MONKEYS, DUNG BEETLES AND SOIL SEED BANK STRUCTURING François FEER, Jean-François PONGE, Sandrine POUVELLE, Sylvie JOUARD UMR 5176 CNRS-MNHN, 4 Avenue du Petit Château, F91800 Brunoy, Email:
[email protected] Dung beetles (Scarabaeidae)
INTRODUCTION
120 species are present into undisturbed rain forest in French Guiana. Among them 76 species are attracted to primate dung.
Howler monkeys (Alouatta sp) are the dominant frugivorous primates living in neotropical forests. Their social groups used to defecate in a clump pattern creating an accumulation of dung under their sleeping sites. Dung is very attractive to dung beetles which bury it with the seeds it contains. Dung beetles are considered as important secondary dispersers of seeds (Andresen & Feer 2005) but their their specific effect on the soil seed bank is poorly known (Julliot 1992). We studied the local effect of faeces accumulation and the result of the dung beetle activity on the composition and the structure of the soil seed bank at the Nouragues field station (French Guiana)
Species list
Methods The structure of the seed bank was analysed on 3 defecation sites (D) and 3 controls (C) situated at a distance of 15 m. Three soil samples of 20 cm diameter were taken on each site 24 h after the defecation. They were analysed in three layers 2 cm thick for seed species richness and abundance. Full seeds potentially viable were distinguished from empty or damaged seeds. The seeds were partially identified with the help of a seed collection in Brunoy Axe 2
Red howler monkey (Alouatta seniculus)
D1 1
RESULTS
2 D3
The abundance of species in the samples were subjected to correspondance analysis (CA). Axes 1 and 2 of CA extracted 43 % and 11 % of the total variance, respectively. The projection of passive variable corresponding to sites D and C and the different depths revealed globally a strong opposition of the species composition between site D and C on the first axis. Nevertheless, at site level, only D1, with the largest number of seeds, clearly separated from other defecation sites which were close to the grouped Control sites with a low number of seeds. The second axis seemed to separate surface from deeper levels for sites D1 and D2.
C1 C2
1
1
C3 C2 C1
C3
3
Axe 1
3
D2
3
D3
2
D1
D2
2 Correspondance analysis. Projection of depth indicator (1: 0-2 cm; 2: 2-4 cm; 3: 4-6 cm) for each defecation site (D in red) and control (C in blue) in the plane of the two first factorial axes. Black letters and lines correspond to global data.
Nb of Seeds
Species Cecropia sciadophylla* Ficus guianensis* Ficus trigona Cecropia obtusa* Coussapoa latifolia* sp5 Psychotria anceps Ficus sp1 Ficus nymphaefolia* Bagassa guianensis* Ludovia lancifolia* Laetia procera Thoracocarpus bissectus sp8 Coussapoa sp. Evodianthus funifer sp6 Asplundia sp. Davilla kunthii sp7 Cecropia sp. Henriettea sp1 sp10 sp4 Cyclantacée indéterminée Henriettea maroniensis Jacaratia spinosa* Miconia sp1 Philodendron sp Piper sp Solanum sp1 Solanum sp2 Solanum sp3 sp2 sp9
Family Cecropiaceae Moraceae Moraceae Cecropiaceae Cecropiaceae
Size (mm) 2.26 x 1.12 0.81 x 0.64 1.14 x 0.83 2.54 x 0.98 1.54 x 1.03 2.15 x1.5 Rubiaceae 3.44 x 3.24 Moraceae 1.52 x 1 Moraceae 1.73 x 1.38 Moraceae 3.97 x 2.28 Cyclantaceae 1.41 x 1.11 Flacourtiaceae 3.42 x 2.17 Cyclantaceae 2.22 x 0.95 2 x 1.5 Cecropiaceae 2.26 x 1.27 Cyclantaceae 1.26 x 0.53 1.8 x 1.5 Cyclanthaceae 1.4 x 0.7 Dilleniaceae 3.29 x 2.7 5.2 x 3.4 Cecropiaceae 2.49 x 1.21 Melastomataceae 0.76 x 0.44 1.9 x 1 3.7 X 3.4 Cyclantaceae 1.9 x 0.82 Melastomataceae 1.32 x 0.76 Caricaceae 8.67 x 5.37 Melastomataceae Araceae 1.6 x 0.7 Piperaceae Solanaceae 3.46 X 2.96 Solanaceae 4.22 x 2.9 Solanaceae 3.6 x 3.2 4x? 3.9 x 1.9
Frequency 659 606 542 350 97 95 80 76 65 64 28 15 13 10 6 6 4 3 3 3 2 2 2 2 1 1 1 1 1 1 1 1 1 1 1
* eaten by howler monkey (Julliot 1994)
300,00 250,00
The variations of the mean number of seeds were subjected to ANOVA (split plot design). The effects of site, treatment (D, C) and depth were not significant.
200,00 150,00 100,00 50,00 0,00 D1
C1
D2
SITES
C2
D3
4-6 cm 2-4 cm 0-2 cm
DEPTH
C3
Mean total number of seeds per sites (defecation site D and control C) and per depth.
Nb of Species
Similar results were obtained with the mean number of viable seeds and the proportion of viable seeds on Source the total. F
P
Between plots Site Error
df 2 3
23606.46 29406.87
MS
0.80
0.526
Within plots Depth Error DepthxSite Error
2 6 4 6
811.06 375.02 327.02 375.02
2.16
0.196
0.87
0.532
The variations of the mean number of species according to site, treatment and depth were not significant. The species richness at the different sites were correlated with the log number of seeds (R2 = 0.83, P = 0.0001). The high number of species recorded at D1was due to a sample effect
14,00 12,00 10,00 8,00 6,00 4,00 2,00
Glass bead experiments Glass beads of 3 sizes (1.6 mm, N = 200; 2.1mm, N = 84 and 3.2 mm, N = 29) were incorporated into 80 g of fresh monkey dung and placed on 4 defecation sites which were used the same day. One week later, five soil samples 2 cm thick were analysed.
0,00 D1
C1
D2
SITES
4-6 cm 2-4 cm C2
0-2 cm
D3
DEPTH
C3
% 80,0
Mean total number of seed species per sites (defecation site D and control C) and per depth.
70,0 60,0 50,0 40,0 30,0 20,0 10,0 0,0
Discussion The density of the seedbank was small in all control sites but it was highly variable in defecation sites. Additional sites should be inventoried in order to evaluate the global quantitative effect of the howler monkeys. The site D1, that showed the highest number of seeds, was also the site the most frequently used by monkeys during the study period. That suggests that the spatio-temporal pattern of use of the sleeping sites may be one of the factors at the origin of the spatial heterogeneity of the density of the seed bank. On sites with high seed density, a large number of seeds were still present at 4-6 cm. Soil must be analysed up to larger depth to correctly assess the effect of dung burial and soil excavation by dung beetles. The experiments with beads showed variations of the burial rates beyond 2 cm depth on the different sites. They are likely related to the variations in abundance, body size and functional group (dweller, roller, tunneller) of the dung beetles. It is confirmed that howler monkeys may help to maintain spatial heterogeneity in the rain forest seed bank and, by locally stimulating dung beetle activity, enhance the turnover of the seed bank.
References Feer, F. (1999). Effects of dung beetles (Scarabaeidae) on seeds dispersed by howler monkeys (Alouatta seniculus) in the French Guiana rain forest. Journal of Tropical Ecology 15, 1-14. Andresen, E. & Feer, F. (2005). The role of dung beetles as secondary seed dispersers and their effect on plant regeneration in tropical rainforests. Pp. 331-349 in P.-M. Forget, J.E. Lambert, P.E. Hulme & S.B. Vander Wall (editors) Seed fate: predation, dispersal and seedling establishment. CABI publishing, Wallingford, UK. Julliot, C. (1992). Utilisation des ressources alimentaires par le singe hurleur roux, Alouatta seniculus en Guyane: impact de la dissémination des graines sur la régénération forestière. PhD, Université de Tours, Tours. Julliot C. (1994). Frugivory and seed dispersal by red howler monkeys: evolutionary aspect. Rev. Ecol. (Terre Vie), 49: 331-341. Julliot C. (1997). Impact of seed dispersal by red howler monkeys (Alouatta seniculus) on the seedling population in the understorey of tropical rain forest. Journal of Ecology, 85: 431-440.
D4 D3 0-2
2-4
D2 4-6
DEPTH (cm)
%
6-8
D1
On average 74.0 % (SD=8.7) of the beads were retrieved, the remainder being buried deeper than 8 cm or moved horizontally. The proportion of buried beads varied significantly according to sites and depths (Χ2= 174.25, P < 0.005). The majority of the beads were near the surface (68.9 %, SD=17.9) but they were always present at 8-10 cm. At site D3 a larger proportion of beads were buried at 2-4 cm and 8-10 cm.
SITE
8-10
Proportion of retrieved glass beads per sites and per depths.
The vertical distribution of the beads was not affected by their size (Χ2 = 9.37, NS)
80 70 60 50 40 30 20 10 0 0-2
2-4
LARGE MID 4-6
DEPTH (cm)
SMALL
6-8
SIZE
8-10 Proportion of retrieved glass beads per depths and per sizes.
