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, Mexico1Miguel Angel Perez Farrera, Pedro F. Quintana-Ascencio,

and Benito Salvatierra IzabaEl Colegio de la Frontera Sur, Apartado Postal 63, San Crist6bal de la Casas, 29200, Chiapas, M6xico,

Andrew P. VovidesApartado 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 ANDREW P. VOVIDES (Apartado Postal 63, Institutode 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 Ceratozamiamatudai geographic distribution, its basic demographic parameiers, and the association of these parameiers withenvironmental factors. A species survey and a review of herbarium collections indicaled that C. matudai occurs onlyon the pacific slopes of the Sierra Madre of Chiapas, Mexico. ~o censuses (1998-1999) were performed in a Pine-Cupressus 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 eachsire were described. This species showed a clumped local distribution on shallow soils on steep slopes. Individualsshowed differences in amount of leaf production, trunk diameier, and height between sires. Neighboring speciescomposition affecled seedling mortality. Because of its low numbers and limiled range we recommend a status changein its IUCN caiegory to endangered. As with other cycads, C. matudai can reach high market values. Ex-situ prop-agation of this and other species may provide incentives among local peasants for conservation of the natural popu-lations and its habitat.

Key words: Cycad, Ceratozamia matudai, population dynamics, persistence, endangered species.

!.,

Cycads are a long-lived group of plants con-sidered ancient and primitive (Crane 1988; Eck-enwalder 1 980a). About 240 species have beenreported worldwide (Osborne et al. 1999). InMexico there are over 40 species of cycads, mak-ing Mexico second world wide in cycad diversity(Vovides, in press). Among these species 80% areendemic to this country (Vovides & Iglesias1994) and 40% restricted to the southern state ofChiapas. In Chiapas most cycads inh~bit tropical

rain forests and montane cloud forests where theyare threatened due to habitat deterioration, andcurrent expansion of agricultural fields and coffeeplantations. Even populations in protected areasare disappearing because of escaped fires and il-legal harvesting (Vovides 1990). Ceratozamiamatudai Lundell is an endemic cycad of the Si-erra Madre of Chiapas. Its conservation status isconsidered to be vulnerable according to Inter-national Union for the Conservation of Nature(Vovides et al. 1997a, Osborne 1995) and the spe-cies is protected by Mexican law (Diario Oficialde la Federaci6n 1994). Remnant populations ofthis ~ies are threatened due to the replacementof forest by coffee plantations in the Soconuscoregion (Schutzman et al. 1988).

Few studies have reported population param-eters of cycads. Population studies of cycadshave described some aspects of their life cycle,phenology, pollination and seed dispersal (Clarket al. 1992; Norstog et al. 1992; Vovides 1991a;Tang 1988). Negron & Breckon (1989) and Vov-ides (1990) described the population structure ofZamia debilis L.f. ex Aiton and Dioon eduleLindl. respectively. They found survivorship re-verse "J" or Deevey type III curves associatedwith high seedling mortality. The study of Ale-jandre et al. (1990) of Ceratozamia mexicana

1 The research was supported by Fauna and Floralnternacional (96/64/15; MAPF), Fondo Mexicanopara 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 and29379N) and a fellowship to MAPF (114869) from ElColegio de la Frontera Sur. We thank Alejandro Her-nandez Yanez and the staff at The Triunfo BiosphereReserve, lnstituto Nacional de Ecologia. T. Milledge,J. De La Cruz Rodriguez, M. Evangelina L6pez Mo-lina, R. Hernandez Jonapa, J. Zaragoza, C. O'Brien,R. Ornduff, N. Ramirez Marcial and D. B. Clark pro-vided invaluable help.

2 Current address: Escuela de Biologia, Universidadde Ciencias y Artes del Estado de Chiapas, CalzadaSamuel Le6n Brindis 151, Thxtla Guti~rrez, Chiapas,Mexico, 29000.

Received for publication July 26, 1999, and in re-vised form July 20, 2000.

291

292 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 127

Brongn.:described the effect of moisture and for-est stand conditions on the survival of this spe-cies. They observed a positive association be-tween cycad number, mostly seedlings and ju-veniles, and tree density.

The knowledge of the life history and the in-fluence of physical and biological factors on pop-ulation growth of endangered taxa provide valu-able information for their management and con-servation (Shemske et al. 1994; Donalson 1995;Menges 1986; Henifin et al. 1981). The goals ofthis study were: (1) to describe Ceratozamia ma-tudai distribution along the Sierra Madre, Chia-pas; (2) to describe its demographic characteris-tics, such as local spatial distribution, and struc-ture in two populations in El lliunfo BiosphereReserve, Chiapas, Mexico; (3) to contrast popu-lation dynamics of C. matudai in an area withoutnoticeable disturbance in a forest dominated byCupressus lusitanica Carr. ("Bosque de Conffer-as'') with another with palm and wood harvestingin a Montane rain forest ("Bosque Mes6filo deMontana"; nomenclature follows Rzedowski1978); and (4) to analyze C. matudai neighbor-hood composition and its demographic effect.

Species Description. Ceratozamia matudai isa dioecious small palm-like plant 16-50 cm tall(Lundell, 1939) with a single aboveground trunk,pinnate leaves spirally arranged forming an opencrown. The male cone is green when immaturebecoming light yellow to light brown at dehis-cence. The female cone is decumbent, light greenwhen immature, and yellow at maturity. The spe-cies is entomophilous with Langurid beetlestransporting pollen between cones (Perez Farrera,personal observation). The seeds are consumedby rodents (Peromyscus sp.), and peccaries (Tay-assu sp.) which may disperse them occasionally.Larvae of Eumaeus debora causes variable dam-age to its leaves (Perez Farrera, pers. observ.).

human disturbance. The prevailing weather istemperate with humid summers (2870 mm totalmean annual precipitation; 21 °C mean annual

temperature; 1992-1998 weather data from FincaPrusia; Garcia 1987). Another population was lo-cated in El Cerro Ovando at the buffer zone ofEl Triunfo, about 25 kIn northwest of Acacoya-

gua, Chiapas (15026'29" N, 920 38'15" W, 1400m altitude). This area is covered by a mosaic ofcoffee plantations (shaded by native tree species)and Lower Montane Rain Forest (Bosque Meso-filo de Montafia). Local peasants harvest palmsand wood for fuel from the forest remnants.

GEOGRAPHIC DISTRIBUTION. Vouchers of Cer-atozamia were collected in eight sites to deter-mine its distribution along the Sierra Madre deChiapas, and deposited at Instituto de HistoriaNatural del Estado de Chiapas, El Colegio de laFrontera Sur, and Universidad de Ciencias y Ar-tes del Estado de Chiapas. Herbarium vouchersand interchanged material (from CaliforniaAcademy of Sciences, Field Museum of Chica-go) available at Universidad Aut6noma Metro-politana de Iztapalapa, Instituto de Ecologia, In-stituto de Historia Natural, and Instituto de Biol-ogi~', Universidad Nacional Aut6noma de Mex-ico were also examined. We recorded collectiondate, collector's name, geographic location andhabitat for each plant examined. This informa-tion was summarized using CAMRIS 3.0.

LocAL SPATIAL DISTRIBUTION, MICROHABrrAT,AND DEMOGRAPillC PARAMETERS. During C. ma-tudai coning season in February of 1998 we es-tablished six 20 X 20 m permanent plots forminga 40 X 60 m transect (2400 m2) in areas with

highest densities of C. matudai in each site. Allplots were used at Ovando, but we selected threeplots, randomly, at El Cipresal because of thelarge number of plants (ca. 800). Spatial distri-bution was determined by methods described by

Greig-SInith (1983) and Kershaw & Looney(1985). We labeled, mapped (to the nearest deci-meter), measured height and basal diameter,counted number of leaves and leaf bases, and re-corded gender and reproductive condition foreach plant within 5 X 5 m subplots. Plants wererevisited during August and December of thesame year at the time of leaf production. Genderwas assigned to each adult individual based onthe presence and shape of cones or their remains.

Several physical and biological parameterswere used to characterize C. matudai habitat. Wemeasured soil depth with a metal rod by drivingit into the soil until rock or stone was struck

Materials and Methods. STUDY SITE. Thisstudy was conducted in two sites on the upperPacific slope of the Sierra Madre de Chiapas, inTriunfo Biosphere Reserve, Chiapas, Mexico.These areas are characterized by steep slopes andrepresent the habitat spectrum of Ceratozamiamatudai in the region. A population in an openforest dominated by Cupressus lusitanica Carr.and Pinus maximinoi H. E. Moore ("Bosque deConiferas") was located in the core of the re-serve, 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

2932000] PEREZ-FARRERA ET AL.: POPULATION DYNAMICS OF CERATOZAMIA MATUDAI

>20 cm) trunk diameter (1,2,3,4,5,6,7,8, ~ 9cm) and leaf number (1,2,3,4,5, ~ 6 leaves)were Qivided in groups including at least 15 in-dividuals each. Soil depth (median = 23 cm),diameter (20 cm), and distance to (137 cm) thenearest tree were classified in dicotornic cate-gories divided by their median. We consideredpresence and absence of ferns, monocotyledo-neae, and other shrubs and herbs. We used SPSSpackage for data analysis.

(Vovides 1990). The mean of three measurementsfor each plant was taken. A clinometer was usedto determine slope in each subplot. We measureddistance to the nearest tree (> 3 cm diameter) andrecorded its diameter and identity. Number ofconspecifics, herbs, shrubs, and ferns were count-ed within a 150 cm radius centered around eachfocal plant. The floristic composition in each sitewas described from a 30 m long random transectaccording to Garcia-Franco et al. (1989).

A logistic regression model (Fienberg 1987)was applied to test for association of the pro-portion of dead plants with 11 variables describ-ing C. matudai attributes and characteristics ofits habitat. Data within each variable wasgrouped in categories. C. matudai, height (cat-egory boundaries: 2,3,4,5,6,7,8,9, 10-20, and

Results. GEOGRAPHIC DISTRIBUTION AND Lo-CAL SPATIAL PATfBRN ANALYSIS. Our collectionsand herbarium surveys indicated morphologicaldifferences between specimens previously iden-tified as C. matudai from the Pacific and north-ern slopes suggesting that this species only oc-

294 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 127

0 Cipresal

. Ovanda

B

1

300 '

250 ->-! 200-j, 150-,I 100-.u. -1.lr-Il,IlrL1~-'-I':""'1 50- .

00-39 4-79 8-119 12-15.9 18-19920-23.9 24-27.9 28-~1.9

C. ma~.i DIAMETER CLASS (an) C

Fig. 2. Frequency distribution of (A) soil depthclasses, (B) neighboring tree diameter around C. ma-tudai, and (C) C. matudai diameter classes.

Urban (68 % importance) were the most fre-quent tree species at Cipresal. The grass Lysiacissp. and small stature conspecifics dominated theherbaceous layer in C. matudai neighborhoodsat this site. Ulmus mexicana Liebm., Clusia gua-temalensis Hemsley and Senecio cobanensis J.Coulter (72%) were the most abundant treeswithin C. matudai neighborhoods at Ovando.Ferns and Aroids dominated the herbaceus layerin this location.

POPULAll0N STRUCTURE AND SURVIVAL. Indi-

viduals of C. matudai had different allometricrelationships between mean total number ofleaves, leaf bases, trunk diameter and height be-tween sites (Table 1). Plants with similar heightin Cipresal had greater trunk diameter, moreleaf-bases and more leaves than in Ovando (Ta-ble 2). C. matudai survivorship curves were re-verse 'J' type curves or Deevey type ill (Deev-ey, 1947) with higher mortality among seedlingsand juveniles (40 % for Cipresal and 32 % forOvando; plants up to 20 cm tall, Fig. 3). Thesesize classes accounted for more than 75% of to-tal plant number in each site (Fig. 2). Mortalitywas higher in the presence of conspecifics (Fig.3, 'fable 3). Greater distance to the nearest tree(> 137 cm dbh), and presence of neighboringmonocotyledonous herbs were associated withlower survival (Fig. 3, Table 3). Presence of oth-er shrubs and herbs decreased mortality com-pared with isolated plants.

FECUNDITY. We only found two female plantsat Cipresa1 and one in Ovando within our sam-pling area during 1998. 1\\'0 more female plantsoccurred outside our sampling area in both sitesduring the same year. Nine female plants conedbefore this study at Cipresal and two at Ovando(based on cone remains). Female cones emergedbetween March and April and matured betweenNovember-December. Female cone weightranged from 1-1.5 kg and included 32 to 56well-developed seeds (n = 2 cones). Seeds col-

lected from ripe cones showed immature embry-os that required 3 to 4 months or more to ma-ture. We found three male plants with cones atCipresal and only two at Ovando during 1998;another 18 male plants showed evidence of con-ing before this study at Cipresal and five atOvando. Male individuals had dehiscent conesfrom July to September. We observed Languridbeetles (Pharaxonotha spp.) in the microsporan-giate scales, the male cone axis, and the pedun-cle. Leaves and cones with evidence of herbiv-ory (Eumaeus debora) and seeds with damage

curs on the Pacific slopes of the Sierra Madrede Chiapas (Pijijiapan, Mapastepec and Acacoy-agua) between 1100 and 1995 m.a.s.l. (Fig. 1).Specimens from the northern slope will be pro-posed as a new species. Living individuals ofthese two groups are easily distinguished. Cer-atozamia matudai presents an aerial, unbranchedtrunk, yellowish leaflet articulations and decum-bent female cones. Populations on the northernslopes of the Sierra Madre had hypogeal,branched trunks, green leaflet articulations jointsand erect female cones; plants that do not fallwithin the C. matudai Lundell's species concept(Lundell 1939).

Ceratozamia matudai distribution was aggre-gated with variation peaking at block size 5 and20 m2 in Mt. Ovando and 10 and 80 m2 in Ci-presal (X2 = 120.14 P < 0.001, 5 d. f.; X2 =125.32 P < 0.001, 5 d. f. respectively). Mostindividuals at Mt. Ovando occurred near smalltrees « 22 cm dbh), while size of tree neighborswas more diverse at Cipresal (Fig. 2). In bothsites they occupied shallow soils « 33 cmdepth) on south slopes, ranging between 31-45% at Cipresal and 40-48 % at Ovando (Fig.2). Ardisia compressa H.B.K, Cupressus /usi-tanica Carr., and Pithecel/obium arboreum (L.)

295PEREZ-FARRERA ET AL.: POPULATION DYNAMICS OF CERATOZ4MIA MATUDAI2000]

cTabl~ 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 ofv"N",inn F pd.f. Mean square

<0.001<0.001<0.001

111

635

21.0961686.701

34.379

52.2243548.779

820.39414.084

3.708251.974

58.250

>0.055<0.001<0.001

111

635

3769.4564,668,816.000

35526.963709.122

1.0161258.739

9.578

>0.314<0.001<0.002

111

635

DiameterSiteLn(Height) (covariate)Site*Ln(Height)Error

Number of leavesSiteHeight (covariate)Site*HeightError

Number of basesSiteHeight (covariate)Site*HeightError

by mammals were found on the ground (proba-bly eaten by Peromyscus sp.).

Discussion. REGIONAL AND LOCAL DISTRIBU-TION. Stevenson (1986) species account locatedC. matudai between the north of the Isthmus ofTehuantepec, Oaxaca, and the Highlands ofGuatemala. Our survey suggested a narrowerdistribution for this species around the centralportion of the Pacific slope of the Sierra Madrede Chiapas. Collections from Oaxaca, the slopetowards the Gulf of Mexico of the Sierra Madreof Chiapas, and Guatemala may belong to othernon-described species.

The observed aggregated distribution patternof C. matudai at our study sites may result fromthe interaction of several environmental factors.Our observations indicated that seedling recruit-ment mostly occurs around already establishedmother plants suggesting poor seed dispersal. C.matudai seeds may have low levels of interac-tion with predators/dispersers because their large

"~"§~

I

Table 2. Life table of Ceratozamia matudai populations at Cipresal and Ovando in the El Triunhfo BiosphereReserve (February 1998-February 1999).

OvandoCipresal

107.8048619.448

175.6855.110

size (2-3 cm diameter) and their high concen-trations of neurotoxins as cycacins, macroza-mins, and BMAA (Whiting, 1963; Norstog etal., 1993; Duncan, 1993). However some ro-dents such as Peromiscus mexicanus feed ons~eds of Dioon edule, among other species, andp;obably influence dispersal of this cycad (Gon-

\-ililez, 1990). Peccaries (Tayassu tajacu) also eatand move seeds of other similar cycads and maydisperse C. matudai seeds (personal observa-tion). The steep topography characteristic of C.matudai habitat may also determine limited dis-persal distances influenced by gravity.

SEEDLING ESTABLISHMENT AND SURVIVAL.

There is little information on mortality rates forcycad seedlings. Zamia spp. had 1-30 % surviv-al after two years (Omduff 1996; Tang 1989;Eckenwalder 1980b). Dioon spp. also had heavymortality rates (Vovides 1990). Herbivory,drought, and predation were the main causes ofdeath found in these studies. Our data suggests

296 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 127

50,

!fjc:ro

"Q.

"0roCD

"0

"6~0

Diameter of C matudai

(1)c:to"0..utoQ)U~

Distance to nearest tree Cover of C. matudai conspecifics

30.

25

20,

15,

10,i

"I

.fjCtV

'Q..

utVQ)

U

~

01Absent Present Present

Monocotvledonae Other shrubs and herbsFig. 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.

297POPULATION DYNAMICS OF CERATOZ4MIA MATUDAI2000] PEREZ-FARRERA ET At

Tabl~ 3. Logistic regression of mortality of C. matudai at Cipresal and Ovando in the Triunfo Biospher,Reserve (n = 639).

Exp (6)p

0.002<0.001

0.0130.002

<0.0010.1860.0040.027

B s,e, W. X2

0.972 0.317 9.420.241 0.051 22.140.603 0.243 6.14

- - 12.181.044 0.308 11.500.430 0.325 1.750.824 0.290 8.06-1.209 0.547 4.89

Variable

1.20721.827

2.842,1.5372.2790.298

0.5660.1640.7800.9640.1560.562

InterceptDiameter of C. matudaiDistance to nearest treeCover of conspecifics

1-25%25-100%

Presence of MonocotyledonaePresence of other spp.Variables not in the equationHeightSoil depthLeaf numberSexDiameter of nearest treeFern presence

the long dry period that occurred during the firstmonths of 1998, we also found frequent evi-dence of pathogenic fungi during the extremelywet months of the second half of the same year.

An understanding of population variationalong species range is important to suggest fu-ture management strategies. Management meth-~s increasing seed production and seedling re-cruitment may increase chances of persistence ofC. matudai. Experimental studies consideringseed predation, seedling establishment, plantcompetition and herbivory may help to designbetter management strategies.

Because of its low numbers «1000 knownindividuals) and limited range (only three knownpopulations) we recommend a status change inits IUCN category (IUCN, 1994; Osborne,1995) to endangered in accordance with Maceand Lande (1991). As with other cycads, C. ma-tudai can reach high market values. Ex-situpropagation and cultivation of this and otherspecies may provide incentives among localpeasants for conservation of the natural popu-lations and its habitat. A carefully designedmanagement plan, including limited harvestingof seeds and plant reintroduction may improvethe chances of long term persistence of this spe-

that herbivory, weather, and neighboring floristiccomposition affected seedling establishment andsurvival of C. matudai. We found lower C. ma-tudai mortality and lower number of seedlingsat Ovando (12% percent dead after a year) thanat Cipresal (20%) where many plants showedevidence of herbivory by caterpillars of Eu-maeus debora. Although similar herbivory wasdescribed for other neotropical cycads we do notknow enough about the importance of this in-teraction (De Vries 1976; Clark and Clark 1991;Vovides 1990). Slow litter decomposition ratesin conifer forests (see Challenger, 1998) mayprovide shelter for C. matuadi seeds and explainthe higher establishment in Cipresal.

As many other shade tolerant cycads, C. ma-tudai was associated with relatively undisturbedsites with poor soils and steep slopes (Vovides1990; Alejandre et al. 1990). Bond (1989) sug-gested that these species are confined to rela-tively more inhospitable habitats because oftheir lower competitive ability in more mesichabitats but higher tolerance to frost, droughtand other physical factors. We found coralloidroots on C. matudai roots. The symbiosis withversicular arbuscular fungus is widely distribut-ed within the group. Endomycorrhiza may in-crease water and nitrogen uptake (Vovides 1990,1991b; Grove et al. 1980; Guo-Fan et al. 1993)improving their survival and growth in shallowand poor soils characteristic of their habitat.

Our results provide the first step towards un-derstand the population biology and conserva-tion status of C. matudai. The data are from lessthan one year and exceptional weather condi-tions associated with "El Nino" affected our re-sults. While we observed manv dead plants after

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