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Original Paper
Abstract: The Rapateaceae is a small, mainly Neotropical fam-
ily of terrestrial or occasionally epiphytic herbs that grow on
mesic, nutrient-poor sites. Some recent studies suggest that
the Rapateaceae may be closely related to the Bromeliaceae,
one of the major families containing CAM plants. To investigate
the photosynthetic pathway in Rapateaceae, the plant carbon-
isotope ratio (d
13
C) was determined for samples from dried her-
barium specimens for 85 of the approximately 100 species in the
family. The d
13
C values ranged from ? 37.7 to ? 19.8 ?. Most Ra-
pateaceae showed d
13
C values typical of C
3
plants. However, six
species (Kunhardtia rhodantha Maguire, Marahuacaea schom-
burgkii (Maguire) Maguire, Saxofridericia compressa Maguire,
Stegolepis grandis Maguire, St. guianensis Klotzsch ex K?rn. and
St. squarrosa Maguire) showed d
13
C values less negative than
? 23 ?, i.e., at the higher end of the range for C
3
plants and at
the lower end of the distribution for plants exhibiting CAM. The
d
13
C values became significantly less negative with increasing
altitude (regression analysis indicating a change from about
? 30.7 ? at sea level to ? 22.5 ? at 2500 m). Although other
environmental factors and the type of tissue analysed may also
influence d
13
C values, these results suggest that some Rapatea-
ceae may be capable of performing CAM. Further studies, in-
cluding measurements of diel gas exchange patterns and leaf
organic-acid fluctuations, would be needed to demonstrate
CAM in Rapateaceae unequivocally, but living material of many
of these enigmatic plants is difficult to obtain.
Key words: Carbon-isotope ratio, photosynthetic pathway,
crassulacean acid metabolism, Rapateaceae, monocotyledons.
Abbreviation:
CAM: crassulacean acid metabolism
Introduction
The Rapateaceae Dumort. is a small family of monocotyledon-
ous herbs with a primarily Neotropical distribution (Fig.1 a).
The only genus occurring outside the Neotropics is the mono-
typic Maschalocephalus in West Africa (Smith, 1934
[40]
; Steven-
son et al., 1998
[41]
). No recent monograph exists for the family,
but it is estimated to comprise 17 genera and approximately
100 species (Givnish et al., 2000
[20]
). Rapateaceae are mostly
plants of moist, partly open habitats, often growing on sandy
infertile soils, although Rapatea spp. are forest understory
herbs, and a few other species grow epiphytically (Epidryos
spp.) or lithophytically (Stegolepis spp.). The family is particu-
larly well-represented in the meadows of the Venezuelan
Guayana, a region of southern Venezuela dominated by an ex-
tensive system of sheer-sided tabletop massifs (tepuis) formed
by the erosion and dissection of uplifted Roraima sandstone
(Huber, 1988
[25]
; Huber, 1995
[26]
). In this region, rapateads are
characteristic and often dominant floristic elements both in
lowland meadows (e.g., Schoenocephalium), which are charac-
terized by deep, sandy, acidic, poorly drained and extremely
nutrient-poor soils, and in the upland (e.g., Stegolepis) and
highland (tepui) meadows (Amphiphyllum, Kunhardtia, Mara-
huacaea, Phelpsiella, Stegolepis) (Huber, 1995
[26]
; L?ttge,
1997
[32]
; Michelangeli, 2000
[37]
). The early evolution of Rapa-
teaceae may have taken place in inundated areas followed by
diversification in lowland Amazonian savannas and elevated
wet savannas (meadows) on tepui summits, with subsequent
re-invasion of lowland habitats (Givnish et al., 2000
[20]
).
Rapateaceae have been commonly allied with Xyridaceae (e.g.,
Cronquist, 1981
[10]
; Dahlgren et al., 1985
[11]
), but links with
Commelinaceae (Venturelli and Bouman, 1988
[42]
) and Brome-
liaceae (Mez, 1896
[36]
; Smith, 1934
[40]
) have also been pro-
posed. An affinity with the latter family has found support in
molecular systematic studies based on the plastid gene rbcL,
which consistently place Rapateaceae near Bromeliaceae
within a commelinoid clade (Chase et al., 1993
[5]
, 1995
[6]
; Du-
vall et al., 1993
[13]
; see also Horres et al., 2000
[24]
). Recently, a
more detailed rbcL analysis resolved Rapateaceae as sister to a
clade comprising the Bromeliaceae and the small Neotropical
aquatic family Mayacaceae (see Fig.1 b; Givnish et al.,
1999
[19]
). However, this relationship was supported only weak-
ly, and a broader analysis incorporating data from one nuclear
(18S rDNA) and two plastid (atpB, rbcL) regions suggested an
alternative arrangement, with the Rapateaceae placed sister
to the remaining Poales, within which the Bromeliaceae and
the Mayacaceae are embedded and widely separated (Chase
et al., 2000
[7]
). This phylogenetic arrangement is also only
weakly supported.
Carbon-Isotope Ratios and Photosynthetic Pathways
in the Neotropical Family Rapateaceae
D. M. Crayn
1, 3
, J. A. C. Smith
2
, and K. Winter
1
1
Smithsonian Tropical Research Institute, P.O. Box 2072, Balboa, Ancon, Republic of Panama
2
Department of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1 3RB, United Kingdom
3
Present address: School of Biological Science, University of New South Wales, UNSW, NSW 2052, Australia
Received: September 9, 2000; Accepted: May 8, 2001
Plant biol. 3 (2001) 569 ? 576
 Georg Thieme Verlag Stuttgart ? New York
ISSN 1435-8603
569
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We are currently conducting a survey of the large Neotropical
family Bromeliaceae using the plant tissue carbon-isotope ratio
(d
13
C) to determine the taxonomic distribution of photosyn-
thetic pathways (crassulacean acid metabolism [CAM] and C
3
).
If future work confirms the possible sister relationship of Rapa-
teaceae and Bromeliaceae (Givnish et al., 1999
[19]
), knowledge
of the photosynthetic pathway in the former would be of great
interest for two reasons: (1) their phylogenetic proximity to the
Bromeliaceae (one of the major families containing CAM
plants) would raise the possibility of CAM being present in
rapateads, some of which are remarkably similar in life form to
certain CAM bromeliads; and (2) knowledge of the photosyn-
thetic pathway in Rapateaceae may aid in determining the an-
cestral photosynthetic pathway for the Bromeliaceae by map-
ping the character states ?CAM? and ?C
3
? onto cladograms un-
der the parsimony criterion. To our knowledge, the photosyn-
thetic pathway has not been determined for any Rapateaceae.
The relative abundance (measured in parts per thousand, ?)
of the stable carbon isotopes
12
C and
13
C in plant tissue (d
13
C
value) has been used extensively as an index of the relative
contribution of CAM to photosynthetic carbon gain (e.g., Os-
mond et al., 1973
[39]
; Griffiths and Smith, 1983
[21]
; Winter et
al., 1983
[45]
; Winter and Smith, 1996
[44]
). In the CAM and C
4
pathways, the primary CO
2
-fixing enzyme is phosphoenol-
pyruvate (PEP) carboxylase, which discriminates less strongly
against the heavier isotope,
13
C, than does ribulose-1,5-bisphos-
phate carboxylase-oxygenase (Rubisco), the primary CO
2
-fix-
ing enzyme in C
3
plants. C
3
plants typically show d
13
C values
in the range ? 35? to ? 23 ?, and CAM plants typically show
d
13
C values in the range ? 19 ? to ? 10? (Osmond et al.,
1973
[39]
; Griffiths and Smith, 1983
[21]
; Winter et al., 1983
[45]
).
In the present work, we have investigated photosynthetic
pathways within Rapateaceae by determining the d
13
C values
for herbarium material of 85 out of the approximately 100 spe-
cies in the family. The significance of these values is discussed
in terms of the ecological characteristics of the species in this
relatively little-studied group of monocotyledons.
Materials and Methods
Samples of dried tissue of species of Rapateaceae were col-
lected from various herbaria (Missouri Botanical Garden, St.
Louis, Missouri, USA; Marie Selby Botanical Gardens, Sarasota,
Florida, USA; US National Herbarium, Smithsonian Institution,
Washington, DC, USA) during 1998 and 1999. Where available,
samples were taken from the leaf lamina. However, some spe-
cies are represented by one or very few (and hence valuable)
collections. Therefore, in some cases samples were taken from
a less taxonomically important part of the specimen, such as
the leaf base or the inflorescence axis. Collection information
was recorded where available from the herbarium sheets and
ecological information from the sheets or from field knowl-
edge (P. Berry, personal communication).
Natural abundance of
12
C and
13
C was measured for each sam-
ple at the Duke University Phytotron (Durham, North Carolina,
USA) using a SIRA Series II isotope ratio mass spectrometer
(Micromass, Manchester, UK) operated in automatic trapping
mode after combustion under oxygen (DUMAS combustion)
of samples (about 5 mg) in an elemental analyser (NA 1500
Series 1, Carlo Erba Instrumentazione, Milan, Italy). The refer-
ence CO
2
, calibrated against standard Pee Dee belemnite, was
obtained from Oztech (Dallas, Texas, USA). A system check of
analysis of combustion and mass spectrometer measurement
was performed after every ten samples. This was achieved
with two working standards of cellulose (Sigma, St. Louis, Mis-
souri, USA), which had d
13
C values of ? 24.10  0.03 ? and
? 23.55  0.06?, respectively. The
12
C and
13
C values were cor-
rected for oxygen isotope contribution using the measured
d
18
O and the method of Craig (1957
[9]
). The d
13
C value was de-
termined from the following formula:
where PDB refers to Pee Dee belemnite.
Fig. 1 a Approximate geographical distribution of Rapateaceae (after
P. Berry, personal communication).
Fig. 1 b A summary of possible relationship of Rapateaceae based on
cladistic analyses of nucleotide sequence data (Chase et al., 1995
[6]
;
Givnish et al., 1999
[19]
; Chase et al., 2000
[7]
). Relationship denoted by
dotted lines lack strong character support and should be considered
tentative.
13
C
sample
/
12
C
sample
d
13
C (?) =
"
? 1
#
? 1000
13
C
PDB
/
12
C
PDB
Plant biol. 3 (2001) D. M. Crayn, J. A. C. Smith, and K. Winter570
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Results
A total of 91 samples was collected and analysed, representing
16 genera and 85 species of Rapateaceae; Duckea cyperaceoi-
dea, D. flava, D. junciformis, D. squarrosa and Rapatea longipes
were each sampled more than once. This represents 85 % of
species in the family based on a current estimate of 100 spe-
cies (Givnish et al., 2000
[20]
). Only one genus, the monotypic
Phelpsiella Maguire, was not sampled.
The d
13
C values for all 91 samples are listed in Table 1. They
ranged from ? 37.7 ? for both Rapatea paludosa and Saxofri-
dericia subcordata to ? 19.8? for Saxofridericia compressa. Five
species were represented by samples obtained from more than
one collection. The d
13
C values for different samples for one
of these, Duckea cyperaceoidea, were very similar (? 28.2 ?,
? 28.2 ?, ? 29.1 ?). The difference between values obtained
for the replicate samples of four other species was somewhat
greater: Rapatea longipes, 1.5 ?; Duckea flava, 1.9 ?; D. junci-
formis, 1.9 ?; D. squarrosa, 4.0 ?. The d
13
C values for the 85
species sampled were approximately normally distributed,
with a mean and standard deviation of ? 28.5 ? and 4.1 ?,
respectively (Fig. 2). Where more than one sample was ana-
lysed for a species, the mean d
13
C value of the replicates was
used.
The great majority of samples analysed showed d
13
C values
characteristic of C
3
plants. Six species (Kunhardtia rhodantha,
Marahuacaea schomburgkii, Saxofridericia compressa, Stegole-
pis grandis, St. guianensis, St. squarrosa), however, showed
d
13
C values ranging from ? 23.0 ? to ? 19.8 ?, which are less
negative than the values typically observed for C
3
plants, but
are intermediate between those typically observed for C
3
plants and those of plants with pronounced CAM. Although
many Rapateaceae occur at low altitudes, all of the plants that
showed d
13
C values less negative than ? 23 ? were collected at
altitudes above 1200 m (Table 1).
Other species showed d
13
C values that are unusually low for C
3
plants. For example, Rapatea paludosa and Saxofridericia sub-
cordata showed d
13
C values of ? 37.7?. A further 14 species
showed d
13
C values more negative than ? 32 ? (Table 1).
The d
13
C values were plotted against altitude for the 73 sam-
ples for which altitudinal data were available. Where an alti-
tudinal range was recorded, the median value was used. The
linear regression indicates a highly significant correlation
(r
2
= 0.420, p < 0.001), with specimens showing less negative
d
13
C values with increasing altitude (Fig. 3). The fitted linear
regression suggested that the d
13
C value increased by 8.2 ?
from ? 30.7 to ? 22.5 ? over an altitudinal range from sea level
to 2500 m, or by an average of 3.3 ? per 1000 m.
Discussion
Based on the d
13
C values obtained in this study, it appears that
most, if not all, Rapateaceae are C
3
plants. Six of the 85 species
studied, however, showed d
13
C values between ? 23.0 ? and
? 19.8 ? (Table 1), which is less negative than the great major-
ity of values recorded for C
3
plants. For example, K?rner et al.
(1988
[31]
) sampled 100 C
3
species from a diverse range of alti-
tudes, habitats and taxonomic groups, and the least negative
d
13
C value recorded was ? 22.7 ?. CAM plants usually show
d
13
C values less negative than ? 19.0?, although there are
some notable exceptions. For example, the confirmed CAM
plants Tillandsia usneoides (L.) L. (Bromeliaceae), Didierea ma-
dagascariensis Baill. (Didiereaceae) and Microsorum puncta-
tum (L.) Copel. (Polypodiaceae) show d
13
C values of ? 19.8 ?
(Griffiths and Smith, 1983
[21]
), ? 21.2 ? (Winter, 1979
[43]
) and
? 22.6 ? (Holtum and Winter, 1999
[23]
), respectively. Thus, the
discovery of d
13
C values less negative than ? 23.0? in Rapatea-
ceae raises the interesting possibility of CAM in this family of
mostly terrestrial mesophytes. These species are unlikely to be
C
4
plants: Kranz anatomy is not known to occur in Rapateaceae
(Carlquist, 1969
[3]
), and these specimens show d
13
C values that
are much more negative than those usually exhibited by C
4
plants (i.e., ? 10 to ? 14 ?; Cerling, 1999
[4]
).
Factors other than photosynthetic pathway that may affect
d
13
C values in plants include altitude, drought stress, relative
humidity, salinity, tissue type and the isotope composition of
the source CO
2
. Previous work has demonstrated a trend to-
ward less negative d
13
C values with increasing altitude in C
3
plants (K?rner et al., 1988
[31]
; Marshall and Zhang, 1993
[34]
;
Cordell et al., 1999
[8]
) associated with lower intercellular CO
2
concentrations. K?rner et al. (1988
[31]
), in their study of 100
species of C
3
plants, found that the mean d
13
C value differed
by 4 ? over an altitudinal range of 5600 m. Within a species,
the difference may be as great as 6? over a range of 2500 m
(Metrosideros polymorpha Gaudich.; Cordell et al., 1999
[8]
).
Our data show a difference of 8.2 ? over a range of 2500 m
according to the linear regression analysis (Fig. 3), one of the
steepest relationships yet reported.
Increasing salinity and drought stress may also lead to less
negative d
13
C values in C
3
plants due to decreased stomatal
conductance and hence increased diffusional limitation of
CO
2
uptake. For example, in the C
3
mangrove Avicennia marina
(Forssk.) Vierh. var. australasica (Walp.) Moldenke, d
13
C values
as high as ? 19.6 ? (with a range of 4.4?) have been reported
(Farquhar et al., 1982
[15]
). However, Rapateaceae are very un-
likely to suffer salt stress in their natural environments. None-
theless, although most Rapateaceae, including those that show
the highest d
13
C values, grow in generally mesic sites, (Ma-
guire, 1982
[33]
), they may experience drought stress during
the dry season (January to March; P. Berry, personal communi-
cation).
The determinations for Saxofridericia compressa (? 19.8 ?) and
Stegolepis grandis (? 21.4 ?) were made on sclerenchyma from
the inflorescence axis, whereas most other determinations
were made on leaf lamina tissue. Tissues that are lipid-rich,
such as those comprised mainly of living cells, are relatively
depleted in
13
C and may therefore show more negative d
13
C
values, whereas tissues composed largely of dead cells, such
as sclerenchyma, may show less negative d
13
C values (Ziegler,
1996
[46]
). However, Winter (1979
[43]
) found little variation in
the d
13
C value between sclerenchymatous and non-scleren-
chymatous organs in CAM plants from Madagascar.
The d
13
C value is dependent on the isotope composition of the
source CO
2
(Farquhar et al., 1989
[16]
), which, in the case of at-
mospheric CO
2
, may vary geographically and chronologically
(Keeling, 1958
[27]
, 1961
[28]
; Keeling et al., 1979
[29]
, 1989
[30]
). For
example, over the period 1956 to 1982, the atmospheric
13
C
composition decreased from ? 6.7 ? (at 314 ppm) to ? 7.9 ?
Photosynthetic Pathways in Rapateaceae Plant biol. 3 (2001) 571
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Table 1 List of carbon-isotope ratios for species of Rapateaceae, together with information on the source of the material and ecology of the
species
Taxon Collector and herbarium
a
Date
b
Altitude
b
(m)
Life
form
c
Mate-
rial
d
d
13
C
(?)
Amphiphyllum
A. rigidum Gleason O. Huber 13225 (MO) 1 520 T* I.I. ? 25.7
Cephalostemon
C. affinis K?rn. B. Maguire 36606 (US) 20. 11. 1953 125 T I.I. ? 28.4
C. angustatus Malme H. Irwin et al. 13859 (US) 9. 3. 1966 1 200 T I.I. ? 27.5
C. gracilis (Poepp. and Endl.) R. H.
Schomb.
S. Hill et al. 12978 (US) 7. 7. 1983 T I.I. ? 27.7
C. microglochin Sandwith O. Huber 4620 (US) 10. 10. 1979 600 T I.I. ? 29.2
C. riedelianus K?rn. W. Anderson et al. 36230 (US) 18. 2. 1972 1 125 T I.I. ? 26.3
Duckea
D. cyperaceoidea (Ducke) Maguire B. Maguire 37573 (US) 7. 2. 1954 110 T I.I. ? 28.2
D. cyperaceoidea (Ducke) Maguire P. Berry and E. Melgueiro 5386 (SEL) 10. 11. 1992 100 T I.I. ? 29.1
D. cyperaceoidea (Ducke) Maguire P. Berry 6269 et al. (MO) 26. 5. 1996 110 T I.b. ? 28.2
D. flava (Link) Maguire G. Davidse 17346 (US) 8. 5. 1979 120 T I.I. ? 29.1
D. flava (Link) Maguire B. Stergios 16365 (US) 9. 11. 1994 T* I.I. ? 31.0
D. junciformis Maguire B. Maguire et al. 41866 (US) 130 T I.I. ? 26.6
D. junciformis Maguire P. Berry and I. Sanchez 5052 (US) 3. 7. 1991 125 T I.I. ? 28.5
D. squarrosa (Willd. ex Link) Maguire G. Davidse et al. 17200 (US) 6. 5. 1979 T I.I. ? 29.7
D. squarrosa (Willd. ex Link) Maguire P. Berry 6131 et al. (MO) 9. 3. 1996 110 T I.I. ? 33.7
Epidryos
E. guayanensis Maguire T. Henkel et al. 4296 (US) 11. 11. 1993 1 150 ? 1 200 E I.I. ? 25.6
E. micrantherus (Maguire) Maguire A. Gentry 65549 et al. (MO) 7. 2. 1989 50 E I.I. ? 31.0
Guacamaya
G. superba Maguire B. Maguire and J. Wurdack 35619 (US) 14. 4. 1953 140 T* I.I. ? 27.7
Kunhardtia
K. radiata Maguire and Steyerm. A. Gentry and P. Berry 14551 (MO) 29. 6. 1975 150 T I.I. ? 28.9
K. rhodantha Maguire Steyermark 105114 (US) 20. ? 22. 9. 1971 1 230 ? 1 240 T I.b. ? 21.9
Marahuacaea
M. schomburgkii (Maguire) Maguire Steyermark et al. 126019 (US) 2. 2. 1982 2 480 ? 2 500 T* I.I. ? 22.6
Maschalocephalus
M. dinklagei Gilg and K. Schum. J. Baldwin Jr. 11364 (MO) 11. 3. 1948 T* I.I. ? 37.3
Monotrema
M. aemulans K?rn. M. Jansen-Jacobs et al. 1429 (US) 3. 9. 1989 240 ? 260 T I.t. ? 28.2
M. affine Maguire B. Maguire et al. 41500 (US) 9/1957 125 T I.t. ? 26.0
M. arthrophyllum (Seub.) Maguire R. Schultes and I. Cabrera s.n. (US) 274 ? 305 T I.I. ? 28.4
M. bracteatum Maguire B. Maguire et al. 36605 (US) 11/1953 150 T I.I. ? 29.9
M. xyridoides Gleason G. Prance et al. 28884 (US) 7. 2. 1984 T I.I. ? 29.7
Potarophytum
P. riparium Sandwith J. Pipoly 9999 (US) 26. 1. 1987 400 T I.I. ? 31.2
Rapatea
R. angustifolia Spruce ex K?rn. B. Maguire et al. 36646 (US) 120 T I.I. ? 31.9
R. aracamuniana Steyerm. R. Liesner and F. Delascio 22197 (MO) 20. 10. 1987 600 T* I.I. ? 30.6
R. chimantensis Steyerm. J. Steyermark 75584 (MO) 5/1953 1 000 T* I.I. ? 33.5
R. circasiana Garc?a-Barr. and Mora J. Zarucchi and M. Balick 1807 (US) 1. 7. 1976 T* I.I. ? 33.8
R. elongata G. K. Schulze B. Maguire et al. 56536 (US) 3. 9. 1963 T I.I. ? 34.2
R. fanshawei Maguire J. Pipoly 7645 (US) 12. 6. 1986 550 T I.I. ? 31.8
R. linearis Gleason J. Pipoly 9513 (US) 21. 12. 1986 25 T I.I. ? 27.6
R. longipes Spruce ex K?rn. C. Berg et al. 19498 (US) 13. 11. 1993 T I.I. ? 35.5
R. longipes Spruce ex K?rn. R. Schultes and I. Cabrera 17500 (US) 18. 9. 1952 T I.I. ? 34.0
R. membranacea Maguire S. Tillet et al. 43972 (US) 3. 7. 1960 1 140 T I.b. ? 28.6
R. muaju Garc?a-Barr. and Mora R. Schultes and I. Cabrera 16621 (US) 5. 6. 1952 213 T I.I. ? 34.8
R. paludosa Aubl. B. Hoffman 1412 (US) 22. 4. 1992 60 ? 70 T I.I. ? 37.7
R. pycnocephala Seub. G. Prance et al. 24960 (US) 6. 11. 1977 T* I.I. ? 30.1
R. sa?lensis B. M. Boom T. Croat 74180 (MO) 10. 2. 1993 350 T I.I. ? 34.3
R. spectabilis Pilg. W. Anderson 11830 (US) 24. 1. 1978 T I.I. ? 34.7
continued next page
Plant biol. 3 (2001) D. M. Crayn, J. A. C. Smith, and K. Winter572
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Table 1 continued
Taxon Collector and herbarium
a
Date
b
Altitude
b
(m)
Life
form
c
Mate-
rial
d
d
13
C
(?)
R. spruceana K?rn. G. Davidse et al. 16887 (US) 30. 4. ? 1. 5. 1979 100 T I.I. ? 28.8
R. steyermarkii Maguire T. McDowell 2812 (US) 24. 5. 1990 900 ? 975 T* I.I. ? 35.1
R. ulei Pilg. T. McDowell 3934 and A. Stobey (MO) 396 T I.I. ? 32.2
R. undulata Ducke G. Prance et al. 23867 (US) 17. 10. 1976 T* I.I. ? 37.5
R. wettsteinii Suess. vel. sp. aff. J. Zarucchi 1970 (MO) 7. 9. 1976 T I.I. ? 30.3
R. xiphoides Sandwith L. Kvist et al. 110A (US) 7. 10. 1987 550 T* I.I. ? 32.9
R. yapacana Maguire R. Kral and O. Huber 70715 (MO) 10. 8. 1983 100 T* I.b. ? 29.3
Saxofridericia
S. aculeata K?rn. G. Prance et al. 4982 (US) 5. 6. 1968 T* I.b. ? 31.1
S. compressa Maguire T. Croat 59543 (US) 1. 12. 1984 2 200 T i.a. ? 19.8
S. duidae Maguire Steyermark et al. 126416 (US) 10. 2. 1982 1 230 T* I.I. ? 25.4
S. grandis Maguire O. Huber 4347 (US) 4. 10. 1979 1 100 T* I.I. ? 29.7
S. inermis Ducke B. Maguire et al. 42624 (US) 11. 1. 1958 110 T I.I. ? 30.1
S. regalis R. H. Schomb. W. Hahn et al. 4491 (US) 13. 4. 1988 500 T i.a. ? 24.7
S. spongiosa Maguire B. Maguire 42621 (US) 10. 1. 1958 150 ? 200 T I.I. ? 25.3
S. subcordata K?rn. W. Kress et al. 94-3635 (US) 50 T I.I. ? 37.7
Schoenocephalium
S. cucullatum Maguire C. Calderon 2747 (US) 2. 7. 1979 T I.I. ? 26.1
S. martianum Seub. A. Gentry and M. Sanchez 65169 (MO) 25. 1. 1989 250 T I.b. ? 28.3
S. schultesii Maguire R. Schultes and I. Cabrera 14506 (MO) 29. 10. 1951 T* I.I. ? 31.2
S. teretifolium Maguire O. Huber and E. Medina 5854 (US) 8. 2. 1981 125 T I.I. ? 29.4
Spathanthus
S. bicolor Ducke G. Davidse et al. 17440 (US) 8. 5. 1979 120 T I.I. ? 25.0
S. unilateralis (Rudge) Desv. P. Mutchnik 738 (US) 14. 2. 1995 50 T* I.I. ? 36.1
Stegolepis
S. albiflora Steyerm. O. Huber 13019 (MO) 1 750 ? 1 800 T I.I. ? 25.2
S. angustata Gleason L. Gillespie and H. Persaud 900 (US) 29. 3. 1989 450 T I.b. ? 25.8
S. cardonae Maguire O. Huber and M. Colella 8929 (US) 10. ? 12. 2. 1984 2 250 L I.b. ? 23.4
S. celiae Maguire G. Davidse and J. Miller 27365 (US) 9. 7. 1984 400 ? 700 L I.I. ? 27.6
S. choripetala Maguire O. Huber 12724 (US) 28. 3. 1988 T I.I. ? 25.6
S. ferruginea Baker S. Tillet et al. 43943 (US) 3. 7. 1960 824 E I.I. ? 30.0
S. grandis Maguire Steyermark et al. 109303 (US) 22. 2. 1974 1 750 ? 1 800 T* i.a. ? 21.4
S. guianensis Klotzsch ex K?rn. B. Hoffman and T. Henkel 3217 (US) 3. 11. 1992 1 800 ? 2 000 T I.I. ? 22.3
S. hitchcockii Maguire R. Cowan and J. Wurdack 31194 (US) 2. 2. 1951 2 000 T I.b. ? 24.7
S. huberi Steyerm. O. Huber 9224 (MO) 1 200 T I.b. ? 27.3
S. humilis Steyerm. R. Liesner 21075 et al. (MO) 26. 5. 1986 2 135 T* I.b. ? 24.3
S. jauaensis Maguire Steyermark et al. 109249 (US) 2 ? 3/1974 1 800 T* i.a. ? 23.6
S. ligulata Maguire J. Luteyn et al. 9480 (US) 14. 2. 1984 1 920 T I.b. ? 23.4
S. linearis Gleason S. Tillet et al. 751-75 (US) 1 ? 2/1975 1 350 L I.b. ? 24.6
S. maguireana Steyerm. O. Huber 12468 (US) 28. 1. 1988 2 150 T I.I. ? 23.0
S. membranacea Maguire G. Prance and J. Guedes 29545 (US) 15. 7. 1985 800 ? 900 L I.I. ? 28.3
S. microcephala Maguire O. Huber 13053 (MO) 1 750 ? 1 800 T* I.I. ? 26.8
S. neblinensis Maguire B. Boom and A. Weitzman 5776 (US) 12. 2. 1985 1 670 ? 1 690 T I.b. ? 24.3
S. parvipetala Steyerm. Steyermark et al. 132044 (US) 22. ? 24. 5. 1986 1 800 ? 1 825 T* I.b. ? 27.0
S. pauciflora Gleason Steyermark 58330 (US) 4. 9. 1944 1 820 ? 2 075 T* I.I. ? 24.2
S. ptaritepuiensis Steyerm. L. Gillespie and D. Smart 2782 (US) 19. 12. 1989 550 T I.b. ? 25.6
S. pulchella Maguire B. Maguire et al. 31744 (US) 2. 2. 1951 1 800 L I.b. ? 24.3
S. pungens Gleason B. Maguire 29669 (US) 23. 11. 1950 2 000 ? 2 300 T I.I. ? 27.2
S. squarrosa Maguire O. Huber 10395 (US) 27. 3. 1985 1 400 T* I.b. ? 22.5
S. steyermarkii Maguire T. Henkel et al. 1533 (US) 20. 2. 1993 1 530 T (E)* I.I. ? 27.2
S. wurdackii Maguire J. Steyermark 75463 (MO) 16. 5. 1953 1 000 ? 1 700 T* I.I. ? 24.9
Windsorina
W. guianensis Gleason B. Maguire 32143 (MO) 17. 10. 1951 T I.I. ? 31.2
a
Herbaria are denoted by their acronyms (Holmgren et al., 1990
[22]
): MO: Mis-
souri Botanical Garden, St. Louis, Missouri, USA; SEL: Herbarium, Marie Selby
Botanical Gardens, Sarasota, Florida, USA; US: United States National Herbar-
ium, Smithsonian Institution, Washington, DC, USA.
b
Refers to the date and the altitude at which the herbarium specimen was
collected. Blank cells indicate the information was not available.
c
The herbarium specimens were obtained from plants growing terrestrially (T),
epiphytically (E), or lithophytically (L). This information was obtained from the
specimen label or where the habit is marked with an asterisk, from published
treatments (Maguire, 1982
[33]
) and field knowledge (P. Berry, personal com-
munication).
d
The material analysed was taken from either: leaf base (l.b.), leaf lamina (l.l.),
leaf tip (l.t.), or the inflorescence axis (i.a.).
Photosynthetic Pathways in Rapateaceae Plant biol. 3 (2001) 573
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(at 342 ppm) (Keeling et al., 1979
[29]
; Mook et al., 1983
[38]
) due
to anthropogenic fossil fuel emissions. As a result, plants col-
lected many years ago may contain relatively more
13
C (and
hence show less negative d
13
C values) compared with those
collected more recently. The specimens sampled in this study
were collected between the years 1944 and 1996, whereas the
six species identified as showing CAM-like d
13
C values were
collected between the years 1971 and 1992. Thus, it is unlikely
that chronological variation in atmospheric carbon isotope
composition can account for the relatively high d
13
C values in
these species.
Of interest is the observation that the rapateads with the least
negative d
13
C values (Kunhardtia rhodantha, Marahuacaea
schomburgkii, Saxofridericia compressa, Stegolepis grandis, St.
guianensis, St. squarrosa), indicating the possibility of CAM,
were all plants growing at middle to high altitudes (Table 1).
While CAM plants are certainly known from high altitudes
(e.g., cacti in the Andes of Chile and Peru; Gibson and Nobel,
1986
[18]
), field studies have shown that the occurrence of CAM
tends to decrease with altitude. In Papua New Guinea, CAM
epiphytes are absent from the highest altitudes (Earnshaw et
al., 1987
[14]
), and in northern Venezuela Clusia L. species do
not perform CAM above about 1500 m (Diaz et al., 1996
[12]
).
The discovery of the restriction of CAM to relatively high alti-
tudes in a family of mesophytes would be of great interest. It
should be noted, however, that these rapateads conform to
the altitudinal trend in d
13
C values discussed above (Fig. 3),
and thus perhaps more likely represent values towards the
upper limit of those occurring in C
3
plants.
Most Rapateaceae grow in mesic conditions in which CAM
would seem to confer little or no ecological advantage. Some
species grow epiphytically (Epidryos spp.) or lithophytically
(Stegolepis spp.), but in habitats where the water supply is at
least seasonally plentiful, such as cloud forests or seepage or
splash zones. In these conditions, it is not expected that there
would be strong selection for improved water economy and
indeed, these species show d
13
C values typical of C
3
plants
(Table 1).
Although d
13
C values can provide unequivocal evidence for the
presence of the CAM pathway, the converse is not necessarily
true: some taxa that can perform CAM under natural condi-
tions show d
13
C values in the range typical of C
3
plants. Grif-
fiths and Smith (1983
[21]
) detected significant nocturnal in-
creases in titratable acidity in two species of Bromeliaceae in
Trinidad, Tillandsia elongata Kunth var. subimbricata (Baker) L.
B. Sm. and Guzmania monostachia (L.) Rusby ex Mez var. mono-
stachia, that had leaf d
13
C values of ? 26.4 ? and ? 26.5 ?,
respectively. Therefore it is possible that other Rapateaceae
with d
13
C values more negative than ? 23.0? might be capable
of performing CAM, but the identification of such plants would
require systematic investigation of living material and is be-
yond the scope of this study. Future work to identify such spe-
cies should perhaps initially be focused on the taxa most close-
ly related to those reported herein to show CAM-like carbon
isotope ratios.
A recent molecular phylogeny of Rapateaceae (Givnish et al.,
2000
[20]
) resolved species of Kunhardtia and Saxofridericia
within a derived clade that was sister to a clade containing, in-
ter alia, species of Marahuacaea and Stegolepis. This suggests
that CAM, if confirmed in those species with the least negative
d
13
C values (viz. Kunhardtia rhodantha, Marahuacaea schom-
burgkii, Saxofridericia compressa, Stegolepis grandis, St. guia-
nensis, St. squarrosa), is a derived condition in Rapateaceae,
and may have arisen more than once in the family. However,
the relationships suggested by the molecular analysis need to
be corroborated by further analyses with other data and more
complete taxon sampling.
Very negative d
13
C values have been reported for plants grow-
ing in moist, shaded conditions (Flanagan et al., 1997
[17]
), in
which high intercellular CO
2
concentrations during photosyn-
thetic CO
2
uptake allow increased isotope discrimination by
Rubisco. However, more negative plant d
13
C values can also
result from
13
C-depleted source air, as can occur in the under-
story of forests (Medina and Minchin, 1980
[35]
; Broadmeadow
and Griffiths, 1993
[1]
; Buchmann et al., 1998
[2]
). The rapateads
with the most negative d
13
C values (e.g., Rapatea paludosa and
Fig. 2 Frequency histogram of d
13
C values of 85 species of Rapatea-
ceae in class intervals of 1.0 ?. For those species for which more
than one sample was analysed, the mean d
13
C value of the replicates
was used.
Fig. 3 Linear regression of d
13
C value against altitude for 73 sam-
ples of Rapateaceae (y = 0.00330 x ? 30.7, r
2
= 0.420, p < 0.001).
Plant biol. 3 (2001) D. M. Crayn, J. A. C. Smith, and K. Winter574
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Saxofridericia subcordata) are generally restricted to wet or
seasonally inundated forest understories (P. Berry, personal
communication) at the low end of the altitudinal range for
the family, where the combination of
13
C-depleted source air
and shady, mesic conditions may have resulted in some of the
most negative d
13
C values yet reported for terrestrial plants
growing under natural conditions (K?rner et al., 1988
[31]
; Far-
quhar et al., 1989
[16]
; Flanagan et al., 1997
[17]
).
This study is consistent with previous work demonstrating a
general increase in d
13
C of plant tissue with increasing altitude
(K?rner et al., 1988
[31]
; Marshall and Zhang, 1993
[34]
; Cordell et
al., 1999
[8]
), but the possibility that CAM may contribute to car-
bon gain in some Rapateaceae cannot be excluded. This needs
to be followed up by studies of day-night gas exchange pat-
terns and tissue organic-acid fluctuations in this family. How-
ever, most Rapateaceae grow in the relatively inaccessible
Guayana Shield and we know of very few species in cultiva-
tion. Even if further investigations confirmed CAM in those
Rapateaceae showing high d
13
C values, this pathway would
still constitute a relatively minor evolutionary theme in this
family. However, it would be of considerable interest since to
date CAM has not been detected in Rapateaceae.
Acknowledgements
We thank the Directors of Marie Selby Botanical Gardens, US
National Herbarium and Missouri Botanical Garden for access
to herbarium collections and Larry Giles (Duke University,
Durham, North Carolina, USA) for sample analysis. The taxo-
nomic and ecological information and comments on the
manuscript provided by Paul Berry (University of Wisconsin,
Madison, Wisconsin, USA) are gratefully acknowledged. This
research was supported by awards from the Andrew W. Mellon
Foundation through the Smithsonian Institution to J. A. C. S.
and K. W.
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K. Winter
Smithsonian Tropical Research Institute
Unit 0948
APO AA 34002-0948
U.S.A.
E-mail: winterk@tivoli.si.edu
Section Editor: C. B. Osmond
Plant biol. 3 (2001) D. M. Crayn, J. A. C. Smith, and K. Winter576