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Macquarie University Researchonline Macquarie University ResearchOnline This is the published version of: Moles, Angela T., Warton, David I. and Westoby, Mark 2003. Do small- seeded species have higher survival through seed predation than large- seeded species? Ecology Vol 8, Issue 12, pp.3148–3161 Access to the published version: http://dx.doi.org/10.1890/02-0662 Copyright: Copyright by the Ecological Society of America. Article published in Ecology Vol 84, Issue 12, pp. 3148–3161 by Angela T. Moles, David I. Warton and Mark Westoby. Ecology, 84(12), 2003, pp. 3148±3161 q 2003 by the Ecological Society of America DO SMALL-SEEDED SPECIES HAVE HIGHER SURVIVAL THROUGH SEED PREDATION THAN LARGE-SEEDED SPECIES? ANGELA T. M OLES,1 DAVID I. WARTON, AND MARK WESTOBY Department of Biological Sciences, Macquarie University, New South Wales 2109, Australia Abstract. Seed ecologists have often stated that they expect larger-seeded species to have lower survivorship through postdispersal seed predation than smaller-seeded species. Similar predictions can be made for the relationship between survivorship through predis- persal seed predation and seed mass. In order to test these predictions, we gathered data regarding survivorship through 24 hours of exposure to postdispersal seed predators for 81 Australian species, and survivorship through predispersal seed predation for 170 Aus- tralian species. These species came from an arid environment, a subalpine environment, and a temperate coastal environment. We also gathered data from the published literature (global) on survivorship through postdispersal seed predation for 280 species and survi- vorship through predispersal seed predation for 174 species. We found a weak positive correlation between seed mass and the percentage of seeds remaining after 24 hours of exposure to postdispersal seed predators at two of three ®eld sites in Australia, and no signi®cant relationship across 280 species from the global lit- erature, or at the remaining ®eld site. There was no signi®cant relationship between seed mass and survivorship through predispersal seed predation either cross-species or across phylogenetic divergences in any of the vegetation types, or in the compilation of data from the literature. Postdispersal seed removal was responsible for a greater percentage of seed loss in our ®eld studies than was predispersal seed predation. On average, 83% of diaspores remained after 24 hours of exposure to postdispersal seed removers, whereas 87% of seeds survived all predispersal seed predation that occurred between seed formation and seed maturity. Mean seed survival was higher in the ®eld studies than in the literature compi- lations, and species showing 100% survival were heavily underrepresented in the literature. These differences may be due to biases in species selection or publication bias. Seed defensive tissue mass increased isometrically with seed mass, but there was no signi®cant relationship between the amount of defensive tissue per gram of seed reserve mass and survivorship through postdispersal seed predation. Key words: Australia; postdispersal seed predation; predispersal seed predation; publication bias; seed defense; seed mass; seed predation vs. seed size. INTRODUCTION There are two main types of seed predation: (1) pre- dispersal seed predation, which occurs while seeds are Plants around the world make seeds in an impres- still on their mother plant, and (2) postdispersal seed sively wide range of sizes, from the dust-like seeds of predation, which occurs once seeds have dispersed orchids that weigh only one millionth of a gram, to the away from their parent. Predispersal seed predation is huge seeds of the double coconut that can weigh an largely carried out by invertebrates such as coleoptera, awesome 20 kg each (Harper et al. 1970). Even within diptera, lepidoptera, and hymenoptera (Crawley 1992, plant communities, there are usually 5±6 orders of mag- Hulme 1998b), many of which develop inside the seeds. nitude of variation in seed mass across species (Leish- Postdispersal seed predation is largely carried out by man et al. 2000). These differences in seed mass can larger organisms such as rodents, but ants are also im- have substantial effects on the chances that seeds will portant postdispersal seed predators (Crawley 1992, survive the different threats to which they are exposed Hulme 1998b). in the course of their development, dispersal, and es- In this paper, we use a combination of ®eld estimates tablishment as seedlings (Westoby et al. 1996, Leish- of survivorship through seed predation (across many man et al. 2000). One hazard that seeds must survive species in three Australian vegetation types) and a com- is seed predation. pilation of previously published estimates of survivor- ship through predation (global) to investigate relation- ships between seed mass and survivorship through Manuscript received 22 October 2002; revised 2 February exposure to pre- and postdispersal seed predation 2003; accepted 6 February 2003; ®nal version received 27 March (henceforth referred to as pre- and postdispersal sur- 2003. Corresponding Editor: T. P. Young. 1 Present address: National Center for Ecological Analysis vivorship). We also investigate relationships between and Synthesis, 735 State Street, Suite 300, Santa Barbara, seed defenses, seed mass, and pre- and postdispersal California 93101-3351 USA. E-mail: [email protected] survivorship. 3148 December 2003 SEED SIZE AND SEED PREDATION 3149 Seed mass and postdispersal survivorship vorship than to the relationship between seed mass and postdispersal survivorship. However, theories based on There is a general expectation that large seeds will apparency and optimal foraging ideas make the same have lower postdispersal survivorship than small seeds predictions for negative relationships between seed (Louda 1989, Blate et al. 1998, Kollmann et al. 1998). mass and predispersal survivorship as for postdispersal A number of reasons have been put forward to explain survivorship. In addition, large seeds might be exposed why this might be the case. First, large seeds might be to predispersal seed predation from a wider range of more apparent to predators (Feeny 1976), and thus seed predators than small seeds, as large seeds can be more likely to be encountered by a seed predator. Sec- colonized by both large and small seed predators, but ond, large seeds might spend longer on or near the soil small seeds can only be colonized by small seed pred- surface than small seeds, because it is more dif®cult ators (Greig 1993, Mucunguzi 1995). Large seeds for large seeds to become incorporated into the soil might also be exposed to predispersal seed predation pro®le through the action of rain or organisms such as for a longer time, as large seeds take longer to complete earthworms (Thompson et al. 1994, Bekker et al. 1998). development than small seeds (Moles and Westoby This would mean that larger seeds would be exposed 2003). to the action of seed predators over a longer period There is a small amount of evidence to suggest that than small seeds (Bekker et al. 1998). Third, optimal large-seeded species might have lower predispersal sur- foraging theory suggests that it might be more ef®cient vivorship than small-seeded species. For instance, for a seed predator to search for a few large seeds rather Moegenburg (1996) showed that some predispersal than many small seeds, given equal handling time for seed predators preferentially oviposit on larger seeds. small and large seeds. (Charnov 1976, Hoffmann et al. As with postdispersal survivorship, results from exist- 1995, Blate et al. 1998). ing cross-species studies are mixed. Greig (1993) found There are two important lines of indirect evidence a negative relationship between seed mass and predis- for larger seeds having lower postdispersal survivor- persal survivorship across ®ve species of Piper (Pi- ship than small seeds. (1) Seed-eating organisms faced peraceae). Janzen (1969) showed that across 36 species with a range of seeds will generally take the largest of Fabaceae, species attacked by bruchids had signif- seeds that they can physically process (Davidson 1977, icantly smaller seeds than those that were not attacked. Nelson and Chew 1977, Chew and De Vita 1980, Auld (1983) found no signi®cant relationship between Abramsky 1983, Moegenburg 1996, Hulme 1998a; but seed mass and predispersal survivorship for 28 Aus- see Smith 1987 and Osunkoya et al. 1994). (2) Cages tralian Fabaceae, and there was a positive relationship that exclude seed predators can result in increased re- between seed mass and predispersal survivorship cruitment of large-seeded species, but no increase in across nine species of Yucca (Keeley et al. 1984). the establishment of small-seeded species (Brown and In this study, we aimed to provide a broad survey Heske 1990, Reader 1993). to test the hypothesis that pre- and postdispersal sur- Despite these arguments and indirect evidence that vivorship might be higher in small-seeded than in large- large seeds are more likely to be eaten by postdispersal seeded species. seed predators than are small seeds, direct evidence for What is the magnitude of seed loss to pre- and a negative relationship between seed size and postdis- postdispersal seed predation? persal survivorship is limited. A few multispecies stud- It is not uncommon for plants to lose 90±100% of ies have shown the predicted negative relationship be- a given seed crop to seed predators (Louda 1989, Craw- tween seed mass and postdispersal
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