Research Article |
Corresponding author: Alexander V. Christianini ( avchristianini@yahoo.com.br ) Academic editor: Ana Maria Leal-Zanchet
© 2020 Ana Y. Y. Meiga, Alexander V. Christianini.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Meiga AYY, Christianini AV (2020) Potential impact of mammal defaunation on the early regeneration of a large-seeded palm in the Brazilian Atlantic Forest. Neotropical Biology and Conservation 15(2): 177-193. https://doi.org/10.3897/neotropical.15.e54017
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Defaunation, the decline in animal species and populations, is biased towards large-bodied animals that have unique roles as dispersers of large seeds. However, it is speculated that these roles may still be performed by smaller animals, such as small mammals like rodents and marsupials, that thrive in defaunated sites. We investigated if small mammals can disperse the large-seeded palm Attalea dubia. We performed the study in a well-conserved Atlantic Forest remnant in southeast Brazil that still harbours large mammals, such as tapirs. Focal observations showed that capuchin-monkeys consumed the mesocarp of the fruits and dropped the seeds beneath the plant crown thereafter. Mammals preyed on ca. 1% and removed ca. 15% of the fallen fruit/seed and deposited them up to 15 m away. Amongst them, small mammals (< 1 kg), such as the squirrel Guerlinguetus brasiliensis and non-identified nocturnal Sigmodontinae, as well as the marsupial Philander frenatus performed the bulk of interactions. Dispersal enhances recruitment, but the short distances of seed removal did not match the current spatial distribution of palm seedlings and juveniles. Recaching rates of hoarded seeds were small (2%) and unlikely to increase distances of seed dispersal achieved. Short distances of dispersal would increase plant clumpiness and negative density-dependent effects with time. Although small mammals can provide legitimate dispersal, they cannot fully replace larger frugivorous mammals and maintain long-distance seed dispersal that feeds plant metapopulation dynamics and seed gene flow.
Defaunação, o declínio de populações e espécies de animais, é enviesada para animais de grande tamanho corporal que têm papéis únicos como dispersores de sementes grandes. Contudo, especula-se se esses papéis podem ainda ser desempenhados por animais menores, como pequenos mamíferos como roedores e marsupiais, que prosperam em sítios defaunados. Assim, investigamos se pequenos mamíferos podem dispersar efetivamente a palmeira de sementes grande Attalea dubia. Executamos este estudo em uma floresta atlântica bem conservada no sudeste do Brasil que ainda tem grandes mamíferos, tais como as antas. Observações focais mostraram que macacos-prego consumiram o mesocarpo dos frutos e derrubaram as sementes da palmeira sob a copa. Mamíferos predaram ca. 1% e removeram ca. 15% desses frutos/sementes caídos e os depositaram a uma distância de até 15 m. Entre eles, pequenos mamíferos (< 1 kg), tais como esquilos Guerlinguetus brasiliensis e Sigmodontinae noturnos não identificados, bem como o marsupial Philander frenatus, executaram a maioria das interações. A dispersão incrementou o recrutamento, mas as distâncias curtas de dispersão de sementes não se ajustaram à distribuição espacial atual das plântulas e juvenis da palmeira. Taxas de redistribuição de sementes estocadas foram pequenas (2%) e provavelmente incapazes de aumentar as distâncias de dispersão alcançadas. Pequenas distâncias de dispersão incrementariam o agrupamento de plantas e efeitos de dependência de densidade negativos com o tempo. Embora pequenos mamíferos possam proporcionar dispersão legítima eles não podem substituir completamente mamíferos frugívoros maiores e manter dispersão de sementes em longa distância necessária à dinâmica de metapopulações e ao fluxo gênico por sementes.
Attalea, defaunation, seed dispersal, seed hoarding, seedling distribution
Attalea, defaunação, dispersão de sementes, distribuição de plântulas, estoque de sementes
Defaunation, i.e. the extirpation of animals by hunting, habitat loss, habitat fragmentation, climate change and pollution, may impact several ecosystem processes (
There is a positive correlation between body size and risk of extinction in mammals, with a predictable size-selective defaunation gradient with increasing disturbance (
The aparent short distances of seed dispersal provided by rodents may be enough for the recruitment of LSP far away from parental plants. For instance, hoarded seeds may be recached several times by different individual agoutis that steal seeds from one another (
In this study, we investigated the role of small mammals in seed dispersal, seedling and juvenile regeneration of the large-seeded palm Attalea dubia (Mart.) Bur. (Arecaceae) in a large and well-conserved site of the Brazilian Atlantic Forest. Our aims were: 1) identify seed dispersers and seed predators; 2) evaluate the fate (e.g. dispersal or predation) of fallen fruits/seeds and the importance of dispersal for plant regeneration; and 3) describe the spatial pattern of seedling and juvenile regeneration and test if small mammal seed dispersal may account for it.
This study was carried out in Carlos Botelho State Park (CBSP), a 37,644 ha protected area covered by old growth humid Atlantic Forest in Southeast Brazil (24°06'55"S, 47°47'18"W). Mean annual temperatures vary between 17° and 22 °C. There is no dry season and mean annual rainfall is between 1700 and 2400 mm. CBSP is neighbour of other protected areas that together cover more than 1 million ha, the largest continuous remnant of Atlantic Forests (
To record the animals that interact with fallen fruits or seeds beneath the crown of A. dubia, an automatic camera-trap (Tigrinus S/A with passive motion and triggered by heat detection) was set under each of five fruiting palms over 24-hours a day for 15 consecutive days (total of 1,800 hours of camera-trap observations) from November 2010 to March 2011. Furthermore, we performed visual observations from October 2010 to March 2011 on other 10 fruiting plants located at least 100 m away from each other. One of us (AYYM) stayed hidden away from a focal plant between 8:00–10:00 a.m. and 4:00–6:00 p.m. during five days (20 h of observations per plant; total sampling effort of 200 h). We recorded animal species that visited the crown or the forest floor around the focal palm and interacted with fruits/seeds, as well as the number of fruits/seeds with which the animal interacted. The animal’s handling behaviour (e.g. removes fruit pulp but drops seed thereafter, preys on the seed or carries seed away) was also noted.
To investigate the fate of fallen seeds, we carried out removal experiments with marked seeds from October 2010 to January 2011. We selected 10 adult palms at least 100 m away from each other and at least 10 m away from any other conspecific fruiting palm. We used ripe, naturally fallen fruits in paired removal stations. We removed fruit pulp and made a small hole at the tip of each seed. A 50 cm nylon thread (0.45 mm width) was attached to the seed and a flagging tape was fixed at the other end to facilitate the tracking of seeds (
We compared the influence of the presence of fruit pulp in the frequency of different categories of fate with G-tests (
To evaluate the fate of non-dispersed seeds, we collected all seeds found within a 2 × 2 m quadrat established below the crown of 10 non-reproductively active adult palms by the end of November 2011. The seeds were carefully inspected and assigned to one out of four categories: intact, preyed on by rodents, preyed on by beetles or rotten. The fate of non-dispersed seeds was compared through an Analysis of Variance (ANOVA) using each palm as a block, random effect factor, considering seed fate categories as fixed treatments and the proportion of seeds in each category at a given palm as the response variable.
To evaluate the importance of seed dispersal for plant regeneration, we mapped all individuals of A. dubia found in 10 × 50 m quadrats (n = 10) within a 0.5 ha plot. Palms were assigned to a life-stage category following
,
where N = number of sample quadrats; Σx = sum of sample counts; Σx2 = sum of squares of sample counts. The distribution is assumed to be random if Id = 0, regular if Id < 1 or clumped if Id > 1 (
During visual observations, we obtained 50 records of animals that could potentially disperse the seeds of Attalea (see
During visual observations, 10 visits of groups of Sapajus nigritus (Goldfuss, 1809) were observed to fruiting Attalea. Each group interacted with a mean of 47 fruits/visit (total of 381 fruits for all visits). They removed the fruits directly from the bunch and ate the mesocarp, spitting and dropping the seeds beneath the palm crown afterwards and providing no dispersal. The squirrel Guerlinguetus brasiliensis (Gmelin, 1788) was recorded in six visits and had contact with one seed per visit. Ten other independent records (in different palms) of squirrels were also obtained from the camera-trap data. Squirrels obtained the fruits either from the plant crown or on the ground and moved to another tree. Then they removed the mesocarp, bit into the endocarp and fed on the endosperm. We did not see squirrels hoarding seeds during visual observations, but hoarding behaviour was documented for other Attalea species (
In total, 46 (15.3%) of fruits and seeds placed on experimental stations were dispersed at a median distance of 3.8 m (range 0.9–15.6 m). Amongst the dispersed fruits/seeds, 39 (85%) were found buried (scatter-hoarded) in soil or under litter, six (13%) above the litter and one (2%) cached amongst the leaves of an epiphytic bromeliad 1 m above ground. Other 47 fruits/seeds (15.6%) were manipulated by animals, including one cleaned seed buried under the seed station, but most of these records (92%) were based on the recovering of broken threads at variable distances from the seed station, without reliable evidence of seed fate. We were not able to find the other 28 fruits and 19 seeds (15.7%) used in the experiments. These fruits/seeds may have been removed further than 20 m from the seed stations and an unknown fraction may have been dispersed or recached. Intact fruits/seeds comprised of 157 records (52.3%) and only two fruits and one seed (total of 1.0%) were found preyed on.
There were differences in the frequency of interactions recorded for fruits and seeds in the removal experiments (G-test, G = 21.5, df = 3, P < 0.001; data from seeds preyed on excluded). The difference was due to a higher frequency of fruits (28.0%) compared to seeds (9.5%) in the category not found. When this category was removed in a subsequent analysis, there was no difference in the frequency of interactions with seeds or fruits (G = 4.72, df = 2, P = 0.095). In the experiment of cleaned seed removal, the distance from an adult palm had no effect on the fate of the seeds (Table
Fate of seeds (n = 200) and fruits (n = 100) of Attalea dubia in removal experiments in the floor of an Atlantic Forest in southeast Brazil. Groups of ten cleaned seeds (endocarps) were placed in a station beneath the crown (black bars) or away (grey bars) from fruiting palms (n = 10). Groups of ten fruits (endocarp plus mesocarp) were placed in a station under the crown of the same palms (white bars). Data are mean ± SE.
Results from a factorial analysis of variance on 999 permutations of raw data on seed (analysis 1) or seed/fruit (analysis 2) removal experiments. Distance from adult plant (near or far), categories of fate (dispersed, intact or not found) and fruit pulp (presence or not) were entered as fixed factors. See text and Figure
Effect | d.f. | MS | F | P-value |
---|---|---|---|---|
Analysis 1 | ||||
Distance from adult palm | 1 | 0.817 | 0.10 | 0.753 |
Category of fate | 2 | 104.62 | 12.42 | 0.001 |
Distance from adult palm x Category of fate | 2 | 17.60 | 2.09 | 0.143 |
Analysis 2 | ||||
Fruit pulp | 1 | 21.35 | 0.16 | 0.654 |
Category of fate | 2 | 52.85 | 6.16 | 0.004 |
Fruit pulp x Category of fate | 2 | 12.35 | 1.44 | 0.231 |
The fate of non-dispersed seeds beneath adult palms was highly variable and not significantly different amongst categories (ANOVA with palms as blocks; categories of seed fate: F = 2.531, df = 3, P = 0.078, Figure
Fate of undispersed seeds (endocarps; n = 253) found in a 2 × 2 m quadrat set below ten adult palms of Attalea dubia in an Atlantic Forest in southeast Brazil. Seeds were inspected and included in each of four categories of seed fate: intact, rotten, preyed on by rodents or by beetles. Boxes indicated median and quartile values followed by range.
We found 18 seedlings and 88 juveniles of A. dubia in the 0.5 ha plot at CBSP. Seedlings were closer to adult palms (median 8.9 m; range 1.5–20 m) than juveniles (median 14.3 m; range 1.7–26.8 m) (Mann-Whitney U-test, U = 439.5, P < 0.01) (Figure
Distances of Attalea dubia fruit/seed dispersal by rodents in an Atlantic Forest in southeast Brazil (n = 46 records of recovered fruits/seeds) (a). Number of seedlings (n = 18; black bars) and juveniles (n = 88; white bars) in relation to the distance to the nearest adult palm (b). The numbers above bars are juvenile/seedling ratios at a given distance class. For both graphs, distances are truncated to 20 m to enable visual comparisons (see text for details).
Small mammals provide legitimate dispersal for the large seeds of Attalea dubia and probably may allow some plant regeneration in the absence of large mammals in defaunated sites. However, the short distances of seed removal recorded are unlikely to reproduce the spatial distribution of seedlings and juveniles in relation to adult plants observed in the field. This suggests that small mammals, such as squirrels (Guerlinguetus brasiliensis), nocturnal Sigmodontinae rodents and marsupials (Philander frenatus), can sustain some plant regeneration at local scales, but cannot account alone for the spatial pattern of A. dubia regeneration observed in CBSP and that it would be necessary for the occasional seed dispersal at greater distances from the parental plant by larger mammals to keep the current palm spatial distribution.
Large mammals such as tapirs are known to remove great numbers of seeds, have a large home-range and long gut passage times allowing seeds to be dispersed further away (
The spatial distribution of seedlings and juveniles at the CBSP suggests that the likelihood of seedling regeneration and the transition from seedling to juvenile stage increases with distance from the parent plant. Regenerants of A. dubia showed an aggregated spatial distribution, while adults were randomly distributed suggesting density-dependent mortality in time that decrease the clumpiness at latter stages (
Removal of seeds away from parent plants by small mammals may increase seed and seedling survival in defaunated sites (see also
We could not assign the fate of 30% of the fruits/seeds in our removal experiments (sum of categories not found and only broken threads recovered). Those fruits/seeds might have been preyed on or removed further away from the 20 m distance radius where we searched for seeds or even been recached by rodents and moved to longer distances. The frequency of seed hoarding behaviour seems to be tied to resource availability, with periods of resource abundance favouring hoarding behaviour (
In conclusion, small mammals that often persist in fragmented landscapes (such as squirrels and other small rodents) may perform legitimate seed dispersal that may keep some plant regeneration in the absence of large mammals. Nevertheless, small mammals are unlikely to compensate entirely for the loss of seed dispersal services provided by large mammals (see also
We thank José L.C. Maia, the Carlos Botelho State Park staff and the Instituto Florestal de São Paulo for research facilities and permission. We thank A.P. Carmignotto for the identification of small mammals and P.H.S.A. Camargo for help in the statistical analysis. B. Beisiegel for loaning us the camera-traps. We thank M.M. Martins and M. Petrere Jr. for comments on earlier versions of the ms and two anonymous reviewers for comments that improved the ms. During the study, the first author received support from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior -–Brasil (CAPES) – Finance Code 001. AVC thanks the support from Conselho Nacional de Pesquisa (CNPq; proc. # 478938/2011-0).