Download Significance and extent of secondary seed dispersal by predatory

Journal of Ecology 2012, 100, 416–427
doi: 10.1111/j.1365-2745.2011.01924.x
Significance and extent of secondary seed dispersal
by predatory birds on oceanic islands: the case of the
Canary archipelago
David P. Padilla1,2*, Aarón González-Castro1 and Manuel Nogales1
1
Island Ecology and Evolution Research Group (IPNA-CSIC), C ⁄ Astrofı´sico Francisco Sánchez 3, 38206 La Laguna,
Tenerife, Canary Islands, Spain; and 2School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, UK
Summary
1. Secondary seed dispersal is a multistep process with two or more phases, which involve different
dispersers that usually extend the distance from the seed’s parent plant. This ecological process has
been recorded in some subtropical oceanic islands, where predatory birds commonly consume
frugivorous lizards and disperse seeds already consumed by the lizards.
2. We evaluated the overall importance of this type of secondary dispersal in the Canary Islands,
the only place worldwide where it has been studied in depth. From an examination of all the islands
and their suitable habitats, we found seeds from 78 plant species inside 2098 shrike pellets and 5304
kestrel pellets. A greater number of species were secondarily dispersed by kestrels (76; 97%) than by
shrikes (26; 34%).
3. Forty-four (56%) of the total species detected in pellets were identified at the species level,
comprising 73% native and 27% introduced species. Seventy per cent of these identified species
were fleshy fruit-bearing plants and 84% of the interactions took place in open habitats, close to
coastal areas.
4. Germination experiments showed that seeds of at least 32 plant species were viable after being
removed from the bird pellets. A similar pattern of seed germination was detected for seeds from
the droppings of lizards and pellets of shrikes, showing both to be effective dispersers. However, the
seeds dispersed by kestrels had different levels of success depending on the number of gut passages
experienced. Seeds that had undergone double gut treatment (lizard and secondary ingestion by
kestrel) had reduced germination rates of many small- and medium-sized seeds compared with seeds
ingested by lizards and discarded inside the lizard guts by kestrels.
5. We also studied the relationship between body length and gape width of lizards in order to assess
limitations on the sizes and quantities of seeds available for secondary dispersal. Kestrels can
disperse a greater number and variety of seeds because they predate larger lizards that potentially
carry greater seed loads.
6. Synthesis. The current results show how these non-standard long-distance dispersal events
produced by predatory birds can be considered as a regular and generalized process on all islands of
the Canary archipelago.
Key-words: Canary Islands, endozoochory, frugivorous lizards, long-distance seed dispersal,
mutualistic interactions, predatory birds, seed germination effectiveness
Introduction
Animal dispersers play a fundamental role in the regeneration
of natural communities and are crucial for maintaining the
structure and diversity of ecosystems (Herrera & Pellmyr 2002;
Dennis et al. 2007). This could involve a single dispersal vector
(i.e. haplochory) or could be a multi-step process (secondary
*Correspondence author. E-mail: [email protected]
seed dispersal), comprising two or more phases. Each of these
phases can offer different benefits to plants, and the same set of
dispersers can effectively disseminate the seeds of multiple
plant species (Vander Wall & Longland 2004). Such mutualistic interactions may produce long-distance dispersal events
(hereafter LDD sensu Nathan 2006). These events play a major
function in determining large-scale processes such as the colonization of unoccupied habitats or islands, population spread,
and the flow of individuals between populations to maintain
2011 The Authors. Journal of Ecology 2011 British Ecological Society
Seed dispersal by predatory birds in the Canaries 417
genetic connectivity or facilitate species coexistence (Nathan
2006; Nathan et al. 2008). In general, LDD is stochastic,
highly unpredictable and difficult to study in time and space
(Greene & Johnson 1995; Higgins & Richardson 1999; Clark,
Lewis & Horvath 2001; Nathan 2006). However, some recent
studies have successfully documented the frequency and distance of these events using models (Nathan et al. 2002; Nathan
& Katul 2005; Levey, Tewksbury & Bolker 2008) or DNAbased genotyping (Jordano et al. 2007). Furthermore, some
ecological studies on secondary seed dispersal have provided
the basis to consider that some processes previously considered
as stochastic may, in fact, not be (Nogales et al. 2007). These
authors comment that some complex ecological interactions
are difficult to study and understand, but they occur regularly
in space and time and seem to be important generalized LDD
events.
Secondary seed dispersal often facilitates a first phase in
which seeds escape from density-dependent seed and seedling
mortality near the parent plant, and a second phase, frequently
characterized by the movement of seeds, which then become
established in favourable microhabitats (Vander Wall & Longland 2004). Secondary seed dispersal systems are widely variable because of the diverse potential combinations of dispersal
agents (Nogales et al. 2007). They could include abiotic (e.g.
wind, water or ballistic mechanisms) and biotic factors such as
scatter-hoarding vertebrates (Vander Wall 2002; Vander Wall,
Kuhn & Gworek 2005) or seed transport by invertebrates such
as ants or dung beetles (Estrada & Coates-Estrada 1991; Levey
& Byrne 1993; Espadaler & Gómez 1996; Andresen 2001; Pizo,
Guimarães & Oliveira 2005; Christianini & Oliveira 2010).
Seed dispersal systems in which vertebrate frugivores participate are often composed of only one phase and therefore one
digestion event (see Ridley 1930; Van der Pijl 1982). However,
this process can become more complex if a second vertebrate
disperser participates through predation on a legitimate frugivore (generally a bird or a lizard) carrying seeds inside its gut.
Although this phenomenon has generally been described
superficially (Grant et al. 1975; Damstra 1986; Hall 1987;
Dean & Milton 1988), it has been studied from an ecological
perspective in some environments in the Canary Islands
(Nogales, Delgado & Medina 1998; Nogales et al. 2002, 2007).
In this archipelago, frugivorous lizards of the genus Gallotia
reach high densities and are often captured by two predatory
birds: Lanius meridionalis Temminck (Southern Grey Shrike)
and Falco tinnunculus L. (Eurasian Kestrel). Therefore, secondary seed dispersal occurs and in this case, involves at least
three native fleshy-fruited plant species with different effects
on viability and germination, depending on the size and hardness of seeds (Nogales et al. 2007). In a recent study, Padilla &
Nogales (2009) described how the stereotyped behaviour of
kestrels during the consumption lizards changes the concept of
kestrels as an illegitimate seed disperser. In particular, they
documented that 89% of the seeds carried inside the lizards
prior to predation were not consumed by kestrels because they
discarded the lizards’ digestive tracts; thus, most seeds ingested
by lizards receive only this gut treatment. Because most seeds
were not affected by kestrel gut treatment, the effectiveness of
their dispersal was dependent on the effect of lizards’ guts. In
addition, the kestrel is distributed on all islands and main islets
of the Canaries, while the shrike is only present on the central
and eastern islands (Tenerife, Gran Canaria, Lanzarote and
Fuerteventura) (Martı́n & Lorenzo 2001). This ecological and
biogeographical scenario is ideal to perform a study to evaluate
the role of these predatory birds as secondary seed dispersers
over the entire Canary archipelago. To our knowledge, this
archipelago is where this particular ecological dispersal
process, involving two vertebrates (lizards + shrikes or lizards + kestrels), reaches its greatest extent worldwide.
The main aims of this study are to evaluate (i) whether these
predatory birds act as generalized secondary dispersal vectors
in the Canaries by documenting the wide variety of plant
species involved in this multi-step ecological process, (ii) the
biogeographical range of the plant species implicated, (iii) the
inter-island variation of the secondary dispersal process in relation to the diversity of plant species on each island, (iv) the
habitat types in which this process occurs, (v) the effectiveness
(sensu Schupp 1993; Schupp, Jordano & Gómez 2010) of dispersal by evaluating seed damage and other factors affecting
germination caused by the different dispersers, and (vi) the
potential limit of seeds secondarily dispersed related to lizard
sizes captured by the two predatory birds based on lizard gape
width and seed diameter.
Considering that Canary lizards (genus Gallotia) are seed
dispersers of at least 50 fleshy-fruited plant species (Valido &
Nogales 1994; Valido 1999; Valido, Nogales & Medina 2003;
Rodrı́guez et al. 2008) and the fact that both shrikes and kestrels preyed intensively on these lacertids, we expect that they
could secondarily disperse the seeds of a much greater number
of plant species in the archipelago than presently known.
Moreover, taking into account the larger body mass of kestrels, which allows them to catch larger lizards that potentially
carry a greater seed load, we hypothesized that kestrels will disperse a greater number of seeds and a wider range of plant species because most fruit sizes do not exceed the gape limit of
these lizards. Lastly, most studies on secondary seed dispersal
have focused on one or two plant species (see Vander Wall &
Longland 2004 and references therein), while this study examines secondary dispersal at the community level.
Material and methods
THE STUDY AREA
The Canary Islands are a volcanic archipelago located about 100 km
from the northwest coast of Africa, consisting of seven main islands
and several islets (Fig. 1), ranging in height from Tenerife (3718 m
a.s.l.) to Lanzarote (671 m a.s.l.). From a geological perspective,
there is an age progression from east to west, with Fuerteventura
being the oldest (c. 22 mya) and El Hierro the youngest (1.2 mya)
(Carracedo & Day 2002). Tenerife is the largest island (2036 km2),
while the smallest is El Hierro (278 km2). The climate in the Canaries
varies according to altitude and orientation. Mean temperature and
annual precipitation ranges from c. 21 C and 100–300 mm in coastal
zones, to c. 9 C and 500–800 mm at higher altitudes (Marzol 2000).
Xerophytic shrubs (coastal zone) occur in the lowlands of all the
2011 The Authors. Journal of Ecology 2011 British Ecological Society, Journal of Ecology, 100, 416–427
418 D. P. Padilla, A. González-Castro & M. Nogales
Canary Islands
Lanzarote
Tenerife
La Palma
Fuerteventura
La Gomera
El Hierro
Gran Canaria
50 km
N
Fig. 1. Map of the Canary Islands showing the localities where the fieldwork was carried out. Circles correspond to kestrel localities, stars to
those of shrikes and triangles to where the two predatory birds were in sympatry.
islands and are characterized by species of the genus Euphorbia
(Euphorbiaceae). The central and western islands also have highly
structured forest zones distributed as a function of altitude and orientation, with a type of Mediterranean forest called thermophilous
woodland, located at 300–550 m a.s.l., composed primarily of
Dracaena draco L. (Agavaceae), Phoenix canariensis Chabaud
(Arecaceae), and Juniperus turbinata Guss. (Cupressaceae). On northern slopes (at 550–1100 m a.s.l.), evergreen laurel forest is the most
humid habitat, consisting of about 20 tree species, several of them
endemic. Some of the most common species are Laurus azorica Seub.
and Persea indica (L.) C. K. Spreng. (Lauraceae), Myrica faya Aiton
(Myricaceae) and Erica arborea L. (Ericaceae). Above there is a
monospecific pine forest (1100–2000 m a.s.l.) of the endemic Pinus
canariensis Chr. Sm. ex DC. (Pinaceae) on the higher islands and
finally, the high mountain zone is characterized by sparse leguminous
shrubs such as Spartocytisus supranubius (L. f.) Christ ex G. Kunkel
and Adenocarpus viscosus (Aiton) DC. (Fabaceae). This last habitat
harbours a great component of endemic plants.
FIELD METHODS
Fieldwork was carried out over four consecutive spring seasons
(2004–2007), when most fleshy-fruited plants produce their crops,
coinciding with the breeding period of both predatory birds. We sampled all the main xerophytic shrublands (coastal and high-mountain)
and thermophilous habitats in the seven Canary Islands. Most fleshyfruited plant species are present in these two habitats, coinciding with
the highest abundance of lizards and the two predatory birds. Pellets
from shrikes were sampled at 21 localities distributed among the
islands, while all kestrel pellets and lizard guts rejected by kestrels
were collected at 61 localities of the archipelago (Fig. 1). Perches and
nests were ideal places to collect pellets from shrikes and kestrels.
Each pellet was stored independently, and seeds were manually
extracted and counted. Status of seeds (damaged and undamaged)
was visually classified using a stereomicroscope (10· magnification).
The appearance of seeds along with lizard remains in the pellets of
both predatory birds was recorded, to confirm the secondary seed
dispersal.
The two predatory birds show different feeding behaviour during
the ingestion of lizards; the shrike often swallows them whole, while
the kestrel discards the digestive tracts before ingestion (Padilla &
Nogales 2009). However, both shrikes and kestrels are legitimate seed
dispersers because they both disperse viable seeds. As kestrels discard
lizard guts, most of the seeds contained in guts are not ingested by
them although they are secondarily dispersed. Because guts rejected
by kestrels rapidly disappear in the field within a few hours or at most
a day (D.P. Padilla, personal observation), the analysis of pellets was
basic to understanding the different interactions and plant species
involved in this secondary seed dispersal process in the whole of the
archipelago. Logically, the study of pellets underestimates the real
numbers of seeds dispersed by kestrels. Nevertheless, it is relatively
easy to infer the actual role of kestrels based on the captivity experiments of Padilla & Nogales (2009), showing that 89% of seeds remain
inside the lizard guts after kestrel predation. Thus, these seeds have
been secondarily dispersed, because they carry the lizards to their
perches to handle and eat. To evaluate the potential long-distance
seed dispersal effected by kestrels on transporting the lizards in their
claws, direct observations of these movements were made at four different localities of Tenerife, using a detailed GPS-supported map of
the study areas in order to reduce bias in the data. Furthermore, to
assess the effectiveness of this interaction between fleshy-fruited
seeds, lizards and kestrels, it is essential to know the effect of lizards
on the germination of these plant species. Therefore, lizard droppings
were routinely collected at the same time. Padilla & Nogales (2009)
confirmed that seeds contained in lizard guts germinated in a similar
proportion as those extracted from their droppings.
The potential effectiveness of the different interactions was evaluated by germination experiments (actually measured as seedling
emergence). Seeds from the different treatments: control plants
(depulped seeds directly collected from the plants), lizards (seeds
extracted from their droppings), and the two predatory birds (seeds
extracted from the shrike and kestrel pellets) were sown and grown
in a greenhouse for exactly six months each year (October–March;
2004–2007), coinciding with the rainfall period. A mean of 200
seeds were sown for most treatments, while in those cases where a
lesser number were recorded all the seeds were planted; each seed
2011 The Authors. Journal of Ecology 2011 British Ecological Society, Journal of Ecology, 100, 416–427
Seed dispersal by predatory birds in the Canaries 419
was sown 5 mm deep independently in a 4-cm2 pot, containing a
standard substrate (50% turf and 50% agricultural soil). This
experiment was carried out at Tagoro (Tenerife; 300 m a.s.l.) with
a night ⁄ day cycle similar to that found in the study areas. Pots
were watered every 2 days, and seedling emergence date was noted
when any seedling part emerged above the soil surface. Data were
recorded every five days.
To verify the influence of lizard length and gape width in the
secondary seed dispersal process, we captured a total of 39 Gallotia
galloti Oudart of different sizes. Morphological measurements
(snout-vent length and external distance between commissural
points – ‘gape-width’) were made on each lizard by the same person
with digital callipers. All the lizards were released unharmed in the
same place they were captured. The combination of these two
measurements allowed us to calculate a linear regression of lizard
body length vs. mouth size. Taking into account the mean and maximum lizard size captured by shrikes (74.0 and 127.4 mm) and kestrels
(94.0 and 165.3 mm) (Padilla, Marrero & Nogales 2007), together
with the equation of the linear regression, we estimated the gape
width of the lizards captured by both predatory birds, and
consequently the diameter limit of seed ⁄ fruit potentially dispersed
secondarily. For this purpose, we consulted our own data base
(IPNA-CSIC), in which we have information on fruit and seed traits
from most fleshy-fruited plants of the Canary Islands.
ANALYSIS
Association between the presence of seeds and lizard remains in
shrike and kestrel pellets was evaluated by Likelihood ratio tests
(G-tests). Number of seeds found in shrike and kestrel pellets was
tested by Mann–Whitney Z tests. Correlation between the number of
native fleshy-fruited plant species present on each island and the number of plant species secondarily dispersed on them was analysed using
Spearman’s rank correlation analysis. Numbers of plant species
secondarily dispersed among each habitat by shrikes and kestrels,
and seedling emergence of uningested (depulped seeds) and ingested
seeds, were compared using several Likelihood ratio tests. As we
carried out multiple independent significance tests, a Bonferroni
correction test was performed (0.05 ⁄ k) to avoid inflated Type I error
rates. The relationship of lizard snout-vent length vs. lizard gapewidth was assessed by Pearson’s correlation analysis. To calculate the
lizard gape-width from lizard snout-vent length, we used a linear
regression model to obtain the theoretical equation of the slope. All
data were analysed with the PASW Statistics software (v. 18.0, SPSS
Inc., Chicago, IL, USA).
plant species (Table 1). We did not record either shrikes or
kestrels feeding directly on fruits.
A total of 10 873 and 5546 seeds appeared in the analysis of
2098 pellets from shrikes and 5304 from kestrels (respectively),
over the entire archipelago (Table 2). A higher frequency of
seeds was found in shrike pellets compared to kestrel (Mann–
Whitney test, Z = )11.81, P < 0.001). However, as only
11% of those seeds primarily dispersed by lizards appeared in
kestrel pellets after predation upon lizards (Padilla & Nogales
2009), we included this correction factor to estimate the actual
number of seeds dispersed by kestrels. Thus, 44 872 seeds were
considered to be secondarily dispersed by kestrels in the
rejected lizard guts. This number of seeds is greater than the
number of seeds secondarily dispersed by shrikes (Z = )9.26,
P < 0.001).
Seeds belonged to 78 plant species; 26 species (34%)
appeared in the shrike pellets and 76 species (97%) in kestrel
pellets. Forty-four different types of seeds (56%) were identified to the species level (Table 1), 5 (6%) to genus level and 29
(37%) were unidentified. Of the 44 identified plant species, 32
were native (73%) and 12 introduced (27%); 14 of the natives
were endemics (32%).
The process of secondary seed dispersal by predatory birds
was clearly related with fleshy-fruited plant species; 68% of the
identified plant species produce fleshy fruits. A highly significant relationship was observed between the numbers of native
fleshy-fruited plant species distributed over the main seven
islands of the archipelago vs. the number of interactions
recorded (rs = 0.96, n = 7, P < 0.001). Those plants
involved in this ecological dispersal process are mainly distributed over the open habitats closest to coastal areas (84% of
these identified plants typically occur in xerophytic shrubland,
while 42% occur in thermophilous woodland). Moreover, a
similar pattern of interactions among the different habitats
was observed between the two predatory birds and the plant
species involved (G4 = 6.59, P = 0.15).
Movements of the two predatory birds were clearly different. Kestrels moved longer distances than shrikes (Kestrel:
506.4 ± 361.2 m; range: 75–1500 m; Shrike: 76.0 ± 49.9 m;
range: 10–250 m). Even when the kestrels transported the
lizards in their claws to handle in the perches, the movements
were notably greater (434.9 ± 329.8 m; range: 60.5–998.1;
n: 16 movements; n: 8 individuals).
Results
SEED DAMAGE AND SEEDLING EMERGENCE
SEEDS SECONDARILY DISPERSED, PLANT SPECIES
INVOLVED AND PREDATORY BIRD MOVEMENTS
Analysis of shrike and kestrel pellets in the Canary Islands confirmed the importance of lizards in the diet of these two predatory birds, with 56.8% and 65% of their pellets (respectively)
containing one or more lizards. Furthermore, a clear association was found between the presence of seeds and lizard prey
remnants in the pellets of shrikes and kestrels (G1 = 244.60,
P < 0.001; G1 = 586.91, P < 0.001, respectively). Thus,
it appears that both predatory birds dispersed seeds after
consuming lizards that had previously eaten fruits of different
In general, the external damage to seeds produced by the primary and secondary dispersers was negligible; only three cases
of significant damage were observed (two in shrikes and one in
lizards; 4.2%) out of 71 interactions studied (see Table 3).
Apparently nearly all seeds were deposited intact after interaction with both primary and secondary dispersers.
Seedling emergence events were recorded in 32 of the 44
identified plant species for at least one of the three different gut
treatments (Table 3). Secondary dispersal was analysed for the
12 plant species for which sample sizes were large enough (see
Table 4). Lizards produced an inconsistent germination effect
2011 The Authors. Journal of Ecology 2011 British Ecological Society, Journal of Ecology, 100, 416–427
420 D. P. Padilla, A. González-Castro & M. Nogales
Table 1. Seeds from different plant species found in droppings of shrikes and kestrels in the Canary Islands: L – Lanzarote, F – Fuerteventura,
C – Gran Canaria, T – Tenerife, G – La Gomera, H – El Hierro, and P – La Palma (islands where some interaction was recorded are indicated in
bold face). Nomenclature of taxa and biogeographic range were partially modified from Izquierdo et al. (2004). Biogeographic range: E –
Endemic, N – Native, and I – Introduced. Fruit type: F – Fleshy, and D – Dry. Habitats: XS – Xerophytic shrubs, TW – Thermophilous
woodland, LF – Laurel forest, PF – Pine forest, and HM – High-mountain shrubs (each plant species was assigned to its most characteristic
habitat). Predatory dispersers: S – Shrikes, and K – Kestrels
Canary Islands
Plant species
Family
L
F
C
T
G
P
H
Biogeogr.
range
Fruit type
Habitats
Predatory
dispersers
Acacia cyclops
Aizoon canariense
Asparagus arborescens
Asparagus nesiotes
Asparagus pastorianus
Asparagus plocamoides
Asparagus umbellatus
Atriplex semibaccata
Bencomia exstipulata
Bituminaria bituminosa
Bosea yervamora
Canarina canariensis
Cistus monspeliensis
Einadia nutans
Euphorbia balsamifera
Ficus carica
Heberdenia excelsa
Juniperus cedrus
Juniperus turbinata
Lantana camara
Launaea arborescens
Lycium intricatum
Lycopersicon esculentum
Mercurialis annua
Mesembryanthemun nodiflorum
Neochamaelea pulverulenta
Opuntia dillenii
Opuntia maxima
Patellifolia patellaris
Plocama pendula
Retama rhodorizoides
Rhamnus crenulata
Rubia fruticosa
Rubus ulmifolius
Rumex lunaria
Scilla haemorrhoidalis
Spartocytisus supranubius
Solanum nigrum
Tamus edulis
Teline stenopetala
Visnea mocanera
Vitis vinifera
Volutaria canariensis
Withania aristata
Mimosaceae
Aizoaceae
Convallariaceae
Convallariaceae
Convallariaceae
Convallariaceae
Convallariaceae
Polygonaceae
Rosaceae
Fabaceae
Amaranthaceae
Campanulaceae
Cistaceae
Chenopodiaceae
Euphorbiaceae
Moraceae
Myrsinaceae
Cupressaceae
Cupressaceae
Verbenaceae
Asteraceae
Solanaceae
Solanaceae
Euphorbiaceae
Aizoaceae
Cneoraceae
Cactaceae
Cactaceae
Chenopodiaceae
Rubiaceae
Fabaceae
Rhamnaceae
Rubiaceae
Rosaceae
Polygonaceae
Hyacinthaceae
Fabaceae
Solanaceae
Dioscoreaceae
Fabaceae
Theaceae
Vitaceae
Asteraceae
Solanaceae
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I
N
E
E
N
E
N
I
E
N
E
E
N
I
N
I
N
N
N
I
N
N
I
I
N
E
I
I
N
E
E
E
N
N
E
E
E
N
N
N
N
I
E
N
D
D
F
F
F
F
F
F
F
D
F
F
D
F
D
F
F
F
F
F
D
F
F
D
D
F
F
F
D
F
D
F
F
F
D
F
D
F
F
D
F
F
D
F
XS
XS
XS
XS
XS
TW
TW
XS
HM
TW
TW
LF
PF
TW
XS
TW
TW
HM
TW
XS
XS
XS
XS
XS
XS
XS
XS
TW
XS
XS
TW
TW
TW
LF
TW
XS
HM
TW
TW
TW
LF
TW
XS
TW
S
S–
S–
S–
S–
S–
K
S–
K
K
K
K
K
K
S
S–
K
K
K
K
S–
S–
K
S–
S–
K
S–
K
S–
S–
K
K
S–
K
K
K
S
S–
K
K
K
K
S–
K
pattern with respect to control seeds (a decrease for six plant
species, five were neutral and one case increased). A neutral
seed germination effect of shrikes vs. lizards was observed for
five plants, whereas an increase was recorded in one case.
When the effect of kestrels vs. lizards on germination was
compared, a significant decrease was recorded for nine plant
species, while a neutral outcome was found in three of them.
Lastly, inter-insular germination patterns in the context
of the Canary archipelago were evaluated in those plant
K
K
K
K
K
K
K
K
K
K
K
K
K
K
K
K
K
species in which a suitable data set of seeds was available
for each secondary disperser on the different islands
(n = 4: Atriplex semibaccata R. Br., Lycium intricatum,
Plocama pendula Aiton and Rubia fruticosa). A similar germination pattern was observed for most of the plant species
over the different islands (P > 0.05, in all cases), and a
higher germination value was only recorded for R. fruticosa
dispersed by kestrels on Gran Canaria (G6 = 43.94,
P < 0.01).
2011 The Authors. Journal of Ecology 2011 British Ecological Society, Journal of Ecology, 100, 416–427
Seed dispersal by predatory birds in the Canaries 421
Table 2. Number of seeds from the different plant species found in pellets from shrikes and kestrels in the Canary Islands
Shrikes
Plant species
Acacia cyclops
Aizoon canariense
Asparagus arborescens
Asparagus nesiotes
Asparagus pastorianus
Asparagus plocamoides*
Asparagus umbellatus
Atriplex semibaccata
Bencomia exstipulata
Bituminaria bituminosa
Bosea yervamora*
Canarina canariensis
Cistus monspeliensis
Einadia nutans
Euphorbia balsamifera
Ficus carica*
Heberdenia excelsa
Juniperus cedrus*
Juniperus turbinata*
Lantana camara
Launaea arborescens
Lycium intricatum*
Lycopersicon esculentum
Mercurialis annua*
Mesembryanthemun nodiflorum
Neochamaelea pulverulenta
Opuntia dillenii
Opuntia maxima*
Patellifolia patellaris
Plocama pendula
Retama rhodorizoides
Rhamnus crenulata*
Rubia fruticosa*
Rubus ulmifolius*
Rumex lunaria
Scilla haemorrhoidalis*
Spartocytisus supranubius
Solanum nigrum*
Tamus edulis
Teline stenopetala
Visnea mocanera
Vitis vinifera
Volutaria canariensis*
Withania aristata
Unidentified seeds*
Total
Number
of seeds
Kestrels
% of
seeds
% of pellets where
at least one seed
was recorded
8
0.073
0.047
1
115
1
1
0.009
1.057
0.009
0.009
0.047
2.14
0.047
0.047
154
1.416
1.19
2
223
0.018
2.050
0.095
1.00
1
6951
0.009
63.928
0.047
13.10
3
67
0.027
0.616
0.142
0.095
14
0.128
0.047
12
6
0.110
0.055
0.57
0.095
1182
10.870
5.14
1
5
0.009
0.045
0.047
0.047
2127
10 873
19.562
1.42
Number
of seeds
CF of
seeds
% of seeds after
CF calculations
% of pellets
where at least one
seed was recorded
35
2
17
283
16
138
0.630
0.035
0.307
0.094
0.037
0.263
17
2
427
2
6
4
69
6
1558
138
16
3455
16
49
32
558
49
12606
0.307
0.035
7.699
0.035
0.109
0.071
1.243
0.109
28.093
0.188
0.037
1.300
0.037
0.075
0.056
0.113
0.018
0.037
71
32
4
574
259
32
1.279
0.577
0.071
0.226
0.490
0.018
1
1
477
10
73
145
4
28
41
167
248
1
4
910
12
3
27
8
8
3859
81
591
1173
32
227
332
1351
2007
8
32
7363
97
24
218
0.017
0.017
8.600
0.180
1.317
2.614
0.505
0.739
3.010
4.472
0.017
0.071
16.408
0.216
0.053
0.485
0.018
0.018
1.809
0.056
0.188
0.339
0.056
0.417
0.417
1.659
0.641
0.018
0.037
5.297
0.037
0.056
0.207
404
20
1
1
3
22
6
685
5546
3269
162
8
8
24
178
49
5542
44 872
7.285
0.361
0.017
0.017
0.053
0.396
0.109
12.350
0.923
0.094
0.018
0.018
0.056
0.113
0.075
2.300
CF, correction factor for seeds dispersed by kestrels, taking into account the results obtained in the experiment in captivity (Padilla &
Nogales 2009).
*Plant species in which at least one seed appeared in the lizard digestive tracts rejected by kestrels.
INFLUENCE OF LIZARD BODY LENGTH AND GAPE
WIDTH IN SECONDARY SEED DISPERSAL
Lizard body-length (SVL) was highly correlated with
gape-width (n = 39 individuals, Pearson’s correlation:
rp = 0.90, P < 0.001; linear regression model: Y = )6.749
+ 0.211X; R2 = 0.82). Bearing in mind the mean body
size of lizards captured by the two secondary seed dispersers (74.0 and 94.0 mm for shrikes and kestrels, respectively), we expected that the diameter limitation of
seeds ⁄ fruits commonly dispersed by shrikes and kestrels
would be 8.9 and 13.1 mm, respectively. Furthermore, if
2011 The Authors. Journal of Ecology 2011 British Ecological Society, Journal of Ecology, 100, 416–427
422 D. P. Padilla, A. González-Castro & M. Nogales
Table 3. Seed effectiveness recorded in the different seed treatments of those plant species consumed and secondarily dispersed by the two
predatory birds (shrikes and kestrels) in the Canary Islands
% of undamaged seeds
Lizards
Plant species
Acacia cyclops
Aizoon canariense
Asparagus arborescens
Asparagus nesiotes
Asparagus pastorianus
Asparagus plocamoides
Asparagus umbellatus
Atriplex semibaccata
Bencomia exstipulata
Bituminaria bituminosa
Bosea yervamora
Canarina canariensis
Cistus monspeliensis
Einadia nutans
Euphorbia balsamifera
Ficus carica
Heberdenia excelsa
Juniperus cedrus
Juniperus turbinata
Lantana camara
Launaea arborescens
Lycium intricatum
Lycopersicon esculentum
Mercurialis annua
Mesembryanthemun nodiflorum
Neochamaelea pulverulenta
Opuntia dillenii
Opuntia maxima
Patellifolia patellaris
Plocama pendula
Retama rhodorizoides
Rhamnus crenulata
Rubia fruticosa
Rubus ulmifolius
Rumex lunaria
Scilla haemorrhoidalis
Spartocytisus supranubius
Solanum nigrum
Tamus edulis
Teline stenopetala
Visnea mocanera
Vitis vinifera
Volutaria canariensis
Withania aristata
56
Shrikes
100
100
100
100
100
100
98.71
100
99.6
92.7
98.2
100
45.16
100
99.02
100
100
96.2
16.66
100
86.7
98.3
94.0
99.57
100
100
100
98.0
100
100
95.4
% of seed germination
Kestrels
Control
Lizards
100
100
100
1.0
32.5
97.5
0.0
59.0
87.0
100
100
100
100
100
100
100
100
100
35.7
3.9
48.2
45.7
14.3
60.0
100
100
100
SS
68.2
23.2
0.0
SS
21.7
10.3
100
100
97.73
100
100
100
100
100
100
100
98.79
100
100
100
100
100
100
100
100
100
100
100
100
100
Shrikes
62.5
0.0
0.0*
89.0
0.0*
100
5.7
100
SS
100
54.1
61.5
47.5
8.0
36.6
29.3
0.0
28.6
38.2
14.3
49.1
47.8
0.0*
66.6
49.6
80.5
52.2
43.0
83.0
38.6
100.0
43.5
0.0
95.7
0.0*
0.0*
33.3
56.1
6.0
0.0*
85.8
75.0
Kestrels
0.0
0.0*
70.0
16.6
0.0*
8.1
0.0*
16.6
0.0
17.4
0.0
10.4
SS
0.0
0.0
0.0*
0.0*
4.2
10.0
3.0
6.9
25
13.3
5.7
12.3
5.0
100
25
4.1
11.1
0.0*
3.8
4.5
0.0
100
0.0*
0.0*
0.0
0.0
SS, sterilized seeds.
*Small sample size recorded (n < 5 seeds).
the maximum body size of the lizards captured by both
predators is considered (127.4 and 165.3 mm for shrikes
and kestrels, respectively), seeds 20.1 and 28.1 mm in
diameter could potentially be secondarily dispersed by
them. However, although a large diameter of seeds is theoretically dispersible by shrikes and kestrels, the largest
diameter detected in the field was clearly smaller (4.7 mm
for shrikes and 12.6 mm for kestrels).
Discussion
SECONDARY SEED DISPERSAL SYSTEMS BY
PREDATORY BIRDS
The results obtained for secondary seed dispersal on the seven
main islands of the Canaries give a clear idea of the great extent
and magnitude of this multi-step ecological process. Although
2011 The Authors. Journal of Ecology 2011 British Ecological Society, Journal of Ecology, 100, 416–427
Seed dispersal by predatory birds in the Canaries 423
Table 4. Statistical results of germination for the different seed
treatments (C – Control, L – Lizards, S – Shrikes and K – Kestrels)
involved in the secondary dispersal of 12 plant species in the Canary
Islands
Germination statistics
Plant species
G
d.f. P
Asparagus nesiotes
25.10 3
Asparagus plocamoides
13.07 2
Canarina canariensis
27.44 2
Heberdenia excelsa
112.51 2
Lycium intricatum
221.48 3
Opuntia dillenii
9.34 3
Plocama pendula
183.12 3
Rubia fruticosa
1118.33 3
Rubus ulmifolius
13.18 2
Scilla haemorrhoidalis
59.62 2
Tamus edulis
27.51 2
Withania aristata
23.49 2
<0.001
0.001
<0.001
<0.001
<0.001
0.025
<0.001
<0.001
0.001
<0.001
<0.001
<0.001
Differences
C>L=S=K
C>L=K; C=K
C=L>K
C>L>K
C>L=S>K
C=L=S=K
C=L=S=K
[((C=L)<S)>K]
C>L=K; C>K
C>L>K
(C<L)>K
(C=L)>K
in previous studies this dispersal system was only described for
three plant species on the island of Lanzarote (Nogales, Delgado & Medina 1998; Nogales et al. 2002, 2007), the current
results reflect that these non-standard LDD mechanisms
involving predatory birds could be considered to occur regularly and generally on all the islands of the archipelago.
Although other frugivorous birds in the Canary Islands such
as warblers, ravens and gulls can act as primary seed dispersers
(Nogales et al. 2005), secondary seed dispersal seems to be one
of the most important mechanisms in the archipelago because
of the high number of plant species involved and the long
distance that seeds could be transported. However, seeds of
many species are often dispersed by a combination of both
standard and non-standard dispersal mechanisms (Higgins,
Nathan & Cain 2003; Nathan et al. 2008).
Island food webs are simpler than those of mainland ecosystems and some species, such as lizards, can reach extremely
high densities (Rodda & Dean-Bradley 2002) as a consequence
of the lower predation and the absence of interspecific competitors on islands (MacArthur, Diamond & Karr 1972;
Olesen & Valido 2003; Valido & Olesen 2007). In the Canaries,
lizards in the genus Gallotia undergo the phenomenon of
density compensation, in which a few predatory bird species
(principally shrikes and kestrels) have a superabundance of
prey resources with lizards being their primary food source
(Padilla, Marrero & Nogales 2007; Padilla et al. 2009). This
abundance of lizards, together with the scarcity of arthropods
on islands, may force them to expand their trophic niche by
exploiting other available resources such as fleshy fruits (Olesen & Valido 2003). So, secondary seed dispersal by predatory
birds is clearly associated with fleshy-fruited plants because the
diet of the primary dispersers (the lizards) is mainly herbivorous, being composed of many fruits (more than 50 plant
species detected; Valido & Nogales 1994; Valido 1999; Valido,
Nogales & Medina 2003; Rodrı́guez et al. 2008).
The higher number of seeds recorded in the shrike pellets
compared with those of the kestrels is because shrikes swallow
the lizards whole (Padilla, Marrero & Nogales 2007); therefore, seeds are expelled from the shrike gizzard in pellets.
Kestrels, however, ingest only 11% of seeds, which later
appear inside their pellets, while the other 89% of seeds appear
inside the lizard guts rejected by the kestrel (Padilla & Nogales
2009). For that reason, when a correction factor was applied in
calculating the actual amount of seeds moved by kestrels, it
was substantially higher than that of shrikes.
Different behavioural patterns may influence the scale and
shape of the dispersal curve. There are some studies that have
demonstrated how incorporating spatially explicit information
on disperser behaviour (e.g. the southern cassowary Casuarius
casuarius L. or the spider monkey Ateles paniscus L.) can produce a significant impact on scale and shape of the dispersal
curve (Westcott et al. 2005; Russo, Portnoy & Augspurger
2006). The feeding behaviour pattern of kestrels in the Canaries reflects the scale on which data can be collected, rather than
the scale on which dispersal occurs. Also, the clearly greater
number of seeds and plant species dispersed by kestrels may be
related with the seed load and their wider distribution. Having
a larger body mass than shrikes, kestrels prey upon the largest
lizards, which have a higher seed dispersal capacity. Therefore,
the larger lizards may act as generalised vectors, transporting
seeds of a large variety of plants, consequently being secondarily dispersed by kestrels. Nathan et al. (2008) noted that larger
animals tend to promote LDD because of their wider home
ranges and greater mobility coupled with greater gut capacity
and longer seed retention times.
The biogeographic range of the 44 plants identified in the
pellets of the two predatory birds is varied and not only native
and endemic species (73%) were recorded but also introduced
ones (27%). If we consider that about 80 native species in the
Canaries produce fleshy fruits, this means that around 40% of
them were involved in secondary seed dispersal by predatory
birds. Furthermore, due to the fact that kestrels reject most
digestive tracts and that these decompose very rapidly, it is
probable that some other undetected plants are involved in this
complex ecological process. At least three plants included in
the IUCN Red List of Threatened Species (IUCN 2010) were
also detected, two of which are vulnerable (Bencomia exstipulata Svent. and Heberdenia excelsa (Aiton) Banks ex DC.) and
the other (Juniperus cedrus Webb & Berthel.) endangered. This
reflects how threatened plants, which are usually restricted to
small and fragmented areas, are involved in secondary seed
dispersal processes to colonize new zones or to connect isolated
patches. However, ecological mechanisms of dispersal do not
distinguish the geographical range of plants and they usually
rely on a wide variety of species, including those introduced
that can infiltrate native seed dispersal networks (Padrón et al.
2011). Although the dispersal of invasive plants by primary
dispersers has been previously described on islands (see review
of Traveset & Richardson 2006; López-Darias & Nogales
2008), their seeds are also present in these complex multi-step
LDD events, spreading their populations. Invasive plants
could affect the native plant community in many ways, not
only in terms of competition for soil and space, but also to
attract dispersers and the use of LDD mechanisms by native
2011 The Authors. Journal of Ecology 2011 British Ecological Society, Journal of Ecology, 100, 416–427
424 D. P. Padilla, A. González-Castro & M. Nogales
species (Trakhtenbrot et al. 2005; Buckley et al. 2006; Traveset
& Richardson 2006).
Most seeds secondarily dispersed were associated with the
two habitats closest to the coast (xerophytic shrub and
thermophilous woodland), and this is clearly related with the
abundance of fleshy-fruited plant species in those habitats. The
laurel forest is the other habitat with many fleshy-fruited
plants, but they are primarily dispersed by forest birds
(Arévalo, Delgado & Fernández-Palacios 2007). Moreover,
shrikes are totally absent from the latter habitat and kestrels
are only present at the laurel forest margins. Despite the
suitable environmental conditions of the high-mountain
shrubland for both predatory bird species, a low number of
seeds was found to be secondarily dispersed there, reflecting
the scarcity of fleshy-fruited plants in this habitat (n = 4
species). Kestrels and shrikes need open habitats for their
hunting strategies, avoiding dense vegetation (e.g. forests
and thickets). So open landscapes, such as grassland or arid
steppes offer favourable conditions for LDD, principally
because of the scarce obstacles to movements of seeds and
their vectors (Ozinga et al. 2004; Nathan et al. 2008).
It is not an easy task to evaluate whether seeds have been
dispersed in their habitats of origin, because some species show
an overlap in distribution. However, there are some plant
species that are unmistakeable indicators of each habitat, and
accordingly all their seeds moved by both predatory birds were
ejected in their original habitats. However, as kestrels habitually fly long distances (Nogales et al. 2007), seeds can easily be
moved over several km, mainly those contained in pellets, but
also those seeds that remain inside the lizards after capture and
transport to a perch, where the guts containing seeds are discarded. In this respect, Nogales, Hernández & Valdés (1999)
commented that the efficient dispersers on high-altitude oceanic islands are mainly those that move seeds within the original habitats where fruits were ingested. Therefore, this is an
important condition for the survival and future recruitment of
these dispersed plants.
THE EFFECTIVENESS COMPONENTS
Seeds found in lizard droppings and lizard digestive tracts,
rejected by kestrels, undergo a single digestion. However, seeds
inside lizards captured and swallowed by shrikes, and those
scant seeds indirectly ingested by kestrels, have a double gut
digestion process. Despite these different gut treatments, the
external seed damage because of the digestive tracts of the
primary and secondary dispersers was insignificant for practically all plant species. This pattern coincides with previous
studies carried out on native dispersers in the Canaries, both
lizards and birds, in which seed damage was apparently low
(Nogales, Hernández & Valdés 1999; Nogales et al. 2005,
2007; López-Darias & Nogales 2008), and also in different
native vertebrates on other islands (e.g. Rick & Bowman 1961;
Traveset 1995).
Of the 78 different plant species found in the pellets of both
predatory birds, at least 32 species were shown to be effectively
dispersed, as evaluated by seedling emergence experiments.
This again gives us a good idea of the magnitude of this secondary seed dispersal process in the Canary Islands. It is clear
that the second phase of this dispersal is critical for the movement of seeds to discrete and predictable microsites, where the
probability of seedling establishment is much higher (Vander
Wall & Longland 2004) and has clear implications in LDD
events. Nogales et al. (2007) demonstrated how shrikes and
kestrels deposited most seeds in suitable microsites where at
least three plant species were present, which suggests that the
origin of those plants was probably associated with the secondary seed dispersal process.
The effects of lizards on germination patterns in comparison
with control seeds was rather uncertain, decreasing seed germinability in half species and being neutral in the other half.
However, it was clear that in one species (Tamus edulis Lowe),
passage through a lizard gut clearly enhanced germination
with respect to control seeds. Although saurochory is considered a characteristic ecological process on islands (Olesen &
Valido 2003), few experiments have been conducted and generally inconsistent germination patterns found (Traveset 1998).
Therefore, in some plants, seed ingestion by reptiles promotes
germination (Rick & Bowman 1961; Cobo & Andreu 1988;
Valido & Nogales 1994), while in others it does not (Whitaker
1987; Traveset 1990; Valido & Nogales 1994).
The germination of seeds ingested by shrikes after predation
upon frugivorous lizards was neutral for most plant species
but was enhanced in one of them (R. fruticosa Aiton). Probably, this last effect is related to the fact that shrikes reduce the
lizard gut passage time, and therefore the gut effect, when they
prey upon them, consequently enhancing germination percentage (Nogales, Delgado & Medina 1998). The important role of
this unspecialized passerine predator as a legitimate disperser
is undoubtedly confirmed, which coincides with the previous
data obtained by Nogales et al. (2007).
In kestrels, the fate of seeds is more complex because they
can remain inside the lizards’ guts after being preyed on by this
raptor, or ejected in kestrel pellets because of their indirect
ingestion. However, the likelihood that a seed follows the first
mentioned fate is practically ten times more than being regurgitated in a kestrel pellet (Padilla & Nogales 2009). This is especially important when seeds are ejected via pellets, because a
significant reduction in germination was found in most species,
coinciding with previous findings by Nogales, Delgado &
Medina (1998) and Nogales et al. (2002, 2007). Therefore,
enzymatic action of this diurnal raptor, which is stronger than
in many other types of birds (Duke, Evanson & Jegers 1976;
Stuart & Stuart 1994), probably has a negative influence on
seed survival. Furthermore, another factor that influences seed
fate is gut passage time (Schupp 1993), which in the case of kestrels (12–23.5 h; Balgooyen 1971; Yalden & Yalden 1985) is
much longer than in shrikes (45–55 min; Olsson 1985). However, in some plant species where seeds are characterized by
hard seed coats [e.g. Asparagus spp. and the introduced Opuntia dillenii (Ker-Gawl.) Haw.], germination was still high. It is
interesting that these hard seeds that maintain their germination capacity intact, and are ejected via kestrel pellets, have an
important chance to undergo an LDD process and be dis-
2011 The Authors. Journal of Ecology 2011 British Ecological Society, Journal of Ecology, 100, 416–427
Seed dispersal by predatory birds in the Canaries 425
persed further (Nogales et al. 2007) than those seeds left inside
the digestive tracts of lizards.
THE ECOMORPHOLOGICAL THRESHOLD OF
SECONDARY SEED DISPERSAL BY VERTEBRATES
Fruit diameter is one of the most important limiting factors for
frugivores to swallow fruits whole (Jordano 2000). Large frugivores can ingest a wide range of fruit sizes, while small fruit
consumers, owing to their ecomorphological restrictions of
gape width, are not able to pick or completely swallow certain
sizes of fruits (Wheelwright 1985, 1993). However, if frugivorous vertebrates can process them (e.g. by squashing) in the
mouth, especially those of fleshy consistency, reducing fruit
diameter, they will be able to swallow them completely (Levey
1987). This is probably happening with most fleshy fruits in the
two lowland habitats of the Canaries, because no huge ecomorphological restriction was recorded in the gape width of
those lizards predated on by shrikes and kestrels. The lizards’
gape width permits them to swallow most fruits present in
these habitats. However, most fruits appearing in shrike pellets
are smaller than those found in those of kestrels. Thus, it
appears that some type of fruit-size selection occurs because of
the different size of lizards caught by the two birds. For this
reason, some medium-large fruits such as J. cedrus, J. turbinata and Neochamaelea pulverulenta (Vent.) Erdtman, each about
8 mm in diameter, show a restrictive interaction with lizards
(see Valido 1999), being accessible to certain large individuals,
only preyed on by kestrels (Padilla, Marrero & Nogales 2007).
Small fruits have greater chances of being handled and swallowed by a wide range of frugivores (Jordano 2000). However,
different studies have reported that large fruit ⁄ seed sizes, with
higher probability of seedling emergence and survival may be
selected by frugivores, thus having important consequences for
plant regeneration (Alcántara & Rey 2003; Gómez 2004; Pizo,
Von Allmen & Morellato 2006; Martı́nez, Garcı́a & Obeso
2007; Rodrı́guez-Pérez & Traveset 2010).
CONCLUDING REMARKS
The quantitative and qualitative results (sensu Schupp 1993)
obtained simultaneously on the variety of ecological factors
analysed in this study support the hypothesis that secondary
seed dispersal by predatory birds has played a greater role in
seed dispersal in the subtropical Canary archipelago, than previously recognized. Although predatory birds are obviously
not typical frugivores, they can play an important role in the
seed dispersal processes of many plant species, acting as primary or secondary seed dispersers (Galetii & Guimarães 2004;
Nogales et al. 2007). All in all, the Canaries are confirmed to
have the highest level of secondary seed dispersal by vertebrates worldwide. However, the frugivory of insular reptiles
has been mentioned in several archipelagos (Rick & Bowman
1961; Iverson 1985; Whitaker 1987; Traveset 1995; Pérez-Mellado & Traveset 1999), so it is highly probable that this process
could occur in many other places. Other cases of secondary
seed dispersal documented include finches and owls as primary
and secondary seed dispersers respectively of Chamaesyce
amplexicaulis (Euphorbiaceae) in the Galápagos Islands
(Grant et al. 1975). These authors suggested that seeds contained in the gut of frugivorous prey may be transported
unharmed from one island to another. Unlike some LDD paradigms based on the difficulty of predicting and documenting
this process in time and space (Greene & Johnson 1995; Higgins & Richardson 1999; Clark, Lewis & Horvath 2001), the
complex seed dispersal systems we focus on are common and
affect a large number of fleshy-fruited plant species and seeds,
which are being dispersed regularly each year in identified habitats. In this case, the potentially important role of this multistep ecological process of seed dispersal in the colonization of
recent insular volcanic areas or other subtropical islands
becomes clear.
Acknowledgements
Heriberto López gave us support with graphics. D. P. P. was partially financed
by a PhD grant awarded by the Canary Government and by a postdoctoral
fellowship from the Spanish Ministry of Education. A. G.-C. benefited from
JAE-PRE fellowships from the Spanish National Research Council (CSIC).
During the development of this prolonged study, we also received funds from
the Canary Government (project: PI042004 ⁄ 037), Spanish Ministry of Science
and Education (projects: CGL 2007-61165 ⁄ BOS and CGL2010-18759 ⁄ BOS)
and the Organismo Autónomo de Parques Nacionales (051 ⁄ 2010). All these
projects have been partially financed by the FEDER program (European
Union). Anna Traveset helped us in the planning and monitoring of the study.
Douglas Levey, Félix M. Medina, Eugene Schupp, Michelle Leishman (Associate Editor) and two anonymous referees greatly improved this contribution.
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Received 22 February 2011; accepted 17 October 2011
Handling Editor: Michelle Leishman
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