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- Materials and methods
It has been assumed for a long time that one of the advantages of endozoochory is germination enhancement – that seeds ingested by frugivores germinate in higher proportions, or more quickly, than non-ingested ones (Traveset & Verdú 2002 and references therein). However, an increasing number of studies have shown that such enhancement is far from universal, and that a variety of factors, both biotic and abiotic, may affect the outcome of seed treatment in the frugivores’ digestive tracts (Traveset et al. 2001a, 2001b; Santamaría et al. 2003; Espinar et al. 2004; Verdú & Traveset 2005). This is of crucial importance for determining the quality of a particular disperser for a plant.
The conditions under which germination tests are performed are known to influence germination success (Bustamante et al. 1993; Figueiredo & Perin 1995; Traveset et al. 2001a, 2001b). It is thus important that seed responses to dispersers’ gut treatments are examined in the field, as it is in the natural environment where we can test if a germination enhancement is adaptive or not. So far, most reported information comes from studies carried out under controlled (thus favourable) circumstances, usually in the laboratory (see review in Traveset & Verdú 2002), yet this may often obscure significant differences between treatments (Herrera 2000; Traveset et al. 2001a, 2001b).
On the other hand, most experimental studies that test the effect of gut passage on seed germination have been performed with only one or a few dispersers from all those available for the plant. Birds and non-flying mammals are the frugivorous taxa for which most data are available, as they are important dispersers for a great variety of plants (see review in Traveset 1998). In contrast, little is known about the effect of reptiles (but see Liu et al. 2004, Nogales et al. 2005 and references therein), despite the fact that they are also effective dispersers in some ecosystems, mainly in islands (Olesen & Valido 2003). Studies that compare the effect of different groups of dispersers on germination are scarce and have shown either consistent (Krefting & Roe 1949; Lieberman & Lieberman 1986; Mandujano et al. 1994; Traveset & Willson 1997) or inconsistent results (Lieberman & Lieberman 1986; Figueiredo & Perin 1995; Engel 1997; Nogales et al. 1998; Nogales et al. 2005). The latter are often attributed to the different retention times in the animals’ guts (Izhaki & Safriel 1990; Barnea et al. 1991; Murphy et al. 1993; but see Barnea et al. 1990; Traveset et al. 2001, 2001a, 2001b), although other factors, such as type of food ingested along with the fruits (with variable water content, pH, proportion of plant material, etc.), are likely to influence the level of mechanical or chemical scarification of the ingested seeds (Traveset 1998; Traveset et al. 2001a, 2001b; Figuerola et al. 2002).
In the present study we chose fleshy fruited plant species common in the Mediterranean Basin, plus one endemic to the Balearic Islands, to examine the effect of seed passage through frugivores’ digestive tracts on emergence rate (speed at which seeds emerge), simultaneously examining both in the field and in an experimental garden over 2 years. Here we use the terms ‘germination’ and ‘emergence’ time indiscriminately, although what we actually measured was the time at which the seedling emerges. For five of the species known to be dispersed both by birds and lizards (Sáez & Traveset 1995), we compared the effect of these two types of disperser. Given the much longer time seeds are retained within the digestive tract of lizards (2–4 days) compared to birds (usually 20–30 min), we hypothesized that the former were more likely to have a significant effect on germination patterns. We further predicted that differences in such patterns would not be detected in the field similarly to the experimental garden, due to the more favourable conditions – mainly temperature and humidity – in the latter.
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- Materials and methods
Seed passage through the digestive tract of frugivores has long been found to affect the germinability and/or the germination rate of many plant species, which, together with the seed shadow and the quantity of ‘intact’ dispersed seeds, are essential factors determining plant reproductive and regeneration success (Schupp 1993). However, only a low fraction of studies have performed germination tests in the field, and they have used either one or a few dispersers (Traveset & Verdú 2002). There are also a few studies showing that the experimental conditions under which tests are carried out may lead to different responses in germination, and that such differences are not consistently in the same direction. One group of studies shows that differences in seed germination between treatments are usually magnified under harsh (field) conditions; for example Herrera (2000) detected germination differences between seeds from two pollination regimes only when planted in the field, but not in the glasshouse. Similarly, Traveset et al. (2001a) detected a positive effect of bird ingestion on seed germination in outdoor conditions, but not in a growth chamber or in a glasshouse. Another group of studies shows the opposite direction, with a greater effect in laboratory compared with field experiments (Bustamante et al. 1992, 1993; Figueiredo & Perin 1995; Yagihashi et al. 1998). Finally, a third group of studies finds similar results between the two conditions (Figueiredo & Perin 1995; Figueiredo & Longatti 1997). The present study further confirms, with a larger number of species, that a species may show germination enhancement/inhibition in the field but not under controlled conditions (in the laboratory or glasshouse), and vice versa: a significant effect of ingestion detected in controlled conditions may be screened off in the field. For Rubia, Rubus and Solanum, results were inconsistent and showed an inverse trend depending on seed germination conditions (Fig. 2). This demonstrates the caution needed when interpreting germination experiments that aim to evaluate the influence of frugivores on the quality of dispersal they provide to plants. Our suggestion is that future studies examining the quality of dispersal only under laboratory or garden conditions should also be carried out in the field, in conditions as natural as possible to the particular plant. However, under field conditions results may also depend on environmental and temporal stochasticity.
The present study also provides evidence for inconsistencies in germination responses depending on frugivore species. The effect of Blackbirds and lizards on germination rate was consistently significant only for S. nigrum in the field (germination was accelerated in the two treatments compared with controls), and for Rubus in the garden (seeds ingested by either frugivore germinated more slowly than controls). A previous study on S. nigrum that tested the effect of Blackbirds and Sardinian Warblers (Sylvia melanocephala) on germination in a common garden (Mas & Traveset 1999) showed a similar non-significant effect of the two bird species. Similar results to these (and also including a third bird species, Pycnonotus xanthopygos) were also found by Barnea et al. (1990), although in that case the test was done under laboratory conditions. In both these previous studies, a significantly positive effect was found for S. luteum, which is also consistent with the effect of Blackbirds found in the experimental garden in the present study. In another previous study, seeds of Rubia ingested by Blackbirds had been shown to germinate more slowly than if ingested by Sardinian Warblers (Traveset et al. 2001a); in such study, Rubus seeds passed through Warblers germinated more slowly than those passed through Blackbirds, although neither frugivore affected germinability. One possible explanation for the contrasting results between studies may be that seeds come from different populations, and it is thus possible that they differ in traits related to germination, such as seed coat structure, coat thickness or seed size. The different source of seeds might also be responsible for the contrasting results found for Osyris (the previous study had shown an important germination enhancement in Blackbird-ingested seeds compared with controls). These inconsistencies have been reported in a variety of species (Lombardi & Motta 1995; Nogales et al. 1999; Nogales et al. 2001, 2005). Even seeds of the same population, but of different age, have shown different germination responses to the same treatment (see References in Traveset 1998).
Differences among frugivores have often been attributed to different retention time in the gut (Barnea et al. 1991; Murphy et al. 1993; but see Barnea et al. 1990; Traveset et al. 2001a, 2001b). Gut passage time reported for passerine birds usually ranges between 20 and 60 min (see review in Traveset 1998), whereas for lizards it usually varies from 32 to 96 h (L. Santamaría, unpublished data). However, our results do not show any consistent effect of retention time on germination responses, as all possibilities were found: enhancement, inhibition or neutral effect of ingestion by lizards relative to the effect of Blackbirds. This suggests that other factors, probably interacting with seed retention time, are also important in determining germination speed and success. Significant effects of ingestion on germination have often been attributed to the degree of seed coat scarification, associated with morphological and physiological characteristics of the frugivores’ digestive tracts (Jordano 1992; Traveset 1998). In addition, differences in the chemical composition of food ingested along with seeds can produce great differences both in seed retention time (Murray et al. 1994; Witmer 1996; I. Charalambidou and co-workers, unpublished data), and in mechanical or chemical abrasion of the ingested seeds (Clench & Mathias 1992) – with direct consequences for germination behaviour.
Seeds of most plant species tended to lose weight after passing through Blackbirds’ digestive tract, a result consistent with that of Traveset et al. (2001a). The outcome probably depends on seed coat structure, not examined in this study. Interestingly, results for the common species (Rubus, Rubia and Osyris) in that previous study and the present one were consistent only for Rubia; in contrast, seed weight of Rubus and Osyris in Traveset et al. (2001a) did not change, or significantly decreased, respectively, after bird ingestion. These inconsistencies may again be attributed to the particular seed traits of each species and population. Moreover, even the gut structure and food composition of each individual frugivore probably affect changes in seed weight. Ongoing research that examines the effects of individual plant and frugivore differences is expected to shed more light on this issue.
In the recent review by Traveset & Verdú (2002), seed ingestion by birds was found to have a significantly greater positive effect on germination than seed ingestion by either non-flying mammals or reptiles, which was mainly attributed to the shorter gut-passage time of the former. The results found in the present study do not follow this trend for most species tested. It is thus clear that a great heterogeneity of results exists, and we are still far from being able to predict the consequences for a given species with particular seed traits and in a particular environment. It is important to note that, even if seed treatment in the frugivore gut enhances germination, this does not necessarily suggest a positive effect on performance of the future plant – specifically on seedling fitness, growth and plant fecundity (Verdú & Traveset 2005).
The microhabitat where the defecated seed is deposited may determine the ultimate success of the seedling and future plant (Rey & Alcántara 2000; Traveset et al. 2003), and is perhaps even more important than the effect of seed treatment in the gut. For this reason, to know the quality of a disperser for a given plant we should combine the effect of ingestion on seed germination change with that of depositing the seeds in different microhabitats. A particular microhabitat may be more suitable for germination and seedling establishment than others but, in turn, may enhance germination of an ingested seed more than others. This possible effect of abiotic conditions has been tested recently with two helophytes (Scirpus littoralis and Scirpus maritimus); seeds ingested by ducks show a higher germination rate than control seeds under low salinity but not under high salinity (Espinar et al. 2004). Further research on how the abiotic environment influences seed germination responses to ingestion by frugivorous species is necessary in order to clarify the qualitative importance of seed dispersers for plant reproduction.