methods
described in Aguilar-Ortigoza& al. (2003) were carried
out to determine occurrence of these chemicals
(Appendix 1). In cases where the informationwas taken
from other sources, references are cited.
Molecular methods. - DNA from fresh leaves
and herbariumspecimenswas extractedusing the 2X
CTABmethodof Doyle& Doyle(1987).TotalDNAand
PCR products were cleaned with QIAquick silica
columns(Qiagen,Inc) accordingto the manufacturer's
protocols.TherbcLexon was amplifiedin two overlap-
ping fragmentsaccordingto the PCRprotocolandtwo
PCR products were sequenced in both directions with
these PCR primers,using the BigDyeTMTerminatorMix
and an ABI 377 automatedsequencer following manu-
facturer'sprotocols (Applied Biosystems, Inc.).
Phylogenetic analyses and alignments. -
Three parsimonyanalyses were performed,morphology
alone, rbcL alone, and a combined analysis. They were
performedwith PAUP 2.0b2 (Swofford, 2000) and ana-
lyzed using Fitch parsimony(Fitch, 1971). The three
analyses were heuristic searches performed with 1000
randomadditionsequence replicatesto look for multiple
optimal-tree islands (Maddison, 1991). Analyses used
TBR (tree bisection reconnection) branch swapping,
MULTrees, steepest descent and ACCTRAN optimiza-
tion. Internal support was evaluated with jackknife
analysis (Farris& al., 1996) of 1000 replicates and 30%
deletion of characters.In morphologicalanalysis charac-
ters were considered unordered. In molecular analysis
contiguous sequenceswere assembledand checked using
Sequencher 3.0 (Genecodes, Inc.); rbcL sequences are
lengthconservedandeasilyalignedby eye.
/ OH
1o
H H
0
OH C15H31
H O
(3) Pentadecyl resorcinolor Cardol (4) Rhusflavanone,a biflavonoid
TAXON 53 (2) * May 2004: 357-364 Aguilar-Ortigoza& Sosa * Compounds in Anacardiaceae

Table 1. Morphological, anatomical and phytochemical character and character-states used in the phylogenetic analy-
ses of genera of Anacardiaceae.
1. Habit of plant: 0 = tree, 1 = shrub. 48. Carpelnumber:0 = five, I = three, 2 = two, 3 = one.
2. Leaves: 0 = paripinnate,1 = imparipinnate,2 = simple. 49. Locules in ovary at anthesis: 0 = five, 1 = three, 2 = one.
3. Leaf shape: 0 = oblong, 1 = elliptic, 2 = ovate, 3 = obovate. 50. Stylar insertion:0 = apical, 1 = ventral-lateral.
4. Leaf texture:0 = chartaceous, 1 = coriaceous. 51. Stigma morphology: 0 = capitate, 1 = spathulate.
5. Leaf duration:0 = evergreen, 1 = deciduous. 52. Ovule orientation:0 = epitropous, 1 = apotropous.
6. Leaf grouping in branches:0 = sparsed, 1 = clustered at apex. 53. Ovules per locule: 0 = two, 1 = one.
7. Leaf margindissection: 0 = serrate, 1 = entire. 54. Ovule integument:0 = two, 1 = one.
8. Rachis: 0 = not winged, 1 = winged. 55. Ovule insertion:0 = apical, 1 = apico-lateral,2 = latero-basal,3 = basal.
9. Terminalleaflet shape: 0 = ovate, 1 = elliptic, 2 = obovate. 56. Fruitform: 0 = ovoid, 1 = oblate, 2 = suborbicular.
10. Apex of the leaf: 0 = acute, 1 = obtuse. 57. Winged fruit:0 = absent, 1 = present.
11. Lamina type: 0 = dorsiventral,I = isobilateral. 58. Peduncule of fruit: 0 = thin, 1 = thick.
12. Foliar epidermis:0 = single-layered, 1 = multi-layered. 59. Fruittrichomes:0 = absent, 1 = present.
13. Foliar hypodermis:0 = absent, I = present. 60. Epidermisof exocarp: 0 = unlignified, 1 = lignified.
14. Stellate trichomes:0 = present, 1 = absent. 61. Hypodermisof exocarp: 0 = absent, 1 = present.
15. Capitatetrichomes:0 = present, 1 = absent. 62. Mesocarp sclereids with resin canals: 0 = absent, 1 = present.
16. Cuticularstriae:0 =random, 1 = radial. 63. Mesocarpwith inner parts lignified: 0 = absent, I = present.
17. Giant stomata:0 = absent, 1 = present. 64. Endocarpnumberof layers: 0 = one, 1 = two, 2 = three, 3 = four.
18. Type of venation: 0 = camptodromous,1 = craspedodromous. 65. Endocarpdiscrete fourth layer: 0 = absent, 1 = with parenchyma,
19. Size of primaryvein: 0 = massive, 1 = stout. 2 = with sclereids.
20. Angle of secondaryvein: 0 = narrow,1 = moderate. 66. Endocarpcrystals in the layer: 0 = absent, 1 = present.
21. Tertiaryveins: 0 = percurrent,1 = reticulate,2 = ramified. 67. Endocarpdiscrete third layer: 0 = absent, 1 = with palisade-shaped
22. Marginalvenation: 0 = fimbriate, 1 = incomplete. sclereids, 2 = with sclereids.
23. Veinlets: 0 = simple, 1 = branched. 68. Endocarpdiscrete second layer: 0 = absent, I = with palisade-shaped
24. Inflorescence position: 0 = terminal, 1 = axilar. sclereids, 2 = with osteosclereids, 3 = with brachysclereids.
25. Inflorescence type: 0 = panicle, 1 = thyrsoid. 69. Endocarpdiscrete first layer: 0 = with sclereids,
26. Cupularinvolucre:0 = absent, 1 = present. I = with palisade-shapedsclereids.
27. Flower sex: 0 = unisexual, 1 = bisexual. 70. Endocarpfirst layer size: 0 =less the twice of rest of layer,
28. Sepal number:0 = three, 1 = four, 2 = five, 3 = six. 1 = more than twice thickness.
29. Calix aestivation:0 = valvate, 1 = imbricate. 71. Number of seeds: 0 = five, 1 = three, 2 = two, 3 = one.
30. Sepal indument:0 = glabrous, 1 = pubescent. 72. Embryo:0 = straigth, 1 = curved.
31. Margin sepal indument:0 = glabrous, 1 = pubescent. 73. Testa:0 = membranous, 1 = crustaceous.
32. Sepal shape: 0 = oblong, 1 = ovate. 74. Endosperm:0 = present, 1 = absent.
33. Petal number:0 = five, 1 = four, 2 = zero. 75. Cotyledon margin:0 = lobed, 1 = entire.
34. Corolla aestivation:0 = imbricate, 1 = valvate. 76. Wood parenchymaapotracheal:0 = absent, 1 = present.
35. Petal shape: 0 = oblong, I = elliptic, 2 = ovate. 77. Wood parenchymaparatracheal:0 = alliform, 1 = banded, 2 = vasicentric.
36. Stamen number:0 = ten, 1 = five, 2 = eigth. 78. Wood ray width: 0 = 1-5 cells, 1 = 6-10 cells.
37. Filament form: 0 = filiform, 1 = subulate. 79. Wood ray type: 0 = heterogeneous IIB, 1 = heterogeneous IIA,
38. Filament indument:0 =glabrous, 1 = pubescent. 2 = heterogeneousIII.
39. Anther form: 0 = pyriform, 1 = rotund,2 = botuliform. 80. Septate wood fibers: 0 = present, 1 = absent.
40. Anther:0 = basifixed, I = dorsifixed. 81. Resin canals in wood rays: 0 = present, 1 = absent.
42. Pollen shape: 0 = prolate, 1 = spheroidal. 82. Resin canals in ploem: 0 = absent, I = present.
42. Pollination:0 = by insects, 1 = by wind. 83. Vessel clusters: 0 = absent, 1 = present.
43. Nectariferousdisk: 0 = intrastaminal,1 = extrastaminal. 84. Starchin vessels: 0 = absent, 1 = present.
44. Disk form: 0 = patelliform, 1 = cotyliform, 2 = columnar. 85. Growthring: 0 = absent, 1 = present.
45. Disk margin:0 = crenate, 1 = lobate. 86. Alkylcatechols: 0 = absent, I = present.
46. Number of disk lobes: 0 = ten, 1 = five. 87. Alkylresorcinols:0 = absent, 1 = present.
47. Carpellodenumber:0 = five, 1 = three, 2 = two, 3 = one. 88. Biflavonoid: 0 = absent, 1 = present.

Reconstructing the history of chemical char-

acters. - To investigate the evolutionary history of RESULTS
chemical characterswe mappedthe presence of each of Phylogenetic relationships. - Morphological
the three phenolic compounds (alkylcatechols, alkylre- analysis recovered a single equally most-parsimonious
sorcinols and biflavonoids) on the strict consensus tree tree (MPT) of 453 steps, with a consistency index (CI) of
using parsimonyoptimizationand the TRACE option of 0.38 and a retentionindex (RI) of 0.52, including a total
MacCladeversion 3.04 (Maddison& Maddison, 1992). of 88 characters,with 86 parsimonyinformativecharac-

359

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 & Sosa* Compoundsin Anacardiaceae
Aguilar-Ortigoza TAXON 53 (2) e May2004:357-364

ters. Fig. 2 represents one of the MPT selected at ran-

Bursera
dom. rbcL analysis recovered21 MPT of 481 steps, with
Ruta
a CI of 0.73 and a RI of 0.61, including 1414 characters,
Dodonaea
with 127 parsimonyinformativecharacters.Fig. 3 repre- Swietenia
sents one of the MPT selected at random.Matrixof com- Tapirira
bined analysis included 1502 characterswith 213 parsi- 62
-E Cyrtocarpa

mony informative characters.Eight MPT of 1002 steps Spondias

were obtainedwith a CI of 0.57 and a RI of 0.53. Fig. 4 Buchanania

representsone of the MPT,selected at random.Topology Blepharocarya

of MPT is very similar in the three analyses. The mor- Anacardium

phological tree is the least supported,with only a few 83 Mangifera

Bonetiella
clades receivingjackknife supportabove 50%. In the tree
Cotinus
analyses the Anacardiaceae clade is always recovered Actinocheita
with good jackknife support.In the three analyses, Clade Comocladia
I and Clade II are recovered.Buchanania is always basal Metopium
in Clade II and Anacardiumand Mangifera form a sub- Amphipterygium
clade. Position of some of the membersof Clade II varies Pistacia

(Figs. 2-4). For example, Blepharocaryais in a subclade Pseudosmodingium

with Anacardium and Mangifera in the rbcL analysis Mosquitoxylum

while in the combined analysis it is in a subcladewith the Schinopsis

Astronium
rest of the taxa of Clade II. The best supportedtopology
Schinus
is from combined analysis in which the Anacardiaceae Rhus
clade is well supported (100% jackknife value). Two Smodingium
clades are found within the family: a well supported Toxicodendron
basal clade formed by Cyrtocarpa, Spondias and
Tapirira,and a second clade with the rest of the genera Fig. 3. One of the 21 MPTtrees of the rbcL analysis of 481
steps, with a Cl of 0.73 and a RI of 0.61. Jackknife per-
centages (>50%) are indicated above the branches.
Bursera
a-
Ruta
0
Dodonaea
(strongly supported90% jackknife value). Buchanania
Svetenia 0
appears basal in this clade. Well supported groups in
62
Tapirira these clade are formed by Actinocheita, Bonetiella and
57 Cyrtocarpa
Comocladia (jackknife value of 94%), Metopium and
Spondias
Buchanania
Mosquitoxylum (97%) and Astronium and Schinopsis
Blepharocarya
(100%).
Anacardium
Character evolution. - Evolution of the chemi-
Mangifera
cal charactersshow different patternsdepending on the
Bonetiella type of toxic phenolic compound. Alkylcatechols
Cotinus evolved in two groups in Anacardiaceae,in a clade (not
Actinocheita u
supported) formed by Actinocheita, Astronium,
Comocladia
Bonetiella, Comocladia, Metopium, Mosquitoxylum,
Metopiumr
Pseudosmodingiumand Schinopsis, and in a subclade
M
(well supported) formed by Smodingium and
Amphipterygium
c
Pistacia <
Toxicodendron.The ancestral condition is the lack of
Pseudosmodingium

Mosquitoxylum
alkylcatechols (Fig. 4). The presence of alkylresorcinols
Schinopsis is restrictedto the clade of Anacardiumand Mangifera
Astronium and in Schinus (Fig. 4). Biflavonoids arose independent-
Schinus ly in Burseraceaeand in Clade II of Anacardiaceaewith
Rhus the exception of Buchanania (Fig. 4).
Smodingium
Toxicodendron

Fig. 2. MPT tree of the morphological analysis of 453 DISCUSSION

steps, with CI of 0.38 and a RI of 0.52. Jackknife percen-
tages (>50%) are indicated above the branches. Phylogenetic analysis. - Our results agree with

360

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TAXON 53 (2) e May 2004: 357-364 Aguilar-Ortigoza& Sosa * Compounds in Anacardiaceae

Ej 0 Dodonaea
previous phylogenetic studies (e.g., Gadek & al., 1996),
80
130
Ruta
O0 Swietenia

M0 Bursera
Outgroup
in thatAnacardiaceaeare a monophyleticgroup.The two
90 Tapirira
lineages in Anacardiaceaementioned in our results are
S65 0 Cyrtocarpa Clade I
also detected in molecular phylogenetic studies (Miller
E0loo 0O Spondias & al., 2001; Pell & Urbatsch, 2001) and in studies that
=0 Buchanania
90 97 me Anacardium
combined charactersets (DNA sequences and morpholo-
WM Mangifera gy, Terrazas& Chase, 1996). Furthermore,endocarpand
0M 0 Blepharocarya
M 0 Cotinus
wood charactersalso indicate two groups in the family,
72
M10 Amphipterygium comprised of the same genera (Wannan& Quinn, 1990,
Pistacia
1991). Two types of endocarp are found in Anacardia-
Schinus Clade II
6me
O0 Rhus
ceae, the Anacardium-type(with discrete and regularly
8Q M80
91 M 0 Smodingium arrangedlayers), three or fewer carpels and a unilocular
M0 Toxicodendron
ovary, and group B with the Spondias-type of endocarp
Actinocheita
84
94
0Bonetiella
(a thick mass of usually lignified and irregularlyoriented
M• M( Comocladia sclerenchyma),more than three carpels and a multilocu-
•
97 0 Metopium
lar ovary. Group B corresponds to tribe Spondiadeae
0 Mosquitoxylum
O Absenceof biflavonoids M•1
6
M Pseudosmodingium
from Engler's (1883) classification or to Clade I, includ-
m Presenceof biflavonoids 100 M 0 Astronium ing Antrocaryon, Cyrtocarpa,Dracontomelon, Haema-
O Absenceof alkylcatechols
andalkylresorcinols M @ Schinopsis
O Presenceof alkylcatechols tostaphis,Harpephyllum,Lannea, Sclerocarya,Spondias
* Presenceof alkylresorcinols and Tapirira,among others. The Spondias clade retained
plesiomorphiccharacterssuch as a gynoecium with five
carpels, fruit often multilocular with a thick endocarp,
Fig. 4. One of the eight MPTof the combined analysis of
1002 steps with CI = 0.57 and RI = 0.53. Jackknife per- lignified, andwith irregularlyorientedsclereids (Wannan
& Quinn, 1990). The Spondias-type of endocarpis also
centages (>50%) are indicated above the branches.
Evolution of alkylcatechols, alkylresorcinols and bifla- present in some Burseraceae(Wannan& Quinn, 1990).
vonoids are mapped onto the tree. The genera of Clade II share morphologicalcharac-
ters such as a tricarpelargynoecium, unilocularfruitwith

Burseraceae .--- C. nigridorsalis

Sapindaceae
C.
Meliaceae rhois
duvauae
Rutaceae C.
Tapirira C. evodiae
Cyrtocarpa C. nigrilineata
Spondias
C. monticola
Buchanania
Anacardium -C. longispiculafa

Mangifera C. spondiasiae

Blepharocarya C. verrucosa
Cotinus C andina
Amphipterygium
C. clausa
Pistacia
Schinus C. mammifex

Rhus C. patagonica
Smodingium C rubra
Toxicodendron
C. orbicola
Actinocheitaorbicola
Bonetiella C. gallifex
Comocladia C. schini
Metopium
C. scrobiocola
Mosquitoxylum
C. catillicola
Pseudosmodingium
Astronium C. hermicitae

Schinopsis L C. terebinthifolii

Fig. 5. Feeding preferences of Calophya species (right) on Anacardiaceae, Burseraceae and Rutaceae hosts (left).
Calophya phylogeny based on Burckhardt & Basset (2000).

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Aguilar-Ortigoza& Sosa * Compounds in Anacardiaceae TAXON 53 (2) e May 2004: 357-364

an endocarpcomposed of discreteandregularlyarranged independentlyat least twice, in the clade of Anacardium

layers of cells (Wannan& Quinn, 1990). One of the well + Mangiferaand in Schinus. These phenolic compounds
supported subclades in Clade II is formed by Schinus, are synthesized in the pericarps of three economically
Rhus, Smodingium and Toxicodendron.They all share importantspecies: the cashew nut (Anacardiumocciden-
characterssuch as imparipinnateleaves sparsely distrib- tale), the mango (Mangifera indica) and the less widely
uted along branches, ovate and chartaceous leaflets; known Brazilianpepper (Schinus terebinthifolius).Their
moreover, they have the same calyx indument,thyrsoid fruitshave been reportedto cause dermatitisin certain
inflorescence and wood having the heterogeneous IIB individuals(Morton,1978, 1981).
type of ray. Rhus and Toxicodendronare cosmopolitan, Spondiaswhich does not producealkylcatechols,
while Schinus is from SouthAmerica and Smodingiumis alkylresorcinolsor biflavonoids has the capacity to syn-
endemic to South Africa. The other subclade, also well thesize phenolic compounds (Corthout & al., 1989).
supported, is formed by Actinocheita, Bonetiella and Spondias mombin L. has been reported to possess the
Comocladia. These three neotropicalgenera share char- metabolicrouteto synthesizethesesubstances,sincethe
precursors of the formation of a related phenol, hep-
acters such as coriaceous leaves, panicle type of inflores-
cence with axillar insertion and imbricatecalyx aestiva- tadecadienyl-phenol,have been detected (Corthout& al.,
tion. Actinocheitaand Bonetiella are endemic to Mexico, 1989).
and Comocladia to Mexico and the West Indies. Biosynthetic routes of alkylcatechols and biflavon-
Metopiumand Mosquitoxylumare a sister group distrib- oids are involved in the shikimatepathway(VanSumere,
uted in Mexico and the West Indies. The closely related 1989). Accumulation of alkylcatechols, alkylresorcinols
group formed by Pseudosmodingium, Astronium and and biflavonoids is in some cases restricted to certain
Schinopsis is also neotropical. organs of the plant. Alkylcatechols and biflavonoids are
Character evolution. - One of the most inter- usually present in leaves and bark. But in some species
estingpatternsof evolutionof the toxic phenoliccom- such as Metopiumbrownei alkylcatechols also found in
pounds in Anacardiaceae is that shown by the wood (Young, 1976). A few Semecarpus species (not
biflavonoids.Burseraceae,includedas an outgroupin included in our analysis) also produce alkylcatecholsin
our analysesand recognizedas sisterto Anacardiaceae fruits(Carpenter& al., 1980). Occurrenceof these chem-
(Gadek& al., 1996; Terrazas& Chase, 1996; Pell & icals in only certainorgansof the plant can be explained
Urbatsch, 2001), synthesizes biflavonoids. These in terms of enzyme specificity and substrates. Schwab
biflavonoids are not producedby the generaof Clade I of (2003), in a review of metabolome diversity, concluded
Anacardiaceae, the Spondiadeae of Engler (1883), but that diversityof metabolitesis causedby low enzyme
they are produced in the taxa of Clade II, arising only specificity but availability of suitable substratesdue to
once in the historyof the group.Wannan& al. (1985) and compartmentationhas also been taken into account.
Young & Aist (1987) previously pointed out this pattern. It has been documentedthat in Anacardiaceae,alkyl-
Furthermore,the genera of Clade I did not produce the catechols are toxic and repellent,and hence an effective
phenolic compounds we considered. The members of defense system against herbivory by insects (Farrell&
Clade II, with the exception of Buchanania, synthesize al., 1991). The diversificationof certaingroupsof insects
biflavonoids. The presence of this compound strongly as a resultof a feeding relationshipwith certaingroupsof
supports the inclusion of Amphipterygium and plants has been reported for a number of groups, e.g.,
Blepharocarya in Anacardiaceae,although these genera Phyllobrotica (Chrysomelidae)and Lamiales (Farrel&
have been considered in Julianiaceaeand Blepharocary- Mitter, 1990; Mitter & al., 1991); Blepharida
aceae, respectively (Airy Shaw, 1965; Hemsley, 1908). (Chrysomelidae) and Bursera (Becerra, 1997). Among
Amphipterygium's flowers lack a corolla and Lamiaceae, species of genera such as Stachys,
Blepharocarya possesses small globose inflorescences Physostegia and Scutellaria produce toxic iridoid (ter-
and their leaves are opposite and pinnate, charactersnot penoids) compounds that restrain several herbivores
common among Anacardiaceae. (Farrel & Mitter, 1990). However, species of
The evolutionary patterns of alkylcatechols and Phyllobroticafeed on species of these Lamiaceae(Mitter
alkylresorcinols in the members of Clade II are not & al., 1991). Phyllobrotica is a genus strictly mono-
straightforward.Alkylcatechols evolved in two groups: phagous (Farrel & Mitter, 1990; Mitter & al., 1991).
in a clade formed by Actinocheita, Astronium, Bursera species producepinene, camphene,phelandrene
Bonetiella, Comocladia, Metopium, Mosquitoxylum, and limonene (terpenes) in resin canals. These terpenes
Pseudosmodingium and Schinopsis, and in a subclade are toxic to most herbivores. However, species of the
formed by Smodingiumand Toxicodendron. monophagousgenus Blepharida feed on certainBursera
Alkylresorcinols are less common than alkylcate- species dependingon a specific terpene (Becerra, 1997).
chols or biflavonoids among Anacardiaceae.They arose Burckhardt& Basset (2000) indicatedthatthe diver-

362

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All use subject to JSTOR Terms and Conditions
TAXON 53 (2) e May 2004: 357-364
sification of the hemipterangenus of insects, Calophya,
is closely relatedto the plants they feed on. Theirphylo-
genetic study of Calophya corroboratessuch relation-
ships, suggesting that these hemipteran insects are
monophagous and only feed on species of the related
groups of plants such as Anacardiaceae, Rutaceae and
Burseraceae(Burckhardt& Basset, 2000). According to
their results, Calophya evodiae feeds on Rutaceae, C.
nigrilineata feeds on Burseraceae, C. spondiasiae on
Spondiaspinnata, C. longispiculata on Buchanania lan-
zan, C. rhois on Cotinus coggygria, C. nigridorsalis on
Rhus trichocarpa; and more than ten species of
Calophyafeed on species of Schinus.When the two phy-
logenies of Calophya and Anacardiaceae with their
closely related groups are compared (Fig. 5), it can be
shown that species of Calophya feed mainly on taxa of
Rutaceae and Anacardiaceaethat are not capable of pro-
ducing toxic phenolic compoundssuch as alkylcatechols.
However, Calophya species are capable of feeding on
taxa of Burseraceae, Rutaceae and Anacardiaceae that
producebiflavonoid andresorcinolphenolic compounds.
Most species of Calophyaare found to feed on species of
Schinus that do not produce alkylcatechols but can syn-
thesize alkylresorcinols and biflavonoids (Fig. 5).
Further information is needed to test whether other
groups of insects are capable of feeding on Anacardia-
ceae that produce alkylcatechols. Bioessays are also
needed to confirm feeding preferences of Calophya
species.
ACKNOWLEDGEMENTS
The projectwas madepossible by a grantfrom CONACYT
Mexico (225260-5-29378Nto VS) and from PROMEP(to CJA-
O). We thankFranciscoLoreafor his help in obtainingherbarium
specimens, and RauilAcevedo, Sergio Avendailo and Santiago
Barriosfor their help with field work. We are gratefulto Bianca
Delfosse for editingthe Englishversionof this manuscript.
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