The importance of tropical rain forest fragments to the conservation of plant species diversity in...

8/7/2019 The importance of tropical rain forest fragments to the conservation of plant species diversity in Los Tuxtlas, Mexico

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The importance of tropical rain forest fragmentsto the conservation of plant species diversity in Los

Tuxtlas, Mexico

VICTOR ARROYO-RODRIGUEZ1,2and SALVADOR MANDUJANO2,*1Division de Postgrado, Instituto de Ecolog a A.C., km 2.5 Ant. Carretera Coatepec No. 351, Xalapa

91070, Veracruz, Mexico; 2Departamento de Biodiversidad y Ecolog a Animal, Instituto de Ecolog a

A.C. km 2.5 Ant. Carretera Coatepec No. 351, Xalapa 91070, Veracruz, Mexico; *Author for

correspondence (e-mail: [email protected])

Received 14 March 2005; accepted in revised form 12 September 2005

Key words: Diversity, Forest fragmentation, Forest remnant, Los Tuxtlas, Mexico, Tropical rain

forest, Vegetation

Abstract. Of what value are forest fragments to the conservation of the tropical rain forest diversity

for a landscape? We compared the changes in composition, diversity, and plant structure of 15

small (176 ha) relatively unprotected forest fragments with those of a large (700 ha) well protected

fragment (LWPF) in Los Tuxtlas, Mexico. The trees, shrubs, lianas, palms, and herbs with

dbh 2.5 cm were sampled in 1000 m2 at each site. For each ecological group (based on light

requirements for germination: primary, secondary, and non-secondary light demanding, NSLD,species) and life form, estimates of species diversity, density, and basal area were analyzed using a

stepwise multiple regression to determine whether there were any relationships between these

variables and fragment characteristics (size, shape index, and isolation). The composition and plant

structure of LWPF were different from those of the small fragments and large trees are absent from

the canopy of the latter. Fragment size best explained the differences in composition and plant

structure. Species composition in the largest fragments was similar to that of LWPF, but there was

no significant difference in total richness between LWPF and the fragments, even though both the

richness and abundance of secondary and NSLD species did differ. LWPF had more large primary

trees in the canopy, and a greater abundance and basal area of palms and herbs. For tropical rain

forest conservation, it is important to maintain the greatest possible number of large fragments and

establish policies that prevent forest remnants from being further reduced in size and increasinglyisolated from each other.

Introduction

Accelerated deforestation is causing the rapid loss and fragmentation of pri-

mary forest in tropical regions. Consequently, what was once continuous forest

is being converted into a landscape comprised of remnant fragments of originalforest of varying sizes, shapes, and isolation distances, and these are immersed

in a matrix of land that has been altered by human activities (Fahrig 2003). The

effects of the forest fragments spatial geometry on plant composition, diver-

sity, and structure are important as they control ecological processes such as

Biodiversity and Conservation (2006) 15:41594179 Springer 2006

DOI 10.1007/s10531-005-3374-8


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speciation, dispersal, migration, competition, extinction, and composition

(Turner et al. 1996; Laurance et al. 2002; Hill and Curran 2003). Therefore, in

order to conserve the remaining forest effectively it is crucial to quantify theinfluence of forest fragment area, shape, and degree of isolation on plant

diversity and structure. Although the effects of habitat loss and fragmentation

on biodiversity are well documented (Fahrig 2003), few studies have focused on

the changes occurring in plant structure in terms of ecological group and life

form, and how changes in these affect the conservation of tropical rain forest at

the landscape scale.

Fragmentation is known to decrease the number of species and produce

substantial changes in community attributes (Dislich and Pivello 2002; Souza

and Martins 2002; Bentez-Malvido and Martinez-Ramos 2003a, b). The edge

of the fragment is the most drastically altered zone, as changes occur there

more rapidly owing to microenvironmental conditions (Laurance and Yensen

1991; Saunders et al. 1991). Tropical forest studies have shown that tree

mortality rate increases near the edges (Laurance et al. 1997, 1998a, b, 2000).

This may result from increased vine density (Laurance et al. 1998a, b), with

the most damage suffered by species that cannot tolerate much light (Bentez-

Malvido 1998; Hill and Curran 2003). This, in turn, results in a higher

recruitment rate of secondary species (Malcolm 1994; Martinez-Ramos and

Alvarez-Buylla 1995; Bentez-Malvido 1998; Dislich and Pivello 2002).

In recent decades, deforestation in Mexico has led to the loss of approxi-mately 90% of tropical rainforest (Flores-Villela and Gerez 1994). This has

been particularly severe in Los Tuxtlas, Veracruz (Dirzo and Garca 1992)

where it is estimated that 75% of the original forest has already disappeared.

The remaining 20% consists mainly of isolated fragments, and only 5% con-

stitutes large well protected areas at elevations over 800 m asl (Estrada and

Coates-Estrada 1996). While there are studies concerning the floristic and

structural characteristics of vegetation in the region (e.g., Pin ero et al. 1977;

Bongers et al. 1988; Ibarra-Manrquez and Sinaca-Coln 1995), most have

been carried out at sites where the vegetation is virtually unaltered, with little

research on the changes that arise from the disturbance of original tropical

forest (e.g., Ibarra-Manrquez et al. 1997a; Castillo-Campos and Laborde

2004).

The purpose of this study is to contribute to the understanding of the veg-

etation changes produced by the loss and fragmentation of tropical rain forest

in the region of Los Tuxtlas. Specifically, the question we address is: What

value do forest fragments have in the conservation of the diversity of tropical

rain forest on the scale of a landscape? To answer this, floristic composition,

species diversity, and vegetation structure are examined for 15 small, relatively

unprotected forest fragments and this data is compared with data for a largewell protected fragment. The effects of fragment size, shape, and isolation

on floristic composition, species diversity, and vegetation structure of the

fragments are also analyzed.

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Methods

Study site

Los Tuxtlas is located in the state of Veracruz, Mexico (Figure 1). The climate

is humid and semi-humid with a mean annual temperature of 2426 C. An-

nual precipitation ranges from 3000 to 4000 mm (Soto and Gama 1997). It was

decreed a National Biosphere Reserve in 1998 (Diario Oficial de la Federacio n

1998), and represents the northern limit of tropical rain forest distribution in

the Americas (Dirzo and Miranda 1990). The Reserve covers 155122 ha, with

elevations from sea level to 1780 m asl (Guevara et al. 2004). Below 700 m the

dominant vegetation type is tropical evergreen rain forest. The study site is

located at the base of the Santa Marta and San Martin Pajapan Volcanoes

(Figure 1), in the southern buffer zone of the Reserve (1818 to 1826 N, and

9445 to 9455 W). It includes eight ejidos belonging to the municipality of

Tatahuicapan de Jua rez. It is bordered by the Tecuanapa and Pilapa Rivers,

the Mexican Gulf Coast, and the foothills of the Santa Marta Mountain Range

at an altitude of 700 m asl. The landscape is characterized by irregular

topography and slopes that often exceed 30. Since the communal lands were

established in the 1970s, deforestation has accelerated steadily. Considering

both the pattern and rate of deforestation of Los Tuxtlas region between 1972

and 1993 (Guevara et al. 2004), we assumed that all the forest fragments westudied were of approximately the same age. Therefore, this factor was not

included in the analysis.

The landscape in the study region has been severely altered. Of 4960 ha of

total study area, only 547 ha (11%) represents primary and secondary tropical

forests. The matrix surrounding the forest fragments is composed principally of

pastures and corn crops. In total, there are 92 fragments, with most (68%)

located in the riparian zones of rivers or streams, though some (24%) are found

on mountaintops, and others (8%) run along the ocean shore in permanently

flooded areas. Eighty-one percent of the fragments are smaller than 5 ha, and

only five (8%) exceed 10 ha, the largest of these covering 76 ha. Mean mini-

mum distance (SD) between fragments is 111 99 m (range: 8438 m), but

85% are less than 200 m apart. The mean distance from one fragment to the

nearest town is 880 656 m (range: 02542 m). Most of the fragments are

irregular in shape as they run along rivers or streams, making them quite long

and narrow with a notable edge effect.

Fragment selection

Fifteen fragments were randomly selected (Figure 1; Table 1) using a digital-

ized vegetation map (Mandujano et al. 2006). The size of each fragment and

the distance to the nearest one were measured using GIS ArcView version 3.2

(Patch Analyst 2.2. module). Fragment shape index was calculated as follows:

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Figure 1. Location of Los Tuxtlas Tropical Biology Station and the fragments selected (in black).

Solid lines indicate routes that connect different towns; rivers appear as dotted lines.

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IF = P/2AP, where P and A are the fragment perimeter and area, respec-tively, measured in meters. This index returns a value of one when fragments

are circular, and a maximum value of five for a completely irregular shape

(Forman and Godron 1986).

As a control, we used the forest of Los Tuxtlas Tropical Biology Station

(Figure 1). This relatively large (700 ha) well protected fragment (LWPF) is in

the core zone of the Los Tuxtlas Biosphere Reserve. This forest has the same

vegetation type as the fragmented landscape (Castillo-Campos and Laborde

2004), and is located at the same elevation. Descriptions of the flora, fauna,

and forest ecology of the station can be found in Gonza lez-Soriano et al.

(1997) and Guevara et al. (2004).

Vegetation sampling

Vegetation was sampled following Gentrys (1982) protocol. We chose this

method because it is logistically simple to carry out, it is economical (in bothtime and money), and it is appropriate for the analysis of species diversity in

tropical forests (see Gentry 1982, pp. 1821). Furthermore, since Gentry

applied this method in several Neotropical forests, it is possible to compare our

data with his substantial data base (maintained by the Missouri Botanical

Table 1. Structural characteristics for 15 forest fragments and a large well protected fragment

(LWPF) studied in Los Tuxtlas, Mexico.

Fragment Fragment characteristics Vegetation characteristics/1000 m2

Altitude

(m asl)

Isolation

(m)

Size

(ha)

Forest

interiora(ha)

Shape

index

No. of

families

No. of

species

No. of

individuals

Basal

area (m2)

F1 475 85 75.6 27.4 2.7 31 53 214 11

F2 175 18 57.2 13.6 2.9 34 61 236 9

F3 350 50 32.6 4 3.1 34 54 279 10

F4 225 196 30 0 4.3 35 71 191 8

F5 200 35 13 0 3.7 41 70 288 7

F6 125 115 11.8 0.2 1.5 32 60 217 4

F7 400 58 7.4 0 2.4 36 71 364 5

F8 100 115 6.7 0 1.7 37 67 248 4

F9 275 57 6.6 0 2.2 36 66 276 5

F10 100 438 3.8 0 2.4 33 57 281 4

F11 275 200 3 0 1.3 37 67 315 5

F12 100 20 2.7 0 1.5 35 66 241 7

F13 275 195.7 1.3 0 1.4 37 77 322 6

F14 250 71 1.1 0 1.7 44 83 343 10

F15 340 110 1 0 1.3 31 56 223 5

LWPF 300 700 1 29 53 216 15

The numbers of families and plant species are indicated, as well as their abundance and basal area.

The fragments are ranked according to size. Isolation = distance to the nearest fragment.aFragment size excluding a 100 m wide edge (see Methods).

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Garden). Ten 50 2 m transects were randomly located in each fragment and

in the LWPF. All species of trees, shrubs, lianas, palms and herbs with

dbh 2.5 cm were recorded. Species were classified according to the light theyrequire for germination: primary species (shade tolerant), secondary species

(shade intolerant), and NSLD (non-secondary light demanding) species. Sec-

ondary species regenerate only in clearings and at the forest edge. NSLD

species can survive in primary or secondary forest, but they need intense light

during the first stage of growth. This ecological group (EG) classification was

based on information from Flora of Veracruz and Neotropical Flora, as well as

several species lists (e.g., Popma et al. 1988; Martinez-Ramos and Alvarez-

Buylla 1995; Ibarra-Manrquez et al. 1997a). Species that appeared only once

in the entire 16000 m2 area we sampled in total were considered locally rare.

Species not identified in the field were collected for identification in the MEXU

(Institute of Biology, UNAM, Mexico, D.F.) and XAL (Institute of Ecology,

A.C., Xalapa, Veracruz) herbaria.

Comparison of fragments and LWPF

Differences in the plant diversity recorded for the 15 fragments and LWPF

were assessed by constructing mean individual-based accumulation curves after

100 randomizations using the EstimateS Program (Colwell 1997). Because theresulting curves underestimated species richness (Colwell and Coddington

1994), we used non-parametric methods provided by the EstimateS Program,

selecting the three methods that have been shown to be the best estimators of

species richness in the tropical rainforest of Costa Rica (Chazdon et al. 1998).

The incidence-based coverage estimators (ICE) Chao-2 and Jack-2 are based

on species incidence (presence/absence). Colwell and Coddington (1994) de-

scribe these methods in full.

Based on the sum of density (trees/unit of area), frequency (number of

transects in which each species appeared/total transects), and dominance (total

basal area for each species), the importance value index (IVI) was calculated

for each species in the 15 fragments and in LWPF (Moore and Chapman

1986). This index provides a more precise understanding of the importance of

different plant species in the fragments and the LWPF.

We quantified the number of species, species density, and the total arboreal

basal area (m2) for all species, as well as for the species of each ecological group

and life form, both in the 15 small fragments and in LWPF. The frequency of

individuals with varying diameter at breast height (dbh) ranges was also cal-

culated for each fragment and LWPF. To analyze the values obtained for the

two environments, Students t-test was used to compare a single observation ofLWPF with the mean from the 15 fragments sampled (Sokal and Rohlf 1995).

So rensens similarity index (S) was calculated between LWPF and each frag-

ment using the following formula: S = 2C/(A + B), where A is the number of

species in fragment i, B is the number of species in LWPF, and Cis the number

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of species found in both. The index was correlated with fragment size, shape,

and isolation. Differences in the proportion of individuals from each life form,

ecological group, and dbh range among the fragments and LWPF, werecompared with chi squared tests (Sokal and Rohlf 1995).

The effects of fragment size, shape, and isolation

To determine the influence of fragment size, shape, and isolation on the veg-

etation characteristics studied, forward stepwise multiple regression analysis

was performed, considering LWPF as the largest (700 ha), most regular frag-

ment (shape index = 1), with zero isolation. Fragment area was first log-

transformed to meet normality assumptions (ShapiroWilk test, p > 0.05). The

independent factors were species richness, density, and total basal area within

each forest fragment and in the LWPF, as well as for each life form and

ecological group. This type of multiple regression allows us to determine the

explanatory value of each independent factor included in the model, with the

beta value indicating their order of importance.

The edge effect exercises its greatest influence within 100 m of the forest edge

(Laurance and Yensen 1991; Laurance et al. 1998b, 2002) and so, to ascertain

the edge effect on fragmented vegetation, ArcView version 3.2 was used to

calculate fragment size by eliminating 100 m of edge from each fragment. Thisreduced size will henceforth be referred to as the fragment interior. With a one-

tailed t-test, we compared the vegetation characteristics mentioned for frag-

ments with and without the interior (Table 1). All analyses were done with

version 5.5 of the Statistica Program for Windows (Statsoft Inc. 2000).

Results

Floristic composition

We sampled a total area of 16000 m2 in 160 belt transects distributed

throughout 15 forest fragments and the LWPF. We recorded 4254 plants

belonging to 60 families, 120 genera, and 190 species. About 91.6% of the

species and 98.4% of the individuals were identified. In the fragments, the

families with the highest number of individuals were Euphorbiaceae (8% of all

plants recorded in fragments), Vochysiaceae (6%), Monimiaceae (6%), Viol-

aceae (4%), and Asteraceae (3%). In LWPF the best represented families were

Palmae (49% of all plants recorded in LWPF), Moraceae (5%), Meliaceae

(5%), Fabaceae (3%), and Euphorbiaceae (3%). In general, the most commonspecies were Astrocaryum mexicanum (Palmae) (323 individuals, 7.6% of the

total), Siparuna andina (Monimiaceae) (260, 6.1%), and Vochysia guatemal-

ensis (Vochysiaceae) (227, 5.3%), although there were differences between the

fragments and LWPF (Table 2).

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In the 15 fragments, certain secondary species were notably abundant,

representing 26% of all plants recorded in them: Siparuna andina

(Monimiaceae), Croton schiedeanus (Euphorbiaceae), and Eupatorium galeotti

(Asteraceae), along with NSLD species such asVochysia guatemalensis

(Vochysiaceae), Tapirira mexicana (Anacardiaceae), and Rinorea guatemalensis

(Violaceae). These species were not recorded in LWPF where the palm

Astrocaryum mexicanum represented 41.9% of all plants present; in fragments

it made up only 5.8% of the total (Table 2). So rensens index indicated that

fragments shared between 15 and 28% of those species found in LWPF, and

that the largest fragments shared a greater number species with LWPF than

smaller ones (R2 = 0.32, p = 0.03; Figure 2).

Species richness

The individual-based species accumulation curves showed that species richness

was far from completely recorded for all fragment sizes and LWPF with our

sampling effort (Figure 3). The three non-parametric estimators showed that

Table 2. Total and relative (%) abundance and basal area of the 10 species with the highest

importance value indices (IVI) for all fragments studied in Los Tuxtlas, Mexico.

Species Family EG Abundance Basal IVI

No. % m2 %

Small relatively unprotected fragments (n = 15)

Vochysia guatemalensis Vochysiaceae NSLD 227 5.6 6.6 6.7 15

Siparuna andina Monimiaceae Sec 260 6.4 1.5 1.5 14

Astrocaryum mexicanum Palmae Pri 233 5.8 0.6 0.6 12

Tapirira mexicana Anacardiaceae NSLD 163 4.0 6.4 6.5 12

Croton schiedeanus Euphorbiaceae Sec 150 3.7 1.3 1.4 10

Pseudolmedia oxyphyllaria Moraceae Pri 121 3.0 2.2 2.2 9

Rinorea guatemalensis Violaceae NSLD 143 3.5 0.6 0.6 8

Terminalia amazonia Combretaceae Pri 45 1.1 15.9 16 7

Dendropanax arboreus Araliaceae NSLD 65 1.6 2.7 2.8 6

Eupatorium galeotti Asteraceae Sec 117 2.9 0.3 0.3 6

Large well protected fragment (n = 1)

Astrocaryum mexicanum Palmae Pri 90 41.9 0.24 1.7 53

Poulsenia armata Moraceae Pri 5 2.3 2.18 15 22

Brosimum alicastrum Moraceae Pri 3 1.4 2.05 14 17

Dussia mexicana Fabaceae Pri 1 0.5 2.14 15 16

Nectandra ambigens Lauraceae Pri 3 1.4 1.64 11 15

Pseudolmedia oxyphyllaria Moraceae Pri 13 6.0 0.40 2.8 15

Cordia megalantha Boraginaceae NSLD 2 0.9 1.43 9.9 13

Guarea glabra race bijuga Meliaceae Pri 5 2.3 0.82 5.7 11Chamaedorea tepejilote Palmae Pri 14 6.5 0.01 0.1 10

Cynometra retusa Caesalpinaceae Pri 7 3.3 0.21 1.5 10

EG, ecological group; Pri, primary; Sec, secondary; NSLD, non-secondary light demanding spe-

cies.

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the average percentage (SD) of recorded species was low (67.4 5.1), and

was lower in LWPF and higher in the 3.8 and 1.1 ha fragments (Tables 1 and

3). Both the observed species richness and mean estimated richness were higher

in the 1.1 and 1.3 ha fragments (Tables 1 and 3). The lowest observed species

richness corresponded to LWPF and the largest fragment (75.6 ha), while the

lowest mean estimated species richness was for the 32.6 and 3.8 ha fragments.

As regards the ecological group classification, of 190 species, 43.2% wereprimary species, 22.6% were secondary species, 18.4% NSLD species, and

15.8% unclassified owing to the lack of relevant information in the literature.

On the basis of frequency of appearance, 21% of all recorded species were

represented by a sole individual (locally rare), while 40% had less than five

individuals (Table 4). Of these locally rare species, 40% were primary species,

22% NSLD species, 23% secondary species, and the rest unclassified. In

general, the richness of primary species that are locally rare and of those that

are very common (>16 individuals in all the samples) was higher in LWPF.

Nevertheless, there was no difference in the species richness of moderately

abundant (616 individuals) primary species between LWPF and the 15 frag-

ments (Table 4). The most common secondary species (>6 individuals) were

more abundant in the fragments than in LWPF, while in contrast locally rare

secondary species were more abundant in LWPF (Table 4). Similarly, the most

common NSLD species (>16 individuals) were more abundant in the frag-

ments than in the LWPF, though locally rare NSLD species were more

abundant in LWPF (Table 4).

Vegetation structure

Although there were no significant differences between the average number

(SD) of individuals in fragments (269 51) and in LWPF (t = 1.08,

df = 14, p = 0.30), the average basal area in fragments (6.6 2.4) was

Figure 2. Linear regression analysis between fragment size and So rensens similarity index,

comparing plant species composition between each fragment and a large well protected fragment(LWPF).

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Figure 3. Individual-based species accumulation curves (mean SD) for plants in a large wellprotected fragment (LWPF) and 15 forest fragments that are not as protected in Los Tuxtlas,

Mexico.

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significantly lower than that recorded for LWPF (t = 3.36, df = 14,

p < 0.005; Table 1). For ecological groups, when compared to fragments,

LWPF had proportionally greater richness (v2 = 13.76, df = 2, p < 0.001)

and abundance (v2 = 158.5, df = 2, p < 0.001) of primary species, while in

fragments, secondary and NSLD species dominated (Figure 4a). Nine of the 10

most important species in LWPF were primary, whereas in fragments, only

three out of 10 were primary species (Table 2).

Table 3. Species richness in forest fragments (n = 15) and a large well protected fragment

(LWPF) studied at Los Tuxtlas, Mexico.

Fragment Sobs Mean ICE Chao-2 Jack-2 Mean %

F1 53 13.3 (2.9) 94.3 82.7 90.1 89.0 (5.9) 59.6

F2 62 14.9 (3.6) 87.7 78.7 92.4 86.3 (7.0) 71.9

F3 53 16.3 (2.6) 74.0 70.4 79.5 74.6 (4.6) 71.0

F4 71 13.6 (3.0) 119.4 106 121.1 115.5 (8.2) 61.5

F5 70 17.2 (2.2) 105.4 91.4 106.5 101.1 (8.4) 69.3

F6 60 16.1 (3.8) 86.3 81.0 92.3 86.6 (5.5) 69.3

F7 71 19.8 (3.0) 101.2 93.0 106.2 100.1 (6.7) 70.9

F8 67 16.4 (2.2) 88.2 94.2 103.4 95.2 (7.7) 70.4

F9 65 16.3 (5.2) 96.2 96.6 104.8 99.2 (4.9) 65.5

F10 58 14.5 (2.9) 79.4 70.4 82.3 77.4 (6.2) 75.0F11 67 19.5 (4.3) 95.9 102.2 106.5 101.5 (5.4) 66.0

F12 61 14.3 (3.7) 89.4 76.0 90.0 85.1 (7.9) 71.7

F13 76 17.9 (4.1) 115.5 119.3 125.3 120 (4.9) 63.3

F14 84 22.2 (3.5) 113.6 109.9 124.6 116 (7.7) 72.4

F15 55 13.0 (5.3) 93.5 84.3 93.1 90.3 (5.2) 60.9

LWPF 52 11.0 (2.3) 98.8 77.1 88.7 88.2 (10.8) 59.0

The observed total species richness (Sobs) is indicated, as are the three different non-parametric

estimators based on the incidence of species (presence/absence): incidence-based coverage estimator

(ICE), Chao-2, and Jack-2 estimators. The mean (SD) of Sobs (per 50 2 m transect), the mean

(SD) of the three estimators, and the percentage of species recorded (Sobs/mean of estima-

tor 100) are also indicated. The fragments are ordered according to size (largest to smallest).

Table 4. Distribution of plant species according to their abundance in the 16000 m2 sampled at

Los Tuxtlas, Mexico.

Abundance No. of species Primary species Secondary species NSLD

LWPFa Fragments LWPF Fragments LWPF Fragments

1 40 9 (+) 0.4 (0.10.8) 2 (+) 0.4 (00.86) 6 (+) 0.2 (00.43)

25 36 8 (+) 0.9 (0.41.5) 1 (=) 1.1 (0.361.8) 1 (=) 0.7 (0.31)

615 46 7 (=) 6.8 (5.58.1) 1 () 1.9 (1.22.6) 3 (=) 2.3 (1.33.3)

1630 30 4 (+) 0.7 (0.21.1) 0 () 2 (1.52.5) 0 () 4.7 (2.75.5)

>30 38 6 (+) 2.3 (1.82.7) 1 () 7.2 (6.67.8) 1 () 6.3 (5.47.1)

The total number of species in each abundance class is indicated, as is the number of primary,secondary, and non-secondary light demanding (NSLD) species sampled in 1000 m2 of a large well

protected fragment (LWPF), as compared to the average number (95% CI) per 1000 m2 on the 15

fragments (CI).aRichness in LWPF is indicated as lower (), higher (+), or not different (=), with respect to the

95% confidence intervals given in parentheses for the fragments.

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Plants were distributed among life forms as follows: 78% of all species were

trees, 9% shrubs, 10% lianas, and 4% palms and herbs. In LWPF we found a

proportionally lower abundance of trees but a higher abundance of palms and

herbs (v2 = 46.6, df = 3, p < 0.001; Figure 4b). The chi square test did not

show significant differences in proportion for the richness or basal area ofdifferent life forms (Figure 4b), however a comparison of means in fragments

and LWPF revealed that the fragments were richer in trees (t = 2.69,

df = 14, p = 0.02) but less basal area of trees (t = 3.28, df = 14, p = 0.006),

as well as less basal area of palms and herbs (t = 5.32, df = 14, p < 0.001).

Figure 4. Percent richness, abundance, and basal area for species belonging to different (a) eco-

logical groups and (b) life forms in a large well protected fragment (LWPF) and in 15 forest

fragments that are relatively unprotected in Los Tuxtlas, Mexico. NSLD = non-secondary light

demanding species.

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With regard to dbh range, there were more thin plants in the fragments

(dbh 60 cm) than in LWPF

(v2

= 31.44, df = 13, p < 0.01). In particular, LWPF featured a greaterproportion of large primary trees (v2 = 6.59, df = 2, p < 0.05), as well as a

lower proportion of secondary individuals (v2 = 122.99, df = 2, p < 0.001)

and NSLD (v2 = 86.5, df = 2, p < 0.001) with dbh of less than 60 cm.

The relationship between vegetation and fragment characteristics

The stepwise regression analysis model indicated that 16 of the 32 dependent

factors analyzed were significant (Table 5). Fragment area best explained dif-

ferences in plant composition and structure as, for the most part, it was the

only independent factor with significant beta values. Fragment isolation was

the only factor that explained differences in the richness of primary species and

NSLD species among fragments, the relationship being negative for the former

but positive for the latter (Table 5). The strongest relationships were for NSLD

species abundance (63%), the basal area of primary species (53%), and the

abundance of palms and herbs (52%). For the remaining dependent factors,

the determination coefficients were below 0.40.

In general, we found that the smallest fragments had the greatest richness

and total abundance, but the lowest total basal area. In terms of ecological

Table 5. Significant results of stepwise multiple regression analysis between the vegetation factors

and size (Log-Area), isolation (distance to neighboring fragment), and shape index of the 16 forest

fragments studied at Los Tuxtlas, Mexico.

Vegetation characteristics R2 Log (Area) Isolation Shape

Total richness 0.24 n.s. 0.61* 0.25 n.s.

No. of primary species 0.27* 0.57*

No. of secondary species 0.48* 0.61* 0.29 n.s. 0.39 n.s.No. of NSLD species 0.39** 0.65**

No. of tree species 0.37* 0.67** 0.42 n.s.

Total abundance 0.21* 0.51*

Abundance of secondary species 0.22 n.s. 0.58* 0.31 n.s.

Abundance of NSLD species 0.63*** 0.64*** 0.37*

Abundance of trees 0.34** 0.62**

Abundance of palms and herbs 0.52*** 0.78*** 0.39 n.s.

Total basal area 0.45** 0.61** 0.25 n.s.

Basal area of primary species 0.53** 0.71*** 0.24 n.s. 0.25 n.s.

Basal area of trees 0.46** 0.61** 0.26 n.s.

Basal area of palms and herbs 0.49*** 0.78*** 0.36 n.s.

No. of individuals with dbh >1020 cm 0.37* 0.56* 0.58 n.s.

No. of individuals with dbh >60 cm 0.36* 0.57* 0.24 n.s.

The beta weights of independent factors and R2 of the multiple model are indicated.

*0.05 >p > 0.01; **0.01p > 0.001; ***p 0:001; () factor not included by the multiple

regression model.

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groups, fragment size was negatively related to secondary species richness,

species abundance and NSLD species abundance, but positively related to

primary species basal area. In the analysis based on life forms, fragment sizewas negatively related to tree richness and abundance but positively related to

tree basal area, and to the abundance and basal area of palms and herbs.

Finally, for dbh range, fragment size was negatively related to the frequency of

plants with 1020 cm dbh, but positively related to the number of trees

with >60 cm dbh (Table 5). We found a positive relationship between total

richness and secondary species richness (r = 0.57, p = 0.02) and also between

total abundance and secondary (r = 0.61, p = 0.01) and NSLD (r = 0.60,

p = 0.015) species abundances.

Once 100 m had been eliminated from the edge to test for the edge effect,

most fragments (73%) had no interior, leaving only four that did (Table 1).

Although fragments F4 and F5 are larger than F6, they have no interior owing

to their irregular shape. Fragments with an interior had lower total species

richness (t = 2.52, df = 13, p = 0.025) and fewer secondary species

(t = 2.29, df = 13, p = 0.04) than LWPF. Although not significant, in

fragments with an interior we noted that total basal area was larger (t = 2.07,

df = 13, p = 0.06) and the abundance of secondary species was lower

(t = 2.08, df = 13, p = 0.06) than in LWPF.

Discussion

Although the Gentrys (1982) methodology was designed principally for the

study of species diversity, and the sample size (0.1 ha) per fragment may be too

small to accurately characterize a plant communitys composition and struc-

ture, our results strongly suggest that in the fragments we studied, the com-

position and structure of vegetation have been subjected to disturbance. While

it is true that compared to LWPF, the fragments exhibit greater richness and

abundance of trees, they were thinner and belonged to secondary and NSLD

species. In the fragments, we found a smaller total basal area, resulting prin-

cipally from the lack of large primary trees in the canopy and to the decreased

abundance and basal area of palms and herbs in the understory. Our results

indicate that fragment size is the factor that best explains differences in plant

composition and structure, with the largest fragments being the most similar to

LWPF.

Differences between the fragments and LWPF

The fact that the richness and abundance of species adapted to life in altered

environments are higher in these fragments indicates that their vegetation is

quite altered. Thus, although it has been reported that the palm Astrocaryum

mexicanum is the most abundant and characteristic plant in Los Tuxtlas

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(Pin ero et al. 1977; Ibarra-Manrquez et al. 1997), it was only the third most

important in these fragments. This could be because it is a primary species that

is very sensitive to the microenvironmental conditions characteristic of theforest edge (Pin ero et al. 1986). Other primary species such as Dialium guian-

ense, Tapirira mexicana, Cynometra retusa, Zanthoxylon kellermanii, and

Pseudolmedia oxyphyllaria all typical of well protected tropical forest in the

region (Bongers et al. 1988; Martinez-Ramos and Alvarez-Buylla 1995; Ibarra-

Manrquez et al. 1997) appeared quite rarely in the fragments, where the

most important species were Croton schiedeanus, Siparuna andina, Rinorea

guatemalensis, andVochysia guatemalensis; all species adapted to life in full-sun

conditions. This agrees with the findings from other studies of tropical forest,

where fragmentation has been reported to favor the colonization of shade

intolerant species (Bentez-Malvido 1999; Hill and Curran 2003). Therefore,

although it is still possible to find arboreal elements typical of well preserved

forest, both the abundance of secondary species and the lack of certain primary

species suggest that these fragments have highly altered flora.

Our results suggest that secondary and NSLD species form an important

part of the regions diversity. Compared with LWPF, the fragments had a

greater diversity of secondary and NSLD species. We recorded a lower pro-

portion of large trees (dbh > 60 cm) in fragments than in LWPF, which may

be promoting the opening of gaps and the establishment of light-demanding

species at the expense of shade tolerant species (e.g., Saunders et al. 1991;Bentez-Malvido 1998). In this sense, we found that the main species missing

from fragments are locally rare primary species. Hence, we can corroborate

Va zquez-Yan ess (1980) position that secondary and NSLD species are sig-

nificantly contributing to the species diversity of the landscape in this highly

fragmented region. Therefore, if we also want to protect the primary species

typical of unaltered tropical forest, it is necessary to conserve the largest

fragments, as they have largest interior areas free from edge effects (e.g.,

Laurance et al. 2002).

The low proportion of large trees and the great abundance of thin individ-

uals (dbh < 20 cm) in the fragments as compared to LWPF (as well as to the

habitats described by Sarukha n 1968; Pin ero et al. 1977; Bongers et al. 1988)

indicate that their vegetation structure has been notably disturbed. Although

the mean basal area extrapolated to one hectare (66 2 m2/ha) fell within the

range reported by Sarukha n (1968) for this type of forest (4575 m2/ha), six of

the 15 fragments had basal areas near the minimum reported by this author.

Overall, these results are in accordance with those of other studies conducted in

Los Tuxtlas region (Va zquez-Yan es 1980; Popma et al. 1988; Martinez-Ramos

and Alvarez-Buylla 1995) and in the Brazilian Amazon (Malcolm 1994;

Bentez-Malvido 1998; Laurance et al. 2002; Bentez-Malvido and Martnez-Ramos 2003a, b), where the plant structure in fragments is commonly found to

be altered, as the tree mortality rate increases (Laurance et al. 1998a, b, 2000)

and the recruitment of small plants in forest clearings and near edges increases

(Malcolm 1994; Bentez-Malvido 1998; Jules 1998; Gigord et al. 1999).

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The effect of fragment size, shape, and degree of isolation

Fragment size was the factor that best explained the differences we observed inplant composition and structure. The species composition of the largest frag-

ments was quite similar to that of LWPF. Fragment area was positively related

to the number of large (dbh > 60 cm) trees, total basal area, and the basal area

of trees and primary species. In contrast, the smallest and most irregular

fragments had the greatest richness and abundance of secondary species,

a greater abundance of NSLD species, a greater abundance of plants with

dbh >1020 cm, and a lower abundance and basal area of palms and herbs.

These data agree with those of other reports in tropical forest that have shown

that fragment size has a marked influence on vegetation composition and

structure. Smaller fragments exhibit more edge effects, thereby increasing the

mortality of large primary trees, and favoring the growth of secondary species

(e.g., Bentez-Malvido 1998; Didham and Lawton 1999; Hill and Curran 2003;

Bentez-Malvido and Martnez-Ramos 2003b). Restoration efforts must seek

to reduce the edge effects in order to protect the diversity and structure of this

tropical rain forest.

Although we expected the largest fragments, being the most heterogeneous,

to have more species than the smaller fragments, this study showed no sig-

nificant linear relationship between fragment size and total species richness.

This could be a consequence of sampling effects. Since the analysis with non-parametric estimators of species richness showed that the LWPF and the

largest fragment had a lower percentage of the expected species recorded than

the smaller fragments, it is possible that our sampling effort was too low to

detect differences in species richness. There are, however, other significant

factors that can reduce the differences in species richness between fragments.

For example, the higher number of secondary species recorded in smaller

fragments would increase the total species richness in these fragments. Fur-

thermore, if we assume that edge effects occur mainly within 100 m of the edge

(Laurance and Yensen 1991; Laurance et al. 1998a, b), given that most of the

fragments are smaller than 20 ha, fragments would be expected to exhibit quite

similar floristic composition and species richness. In this sense, by eliminating

100 m of edge, we demonstrated that fragments with an interior had lower

richness and abundance of secondary species than fragments without interior,

while their basal area was greater. Finally, another factor is the relatively short

time since fragmentation occurred (Turner et al. 1996; Dislich and Pivello

2002). At the study site, most of the fragments have been isolated for less than

20 or 30 years (Guevara et al. 2004). Since most of the primary arboreal ele-

ments of high unaltered forest can live for many decades (Martnez-Ramos and

Alvarez-Buylla 1995), the persistence of these trees can diminish the differencesin species richness.

Fragment isolation was associated negatively and significantly with primary

species richness, but positively with both the richness and abundance of

NSLD species. The most isolated fragments also tended to exhibit greater

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richness of secondary species but had a lower total basal area, a lower basal

area of primary species, and fewer large trees. Since most tropical trees,

shrubs, and lianas are dispersed by animals (Gentry 1982; Ibarra-Manrquezet al. 1991), and given that Los Tuxtlas has suffered a particularly severe loss

of fauna (Dirzo and Miranda 1990), fragment isolation may be modifying the

dispersal capacity of many plants, which would in turn alter the composition

and structure of forest fragment vegetation. Our results suggest that this

process is negatively affecting the primary species, while in contrast secondary

and NSLD species seem to be positively affected by fragment isolation.

Augspurger and Franson (1988; for neotropical forest) and McDonell and

Stiles (1983; for temperate forest) reported that anemochorous species are

abundant in light gaps and regenerating forest. In Los Tuxtlas there are a lot

of wind dispersed secondary and NSLD species (Ibarra-Manrquez et al.

1991). Since the main component of the surrounding matrix is pasture, and

there are heavy winds coming from the Gulf of Mexico (Soto and Gama

1997), increased isolation may be positively affecting these light-demanding

anemochorous species. Nevertheless, the loss of fauna in Los Tuxtlas (Dirzo

and Miranda 1990) could be negatively affecting most of the primary

zoochorous species. Further research is necessary to understand how frag-

mentation can alter the different dispersal vectors and hence, plant species

diversity.

Conservation implications

Of what value are forest fragments for the conservation of tropical rain

forest diversity at the landscape scale? Our results clearly indicate that

as fragments become smaller, more irregularly shaped and more isolated,

their floristic composition, species diversity, and arboreal structure are

increasingly radically modified. Thus, for example, a 1-ha fragment does not

represent a random sample of 1 ha from a large well protected tropical rain

forest. As a result, from the perspective of conserving original tropical

forest, as fragments become smaller, their conservation importance also

decreases.

Similar to proposals for the conservation of bird diversity (Estrada et al.

2000), bats (Estrada and Coates-Estrada 2001), land mammals (Estrada et al.

1994), and specifically for primates (Estrada and Coates-Estrada 1996;

Mandujano et al. 2006; Arroyo-Rodrguez and Mandujano in press), our re-

sults support a landscape-oriented proposal for conserving plant diversity in

the region. It is thus necessary to maintain as many large fragments as possible;

furthermore, policies must be established that prevent the reduction and iso-lation of forest remnants. Considering that expanses of pasture devoid of trees

is the extreme outcome of continual reduction in fragment size, the conser-

vation of even small fragments is a worthy endeavor given that they still

contain shrub and tree species typical of the original tropical forest and thereby

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represent an important part of the genetic diversity of the region. The urgent

need to conserve the most extensive areas of well protected tropical forest

cannot be overstated. In regions where there has been considerable loss andfragmentation of forest, however, the conservation of the greatest diversity will

only be possible at the landscape, not fragment, level (da Silva and Tabarelli

2000). In this regard, subsequent studies will allow us to evaluate the spatial

configuration of elements in a landscape that maximizes the species diversity of

tropical rain forest on those landscapes.

The numerous negative effects of fragmentation are due to post-fragmen-

tation extraction of forest products and other anthropogenic activities, these

being more severe in unprotected areas. Even though the landscape we studied

is one of the buffer zones of the Los Tuxtlas Biosphere Reserve, some

anthropogenic activities were observed in the fragments during this study. For

example, the inhabitants of this region often remove plants from the lower

layer to allow cattle to enter the fragments (they use them for shade). Tree

felling was also observed, since the local population uses wood to build their

houses, and for fuel. In a study of 860 native flowering plant species of Los

Tuxtlas, Ibarra-Manrquez et al. (1997b) reported that 19% was employed by

the local population as timber, for fuel, for ornamental purposes, for edible

fruit, leaves or flowers, and for artwork. Since 66.3% of these species were

recorded for our study sites, it is possible that the post-fragmentation

extraction of forest products is significantly modifying the vegetation of theseforest remnants. Since small forest fragments are easier to access, and most

(81%) of the fragments we studied were smaller than 5 ha, urgent protection

measures are required to reduce the potential impact of this anthropogenic

activities on the smallest forest fragments. Given that we cannot evaluate the

long term outcome of these activities, further research is necessary to quantify

the impact of human activities on plant composition, species diversity and

forest structure.

Acknowledgments

The authors would like to thank the Instituto de Ecologa, A.C. The first

author was granted a scholarship by the Universidad Auto noma de Madrid

and Santander-Central Hispano Bank. R. Mateo-Gutie rrez assisted with

fieldwork. F. Gonza lez-Medrano (Institute of Biology, UNAM) and

G. Castillo-Campos (INECOL) helped with species identification and classi-

fication. R. Palacios-Silva provided GIS support. F. Escobar made valuable

comments on the first draft. J. Bentez-Malvido, D. Pin ero, S. Guevara andJ. Laborde made valuable suggestions on how to improve the final manuscript.

Finally, we are grateful to B. Delfosse for editing the final version of the

manuscript in English.

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