Landscape Regeneration by Seeds and Successional Pathways to Restore Fragile
Tropandean Slopelands
Fausto O. Sarmiento
Mountain Research and Development, Vol. 17, No. 3, The United Nations University. Managing
Fragile Ecosystems in the Andes. (Aug., 1997), pp. 239-252.
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Mon Dec 3 12:24:54 2007
LANDSCAPE REGENERATION BY SEEDS AND SUCCESSIONAL PATHWAYS
TO RESTORE FRAGILE TROPANDEAN SLOPELANDS
Centerfor L a t i n American a n d Caribbean Studies a n d Institute of Ecology G40 Baldwin Hall, University of Geo:eorgia Athens, Georgia 30602-1 6 1 9, U S . A . ABSTRACT Although land abandonment in the equatorial Andes is a process that complicates the mosaic of land uses in Tropandean
landscapes, in some cases land abandonment further contributes to the process of degradation. This includes not only soil but also
the species composition and community structure of montane forest patches and, where succession fails, recalcitrant pasture grasses.
In order to examine failed succession, studies were undertaken on the lack of seed input, the ability of seed dispersers, the efficacy
of avian roosting from perches, the removal of seeds, germination from seeded scats, seedlings among the tussock grasses, and the
recruitment of saplings of montane forest trees. It is suggested that regeneration by seeding may be possible only if proactive removal
techniques of the aerial tillers of grass species and their extensive root mass is eliminated. However, pasture conversion to forest using
Psidium guajaba as pioneer tree to enhance dispersal outwards from the forest edge, coupled with seasonally-driven seed rain episodes,
is aposterion'. Land-use and land-clearing patterns dictate the outcome of the regenerating phenosystem. This means that policies and
practices of montane forest clearing must include treefall 'survivors' to enhance frugivory, to provide shade and regeneration of
interspersed patches, and to stimulate dispersal for rapid initiation of ecological succession.
RESUME Eginiration d u paysage par ensernencement et voies de succession pour la restauration des sols pentus fragiles des Andes tropicales. Bien
que l'abandon des terres dans les Andes kquatoriales constitue un processus compliquant la mosai'que d'exploitation des terres dans les
Andes tropicales, il contribue dans certains cas au processus de dkgradation. Ce processus n'affecte pas seuleinent le sol, mais
kgalement la composition des espcces et la structure communautaire des aires forestikres kparses, et, lorsque la succession echoue, les
herbes de pkturage rkcalcitrantes. Dans le but d'examiner l'kchec de la succession, des etudes ont kt6 effectukes en rapport avec le
manque d'apport de semences, la performance des disskminateurs de semences, I'efficacitk des perchoirs aviens, I'extraction des
semences, la germination i partir d1excr6ments contenant des semences, les semis parmi les buttes de gazon et le recrutement de
gaulis d'arbres de for& alpestres. Les ktudes suggkrent que la rkgknkration par ensemencement peut n'ctre possible que si des
techniques d'extraction proactive des talles akriennes des graminkes sont appliqukes et que leur knorme masse de racines est kliminke.
Nkanmoins, la conversion des pkturages en forets, utilisant le Psidium guajaba en tant qu'arbre pionnier pour la disskmination vers
I'extkrieur 2 partir de la lisikre de la for&, de concert avec les kpisodes de pluie de semences saisonnicres, est aposten'm'. Les habitudes
d'exploitation et de dkfrichement des terres dkterminent le rksultat de la rkgkneration du phknosyst2me. Cela signifie que la politique
et les pratiques de dkfrichement de la for& alpestre doit inclure les survivants de I'abattage afin de favoriser les especes frugivores,
de fournir de l'ombre et de permettre la rkgknkration des aires kparses, et de stimuler la disskmination pour demarrer la succession
Ccologique.
ZUSAMMENFASSUNG Landschaf?regenmation durch Aussaat, sowie Sukzssionswege zur Wederherstellunggefiihrdeter tropischer Abhangsystenze i n
den Anden. Landaufgabe in den Aquatorregionen der Anden verkompliziert das Mosaik der Landnutzung und tragt in einigen Fallen
zur Umweltzerstijrung bei. Hiervon ist nicht nur der Boden betroffen, sondern auch die Artenzusammensetzung und Lebensgemeinschaftsstruktur montaner Waldflachen und, im Falle verhinderter Sukzession, von ausdat ernden Weidegrasarten. Um Grunde
fur verhinderte Sukzession zu finden wurden Untersuchungen zu mangelndem Sameneintrag, zur Samenverbreitung, zum EinfluR
von Vhgeln, zu Samenvernichtung, Keimung von samenhaltigen Tierausscheidungen, Keimung zwischen Grasbt~scheln,sowie zur
Rekrutierung junger Bergwaldbaume durchgefuhrt. Es scheint, daR Regeneration durch Aussaat nur nach aktiver Entfernung von
Wurzelauslaufern und den massiven Wurzelsystemen verschiedener Grasarten m6glich ist. Umwandlung von Weide- zu Waldflachen
mit Hilfe von Psidium guajaba als eine die Verbreitung vom Waldrand her fijrdernde Pionierbaumart ist an jahreszeitlich kontrollierte
Aussamungsepisoden gebunden. Landnutzungs- und Landrodungsmuster bestimmen das Endergebnis des sich regenerierenden
Phanosystems. Dies bedeutet, daR Richtlinien und Praktiken in montaner Waldrodung "Rodunguberlebende," die brachliegenden
Flachen beschatten, Frugivorie und Regeneration fijrdern und Verbreitung stimulieren, und so der 6kologischen Sukzession zu einem
guten Start verhelfen, berucksichtigen sollten.
RESUMEN Regeneracio'n del palsaje mediante semillas y senderos sucesionales para restaurar las laderas frigiles de los Andes tropicales. Si bien
el abandono de la tierra en 10s Andes ecuatoriales constituye un proceso que complica el mosaic0 de gesti6n territorial en 10s paisajes
tropandinos, se hace evidente en algunos casos que el abandono contribuye a h mis a la degradaci6n de laderas frigiles. Esto se da
no s610 por las caracteristicas del suelo, sino tambikn por la composici6n de especies, la estructura de la comunidad de 10s retazos de
selva de montafia y por la utilizaci6n de especies de hierbas recalcitrantes que son usadas ampliamente, en donde no prospera la
sucesi6n ecol6gica. Con el prop6sito de responder a preguntas sobre la malograda sucesi6n se examinan hip6tesis sobre la falta de
0International Mountain Society and United Nations University
ingreso de semillas, la habilidad de 10s dispersores, la eficacia de la deposici6n desde las perchas, la remoci6n de semillas, la
germinaci6n de muestras fecales con semilla, el retofio en medio del pastizal y el reclutamiento de renuevos de Brboles del bosque
montano. Se sugiere que la conversi6n del pastizal hacia el bosque usando Psidium guajaba como Brbol pionero para mejorar la
dispersi6n hacia fuera del filo del bosque, junto a 10s episodios de lluvia de semillas impulsados por las estaciones es aposta'on. Debido
a que 10s patrones de aclareo y de uso de la tierra dictan el fenosistema regenerative, se argumenta que las politicas y las prjcticas de
tala del bosque de montafia deben incluir "sobrevivientes" que estimulen la frugivoria, que proporcionen sombra en retazos
interspersos de regeneraci6n y que estimulen la dispersidn de semillas para energizar la sucesi6n ecol6gica.
INTRODUCTION
Natural seed dispersal is one of the potential mechanisms for conversion of abandoned pastures to forests in
degraded slopelands of the Andean Piedmont. Unfortunately, dispersal of introduced species associated with
agro-ecosystems is resulting in the replacement of many
native species of the original forest communities. Moreover, there are several sites in the Andean region in which
natural regeneration of forest has not occurred, even
after the pastures are no longer grazed: in places on the
semi-arid western Peruvian flanks, for instance, the loss of
forest cover has resulted in a notorious 'advance of the
desert' (Young, 1992) and in wetter regions, such as in
the Colombian Sierra Nevada de Santa Marta, deforestation of entire watersheds has eliminated nearby seed
sources that could provide regeneration loci of the original forest cover (Aide and Cavelier, 1994). In Ecuador,
land abandonment has been correlated with land degra-
dation in an Interandean setting (Harden, 1996),and the
impact of pre-Colombian settlements, transhumance, and
trade routes is evident in the Upper Guayllabamba river
basin of northwest Ecuador (Sarmiento, 1994). Human
impacts on montane landscapes have modified the original plant composition to such an extent that the contemporary old-growth forest may be in part anthropogenic
(Sarmiento, 1987). A review of the literature on Andean
ecology provides unequivocal evidence that the entire
eco-region is a cultural landscape (Troll, 1968; Ellenberg,
1979; Balslev and Luteyn, 1992; Churchill et al., 1995).
Improved knowledge of the dynamics of seed dispersal,
especially the role of birds and other animals, should
provide a basis for restoration of degraded Tropandean
landscapes, which is considered a challenge for conservation in the region (Sarmiento, 1995 a).
HAS SUCCESSION FAILED IN THE ANDES?
It is widely accepted that results from the study of
ecological patterns and processes in temperate ecosystems do not fully apply to the tropical realm. As Harden
(1996) noted, the classical theme of old field succession
as studied in the Appalachian Mountains is not applicable
to the tropical Andes; but, even her comparison with the
Spanish Pyrenees is not fully adequate. Moreover, numerous studies of the patterns and processes occurring in
tropical lowland sites conclude that they differ from those
in the neighboring highlands Uanzen, 1967; Myster and
Sarmiento, 1997; Sarmiento, 1997). With constraints imposed by topography, tropical montane forests are naturally affected by cloudiness and low temperatures (Bohlman et al.. 1995). Landslides also contribute to the
gap-dynamic landscape mosaic (Myster and Fernandez,
1995), thus conditioning the pattern of succession against
the shade-tolerant seedlings on recently barren slopes.
Furthermore, with anthro<ogenic disturbances, suc6 as
clearing for pasture, the successional trajectory changes
towards a different community structure of seedlings that
may never grow tall because of the competition with
resistant tussock grasses.
In some montane sites, succes"
sion is arrested even where grazing grounds have been
abandoned. Deflected succession (Godwin, 1929), as a
result of grazing relaxation, may have modified successional pa<hways-of montane forests (Gibson and Brown,
1992) where the ergodic hypothesis-the spatial variation
amongst sites of different ages is equivalent to temporal
change at one site-cannot be tested due to the unreliability of land-use history of the montane forest sites.
Although land degradation is often correlated with
diminishing nutrient-holding capacity, carbon sequestration, soil pH, and overall fertility, this paper emphasizes
the role of seed dispersal and factors that influence germination and seedling establishment. The question asked
is whether there is a correlation between impoverished
biota and the regeneration of natural ecosystems or
fallow/abandoned lands. If so, then restoration ecology
should play a critical role in the management of tropical
mountainous areas for conservation of eco-diversity
(Naveh, 1994). The Tropandean landscape should be restored towards a 'healthy' condition (Hamilton, 1996)
which is the basis for mountain sustainable development
(Ives and Messerli, 1989; Denniston, 1995).
Limitations for forest recovery in degraded pastures,
within the mosaic of land uses of Tropandean landscapes,
range from ecological to socioeconomic. The research
reported here focuses on succession in abandoned pastures as a natural process. While anthropogenic obstacles
for forest regeneration are not the focus of this paper, it
is acknowledged that, in most cases, these are the
stronger limiting factors and they exert greater control
than do the bio-ecological ones. This is because rural
landscapes are embedded in a matrix of several land-use
types, without planning, and with dubious resource management policies.
FIGURE1. T h e location o f three domains o f Tropandean landscapes in the equatorial Andes ( o n the
equator) and the location o f the study site: Interandean (highland plateaus between the two longitudinal cordilleras interconnected with transversal
'nudos');Cisandean (eastern flanks towards the Amazon); and Transandean (western flanks and piedmont towards the Pacific Ocean).
THE STUDY AREA
Studies were undertaken on the lack of regeneration of
montane forests in northwestern Ecuador (Figure I ) ,
where the presence of an introduced tussock grass (Setarid sphacelata) is now the dominant feature of the landscape, Here, arrested succession has prevented recolonization by forest trees into cleared slopelands and has
exacerbated soil erosion and overall degradation of the
area. Other grasses (Table 1) are also used for pasturelands in the area; however, the popularity of 'pasto miel'
among the local farmers is regrettable.
The experimental setting for study of seed dispersal
and regeneration was located around the Maquipucuna
range, including the Maquipucuna Reserve, Barrio Las
Palmas, La Isla site, and Chichipunta. Figure 2 shows
sampling sites in an illuminated digital model of slope
effects of the reserve. The study area lies within the
Upper Guayllabamba river basin (0" 05' N, 78" 37' W),
that occupies the Andean Piedmont of the southern limit
of the Choc6 biotic province. The Maquipucuna Reserve
extends from an elevation of 1,150 m at the Umachaca
River bridge to 1,970 m at the summit of Mount Montecristi, thus providing an elevational continuum from
lower montane-transitional-to
upper montane-forest
communities (sensu Grubb et at., 1963). Old-growth forest
is most common towards the upper reaches of the reserve
while secondary growth and abandoned fields and pastures are most common at lower elevations, especially
near the river. Altitudinal transect studies (Raguso and
Gloster, 1993; Sarmiento, 1994) show that the habitat
affinities in taxa often respond to impacted systems, such
as montane old-growth, bamboo thickets, successional
meadows, young secondary forest regrowth, forest edges,
and riparian forests. A florula of the reserve was compiled
by Webster (1993). A checklist of birds was compiled by
Sarmiento (1996). The soil (Andosol) is developed from
volcanic ash deposits; it is dark and rich in organic
matter, medium-textured, and moderately fertile- The
deposition of ash and tephra originated from two nearby
volcanoes that produced Plinian eruptions about 2,000
years ago (Pulilahua volcano) and about 330 years ago
(Pichincha volcano). Evidence of both ancient land occupation (by the Yumbos) and modern human impact is
noticeable in the lower portion and is described in the
epistemographic effect (Sarmiento, 1995 b) of naming
the landscape features in the reserve.
The reserve setting is typical of the tropical Andes, with
temperature regimes ran$ng between a daytime mean of
27°C and a nighttime mean of 14"C, with a mean annual
average of about 20.7"C. The rainfall also shows a typical
tropical pattern, associated with a dry season from-midJune to late-September with a minimum in July, and a
rainy season from October to late May with a maximum
in March (Figure 3).
242 / MOUNTAIN
RESEARCH
AND DEVELOPMENT
T ~ L1 E
Different grass species and their habit in the study area
Latin name
Local name
English name
Habit
Pat?
Upper montane
Panicum clandestinum
Holcus lanatus
Lolium perenne
Digitaria decumbes
Melinis minutzjlora
kikuyo
holco lanudo
reygras
pangola
gordura
african grass
hairy grass
ryegrass
crabgrass
melina grass
1
1
1
1
2
3
3
3
3
3
Lower m o n t a n e
Digitaria sanguinalis
Pennisetum ofJicinale
Brachiana c f umbilicola
Setaria sphacelata
Setaria paruzjlora
Sporobolus poiretii
Pennisetum purpureum
Axonopus scopan'us
Paspalurn conjugatum
Brachiaria c f decumb~s
Axonopur micay
chirimbilla
pasto elefante
hierba baja
pasto miel
grama
pia
grama morada
gramalote
grama
saboya negro
pasto xnicay
large crabgrass
elephant grass
covered grass
foxtail grass
foxtail grass
grass
amazon grass
carpet grass
grass straw
saboya grass
micay grass
1
4
3
3
3
4
4
3
3
4
3
3
2
1
2
2
2
2
1
1
2
1
T h e grass habit is differentiated between superficial ( 1 : scandent) and bunches ( 2 : tussock)
and t h e patry is determined between introduced (3: planted) and native (4: natural).
METHODS
Possible mechanisms to ensure rapid initiation of succession and to facilitate natural regeneration were investigated. Important questions emerged: can we manage
arrested succession as a starting point of forest regrowth?
What is the role of active dispersal for maintenance of
cloud-forest cover? How can we use dispersers for restoration practices? Is land use a valid predictor in forest regeneration? If so, how are differeni disturbance regimes
affecting the outcome of recovery?
The research was conducted in abandoned pastures
surrounded by old-growth (i.e., pastures planted with Setaria sphacelata, with natural ~ i s t a r i saan&inalis pasture,
and with guava Psidium guajaba, and forest edges and oldgrowth forest patches). An electronic map of the reserve
was produced by digitizing IGM quadrangle sheets at
scales of 1:50,000 and 1:25,000. To enable relational database comparisons, ARC/INFO software on Unix Sun stations was used. Errors on topographic charts were corrected by comparing black-and-white air photography
1:40,000 (1987) and by ground-truthing using a portable
GPS Trailblazer with 30 m ground resolution with estimates of elevation (in meters) and geographic coordinates (N latitude and W longitude). To assist GPS readings from satellites in semi-closed canopy situations, an
antenna attached to a 6 m extension pole was used to
of
capture position data on site. ~ o p o l o ~ i c relations
al
landscape features in mountainous terrain were detected
with a digital elevation model produced by the Triangular
Irregular Network (TIN) routine. A comparison among
landslide sites for natural disturbance and abandoned
pastures for anthropogenic disturbance was produced
(Myster and Sarmiento, 1997). Modeling of wind-swept
slopes (for example, morning katabatic winds on the
study site) or the illumination regime was possible with
TIN. Due to the equatorial location of the reserve, no
analysis of aspect was performed.
seedfall o i anemochorous seeds was captured with a
modified Gorchov et al. (1993) method in an array of 30
seed traps interspersed in randomized blocked sampling
stations at the forest edge, and at sites 5 m, 10 m, 25 m,
50 m, and 100 m into the pasture. This trapping method
was selected rather than boxes with sterile sand at ground
level (Loiselle et al., 1996) because it gives a direct estimate of seed rain and catches the fali without interference from grass tillers. Seed trap harvesting was performed by an assistant on a weekly basis from A ~ ~ g u1994
st
to .July 1995. Each individual seed becomes a 'seed record'in the same way that each individual twig or leaf
fragment becomes a 'litter record.' Weekly collection aslowed for a better time series analysis and forestalled
decomposition of seeds on site. Each sampling unit was
harvested and seeds were fixed in alcohol, dried, labeled,
--.
houses
- road network
'
FIGURE
2 . Digital elevation model with TIN for GIs analysis in ARC/INFO. The sampling sites are shown within the slope/forest
retention composite map, with perspective view to the east, afternoon illumination, weed-tolerance of 10 m, and 1.5 vertical
exaggeration factor.
Temperature regime
I
I
Time (months)
OMAX
.MIN
Rainfall regime
1
I
450
Tlme (months)
FIGURE
3. The climatic regime at the Maquipucuna Reserve in
1991-1992, as representative of typical Tropandean sites affected
with a sinuous rainfall curve but with overall yearly constant
mean temperature.
and saved in vials. A data matrix with counts of individual
diaspores/m2, separated by two seed-size classes, was established with tabula~ionof leaf- and twig-litterfall and
the collection of other wind-blown struct~lres,such as ash,
insect remains, grass, and pellets. Visual classification,
count, and collection provided numerical information on
seed rain. Weighted biomass from seedfall and litterfall
was also recorded for comparison. A separate compilation
of seeds from fruits of collected plants provided references for vouchers for the seed catalog.
Seed shadow yieided samples of defecated or regurgitated seeds, carried away by frugivorous forest-dwelling
species. Bagging was performed with extensive mistnetting of birds and bats at the study site; this collection
process was performed for 120 sampling hours. Fifteen
catching stations with 3.5 m poles were scattered between
the sampling units in three different pasture types. When
feces or regurgitate contained a group of seeds, each seed
was considered a 'seed record.' For the captured species
with combined diets, frugivory and insectivory were
checked but only seeds were counted.
Estimates of seed shadows were also made by walking
randomly among the three treatment areas, looking for
fecal droppings along 14 linear transects of 20 m each.
When fecal material was found, the location and extent of
the scat were recorded and a photograph was taken. Also,
seeded fecal droppings were collected in the permanent
seed traps. Registering of fecal fall within the traps was
also monitored during one year of continuous weekly
sampling. A catalog of seeds from seed rain and seed
shadow was initiated following the Klein technique that
includes cleaning seeds in a two-step procedure: a) pre-
cleaning operation with scalping by screens of finer
meshes, or hulling of the mixture and impurities, and
b) mechanical separation, drying, chemical cleaning (diluted alcohol), and delinting.
Secondary dispersal was established by experimentation of seed removal. Instead of developing feeding stations, a series of open sampling sites were used to test the
importance of seed size and palatability for dispersal into
the pasture areas. Some authors refer to the removal of
seeds as 'seed predation' (Janzen, 1971; Jordano, 1983,
1992); however, to be consistent with the terminology
of foraging ecology (Sarmiento, 1986),including chances
of secondary dispersal that increase the seed shadow of
many species, I refer to my findings as seed 'removal,' as
in the myrmechory- or rodentichory-mediated burying of
seeds for subsequent consumption or haphazard germination). From the 5 pools of seeds, removal indices for 5
scattered daily removal periods were calculated as O=untouched to l=gone. The ratio of gone/untouched,
termed 'removal efficacy' was generated for each of the 7
pasture exclosure areas for comparison between pasture
types and within each pasture type. In perching experiments, bamboo strips provided artificial roosting and
resting surfaces for pasture-forest vagrants, in contrast to
Holl's (1995) technique using branches of Inga trees for
perches. Five of the perches were enhanced with ripened
peeled banana to attract birds for sitting and potential
defecation (Robinson and Handel, 1993). Seed traps
under perches allowed a collection in 1 m2 surface area
of potential deposition.
Force-fed guava fruits provided the source for experimental regeneration. Seeds placed in homogenized river
sand for germination were monitored and watered with
fine mist for three weeks inside shade houses (after Loiselle et al., 1996). Saplings were counted and weighted;
measurements of roots and shoots were recorded. A seedbank experiment was also carried out, on site, to obtain
data on regeneration of the potential community if pasture were removed. Experimental removal of 1 m2 Setam'a
sphacelata quadrats under 7 seed traps required extensive
clearing with machete (4 sites) and Roundup herbicide
(3 sites). Samples were placed in plastic pots to check for
germination of the seed bank in controlled shade house
conditions for comparison. To test for potential germination of fecal-embedded seeds, 75 samples of seeds were
placed under a germination chamber in the laboratory,
using a bedding of soaked Sphagnum moss for seed-bed
culture, and 75 samples were placed on cotton-topped
plastic funnels filled with vermiculite and were irrigated
daily with 20 ml of a fine mist. The moss containers were
arranged randomly under a 12-hour light regime, simulating daily cycles, for five weeks.
Finally, the woody plants were recorded from 7 circular
10 m-diameter plots. Taxonomy studies, measurements of
height and diameter at breast height (dbh), and tagging
were undertaken for each plant greater than 50 cm
height or 2 cm dbh. Percent cover was also estimated
using the spherical grid method. Importance values were
calculated and correspondence analysis was performed by
parameterizing the tables of vegetation cover. Iterative
measures were taken in each one of the sampling stations
at 12-month intervals to check for growth, recruitment, or
extinction. Selection of circular plots in lieu of permanent quadrats for vegetation analysis avoided artifacts of
sampling in seed dispersal due to the natural tendency
for circular dispersion (Rapoport, 1982).
DATA A
The study allows for generalization to be made for seed
dispersal patterns over both dry and rainy seasons. Longt e r h climatic records in the tropical Andes show episodes
of wet and dry years, and indicate pulses triggered by the
El Niiio Southern Oscillation (ENSO) over spans of approximately ten years. The yearly data of the reserve,
however, approximate the long-term average. For the present purpose, therefore, it is assumed that the weather
pattern that occurred for the duration of the study is
Eepresentative of Tropandean landscapes and it is not a
local phenomenon. Parametric statistics assumes the normality of seed rain (sensu Hairston, 1989). Normally distributed fall of seeds and litter is a reflection of a highly
probabilistic event which is thought to be independent of
other factors. Independent readings of the seedfall are
also taken as a reflection of normal phenological responses of the montane forest of the Andean Piedmont as
a whole. For other processes of seed ecology, such as seed
shadow or seed removal, where independence may be
questioned, non-parametric statistics were applied. The
probabilistic nature of dispersal events are thought to be
highly influenced by chance (Feisinger, pers. comm.);
however, it was assumed that the patterns registered here
are a manifestation of a more generalized trend that sets
the likelihood of regeneration by seeds: hence its predictive power. A final assumption establishes an alpha
index level (a = 0.05) as significant. Significance levels,
however, have to be taken within the context of the descriptive and inference statistics, since biological significance may greatly differ from statistical significance, particularly in instances such as seed dispersal (Howe,
1989).
For data analyses SYSTAT 5.2., ECOSTAT , and EXCEL
5.1 were used. Two-way analysis of variance (ANOVA
model 111) was applied to the importance of pasture locations (6 locations, random effect) and treatment type (3
treatments, fixed effect) in determining the number of
individual plant species' seeds occurring in seed traps.
When appropriate, different BIIOVA models were used in
each treatment as pasture type and success of collecting
varied. A Wilks-Shapiro test for normality of dependent
variables was used (Sokal and Rohlf, 1981j. When necessary, dependent variables were log transformed to meet
assumptions of normality for AYOVA.
To examine whether the distribution of seeds differed
among pasture locations, a chi-square contingency analysis
was applied; seedlings were first characterized into dispersal modes according to literature accounts (Gentry,
1983; Loiselle and Blake, 1990) and personal observations.
For comparison between habitat variation of pasture sites,
all trap data within paired sites were combined. A pooling
of the seed-rain data provides a matrix for establishing
variation within and between the three treatments.
Seedfall and litterfall summary statistics were compared
by correlation analysis. Linear regression methods helped
analyze the effects of seedfall and litterfall on the pooled
data, although separate individual regressions were
needed to verify low R2 values of some samples (GreyMatter International, 1994). For accounts of individual
scat dispersion, the kurtosis of the data on captured dispersers had to be treated with an F test. Seed-shadow data
were analyzed differently, and this included cluster analysis with a data matrix composed of the number of seeds
collected for each plant species for location and treatment (i.e., natural pasture site B62). To simplify the matrix array seeds were removed if they were from an unknown family (unidentified) or of a species characterized
for only one record. Data were then relativized by row
and column totals in order to weight seeds and sites
equally; this was because the primary interest was to un-
derstand the similarities among sites due to seed species
comwosition, rather than abundance of seed rain.
For the regeneration experiments, summary statistics
include Spearman's correlation to establish monotonicity
between seed size and palatability for seed removal.
ANOVA was also used to compare differences between
samples and within samples of the Psidium guajaba seedlings coming out of the block treatments. A transition
matrix was developed for the on-site regeneration of
pooled sampling units to test for components by factor
analysis. This allowed comparison of microsite regeneration in natural disturbances (landslides) versus humanmade disturbances (clearing for pasture). Euclidean
distances obtained by algorithms of Householder tridiagonalization and QL implicit iterations were used after
excluding missing data for computation (Wilkinson,
1992). Similarity indices among circular plots were developed as well as Student's t-test statistics to check for differences in the two measurements separated by one year of
natural weathering and survival. Ortolano (1984) suggested the 'BACI' model for characterization of ecological changes, when data are obtained Before ( t o ) and
After ( t r ) in specific Control and Impact settings on the
ecosystem under surveillance, and this was applied (t = 0)
for a hypothetical disturbance regime after one year of
first measurement ( t + I = I ) .
RES
The hypothesis of lack of seed input for regeneration
of the montane tropical forest ecosystems is falsified by
evidence of amounts of incoming seeds by dispersal and
the overall seed dynamics. Figure 4 shows the total biomass accumulation from litterfall; seed-rain data are
roughly 10% of the total fall; the seasonal variation of
seedfall peaks in the rainy season. Seed density was 366.5
g/m2, in contrast to the biomass from leaves, twigs, and
such, that was 89.19% (3,026.78 g/m2) of a total cumulative biomass of 339.33 kg/ha/yeac Over the course of
this study a total of 24,011 seeds from at least 20 families
and 57 plant species were recorded from seed traps. The
range of the average density of seed rain per seed trap
varied from 39 to 4610 seeds/m2/year; the maximum
number of seeds recorded from any one trap during any
sampling collection was 760 seeds/m2/week at the peak
of the rainy season (21 March 1995). Pooled data of seed
rain by plant species offer special dispersal curves associated with proximity to forest edge or the pasture interior. Wind-dispersed species abound in the catch, with
contributions of Setaria (21.76%), Digitaria (15.91%), Vernonia (9.77%), Begonia (7.79%), Axonopus (6.87%),Baccharis (4.29%), and Sida (3.98%). Contribution of seed
rain and seed shadow (from collected scats over the seed
trap) correlates with plant sources dispersed by frugivorous dispersers but with an increased contribution in numbers of each of the few species. Conversely, the input of
seed rain was scattered among more species, but the
contribution of each was lower than the observed endozoochory. For example, one species alone, Cecropia mono-
stachya, represents 41.06%. Other contributions from
Piper (21.06%),Ficus (8.99%), Miconia (8.04%), and Psidium (4.61%) are also individually high (Figure 5).
Small seeds were almost always removed from the standard pool of seeds, especially rice seeds (90.28%),guavas
(86.42%), peanuts (85.97%), and figs (30.00%). Other
seeds from 'chirimoyas' (47.28%), 'pagches' (43.10%),
and 'guabas' (8.50%) were partially taken. On the other
hand, some seeds were never touched, including 'carachacoco' ( 0 % ) and 'caimito' (O%), o r just barely
touched, such as the 'tomatillos' (4.14%) and 'corosos'
(6.24%).Lack of removal of Dyalanthera (cf. Otoba) gordoniifolia does not mean absence of predation of this autochoric diaspora; there is evidence that the fruits of
'carachacoco' are eaten by parrots (Amazona mercenaria),
green toucans (Aulachorhjnchus haematopygyus), and trogons (Trogon collaris). Also, fallen seeds are gathered by
the common squirrel (Sciurms granatensis) and the common rabbit (Sylvilaffus brassiliensis andinum) in the oldgrowth surroundingthe pasture study area. Seed size was
negatively correlated with removal success (Spearman's
correlation, Rs = -0.83, N = 25, df = 1) since almost all of
the small seeds were, indeed, removed. The bigger the
seed, the smaller the chance of removal. Overall, it seems
that the removal of seeds in the forest and in the pasture
are equivalent during the wet season (0.39 = 0.38) whilst
removal in the forest becomes more important than in
pasture (0.62 > 0.39) in the dry season (Table 2).
The investigation shows that avian perches in the open
pasture were-not used as resting places; only 4 seeded
BIOMASS ACCUMULATION
weekly wllectlon of one continuous year
S
m
) t
L
r
n
FIGURE
4. The biomass accumulation in one year of continuousweekly records. The spurious correlation between litterfall and seedfall
can be observed when the peaks are out of phase; however, a clear pattern of contribution of about 10%of seeds towards the total
fallen biomass is recorded.
1
seed rain per habitat type
-.
--- planted pasture 15 80%
p
--
-. ..-
jnatural pasture 34.63%
5. Proportional seed rain per pasture type.
FIGURE
Guava pasture (Psidium guajaba) significantly enhances seed rain in comparison with the natural
pasture (Digitaria sanguinalis) and the planted pasture (Setaria sphacelata).
scats came from perching, from a total of 49 scats registered as a result of perching. Increased fecal deposition
came mainly from insectivorous birds, particularly the
smooth-billed ani (Cuculidae: Cmtophaga ant) that was the
most conspicuous bird of the pastures in the study area,
contribut&n
" 31 scats void of seeds but with manv.insect
remains (e.g., termites, spiders, and grasshoppers). Figure
6 shows that entomophagous diets are correlated with
open pasture while frugivorous diets are negatively
correlated.
Differences among treatments were not significant (Single factor ANOVA, F = 0.29, p = 0.9, df = 26), suggesting
-
-
'
2
1
,
guava pasture 49.56%
that the low embedding of fecal material around the
dispersed seed is not a factor favoring germination. Similar results were obtained from the study looking at the
germination response of Cecropia monostachya seeds in
bird scats. Fecally-embedded seeds showed no difference
in potential germination when compared to seeds obtained from fresh fruits. On-site germination shows a
different trend-although the dominant tussock grass
gives a monospecific appearance to the pasture, underneath a canopy of Setaria sphacelata a number of seedlings
may be found. A total of 58 species were identified in the
quadrats, almost of all them were old-field related herba-
TMLE2
Correlation matrix ofseed m o v a l in (a) ruet and (b) ddry seasons in 7 habitat tjpes
a) Wet season
Wet sites
FOR
FORED
GUA 1
GUA2
PAS ED
PAS 1
PAS 2
FOR
FOR ED
1.000
0.92
0.776
0.840
0.638
0.849
0.803
1.000
0.78'7
0.830
0.707
0.850
0.781
1.000
0.747
0.661
0.820
0.614
1.000
0.754
0.909
0.844
1.000
0.625
0.065
1.000
0.862
1.000
Dry sites
FOR
FORED
GUA 1
GUA 2
PAS ED
PAS 1
PAS 2
FOR
FOR ED
1.000
0.641
0.459
0.782
0.684
0.529
0.767
1.000
0.628
0.753
0.653
0.740
0.749
1.000
0.629
0.632
0.765
0.716
1.000
0.716
0.738
0.937
1.000
0.752
0.721
1.000
0.814
1.000
GUA 1
GUA 2
PAS ED
PAS 1
PAST 2
b) Dry season
GUA 1
GUA 2
PAS ED
PAS 1
PAS 2
FOR: old growth forest;
FOR ED; forest edge;
GUA 1: guava pasture open canopy;
GUA 2: guava pasture closed canopy;
PAS ED: pasture edge;
PAS 1: planted pasture;
PAS 2: planted pasture.
Insect scats
\
C
\
seeded scats
6-------
\\-_--
7
0
r111
-
o
--
5
10
-
-
4
--
-
25
5o
DISTANCE FROM THE EDGE (in meters geometncal scale)
ceous flora, with the exception of potential pioneers of
'chandor' (Papaveracea: Bocconia frutescens), 'guayava'
(Myrtaceae: Psidium guajaba), 'colcas9 (Melastomataceae:
Miconia sp), 'cordoncillo9 (Piperaceae: Piper aduncum),
and 'chilcango' (Asteraceae: Baccha~ssp.) as evidence of
frugivory and seed dispersal. When Setaria sphacelata grass
was removed from the quadrat by hand, the regeneration
included a great proportion of forbs from Asteracea, Fabaceae, Malvaceae, Euphorbiaceae, and Poaceae, The
EL
- -
300
FIGUKE
6. The correlation of proportion of scats
and distance away from the forest edge shows the
preference for insectivorous birds defecating in
the open pasture in contrast to frugivorous birds
that concentrate their droppings to the 5 m closest to the edge.
absence of sciads is a reflection of the trend favoring
shade-intolerant species to appear in the cleared pasture.
No tree seedlings germinated on the site, but there were
a few sprouts from older root stocks or stumps left amidst
the pasture. A clear trend towards pasture encroachment
is evident in the data from vegetation dynamics, with
Psidium guajaba saplings not occurring in the second survey. Conversely, recruitment was limited to only 2 saplings
of Psidium guajaba and Piper aduncum.
0
r
-
\
R
-
\
.
E
'ESCOBILLA'
-Stda
-forrnichory dnven
3
n
&/'
clearcut
I
- --
/
\
YOUNG
~ R ~ W T H i PR~GRESIVEMONTANE ~ C C E SSI O NI
FOREST
-- - - -
-
"CORDONCILLO"
chiropchory driven
"COLCA"
I
"PASTIZAL"
- -
--
I--
planted
Setaria
-
-
-
-
-
A
- - - -
abandonment
oEnECTE0
'
orn~thochorydnven
C
-A "PASTO MIEL"
/
,
, NO I , , S
--'
-
'-
-,
ARRESTED
-
-SLkXESSlON
-
FIGURE7. The three successional pathways are presented in the model that considers land-use history (i.e., cultivation, burning,
abandonment) as an important factor to the successional trajectory of the plant oligarchies of secondary growth, named after the local
usage. Abandonment of Setaria sphacelata pastures generates deflection, or arrests succession, which further degrades the fragile
slopelands, impeding the regeneration of natural montane forest species.
It can be concluded that the healthier the pasture, the
smaller the chance of regeneration of forest trees, not
due to fewer incoming seeds, but to the competitive ability of the tussock. The main result shows that there is a
potential for regeneration by seeds; however, the presence of a stronger competitor for physical space, the
foxtail grass Setam'a sphacelata, made no 'safe sites' available for incoming seeds. Comparison between the natural
Digitaria pasture, the guava Psidium pasture, and the
planted Setam'a pasture demonstrates that guava sites receive the most seed input and also provide the better
chances for establishment. Thus, having Psidium guajaba
in the natural pasture may serve as a stepping-stone mechanism to bring back dispersers into the area and quicken
its recovery.
THE DISPERSAL-SUCCESSION CONNECTION
It is assumed that the original montane forest associations will be re-established in gaps created by natural
disturbances with small or moderate size patches. Microsite patch recovery has been studied in the reserve by
Myster and Sarmiento (1997) in relation to landslides,
corroborating this assumption of progressive successional
continuum back to montane forests in small natural disturbances. According to (1) the oral history of residents
in the area (Marianitas villagers, pers. comm.), (2) recorded changes of specific lots froni 1988 (Castro, pers.
comm.), and (3) personal observational data gathered
from 1982, there is support for the hypothesis of three
distinct successional pathways following anthropogenic
disturbance related to pasture or agriculture in the
macro-sites (i.e., larger clearings). The disturbed areas
should not be seen as gaps in the forest canopy but rather
as a matrix of alternative communities,
Three successional pathways (Figure '7) are identified
depending on prior land uses: progressive, deflected, and
arrested successional scenarios are possible depending on
the treatment received after cultivation (either burning,
abandonment, or planting). The graphic model shows the
pathways after clear-cut following either (a) corn and
beans, (b) pasture, or (c) sugarcane as the starting options for the establishment of the three pathways, namely,
(I) 'balzar," (E) 'chirimbilla,' and (D) 'chilcal.'
1. Balzar appears when agriculture (mainly corn and
sugarcane plantation) follows clearing with no burning or grazing involved. It is characterized mainly by
'guarumo' Cecropia monostachya, 'balza' Ochromu pyramidale, 'caracha-coco' Otoha (cf. Djalanthera) gordoniifolia dominating the canopy, and solanaceous
shrubs (mainly Solanum aceriJolium) and Saurauia
spp., Althrrriantera spp., and Asc&ias curassavica in
the understory.
2. Chirimbilla appears when natural pasture establishes after the clearing and grazing keeps the community in place. The common species of this phase
includes 'pichu15n9 Vmonia pattens, 'chilca' Buccharis
~ululahue?zsis,'chandos9Bocconia frutescens as treelets
amidst crabgrass or khirimbilla9 (Digitaria sanpi9znlis: Poaceae), Bidens pzlosa, and Heliotropium spp. in
the understory
3. Chilcal appears when the natural pasture has been
established, but when limited grazing has kept
monospecific stands as a pseudo-orchard, locally
known as 'guayaval.' Old guayavales retain tall guava
trees within the prevalence of chilca, known as 'chilcango', but younger ones are more associated with
'pimientas' Pepmia spp., 'toas' Xanthosoma sagittifie
lia, and 'ortiguillo' Urn spp.
FIGURE8. Three seeds that represent the tendency of dispersal
associated with regeneration of montane forest into abandoned
pastures: left, Piper nduncum (a bat specialist); center. Micmia
aeruginosa (a bird specialist);and right, Ceovpia monostuchya (a
generalist) are shown as example of morphotypes in diasporas.
woody shrubs in check, favoring rapid dominance
by (E) 'colcas' (Miconia spp: Melastomataceae) and
(E) 'cordoncillo' (Piper aduncum: Piperaceae) in almost monospecific stands. Conversely, if the area was
burned to weed out the natural regrowth, the direction of succession changes towards (R) 'escobilla'
(Sida rhombzplia: Malvaceae) and 'chilca' (Baccharis
latifiolia: Asteraceae) as the dominant shrub species.
Also frequent here is 'supirrosa' (Lantana camam:
Verbenacea). In some cases, 'guayava' trees (Psidium
guajaba: Myrtaceae) become dominant, creating
In the Sdaria sphacelata planted pasture (C) it is argued
that no succession is occurring. The only few isolated
trees were either (1) planted on purpose-i.e., 'guaba'
(Inga expectabilis: Leguminosae), 'naranja agria' (Xantho@urn sp: Rutaceae), and erythrina (Elythrina smithiana:
Leguminosae), (2) left without cutting at the time of the
clearing-i.e., 'helecho arborescente' (Trichipterixp'lossisima: Cyatheaceae), 'pagche' (Nectandm membmnosa: Lauraceae), or 'arrayan' (Eugenia cf. dibmchiata: Myrtaceae),or
(3) sprouting out of stumps or roots left there after the
clearing.
It is clear that secondary dispersal of elaiosomic seeds
favors formichory; hence, the presence of genera Cyperus,
Desmodium, Sida, Lantana, and Digitaria in the regenerating community underneath the Setaria pasture. It is also
clear that the seed shadow is made of fruits of generalized
consumption for several animal taxa; of special interest
among them are Psidium guajaba, Ficus ikpida, and Cecm
pia monostachya. Indeed, Cecmpia seeds were the most conspicuous item in seeded scats, representing 41.06% of the
catch. On the other hand, the plants exhibiting specialized consumption are almost exclusive of its own disperser; for instance, ortothropous seeds of Piper aduncum
(Piperaceae),whose dispersal is mostly attributable to one
single fruit bat 'chimbilaco' (Phillostomidae: Carollia perspicilliata), produced 71% of the Piper seed count. Similarly, campylotropous seeds of Miconia aeruginosa (Melastomataceae) were only obtained from bird scats (Figure
8). Seeds from Siparuna pyricarpa (Monimiaceae) were
found only in scats from the barbet toucan 'yumbo' (Cap
itonidae: Semnornis mmphastinw). Other bird-dispersed
seeds belonged to Rubiaceae, Solanaceae, Moraceae, Poaceae, Myrtaceae, and Lauraceae. The guild of dispersers
determined in this study is presented in Table 3.
CONCLUSION
In some instances succession fails (Woodwell, 1992);
this is particularly so in the tropical Andes, where human
impacts have conditioned landscape character for millennia and have been known to ecologists for centuries (Sarmiento, 1995 c). Harden (1996) argues that forest regeneration in tropical mountains follows different
pathways to those of traditional old-field succession in
temperate mountains (i.e., the Appalachians in eastern
U.S.A.). Moreover, it is argued here that succession in the
tropical Andes is also different from that suggested for
lowland tropical forest sites in Mexico (Los Tuxtlas),
Costa Rica (La Selva), Panama (Barro Colorado), Colombia (Sierra Nevada de Santa Marta), Guyana (Mabura
Hill), Venezuela (San Carlos), Brazil (Fazenda Vithria),
and Peru (Manu). Hamilton et al. (1993),using examples
of cloud forests, emphasized the processes that separate
highland-lowland environments, but no indication of
seed ecology was provided.
The role of frugivores in increasing chances of germination by extending the seed shadow is important because they help to find 'safe sites' in sparsely planted
tussocks (Figure 9). Nevertheless, traditional techniques
to attract frugivores, such as perches, did not produce a
significant contribution for the recruitment of seeded
scats.
In the Maquipucuna Reserve, isolated small trees
amidst the pasture result from sprouting of older root
stock. Taller trees are remnants of the initial clear-cut, left
in place for the purpose of obtaining timber; good examples are the tallest 'pagche' (Nectadm membranacea) and
250 / MOUNTAINRESEARCHA N D DEVELOPMENT
TABLE3 Frugivorous disperser guilds from zoochorous seeds collected at the study site. (A) Birds, (B) bats and (C) mammals. Note local names follow the local usage ofthe Upper Guayllabamba River Basin area.
Family
Latin name
Local name
English name
Semnornis mmphastinus
Ampeloides tschudi
Crotophaga ani
Sporophila lz~ctuosa
Tiaris oliuaceae
Aulachorhynchus haematopygiu~
Andigena hminirostris
Amazona mercenaria
Pionus sordidus
Tangdra rujigula
Tangara xanthocephala
Tersina uiridis
Thraupis episcopus
T m p n masena
Trogon collaris
Turdus serranus
yumbo
carcarina
garrapatero
espiguero
jilguero
marrajo
tucin pic0 laminado
lora
lora chillona
sigcha
tanagra
azulejo
azulina
guajalito pechirojo
guajalito beteado
mirlo serrano
barbet toucan
scaled fruiteater
smooth-billed ani
black and white seedeater
yellow-faced grassquit
crimson-rumped toucanet
plate-billed mountain toucan
scaly-naped parrot
red-billed parrot
rufous-throated tanager
saffron-crowned tanager
s~vallowtanager
blue-grey tanager
masena trogon
collared trogon
glossy-black thrush
Artibeus lituratus
Carollia castanea
Carollia perspicillata
Phyllostomus hastatus panamensis
Sturnina eqthmmos
Sturnina ludouici
Varnpirops cf. infuscus
murci6lago list6n
chimbilaco rojizo
chimbilaco
murcikgalo
chimbilaco
chimbilaco flaco
vampiro
common fruit bat
fruit bat
fruit bat
fruit bat
fruit bat
fruit bat
vampire bat
Sciurus carolinensis
Didelphis marsupialis
Dasypus novemcinctus
Syluilagus brassiliensis
Oryzomysspp
b n o m i s banickii
Agouti paca
Syluilagus brassiliensis andinum
Coendu bicolor
Tremactos ornatus
P r o ~ o ncancrivorous
Potos jlavus
Mazama @nu
ardilla
zarigueya
muli ta
conejo de campo
rat6n de campo
pacarana
guanta
conejo de monte
puerco espin
oso frontino
tej6n
cusumbo
soche
red squirrel
opossum
armadillo
wild rabbit
mouse
tailed paca
paca
wild rabbit
porcupine
andean bear
racoon
tutamono
red deer
A) Birds
Capitonidae
Cotingidae
Cuculidae
Emberiziadae
Emberizidae
Ramphastidae
Ramphastidae
Psittacidae
Psittacidae
Thraupidae
Thraupidae
Thraupidae
Thraupidae
Trogonidae
Trogonidae
Turdidae
B ) Bats
Phyllostomidae
Phyllostomidae
Phyllostomidae
Phyllostomidae
Phyllostomidae
Phyllostomidae
Phyllostomidae
C ) Mammals
Sciuridae
Didelphidae
Dasypodidae
Leporidae
Cricetidae
Dinomydae
Agoutidae
Leporidae
Erethizontidae
Ursidae
Procyonidae
Procyonidae
Cervidae
two 'helechos arb6reos.' There are no available records of
bird visitation to the treeferns (Tnchiptenx pilossisirna)
although they occupy a prime location in the pasture,
This situation contrasts with records from Las Palmas,
where the only standing trees amidst pasture were Andean wax palms (Ceroxylum andinurn) which were often
visited for foraging on both canopy and ground levels.
These findings suggest that the initial pattern and composition of clearing is a major influence on the fate of
regenerating forest patches (but see Kattan and ABvarezL6pez, 1996). Selection of 'survivors' of a treefall should
favor the potential 'attractiveness' for frugivory, the 'adequacy' for shade to grazers, and the suitability for dispersal enhancement. Hence, palms should be left stand-
FIGURE
9. A panoramic view of the Culantroparnba
'anejo: in the Upper Guayllabamba river basin (now
renamed 'Cartagena' as a reflection of the recent
Colombian immigration to the area), showing the
shredding of Tropandean forests into nonregenerating patches amidst the matrix of pasture.
In the foreground, holes for ramets of Setdria sphae
htu are aligned with no concern for contouring or
terracing. Here, individual grass plants produce
abundant root mats and intricate tiller's canopy,
both of which prevent establishment of potentially
bird- or batdispersed forest trees.
ing and Psidium guajaba should be planted among the
pasture to enhance dispersal and induce rapid succession
for pasture conversion to forest.
Fallow and abandonment of Setana pastures on steep
slopes further degrade the landscape and exacerbate the
paucity of local and downstream communities, which in
most cases are in conflict with conservation approaches
(Perreault, 1996). Regeneration and rehabilitation of
montane tropical forest do not depend on time alone
(Brown and Lugo, 1994). National policies on livestock
and dairy production should be revised to detain govern-
mental subsidies to forest clearing for pasture and to
introduce incentives for a less extensive and more costeffective cattle ranching in montane areas (Rhoades,
1997). It is time for politicians to realize that there is no
longer an agricultural frontier for land development in
western Ecuador and throughout the Tropandean ecoregion and, moreover, that restoration science and management of degraded slopelands is the most appropriate
option for providing a base for sustainable development
in the fragile lands of the tropical Andes.
ACKNOWLEDGEMENTS
The research in Ecuador was partially supported by the
MacArthur Foundation and the Scott Neotropic Fund of
the Lincoln Park Zoological Society. I thank Eugene
Odum for discussions on successional theory and Ronald
Carroll for insights on sustainability. I also thank Arsenio
Barren, Luis Pozo, Espiridi6n Mosquera, and Saskia
Wolsak for assistance in the field. I am grateful to the
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