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Keywords:

  • Frugivory;
  • germinability;
  • rate of seedling emergence;
  • seed ingestion;
  • seed mass

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References
  10. Appendix
  • 1
    On the west coast of Norway, Turdus spp. (Thrushes) are important dispersal agents of Sorbus aucuparia L. (Rowan) seeds, and avian and mammalian gut treatment often alters seed germination characteristics. In the present study the effects of avian gut treatment on S. aucuparia seeds are described, with emphasis on subsequent seedling growth.
  • 2
    Seeds ingested by Turdus spp. and non-ingested control seeds were sown singly or multiply in soil, in pomes, or in bird droppings.
  • 3
    Defecated seeds were ≈9% heavier than control seeds, and seedling growth was faster from defecated seeds than controls. In addition, differences in the rate of seedling emergence were found, with seedlings from ingested seeds appearing first.
  • 4
    The increased growth may be due to seedlings emerging earlier from defecated seeds, giving them an extended growth period at a time of increasing day length.
  • 5
    We argue that factors such as seedling growth, rate of seedling emergence and seed mass, in addition to percentage seed germination, are important in determining seedling survival.

Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References
  10. Appendix

When studying what avian seed ingestion means for seed and seedling survival, the advantages of seed movement away from parent plants are well known (reviewed by Schupp 1993). Avian seed ingestion increases, decreases, or has no influence on seed germination (Barnea, Yom-Tov & Friedman 1990; Holthuijzen & Sharik 1985; Murray 1988). In a review, Traveset (1998) found that enhancement of germination occurs about twice as often as inhibition, and germination is more likely to be enhanced in trees and shrubs in the temperate zone than in the tropics. Factors such as retention time, type of food ingested with fruits, and seed coat structure and thickness also influence germination responses (Traveset 1998).

It is commonly considered advantageous for the plant if germinability (defined as final germination percentage) is increased. Likewise, it is disadvantageous for the plant if seed ingestion reduces germination success (Holthuijzen & Sharik 1985; Krefting & Roe 1949; Murray 1988). Mechanical or chemical scarification of the seed coat, which makes it more permeable to water and gases (Agami & Waisel 1988; Barnea et al. 1990; Izhaki & Safriel 1990); the escape from germination inhibitors in fruit pulp (Ketring 1973; Rick & Bowman 1961; Temple 1977); and fertilizing effects of faeces, especially following mammalian gut passage (Dinerstein & Wemmer 1988; Quinn et al. 1994; Traveset, Bermejo & Willson 2001a), are mechanisms by which frugivores affect seed germinability and germination rate (defined as speed of seed germination). Moreover, with regard to fertilizing effects, Traveset et al. (2001a) found that seeds of Rubus spectabilis Pursh had a higher germination rate when germinated in animal manure (from Ursus arctos L., Brown Bears) than in manure containing fruit pulp or vegetation fibre. No such effect was found for Vaccinium ovalifilium Smith ex Rees/alaskaense Howell, although all seedlings grew faster when fertilized by animal manure. Traveset et al. (2001a) argued that this is due to high concentrations of calcium phosphate. Seed size also influenced how seeds are affected by gut treatment. Small seeds are retained longer in the digestive tract and thus are more likely than large seeds to be abraded, and this explained why germination rates of small seeds increased while those of larger seeds did not (Traveset & Verdú 2001; Traveset, Reira & Mas 2001b).

On the west coast of Norway, the density distribution of Sorbus aucuparia L. (Rowan) corresponds to the main autumn migration route and stopover sites of Turdus spp. (Thrushes), with the highest density of trees and Turdus spp. in the outer coastal regions (personal observation). Ringing recoveries show that these birds emanate from Fennoscandia and North-west Russia, and that they spend several weeks in Norway before embarking on their southbound migration. Thus, Turdus spp. are potentially important dispersal agents of S. aucuparia seeds. The objective of this study is to examine whether S. aucuparia seeds also benefit from avian gut passage with respect to seed germination and seedling growth. In a follow-up study, the effect of gut passage on seed mass is also examined. We discuss the ecological implications for the plant and possible mechanisms explaining our findings. This study is the first to describe an increase in seed mass and seedling growth following avian gut passage of seeds.

Materials and Methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References
  10. Appendix

Study Species

Sorbus aucuparia is a deciduous tree 15–20 m high and has multiseeded orange pomes in clusters. The pomes are two- to five-celled, with one or to two small, brown seeds in each cell (Raspé, Findlay & Jacquemart 2000). Sorbus aucuparia seeds have embryo and seed coat dormancy, both of which can be broken by cold stratification (Devillez, Fraipont & Tissot 1980; Flemion 1931; Zentsch 1968). With a mean diameter of ≈9 mm, S. aucuparia pomes are swallowed whole by all but the smallest frugivores (Snow & Snow 1988).

Turdus spp. were the only frugivorous birds feeding on S. aucuparia pomes present at the time of seed collection. Although Turdus iliacus L. (Redwings) were the dominant species, Turdus merula L. (Blackbird), Turdus pilaris L. (fieldfare), and Turdus philomelos Brehm (Song Thrush) were also present. All are migratory birds between ≈21 and 27 cm in length, foraging mainly on fruit in autumn and winter (Cramp 1988). Turdus spp. are classified as dispersers rather than seed predators (Herrera 1984). Meal sizes for T. merula (mean weight ≈100 g) are about 10 fruits with diameters 8–10 mm (≈7 g). A meal is taken in about 1 min, with an interval of about 20 min between meals (Snow & Snow 1986). We were unable to distinguish droppings from the different species.

Seedling Emergence and Growth

The seeds and pomes used in the growth study were collected 13–14 October 1995 on Turøy (60°27′ N, 04°55′ E) in western Norway. Approximately 150 droppings containing S. aucuparia seeds were collected from slopes of naked rock near the only deciduous spinney on the island. Twenty clusters of pomes were picked arbitrarily from the first 10 S. aucuparia trees found. All seeds extracted from droppings, and a corresponding number of seeds from pomes (nearly all), were sown.

The seeds were extracted by hand from pomes and droppings, and sown as described below, allowing us to study the response of seed gut passage on seedling emergence and seedling growth under six different germination conditions. As seeds aggregate in varying numbers in bird droppings, we sowed seeds singly (120 pots) or in groups of two (72 pots), three (72 pots), and four (72 pots). In addition, single seeds were sown in arbitrarily selected bird droppings (120 pots) and in pomes (120 pots). When sown in pomes, seeds were placed in arbitrarily selected cores which were then reinserted in the pomes (again arbitrarily selected). Ingested seeds would, of course, never be reinserted in pomes under natural conditions, but as the main objective was to study the effect of gut passage on seedling growth, and as seeds sometimes germinate in S. aucuparia pomes, we included this option in the present study. We believe that due to rainy and snowy winter conditions, seeds sown directly in soil best simulate natural Norwegian conditions. To examine if the opening of pomes influenced seed emergence, single unopened pomes (60 pots) were also sown.

The seed groups were all sown in Jiffy pots (made of compressed peat) on 23–25 October 1995. A commercial potting soil was used (Huminal plantejord, Norsk Hydro). When sowing, the pots were nearly filled with soil (approximately 5 mm from the brim), the seed(s) were added (in a pile when more than one seed), and additional soil was added giving a sowing depth of ≈5 mm.

To break the embryo dormancy (Devillez et al. 1980; Flemion 1929; Zentsch 1968) under natural conditions, all pots were dug down to turf level on a germination site in an open field at Homme (at the southernmost tip of Norway, 58°03′ N, 07°17′ E) on 27 October 1995. To offer some protection from black frost they were covered with a thin cloth and Horse Chestnut (Aesculus hippocastanum L.) leaves. On 26 April 1996, cloth and leaves were removed and the emerging seedlings were tallied daily. Day of emergence is defined as the day when a seedling was first visible.

Exactly 28 days after emergence, each growing seedling was moved from the germination site and placed in the middle of a 30 × 30 cm square of turned turf. To avoid interaction between the growing seedlings they were placed 1 m from neighbouring seedlings. Vegetation in this field consists mainly of Trifolium pratense L., Trifolium repens L. and the grasses Phleum pratense L., Festuca pratensis Huds. and Poa pratensis L. The field site was watered regularly twice a week during the growing season, and the grass around the seedlings mown once a week. During seedling emergence, the maximum temperature increased steadily from 7·4 °C on 27 April to 10·6 °C on 12 May. During the same period, cloud cover thinned out gradually. Mean temperature and precipitation in the summer of 1996 were 14 °C and 43 mm, respectively (data from the nearby Lindesnes Weather Station, ≈15 km, courtesy of the Norwegian Meteorological Institute, DNMI).

Eight weeks after the individual day of seedling emergence, the growth variables (length of stem, leaf number, and length and width of longest leaf) were recorded for the first time. These measurements were repeated every 4 weeks through the whole of the first growth season. The seedlings’ stem length was measured from ground level to apical shoot using a folding ruler. The number of fully expanded leaves was counted, and length and width of the longest leaf measured with a slide caliper. The length was defined as length from the rachis at the petiole base of the first pair of (innermost) leaflets to the tip of the apical leaflet. The width was defined as length from tip to tip of the same first pair of leaflets. All growth variables were measured to ±0·5 mm. Where there were more than one seedling per pot, the seedlings with the longest stems after 8 weeks were measured, irrespective of how many seedlings were growing in the pot. (An unequal number of growing seedlings in pots where more than one seed was sown is assumed to increase the group variance, and increased variance yields a more conservative statistical test result.) Only pots where the initial number of seedlings survived the whole season were used in calculations. Seeds sown in pomes were excluded from the growth experiment due to few emerging seedlings.

Seed Mass

As seedlings from defecated seeds grew larger than control seedlings, we decided to examine the effect of ingestion on seed mass. During 19–22 October 1996, two T. merula were held in captivity, starved for 12 h overnight, then fed only S. aucuparia pomes. To prevent the birds from feeding selectively on larger pomes, they were fed limited amounts and not given a fresh supply until all pomes were eaten. Water was freely available.

The pomes were collected (on Turøy) from 30 arbitrarily selected S. aucuparia trees on 17 and 19 October 1996 (again the first trees we could find). Two clusters of pomes were arbitrarily picked from each tree, one for each treatment group (randomly assigned), so that half the pomes were given to the birds while the seeds from the remainder were extracted by hand. The resulting bird droppings were allowed to dry, then crumbled, and the seeds removed by hand. The seeds from both treatments were briefly (<60 s) submerged in water to wash off remainders of dropping or fruit flesh adhering to the seeds. Floating seeds, believed to be incapable of germination, were removed from the sample. All seeds were allowed to dry at room temperature for 2 weeks. Both samples consisted of a little over 500 seeds. A random subsample of 250 was drawn from each treatment and the seeds were weighed individually to an accuracy of ±0·1 mg. To examine if water absorption caused the differences observed, 50 new seeds, again selected at random from both treatments, were weighed and placed in an electric airing cupboard at 50 °C until constant weight was achieved. They were then left to adjust to room humidity and weighed again. The mean mass of the 50 dried seeds, as a percentage of original weight, was calculated for both treatments and used to individually correct the weight of the original two sets of 250 seeds. These converted values were then tested statistically.

Statistics

Several different statistical methods, all with critical P values set to 0·05, were used due to the various experimental designs and the nature of the experiments.

A Student's t-test was used to test for differences in mean seed mass between ingested and control seeds. When testing for differences in percentage seedling emergence, the χ2 goodness of fit procedure was followed according to Zar (1996), using the Yates correction for continuity. According to Fox (1993), failure–time analysis should be used when testing for differences in rate of seedling emergence. The Wilcoxon life-table method was applied as it is most sensitive to differences early in the time series when testing for differences in homogeneity of the seedling survivorship functions (SAS Institute Inc. 1989).

Repeated measures ancova (SAS Institute Inc. 1989) was used to compare the seedlings’ growth performance of the single growth parameters length of stem, number of leaves, and length and width of longest leaf. Day of emergence was treated as a covariate to exclude random differences in weather conditions. (For an introduction to repeated measures, consult von Ende 2001.) For an overall comparison of the seedlings’ growth performance, combining probabilities were conducted according to Sokal & Rohlf (1995). The doubly multivariate repeated-measures manova design (SAS Institute Inc. 1989) is unsuitable for our data due to the decrease in power of the test with increasing number of dependent variables in combination with low sample size (von Ende 2001).

Homogeneity of variance was tested using the Box M multivariate test procedure. Critical P value was set to 0·01. Log transformation (in measures of length) and square root transformation (in counts) were used in cases where the Box M-tests indicated unequal variances (Sokal & Rohlf 1995).

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References
  10. Appendix

Seed Mass

The dry weight ranges of ingested and control seeds were 1·1–5·0 and 1·0–5·5 mg, respectively, and seeds that had passed through the digestive system of T. merula weighed more than those extracted from pomes. The mean difference between the two seed treatments amounted to 0·27 mg or 9% (mean ± SE weight of experimental seeds = 2·98 ± 0·061 mg, n = 250; mean weight of controls = 2·71 ± 0·052 mg, n = 250; t = 3·302, df = 487, P < 0·001). Drying reduced the mean weight of seeds taken from pomes and droppings to 95·3 and 94·6% of the original weight, respectively.

Seedling Emergence

Irrespective of treatment, >80% of the single seeds emerged, as did 70% of the seeds sown in bird faeces (Fig. 1). As the number of seeds sown per pot increased from one to four, the percentage seedling emergence decreased steadily from about 85 to 60% for the control seeds, and from 80 to 70% for the treated seeds. These variations in percentage seedling emergence were statistically different only when four seeds were sown together (χ2 = 4·427, df = 1, P < 0·001). As expected, percentage seedling emergence dropped in seeds sown in pomes, and fewer than 30% of these seeds sprouted. None of the seeds in unopened pomes emerged.

image

Figure 1. Percentage seedling emergence from ingested and control seeds.

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In pots with one to three seeds, seedlings from defecated seeds emerged several days earlier than those from the control group (Fig. 2a–c), giving differences in survivorship functions (single seed: χ2 = 15·91, df = 1, P < 0·001; two seeds: χ2 = 25·25, df = 1, P < 0·001; three seeds: χ2 = 24·61, df = 1, P < 0·001). Single seeds sown in bird droppings were an exception to this pattern, with control seedlings emerging first (Fig. 2e, χ2 = 4·06, df = 1, P = 0·044). When four seeds were sown together, and when single seeds were sown in pomes, no differences in germination pattern were found (Fig. 2d,f, four seeds: χ2 = 1·47, df = 1, P = 0·23; Single seed in pomes: χ2 = 0·71, df = 1, P = 0·40).

image

Figure 2. Rate of seedling emergence. Day of emergence represents the day seedlings were first visible counted from the day the first seedling emerged. (•) Ingested; (○) control groups.

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Seedling Growth

Seedlings from ingested seeds showed better growth performance with regard to overall growth when combining the four variables: number of leaves, growth of stem, and length and width of largest leaf compared to control seedlings. Either the growth curves of seedlings from ingested seeds have a faster rate of increase, or the level of the growth curves was higher for the ingested than the control seedlings (Table 1; see Appendix for detailed test statistics). In most cases this difference in growth between treatments was also evident for the four individual variables (Table 1;Appendix).

Table 1.  Growth of seedlings and summary P values from the repeated-measures ancova on the single-growth variables of Sorbus aucuparia stem length, number of leaves, and length and width of longest leaf from ingested (exp.) and control (cont.) groups during the 1996 growth season
Growth variableTreatmentnMean value ± SD Age of seedlings in weeks Parallelism: PLevel: P
8121620
  1. The parallelism hypothesis tests for differences in shapes of the growth-response curves; the levels hypothesis is a comparison of levels of the same curves. The latter is of interest only if shapes are found not to differ (parallelism: P > 0·05). All seedlings grew larger during the summer (time: P < 0·067). Detailed test statistics are given in the Appendix. Combining probabilities gives information on the overall growth performance of the seedlings when all four growth variables are combined.

Length of stems (cm):
Single seedexp.180·94 ± 0·201·53 ± 0·412·15 ± 0·562·75 ± 0·860·003 
 cont.320·93 ± 0·301·48 ± 0·602·15 ± 0·912·54 ± 1·20  
Two seedsexp.121·16 ± 0·231·74 ± 0·312·66 ± 0·573·55 ± 1·320·6330·011
 cont.141·08 ± 0·451·91 ± 1·022·44 ± 1·442·90 ± 1·65  
Three seedsexp.181·27 ± 0·302·18 ± 0·453·15 ± 1·423·97 ± 1·490·037 
 cont.141·31 ± 0·352·12 ± 0·652·91 ± 0·813·84 ± 1·39  
Four seedsexp.161·35 ± 0·372·00 ± 0·542·84 ± 1·123·76 ± 1·920·001 
 cont.201·26 ± 0·291·90 ± 0·562·41 ± 0·823·15 ± 1·57  
Single seed in droppingexp.210·95 ± 0·291·74 ± 0·592·26 ± 0·692·87 ± 1·050·006 
 cont.160·89 ± 0·241·38 ± 0·401·88 ± 0·592·43 ± 0·90  
Number of leaves:
Single seedexp.182·45 ± 0·634·55 ± 0·896·75 ± 1·547·58 ± 1·930·0590·333
 cont.322·83 ± 0·694·53 ± 1·496·33 ± 2·467·21 ± 2·96  
Two seedsexp.122·90 ± 0·495·13 ± 0·547·04 ± 0·898·41 ± 1·480·4140·735
 cont.142·79 ± 0·614·44 ± 1·635·84 ± 3·186·58 ± 3·55  
Three seedsexp.183·01 ± 0·745·56 ± 0·847·98 ± 0·928·74 ± 1·510·2180·021
 cont.143·18 ± 0·974·13 ± 1·227·66 ± 1·948·64 ± 2·65  
Four seedsexp.163·13 ± 0·875·21 ± 0·947·61 ± 2·138·21 ± 2·210·001 
 cont.202·40 ± 0·694·93 ± 1·127·16 ± 1·447·84 ± 2·17  
Single seed in droppingexp.213·07 ± 0·705·14 ± 0·766·99 ± 1·777·94 ± 2·030·0830·719
 cont.162·55 ± 0·534·35 ± 0·975·95 ± 1·607·16 ± 2·45  
Length of longest leaf (cm):
Single seedexp.180·95 ± 0·201·52 ± 0·492·77 ± 0·903·55 ± 1·370·001 
 cont.320·89 ± 0·161·41 ± 0·682·53 ± 1·613·11 ± 2·12  
Two seedsexp.121·09 ± 0·141·55 ± 0·353·03 ± 0·854·55 ± 1·230·1170·078
 cont.141·01 ± 0·281·74 ± 1·102·75 ± 2·143·47 ± 2·89  
Three seedsexp.181·16 ± 0·121·90 ± 0·623·75 ± 1·164·85 ± 1·650·8900·832
 cont.141·10 ± 0·191·95 ± 0·673·67 ± 1·324·52 ± 1·49  
Four seedsexp.161·16 ± 0·251·74 ± 0·763·59 ± 1·804·27 ± 2·280·001 
 cont.201·06 ± 0·191·67 ± 1·112·97 ± 1·323·71 ± 1·72  
Single seed in droppingexp.210·97 ± 0·191·58 ± 0·542·92 ± 1·493·58 ± 1·800·006 
 cont.160·81 ± 0·161·04 ± 0·391·99 ± 0·942·60 ± 1·22  
Width of longest leaf (cm):
Single seedexp.180·79 ± 0·201·14 ± 0·261·46 ± 0·521·83 ± 0·640·029 
 cont.320·88 ± 0·191·06 ± 0·421·36 ± 0·551·52 ± 0·67  
Two seedsexp.120·87 ± 0·171·00 ± 0·181·62 ± 0·331·92 ± 0·590·0710·025
 cont.141·07 ± 0·251·26 ± 0·571·52 ± 0·711·71 ± 0·96  
Three seedsexp.181·01 ± 0·161·21 ± 0·361·79 ± 0·492·05 ± 0·610·9840·515
 cont.141·04 ± 0·201·29 ± 0·361·68 ± 0·411·74 ± 0·50  
Four seedsexp.160·97 ± 0·251·26 ± 0·591·86 ± 0·662·15 ± 0·900·001 
 cont.200·92 ± 0·181·20 ± 0·371·53 ± 0·531·82 ± 0·65  
Single seed in droppingexp.210·93 ± 0·211·16 ± 0·321·54 ± 0·461·76 ± 0·450·010 
 cont.160·79 ± 0·120·91 ± 0·221·21 ± 0·371·45 ± 0·59  
Combining probabilities:      inline imageinline image
Single seed      0·001 
Two seeds      0·1400·005
Three seeds      0·2710·084
Four seeds      0·001 
Single seed in dropping      0·001 

Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References
  10. Appendix

To prevail in the competition for survival a seedling has to outgrow its competitors. The results from the growth study show that treated seedlings grew better in their first growth season compared to control seedlings. Similar findings in other studies have been attributed to fertilizing effects by manure deposited along with seeds (Dinerstein & Wemmer 1988; Quinn et al. 1994; Traveset et al. 2001a). This can be discarded as the reason in this study, as seedlings sown without droppings showed the same increased growth. Other findings in this study suggest three explanations for this difference in growth performance. First, seedlings from treated seeds emerged earlier in spring, thus enjoying an extended growth period with increasing day length compared to control seedlings. Second, seed coat abrasion can reduce germination energy costs. Third, seed mass increased following gut passage.

Seedling Emergence

Mechanical and chemical scarification of the seed coat might explain both the observed displacement in rate of seedling emergence, and reduced energy spent on germination. If defecated seeds have a thinner seed coat with enhanced permeability to gases and water (Barnea et al. 1990; Crocker & Barton 1957), this could reduce the time needed to initiate germination (Howe & Smallwood 1982; Howe 1977; Glyphis, Milton & Siegfried 1981). It could also reduce the time because lower internal pressure is needed to crack open the seed. Both these factors will contribute to prolonging the growth season and explaining the differences in rate of seedling emergence observed between ingested and control seeds. However, Pulliainen & Erkinaro (1978) show that the surface structure of S. aucuparia seeds having passed through the digestive system of Bombycilla garrulus L. (Waxwing) was similar to control seeds. On the other hand, as Snow & Snow (1988) claim that B. garrulus is physiologically better adapted than Turdus spp. to a pure fruit diet, and Herrera (1984) found that fruit specialists have shorter mean times for gut passage than non-specialists, this might result in longer gut retention time and thus more seed coat abrasion in Turdus spp. than in B. garrulus. However, Pulliainen & Erkinaro's (1978) findings could also indicate that the seed coat of S. aucuparia seeds are robust to scarification while in the gut, although the composition of ingested foods and seed size also influences the level of scarification (Traveset 1998; Traveset & Verdú 2001; Traveset et al. 2001b; Traveset, Reira & Mas 2001c). Emerging early in spring, however, can also be a hazard. Traveset et al. (2001b) showed that early germination in relatively dry years might not be advantageous, but this kind of water stress is less likely to occur in the wet and rather cold Norwegian summer.

In addition to the benefit of a prolonged growth season, mechanical and chemical scarification of the seed coat might also reduce seed germination energy costs by making it easier for the hypocotyl to break out of the seed. The saved energy could then be spent on subsequent seedling growth. This could explain the finding that seedlings from ingested seeds grew faster than controls when sown singly in droppings, even though control seedlings emerged first. Our findings suggest that ingestion by Turdus spp. may give the emerging S. aucuparia seedlings a head start in the short Nordic growth season, and thereby an advantage in the fight for survival.

With regard to seedling emergence in general, the proportion of emerging seedlings differed between treatments only when four seeds were sown together. However, percentage seedling emergence appears to be influenced by factors such as crowding, bird droppings, and being embedded in or removed from pomes. No emergence from unopened pomes, and greatly reduced emergence from seeds reinserted into pomes, were expected due to the presence in the pomes of the germination inhibitor parasorbic acid (Ketring 1973). We believe that the reduction in seedling emergence when sown in bird droppings is due to an excess of nutrients or unfavourable pH in addition to the inhibitor, but this needs to be tested. Crowding also influenced seeds from the two treatment groups. In both groups, percentage emergence decreased as the number of seeds sown together increased. Control seeds suffered more severely from this grouping depression than did the seeds from the experimental groups, and as the number of seeds sown together reached four, this difference became statistically different. We have no explanation as to why control seeds had reduced seedling emergence as a function of seedling density while ingested seeds did not. A few other studies have suggested that crowding depression is due to excretion of growth inhibitors by seeds or seedlings (Barnea, Yom-Tov & Friedman 1992; Crocker & Barton 1957), although this has, to our knowledge, never been demonstrated.

Seed Mass

Several authors have demonstrated a positive correlation between seedling size and seed mass (Stanton 1984; Wulff 1986; Zimmerman & Weis 1983), and Zhang & Maun (1993) argued that endosperm mass, rather than embryo size, is the major determinant of seedling size. The dry weight ranges of seeds found in this study (ingested seeds 1·1–5·0 mg; control seeds 1·0–5·5 mg) were larger than the 1·15–4·14 mg range reported for S. aucuparia by Raspéet al. (2000).

The increase in seed mass found in the present study also contrasts with findings of Traveset et al. (2001c) where seed weight of Rubia peregrina L., Osyris alba L. and Phillyrea spp. decreased after passage through T. merula guts. Those authors found no differences in seed coat thickness between treatments, indicating that reduction of the seed coat cannot explain the reduction in seed mass following gut passage.

We have no explanation for the observed 0·27 mg (9%) increase in mean seed mass, as no chemical analyses were conducted on the seeds, but the selection of large pomes by birds (Guitian et al. 1994) can be excluded as all pomes given to the birds were consumed. Hence we do not know if this increase in seed mass results in increased seedling growth. This finding suggests that S. aucuparia seeds increase in mass following avian gut passage, but biochemical analyses must be conducted before we can understand the mechanisms and implications of this phenomenon.

Conclusion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References
  10. Appendix

The present study shows that, in addition to seed dispersal, at least for S. aucuparia, avian gut treatment is also advantageous to seedling growth for several reasons. First, growing larger more quickly is a clear advantage in seedling competition. Second, a larger seedling with a deeper root system should be more resistant to drought (Fenner 1985). Third, larger leaves should also improve the seedlings’ ability to endure browsing by small herbivores such as snails (Fenner 1985). Finally, larger seedlings have an increased winter survival rate (Maruta 1994) and will presumably get a head start in spring by having more food reserves in the roots than smaller seedlings. Therefore it is reasonable to assume that, even if there is a reduction in percentage germination following avian seed ingestion (traditionally believed to be disadvantageous to the plant), this may be compensated for, or even outweighed, by an increase in the seedlings’ competitive abilities due to increased growth.

We suggest that ingestion of S. aucuparia seeds by Turdus spp. increases seedling growth by reducing the energy costs of germination and reducing the seedlings’ time of emergence compared to seedlings from control seeds, and that these are contributing factors explaining the distribution of S. aucuparia trees on the west coast of Norway. The effect of seed ingestion on rate of seedling emergence and seedling growth must be addressed, as well as percentage germination and effect on seed mass, before further conclusions can be drawn about the advantages or disadvantages of avian seed ingestion. In addition, mechanisms explaining these findings are urgently required.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References
  10. Appendix

We thank the Faculty of Mathematics and Natural Sciences, University of Bergen, for financial support, A. Breistøl, G. Grønstøl, G. O. Hellekjær and K. H. M. Jensen for suggestions and improvements of the manuscript, and G. Andersen, O. Billing Hansen, J. Hellekjær, K. Hellekjær and K. J. Hellekjær; T. Lislevand and A. T. Mjøs; L. Rosef, P. H. Salvesen and T. Smith, for help with planning and conducting the field work. We would also like to express gratitude to A. Traveset, Y. Yom-Tov, C. H. Greenberg and E. W. Schupp for valuable comments on earlier versions of this manuscript.

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References
  10. Appendix
  • Agami, M. & Waisel, Y. (1988) The role of fish in distribution and germination of seeds of the submerged macrophytes Najas marina and Ruppia maritima. Oecologia 76, 8388.
  • Barnea, A., Yom-Tov, Y. & Friedman, J. (1990) Differential germination of two closely related species of Solanum in response to bird ingestion. Oikos 57, 222228.
  • Barnea, A., Yom-Tov, Y. & Friedman, J. (1992) Effect of frugivorous birds on seed dispersal and germination of multi-seeded fruits. Acta Ecologica 13, 209219.
  • Cramp, S. (1988) Handbook of the Birds of Europe, the Middle East and North Africa: The Birds of the Western Palearctic, Vol. 5: Tyrant Flycatchers to Thrushes. Oxford University Press, New York.
  • Crocker, W. & Barton, L.V. (1957) Physiology of Seeds: An Introduction to the Experimental Study of Seeds and Germination Problems. Chronical Botanica Company, Waltham, MA.
  • Devillez, F., Fraipont, J. & Tissot, M. (1980) Effects of seed pretreatments on the embryo behaviours of Sorbus aria, Sorbus aucuparia, and Sorbus torminalis sowed in different positions. Bulletin de la Classe Des Sciences Academie Royale de Belgique 5E Serie 66, 162182.
  • Dinerstein, E. & Wemmer, C.M. (1988) Fruits Rhinoceros eat: dispersal of Trewia nudiflora (Euphorbiaceae) in lowland Nepal. Ecology 69, 17681774.
  • Von Ende, C.N. (2001) Repeated-measures analysis: growth and other time-dependent measures. Design and Analysis of Ecological Experiments, 2nd edn (eds S.M.Scheiner & J.Gurevitch), pp. 134157. Oxford University Press, New York.
  • Fenner, M. (1985) Seed Ecology. Chapman & Hall, London.
  • Flemion, F. (1929) Dormancy, after-ripening, and germination of Sorbus aucuparia. American Journal of Botany 16, 854.
  • Flemion, F. (1931) After-ripening, germination and seed vitality of seeds of Sorbus aucuparia. Contributions of the Boyce Thompson Institute 3, 413439.
  • Fox, G.A. (1993) Failure–time analysis: emergence, flowering, survivorship, and other waiting times. Design and Analysis of Ecological Experiments (eds S.M.Scheiner & J.Gurevitch), pp. 253289. Chapman & Hall, London.
  • Glyphis, J.P., Milton, S.J. & Siegfried, W.R. (1981) Dispersal of Acacia cyclops by birds. Oecologia 748, 138141.
  • Guitian, J., Munilla, I., Guitian, P. & Lopez, B. (1994) Frugivory and seed dispersal by redwings (Turdus iliacus) in southwest Iceland. Ecography 17, 314320.
  • Herrera, C.M. (1984) Adaptation to frugivory of Mediterranean avian seed dispersers. Ecology 65, 609617.
  • Holthuijzen, A.M.A. & Sharik, I.L. (1985) The avian seed dispersal system of the eastern red cedar (Juniperus virginiana). Canadian Journal of Botany 63, 15081515.
  • Howe, H.F. (1977) Bird activity and seed dispersal of a tropical wet forest tree. Ecology 58, 539550.
  • Howe, H.F. & Smallwood, J. (1982) Ecology of seed dispersal. Annual Review of Ecology and Systematics 13, 201228.
  • Izhaki, I. & Safriel, U.N. (1990) The effect of some Mediterranean shrub land frugivores upon germination patterns. Jounal of Ecology 78, 5665.
  • Ketring, D.L. (1973) Germination inhibitors. Seed Science and Technology 1, 305324.
  • Krefting, L.W. & Roe, E.I. (1949) The role of some birds and mammals in seed germination. Ecological Monographs 19, 269286.
  • Maruta, E. (1994) Seedling establishment of Polygonum cuspidatum and Polygonum weyrichii var. alpinum at high altitudes of Mt Fuji. Ecological Research 9, 205213.
  • Murray, K.G. (1988) Avian seed dispersal of three neotropical gap dependent plants. Ecological Monographs 58, 271298.
  • Pulliainen, E. & Erkinaro, E. (1978) The digestibility of rowan-berry seeds, Sorbus aucuparia L., for the Waxwing, Bombycilla garrulus L., as studied by scanning electron microscope. Aquilo Seriologica Zoologica 18, 1516.
  • Quinn, J.A., Mowrey, D.P., Emanuele, S.M. & Whalley, R.D.B. (1994) The ‘foliage is the fruit’ hypothesis: Buchloe dactyloides (Poaceae) and the shortgras prairie of North America. American Journal of Botany 81, 15451554.
  • Raspé, O., Findlay, C. & Jacquemart, L. (2000) Sorbus aucuparia L. Journal of Ecology 88, 910930.
  • Rick, C.M. & Bowman, R.I. (1961) Galápagos tomatoes and tortoises. Evolution 15, 407417.
  • SAS Institute Inc. (1989) SAS/STAT User's Guide, Version 6,4th edn, Vol. 2. SAS Institute Inc., Cary, NC.
  • Schupp, E.W. (1993) Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 107/108, 1529.
  • Snow, D. & Snow, B. (1986) Some aspects of avian frugivory in a north temperate area relevant to tropical forest. Frugivores and Seed Dispersal (eds A.Estrada & T.H.Fleming), pp. 159164. Dr W. Junk Publishers, Dordrecht, the Netherlands.
  • Snow, B. & Snow, D. (1988) Birds and Berries. A Study of an Ecological Interaction. T. & A.D. Poyser, Carlton.
  • Sokal, R.R. & Rohlf, F.J. (1995) Biometry. W.H. Freeman, New York.
  • Stanton, M.L. (1984) Seed variation in wild radish: effect of seed size on components of seedling and adult fitness. Ecology 65, 11051112.
  • Temple, S.A. (1977) Plant–animal mutualism: coevolution with dodo leads to near extinction of plant. Science 197, 885886.
  • Traveset, A. (1998) Effect of seed passage through vertebrate frugivores’ guts on germination: a review. Perspectives in Plant Ecology, Evolution and Systematics 1/2, 151190.
  • Traveset, A. & Verdú, M. (2001) A meta-analysis of gut treatment on seed germination. Frugivores and Seed Dispersal: Ecological, Evolutionary and Conservation Issues (eds D.Levey, M.Galetti & W.Silva). CAB International, Wallingford, UK.
  • Traveset, A., Bermejo, T. & Willson, M.F. (2001a) Effect of manure composition on seedling emergence and growth of two common shrub species of southeast Alaska. Plant Ecology 155, 2934.
  • Traveset, A., Reira, N. & Mas, R.E. (2001b) Ecology of fruit-colour polymorphism in Myrtus communis and differential effects of birds and mammals on seed germination and seedling growth. Journal of Ecology 89, 749760.
  • Traveset, A., Reira, N. & Mas, R.E. (2001c) Passage through bird guts causes interspecific differences in seed germination characteristics. Functional Ecology 15, 669675.
  • Wulff, R.D. (1986) Seed size variation in Desmodium paniculatum. III. Effects on seedling growth and physiological performance. Journal of Ecology 74, 115121.
  • Zar, J.H. (1996) Biostatistical Analysis. Prentice Hall, London.
  • Zentsch, W. (1968) Stratification of Sorbus aucuparia seeds. Proceedings of the International Symposium on Seed Physiology of Woody Plants (eds S.Bialobok & B.Suska), pp. 127132. Institute of Dendrology and Kornik Arboretum Polish Academy of Sciences, Poland.
  • Zhang, J. & Maun, M.A. (1993) Components of seed mass and their relationships to seedling size in Calamovilfa longifolia. Canadian Journal of Botany 71, 551557.
  • Zimmerman, J.K. & Weis, I.M. (1983) Fruit size variation and its effects on germination and seedling growth in Xanthium strumarium. Canadian Journal of Botany 61, 23092315.

Appendix

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References
  10. Appendix
Table 2. ancova analysis, detailed test statistics
Seed groupGrowth variableSourcePillai's traceFPSourcePillai's traceFPBox MP
Single seedStem lengthParallelism0·264 5·380·003    10·3890·500
 LeavesParallelism0·151 2·670·059Level0·0721·170·33320·6700·046
 Leaf lengthParallelism0·42210·40·001    26·5350·008
 Leaf widthParallelism0·180 3·290·029    13·1200·299
Two seedsStem lengthParallelism0·077 0·580·633Level0·4044·740·01143·2870·001
 LeavesParallelism0·125 1·000·414Level0·0580·4280·73525·1330·024
 Leaf lengthParallelism0·240 2·210·117Level0·2722·620·07829·7280·007
 Leaf widthParallelism0·279 2·710·071Level0·3543·830·02525·1810·002
Three seedsStem lengthParallelism0·266 3·260·037    32·0720·002
 LeavesParallelism0·149 1·570·218Level0·2993·840·02118·6290·103
 Leaf lengthParallelism0·023 0·210·890Level0·0310·2900·83212·1790·407
 Leaf widthParallelism0·006 0·050·984Level0·0800·7810·51514·8560·243
Four seedsStem lengthParallelism0·431 7·820·001    11·9150·408
 LeavesParallelism0·486 9·770·001    11·9130·408
 Leaf lengthParallelism0·62717·40·001     4·3550·956
 Leaf widthParallelism0·54312·30·001     8·2500·708
Single seed in droppingStem lengthParallelism0·317 4·950·006    13·6220·292
 LeavesParallelism0·185 2·430·083Level0·0410·4500·719 9·1380·630
 Leaf lengthParallelism0·319 5·000·006    11·5540·432
 Leaf widthParallelism0·295 4·460·010    19·6770·070