BIOTROPICA 33(3): 487–494 2001

Seed Dispersal of the Mistletoe Psittacanthus schiedeanus by Birds

in Central Veracruz, Mexico1

Lorena López de Buen2 and Juan Francisco Ornelas3

Departamento de Ecologı́a y Comportamiento Animal, Instituto de Ecologı́a, A.C., km 2.5 antigua carretera a
Coatepec, Apdo. Postal 63, 91000 Xalapa, Veracruz, México

ABSTRACT
Mistletoes are hemiparasitic plants that frequently depend on frugivores for seed dispersal; yet their seed dispersal
ecology is still poorly known. The mistletoe Psittacanthus schiedeanus (Loranthaceae) was studied for a five-month
period in cloud forest remnants in central Veracruz, Mexico, to determine its seed dispersal ecology. We hypothesized
that dispersal ecology of this mistletoe species is directly affected by the fruit-eating bird abundance, and asked if this
species is following the high-investment strategy as suggested by Godschalk (1983). To evaluate this, we determined
the morphological and nutritional characteristics of mistletoe fruit, the availability of ripe fruits along the mistletoe
fruiting phenology, and the abundance of fruit-eating birds. Because P. schiedeanus is dispersed by generalist rather
than specialist birds, we asked if this mistletoe species is ripening fruits during the fruit scarcity time (with highest
possibilities of being consumed and dispersed by birds). We compared P. schiedeanus ripe fruit production to the cloud
forest tree leaf fall and fruit production. Psittacanthus schiedeanus matures its nutritious fruits from November to April,
with a peak of abundance in January and February. We found a synchrony between the abundance of P. schiedeanus
ripe fruits and the abundance of Gray Silky-flycatchers (Ptilogonys cinereus) and Social Flycatchers (Myiozetetes similis);
however, this was not the case with Cedar Waxwings (Bombycilla cedrorum), although these birds play an important
role in the mistletoe dispersal. The fruiting pattern of P. schiedeanus, together with the fact that it is an important
food resource for generalist rather than specialist frugivorous birds, suggest that this mistletoe is using the nutrient
investment strategy to attract dispersers during a time of fruit scarcity.

RESUMEN
Los muérdagos son plantas hemiparásitas que a menudo dependen de las aves frugı́voras para dispersar sus semillas;
sin embargo, sus estrategias de dispersión son poco conocidas. El muérdago Psittacanthus schiedeanus (Loranthaceae)
se estudió durante cinco meses en un remanente de bosque mesófilo de montaña en el centro de Veracruz, México,
para determinar la ecologı́a de dispersión de sus semillas por las aves. Presumimos que la ecologı́a de dispersión de
este muérdago está relacionada directamente con la abundancia de las aves frugı́voras; y nos preguntamos si esta especie
sigue la estrategia de alta inversión en nutrimentos sugerida por Godschalk (1983). Para evaluar esto, determinamos
las caracterı́sticas morfológicas y nutritivas de los frutos del muérdago, la disponibilidad de frutos maduros a lo largo
de su fenologı́a de maduración de frutos y la abundancia de las aves frugı́voras. Debido a que P. schiedeanus es
dispersado por aves generalistas, nos preguntamos si los frutos de este muérdago maduran cuando hay escasez de otros
frutos. Comparamos la producción de frutos maduros de P. schiedeanus con la caı́da de las hojas y la producción de
frutos en los árboles de bosque mesófilo de montaña. Psittacanthus schiedeanus madura sus frutos nutritivos de no-
viembre a abril, con un pico de abundancia en enero y febrero. Durante el perı́odo de estudio, encontramos sincronı́a
entre la abundancia de frutos maduros de P. schiedeanus y la abundancia de las aves Ptilogonys cinereus y Myiozetetes
similis; sin embargo, este no fue el caso con Bombycilla cedrorum, a pesar del papel importante que estas aves juegan
en la dispersión de este muérdago. El patrón de fructificación de P. schiedeanus, aunado a que es un recurso alimentario
importante para aves generalistas, en lugar de especialistas, sugiere que este muérdago está utilizando una estrategia
de alta inversión en nutrimentos para atraer dispersores durante el tiempo de escasez de frutos.

Key words: Cedar Waxwings; cloud forest; Gray Silky-flycatchers; mistletoe fruits; Psittacanthus schiedeanus; seed dispersal;
social flycatchers; Veracruz, Mexico.

MISTLETOES ARE HEMIPARASITIC FLOWERING PLANTS

1 Received 8 March 2000; revision accepted 22 August
2000.
2 Current address: Centro de Ecologı́a y Pesquerı́as, Di-
rección General de Investigaciones, Universidad Veracru-
zana, Km 3.5 Carretera Xalapa-Las Trancas, Avenida Dos
Vistas s/n, 91000 Xalapa, Veracruz, México.
3 Corresponding author: E-mail: ornelasj@ecologia.
edu.mx
that draw water and mineral resources from their
perennial host plants by means of haustoria (Kuijt
1969, Burger & Kuijt 1983, Calder & Bernhardt
1983). Several studies have shown temporal and
spatial associations between fruit abundance and
frugivore bird abundance (Levey 1988, Recher
1990, Rey 1995, Martı́nez del Rio et al. 1996).

487
488 López de Buen and Ornelas
Other studies have suggested the importance of
fruit conspicuousness and nutritional rewards for
the birds to choose mistletoe fruits and then dis-
perse them (Wheelwright et al. 1984, Willson &
Whelan 1990, Willson et al. 1990, Avery et al.
1995). The establishment of mistletoes in host
branches depends not only on seed and host char-
acteristics but also on the foraging behavior of the
birds consuming mistletoes (Reid et al. 1995, Ló-
pez de Buen & Ornelas 1999). Some mistletoes
have a set of specialized avian dispersers and main-
tain a mutualistic relationship with them (Snow
1981a,b; Davidar 1983; Reid 1989); i.e., avian dis-
persers obtain nutrients from the succulent mistle-
toe fruit pulp and then deposit the seeds with their
viscous endocarp onto an adequate site for their
germination and establishment while defecating or
regurgitating them (Monteiro et al. 1992, Overton
1994, Sargent 1995, López de Buen & Ornelas
1999). Snow (1981a, b) proposed that mistletoes
should offer highly nutritious fruits for the spe-
cialized bird consumers to afford an almost mo-
nophagous diet during the entire fruiting period.
The continuum of seed dispersal strategies in
flowering plants going from a ‘‘high investment in
nutrients’’ (one-seeded, large fruits with the pulp
being rich in proteins and lipids, and dispersed by
specialized frugivores) to a ‘‘low investment in nu-
trients’’ (many-seeded, small fruits with the pulp
being rich in water and carbohydrates, and dis-
persed by opportunistic–generalist frugivores) has
been suggested previously (Janzen 1970; McKey
1975; Snow 1971, 1981a, b; Howe & Smallwood
1982); however, the generality and usefulness of
this ecological paradigm has been recently ques-
tioned (Restrepo 1987, Howe 1993).
Godschalk (1983) proposed that among mis-
tletoes, the Loranthaceae family with large, one-
seeded, highly nutritious fruits (i.e., protein and
lipids) dispersed by specialized avian frugivores
should follow the high investment strategy; whereas
the Viscaceae with small, many-seeded, less nutri-
tive fruits (i.e., water and sugars) dispersed by more
generalized avian frugivores should follow the low
investment strategy. In this study, we provide an
alternative explanation to Godschalk⬘s (1983) pro-
posal in explaining the ‘‘high investment strategy’’
of the mistletoe Psittacanthus schiedeanus (Cham &
Schiecht) Blume ex Schultes, a species in the Lor-
anthaceae. In central Veracruz, Mexico, this mistle-
toe is an abundant parasite infecting several tree
species at remnants of cloud forest (López de Buen
& Ornelas 1999). Several bird species have been
observed feeding occasionally on its fruits, but Ce-
dar Waxwings (Bombycilla cedrorum Vielliot), Gray
Silky-flycatchers (Ptilogonys cinereus Swainson), and
Social Flycatchers (Myiozetetes similis Spix) are the
most important seed dispersers in the area (López
de Buen & Ornelas 1999).
López de Buen and Ornelas (1999) have pro-
posed that preference for some tree host species by
P. schiedeanus fruit-eating birds affects mistletoe dis-
persal directly; they also suggested that these birds
track the abundance of mistletoes because the black
ripe fruits have very conspicuous orange pedicels
and most of the host species shed their leaves dur-
ing winter. In this paper, we examine the ecology
of P. schiedeanus seed dispersal and ask if the abun-
dance of fruit-eating birds is associated with the
abundance of mistletoe ripe fruits and their re-
moval. To answer these questions, we monitored
fruit ripening phenology and evaluated the size and
nutritional characteristics of ripe mistletoe fruits.
We then estimated the number of fruits presum-
ably removed by the main consumers and assessed
the relationship between mistletoe fruit abundance
and the abundance of the main avian consumers.
Finally, we determined if this mistletoe is fruiting
at a time with the highest probability of being dis-
persed and compared the availability of mistletoe
ripe fruits to the phenological changes in leaf fall
and fruit production of the cloud forest trees in the
area, to suggest that this mistletoe species is using
the nutrient investment strategy to attract dispers-
ers during a time of fruit scarcity.
MATERIALS AND METHODS
STUDY SITE.—This study was conducted from No-
vember 1996 to April 1997, in a cloud forest rem-
nant of 100 ⫻ 900 m near Xalapa, Veracruz, Mex-
ico (19⬚30⬘N, 96⬚57⬘W; 1300 m elev.). Mean an-
nual precipitation is 1500 mm and mean temper-
ature is 18⬚C. The climate is mild and humid
throughout the year, with a dry and cool season
from November to March (Williams-Linera 1997).
Liquidambar styraciflua var. mexicana Oested (Ha-
mamelidaceae), Quercus germana Cham. & Schldl.,
Q. leiophylla A. D. C. (Fagaceae), Platanus mexi-
cana Moric. (Platanaceae), Acacia pennatula Cham.
& Schltdl. (Leguminosae), Crataegus mexicana Mo-
ciño and Sessé (Rosaceae), Persea americana Miller
(Lauraceae), and Citrus maxima (Burm.) Merr. C.
(Rutaceae), are the most common tree species (Cas-
tillo-Campos 1991, Williams-Linera 1997).
STUDY SPECIES.—Cedar Waxwings are winter visi-
tors to the study site from January to April, in

flocks of 15 to 80 individuals; Gray Silky-flycatch-
ers are common from November to March in pairs
or small groups of 3 to 6 individuals, but wander
into adjacent habitats after winter; and Social Fly-
catchers are resident throughout the year in the
area in pairs or small groups (as Gray Silky-fly-
catchers; Howell & Webb 1995, López de Buen &
Ornelas 1999). The three species consume the en-
tire fruit of P. schiedeanus. Cedar Waxwings and
Gray Silky-flycatchers defecate complete and viable
seeds, whereas Social Flycatchers regurgitate com-
plete viable seeds (López de Buen & Ornelas
1999).
FRUIT SIZE AND NUTRITIONAL VALUE.—Because the
birds feed only on mature mistletoe fruits (López
de Buen & Ornelas 1999), we measured the length
and width of black ripe fruits (N ⫽ 600), with a
digital caliper. Fruit weight was estimated with an
analytical balance. These fruits were weighted wet
(with and without seeds; N ⫽ 300) and dry (with-
out seeds; N ⫽ 300).
Nutritional values of ripe fruits were deter-
mined from 1620 fruits (221.36 g of fruit pulp)
collected from the forest floor beneath mistletoe
plants growing on L. styraciflua trees. We selected
this host species because it is preferred by birds and
by P. schiedeanus (López de Buen & Ornelas 1999,
López de Buen 2000). Only the fruit pulp was
analyzed because it is the only part digested by
birds. Fruit pulp was separated into six samples
(36.89 ⫾ 0.81 g) and dried by drying in cool
(11.93 ⫾ 0.75 g pulp dry mass). Nutritional con-
tent (%) with pulp dry mass was estimated accord-
ing to the following standard procedures: (1) pro-
teins by the micro-Kjeldahl method, (2) lipids by
the Soxhlet extraction method, (3) sugars by the
Luff-School method, (4) crude fiber by the asbes-
tos-free method, and (5) ash by burning the ma-
terial (Horwitz 1980, Hart & Fisher 1991, Lees
1994).
MISTLETOE AND FRUGIVOROUS BIRD ABUNDANCE.—
From 30 November 1996 to 18 April 1997, the
phenology and abundance of P. schiedeanus fruits
were followed weekly by counting the number of
green immature (⬍10 mm long), red–green unripe
(⬎10 mm long), black ripe, and removed (only the
peduncles left without the berry) fruits (N ⫽ 20
counts). We tagged 320 infructescenses from 20
individual mistletoe plants located between 2.5–3.5
m high in the host trees. These mistletoes were
growing onto L. styraciflua (1 mistletoe plant onto
one tree, 40 infructescenses and 174 fruits), A. pen-
Seed Dispersal in Mistletoe 489
natula (1 mistletoe plant onto one tree, 80 infruc-
tescenses and 308 fruits), C. mexicana (15 mistletoe
plants onto two trees, 160 infructescenses and
1017 fruits), and C. maxima (3 mistletoe plants
onto two trees, 40 infructescenses and 152 fruits).
We selected only the mistletoe plants in an area of
100 ⫻ 900 m that were accessible by a staircase.
The initial number of mistletoe fruits was 1651,
but numbers decreased as the fruiting season pro-
gressed.
The total number of each of the P. schiedeanus
fruit-eating bird species (Cedar Waxwings, Gray
Silky-flycatchers, and Social Flycatchers) was esti-
mated by counting the number of individuals fly-
ing, perching, or feeding during the time of mis-
tletoe fruit production, in a 100 ⫻ 900 m area.
Bird counting was done during a two-day intensive
bird search each week (0700–0900 h) when the
ripe fruit abundance was low (30 November 1996–
10 January 1997, and 12–18 April 1997; 24 h of
bird searching total), and seven days per week
(0700–0900 h) when the ripe fruit abundance was
high (11 January–11 April 1997; 196 h of bird
searching total; N ⫽ 20 counts). We used the non-
parametric Spearman’s coefficient of rank correla-
tion to test if the abundance of P. schiedeanus fruit-
eating birds (N ⫽ 20 counts) was correlated with
the abundance of mistletoe ripe fruits and mistletoe
ripe fruits removed (N ⫽ 20 counts). Because data
were not normally distributed (Zar 1984), we
square root (⫹0.5) transformed them for the anal-
ysis, but original data are reported in the figures.
MISTLETOE FRUIT PRODUCTION AND THE LOSS OF
LEAVES IN THE HOSTS .—Because we expected that P.
schiedeanus was using the nutrient investment strat-
egy to attract dispersers during a time of fruit scar-
city, when the orange pedicels and black fruits were
most conspicuous, we correlated the mistletoe ripe
fruit production (MFR) with the fruit production
and leaf loss of cloud forest tree species. The mean
number of mistletoe ripe fruits per month (MRF)
was estimated as: ⌺MRFi/Ni, where ⌺MRFi ⫽ to-
tal number of mistletoe ripe fruits per month i and
Ni ⫽ number of fruit monitoring sessions in
month i. Fruit production and leaf loss of cloud
forest tree species data were obtained from a phe-
nological study conducted by Williams-Linera
(1997) close to our study site (⬍500 m). She had
followed 107 tagged individuals representing 24
tree species from cloud forest (9 species were tem-
perate and deciduous, 1 temperate and evergreen,
11 tropical and evergreen, and 2 tropical and de-
ciduous), and carried out monthly phenological
490 López de Buen and Ornelas
observations on leaf fall and fruiting for five years
(January 1990–December 1994). She scaled the
phenological stages from 0 to 100 percent in five
categories (0, 1–25, 26–50, 51–75, and 76–100%)
and averaged these values for each of the 24 tree
species using a phenological index. We expected to
find a positive correlation between the P. schiedean-
us ripe fruit abundance and the loss of leaves from
the 24 cloud forest tree species of Williams-Linera
and a negative correlation between the P. schiedean-
us ripe fruit abundance and the fruiting production
of the 24 cloud forest tree species reported by Wil-
liams-Linera (1997). We used the nonparametric
Spearman’s coefficient of rank correlation because
data were not normally distributed for both anal-
yses of correlation (Zar 1984).
RESULTS
FRUIT SIZE AND NUTRITIONAL VALUE.—Psittacanthus
schiedeanus matures its fruits asynchronously dur-
ing all its fruiting period. One mistletoe plant may
produce up to 21 infructescenses (x̄ ⫾ SD ⫽ 20.7
⫾ 23.09; N ⫽ 20) with 5 fruits per infructescense
(5.16 ⫾ 3.05; N ⫽ 320), and each infructescence
has fruits in different ripeness stages. Fruits change
in color and size from the green immature (length
7.5 ⫾ 2.1, width 5.5 ⫾ 1.5; N ⫽ 300) through
the red–green unripe (length 12.4 ⫾ 1.2, width 8.4
⫾ 0.7; N ⫽ 300) to the black ripe (length 13.8 ⫾
0.9, width 9.5 ⫾ 0.7; N ⫽ 600) stages.
In ripe fruits of P. schiedeanus, more than half
of the fruit weight (63.6%) was constituted by the
fruit without seed (572.3 ⫾ 0.1 mg of wet fruit
without seed ⫻ 100/899.1 ⫾ 0.1 mg of total wet
fruit weight; N ⫽ 600 fruits without seeds). The
single seed constituted 36.4 percent of total fruit
weight (326.8 ⫾ 0.2 mg of seed ⫻ 100/899.1 ⫾
0.1 mg of total fruit weight; N ⫽ 300 seeds and
N ⫽ 600 fruits with seeds).
Water accounted for 91.3 percent of total fruit
weight (difference between wet and dry fruits). To-
tal solids in the fruit were 8.7 percent. The outer
part of the pericarp and pulp constituted 5.5 per-
cent (63.6% of total fruit weight ⫻ 8.7% of total
solids/100), and seed comprised 3.2 percent of the
FIGURE 1. (a) Immature, unripe, and ripe abundance of Psittacanthus schiedeanus fruits, and number of ripe fruits
removed per mistletoe plant from November 1996 to April 1997, and (b) their relationship to the abundance of
Cedar Waxwings (Bombycilla cedrorum), Gray Silky-flycatchers (Ptilogonys cinereus), and Social Flycatchers (Myiozetetes
similis) during the same period. Data are means, and error bars indicate SE.
total solids (36.3% of total fruit weight ⫻ 8.7% of
total solids/100).
Psittacanthus schiedeanus pulp was nutritious.
Water represented 67.8 ⫾ 0.3 percent, and total
solids constituted 32.2 percent ⫾ 0.29. Lipids rep-
resented most of the pulp dry mass (44.2% ⫾ 1.8),
followed by crude fiber (35.3% ⫾ 1.9), sugars
(12.4% ⫾ 0.8), proteins (6.5% ⫾ 0.3), and ash
(1.6% ⫾ 0.1). Lipids were 3.6 times more than
sugars (44.2 and 12.4%, respectively). A sample
size of six was used in all cases.
MISTLETOE AND FRUGIVOROUS BIRD ABUNDANCE.—
Ripe fruits of P. schiedeanus were available from
December 1996 to early April 1997 (Fig. 1a); how-
ever, the highest abundance of ripe fruits was in
January and February. Highest ripe fruit removal
occurred in late January and March. Low numbers
of Gray Silky-flycatchers and Social Flycatchers
were observed throughout the mistletoe fruiting
season; however, Cedar Waxwings were abundant
in late January and then decreased as the fruiting
season progressed (Fig. 1b). Numbers of Cedar
Waxwings were highly variable by mid-March and
April.
Observed variation in mean abundance of the
Gray Silky-flycatchers was positively correlated
with the variation in mistletoe ripe fruit abundance
(r ⫽ 0.75, N ⫽ 20, P ⬍ 0.001) and mistletoe ripe
fruits removed (r ⫽ 0.62, N ⫽ 20, P ⬍ 0.01).
Variation in mean abundance of Cedar Waxwings
was not correlated with variation in mistletoe ripe
fruit abundance (r ⫽ 0.19, N ⫽ 20, P ⬎ 0.05)
but was significantly correlated with ripe fruits re-
moved (r ⫽ 0.27, N ⫽ 20, P ⬍ 0.05). In contrast,
a nonsignificant relationship was found between
mean abundance of Social Flycatchers in relation
to the mistletoe ripe fruit abundance (r ⫽ ⫺0.05,
N ⫽ 20, P ⬎ 0.05) and mistletoe ripe fruits re-
moved (r ⫽ 0.22, N ⫽ 20, P ⬎ 0.05).
MISTLETOE FRUIT PRODUCTION AND THE LOSS OF
HOST LEAVES .—Fruit ripeness of P. schiedeanus oc-
curred mostly in winter when the cloud forest trees
shed their leaves and there were almost no other
ripe fruits available. As expected, we observed that
→
Seed Dispersal in Mistletoe 491
492 López de Buen and Ornelas
FIGURE 2. Relationship between the number of ripe
fruits of Psittacanthus schiedeanus mistletoe and tree leaf
fall and fruiting trees of cloud forest in an area nearest
the study site. The tree fruiting and leaf falling data are
phenological index values obtained from a five-year study
by Williams-Linera (1997). Numbers of fruiting mistle-
toes were also calculated as an index as described in the
text. Open squares represent number of ripe mistletoe
fruits and filled squares represent (a) falling leaves and (b)
fruiting trees. Error bars indicate SE.
the mistletoe ripe fruit production was positively
correlated with leaf fall (r ⫽ 0.77, N ⫽ 12, P ⬍
0.01) and negatively correlated with the fruiting of
cloud forest trees (r ⫽ ⫺0.77, N ⫽ 12, P ⬍ 0.01;
Fig. 2).
DISCUSSION
Psittacanthus schiedeanus, because of its nutritious
fruits (6% proteins, 44% lipids, and 12% sugars
in pulp) and few fruits per infructescense during
six months of the year (November–April), seems to
follow the seed dispersal strategy of high invest-
ment, as suggested by Godschalk (1983) for Lor-
anthaceae mistletoes. More sugar than lipids in
fruits appears to be the prevailing pattern in bird-
dispersed fruits (Herrera 1987). In addition, con-
trasting physiological mechanisms are required for
the digestion and assimilation of sugars and lipids
(Martı́nez del Rio et al. 1989, Witmer 1996, Wit-
mer & Van Soest 1998). The P. schiedeanus fruits
with a higher content of lipids than sugars belong
to the minority of plant species that produce high-
energy fruits (Herrera 1987), but are eaten and dis-
persed by generalist frugivores like the migrant Ce-
dar Waxwings (López de Buen & Ornelas 1999).
These migrant birds are able to subsist on fruits
with high sugar and low lipid contents for extended
periods without losing body mass, although they
also consume some lipid-rich foods (Stiles 1980,
McPherson 1987, Witmer 1996). In addition,
these migrant birds consume the mistletoe Phora-
dendron serotinum (Viscaceae) which have small
fruits (48–112 mg) with less protein (5.25%) and
lipids (6%) but more sugars (33%; McPherson
1987, Witmer 1996) than P. schiedeanus. In fact,
P. serotinum has been identified as one of the most
important fruits consumed by Cedar Waxwings in
temperate areas (McPherson 1987, Witmer 1996).
Among the other P. schiedeanus dispersers, Gray
Silky-flycatchers (López de Buen & Ornelas 1999)
are similar to Cedar Waxwings in also having a
high proportion of fruits in their diet; however,
they also consume insects (Howell & Webb 1995).
Social Flycatchers include many insects in their diet
in addition to fruits (Kantak 1979, Wheelwright et
al. 1984, Howell & Webb 1995). The dispersal
system of P. schiedeanus by these generalized fru-
givorous birds provides no evidence for this mistle-
toe species relying on specialized frugivores, and we
conclude that this study does not provide support
for Godschalk⬘s (1983) proposal.
Psittacanthus schiedeanus fruits ripen during
winter when most of the trees shed their leaves and
other fruits are scarce (Williams-Linera 1997). Ripe
fruit production peaked in January and February,
simultaneously with the peak in leaf fall and ab-
sence of fruit production by most other trees in the
area (Williams-Linera 1997). This may be an ad-
equate seed dispersal strategy developed by P. schie-
deanus, because its black ripe fruits with orange
pedicels can be very conspicuous to frugivorous
birds (López de Buen & Ornelas 1999) at a time
when most of the alternative food resources of for-
est trees are absent (Fig. 2). Removal of mistletoe
ripe fruits by birds occurred continuously during
the period of ripe fruit production, but fruit-eating
bird abundance was not always coincident with the
abundance and removal of the ripe fruits. In fact,
fruit removal during the day cannot be attributed
entirely to avian consumers because we also ob-
served squirrels (Sciurus aureogaster Cuvier) eating
ripe fruits.
Given that the abundance of Gray Silky-fly-
catchers varied proportionally with the abundance
 Seed Dispersal in Mistletoe 493

of mistletoe ripe fruits and that ripe fruit removal
was positively correlated with the abundance of Ce-
dar Waxwings, we suggest that P. schiedeanus fruits
are an important resource to both resident and mi-
gratory frugivorous birds. Other factors besides the
availability of P. schiedeanus ripe fruits may have
influenced the number of birds in the area (Levey
1988, Loiselle & Blake 1994). For instance, num-
bers of Cedar Waxwings vary over the fruiting sea-
son and among years for reasons other than mis-
tletoe fruit abundance (Brugger et al. 1994). We
have observed them in the study area every other
year (observed during the 1996–1997 fruiting sea-
son, not observed during 1997–1998, observed
during 1998–1999, and not observed during
1999–2000; López de Buen 2000). Yet, the rela-
tionship between the mistletoe ripe fruit removal
and Cedar Waxwing abundance at a time when
other resources are scarce, suggests the importance
of the fruits as a resource for the migrant frugivo-
rous birds.
Cedar Waxwings may represent a recent colo-
nization event into the mistletoe–bird interaction;
however, they could be acting as good, long-dis-
tance seed dispersers because of their abundance,
flocking behavior, and daily movements (López de
Buen & Ornelas 1999). Cedar Waxwings may be
including the P. schiedeanus fruits in their diet and
increasing their lipid reserves for their flight back
to harbor zones, in spite of their physiological lim-
itations in sugar and lipid assimilation (Martı́nez
del Rio et al. 1989).
Our data suggest that this mistletoe is produc-
ing fruits of a high nutritional value when some
groups of avian seed dispersers are present and few
fleshy fruit species are available. These results must
be interpreted with caution since both nutritional
quality of fruits and phenology of fruit maturation
may be strongly influenced by phylogenetic effects
(Herrera 1992, Jordano 1995). In any case, to
demonstrate the matching between the high in-
vestment strategy in P. schiedeanus and the related
ecological specialization of its frugivores, further in-
formation on major consumers along its geographic
range would be necessary.
ACKNOWLEDGMENTS
We thank M. C. Arizmendi, R. Dirzo, J. G. Garcı́a-Fran-
co, C. Herrera, C. Lara, C. Martı́nez del Rio, P. Rey, V.
J. Sosa, and two anonymous reviewers for their critical
comments on various versions of this paper. Thanks also
to S. Irissón and A. Martı́nez (Departamento de Ecologı́a
de Suelos, Instituto de Ecologı́a, A.C. Xalapa, Veracruz,
México) for help in fruit analyses. The Departamento de
Ecologı́a y Comportamiento Animal, Instituto de Ecol-
ogı́a, A.C., and a scholarship from CONACyT, México
(No. 95014) to L. López de Buen supported this study.
This work constitutes partial fulfillment of L.L.B. doc-
torate in Ecologı́a y Manejo de Recursos Naturales at the
Instituto de Ecologı́a, A.C.

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