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Cone Idioblasts of Eleven Cycad Genera: Morphology, Distribution, and
Significance
Andrew P. Vovides
Botanical Gazette, Vol. 152, No. 1. (Mar., 1991), pp. 91-99.
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BOT. GAZ. 152(1):91-99. 1991.
0 1991 by The University of Chicago. All rights reserved.
0006-8071 /91/5201-0012$02.00
CONE IDIOBLASTS OF ELEVEN CYCAD GENERA: MORPHOLOGY,
DISTRIBUTION, AND SIGNIFICANCE
ANDREW P. VOVIDES
Fairchild Tropical Garden, 11935 Old Cutler Road, Miami, Florida 33156; and Instituto de Ecologia, A.C., Apdo Postal 63,
Xalapa, Veracruz 91000, Mexico
Sporophylls from strobili of 16 species among 11 genera of cycads were examined for idioblasts. Thinwalled secretory-like idioblasts were found in the majority of taxa and thick-walled sclerenchyma-type idioblasts were found in the minority. With the exception of Cycas rumphii and Stangeria eriopus, where
secretory idioblasts were in the epidermis and/or hypodermis, none were found in the sporophyll parenchyma of these species. Most idioblasts stained ninhydrin-Schiff-positive, and tannins were present also.
Sporophyll idioblasts appear to be related to interactions with insect predators and/or cosymbionts and may
form part of a complex pollination syndrome. The lack of idioblasts in stem tissue and low concentration
in leaflet tissue of Zamiafutfiuracea compared with sporophyll tissue is significant support to this hypothesis.
On the basis of almost universal occurrence of these idioblasts in the sporophylls, we suggest that insect
symbiosis related to pollination may be common to most cycad genera.
Introduction
Idioblasts may be classified into three major categories: secretory, tracheoid, and sclerenchymatous (FOSTER1956). The term "idioblast" may be
applied to a range of cell types from parenchyma
cells with specialized contents like tannin cells and
oil cells to scelerenchymatous cells, idioblastic
sclereids, or trichoblasts that are distributed randomly in the soft tissues of organs for which they
and CHALK1979). The
provide support (METCALFE
presence of idioblasts in cycads has been noted for
some time (GREGUSS1968), but little is known of
their function. NORSTOGand FAWCETT
(1989) and
NORSTOGand VOVIDES(unpubl. data) relate the
idioblasts from staminate and ovulate cones of the
Mexican cycad Zamia furfuracea to a complex
weevil-pollination syndrome. The idioblasts stain
ninhydrin-Schiff (NIN) and periodic acid-Schiff
(PAS) positive (NORSTOG
and FAWCETT
1989). Recent analysis of cycad tissues by DUNCAN
et al. (in
press) has shown the presence of a powerful neurotoxin 2-amino-3-(methylamino)-propanoic acid
(BMAA). This toxin is sequestered in the larval
phase of the weevil pollinator and incorporated into
the pupa case (NORSTOG,
DUNCAN,
and FAWCETT
in preparation). DUNCAN
et al. (in press) and NORSTOG et al. (1986) suggest that these toxins are contained within idioblasts in the parenchyma tissues
of the staminate and ovulate cone sporophylls of
Z. fufuracea. Cycads are also toxic to most mammals including humans (WHITING1963, 1965).
Another ergastic substance present in cycads is
calcium oxalate (CWERLAIN 1919) usually in the
Manuscript received April 1990; revised manuscript received
September 1990.
Address for correspondence and reprints: ANDREW
P. VOVIDES,Instituto de Ecologia, A.C., Apdo Postal 63, Xalapa, Veracruz 9 1000, Mexico.
form of crystals or druses. Though very widespread in angiosperms and much studied by anatomists there are differences of opinion as to the
significance of calcium oxalate crystals in metabolism (METCALFE
and CHALK1983).
This investigation is a survey of the cones of 16
species among 11 genera of cycads growing at
Fairchild Tropical Garden (FTG), undertaken to
describe idioblasts within their sporophyll tissues
in comparison to those found in the sporophyll tissues of Z. furfuracea.
Material and methods
Micro- and megasporophylls from early and near
maturity cones were fixed in formalin-acetic acidalcohol (FAA) then embedded in wax for microtome sectioning. Cross and longitudinal sections,
20 pm thick, were taken and duplicate slides were
prepared for histochemical staining using NIN
(proteins), PAS (carbohydrates), phloroglucinol-HC1
(lignin), iodine (starch), and ferrous sulfate (tannins). Crossed polaroids were used on the microscope to detect birefringent crystals, and calcium
oxalate was tested for with concentrated HCl
and CHALK1983). Staining and mount(METCALFE
ing procedures were according to JENSEN(1962)
(1940). For Bowenia and Microcyand JOHANSEN
cas, herbarium specimens were hydrated by boiling in water for 15 min and cooling (repeated three
times) before fixing and dehydrating as with fresh
material.
Cross sections of leaflet and stem of Zamia furfuracea and leaflet of Encephalartos altensteinii
were taken for comparison with the cone tissue.
A Leitz Ortholux 2 microscope was used for
photomicrography with Kodak Plus-X film (125
ASA) and Kodabrome RC paper for prints. The
taxa examined are listed with their FTG accession
no. or collectors' number for the herbarium material examined at FTG (table 1).
92
BOTANICAL GAZETTE
TABLE I
Species
Garden accession no.
Voucher no.
Bovvenia spectabilis Hook. ex Hook. f . . . . . . . . . . Ceratozamia mexicana Brongn. . . . . . . . . . . . . . . . . C . mexicana var. robusta Miq. . . . . . . . . . . . . . . . . Cycas rumphii Miq. . . . . . . . . . . . . . . . . . . . . . . . . . Chigua restrepoi Stevenson . . . . . . . . . . . . . . . . . . . Dioon edule Lindl. . . . . . . . . . . . . . . . . . . . . . . . . . . D. spinulosum Dyer . . . . . . . . . . . . . . . . . . . . . . . . . Encephalartos bubalinus Melville . . . . . . . . . . . . . . E. ferox Bertolini . . . . . . . . . . . . . . . . . . . . . . . . . . . E . hildebrandtii. A. Braun et Bouche . . . . . . . . . . . E. manikensis (Gilliland) Gilliland. . . . . . . . . . . . . . Lepidozamia hopei Regel . . . . . . . . . . . . . . . . . . . . . Macrozamia lucida L.A.S. Johnson . . . . . . . . . . . . Microcycas calocoma (Miq.) D.C. . . . . . . . . . . . . . Stangeria eriopus (Kuntze) Nasn . . . . . . . . . . . . . . . Zamia fischeri Miq. . . . . . . . . . . . . . . . . . . . . . . . . 2. lindenii Regel ex Andre. . . . . . . . . . . . . . . . . . . . Observations
All genera examined had at least secretory idioblasts throughout the parenchyma of the sporophyll
tissues (figs. 1-20). Exceptions to these observations were Cycas and Stangeria, which had few
idioblasts that were confined to the epidermal and/
or hypodermal cells. All idioblasts were found to
be NIN-positive except those of Cycas rumphii,
Chigua restrepoi, Microcycas calocoma, and Stangeria eriopus. All trichoblasts and idioblastic
sclereids had lignified thick secondary cell walls,
the trichoblasts were 7-15 times longer than wide
and were often branched at their ends (figs. 6, 7).
The idioblastic sclereids were oblong, angular, or
isodiametric resembling stone-cells but each with
a large lumen. Most showed heavy pitting in their
thick secondary walls (figs. 10, 12). Most species
showed crystals and druses in their tissues, and some
Encephalartos species showed druses associated
with their cuticles.
Bowenia spectabilis (fig. 1) microsporophylls
contained secretory, parenchymatous idioblasts and
oblong, angular to isodiametric, thick-walled,
idioblastic sclereids that were NIN-positive and
PAS-negative. Epidermal cells stained NIN-positive. Megasporophylls were not examined. Most
idioblasts and epidermal cells stained for tannins.
Idioblast break-down was not detected.
Ceratozamia mexicana (fig. 2), in microsporophylls, idioblasts were more concentrated in the
hypodermis, and the trichoblasts were mostly PAS
negative. Much starch was present throughout the
parenchyma with very few idioblasts breaking down.
Megasporophylls of C . mexicana var. robusta (immature cone) had both parenchymatous, secretory
idioblasts, and septate trichoblasts that were NINand PAS-positive. Their idioblasts and epidermal
cells also contained tannins. Calcium oxalate druses
were found in cells near the epidermis and very
little starch was present in the parenchyma. Some
of the secretory idioblasts have transfer cell walllike structures but no evidence of breakdown.
FIGS. 1-10.-Microand megasporophylls in section. Fig. 1, Bovvenia spectabilis cross section of microsporophyll, idioblasts
(arrows), iodine-fast green (IFG); insert a=ninhydrin-Schiff (NIN) stain. Fig. 2, Ceratozamia mexicana cross section of microsporophyll, secretory idioblasts (arrow) NIN stain; insert a = C . mexicana var. robusta cross section of megasporophyll, trichoblast
(large arrow), secretory transfer cell-like idioblast (small arrow), NIN stain; insert b=microsporophyll parenchyma cells packed
with starch, IFG stain. Fig. 3, Chigua restrepoi cross section of megasporophyll, secretory idioblasts (arrows); insert a=transfer
cell-like secretory idioblast, ferrous sulfate stain for tannins (black). Fig. 4, Cycas rumphii cross section of micro- and megasporophylls (insert a ) idioblasts and tannin-filled epidermal cells (arrows). Figs. 5, 6, Dioon edule. Fig. 5, Cross section of
microsporophyll, idioblasts (arrows) NIN stain; insert a=starch-filled parenchyma cells, IFG stain. Fig. 6, Longitudinal section
of megasporophyll with trichoblasts (large arrow) and secretory idioblasts (small arrow) NIN stain; insert a=tannin-filled epidermal
cells, ferrous sulfate stain. Figs. 7, 8, Dioon spinulosum. Fig. 7, Longitudinal section of microsporophyll, NIN-positive secretory
idioblasts (arrows) and trichoblast; insert a=starch-filled parenchyma cells, IFG stain; insert b=tannin-filled idioblasts, ferrous
sulfate stain. Fig. 8, Cross section of megasporophyll showing NIN-positive secretory idioblasts with some having transfer celllike appearance (insert a). Fig. 9, Encephalartos bubalinus, cross section of megasporophyll, NIN-positive idioblasts (arrows),
transfer cell-like secretory idioblasts (small arrow). Fig. 10, Encephalartosferox, cross section of microsporophyll, NIN-positive
secretory idioblasts and pitted idioblastic sclereids; insert a=starch-filled parenchyma cells, IFG stain. All bars 50 km.
VOVIDES-CYCAD
Chigua restrepoi (fig. 3 ) rnegasporophylls contained secretory, parenchymatous idioblasts near
the epidermis that stained NIN-negative and mostly
PAS-negative. Trichomes stained NIN-positive.
Microsporophylls were not examined. Most idioblasts and epidermal cells stained for tannins. Many
idioblasts showed transfer cell wall-like structures
and appeared to be breaking down. Few druses were
found in sporophyll tissues associated with the epidermis. No starch was detected in the sporophyll
parenchyma.
Cycas rumphii (fig. 4 ) micro- and megasporophylls contained a few secretory idioblasts in the
first layers of cells beneath the epidermis (hypodermis) but not elsewhere. Microsporophylls also had
thick-walled isodiametric, idioblastic sclereids. The
epidermal cells and idioblasts were NIN- and PASnegative and contained tannins, but trichomes were
found to be NIN-positive. Druses were found in
both micro- and megasporophyll tissues, especially
near the epidermis, and some druses were scattered
in the base of the microsporophyll stalk. Very little
starch was detected in megasporophyll parenchyma, but much was found in the microsporophyll tissue. The breakdown of idioblasts in the
megasporophylls was not detected.
Dioon edule (figs. 5 , 6) micro- and megasporophylls contained secretory, parenchymatous
idioblasts and thick-walled, septate trichoblasts that
were NIN- and PAS-positive. Some epidermal cells
of the microsporophyll were NIN-positive, and all
epidermal cells of the megasporophyll and trichomes were NIN-positive. Idioblasts and epidermal cells of both micro- and rnegasporophylls were
rich in tannins. No idioblast breakdown was detected in the megasporophyll (immature cone), but
some secretory idioblasts of the rnicrosporophyll
were seen to have a transfer cell wall-like structures. Few druses were found in both sporophyll
tissues. No starch was detected in the megasporophylls, but much starch was found in the microsporophyll parenchyma.
Dioon spinulosum (figs. 7 , 8) micro- and megasporophylls contained secretory, parenchymatous
idioblasts and thick-walled septate trichoblasts that
CONE IDIOBLASTS
95
were NIN- and PAS-positive in megasporophyll
tissues and NIN-positive and mostly PAS-positive
in microsporophylls. Epidermal cells of both micro- and megasporophylls were NIN-positive. Most
idioblasts in the microsporophyll, and all epidermal cells of both micro- and megasporophylls, were
rich in tannins. Almost all idioblasts showed transfer cell wall-like structures in the megasporophyll,
but some secretory idioblasts of the microsporophyll were also seen to have transfer cell wall-like
structures. Few druses were found in both sporophyll tissues. No starch was detected in the megasporophylls, but much starch was found in the
microsporophyll parenchyma.
Encephalartos bubalinus (fig. 9 ) megasporophylls contained secretory, parenchymatous idioblasts and oblong, angular to isodiametric, thickwalled, pitted, idioblastic sclereids that were
NIN-positive and mostly PAS-negative. Microsporophylls were not examined. All idioblasts
and epidermal cells stained for tannins. Few idioblasts showed transfer cell wall-like structures and
were breaking down. Druses were found in sporophyll tissues associated with the epidermis and cuticle. No starch was detected in the sporophyll
parenchyma.
Encephalartos ferox (fig. 10) microsporophylls
contained secretory, parenchymatous idioblasts and
oblong, angular to isodiametric, thick-walled, pitted, idioblastic sclereids that were NIN-positive and
mostly PAS-positive. Megasporophylls were not
examined. Most idioblasts but no epidermal cells
stained for tannins. Some idioblasts showed transfer cell wall-like structures and appeared to be
breaking down. A few druses were found in sporophyll tissues associated with the epidermis and
cuticle. Starch was detected in the sporophyll
parenchyma.
Encephalartos hildebrandtii (fig. 1 1) micro- and
rnegasporophylls contained secretory, parenchymatous idioblasts and oblong, angular to isodiametric, thick-walled, pitted, idioblastic sclereids
that were NIN- and PAS-positive in megasporophyll tissues and NIN-negative and mostly PASnegative in the microsporophyll. Epidermal cells
FIGS. 1 I-20.-Microand megasporophylls in cross section. Fig. 1 1, Encephalartos hildebrandtii, microsporophyll with NINpositive secretory idioblasts and idioblastic sclereids; insert a=megasporophyll with NIN-positive transfer cell-like secretory idioblasts (arrow). Fig. 12, Encephalartos manikensis, microsporophyll with NIN-positive secretory idioblasts and large, pitted idioblastic sclereids (insert a). Fig. 13, Lepidozamia hopei, megasporophyll with tannin-filled secretory idioblasts near epidermis
(small arrow) and transfer cell-like (large arrow); insert a=NIN-positive idioblasts. Fig. 14, Macrozamia lucida, megasporophyll
with NIN-positive idioblasts; insert a=microsporophyll with NIN-positive idioblasts; insert b=microsporophyll with tannin-filled
idioblasts, transfer-like cells (arrows). Fig. 15, Microcycas calocoma, megasporophyll; insert a=microsporophyll, tannin-filled
idioblasts (arrows). Figs. 16, 17, Stangeria eriopus. Fig. 16, Microsporophyll with tannin-filled epidermal idioblasts (arrow);
insert a=starch-filled parenchyma cells (arrow), IFG stain; insert b=megasporophyll, ferrous sulfate stain showing tannin in epidermal idioblasts. Fig. 17, Megasporophyll with mostly NIN-negative epidermal idioblasts (insert a); insert b shows NIN-positive
epidermal glandular hair. Figs. 18, 19, Zamiafischeri. Fig. 18, Young microsporophyll with small (undeveloped) secretory idioblasts (arrows) some of which are NIN-positive; insert a=microsporophyll at pollen release with large, fully developed, intact
NIN-positive secretory idioblasts. Fig. 19, Megasporophyll with NIN-positive secretory idioblasts; insert a=transfer cell-like
idioblast. Fig. 20, Zamia lindenii, megasporophyll with NIN-positive secretory idioblasts. All bars 50 km.
96
BOTANICAL GAZETTE
of the megasporophyll only were NIN-positive. Most
idioblasts and some epidermal cells of the megasporophyll and a few idioblasts of the microsporophyll were rich in tannins. Almost all idioblasts
showed transfer cell wall-like structures and appeared to be breaking down in the megasporophyll,
but only a few idioblasts of the microsporophyll
were seen to show this phenomenon. A few druses
were found in both sporophyll tissues associated
with the epidermis. No starch was detected in the
megasporophyll, but starch was found in the microsporophyll parenchyma.
Encephalartos manikensis (fig. 12) microsporophylls contained secretory, parenchymatous
idioblasts and oblong, angular to isodiametric, thickwalled, pitted, idioblastic sclereids that were NINand PAS-positive, epidermal cells stained NINpositive. Megasporophylls were not examined. Some
idioblasts showed transfer cell wall-like structures
and evidence of breakdown. A few druses were
found in sporophyll tissues associated with epidermis and cuticle. Starch was detected in the sporophyll parenchyma.
Lepidozamia hopei (fig. 13) rnegasporophylls
contained secretory, parenchymatous idioblasts
concentrated near the epidermis that stained NINand PAS-positive; microsporophylls were not
examined. All idioblasts and epidermal cells stained
for tannins. Most idioblasts showed transfer cell
wall-like structures and evidence of breakdown.
Few druses were found in the sporophyll tissues.
No starch was detected in the sporophyll
parenchyma.
Macrozamia lucida (fig. 14) micro- and megasporophylls contained secretory, parenchymatous
idioblasts and idioblastic sclereids that were NINand PAS-positive in rnicrosporophyll tissues and
NIN-negative and mostly PAS-negative idioblastic
sclereids in the megasporophyll. Epidermal cells of
both micro- and megasporophylls were NIN-positive as well as trichomes on megasporophylls. All
idioblasts and epidermal cells of both micro- and
megasporophylls were rich in tannins. Idioblasts of
both micro- and megasporophylls showed transfer
cell wall-like structures and evidence of breakdown. Druses were found in rnicrosporophyll tissues associated with the epidermis. No starch was
detected in the megasporophyll, but starch was found
in the microsporophyll parenchyma.
Microcycas calocoma (fig. 15) micro- and megasporophylls contained secretory, parenchymatous
idioblasts that stained NIN- and PAS-negative
in rnicrosporophyll tissues and were NIN-positive
and PAS-negative idioblastic sclereids in megasporophylls. Trichomes of both micro- and megasporophylls stained NIN- and PAS-positive. Most
epidermal cells of megasporophylls stained NINpositive, but few epidermal cells of the microsporophyll stained similarly. Most idioblasts of mi-
[MARCH
cro- and megasporophylls were rich in tannins.
Idioblasts of microsporophylls showed transfer cell
wall-like structures and evidence of breakdown;
those of rnegasporophylls appeared crushed. Druses
were found scattered throughout in microsporophyll tissues, but they were near the epidermis in
megasporophylls.
Stangeria eriopus (figs. 16, 17) micro- and
megasporophylls contained secretory, parenchymatous idioblasts associated only with the epidermis. Most of the idioblasts stained NIN- and PASnegative in microsporophylls which also have NINpositive thick-walled hypodermal cells, and they
were NIN- and PAS-positive in rnegasporophylls.
Trichomes and glandular hairs of both micro- and
megasporophylls stained NIN- and PAS-positive.
Few idioblasts of micro- and rnegasporophylls were
rich in tannins. Idioblasts in the epidermis of
megasporophylls showed transfer cell wall-like
structures and evidence of breakdown. Druses were
found scattered throughout in micro- and megasporophyll tissues. Starch was detected in microsporophyll parenchyma, but very little was present
in megasporophyll tissue.
Zamia fischeri (figs. 18, 19) micro- and megasporophylls contained secretory, parenchymatous
idioblasts mostly concentrated near the epidermis,
most of which stained NIN- and PAS-positive
in rnegasporophylls but PAS-negative in microsporophylls. Trichomes of both micro- and megasporophylls stained NIN- and PAS-positive. Idioblasts of megasporophylls were rich in tannins. No
tannins were detected in young microsporophyll
idioblasts and little tannin was detected in idioblasts of mature microsporophylls. Idioblasts of
megasporophylls showed transfer cell wall-like
structures and evidence of breakdown. Fqw druses
were found scattered throughout in micro- and megasporophyll tissues. Much starch was detected in the
parenchyma of mature microsporophylls, but there
was none in the parenchyma of young microsporophylls. Idioblast size is notably smaller in young
than in mature microsporophylls.
Zamia lindenii (fig. 20) megasporophylls contained secretory, parenchymatous idioblasts that
stained NIN-positive and mostly PAS-negative; trichomes stained NIN-positive. Microsporophylls
were not examined. Tannins were not present in
any of the idioblasts or epidermal cells. No idioblasts showed transfer cell wall-like structures or
evidence of breakdown. Few druses were found in
sporophyll tissues near the epidermis. No starch was
detected in the sporophyll parenchyma.
The frequency of idioblasts in megasporophylls
of a receptive ovulate cone of Zamia furfuracea
ranges from 52 to 79 per mm2 of sporophyll tissue
with a mean of 64 (N = 3). The stem tissue did
not show any idioblasts; in leaflet tissue few NINpositive idioblasts were seen associated with the
19911
VOVIDES-CYCAD
97
CONE IDIOBLASTS
blast breakdown and toxin secretion. NORSTOG
and FAWCETT
(1989) and VOVIDES,NORSTOG,
and
DUNCAN(unpublished data) have recently drawn
attention to the function of these cells in cycads
in relation to an insect pollination syndrome in
Discussion
Z . furfuracea. Beetle pollination of Z . furfuracea, Z. pumila, and probably other cycads, is
Idioblasts in plants, in general, vary widely in
linked with a food reward (starch) as well as brood
morphology and have presumedly different funcplace and shelter in the staminate cones. Such retions that generally have not been studied in detail.
wards are not present in ovulate cones of Zamia,
They may contain ergastic material such as oils,
but nevertheless, pollinating beetles visit them
mucilage, tannins, phenolic compounds, and crysbriefly thereby completing pollination (NORSTOG
et
tals (FOSTER1956; ZOBEL1986). The cycads studal. 1986; NORSTOG
1987; TANG1987; NORSTOG
and
ied appear to have two types of idioblasts in their
FAWCETT1989). What attracts the insect to the
cones: secretory idioblasts and sclerenchymatous,
ovulate cones is not known, although fragrances
the former to a greater extent. Secretory idioblasts
may act as attractants (TANGunpublished data).
appear to be similar in morphology throughout the
More important, idioblasts of Z . furfuracea have
genera, differing only in size. The sclerenchymabeen found to contain 2-amino-3-(methylamino)tous idioblasts vary greatly among the genera rangpropanoic acid (BMAA) (DUNCAN,
personal coming from thick-walled, trichoblast-type cells of
munication) and may also contain other toxins and
Ceratozamia to the pitted, idioblastic sclereids of
function differentially in staminate cones and ovuEncephalartos. Some of the secretory idioblasts,
late cone sporophylls. The presence of tannins may
especially prior to and during breakdown, show
transfer cell wall structures described by GUNNING be associated with phenolic compounds (ZOBEL
1986). The presence of NIN-positive sporophyll
and PATE (1969) and in Zamia furfuracea
idioblasts in both sexes seems to be significant in
(NORSTOG
and FAWCETT1989). The latter authors
that idioblasts are generally intact in staminate cones,
considered this appearance to be evidence of idio-
vascular bundles, ranging from 11 to 20 per mm2
of leaflet tissue with a mean of 15.7 (N = 3). No
idioblasts were seen in E . altensteinii leaflet tissue.
TABLE 2
SUMMARY
OF IDIOBLAST DATA AND OTHER CELL CONTENTS
18 TAXA AMONG l l CYCAD
GENERA
Species
Sex
Bowenia spectabilis . . . . . . . . . . . . . .
Ceratozamia mexicana . . . . . . . . . . . .
C . mexicana var. robusta. . . . . . . . . .
Chigua restrepoi . . . . . . . . . . . . . . . . .
Cycas rumphii.. . . . . . . . . . . . . . . . . .
C . rumphii.. . . . . . . . . . . . . . . . . . . . .
Dioon e d u l e . . . . . . . . . . . . . . . . . . . . .
D . edule . . . . . . . . . . . . . . . . . . . . . . .
D. spinulosum.. . . . . . . . . . . . . . . . . .
D. spinulosum.. . . . . . . . . . . . . . . . . .
Encephalartos bubalinus . . . . . . . . . .
E.ferox . . . . . . . . . . . . . . . . . . . . . . . .
E . hildebrandtii.. . . . . . . . . . . . . . . . .
E . hildebrandtii. . . . . . . . . . . . . . . . . .
E . manikensis . . . . . . . . . . . . . . . . . . .
Lepidozamia hopei . . . . . . . . . . . . . . .
Macrozamia lucida . . . . . . . . . . . . . . .
M . lucida.. . . . . . . . . . . . . . . . . . . . . .
Microcycas calocoma . . . . . . . . . . . . .
...
M . calocoma . . . . . . . . . . . . . . .
.
Stangeria eriopus . . . . . . . . . . . . . . . .
S. eriopus . . . . . . . . . . . . . . . . . . . . . .
Zumia fischeri . . . . . . . . . . . . . . . . . . .
Z.fischeri . . . . . . . . . . . . . . . . . . . . . .
Z . lindenii . . . . . . . . . . . . . . . . . . . . . .
M
M
F
F
M
F
M
F
M
F
F
M
M
F
M
F
M
F
M
F
M
F
M
F
F
Idioblast
transfer cell/
breakdown"
OF SPOROPHYLLS OF
Starch
Ninhydrin
"here
some or few idioblasts show transfer cell-like structures or breakdown in the text,
it is considered negative in this summary.
98
BOTANICAL GAZETTE
but in ovulate cones they break down probably releasing toxin just before receptivity to pollen (NORSTOG and FAWCETT
1989). Because idioblasts of
staminate cones do not break down and since the
life cycle of the insect is completed in the staminate cones, it is thought that the function of staminate-cone idioblasts is to sequester toxin. Further,
the larvae make their pupa cases from their excrement, and these are found to be rich in the cycad
neurotoxin, BMAA. The BMAA thus incorporated
in the pupa case may serve the larva as protection
from predation during metamorphosis (NORSTOG,
DUNCAN, and FAWCETT,
unpublished data).
The presence of idioblasts in sporophylls of both
sexes and the predominance of starch in the microsporophylls of the taxa studied is assumed to be
related to interactions of one kind or another with
insect predators and/or cosymbionts giving rise to
a similar pollination syndrome described for
Z. furjiuracea by NORSTOGand FAWCETT
(1989).
Although insects related to cones of other cycads
remain unidentified to species, weevils in the genus Rhopalotria and Languriid beetles have been
isolated from cones of Dioon edule, D. spinulosum, Ceratozamia mexicana, and D. califanoi,
all collected from natural habitats in Mexico (VOVIDES, in press).
A different pollination syndrome from that of
Z. furfuracea may be found in Cycas rumphii and
Stangeria eriopus, which lack idioblasts in the sporophyll parenchyma tissues. The breakdown of
idioblasts in the microsporophylls of Macrozamia
lucida appears to be exceptional.
Cycad tissues in general are toxic and some insect species are known to specialize in feeding on
their leaves such as Sierarctia echo, Eumaeus atala
florida, and in Mexico, Eumaeus debora, all Lepidoptera. These insects sequester cycad toxins (TEAS
1967; ROTHSCHILD
et al. 1986) but E. debora rarely
[MARCH
feeds on cycad cones in Mexico. Though secretory
idioblasts may be found in other cycad tissues such
as leaves, their concentration is not the same as in
the sporophylls. In 2. furjiuracea, the absence of
idioblasts in the stem tissue and, at best, few idioblasts in leaflet tissue is significant. This supports
the hypothesis that the high concentration of idioblasts in sporophyll tissue is probably related to the
coevolution of a complex pollination symbiosis involving highly destructive insect species such as
weevils.
Vascular plants especially angiosperms that are
insect pollinated, have developed specialized
mechanisms to attract insects to flowers. These
mechanisms range from simple nonspecialized, radial symmetrical flowers (Ranunculus type), which
are pollinated by a number of different insect species, to the most complex and highly specialized
systems found in orchids, where a given orchid
species has coevolved with a given insect species.
The rewards the insects receive mostly are in the
form of food, pollen, brood place, and shelter
(FAEGRI
and VAN DER PIJL 1979). This seems to
hold also for at least some cycads, where the pollen- and starch-rich staminate cones serve as sheltering sites and brood places where the insects
complete their life cycles (NORSTOGand FAWCETT
1989).
Acknowledgments
I am deeply grateful to KNUTNORSTOGfor his
guidance and advice throughout this research and
JACKB. FISHER
for carefully revising the manuscript. I thank Fairchild Tropical Garden for laboratory facilities and access to the living cycad coland
lection. I give special thanks to NELLJENNINGS
ARTHURMONTGOMERY
whose financial support from
the Montgomery Foundation made this research
possible.
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