1986). Analogous spectra of feeding behaviors exist
in bats and primates (Jordano 1992).
In Monteverde, the same dichotomy of fruit-han-
dling behaviors occurs among birds that consumed
fruits of three species of common "pioneer" plants
(Murray 1986b, 1988). Fruits of these species were
invariably ingested whole by Black-faced Solitaires,
Prong-billed Barbets, and Black-and-yellow Silky-
Flycatchers, with the result that seeds were widely
dispersed. Common Bush-Tanagers, Spangle-cheeked
Tanagers, and Yellow-thighed Finches fed on the same
fruit species by mashing and failed to ingest most of
the seeds; most were dropped near the parent plant,
with little chance of landing in a treefall gap. Seeds
ingested by the finch were destroyed in the gut
(Murray 1988). Small tanagers are so proficient at
separating seeds from pulp that they probably serve
as dispersal agents only for plants with minute (<1
mm) seeds (e.g., Ericaceae, Melastomataceae, Ges-
neriaceae, some Rubiaceae). Visitors to the fig Ficus
pertusa include small tanagers such as euphonias
and Golden-browed Chlorophonias who mash fruits,
dropping the seeds beneath the parent. Emerald Tou-
canets ingest them whole, probably dispersing them
more widely (Bronstein and Hoffman 1987).
Diet breadths of animals, "disperser breadths" of plants,
and the "specialization-generalization" paradigm. Two
seminal papers on plant-frugivore coevolution (Snow
1971, McKey 1975) spawned many studies on plant-
frugivore interactions. Most modern students of plant-
frugivore interactions (including those at Monteverde)
trace their interest to these or related papers (e.g.,
Howe and Primack 1975, Howe 1977). McKey (1975)
proposed that the coevolutionary process led to the
development of two groups of fruit-eating birds and
fleshy-fruited plants. He defined specialized frugi-
vores as those that derive most or all of their carbo-
hydrates, proteins, and lipids from fruit and that pos-
sess the morphological and physiological adaptations
that result in "high-quality" dispersal service to their
food plants (e.g., reduction in the muscular wall of the
stomach, reliability of visitation to fruiting plants,
heavy dependence on fruits as a food source). The
high-quality dispersal service they render favored the
evolution of small crops of fruits with dense, firm
flesh rich in proteins and lipids ("high-reward" fruits).
Specialized frugivores are large and tend to swallow
fruits whole, favoring the evolution of large fruits with
single large seeds that cannot be consumed by small
birds. Specialized frugivores and high-reward plants
should interact intensively, each bird species deriv-
ing most of its food from a small set of food plants,
and each high-reward plant relying on a small subset
of the potential seed dispersers. In Monteverde, Re-
splendent Quetzals, Keel-billed Toucans, and many
of their food plants, especially those in the avocado
family (Lauraceae), are classic examples of special-
ized frugivores and their coevolved and specialized
food plants under McKey's (1975) scheme.
McKey's "opportunistic" frugivores are those who
use fruits primarily as a source of carbohydrates and/
or water but rely on other foods as sources of lipids
and proteins. Many are primarily insectivorous or are
frugivorous as adults but feed insects to their nest-
lings. The great majority of fruit-eating birds fall into
this category. Since they were thought to lack an inti-
mate mutualistic relationship with particular plants,
opportunistic frugivores would lack many of the ad-
aptations that ensure the high-quality dispersal ser-
vice rendered to plants by specialized frugivores. The
plants that rely on opportunistic frugivores for seed
dispersal must make their fruits available to as wide
a variety of birds as possible, so such fruits are small,
succulent, and carbohydrate-rich and contain numer-
ous small seeds that can be swallowed even by small
birds ("low-reward" fruits). Because they are small,
such fruits can be produced in great abundance.
Tanagers, finches, and thrushes at Monteverde are
opportunistic frugivores, and most members of the
Melastomataceae, Solanaceae, and Rubiaceae pro-
duce low-reward fruits.
Pollen dispersal and seed dispersal by animals were
contrasted by Wheelwright and Orians (1982). They
concluded that the expectation of tight coevolution
of specialist frugivores and high-reward fruiting
plants was largely misguided:Plants benefit by directing pollen dispersers to
a definite, recognizable "target," a conspecific
flower, and they can provide incentives at flow-
ers which serve to attract potential pollinators.
In effect, there is "payment upon delivery" of
the pollen. In contrast, for seeds the target (an
appropriate site for germination and estab-
lishement) is seldom readily discernible, and
dispersal beneath a conspecific plant may ac-
tually be undesirable. Another important differ-
ence is that frugivores are "paid in advance."
(p. 410)The key requirement for tight coevolution of highly
specialized frugivores and high reward plants—con-
sistently higher dispersal quality by dietary special-
ists than by generalists—is unlikely to occur. Instead,
many different birds are likely to provide approxi-
mately similar dispersal quality to many plant spe-
cies. Over time, the net result should not be tight co-
evolution but "diffuse" coevolution (sensu Janzen
1980), whereby many unrelated plants and dispers-
ers converge on the same broad suites of fruit and259 Plant-Animal Interactions