Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51599, enero-diciembre 2023 (Publicado Jun. 28, 2023)

Dispersion of seeds at night and day in sub-Andean forests,

Cueva Los Guacharos Park, Colombia

Sebastián Bautista Plazas1*; https://orcid.org/0000-0003-2739-038X

Pablo Roberto Stevenson Diaz1; https://orcid.org/0000-0003-2394-447X

1. Laboratorio Ecología de Bosques Tropicales y Primatología, Universidad de los Andes, Carrera 1 No 18A 12, Bogotá

111711, Colombia; sebastianbautista386@gmail.com (*Correspondencia), pstevens@uniandes.edu.co

Received 30-VI-2022. Corrected 21-IV-2023. Accepted 23-VI-2023.

ABSTRACT

Introduction: Much has been argued about the importance of the role that different types of frugivores play as

seed dispersers in plant communities, but few studies have been actually carried out.

Objective: We evaluated and compared diurnal and nocturnal seed dispersal in primary and secondary sub-

Andean forests in Southern Colombia.

Methods: We estimated number and biomass (kg/ha) of seeds dispersed over one year (2017) using 60 fruit traps

that were checked before sunrise and before sunset for 10 continuous days every two months.

Results: We found that from 1 874 dispersed seeds, 55.8 % (10.9 kg/ha) were collected during the day and 44.2

% (6.39 kg/ha) at night. There were no significant differences between diurnal and nocturnal seed dispersal in

number of seeds or biomass. We also found no difference in seed dispersal between primary and secondary forest

over time. Within diurnal organisms, primates and fruit-eating birds appear to be primarily responsible for this

ecosystem service during the day; while bats, birds (e.g. oilbirds), and probably primates did so during the night.

Conclusions: Diurnal and nocturnal dispersal seem to be equal in terms of number and weight of seeds, but not

in the similarity of dispersed plant species. It remains a challenge to recognize the relative importance of differ-

ent fruit-eating organisms as seed dispersers using fruit trap methods.

Key words: seed dispersal; hanging seed traps; day and night frugivores; phenology; Andean forest.

RESUMEN

Dispersión de semillas nocturna y diurna en un bosque sub-Andino,

Parque Cueva Los Guacharos, Colombia

Introducción: Mucho se ha discutido sobre la importancia del papel que juegan diferentes tipos de frugívoros

como dispersores de semillas en las comunidades vegetales, pero en realidad se han realizado pocos estudios.

Objetivo: Evaluamos y comparamos la dispersión diurna y nocturna de semillas en bosques subandinos prima-

rios y secundarios en el sur de Colombia.

Métodos: Estimamos el número y la biomasa (kg/ha) de semillas dispersadas durante un año (2017) utilizando

60 trampas de frutos que se revisaron antes del amanecer y antes del atardecer durante 10 días continuos cada

dos meses.

Resultados: Se encontró que, de 1 874 semillas dispersas, el 55.8 % (10.9 kg/ha) se recolectaron durante el día

y el 44.2 % (6.39 kg/ha) durante la noche. No hubo diferencias significativas entre la dispersión de semillas

diurna y nocturna en número de semillas o biomasa. Tampoco encontramos diferencias entre la dispersión de

semillas en el bosque primario y el bosque secundario a lo largo del tiempo. Dentro de los organismos diurnos,

los primates y las aves frugívoras parecen ser los principales responsables de este servicio ecosistémico durante

https://doi.org/10.15517/rev.biol.trop..v71i1.51599

CONSERVACIÓN

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51599, enero-diciembre 2023 (Publicado Jun. 28, 2023)

INTRODUCTION

Seed dispersal is one of the most important

interactions in tropical forests (Howe & Small-

wood, 1982; Willson & Traveset, 2000). It is

fundamental for the subsistence of plant com-

munities over time (Cain et al., 2000; Chaz-

don, 2003; Stevenson, 2011), since frugivores

can modify demographic processes, population

dynamics, potential recruitment area, and den-

sity-dependent processes (Connell et al., 1984;

Janzen, 1971; Nathan & Muller-Landau, 2000;

Willson, 1993). Several organisms perform

seed dispersal services in different ecosystems,

where birds and mammals have been suggested

as the main ones dispersing seeds of many

tropical plant species (Howe, 1990).

Bats have been considered the main noc-

turnal seed dispersers (Fleming & Heithaus,

1981; Mello et al., 2011). Different studies

have cataloged bats as efficient seed dispersers

from a quantitative point of view, finding that

they move a high number of seeds by consum-

ing large amounts of fruit, even more than birds

(Brosset et al., 1996; Duncan & Chapman,

1999; Medellin & Gaona, 1999). Bats are also

effective seed dispersers, with high germina-

tion percentages after seeds pass through-

out their digestive system (Fleming, 1988;

Vasquez-Yanes & Orozco-Segovia, 1986).

Some authors highlight bats as important

seed dispersers because when defecating in

flight they are more likely to deposit seeds

in forest clearings and open areas than birds

and primates, playing a very important role

in forest regeneration (Korine & Kalko, 2005;

Thies & Kalko, 2004; Thomas et al., 1988).

For other nocturnal mammals such as opos-

sums (Didelphidae), raccoons and mountain

dogs (Procyonidae), and rodents (Rodentia)

efficient seed dispersal has also been observed

(Fleming & Williams, 1990; Howe, 1990;

Jansen et al. 2012).

In contrast, diurnal birds have been con-

sidered the main dispersers in a variety of

habitats (Howe, 1977; Wang & Smith, 2002;

Wenny et al., 2016). Birds have been described

as efficient seed dispersers due to their wide

home ranges, flight capacity, broad frugivo-

rous diet, and the likelihood of recruitment

(Herrera & Jordano, 1981; Levey et al., 2005;

Stiles, 1980). Due to the great morphologi-

cal, behavioural, and ecological diversity of

frugivorous birds, it has been found that they

are also important in the restoration of forests

and especially increasing the connectivity of

patches isolated as a consequence of forest

fragmentation, in addition to promoting plant

diversity (Carlo & Morales, 2016; Emer et al.,

2018). As a particular case in neotropical for-

ests is a nocturnal frugivorous bird known as

oilbird (Steatornis caripensis), which presents

a diverse diet of fruits and seeds, and a great

capacity to disperse a high number of seeds

(Stevenson et al., 2017).

On the other hand, in tropical zones, it has

been shown that diurnal primates play dispro-

portionate ecological roles as seed dispersers

(Link & Di Fiore, 2006). Because of their high

abundance and large size relative to other fru-

givores in many tropical forests (Bravo, 2012;

Campbell et al., 2016), their large biomass,

el día; mientras que los murciélagos, las aves (por ejemplo, los guácharos) y probablemente los primates lo

hicieron durante la noche.

Conclusiones: La dispersión diurna y nocturna parecen ser iguales en número y peso de semillas, pero no en

la similitud de especies de plantas dispersadas. Sigue siendo un desafío reconocer la importancia relativa de los

diferentes organismos frugívoros como dispersores de semillas utilizando métodos de trampa de frutos.

Palabras clave: dispersión de semillas; trampas colgantes de semillas; frugívoros diurnos y nocturnos; fenología;

bosque andino.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51599, enero-diciembre 2023 (Publicado Jun. 28, 2023)

and their ability to ingest large seeds, primates

are also considered efficient seed dispersers

(Chapman & Dunham, 2018; Stevenson et

al., 2005). Additionally, they disperse high

amounts of seeds over long distances, are effec-

tive seed dispersers, and their seed dispersal

pattern shows a high correlation with seedling

recruitment (Gelmi-Candusso et al., 2019; Ste-

venson et al., 2002; Zárate et al., 2019).

The purpose of this study is to compare

daytime and nighttime seed dispersal, as an

approximation to seed dispersal roles of diurnal

and nocturnal arboreal and flying frugivores in

a secondary and primary sub-Andean forest

of Colombia. We expect to find differences in

the amount, biomass and species of seeds dis-

persed between day and night.

MATERIALS AND METHODS

Study area: The study was conducted in

the Cueva de Los Guácharos National Natural

Park (PNNCG) located in the department of

Huila and the Southwestern part of the depart-

ment of Caquetá (Colombia). The predominant

habitat is a sub-Andean forest, both primary

and secondary, the latter being a forest with a

growth close to 40 years (Prada & Stevenson,

2016). The study area is on average at 2 000

m.a.s.l. with a mean temperature of 18.8 °C.

The annual precipitation is 2 284 mm and the

rainy season presents a bimodal pattern with

a first peak between March and June, and a

second peak between September and October.

Species richness of different organism groups

has been partially registered for PNNCG. Prada

and Stevenson (2016) report 458 species/mor-

phospecies of trees, about 200 bird species

(Stevenson et al., 2022), 10 species of medium

and large mammals (Gast & Stevenson, 2021),

11 species of small nonflying mammals (Bau-

tista-Plazas et al., 2017), 5 species of primates

(Vargas et al., 2014) and 25 species of bats

(Walteros-Vergara, 2018).

Seed dispersal: Hanging traps of 0.56 m²

were used to capture the dispersed seeds, the

porosity of the traps was < 1 mm to ensure

that small seed species were represented in the

study. The material was cloth and they were

tied to four nearby trees, following the recom-

mendations of Stevenson & Vargas (2008). A

total of 60 traps were arranged in four 1 km

long linear transects, two of these transects

were placed in the secondary forest and two in

the primary forest, each with 15 hanging traps.

The location of each trap within the transect

was determined by three random numbers: 1.

The space between adjacent traps (between 15

and 20 m), 2. The side of the trails (right or

left), and 3. The distance to the trails (between

1 and 10 m).

Traps of each transect were checked before

sunrise (5:00) and before sunset (17:00) for

10 continuous days every two months (Febru-

ary, April, June, August, October, December)

throughout 2017. Once the contents were col-

lected, the seeds were identified at the species

level when possible. This material was dried

in a portable oven at an average temperature

of 60 °C to achieve constant dry weight. Then,

we counted the number of dispersed seeds and

estimated the biomass of dispersed seeds (kg/

ha) (Stevenson, 2004). Seeds were classified as

dispersed when they were associated with dung

and all the adult trees, lianas, and shrubs within

a 10 m radius of each hanging trap were identi-

fied to discern whether the seeds deposited in

the trap were dispersed or came from nearby

parents (Stevenson, 2007). Besides, it was cor-

roborated that they were dispersed seeds since

there were no immature fruits, whole fruits, or

flowers of the same species in each trap.

Statistical analysis: A linear mixed model

was used to evaluate the fixed effects as time

(day/night) and forest type (primary/second-

ary), and month as a random effect (Febru-

ary, April, June, August, October, December),

on the logarithm of the number of dispersed

seeds and the logarithm of dispersed seeds

biomass (kg/ha). The linear mixed model was

carried out using “lme4” and “lmerTest” pack-

ages from software R 4.2.3 (R Core Team,

2023). We also estimated random effects for

each month and their interval estimate using

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51599, enero-diciembre 2023 (Publicado Jun. 28, 2023)

“merTools” package. We calculate similarity

between seed species dispersed in the day and

seeds dispersed in the night with the Jaccard

similarity index using “Vegan” package.

RESULTS

A total of 93 species of seeds were identi-

fied, 65 species were dispersed during the day

and 56 during the night. We found that around

half of the species dispersed in the day were not

shared with the species dispersed in the night

(Jaccard similarity index = 0.54). Twenty-eight

species were exclusively dispersed during the

night and 37 during the day.

The plant species with the highest seed

biomass dispersed during the day were Alcho-

rnea grandis, Tapirira guianensis subandina,

Chamaedorea linearis, Guettarda crispiflora,

and Rollinia dolichopetala. On the other hand,

the plant species with the highest seed biomass

dispersed at night were Tapirira g. subandina,

Sapium stylare, Hyeronima huilensis, Rollinia

dolichopetala and Anthurium multinervium.

The plant species with the highest number

of seeds dispersed during the day were Ficus

sp.1, Cecropia telenitida, Solanum sp.1, Morus

insignis, and Cecropia angustifolia. In contrast,

at night the highest number of dispersed seeds

were recorded for Ficus sp.1, Cecropia teleni-

tida, Anthurium multinervium, Solanum sp.1,

and Hieronyma andina.

We recorded a total of 1 874 effectively

dispersed seeds, of which 1 046 (55.8 %) were

collected during the day and 828 (44.2 %) at

night. The total dispersed seed biomass was

higher in the day with 10.96 kg/ha, while for

night it was 6.39 kg/ha; however, the variation

was large and no significant differences were

found (T = -1.25, P = 0.22, Fig. 1A). Similarly,

no significant differences were found between

Fig. 1. A. Biomass of seeds dispersed (kg/ha) day and night at secondary and primary forest in PNNCG. B. The number of

seeds dispersed day and night at secondary and primary forest in PNNCG.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51599, enero-diciembre 2023 (Publicado Jun. 28, 2023)

the number of seeds dispersed during the day

and night (T = 0.18, P = 0.85, Fig. 1B).

In the primary forest, a total of 995 seeds

were dispersed (551 during the day and 444 at

night) and 879 (495 during the day and 384 at

night) in the secondary forest, no significant

differences were found in the number of seeds

between forest types (T = 0.41, P = 0.68, Fig.

1B). Additionally, we did not observe a sig-

nificant difference between the primary and

secondary forests in the biomass of dispersed

seeds (T = 1.58, P = 0.13, Fig.1A), a total of

10.79 kg/ha of seeds was dispersed in the pri-

mary forest and 6.57 kg/ha in the secondary

forest. No significant differences were found

in the number or biomass (kg/ha) of seeds

dispersed between the months sampled. How-

ever, April and August recorded the highest

number and biomass of dispersed seeds, while

in October and December the lowest seed dis-

persion (Fig. 2).

DISCUSSION

Both, birds and bats, have been widely

regarded as the main seed dispersers of day and

night seeds respectively, in terms of the num-

ber of seeds transported (Fleming & Heiathus,

1981; Janson, 1983; Levey et al., 2002; Mello

et al., 2015; Wenny & Levey, 1998). In this

study, we did not observe marked differences

in the number of seeds dispersed during the

day and night, nor in the number of plant spe-

cies dispersed in these two periods. Our results

agree with what was found for trees isolated

within grasslands by Galindo-González et al.

(2000), however, for other tropical forests, a

greater dispersion of seeds by one of the two

Fig. 2. A. Biomass of seeds dispersed (kg/ha) through the year at PNNCG. B. The number of seeds dispersed through the

year at PNNCG.

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51599, enero-diciembre 2023 (Publicado Jun. 28, 2023)

large groups (birds or bats) has been reported

(Gonzales et al., 2009; Ingle, 2003; Jacomassa

& Pizo, 2010;).

We did not find a greater nocturnal seed

dispersal for any of the studied forests (pri-

mary and secondary), although we observed

a slightly higher seed biomass at night in

secondary forests than in primary forests. This

contrasts with what was found by other authors

where bats are more important in successional

forest states where they disperse significantly

more seeds and are important for the natural

regeneration of ecosystems (Duncan & Chap-

man, 1999; Medellin & Gaona, 1999). This can

be explained by the fact that secondary forests

in the study area are relatively old (ca. 40 years

in recovery).

Similarly, it has been suggested that birds

have greater importance in terms of seed dis-

persal within mature forests than in disturbed

forest in recovery and with fragmentation

(Ingle, 2003; Whittaker & Jones, 1994). How-

ever other studies support that seed dispersal by

birds is crucial in forest regeneration for dis-

turbed habitats (Carlo & Morales, 2016; Saave-

dra et al., 2014). In our case, although there are

no notable differences in diurnal seed dispersal

between primary and secondary forests, our

results show a greater value in both the number

of seeds and the biomass of seeds dispersed by

diurnal animals for the secondary forest.

For our study forest, there was high vari-

ability in the dispersion of seeds at day and

night, being slightly higher during the day both

in biomass and number of dispersed seeds. The

slightly higher biomass and seed count during

the day is expected since not only bird drop-

pings but also primate droppings were found in

seed traps collected at day-time In the PNNCG

study site, it has been reported that the most

abundant primates in the area are the woolly

monkeys (Lagothrix lagothricha) who disperse

a large number of seeds, with an average of

11 000 seeds km² day-¹ (Ramírez et al., 2014).

This explains the high dispersion of large seeds

such as Tapirira g. subandina, Sapium stylare,

and Rollinia dolichopetala which are known to

be heavily consumed and dispersed by woolly

monkeys (Ramírez et al., 2014). Additionally,

in the area there are other species of primates

such as Sapajus apella, Alouatta seniculus and

Saimiri sciurus, which could also disperse large

seeds (Chapman, 1995), but occur at very low

density (Vargas et al., 2014).

Within the seeds dispersed at night, we

found a high number of seeds from Tapirira g.

subandina which is the most important plant

for the population of woolly monkeys and has

not been reported in the diet of bats. Therefore,

we believe that this species and other plants

preferred by monkeys (e.g. Rollinia dolichope-

tela) are dispersed during nighttime by pri-

mates in their sleeping trees. These nocturnal

depositions by primates are important and

should be considered for nocturnal dispersal

as they can comprise up to 19 % of the total

seeds dispersed during the day by primates

(Stevenson, 2007). We cannot rule out that

these seeds were dispersed by other nocturnal

organisms such as nocturnal monkeys (Aotus

sp), Potos flavus, or marsupials, but presum-

ably, the effect of the wooly monkeys could

be greater, given their high abundance (ca. 20

individuals/km2) (Vargas et al. 2014). It is also

important to bear in mind that the study area

has a large oilbird colony (Steatornis carip-

ensis). This species could also be responsible

for nocturnal seed dispersal of species such as

Chamaedorea linearis, Hedyosmum cuatreca-

zannum and Nectandra sp. which are part of

the diet of this nocturnal bird (Stevenson et al.,

2017). Nevertheless, nocturnal seeds dispersal

from species such as Tapirira g. subandina,

Rollinia dolichopetala and Hieronyma huilen-

sis, probably come from diurnal frugivores,

because of their size and not being registered

in the oilbird’s diet.

Our observations indicated that the trends

in both the number and amount of biomass of

seeds dispersed at night and daytime generally

kept the same trend overtime with April being

the month of greatest dispersal and October

the one with the least dispersal. Seed dispersal

at this location seems to be affected mainly

by changes in fruit production throughout

the year. In fact, the months with higher fruit

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51599, enero-diciembre 2023 (Publicado Jun. 28, 2023)

production also showed a peak in the number of

dispersed seeds (Bautista, unpublished). Addi-

tionally, when there is greater production of

fruits, more visits of fruit eaters are expected.

So, it seems that it could be important in future

studies to evaluate productivity as predictor

of the amount of seed dispersion, as has been

observed in other studies (Albrecht et al. 2012;

Hampe, 2008).

Knowing the dispersion of seeds in for-

ests with different degrees of disturbance is of

vital importance to understand the processes

of natural regeneration (Gorchov et al., 1993;

Uriarte & Chazdon, 2016). It is also essential to

estimate the contribution of different organisms

to the seed rain of particular species within

the plant community (Howe, 1990). From the

results found in this study, we can say that for

the primary and the old secondary sub-Andean

forests of the PNNCG, share many frugivores

such as primates and birds (Vargas et al., 2014),

which may explain the lack of differences in

diurnal and nocturnal dispersal.

Our main conclusion was diurnal and

nocturnal dispersal but that is not saying much

about seed dispersal by birds and primates vs.

bats, and that in natural tropical forests the

role of primates and nocturnal birds might be

substantial, where they reach high densities and

are not subject to hunting (Howe, 1990; Ste-

venson, 2011; Stevenson et al., 2017; Wright

et al., 2000). For this reason, it is imperative

to generate conservation strategies to protect

the different species of seed-dispersing organ-

isms, since the persistence of multiple species

and ecosystems depends on them (Chazdon &

Guariguata, 2016; Kozlowski, 2002). By pre-

serving these organisms, damages to the plant

community such as deforestation, fragmenta-

tion, and loss of species can be ameliorated

and remedied (Bacles et al., 2006; Cramer et

al., 2007; McConkey et al., 2012; Ozinga et al.,

2009), because frugivores help in the processes

of regeneration and restoration of degraded

forests (Parrotta et al., 1997).

Ethical statement: the authors declare

that they all agree with this publication and

made significant contributions; that there is no

conflict 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 acknowledgments

section. A signed document has been filed in

the journal archives.

ACKNOWLEDGMENTS

To the PNNCG staff for their collaboration

and hospitality. We thank Alejandro Nassar,

Juliana Penagos and Carolina Garcia for their

contribution taking data on dispersed seeds.

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