649

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(2): 649-664, April-June 2021 (Published Jun. 09, 2021)

Phenology of the endangered palm Ceroxylon quindiuense

(Arecaceae) along an altitudinal gradient in Colombia

Blanca Martínez

*; https://orcid.org/0000-0002-7074-3534

René López Camacho

; https://orcid.org/0000-0003-2026-0371

Luis Santiago Castillo

; https://orcid.org/0000-0003-2193-7516

Rodrigo Bernal

; https://orcid.org/0000-0002-9832-8498

1. Universidad Distrital Francisco José de Caldas, Bogotá, Colombia; bamartinezh@correo.udistrital.edu.co

(*Correspondence), rlopezc@udistrital.edu.co

2. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Bogotá, Colombia;

lcastillo@humboldt.org.co

3. Reserva Natural Guadualito, Montenegro, Quindío, Colombia; rgbernalg@gmail.com

Received 27-XI-2020. Corrected 20-III-2021. Accepted 18-V-2021.

ABSTRACT

Introduction: Understanding the phenology of plant populations is vital for their conservation and management.

We studied the vegetative and reproductive phenology of the endangered palm Ceroxylon quindiuense along an

altitudinal gradient in the Central Cordillera of Colombia. Objective: We describe the leaf production rate, and

flowering and fruiting cycles, and calculate food offer for the fauna, as a tool for the proper management of the

palm. Methods: At each sampling site (2 400, 2 600, 2 800, 3 000 m.a.s.l.), we marked 40 adult individuals (20

pistillate, 20 staminate), which we followed bimonthly for 24 months. We studied leaf production by counting

fallen leaves. We followed flower and fruit production through observations with binoculars and photographs.

Results: Each adult individual produced, on average, one leaf every 69 days. Although isolated individuals

flowered throughout the year, most palms flowered synchronously at each elevation in October 2016-August

2017 and in August 2018-February 2019 and had ripe fruits 7-13 months later. Flowering started at 2 600 m, fol-

lowed by 2 800 and 3 000 m. Palms at 2 400 m, the lower limit of the palm stands in the area, showed a singular

behavior, with scarce flower and fruit production, some individuals that changed sex, and a higher proportion

of pistillate palms. Each palm produced 1-11 (x

= 5.3, SD = 2.2) inflorescences and 1-10 (x

= 5.3, SD = 2.2)

infructescences. The average number of fruits per infructescence was 4 465 (SD = 1 488). With an estimated

population of adult palms between 256 000 and 600 000 and an overall ratio of pistillate: staminate individuals

1:1 or 1:2, total fruit production in the area during each fruiting period is estimated as 2.0-7.1 billion fruits.

Conclusions: The huge number of flowers and fruits and their gradual availability along the altitudinal gradient

have a major impact on the spatial and temporal distribution of food offer for fauna associated with the palm.

Key words: altitudinal gradient; flowering; fruiting; leaf production; palm phenology.

Martínez, B., López Camacho, R., Castillo, L.S., & Bernal,

R. (2021). Phenology of the endangered palm Ceroxylon

quindiuense (Arecaceae) along an altitudinal gradient in

Colombia. Revista de Biología Tropical, 69(2), 649-664.

https://doi.org/10.15517/rbt.v69i2.44835

Palms are an important element in the

dynamics of tropical ecosystems: e.g., by influ-

encing the distribution and behavior of animals,

which could affect other ecosystem functions,

such as plant regeneration (Salm, Jalles-Filho,

& Schuck-Paim, 2005; Beck, 2007; Keuroghl-

ian & Eaton, 2009) and soil properties (Young,

Raab, McCauley, Briggs, & Dirso, 2010).

Palms are a vital food source for many animal

species (e.g., Zona & Henderson, 1989; Peres,

650

Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(2): 649-664, April-June 2021 (Published Jun. 09, 2021)

1994; Galetti, Ziparro, & Morellato, 1999;

Scariot, 1999; Genini, Galetti, & Morellato,

2009; Giombini, Bravo, & Tosto, 2016). They

also play an important role for human popu-

lations, which use them as a source of food,

raw construction materials, and for making

a variety of implements, among many other

uses (e.g., Bernal, 1992; Henderson, Galeano,

& Bernal, 1995; Johnson, 2011; Bernal &

Galeano, 2013).

The Quindío wax palm, Ceroxylon quin-

diuense, is an abundant species in the cloud

forests of Colombia and Perú. In Colombia, it

grows in the three Andean ranges, although it

is more abundant in the Central Cordillera. Its

largest populations are located in the Tochecito

River basin, in the municipalities of Cajamarca

and Ibagué, Department of Tolima (Bernal,

Galeano, & Sanín, 2015), where the number

of adults has been estimated between 256 000

(Jiménez, 2017) and 600 000 individuals (Ber-

nal et al., 2015; Instituto Humboldt, 2016).

C. quindiuense is recognized worldwide

for being the world’s tallest palm, reaching

60 m in height (Bernal, Martínez, & Sanín,

2018), and Colombia’s national tree. It is con-

sidered Endangered (EN) (Galeano & Bernal,

2005), mainly due to habitat transformation as

result of human activities, especially agricul-

tural expansion. Conservation of this species

requires a thorough understanding of its popu-

lation dynamics and phenological cycles, as

well as of the underlying factors.

Phenology studies the occurrence of repet-

itive biological events and the biotic and abi-

otic environmental factors that control them.

A better understanding of the phenology of

a plant species makes it possible to evaluate,

for instance, flower and fruit availability for

the local fauna (e.g., Morellato et al., 2000;

Cabrera & Wallace, 2007), or litter produc-

tion for soil formation and nutrient input (e.g.,

Vitousek, 1984; Sayer et al., 2020), all of

which are fundamental aspects to understand

forest dynamics.

Although the conservation and manage-

ment plan for C. quindiuense in Colombia

(Bernal et al., 2015) stresses the need to

conduct phenological studies, only a single

short-term work performed by Girón-Vander-

huck, Salazar, and Agudelo (2001a) is avail-

able. In this paper we present the results of a

two-year phenological study carried out along

an altitudinal gradient in the Tochecito River

basin, in the Central Cordillera of Colombia,

where the largest palm stands of this species

are found. We describe leaf production rate,

and flowering and fruiting cycles, and contrast

them among elevations. We also calculate the

food offer for the fauna, as a tool for the proper

management of this species in the area. As tem-

perature in the tropical Andes decreases by ca.

0.6º per 100 m increase in elevation (Ramírez,

Roldán, & Yépez, 2004), this change in tem-

perature is expected to influence phenology

along the gradient. Because no similar studies

appear to have been made in the Andes, we

expected differences in parameters to occur,

but did not have any clue of the direction of

variation, if any. We hypothesized that the

flowering sequence along the gradient would

somehow be similar to the sequential flower-

ing of several Ceroxylon species, described

by Carreño-Barrera, Madriñán, and Núñez-

Avellaneda (2013).

MATERIALS AND METHODS

Study area: The study area is in the

Tochecito River basin, in the Department of

Tolima, on the Eastern slope of the Central

Cordillera of Colombia (4°30’45”-4°31’34”

N & 75°30’29”-75°26’31” W), between 2 400

and 3 000 m elevation (Fig. 1). It is a mountain

area of 8 890 ha, of which 43 % have some type

of palm cover (cloud forest remnants or sec-

ondary forests dominated by very dense palm

stands, cloud forest remnants or secondary

forests with some palms, matrix of pastures and

crops with very dense palm stands, and matrix

of pastures and crops with some palms) (Insti-

tuto Humboldt, 2016). The rainfall regime is

bimodal, with the rainiest period between June

and November, and the driest period between

February and March (IDEAM, 2020).

651

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(2): 649-664, April-June 2021 (Published Jun. 09, 2021)

Study species: Ceroxylon quindiuense is

a single-stemmed palm, reaching up to 60 m in

height (Bernal et al., 2018) and 36 cm in diam-

eter at breast height. Its crown consists of 12-27

blue-green leaves, with the pinnae covered on

the underside by a woolly whitish indument.

It is a dioecious species, although, in some

cases, individuals change sex (Martínez, Sanín,

Castillo, López, & Bernal, 2018). The inflo-

rescences are interfoliar, repeatedly branched,

supported by a long peduncle, and bearing

several thousand small, whitish flowers, which

have anthesis almost simultaneously for one

to a few days (personal observation, 2012 to

2020; Carreño-Barrera et al., 2013). Although

the flowers of both sexes look very similar, sta-

minate and pistillate inflorescences are easily

recognized, even from a great distance. Pistil-

late inflorescences remain with their rachillae

completely extended, at a wide angle with the

rachis, even after fruiting and falling to the

ground. In the staminate inflorescences, on the

other hand, the rachillae are closely appressed

to the rachis after anthesis, so that the old inflo-

rescences have a broom-like appearance (Mar-

tínez et al., 2018). Each palm produces several

infructescences simultaneously and each one

bears thousands of spherical fruits, 1-2 cm in

diameter, smooth and orange-red when ripe

(Galeano & Bernal, 2010; Sanín & Galeano,

2011).

Data collection: We surveyed four sites

located at intervals of 200 meters along an

elevation gradient starting at 2 400 m.a.s.l. and

ending at 3 000 m.a.s.l., (2 400, 2 600, 2 800 and

3 000 m.a.s.l., Fig. 1). At each elevation, indi-

viduals were selected within a range of +/- 25

m with respect to the elevation value. The 2 400

m site was established in a secondary forest and

Fig. 1. Location of the Ceroxylon quindiuense study area in the Central Cordillera of Colombia. Sampling sites at different

altitudes: 1: Las Cruces (2 400 m.a.s.l.); 2: Galleguito (2 600 m.a.s.l.); 3-4: La Carbonera (2 800 and 3 000 m.a.s.l.). Based

on IGAC (2014) layers.

652

Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(2): 649-664, April-June 2021 (Published Jun. 09, 2021)

the remaining sites were established in pastures

with isolated palm trees, overgrown pastures,

or forest edge (Fig. 2).

Adult Quindío wax palms emerge out of

the forest canopy. For this reason, observing

the crowns from within the forest is almost

impossible; however, casual observations in the

area over several years have shown that palms

growing in both forests and pastures follow the

same phenological pattern (timing, duration,

frequency and intensity in leafing, flowering,

and fruiting) (personal observation from 2005

through 2018). The individuals in this study

were thus selected in clean pastures with cattle

Fig. 2. Ceroxylon quindiuense at the Tochecito River basin, Colombia. A. Palms surviving in pastures; B. Palm-dominated

forest fragment.

653

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(2): 649-664, April-June 2021 (Published Jun. 09, 2021)

presence, overgrown pastures, or secondary

forests, in which the palm crowns were visible

(Fig. 2).

At each sampling site, 40 adult individu-

als 20-40 meters tall were chosen (20 stami-

nate and 20 pistillate), taking a random initial

individual and thereafter selecting the closest

neighbor that was within the elevation belt of

50 m described above. Each individual was

marked with an aluminum plate tied to the stem

with a nylon thread, at a height of 1.6 m above

the ground.

We made observations of reproductive

structures using binoculars and photographs.

The phenological data were recorded bimonth-

ly between October 2017 and October 2019. In

each of the selected individuals, the presence of

reproductive structures was evaluated, taking

into account the following phenophases: bud:

reproductive structure wrapped in the pedun-

cular bracts; flower: inflorescence composed

of yellowish-white flowers at anthesis; old

inflorescence: inflorescence in which almost

100 % of the flowers have fallen and only the

axes remain; immature fruits: infructescence

with well-formed fruits, which have reached

their final size but are still green; ripe fruits:

infructescence in which almost all fruits are

orange-red; old infructescence: infructescence

that has lost 100 % of its fruits and of which

only the axes remain. During the observations,

the ripe fruits category was divided into three

subcategories, which were pooled for some of

the analyses: ripe fruits 1: ripe infructescence

in which more than 50 % of the fruits persist;

ripe fruits 2: ripe infructescence in which

20-50 % of the fruits persist; ripe fruits 3: ripe

infructescence in which less than 20 % of the

fruits persist.

To follow the development of each of the

reproductive structures, we took its position

in the crown, choosing a fixed point in the

terrain, from which the crown was seen as a

clock dial, in which the structures were located

in a clockwise direction, starting from six. The

apex of the reproductive structure was taken as

an indicator of the position on the dial. Each

crown was observed from different angles to

corroborate the structure’s stage.

In addition to the reproductive stage, we

recorded leaf production for each individual

at altitudes of 2 600, 2 800, and 3 000 m. To

do this, we followed 84 palms (37, 18 and

29 individuals, respectively) over 18 months,

counting, in each observation, the number of

fallen leaves found around the palm’s base.

Once counted, fallen leaves were removed

from the place to facilitate the next count. The

number of fallen leaves between two observa-

tions was assumed to correspond to the number

of leaves produced by the palm, since in the

long term, the number of leaves on the crown

remains constant (Tomlinson, 1963; Corner,

1966). Leaf production was not followed at the

2 400 m site, as it lay on a very steep and inac-

cessible slope, which could be observed with

binoculars and photographed, but in which

the palms were inaccessible. Additionally, to

know the contribution of biomass to the basin,

we weighed all fallen leaves and old inflores-

cences and infructescences in the August 2019

observation. To estimate the number of fruits

per infructescence, we randomly took six ripe

infructescences fallen on the ground, from

which we removed and counted all fruits. The

fresh and dry weight of 100 fruits and their

respective seeds were obtained, to calculate

the total weight of the food supply offered

by the palms.

Data analysis: Since palms present a

structure composed of successive leaf-inflores-

cence-internode modules (Henderson, 2002),

the development of each of their reproductive

structures (buds, inflorescences, and infruc-

tescences) can be followed individually. As

floral anthesis lasts only 2-3 days (personal

observation from 2005 through 2018; Carreño-

Barrera et al., 2013; Carreño-Barrera, Núñez-

Avellaneda, Sanín, & Campos, 2020), and our

observations were bimonthly, the probability of

finding an inflorescence at anthesis during the

observation period was low. For this reason,

for each reproductive structure, the month of

its flowering was interpolated between the last

654

Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(2): 649-664, April-June 2021 (Published Jun. 09, 2021)

observation in which it was found in bud and

the appearance of a structure with early devel-

oping fruits.

On the other hand, the total development

time from flower to ripe fruits observed in 211

inflorescences at the 2 600, 2 800, and 3 000 m

elevations was taken as the median value for

each site. This value was applied retrospec-

tively to those structures that were in ripe fruit

at the time when our observations started in

October 2017, and prospectively to those in

flowering in October 2019. In this way, the

data taken to the pistillate individuals for 24

months allowed us to extrapolate the behavior

of the flowering cycles twelve months back-

wards until October 2016, and eight months

forward, until June 2020. Thus, flowering and

fruiting cycles in pistillate individuals in this

study cover almost four years. At the 2 400 m

elevation, only the data of the single individual

that had a complete cycle were used. For the

staminate inflorescences, due to their ephem-

eral nature, no extrapolations or interpolations

could be done.

The duration of the fruiting period was

determined as the number of months between

the appearance of ripe infructescences in any

of the three states (ripe fruits 1, 2 or 3) and

the fall of all fruits (old infructescence). To

determine the fruiting peaks at each elevation,

only ripe infructescences with almost 100 % of

their fruits (ripe fruits 1) were considered, to

avoid counting the same infructescence in two

consecutive observations.

The development time of female repro-

ductive structures from pistillate flower to

ripe fruit at each elevation was taken as the

median number of months it took the pistillate

inflorescences for which a complete cycle was

observed (i.e., from the appearance of flowers

to the appearance of ripe fruits 1).

As our data were not normally distrib-

uted, we used Kruskal-Wallis tests to compare

the development time from flower to ripe

fruit, and leaf production between the differ-

ent elevations, and between sexes. We used

Spearman correlation to correlate precipita-

tion data with flowering and fruiting. We used

circular statistics to evaluate seasonality in the

C. quindiuense reproductive phenology and

also to find differences in the seasonal patterns

among altitudes. This circular statistic requires

months to be transformed to angles (Zar, 1999;

Morellato et al., 2000). As our field observa-

tions indicate that C. quindiuense shows a

2-year reproductive cycle, we used intervals of

15 degrees between months, being November

2019: 7.5° and October 2019: 352.5°. We dis-

missed the October 2017 data in the circular

analysis as we only considered a 24-month

cycle in the statistics.

The circular statistical analyses were done

using the ORIANA v.4.02 software (Kovach,

1994). The evaluated parameters were: mean

vector, length of mean vector, median, and

circular standard deviation. As some of our

data are not normally distributed (they do not

match the von Mises distribution), we used the

Rao’s non-parametric test (U) for uniformity at

each elevation and for every type of reproduc-

tive structure (i.e., pistillate inflorescences,

staminate inflorescences and infructescences).

This test points out the probability of the data

being randomly distributed. If the test rejects

the hypothesis of uniformity, it means that

the studied population shows seasonality in

its reproduction. Then, we used the Watson

non-parametric test to compare seasonal-

ity among the different elevations and for

each type of reproductive structure. Here, the

hypothesis is that the mean vectors of the two

sampled populations are not significantly dif-

ferent. If this hypothesis is rejected, it means

the reproductive phenology is asynchronical

between altitudes (Morellato et al., 2000).

Only field data were included in the statistical

treatments.

RESULTS

Development time of the 211 reproductive

structures from pistillate flower to ripe fruit

ranged from seven to eleven months and dif-

fered among sites (Table 1). It took longer for

the individuals at 2 800 and 3 000 m than for

those at 2 400 and 2 600 m (χ² = 84.737). There

655

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(2): 649-664, April-June 2021 (Published Jun. 09, 2021)

were significant differences between 2 600 and

2 800 m (P = 7.3e-14) and between 2 600 and

3 000 m (P = 2.2e-16), but not between 2 800

and 3 000 m.

The observed events and the correspond-

ing extrapolations showed that between Octo-

ber 2016 and June 2020 there were two major

pistillate flowering events and two major fruit-

ing events in the Tochecito River basin. The

flowering events happened between October

2016 and August 2017 and between August

2018 and February 2019. The fruiting events

took place between September 2017 and April

2018 and between May 2019 and January 2020

(Fig. 3).

During the 24 months analyzed with circu-

lar statistics, flowering and fruiting showed a

seasonal behavior for all the elevations (Rao’s

Spacing Test (U) P < 0.01, length of mean vec-

tor > 0.6). Only female palms at 2 400 showed

no flowering peaks (U = 180, 0.1 > P > 0.01),

possibly explained by the low number of pis-

tillate flowers recorded at this site (6 female

inflorescences) (Table 2). Furthermore, flower-

ing and fruiting peak events were significantly

different among all elevations (Watson U

test, Table 3), supporting the idea that this

palm population has an altitudinally sequential

reproductive phenology (Table 3).

TABLE 1

Development time of reproductive structures of Ceroxylon quindiuense in Tochecito, Tolima,

Colombia, from pistillate flower to ripe fruit

Elevation

(m.a.s.l.)

Number of inflorescences with a full cycle observed

(number of individuals)

Duration (Months)

Range Median

2 400 1 (1) 7

2 600 50 (11) 7-11 8

2 800 74 (13) 8-13 11

3 000 86 (14) 8-12 11

Fig. 3. Number of pistillate inflorescences and mature infructescences of Ceroxylon quindiuense at the Tochecito River

basin, Colombia, at four elevations (2 400 to 3 000 m.a.s.l.), between 2016 and 2020.

656

Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(2): 649-664, April-June 2021 (Published Jun. 09, 2021)

TABLE 2

Descriptive and circular statistics for the 24-month reproductive phenological

cycle of Ceroxylon quindiuense in Tochecito, Tolima, Colombia

Elevation

(m.a.s.l.)

Observations

(N)

Mean vector

(month-year)

Length of mean

vector (r)

Median

(month-year)

Circular

Rao’s Spacing

Test (U)

Rao’s Spacing

Test (p)

Staminate inflorescences

2 400 12

95.6°

0.718

67.5°

46.6° 255 < 0.01

(May-18) (Mar-18)

2 600 114

158.3°

0.583

172.5°

59.5° 315.789 < 0.01

(Sep-18) (Oct-18)

2 800 143

157.3°

0.292

187.5°

89.9° 322.238 < 0.01

(Sep-18) (Nov-18)

3 000 168

183.9°

0.164

202.5°

109.0° 317.143 < 0.01

(Nov-18) (Dec-18)

Pistillate inflorescences

2 400 6

154.6°

0.613

172.5°

56.7° 180 0.10 > P > 0.05

(Sep-18) (Oct-18)

2 600 54

175.4°

0.97

187.5°

14.2° 333.333 < 0.01

(Oct-18) (Nov-18)

2 800 104

186.9°

0.655

187.5°

52.7° 321.923 < 0.01

(Nov-18) (Nov-18)

3 000 137

221.0°

0.65

232.5° 53.2°

336.35 < 0.01

(Jan-19) (Feb-19)

Infructescences

2 400 75

32.3°

0.886

37.5°

28.2° 321.6 < 0.01

(Jan-18) (Jan-18)

2 600 60

308.1°

0.85

307.5°

32.7° 318 < 0.01

(Jul-19) (Jul-19)

2 800 176

2.9°

0.802

7.5°

38.1° 335.455 < 0.01

(Nov-17) (Nov-17)

3 000 117

43.8°

0.766

52.5°

41.8° 326.154 < 0.01

(Jan-18) (Feb-18)

TABLE 3

Square matrix showing the Watson U

test results for each reproductive structure and comparing altitudes

for the 24-month reproductive phenological cycle of Ceroxylon quindiuense in Tochecito, Tolima, Colombia

Elevation (m.a.s.l.) 2 400 2 600 2 800 3 000

2 400 —

SF < 0.05

PF < 0.05

IF < 0.001

SF < 0.001

PF < 0.05

IF < 0.001

SF < 0.002

PF < 0.01

IF < 0.001

2 600

SF: 0.225

PF: 0.225

IF: 2.947

—

SF < 0.001

PF < 0.02

IF < 0.001

All < 0.001

2 800

SF: 0.524

PF: 0.206

IF: 2.486

SF: 1.098

PF: 0.243

IF: 3.358

— All < 0.001

3 000

SF: 0.359

PF: 0.286

IF: 1.718

SF: 1.772

PF: 4.22

IF: 3.629

SF: 0.461

PF: 5.444

IF: 4.984

—

scores (lower half) and probabilities (upper half). SF: Staminate inflorescences, PF: Pistillate inflorescences, and

IF: Infructescences.

657

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(2): 649-664, April-June 2021 (Published Jun. 09, 2021)

During each flowering and fruiting event,

the peaks were not simultaneous at the differ-

ent elevations. For the first major event (2016-

2017), the flowering peak took place first at

2 800 m in January 2017, followed by 2 600 m

in February, 3 000 m in March and ending at

2 400 m in June. However, because the flower-

to-fruit development time was different among

elevations (Table 1), the order of appearance of

the fruiting peaks along the gradient was not

the same as that of flowering peaks. The first

peak of ripe fruits started at 2 600 m in October

2017, and from there advanced upward to 2 800

m (December) and downward to 2 400 m (Janu-

ary 2018), ending at 3 000 m in February 2018.

During the second major event, flowering

had a first peak at 2 400 m in October 2018,

although with just three inflorescences, at 2 600

and 2 800 m in November, and 3 000 m in Feb-

ruary 2019. Fruiting peaks started at 2 400 m in

May 2019 and ascended along the gradient to

2 600 m (June), 2 800 m (October), ending at

3 000 m in January 2020. For each elevation, 24

months elapsed between the two major flower-

ing peaks and 22-24 months between the two

major fruiting peaks (Fig. 3). In the first major

fruiting event there were 369 infructescences,

whereas in the second major event they were

256 (Fig. 3). Because of the steep terrain, the

great abundance of palms and the strikingness

of ripe infructescences, the altitudinal shift of

the fruiting process is an appealing feature of

the basin’s landscape.

In addition to the two major flowering

events mentioned above, there were two minor

ones: the first between October 2017 and April

2018, and another between July and September

2019. At the peaks of these events, the number

of inflorescences produced was 6-24 times

smaller than in the major ones. During these

minor events, there were no inflorescences at

some sites (Fig. 4).

Furthermore, the reproductive behavior

of pistillate individuals was clearly related to

elevation (Watson U

test, Table 3). While the

number of palms that went through two flow-

ering and fruiting cycles increased uphill (4

individuals at 2 400 m, 11 individuals at 2 600

m, 15 individuals at 2 800 m, 20 individuals

at 3 000 m, N = 80 individuals), the number

of palms with a single cycle decreased (16

individuals at 2 400 m, 9 individuals at 2 600

Fig. 4. Number of staminate and pistillate inflorescences of Ceroxylon quindiuense at the Tochecito River basin, Colombia,

at four elevations (2 400 to 3 000 m.a.s.l.), between 2016 and 2020.

658

Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(2): 649-664, April-June 2021 (Published Jun. 09, 2021)

m, 4 individuals at 2 800 m, 0 individuals at

3 000 m, N = 80 individuals). The total number

of infructescences per cycle also increased

with elevation (cycle one: 74 infructescences

at 2 400 m, 85 infructescences at 2 600 m, 115

infructescences at 2 800 m, 105 infructescences

at 3 000 m, N = 80 individuals; cycle two: 5

infructescences at 2 400 m, 54 infructescences

at 2 600 m, 59 infructescences at 2 800 m, 114

infructescences at 3 000 m, N = 80 individuals),

regardless of the number of cycles.

The average number of inflorescences pro-

duced per individual for the first major flower-

ing event was 5.3 (N = 72, SD = 2.1) and, for

the second, 5.1 (N = 50, SD = 2.3). Not all indi-

viduals flowered and fruited in every reproduc-

tive event. During the study period, 60 % of the

80 pistillate individuals went through two flow-

ering and fruiting cycles, whereas 39 % only

one. A single individual, at 2 800 m elevation,

went through three flowering cycles (Decem-

ber 2016, January 2018, November 2018).

The average number of infructescences

produced per individual for the two major

fruiting events was 5.3 (N

= 69, N

= 50, SD

= 2.2). The average number of fruits per

infructescence was 4 465 (N = 6, SD = 1 488).

The fresh weight of each fruit was on average

2.5 g (N = 100, SD = 0.3 g) and the weight of

the edible fleshy pericarp was 1.15 g (N = 100).

The data for staminate inflorescences

cannot be extrapolated, so we only included

two-year data. Furthermore, because of the

ephemeral anthesis of the inflorescence and the

persistence of old inflorescences for several

months (personal observation; Carreño-Barrera

et al., 2013), it was not easy to individually

monitor each structure in its old inflorescence

stage. For this reason, we only considered those

inflorescences that we observed at anthesis or

whose flowering had evidently taken place a

few days before our observation. During the

two years of our study, there were always at

least a few staminate inflorescences in the

basin. At our sampling sites, there were only

two months (March and August 2019) in which

no palm had any inflorescences.

But amid this year-round staminate flow-

ering, two groups of well-defined peaks were

evident at each altitude (Fig. 4) (Rao’s Spacing

Test P < 0.01, length of mean vector > 0.1). At

elevations 2 800 and 3 000 m., the length of the

mean vector had values close to zero (0.292

and 0.164, respectively), which shows that

although there is a seasonality, it is not very

well marked. A minor peak occurred between

January and March 2018, and another one,

almost twice as large, between October 2018

and February 2019. The largest of these groups

of peaks coincided with the second major pis-

tillate flowering event. The smaller of them

largely matched the minor pistillate flowering

event between January and April 2018 (Fig. 4).

The number of leaves in the crown was

12-27 (Me = 18, SD = 2.4, N = 160) and the

median number of leaves produced per indi-

vidual in 18 months was eight (N = 83, SD =

2.2), that is, 5.3 leaves per year (one leaf every

69 days). There was no difference in leaf pro-

duction rate among elevations (χ2 = 1.9844, P

= 0.3708), or between staminate and pistillate

individuals (χ2 = 0.45817, P = 0.4985). Each

fallen leaf weighted 2.86 kg on average (N =

66, SD = 1.3 kg). On the other hand, the aver-

age weight of an old male inflorescence was

1.84 kg (N = 20, SD = 1.12 kg), whereas old

infructescences weighted 2.35 kg (N = 15,

SD = 0.97 kg).

Although the overall trend of flowering

graphically suggests a higher production of

female inflorescences when rainfall decreases

(Fig. 5), statistically there was no significant

correlation (R

= -0.107236, P = 0.4832).

The number of infructescences produced in

the basin and the precipitation did not show a

statistically significant correlation either (R

-0.0105917, P = 0.9449).

DISCUSSION

The sequential flowering of C. quindi-

uense along the altitudinal gradient at our study

site probably plays the same role as the orches-

trated flowering of several species growing

along a gradient elsewhere in the Colombian

659

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(2): 649-664, April-June 2021 (Published Jun. 09, 2021)

Andes, as described by Carreño-Barrera et al.

(2020), as a mechanism to enhance pollination.

The staminate flowers of C. quindiuense are a

vital food source and a place of reproduction

for several species of nitidulid beetles of the

genus Mystrops, the main pollinators of Cer-

oxylon species (Carreño-Barrera et al., 2020).

The insects and the palms maintain a close

relationship of pollinator-plant specificity that

makes them highly dependent on each other.

To maintain pollinator populations, palms of

the genus Ceroxylon have developed strategies

that allow them to have a constant supply of

pollen for the beetles. Where several Ceroxylon

species co-occur, one of these strategies is the

asynchronous flowering of the different Cer-

oxylon species along the gradient, so that there

is a steady offer of flowers over a long period

of time (Carreño-Barrera et al., 2020).

At our study area, however, this strategy

would not work, as there is only one other spe-

cies of Ceroxylon in the basin, C. parvifrons,

represented by just a handful of individuals

(ca. ten detected by us so far), growing above

the upper limit of the large stands of C. quin-

diuense. A long-term phenological study of C.

quindiuense along an elevational gradient, in

an area where other species of the genus co-

occur, as in Southern Colombia, would help to

test this hypothesis.

During the seven-month flowering season

of C. quindiuense at our study sites, the popu-

lations of nitidulids probably migrate along

the altitudinal gradient, following the offer of

food and breeding sites. In the months when

flowering is less abundant, the populations of

Mystrops spp. probably undergo a significant

decline, and these insects would survive on

the isolated palms that flower asynchronously

throughout the year. This pattern of isolated

flowering individuals that maintain the pol-

linator’s population has also been found for

staphylinids associated with Phytelephas mac-

rocarpa (as P. seemannii), another dioecious

palm related to Ceroxylon (Bernal & Ervik,

1996). Thus, highly specialized nitidulid spe-

cies associated with wax palms depend on

healthy and large population of their hosts for

local persistence. As wax palm populations

dwindle, there will be lesser chances for these

beetle species to survive.

Fig. 5. Monthly pistillate flowering and fruiting of Ceroxylon quindiuense at the Tochecito River basin, Colombia, between

2016 and 2020, combined with rainfall data for the area. Rainfall data from IDEAM, Toche Climatological Station

(21210180) (IDEAM, 2020).

660

Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(2): 649-664, April-June 2021 (Published Jun. 09, 2021)

Another strategy for maintaining pollina-

tor populations in our study area is probably

the reproductive alternation between individu-

als in the population over the years. Whereas

60 % of the observed individuals went through

two flowering cycles during the 44 months of

the study, 39 % of them went through a single

cycle. The gradual increase, along the eleva-

tion gradient, both in the number of individu-

als with two cycles and in the total number of

infructescences produced, results in an altitu-

dinal shift of the number of flowers and fruits

available in the basin.

Moreover, the finding of an individual that

had three flowering cycles and another that

only flowered in abundance once after many

months of having no reproductive evidence

suggests that there could be at least three flow-

ering frequencies in the basin, with different

amplitudes. The occasional synchrony of these

three frequencies would explain the periodic

occurrence of a large C. quindiuense fruiting

event in the Central Cordillera of Colombia,

which has been reported to happen every six to

seven years (Bernal et al., 2015).

On the other hand, the number of infruc-

tescences produced by the palms in each cycle

was not the same. In the second fruiting cycle,

the total number of infructescences at our study

sites decreased from 399 to 262. This alterna-

tion of high with lower production cycles, in

which not all individuals produce fruits, is

probably related to the severe stress suffered

by the palms after a mass fruiting event (Ber-

nal et al., 2015). In individuals that produce

seven to nine infructescences, several leaves

dry off shortly after the fruiting season, giving

the palm a sickly appearance; however, palms

recover completely after a few months. Those

palms do not produce so many infructescences

in their next cycle, or even do not produce any

infructescence at all, as might be the case with

individuals that had only one cycle.

The anomalous behavior of the sampling

site located at 2 400 m is particularly interest-

ing. This site had a different male:female ratio

than the other three sites (2:3 vs. 1:1); five

individuals that changed sex (four from male to

female and one from female to male) (Martínez

et al., 2018); and an adult individual that never

exhibited any reproductive structures. More-

over, this site had the highest number of palms

with a single fruiting cycle and the lowest total

number of infructescences. Interestingly, the

2 400 m site is at the lower limit of the huge

palm stands of this basin; although C. quindi-

uense is distributed there from 2 000 to 3 100

m, only isolated individuals are found below

2 400 m, often on very steep slopes.

The number of adult palms in the Toch-

ecito River basin has been estimated between

256 158 (Jiménez, 2017) and 600 000 (Bernal

et al., 2015; Instituto Humboldt, 2016), and

the proportion of pistillate individuals to sta-

minate between 1:1 (Girón-Vanderhuck et al.,

2001a; Sanín, 2013; Sanín, Anthelme, Pin-

taud, Galeano, & Bernal, 2013; Bernal et al.,

2015) and 1:2 (Jiménez, 2017). Table 4 shows

the estimated fruit production, based on data

reported by Jiménez (2017) and Bernal et al.

(2015) and Instituto Humboldt (2016), taking

the area reported by Castillo and Díaz (2016).

Ceroxylon quindiuense fruits are consumed

by numerous species of birds, as Green Jay

(Cyanocorax yncas), Crimson-Rumped Tou-

canet (Aulacorhynchus prasinus), Black-Billed

Mountain Toucan (Andigena nigrirostris),

thrushes (Turdus spp.), parrots (Hapalopsit-

taca fuertesi, H. amazonina and Ognorhynchus

icterotis) (Galeano & Bernal, 2010; Sanín &

TABLE 4

Fruit production of Ceroxylon quindiuense by reproductive event in the Tochecito River basin, Tolima, Colombia

Source for estimation of

the number of individuals and

the proportion of sexes

Number of adult

female individuals

Number of

infructescences

produced

Number of fruits

Overall weight of the

edible fleshy pericarp (t)

Jiménez (2017) 85 385 452 540 2 020 293 333 2 324

Bernal et al. (2015) 300 000 1 590 000 7 099 350 000 8 164

661

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(2): 649-664, April-June 2021 (Published Jun. 09, 2021)

Galeano, 2011; Bernal et al., 2015). The huge

number of fruits produced during a fruiting

event (between 2.0 and 7.1 billion fruits) rep-

resents a supply of edible pulp of 2 324-8 164

tons over an eight-month period. The altitudinal

shift of this food supply should have a tremen-

dous impact on the associated fauna and prob-

ably causes altitudinal migrations of animals in

the basin, as has already been documented for

other plant species at various sites (e.g., Levey,

1988; Loiselle & Blake, 1991; Laps, 1996;

Kimura, Yumoto, & Kikuzawa, 2001; Malizia,

2001; Castro, Galetti, & Morellato, 2007).

During the twelve months in which few or

no fruits of C. quindiuense are available in the

basin, the frugivores must turn to other food

sources. In the Tochecito River basin there are

at least 237 species of trees and shrubs (Girón-

Vanderhuck, Agudelo, & Macías, 2001b),

among which we have identified at least 101,

mainly in the families Solanaceae, Melasto-

mataceae, Myrsinaceae, Rubiaceae and Laura-

ceae; that could be potential food sources for

the fauna in times when Ceroxylon fruits are

not available. Information on the phenological

cycles of these species and the quantification

of their food supply are vital for understanding

the spatial and temporal dynamics of the fauna

associated with C. quindiuense.

Besides its impact on the populations of

pollinators and frugivores, C. quindiuense has

another major effect on the ecosystems in the

double-canopy forests of this basin, where the

palms make “a forest above the forest”. With

the large number of adult palms, each produc-

ing 5.3 leaves per year and each of these with

an associated old inflorescence or old infructes-

cence, the palm’s contribution of biomass to the

basin (not including flowers and fruits) is esti-

mated to be 6 605-15 739 tons per year, i.e., ca.

3-7.2 tons per hectare. This astonishing amount

of biomass, coming from an extra emergent

canopy (not including that from the forest

canopy below) could make Tochecito and its

palm-rich forests one of the most productive

ecosystems in the high Andes. For example,

Vitousek (1984) and Wallis et al. (2019) have

reported annual values of 3.7 to 11.6 tons of

litter production per hectare in what we assume

are single-canopy Neotropical mountain for-

ests. Furthermore, the large size and weight of

the leaves and old infructescences, and their

fall from heights greater than 40 m, undoubt-

edly have an important role in shaping regen-

eration in the palm-dominated forests. Because

of this, conserving Ceroxylon quindiuense in

the Tochecito River basin is vital for conserv-

ing the whole ecosystem in the area.

Ethical statement: authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are

fully and clearly stated in the acknowledge-

ments section. A signed document has been

filed in the journal archives.

ACKNOWLEDGMENTS

We thank the Cardona Lozano family

(Marlene, Francis, Oscar, César, Leandro, Sar-

ita, Osquítar), Francisco Javier Trujillo (Pachi-

to) and his family, for their hospitality and

friendship during the data collection time, Wil-

liam Vargas for information about the flora of

the region, Steven Bernal, Arthur Campos and

Javier Carreño for information about circular

statistics, the Alexander von Humboldt Insti-

tute and Nature and Culture International for

financial support, and Idea Wild for donation

of equipment.

RESUMEN

Fenología de la palma en peligro

Ceroxylon quindiuense (Arecaceae) a lo largo

de un gradiente altitudinal en Colombia.

Introducción: Comprender la fenología de las pobla-

ciones de plantas es vital para su conservación y manejo.

Estudiamos la fenología vegetativa y reproductiva de la

palma amenazada Ceroxylon quindiuense a lo largo de un

gradiente altitudinal en la Cordillera Central de Colombia.

Objetivo: Describimos la tasa de producción de hojas, los

ciclos de floración y fructificación, y calculamos la oferta

662

Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(2): 649-664, April-June 2021 (Published Jun. 09, 2021)

alimentaria para la fauna, como una herramienta para el

adecuado manejo de la palma. Métodos: En cada sitio de

muestreo (2 400, 2 600, 2 800, 3 000 m.s.n.m.), marcamos

40 individuos adultos (20 pistilados, 20 estaminados), que

seguimos bimestralmente durante 24 meses. Estudiamos la

producción de hojas contando las caídas al suelo. Seguimos

la producción de flores y frutos a través de observaciones

con binoculares y fotografías. Resultados: Cada indivi-

duo adulto produjo, en promedio, una hoja cada 69 días.

Aunque los individuos aislados florecieron durante todo el

año, la mayoría de las palmas florecieron sincrónicamente

en cada elevación entre octubre 2016 y agosto 2017 y de

agosto 2018 a febrero 2019 y tuvieron frutos maduros entre

7-13 meses después. La floración comenzó a los 2 600 m,

seguida de los 2 800 y los 3 000 m. Las palmas a 2 400 m,

límite inferior de los palmares de la zona, mostraron un

comportamiento singular, con escasa producción de flo-

res y frutos, varios individuos que cambiaron de sexo y

una mayor proporción de palmas pistiladas. Cada palma

produjo 1-11 (x

= 5.3, SD = 2.2) inflorescencias y 1-10 (x

= 5.3, SD = 2.2) infrutescencias. El número promedio de

frutos por infrutescencia fue de 4 465. Con una población

estimada de palmas adultas entre 256 000 y 600 000 y una

proporción total de individuos pistilados: estaminados 1:1

o 1:2, la producción total de frutos en el área durante cada

período de fructificación se estima en 2.0-7.1 mil millones

de frutos. Conclusiones: La gran cantidad de flores y fru-

tos y su progresiva disponibilidad a lo largo del gradiente

tienen un impacto importante en la distribución espacial y

temporal de la oferta de alimento para la fauna asociada

a la palma.

Palabras clave: gradiente altitudinal; floración; fructifica-

ción; producción de hojas; fenología de palmas.

REFERENCES

Beck, H. (2007). Synergistic impacts of ungulates and fall-

ing palm fronds on saplings in the Amazon. Journal

of Tropical Ecology, 23(5), 599-602.

Bernal, R. (1992). Colombian palm products. In M. Plot-

kin & L. Famolare (Eds.), Sustainable harvest and

marketing of rain forest products (pp. 158-172).

Washington D.C., USA: Island Press.

Bernal, R., & Ervik, F. (1996). Floral biology and pollina-

tion of the dioecious palm Phytelephas seemannii

in Colombia: An adaptation to Staphylinid beetles.

Biotropica, 28(4), 682-696.

Bernal, R., & Galeano, G. (2013). Cosechar sin destruir-

Aprovechamiento sostenible de palmas colombianas.

Bogotá, Colombia: Instituto de Ciencias Naturales,

Universidad Nacional de Colombia Press.

Bernal, R., Galeano, G., & Sanín, M.J. (2015). Plan de

conservación, manejo y uso sostenible de la palma

de cera del Quindío (Ceroxylon quindiuense), Árbol

Nacional de Colombia. Bogotá, Colombia: Ministe-

rio de Ambiente y Desarrollo Sostenible - Universi-

dad Nacional de Colombia Press.

Bernal, R., Martínez, B., & Sanín, M.J. (2018). The world’s

tallest palms. Palms, 62(1), 5-16.

Cabrera, H., & Wallace, R. (2007). Patrones fenológicos de

ocho especies de palmeras en un bosque amazónico

de Bolivia. Revista Boliviana de Ecología y Conser-

vación Ambiental, 21(1), 1-18.

Carreño-Barrera, J., Madriñán, S., & Núñez-Avellaneda,

L.A. (2013). Ecología de la polinización de tres pal-

mas de cera (Ceroxylon parvifrons, C. ventricosum

y C. vogelianum) coexistentes en el sur de los Andes

de Colombia (Tesis de Maestría). Universidad de los

Andes, Bogotá, Colombia. Retrieved from https://

repositorio.uniandes.edu.co/handle/1992/11983

Carreño-Barrera, J., Núñez-Avellaneda, L.A., Sanín., M.J.,

& Campos, A. (2020). Orchestrated flowering and

interspecific facilitation: Key factors in the mainte-

nance of the main pollinator of coexisting threatened

species of Andean wax palms (Ceroxylon spp.).

Annals of the Missouri Botanical Garden, 105(3),

281-299.

Castillo, L.S., & Díaz, J. (2016). Resumen descriptivo de

las unidades de cobertura de la tierra para Tochecito.

Instituto de Investigación de Recursos Biológicos

Alexander von Humboldt y Naturaleza y Cultura

Internacional. (Unpublished report).

Castro, E.R., Galetti, M., & Morellato, P.C. (2007). Repro-

ductive phenology of Euterpe edulis (Arecaceae)

along a gradient in the Atlantic rainforest of Brazil.

Australian Journal of Botany, 55(7), 725-735.

Corner, E. (1966). The Natural History of Palms. London,

UK: Weindenfeld and Nicholson Press.

Galeano, G., & Bernal, R. (2005). Palmas (familia Are-

caceae o Palmae). En E. Calderón, G. Galeano, &

N. García (Eds.), Libro Rojo de Plantas de Colom-

bia (pp. 59-223). Bogotá, Colombia: Ministerio de

Ambiente, Vivienda y Desarrollo Territorial/ Instituto

Alexander von Humboldt/Instituto de Ciencias Natu-

rales Press.

Galeano, G., & Bernal, R. (2010). Palmas de Colombia:

guía de campo. Bogotá, Colombia: Instituto de Cien-

cias Naturales, Universidad Nacional de Colombia

Press.

Galetti, M., Ziparro, V., & Morellato, L.P. (1999). Fruit

phenology and frugivory on the palm Euterpe edulis

in a lowland Atlantic forest of Brazil. Ecotropica, 5,

115-122.

Genini, J., Galetti, M., & Morellato, L.P. (2009). Fruit

phenology of palms and trees in an Atlantic rainforest

land-bridge island. Flora, 204(2), 131-145.

663

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(2): 649-664, April-June 2021 (Published Jun. 09, 2021)

Giombini, M.A., Bravo, S.P., & Tosto, D.S. (2016). Seed

dispersal of the palm Syagus romanzoffiana by tapirs

in the semi-deciduos Atlantic forest of Argentina.

Biotropica, 41(4), 408-413.

Girón-Vanderhuck, M., Salazar, G.E., & Agudelo, F.D.

(2001a). Estructura poblacional de la palma de cera

Ceroxylon quindiuense (Karst.) H. Wendl. en Toche,

Tolima. En M. Girón-Vanderhuck (Ed.), Bosques de

palma de cera (pp. 31-41). Armenia, Colombia: Uni-

versidad del Quindío Press.

Girón-Vanderhuck, M., Agudelo, C.A., & Macías, D.

(2001b). Estructura y diversidad florística de tres

bosques de palma de cera. En M. Girón-Vanderhuck

(Ed.), Bosques de Palma de Cera (pp. 127-157).

Armenia, Colombia: Universidad del Quindío Press.

Henderson, A. (2002). Evolution and Ecology of Palms.

New York, USA: The New York Botanical Garden

Press.

Henderson, A., Galeano, G., & Bernal, R. (1995). Field

Guide to the Palms of the Americas. Princeton, USA:

Princeton University Press.

Instituto Humboldt (Instituto de Investigación de Recursos

Biológicos Alexander von Humboldt). (2016). Propu-

esta para la creación de un santuario de flora nacio-

nal para la Palma de Cera (Ceroxylon quindiuense)

(Unpublished report).

IDEAM (Instituto de Hidrología, Meteorología y Estudios

Ambientales). (2020). Consulta y Descarga de Datos

Hidrometeorológicos. Retrieved from http://dhime.

ideam.gov.co/atencionciudadano

IGAC (Instituto Geográfico Agustín Codazzi). (2014).

Base cartográfica integrada a escala 1:100.000 en

formato Geodatabase, actualizada a 2014. Retrieved

from https://geoportal.igac.gov.co/contenido/

datos-abiertos-cartografia-y-geografia

Jiménez, I. (2017). Estado actual de conservación de la

población de Ceroxylon quindiuense (H. Karst.)

H.Wendl (Arecaceae) en la microcuenca del río

Tochecito, Tolima (Tesis de pregrado). Pontificia

Universidad Javeriana, Bogotá, Colombia.

Johnson, D. (2011). Non wood forest products. Tropical

Palms. Rome, Italy: Food and Agriculture Organiza-

tion of the United Nations.

Keuroghlian, A., & Eaton, D.P. (2009). Removal of palm

fruits and ecosystem engineering in palm stands by

white-lipped peccaries (Tayassu pecari) and other

frugivores in an isolated Atlantic Forest fragment.

Biodiversity and Conservation, 18(7), 1733-1750.

Kimura, K., Yumoto, T., & Kikuzawa, K. (2001). Fruit-

ing phenology of fleshy-fruited plants and seasonal

dynamics of frugivorous birds in four vegetation

zones on Mt. Kinabalu, Borneo. Journal of Tropical

Ecology, 17(6), 833-858.

Kovach, W.L. (1994). Program: Oriana for Windows (Ver-

sion 4.02). Retrieved from https://www.kovcomp.

co.uk/oriana

Laps, R.R. (1996). Frugivoria e dispersão de sementes de

palmiteira (Euterpe edulis, Martius, Arecaceae) na

Mata Atlantica, sul do Estado de São Paulo (Mas-

ter’s thesis). Universidade Estadual de Campinas,

Instituto de Biologia, Campinas, São Paulo, Brazil.

Retrieved from http://www.repositorio.unicamp.br/

handle/REPOSIP/316282

Levey, D.J. (1988). Spatial and temporal variation in Costa

Rican fruit and fruit-eating bird abundance. Ecologi-

cal Monographs, 58(4), 251-26.

Loiselle, B.A., & Blake, J.G. (1991). Temporal variation in

birds and fruits along an elevational gradient in Costa

Rica. Ecology, 72(1), 180-193.

Malizia, L. (2001). Seasonal fluctuations of birds, fruits,

and flowers in a subtropical forest of Argentina. The

Condor, 103(1), 45-61.

Martínez, B., Sanín, M.J., Castillo, L.S., López, R., &

Bernal, R. (2018). Sex change in the dioecious palm

Ceroxylon quindiuense (Arecaceae). Ecology, 99(6),

1501-1503.

Morellato, L.P., Talora, D.C., Takahasi, A., Bencke, C.,

Romera, E., & Ziparro, V. (2000). Phenology of

Atlantic rain forest trees: a comparative study. Bio-

tropica, 32(4b), 811-823.

Peres, C. (1994). Composition, density, and fruiting phe-

nology of arborescent palms in an Amazonian terra

firme forest. Biotropica, 26(3), 285-294.

Ramírez, J.J., Roldán, P.G., & Yépez, G.A. (2004). Altitu-

dinal Variation of the Numerical Structure and Bio-

diversity of the Taxocenosis of Ephemeroptera in the

South, North, and Central Regions of the Department

of Antioquia, Colombia. Acta Limnologica Brasilien-

sia, 16(4), 329-339.

Salm, R., Jalles-Filho, E., & Schuck-Paim, C. (2005). A

model for the importance of large arborescent palms

in the dynamics of seasonally-dry Amazonian forests.

Biota Neotropica, 5(2), 151-156.

Sanín, M.J. (2013). Estudios ecológicos y Evolutivos

en Ceroxylon (Palmae: Ceroxyloideae) (Doctoral

dissertation). Universidad Nacional de Colombia,

Bogotá, Colombia. Retrieved from https://docplayer.

es/47608857-Estudios-ecologicos-y-evolutivos-en-

ceroxylon-palmae-ceroxyloideae.html

Sanín, M.J., & Galeano, G. (2011). A revision of the

Andean wax palms, Ceroxylon (Arecaceae). Phyto-

taxa, 34(1), 1-64.

Sanín, M.J., Anthelme, F., Pintaud, J.C., Galeano, G.,

& Bernal, R. (2013). Juvenile resilience and adult

longevity explain residual populations of the Andean

664

Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(2): 649-664, April-June 2021 (Published Jun. 09, 2021)

Wax Palm Ceroxylon quindiuense after deforestation.

PLoS One, 8(10), e74139.

Sayer, E.J., Rodtassana, C., Sheldrake, M., Bréchet, L.M.,

Ashford, O.S., Lopez-Sangil, L., ... Tanner, E.V.J.

(2020). Revisiting nutrient cycling by litterfall -

Insights from 15 years of litter manipulation in

old-growth lowland tropical forest. Advances in Eco-

logical Research, 62, 173-223.

Scariot, A. (1999). Forest fragmentation effects on palm

diversity in Central Amazonia. Journal of Ecology,

87(1), 66-76.

Tomlinson, P.B. (1963). Measuring growth rates in palms.

Principes, 7(1), 40-44.

Vitousek, P.M. (1984). Litterfall, nutrient cycling, and

nutrient limitation in tropical forest. Ecology, 65(1),

285-298.

Wallis, C.I.B., Homeier, J., Peña, J., Brandl, R., Farwig,

N., & Bendix, J. (2019). Modeling tropical montane

forest biomass, productivity and canopy traits with

multispectral remote sensing data. Remote Sensing of

Environment, 225(1), 77-92.

Young, H.S., Raab, T.K., McCauley, D.J., Briggs, A.A., &

Dirso, R. (2010). The coconut palm, Cocos nucifera,

impacts forest composition and soil characteristics at

Palmyra Atoll, Central Pacific. Journal of Vegetation

Science, 21(6), 1058-1068.

Zar, J.H. (1999). Biostatistical Analysis. New Jersey, USA:

Prentice-Hall.

Zona, S., & Henderson, A. (1989). A review of animal-

mediated seed dispersal of palms. Selbyana, 11, 6-21.