Agriculture as matchmaker of an unexpected mutualism: Great bustard
disperses and enhances emergence of domestic olive seeds
Miguel Delibesa , Casimiro Corbachob , Gemma Calvoa , José María Fedriania,∗
a
Estación Biológica de Doñana (CSIC), Avda. Américo Vespucio s/n, Isla de la Cartuja, 41092 Sevilla, Spain
de Zoología, Facultad de Ciencias, Universidad de Extremadura, Avda. de Elvas s/n. 06071 Badajoz, Spain
b Área
Abstract
By changing the habitats and altering plant traits, agriculture has severely disrupted many plant–animal mutualisms. Interestingly, however, the intensification of agricultural practices could also facilitate mutualistic relationships between species with
naturally mismatching phenotypes. We illustrate the potential of the great bustard (Otis tarda), a large steppe bird, as disperser
of domestic olive (Olea europaea) seeds, originally a forest species. In an area of southwestern Spain, 30% of bustard faeces
included olive stones (from 1 to 13). Only 1.7% of the bustard-ingested olive seeds were broken. Moreover, using a sowing
experiment, we show bustard ingestion enhanced seedling emergence, which reached 8.8%, 3.4% and 0.0% for bustard-ingested,
hand-depulped, and control seeds, respectively. As expected for Mediterranean habitats, seedling mortality was very high in
the first summer for all seed treatments. In 6 out of 19 non-plowed patches within our study area, we found olive saplings of
different ages likely to emerge from bustard-dispersed seeds. Given the large size of domestic olive fruits, bustards are among
the few local animals able to disperse their seeds and thus to assist in the forestation of field boundaries and abandoned lands.
Paradoxically, because bustards are rather restricted to open habitats, their success in shaping the habitat (i.e., ‘planting’ olive
trees) could lead to their own removal from the resulting forested landscape.
Zusammenfassung
Indem sie Lebensräume und die Eigenschaften von Pflanzen verändert, hat die Landwirtschaft nachhaltig zahlreiche
Tier-Pflanze-Mutualismen gestört. Indessen kann die Intensivierung der Landwirtschaft auch mutualistische Beziehungen
ermöglichen, und zwar zwischen Arten, deren Phänotypen von Natur aus nicht zueinander passen.
Wir demonstrieren das Potential der Großtrappe Otis tarda (ursprünglich ein Steppenvogel) als Samenverbreiter für die
Kulturolive Olea europaea, die ursprünglich eine Waldart ist. In einem Untersuchungsgebiet im Südwesten Spaniens enthielten 30% der Kotproben der Großtrappe Olivenkerne (1–13 Stück). Nur 1,7% der von Großtrappen aufgenommenen Kerne
waren zerbrochen. In einem Aussaatversuch zeigten wir, dass die Aufnahme durch Großtrappen die Keimung begünstigte:
die Keimungsraten betrugen 8,8% für von Großtrappen aufgenommene Kerne, 3,4% für Kerne, die von Hand entpulpt worden waren, und 0,0% für unbehandelte Kontrollen. Wie für mediterrane Habitate erwartet, war die Keimmortalität im ersten
Sommer bei allen Behandlungen sehr hoch. Auf 6 von 19 ungepflügten Stellen fanden wir in unserem Untersuchungsgebiet
Olivenschößlinge, die vermutlich aus von Großtrappen verbreiteten Samen hervorgegangen waren.
∗ Corresponding author.
Tel.: +34 954466700; fax: +34 95462125.
E-mail address: fedriani@ebd.csic.es (J.M. Fedriani).
Angesichts der Größe der Kulturoliven gehören Großtrappen zu den wenigen einheimischen Arten, die ihre Samen verbreiten
und damit zur Bewaldung von Feldrainen und Brachflächen beitragen können. Da die Großtrappe eher in offenen Lebensräumen
vorkommt, könnte ihre erfolgreiche Habitatgestaltung durch das “Pflanzen” von Olivenbäumen zu ihrem eigenen Verschwinden
aus der resultierenden aufgeforsteten Landschaft führen.
© 2011 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved.
Keywords: Artificial selection; Fruit size; Habitat shaping; Mediterranean habitat; Old-field recolonization; Olea europaea; Seed dispersal;
Spain
Introduction
Intensive agriculture has severely modified not only the
patterns of land use worldwide, but also the genotypes and
phenotypes of cultivated plant species. As a consequence,
agricultural practices have disrupted many plant–animal
mutualisms, which are necessary for sustaining life on
Earth (e.g., pollination, seed dispersal; Bond 1994; Ellstrand
2002; Tylianakis, Didham, Bascompte, & Wardle 2008). For
instance, habitat changes and insecticides have generated an
important global deficit of pollinators, which in some areas
even threatens some crop yields (e.g. Klein et al., 2007;
Aizen, Garibaldi, Cunningham, & Klein 2009). Similarly,
habitat loss and hunting are alarmingly reducing the number and diversity of animal seed dispersers, which seriously
threatens forest renewal (e.g. Moran, Catterall, & Kanowski
2009). A less considered intriguing effect of agriculture is the
enabling of novel ecological interactions when, for example,
crop species brought beyond their natural range are pollinated by native species (e.g. Kremen, Williams, & Thorp
2002). Even less explored is the potential of agriculture as
a ‘matchmaker’ of mutualistic interactions between species
with naturally mismatching phenotypes.
In the case of plants dispersed by vertebrates, agriculture
most often has disrupted this mutualism by modifying the
composition and structure of habitats and changing the traits
of cultivated plants. For example, by artificially enhancing
fruit size, relatively small-sized dispersers become unable
to swallow them and subsequently deliver their seeds. As a
result, many potential seed dispersers become pulp predators
(Rey and Gutiérrez 1996) and occasionally even agricultural
pests (e.g. De Grazio 1978).
The olive tree (Olea europaea) and its seed consumers
and dispersers represent a good example of such mutualism
disruptions, as recently stated by Rey (2011). In Southern
Spain, wild olive fruits are consumed by many species of
small birds, especially of the genera Sylvia and Turdus, but
most of them are unable to swallow the big drupes and/or
to live in cultivated monospecific olive orchards, because of
the lack of a diverse understorey vegetation and of complementary food (Rey 1993, 2011; Rey, Gutiérrez, Alcántara,
& Valera 1997). As a consequence, domestic olive seeds are
thought to be scarcely dispersed by wildlife, in spite of many
drupes remaining on the trees after harvest.
As mentioned above, however, human habitat modification
and artificial selection of fruit traits could result in a matching
of naturally mismatched phenotypes. To illustrate this overlooked possibility, we report about the role of a large steppe
bird, the great bustard (Otis tarda), as a legitimate disperser
of a cultivar of domestic olive seeds in southwest Spain. We
show that: (i) bustards regularly eat olive fruits; (ii) bustards
regularly defecate undamaged seeds in sites apparently favorable for seedling emergence; and (iii) emergence is enhanced
as a result of seed passage through the bird gut. Seed passage through bustard guts includes two different treatments
potentially altering the amount and speed of seedling emergence: the mechanical removal of the pulp and the mechanical
and chemical scarification of the stony endocarp (Traveset,
Robertson, & Rodríguez-Pérez 2007). Thus, (iv) we distinguish between the effects of these two treatments following
Samuels and Levey (2005). We also evaluate difference in
size between bustard-ingested and non-ingested seeds and
suggest potential underlying mechanisms. Finally, we discuss
the potential of agriculture as a ‘matchmaker’ of new interactions, as exemplified by the bustard-olive tree relationship
in southern Spain, and speculate about its implications in a
scenario of reforestation of set-aside lands and in the context of invasive species research (e.g. Spennemann & Allen
2000a).
Study site and system
The study was carried out at Llanos de la Albuera-Valverde
de Leganés, an area of about 10,000 hectares near Badajoz city (Extremadura, SW Spain). Climate is Mediterranean
subhumid, with hot and dry summers and wet and mild winters. Annual rain is about 400–600 mm and average annual
temperature 14–16 ◦ C. The area is a flat, mainly unirrigated
and very heterogeneous agro-ecosystem with cereal (about
45%), vineyard (15%), olive (13%), sunflower and leguminous (10%) cultivations, and some open “dehesas” and
pastures.
The oleaster or wild olive tree Olea europaea var. sylvestris
L. (Oleaceae) is a small tree domesticated long ago at several
times in several places to become the more characteristic cultivated tree in the Mediterranean Basin (Loumou & Giourga
2003). The global cultivated surface of domestic varieties
exceeded 100,000 square km in 2008, with 28% of this in
Spain and Portugal (http://www.fao.org/corp/statistics/en).
World average yield of olive drupes is about 1.7 tonnes/ha,
mainly devoted to the production of oil. The fruit pericarp
comprises a thin epicarp, a fleshy mesocarp, and a stony
endocarp that encloses the embryo. Olive orchards are
monospecific stands with trees regularly distributed. They
are important feeding places for wintering small-sized birds
in Mediterranean Europe (e.g. Rey 1993).
In our study site, most olive trees belonged to the “carrasqueñ a” cultivar and spacing among trees was usually
between 8 and 16 m. This variety is characterized by the
large size of the fruits, which are used preferentially for
direct consumption; usually harvest is early, at the beginning of the autumn, but many drupes (5–10% of the crop;
unpublished data) remain unharvested on the trees, where
they continue to mature before falling to the ground during
the winter. Average measures of 161 fallen drupes, collected
at the beginning of February 2011 under 16 different trees in
three orchards, were: weight (g) = 4.32 ± 0.08 (mean ± SE),
length (mm) = 22.49 ± 0.22, width (mm) = 17.95 ± 0.12.
The great bustard is probably the heaviest extant flying bird
in the world. In Spain, mean weight of females is 4–5 kg and
that of males is 10–12 kg (Alonso & Palacín 2009). It ranges
across central and southern Europe (with a small population
in northern Morocco), Western Russia and some temperate
areas of central and eastern Asia to the Pacific, occupying
open steppe grasslands and extensively cultivated fields (Del
Hoyo, Elliot, & Sargatal 1996). The status of the species in
the 2011 IUCN Red List is Vulnerable (IUCN 2011). Great
bustards are omnivorous, eating mainly green plant material and secondarily insects, with grains (wheat, barley, etc.)
and some other seeds also being common foods (Alonso and
Palacín 2009). In Spain they are partially migratory, with
most males and about half of the females making seasonal
movements, which can reach up to 260 km. Natal dispersal
averages 18 km but reaches up to 180 km (Alonso and Palacín
2009). In addition, when disturbed at their resting and feeding grounds, bustards often run or fly several hundred meters
to some kilometres away (Sastre, Ponce, Palacín, Martín, &
Alonso 2009). Thus, the potential of the species to disperse
seeds over long distances is evident, but as yet unexplored.
In our study site, about 200–250 bustards are resident and
breed at the zone, but about 1500 individuals, particularly
females, stay there during the winter (November to February; Corbacho et al. 2005), which coincides with the olive
ripening season.
Methods
To assess the potential of bustards as dispersers of domestic
olives, we collected their seeds during the end of two nonconsecutive ripening seasons (i.e., from January to February)
in 2007 and 2011, respectively. During the 2007 season, we
collected olive drupes and bustard faeces in and around three
orchards (separated by 1.5–6.0 km) and used those samples
for our seed sowing experiment (see below). In the 2011 season, we collected bustard faeces in two of the three orchards
and these samples were used to estimate the following
metrics: (i) the proportion of faeces with olive stones, (ii)
the number of seeds per faecal sample, and (iii) the percentage of seeds damaged after gastro-intestinal passage. In
addition, we measured and compared the size of bustarddefecated and hand-depulped seeds collected in two target
orchards.
The effect of bustard-ingestion on seedling emergence was
evaluated through a common garden seed sowing experiment.
To separate the effect of pulp removal from that of seed scarification on the percentage and speed of seedling emergence
and survival (Samuels & Levey 2005), we compared the fate
of bustard-ingested (n = 250), hand-depulped (n = 175), and
control seeds (i.e., whole ripe drupes with the pulp attached;
n = 175) collected in the same tree olive orchards. Ripe olive
fruits were collected from the ground under a minimum of
five trees per orchard. A fraction of such drupes was depulped
to obtain clean seeds, while the remaining fraction was used
as “control” seeds in the sowing experiment. In March 2007,
seeds were shallowly (∼5 mm depth) covered with in situ
soil within open-bottomed plastic pots (18 cm in diameter)
set in open ground. Pots (10, 7 and 7 for bustard-ingested,
hand-depulped, and control seeds, respectively) were buried
about 14 cm, with the rim remaining 2 cm above the surface.
In each pot, 25 seeds of a particular treatment were sowed.
To avoid removal by vertebrate seed predators (e.g., rodents;
Alcántara, Rey, Sánchez-Lafuente, & Valera 2000), we protected the sowings with wire cages. We monitored monthly
seedling emergence and survival from the sowing to February
2011.
To evaluate whether olive seed dispersal by bustards lead
to some seedling establishment within suitable habitats in
our study area (i.e., non-plowed patches), we rigorously
surveyed (in September of 2011) 19 unplowed patches of
variable size within the plowed matrix of cultivated lands.
Most of them (16) were small (10–15 m2 ) and corresponded
to the area beneath Quercus ilex and Pinus pinea adult
trees scattered throughout the study site (see Appendix A).
The remaining surveyed patches are two hedgerows (∼40
and 50 m2 , respectively) and an area (∼4000 m2 ) temporally
waterlogged during winter storms. In addition, we surveyed
four linear transects (211, 304, 621, and 716 m) along olive
cultivation edges that appeared to be seldom plowed.
Data on seed size were analyzed fitting generalized linear mixed models using Glimmix procedure (SAS 2008).
Because a preliminary mixed model for the percentage of
seedling emergence did not converge, such data were analyzed by fitting a generalized model using Genmod procedure
(SAS 2008), with pot as the experimental unit. For the
response variables seed size (length and width) and proportion (seedling emergence), we specified in the models
the appropriate error (normal and binomial, respectively)
and the canonical link function (SAS 2008). In the case
of seed size, the source orchard and the block (i.e., faecal
sample and the olive tree for bustard-ingested and control
seeds, respectively) nested within orchard were included in
the mixed models as random factors and thus their potential
(A)
14
12
Emergence (%)
effects controlled for. To evaluate the effect of seed treatment on seedling survivorship, we used failure-time analyses
by fitting Cox proportional hazard regression models (e.g.,
Fedriani & Delibes 2011). The response variable was the
number of months between seedling emergence and death.
The effect of experimental block was accounted for by
including it in the models as a “frailty” (random) term.
The significance of seed treatment was evaluated following
Therneau and Grambsch (2000).
10
8
6
4
2
0
0
Results
Frequency of occurrence of olive seeds in
bustard faeces and percentage of harmed seeds
Bustard
Hand-depulped
Control
(B)
Emergence
Survival
As a whole, 30.0% of bustard faeces (n = 167) included
olives stones, ranging from 18.1% (n = 72) to 38.9% (n = 95)
in the two orchards sampled in 2011. The average number
of complete stones per dropping that contained olive seeds
was 4.96 ± 0.51 (mean ± SE; n = 46), ranging from 1 to 13,
with the mode in 2–3 seeds per faecal sample. All faeces
were collected on plowed lands (mainly olive orchards and
their borders) where olive seeds potentially could germinate.
Moreover, our field observations indicated that most other
habitats used by bustards (abandoned fields, orchard margins,
etc.) were also suitable for seedling emergence (see Sapling
Survey below).
In a sample of 229 seeds from 47 faeces, only four seeds
(i.e. 1.75%) were broken. Defecated seeds were slightly
shorter (13.70 ± 0.15) and narrower (8.68 ± 0.06; in both
cases n = 228) than hand-depulped ones (14.29 ± 0.18 and
8.81 ± 0.05, respectively; n = 161). Those differences were
either significant (F1, 342 = 6.18, P = 0.013) or marginally
significant (F1, 342 = 3.39, P = 0.067), respectively. These
results suggest that bustards tend to feed on the smaller olive
seeds and/or that seeds are strongly scarified during passage
through bustard guts.
Seedling emergence and survival
Overall, only 28 seedlings (4.7% out of 600 sowed seeds)
emerged. Seed treatment had a significant (Genmod Procedure, F2, 21 = 5.08, P = 0.016) effect on the percentage of
seedling emergence (Fig. 1A), being 8.8%, 3.4% and 0.0% for
bustard-ingested, hand-depulped, and control seeds, respectively. In pair-wise comparisons, differences were significant
between bustard-ingested and control seeds (Genmod Procedure, F1,15 = 11.10, P = 0.005) and non significant between
bustard-ingested and hand-depulped seeds (Genmod Procedure, F1,15 = 1.51, P = 0.238). The initiation of seedling
emergence was delayed. Once initiated, however, emergence
took place in a rather synchronized fashion (Fig. 1B), at least
at the level of temporal resolution employed (i.e., a month).
The first seedling emerged from a bustard defecated seed in
Seedling fate (%)
100
80
60
Hand-depulped
Bustard-ingested
40
20
0
Fig. 1. (A) Mean percentage (±SE) of emergence of olive (domesticated Olea europaea) seeds ingested by bustards, hand-depulped,
and untreated controls. (B) Cumulative percentage of emergence
and survival for seedlings from bustard-ingested and hand-depulped
olive seeds. Seedling emergence started in February 2008, eleven
months after seed sowing. Number of seedlings were 22 and 6 for
bustard-ingested and hand-depulped seeds, respectively. Note that
no seedling emerged from control seeds.
February 2008, eleven months after sowing. The remaining
seedlings sprouted in March 2008, just one year after sowing. No seedlings emerged in the subsequent 14 months of
monitoring.
Most seedling mortality occurred shortly after emergence,
apparently due to desiccation. Only one seedling (from a
hand-depulped seed) survived the harsh summer drought of
2008 (and was still alive in February 2011). Our Cox regression analysis indicated that the estimated relative risk of
death for seedlings emerged from hand-depulped seeds was
0.35-fold that for seedlings from bustard-ingested seeds, and
the difference was significant (χ2 = 4.20, df = 1, P = 0.040).
When we made a similar analysis excluding the only seedling
alive at the end of the study, the relative risk of death for
seedlings emerged from hand-depulped seeds was still lower
(0.50-fold) than for seedlings from bustard-ingested seeds,
although the difference was not significant (P = 0.157) probably due to small sample sizes.
Sapling survey
Overall we found 19 saplings, distributed in 31.6% of surveyed patches (n = 19). Five samplings were small (<5 cm
height), ten were of intermediate size (>5 cm and < 1.5 m
height), and four were large (>2 m height; see Appendix A).
Mean distance from olive saplings to nearest olive orchard
border was 218.5 ± 106.2 m (mean ± SE) and ranged from
10 to 2100 m (Appendix A). No sapling was found in the
four linear transects along olive cultivation edges.
Discussion
Mutualistic interactions between endozoochore fleshyfruited plants and their vertebrate dispersers basically consist
of the exchange of food for movement for plant propagules
(Herrera 2002). In this sense, our results suggest that bustards act as legitimate seed dispersers (sensu Schupp et al.,
2010) of olive trees. In this apparently genuine mutualistic relationship, the bird gains from the abundant and very
nutritious (40–66% of dry mass are lipids; Rey 2011) olive
fruits, while the plant could find in the bustard one of very
few bird species able to swallow their large drupes and disperse the seeds over long distances (another candidate bird
could be the common crane, Grus grus, but its use of olive
orchards is very infrequent). In fact, olive fruits in our study
area have a width exceeding the gape size of most bird species
in Mediterranean Spain (Herrera 1984). Such enlarged fruit
size frequently shifts the functional role of small birds from
seed dispersers to pulp predators (Rey et al. 1997). Indeed,
the relatively small size of bustard-ingested seeds suggested
that these birds tend to feed on the smaller olive drupes (e.g.,
Rey et al. 1997), though it could also relate to strong erosion of seed during passage through the bustard gut (e.g.,
Traveset et al. 2007; Fedriani & Delibes 2009). Nonetheless,
large-sized bustards are able to consume daily great numbers
of olive drupes of variable sizes, which are ingested whole
and then dispersed in small (1–13 seeds) “packages” (see
Appendix A).
However, from the seed perspective, simply being moved
is not sufficient because not all movement is the same. Thus,
if bustards move many olive seeds but destroy almost all of
them, or deposit them in such high densities that nearly all
die, or carry them to an inappropriate habitat, etc., then this
would be not much of a mutualism (Schupp et al., 2010). We
have shown that most seeds pass unharmed through bustard
guts and that emergence success of such seeds is higher than
for both hand-depulped and control seeds. This suggests that
both pulp removal and scarification contributed to the emergence enhancement of bustard-ingested seeds (Samuels &
Levey 2005). However, scarification did not have an effect
on the speed of seedling emergence (Fig. 1B), but lack of
seedlings from control seeds prevents further inferences. The
low survival of our experimental seedlings is not surprising,
as seedlings are frequently unable to survive in open
microhabitats in the harsh summer droughts typical of
Mediterranean habitats (Pugnaire & Valladares 2007).
Nonetheless, in some of the sampled non-plowed patches
within our study area, we have found several olive saplings
of different ages. Although we cannot assert that all these
saplings came from bustard dispersed olive seeds, every
evidence gathered during our study strongly suggest that
bustards are the major local legitimate dispersers. Further
research is certainly needed to evaluate, for example, the
spatial variation (e.g., microhabitat) in the effect of bustard
ingestion and dispersal on the establishment of domestic olive
seedlings.
Our study documents how intensive agriculture can act as
a matchmaker of the odd “marriage” between a former forest
tree and a large steppe bird. The great bustard requires very
open grounds to live; Morales and Martín (2002) pointed out
that for bustards “a clear view over 1 km or more on at least
three sides is apparently essential, as well as uninterrupted
mobility in all directions on ground”. Thus, the species does
not occupy the Mediterranean forests where wild olive trees
are present. The plantation design of commercial olive trees
in grids 10 m × 10 m or more, and the removal of vegetation (through the use of herbicides and plowing) around and
under the trees, makes these orchards resemble wooded open
steppes that bustards select as feeding grounds. However,
these humanized habitats have some constraints at the local
and landscape levels. Locally, bustards frequently use only
the periphery of olive orchards and, thus, they probably need
a patchy landscape where olive orchards are not the dominant
element. Also, bustards occupy plains and gently undulating
landscapes, but cannot use olive groves on mountain hillsides.
Small birds cannot disperse domestic olive seeds because
centuries of artificial selection have enlarged olive fruit size,
preventing small birds from swallowing them. In contrast,
large drupe size and high lipid content have favored largesized bustards acting apparently as effective dispersers (sensu
Schupp et al., 2010). On the other hand, artificial selection
could have favored also the earlier fruit fall, which should
be advantageous for ground foragers (like the bustard) rather
than the usual consumers of wild olive fruits (many small
passerine birds), which feed mainly in the tree crown.
Interestingly, however, the bustard-olive tree mutualism
appears unstable in the long term, since a hypothetical reforestation of abandoned arable lands by olive trees in synergy
with other trees (e.g., Quercus ilex), shrubs (e.g., Pistacia
lentiscus), and tall weeds (Gramineae, Umbelliferae) would
exclude the bustards from such habitats. The interaction
between olive trees and bustards could be labeled as an opportunistic “pseudo-mutualism”. So, agricultural practices are
not only the matchmakers, but also the guarantors of this
bustard-olive tree interaction, because the annual plow up of
fields removes practically all emerged olive seedlings (except
those underneath some natural trees) as well as any other
plant colonizer. For the same reason, agricultural practices
could break this artificial mutualism, at least into two opposed
directions: (1) by intensifying the exploitation, as currently
happens, and (2) by diversifying olive orchards, to enhance
biodiversity. The current local trend is to promote the irrigation of olive orchards, which allows a higher olive tree
density and, thus, prevents bustard access to such orchards.
A suitable alternative to agricultural intensification should be
the promotion of multi-species hedgerows, copses and stream
vegetation beds in olive orchards to enhance the biodiversity
of frugivorous birds, as recently suggested by Rey (2011).
Although this would remove bustards from the orchards, it
would increase their role as reservoir and feeding areas for
many other species.
Our observations can be generalized to other areas, as
the use of olive tree orchards by the great bustard has been
described in other parts of Spain, such as Castilla-La Mancha (López-Jamar et al. 2010). Also, olive drupes have been
recorded previously as food of great bustards near our study
area (Suárez-Caballero 2002, found drupes in 9 of 22 bustard
stomachs), in Andalucía (Redondo & Tortosa 1994), and in
southern Portugal (Rocha, Marques, & Moreira 2005).
To investigate the effectiveness of birds and other dispersers in enhancing seedling emergence and establishment
of domestic olive seedlings is paramount for the study
of the invasion ecology and the control and management of plant invaders in these humanized landscapes.
Given the rural depopulation trend and the measures
promoting environmentally heterogeneous farming by
the Common Agricultural Policy (e.g. by leaving field
boundaries uncultivated and planting trees and hedges; see
http://ec.europa.eu/agriculture/publi/capexplained/cap en.pdf),
it should be possible for many marginal agricultural areas to
be reforested by seeds dispersed by animals that use open
lands (Thompson 2005). In this scenario, olive seed dispersal
by bustards would assist the colonization of abandoned
lands. Additionally, cultivated olive trees escaping from
commercial orchards are becoming a problematic invader
weed in several Mediterranean-climate countries all around
the World (e.g. California, Hawaii, South Africa, Australia;
see revisions in Spennemann & Allen 2000a,b). Thus,
understanding the effectiveness of seed dispersal in these
situations is important for being able to predict both wood
regeneration following land abandonment and the threat of
olive invasion into exotic habitats.
Acknowledgements
We thank Pedro J. Rey, Miguel Delibes-Mateos, Geno
Schupp, and two anonymous reviewers for helpful comments
on an earlier version of the manuscript. We appreciate Ramón Perea and Encarni Rico field assistance. The
Spanish Ministerio de Medio Ambiente (National Park
Service, grant 070/2009) and Ministerio de Educación y
Ciencia (CGL2007-63488/BOS and CGL2010-21926/BOS)
supported this study.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in the online version, at
doi:10.1016/j.baae.2011.11.003.
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