Food plant diversity as broad-scale determinant
of avian frugivore richness
W. Daniel Kissling1,2,*, Carsten Rahbek3and Katrin Bo ¨hning-Gaese1,2
1Community and Macroecology Group, Department of Ecology, Institute of Zoology,
Johannes Gutenberg-University, 55099 Mainz, Germany
2Virtual Institute Macroecology, Theodor-Lieser-Strasse 4, 06120 Halle, Germany
3Center for Macroecology, Institute of Biology, Universitetsparken 15, 2100 Copenhagen, Denmark
The causes of variation in animal species richness at large spatial scales are intensively debated. Here, we
examine whether the diversity of food plants, contemporary climate and energy, or habitat heterogeneity
determine species richness patterns of avian frugivores across sub-Saharan Africa. Path models indicate
that species richness of Ficus (their fruits being one of the major food resources for frugivores in the tropics)
has the strongest direct effect on richness of avian frugivores, whereas the influences of variables related to
water–energy and habitat heterogeneity are mainly indirect. The importance of Ficus richness for richness
of avian frugivores diminishes with decreasing specialization of birds on fruit eating, but is retained when
accounting for spatial autocorrelation. We suggest that a positive relationship between food plant and
frugivore species richness could result from niche assembly mechanisms (e.g. coevolutionary adaptations
to fruit size, fruit colour or vertical stratification of fruit presentation) or, alternatively, from stochastic
speciation–extinction processes. In any case, the close relationship between species richness of Ficus and
avian frugivores suggests that figs are keystone resources for animal consumers, even at continental scales.
Keywords: Africa; coevolution; community assembly; macroecology; plant–frugivore interactions;
spatial autoregressive model
A large number of hypotheses have been proposed to
explain patterns of species richness at broad spatial scales
(Willig et al. 2003). Based on high correlations with
species richness, contemporary climate and energy
variables (e.g. precipitation, temperature and/or evapo-
transpiration) are often thought to explain spatial variation
in species richness better than any other non-climatic
variable (Wright 1983; Hawkins et al. 2003a; Currie et al.
2004). However, a number of other factors also determine
broad-scale patterns of species richness, including topo-
graphy, habitat diversity, or regional and evolutionary
history (e.g. Rahbek & Graves 2001; Jetz & Rahbek 2002;
Willig et al. 2003). Despite a century of debate about the
primary determinants of species richness, the underlying
causal mechanisms behind the patterns still remain
vague (Willig et al. 2003; Currie et al. 2004; Rahbek
et al. 2007).
For vascular plants, it is widely argued that precipi-
tation and ambient energy are the main drivers of species
richness (Hawkins et al. 2003a; Field et al. 2005). Water
availability, heat and light directly influence plant growth
and productivity and are essential to plant physiological
processes (Waide et al. 1999; Field et al. 2005). Higher
productivity might result in more species because
physiological tolerances of individual species vary for
different climatic conditions (‘physiological tolerance
hypothesis’; Currie et al. 2004), or, alternatively, because
more productive areas are warmer and evolutionary
rates might be faster at higher ambient temperatures
(‘speciation rate hypothesis’; Allen et al. 2006). For
animals, especially for endotherms, the relationships
between species richness and water, energy and climate
are less pronounced than for plants (Rahbek & Graves
2001; Jetz & Rahbek 2002; Hawkins et al. 2003a,b). One
likely explanation is that energy might not directly
influence animal species richness via its effect on animals’
physiological requirements or evolutionary rates, but
rather indirectly via trophic relationships (Wright 1983;
Hawkins et al. 2003a,b; Currie et al. 2004). This
determined by the abundance, distribution and diversity
of food resources (e.g. plant biomass for herbivores, fruits
At small spatial scales, animal species richness can be
associated with the abundance, diversity or partitioning
of food resources (e.g. Herrera 1985; Siemann et al.
1998; Novotny et al. 2006). This relationship is however
difficult to test at large spatial extents because it is
difficult to map food resources for animal groups at
continental scales (e.g. insects for insectivorous birds).
One possibility to test for a link between animal species
richness and resources is to relate the species richness of
animals to that of their food items (e.g. food plants;
Hawkins & Porter 2003; Ma ´rquez et al. 2004; Novotny
et al. 2006). However, correlations between animal and
plant species richness can also result from both groups
responding similarly to the same environmental variables.
After accounting for these environmental variables, a
convincing dependency of animal on plant species
Proc. R. Soc. B (2007) 274, 799–808
Published online 11 January 2007
Electronic supplementary material is available at http://dx.doi.org/10.
1098/rspb.2006.0311 or via http://www.journals.royalsoc.ac.uk.
*Author for correspondence (firstname.lastname@example.org).
Received 5 October 2006
Accepted 5 December 2006
This journal is q 2007 The Royal Society
richness has not been demonstrated so far at broad spatial
scales (Hawkins & Porter 2003; Hawkins & Pausas 2004;
Ma ´rquez et al. 2004).
Plant–frugivore interactions might be an ideal model
system for continental analyses of animal and plant species
richness. Most frugivorous animals heavily rely on fruits,
particularly in the tropics (Fleming et al. 1987). In a
number of fine-scale field studies, it has been shown that
the richness offrugivorous animals is largely dependent on
fruit availability (e.g. Herrera 1985; Fleming et al. 1987;
Bleher et al. 2003). Among the fruiting plants, the fig
genus (Ficus) has been considered to be a keystone plant
resource for many frugivores owing to large crop sizes and
asynchronous fruiting patterns throughout the year
(Terborgh 1986; Lambert & Marshall 1991; Shanahan
et al. 2001a; Bleher et al. 2003; Harrison 2005; but see
Gautier-Hion & Michaloud 1989). Thus, the diversity and
abundance of figs might set the carrying capacity for
frugivorous animals in the tropics. Correspondingly,
Goodman & Ganzhorn (1997) proposed that avian
frugivore richness might depend directly on species
richness of Ficus trees. However, no rigorous test of this
‘fig–frugivore-richness hypothesis’ has been conducted at
a large regional scale such as a continent.
In this study, we examine whether the richness of Ficus
species at a continental scale (i.e. sub-Saharan Africa)
influences avian consumer richness by examining a
comprehensive database with a resolution of 18 latitude
and longitude, summarizing the distribution of all
breeding birds (nZ1771), all Ficus species (nZ86) and
five climatic and environmental variables (precipitation,
temperature, productivity, topography and ecosystem
diversity). We classify frugivorous birds into three classes
(obligate, partial and opportunistic fruits eaters) and
predict the association between frugivore and Ficus
richness to be stronger for those frugivores that are more
specialized on fruit eating. We apply path analysis to
disentangle inter-correlations between variables and
compare the results of this non-spatial method with
those of spatial regression models that account for the
spatial autocorrelation structure within our dataset.
2. MATERIAL AND METHODS
(a) Bird data
We used an updated version (29 September 2005) of the
comprehensive distribution database of African breeding
birds compiled by the Zoological Museum, University of
Copenhagen (see Burgess et al. (1998) and Brooks et al.
(2001) for methodology; Jetz & Rahbek (2002) for sources
used for mapping). Maps for each species represent a
conservative extent-of-occurrence extrapolation of the breed-
ing range at a resolution of 18!18 cells (latitude–longitude).
Data were compiled from the standard reference works and
dozens of other published references (including recent atlases
and unpublished research) and, for difficult regions and taxa,
experts’ opinions were sought (the full list of sources is
available at http://www.zmuc.dk/commonweb/research/bio
data.htm). Most of the northern part of continental Africa,
the Sahara, is marked by extreme species scarcity (Jetz &
Rahbek 2002) and almost all species in it and North of it
belong to the Eurasian biome. We thus focused our analyses
on all 1771 breeding bird species south of the Saharan desert
ecoregion (figure 1e) with ecoregion boundaries for the South
Sahara as northern boundary (Olson et al. 2001). Our sub-
Saharan database contains 434 789 records on 1737 cells.
The extent of the grid was chosen to be similar to the one
used by Jetz & Rahbek (2002) to make the results
comparable. We therefore excluded cells containing less
(a) obligate frugivores(b) partial frugivores
(d) opportunistic fruit-eaters(e) all birds
rs = 0.89
rs = 0.62
rs = 0.72
rs = 0.59
Figure 1. Geographical patterns of species richness in sub-Saharan Africa. (a) Obligate frugivores (92 species), (b) partial
frugivores (200 species), (c) all Ficus trees (86 species), (d) opportunistic fruit eaters (290 species) and (e) all breeding birds
(1771 species). Equal frequency classification is shown, with colour ramps indicating minimum (dark blue, bottom of legend)
and maximum (dark red, top of legend) species richness. Note that the scale of richness differs among figures.
800 W.D. Kissling et al.
Fig diversity and avian frugivore richness
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