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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 + + + + + ) ) + ) + ) ) ) ) + + ) ) ) + + + + + + ) + + + ) ) + + ) + + ) + ) ) ) + + ) + + + + + ) + + ) + + ) ) ) + + + ) ) + + + + + + ) + + + + + + + + + + ) + ) ) + + + ) + + + ) + + + + ) + + + + + + + + + + + + + + + + + + + + + + + + + + + ) + + + + + + + + + + ) + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + ) + + ) + + + + ) + + + + ) + + + + + + + + + + + + + + + + + + + + + + ) + + + + + + + ) + + ) ) + + + + + + + + + + + + + + + + + + + + ) + + + + + + + + + + + + + + + + + + ) + + ) ) ) + + ) + + + + ) + + + ) + ) + ) + + + ) + + + + + + + + + + ) + + + + + + + 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). 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