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Soil Seed Banks and Regeneration of Neotropical Dry Deciduous and Gallery Forests in

Augusto Uasuf1 Mulualem Tigabu2 Per Christer Odén2

1University of Freiburg 79085 Freiburg Germany 2 Faculty of Forest Sciences Southern Swedish Forest Research Centre PO Box 44 230 53 Alnarp Sweden

Photograph 1. Firewood extraction from the Chacocente Wildlife Refuge, Nicaragua, which is a typical anthropogenic disturbance of tropical dry forests Photo by Guillermo Castro-Marin. 5PtsUas299:280doschun 02/03/09 18:34 Page50

50 BOIS ET FORÊTS DES TROPIQUES, 2009, N° 299 (1) FOCUS / REGENERATION OF NEOTROPICAL DRY FORESTS A. Uasuf, M. Tigabu, P. C. Odén

RÉSUMÉ ABSTRACT RESUMEN

RÔLE DES BANQUES DE SEMENCES SOIL SEED BANKS AND PAPEL DE LOS BANCOS DE SEMILLAS DU SOL DANS LA RÉGÉNÉRATION REGENERATION OF NEOTROPICAL DEL SUELO EN LA REGENERACIÓN DE DES FORÊTS SÈCHES DE FEUILLUS DRY DECIDUOUS AND GALLERY BOSQUES SECOS DE FRONDOSAS ET DES FORÊTS-GALERIES EN ZONE FORESTS IN NICARAGUA Y DE GALERÍA EN LA ZONA NÉOTROPICALE DU NICARAGUA NEOTROPICAL NICARAGÜENSE

Le déclin des forêts sèches tropicales et la Today, the depletion of tropical dry El declive de los bosques secos tropicales y nécessité de les restaurer sont aujourd’hui forests and the need for their restora- la necesidad de restaurarlos son realida- des réalités largement reconnues. Pour la tion are well recognized. In restoring des ampliamente aceptadas hoy en día. restauration de forêts dégradées, la pre- degraded forests, the first step is to Para la restauración de bosques degrada- mière étape consiste toujours à quantifier quantify the actual and potential levels dos, la primera etapa sigue consistiendo les niveaux réels et potentiels de régénéra- of natural regeneration, examining the en cuantificar los niveles reales y potencia- tion naturelle, en analysant le rôle des role of soil seed banks as propagule les de regeneración natural, analizando el banques de semences du sol dans la dis- donors. In this study, we assessed the papel de los bancos de semillas del suelo sémination de propagules. Pour cette composition, density and spatial distri- en la diseminación de propágulos. Para étude, nous avons évalué la composition, bution of the soil seed bank and este estudio, se evaluó la composición, la densité et la distribution spatiale de la seedling populations in dry deciduous densidad y distribución espacial del banco banque de semences du sol et des popu- and gallery forests of the Chacocente de semillas del suelo y de las poblaciones lations de jeunes dans les forêts Wildlife Refuge in Nicaragua. A total of de plantitas silvestres en los bosques sèches de feuillus et les forêts-galeries du 17 species were found in the soil seed secos de frondosas y los bosques de gale- refuge de Chacocente au Nicaragua. Au bank of the deciduous forest, with a ría del refugio de Chacocente en Nicaragua. total, 17 espèces ont été repérées dans la viable seed density of 466 seeds/m2. Se identificó un total de 17 especies en el banque de semences du sol dans la forêt In the gallery forest, a total of 24 banco de semillas del suelo en el bosque de feuillus, avec une densité de semences species were found in the soil seed de frondosas, con una densidad de semi- viables de 466 semen ces/m2. Dans la bank with a viable seed density of llas viables de 466 semillas/m2. En el bos- forêt-galerie, 24 espèces ont été repérées 1257 seeds/m2. The spatial analysis of que de galería, se identificaron 24 especies dans la banque de semences du sol, avec the soil seed bank revealed clumped en el banco de semillas del suelo, con una une densité viable de 1 257 semences/m2. and uniform distributions in both densidad viable de 1257 semillas/m2. El Une analyse spatiale de la banque de forests, depending on the species. The análisis espacial del banco de semillas semences a révélé des répartitions par total seedling density in the deciduous reveló distribuciones agrupadas o unifor- paquets ou uniformes dans les deux types and gallery forests was 6250 and 6600 mes en ambos tipos de bosque, depen- de forêts, suivant les essences. La densité individuals/ha, respectively. The spa- diendo de las especies. La densidad global globale des jeunes plants dans les forêts à tial distribution of seedling popula- de plantas jóvenes en los bosques de fron- feuillus et les forêts-galeries s’établissent tions varied from clumped to uniform dosas y en los de galería es, respectiva- respectivement à 6 250 et 6 600 indivi- depending on the species. The similar- mente, de 6250 y 6600 individuos/ha. En dus/ha. En termes de distribution spatiale, ity between the soil seed bank, cuanto a la distribución espacial, los roda- les peuplements de jeunes plants sont seedling layer and above-ground vege- les de plantas jóvenes se reparten por gru- répartis par paquets ou uniformément, tation was low in both forest sites. It pos o uniformemente, dependiendo de las suivant les essences. La similitude entre may be concluded that the number of especies. El índice de similitud entre el banque de semences du sol, couche de seed bank species and the quantity of banco de semillas del suelo, la capa de jeunes plants et végétation aérienne est soil-stored seeds are relatively low. plantas jóvenes y la vegetación aérea es faible sur les deux sites. Cela permet de Regeneration was abundant in some bajo en ambos sitios. Esto permite concluir conclure que le nombre d’espèces dans species, but poor in many others. The que el número de especies en los bancos les banques de semences du sol et la natural regeneration process should de semillas del suelo y la cantidad de semi- quantité de semences stockées dans le therefore be assisted through direct llas almacenadas en el suelo es relativa- sol sont relativement faibles. La régénéra- seeding, planting seedlings and mente escaso. La regeneración es abun- tion est abondante pour certaines manipulation of the site to improve dante en algunas especies, pero baja en essences mais faible pour d’autres. Il environmental conditions for seedling otras. Por ello, es conveniente ayudar al convient donc d’assister le processus de establishment and growth. proceso de regeneración natural mediante régénération naturelle par ensemence- siembra directa, establecimiento de plan- ment direct, établissement de jeunes Keywords: tropical dry forest, tas jóvenes y adecuación de los sitios para plants et aménagement des sites afin seedling bank, spatial pattern, mejorar las condiciones de arraigo y creci- d’améliorer les conditions de prise et de Morisita’s index, restoration. miento de las plantas jóvenes. croissance des jeunes plants. Palabras clave: bosque tropical seco, Mots-clés : forêt tropicale sèche, banco de semillas del suelo, distribu- banque de semences du sol, distri- ción espacial, índice de Morisita, res- bution spatiale, index de Morisita, tauración. restauration. 5PtsUas299:280doschun 02/03/09 18:34 Page51

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Introduction 1997; Vallejo et al., 2006). Natural regeneration is the cheapest approach Tropical dry forests are among for rehabilitating degraded forest the most severely degraded and ecosystems, provided that the previ- threatened forest ecosystems in Cen- ous disturbance has left some residu- tral America (Janzen, 2002). Histori- als (e.g. soil seed banks, mother trees cally, these forest formations have or root shoots) that can serve as “suc- been extensively converted into other cession primers”. The first step in any Photograph 2. land uses, such as crop fields and/or forest restoration endeavour is there- A typical Neotropical dry forest formation in range lands (Gillespie, 1999). Forest fore a site assessment to quantify the Chacocente Wildlife Refuge, Nicaragua remnants probably represent less actual and potential levels of natural Photo by Guillermo Castro-Marin. than 2% of the original dry forest regeneration, to examine the presence along the Pacific coast of Mesoamer- of “succession primers” and to deter- This study was carried out at Cha- ica, an area extending from to mine whether intervention is needed cocente Wildlife Refuge in Nicaragua, western (Sabogal & Valerio, to accelerate the natural regeneration which was established in 1983 to pro- 1998). Nicaragua is the largest coun- process (Wijdeven & Kuzee, 2000). tect the remaining fragments of tropical try in (land area ca. In the restoration of commu- dry forest along the Central American 130 000 km2), and its tropical dry for- nities in degraded forests, the idea of Pacific coast as well as the nesting est areas cover ca. 2 500 km2, repre- exploiting soil seed banks may sound beaches of endangered species of senting 2.1% of the total forest cover attractive. The soil seed bank refers to marine turtles, the olive ridley (Lepi- (Roldan, 2001). Tropical dry forests all viable seeds and fruits present on or dochelys olivacea) and leatherback have been under heavy pressure from, in the soil and associated litter/humus. (Dermochelys coriacea) (Anonymous, among others, extensive ranching dur- Soil seed banks can be either transient, 2002). Despite natural and anthro- ing the 1960s and 1970s (Janzen, with seeds that germinate within a year pogenic disturbances (photograph 1) 2002). In addition, since the begin- of initial dispersal, or persistent, with due to commercial timber extraction (of ning of the last century, there has seeds that remain in the soil for more species such as Swietenia humilis, been extensive harvesting of commer- than 1 year (Simpson et al., 1989). Cedrela odorata, Bombacopsis quinata, cially valuable species for export, They exhibit spatial and temporal varia- Dalbergia retusa, Guaicum sanctum), such as Swietenia humilis, Guaiacum tions, reflecting their initial dispersal illegal felling for local consumption, sanctum, Cedrela odorata, Dalbergia onto the soil and subsequent move- conversion to agricultural lands and fire retusa and Bombacopsis quinatum. ment (Simpson et al., 1989). The pool (Roldan, 2001), the Chacocente Although the primary dry forest of long-lived seeds in the soil accumu- Wildlife Refuge is still one of the rela- has almost disappeared along the lates over many decades and forms a tively intact dry forest formations with Pacific coast, there are remaining frag- source of propagules that ensures con- distinct dry deciduous (photograph 2) ments or patches of dry forests tinual occupation of a site after distur- and gallery (photograph 3) forests. It (Janzen, 2002). These remaining frag- bances, while serving as a gene pool by thus offers invaluable opportunities for ments are considered to be the most buffering genetic changes in the popu- research on the restoration of degraded endangered ecosystems in the low- lation. An understanding of soil seed tropical dry forests in Central America. land tropics, and immediate restora- bank dynamics in degraded forests, The general aim of this study was to tion measures are urgently needed which include gains through seed rain, gain knowledge about the soil seed (Janzen, 2002). Restoration or, more losses due to seed predation, seed bank and the extent of natural regener- strictly speaking, ecological restora- death and transfer into the active seed ation in dry deciduous and gallery tion, is defined by the Society for bank to germinate and form a seedling forests that can be used for the restora- Ecological Restoration as “the process bank, is paramount before deciding tion of such disturbed forest ecosys- of assisting the recovery and manage- whether intervention is needed to tems. The specific objectives were: ment of ecological integrity. Ecological assist the natural regeneration process. 1) to determine the composition, integrity includes a critical range of Natural regeneration is also heteroge- density, and spatial distribution of variability in biodiversity, ecological neous across the landscape, depend- the soil seed bank, processes and structures, regional and ing on seed dispersal, viability, dor- 2) to determine the floristic composi- historical context, and sustainable cul- mancy, predation, herbivory, rainfall tion, density and spatial distribution tural practice”. Four possible methods and topographic, edaphic and light of naturally regenerating seedlings of for restoring natural vegetation exist: conditions (Khurana & Singh 2001; woody species, and (i) natural regeneration, (ii) direct Enoki & Abe 2004). Determining the 3) to analyze the relationships seeding, (iii) planting seedlings, and spatial patterns of natural regeneration between the soil seed banks and the (iv) incorporating restoration goals in is therefore also essential in designing standing vegetation in dry deciduous plantation programs (Lamb et al., an appropriate restoration technique. and gallery forests. 5PtsUas299:280doschun 02/03/09 18:34 Page52

52 BOIS ET FORÊTS DES TROPIQUES, 2009, N° 299 (1) FOCUS / REGENERATION OF NEOTROPICAL DRY FORESTS

Materials and Methods

Study area

The study was carried out in Chacocente Wildlife Refuge (11°30’ - 11°35’ N and 86°08’ - 86°14’ W), on the south-west Pacific coast of Nicaragua (figure 1). The Refuge con- sists of closed dry deciduous forest (1 099 ha), gallery forest (471 ha), open low forest (1 842 ha), fallows (554 ha), cropland (311 ha), grass- land (294 ha), and beach areas (71 ha) (Anonymous, 2002). The gallery forest, defined as narrow patches along the fringes of semi- permanent watercourses, occurs along the main water course, the Río Escalante. Chacocente has a 7-month dry season with less than 50 mm pre- cipitation per month. During the rainy season (June-October), rainfall is irregular with many days without rain- fall (Anonymous 2002). Mean annual precipitation during the last 14 years (1990-2003) was 1 422 mm, with a maximum in 1995 (1 962 mm) and a minimum in 1991 (991 mm). Mean monthly maximum and mini- mum temperatures were 28.3ºC and 26.2ºC respectively. Soils in the dry Figure 1. deciduous forest type are classified Location of the Chacocente Wildlife Refuge, Nicaragua, as Vertic and Ferric Luvisols (Sabogal where the present study was conducted. & Valerio 1998) while those in the gallery forest are Eutric Fluvisols. ners in order to get a better representa- seeds recovered by sieving was deter- Soil seed bank tion of the soil sample (figure 2). From mined by germination and cutting tests assessment each quadrat, four soil layers of 3 cm after they were identified. Germination thickness each to a depth of 12 cm tests were carried out with Jacobsen’s In each of the dry deciduous and (0-3, 3-6, 6-9 and 9-12 cm) were col- apparatus at 20 ± 2°C with illumination gallery forests, two permanent sample lected using a sharp knife and spoon. of ca. 20 mE m-2 s-1 (Fluorescent lamp plots were established in 1994 by Uni- Soil samples taken from each quadrat F 40 W / 33 RS cool white light) for six versidad Nacional Agraria, Managua, within a subplot were mixed to form a weeks. After six weeks of incubation, Nicaragua, to monitor changes in biodi- soil composite, in order to reduce vari- the viability of seeds that had not ger- versity. The area of each permanent ability within the sub plots. The soil minated was assessed by cutting. plot was 1.0 ha, as in the case of most samples per subplot were then put in Seeds with a firm white embryo were biodiversity monitoring plots in the separate plastic bags with the relevant considered viable while seeds that Neotropics, and each was further information. To recover seeds from the were covered with fungi, collapsed divided into 25 subplots of 20 × 20 m soil, the soil samples were sieved with when pinched and had grey, yellow, or to carry out detailed inventories. In different mesh sizes ranging from brownish embryos were considered each subplot (20 × 20 m) within each 0.5 mm to 5 mm, on the assumption dead (Teketay & Granström, 1995; forest type, two quadrats measuring that seed sizes of most woody species Baskin & Baskin, 1998). 15 × 15 cm were laid in opposite cor- fall within this range. The viability of 5PtsUas299:280doschun 02/03/09 18:34 Page53

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Total sampling area Alternated samples in successive subplots

Inventory of the standing 1 2 3 4 5 vegetation

Species composition and the number of individuals making up the standing vegetation (seedlings, 6 7 8 9 10 saplings and mature trees) were assessed in each of the permanent plots. In this study, seedlings were considered as individuals ≤ 150 cm in height (Teketay, 1997), saplings as 11 12 13 14 15 individuals between 1.5 and 4 m in height, and mature trees as individu- als ≥ 5 cm in diameter at breast height (dbh). To assess seedling pop- ulations, two quadrats of 2 × 2 m 16 17 18 19 20 were laid in opposite corners of each 20 x 20 m subplot (figure 2), while the populations of both saplings and mature trees were assessed in each of the 25 subplots (20 × 20 m). 21 22 23 24 25

Data analysis 15 x 15 cm The soil seed flora was identi- fied to species level with the assis- tance of Faculty members of 2 x 2 m Universidad Nacional Agraria (Nicaragua) and relevant literature (Salas, 1993). The standing vegeta- 20 x 20 m tion (seedlings, saplings and mature trees) was also identified to species Figure 2. level. Density and vertical distribu- Lay-out of sampling design employed for assessing the soil seed bank, seedling populations and aboveground vegetation in the dry deciduous tion of seeds in the soil as well as the and gallery forests of the Chacocente Wildlife Refuge, Nicaragua. density of seedlings were determined using simple mathematical calcula- tions. Sorensen’s similarity index sapling and adult tree species in the values for Morisita’s index were cal- (Krebs, 1999) was used to compare deciduous forest but not in the culated using the following formulae: the similarity between the species gallery forest). Sorensen’s coefficient Uniform index = composition of the soil seed bank ranges from zero (no species in com- and the above-ground vegetation mon) to 1.0 (identical set of species). (seedlings, saplings and mature The spatial distribution of seeds trees) as well as between seedlings and seedlings across the study site Clumped index = and the upper canopy using the fol- was analyzed using the standardized lowing formula: Morisita index, which is independent of population density and size (Krebs, 1999). First, Morisita’s index Where and (values of Ss(Sorensen’s similarity coeffi- (Id) was calculated using the follow- chi-squared with (n-1) degrees of cient), a (number of seed bank/ ing formula: freedom that has 97.5% and 2.5% of seedling/sapling and adult tree the area to the right, respectively); Xi species present in deciduous forest (Number of seeds/seedlings in sub- and gallery forest), b (number of seed plot) i and n (Number of subplots). bank/seedling/sapling and adult Where Xi (the number of The standardized Morisita index (Ip) tree species present in the gallery for- seeds/seedlings of a species in i was then calculated with one of the est but not in the deciduous forest), c subplots), Q (the number of sub- following three formulae: (number of seed bank/seedling/ plots) and N = ∑ Xi. Then two critical 5PtsUas299:280doschun 02/03/09 18:34 Page54

54 BOIS ET FORÊTS DES TROPIQUES, 2009, N° 299 (1) FOCUS / REGENERATION OF NEOTROPICAL DRY FORESTS

1) ;

When Id ≥ Mc > 1.0,

2) ;

When Mc > Id ≥ 1.0, or

3) ;

When 1.0 > Id > Mu The standardized Morisita index of dispersion ranges from -1 to +1 with 95% confidence limits at ± 0.5. A random pattern gives a value of zero, a clumped pattern is above zero and a uniform pattern below zero (Krebs, 1999). In the analysis of spatial pat- Photograph 3. terns, species with at least two seeds The evergreen gallery forest along the Río Escalante in Chacocente Wildlife or seedlings were considered. Refuge, Nicaragua Photo by Guillermo Castro-Marin.

a Deciduous forest 1 200 1 000 800 600 400

Seed density 200 0 1234 soil depth class

b Gallery forest 6 000 5 000 4 000 3 000 2 000

Seed density 1 000 0 1234 soil depth class

Figure 3. Vertical distribution of seeds recovered from soil samples collected from deciduous (a) and gallery (b) forests. Chacocente Wildlife Refuge, Nicaragua. 5PtsUas299:280doschun 02/03/09 18:35 Page55

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Table 1. Density (seeds/m²), frequency and viability of seeds recovered from soil samples.

Species Family/Subfamily LF** Density Frequency% Viability

A Dry deciduous forest

Allophylus psilospermus Sapindaceae T 333 24 20 Bixa orellanea* Bixaceae S 22 4 100 Caesalpinia coriaria Caesalpinioideae T 22 4 100 Canavalia sp.* Caesalpinioideae H 133 8 100 Casearia tremula Flacourtiaceae T 22 40 Cenchrus echinatus Poaceae G 22 40 Centrosema sp. Papilionoideae L 67 80 Chomelia speciosa T 133 16 50 Eleusine indica Poaceae G 67 40 Hybanthus attenuatus Violaceae L 22 40 Lysiloma divaricatum Mimosoideae T 244 20 0 Myrospermum frutescens Papilionoideae T 44 80 Paspalum sp. Poaceae G 67 12 0 Stemmadenia obovata Apocynaceae T 89 12 75 Tabernaemontana sp. Apocynaceae T 22 40 Tithonia rotundifolia* Asteraceae H 22 4 100 Trichilia hirta* Meliaceae T 67 8 100

B Gallery forest

Achotocarpus nigricans Achotocarpaceae T 22 40 Alvaradoa amorphoides Simaroubaceae T 2 511 48 19 Apeiba tibourbou Tiliaceae T 111 16 0 Bursera simarouba Burseraceae T 67 8 100 Cenchrus echinatus Poaceae G 22 4 100 Chomelia speciosa* Rubiaceae T 556 36 28 Coursetia elliptica Papilionoideae T 111 80 Cucumis anguria Cucurbitaceae H 22 40 Erythroxylum havanense Erythroxylaceae T 67 80 Esenbeckia litoralis Rutaceae T 22 40 Guazuma ulmifolia Sterculiaceae T 689 20 13 Karwinskia calderonii Rhamnaceae T 178 24 13 Luehea speciosa Tiliaceae T 1 289 28 26 Phyllanthus amarus Euphobiaceae H 267 16 0 Pithecellobium saman Mimosoideae T 22 40 Priva lappulacea Verbenaceae H 156 40 Sida acuta Malvaceae H 133 40 Sida rhombifolia Malvaceae H 67 40 Simarouba glauca* Simaroubaceae T 511 16 17 Spondias mombin Anacardiaceae T 22 40 Tabernaemontana sp. Apocynaceae T 22 40 Terminalia oblonga Combretaceae T 133 80 Trichilia hirta Meliaceae T 67 80 Waltheria americana Sterculiaceae H 22 40

* Seeds with physical dormancy ** LF = Life forms (T = trees, G = grass, H = herbaceous plants) 5PtsUas299:280doschun 02/03/09 18:35 Page56

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Results the sample plots, respectively. In the Chomelia speciosa and Stemmadenia gallery forest, the total numbers of obovata, had a high proportion of Composition and density species and seeds recovered from all viable seeds, as determined by the of the soil seed bank soil samples were 24 and 319, respec- cutting test. In contrast, some seeds tively. Trees had the highest number of of Allophylus psilospermus had undif- The total number of species recov- species (17) and seeds (288), account- ferentiated embryos when closely ered from the soil samples collected in ing for 90% of the total seed density examined after dissection. Species the deciduous forest was 17, represent- (7 088 seeds/m2) and 98% of the total with hard seed coats, such as ing trees, shrubs, herbs, grasses and viable seed density (1 257 seeds/m2), Canavalia sp., responded positively climbers (table IA). Fabaceae made up while the remaining 10% was distrib- to germination after mechanical scari- the dominant family with five species, uted between herbs and grasses (table fication. It should be noted that most followed by Poaceae with three species. IB). The tree species with significant of the species with 100% seed viabil- The total number of seeds obtained representation in the soil seed bank ity had one or two seeds in total. A from all soil samples collected down to were Alvaradoa amorphoides, Chome- similar trend was observed for seeds a depth of 12 cm was 63, corresponding lia speciosa, Luehea speciosa, Gua - recovered from soil samples taken to a total density of 1 400 seeds/m2, zuma ulmifolia, and Simarouba glauca, from the gallery forest, where only and a viable seed density of with a frequency of 48, 36, 28, 20 and eight species showed some germina- 466 seeds/m2. Trees made up a major 16% respectively. tion (table IB). After dissection, most component of the soil seed bank, and The seeds of most species recov- of the seeds appeared to be empty or the most abundant species in the soil ered from the deciduous forest did had dead embryos, for example seed flora were Allophylus psilosper- not germinate and the cutting test Simarouba glauca. mus and Chomelia speciosa with 24% also revealed that they were dead and 16% of frequency of occurrence in (table IA). Some species, such as

Deciduous forest 1,2 1,0 0,8 0,6 0,4

Ip 0,2 0,0 -0,2 -0,4 -0,6 -0,8

T. hirta E. indica C. speciosa S. obovata L. divaricatum Canavalia sp. M. frutescens Paspalum sp. A. psilospermus Centrosema sp. species

Gallery forest 1,2 1,0 0,8 0,6 0,4

Ip 0,2 0,0 -0,2 -0,4 -0,6 -0,8

S. acuta T. hirta S. glauca P. amarus T. oblonga C. elliptica C. speciosa L. speciosa G. ulmifolia A. tibourbou K. calderonii P. lappulacea B. simarouba S. rhombifolia E. havanense A. amorphoides Species

Figure 4. Spatial distribution of soil seed banks in the dry deciduous and gallery forests. Chacocente Wildlife Refuge, Nicaragua (Ip = Standardized Morisita’s index). 5PtsUas299:280doschun 02/03/09 18:35 Page57

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Table 2. Density of naturally regenerating seedlings (individuals/ha) and their Spatial distribution frequency of occurrence in sample plots. of the soil seed bank Species Family/Subfamily Density Frequency The vertical distribution of seeds recovered from soil samples collected A Dry deciduous forest from the deciduous forest showed high density in the litter layer (0-3 cm) Acacia costaricencis Mimosoideae 200 8 and a gradual decrease in density Allophylus psilospermus Sapindaceae 50 4 with increasing depth up to 9 cm and a slight increase afterwards (figure Allophylus racemosus Sapindaceae 50 4 3a). Of the total number of seeds Bursera simarouba Burseraceae 50 4 recovered, 71% were found in the lit- Caesalpinia exostema Caesalpinioideae 150 12 ter layer and 16%, 3% and 9% in the Capparis pachaca Capparidaceae 500 32 three successive soil layers, respec- Casearia corymbosa Flacourtiaceae 200 12 tively. Although the seeds of most Casearia tremula Flacourtiaceae 150 8 species were entirely confined to the litter layer, those of a few species Coccoloba caracasana Polygonaceae 50 4 were represented at different depths, Cordia gerascanthus Boraginaceae 800 20 albeit in small numbers. The vertical Diospyrus nicaraguensis Ebenaceae 50 4 distribution of seeds recovered from Esenbeckia litoralis Rutaceae 150 12 soil samples in the gallery forest Guarea glabra Meliaceae 50 4 showed a similar decreasing trend Gyrocarpus americanus Hernandiaceae 50 4 with increasing depth (figure 3b). From the total number of seeds recov- Haematoxylon brasilleto Caesalpinioideae 50 4 ered, 74% were found in the litter Jacquinia aurantiaca Theophrastaceae 1 400 36 layer and 11%, 9% and 6% in the Lonchocarpus minimiflorus Papilionoideae 900 20 three successive soil layers. Most of Myrospermum frutescens Papilionoideae 50 4 the seeds of some species were Pithecellobium dulce Mimosoideae 50 4 entirely confined to the litter layer Pithecellobium platylobum Mimosoideae 50 4 while some species were distributed through all depths, although in small Simarouba glauca Simaroubaceae 50 4 numbers. The horizontal distribution Spondias mombin Anacardiaceae 50 4 of the soil seed bank in the decidu- Stemmadenia obovata Apocynaceae 700 12 ous forest showed both clumped and Thounidium decandrum Sapindaceae 350 20 uniform patterns, depending on the Zizyphus guatemalensis Rhamnaceae 100 8 species (figure 4). The five species with a clumped distribution were Lysiloma divaricatum, Allophylus B Gallery forest psilospermus, Chomelia speciosa, Canavalia sp. and Eleusine indica, Acacia costaricencis Mimosoideae 50 4 which also had a fairly high frequency Calycophyllum candidissimum Rubiaceae 100 8 of occurrence in the plots compared Capparis pachaca Capparidaceae 500 32 to the remaining five species with uni- Casearia corymbosa Flacourtiaceae 50 4 form distribution. In the gallery forest, Coccoloba caracasana Polygonaceae 50 4 the majority of the species displayed a clumped distribution. However, a Guaiacum sanctum Zigophyllaceae 300 24 few species, such as Karwinskia Gyrocarpus americanus Hernandiaceae 1 900 36 calderonii, Bursera simarouba and Karwinskia calderonii Rhamnaceae 50 4 Trichilia hirta, showed a uniform dis- Pithecellobium saman Mimosoideae 650 16 tribution (figure 4). Randia aculeata Rubiaceae 650 36 Senna atomaria Caesalpinioideae 50 4 Simarouba glauca Simaroubaceae 750 28 Spondias mombin Anacardiaceae 150 8 Stemmadenia obovata Apocynaceae 50 4 Thounidium decandrum Sapindaceae 900 20 Trichilia moschata Meliaceae 350 20 Zizyphus guatemalensis Rhamnaceae 50 4 5PtsUas299:280doschun 02/03/09 18:35 Page58

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Species composition and density of seedling populations

The total number of species recorded from the dry deciduous for- est was 25 (table IIA). Most of the species belonged to the Fabaceae (Papilionoideae, Mimosoideae and Caesalpinioideae). The total seedling density was 6250 individuals/ha and the mean was 250 ± 69 individu- als/ha. The species with 10 or more individuals were Stemmadenia obo- vata, Lonchocarpus minimiflorus, Cordia gerascanthus, Capparis pachaca and Jacquinia aurantiaca. In addition, these species had the high- Photograph 4. est frequency of occurrence in the Patchiness in the regeneration of seedlings of some species resulting in clumped plots surveyed. In the gallery forest, a distribution in dry deciduous forest of the Chacocente Wildlife Refuge, Nicaragua total of 17 species and 132 individu- Photo by Guillermo Castro-Marin. als were recorded (table IIB). The families most represented were Similarity between the soil Fabaceae, Rubiaceae and Rham- seed banks, seedlings and saman, Simarouba glauca, Spondias naceae with three, two and two the above-ground vegetation mombin, Terminalia oblonga and species, respectively. The total den- Trichilia hirta in the gallery forest. The sity was 6600 individuals/ha with a Within each forest community, similarity in species composition mean of 388 ± 118 individuals/ha. similarity between the soil seed flora between the seedling and The species most represented were and the seedling layer was low (table sapling/tree layers was relatively Simarouba glauca, Pithecellobium III). In the deciduous forest, four higher in the deciduous than the saman, Randia aculeata, Thounidium species, namely Allophylus gallery forest (table III). It was found decandrum, Capparis pachaca and psilospermus, Casearia tremula, that the understory and the overstory Gyrocarpus americanus. Similarly, Myrospermum frutescens and Stem- had 22 species in common in the these species were more frequent in madenia obovata, were found in both deciduous forest and 15 species in the plots surveyed. the soil seed bank and the seedling the gallery forest. layer. The soil seed bank and the Comparisons between forest Spatial distribution seedling layer in the gallery forest communities showed low similarity of seedling populations also had four species in common: in soil seed flora (table III). The Karwinskia calderonii, Pithecellobium species of soil seed flora that were The spatial distribution of natu- saman, Simarouba glauca and Spon- common to both forest communities rally regenerated seedlings in the dias mombin. The same trend was were Cenchrus echinatus, Chomelia deciduous forest showed both observed when comparing the speciosa, Tabernaemontana sp. and clumped and uniform distributions, species composition of the soil seed Trichilia hirta. Similarity in the depending on the species (figure 5). bank and saplings/trees. Species in species composition of the seedling Of the 12 species that had more than common between the soil seed bank layer between the two forest commu- one seedling, six exhibited a and saplings/trees were Allophylus nities was relatively higher than for clumped distribution (photograph 4) psilospermus, Casearia tremula, Cae- soil seed flora. The common species and the remaining six displayed a salpina coriaria, Chomelia speciosa, were: Acacia costaricensis, Capparis uniform pattern of distribution. Lysiloma divaricatum, Myrospermum pachaca, Casearia corymbosa, Coc- Similarly, the seedling population of frutescens and Stemmadenia obo- coloba caracasana, Gyrocarpus four species from the gallery forest vata in the deciduous forest, and americanus, Simarouba glauca, exhibited a clumped distribution Achotocarpus nigricans, Bursera Spondias mombin, Stemmadenia while six species displayed a uniform simarouba, Guazuma ulmifolia, Kar- obovata, Thounidium decandrum pattern (figure 5). winskia calderonii, Pithecellobium and Zizyphus guatemalensis. 5PtsUas299:280doschun 02/03/09 18:35 Page59

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Discussion ment, many trees and shrubs form anobiid beetles feeding regularly on large seedling populations in the for- the fruits and seeds of some plant Soil seed banks est. This is evidenced by the low simi- species, such as Guazuma ulmifolia larity found in this study (19% for both and Pithecellobium saman, have been Results from this study revealed dry deciduous and gallery forests) observed (Janzen, 1988) Thirdly, con- that most plant species in the dry between the seed bank and the sumption of flowers and developing deciduous and gallery forests accu- seedling bank. Secondly, those seeds ovules at an early stage of reproduc- mulate small quantities of viable that do not germinate are consumed tive growth influences the build-up of seeds in the soil. The lack of reserves by predators or succumb to attack by the soil seed bank (Thompson, 2000). of long-lived seeds in the soil of tropi- micro-organisms (Thompson, 2000). The number of viable seeds may be cal dry forests can be attributed to a We observed exit holes made by reduced by pre-dispersal predation, number of factors. First, the seeds of emerging larvae or adult insects in such as attacks by larvae on still soft several woody species are large with a seeds of Myrospermum frutescens full-sized seeds of Cedrela odorata high moisture content, which is and Chomelia speciosa collected from (Janzen, 1988). Our findings concur indicative of adaptation to immediate the deciduous forest and in seeds of with previous studies in several pri- germination and seedling establish- Chomelia speciosa, Simarouba mary or secondary forest formations in ment under the forest canopy (Teketay, glauca, Spondias mombin and the tropics (Teketay & Granström, 1997; Wassie & Teketay, 2006). By Coursetia elliptica collected from the 1995; Wijdeven & Kuzee, 2000). immediate germination and establish- gallery forest. Several species of

Deciduous forest 0,8 0,6 0,4 0,2

Ip 0,0 -0,2 -0,4 -0,6 -0,8

S. obovata C. pachaca C. tremula E. litoralis A. costaric. J. aurantiaca C. exostema Z. guatemal L. minimiflorus T. decandrum C. corymbosa C. gerascanthus Species

Gallery forest 1,0 0,8 0,6 0,4 0,2 Ip 0,0 -0,2 -0,4 -0,6 -0,8

S. glauca P. saman S. mombin C. pachaca R. aculeata T. moschata G. sanctum G. americanus T. decandrum Species C. candidissimum

Figure 5. Spatial distribution of seedling populations in the dry deciduous and gallery forests. Chacocente Wildlife Refuge, Nicaragua (Ip = Standardized Morisita’s index). 5PtsUas299:280doschun 02/03/09 18:35 Page60

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It is interesting to note that the tial heterogeneity of the parent plants Seedling populations seeds of four species from the decid- in the field (Shaukat & Siddiqui, uous forest and two species from the 2004). These variations may reflect The seedling populations in the gallery forest exhibit physical dor- differences among species in terms of deciduous and gallery forests were mancy, and germinate fairly well after seed longevity in the soil, modes of represented by 25 and 17 species, mechanical scarification. These seed dispersal and subsequent respectively. Fabaceae had the largest species possibly form a persistent movement, seed predation, and prob- number of species in the deciduous soil seed bank. Dormancy favours the ably differences in the slope of the forest and Fabaceae, Rubiaceae and accumulation of seeds in soils landscape and local edaphic condi- Rhamnaceae in the gallery forest. (Teketay & Granström, 1995; tions where the seeds land. Similar Fabaceae make up the dominant tree Wassie & Teketay, 2006) and is results have been reported from stud- and shrub family in most dry Neotrop- selected for in most tropical dry for- ies made in other dry forest forma- ical forests (Sabogal & Valerio, est species in response to long dry tions (Teketay & Granström, 1995; 1998; Gillespie et al., 2000), and seasons and unreliable rainy periods Senbeta & Teketay, 2002). Rubiaceae in gallery forests (González (Baskin & Baskin, 1998). In viable Similarity in the species compo- et al., 2006). In the deciduous forest, non-dormant seeds that accumulate sition of the soil seed bank and the five species, namely Capparis in fairly large numbers in the soil, standing vegetation was low for both pachaca, Cordia gerascanthus, dormancy may be induced if the dry deciduous (20%) and gallery Jacquinia aurantiaca, Lonchocarpus seeds are dispersed under dense (25%) forests. Several studies have minimiflorus and Stemmadenia obo- canopy or buried in the soil (Teketay shown a similar pattern of dissimilar- vata had ≥ 500 seedlings/ha. Simi- & Granström, 1995). ity between the seed bank and stand- larly, Gyrocarpus americanus, Thouni- The spatial distribution, both ing vegetation (Teketay & Gran - dium decandrum, Simarouba glauca, vertical and horizontal, of seeds of ström, 1995; Senbeta & Teketay, Randia aculeata Pithecellobium different species and forest communi- 2002), suggesting that regeneration saman and Capparis pachaca had ties varied greatly. The spatial distri- of woody species from seeds in these seedling densities ≥ 500 indivi - bution of seeds in the soil is primarily tropical dry forests would be ham- duals/ha. Except for S. obovata, Pithe- a function of the dispersal process. pered by the removal of mature indi- cellobium saman and Simarouba The number of seeds that falls on a viduals in the standing vegetation. glauca, other species were not particular area depends on a multi- This, in turn, implies that restoration encountered in the soil seed bank. tude of factors, such as height, dis- of tropical dry forests would be diffi- This indicates that seedling banks tance and concentration of the seed cult and slow to accomplish if they could be a strategy for the persistence source, seed dispersal, nature and are severely degraded. of these species in the community. A activity of dispersal agents and spa- similar finding was reported from a dry Afromontane forest where some species completely lack long-lived reserves of seeds in the soil (Teketay, 1997). Many climax species are shade Table 3. tolerant, germinating and becoming Comparison of species similarity, based on Sorensen’s index, established in the shaded understory, between soil seed flora, seedlings and above-ground vegetation thus build seedling banks. For exam- (saplings and mature trees) within and between forest communities. ple, L. minimiflorus regenerated abun- Within forest community Deciduous Gallery dantly on gentle and steep slopes under partial shading (photograph 5) Soil seed bank vs. seedling layer 0.19 0.19 in the dry forests of Nicaragua (Cas- Soil seed bank vs. sapling/tree layer 0.20 0.25 tro-Marin, 2005). The most suitable environmental conditions for the ger- Seedling vs. sapling/tree layers 0.58 0.46 mination of Calycophyllum candidissi- mum were those with no direct sun- Between forest communities Gallery forest light (Morales, 2004). Some species Deciduous forest Soil seed bank Seedling layer respond positively to gaps, as their seeds require light to germinate (pio- Soil seed bank 0.19 neer species). Tabebuia ochracea, Seedling layer 0.47 Gyrocarpus americanus and Lysiloma divaricatum regenerate well under canopy gaps (Morales, 2004). Simi- larly, abundant regeneration of 5PtsUas299:280doschun 02/03/09 18:35 Page61

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G. americanus was observed in gaps that are completely exposed to direct sunlight on our study (Gonzalez, 2005). The spatial distribution of seedlings varies from species to species in both deciduous and gallery forests. Clumped or aggregated spatial patterns are very common among species in tropical forests (Hubbell, 1979; Condit et al., 2000). Poor dis- persal of propagules and limitations to recruitment (soil nutrients, light, mois- ture, etc) may result in such patterns (Bunyavejchewin et al., 2003). Conse- quently, resource-based niche differ- entiation results in habitat specializa- tion, so that different species are best suited to different habitats, where they are competitively dominant and rela- tively more abundant. The distribution pattern of trees is affected by numer- ous biotic and abiotic factors and their interaction, but topography is a major physical factor which affects the com- position, growth, and distribution of Photograph 5. Regeneration under partial shading in dry deciduous forest of the Chacocente tropical forests (Enoki & Abe, 2004). Wildlife Refuge, Nicaragua The refuge (study site) has an irregular Photo by Guillermo Castro-Marin. landscape with altitudes increasing inland from sea level to ca. 300 m lack of correspondence, among oth- species regenerated abundantly in above sea level (Anonymous, 2002). ers, may be caused by biotic factors both forest communities, the majority In the deciduous forest, this irregular- such as herbivory, or by abiotic fac- were less well represented. ity of the relief can be clearly observed. tors such as tree fall. When compar- Restoration measures should there- In contrast, gallery forests occur on flat ing the understory vegetation of the fore be introduced to assist the natural land. Different slope gradients may gallery and deciduous forests, only a regeneration process, such as direct have positive or negative effects on few species that were present in the seeding, planting seedlings of less seedling establishment. Haematoxy- gallery forest were represented in the abundant species and manipulation of lon brasiletto occurred mainly on flat deciduous forest, which could be the sites to improve site-related fac- land (Törnqvist, 2004), and was attributed to specific niche require- tors for seedling establishment and almost absent at higher altitudes, ments of the constituent species. survival. As this study did not attempt while C. candidissimum mainly to explain factors that cause low seed appeared in fairly undisturbed lowland density in the soil, further study is rec- forests, close to the coast. Although Conclusion: ommended to describe rates of preda- this species was represented in the implications tion, dispersal mechanisms, seed rain deciduous forest, close to the coast, for restoration and germination ecology. higher densities of saplings and mature trees of C. candidissimum were Results from this study suggest a Acknowledgements found in the gallery forest, where a flat paucity of soil seed banks in both for- Financial support for this study was relief is predominant. On the other est communities, so that soil seed obtained from the Swedish Interna- hand, optimal conditions for the estab- banks may not be an effective propag- tional Development Cooperation lishment of L. divaricatum, T. ochracea ule donor for natural species regenera- Agency (Sida). Thanks are due to Clau- and G. americanus were on steep tion. In addition, analysis of the spatial dio Calero, at the National Agricultural slopes (Morales, 2004). pattern of soil seed banks revealed University, Nicaragua, for his support For both forest communities, the patchiness, which in turn has signifi- with species identification and to similarity in species composition cant consequences for the distribution Benigno Gonzalez Rivas and Guillermo between the seedling population and of naturally regenerating individuals Castro Marín for arranging the field- the overstory vegetation was low. This across the landscape. Although some work and providing the pictures. 5PtsUas299:280doschun 02/03/09 18:35 Page62

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