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Intersite comparison Fruit characteristics in a dry deciduous and a humid littoral forest of Madagascar: evidence for selection pressure through abiotic constraints rather than through co-evolution with lemurs as seed dispersers. AN BOLLEN, GIUSEPPE DONATI, JOANNA FIETZ, DOROTHEA SCHWAB, JEAN-BAPTISTE RAMANAMANJATO, LAURENT RANDRIHASIPARA, LINDA VAN ELSACKER , JÖRG GANZHORN FRUITS AND FRUGIVORES (L DEW, J-P BOUBLI) (IN PRESS) ABSTRACT Fruit and seed characteristics are compared between a dry deciduous forest in the west and a humid littoral forest in the south-east of Madagascar to discriminate between the role of abiotic factors (humidity, climate, soil characteristics) and frugivorous vertebrates for the evolution of morphological and biochemical fruit characteristics. The sites differed in abiotic conditions but contain very similar communities of frugivorous vertebrates. Fruit selection by two lemur species (Eulemur fulvus and Cheirogaleus medius) that are important for seed dispersal and that are present at both study sites, was compared between sites to examine fixed selection criteria that could give rise to possible co-evolution between frugivores and their fruit species on the one hand or to dietary flexibility of the frugivores on the other hand. Our results show that most fruit characteristics differ significantly between study sites. Food selection by both lemur genera in relation to morphological and biochemical fruit characteristics co-varies closely with their representation at a given site. These results indicate that morphological and biochemical characteristics are more likely the result of abiotic conditions rather than of interactions between frugivorous lemurs and their food. INTRODUCTION The study of interactions between fruits and their vertebrate consumers has generated a great deal of interest in recent decades, especially in tropical forests where most plant species depend on frugivorous animals for dispersal of their seeds (see Willson et al. 1989 for a review). Attracting frugivores is crucial for these plants in order to ensure reproduction by seed dispersal (Howe and Smallwood 1982). Morphological fruit characteristics, such as colour, pulp richness, hardness of the shell, seed size, and patterns of spatio-temporal distribution have been interpreted as co-adapted features that govern animals' choice of fruit species. 111
Chapter 4 Most seed dispersal studies and reviews of correlations between frugivore food selection and fruit characteristics have produced little empirical support for tight co-evolutionary relationships (Howe and Smallwood 1982; Herrera 1984; Howe 1984; Gautier-Hion et al. 1985; Fisher and Chapman 1993; Chapman 1995; Erikkson and Ehrlen 1998; Lambert and Garber 1998), as most plant species do not depend on one single species of disperser. In most cases a range of taxonomically distinct frugivores may consume and disperse the seeds of the same fruiting species (Gautier-Hion et al. 1985; Herrera 1986; Ganzhorn 1988; Chapman 1995; Chapman and Chapman 1996; Bollen et al., Chapter 2, 3). Fruit traits are likely to evolve in response to other selection pressures or may perform more than one function (Willson and Whelan 1990). Data from the fossil record suggest that morphological fruit traits often have remained relatively constant for millions of years (Fisher and Chapman 1993; Chapman 1995). Primates represent a major group of mammalian seed dispersers in the tropics. Studies have demonstrated that many primate species rely heavily on fruit and that they represent a large component of the frugivore biomass (25-40%, Terborgh 1983; Bourlière 1985; Chapman 1995; Julliot 1996; Chapman and Onderdonk 1998; Lambert and Garber 1998). In Madagascar, lemurs have been postulated to be important seed dispersers (Ralisoamalala 1996; Scharfe and Schlund 1996; Dew and Wright 1998; Overdorff and Strait 1998; Birkinshaw 1999, 2001; Ganzhorn et al. 1999a) in particular since the guild of frugivorous birds and bats is depauperate in this island as compared to other continents (Fleming et al. 1987; Wright and Martin 1995; Goodman and Ganzhorn 1997; Wright 1997a; Böhning-Gaese et al. 1999; Ganzhorn et al. 1999a). In this study, we investigate whether morphological and biochemical fruit characteristics can be linked to abiotic conditions or whether there is evidence for co-evolution between these fruit characteristics and the main consumers that are involved in seed dispersal, i.e. Eulemur fulvus and Cheirogaleus medius. We selected two types of forest in Madagascar growing under very different climatic and edaphic conditions: evergreen littoral wet forest and dry deciduous forest. Both sites had a similar complement of frugivore species, having six genera and five species in common. The following predictions were tested: 1. If fruit characteristics evolved mainly in response to abiotic conditions we expect different morphological and biochemical fruit characteristics at the two sites 2. If fruit characteristics co-evolved in response to selective pressure of consumers we expect that characteristics of food items at both sites do not differ, as the guild of frugivorous vertebrates is very similar at both sites. 3. The second prediction listed above requires that selection criteria of frugivores are species-specific. We therefore predict that these consumers will have a specialised diet irrespective of fruit availability, as is supposed by co-evolution. 112
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Fruit-frugivore interactions in a M
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Cover photographs: Front: Back: -
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Table of contents III. General conc
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Acknowledgements A special word of
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PREFACE Preface This work brings to
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General introduction Finally, seed
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General introduction high as 98% fo
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’Hazo tokana tsy mba ala’ One t
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Chapter 1 changes in resource avail
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Chapter 1 For analyses we narrowed
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Chapter 1 Fig. 2. Seasonal variatio
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Chapter 1 80 70 60 50 40 30 20 10 0
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Chapter 1 Fig 4. Comparison of data
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Chapter 1 Table 4. Data on phenolog
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Chapter 1 Relation with abiotic fac
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Chapter 1 Malagasy rainforests disp
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Chapter 1 Appendix I Continued Fami
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Chapter 1 Appendix I Continued Fami
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Malagasy proverb Drawing © Giusepp
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Chapter 2 the successful establishm
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Chapter 2 40 Table 1. The frugivore
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Chapter 2 Statistical analyses To v
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Chapter 2 Overall fruit trap data d
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Chapter 2 Table 3. Morphological an
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Chapter 2 depressed seeds (Fig. 3a)
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Chapter 2 Fig. 3. Ordination plot o
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Chapter 2 On a community level the
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Chapter 2 Appendix II. Plant-animal
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Malagasy proverb Lemur drawing © S
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Page 71 and 72: Chapter 3 dominant plant families s
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Page 75 and 76: Chapter 3 Table 4 Continued Paramet
Page 77 and 78: Chapter 3 Besides testing feeding s
Page 79 and 80: Chapter 3 and do not consume the fi
Page 81 and 82: Chapter 3 (1997) already pointed ou
Page 83 and 84: Chapter 3 1989; Galetti 1993; Saini
Page 85 and 86: Chapter 3 Appendix I. All plant spe
Page 87 and 88: Chapter 3 Other SD Hss Rats Rr Ew 8
Page 90 and 91: Pteropus rufus Feeding ecology of P
Page 92 and 93: Pteropus rufus number per species a
Page 94 and 95: Pteropus rufus Table 1 Continued Fr
Page 96 and 97: Pteropus rufus larger number of spe
Page 98 and 99: Table 2 Continued Number of seeds/d
Page 100 and 101: Pteropus rufus Food selection: expl
Page 102 and 103: Pteropus rufus presence. On the oth
Page 104 and 105: Pteropus rufus Marshall (1983). Occ
Page 106 and 107: Coracopsis nigra The feeding ecolog
Page 108 and 109: Coracopsis nigra fruit pulp (70%) b
Page 110 and 111: Coracopsis nigra Table 1 Continued
Page 112 and 113: Coracopsis nigra Table 2. Morpholog
Page 115: Malagasy proverb Drawing of fruits
Page 119 and 120: Chapter 4 Mean temperature is aroun
Page 121 and 122: Chapter 4 Number of seeds: 1-2, 3-1
Page 123 and 124: Chapter 4 Fig. 2. Monthly fruit ava
Page 125 and 126: Chapter 4 120 Table 3. Soil charact
Page 127 and 128: Chapter 4 Table 4. Morphological ch
Page 129 and 130: Chapter 4 Table 5. Biochemical char
Page 131 and 132: Chapter 4 Chemistry At both sites,
Page 133 and 134: Chapter 4 considering species numbe
Page 137 and 138: ’Ny valala tsy indroa mandry eo a
Page 139 and 140: Chapter 5 environmental degradation
Page 141 and 142: Chapter 5 at a very low density in
Page 143 and 144: Chapter 5 Table 1. A list of plant
Page 145 and 146: Chapter 5 (Ganzhorn et al. 1999a).
Page 147 and 148: Chapter 5 Animals The degree of vul
Page 149 and 150: Chapter 5 comm.). Mixed species pla
Page 151 and 152: Chapter 5 data are needed we believ
Page 153 and 154: General conclusion as in other site
Page 155 and 156: General conclusion selection pressu
Page 157 and 158: General conclusion are consumed by
Page 159 and 160: Samenvatting omstandigheden zijn bo
Page 161 and 162: Samenvatting vruchtkenmerken. Beide
Page 163 and 164: Samenvatting zaadverspreiding moete
Page 165 and 166: Résumé température et précipita
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Résumé (Sud-est de Madagascar) et
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Résumé des frugivores sur l’év
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References Bollen A, Van Elsacker L
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References Dowsett JR (2000) Le sta
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References Godfrey LR, Junger WL, R
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References Janson CH, Chapman CA (1
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References Marshall AG (1983) Bats,
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References Rabevohitra R, Lowry PP,
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References Tattersall I (1982) The
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family Loganiaceae scientific name
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