Differential Seed Dispersal by Birds of the Tree Casearia nitida (Flacourtiaceae)

Author(s): Henry F. Howe and Richard B. Primack

Reviewed work(s):
Source: Biotropica, Vol. 7, No. 4 (Dec., 1975), pp. 278-283
Published by: The Association for Tropical Biology and Conservation
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Differential Seed Dispersal by Birds of the Tree Casearia nitida
(Flacourtiaceae)
Henry F. Howe
Museum of Zoology, University of Michigan, Ann Arbor, Michigan 48104 U.S.A.
and
Richard B. Primack
Department of Botany, Duke University, Durham, North Carolina 27706 U.S.A.

ABSTRACT
Data are presented which demonstrate (1) flight patterns of frugivorous birds are responsible for directional patterns
of seed dispersal, (2) these patterns influence seed mortality, and (3) dispersal of seeds away from the parent tree is
more likely to result from behaviors characteristic of obligate frugivores (Ramphastos sulfuratus and R. swainsonii)
than opportunistic frugivore/insectivores (Myiozetetes similts and M. granadensis). Investment by the parent tree in a
seed carried by a specialized frugivore is less likely to be wasted than investment in a seed carried by an opportunistic
frugivore because specialists are more likely to carry seeds away from areas of high seed mortality than opportunists.

PLANTS HAVE A VARIETY OF CHARACTERISTICS
which result in dispersal of their seeds by fruit-
eating animals. These involve the structure of the
fruit (van der Pijl 1969) or other aspects of plant
reproductive biology (Snow 1965; Smythe 1970;
Snow 1971). Previous studies consider the effects
of treatment by the digestive tract on the germina-
tion of seeds (Darwin 1859; Kerner 1897; Rick and
Bowman 1961), the effects of long-distance dispersal
on the biogeography of plants (Cruden 1966; Carl-
quist 1974), effects of dispersal on the survivorship
of seeds which suffer high levels of animal preda-
tion (janzen 1971), and the expected influence of
such predation on the local dispersion of plants (Jan-
zen 1970). The variety and abundance of fruits in
the tropics is correlated with a diverse bird fauna
showing varying degrees of specialization for fru-
givory and seed dispersal (Wetmore 1914; Keast
1958; Orians 1969; Karr 1971; Morton 1973).
Absent frcm previous studies are quantitative
data showing the patterns of seed distribution pro-
duced by movements of different kinds of dispersers
and the effects of this dispersal on the survivorship
of seeds. Such information is particularly desirable
in view of McKey's (1975) argument that the dis-
persal of seeds by "specialized" birds which are ob-
ligate frugivores should be qualitatively different
from dispersal by "opportunistic" birds which fac-
ultatively feed on fruit or insects. If this point of
view accurately reflects close coevolutionary relation-
ships between obligate frugivores and the plants
upon which they feed, we predict that specialists
should also produce patterns of seed distribution and
NOTE ADDED IN PROOF: The binomial for all central
American Casearia nitida has been changed to Casearia
corymbosa H. B. K.
resulting seed mortalitymore beneficial to the plant
than those produced by birds with less dependence
on fruit. This paper offers a partialtest of this pre-
diction and suggests furtherresearchwhich will elu-
cidate relationshipsbetween plants and their dispersal
agents.
STUDY SITE AND ORGANISMS
Investigationswere conductedin an abandonedcocoa
(Theodroma cacao L., Sterculiaceae) plantation at
Finca la Selva, Provincia de Heredia, Costa Rica,
between 17 and 20 Januaryand on 5 March 1974.
The site was at approximately80 m elevation on the
flood plain of the Rio Puerto Viejo in the Lowland
Wet Forest Zone (Holdridge 1967) at 10? 26' N
and 830 59' W. Slud (1960) gives a general de-
scription of the area.
Seed and seedling distributions and bird move-
ments were studied in the vicinity of two Casearia
nitida (L.) Jacq. (Flacourtiaceae) trees which were
70 m apartand approximately23 m high. Diameters
at breast height were 0.50 and 0.75 m with crown
edges from the trunks 6 m south and 4 m north and
6 m south and 5 m north, respectively. These two
trees and three other known conspecifics in the area
were in full fruit in January. None were in fruit
in March. Fruits are produced in dense masses on
the upper side of the branches. They are three-
parted capsules which split upon ripening and ex-
pose a single round seed (diameter 7-8 mm) covered
by a thin red aril. Birds pick arillate seeds out of
the capsule and either swallow them and pass the
seeds unharmedthroughthe digestive tractor remove
the aril and regurgitate the seeds. We observed
seeds germinate without either treatment. At La
Selva, C. nitida occupies a narrow band of alluvial

278 BIOTROPICA 7(4): 278-283 1975

soils adjacent to the Rio Puerto Viejo and its
tributaries (G. Hartshorn, pers. comm.).
The most common birds seen eating the arillate
Casearia seeds were the Social Flycatcher (Myio-
Transect III
zetetes similis (Spix), Tyrannidae), the Gray-capped
Flycatcher (M. granadensis Lawrence), the Masked
Tityra (Tityia semifasciata (Spix), Cotingidae), the
CA
Keel-billed Toucan (Ramphastos sulfuratus Gould,
Ramphastidae), and Swainson's Toucan (R. swafin-
S^CA Casearia 2
sonii Gould). Other species seen on fewer than
10 occasions were the Collared Aracari (Pteroglossus cH\
torquatus (Gmelin), Ramphastidae), Rufous Mour- R Transect 11
ner (Rhytipterna holerythra (Sclater and Salvin),
Cotingidae), and Scarlet-rumped Tanager (Ram-
phocelus passerinii Bonaparte, Thraupidae).
The two flycatchers were often indistinguishable
R Casearia I
in flight, but occurred in mixed groups and shared
N
the characteristic behavior of repeatedly flying from
the fruiting trees to neighboring non-fruiting trees
Transect I
at frequent intervals. These flycatchers are known
to depend heavily on fruit and insects for food
(Skutch 1960) and were observed to feed on arillate
seeds and insects at the Casearia trees. Another fre-
quent visitor, the tityra, arrived and left singly or in
pairs and was observed to eat only arillate seeds at FIGURE 1. Relationship of the position of perch trees
the Casearia trees, although this bird is also known (capital letters) to the two fruiting Casearia nitida trees
to eat insects regularly (Skutch 1946, 1954). The and to the three 70 m transects I, II, and III. The perch
trees are: C=Castilla elastica, CA=Cordia alliodoria,
two toucans were observed to eat only arillate seeds. H-Hernandia spp., R=Rollinia microsephala, S=Sapi-
These two species are known to depend almost ex- um pachystachys.
clusively on fruit as adults (Van Tyne 1929; Skutch
1971), although they sometimes take young birds
A one-meter-wide transect was laid out 70 m be-
(Skutch 1966). Small loose flocks of both toucans tween the trees and 70 m beyond each tree, resulting
straggled in to one or the other of the fruiting trees, in one straight 210 m transect divided into three
feed for a time, and then flew alone or in single file
parts by the bases of the two trees (Transects I, II,
to the next Casearia. Each small flock of three to
and III in fig. 1 ). All leaf litter was carefully
seven individuals visited both trees before passing
searched (i.e. picke-d over) in situ within one-square-
from sight. Sometimes different groups of toucans
meter enclosures for the entire length of the transect.
passed each other going in opposite directions. They
All C. nitida seeds were counted. Thus the data
gave the distinct impression that they visited trees on
yielded 210 separate counts representing each square
a regular feeding route, but data on marked in-
meter of the transect.
dividuals are not available. Toucans and tityras were
The study site was revisited on 5 March. A simi-
active in the fruiting trees from approximately 0600
to 0900 hours but were not usually present in late lar transect was evaluated for seedlings directly ad-
morning or afternoon. Flycatchers were present all jacent to the original one. This displacement was
necessary to avoid counting seedlings on the original
day, but fed primarily on insects in late morning
and afternoon. transect where the leaf litter had been highly dis-
turbed during the January counting. No intact
METHODS ungerminated seeds were found in either transect,
Birds were observed with binoculars. The number suggesting that this species does not have extended
and direction of flights away from each tree (those dormancy. Germination had occurred above the
flights with seed dispersing potential) were recorded ground; the radical penetrating the ground and lift-
for each bird species. Short flights to neighboring ing the cotyledons above the soil. There was no
trees (fig. 1) were distinguished from flights direct- evidence of rodent damage to seeds or seedlings in
ly to the other Casearia and from long flights out of either January or March; thus, if rodents do utilize
the sight of the observers. C. nitida seeds, they hoard them and chew none in

Seed Dispersal of Casearia nitida 279

sitg, which is not likely since seeds counted in Jan- three categoriesof disperserstended to fly long dis-
uary were represented on the original transect in tancesaway from the fruiting trees to unknowndesti-
March by seed coats (the endosperm having de- nations the same proportion of times. But toucans
cayed) or seedlings. Flocks of the White-crowned were much more likely to fly to another Casearia
Parrot (Pionus senilis (Spix), Psittacidae) ate and than were the flycatchers,and flycatcherswere much
destroyedseeds of Stryphnodendronexcelsum Harms more likely to fly to neighboring perch trees than
(Leguminosae) a few meters away, but none fed on toucans. Tityras showed intermediatefrequenciesof
C. nitida. Thus there is circumstantialevidence that both categories of flight. Thus a seed dropped in
only the aril and not the seed is palatable to birds flight by a toucan was much more likely to land
and rodents. We think that seeds representedby between Casearia trees than a seed dropped by a
seedlings in Marchaccountedfor most, if not all, of flycatcher. Seeds dropped from perch trees directly
those not destroyed by insects (evidenced by exit adjacentto the crown of the Caseariatrees (Cordia,
holes in January) and fungi between the Januaryand Rollinia, and Sapiam on fig. 1) appearedto extend
March countings. the area of high density beyond the crown of the
fruiting trees.
RESULTS Since these toucansmay be 13 to 22 times heavier
Figure 1 shows the position of the transects with than either species of flycatcher observed in this
respect to trees where foraging birds (usually fly- study and are almost totally dependent on fruit for
catchers) perched near Caseariatrees. Other trees food (table 2), it is assumedthat an individualtou-
were used for perching, but crown foliage density can carries more seeds than an individual flycatcher.
made observation impossible. More flights were This statement is borne out by contents of Ram-
made from Caselaria1 to a nearby Rollinia micro- phastos sulfuratus stomachs in the collection of the
sephalaStandl. (Annonaceae) than to any other tree, Museum of Zoology, University of Michigan. The
while the majority of flights from Casearia2 were material was collected in 1926 in Costa Rica and
to a Cordiaalliodora (Ruiz & Pav.) (Boraginaceae) Panama;five containedCasearia-sizedseeds and were
and a Sapium pachystachysSchum & Pittier (Eu- thus relevant to this study. Seeds numberedfive to
phorbiaceae) next to the crown edge of the fruiting 25, although the seed-carryingcapacity of this tou-
tree. The Castillaelstica Cervantes(Moraceae) and can is undoubtedlyhigher than 25 since the stomachs
Hernandia spp. (Hernandaceae) between the two also contained other plant material. The stomach
fruiting trees were often used as perch trees; they contents of one of these toucans would entirely fill
were frequently stop-over points when birds flew the body cavity of a Myiozetetes flycatcher which,
from one Caseariato another. There were 48 direct it should be remembered,also eats insects at the
flights recordedbetween Caseariatrees and 15 flights trees.
away from the Caseariatrees along transectsI and If flight patterns of birds do not influence the
III. Thirty-sevenflights were recordedto perching distribution of seeds and seedlings, it is reasonable
trees along transectII and 11 to trees on transectsI to expect that the distributionof seeds where birds
and III combined. Flights to the Castilla and fly between the two trees will be similar to the sum
Hernandiatrees (mostly by toucans) were scored as of distributionsin directionsaway from the same two
flights to perch trees,although many birds continued trees where birds rarely flew. The distribution of
on to the other Casearia. In-flight defecation was seeds on transect II between the two Caseariatrees
observed but could not be quantified. was compared with the summed distributions of
Table 1 shows that behavioral patterns of fly- transectsI and III in opposite directions from the
catchers, tityras, and toucans are different with re- inter-tree line. Using the parent trees as origins,
spect to relevant dispersing flights (o<0.001). The the distal portion of transect I was summed with

TABLE 1. Flight directions of three genera of frugivorous birds leaving two Casearia nitida trees.

Flights away Casearia to

Total no. Perch flights: from Casearias: Czsearia flights:
Genus of flights no. (percent) no. (percent) no. (percent)

Ramphastos 45 17 (38%) 6 (13%) 22 (18%)

Tityra 62 41 (66% ) 10 (16% ) 11 (18% )
Myiozetetes 248 193 (76% ) 40 ( 16% ) 15 ( 6% )a
a Differences in the distribution of flights are highly significant (p<0.001, X2 = 96.7, df = 4).

280 Howe and Primack

TABLE 2. Weights and general food habits of four frugivores at two Casearia nitida trees.
Mean weight
Species Sex (n) (grams) Food Food reference

Ramphastos swainsonii 8 (5) 661a fruit Skutch 1971, Van Tyne 1929
9 (2) 584
Ramphastos sulfuratus 8 (11) 410 Skutch 1971, Van Tyne 1929
9 (10) 383
Tityra semifasciata 8 (8) 80 insect, fruit Skutch 1946, 1954
9 (4) 89 "
Myiozetetes similis' 8 (7) 30 P Skutch 1960
9 (6) 28
a Weights are from specimen labels at the Museum of Zoology, University of Michigan, Ann Arbor, Michigan 48104, U.S.A.
bOne female of the similar M. granadensis in the Museum of Zoology weighted 29 grams when it was collected.

the complementary meter squares of the proximal density dependent and due to dispersal of agents
portion of transect III, and the distal portion of tran- (probably insects) from areas of high seedling
sect III was summed with the proximal portion of density.
transect I. Figure 2 compares the between-tree dis-
tribution (transect II; n 1201) square for square Transect II
with the summed distribution (transect I plus tran- o Transect I plus IlIl -------?
sect III; n = 860). The Komolgorov-Smirnov two-
sample test showed that the between-tree and
summed distributions were different (p?0.01). A
repetition of the procedure with March transects ~40 '
indicated that the distribution of seedlings between
trees (transect II; n - 377) was greater than the
en
sum of the distributions away from the trees (tran-
sects I plus III; n - 123; p<0.001). To eliminate (0202 ? %

the possibility that conclusions were influenced by A 01

202
peculiarities of the individual tree crowns, the analy-
sis of seed and seedling data was repeated for meter-
square plots more than 10 m from the tree trunks
(well beyond the 6 m crown edges). There were Tree 10 20 30 30 20 10 Tree
Distance in Meters
still more seeds and seedlings between trees than in
the sum of the two transects away from other trees
FIGURE 2. Three point means showing seed (top) and
(both p<0.001), even when the difference under seedling (bottom) distributions between (transect II)
the Castilla and Hernandia perch trees was not con- and away from (transectsI plus III) two fruiting Casearia
sidered. nitida trees. See text for further explanation.
Assuming that the patterns of dispersal and seed
mortality were similar before and after the January
04
census, it is possible to obtain a rough idea of seed
survivorship by dividing the three point means from
transect II in figure 2a by the corresponding ones X 3. 0
c
in figure 2b. As indicated in figure 3, mortality was a 0

relatively high under the crowns of the parent trees g 2.

as compared with areas between trees. Relatively
more seeds survived to the seedling stage under the
0) 1.
.0 0 0 *
Castilla and Henrndia perch trees (fig. 1) than
*
under parent trees (fig. 3), but survivorship directly Q *QQ~~~~~ .

under the perch trees (22 m from Casearia 2) was

Tree 10 20 30 30 20 1O Tree
depressed relative to survivorship of seeds under the Distance In Meters
crown edges of the two perch trees (13 and 30 m
from Casearia 2 at the right axis of fig. 3). This FIGURE 3. Relative survival of seeds under and between
two Casearia nitida trees.
finding suggests that mortality of seedlings was both

Seed Dispersal of Casearia nitida 281

DISCUSSION
Data presented here demonstrate ( 1 ) flight patterns
of birds are responsible for directional patterns of
seed dispersal, (2) these patterns influence seed
mortality, and (3) dispersal of seeds in suitable
habitats between parent trees is more likely to re-
sult from behaviors characteristic of specialized tou-
cans than those of the two opportunistic flycatchers
studied. Investment by the parent tree in a seed
carried by a toucan is less likely to be wasted than
investment in a seed carried by a flycatcher. This
situation is primarily true because toucans are more
likely to carry seeds away from areas of high seed
mortality but within suitable alluvial habitats than
flycatchers.
The presence at C. nitida of five common dis-
persers of widely different sizes, degrees of de-
pendency on fruit, and foraging behaviors suggests
that selection by bird dispersers is different in this
tree than it is upon large-seeded species such as
Iriartia exorrhiza Mart. (Palmae) which are dis-
tributed by large frugivores such as toucans (Van
Tyne 1929) or small-seeded trees such as Cecropia
spp. (Moraceae) which are dispersed by a variety
of birds and mammals (e.g. Eisenmann 1961). There
was no indication that arillate seeds of C. nitida were
superabundant on any particular day as noted by
Willis (1966) in tree species visited by numerous
species of birds. Because few trees fruit during
the seed drop of C. nitida (Frankie, Baker, and Opler
1974), we think that this species is in a position
to utilize both "high-quality" and "low-quality" dis-
persers (sensu McKey 1975; cf. Leck 1972). A Studies. The work started during a course in Tropical
premium on dispersal by the abundant flycatchers
would exist in years when relatively uncommon tou-
cans were absent. A detailed model will be pre-
sented elsewhere.
Much more evidence is needed for evaluation
of the ecological and selective importance of co-
evolutionary relationships between dispersal agents
and the plants upon which they feed. We suggest
that the following information is most critical: (1)
proportions of seeds carried by specialists and op-
portunists, (2) whether or not specialists follow
daily non-random feeding routes, (3) patterns of
seed distribution produced by different dispersers,
and (4) seedling survival with respect to these pat-
terns. A remarkable variety of coevolutionary re-
lationships has been demonstrated between plants
and pollinators (Faegri and van der Pijl 1966).
That a high degree of coordination between plants
and obligate dispersers exists is predictable from the
fact that the successful dispersal of one seed may be
worth the dispersal of "thousands" of pollen grains
(Grant 1958).
ACKNOWLEDGEMENTS
We wish to thank G. Hartshorn for assistance with tree
identification and J. Vandermeer for encouragement. J.
Antonovics, N. Christensen, D. Janzen, P. Opler, R. Payne,
P. Richards, and J. Silander offered helpful criticisms of
earlier drafts of the manuscript. The authors profited great-
ly from discussions with G. Estabrook. H. F. Howe and
R. B. Primack were supported in Costa Rica through grad-
uate fellowships from the University of Michigan and Duke
University. The March transect was made possible by a
grant to H. F. Howe from the Organization for Tropical
Ecology sponsored by the Organization for Tropical Studies.

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Seed Dispersal of Casearia nitida 283