Seed dispersal syndrome

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Seed dispersal syndromes are morphological characters of seeds correlated to particular seed dispersal agents. [1] [2] [3] [4] Dispersal is the event by which individuals move from the site of their parents to establish in a new area. [5] A seed disperser is the vector by which a seed moves from its parent to the resting place where the individual will establish, for instance an animal. Similar to the term syndrome, a diaspore is a morphological functional unit of a seed for dispersal purposes. [6]

Contents

Characteristics for seed dispersal syndromes are commonly fruit colour, mass, and persistence. [4] These syndrome characteristics are often associated with the fruit that carries the seeds. Fruits are packages for seeds, composed of nutritious tissues to feed animals. However, fruit pulp is not commonly used as a seed dispersal syndrome because pulp nutritional value does not enhance seed dispersal success. [5] Animals interact with these fruits because they are a common food source for them. Although, not all seed dispersal syndromes have fruits because not all seeds are dispersed by animals. Suitable biological and environmental conditions of dispersal syndromes are needed for seed dispersal [2] and invasion success [1] such as temperature and moisture.

Seed dispersal syndromes are parallel to pollination syndromes, which are defined as floral characteristics that attract organisms as pollinators. [7] They are considered parallels because they are both plant-animal interactions, which increase the reproductive success of a plant. However, seed dispersal syndromes are more common in gymnosperms, while pollination syndromes are found in angiosperms. [5] Seeds disperse to increase the reproductive success of the plant. The farther away a seed is from a parent, the better its chances of survival and germination. Therefore, a plant should select certain traits to increase dispersal by a vector (i.e. bird) to increase the reproductive success of the plant.

Evolution

Seeds have evolved traits to reward animals to enhance their dispersal abilities. [5] Differing foraging behaviours of animals can lead to selection of dispersal traits and spatial variation [3] [8] such as increase in seed size for mammal dispersal, which can limit seed production. [9] Seed production is limited by some seed syndromes because of their cost to the plant. Therefore, seed dispersal syndromes will evolve in a plant when the trait benefit outweighs the cost. [1] The seed dispersers themselves play an essential role in syndrome evolution. [10] For example, birds put strong selection pressure on seeds for colour of fruits because of their enhanced vision. Illustrations of such colour evolution include green colour being produced because its photosynthesis abilities are less costly [11] while red colour emerges as a byproduct for protection from arthropods. [9]

For visible characteristic differences to develop between dispersers and non-dispersers a few conditions need to be met 1. Specialization must increase dispersal success whether morphological, physiological or behavioural 2. Energy investment for dispersal will be taken from energy investment of other traits 3. Dispersal traits will benefit the dispersers over non-dispersers. Phenotypic (visible characteristics) differences in non-dispersers and dispersers can be caused by external factors, kin competition, intraspecific competition and habitat quality. [1]

History

In 1930, Ridley wrote an important book called The dispersal of plants throughout the world, which goes into detail about each form of dispersal; dispersal by wind, water, animals, birds, reptiles and fish, adhesion, and people. He details the morphology and traits for each dispersal method, which are later described as seed dispersal syndromes. This began the idea of seed trait selection being associated with a form of seed dispersal. Then in 1969 van der Pijl identified seed dispersal syndromes based on each mechanism of seed dispersal in his book Principles of Dispersal in Higher Plants. He is the pinnacle of seed dispersal syndromes and is cited by many scientists who study seed dispersal syndromes. He describes the morphology of interactions between fruits and flowers, and classifies dispersal in invertebrates, fish, reptiles, birds, mammals, ants, wind, water and the plant itself. Janson in 1983 continued the study on seed dispersal syndromes and classified seed dispersal syndromes of fruit by size, colour and husk or no husks in species of Peruvian tropical forest. He went in depth about the interaction between plants that have adapted to seed dispersal by birds and mammals. Willson, Irvine & Walsh in 1989 added more factors to the study of seed dispersal syndromes and looked at differing fleshy fruits and their correlation to moisture and differing ecological factors. They looked at bird-dispersal and mammal-dispersal and how the fruits differed in dispersal syndromes such as colour and size. These scientists began the theory and ideas behind seed dispersal syndromes that are crucial to the evolution of reproduction in plants.

Types and functions

Dispersal syndromes have been previously classified by: size, colour, weight, protection, flesh type, number of seeds, weight and start time of ripening. [3] [4] [9] [12] Syndromes are often associated with the type of dispersal and morphology. Also chemical composition can influence the disperser’s fruit choice. [4] The following are types of seed dispersal and their syndromes.

Anemochory

Example of a syndrome of anemochory Taraxacum sect. Ruderalia MHNT.jpg
Example of a syndrome of anemochory

Anemochory is defined as seed dispersal by wind. Common dispersal syndromes of anemochory are wing structures [8] and brown or dull coloured seeds without further rewards. [12] Van der Pijl named seeds for anemochory flyers, rollers, or throwers to represent the seed dispersal syndromes and their behaviour. Flyers are typically categorized as dust diaspores, balloons, plumed or winged. Dust diaspores are small flat structures on seeds that appear to be the transition to wing diaspores, balloons are inflated seed characteristics and plumes are hairs or elongation seed characteristics. [13] Wings have evolved to increase dispersal distance to promote gene flow. [8] Anemochory is commonly found in open habitats, [14] canopy trees, [10] and dry season deciduous forests. [14] Wind dispersers mature in the dry season for optimum high long-distance dispersal [2] [12] to increase success of germination.

Barochory

Barochory is seed dispersal by gravity alone in which a plant's seeds fall beneath the parent plant. [8] These seeds commonly have heavy seed dispersal syndromes. [13] However, heavy seeds may not be a form of seed dispersal syndrome, but a random seed characteristic that has no dispersal purpose. It has been thought[ by whom? ] that barochory does not develop a seed dispersal syndrome because it does not select for characters to enhance dispersal. It is questionable whether barochory is dispersal at all.

Hydrochory

Hydrochory is seed dispersal by water. [13] Seeds can disperse by rain or ice or be submerged in water. Seeds dispersed by water need to have the ability to float and resist water damage. They often have hairs to assist with enlargement and floating. More features that cause floating are air space, lightweight tissues and corky tissues. Hydrochory syndromes are most common in aquatic plants. [13] [15]

Zoochory

Zoochory is the dispersal of seeds by animals and can be further divided into three classes.

  1. Endozoochory is seed dispersal by animal ingestion and defecation of a seed. In a mutualistic behavior, the animal is rewarded with nutritious fruit while harmlessly dispersing the seed or seeds, thereby increasing their fitness and chances for survival.
  2. Synzoochory is dispersal of diaspores by the mouthparts of animals, and
  3. Epizoochory is the accidental dispersal by animals. [13] Differing characteristics of zoochory syndromes include coloured fruits, scented fruits, and different textures for different animals.

Endozoochory syndrome characteristics will develop based on palatability of the fruit by an organism. For example, mammals are attracted to scent of a seed and birds are attracted to colour. Endozoochory syndromes have evolved to be ingested by animals and later bypassed in a new environment so the seed can germinate. [16] Synzoochory should possess hard skins to protect seeds from damage of mouthparts; for example, sharp beaks on animals such as birds or turtles. Epizoochory commonly has burrs or spines to transport seeds on the outside of animals. These syndromes are highly associated with animals that have fur, [13] while burrs would be lacking on seeds that are dispersed by reptiles because of their smooth skin. It is believed that not all animals that interact with plant fruits are dispersers because some animals do not increase the successful dispersal of seeds but consume and destroy them. Therefore, some animals are dispersers and some are consumers.

Mammalochory

Mammalochory is specifically the seed dispersal by mammals. The dispersal syndromes for mammalochory include large fleshy fruit, green or dull coloured fruits, and husked or unhusked. [3] [4] [9] [11] [13] [17] The seeds tend to have more protection to prevent mechanical destruction. Mammals rely on smell more than vision for foraging, which causes the seeds they disperse to be more scented compared to bird-dispersed seeds. [18] Animal-dispersed seeds ripen in rainy season when foraging activity is high, resulting in fleshy diaspores. [2] [10] [12] Mammals consume fruits whole or in smaller pieces, [11] which explains the larger seed syndromes. Mammalochory syndromes can increase the reproductive success of the plant compared to seed dispersal syndromes of a plant associated with barochory for example. An example of seed dispersal syndromes associated with mammals that increases reproductive success would be seed-consuming rodents that increase germination by burial of seeds. [19]

Ornithochory

Ornithochory is seed dispersal by birds. Common syndrome characteristics include small fleshy fruits with bright colours and without husks. [3] [9] [11] [13] [14] Ornithochory is common in temperate zones [12] and oceanic islands because of absence of native mammals. [14] Birds have heightened colour vision and swallow seeds and fruits whole, [11] explaining the small and coloured characteristics of dispersal syndromes. Birds have a weak sense of smell, therefore ornithochory syndromes would specialize more in colour than scent, [13] in comparison to mammalochory. Ornithochory can increase the reproductive success of a plant because a bird’s digestive tract increases seed germination [19] after it has been bypassed and dispersed by the bird.

Myrmecochory

Myrmecochory is seed dispersal by ants. Myrmecochory is considered an ant-plant mutualistic relationship. [2] [8] The common syndrome traits for myrmecochory are elaiosomes, and are often hard and difficult to damage. [8] [13] Elaiosomes are structures that attract ants because they are high in lipid content, providing important nutrients for the ant. [8] Without ants, seed dispersal becomes barochory and dispersal success declines. [2] [8] It is debated if ants are good dispersers and if plants would select for ant dispersal. Ants do clearly interact with seeds, however ants cannot travel very long distances. Therefore, would a plant select for a bird over an ant when birds can disperse seeds much farther than ants, increasing a plant's reproductive success.

Problems in seed dispersal syndromes

Some scientists are skeptical whether seed dispersal syndromes actually exist because their parallel, pollination syndromes, are often disputed in scientific literature. Seed dispersal syndromes do not seem to have much disagreement among scientists. It is unclear whether this is due to lack of research or interest in seed dispersal syndromes, or that scientists agree with the idea of seed dispersal syndromes. It also may be that seed dispersal syndromes are harder to test because once seeds disperse they are difficult to collect and study. Jordano (1995) states that the evolution of fruit traits for seed dispersal success is only dependent on diameter. [16] This is one scientist’s perspective but does not appear to be the common consensus among scientists. Colour and olfaction are other common seed dispersal syndromes tested and discussed in scientific literature, with equivocal results. One possible reason is that adaptive variation in fruit colours could be scale dependent, occurring only on broad taxonomic scales rather than within assemblages of either bird-dispersed or mammal-dispersed fruit species. [20] One limitation to seed dispersal syndromes mentioned is the limited definitions of syndrome characteristics such as odour or texture. [11] It is possible that there has not been enough research to test these characteristics or they do not play a role in seed dispersal syndromes.

The differences in seed dispersal syndromes appear to be weak, but do exist. There needs to be consideration for the possibility that these syndromes evolved not to benefit seed dispersal but possibility to combat other selective pressures. [16] For example, syndromes may have developed to combat predation or environmental hazards. Predation could produce a secondary metabolite syndrome. Secondary metabolites are compounds that are not used for the primary function of a plant and are normally used as defense mechanisms. [21]

Further research

Seed dispersal syndromes have not been studied in complete breadth for every seed dispersal method. Therefore, further research should be conducted to fill the gaps of knowledge about dispersal syndromes. The following are problems areas or directions research can continue on the study of seed dispersal syndromes. There is a lack of understanding of morphology in correlation to behavioural traits of dispersers. [1] [12] Research in this area would assist in the understanding of why particular dispersers are selected by plants to enhance reproductive success. Also, understanding movement strategies of factors affecting departure to settlement [1] is important in determining whether seed dispersal syndromes are only affect by plant selection for a disperser. There are few studies concerning phenotype-dependent dispersal and how it affects spatial structures of populations. [1] [12] Distance of dispersal is not researched in enough detail to correlate to a seed dispersal syndrome. More experimental field studies on plant-animal interactions regarding seed dispersal need to be conducted [9] [14] for a thorough understanding of seed dispersal syndromes. There is limited knowledge about the presence of elaisomes and ant behaviour affecting seed dispersal, and how ant-plant interactions evolved under various plant traits. [8] Understanding these interactions would help clarify if myrmecochory did evolve seed dispersal syndromes. Micro and macroevolutionary processes are needed to determine the effects of biological dispersal of seeds. [9] There cannot be inferences about seed dispersal syndromes without robust phylogenies and evolutionary studies. There is also a gap in the understanding of genetic consequences of zoochory. [16] Using genetics could help clarify if these syndromes were formed at random or if they correspond to evolution of seed dispersal. It is unclear if these seed dispersal syndromes evolved for specialization between plants and animals to increase seed dispersal success or if these syndromes are simply formed from generalist plant-animal interactions. Understanding these relationships would clarify the confusion about seed dispersal syndromes and if they are true examples of evolution increasing plant reproductive success or if they have developed without selective pressures.

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<span class="mw-page-title-main">Food</span> Substances consumed for nutrition

Food is any substance consumed by an organism for nutritional support. Food is usually of plant, animal, or fungal origin and contains essential nutrients such as carbohydrates, fats, proteins, vitamins, or minerals. The substance is ingested by an organism and assimilated by the organism's cells to provide energy, maintain life, or stimulate growth. Different species of animals have different feeding behaviours that satisfy the needs of their metabolisms and have evolved to fill a specific ecological niche within specific geographical contexts.

<span class="mw-page-title-main">Seed</span> Embryonic plant enclosed in a protective outer covering

In botany, a seed is a plant embryo and food reserve enclosed in a protective outer covering called a seed coat (testa). More generally, the term "seed" means anything that can be sown, which may include seed and husk or tuber. Seeds are the product of the ripened ovule, after the embryo sac is fertilized by sperm from pollen, forming a zygote. The embryo within a seed develops from the zygote and grows within the mother plant to a certain size before growth is halted.

<span class="mw-page-title-main">Drupe</span> Fleshy fruit with hard inner layer (endocarp or stone) surrounding the seed

In botany, a drupe is an indehiscent type of fruit in which an outer fleshy part surrounds a single shell of hardened endocarp with a seed (kernel) inside. These fruits usually develop from a single carpel, and mostly from flowers with superior ovaries.

<span class="mw-page-title-main">Convergent evolution</span> Independent evolution of similar features

Convergent evolution is the independent evolution of similar features in species of different periods or epochs in time. Convergent evolution creates analogous structures that have similar form or function but were not present in the last common ancestor of those groups. The cladistic term for the same phenomenon is homoplasy. The recurrent evolution of flight is a classic example, as flying insects, birds, pterosaurs, and bats have independently evolved the useful capacity of flight. Functionally similar features that have arisen through convergent evolution are analogous, whereas homologous structures or traits have a common origin but can have dissimilar functions. Bird, bat, and pterosaur wings are analogous structures, but their forelimbs are homologous, sharing an ancestral state despite serving different functions.

<span class="mw-page-title-main">Pollination</span> Biological process occurring in plants

Pollination is the transfer of pollen from an anther of a plant to the stigma of a plant, later enabling fertilisation and the production of seeds, most often by an animal or by wind. Pollinating agents can be animals such as insects, for example beetles; birds, butterflies, and bats; water; wind; and even plants themselves. Pollinating animals travel from plant to plant carrying pollen on their bodies in a vital interaction that allows the transfer of genetic material critical to the reproductive system of most flowering plants. When self-pollination occurs within a closed flower. Pollination often occurs within a species. When pollination occurs between species, it can produce hybrid offspring in nature and in plant breeding work.

<span class="mw-page-title-main">Frugivore</span> Organism that eats mostly fruit

A frugivore is an animal that thrives mostly on raw fruits or succulent fruit-like produce of plants such as roots, shoots, nuts and seeds. Approximately 20% of mammalian herbivores eat fruit. Frugivores are highly dependent on the abundance and nutritional composition of fruits. Frugivores can benefit or hinder fruit-producing plants by either dispersing or destroying their seeds through digestion. When both the fruit-producing plant and the frugivore benefit by fruit-eating behavior the interaction is a form of mutualism.

<span class="mw-page-title-main">Seed dispersal</span> Movement or transport of seeds away from the parent plant

In spermatophyte plants, seed dispersal is the movement, spread or transport of seeds away from the parent plant. Plants have limited mobility and rely upon a variety of dispersal vectors to transport their seeds, including both abiotic vectors, such as the wind, and living (biotic) vectors such as birds. Seeds can be dispersed away from the parent plant individually or collectively, as well as dispersed in both space and time. The patterns of seed dispersal are determined in large part by the dispersal mechanism and this has important implications for the demographic and genetic structure of plant populations, as well as migration patterns and species interactions. There are five main modes of seed dispersal: gravity, wind, ballistic, water, and by animals. Some plants are serotinous and only disperse their seeds in response to an environmental stimulus. These modes are typically inferred based on adaptations, such as wings or fleshy fruit. However, this simplified view may ignore complexity in dispersal. Plants can disperse via modes without possessing the typical associated adaptations and plant traits may be multifunctional.

<span class="mw-page-title-main">Myrmecochory</span> Seed dispersal by ants

Myrmecochory ( ; from Ancient Greek: μύρμηξ, romanized: mýrmēks and χορεία khoreíā is seed dispersal by ants, an ecologically significant ant–plant interaction with worldwide distribution. Most myrmecochorous plants produce seeds with elaiosomes, a term encompassing various external appendages or "food bodies" rich in lipids, amino acids, or other nutrients that are attractive to ants. The seed with its attached elaiosome is collectively known as a diaspore. Seed dispersal by ants is typically accomplished when foraging workers carry diaspores back to the ant colony, after which the elaiosome is removed or fed directly to ant larvae. Once the elaiosome is consumed, the seed is usually discarded in underground middens or ejected from the nest. Although diaspores are seldom distributed far from the parent plant, myrmecochores also benefit from this predominantly mutualistic interaction through dispersal to favourable locations for germination, as well as escape from seed predation.

<span class="mw-page-title-main">Elaiosome</span> Fleshy structures attached to the seeds of plants

Elaiosomes are fleshy structures that are attached to the seeds of many plant species. The elaiosome is rich in lipids and proteins, and may be variously shaped. Many plants have elaiosomes that attract ants, which take the seed to their nest and feed the elaiosome to their larvae. After the larvae have consumed the elaiosome, the ants take the seed to their waste disposal area, which is rich in nutrients from the ant frass and dead bodies, where the seeds germinate. This type of seed dispersal is termed myrmecochory from the Greek "ant" (myrmex) and "circular dance" (khoreíā). This type of symbiotic relationship appears to be mutualistic, more specifically dispersive mutualism according to Ricklefs, R.E. (2001), as the plant benefits because its seeds are dispersed to favorable germination sites, and also because it is planted by the ants.

<span class="mw-page-title-main">Flower</span> Reproductive structure in flowering plants

A flower, also known as a bloom or blossom, is the reproductive structure found in flowering plants. Flowers consist of a combination of vegetative organs – sepals that enclose and protect the developing flower, petals that attract pollinators, and reproductive organs that produce gametophytes, which in flowering plants produce gametes. The male gametophytes, which produce sperm, are enclosed within pollen grains produced in the anthers. The female gametophytes are contained within the ovules produced in the carpels.

<span class="mw-page-title-main">Pollination syndrome</span> Flower traits that attract pollinators

Pollination syndromes are suites of flower traits that have evolved in response to natural selection imposed by different pollen vectors, which can be abiotic or biotic, such as birds, bees, flies, and so forth through a process called pollinator-mediated selection. These traits include flower shape, size, colour, odour, reward type and amount, nectar composition, timing of flowering, etc. For example, tubular red flowers with copious nectar often attract birds; foul smelling flowers attract carrion flies or beetles, etc.

<span class="mw-page-title-main">Seed predation</span> Feeding on seeds as a main or exclusive food source

Seed predation, often referred to as granivory, is a type of plant-animal interaction in which granivores feed on the seeds of plants as a main or exclusive food source, in many cases leaving the seeds damaged and not viable. Granivores are found across many families of vertebrates as well as invertebrates ; thus, seed predation occurs in virtually all terrestrial ecosystems. Seed predation is commonly divided into two distinctive temporal categories, pre-dispersal and post-dispersal predation, which affect the fitness of the parental plant and the dispersed offspring, respectively. Mitigating pre- and post-dispersal predation may involve different strategies. To counter seed predation, plants have evolved both physical defenses and chemical defenses. However, as plants have evolved seed defenses, seed predators have adapted to plant defenses. Thus, many interesting examples of coevolution arise from this dynamic relationship.

<span class="mw-page-title-main">Heterospory</span> The production of spores of two different sizes and sexes by several groups of land plants

Heterospory is the production of spores of two different sizes and sexes by the sporophytes of land plants. The smaller of these, the microspore, is male and the larger megaspore is female. Heterospory evolved during the Devonian period from isospory independently in several plant groups: the clubmosses, the ferns including the arborescent horsetails, and progymnosperms. This occurred as part of the process of evolution of the timing of sex differentiation.

<span class="mw-page-title-main">Fruit (plant structure)</span> Internal makeup of fruits

Fruits are the mature ovary or ovaries of one or more flowers. They are found in three main anatomical categories: aggregate fruits, multiple fruits, and simple fruits.

<span class="mw-page-title-main">Diaspore (botany)</span> Plant seed or spore and tissues that aid dispersal

In botany, a diaspore is a plant dispersal unit consisting of a seed or spore plus any additional tissues that assist dispersal. In some seed plants, the diaspore is a seed and fruit together, or a seed and elaiosome. In a few seed plants, the diaspore is most or all of the plant, and is known as a tumbleweed.

<span class="mw-page-title-main">Dispersal vector</span> Transporters of biological dispersal units

A dispersal vector is an agent of biological dispersal that moves a dispersal unit, or organism, away from its birth population to another location or population in which the individual will reproduce. These dispersal units can range from pollen to seeds to fungi to entire organisms.

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<span class="mw-page-title-main">Evolutionary anachronism</span> Attributes of living species that arose due to coevolution with other now-extinct species

Evolutionary anachronism, also known as "ecological anachronism", is a term initially referring to attributes of native plant species that seemed best explained as having been favorably selected in the past due to their coevolution with plant-eating megafauna that are now extinct. Diminished effectiveness and distance of seed dispersal by fruit-eating mammals inhabiting the same ecosystems today suggest maladaptation. Maladaptation of such fruiting plants will intensify as ongoing climate change shifts the physical and ecological conditions within their current geographic range.

Diplochory, also known as “secondary dispersal”, “indirect dispersal” or "two-phase dispersal", is a seed dispersal mechanism in which a plant's seed is moved sequentially by more than one dispersal mechanism or vector. The significance of the multiple dispersal steps on the plant fitness and population dynamics depends on the type of dispersers involved. In many cases, secondary seed dispersal by invertebrates or rodents moves seeds over a relatively short distance and a large proportion of the seeds may be lost to seed predation within this step. Longer dispersal distances and potentially larger ecological consequences follow from sequential endochory by two different animals, i.e. diploendozoochory: a primary disperser that initially consumes the seed, and a secondary, carnivorous animal that kills and eats the primary consumer along with the seeds in the prey's digestive tract, and then transports the seed further in its own digestive tract.

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References

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  2. 1 2 3 4 5 6 Griz, L.M.S. & Machado, I.C.S. (2001). Fruiting phenology and seed dispersal syndromes in caatinga, a tropical dry forest in the northeast of Brazil. Journal of Tropical Ecology, 17, 303-321.
  3. 1 2 3 4 5 Link, A. & Stevenson, P.R. (2004). Fruit dispersal syndromes in animal disseminated plants at Tinigua National Park, Colombia. Revista Chilena de Historia Natural, 77, 319-334.
  4. 1 2 3 4 5 Tamboia, T., Cipollini, M.L. & Levey, D.J. (1996). An Evaluation of Vertebrates Seed Dispersal Syndromes in Four Species of Black Nightshade. Oecologia, 107(4), 522-532.
  5. 1 2 3 4 Herrera, C. M. & Pellmyr, O. (2002).Plant Animal Interactions: An Evolutionary Approach. USA: Blackwell Science Ltd
  6. ↑ Booth, D. T. (1990). Plant diaspore functions. Journal of Seed Technology, 14(1), 61-73.
  7. ↑ Fenster, C. B., Armbruster, W. S., Wilson, P., Dudash, M. R. & Thomson, J. D. (2004). Pollination Syndromes and Floral Specialization. Annual Review of Ecology, Evolution and Systematics, 35, 375-403.
  8. 1 2 3 4 5 6 7 8 9 Castro, S., Ferrero, V., Loureiro, J., Espadaler, X., Silveira, P. & Navarro, L. (2010). Dispersal mechanisms of the narrow endemic Polygala vayredae: dispersal syndromes and spatio-temporal variations in ant dispersal assemblages. Plant Ecology, 207, 359-372.
  9. 1 2 3 4 5 6 7 Fischer, K.E. & Chapman, C.A. (1993). Frugivores and Fruit Syndromes: Differences in Patterns at the Genus and Species Level. Oikos, 66(3), 472-482.
  10. 1 2 3 Butler, D.W., Green, R.J., Lamb, D., McDonald, W.J.F. & Forster, P.I. (2007). Biogeography of seed-dispersal syndromes, life-forms and seed sizes among woody rain-forest plants in Australia’s subtropics. Journal of Biogeography, 34, 1736-1750.
  11. 1 2 3 4 5 6 Lomascolo, S.B., Speranza, P. & Kimball, R.T. (2008). Correlated evolution of fig size and color supports the dispersal syndromes hypothesis. Oecologia, 158, 783-796.
  12. 1 2 3 4 5 6 7 Du, Y., Mi, X., Liu, X., Chen, L. & Ma, K. (2009). Seed dispersal phenology and dispersal syndromes in a subtropical broad-leaved forest of China. Forest Ecology and Management, 258, 1147-1152.
  13. 1 2 3 4 5 6 7 8 9 10 van de Pijl, L. (1969). Principles of dispersal in higher plants. Springer, Berlin Heidelberg, New York.
  14. 1 2 3 4 5 Armesto, J.J. & Rozzi, R. (1989). Seed Dispersal Syndromes in the Rain Forest of Chiloe: Evidence for the importance of Biotic Dispersal in a Temperate Rain Forest. Journal Biogeography, 16(3), 219-226.
  15. ↑ Ridley, H.N. (1930). The dispersal of plants throughout the world. Reeve, Ashford, United Kingdom.
  16. 1 2 3 4 Herrera, C. M. & Pellmyr, O. (2002). Plant Animal Interactions: An Evolutionary Approach. USA: Blackwell Science Ltd.
  17. ↑ Willson, M.F., Irvine, A.K. & Walsh, N.G. (1989). Vertebrate dispersal syndromes in some Australian and New-zealand plant-communities, with geographic comparisons. Biotropica, 21, 133-147.
  18. ↑ van der Pijl, 1969
  19. 1 2 Hollander, J.L. & Vander Wall, S.B. (2009). Dispersal syndromes in North American Ephedra. International Journal of Plant Sciences, 170(3), 323-330.
  20. ↑ Lim, Ganges; Burns, Kevin C. (2021-11-24). "Do fruit reflectance properties affect avian frugivory in New Zealand?". New Zealand Journal of Botany: 1–11. doi:10.1080/0028825X.2021.2001664. ISSN   0028-825X. S2CID   244683146.
  21. ↑ Futuyma, D. J. & Agrawal, A. A. (2009). Macroevolution and the biological diversity of plants and herbivores. Proceedings of the National Academy of Sciences of the United States of America, 106(43), 18054-18061.
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