Int. J. Plant Sci. 169(7):863–870. 2008.
Ó 2008 by The University of Chicago. All rights reserved.
1058-5893/2008/16907-0004$15.00 DOI: 10.1086/589888
EVOLUTION OF SEED SIZE AND BIOTIC SEED DISPERSAL IN ANGIOSPERMS:
PALEOECOLOGICAL AND NEOECOLOGICAL EVIDENCE
Ove Eriksson1
Department of Botany, Stockholm University, SE-106 91 Stockholm, Sweden
Origins of biotic seed dispersal by vertebrates and evolution of different seed sizes are conspicuous features in
angiosperm evolution. In the Cretaceous, angiosperms remained small seeded, and biotic seed dispersal was rare.
In the Early Tertiary, average seed size increased drastically, and biotic seed dispersal by vertebrates became
common. Later in the Tertiary, along with climate cooling and the opening of vegetation, average seed size
dropped. Fossil data suggest a positive correlation between seed size and biotic seed dispersal. This article
examines three hypotheses: (1) the coevolution hypothesis, which suggests that evolution of large seeds and biotic
dispersal were driven by interactions between plants and frugivorous vertebrates; (2) the recruitment hypothesis,
which suggests that vegetation change altered recruitment conditions that favored large seeds and in turn
promoted biotic dispersal; and (3) the life-form hypothesis, which suggests that large seeds and biotic dispersal
evolved as coadapted traits along with evolution of large plant life-forms. The hypotheses are complementary
rather than mutually exclusive. Evidence suggest that changes in vegetation structure (open vs. closed) are
probably a primary driving mechanism of seed size and dispersal evolution, but life-forms, seed sizes, and biotic
dispersal systems have evolved as coadapted sets of traits in response to these environmental changes.
Keywords: coevolution, fleshy fruits, plant size, seed size evolution, seedling recruitment.
Introduction
The Problem: Seed Size and Biotic Seed Dispersal
from the Cretaceous to the Present
Angiosperms have evolved a tremendous variation in seed
size and seed dispersal systems. Seed sizes range from minute
dust seeds, such as in orchids and weighing a few micrograms,
to giants such as the nuts of some palms, weighing more than
10 kg (Leishman et al. 2000). Although seed dispersal is often
unassisted, that is, with seeds lacking structures adapted to specific dispersal agents, many plants have evolved means to promote seed transport by external agents—by water, by wind or
animals, and most commonly, by mammals, birds, and ants.
This article synthesizes paleoecological and neoecological evidence relevant to the evolution of seed size and its association
with vertebrate-mediated seed dispersal, that is, dispersal of
seeds after animals have collected or ingested fruits (henceforth,
‘‘biotic dispersal’’). Most of the vertebrate-dispersed fruits are
fleshy, that is, containing a juicy fruit pulp, but there are also biotically dispersed fruits that are leathery or dry, such as nuts.
The term ‘‘fleshy fruits’’ also incorporates seed dispersal systems
where the attractive fleshy tissue is not morphologically a part
of the fruit (e.g., strawberries). More specifically, I address the
question of how to explain a broad pattern of evolutionary
changes in seed size and in biotic seed dispersal by vertebrates
from observations of paleofloras sampled from the Early Cretaceous (age ;124 Myr) to the Pliocene (age ;2 Myr).
1
Angiosperms first appeared in the fossil record in the Early
Cretaceous around 130 Ma (Crane et al. 1995). In contrast to
the extraordinary variation in contemporary angiosperm seed
size and dispersal systems, there is no substantial variation in
seed size and dispersal systems during approximately the first
half of angiosperm existence. Tiffney (1984), later corroborated
by Eriksson et al. (2000a), concluded that during most of the
Cretaceous, angiosperm seeds were generally small (typically
;1 mm3), and seed dispersal was mostly unassisted. One exception is from one of the oldest known floras from Famalicão,
Portugal (Eriksson et al. 2000b), where ;25% of the species
had small drupes or berries. However, overall, there is little evidence of biotic seed dispersal in angiosperms before the Late
Cretaceous (Wing and Tiffney 1987b; Wing and Boucher 1998;
Tiffney 2004). From the Late Cretaceous, and especially after
the Cretaceous-Tertiary (K/T) boundary (65 Ma) in the Paleocene (;65–55 Ma) and the Eocene (;55–38 Ma), there was a
dramatic increase in both seed size and range of seed sizes (fig.
1). The peak occurred in the Early to Middle Eocene (;55–42
Ma). In the Oligocene (;38–25 Ma), the Miocene (;25–5 Ma),
and the Pliocene (;5–2 Ma), average seed size dropped, but the
seed size range remained more or less the same (varying between
three and six orders of magnitude). As a comparison, the seed
size range in extant floras typically is around five to six orders
of magnitude (Leishman et al. 1995).
Seed dispersal systems are not randomly distributed among
plants with different seed size. In species with biotic seed dispersal,
excluding seed dispersal by ants and adhesive seed dispersal externally on animal fur and feathers, seeds are typically in the upper
E-mail: ove.eriksson@botan.su.se.
Manuscript received December 2007; revised manuscript received April 2008.
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(3) Why did seed size drop after the Eocene? and (4) Why is
there a positive relationship between seed size and biotic seed
dispersal?
Wing and Tiffney (1987b) made a thorough summary of the
changing interactions between angiosperms and herbivores from
the Cretaceous to the Tertiary. They proposed a model in which
the varying impact of large generalized herbivores was seen as a
key driver of the interaction and the resulting changing patterns
of angiosperm seed and fruit traits and vegetation. After the demise of large dinosaur herbivores at the K/T boundary and the
subsequent radiation of small, arboreal, frugivorous birds and
mammals, there was a major shift in the selection regimes in angiosperms, favoring larger seeds, biotic dispersal, and development of closed vegetation. Wing and Tiffney (1987b) suggested
that several mechanisms were involved in this process. Without
the effect of large generalized herbivores, competition among
plants increased, leading to denser vegetation and in turn promoting larger plants with larger seeds. The interactions between
plants and small animals resulted in a ‘‘coevolutionary spiral’’ in
which increasing abundance of seeds and fruits as resources for
frugivores stimulated frugivory that favored plant dispersal.
The coevolution hypothesis, the recruitment hypothesis, and
the life-form hypothesis will be examined in this article. These
focus on different specific mechanisms that are all included in
(and compatible with) the general model by Wing and Tiffney
(1987b). The first two hypotheses have been inferred post hoc
from the paleoecological information that they were intended
to explain, whereas the third hypothesis derives from a combination of comparative studies of seed size and predictions from
life-history theory.
Possible Solutions: Three Hypotheses
Fig. 1 Median seed size (A) and seed size range (orders of magnitude;
B) in 25 paleofloras from the Early Cretaceous to the Pliocene (redrawn
from Eriksson et al. 2000a).
The ideas behind the coevolution hypothesis were discussed
by Tiffney (1984) and Wing and Tiffney (1987b) but were suggested explicitly by Tiffney (2004). Although the model developed
part of the seed size range, most common in plants with seeds
heavier than 0.1 g, and biotic dispersal is dominating in the seed
size range above 1 g (Hughes et al. 1994). However, there are examples of biotically dispersed plants with smaller seeds, particularly in berries (e.g., Vaccinium, Ericaceae). Biotic seed dispersal is
generally most frequent in forest communities, especially in the
tropics, where it is sometimes a totally dominating seed dispersal
system among woody plant species (Fleming et al. 1987; Willson
et al. 1990).
On the basis of 25 paleofloras examined by Eriksson et al.
(2000a), there is evidence of a strong positive relationship between seed size and the fraction of species with biotic seed dispersal (fig. 2). Such a strong relationship between seed size
and the occurrence of biotic dispersal has been questioned by
other studies, and I will return to this later; however, viewed
from the paleoecological evidence, the changes in angiosperm
seed size over the past 130 Myr are mirrored by changes in
the frequency of biotic seed dispersal.
On the basis of figures 1 and 2, I addressed four questions
about the evolution of angiosperm seed size and dispersal systems: (1) Why were seeds generally small and biotic seed dispersal rare during most of the Cretaceous? (2) What caused
the dramatic increase in seed size during the Early Tertiary?
Fig. 2 Relationship between the fraction of species with biotic seed
dispersal (mainly ‘‘fleshy fruits’’) and the median seed size in 25 paleofloras from the Early Cretaceous to the Pliocene (data from Eriksson
et al. 2000a; r ¼ 0.844, P < 0.001).
ERIKSSON—EVOLUTION OF SEED SIZE AND BIOTIC SEED DISPERSAL
by Wing and Tiffney (1987b) was based on several mechanisms,
Tiffney (2004, p. 15) emphasized the key role of the interactions between plants and frugivores: ‘‘A clear upsurge occurred in the importance of biotic dispersal in the Tertiary.
Central to this are birds and mammals that, because of their
small size, have organ-level interactions with plants . . . Wing
and Tiffney (1987a, 1987b) and Tiffney (1992) postulated
that the radiation of small vertebrates led to the rise in dispersal
and the subsequent establishment of closed-canopy forest.’’
Tiffney (2004) argued that the key event that triggered the radiation of angiosperm seed sizes and dispersal systems was the
simultaneous radiation of frugivores during the Early Tertiary.
Mammals such as primates, rodents, and bats, common presentday frugivores, and several groups of potentially frugivorous
birds radiated during the Paleocene and the Eocene. According
to Tiffney (2004), this new arena for plant-animal coevolution
allowed plants to evolve larger seeds, which were suitable for
establishing offspring under closed canopies. This process promoted the establishment of closed forests, known to have developed during the Paleocene and the Eocene.
The coevolution hypothesis implies a causal chain: the radiation of frugivores!coevolution with plants!evolution of larger
seeds and biotic seed dispersal!development of closed vegetation. The paucity of suitable seed-dispersing vertebrates is the
reason seed size remained small and biotic seed dispersal was
rare during the Cretaceous. The radiation of frugivorous mammals and birds caused the increase in seed size and the association between large seeds and biotic dispersal. However, on the
basis of the coevolution hypothesis, it is difficult to explain why
seed size dropped after the Eocene. All the prominent groups of
frugivores were present during that time and are still present in
extant faunas.
The recruitment hypothesis was also discussed by Tiffney
(1984) and Wing and Tiffney (1987b) but was suggested explicitly by Eriksson et al. (2000a). According to this hypothesis, the
key event was the change in vegetation composition during the
Early Tertiary. In contrast to the more open vegetation dominating during the Cretaceous, an ecologically new kind of environment was established in the Tertiary: closed, probably
multistratal forests dominated by angiosperms. According to
Wing and Sues (1992, p. 389), ‘‘This appears to be the most dramatic structural shift to take place in terrestrial ecosystems
from their full establishment in the mid-Permian to the present
day.’’ The main drivers of this change were most likely climate,
increasing temperature, and precipitation, but the expansion of
forests may also have been promoted by a general lack of large
herbivores after the demise of the dinosaurs at the CretaceousTertiary boundary (Wing and Tiffney 1987b; Collinson and Hooker
1991). A closed vegetation implies a strong competition for
light at ground level, favoring evolution of increasing seed
size. Because of a trade-off between seed size and seed number
(for a plant of a given size allocating a given amount of resources to seeds), an increase in seed size means fewer seeds.
With a given seed dispersal shadow, fewer seeds from the mother
plant means that fewer offspring can be established some distance away from the mother plant (Eriksson and Jakobsson
1999). Thus, increasing seed size implies a cost in terms of reduced dispersal because the departure-related benefits of dispersal (Herrera 2002) are reduced. Vertebrates are the only
vectors capable of transporting large seeds in terrestrial envi-
865
ronments, and biotic seed dispersal was therefore favored. Evolution of specialized frugivores, according to this hypothesis,
is not a cause but an effect of evolution of large seeds. Presence of fruit-eating animals is a prerequisite, but they may initially not have been specialized frugivores. When vegetation
became more open again during the Oligocene, the Miocene,
and the Pliocene, selection favored small-seeded plants under
conditions where recruitment was not light limited.
Tiffney (2004, p. 19) summarized the difference between the
coevolution and recruitment hypotheses as follows: ‘‘Tiffney
(1984) and Wing and Tiffney (1987a, 1987b) suggested that
the radiation of birds and mammals established dispersal agents
scaled to move organs, which, in turn, allowed larger disseminule size and, ultimately, the establishment of closed forests with
low-light germination regimes. Eriksson et al. (2000a) countered that these relations were inverted and that a warmer climate and increased precipitation allowed the establishment of
closed forest, which shifted the ecological constraints on seed
recruitment . . . and led to larger seeds. The dispersal agents
therefore tracked, not led, the increase in seed size.’’
The recruitment hypothesis thus implies a causal chain that is
the reverse of the coevolution hypothesis: closed vegetation!
evolution of larger seeds!evolution of biotic dispersal!radiation
of frugivores. The open vegetation explains why seed sizes remained small during the Cretaceous and biotic dispersal was
not promoted. Vegetation changes caused both the increase
and the following drop in seed size during the Tertiary, and
biotic dispersal is positively related to seed size because of its
function in dispersal of large seeds.
The third life-form hypothesis was also discussed by Wing
and Tiffney (1987b), but it was suggested explicitly by Moles
et al. (2005a), and it also incorporates aspects developed in
Moles and Westoby (2004, 2006) and Moles et al. (2004,
2005b). This hypothesis differs from the previous hypotheses
because it was not formulated as a specific solution to the pattern of seed size evolution depicted in figures 1 and 2. Instead,
it was suggested as an explanation for evolution of seed size in
general. The life-form hypothesis does not consider why there
is a positive relationship between seed size and biotic dispersal,
but it is fully compatible with the explanation for such a relationship that is given by the recruitment hypothesis. Moles
et al. (2005a) analyzed relationships between seed size, biotic
dispersal, and plant growth form (vegetation), and in that context, they commented on Tiffney (1984) and Eriksson et al.
(2000a), that is, on the coevolution and the recruitment hypotheses, and suggested an alternative hypothesis.
Basically, the life-form hypothesis is similar to the recruitment hypothesis in that vegetation change, from open to closed
forest systems, may be the initial driver of seed size evolution.
The key difference in the life-form hypothesis, compared to the
recruitment hypothesis, is that evolution of larger seeds is not
caused by a process in which larger seeds increase the likelihood of recruitment under closed canopies. Instead, evolution
of increasing seed size is a consequence of larger and more longlived plants having a longer juvenile period. To improve survival during this longer period to maturity, seeds must contain
more resources, and therefore selection favors larger seeds in
large and long-lived plants. Inspired by a theory by Charnov
(1993) that predicted a positive relationship between offspring
and adult size in mammals, Moles et al. (2005a) suggested
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that any factor that causes increasing plant size (and longer
life span) also drives evolution of larger seeds.
According to the life-form hypothesis, seeds were small during the Cretaceous because angiosperms were generally small.
The drastic increase in seed size in the Early Tertiary occurred
because plants generally increased in size along with the development of closed subtropical and tropical forests, and the
drop in seed size from the Oligocene occurred because the average plant size decreased. The curve depicting changes in
seed size (fig. 1) would, according to the life-form hypothesis,
mirror the average (and range) of angiosperm plant size and
life span.
Examining the Hypotheses: Paleoecological and
Neoecological Evidence
The Coevolution Hypothesis
Interactions between plants and their seed dispersers are
generally considered as ‘‘diffuse,’’ meaning that the interaction
occurs between a whole group of plants (e.g., several species
with a certain type of fleshy fruits) and a whole group of animals (e.g., frugivorous primates; Howe and Smallwood 1982;
Wheelwright and Orians 1982; Herrera 1985, 2002). Evidence
suggests that the morphology of biotically dispersed fruits in
many lineages has changed little since they originated in the
Early Tertiary (Collinson and Hooker 1991; Bremer and Eriksson
1992; Jordano 1995), despite that the composition of the disperser fauna has changed much since that time. For example,
Eriksson et al. (2000a) found that on average 91% of the lineages included in a data set from 22 paleofloras had not changed
fruit type since the time the floras were deposited (which
ranged between 2 and 87 Ma). The coevolution hypothesis
implies that the interactions between animal dispersers and
fruit traits (the arena for selection on fruit traits) resulted in
directional selection and adaptive change in the Paleocene and
the Eocene when a major phase of evolution of biotic dispersal
took place. In contrast, the interactions during the epochs following the Eocene resulted in stabilizing selection (and thus
trait stasis) or were subjected to constraints imposed by the
morphological structure of biotically dispersed fruits.
An important question is whether there were no (or few) potential seed-dispersing vertebrates during the Cretaceous, and,
if this were the case, whether a paucity of vertebrate seed dispersers constituted a constraint for the evolution of large seeds.
Although there is very limited evidence available on potential
vertebrate seed dispersers before the Late Cretaceous, two lines
of evidence suggest that it is unlikely that a general lack of seed
dispersers constrained evolution of large angiosperm seeds.
First, although it is controversial, molecular evidence suggests
that several groups of mammals that became important frugivores during the Tertiary, for example, primates and rodents,
originated in the Cretaceous (Adkins et al. 2001; Archibald
et al. 2001; Douzery et al. 2003; Soligo and Martin 2006;
Steiper and Young 2006; Bininda-Emonds et al. 2007; Martin
et al. 2007). One of the most abundant groups of Cretaceous
mammals, the multituberculates, is known from the Late Cretaceous and the Early Tertiary to have had seeds and fruits in its
diet (Krause 1982; Del Tredici 1989; Collinson and Hooker
1991), and some multituberculates were arboreal (Jenkins and
Krause 1983). It is possible that multituberculates evolved this
feeding habit earlier during the Cretaceous. Second, early seed
plants (seed ferns, gymnosperms) evolved fleshy structures apparently suitable for attracting seed dispersers, long before angiosperms originated (Tiffney 2004). It therefore seems likely
that potential plant-seed disperser interactions existed during
the Cretaceous, when angiosperms evolved and diversified.
There is also evidence for interactions between seed-dispersing
animals and angiosperms from one of the earliest angiosperm
floras (age ;124 Myr), in which about a quarter of the species
possessed small but fleshy fruits (Eriksson et al. 2000b). It has
been suggested, however, that the initial function of the fleshy
tissue in angiosperm fruits was not disperser attraction but protection from seed predators (Mack 2000).
A second important question is the timing of evolution of
known vertebrate seed dispersers in relation to the origin of biotic seed dispersal during the Paleocene and the Eocene. Major
groups of frugivorous birds, for example, fruit pigeons, toucans, hornbills, and passerines such as thrushes, manakins, and
cotingids, are not found in the fossil record before the Miocene
or are not known at all from fossils (e.g., toucans; Feduccia
1996). An earlier origin of the passerines in the Southern Hemisphere has been suggested (Ericson et al. 2003), and molecular
data indicate that modern birds originated in Cretaceous, but
fossil evidence is lacking (Feduccia 1996; Chiappe and Dyke
2002). The most common group of Cretaceous birds is the extinct enantiornithes (Chiappe and Dyke 2002). Most of these
birds were toothed, and many species lived in nearshore environments, suggesting that they foraged on aquatic animals.
Some enantiornithes have been found in inland deposits, but
their feeding habits are not known. Thus, although birds are
important frugivores in the extant fauna, there is not much evidence suggesting that they were a significant part of the plantdisperser interactions in the Early Tertiary.
In contrast to the lack of evidence for frugivorous birds, several Late Cretaceous and Early Paleocene mammals included
seeds and fruit in their diet. During the Late Cretaceous, the
dominating group of seed and fruit-eating mammals was the
multituberculates, small rodentlike mammals, many of which
were arboreal (Collinson and Hooker 1991). Multituberculates
remained important seed and fruit eaters during the Paleocene,
but they were accompanied by two other groups of fruit-eating
mammals, the primate-like plesiadapiforms and condylarths
(primitive ungulates; Bininda-Emonds et al. 2007; Bloch et al.
2007). A major radiation of primates and rodents occurred
around the Paleocene-Eocene boundary (Collinson and Hooker
1991; Bowen et al. 2002; Gingerich 2006), and both groups developed to become important seed dispersers. Rodents were
feeding mainly on hard, dry fruit types; nut size in the families
Betulaceae, Fagaceae, and Juglandaceae increased from the Late
Paleocene, and large nuts became abundant by the late Eocene
(Collinson and Hooker 1991). Collinson and Hooker suggested
that this interaction is a plausible case of diffuse coevolution
between plants and mammals. Nuts are one-seeded fruits, so
an increase in fruit size is likely to indicate a simultaneous increase in seed size.
There are several other putative examples of diffuse coevolution between plants and seed-dispersing mammals during
Paleocene and Eocene. Bloch et al. (2007) suggested that dental features of plesiadapiforms adapted to a changing diet from
ERIKSSON—EVOLUTION OF SEED SIZE AND BIOTIC SEED DISPERSAL
insectivory to granivory and frugivory, along with an increasing
abundance of seeds and fruits as a food source. Soligo and Martin (2006) and Martin et al. (2007) argued that primates originated in the Cretaceous (but see Silcox et al. 2007; Soligo and
Martin 2007) and shifted to a vegetarian diet, mainly fleshy
fruits, when this new food source become available. Changes in
the visual apparatus (forward-facing eyes) was suggested as a
result of adaptations to frugivory. Since the first fossil evidence
of primates are from the Eocene (Gingerich 2006; Martin et al.
2007), it is reasonable that the abundance of fruit as a food
source promoted the radiation of primates, even if the primate
lineage is older.
Thus, interactions between plants and several groups of
mammals (e.g., multituberculates, plesiadapiforms, primates,
and rodents) may, at least from the perspective of timing, have
been instrumental in the evolution of biotic dispersal systems.
In contrast, fossil evidence suggests that one of the most important groups of extant frugivorous mammals, fruit bats, did not
become abundant until the Miocene (although molecular evidence indicates an earlier origin of bats; Teeling et al. 2005).
The evidence reviewed suggests that diffuse coevolution
with mammals is likely to have played an important role for
the origin and early evolution of biotic dispersal, although this
role may not have been as a trigger of the selection process
for larger seeds. The coevolution hypothesis does not explain
why evolving larger seeds was favorable in the first place.
Even if potential seed-dispersing vertebrates became increasingly abundant during the Early Tertiary, thereby enhancing
seed dispersal if plants developed fleshy fruits, there is no reason why seeds would not have remained small (and thus more
numerous). Even if coevolution with seed-dispersing vertebrates was a mechanism contributing to the radiation of seed
sizes and biotic dispersal systems in the Early Tertiary, this
process must have included some component of advantage of
larger seeds, as suggested by the recruitment and the life-form
hypotheses. It seems reasonable to conclude that the coevolution hypothesis is not sufficient to explain the patterns depicted in figures 1 and 2. The coevolution hypothesis is not
compatible with the (admittedly limited) evidence for the existence of potential seed dispersers before the Late Cretaceous,
and it provides no explanation of why seed size increased in
the first place or why seed size dropped after the Eocene.
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plants with large seeds (Salisbury 1942; Hughes et al. 1994;
Butler et al. 2007).
The recruitment hypothesis predicts that vegetation shifts
from open to closed vegetation, which leads to selection for
larger seeds with biotic dispersal or, if viewed in a shorter ecological timescale, leads to species sorting that favors those species in the species pool that possess these traits. Apart from
being congruent with the patterns of change in seed size and
biotic dispersal depicted in figures 1 and 2, this prediction is
also supported by comparative analyses of changes within angiosperm lineages in fruit types in relation to vegetation shifts,
which recurred during the Tertiary (Bolmgren and Eriksson
2005). Indirect support is also gained from studies of foraging
strategies of Miocene mammals in which the proportion of
frugivores was lower in savanna vegetation than in forests
(Fortelius et al. 1996). Large-scale vegetation changes during
the Tertiary, shifting between closed forests, open woodland,
and open grasslands (which developed during the Miocene
and the Pliocene; e.g., Jacobs et al. 1999; Strömberg 2005;
Strömberg et al. 2007), were driven by climate change. Periods
of cooling, for example, at the Eocene-Oligocene transition
(Prothero 1994) were associated with development of more
open vegetation. Indeed, average seed size from the paleofloras
examined by Eriksson et al. (2000a) was correlated with a paleotemperature curve derived by Zachos et al. (2001) for the Late
Cretaceous to the Pliocene (fig. 3). A similar result was obtained by Moles et al. (2005a) when correlating seed size and
temperature across extant species. They found an even stronger
correlation between seed size and precipitation.
There is also evidence that does not support the recruitment
hypothesis, or at least not the direct connection between evolution of larger seeds and biotic dispersal. First, in the flora of Famalicão from the Early Cretaceous, ;25% of the species had
drupes or berries, but seed sizes averaged 0.78 mm3 (Eriksson
The Recruitment Hypothesis
The recruitment hypothesis rests on a number of assumptions that are supported by evidence. (1) Recruitment under
shaded conditions is generally improved by increasing seed
size (Foster 1986; Leishman and Westoby 1994; Moles and
Westoby 2004). (2) There is a trade-off between seed size and
seed number, implying that an increasing seed size for a plant
of a given size and resource allocation to seeds leads to a reduced seed production (Henery and Westoby 2001; Moles
et al. 2004). (3) Biotic seed dispersal is associated with an increase in seed dispersal distance, as compared with unassisted
dispersal (Portnoy and Willson 1993), which means that a
cost of reduced dispersal due to lower seed production may be
offset by biotic dispersal. Biotic dispersal may also result in directed dispersal to suitable recruitment sites (Wenny and Levey
1998). (4) Seed dispersal by vertebrates is overrepresented among
Fig. 3 Relationship between median seed size in 19 paleofloras from
the Late Cretaceous to the Pliocene (from Eriksson et al. 2000) and deep
sea temperature, based on fig. 2 in Zachos et al. (2001). Floras examined
by Eriksson et al. (2000a) with an age outside the temporal range
covered by Zachos et al. were excluded, and the temperature for the time
of the youngest flora from the Pliocene, with a temperature below the
scale shown by Zachos et al., was set to 0°C (r ¼ 0.485; P ¼ 0.02).
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et al. 2000b). Assuming that fleshy tissue of the fruits functioned
to attract dispersers (but see Mack 2000), this suggests that biotic
dispersal may evolve without being associated with particularly
large seeds. Second, in subtropical forest in Australia, Butler et al.
(2007) found a generally strong association between possession
of fleshy fruits and large seeds across all studied sites. In contrast,
the seed sizes within sites did not differ between species with and
without fleshy fruits, indicating a weak causal relationship between seed size and biotic seed dispersal. Third, in a comparative
phylogenetic analysis, Moles et al. (2005a) found that dispersal
syndrome (biotic vs. abiotic) accounted for only 3% of the variation in seed size contrasts. The largest effect on seed size was
found for growth form (herb vs. shrub vs. tree), where larger
growth forms are associated with increasing seed size.
The strongest argument for the recruitment hypothesis is
that it provides an explanation for the initial evolution of increasing seed size. However, when it comes to explaining the
evolution of biotic dispersal, the evidence is weaker, and it
seems likely that other mechanisms than large seeds per se,
must be invoked for explaining evolution of biotic dispersal.
The Life-Form Hypothesis
The weak relationship between dispersal syndrome and seed
size contrasts led Moles et al. (2005b) to suggest the life-form
hypothesis. In the context of the pattern depicted in figures
1 and 2, this hypothesis is critically dependent on how the
changes in seed size and biotic dispersal are related to changes
in plant size and life span. For the Tertiary, the trends in seed
size and biotic dispersal, with a peak in the Eocene, a decline
during the Oligocene, and a leveling off during the Miocene
and the Pliocene, would fit well with the life-form hypothesis if
we assume that average plant size and life span decreased as
vegetation became more open after the forest cover maximum
in the Eocene.
The life-form hypothesis implies that angiosperms must
have been generally small during the Cretaceous. Several studies suggest that early angiosperms were shrubs or small trees,
or even herbs, and large angiosperm trees were less common
during most of the Cretaceous than they were during the
Tertiary (Wing and Tiffney 1987b; Wing and Boucher 1998).
Although open canopy, broad-leaved evergreen woodland existed during Late Cretaceous (Upchurch and Wolfe 1987),
closed forests during the Cretaceous were composed mainly of
conifers (Wing and Sues 1992).
A complicating issue when comparing the recruitment and
the life-form hypotheses is that these hypotheses are difficult
to distinguish based on interpretations of vegetation. Both
would make the same prediction, since tree cover both creates
an environment where recruitment occurs in shade and where
plants are generally large and long lived. Both hypotheses focus on the requirements for successful recruitment in systems
dominated by large plants. The key issue is whether the increasing competition for light during seedling establishment
or the necessity of survivorship during an increasing length of
time until maturity was the main driver of selection for larger
seeds. This issue has to be resolved by observational and experimental studies in extant plants and by further development of life-history theory. The suggestion by Moles et al.
(2004, 2005a, 2005b) that increasing seed size is associated
with selection for large plant size and longer life span has
been questioned. Grubb et al. (2005) claimed that a simple relationship between plant size and seed size is not supported by
data, a claim that was disputed by Moles et al. (2005c), who
argued that Grubb et al. had based their conclusion on a toolimited data set. Furthermore, Rees and Venable (2007) questioned whether the theory by Charnov (1993) actually supports
the suggestion by Moles et al. that seed size evolution is driven
by selection for juvenile time to maturity. In a reanalysis of
this theory, Rees and Venable (2007, p. 926) found that a positive relationship between seed size and plant size is predicted
only ‘‘if unrealistic assumptions are made about the effects of
seed mass on survival, such as the effect of seed mass on instantaneous survival persisting to adulthood.’’
Irrespective of the differences in the exact mechanisms promoting evolution of larger seeds, it seems reasonable that the
dramatic increase in seed size during the Early Tertiary and
the following drop in seed size after the Eocene were driven
by the changing composition of the vegetation, which affected
conditions during recruitment and juvenile development. However, there seems to be no conclusive evidence available for distinguishing between these two mechanisms.
Conclusions: A Synthesis of Coevolution,
Recruitment, and Life-Form
In the ‘‘Introduction,’’ four questions were asked: (1) Why
were seeds generally small and biotic seed dispersal rare during most of the Cretaceous? (2) What caused the dramatic increase in seed size during the Early Tertiary? (3) Why did seed
size drop after the Eocene? (4) Why is there a positive relationship between seed size and biotic seed dispersal? After an
examination of three proposed hypotheses, mainly based on
Eriksson et al. (2000a), Tiffney (2004), and Moles et al. (2005a),
I conclude that none of these hypotheses, viewed individually,
is fully compatible with paleo- and neoecological evidence but
that they all are partly supported and do contribute to answering the questions. This implies indirect support for the model
suggested by Wing and Tiffney (1987b), which incorporates
all three mechanisms.
Summarizing the evidence, it seems likely that the drastically
changing environmental conditions that occurred in the Early
Tertiary because of climate change and a paucity of large herbivores created a new arena for selection, one that was fundamentally different from what angiosperms experienced in the
Cretaceous. The changing conditions caused a mismatch between angiosperm life-history traits and environment (Ackerly
2003), and in this context, recruitment processes and coevolution between plants and mammals were both involved in promoting changes in seed size and biotic dispersal systems in
angiosperms. It is likely that large and long-lived plant lifeforms, large seed sizes, and biotic dispersal systems evolved as
sets of coadapted traits.
A tentative suggestion is that the change in seed size was
mainly driven by the changing composition of vegetation. Undisturbed and closed forest vegetation, as developed during
the global warming period in the Early Tertiary and with a
peak in the Eocene, when the fauna was devoid of any large
herbivores after the demise of the dinosaurs, created an envi-
ERIKSSON—EVOLUTION OF SEED SIZE AND BIOTIC SEED DISPERSAL
ronment where plants with large seeds were favored. The exact mechanism causing this advantage, whether competition
for light or long juvenile periods, cannot be identified. Seed
size dropped as vegetation became more open after the Eocene
and as grasslands developed during the Miocene and the Pliocene. Interestingly, a similar drop in seed size is currently apparent along a latitudinal gradient from the equator poleward, at
;25° from the equator (Moles et al. 2007). This result indicates that a more complete sampling of seed sizes in paleofloras, allowing for an examination of seed size variation along
paleolatitudes in the Tertiary, would be needed to gain a deeper
insight in the evolutionary trends in seed size. Most of the floras
used in Eriksson et al. (2000a) were from Europe, that is,
within a relatively limited range of latitudes. It might well be
that there was no drop in seed size in tropical floras after the
Eocene.
Although interactions with seed-dispersing vertebrates are
not likely to be a primary mechanism for evolution of larger
seeds during the Early Tertiary, coevolution between plants
and mammals was probably an essential component of the
evolution of biotic dispersal systems. Specialized frugivory
evolved along with the changing features of seeds and fruits,
indicating that during a formative phase from the Late Paleocene to the Eocene, both plant and mammal traits were reciprocally altered. Apart from feeding habits in general, there are
several suggestive examples of mammal traits that evolved as
adaptations to frugivory, such as the dentition in plesiadapiforms (Bloch et al. 2007) and the visual apparatus in primates
(Soligo and Martin 2006). The abundance of large seeds and
869
fleshy fruits provided a new food niche dimension, and it may
be that these new food resources promoted the radiation of frugivorous mammals in the Eocene. It is suggestive that BinindaEmonds et al. (2007) found that the diversification rate of
mammals was low after the K/T boundary and did not start to
increase until the Eocene, coinciding with the peak of average
seed size and the fraction of biotic dispersal in plants.
The observed stasis in fruit traits since the origin of fleshy
fruits and large, dry fruits (Collinson and Hooker 1991; Eriksson
et al. 2000a) reflects a pattern of evolutionary conservatism.
That shifts in fruit type (biotic vs. abiotic) nevertheless have
occurred along with vegetation shifts (open vs. closed) later in
the Tertiary suggests that fruit-type shifts are not constrained
if vegetation structure changes (Bolmgren and Eriksson 2005).
Thus, stabilizing selection rather than evolutionary constraints
is the most likely cause for trait conservatism in those lineages
where fruit types have remained stable. As long as plant species continue in their original environments, there seems to be
no strong selection to alter those functioning biotic seed dispersal systems that originated more than 40 million years ago
in the forests of the Eocene.
Acknowledgments
I am grateful to A. T. Moles, J. Ehrlén, P. R. Crane, S. A. O.
Cousins, and two anonymous reviewers for valuable comments
on the manuscript. This study was supported by the Swedish
Research Council.
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