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Vertical stratification of seed-dispersing vertebrate communities and their

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Biol. Rev. (2020), pp. 000–000. 1
doi: 10.1111/brv.12664

Vertical stratification of seed-dispersing

vertebrate communities and their interactions
with plants in tropical forests
Sarina Thiel1* , Marco Tschapka2,3 , Eckhard W. Heymann4† and Katrin Heer1†
1
Department of Conservation Biology, Philipps University Marburg, Karl-von-Frisch-Strasse 8, Marburg, Germany
2
Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Albert Einstein Allee 11, Ulm, Germany
3
Smithsonian Tropical Research Institute, Apartado, 0843–03092, Balboa, Ancon, Republic of Panama
4
Verhaltensökologie & Soziobiologie, Deutsches Primatenzentrum - Leibniz-Institut für Primatenforschung, Kellnerweg 4, Göttingen, Germany

ABSTRACT

Vertical stratification (VS) is a widespread phenomenon in plant and animal communities in forests and a key factor for
structuring their species richness and biodiversity, particularly in tropical forests. The organisms composing forest com-
munities adjust and shape the complex three-dimensional structure of their environment and inhabit a large variety of
niches along the vertical gradient of the forest. Even though the degree of VS varies among different vertebrate groups,
patterns of compositional stratification can be observed across taxa. Communities of birds, bats, primates, and non-flying
small mammals are vertically stratified in terms of abundance, species richness, diversity, and community composition.
Frugivorous members of these taxa play important roles as seed dispersers and forage on fruit resources that, in turn, vary
in quantity and nutritional value along the vertical gradient. As a consequence, plant–seed disperser interaction networks
differ among strata, which is manifested in differences in interaction frequencies and the degree of mutual specialization.
In general, the canopy stratum is composed of strong links and generalized associations, while the lower strata comprise
weaker links and more specialized interactions. Investigating the VS of communities can provide us with a better under-
standing of species habitat restrictions, resource use, spatial movement, and species interactions. Especially in the face of
global change, this knowledge will be important as these characteristics can imply different responses of species and taxa
at a fine spatial scale.

Key words: stratum, plant–animal interactions, seed dispersal, frugivory, birds, bats, primates, non-flying small mammals,
fruits, tropical forests

CONTENTS

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
(1) VS as a guiding principle in ecology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
(2) VS of tropical forests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
(3) Importance of vertebrate seed dispersers in tropical forests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
(4) The threat of global change . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
(5) Challenges to be resolved . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
II. Methods: literature research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
III. Species diversity and distribution across forest strata . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
(1) Bat communities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
(2) Bird communities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
(3) Non-flying small mammal communities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5

* Address for correspondence (Tel: +49 6421 2823479; E-mail: sarina.thiel@googlemail.com)

†
Authors contributed equally to this work.

Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
2 Sarina Thiel and others

(4) Primate communities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6

IV. Vs of fruit quantity and quality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
V. Vs of interactions between plants and seed dispersers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
VI. Discussion and outlook . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
(1) Patterns of VS across taxa and tropical regions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
(2) VS and trait evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
(3) Effects of global change on vertically stratified forests and seed-disperser communities . . . . . . . . . . . . . 8
(a) Local anthropogenic effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
(b) Global effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
(c) Impacts on plant–animal interaction networks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
(4) High variability of data quality among taxa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
(5) Outlook . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
VII. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
VIII. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
IX. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
X. Supporting information . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16

“One of the outstanding general principles of commu-
nity organization is that of stratification. Nearly all
communities share a well-defined lamination into a
column of strata upon a vertical organismal gradient”
(Allee et al., 1949, p. 442).
I. INTRODUCTION
(1) VS as a guiding principle in ecology
The vertical organization of structures, microclimate, and
biota in ecosystems has been a recurring topic in scientific
research and ecosystem description since the 1950s (Allee
et al., 1949; Richards, 1952; Geiger, 1965; Smith, 1973;
Bongers, 2001) and the concept of vertical stratification
(VS) is one aspect of this (Richards et al., 1996). In science,
the general term ‘stratification’ is used to describe distinct,
but closely related and interconnected phenomena. VS can
refer to the vertical layering of microclimate, leaf mass, food
resources, or animal communities. Allee et al. (1949) per-
ceived VS as a general phenomenon of plant and animal
communities in terrestrial (forests, deserts, grasslands) and
aquatic (oceans, intertidal zones, lakes) environments. For
example, fresh- and saltwater environments exhibit gradients
of water pressure, temperature, light intensity, wavelength
absorption, and other abiotic factors (Allee et al., 1949).
Grassland can be divided into subterranean, floor, and her-
baceous layers. Forest communities mostly have six vertical
strata: soil, forest floor, herbaceous, shrub, tree, and emer-
gent layers. Organisms composing these communities adjust
to the vertically stratified environment (Allee et al., 1949).
Whereas for aquatic environments and grasslands many
early studies described the VS of abiotic and biotic factors
(Shelford & Gail, 1922; Woltereck, 1932; Henrici, 1939;
ZoBell, 1946), knowledge about forest stratification was for
many years more or less restricted to the lower layers (Allee
et al., 1949). During the last 30 years, improved access to
the forest canopy has changed our understanding of key eco-
system processes substantially (Ozanne et al., 2003).
The vertical pattern of microenvironmental conditions such
as temperature, light, humidity, and wind on the forest is
determined by its plant species composition and three-
dimensional structure (Geiger, 1965; Parker, 1995). Vertical
climatic gradients within forests are more pronounced than
those defined by latitude and elevation. Climate may vary by
as much as 4 C and 10% humidity along a 20–30 m vertical
forest gradient, which is equivalent to over 400 m in altitude
and hundreds of kilometres in latitude (Scheffers et al., 2013).
In general, circadian climatic variations of the upper canopy
are much stronger than those in the lower layers. For instance,
the canopy temperature of a tropical lowland rainforest in
Costa Rica ranges during the day from 20.5 C to 27 C, com-
pared to 22 C to 25 C in the understorey (Fetcher, Ober-
bauer, & Strain, 1985). Also, the vapour pressure deficit in
the understorey is stable at around 0.2 kPa, but ranges from
0.3 to 0.9 kPa in the canopy (Fetcher et al., 1985). Forest type
and structure influence microclimatic profiles, light quality,
and light quantity (Shaw, 2004). Evergreen forests, for exam-
ple, allow less light through the canopy than deciduous hard-
woods, affecting forest floor biota and lower-canopy
environments (Kato & Yamamoto, 2002). In submontane
evergreen forests and tropical dry forests, foliage shows the
highest density in the canopy and the understorey, with more
open spaces in the midstorey (Terborgh & Weske, 1969;
Pearson, 1971; Terborgh, 1980). Vertically organized plant
structures comprise leaves, reproductive parts, trunks,
branches, butts, roots, and deadwood (Shaw, 2004). For
instance, in different types of temperate and tropical forests,
flowers and fruits show higher abundance in the canopy,
whereas tree trunks and dead leaves dominate under- and
midstorey levels (Terborgh, 1980; Marra & Remsen, 1997).
(2) VS of tropical forests
Due to their diversity and structural complexity, tropical for-
ests are of particular interest for the study of VS of ecological
communities. Their canopies can reach heights of >50 m,
spanning from the lowest herbs to the emergent layers

Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.
Stratification in tropical forest frugivores
(Richards, 1952). Their complex three-dimensional structure
and the diversity of microenvironments along the vertical
gradient provide ample opportunities for niche diversifica-
tion (Ozanne et al., 2003). Thus, VS has been considered a
pivotal factor shaping the species richness and diversity of
tropical forests (Condit et al., 2002; Wright, 2002; Ozanne
et al., 2003; Pennington & Dick, 2010; Sedio, Wright, &
Dick, 2012). Furthermore, their canopies are considered to
be hotspots of biological diversity (Ozanne et al., 2003; Naka-
mura et al., 2017).
(3) Importance of vertebrate seed dispersers in
tropical forests
The vertical pattern of microenvironmental conditions within
forests is crucial as it affects the distribution of forest biota,
the behaviour of vertebrates, and numerous other aspects of
ecosystem functioning (Shaw, 2004). For instance, many stud-
ies have observed VS for birds, bats, primates, and small non-
flying mammals in terms of community composition, species
diversity, richness, and abundance (e.g. Buchanan-Smith
et al., 2000; Kalko & Handley, 2001; Cunha & Vieira, 2002;
Vieira & Monteiro-Filho, 2003; Buzzard, 2006; Chmel et al.,
2016; Gregorin et al., 2017; Dinanti, Winarni, & Supriatna,
2018). In tropical rainforests, these vertebrates are among the
most important seed dispersers (Fleming, 1993; Fleming &
Kress, 2013). Up to 90% of tropical rainforest plant species
produce fleshy fruits that are consumed and their seeds dis-
persed by birds, bats, primates, and non-flying small mammals
(Howe & Smallwood, 1982; Lobova, Geiselman, & Mori,
2009). Sekercioglu (2006) suggested that birds disperse the
seeds of more than 70% of the woody plants bearing fleshy
fruits. Furthermore, seed dispersal by primates has been associ-
ated with the maintenance of tropical rainforest diversity
(Link & Di Fiore, 2006). Lastly, frugivorous bats are the most
important seed dispersers in highly disrupted forests, as frag-
ments are better reached by bats than by birds and primates,
due to the lack of appropriate perching and nesting sites
(Medellin & Gaona, 1999; Melo et al., 2009; Muscarella &
Fleming, 2007, but see Farwig, Böhning-Gaese, & Bleher,
2006). Rainforest plants may profit substantially from seed-
dispersing vertebrates, as these move over longer distances
and thus maintain gene flow among populations on larger spa-
tial scales, enable escape from high mortality near mother
plants, and allow the colonization of new sites (Nathan &
Muller-Landau, 2000). Hence, seed dispersal is vital for main-
taining plant biodiversity and thus is the foundation for survival
and sustainability (Cordeiro & Howe, 2003; Sekercioglu,
2006). Since plant and vertebrate communities show VS, it is
plausible to assume differences among strata in the patterning
of plant–animal interactions such as seed dispersal.
(4) The threat of global change
Tropical forests are under immense pressure due to anthro-
pogenic factors such as forest degradation, land-use changes,
and climate change (Lewis, 2006). These factors alter forest
Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.
3
structure and constitute serious threats to the biological
diversity of the tropics. Understanding their consequences
for the persistence of native populations and communities
remains a daunting challenge (Dobson, 2005). To date, stud-
ies have revealed that susceptibility to changing conditions
varies among focal taxa and functional species groups
(Medellin & Gaona, 1999; Lewis, 2006; Philpott et al.,
2008; Ranganathan et al., 2008; Kirika et al., 2008a; Kirika,
Farwig, & Böhning-Gaese, 2008b; Grass, Berens, & Farwig,
2014). It is highly probable that these changes will also affect
the vertical distribution of communities. Thus, it is evident
that we need a better resolved understanding of species char-
acteristics and interactions to be able to understand how ver-
tically stratified tropical forests and their affiliated species and
ecosystem functions will perform under global change.
(5) Challenges to be resolved
VS of tropical forest biota has both ecological and evolution-
ary consequences for biodiversity and ecosystem functioning.
Investigating VS of single taxa but also of essential species
interactions such as seed dispersal should be a focal point of
research to understand the underlying abiotic and biotic fac-
tors structuring diversity at a finer scale. It can provide a
more detailed picture of vertical patterns exhibited by forest
biota and the effects on species habitat preferences, resource
use, spatial movement, and species interactions.
Herein, we review current knowledge about VS of species
communities and resources, with particular emphasis on
vertebrate taxa acting as seed dispersers in tropical forests.
Further, we summarize existing literature on the VS of
plant–seed disperser interactions and species networks and
discuss its evolutionary and ecological implications. We con-
clude with a consideration of the implications of global cli-
mate change and outline directions for future research.
II. METHODS: LITERATURE RESEARCH
Our literature search was based on Google Scholar (https://
scholar.google.de/) and Web of Science (https://apps.
webofknowledge.com/) using all available years and a com-
bination of the following key words: “vertical stratification”
OR “forest strata” AND “tropics” OR “rainforest” AND
“birds” OR “bats” OR “primates” OR “mammals” OR
“fruits” OR “plant–animal interactions” OR “frugivory”
OR “seed dispersal”. The online database search was last
performed in September 2020 on titles, abstracts, and key
words in both databases. From the list of studies obtained,
we used their titles to identify relevant studies and scanned
their abstracts for information on VS. In order to be included
in this review, the study had to be conducted in one of the
main tropical forest types (following the definition of
Thomas & Baltzer, 2002) and provide information on VS
or canopy communities of seed-dispersing birds, bats, pri-
mates, or other small non-flying mammals, VS of fruit crops,
4 Sarina Thiel and others
or VS of plant–seed disperser interactions with animals
belonging to the groups mentioned above in the tropics.
For all relevant studies, we consulted the main text and
extracted information regarding taxon, diet (only frugivores
and omnivores were included), geographic region, height
division of strata, the VS parameters examined, morphology
of plant and animal traits, and possible drivers and benefits of
VS. We use the terms ‘stratification’, ‘lower/middle/higher
strata’, or respectively ‘understorey’, ‘midstorey’, and ‘can-
opy’ accordingly to the respective paper. However, as the
usage of these terms is often very vague and differs among
studies (for a more detailed analysis, see Parker &
Brown, 2000), we only included studies that used ‘stratifica-
tion’ as a synonym for height and that specified height divi-
sion of strata. Studies consistently divided the forest into
2–4 strata (see online Supporting Information, Table S1)
and even though emergent trees could be considered as an
additional stratum, most studies either assigned them to the
canopy stratum or did not include them in their observations.
We also searched the references and citation records of the
included studies for other studies that could provide
additional data.
We found 15 papers published between 1994 and 2020
targeting bats, 15 papers published between 1969 and 2018
targeting birds, 16 papers published between 1977 and
2019 targeting non-flying small mammals, 31 papers pub-
lished between 1972 and 2010 targeting primates (Table S1),
three papers published between 2002 and 2014 targeting
plants, and four papers published between 2001 and 2018 tar-
geting plant–animal networks (Table S2). Even though we
may not have found all studies targeting our question, and
given that the file drawer problem (studies with significant
results are published more often than those finding no signifi-
cant patterns; Arnqvist & Wooster, 1995) may be relevant to
our study, our search criteria were intended to be exhaustive.
We did not include any unpublished results.
III. SPECIES DIVERSITY AND DISTRIBUTION
ACROSS FOREST STRATA
(1) Bat communities
Bat communities in forests of the Paleo- and Neotropics show
similar patterns of VS (Table S1). Species are heteroge-
neously distributed between the canopy and the understorey
with the canopy being intensively used (Francis, 1994; Sam-
paio et al., 2003; Rex et al., 2008; Gregorin et al., 2017).
Whereas numbers of individuals are generally higher in the
understorey, species richness and diversity are higher in the
canopy with distinct differences in community composition
(Bernard, 2001; Kalko & Handley, 2001; Silva et al., 2020).
Most of these differences in habitat use can be explained by
differences in echolocation and wing morphology, which
are intimately linked to foraging behaviour and diet, as well
as roost-site preferences (Kalko, Handley, & Handley, 1996;
Hodgkison et al., 2004; Olaya-Rodríguez, Pérez-Torres, &
Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.
Londoño-Murcia, 2019). In bats, echolocation is an important
sensory system that determines profoundly the interaction of
animals with the surrounding habitat structure (Denzinger,
Tschapka, & Schnitzler, 2018).
The echolocation and wing morphology of bat species
with short, high-frequency signals and short, broad wings
(Fig. 1) are adapted to foraging in the dense understorey of
tropical forests (Duya, Fidelino, & Ong, 2017; Denzinger
et al., 2018). For example, many well-sampled species of the
Neotropical genera Carollia and Sturnira (Kalko & Handley,
2001; Delaval, Henry, & Charles-Dominique, 2005; Pereira,
Marques, & Palmeirim, 2010) or the African genus Epomops
(Henry et al., 2004) are solely found in the understorey. They
mostly feed on fruit produced by shrubs and treelets of the
families Clusiacae, Piperaceae, and Solanaceae and use day
roosts near the ground (Fleming & Heithaus, 1986). Frugi-
vores with short, high-frequency signals, but long and narrow
wings (Fig. 1) are better adapted to hunt in the less-cluttered
canopy (Denzinger et al., 2018; Olaya-Rodríguez et al., 2019).
For example, phyllostomid bats of the Neotropical subfamily
Stenodermatinae [e.g. Chiroderma, Uroderma, Platyrrhinus (Vam-
pyrops)] and some species of the African and Asian subfamily
Pteropodinae (e.g. Micropteropus, Desmalopex, Eonycteris) pri-
marily forage in the canopy (Lim & Engstrom, 2001; Henry
et al., 2004; Carvalho, Fabián, & Menegheti, 2013; Duya
et al., 2017). Here, they feed on figs and other Moraceae
and utilize day roosts in the sub-canopy (Bernard, 2001;
Kalko & Handley, 2001; Henry et al., 2004).
(2) Bird communities
With improved access to the canopy of tropical forests and
the development of new techniques such as the use of canopy
cranes or ground-to-canopy mist nets (Walther, 2002b, 2003;
Naka, 2004; Chmel et al., 2016; Klimento & Richards, 2018),
researchers have obtained detailed data on the VS of bird
guilds and a fuller picture of bird diversity. Overall abun-
dance (Orians, 1969; Pearson, 1971; Bell, 1982; Dinanti
et al., 2018), species diversity (Jayson & Mathew, 2003; Chmel
et al., 2016), and community composition (Terborgh, 1980;
Walther, 2002a) clearly differ among the strata of tropical for-
ests (Table S1).
The vast majority of studies showed a VS of trophic bird
guilds with an increasing abundance and diversity of frugivo-
rous and omnivorous birds towards the canopy (Greenberg,
1981b; Firth, 1984; Shanahan & Compton, 2001; Naka,
2004; Dinanti et al., 2018). Body mass and wing size appear to
be structuring factors as they can to some extent constrain the
use of vertical strata (Fig. 1). Canopy-feeding seed dispersers
are mainly large-bodied species like toucans, trogons, hornbills,
fruit pigeons, or birds of paradise, for which moving in the dense
vegetation of lower forest strata and resting on the mostly thin
branches there is difficult (Bell, 1982; Fleming & Kress, 2013).
The seed dispersers feeding in the understorey of tropical forests
are primarily smaller species such as manakins, bulbuls, and
flowerpeckers (Karr, 1976; Fleming, 1988; Chmel et al., 2016).
Stratification in tropical forest frugivores 5

Fig 1. Schematic representation of a vertically stratified tropical forest and its inhabitants. Even though the degree of vertical
stratification (VS) differs among different seed-dispersing vertebrate groups, all reviewed studies reported significant patterns of
compositional stratification across taxa. The bar plots indicate the number of studies that found significant patterns of VS for bats,
birds, non-flying small mammals, and primates in Africa (black), Asia (dark grey), Australia (grey), and the Neotropics (light grey).

Foliage density in combination with the availability of food
resources seems to be an important driver of the vertical distri-
bution of bird communities. There seems to be a link between
foliage density and bird diversity and abundance in tropical
forests all over the world (MacArthur, 1964; Pearson, 1971;
Bell, 1982; Jayson & Mathew, 2003). Species from strata with
lower vegetation density have larger vertical foraging niches
than species foraging in strata with dense vegetation
(Walther, 2002a). Frugivorous birds are far less abundant in
the understorey, where vegetation density is high, whereas
the high fruit availability in the canopy leads to increased
abundance and diversity of frugivorous and omnivorous birds
(Terborgh, 1980; Bell, 1982; Chmel et al., 2016). Nevertheless,
available food density for entire avian communities is difficult
to assess accurately, as diet composition is still unknown for
many tropical bird species (Hutto, 1990; Chmel et al., 2016).
(3) Non-flying small mammal communities
VS of rodents and marsupials is extremely common in tropical
rainforests (Table S1; Stallings, 1989; McClearn et al., 1994;
Voss, Lunde, & Simmons, 2001; Helder, Macedo, & Cruz
Loss, 2019). Community composition and abundance differ
among strata (Charles-Dominique et al., 1981; Voss &
Emmons, 1996; Grelle, 2003). The majority of species seem
to use only one stratum, whereas others move across the
vertical gradient (Adam, 1977; Malcolm, 1991; Rader &
Krockenberger, 2006). Didelphid marsupials like Caluromys
philander and Gracilinanus agilis, for instance, generally constitute
the most common group in the canopy of Neotropical forests
(Vieira & Monteiro-Filho, 2003), whereas other species like
Marmosops incanus or Marmosa murina are typical understorey
foragers (Cunha & Vieira, 2002; Vieira & Monteiro-Filho,-
2003; De Faria Calazans & Bocchiglieri, 2019). Body size
and locomotor behaviour define the use of vertical space in
small mammal communities (Fig. 1). The ability of species to
deal with branches of variable diameters and inclination can
restrict their use of vertical strata (Cunha & Vieira, 2002).
Availability and access to food resources are important fac-
tors for the differential use of forest strata (Vieira & Monteiro-
Filho, 2003; Lambert, Malcolm, & Zimmermann, 2005;
Rader & Krockenberger, 2006). Species living in the canopy
have a higher proportion of fruits in their diet than species of
the understorey (Malcolm, 1991; Emmons, 1995; Cunha &
Vieira, 2002). By foraging on canopy resources, species may
reduce competition at ground level (Passamani, 1995). Espe-
cially when resources are scarce, canopy access can translate
into increased efficiency in finding resources, as canopy-
dwelling species can access fruits that are only accessible to com-
petitors on the ground after they fall (Layne, 1970; Rader &
Krockenberger, 2006). Predator avoidance is considered to be
another driver of canopy use (Schoener, 1974; Passamani,

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6 Sarina Thiel and others
1995). Therefore, VS contributes to reducing interspecific com-
petition and to enable the co-existence of many sympatric spe-
cies and thus the maintenance of diverse communities of small
mammals in tropical forests (Schoener, 1974).
(4) Primate communities
VS of sympatric species emerges as a consistent pattern in
primate communities, particularly in the Neotropics and in
Africa (Table S1; Pook & Pook, 1982; Cords, 1987;
Gautier-Hion, 1988; Lopes & Ferrari, 1994; Kaplin &
Moermond, 2000; Pozo-R & Youlatos, 2005). Body mass
and locomotion seem to be structuring factors for VS in Afri-
can and Neotropical primates (Youlatos, 1999; Buchanan-
Smith et al., 2000; Heymann, Encarnación, & Canaquín,
2002). Larger species usually occupy higher strata, where
they rarely use vertical supports and commonly jump from
branch to branch (Fig. 1). Smaller species, by contrast, live
in lower forest levels, use vertical substrates like vines,
branches, and twigs extensively, and perform vertical cling-
ing and leaping between trunks to locomote (Fleagle &
Mittermeier, 1980; Buchanan-Smith et al., 2000; Heymann
et al., 2002). An exception are large terrestrial or semi-
terrestrial species like Mandrillus leucophaeus and Cercopithecus
campbelli that occupy lower strata of African tropical forests
than sympatric guenon species (Gartlan & Struhsacker,
1972; Buzzard, 2006). The role of body mass in VS is less
pronounced for African, Asian, and Malagasy primate com-
munities (MacKinnon & MacKinnon, 1980; Ungar, 1996).
This difference between the Neotropics and other regions
could be a consequence of Neotropical primates being on
average significantly smaller than their Paleotropical coun-
terparts (Kappeler & Heymann, 1996). However, more
detailed studies of Paleotropical primate communities are
needed to examine this question.
Differences in diet composition between primate species
ranging at different heights suggest that VS facilitates niche
segregation (ecological partitioning), thus allowing their sym-
patric coexistence. For instance, Cercopithecus diana generally
forage on fruits in higher strata, Cercopithecus petaurista mostly
feed on foliage in the middle stratum, and Cercopithecus camp-
belli mainly eat fruits and animal prey in lower strata of Afri-
can tropical forests (Buzzard, 2006). The Neotropical species
Ateles paniscus and Chiropotes satanas are very similar in their use
of forest strata but differ in diet: the former consuming pri-
marily fruit pulp, the latter being a seed predator, while Pithe-
cia pithecia – also a seed predator – occupies lower strata than
C. satanas.
The role of VS for niche segregation becomes particularly
obvious in interspecific associations (mixed-species groups) of
closely related taxa. In associations formed by species of the
Neotropical tamarin genera Leontocebus (comprising what
was previously considered subspecies of Saguinus fuscicollis)
and Saguinus (S. imperator, S. labiatus, S. mystax), the former
occupies on average lower strata than the latter (Yoneda,
1980, 1984; Norconk, 1990; Buchanan-Smith, 1999). While
they mainly feed on the same plant food resources, different
Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.
foraging heights are associated with different prey-capture
strategies (for example, use of the trunk surface, bark, and
crevices versus use of foliage as foraging substrates) that reduce
overlap in the animal portion of the diet (Peres, 1993b;
Nickle & Heymann, 1996; Smith, 2000; Porter, 2001).
Apart from facilitating sympatric coexistence, vertical seg-
regation in interspecific associations provides benefits in
terms of complementary vigilance (Peres, 1993a), reduced
individual efforts for vigilance (Cords, 1990; Oates &
Whitesides, 1990; Hardie & Buchanan-Smith, 1997; Wol-
ters & Zuberbühler, 2003), and increased foraging efficiency
(Terborgh, 1983; Podolsky, 1990; Peres, 1992, 1996).
IV. VS OF FRUIT QUANTITY AND QUALITY
Food resource availability seems to be one of the key factors
determining VS and canopy use of vertebrates in tropical for-
ests. Naturally, there is a strong relationship between quality,
quantity, and distribution of food and the number and den-
sity of fruit consumers (Smythe, 1982; Loiselle &
Blake, 1991). Tropical rainforests are highly seasonal envi-
ronments regarding phenology and fruit availability
(Foster, 1982; Sabatier, 1985; Kinnaird, O’Brien, & Suryadi,
1996; Wikelski, Hau, & Wingfield, 2000). Whenever
resources are limited, competition arises and the organiza-
tion of animal assemblages and the coexistence of species
are affected (Houle, Vickery, & Chapman, 2006). This raises
the question of whether fruit production, for instance in
terms of quantity and quality of fruit crops in tropical forests
also shows patterns of VS.
The quantity and quality of fruits do differ among forest
strata (Table S2). In many tropical forests around the world,
fruit abundance and density are higher in the canopy than in
the lower strata (Shanahan & Compton, 2001; Schaefer,
Schmidt, & Wesenberg, 2002; Houle, Chapman, &
Vickery, 2007). Also, fruits of canopy trees are often larger
and contain more water, sugar, and fruit pulp dry matter
per fruit compared to fruits of understorey trees
(Shanahan & Compton, 2001; Houle et al., 2007). A study
on diverse Ficus species in a Bornean lowland rainforest
showed that canopy figs were produced in a greater size
range than those of the understorey. Furthermore, fig crops
were considerably larger in the canopy (Shanahan &
Compton, 2001). The quantity and quality of fruits not only
vary among species and trees of different forest strata, they
can even vary within a fruit tree. For 15 tree species in the
Kibale National Park of Uganda, canopy feeding sites pro-
duced a higher density and nutritional value of food than
lower feeding sites on the same tree (Houle, Conklin-Brit-
tain, & Wrangham, 2014).
These findings explain, at least partially, why some species
show a pronounced preference for the canopy and why com-
munities are vertically stratified. For instance, Schaefer
et al. (2002) observed that most large avian frugivores fed in
the middle strata where fruits were largest. Smaller frugivorous
Stratification in tropical forest frugivores
birds like tanagers and warblers, by contrast, were mainly
observed feeding on the smaller fruits in the canopy
(Greenberg, 1981a; Thiollay & Jullien, 1998; Schaefer
et al., 2002). These observations differ from the general pat-
tern, that large fruits mainly occur in the canopy and that
large seed dispersers thus mainly feed in the canopy and small
ones in the understorey, but demonstrate how fruit availabil-
ity can shape VS of seed-disperser communities. However,
differences in fruit production among forest strata in terms
of abundance, size, and nutrient content may not only induce
a VS of seed-dispersing species based on their resource
requirements, but also have the potential to cause competi-
tion. For instance, all primate species in the Kibale National
Park preferred to feed in higher strata when alone (Houle,
Chapman, & Vickery, 2010). However, in the presence of
dominant species that were able to monopolize the canopy
as a feeding site, subordinates retreated to feeding sites in
lower forest strata (Houle et al., 2010).
In summary, the availability of fruits in terms of fruit num-
bers, fruit sizes, and calorific value of fruits differ among for-
est strata. Many factors can potentially influence the actual
patterns, including climatic conditions, phylogenetic diver-
sity, and the floristic composition of the forest. Nevertheless,
stratification of fruit resources obviously could influence the
vertical niches of seed-dispersing species.
V. VS OF INTERACTIONS BETWEEN PLANTS
AND SEED DISPERSERS
Understanding the structure of species interactions across
vertical gradients is crucial in explaining global biodiversity
patterns. Above, we have established that bird, bat, primate,
and small mammal assemblages exhibit patterns of VS. Addi-
tionally, the quantity and nutritional value of fruits have been
shown to vary along the vertical gradient. This leads to the
assumption that these differences among forest strata may
also affect plant–animal interactions, for instance in terms
of interaction frequencies and mutual specialization, particu-
larly concerning plants and their frugivorous seed dispersers.
Schleuning et al. (2011) reported that the degree of
generalization in the plant–frugivore network in a Kenyan
rainforest was vertically stratified, probably caused by the
resource-oriented utilization of fruits. In the understorey,
opportunistic frugivores were abundant and, due to limited
fruit choice and availability, were rather specific in their fruit
choice. By contrast, obligate frugivores moved predomi-
nantly within the canopy, where they could forage on a large
range of plant species with fleshy fruits (Schleuning
et al., 2011). Consequently, the canopy network was composed
of strong links and generalized associations, whereas the under-
storey was characterized by weak links and more specialized
associations (Schleuning et al., 2011). These findings are in line
with a study of frugivore assemblages on Ficus trees
(Shanahan & Compton, 2001). Figs of understorey trees were
mainly consumed by small non-flying mammal species and
Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.
7
small bulbuls, whereas the larger figs of canopy species
attracted a more diverse assemblage of large-bodied bird and
mammal species (Table S2; Shanahan & Compton, 2001).
It becomes evident that seed-disperser and plant traits also
differ among forest strata. Plant traits such as plant height,
fruit morphology, and nutritional content are determinants
of seed-disperser foraging behaviour and fruit-removal rates
(Blendinger, Loiselle, & Blake, 2008; Muñoz et al., 2017). At
the same time, seed-disperser traits such as body size, wing
shape, and sensory and locomotory physiology determine
their fruit choices and foraging height (Jordano, 1995;
Bender et al., 2018). In mutualistic interactions such as seed
dispersal, evolution will have favoured matching of traits
between partners (Thompson, 2005). VS plays an important
role in this diversification of plant fruit structures, dispersal
devices, and disperser traits. First, plant height affects seed
dispersers that have preferences for particular forest strata
(Shanahan & Compton, 2001; Schleuning et al., 2011; Muñoz
et al., 2017). In terms of trait matching, for instance, wing shape
of avian seed dispersers was shown to be highly related to plant
height (Bender et al., 2018). While rounded wings allow birds
to forage in the dense forest understorey, birds with pointed
wings are better equipped to move quickly and forage in the
canopy (Moermond & Denslow, 1985). Second, disperser seed
consumption is also affected by fruit and seed size. Seed size
can limit consumption due to morphological constraints of
the frugivores (Jordano, 1995) and the importance of traits
related to size matching in interaction networks is well estab-
lished (Woodward & Warren, 2007; Maglianesi, Böhning-
Gaese, & Schleuning, 2015; Bender et al., 2018). In vertically
stratified forests, different sets of morphological traits have
evolved among strata and VS appears to be an important fac-
tor shaping plant and seed-disperser traits and thus structuring
the variety of their mutualistic interactions (see Table S2 and
Section VI.2).
The VS of seed-disperser assemblages and their traits has
implications for the plant species that depend on the dispersal
of their seeds. In the canopy, the high abundance and diver-
sity of obligate frugivores provides reliable seed-dispersal ser-
vices for the trees (Schleuning et al., 2011) due to their
generalized fruit choice (Loiselle & Blake, 1990; Carlo, Col-
lazo, & Groom, 2003; Wallace, 2006). Dispersal by diverse
frugivores might improve the quality of seed dispersal due
to complementary effects (Fleming, 1993; Schleuning,
Fründ, & García, 2015; Rother, Pizo, & Jordano, 2016).
Such complementary effects include different dispersal dis-
tances away from the mother plant and deposition in differ-
ent microhabitats (Jordano et al., 2007). These effects are
induced by differences in seed-disperser traits such as body
size, feeding style, and mobility (Shanahan & Compton,
2001; Jordano et al., 2007; Kissling, Böhning-Gaese, &
Jetz, 2009). Based on the diversity of seed-disperser traits in
species-rich assemblages, canopy fruiting species were
expected to achieve greater spatial homogeneity of seed rain
(Shanahan & Compton, 2001). Furthermore, they were sug-
gested to experience a higher dispersal probability and reli-
ability (Shanahan & Compton, 2001). The larger fruits in
8 Sarina Thiel and others
the canopy tend to attract large-bodied frugivores
(Lambert, 1989a; Kalko et al., 1996), which need to eat more
fruits than small frugivores and thus are more reliable seed
dispersers (Shanahan & Compton, 2001). Additionally, their
gut passage time is longer and they travel further, whereby
seeds are dispersed over larger distances (Lambert, 1989b).
By contrast, plants in the understorey depend mainly on
seed-dispersal services provided by rare and opportunistic
frugivores, which are specialized on certain plant species
which may result in a lower effectiveness of seed dispersal.
Additionally, small understorey frugivores tend to have
shorter gut passage times, resulting in shorter dispersal dis-
tances (Westcott & Graham, 2000).
The obligate and opportunistic frugivores of higher and
lower forest strata, respectively, occupy a crucial ecological
role as seed dispersers for tropical plant species. High abun-
dance and generalized fruit choice of obligate frugivores
could mitigate spatiotemporal variation in the abundance
of consumer species and thus increase the robustness of
seed-dispersal interactions (Schleuning et al., 2011). This
might render canopy trees more resilient towards disruption
such as habitat fragmentation, human interference, or the
drop out of single dispersers (Farwig et al., 2006; Kirika
et al., 2008a, 2008b). Seed-dispersal interactions in the
under- and midstorey, by contrast, are far more sensitive
towards species loss when they depend on fewer and more
specialized species (Cordeiro & Howe, 2003; Schleuning
et al., 2011).
VI. DISCUSSION AND OUTLOOK
(1) Patterns of VS across taxa and tropical regions
Communities of bird, bat, primate, and non-flying small
mammal species are all vertically stratified in terms of abun-
dance, species diversity, and community composition. When
comparing patterns of VS across taxa, it becomes clear that
these are influenced by different taxon-specific traits. For
birds, body and wing size can to some extent constrain the
use of certain vertical strata. Whereas birds are mostly active
during daytime and visually oriented, bats are nocturnal and
constrained by their echolocation system in combination
with their morphology. Finally, in primate and non-flying
small mammal communities, VS, body size, and locomotor
behaviour are strongly related (Fig. 1). So far, studies com-
paring VS among different seed-disperser taxa and examin-
ing, for instance, how they affect one another and how
competition or interaction might shape their distribution
across forest strata are very rare. One of the few examples
of cross-taxa comparisons was conducted by Poulsen
et al. (2002) who found that hornbills and primates utilize dif-
ferent kind of fruits, resulting in a rather low dietary overlap,
and that hornbills feed in higher forest strata than primates.
In assembling studies for this review, a distinct geographi-
cal bias in favour of studies conducted in the Neotropics
Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.
became apparent. Depending on the respective taxa,
between 60 and 80% of all studies have been conducted in
Neotropical forests (Tables S1 and S2). Although studies
from Africa, Asia, and Australia report patterns of VS for
communities of bird, bat, primate, and non-flying small
mammal species comparable to those in the Neotropics,
these conclusions are based on a relatively small number of
studies. More research is needed to close this research gap
on VS of seed-disperser communities in other tropical
regions.
Nevertheless, despite the differences in biological charac-
teristics of species, and incongruencies in sampling tech-
niques, effort, and geographical distributional limits, it is
evident that local species assemblages adjust to their verti-
cally stratified environment.
(2) VS and trait evolution
VS influences the evolution of plant–animal trait pairs, for
instance, plant height and wing shape, or crop size and body
mass (Bender et al., 2018). Co-varying morphological charac-
ter complexes (e.g. fruit size and colour) evolved in response
to selection by particular groups of seed dispersers (Gautier-
Hion et al., 1985; Fischer & Chapman, 1993; Shanahan
et al., 2001; Hodgkison et al., 2007). It is conceivable that these
character complexes respond also to VS of seed dispersers.
Furthermore, additional fruit characteristics, for instance
fruit odours, are likely to show patterns of VS. Different dis-
perser groups like bats, birds, primates, and non-flying small
mammals are attracted by different fruit scents. Primate-
compared to bird-dispersed fruits, for instance, have espe-
cially rich odours, which are informative about ripeness
(Nevo et al., 2016, 2018). Consequently, depending on the
degree of specialization in plant–seed disperser networks,
VS may also be expected in fruit odours.
Light environments are highly variable among forests and
among forest strata (Endler, 1993). Perceived fruit colours
depend on the interaction between the ambient light spec-
trum and the reflectance spectrum of fruits (Endler, 1993).
Since the colour of fleshy fruits may have evolved to maxi-
mize visual detection by seed dispersers (e.g. Willson &
Whelan, 1990; Schaefer, Schaefer, & Levey, 2004), and since
fruit colour varies between bird- and primate-dispersed fruits
(Valenta et al., 2018), VS in fruit colour can be expected.
Finally, plant species that provide fruits across all vertical
strata (e.g. the Neotropical liana Marcgravia longifolia), and
thus are subject to differential selection pressures from verti-
cally stratified seed-disperser communities, represent test
cases that allow the study of the role of VS on trait evolution.
(3) Effects of global change on vertically stratified
forests and seed-disperser communities
(a) Local anthropogenic effects
Land-use changes – ranging from selective logging to habi-
tat loss and fragmentation – are the main drivers of global
change, threatening plant and seed-disperser communities
Stratification in tropical forest frugivores
of tropical forest ecosystems (Vitousek et al., 1997; Sala
et al., 2000). These drivers significantly alter forest structure,
community composition of plants, sapling and tree densi-
ties, and understorey density (Malcolm & Ray, 2000;
Lefevre, Sharma, & Rodd, 2012). For instance, edge phe-
nomena such as increased desiccation stress, wind shear,
and wind turbulence (Laurance et al., 1997, 1998) sharply
elevated the mortality of slow-growing, large-seeded, and
high-canopy trees, and produced shifts in tree species com-
position and size distribution (Laurance et al., 2006). Large
trees are also often removed in selectively logged forests,
resulting in numerous openings in the forest canopy
(Struhsaker, 1997). And while biological invasions are rare
in undisturbed tropical forests, exotic species frequently
invade disturbed tropical forests (Fine, 2002). Fast-growing
pioneer tree and shrub species such as Syzygium jambos in
Costa Rica (DI Stefano et al., 1998), Lantana camara in
India (Joshi, Mudappa, & Shankar Raman, 2015), or Cecro-
pia peltata in Malaysia (Putz & Holbrook, 1988) can rapidly
change the structure and density of forest under- and mids-
tories. Numerous studies have already shown that the sus-
ceptibility of seed dispersers to changes in forest structure
and species composition differs among focal taxa and func-
tional species groups (Medellin & Gaona, 1999; Farwig,
Sajita, & Böhning-Gaese, 2008; Grass et al., 2014). Consid-
ering that global change effects alter the physical structure
of forest strata, these differences are likely even more pro-
nounced in view of the VS of seed-disperser communities.
However, studies investigating the effects of land-use
changes on vertically stratified communities are very rare.
In the Amazonian rainforest of Brazil, for instance,
canopy-foraging bats were shown to be less sensitive to frag-
mentation than understorey species, as they tend to be more
mobile (Silva et al., 2020). Nevertheless, understorey species
also adapted to the higher post-fragmentation vegetation
density of the understorey by foraging higher (Silva
et al., 2020). In the southwestern Central African Republic,
decreased canopy cover following selective logging led to a
shift in small-mammal biomass from the canopy stratum
downward to the ground (Malcolm & Ray, 2000). In South
India, a decline in tree cover with the subsequent invasion of
L. camara selectively favoured avian seed dispersers adapted
to lower vegetation, whereas forest specialists of the canopy
declined (Aravind et al., 2010). Overall, understanding how
global change effects impact the VS of seed-disperser com-
munities of different taxa and functional groups remains an
important challenge.
Agroforestry – intentional management of agricultural
crops with shade trees – could constitute a compromise that
allows reducing deforestation in the tropics, while simulta-
neously improving rural livelihoods (Ashley, Russell, &
Swallow, 2006). For instance, bat and bird assemblages
occurring in banana and multistrata cacao agroforestry sys-
tems in Costa Rica are abundant, species rich, and very
diverse (Harvey, & Gonzáles Villalobos, 2007). Similarly,
mixed fruit orchards in Thailand harbour up to 50% of the
bird species inhabiting neighbouring forests (Round, Gale, &
Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.
9
Brockelman, 2006). Williams-Guillén et al. (2006) reported
that shade coffee plantations with a high diversity of shade
trees provide suitable habitat and serve as corridors between
forest fragments for mantled howler monkeys Alouatta palliata.
These and many other examples across the tropics show that
agroforestry systems with diverse canopy cover and less-
intensive management have high species richness, harbour
significant parts of the local fauna, and could thus play an
important role in biodiversity conservation [see Bhagwat
et al. (2008); Udawatta, Rankoth, & Jose (2019) and refer-
ences therein]. However, the implications of the simplifica-
tion of the vertical structure, with a thinned canopy and a
less-dense stratum below, for vertically stratified communi-
ties have not been studied in detail. Neither are there studies
examining whether the tree species composing this simplified
canopy layer still offer sufficient resources for the large seed-
dispersing species foraging in the canopy, nor whether those
systems with complete suppression of native understorey veg-
etation still sustain species normally inhabiting the dense veg-
etation of the lower forest strata. Additionally, studies
investigating how the associated changes affect the ecological
functionality in plant–animal networks are urgently needed.
For instance, Bakermans et al. (2012) highlighted the need
explicitly to consider attributes of various forest strata. VS
of coffee plantations with shade trees in the Venezuelan
Andes contributed to a high diversity of migratory birds.
Upper-canopy foragers were positively associated with the
number of large trees and tree canopy height, and low-
canopy and ground foragers with the number of small and
medium-sized trees and shade cover (Bakermans
et al., 2012). Furthermore, bats and birds react in different
ways to the structural and floristic simplification in agrofor-
estry systems (Faria et al., 2006). In shade cacao plantations
in Brazil, bat assemblages are as species rich, diversified,
and abundant as in pristine forests, and maintain all species
and feeding guilds (Faria et al., 2006). For bats, the combina-
tion of a less-dense although still vertically stratified habitat
with the maintenance of major food resources may even be
beneficial as they can move and forage more easily (Faria
et al., 2006). For the bird community, by contrast, the com-
plete suppression of native understorey vegetation leads to
a decrease in forest-dependent species of the forest interior
and an increase in edge and open-field bird species (Faria
et al., 2006). These results show that the habitat modification
in agroforestry systems affects various biological groups, and
groups inhabiting the different strata, in different ways. Agro-
forestry systems cannot truly substitute the original forest,
and, even though the importance of multistrata agroforestry
systems is increasingly recognized (Young, 2018), more
research is needed examining the effects of these systems on
vertically stratified communities.
Besides agroforestry systems, secondary forests and tree
plantations are expanding rapidly in the tropics (Mace,
Masundire, & Baillie, 2005; Wright, 2005). Their contribu-
tion to offset biodiversity loss from deforestation has been
suggested, as they apparently allow the survival of some forest
species and furthermore, provide complementary benefits in
10
terms of ecosystem goods and services (Myers, 1997; Linden-
mayer & Franklin, 2002). For instance, in the northeastern
Brazilian Amazon, surprisingly high numbers of primary for-
est mammal and bat species were found in areas of native
regeneration and exotic tree plantations with an understorey
of native shrubs (Barlow et al., 2007). However, these areas
were still surrounded by an intact forest matrix and further-
more, variability across taxa was high. In contrast to the find-
ings for bats and mammals, the species richness of birds was
significantly lower in secondary forests and tree plantations
than in primary forests. Also, community composition dif-
fered between primary and secondary forests for all focal taxa
(Barlow et al., 2007). In a review of tropical forest regenera-
tion, Dunn (2004) concluded that species richness can be
predicted to resemble that of primary forests roughly
20–40 years after land abandonment. Nevertheless, the
recovery of community composition differed among taxa.
For birds, it took much longer than the recovery of species
richness [Dunn (2004) and references therein]. However,
considering the VS of communities, conclusions for entire
animal taxa are unlikely to be reliable. For instance, the early
stages of forest regeneration only contain shrubs and small
trees, but no high canopy layer. As tall canopies provide
additional resources and greater vertical foraging space, they
provide more opportunity for the coexistence of species than
low-stature forests (Bakermans et al., 2012). It can be pre-
dicted that these early succession habitats are unable to sup-
port species normally inhabiting the canopy layer of tropical
forests. Furthermore, with a low canopy height and less VS,
the understorey environment shows marked differences in
temperature, light, and moisture conditions compared to pri-
mary forests (Lebrija-Trejos et al., 2011). Therefore, investi-
gations about how these different environmental conditions
affect understorey species are needed. Generally, more stud-
ies are necessary that examine the relationship between ver-
tically stratified communities and forest regeneration.
(b) Global effects
Global climate effects such as changes in temperature, pre-
cipitation, humidity, or extreme weather events are pre-
dicted to increase the damage to tropical rainforests
(Wright, 2005; Malhi et al., 2009), but they might not be uni-
form across all vertical strata. The available evidence indi-
cates that the three-dimensional structure and community
composition of tropical forests are going to change. Rapid
increases of aboveground biomass, stem density, basal area,
recruitment, mortality, and the relative importance of lianas
and canopy tree species at the expense of understorey tree
species have been recorded and are considered to be linked
to rising atmospheric CO2 concentrations and an increase
in photosynthetically active radiation, although the actual
mechanisms are still unclear (Phillips et al., 2002, 2004; Baker
et al., 2004; Laurance et al., 2004; Lewis et al., 2004). Such
changes in tropical forest structure will affect the vertical dis-
tribution of the associated seed-dispersing vertebrate com-
munities. Furthermore, climate change is predicted also to
Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.
Sarina Thiel and others
affect plant phenology. For instance, an exclusion experi-
ment in an eastern-central Amazon forest examining the
effects of severe drought episodes on canopy dynamics, emis-
sions of greenhouse gases, and other ecological functions
demonstrated a thinning of the canopy and a decline of fruit-
ing in the treatment plots (Nepstad et al., 2002). Significant
and unexpected changes or crashes of fruit availability will
greatly impact frugivorous vertebrates and thus seed dis-
persal (Butt et al., 2015; Morellato et al., 2016). It has been
suggested that vertical movement along the gradient might
allow more-flexible species to tolerate changes in tempera-
ture and to seek buffered conditions within particular micro-
habitats (Scheffers et al., 2017; Scheffers & Williams, 2018).
Canopy visitors, for instance, might shift their vertical distri-
bution downwards in response to droughts (Bickford, 2005;
Scheffers et al., 2013). Canopy species, however, which spe-
cialize on particular resources in this stratum or are restricted
in their usage of space by morphological traits, cannot easily
translocate their habitat downwards. They may reach their
thermal limit due to increasing droughts and dry seasons
and thus, depending on how harsh the conditions become,
may face extinction from the canopy layer of tropical forests.
(c) Impacts on plant–animal interaction networks
Ultimately, the impacts of the main drivers of global change
are predicted not only to affect species abundances, commu-
nity composition, and organismal physiology but also to
cause serious alterations to the networks of interactions
among species (Sala et al., 2000; Tylianakis et al., 2008). We
discussed above that the differences in responses of plant
and animal species to drivers of global change may favour
certain species or growth forms over others. As plant and ani-
mal communities are linked by their mutualistic relation-
ships, negative effects on the composition of plants may
ultimately cause changes in seed-disperser communities and
vice versa (Lefevre et al., 2012). Differences in the susceptibility
of interaction networks to drivers of global change have
already been suggested (Schleuning et al., 2011; Grass
et al., 2014). For instance, networks comprising strong links
and generalized associations seem to be less prone to disrup-
tion than those characterized by weak links and more-
specialized interactions (Schleuning et al., 2011). However,
the consideration that species and network characteristics
and traits also differ among strata adds an additional layer
of complexity to the variability of responses to environmental
change. For instance, habitat modification in agroforestry
systems may not strongly affect the networks of the canopy
strata but may represent a particular threat to the plant–seed
disperser networks of forest understories. As the native
understorey vegetation is suppressed in agroforestry systems,
this will result in a loss of understorey seed-dispersing species
specialized on particular understorey fruiting plants. Threats
to the network of the canopy stratum, by contrast, may be
induced by other drivers of global change. On one hand, it
has been argued that canopy trees are especially vulnerable
to forest degradation, fragmentation, and selective logging
Stratification in tropical forest frugivores
(Bello et al., 2015). They often produce fruits with a single,
large seed (Roth, 1987), which can only be dispersed by a
small number of large-bodied frugivores (Levey, 1987; Peres
et al., 2016; Whitworth et al., 2019). As large-bodied arboreal
species in general face disproportionately high threats of
extinction due to hunting and habitat loss, dependent canopy
trees are at particular risk of losing their dispersers
(Peres, 2000; Whitworth et al., 2019). On the other hand,
canopy trees have been suggested to be more robust towards
disruption when interactions in the canopy are generalized
and the seeds of canopy-fruiting trees are dispersed by many
different dispersers. This should render the plants more
robust to the loss of single disperser species (Shanahan &
Compton, 2001; Schleuning et al., 2011). However, if
increasingly extreme temperatures and droughts in the can-
opy, due to climate change, cause the loss of many seed-
dispersing species from this stratum, the plant species fruiting
there will also be left with a reduced spectrum or even with-
out dispersers. The consequences may include lower seedling
establishment and survival, and ultimately decreased abun-
dance of such dependent plant species (Bleher & Böhning-
Gaese, 2001; Makana & Thomas, 2004). These examples
show that the effects of different drivers of global change
are likely to be extremely variable and may also differ among
strata.
(4) High variability of data quality among taxa
Due to different taxon-specific characteristics and beha-
vioural patterns, different sampling methods have to be used,
resulting in highly variable data quality among groups. For
birds, focal observations from the ground and canopy towers,
complemented by mist netting, have led to reliable and large
data sets, including high numbers of species. By contrast, for
bats, primates, and non-flying small mammals, small sample
size is a common problem. Studies on primates mostly rely on
behavioural observations. These may be more difficult than
focal observations of birds, as primate groups need to be
habituated in order to follow them consistently through the
forest. Inherently, this type of data gathering leads to rather
small data sets based on few species and a limited number
of individuals. The same problem applies to the nocturnally
active bats and the frequently crepuscular non-flying small
mammals. In order to investigate these species, capturing
devices such as mist nets and traps need to be installed at
varying heights in the forest. Difficulties in the placement
and configuration of these devices complicate the achieve-
ment of large and reliable sample sizes and allow in most
cases sampling of only a part of the local fauna and frequently
not over the entire vertical gradient (Kalko &
Handley, 2001). However, a number of recent methodologi-
cal advances are promising. For example, with increased
access to the canopy of tropical forests enabled by the expan-
sion of infrastructure such as canopy towers, new equipment
for rope climbing, and the use of drones, data collection in
the canopies of tropical forests is constantly improving
(Nakamura et al., 2017). At the same time, recent
Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.
11
technological improvements in monitoring systems now
enable the collection of a wide range of ecological data for
terrestrial wildlife. For instance, camera traps have proved
to be a useful, cost-effective, and relatively low-effort tech-
nique (Gregory et al., 2014; Moore et al., 2020). Furthermore,
the development of automated radio-tracking systems
(Gottwald et al., 2019) will likely allow us to determine the
vertical movement patterns even of small animals (see Rip-
perger et al., 2020) in the near future and thus will provide
an increasingly detailed view of vertical movements of indi-
vidual animals.
(5) Outlook
Understanding the importance of VS for mutualistic interac-
tions requires data at a high resolution along the vertical gra-
dient, and remains an important challenge particularly in the
context of global change. Future investigations should focus
on answering the following questions.
(1) How common is VS of interaction networks such as
observed by Schleuning et al. (2011) across tropical for-
est ecosystems?
(2) Does VS in the vegetation structure exert selection
pressures on associated seed dispersers (and other
groups of animals)?
(3) What is the role of competition versus mutualistic inter-
actions among taxa in shaping the distribution of
plants and their seed dispersers among forest strata?
(4) Do seed-dispersing species shift strata at different times
of the year in response to phenological changes in food
availability?
(5) If an attractive food resource is available beyond the
preferred stratum, do species acting as seed dispersers
still remain within their preferred vertical niche?
(6) What are the consequences of changing interaction
frequencies and degree of mutual specialization across
strata for the species involved and for whole networks?
(7) Do networks in higher strata have higher robustness
towards disruption and the drop out of single species?
Does high biodiversity across strata enhance the resil-
ience of seed-dispersal mutualisms to global change?
(8) How will global change affect VS, biodiversity, and
species interactions such as seed dispersal, and are
these effects similar or different among tropical regions
and ecosystems?
VII. CONCLUSIONS
(1) The importance of VS as a crucial determinant of spe-
cies richness and diversity in tropical forests is undeni-
able. The structural complexity of tropical forests
creates vertically stratified ecosystems with a broad
range of environmental conditions, for example, in
microclimate and light. This allows for the coexistence
of species with largely similar ecological requirements
12
by forming stratified communities along the vertical
gradient.
(2) Plant–seed disperser interaction networks and the
degree of specialization and interaction strength
within these networks change across the vertical gradi-
ent. In vertically stratified forests, different sets of mor-
phological traits have evolved among strata and VS
appears to be an important factor in shaping plant
and seed-disperser traits and thus structuring the vari-
ety of their mutualistic interactions.
(3) Global change is likely to affect and alter patterns of VS
in tropical forests, but further research is needed. Exam-
ining the links between species’ distribution, dispersal
capabilities, and plant–seed disperser interactions at
fine spatial scales and across the vertical gradient will
be crucial. Answering these questions in complex tropi-
cal forests requires the establishment of long-term mon-
itoring programs including vertically stratified surveys.
VIII. ACKNOWLEDGEMENTS
We thank the DFG for funding the project “Vertical Stratifica-
tion of plant-animal interactions and their impact on pollination
and seed dispersal within a single Neotropical plant species” to
K.H. (HE 7345/5-1), E.W.H. (HE 1870/27-1), and M.T.
(TS 81/14-1). We are grateful to Luis Guzman Duchen for con-
tributing the drawing and to Malika Gottstein for her comments
and suggestions on an earlier version. Finally, we thank two
anonymous reviewers for their constructive feedback.
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X. Supporting information
Additional supporting information may be found online in
the Supporting Information section at the end of the article.
Table S1. Studies of specific seed-dispersing vertebrate taxa
and their most important results regarding vertical stratifica-
tion (VS).
Table S2. Studies of plants and plant–seed disperser inter-
actions in tropical forests and their most important results
regarding vertical stratification (VS).