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Habitat fragmentation disrupts a plant-

disperser mutualism in the temperate forest of
South America

Article in Biological Conservation · September 2007

DOI: 10.1016/j.biocon.2007.06.014

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journal homepage: www.elsevier.com/locate/biocon

Habitat fragmentation disrupts a plant-disperser mutualism

in the temperate forest of South America

Mariano A. Rodrı́guez-Cabala,b,*, Marcelo A. Aizena, Andrés J. Novaroc

a
Laboratorio Ecotono-CRUB, Universidad Nacional del Comahue, Quintral 1250, (8400) San Carlos de Bariloche, Rı́o Negro, Argentina
b
Department of Wildlife Ecology and Conservation, University of Florida, P.O. Box 110430, Gainesville, FL 32611-0430, USA
c
CONICET-WCS, Centro de Ecologı́a Aplicada del Neuquén, C.C. 7, (8371) Junı́n de los Andes, Neuquén, Argentina

A R T I C L E I N F O A B S T R A C T

Article history: The disruption of dispersal mutualisms may have profound consequences for seedling
Received 5 September 2006 recruitment, plant demography, and population persistence, with potential cascading
Received in revised form effects throughout the rest of the community. In the temperate forest of South America,
6 April 2007 the seeds of the mistletoe Tristerix corymbosus, a proposed key species, are dispersed solely
Accepted 18 June 2007 by the endemic marsupial Dromiciops gliroides. In three sites that included two contrasting
Available online 14 August 2007 habitats, one fragmented and the other not, we assessed effects of forest fragmentation on
marsupial abundance, fruit removal, seed dispersal and seedling recruitment rates. We also
Keywords: compared the age structure of mistletoe populations between fragmented and non-frag-
Dromiciops gliroides mented forest habitats. Fragmentation affected negatively marsupial abundance, fruit
Habitat fragmentation removal, seed dispersal, and seedling recruitment. The local extinction of D. gliroides was
Keystone mutualism associated with the complete disruption of mistletoe seed dispersal. Mistletoe populations
Mutualism disruption in fragmented forests exhibited a deficiency in juveniles because of a lack of recruitment.
Seed dispersal Thus, effects of forest fragmentation on this dispersal mutualism have clear demographic
Tristerix corymbosus consequences, which may compromise the survival of mistletoe populations.
Ó 2007 Elsevier Ltd. All rights reserved.

1. Introduction on species interactions due to local extinctions and/or

replacement of interactive partners (Kareiva, 1987; Saunders
Plant–animal mutualisms, including pollination and seed dis- et al., 1991; Aizen and Feinsinger, 1994a,b; Esseen, 1994; San-
persal, are essential interactions not only for the persistence tos and Tellerı́a, 1994; Santos et al., 1999). In turn, the disrup-
of mutualistic partners, but also for biodiversity maintenance tion of these interactions, particularly of plant–animal
and ecosystem integrity (Tabarelli et al., 1999; Traveset, 1999; mutualisms, may cascade through the community increasing
Christian, 2001; Cagnolo et al., 2006). The disruption of polli- extinction rates of species directly or indirectly involved in
nation and seed dispersal mutualisms can affect sexual these relationships (Aizen and Feinsinger, 1994a; Bond, 1994;
reproduction, patterns of gene flow, plant recruitment and Harrison and Bruna, 1999; Traveset and Riera, 2005). Particu-
population demography, other interspecific interactions, and larly, these cascading effects may worsen when the affected
also species potential for evolutionary change (Wilson et al., mutualists are also keystone species. Despite the ecological
1995). importance of these species, and of the interactions they
Fragmentation and, more generally, alteration of natural are involved in, fragmentation studies focused on keystone
habitats due to human activities can have profound effects mutualists are rare.

* Corresponding author: Address: Department of Wildlife Ecology and Conservation, University of Florida, P.O. Box 110430, Gainesville, FL
32611-0430, USA. Tel.: +352 846 0647; fax: +352 392 698.
E-mail addresses: rcabal@ufl.edu (M.A. Rodrı́guez-Cabal), marcelo.aizen@gmail.com (M.A. Aizen), anovaro@wcs.org (A.J. Novaro).
0006-3207/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biocon.2007.06.014
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196 B I O L O G I C A L C O N S E RVAT I O N 1 3 9 ( 2 0 0 7 ) 1 9 5 –2 0 2

Here we assess effects of forest fragmentation on seed dis- Austrocedrus chilensis. The understory is dominated by the
persal of the mistletoe Tristerix corymbosus (L.) Kuijt, a key- shrubs Aristotelia chilensis and Maytenus boaria, the main hosts
stone species from the temperate forest of South America. of T. corymbosus, Azara microphylla and the bamboo Chusquea
This plant species represents the main, and in some regions culeou (Mermoz and Martı́n, 1986). Introduced plants are also
the sole winter nectar source for Sephanoides sephaniodes Gray common in the fragmented sites, including Prunus sp., Populus
(Aizen, 2003), the only year-round resident hummingbird in spp., and scotch broom, Cytisus scoparius.
this forest and responsible for the pollination of nearly 20% T. corymbosus produces fruits that are green when ripe.
of the highly endemic woody flora of this biome (Smith- Typical of Loranthaceae, each fruit contains only one seed
Ramirez, 1993; Armesto et al., 1996; Aizen and Ezcurra, 1998; that lacks teguments. When defecated, the sticky pulp sur-
Aizen et al., 2002). rounding the seed facilitates its attachment to the branch.
Because of its aerial parasitic habit, seed dispersal repre- Seeds can be dispersed singly or more commonly in ‘‘neck-
sents a critical step in a mistletoe life cycle. Thus, it is not sur- laces’’ of up to 20 seeds linked by viscin threads.
prising that dispersal of mistletoe seeds is usually carried out This study was carried out in three sites between 18 and
by specialized birds (Reid, 1991). In the temperate forest of 30 km west of the city of San Carlos de Bariloche (41°S,
southern South America, however, the seeds of T. corymbosus 71°W): Cerro Campanario, Llao-Llao, and Villa Tacul. In each
are exclusively and efficiently dispersed by the marsupial site, we selected two adjacent habitat units, one represented
Dromiciops gliroides Philippi (Amico and Aizen, 2000; Aizen, by a mosaic of several forest fragments of 1–5 ha each and
2003). the other by a continuous forest >1500 ha that neighbors an
This marsupial consumes massive amounts of T. corymbo- extensive forest area protected within the National Park.
sus fruits during the austral summer, ingesting and defecat- The two habitat units within a given site were chosen based
ing the soft mistletoe seeds undamaged. In addition, most on similarity in vegetation structure and composition, and
defecated seeds are stuck to branches and the passage the occurrence of a population of T. corymbosus with >40 indi-
through the marsupial’s gut is crucial to trigger germination viduals within each habitat unit. Fragments were surrounded
(Amico and Aizen, 2000). D. gliroides is considered a true living by a clearcut matrix, which was periodically brushed and/or
fossil (Marshall, 1978; Kelt and Martı́nez, 1989; Spotorno et al., mowed. Nearest-neighbor distances between fragments ran-
1997; Springer et al., 1998), and this mistletoe–marsupial dis- ged between 60 and 500 m. The two study populations within
persal interaction might represent a very ancient mutualism each site were <1 km apart. Thus, our experimental design in-
that could have preceded the origin of more widespread mis- volved paired comparisons between mistletoe populations in
tletoe-bird dispersal (Amico and Aizen, 2000). Given the high fragmented and continuous forest habitats.
dependence of the mistletoe on D. gliroides for seed dispersal,
the disruption of this mutualistic interaction might have di- 2.1. Marsupial abundance
rect implications for the survival of T. corymbosus populations
with ramifying consequences on different components of the We estimated the abundance of D. gliroides by means of live-
biota. trapping. We used wire traps (Tomahawk-style) baited with
Our specific goals were to determine how forest fragmen- banana and apple, and sampled each habitat unit with 20
tation affects: (1) marsupial abundance, (2) fruit removal, (3) traps placed about 5 m apart along a 100 m transect. In the
seed dispersal, and (4) seedling recruitment. The assessments fragmented habitats traps were placed in 2–3 forest frag-
of all the stages involved in the dispersal process allow us to ments. Traps were run over four consecutive days each
make strong inference on how human-driven disturbance month from December to March. Traps were checked daily
may influence a highly specialized dispersal interaction. In and all trapped marsupials were marked with an individual
addition, we compared the age structure of mistletoe popula- code based on ear perforations. Marked marsupials were re-
tions between fragmented and non-fragmented habitats to leased in the same place where captured (see Wilson et al.,
evaluate the potential demographic consequences of the dis- 1996).
ruption of this mistletoe–marsupial mutualism. Here we pres- We used the minimum-number-alive (MNA) index (Con-
ent results from a field study that strongly suggest that roy, 1996) as an estimator of D. gliroides abundance. The lack
habitat fragmentation has disruptive effects on a keystone of recaptures in the fragmented habitats precluded the use
interaction for the conservation of the temperate forest of of abundance estimators based on capture–recapture meth-
South America. ods (Nichols and Pollock, 1983; Nichols and Dickman, 1996)
for all habitat units. However, capture–recapture estimates
2. Materials and methods of abundance for the continuous forest units resulted in sim-
ilar qualitative differences between sites and habitat units as
This study was carried out in three sites adjacent to Nahuel the minimum-number-alive (results not shown).
Huapi National Park, Argentina, in the 2000/2001 austral
summer (December–March), the main fruiting and dispersal 2.2. Seed dispersal
season of T. corymbosus (Aizen, 2003). Mean annual precipita-
tion in the study area is ca. 1800 mm. January and July tem- In each habitat unit, using small paper tags we marked imma-
peratures average 15 and 3 °C, respectively. Native forest ture fruits in each of 12 plants chosen at random. At weekly
vegetation in the area belongs to the Subantartic biogeo- intervals over the sampling period, we recorded the status
graphical region (Cabrera, 1976). Dominant trees are the ever- of each fruit according to one of the following categories:
green southern-beech Nothofagus dombeyi and the conifer developing fruit, ripe fruit, removed fruit, and senescent
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B I O L O G I C A L C O N S E RVAT I O N 1 3 9 ( 2 0 0 7 ) 1 9 5 –2 0 2 197

(non-removed) fruit. Ripe fruits are green but soft to the dispersal rates as the total number of seeds dispersed found
touch. A fruit was considered removed when it was ripe in along each transect divided by the total number of fruits pro-
one census but it was missing in following censuses. Fruits duced by the mistletoes present on the transect. This estima-
disappearing from the plant when ripe imply animal removal tion assumes that the number of seeds dispersed from
(see Aizen, 2003 for further details). As fruits senesced or were mistletoes occurring on tagged shrubs to surrounding non-
removed, we marked new fruits to monitor a constant num- tagged shrubs was similar to the number of seeds dispersed
ber of 20 fruits per plant over the sampling period. Fruit re- from mistletoes on surrounding non-tagged shrubs to the
moval was estimated as the percent of all tagged fruits shrubs tagged along each transect. Although this assumption
removed over the sampling period. To estimate dispersal may not be necessarily true, these dispersal estimates should
rates, we tagged 100 shrubs and tree saplings (DBH < 15 cm) not be biased by habitat type and thus they are useful for
about 2 m apart along a 200 m transect at each site and hab- comparative purposes.
itat unit. In the fragmented habitat units, these plant tran-
sects encompassed 2–3 forest fragments and overlapped the 2.3. Seedling establishment and age distribution
marsupial-trapping transects. Tagged shrubs included host
and non-host plants. We counted the number of reproductive We evaluated the effect of habitat fragmentation on seedling
individuals of T. corymbosus on the tagged plants and esti- establishment over two years. In December (late spring) 2000
mated the number of fruits (=seeds) produced by each mistle- and 2001, we counted all new mistletoe seedlings (those pre-
toe. At weekly intervals, we marked all new feces found on senting the first true two leaves) occurring on the shrubs
tagged shrubs and counted seeds in each feces. We estimated tagged along each transect. These seedlings established from

Campanario Tacul Llao-Llao

40
No. D. gliroides

30

20

10

100
% fruits removed

80

60

40

20

8
% seeds dispersed

7
6
5
4
3
2
1
0
% seedlings established

0.45
0.40
0.35
0.30
0.25
0.20
0.15
0.10
0.05
0.00
Continuous Fragmented Continuous Fragmented Continuous Fragmented
Habitat type Habitat type Habitat type

Fig. 1 – Seed dispersal and seedling establishment of Tristerix corymbosus in continuous vs. fragmented forest at Campanario,
Tacul, and Llao-Llao: (a) minimum number of Dromiciops gliroides individuals in each sampled area, (b) number of fruits
removed, (c) seeds dispersed, and (d) seedlings established as a percent of the number of fruits (=seeds) produced. In (b), T-
bars represent + 1 SE.
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the seeds dispersed during the previous fruiting season, aus- and three continuous) was considered as a replicate. Because
tral summers 1999/2000 and 2000/2001, respectively. Seedling disperser abundance should have an overriding influence on
establishment was estimated as the (median) number of mistletoe seed dispersal and establishment, we related the
seedlings per host plant for both 2000 and 2001 seedling variables we hypothesized to depict the dispersal process;
counts; and also as a percent of seed production by the focal i.e., number of marsupials vs. no. fruits removed and no.
reproductive mistletoes for the seedlings counted only during seeds dispersed, no. fruits removed vs. no. seeds dispersed,
2001, the year we had estimations of seed production. and no. seeds dispersed vs. no. seedlings established. Number
We studied the age structure of the mistletoe populations of fruits removed, seeds dispersed, and seedlings established
occurring in each site and habitat unit. To develop a non- were expressed as a percent of fruit (=seed) production.
destructive age index, we first collected 40 individual mistle-
toes, encompassing the range of observed sizes, from different 3. Results
study sites and different hosts. Each T. corymbosus individual
was harvested along a 5 cm long segment of the host branch The estimated minimum number of marsupials present at
centered at the attachment point of the mistletoe. We mea- each sampling habitat unit ranged between 0 and 29 individ-
sured diameter of the mistletoe scar, maximum basal diame- uals. We found a consistent effect of forest fragmentation on
ter of the mistletoe, diameter of the host branch at the the abundance of D. gliroides. In all three sites, the estimated
infection, length of the longest mistletoe branch, number of number of dispersers was lower in the fragmented habitat
branch tips, maximum branching order, and the length of unit than in the nearby continuous forest (t = 1.79, p = 0.11;
the infection scar. Fig. 1a). We did not capture any D. gliroides in the fragmented
We estimated mistletoe age by counting the number of an- habitat at Campanario. Large differences also occurred
nual growth rings of the host plant at the infection from the among the three continuous forest units. For instance, mar-
host bark to the end of the deepest mistletoe haustorial con- supial abundance in the continuous forest at Campanario
nection. The accuracy of this method to age mistletoes and a was as low as in the fragmented forest at either Tacul or
detailed description of the histological procedure we used can Llao-Llao (Fig. 1a).
be found in Norton et al. (1997). The coefficient of determina- The abundance of reproductive mistletoes was relatively
tion (r2) of the regressions between age and each of the seven higher in the continuous than in the nearby fragmented hab-
morphological variables we measured, ranged between 0.45 itat. Along the transects set in the continuous and frag-
and 0.73 (Rodrı́guez Cabal, 2003). We chose the regression mented habitat units, we found, respectively, 25 and 19
with the best fit, i.e. between age and the length of the longest reproductive mistletoes at Campanario; 46 and 18 at Tacul;
mistletoe branch, as a non-destructive age estimator (age in and 43 and 23 at Llao-Llao (t = 2.80, p = 0.11). However, the
years = 0.086 * length in cm + 1.968, n = 40, r2 = 0.73). We used number of fruits produced per mistletoe showed a more
this linear equation to estimate the age of all mistletoes equivocal trend. The mean ± 1 SE number of fruits produced
(one-yr old seedlings excluded) found on tagged shrubs and per reproductive plant was 891.2 ± 33.4 (continuous) and
treelets at each site and habitat unit. 736.7 ± 37.8 (fragmented) at Campanario, 641.9 ± 42.5 and
1264.4 ± 89.6 at Tacul, and 409.8 ± 12.6 and 740.9 ± 45.7 at
2.4. Data analysis Llao-Llao (t = 1.17, p = 0.36). Thus, mean total fruit produc-
tion per transect for the fragmented and continuous habitat
We used a paired t-test to compare marsupial abundance, types were 23,143 vs. 17,933, respectively (t = 2.21, p = 0.16).
number of reproductive mistletoes, fruit production, fruit re- Additionally, we found 59 (continuous) and 65 (fragmented)
moval, seed dispersal, and seedling establishment between host plants among the 100 shrubs sampled in each of the
fragmented and non-fragmented habitat units considering two habitat units at Campanario, 97 and 55 at Tacul, and 90
each site as a replicate (i.e., two degrees of freedom). Exclud- and 72 at Llao-Llao. Therefore, the mean number of reproduc-
ing the number of reproductive mistletoes and fruit produc- tive mistletoes per host plant was higher in the continuous
tion per mistletoe and transect, these tests were one-tailed than in the fragmented forest (0.46 vs. 0.31 mistletoes/host;
because of the hypothetical disruptive effect of habitat frag- t = 18.67, p < 0.005).
mentation on the dispersal process. In addition, because of The percent of tagged fruits removed over the 10-wk sam-
the logistic difficulties to achieve high replication in this type pling period ranged between 30.2% and 86.8%; with the frag-
of conservation studies we used a more liberal significance le- mented forest at Campanario showing the lowest rate of
vel of a = 0.10 (Vázquez and Simberloff, 2004). In any event, we fruit removal and the continuous forest at Llao-Llao the high-
combined p-values from the t-tests of the four variables de- est rate. Fruit removal was consistently higher in the contin-
picted in Fig. 1 for a composite test of the fragmentation effect uous forest than in the fragmented forest unit at all three
on the study dispersal process (p. 779, Sokal and Rohlf, 1981). sites (t = 3.68, p = 0.03; Fig. 1b).
We represented the age structure of mistletoes in each The estimated percentage of all seeds (=fruits) produced
habitat unit grouping observations in 2-yr classes. We com- that were dispersed successfully ranged between 0% and
pared the frequency distribution of individual ages between 6.2%. We found no seeds dispersed in the fragmented forest
mistletoe populations in the fragmented and non-fragmented at Campanario, whereas the largest percentage of seeds dis-
habitat unit of each site by means of a Kolmogorov–Smirnov persed was recorded in the continuous forest at Llao-Llao.
test (Zar, 1984). The percentage of seeds dispersed was consistently larger in
We summarized our main results using regression analy- continuous forest than in the nearby fragmented habitat unit
sis where each of the six habitat units (i.e., three fragmented at all three sites (t = 1.98, p = 0.09; Fig. 1c).
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The number of one-year seedlings per host plant was populations in continuous forest had a large proportion of
consistently higher at the continuous than at the frag- young individuals (<6 years old) and were slightly j-shaped.
mented habitat unit in both 2000 (9 vs. 0 for Campanario; In contrast, populations in the fragmented forests exhibited
24 vs. 0 for Tacul; 66 vs. 2 for Llao-Llao; t = 1.99, p = 0.09) a deficiency of new recruits and the most populous age clas-
and 2001 (4 vs. 0 for Campanario; 33 vs. 0 for Tacul; 72 vs. ses were either 6–7 or 8–9 year old. Very young mistletoes
3 for Llao-Llao; t = 1.88, p = 0.10). A similar trend was ob- were absent at both Campanario and Tacul (Fig. 2).
served when the numbers of seedlings established in 2001 Regression analysis showed that the abundance of D. gliro-
were expressed as a percent of the seeds produced during ides was a good and significant predictor of fruit removal
the previous summer (t = 2.00, p = 0.09; Fig. 1d). Although this (Fig. 3a), whereas fruit removal was a good predictor of seed
difference was weaker for Campanario than the other two dispersal (Fig. 3b). Most notably, the abundance of D. gliroides
sites, we were unable to find any seedlings in the frag- closely predicts the number of seeds dispersed (Fig. 3c), and
mented forest at that site. the number of seeds dispersed the number of seedlings estab-
We estimated that about 5% of the dispersed seeds germi- lished (Fig. 3d) after accounting for differences in seed
nated, infected the host and established a seedling in the con- production.
tinuous forest at Campanario. This figure could not be
estimated for the fragmented forest at this site because of a 4. Discussion
lack of seeds dispersed there. Similarly, values were 7.8%
(continuous) vs. 0% (fragmented) for Tacul, and 6.7% vs. Our results suggest that the negative impacts of forest frag-
3.5% for Llao-Llao. mentation on the abundance of a marsupial seed disperser
Overall, we found a consistent disruptive fragmentation can have a strong impact on the dynamics of seeds and seed-
effect on the mistletoe–marsupial dispersal interaction. Com- lings, with potential effects on the overall demography of
bining p-values from individual t-tests for each of the four mistletoe populations. Declines in the number of individuals
variables depicted in Fig. 1 resulted in a highly significant of the seed disperser, D. gliroides, related closely to declines
composite effect (X2 = 20.75, df = 8, p < 0.01). in the removal of fruits and dispersal of seeds of the mistletoe
Estimated mistletoe ages ranged between 2 and 16 years T. corymbosus. The number of seeds dispersed linked directly
old. Age distributions of mistletoe populations in continuous to the number of seedlings established and new recruits in
and fragmented forest were different (K–S = 0.242, p < 0.005 the study mistletoe populations. Our results imply that the lo-
for Campanario; K–S = 0.233, p < 0.03 for Tacul; and K– cal extinction of the marsupial may completely disrupt this
S = 0.287, p < 0.001 for Llao-Llao). At all three sites, mistletoe plant-disperser mutualism dooming mistletoe populations
to extinction with unknown, but presumed widespread com-
munity-level consequences.
Effects of forest fragmentation and alteration on popula-
60
Campanario tions of D. gliroides may involve multiple and compounding di-
50 Continuous
Fragmented rect and indirect factors. First, this highly endemic marsupial
40
is mostly arboreal, dwelling in cavities high in the canopy of
30
old-growth Nothofagus forests. Thus, one direct cause of the
20
decline of D. gliroides in fragmented forests can be a reduction
10
in the absolute amount and average patch size of its favored
No. of mistletoe individuals (%)

0
habitat. This could be the case of the fragmented habitat at
60 Llao-Llao where well-defined small forest patches remain rel-
Tacul
50 atively isolated in the middle of a golf course in what was pre-
40 viously continuous forest. Second, diverse indirect effects can
30 permeate through the borders of the remnant forest patches
20
(Murcia, 1995), including an increase in predation (Andren
and Angelstam, 1998; Nupp and Swihart, 1998) by native
10
and introduced vertebrates, particularly domestic cats (Eben-
0
hard, 1988; Crooks and Soule, 1999). This might be the case of
60 the fragmented habitat at Campanario, where forest rem-
Llao-Llao
50 nants are surrounded by a suburban matrix of gardens and
40 plant nurseries.
30 In addition, distances as short as 50–100 m across an
20 inhospitable habitat can represent powerful barriers that can-
10 not be traversed by many small forest mammals (Bierregaard
0 et al., 1992). This seems to be the case of D. gliroides. This mar-
2-3 4-5 6-7 8-9 10-11 12-13 >14 supial was almost absent in some of the study fragments de-
spite the high abundance of mistletoe fruits there and
Age (yr)
proximity (<100 m) of these fragments to continuous forest.
Fig. 2 – Age structure of T. corymbosus populations occurring This hypothesized reduction in the dispersal of D. gliroides
in continuous vs. fragmented forest at Campanario, Tacul, due to habitat fragmentation could difficult the ‘‘rescue’’ of
and Llao-Llao. the small marsupial populations that might be trapped in
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200 B I O L O G I C A L C O N S E RVAT I O N 1 3 9 ( 2 0 0 7 ) 1 9 5 –2 0 2

Forest fragmentation affected negatively mistletoe fruit re-

90 2
r = 0.75, p < 0.01 moval and seed dispersal. Although, D. gliroides is the sole
75 seed disperser of T. corymbosus at least in the temperate forest
% fruits removed

60 of South America (Amico and Aizen, 2000; Aizen, 2003), mis-

45 tletoe fruits are also predated by a few species of birds (e.g.,
Phrygilus patagonicus) and mice (e.g., Oligoryzomys longicauda-
30
Continuos tus and Abrotrix olivaceus). The presence of non-dispersing
15 Fragmented frugivores could explain the removal of mistletoe fruits in
0 the fragmented forest habitat at Campanario, where we did
0 10 20 30 not capture marsupials. However, although some of these
No.D. gliroides animals are very opportunistic (e.g., P. patagonicus and O. lon-
gicaudatus) and might increase their presence in disturbed
7 habitats, the abundance of D. gliroides seems to exert an over-
2 riding influence on mistletoe fruit removal (Fig. 3a) and be
6 r = 0.71, p < 0.02
% seeds dispersed

highly predictive of seed dispersal (Fig. 3c).

5
Fragmentation greatly affected the establishment of mis-
4
tletoe seedlings. Number of seedlings declined strongly in
3 the fragmented forest units and these effects were highly
2 consistent across two seedling cohorts. Because mistletoe
1 seed germination and seedling establishment are particularly
0 susceptible to desiccation (Sargent, 1995; Yan and Reid, 1995),
10 20 30 40 50 60 70 80 90
increased mortality due to water stress in the more light-ex-
posed fragmented forest environment could be a plausible
% fruits removed
explanation for the patterns we found (Harrison and Bruna,
7 1999; Bruna, 2002). The potential for this contributing factor
2 is partially supported by our results, i.e., a trend towards a de-
6 r = 0.98, p < 0.001
% seeds dispersed

crease in the number of seedlings established per dispersed

5
seed in at least two of the fragmented habitat units. However,
4 seed dispersal seems to be the overriding factor limiting the
3 number of established seedlings in T. corymbosus (Fig. 3d).
2 Two synergetic effects reinforce this relationship: (1) the
1
highly specific dispersal process itself that involves the defe-
cation and ‘‘gluing’’ of seeds onto branches of an appropriate
0
host plant, and (2) the passage through the marsupial guts
0 10 20 30
that is critical for triggering seed germination (Amico and Ai-
No.D. gliroides
zen, 2000).
The dispersal link has been perceived as particularly criti-
0.9
2
cal and vulnerable in mistletoe life cycle (Reid, 1991). In our
% seedlings established

0.8 r = 0.99, p < 0.001 study system, the disruption of the interaction between D.
0.6
gliroides and T. corymbosus may have implications not only
for seedling establishment, but also mistletoe population
0.4 dynamics. A decline in juveniles in all three fragmented pop-
0.3 ulations and a lack of new recruits in two of these populations
imply that altered patterns in seed dispersal can have impor-
0.2
tant demographical consequences. In addition, we observed a
0.0 decline in the abundance of reproductive mistletoes, not ex-
0 1 2 3 4 5 6 7 plained by host availability, which in turn could promote fur-
% seeds dispersed ther declines of marsupial populations in forest remnants.
Thus, we forecast that fragmentation of these southern for-
Fig. 3 – Regressions of the number (a) of individuals of
ests could not only involve the local extinction of D. gliroides,
Dromiciops gliroides vs. fruits removed, (b) fruits removed vs.
but also of the mistletoe T. corymbosus through the disruption
seeds dispersed, (c) number of individuals of Dromiciops
of its dispersal mutualism. This is to our knowledge one of
gliroides vs. seeds dispersed, and (d) seeds dispersed vs.
the first fragmentation studies linking seed dispersal and
seedlings established considering each habitat unit as a
plant demography. Only a few studies have focused on effects
replicate. Plant variables are expressed as a percent of the
of habitat fragmentation on the plant-disperser mutualism.
fruits produced (see Section 2).
In Tanzania, for example, fragmentation of mountain rainfor-
est leads to impoverished assemblages of frugivorous species,
fragments, increasing the chance of their collapse due to lower rates of seed dispersal, seedling establishment and
either demographic or genetic bottlenecks (see Brown and juvenile recruitment of populations of several animal-dis-
Kodric-Brown, 1977). persed tree species (Cordeiro and Howe, 2001; Cordeiro and
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