1. Received__________________; revision accepted_____________________.
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Razafindratsima and Krauss3
POST-DISPERSAL SEED FATE IN MADAGASCAR4
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Title: Post-dispersal Predation and Removal of Seeds as a Function of Habitat Disturbance10
in Ranomafana Rainforest, Madagascar11
12
Onja H Razafindratsima1,2,* and Jacob Krauss113
1Department of BioSciences | Rice University | 6100 Main St. | Houston, TX 7700514
2Centre ValBio | BP 33 | Ranomafana, Ifanadiana 312 | Madagascar15
* Corresponding authoremail: onja@ricealumni.net

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ABSTRACT1
2
Post-dispersal predation and removal of seeds by rodents may play a critical role in plant3
recruitment dynamics, influencing regeneration in disturbed forest habitats. In Madagascar’s4
forests, increasing anthropogenic pressures and habitat alterations are contributing toward major5
declines in large-bodied frugivore populations; yet, the potential for rodents to mitigate this loss6
is relatively unknown. In this study, we investigated seed predation and removal post-dispersal in7
two habitat types with different levels of disturbances in the rainforest of Ranomafana National8
Park. We conducted experiments using tagged seeds of two native, vertebrate-dispersed, long-9
lived and large-seeded tree species. We found that disturbed and undisturbed forest habitats have10
different outcomes of seed fate such that: (i) seed predation was lower and removal of seeds was11
higher in disturbed than undisturbed habitat; (ii) a large proportion of the removed seeds were12
missing and none of the retrieved ones were cached in the disturbed habitat, whereas in the13
undisturbed habitat, half of the removed seeds were found but only a small proportion were14
cached in burrows. The distance seeds were moved from initial placement was short. Our15
findings form a preliminary account of the importance of rodents in Malagasy rainforests in16
secondary dispersal of seeds. They may play a role in primary seed dispersal as well in habitats17
where primary dispersers are scarce or even absent, with implications for forest regeneration; but18
this warrants further study.19
20
Key words: Abrahamia thouvenotii; Cryptocarya crassifolia; frugivorous vertebrate; Nesomys21
rufus; forest regeneration; rodents; seed dispersal; tropical forest22
23

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RESUMÉ1
2
Après dissémination primaire de graines, certains mécanismes écologiques comme la prédation3
et la dispersion secondaire par des rongeurs jouent un rôle primordial dans la dynamique de4
recrutement des plantes, influençant ainsi le processus de régénération des forêts perturbées.5
Dans les forêts tropicales malgaches, des incessantes pressions anthropiques et destructions6
forestières contribuent largement au déclin des vertébrés frugivores importants dans la7
dissémination primaire de graines de la majorité des plantes à Madagascar. Par contre, la8
potentialité des rongeurs pour mitiger les effets de la perte de ces disséminateurs primaires sur la9
forêt est relativement inconnue. Dans la présente étude, nous avons examiné ces mécanismes10
post-dispersion dans deux habitats ayant différents niveaux de perturbation, en effectuant des11
expériences utilisant des graines marquées de deux espèces de plantes, dans la forêt humide du12
Parc National Ranomafana. Nos résultats constituent une étude préliminaire sur l'importance des13
rongeurs dans les forêts malgaches dans la dispersion secondaire de graines, et probablement14
aussi dans la dispersion primaire de graines dans les habitats perturbés où les disséminateurs15
primaires sont rares, voire inexistants, avec des implications pour la régénération des forêts.16
Néanmoins, une étude plus approfondie serait nécessaire.17
18
IN THE FACE OF INCREASING THREATS TO TERRESTRIAL ECOSYSTEMS, SPECIAL EMPHASIS HASBEEN19
placed in understanding the consequences of habitat disturbances on plant and animal20
populations as well as their interactions. Habitat alterations have been recognized to have21
negative consequences on animal-mediated seed dispersal processes, affecting plant recruitment22
and subsequently forest regeneration (Farwig & Berens 2012). Given that post-dispersal seed23

4. Razafindratsima and Krauss
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predation and secondary dispersal play a crucial role in plant population dynamics (Wang &1
Smith 2002, Vander Wall, Kuhn, et al. 2005, Hulme 1998), understanding these processes can2
provide us insights on the regeneration of disturbed forests.3
Previous studies have shown that in the tropics, terrestrial vertebrate frugivores and/or4
granivores play an important role as either secondary dispersers, predators or both for large-5
seeded plant species (e.g., Beck 2005, Forget & Milleron 1991); however, we know relatively6
little about their role and activities related to seed dispersal in the tropical forests of Madagascar7
(but see Dausmann et al. 2008). The communities of terrestrial fauna in Madagascar are mainly8
composed of rodent species (Garbutt 2007), but it is not well-known to what extent they may act9
as seed dispersers and/or predators (but see Goodman & Sterling 1996), as observed in other10
systems (e.g., Forget 1990, Forget & Milleron 1991, Aliyu et al. 2014). Understanding post-11
dispersal seed fate is critical in Madagascar because of the alarming anthropogenic disturbances12
(such as clear-cutting of forests and fragmentation) that affect both the plant and animal13
populations in Madagascar’s forests (Ganzhorn et al. 2001, Harper et al. 2007, Watson et al.14
2004, Allnutt et al. 2013). In Madagascar, anthropogenic pressures and habitat alterations have15
led to significant declines and/or local extinctions of frugivorous vertebrates, including the16
extinction of at least 34 megafauna species, some of which may have acted as seed dispersers17
(Pedrono et al. 2013, Crowley et al. 2011); and the extant communities are highly threatened to18
extinction. The decline or complete elimination of large vertebrates is often associated with an19
increase in the abundance and diversity of rodent populations (Ganzhorn 2003, Young et al.20
2014, Dirzo et al. 2007). Therefore, secondary seed dispersal by rodents might be crucial for the21
regeneration of disturbed forests and the persistence of large-seeded plant species in the case of22
extinction of their primary dispersers (Jansen et al. 2012, Cao et al. 2011).23

5. Razafindratsima and Krauss
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Post-dispersal processes may vary with different levels of forest disturbance depending1
on the density of rodent populations as well as the availability of food resources (i.e., seeds)2
accessible to them, in different habitats. In disturbed habitats, seed predation may be higher as a3
result of greater density of rodents compared to undisturbed habitats (Asquith et al. 1997, Forget4
& Cuijpers 2008, Guariguata et al. 2000). Additionally, secondary removal of seeds may be5
lower in disturbed habitat because of high density of seeds falling under conspecifics in the6
absence and/or low abundance of dispersers (Forget & Cuijpers 2008, Chauvet et al. 2004).7
Alternatively, high density of seeds at conspecific and community levels may trigger rodents to8
scatter hoard seeds, which may influence seedling recruitment (Forget & Cuijpers 2008).9
In this study, we focused on two long-lived frugivore-dispersed tree species in10
southeastern Malagasy rainforest to investigate the impacts of forest disturbance on post-11
dispersal processes. We examined (1) how disturbed and undisturbed habitats differ in patterns12
of post-dispersal seed predation, (2) how they differ in patterns of secondary removal of seeds,13
and (3) whether secondarily removed seeds are hoarded. We carried out thread-marking seed14
experiments and observed animal activities using camera traps. Understanding seed fate in15
threatened systems such as Madagascar’ forests can have implications for understanding patterns16
of diversity and persistence of some plant species that have lost their primary dispersers. For17
example, rodents can partially compensate for the loss of large frugivores in their effective seed-18
dispersal role through scatter-hoarding of seeds (Jansen et al. 2012, Cao et al. 2011).19
20

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METHODS1
2
STUDY SITE AND SPECIES. – We tested for the effect of forest disturbance on secondary removal3
and post-dispersal predation of two plant species (Cryptocarya crassifolia and Abrahamia4
thouvenotii) in the rainforest of Ranomafana National Park (RNP), Madagascar (Fig. 1; 47°18’-5
47°37’E, 21°02 - 21°25S). RNP covers 41,000 ha of evergreen montane forest (Wright &6
Andriamihaja 2002), with plant communities of more than 330 known species (Razafindratsima7
& Dunham 2015). The climate in RNP is seasonal with a peak of wet season in January-March8
and a peak dry season in June-October; average monthly rainfall ranges from 10-1200 mm, and9
average yearly temperature ranges from 4-32ºC (Dunham et al. 2011, Wright et al. 2012). This10
study was conducted in two habitat types within RNP, one in disturbed secondary forest and one11
in natural primary forest. The habitat in Vohiparara is characterized by secondary and heavily12
logged forest; while Valohoaka is composed of a mixture of undisturbed and selectively logged13
forest (Gerber et al. 2010, Razafimahaimodison 2003). The community of terrestrial vertebrates14
in the area, which could be potential secondary seed dispersers and/or predators, includes eight15
native rodent species (Brachytarsomys albicauda, Brachyuromys betsileoensis, Gymnuromys16
roberti, Nesomys rufus, Nesomys audeberti, Eliurus tanala, Eliurus minor and Eliurus webbi)17
and one introduced rat Rattus rattus in both secondary and primary forest, and the introduced18
mouse Mus musculus in secondary forest only (Lehtonen et al. 2001, Carleton & Schmidt 1996).19
The invasion of Rattus rattus was found to be associated with forest disturbance levels, with high20
density near forest edge (Lehtonen et al. 2001) .21
The studied plant species, Cryptocarya crassifolia (Lauraceae) and Abrahamia22
thouvenotii (Anacardiaceae), are long-lived canopy trees with large-sized single ovoid seeds23

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(respectively, length and width: 20 x 19 mm and 22 x 16 mm – Razafindratsima and Dunham1
2015, Razafindratsima unpbl. data). Fruiting occurs from March-October for Cryptocarya2
(Razafindratsima & Dunham 2015) and from April-August for Abrahamia (Razafindratsima3
unpbl. data). The primary dispersers of their seeds include Malagasy primates (Razafindratsima4
et al. 2014, Razafindratsima & Dunham 2015). These plant species were chosen because they are5
common in RNP and were fruiting during our study period.6
7
EXPERIMENTAL DESIGN. – We conducted seed fate experiments in June-August 2014 during their8
fruiting period, at the end of wet season and starting dry season. Seeds were manually extracted9
from fresh ripe fruits collected on the ground of fruiting trees, and sun-dried before the10
experiment. To determine seed fate, we attached on each seed a non-conspicuous string (~ 7511
cm) with a flagging of ~15 cm at the distal end of the string to tag and track its movement from12
initial placement (Wenny 2000, Forget & Cuijpers 2008). The flagging was buried under leaf13
litter to make it less visible to animals. For the string, we initially used fishing line; but14
unfortunately, rodents in our study system chewed off the line in almost all cases, so we replaced15
the fishing line with thin metal wire. Both tagging methods have been proved to be effective in16
studying seed fate in other systems (Forget & Wenny 2004, Xiao et al. 2006, Wenny 2000). We17
took this different type of string into account in our data analyses.18
In each site (undisturbed and disturbed), we haphazardly established 80 plots (40 per19
plant species) spaced at least 100 m apart and located at least 5 m away from main trails to avoid20
human disturbance. We placed, in each plot, 5 marked seeds above the ground cleared of litter21
and marked with a wire flag (Forget & Cuijpers 2008). Seeds in each plot were counted after 1,22
3, 7 and 14 days; seeds are usually no longer attractive to rodents after 14 days due to desiccation23

8. Razafindratsima and Krauss
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or fungal attack (Forget & Cuijpers 2008, Forget et al. 2000). We also looked for any sign of1
seed predation, such as bite marks or if only pieces of the seed remained. We searched for any2
removed seed in 25-m radius surrounding the plot. Once a seed is retrieved, we checked the end3
of the string where the seed had been attached to determine its fate: if it was entirely removed4
from or if it remained attached to the string; or if the seed has been eaten, it is classified as killed5
by seed predators; otherwise, uneaten seeds will be left in the new location and included in6
subsequent censuses (Wenny 2000). We also measured the distance between the initial plot7
placement and the new retrieval location, and recorded whether the retrieved seed had been8
cached, buried or left in the open. Cached and buried seeds were dug for tag identification if9
necessary and to check its status, but then were put back in the same location. After the 14th10
monitoring day, we put new seeds in the same plots.11
12
DATA ANALYSES. – We analyzed our data using a generalized nonlinear model (GNM) in R 3.0.313
(The R Foundation for Statistical Computing), with habitat type (disturbed and undisturbed),14
seed species and the type of string used (fishing line vs. metal wire) treated as fixed effects.15
Replicates were based on proportion of seeds being predated or removed in each plot.16
17
RESULTS18
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Our data show that overall on-site post-dispersal predation was low (10.14%, n = 2200), and was20
lower in disturbed than undisturbed habitat (Fig. 2; β = -0.04, P = 0.03), with very low to no21
predation for Cryptocarya (Fig. 2; β = -0.21, P < 0.0001). The type of string used in the22

9. Razafindratsima and Krauss
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experiment (fishing line vs. metal wire, nested within seed species) did not have any significant1
effect on the observed predation (β = 0.08, P = 0.382).2
Secondary removal of seeds (Fig. 3) was higher in disturbed than undisturbed habitat (β3
= 0.06, P = 0.01), but not significantly different among the two seed species (β = -0.03, P =4
0.12). The type of string used had a significant effect on the removal of seeds from the plots,5
with lower removal using metal wire (β = -0.17, P < 0.0001). Overall, 14.91% of seeds in the6
experiment plots were removed. Among the removed seeds (n = 328), only 11.49% (n = 235)7
were retrieved for the plots in disturbed site and 54.84% (n = 93) in undisturbed site, at an8
average distance of 1.63 m (up to 8 m). Of the retrieved seeds, 17.65% were found cached in9
rodent burrow for those in undisturbed habitat, while others were either cached under leaf litter10
of left in the open; but we did not find any occurrence of caching in disturbed habitat. The11
retrieved seeds were left on their new locations for subsequent monitoring; among these, we12
found that subsequent removal and predation occurred only in 3 plots (n = 19) in undisturbed13
habitat; whereas none occurred in the disturbed habitat.14
15
DISCUSSION16
17
Understanding post-dispersal processes, such as predation and secondary removal of seeds, has18
an important implication for our understanding of forest regeneration in the face of increasing19
anthropogenic disturbances. This is especially important in the tropics, where a majority of tree20
species are adapted for seed dispersal by vertebrates (Howe & Smallwood 1982) that are highly21
threatened by habitat disturbance. In Madagascar’s forests, the low richness and abundance of22
frugivores, coupled with the tight associations between trees and frugivores as primary seed23

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dispersers suggest substantial disadvantages for the effective establishment of trees in forests1
where such frugivores are absent (Razafindratsima 2014). However, the importance of post-2
dispersal events in Madagascar’s forests, which influence plant recruitment dynamics (Wang &3
Smith 2002, Vander Wall, Kuhn, et al. 2005, Hulme 1998), has rarely been examined (e.g.,4
Dausmann et al. 2008). In this study, we show that disturbed and undisturbed forest habitats have5
different outcomes of seed fate, and that secondary dispersal of seeds by rodents may play a6
crucial role in the regeneration of disturbed habitat.7
The different outcomes observed between the two habitat types in this study may be a8
result of their differences in the density, diversity and abundance of rodent populations that may9
predate and/or remove seeds. The dynamics of rodent populations are often associated with10
forest disturbance and defaunation (Ganzhorn 2003, Young et al. 2014, Dirzo et al. 2007). In11
Ranomafana, for example, heavy logging is associated with the loss of some endemic rodent12
species, but an increase in the abundance of non-native rodent species (Lehtonen et al. 2001).13
Thus, the high removal of seeds in the disturbed habitat, which is dominated by secondary14
growth following clear-cutting and selectively logging (Gerber et al. 2010, Razafimahaimodison15
2003), may be a result of higher abundance of some rodent species in such habitat as compared16
to the undisturbed habitats. In a concurrent study, we observed from camera traps Nesomys rufus17
eating or sniffing seeds in our experimental plots in the undisturbed habitat (Razafindratsima18
unpbl. data), suggesting that this species may play an important role in the post-dispersal process19
in Ranomafana. The availability of food resources accessible to seed predators, which may vary20
between the two habitats, may also influence post-dispersal predation of seeds. For example,21
high abundance of fruits fallen underneath the crowns of parent trees, when primary seed22
dispersers are scarce or absent, can provide enough food for the rodents (Chauvet et al. 2004,23

11. Razafindratsima and Krauss
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Howe & Smallwood 1982); this may explain the low predation of seeds in the disturbed habitat.1
The effects of forest disturbance on seed predation might be more complex than this because the2
passage of seeds through the digestive tract of lemurs, which are among the primary dispersers of3
these two plant species in Ranomafana (Razafindratsima et al. 2014, Razafindratsima & Dunham4
2015), can render seeds unattractive to seed predators (Spehn & Ganzhorn 2000). Alternatively,5
difference in habitat characteristics (e.g., canopy cover and understory density) and the6
abundance of fruit production in these two forest types could also affect post-dispersal processes7
(Forget et al. 2002, Razafindratsima & Dunham 2015, Hulme 2002, Bowers & Dooley 1993).8
Our results also show that post-dispersal predation of seeds differed between plant9
species, but not seed removal; probably resulting from their differences in seed traits,10
palatability, chemical content and profitability (Aliyu et al. 2014, Forget & Milleron 1991,11
Hulme & Benkman 2002, Lai et al. 2014). Abrahamia has a softer and thinner endocarp than12
Cryptocarya (Razafindratsima, pers. obs.) allowing predators to easily consume the seed, and13
thus maximizing their energy intake while reducing the costs associated with seed handling14
(Hulme & Benkman 2002). Biochemical contents present in some seed species, such as toxins15
and certain amino acids, may also act as deterrents for granivores (Hulme & Benkman 2002,16
Bodmer 1991); however, further investigation is needed to see whether these two species differ17
in their chemical contents. Conversely, certain seed species may also be favored over another18
because of its rewarding value (Hulme & Benkman 2002, Lai et al. 2014).19
Previous studies suggest that the significant decline and/or loss of large frugivores as20
primary seed dispersers might eventually lead to local extinction of large-seeded tree species,21
which rely on such groups for their dispersal (Farwig & Berens 2012, McConkey et al. 2012,22
Stoner et al. 2007). However, primary dispersal limitation does not necessarily translate into23

12. Razafindratsima and Krauss
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dispersal failure, because species, such as scatter-hoarding rodents (Cao et al. 2011, Jansen et al.1
2012), with equivalent ecological services might compensate or replace the frugivore loss2
(García et al. 2013, Peterson et al. 1998). Although we were unable to recover a majority of the3
removed seeds in both habitats and we did not find evidence of scatter-hoarding, our data form a4
preliminary account of the importance of rodents in Ranomafana in secondary dispersal of seeds,5
with implications for forest regeneration. Removal of seeds from the ground was more likely to6
occur in the disturbed habitat, where large-bodied primary dispersers such as lemurs are expected7
to be in low density or even absent. Therefore, rodents can play a role as both primary and8
secondary dispersal agent of Cryptocarya crassifolia and Abrahamia thouvenotii, and possibly9
other large-seeded tree species, in such a habitat, if other frugivores fail to fill the role as primary10
dispersers, similar to what was observed in other systems (e.g., Cao et al. 2011, Jansen et al.11
2012). Secondary removal of seeds may allow the plant to reach a more favorable microsite for12
its establishment and escape the effects associated with close proximity to parent trees (Vander13
Wall, Kuhn, et al. 2005, Vander Wall, Forget, et al. 2005). Our findings indicate short dispersal14
distance from initial locations; but the removed seeds that were unaccounted for may have been15
moved further, even outside our 25 m retrieval limit, which might be really important for16
survival. Removed seeds may also be forgotten or abandoned in the caches and thus may survive17
to germinate later (Forget 1990, Hulme & Benkman 2002). Furthermore, they might be removed18
again and re-cached (Cao et al. 2011, Jansen et al. 2012, Xiao et al. 2005), reducing the relative19
density within caches and increasing dispersal distances.20
Mechanisms underlying post-dispersal seed fate are certainly complex with interacting21
effects of different factors, including tree abundance, fruit production, relative abundance of22
seeds, frugivore and granivore density and diversity, animal behavior, environmental variables23

13. Razafindratsima and Krauss
12
and season (Farwig & Berens 2012, Cordeiro et al. 2009, Forget & Milleron 1991, Jorge &1
Howe 2009, Schleuning et al. 2011). During the course of this study, we were unable to address2
all these factors specifically; but our findings open up discussion to new perspectives for detailed3
examination of post-dispersal processes and the role of rodent species in forest regeneration in4
Madagascar’s forests in a more comprehensive framework. While our results indicate that5
rodents could play a role in the fate of large seeds in Ranomafana, further investigation using6
technology that reduces uncertainty (Wróbel & Zwolak 2013) are needed to elucidate their7
effectiveness as seed dispersers and to extend our understanding of secondary seed dispersal in8
Madagascar’s forests; although the use of Passive Integrated Transponder (PIT) in the rainforest9
of Ranomafana was not as successful (Razafindratsima, unpbl. data) as in other systems (e.g.,10
Suselbeek et al. 2013). More research is also needed to understand what species of rodents and to11
what degree they might help maintain the diversity and persistence of large-seeded plant12
communities.13
14
ACKNOWLEDGMENTS15
16
Research and logistical support was provided by Rice University, MICET and Centre ValBio;17
and through grants to O.H.R from Rice University (Wagoner Foreign Study Scholarship) and18
The Rufford Foundation (Rufford Booster Grant). O.H.R. was also supported by Schlumberger19
Foundation. We thank Madagascar National Parks and the Malagasy Ministry of Forest and20
Water for research permission. We are also grateful to Fenosoa Rojoarivelo, Parfait Rafalinirina,21
Jocelyn Mamiharalala, Nerée Beson, and Jean-Claude Ramanandraibe for their assistance with22
fieldwork, and to Amy Dunham for valuable comments.23

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1
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FIGURE LEGENDS1
Figure 1 – Location of study sites within Ranomafana National Park, Madagascar.2
3
Figure 2 – Average (±SE) percentage of Cryptocarya crassifolia and Abrahamia thouvenotii4
seeds predated on the experimental plots at two habitat types (disturbed vs. undisturbed) in5
Ranomafana National Park, Madagascar for.6
7
Figure 3 – Average (±SE) percentage of Cryptocarya crassifolia and Abrahamia thouvenotii8
seeds that were secondary removed from the experimental plots differed between the two habitat9
types (disturbed vs. undisturbed) in Ranomafana National Park, Madagascar10

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Figures1
Fig. 12
3

25. Razafindratsima and Krauss
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Fig. 21
2
0.00
0.10
0.20
0.30
0.40
disturbed undisturbed
seedpredationrates
Abrahamia
Cryptocarya

26. Razafindratsima and Krauss
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Fig. 31
2
0.00
0.10
0.20
0.30
disturbed undisturbed
seedremovalrates
Abrahamia
Cryptocarya