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Journal of the Torrey Botanical Society 127(4), 2000, pp. 291-299
Population dynamics of Ceratozamia matudai Lundell
(Zamiaceae) in el Triunfo Biosphere Reserve,
Chiapas, Mexico1
Miguel Angel Perez Farrera, Pedro F. Quintana-Ascencio,
and Benito Salvatierra Izaba
El Colegio de la Frontera Sur, Apartado Postal 63, San Crist6bal de la Casas, 29200, Chiapas, M6xico,
Andrew P. Vovides
Apartado Postal 63, lnstituto de Ecologfa, 91000, Xalapa, Veracruz, Mexico.
PEREZ-FARRERA
M.
A., P. F: QUINTANA-AscENCIO,
E. B. SALVATIERRA lzABA
(Colegio
de la Froniera
Sur, Apartado
Postal63,San Crist6bal de la Casas, 29200, ClIiapas, Mexico) AND ANDREWP. VOVIDES (Apartado Postal 63, Instituto
de Ecologfa, 91000, Xalapa, Veracruz, Mexico). Population dynamics of Ceratozamia matudai Lundell (Zarnaceae)
in el Triunfo Biosphere Reserve, Chiapas, Mexico. J. Torrey Bot. Soc. 127:291-299. 2000.-We describe Ceratozamia
matudai geographic distribution, its basic demographic parameiers, and the association of these parameiers with
environmental factors. A species survey and a review of herbarium collections indicaled that C. matudai occurs only
on the pacific slopes of the Sierra Madre of Chiapas, Mexico. ~o censuses (1998-1999) were performed in a PineCupressus forest in the core zone of the Triunfo Biosphere Reserve, and a Montane Rain Forest in its buffer zone.
Neighboring floristic composition, soil depth, and slope around marked and mapped C. matudai individuals in each
sire were described. This species showed a clumped local distribution on shallow soils on steep slopes. Individuals
showed differences in amount of leaf production, trunk diameier, and height between sires. Neighboring species
composition affecled seedling mortality. Because of its low numbers and limiled range we recommend a status change
in its IUCN caiegory to endangered. As with other cycads, C. matudai can reach high market values. Ex-situ propagation of this and other species may provide incentives among local peasants for conservation of the natural populations and its habitat.
Key words:
Cycad, Ceratozamia
matudai, population
dynamics,
persistence, endangered species.
!.,
Cycads are a long-lived group of plants considered ancient and primitive (Crane 1988; Eckenwalder 1980a). About 240 species have been
reported worldwide (Osborne et al. 1999). In
Mexico there are over 40 speciesof cycads, making Mexico second world wide in cycad diversity
(Vovides, in press). Among these species80% are
endemic to this country (Vovides & Iglesias
1994) and 40% restricted to the southern state of
Chiapas. In Chiapas most cycads inh~bit tropical
1The research was supported by Fauna and Flora
lnternacional (96/64/15; MAPF), Fondo Mexicano
para la Conservacion de la Naturaleza (B2-134;
MAPF), U.S. Fish and Wildlife Service (G99-350;
MAPF), MAB- Tropical Ecosystem Directorate (sin;
MAPF), CONACYT to APV (1837P-N9507 and
29379N) and a fellowship to MAPF (114869) from El
Colegio de la Frontera Sur. We thank Alejandro Hernandez Yanez and the staff at The Triunfo Biosphere
Reserve, lnstituto Nacional de Ecologia. T. Milledge,
J. De La Cruz Rodriguez, M. Evangelina L6pez Molina, R. Hernandez Jonapa, J. Zaragoza, C. O'Brien,
R. Ornduff, N. Ramirez Marcial and D. B. Clark provided invaluable help.
2 Current address: Escuela de Biologia, Universidad
de Ciencias y Artes del Estado de Chiapas, Calzada
Samuel Le6n Brindis 151, Thxtla Guti~rrez, Chiapas,
Mexico, 29000.
Received for publication July 26, 1999, and in revised form July 20, 2000.
rain forests and montane cloud forests where they
are threatened due to habitat deterioration, and
current expansion of agricultural fields and coffee
plantations. Even populations in protected areas
are disappearing becauseof escapedfires and illegal harvesting (Vovides 1990). Ceratozamia
matudai Lundell is an endemic cycad of the Sierra Madre of Chiapas. Its conservation status is
considered to be vulnerable according to International Union for the Conservation of Nature
(Vovides et al. 1997a,Osborne 1995) and the species is protected by Mexican law (Diario Oficial
de la Federaci6n 1994). Remnant populations of
this ~ies
are threateneddue to the replacement
of forest by coffee plantations in the Soconusco
region (Schutzman et al. 1988).
Few studies have reported population parameters of cycads. Population studies of cycads
have described some aspects of their life cycle,
phenology, pollination and seed dispersal (Clark
et al. 1992; Norstog et al. 1992; Vovides 1991a;
Tang 1988). Negron & Breckon (1989) and Vovides (1990) described the population structure of
Zamia debilis L.f. ex Aiton and Dioon edule
Lindl. respectively. They found survivorship reverse "J" or Deevey type III curves associated
with high seedling mortality. The study of Alejandre et al. (1990) of Ceratozamia mexicana
291
292
JOURNAL OF THE TORREY BOTANICAL
Brongn.:described the effect of moisture and forest stand conditions on the survival of this species. They observed a positive association between cycad number, mostly seedlings and juveniles, and tree density.
The knowledge of the life history and the influence of physical and biological factors on population growth of endangeredtaxa provide valuable information for their management and conservation (Shemske et al. 1994; Donalson 1995;
Menges 1986; Henifin et al. 1981). The goals of
this study were: (1) to describe Ceratozamia matudai distribution along the Sierra Madre, Chiapas; (2) to describe its demographic characteristics, such as local spatial distribution, and structure in two populations in El lliunfo Biosphere
Reserve, Chiapas, Mexico; (3) to contrast population dynamics of C. matudai in an area without
noticeable disturbance in a forest dominated by
Cupressus lusitanica Carr. ("Bosque de Confferas'') with another with palm and wood harvesting
in a Montane rain forest ("Bosque Mes6filo de
Montana"; nomenclature follows Rzedowski
1978); and (4) to analyze C. matudai neighborhood composition and its demographic effect.
Species Description. Ceratozamia matudai is
a dioecious small palm-like plant 16-50 cm tall
(Lundell, 1939) with a single aboveground trunk,
pinnate leaves spirally arranged forming an open
crown. The male cone is green when immature
becoming light yellow to light brown at dehiscence. The female cone is decumbent, light green
when immature, and yellow at maturity. The species is entomophilous with Langurid beetles
transporting pollen between cones (Perez Farrera,
personal observation). The seeds are consumed
by rodents (Peromyscus sp.), and peccaries (Tayassu sp.) which may disperse them occasionally.
Larvae of Eumaeus debora causesvariable damage to its leaves (Perez Farrera, pers. observ.).
Materials and Methods. STUDYSITE. This
study was conducted in two sites on the upper
Pacific slope of the Sierra Madre de Chiapas, in
Triunfo Biosphere Reserve, Chiapas, Mexico.
These areasare characterizedby steep slopes and
represent the habitat spectrum of Ceratozamia
matudai in the region. A population in an open
forest dominated by Cupressus lusitanica Carr.
and Pinus maximinoi H. E. Moore ("Bosque de
Coniferas") was located in the core of the reserve, about 30 kIn north of Mapastepec,Chiapas
(15038'10" N, 92048'17 W; 1800 m of altitude).
This site did not show any evidence of recent
SOCIETY
[VOL. 127
human disturbance. The prevailing weather is
temperate with humid summers (2870 mm total
mean annual precipitation; 21 °C mean annual
temperature; 1992-1998 weather data from Finca
Prusia; Garcia 1987). Another population was located in El Cerro Ovando at the buffer zone of
El Triunfo, about 25 kIn northwest of Acacoyagua, Chiapas (15026'29" N, 920 38'15" W, 1400
m altitude). This area is covered by a mosaic of
coffee plantations (shaded by native tree species)
and Lower Montane Rain Forest (Bosque Mesofilo de Montafia). Local peasants harvest palms
and wood for fuel from the forest remnants.
GEOGRAPHICDISTRIBUTION. Vouchers of Ceratozamia were collected in eight sites to determine its distribution along the Sierra Madre de
Chiapas, and deposited at Instituto de Historia
Natural del Estado de Chiapas, El Colegio de la
Frontera Sur, and Universidad de Ciencias y Artes del Estado de Chiapas. Herbarium vouchers
and interchanged
material (from California
Academy of Sciences, Field Museum of Chicago) available at Universidad Aut6noma Metropolitana de Iztapalapa, Instituto de Ecologia, Instituto de Historia Natural, and Instituto de Biologi~', Universidad Nacional Aut6noma de Mexico were also examined. We recorded collection
date, collector's name, geographic location and
habitat for each plant examined. This information was summarized using CAMRIS 3.0.
LocAL SPATIAL DISTRIBUTION,MICROHABrrAT,
AND DEMOGRAPillCPARAMETERS.During C. matudai coning season in February of 1998 we established six 20 X 20 m permanent plots forming
a 40 X 60 m transect (2400 m2) in areas with
highest densities of C. matudai in each site. All
plots were used at Ovando, but we selected three
plots, randomly, at El Cipresal because of the
large number of plants (ca. 800). Spatial distribution was determined by methods described by
Greig-SInith
(1983) and Kershaw & Looney
(1985). We labeled, mapped (to the nearest decimeter), measured height and basal diameter,
counted number of leaves and leaf bases, and recorded gender and reproductive condition for
each plant within 5 X 5 m subplots. Plants were
revisited during August and December of the
same year at the time of leaf production. Gender
was assigned to each adult individual based on
the presence and shape of cones or their remains.
Several physical and biological parameters
were used to characterize C. matudai habitat. We
measured soil depth with a metal rod by driving
it into the soil until rock or stone was struck
2000]
PEREZ-FARRERA ET AL.: POPULATION DYNAMICS OF CERATOZAMIA MATUDAI
(Vovides 1990). The mean of three measurements
for each plant was taken. A clinometer was used
to determine slope in each subplot. We measured
distance to the nearesttree (> 3 cm diameter) and
recorded its diameter and identity. Number of
conspecifics, herbs, shrubs, and ferns were counted within a 150 cm radius centered around each
focal plant. The floristic composition in each site
was described from a 30 m long random transect
according to Garcia-Franco et al. (1989).
A logistic regression model (Fienberg 1987)
was applied to test for association of the proportion of dead plants with 11 variables describing C. matudai attributes and characteristics of
its habitat. Data within each variable was
grouped in categories. C. matudai, height (category boundaries: 2,3,4,5,6,7,8,9, 10-20, and
293
>20 cm) trunk diameter (1,2,3,4,5,6,7,8, ~ 9
cm) and leaf number (1,2,3,4,5, ~ 6 leaves)
were Qivided in groups including at least 15 individuals each. Soil depth (median = 23 cm),
diameter (20 cm), and distance to (137 cm) the
nearest tree were classified in dicotornic categories divided by their median. We considered
presence and absence of ferns, monocotyledoneae, and other shrubs and herbs. We used SPSS
package for data analysis.
Results. GEOGRAPHICDISTRIBUTION AND LoCAL SPATIAL PATfBRN ANALYSIS. Our collections
and herbarium surveys indicated morphological
differences between specimens previously identified as C. matudai from the Pacific and north-
ern slopes suggesting that this species only oc-
294
JOURNAL OF THE TORREY BOTANICAL
0 Cipresal
. Ovanda
300 '
250 >! 200j
, 150,I 100.
u.
-
50- 1.lr-Il,IlrL1~-'-I':""'1
1
.
0
0-39 4-79 8-11912-15.9
18-19920-23.9
24-27.9
28-~1.9
C.ma~.i DIAMETER
CLASS(an)
C
Fig. 2. Frequency distribution of (A) soil depth
classes, (B) neighboring tree diameter around C. matudai, and (C) C. matudai diameter classes.
curs on the Pacific slopes of the Sierra Madre
de Chiapas (Pijijiapan, Mapastepec and Acacoyagua) between 1100 and 1995 m.a.s.l. (Fig. 1).
Specimens from the northern slope will be proposed as a new species. Living individuals of
these two groups are easily distinguished. Ceratozamia matudai presents an aerial, unbranched
trunk, yellowish leaflet articulations and decumbent female cones. Populations on the northern
slopes of the Sierra Madre had hypogeal,
branched trunks, green leaflet articulations joints
and erect female cones; plants that do not fall
within the C. matudai Lundell's species concept
(Lundell 1939).
Ceratozamia matudai distribution was aggregated with variation peaking at block size 5 and
20 m2 in Mt. Ovando and 10 and 80 m2 in Cipresal (X2 = 120.14 P < 0.001, 5 d. f.; X2 =
125.32 P < 0.001, 5 d. f. respectively). Most
individuals at Mt. Ovando occurred near small
[VOL. 127
Urban (68 % importance) were the most frequent tree species at Cipresal. The grassLysiacis
sp. and small stature conspecifics dominated the
herbaceous layer in C. matudai neighborhoods
at this site. Ulmus mexicana Liebm., Clusia guatemalensis Hemsley and Senecio cobanensis J.
Coulter (72%) were the most abundant trees
within C. matudai neighborhoods at Ovando.
Ferns and Aroids dominated the herbaceus layer
in this location.
POPULAll0N
B
SOCIETY
STRUCTURE AND SURVIVAL.
Indi-
viduals of C. matudai had different allometric
relationships between mean total number of
leaves, leaf bases, trunk diameter and height between sites (Table 1). Plants with similar height
in Cipresal had greater trunk diameter, more
leaf-bases and more leaves than in Ovando (Table 2). C. matudai survivorship curves were reverse 'J' type curves or Deevey type ill (Deevey, 1947) with higher mortality among seedlings
and juveniles (40 % for Cipresal and 32 % for
Ovando; plants up to 20 cm tall, Fig. 3). These
size classes accounted for more than 75% of total plant number in each site (Fig. 2). Mortality
was higher in the presence of conspecifics (Fig.
3, 'fable 3). Greater distance to the nearest tree
(> 137 cm dbh), and presence of neighboring
monocotyledonous herbs were associated with
lower survival (Fig. 3, Table 3). Presenceof other shrubs and herbs decreased mortality compared with isolated plants.
FECUNDITY.We only found two female plants
at Cipresa1 and one in Ovando within our sampling area during 1998. 1\\'0 more female plants
occurred outside our sampling area in both sites
during the same year. Nine female plants coned
before this study at Cipresal and two at Ovando
(based on cone remains). Female cones emerged
between March and April and matured between
November-December. Female cone weight
ranged from 1-1.5 kg and included 32 to 56
well-developed
seeds (n
=2
cones). Seeds col-
lected from ripe cones showed immature embryos that required 3 to 4 months or more to mature. We found three male plants with cones at
Cipresal and only two at Ovando during 1998;
another 18 male plants showed evidence of contrees« 22 cm dbh), while sizeof treeneighbors ing before this study at Cipresal and five at
was more diverse at Cipresal (Fig. 2). In both Ovando. Male individuals had dehiscent cones
sites they occupied shallow soils « 33 cm from July to September. We observed Langurid
depth) on south slopes, ranging between 31- beetles (Pharaxonotha spp.) in the microsporan45% at Cipresal and 40-48 % at Ovando (Fig. giate scales, the male cone axis, and the pedun2). Ardisia compressa H.B.K, Cupressus /usi- cle. Leaves and cones with evidence of herbivtanica Carr., and Pithecel/obium arboreum (L.)
ory (Eumaeus debora) and seeds with damage
2000]
295
PEREZ-FARRERA ET AL.: POPULATION DYNAMICS OF CERATOZ4MIA MATUDAI
c
Tabl~ I. Results of analysis of covariance of C. matudai trunk diameter, number of leaves. and number of
basis among sites with trunk height as covariate.
Source of
v"N",inn
d.f.
Diameter
Site
Ln(Height) (covariate)
Site*Ln(Height)
Error
1
1
1
635
1
1
1
635
Number of leaves
Site
Height (covariate)
Site*Height
Error
Number of bases
Site
Height (covariate)
Site*Height
Error
1
1
1
635
F
p
107.804
8619.448
175.685
5.110
21.096
1686.701
34.379
<0.001
<0.001
<0.001
52.224
3548.779
820.394
14.084
3.708
251.974
58.250
>0.055
<0.001
<0.001
1.016
1258.739
9.578
>0.314
<0.001
<0.002
Mean square
3769.456
4,668,816.000
35526.96
3709.122
size (2-3 cm diameter) and their high concentrations of neurotoxins as cycacins, macrozamins, and BMAA (Whiting, 1963; Norstog et
Discussion. REGIONAL AND LOCAL DISTRIBU- al., 1993; Duncan, 1993). However some rodents such as Peromiscus mexicanus feed on
TION. Stevenson (1986) species account located
C. matudai between the north of the Isthmus of
s~edsof Dioon edule, among other species, and
Tehuantepec, Oaxaca, and the Highlands of
p;obably influence dispersal of this cycad (GonGuatemala. Our survey suggested a narrower \-ililez, 1990). Peccaries (Tayassu tajacu) also eat
distribution for this species around the central
and move seedsof other similar cycads and may
portion of the Pacific slope of the Sierra Madre
disperse C. matudai seeds (personal observade Chiapas. Collections from Oaxaca, the slope
tion). The steep topography characteristic of C.
towards the Gulf of Mexico of the Sierra Madre
matudai habitat may also determine limited disof Chiapas, and Guatemala may belong to other
persal distances influenced by gravity.
by mammals were found on the ground (probably eaten by Peromyscus sp.).
non-described species.
The observed aggregated distribution pattern
of C. matudai at our study sites may result from
the interaction of several environmental factors.
Our observations indicated that seedling recruitment mostly occurs around already established
mother plants suggesting poor seed dispersal. C.
matudai seeds may have low levels of interaction with predators/dispersers because their large
SEEDLING
ESTABLISHMENT
AND
SURVIVAL.
"
~
"
There is little information on mortality rates for §~
cycad seedlings. Zamia spp. had 1-30 % surviv- I
al after two years (Omduff 1996; Tang 1989;
Eckenwalder 1980b). Dioon spp. also had heavy
mortality rates (Vovides 1990). Herbivory,
drought, and predation were the main causes of
death found in these studies. Our data suggests
Table 2. Life table of Ceratozamia matudai populations at Cipresal and Ovando in the El Triunhfo Biosphere
Reserve (February 1998-February 1999).
Cipresal
Ovando
296
JOURNAL OF THE TORREY BOTANICAL
SOCIETY
[VOL. 127
50,
!fj
c:
ro
"Q.
"0
ro
CD
"0
"6
~
0
Diameter of C matudai
(1)
c:
to
"0..
u
to
Q)
U
~
Distance to nearest tree
Cover of C. matudai conspecifics
30.
25
.fj
C
tV
'Q..
u
tV
Q)
U
~
20,
15,
10,
"I
i
01
Absent
Present
Monocotvledonae
Present
Other shrubs and herbs
Fig. 3. Proportion of c. matudai dead individuals sorted by classes of diameter, distance to nearest tree,
cover of conspecifics. and presence or absence of monocotvlidonae and other shrubs and herbs.
2000]
PEREZ-FARRERA ET At
POPULATION DYNAMICS OF CERATOZ4MIA MATUDAI
297
Tabl~ 3. Logistic regression of mortality of C. matudai at Cipresal and Ovando in the Triunfo Biospher,
Reserve (n = 639).
Variable
B
s,e,
W. X2
p
Intercept
Diameter of C. matudai
Distance to nearest tree
Cover of conspecifics
1-25%
25-100%
Presence of Monocotyledonae
Presence of other spp.
Variables not in the equation
Height
Soil depth
Leaf number
Sex
Diameter of nearest tree
Fern presence
0.972
0.241
0.603
1.044
0.430
0.824
-1.209
0.317
0.051
0.243
0.308
0.325
0.290
0.547
9.42
22.14
6.14
12.18
11.50
1.75
8.06
4.89
0.002
<0.001
0.013
0.002
<0.001
0.186
0.004
0.027
that herbivory, weather, and neighboring floristic
composition affected seedling establishment and
survival of C. matudai. We found lower C. matudai mortality and lower number of seedlings
at Ovando (12% percent dead after a year) than
at Cipresal (20%) where many plants showed
evidence of herbivory by caterpillars of Eumaeus debora. Although similar herbivory was
described for other neotropical cycads we do not
know enough about the importance of this interaction (De Vries 1976; Clark and Clark 1991;
Vovides 1990). Slow litter decomposition rates
in conifer forests (see Challenger, 1998) may
provide shelter for C. matuadi seedsand explain
the higher establishment in Cipresal.
As many other shade tolerant cycads, C. matudai was associated with relatively undisturbed
sites with poor soils and steep slopes (Vovides
1990; Alejandre et al. 1990). Bond (1989) suggested that these species are confined to relatively more inhospitable habitats because of
their lower competitive ability in more mesic
habitats but higher tolerance to frost, drought
and other physical factors. We found coralloid
roots on C. matudai roots. The symbiosis with
versicular arbuscular fungus is widely distributed within the group. Endomycorrhiza may increase water and nitrogen uptake (Vovides 1990,
1991b; Grove et al. 1980; Guo-Fan et al. 1993)
improving their survival and growth in shallow
and poor soils characteristic of their habitat.
Our results provide the first step towards understand the population biology and conservation status of C. matudai. The data are from less
than one year and exceptional weather conditions associated with "El Nino" affected our results. While we observed manv dead plants after
Exp (6)
1.2072
1.827
2.842
,1.537
2.279
0.298
0.566
0.164
0.780
0.964
0.156
0.562
the long dry period that occurred during the first
months of 1998, we also found frequent evidence of pathogenic fungi during the extremely
wet months of the second half of the same year.
An understanding of population variation
along species range is important to suggest future management strategies. Management meth~s increasing seed production and seedling recruitment may increase chancesof persistence of
C. matudai. Experimental studies considering
seed predation, seedling establishment, plant
competition and herbivory may help to design
better management strategies.
Because of its low numbers «1000 known
individuals) and limited range (only three known
populations) we recommend a status change in
its IUCN category (IUCN, 1994; Osborne,
1995) to endangered in accordance with Mace
and Lande (1991). As with other cycads, C. matudai can reach high market values. Ex-situ
propagation and cultivation of this and other
species may provide incentives among local
peasants for conservation of the natural populations and its habitat. A carefully designed
management plan, including limited harvesting
of seeds and plant reintroduction may improve
the chances of long term persistence of this spe-
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