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Fruit production and predispersal seed fall and predation in Rhamnus alaternus (Rhamnaceae)
Acta Oecologica 27 (2005) 115–123 www.elsevier.com/locate/actoec
Original article
Fruit production and predispersal seed fall and predation in Rhamnus alaternus (Rhamnaceae) Josep M. Bas *, Crisanto Gómez, Pere Pons Departament de Ciències Ambientals, Campus de Montilivi, Universitat de Girona, 17071 Girona, Spain Received 20 July 2004; accepted 13 October 2004 Available online 26 November 2004
Abstract In the reproductive cycle of fleshy-fruited plants, and before the seeds are dispersed, some fruits fall down or are predated on the branches. Here, we study the predispersal biology of Rhamnus alaternus in the north-east of the Iberian Peninsula over a 4-year period. Specifically, we examined fruit production, fructification and the phenology of ripening, together with the causes and the consequences of the predispersal loss in female plants. In addition, we evaluated the influence of the biometric traits and the spatial distribution of plants with regard to these aspects. The total estimated fruit production and fruiting phenology varied between localities and years, and there was no relation either to the plant biometry or to the spatial situation. The ripening period was between April and August, with a mean period of fruit permanence on the branches of 102 days. The maximum presence of ripe fruits was from early June to July, 54 days in average after fruit ripening began. The interaction of animals with the fruits has four important consequences: (a) losses in the initial production due to depredation of seeds, mainly by rodents; (b) direct fall of fruit and seeds under the cover of the female plants due to invertebrate predators of pulp; (c) reduction of the period of fruit availability on the branches; and (d) reduction of the proportion of ripe fruits on branches. In summary, the number of seeds available to be dispersed by frugivorous vertebrates is considerably reduced as a consequence of predispersal effects. © 2004 Elsevier SAS. All rights reserved. Keywords: Evergreen buckthorn; Fleshy fruit; Plant–animal interaction; Seed and fruit fall; Seed predation
1. Introduction Fruit and seed production are essential processes in the reproductive biology of plants. Interactions with dispersers and seed predators have effects on the demography of plants with fleshy fruits (Janzen, 1971; Traveset, 1993; Jordano, 1995b; García, 1998). The fruit ripening in specific periods and quantities provides food for the vertebrate frugivores that subsequently disperse the seeds. Initially, the specific phenological patterns of fruit production were considered to be the result of selective pressures exerted by seed-dispersing vertebrates (Thompson and Willson, 1979; Herrera, 2002). However, other biotic and abiotic factors also play important roles in the evolution of the fruiting phenology (Herrera, 2002). In
* Corresponding author. E-mail address: [email protected] (J.M. Bas). 1146-609X/$ - see front matter © 2004 Elsevier SAS. All rights reserved. doi:10.1016/j.actao.2004.10.004
fact, it is difficult to establish direct relations between plants and dispersers, due to the temporal and spatial variability of the ripening phenology and of frugivore populations (Wheelwright, 1986; Rey, 1995; Guitián, 1998; Herrera, 1998). The predispersal loss and movement of diaspores from branches, by biotic or abiotic means, has consequences on the production of viable, available seeds for the disperser agents (Herrera, 2002). Abiotic losses can be caused by adverse weather conditions or limited resources (Guitián, 1993), which can lead to seed abortion or to the fall of developed fruits or viable seeds from the plant. In the last case, seeds accumulate beneath the plant (Krüsi and Debussche, 1988; Masaki et al., 1994; Kollmann and Pirl, 1995) and cannot escape, at least initially, the high mortality rate near the parental plant (Howe and Smallwood, 1982). Biotic losses are related mainly to two different plant–animal interactions in the predispersal stage: pulp eaters and seed predators. Pulp removal negatively affects the attractiveness of the fruit to the dispersers, favouring the fall of the fruit/seeds
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under the plants (Traveset, 1993; Jordano, 1995a; García, 1998). In addition, the predation of seeds causes direct losses of the initial production (Janzen, 1971). This study attempts to characterise the predispersal fruit ecology of R. alaternus in the north-east of the Iberian Peninsula, aiming to: (a) examine in detail the phenology of fruit production and ripening, and to characterise the initial production; (b) evaluate whether the biometric attributes and spatial distribution of the plants influence production and phenology; (c) characterise the predispersal removal of diaspores from the branches (splitting of the entire fruit, fall of isolated seeds and depredation of seeds); and (d) identify the specific agents involved in the manipulation of fruit on the branches.
2. Materials and methods 2.1. Study species Our study plant, R. alaternus L. (Rhamnaceae), is a perennial and dioecious shrub, common in shrublands and oak woods of the Mediterranean region. The flowers are pollinated by wind and insects, and the ripe fruits are black drupes dispersed by birds (Herrera, 1984a; Bas, 2001). Every fruit has 2–5 seeds (Bas et al., 2002) and every seed is included in an endocarp that, on having dried-off, is opened and expels the seed short distances (Bas and Gómez, 2001). Production and ripening of R. alaternus fruits has been mentioned in different studies in the western Mediterranean region, with fruits ripening between May and October (Herrera, 1984a; Debussche and Isenmann, 1992; Aronne and Wilcock, 1997), but predispersal fruit/seed predation has not been previously studied in this species. However, several animal taxa have been recognised as general predispersal predators on Mediterranean fleshy-fruited plants: rodents (Obeso, 1998), birds of the families Fringillidae and Paridae (Traveset, 1993, 1994a; Jordano, 1995b) and arthropods (Herrera, 1984b; Krüsi and Debussche, 1988; Traveset, 1993, 1994b; Alcántara et al., 1997; García, 1998). 2.2. Study sites The study was carried out from 1996 to 1999 at three localities in coastal areas of Catalonia, in northeastern Spain, that have been proposed as future Natural Parks. Two of these sites, Mas de la Figuera (LOC1) and Aigua Blanca (LOC2), are situated on Les Gavarres Massif (41°54′N 02°56′E, 185 and 295 m above sea level, respectively). The third area, Aixart d’en Pi (LOC3), is located on El Montgrí Massif (42°05′N 03°11′E, 95 m above sea level). All the areas are characterised by a Mediterranean-type climate: annual mean rainfall of around 625 mm, minimum monthly mean temperatures of 7.5 °C in January, and maximum monthly mean temperatures of 24 °C in July–August. The vegetation is dominated by sclerophyllous species, in Les Gavarres a for-
est dominated by Quercus suber and understorey composed of Arbutus unedo, Erica arborea and Cistus monspeliensis; and in El Montgrí, a shrubland community made up of Quercus coccifera, Rosmarinus offıcinalis, Cistus albidus and Brachypodium retusum. 2.3. Phenology of fruit production and ripening The production and phenology of fruits was followed on 20, 17 and 20 females chosen at random in LOC1, LOC2 and LOC3, respectively. Fruits were counted on one random branch per female, and followed during the whole process of ripening (LOC1 and LOC2: 1996, 1997 and 1998; LOC3: 1998 and 1999), until there were no longer any fruits on the branches. The selected branches were 1-m long approximately and were ramifications from the main trunk. The total initial production of fruits was measured 1–3 weeks before ripening started, when the fruits were of a considerable size (3–4 mm in diameter; beginning of April to the end of May) but before fruit maturity (maximum fruit width = 9.9 mm; Bas et al., 2002). The fruit distribution on branches is representative of the global distribution in the symmetrical crown, a fact that allowed us to estimate with sufficient precision the total initial production of the plant. Every 7–20 days, the number of unripe, ripe and dried fruits was assessed. A fruit was considered unripe when it did not have the final blueblack colour of mature fruit. A dry fruit had dry pulp, and it could originate from unripe as well as from ripe fruit. 2.4. Biometric characteristics and spatial distribution of female plants Structural variables of the plants were taken to evaluate the similarity between the studied localities. The height, the diameter of the trunk at 5 cm above the soil, the area of the top projection and the top volume of plants were measured in the marked female plants. The projection area was calculated by the maximum and minimum horizontal measures of the top, and the volume was estimated by similarity to geometric figures (Herrera and Jordano, 1981; Traveset, 1994a). We also measured the distance from the selected female plants to the two nearest male and female plants (Traveset, 1994a; Guitián, 1995). And we evaluated if there was an influence of these biometric characteristics and spatial variables on the fruit production. 2.5. Fruit and seed losses Two different methodologies were used to identify the causes of the fruit loss from the branches: counting fruits in trays placed below the maternal plants, and counting fruits on branches from which animals were excluded. In the first one, 1–3 trays of 800 cm2 were placed under the maternal plant with an 8 mm metallic mesh to prevent access to vertebrates, in a number that was changing according to the projection area of the plant. The content of the trays was collected and
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identified later in the laboratory as whole fruit and whole or broken endocarps. We counted the endocarps (one endocarp per seed) instead of the seeds because the elaiosome adhering to the seeds (Bas et al., 2002) is attractive to ants and stimulates seed removal (Bas and Gómez, 2003; Gómez et al., 2003) and, consequently, counts of the seeds would underestimate their real number. To differentiate the endocarps that had fallen directly off the branches from the ones that were due to depositions, we looked at the external characteristics. The endocarps fallen from the plant still had intact pieces of adhering pericarp or mesocarp, whereas those from excrement were blackish and did not have adhering pulp. In 1998 and 1999, fallen fruits were separated into unripe and mature fruits. In order to quantify pedicel influence on fruit opening the occurrence of the pedicel in fallen fruits was annotated, and we checked if the fruit opened after 25 days in the laboratory. In this way we could also estimate if the free seeds from the trays came directly from the branches or from fruit that opened later on the soil. The second method used consisted in randomly choosing by locality and year 10 additional branches (one per plant) which were excluded using mosquito netting. These exclusions were made when the fruit was developed (3–4 mm diameter) in order to avoid manipulation by rodents, birds and insects. Plants chosen for branchexclusion treatments were located a minimum of 30 m from the plants selected as controls to avoid altering the behaviour of the frugivores or predators in the free branches. Due to the entry of rodents onto some of the selected branches, finally only five exclusions were considered (LOC1 1996, 1997 and 1998; LOC2 1996; and LOC3 1998). The fruits remaining on the excluded branches and the fruits fallen inside the mosquito netting were counted every 7–20 days, distinguishing between unripe and mature fruits. Finally, to find out about the possible predators (of pulp or seeds), direct observations on the branches were made during the whole season and 14 live traps for rodents were installed at each locality.
2.6. Statistical analysis Parametric statistical analyses were used for the analysis of biometric traits of the plants and predispersal seed fate (one-factor ANOVAs) and for test the significance between non-excluded and excluded branches (Student’s t test). Logarithmic transformations were used to normalise the measurements. When the ANOVA was significant, the means were compared using the Scheffé post-hoc test (Zar, 1984). Repeated measure ANOVAs were used to compare the mean fruit production between localities and years. In these cases, the variable “year” was considered as the within-subject effect, and the variable “localities” as the between-subject effect. Locally, we used the v2 of comparison of frequencies and Spearman’s rank correlation test for the comparison of the variables. Data are reported as means (± s.e) and range.
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3. Results 3.1. Total fruit production and characteristics of female plants Annual variability in initial production of fruit was considerable. Production by the same plant varied from 1.3 to 122.0-fold (mean ± s.e. = 13.3 ± 27.5 fold, n = 20) between years in LOC1, 1.6 to 41.5-fold (7.3 ± 9.7, n = 17) in LOC2 and 1.0 to 154.0-fold (21.5 ± 35.1, n = 20) in LOC3. Across years, there was no tendency for some plants to always produce many fruits, and other plants to always produce fewer fruits. Interrelation only exists in LOC1 and LOC2 of the year 1997 and 1998 (rs = 0.60, P = 0.005, n = 20 trees and rs = 0.71, P = 0.001, n = 17 trees, respectively). The estimated total production of fruits (fruits/m3) was different between localities and years (Fig. 1). A repeatedmeasure ANOVA indicated no significant effects of year (F2,35 = 0.22, P = 0.64) and localities (F1,35 = 1.15, P = 0,29) on total fruit production; however, there was a significant effect of their interaction (F2,35 = 5.72, P < 0.05). At LOC3 there was a significant effect of the year on fruit production (F1,19 = 23.0, P < 0.05). The female plants showed important variability in biometric characteristics and in spatial distribution (Table 1). Significant differences between the localities were observed for four of the measured variables (height F2,24 = 13.40, P < 0.05; stem diameter F2,24 = 5.06, P < 0.05; projection area F2,24 = 8.93, P < 0.05; top volume F2,24 = 11.94, P < 0.05). However, these differences were due only to differences between LOC3 and the two localities of Les Gavarres (LOC1 and LOC2) (Scheffé post-hoc test, P <0.05), due to the smaller plant size in El Montgrí (LOC3). On the other hand, plant density was twice as high in LOC1 and LOC2 as in LOC3 (Table 1). The structural variables were intercorrelated (Spearman correlation, P < 0.05 for each pair of variables) and initial fruit production (fruit/m3) did not show a significant correlation with any of these four variables (P > 0.05). There was no relationship between initial fruit production (fruit/m3) and the nearest neighbour distances for any of the localities and years analysed (P > 0.05).
Fig. 1. Estimated fruit production/plant (dark columns) and fruit number/m3 (white columns) at the three study localities and for different years (LOC1, n = 20 plants; LOC2, n = 17 plants; and LOC3, n = 20 plants). Vertical bars denote standard errors of the mean.
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Table 1 Biometric characteristics and spatial distribution of Rhamnus alaternus female plants at three study localities (mean ± s.e. (range)). Study areas: Les Gavarres (LOC1: Mas de la Figuera; and LOC2: Aigua Blanca) and El Montgrí (LOC3: Aixart d’en Pi) Height (m) Long diameter (m) Short diameter (m) Projection area (m2) Top volume (m3) Stem diameter (cm) Distance to first nearest female plant (m) Distance to second nearest female plant (m) Distance to first nearest male plant (m) Distance to second nearest male plant (m)
LOC1 (n = 20 plants) 2.91 ± 0.76 (1.90–4.50) 2.22 ± 0.91 (0.80–4.40) 1.59 ± 0.61 (0.70–2.80) 3.13 ± 2.35 (0.44–8.36) 1.74 ± 1.71 (0.14–6.27) 6.55 ± 3.72 (2.00–15.00) 2.47 ± 1.85 (0.40–8.40) 5.08 ± 3.02 (1.50–11.00) 2.84 ± 2.15 (0.25–8.75) 6.12 ± 2.84 (2.00–11.50)
LOC2 (n = 17 plants) 3.67 ± 0.81 (2.20–5.10) 2.26 ± 0.87 (1.10–3.80) 1.91 ± 0.78 (1.10–3.70) 3.87 ± 3.09 (0.95–11.04) 2.60 ± 2.47 (0.41–8.28) 5.35 ± 3.14 (2.00–15.00) 2.56 ± 1.94 (0.10–7.00) 4.69 ± 2.88 (1.10–11.50) 2.37 ± 2.06 (0.25–8.50) 5.09 ± 3.34 (2.00–16.50)
LOC3 (n = 20 plants) 2.33 ± 0.83 (1.10–4.50) 1.40 ± 0.55 (0.80–2.90) 1.15 ± 0.49 (0.60–2.30) 1.46 ± 1.23 (0.38–5.24) 0.63 ± 0.68 (0.10–2.79) 3.69 ± 1.45 (1.60–6.10) 5.77 ± 4.96 (1.10–2.10) 9.75 ± 7.02 (3.50–33.00) 6.13 ± 5.24 (0.80–18.00) 9.41 ± 6.79 (2.00–25.00)
3.2. Phenology of fruit production and ripening
3.4. Fruit and seed fall underneath branches
Mature fruits were present on plants from the beginning of April to mid-August (Fig. 2), i.e. during 102.4 ± 26.7 (57– 150) days. A total of 53.7 ± 16.5 (19–73) days passed from the beginning of maturation until the period of maximum presence of mature fruit (beginning of June–July). This maximum presence of mature fruits in the branches never exceeded 30% of the initial production, though in July and August it sometimes accounted for 100% of the remaining fruit (finally dried) (Fig. 2). Dry fruits include both unripe and mature fruits that had dried on the plant. Dry fruits always accounted for only a small (4.9 ± 2.8%) proportion of the whole initial production. Depending on the locality and year their number varied from 0 to 658.4 (150.6 ± 226.3, n = 8) dry fruits/m3. Dried fruits remained present on plants for 32–89 (63.5 ± 22.7, n = 8) days beyond the period of maximum presence of mature fruits. Total production (fruit/m3) was not related either to the date at which maturation began on the plant (rs = 0.18, P > 0.05) or to the entire number of mature fruits produced by the plant (rs = 0.69, P > 0.05). Also, total production (fruit/m3) was independent of the period (days) during which fruit was kept on the branches and from the time elapsed until maximum maturation (rs = 0.14, P = 0.74 and rs = 0.02, P = 0.95, respectively).
A total of 442 ± 413 fruits/m2 (49–1214, n = 7) were collected, which represented a total fall of 1879 ± 2873 (134–8286, n = 7) fruits per plant (Fig. 3). We have found 208 ± 199 (47–564, n = 7) seeds/m2, which means 589 ± 717 (180–2176, n = 7) entire seeds/plant (Fig. 4). Fruit fall (fruits/m2) was different among years in all localities (F1,28 = 73.4, P < 0.05 at LOC2; F1,37 = 10.7, P < 0.05 at LOC3 and F2,52 = 17.4, P < 0.05 at LOC1). Annual differences also appear when we assess the estimated fall per plant (F1,28 = 25.6, P < 0.05 at LOC2; F1,37 = 5.2, P < 0.05 at LOC3 and F2,52 = 10.1, P < 0.05 at LOCl). This fruit fall/plant represented 28.7 ± 10.1% of the estimated fruit production/plant. More unripe fruits than ripe fruits fell from the branches (73.4 ± 12.7%, 60.0–87.5, n = 7), most of the unripe fruits fell with pedicel (90.8 ± 4.2%; 87.8–96.7, n = 4). In contrast, on the branches from which animals were excluded the majority of fallen fruits were mature (84.9 ± 14.7%, 62.2–99.0, n = 5) (v2 = 66.6, P < 0.05). In this case, mature fruits fallen with pedicel were in a minority (42.3 ± 17.1%, 23.7–64.6, n = 4). Once on the soil, the liberation of seeds from the opening of the fruit is very low. Unripe fruits never opened, whereas the mature ones opened in 11.4% (without pedicel) and 1.8% (with pedicel) of the cases. The frequency of free seeds inside the excluded branches was also very low (1.4% of the seeds are free). The phenology of fruit and seed fall below the plants was variable, from the beginning of May until mid-August, with a maximum between June and July (Fig. 5). The first presence of fruits and seeds in the trays did not depend on the initial production (rs = 0.06, P = 0.90 and rs = 0.09, P = 0.85, respectively). Though there was a negative correlation between the beginning of the presence of fruits or seeds in the trays and the time that the fruit remained on the branches, this relation was also not significant (rs = -0.62, P = 0.14 and rs = –0.71, P = 0.07, respectively). The fall of fruits was strongly related to the entire initial production in the majority of localities (rs = 0.67, P < 0.05 and rs = 0.72, P < 0.05 at LOC2 1996 and LOC2 1998, respectively; rs = 0.52, P < 0.05 and rs = 0.61, P < 0.05 at LOC3 1996 and LOC3 1998, respectively; rs = 0.51, P < 0.05 and rs = 0.58,
3.3. Effect of interactions with animals on the phenology and the presence of ripe fruit The exclusion of animals from branches had two important consequences. Firstly, it lengthened the period during which fruits remained on the branches, in extreme cases for more than 2 months (T Student; t = –3.94, P < 0.05) (Fig. 2). Secondly, it increased the proportion of mature fruit on the branches (T Student; t = –6.86, P < 0.05). Whereas in the control branches this proportion was never larger than 30%, on the branches from which animals were excluded it was substantially higher (90%). This indicates that animals, both predators and dispersers, preferentially consume mature fruits.
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Fig. 2. Right and left figures show the number of total fruits (white circles) and mature fruits (dark circles) on branches relative to initial fruit production. Moreover, the left figures show the number of total fruits (white triangles) and mature fruits (dark triangles) on branches excluded relative to initial fruit production on exclusion branches. The grey areas correspond to the difference of the proportion of green (clear area) and mature fruits (dark area) between excluded and non-excluded branches. See Section 2 for details.
P < 0.05 at LOCl 1997 and LOC1 1998, respectively). The fall of whole fruits was strongly related to the fall of entire seeds for the seven combinations of locality and year (rs = 0.86, P < 0.05). 3.5. Predispersal seed predation A total of 1567 ± 1172 (243–3796, n = 7) predated seeds/m2 and 4322 ± 2644 (355–8182, n = 7) predated seeds/plant were collected. The extent of predation depended neither on the initial production of fruit (rs = 0.47, P = 0.29) nor on the number of fruit and entire seeds fallen from the branches (rs = 0.09, P = 0.85 and rs = –0.02, P = 0.97,
Fig. 3. Estimate fruit fall/plant (grey columns) and fruit fall number/m2 (white columns) at the three study localities (LOC1, n = 20 plants; LOC2, n = 17 plants; and LOC3, n = 20 plants). Vertical bars denote standard errors of the mean.
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the mesocarps of unripe fruits, and bugs (Gonocerus insidiator [Coreidae] and Eusarcoris inconspicua [Pentatomidae]) that sucked fluid in mature fruits. Also, some ants (Camponotus piceus, Camponotus lateralis, Lasius cinereus, Linepithema humile and Tapinoma nigerrimum) fed on the sweet pulp of ripe fruits directly on the branches. No predispersal seed predation by ants was observed.
4. Discussion Fig. 4. Number of fallen seeds/m (barred columns), predated seeds/m (white columns), estimated number of fallen seeds per plant (black columns) and estimated number of predated seeds per plant (grey columns) at the three study localities (LOC1, n = 20 plants; LOC2, n = 17 plants; and LOC3, n = 20 plants). 2
2
respectively). Therefore, predispersal predation was not higher in plants producing more fruits. This predation began when fruits had developed (3–4 mm in diameter) (Fig. 5); timing of the beginning of predation did not determine the length of the period that fruit remained on the branches (rs = –0.67, P = 0.10). Judging by the characteristics of manipulated fruit and seeds, and the captures in traps, rodents were the main predispersal predators of seeds, Apodemus sylvaticus at all three localities (79% of all rodents captured), and Mus spretus at LOC3 and LOCl (21% of all captures). The main animals responsible for pulp removal were the caterpillars of Microlepidopterans (Geometridae) that fed on
The entire initial fruit production and the fructification phenology of fruit maturation in R. alaternus showed variability at two levels: (a) temporal, whether in the same period or in different years; and (b) spatial, between the studied localities and between individuals at the same locality. In the north-west of the Iberian Peninsula, the total production of fruit of R. alaternus is not globally related to the characteristics of individual plants or to the spatial situation with regard to nearby male or female plants (Guitián, 1995). Although plant biometry can be important, environmental variables such as temperature, water availability, wind force or soil nutrients probably have greater effects on components of reproductive success (number of flowers, pollinated flowers, etc.) and therefore on the amount of fruits finally matured (Chiarucci et al., 1993). In our study, plant density does not seem to determine pollen availability, proportion of polli-
Fig. 5. Phenology of fruit falling (number/m2, black circles), seed falling (number/m2, black diamonds) and seed predation (number/m2, white diamonds) underneath the maternal plants of R. alaternus at the three studied localities.
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nated flowers and fruit development. As a probable consequence, the number of fruits on the different branches showed a large variability, albeit without clear tendencies between different years. The fruit ripening period of R. alaternus is from the beginning of April until mid-August shows large variability among localities and years. The average period during which mature fruits are present is 100 days, with variation among localities and years (range = 30–135 days). This period does not coincide with those stated for other localities in the Mediterranean basin, e.g., from June to July in Italy (Aronne and Wilcock, 1997), from June to September in the southern France (Debussche and Isenmann, 1992) or from May to October southern Spain (Herrera, 1984a). Nor does the timing of maximum presence of ripe fruit in the middle of the ripening period (beginning June–beginning July) fully coincide with other studies, which mention July (Herrera, 1984a; Debussche et al., 1987). The early fruiting during spring–summer that we detected in R. alaternus is uncommon in species with fleshy fruits in Europe and the Mediterranean basin. In this period only 7–13% of the species in southern Spain bear mature fruit (Herrera, 1984a), compared to 12% in the eastern Mediterranean (Izhaki and Safriel, 1985) and 33% in temperate zones of Europe (Snow and Snow, 1988). Its early fruiting is probably why R. alaternus has not been detected in the majority of frugivore and seed dispersal studies, and why only a few authors mention it (Debussche and Isenmann, 1983; Herrera, 1984a; Sunyer, 1994). Producing fruits in this period might affect seed dispersal by birds, as it coincides with birds’ breeding seasons. Communities of frugivorous birds may be more stable in successive years (Bas, 2001) than are those feeding on fruits during autumn and winter, when the majority of species bear ripe fruits. Abundances of migrating and wintering frugivorous birds are variable between years, leading to interannual differences in zoochory (Debussche and Isenmann, 1983; Herrera, 1984a). The interaction of R. alaternus with animals that continuously remove mature fruits remains demonstrated by the low proportion of mature fruit on control branches (<30% of initial production) compared to excluded branches and the reduction of the period with mature fruit on the control branches. Also, the less rigorous climatic conditions when fruits of R. alaternus mature considerably affect post-dispersal processes, such as the secondary dispersal and predation of seeds by ants (Bas and Gómez, 2003; Gómez et al., 2003). These interactions are less probable in unfavourable periods (Traveset, 1994b; Hulme, 1997; Alcántara et al., 2000). Predispersal losses of seeds from branches are due to three causes: falling of unripe or mature fruit, loss of entire seeds from fruit opening on the branches, and seeds predated on the branches. Predated seeds accounted for 7.5 times more seeds than free seeds fallen from the branches and 1.2 times more seeds than seeds inside fallen fruit. Ripe (84%) and unripe fruits (16%) fall from the branches naturally. Some authors define this gravitational fall of fruit and seeds as a primary
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dispersal mechanism, i.e. “barochory” (Chambers and MacMahon, 1994; Masaki et al., 1994; Kollmann and Pirl, 1995). Though the exclusion trays isolate the rodents, other animals, such as ants or beetles, might get in to remove the diaspores (Beattie, 1985). However, we believe there was no underestimation of the tray counts, since the presence of large harvester ants (genus Messor) or of seed-eating beetles (Carabidae, subfamily Harpalinae) was very low in our case (Bas, 2001), probably because the plants we studied were in places with heavy vegetation cover. Also, the fact that we count the endocarp on trays, which are not attractive to ants (Bas, 2001), could also have helped to avoid this effect (Aronne and Wilcock, 1994; Bas and Gómez, 2003; Gómez et al., 2003). The accumulation of fruits and entire seeds underneath the plants has been detected in other species with fleshy fruits (Sallabanks, 1992), including other species of Rhamnus (Archibold et al., 1997). In R. alaternus the opening of fruit on the branches, with the subsequent fall of free seeds underneath the plants, has already been described (Aronne & Wilcock, 1994). In our study, the fact that the proportion of endocarps without pulp on control branches (13.8%) was much higher than the proportion on animal-excluded branches (1.4%) makes us think that some external mechanism increases this proportion. A built-in mechanism for liberating seeds does not exist, contrary to the proposal of Aronne & Wilcock, (1994). On the other hand, the manipulation of fruit by seed predators and pulp removers on branches, and the opening of the fallen fruits, determine the presence of free seeds on the ground. The observation of moth larvae feeding nocturnally on the pulp of unripe fruit during the period of our study, previously observed in other species of fleshy plants by Krüsi and Debussche (1988) and Alcántara et al. (1997), might explain the direct fall of seeds and endocarps unprotected by pulp. Tits of the family Paridae, potential pulp predators of mature fruits, were not observed eating pulp in the different areas (Bas, 2001). On the other hand, bugs observed sucking fluid from the pulp in mature fruit contribute to the drying of the fruit (Traveset, 1994b), causing them to fall from the branches. Also, physiological stress in periods of adverse climatic conditions (high wind, low water and nutrient availability) can increase the number of fallen fruits. This situation could have occurred in LOC2 in 1998, given the high presence of fallen fruits in all the trays. Unlike in other areas of the Iberian Peninsula where birds are the main seed predators (Herrera, 1984a, Traveset, 1994a, Jordano, 1995b), in our study seed predation was due mainly to rodents, as suggested by our observations of the physical characteristics of the predated endocarps and seeds, our direct observations of Apodemus sylvaticus feeding on branches, and the low density of granivorous birds in the study areas. The rarity presence of other rodents (e.g. Sciurus vulgaris) and granivorous insects suggests that there might only be occasional predispersal predators of R. alaternus seeds. The predispersal predation of seeds by rodents directly
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on woody plants with fleshy fruit has been described on very few occasions (Obeso, 1998). The rodents discard the pulp and eat the seeds, and predate more often on unripe fruits because they have proportionally more endosperm (Jordano, 1989; Traveset, 1994b). Thus, most mature fruits are removed by frugivorous birds (Bas, 2001), whereas the rodents limit the total production of mature fruits available for the dispersers. Fruit selection by rodents has also been detected by Obeso (1998), who described how rodents predated fruits with viable seeds more often than fruits with aborted seeds. In fact, we assume that the predispersal removers of pulp and seeds play a significant role on the reproductive success of R. alaternus, both indirectly due to the reduction in the number of fruits available for the dispersers, and directly by causing loss of viability of the seeds before they have been dispersed. To sum up, the effects of the external factors significantly affect the predispersal fruit ecology of R. alaternus more than do the spatial situation and the specific characteristics of the different plants.
Acknowledgements We are grateful to A. Bou, G. Pasqual, M. Sais and G. Vila for assistance during field and laboratory work. We also thank A. Traveset, J. Guitián and two anonymous reviewers for critical reading and comments of the manuscript. The research was supported in part by MICYT (REN2000-0300C02-02/GLO) and MEC (CGL2004-05240-C02-02/BOS).
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Chambers, J.C., MacMahon, J.A., 1994. A day in the life of a seed: movements and fates of seeds and their implications for natural and managed systems. Annu. Rev. Ecol. Syst. 25, 263–292. Chiarucci, A., Pacini, E., Loppi, S., 1993. Influence of temperature and rainfall on fruit and seed production of Arbutus unedo L. Bot. J. Linn. Soc. 111, 71–82. Debussche, M., Isenmann, P., 1983. La consommation des fruits chez quelques fauvettes méditerranéennes (Sylvia melanocephala, S. cantillans, S. hortensis, S. undata) dans la région de Montpellier (France). Alauda 51, 302–308. Debussche, M., Isenmann, P., 1992. A Mediterranean bird disperser assemblage: composition and phenology in relation to fruit availability. Terre et la Vie 47, 411–431. Debussche, M., Cortez, J., Rimbault, I., 1987. Variation in fleshy fruit composition in the Mediterranean region: the importance of ripening season, life-form, fruit type and geographical distribution. Oikos 49, 244–252. García, D., 1998. Interaction between juniper Juniperus communis L. and its fruit pest insects: pest abundance, fruit characteristics and seed viability. Acta Oecologica 19, 517–525. Gómez, C., Pons, P., Bas, J.M., 2003. Effects of the Argentine ant (Linepithema humile Mayr) on seed dispersal and seedling emergence of Rhamnus alaternus L. (Rhamnaceae). Ecography 26, 532–538. Guitián, J., 1993. Why Prunus mahaleb (Rosaceae) produces more flowers than fruits. Am. J. Bot. 80, 1305–1309. Guitián, J., 1995. Sex ratio, reproductive investment and flowering phenology in dioecious Rhamnus alaternus (Rhamnaceae). Nord. J. Bot. 15, 139–143. Guitián, P., 1998. Latitudinal variation in the fruiting phenology of a birddispersed plant (Crataegus monogyna) in Western Europe. Plant Ecol. 137, 139–142. Herrera, C.M., 1984a. A study of avian frugivores, bird-dispersed plants, and their interaction in Mediterranean scrublands. Ecol. Monogr. 54, 1–23. Herrera, C.M., 1984b. Avian interference of insect frugivory: an exploration into the plant–bird–fruit pest evolutionary triad. Oikos 42, 203–210. Herrera, C.M., 1998. Long-term dynamics of Mediterranean frugivorous birds and fleshy fruits: a 12-year study. Ecol. Monogr. 68, 511–538. Herrera, C.M., Jordano, P., 1981. Prunus mahaleb and birds: the highefficiency seed dispersal system of a temperate fruiting tree. Ecol. Monogr. 51, 203–218. Herrera, C.M., 2002. Seed dispersal by vertebrates. In: Herrera, C.M., Pellmyr, O. (Eds.), Plant–Animal Interactions. An Evolutionary Approach. Blackwell Science, England, pp. 185–208. Howe, H.F., Smallwood, J., 1982. Ecology of seed dispersal. Annu. Rev. Ecol. Syst. 13, 201–228. Hulme, P.E., 1997. Post-dispersal seed predation and the establishment of vertebrate dispersed plants in Mediterranean scrublands. Oecologia 111, 91–98. Izhaki, I., Safriel, U.N., 1985. Why do fleshy-fruit plants of the Mediterranean scrub intercept fall—but not spring—passage of seed-dispersing migratory birds? Oecologia 67, 40–43. Janzen, D.H., 1971. Seed predation by animals. Annu. Rev. Ecol. Syst. 2, 465–493. Jordano, P., 1989. Pre-dispersal biology of Pistacia lentiscus (Anacardiaceae): cumulative effects on seed removal by birds. Oikos 55, 375–386. Jordano, P., 1995a. Frugivore-mediated selection on fruit and seed size: birds and St. Lucie’s cherry, Prunus mahaleb. Ecology 76, 2627–2639. Jordano, P., 1995b. Spatial and temporal variation in the avian-frugivore assemblage of Prunus mahaleb: patterns and consequences. Oikos 71, 479–491. Kollmann, J., Pirl, M., 1995. Spatial pattern of seed rain of fleshy-fruited plants in a scrubland–grassland transition. Acta Oecologica 16, 313–329. Krüsi, B.O., Debussche, M., 1988. The fate of flowers and fruits of Cornus sanguinea L. in three contrasting Mediterranean habitats. Oecologia 74, 592–599.
J.M. Bas et al. / Acta Oecologica 27 (2005) 115–123 Masaki, T., Kominami, Y., Nakashizuka, T., 1994. Spatial and seasonal patterns of seed dissemination of Cornus controversa in a temperate forest. Ecology 75, 1903–1910. Obeso, J.R., 1998. Patterns of variation in Ilex aquifolium fruit traits related to fruit consumption by birds and seed predation by rodents. Ecoscience 5, 463–469. Rey, P.J., 1995. Spatio-temporal variation in fruit and frugivorous bird abundance in olive orchards. Ecology 46, 1625–1635. Sallabanks, R., 1992. Fruit fate, frugivory, and fruit characteristics: a study of the hawthorn, Crataegus monogyna (Rosaceae). Oecologia 91, 296– 304. Snow, B., Snow, D.W., 1988. Birds and Berries. A Study of an Ecological Interaction. T. & A.D. Poyser, Waterhouses, England. Sunyer, J.R., 1994. Observacions de la dispersió ornitòcora del llampúdol (Rhamnus alaternus). Anuari Ornitològic Balear 9, 47–50.
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Thompson, J.N., Willson, M.F., 1979. Evolution of temperate fruit/bird interactions: phenological strategies. Evolution 33, 973–982. Traveset, A., 1993. Weak interactions between avian and insect frugivores: the case of Pistacia terebinthus L. (Anacardiaceae). Vegetatio 107, 191–203 /108. Traveset, A., 1994a. Influence of type of avian frugivory on the fitness of Pistacia terebinthus L. Evol. Ecol. 8, 618–627. Traveset, A., 1994b. Cumulative effects on the reproductive output of Pistacia terebinthus (Anacardiaceae). Oikos 71, 152–162. Wheelwright, N.T., 1986. A seven-year study of individual variation in fruit production in tropical bird-dispersed tree species in the family Lauraceae. In: Estrada, A., Fleming, T.H. (Eds.), Frugivores and Seed Dispersal. Dr. W. Junk publishers, Dordrecht, pp. 21–37. Zar, J.H., 1984. Biostatistical Analysis. Prentice Hall International Editions, New Jersey.
Original article
Fruit production and predispersal seed fall and predation in Rhamnus alaternus (Rhamnaceae) Josep M. Bas *, Crisanto Gómez, Pere Pons Departament de Ciències Ambientals, Campus de Montilivi, Universitat de Girona, 17071 Girona, Spain Received 20 July 2004; accepted 13 October 2004 Available online 26 November 2004
Abstract In the reproductive cycle of fleshy-fruited plants, and before the seeds are dispersed, some fruits fall down or are predated on the branches. Here, we study the predispersal biology of Rhamnus alaternus in the north-east of the Iberian Peninsula over a 4-year period. Specifically, we examined fruit production, fructification and the phenology of ripening, together with the causes and the consequences of the predispersal loss in female plants. In addition, we evaluated the influence of the biometric traits and the spatial distribution of plants with regard to these aspects. The total estimated fruit production and fruiting phenology varied between localities and years, and there was no relation either to the plant biometry or to the spatial situation. The ripening period was between April and August, with a mean period of fruit permanence on the branches of 102 days. The maximum presence of ripe fruits was from early June to July, 54 days in average after fruit ripening began. The interaction of animals with the fruits has four important consequences: (a) losses in the initial production due to depredation of seeds, mainly by rodents; (b) direct fall of fruit and seeds under the cover of the female plants due to invertebrate predators of pulp; (c) reduction of the period of fruit availability on the branches; and (d) reduction of the proportion of ripe fruits on branches. In summary, the number of seeds available to be dispersed by frugivorous vertebrates is considerably reduced as a consequence of predispersal effects. © 2004 Elsevier SAS. All rights reserved. Keywords: Evergreen buckthorn; Fleshy fruit; Plant–animal interaction; Seed and fruit fall; Seed predation
1. Introduction Fruit and seed production are essential processes in the reproductive biology of plants. Interactions with dispersers and seed predators have effects on the demography of plants with fleshy fruits (Janzen, 1971; Traveset, 1993; Jordano, 1995b; García, 1998). The fruit ripening in specific periods and quantities provides food for the vertebrate frugivores that subsequently disperse the seeds. Initially, the specific phenological patterns of fruit production were considered to be the result of selective pressures exerted by seed-dispersing vertebrates (Thompson and Willson, 1979; Herrera, 2002). However, other biotic and abiotic factors also play important roles in the evolution of the fruiting phenology (Herrera, 2002). In
* Corresponding author. E-mail address: [email protected] (J.M. Bas). 1146-609X/$ - see front matter © 2004 Elsevier SAS. All rights reserved. doi:10.1016/j.actao.2004.10.004
fact, it is difficult to establish direct relations between plants and dispersers, due to the temporal and spatial variability of the ripening phenology and of frugivore populations (Wheelwright, 1986; Rey, 1995; Guitián, 1998; Herrera, 1998). The predispersal loss and movement of diaspores from branches, by biotic or abiotic means, has consequences on the production of viable, available seeds for the disperser agents (Herrera, 2002). Abiotic losses can be caused by adverse weather conditions or limited resources (Guitián, 1993), which can lead to seed abortion or to the fall of developed fruits or viable seeds from the plant. In the last case, seeds accumulate beneath the plant (Krüsi and Debussche, 1988; Masaki et al., 1994; Kollmann and Pirl, 1995) and cannot escape, at least initially, the high mortality rate near the parental plant (Howe and Smallwood, 1982). Biotic losses are related mainly to two different plant–animal interactions in the predispersal stage: pulp eaters and seed predators. Pulp removal negatively affects the attractiveness of the fruit to the dispersers, favouring the fall of the fruit/seeds
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under the plants (Traveset, 1993; Jordano, 1995a; García, 1998). In addition, the predation of seeds causes direct losses of the initial production (Janzen, 1971). This study attempts to characterise the predispersal fruit ecology of R. alaternus in the north-east of the Iberian Peninsula, aiming to: (a) examine in detail the phenology of fruit production and ripening, and to characterise the initial production; (b) evaluate whether the biometric attributes and spatial distribution of the plants influence production and phenology; (c) characterise the predispersal removal of diaspores from the branches (splitting of the entire fruit, fall of isolated seeds and depredation of seeds); and (d) identify the specific agents involved in the manipulation of fruit on the branches.
2. Materials and methods 2.1. Study species Our study plant, R. alaternus L. (Rhamnaceae), is a perennial and dioecious shrub, common in shrublands and oak woods of the Mediterranean region. The flowers are pollinated by wind and insects, and the ripe fruits are black drupes dispersed by birds (Herrera, 1984a; Bas, 2001). Every fruit has 2–5 seeds (Bas et al., 2002) and every seed is included in an endocarp that, on having dried-off, is opened and expels the seed short distances (Bas and Gómez, 2001). Production and ripening of R. alaternus fruits has been mentioned in different studies in the western Mediterranean region, with fruits ripening between May and October (Herrera, 1984a; Debussche and Isenmann, 1992; Aronne and Wilcock, 1997), but predispersal fruit/seed predation has not been previously studied in this species. However, several animal taxa have been recognised as general predispersal predators on Mediterranean fleshy-fruited plants: rodents (Obeso, 1998), birds of the families Fringillidae and Paridae (Traveset, 1993, 1994a; Jordano, 1995b) and arthropods (Herrera, 1984b; Krüsi and Debussche, 1988; Traveset, 1993, 1994b; Alcántara et al., 1997; García, 1998). 2.2. Study sites The study was carried out from 1996 to 1999 at three localities in coastal areas of Catalonia, in northeastern Spain, that have been proposed as future Natural Parks. Two of these sites, Mas de la Figuera (LOC1) and Aigua Blanca (LOC2), are situated on Les Gavarres Massif (41°54′N 02°56′E, 185 and 295 m above sea level, respectively). The third area, Aixart d’en Pi (LOC3), is located on El Montgrí Massif (42°05′N 03°11′E, 95 m above sea level). All the areas are characterised by a Mediterranean-type climate: annual mean rainfall of around 625 mm, minimum monthly mean temperatures of 7.5 °C in January, and maximum monthly mean temperatures of 24 °C in July–August. The vegetation is dominated by sclerophyllous species, in Les Gavarres a for-
est dominated by Quercus suber and understorey composed of Arbutus unedo, Erica arborea and Cistus monspeliensis; and in El Montgrí, a shrubland community made up of Quercus coccifera, Rosmarinus offıcinalis, Cistus albidus and Brachypodium retusum. 2.3. Phenology of fruit production and ripening The production and phenology of fruits was followed on 20, 17 and 20 females chosen at random in LOC1, LOC2 and LOC3, respectively. Fruits were counted on one random branch per female, and followed during the whole process of ripening (LOC1 and LOC2: 1996, 1997 and 1998; LOC3: 1998 and 1999), until there were no longer any fruits on the branches. The selected branches were 1-m long approximately and were ramifications from the main trunk. The total initial production of fruits was measured 1–3 weeks before ripening started, when the fruits were of a considerable size (3–4 mm in diameter; beginning of April to the end of May) but before fruit maturity (maximum fruit width = 9.9 mm; Bas et al., 2002). The fruit distribution on branches is representative of the global distribution in the symmetrical crown, a fact that allowed us to estimate with sufficient precision the total initial production of the plant. Every 7–20 days, the number of unripe, ripe and dried fruits was assessed. A fruit was considered unripe when it did not have the final blueblack colour of mature fruit. A dry fruit had dry pulp, and it could originate from unripe as well as from ripe fruit. 2.4. Biometric characteristics and spatial distribution of female plants Structural variables of the plants were taken to evaluate the similarity between the studied localities. The height, the diameter of the trunk at 5 cm above the soil, the area of the top projection and the top volume of plants were measured in the marked female plants. The projection area was calculated by the maximum and minimum horizontal measures of the top, and the volume was estimated by similarity to geometric figures (Herrera and Jordano, 1981; Traveset, 1994a). We also measured the distance from the selected female plants to the two nearest male and female plants (Traveset, 1994a; Guitián, 1995). And we evaluated if there was an influence of these biometric characteristics and spatial variables on the fruit production. 2.5. Fruit and seed losses Two different methodologies were used to identify the causes of the fruit loss from the branches: counting fruits in trays placed below the maternal plants, and counting fruits on branches from which animals were excluded. In the first one, 1–3 trays of 800 cm2 were placed under the maternal plant with an 8 mm metallic mesh to prevent access to vertebrates, in a number that was changing according to the projection area of the plant. The content of the trays was collected and
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identified later in the laboratory as whole fruit and whole or broken endocarps. We counted the endocarps (one endocarp per seed) instead of the seeds because the elaiosome adhering to the seeds (Bas et al., 2002) is attractive to ants and stimulates seed removal (Bas and Gómez, 2003; Gómez et al., 2003) and, consequently, counts of the seeds would underestimate their real number. To differentiate the endocarps that had fallen directly off the branches from the ones that were due to depositions, we looked at the external characteristics. The endocarps fallen from the plant still had intact pieces of adhering pericarp or mesocarp, whereas those from excrement were blackish and did not have adhering pulp. In 1998 and 1999, fallen fruits were separated into unripe and mature fruits. In order to quantify pedicel influence on fruit opening the occurrence of the pedicel in fallen fruits was annotated, and we checked if the fruit opened after 25 days in the laboratory. In this way we could also estimate if the free seeds from the trays came directly from the branches or from fruit that opened later on the soil. The second method used consisted in randomly choosing by locality and year 10 additional branches (one per plant) which were excluded using mosquito netting. These exclusions were made when the fruit was developed (3–4 mm diameter) in order to avoid manipulation by rodents, birds and insects. Plants chosen for branchexclusion treatments were located a minimum of 30 m from the plants selected as controls to avoid altering the behaviour of the frugivores or predators in the free branches. Due to the entry of rodents onto some of the selected branches, finally only five exclusions were considered (LOC1 1996, 1997 and 1998; LOC2 1996; and LOC3 1998). The fruits remaining on the excluded branches and the fruits fallen inside the mosquito netting were counted every 7–20 days, distinguishing between unripe and mature fruits. Finally, to find out about the possible predators (of pulp or seeds), direct observations on the branches were made during the whole season and 14 live traps for rodents were installed at each locality.
2.6. Statistical analysis Parametric statistical analyses were used for the analysis of biometric traits of the plants and predispersal seed fate (one-factor ANOVAs) and for test the significance between non-excluded and excluded branches (Student’s t test). Logarithmic transformations were used to normalise the measurements. When the ANOVA was significant, the means were compared using the Scheffé post-hoc test (Zar, 1984). Repeated measure ANOVAs were used to compare the mean fruit production between localities and years. In these cases, the variable “year” was considered as the within-subject effect, and the variable “localities” as the between-subject effect. Locally, we used the v2 of comparison of frequencies and Spearman’s rank correlation test for the comparison of the variables. Data are reported as means (± s.e) and range.
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3. Results 3.1. Total fruit production and characteristics of female plants Annual variability in initial production of fruit was considerable. Production by the same plant varied from 1.3 to 122.0-fold (mean ± s.e. = 13.3 ± 27.5 fold, n = 20) between years in LOC1, 1.6 to 41.5-fold (7.3 ± 9.7, n = 17) in LOC2 and 1.0 to 154.0-fold (21.5 ± 35.1, n = 20) in LOC3. Across years, there was no tendency for some plants to always produce many fruits, and other plants to always produce fewer fruits. Interrelation only exists in LOC1 and LOC2 of the year 1997 and 1998 (rs = 0.60, P = 0.005, n = 20 trees and rs = 0.71, P = 0.001, n = 17 trees, respectively). The estimated total production of fruits (fruits/m3) was different between localities and years (Fig. 1). A repeatedmeasure ANOVA indicated no significant effects of year (F2,35 = 0.22, P = 0.64) and localities (F1,35 = 1.15, P = 0,29) on total fruit production; however, there was a significant effect of their interaction (F2,35 = 5.72, P < 0.05). At LOC3 there was a significant effect of the year on fruit production (F1,19 = 23.0, P < 0.05). The female plants showed important variability in biometric characteristics and in spatial distribution (Table 1). Significant differences between the localities were observed for four of the measured variables (height F2,24 = 13.40, P < 0.05; stem diameter F2,24 = 5.06, P < 0.05; projection area F2,24 = 8.93, P < 0.05; top volume F2,24 = 11.94, P < 0.05). However, these differences were due only to differences between LOC3 and the two localities of Les Gavarres (LOC1 and LOC2) (Scheffé post-hoc test, P <0.05), due to the smaller plant size in El Montgrí (LOC3). On the other hand, plant density was twice as high in LOC1 and LOC2 as in LOC3 (Table 1). The structural variables were intercorrelated (Spearman correlation, P < 0.05 for each pair of variables) and initial fruit production (fruit/m3) did not show a significant correlation with any of these four variables (P > 0.05). There was no relationship between initial fruit production (fruit/m3) and the nearest neighbour distances for any of the localities and years analysed (P > 0.05).
Fig. 1. Estimated fruit production/plant (dark columns) and fruit number/m3 (white columns) at the three study localities and for different years (LOC1, n = 20 plants; LOC2, n = 17 plants; and LOC3, n = 20 plants). Vertical bars denote standard errors of the mean.
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Table 1 Biometric characteristics and spatial distribution of Rhamnus alaternus female plants at three study localities (mean ± s.e. (range)). Study areas: Les Gavarres (LOC1: Mas de la Figuera; and LOC2: Aigua Blanca) and El Montgrí (LOC3: Aixart d’en Pi) Height (m) Long diameter (m) Short diameter (m) Projection area (m2) Top volume (m3) Stem diameter (cm) Distance to first nearest female plant (m) Distance to second nearest female plant (m) Distance to first nearest male plant (m) Distance to second nearest male plant (m)
LOC1 (n = 20 plants) 2.91 ± 0.76 (1.90–4.50) 2.22 ± 0.91 (0.80–4.40) 1.59 ± 0.61 (0.70–2.80) 3.13 ± 2.35 (0.44–8.36) 1.74 ± 1.71 (0.14–6.27) 6.55 ± 3.72 (2.00–15.00) 2.47 ± 1.85 (0.40–8.40) 5.08 ± 3.02 (1.50–11.00) 2.84 ± 2.15 (0.25–8.75) 6.12 ± 2.84 (2.00–11.50)
LOC2 (n = 17 plants) 3.67 ± 0.81 (2.20–5.10) 2.26 ± 0.87 (1.10–3.80) 1.91 ± 0.78 (1.10–3.70) 3.87 ± 3.09 (0.95–11.04) 2.60 ± 2.47 (0.41–8.28) 5.35 ± 3.14 (2.00–15.00) 2.56 ± 1.94 (0.10–7.00) 4.69 ± 2.88 (1.10–11.50) 2.37 ± 2.06 (0.25–8.50) 5.09 ± 3.34 (2.00–16.50)
LOC3 (n = 20 plants) 2.33 ± 0.83 (1.10–4.50) 1.40 ± 0.55 (0.80–2.90) 1.15 ± 0.49 (0.60–2.30) 1.46 ± 1.23 (0.38–5.24) 0.63 ± 0.68 (0.10–2.79) 3.69 ± 1.45 (1.60–6.10) 5.77 ± 4.96 (1.10–2.10) 9.75 ± 7.02 (3.50–33.00) 6.13 ± 5.24 (0.80–18.00) 9.41 ± 6.79 (2.00–25.00)
3.2. Phenology of fruit production and ripening
3.4. Fruit and seed fall underneath branches
Mature fruits were present on plants from the beginning of April to mid-August (Fig. 2), i.e. during 102.4 ± 26.7 (57– 150) days. A total of 53.7 ± 16.5 (19–73) days passed from the beginning of maturation until the period of maximum presence of mature fruit (beginning of June–July). This maximum presence of mature fruits in the branches never exceeded 30% of the initial production, though in July and August it sometimes accounted for 100% of the remaining fruit (finally dried) (Fig. 2). Dry fruits include both unripe and mature fruits that had dried on the plant. Dry fruits always accounted for only a small (4.9 ± 2.8%) proportion of the whole initial production. Depending on the locality and year their number varied from 0 to 658.4 (150.6 ± 226.3, n = 8) dry fruits/m3. Dried fruits remained present on plants for 32–89 (63.5 ± 22.7, n = 8) days beyond the period of maximum presence of mature fruits. Total production (fruit/m3) was not related either to the date at which maturation began on the plant (rs = 0.18, P > 0.05) or to the entire number of mature fruits produced by the plant (rs = 0.69, P > 0.05). Also, total production (fruit/m3) was independent of the period (days) during which fruit was kept on the branches and from the time elapsed until maximum maturation (rs = 0.14, P = 0.74 and rs = 0.02, P = 0.95, respectively).
A total of 442 ± 413 fruits/m2 (49–1214, n = 7) were collected, which represented a total fall of 1879 ± 2873 (134–8286, n = 7) fruits per plant (Fig. 3). We have found 208 ± 199 (47–564, n = 7) seeds/m2, which means 589 ± 717 (180–2176, n = 7) entire seeds/plant (Fig. 4). Fruit fall (fruits/m2) was different among years in all localities (F1,28 = 73.4, P < 0.05 at LOC2; F1,37 = 10.7, P < 0.05 at LOC3 and F2,52 = 17.4, P < 0.05 at LOC1). Annual differences also appear when we assess the estimated fall per plant (F1,28 = 25.6, P < 0.05 at LOC2; F1,37 = 5.2, P < 0.05 at LOC3 and F2,52 = 10.1, P < 0.05 at LOCl). This fruit fall/plant represented 28.7 ± 10.1% of the estimated fruit production/plant. More unripe fruits than ripe fruits fell from the branches (73.4 ± 12.7%, 60.0–87.5, n = 7), most of the unripe fruits fell with pedicel (90.8 ± 4.2%; 87.8–96.7, n = 4). In contrast, on the branches from which animals were excluded the majority of fallen fruits were mature (84.9 ± 14.7%, 62.2–99.0, n = 5) (v2 = 66.6, P < 0.05). In this case, mature fruits fallen with pedicel were in a minority (42.3 ± 17.1%, 23.7–64.6, n = 4). Once on the soil, the liberation of seeds from the opening of the fruit is very low. Unripe fruits never opened, whereas the mature ones opened in 11.4% (without pedicel) and 1.8% (with pedicel) of the cases. The frequency of free seeds inside the excluded branches was also very low (1.4% of the seeds are free). The phenology of fruit and seed fall below the plants was variable, from the beginning of May until mid-August, with a maximum between June and July (Fig. 5). The first presence of fruits and seeds in the trays did not depend on the initial production (rs = 0.06, P = 0.90 and rs = 0.09, P = 0.85, respectively). Though there was a negative correlation between the beginning of the presence of fruits or seeds in the trays and the time that the fruit remained on the branches, this relation was also not significant (rs = -0.62, P = 0.14 and rs = –0.71, P = 0.07, respectively). The fall of fruits was strongly related to the entire initial production in the majority of localities (rs = 0.67, P < 0.05 and rs = 0.72, P < 0.05 at LOC2 1996 and LOC2 1998, respectively; rs = 0.52, P < 0.05 and rs = 0.61, P < 0.05 at LOC3 1996 and LOC3 1998, respectively; rs = 0.51, P < 0.05 and rs = 0.58,
3.3. Effect of interactions with animals on the phenology and the presence of ripe fruit The exclusion of animals from branches had two important consequences. Firstly, it lengthened the period during which fruits remained on the branches, in extreme cases for more than 2 months (T Student; t = –3.94, P < 0.05) (Fig. 2). Secondly, it increased the proportion of mature fruit on the branches (T Student; t = –6.86, P < 0.05). Whereas in the control branches this proportion was never larger than 30%, on the branches from which animals were excluded it was substantially higher (90%). This indicates that animals, both predators and dispersers, preferentially consume mature fruits.
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Fig. 2. Right and left figures show the number of total fruits (white circles) and mature fruits (dark circles) on branches relative to initial fruit production. Moreover, the left figures show the number of total fruits (white triangles) and mature fruits (dark triangles) on branches excluded relative to initial fruit production on exclusion branches. The grey areas correspond to the difference of the proportion of green (clear area) and mature fruits (dark area) between excluded and non-excluded branches. See Section 2 for details.
P < 0.05 at LOCl 1997 and LOC1 1998, respectively). The fall of whole fruits was strongly related to the fall of entire seeds for the seven combinations of locality and year (rs = 0.86, P < 0.05). 3.5. Predispersal seed predation A total of 1567 ± 1172 (243–3796, n = 7) predated seeds/m2 and 4322 ± 2644 (355–8182, n = 7) predated seeds/plant were collected. The extent of predation depended neither on the initial production of fruit (rs = 0.47, P = 0.29) nor on the number of fruit and entire seeds fallen from the branches (rs = 0.09, P = 0.85 and rs = –0.02, P = 0.97,
Fig. 3. Estimate fruit fall/plant (grey columns) and fruit fall number/m2 (white columns) at the three study localities (LOC1, n = 20 plants; LOC2, n = 17 plants; and LOC3, n = 20 plants). Vertical bars denote standard errors of the mean.
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the mesocarps of unripe fruits, and bugs (Gonocerus insidiator [Coreidae] and Eusarcoris inconspicua [Pentatomidae]) that sucked fluid in mature fruits. Also, some ants (Camponotus piceus, Camponotus lateralis, Lasius cinereus, Linepithema humile and Tapinoma nigerrimum) fed on the sweet pulp of ripe fruits directly on the branches. No predispersal seed predation by ants was observed.
4. Discussion Fig. 4. Number of fallen seeds/m (barred columns), predated seeds/m (white columns), estimated number of fallen seeds per plant (black columns) and estimated number of predated seeds per plant (grey columns) at the three study localities (LOC1, n = 20 plants; LOC2, n = 17 plants; and LOC3, n = 20 plants). 2
2
respectively). Therefore, predispersal predation was not higher in plants producing more fruits. This predation began when fruits had developed (3–4 mm in diameter) (Fig. 5); timing of the beginning of predation did not determine the length of the period that fruit remained on the branches (rs = –0.67, P = 0.10). Judging by the characteristics of manipulated fruit and seeds, and the captures in traps, rodents were the main predispersal predators of seeds, Apodemus sylvaticus at all three localities (79% of all rodents captured), and Mus spretus at LOC3 and LOCl (21% of all captures). The main animals responsible for pulp removal were the caterpillars of Microlepidopterans (Geometridae) that fed on
The entire initial fruit production and the fructification phenology of fruit maturation in R. alaternus showed variability at two levels: (a) temporal, whether in the same period or in different years; and (b) spatial, between the studied localities and between individuals at the same locality. In the north-west of the Iberian Peninsula, the total production of fruit of R. alaternus is not globally related to the characteristics of individual plants or to the spatial situation with regard to nearby male or female plants (Guitián, 1995). Although plant biometry can be important, environmental variables such as temperature, water availability, wind force or soil nutrients probably have greater effects on components of reproductive success (number of flowers, pollinated flowers, etc.) and therefore on the amount of fruits finally matured (Chiarucci et al., 1993). In our study, plant density does not seem to determine pollen availability, proportion of polli-
Fig. 5. Phenology of fruit falling (number/m2, black circles), seed falling (number/m2, black diamonds) and seed predation (number/m2, white diamonds) underneath the maternal plants of R. alaternus at the three studied localities.
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nated flowers and fruit development. As a probable consequence, the number of fruits on the different branches showed a large variability, albeit without clear tendencies between different years. The fruit ripening period of R. alaternus is from the beginning of April until mid-August shows large variability among localities and years. The average period during which mature fruits are present is 100 days, with variation among localities and years (range = 30–135 days). This period does not coincide with those stated for other localities in the Mediterranean basin, e.g., from June to July in Italy (Aronne and Wilcock, 1997), from June to September in the southern France (Debussche and Isenmann, 1992) or from May to October southern Spain (Herrera, 1984a). Nor does the timing of maximum presence of ripe fruit in the middle of the ripening period (beginning June–beginning July) fully coincide with other studies, which mention July (Herrera, 1984a; Debussche et al., 1987). The early fruiting during spring–summer that we detected in R. alaternus is uncommon in species with fleshy fruits in Europe and the Mediterranean basin. In this period only 7–13% of the species in southern Spain bear mature fruit (Herrera, 1984a), compared to 12% in the eastern Mediterranean (Izhaki and Safriel, 1985) and 33% in temperate zones of Europe (Snow and Snow, 1988). Its early fruiting is probably why R. alaternus has not been detected in the majority of frugivore and seed dispersal studies, and why only a few authors mention it (Debussche and Isenmann, 1983; Herrera, 1984a; Sunyer, 1994). Producing fruits in this period might affect seed dispersal by birds, as it coincides with birds’ breeding seasons. Communities of frugivorous birds may be more stable in successive years (Bas, 2001) than are those feeding on fruits during autumn and winter, when the majority of species bear ripe fruits. Abundances of migrating and wintering frugivorous birds are variable between years, leading to interannual differences in zoochory (Debussche and Isenmann, 1983; Herrera, 1984a). The interaction of R. alaternus with animals that continuously remove mature fruits remains demonstrated by the low proportion of mature fruit on control branches (<30% of initial production) compared to excluded branches and the reduction of the period with mature fruit on the control branches. Also, the less rigorous climatic conditions when fruits of R. alaternus mature considerably affect post-dispersal processes, such as the secondary dispersal and predation of seeds by ants (Bas and Gómez, 2003; Gómez et al., 2003). These interactions are less probable in unfavourable periods (Traveset, 1994b; Hulme, 1997; Alcántara et al., 2000). Predispersal losses of seeds from branches are due to three causes: falling of unripe or mature fruit, loss of entire seeds from fruit opening on the branches, and seeds predated on the branches. Predated seeds accounted for 7.5 times more seeds than free seeds fallen from the branches and 1.2 times more seeds than seeds inside fallen fruit. Ripe (84%) and unripe fruits (16%) fall from the branches naturally. Some authors define this gravitational fall of fruit and seeds as a primary
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dispersal mechanism, i.e. “barochory” (Chambers and MacMahon, 1994; Masaki et al., 1994; Kollmann and Pirl, 1995). Though the exclusion trays isolate the rodents, other animals, such as ants or beetles, might get in to remove the diaspores (Beattie, 1985). However, we believe there was no underestimation of the tray counts, since the presence of large harvester ants (genus Messor) or of seed-eating beetles (Carabidae, subfamily Harpalinae) was very low in our case (Bas, 2001), probably because the plants we studied were in places with heavy vegetation cover. Also, the fact that we count the endocarp on trays, which are not attractive to ants (Bas, 2001), could also have helped to avoid this effect (Aronne and Wilcock, 1994; Bas and Gómez, 2003; Gómez et al., 2003). The accumulation of fruits and entire seeds underneath the plants has been detected in other species with fleshy fruits (Sallabanks, 1992), including other species of Rhamnus (Archibold et al., 1997). In R. alaternus the opening of fruit on the branches, with the subsequent fall of free seeds underneath the plants, has already been described (Aronne & Wilcock, 1994). In our study, the fact that the proportion of endocarps without pulp on control branches (13.8%) was much higher than the proportion on animal-excluded branches (1.4%) makes us think that some external mechanism increases this proportion. A built-in mechanism for liberating seeds does not exist, contrary to the proposal of Aronne & Wilcock, (1994). On the other hand, the manipulation of fruit by seed predators and pulp removers on branches, and the opening of the fallen fruits, determine the presence of free seeds on the ground. The observation of moth larvae feeding nocturnally on the pulp of unripe fruit during the period of our study, previously observed in other species of fleshy plants by Krüsi and Debussche (1988) and Alcántara et al. (1997), might explain the direct fall of seeds and endocarps unprotected by pulp. Tits of the family Paridae, potential pulp predators of mature fruits, were not observed eating pulp in the different areas (Bas, 2001). On the other hand, bugs observed sucking fluid from the pulp in mature fruit contribute to the drying of the fruit (Traveset, 1994b), causing them to fall from the branches. Also, physiological stress in periods of adverse climatic conditions (high wind, low water and nutrient availability) can increase the number of fallen fruits. This situation could have occurred in LOC2 in 1998, given the high presence of fallen fruits in all the trays. Unlike in other areas of the Iberian Peninsula where birds are the main seed predators (Herrera, 1984a, Traveset, 1994a, Jordano, 1995b), in our study seed predation was due mainly to rodents, as suggested by our observations of the physical characteristics of the predated endocarps and seeds, our direct observations of Apodemus sylvaticus feeding on branches, and the low density of granivorous birds in the study areas. The rarity presence of other rodents (e.g. Sciurus vulgaris) and granivorous insects suggests that there might only be occasional predispersal predators of R. alaternus seeds. The predispersal predation of seeds by rodents directly
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on woody plants with fleshy fruit has been described on very few occasions (Obeso, 1998). The rodents discard the pulp and eat the seeds, and predate more often on unripe fruits because they have proportionally more endosperm (Jordano, 1989; Traveset, 1994b). Thus, most mature fruits are removed by frugivorous birds (Bas, 2001), whereas the rodents limit the total production of mature fruits available for the dispersers. Fruit selection by rodents has also been detected by Obeso (1998), who described how rodents predated fruits with viable seeds more often than fruits with aborted seeds. In fact, we assume that the predispersal removers of pulp and seeds play a significant role on the reproductive success of R. alaternus, both indirectly due to the reduction in the number of fruits available for the dispersers, and directly by causing loss of viability of the seeds before they have been dispersed. To sum up, the effects of the external factors significantly affect the predispersal fruit ecology of R. alaternus more than do the spatial situation and the specific characteristics of the different plants.
Acknowledgements We are grateful to A. Bou, G. Pasqual, M. Sais and G. Vila for assistance during field and laboratory work. We also thank A. Traveset, J. Guitián and two anonymous reviewers for critical reading and comments of the manuscript. The research was supported in part by MICYT (REN2000-0300C02-02/GLO) and MEC (CGL2004-05240-C02-02/BOS).
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