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Feeding habits of small mammals in agroecosystems of central Argentina
Mammalian Biology
Mamm. biol. 68 (2003) 91±101 ã Urban & Fischer Verlag http://www.urbanfischer.de/journals/mammbiol
Zeitschrift fuÈr SaÈugetierkunde
Original investigation
Feeding habits of small mammals in agroecosystems of central Argentina By FABIANA CASTELLARINI, CLAUDIA DELLAFIORE, and J. POLOP Departmento de Ciencias Naturales, Universidad Nacional de RõÂo Cuarto, RõÂo Cuarto, Argentina Receipt of Ms. 27. 12. 2001 Acceptance of Ms. 13. 06. 2002
Abstract Feeding habits of sympatric species of small mammals in agroecosystems of central Argentina were analysed using micro-histological analysis of stomach contents. All small mammal species were omnivores, but species changed their diets in relation to the habitat disturbance level. Calomys species showed more dietary overlap in greatly and moderately disturbed habitats than in less disturbed habitats. Calomys species and Akodon dolores behaved in opposite ways. The high degree of dietary overlap among Calomys species was explained by the chance disturbance hypothesis, and their low degree of dietary overlap by classical resource partitioning. The high dietary overlap between Calomys species and A. dolores was explained via the generalization-specialization hypothesis. Key words: Rodents, communities, diets, agroecosystems, disturbance
Introduction Small mammal species habitating central pampas of Argentinia show different associations closely related to land use. Calomys species, and especially Calomys laucha, are numerically dominant in crop fields; Calomys musculinus, Calomys venustus and Akodon dolores coexist in the borders and fence rows, and C. venustus and A. dolores are dominant in more stable habitats like natural grasslands (Kravetz and Polop 1983; Polop et al. 1985). Concerning disturbance, cropped fields have the highest disturbance level, and natural grassland represents the least disturbed habitat. The habitats with natural vegetation around the crops, known as borders or fence rows, plus roadsides and railway banks, are considered to be intermediate regarding dis1616-5047/03/68/03-091 $ 15.00/0.
turbance (Crespo et al. 1970; Kravetz and Polop 1983; Mills et al. 1991). Studies of the diet of small mammals of Argentinian pampas showed that all species are largely omnivorous, with seasonal variation in their diets (MartõÂnez et al. 1990; Bilenca et al. 1992; Dellafiore and Polop 1994, 1998; Ellis et al. 1998; Castellarini et al. 1998; Castellarini and Polop 2002). However, these studies are difficult to compare not only for differences in seasons and habitats sampled but also for differences in the category of food item identification. Some studies grouped food items into categories of seed, leaves and arthropods, and others according to genus and species, which led to a misleading interpretation about the
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use of food resource. On the hypothesis that small mammal species of the Argentinian pampas show spatial variations in their feeding habits, with diets that overlap more in more disturbed habitats than in less-disturbed habitats, the aims of this study were to: 1) analyse the food partitioning between coexisting species in habitats with different levels of disturbance and 2) integrate our results with other earlier studies.
Material and methods Study Area This study was carried out in farmlands of four localities of CoÂrdoba Province, in central Argentina: RõÂo Cuarto (33°7'17'' S, 64°21'41'' W), Villa Dolores (31°56'26'' S, 65°14'46''), Cruz del Eje (30°44' S, 64°48' W) and Villa de MarõÂa (29°54' S, 63°43' W). Trapping was conducted during autumn 1991 and 1992, in three landscape units: cropped fields, borders and natural grasslands. Small mammals were trapped by trap-lines 50 m long with two snap-traps per station 5 m apart, set for four consecutive nights in two repeated units per locality. Samples with at least two coexisting species with a minimal size of five individuals were considered. A total of 157 stomach contents was analysed: 61 C. venustus, 46 A. dolores, 41 C. musculinus and 9 C. laucha. The number of stomachs per habitat was 50 in cropped fields, 47 in borders and 60 in grasslands. Diet composition was determined by micro-histological analysis of stomach contents, which were prepared using the Strittmater's technique, modified by Scaglia et al. (1981). Food items were identified by comparison with reference histoepidermic samples prepared with plants collected in each habitat sampled. The seed reference slides were prepared using the Jeffrey technique, modified by Dellafiore and Polop (1994), and the leaf reference slides with the Strittmater's technique, modified by Scaglia et al. (1981). Arthropods were identified at the class taxon because the histological features in the fragments of stomach contents were too small for them to be assigned to a subordinate taxonomic group. Diet quantification was carried out: two slides per animal were analysed, observing 20 random microscopic fields per slide under 100 ´ magnification. Only the fields with recognizable fragments were considered. Frequencies were converted to relative densities using the algorithm of Facker and Brischle (1944).
Plant cover was estimated at each habitat according to the quadrat method (Braun-Blanquet 1979), taking samples over line-traps 10 m apart. Plant reference material was collected in all habitats and prepared using the diaphanization technique (Strittmater 1973). Seed patterns were framed using Jeffrey's technique (Johansen 1940).
Data analysis Dietary composition of small mammals from each landscape unit were compared taking into account food items with mean percentage more than 1%. Similarity between diets was analysed with a multidimensional scaling analysis (MDS) using the simplified Morisita's index in the similitude matrix (Horn 1966): CH = 2SXijXik/[(S Xij2/Nj2) + (S Xik2/Nk2)] NjNk where CH is the Morisita's index, Xij and Xik number of i species in j and k samples; SXij = Nj total of individuals in sample j and SXik = Nk total of individuals in sample k. The estimation of the goodness of fit of results and the number of dimensions to use was determined using Kruskal's stress values (Bisquerra Alzina 1989). The groups in the MDS's configuration were compared using a MANOVA test. Here, each dimension was considered as a new variable. In post hoc comparisons, the Tukey's test for unequalsized samples was used. The importance of each food item in the group ordination was analysed by their correlation to each dimension of MDS, using the Spearman's coefficients (Zar 1996). Dietary range for each species and habitat was determined using Levin's algorithm: B = 1/S(p2), where p is the relative frequency of occurrence of each dietary item (Levins 1968). Finally, to compare our results with earlier studies a triangular plot was performed using other authors' data (Tab. 1) and our own results. The data set consisted of the mean proportions of a broad range of food items, i. e. seeds, leaves and arthropods, consumed only during autumn and from habitats with equal disturbance levels.
Results A total of 54 food items was distinguished: 25 kinds of seed, 26 types of leaves and only one category of arthropods (Tab. 2). According to Kruskal's stress values, two dimensions were selected in the MDS to explain similarities in diets of small mammals from crop fields and borders, and three di-
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Table 1. Summary of mean results of small mammal diets in a pampa agroecosystems of Argentina. (Su = summer, Au = autumn and Wi = winter, OM = omnivorous, GR = granivorous, IN = insectivorous, FO = folivorous. Broad identification category are seeds, leaves and arthropods. Asterisk in identification category means that data format are not available to do comparisons). Species
Habitat
Season
Identification Category
Main Feeding habits
Source
Akodon azarae
Borders Borders
Su±Au All
Broad Species*
OM GR ± IN
BILENCA et al. 1992 ELLIS et al. 1998
Akodon dolores
Railway bank
Wi
Species
OM
MARTINEZ et al. 1990
Calomys laucha
Crops fields Crops fields Crops fields
Su±Au Su±Au All
Broad Species Species*
FO ± GR GR GR
BILENCA et al. 1992 DELLAFIORE and POLOP 1998 ELLIS et al. 1998
Calomys musculinus
Crops fields Border
Su±Au All
Species Species*
GR GR
DELLAFIORE and POLOP 1994 ELLIS et al. 1998
Calomys venustus
Railway bank
All
Species
FO ± GR
CASTELLARINI and POLOP 1998, 2002
mensions to explain similarities of diet in grasslands (Figs. 1, 2 and 3). Crop fields: Three significantly different groups of diets were recognized in the crop fields (Manova test: Wilk's l = 0.08, df1 = 8, df2 = 88, P < 0.000, and Tukey's test P = 0.02). The
first group included diets of A. dolores; the second one, diets of C. venustus; and the third diets overlapping C. venustus and C. musculinus. Diets of C. laucha were an intermediate group between diets of A. dolores and C. venustus in the crop field 1 (Fig. 1).
Fig. 1. Final 2D configuration in MDS analysis of rodents diets of crop fields in agroecosystems of CoÂrdoba, central Argentina. Calomys venustus (circles), C. musculinus (squares), C. laucha (asterisks) and A. dolores (triangles). Localities: RõÂo Cuarto (closed symbols) and Villa de MarõÂa (open symbols). Kruskal's stress = 0.14.
Clc1 (9)
Cvc2 (7)
Cmc2 (16)
Adc2 (8)
Cvb1a Cvb1b Cmb1b Cmb1a Adb1a Cvg2 (12) (6) (8) (11) (10) (6)
Cvg3 (12)
Cvg4 (8)
Cmg4 (6)
Adg2 (9)
Adg3 (10)
Adg4 (9)
83.46 1.72 T T ± ± ± ± ± ± ± ± ± ± T ± ± ± ± ± ± ± ± ± ±
58.73 T T ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
± ± 53.12 ± 4.17 ± ± ± ± ± 17.95 13.78 ± 5.11 T ± ± ± ± ± ± ± ± ± ±
±
± ± 11.60 ± ± ± ± ± ± 2.62 ± 6.61 ± 7.74 T ± ± ± ± ± ± ± ± ± ±
19.26 ± 30.93 ± ± ± ± ± ± 13.54 7.87 ± 3.81 ± ± 1.17 ± ± 5.23 ± ± ± ± ± ±
± ± T ± ± ± ± ± ± ±
± ± ± ± ± ± ± ± ± ± ± T ± 45.77 ± ± ± ± ± ± ± ± ± ± ±
± ± T T ± 1.02 24.75 ± T 19.97 5.78 T 7.09 23.49 ± ± ± ± ± ± ± ± ± ± ±
± ± ± ± ± ± ± 13.52 ± ± ± T ± ± ± ± 4.04 ± ± ± ± ± ± ± ±
± ± 5.45 ± ± ± ± ± ± ± 28.81 ± ± ± ± ± 7.18 ± ± ± ± 2.36 2.40 ± ±
± ± ± ± ± ± 13.42 1.16 ± T ± T ± 45.83 ± ± 14.14 ± ± ± ± ± ± ± ±
Seeds Eleusine indica Zea mays Chenopodium album Melilotus albus Oxalis crysantha Bidens subalternans Salsosla kali Solanum elegnifolium Sphaeralcea bonariensis Amaranthus sp. Sorghum sp. Lycium sp. Setaria sp. Malvaceae Gramineae 1 Gramineae Gramineae 3 S1 S2 S3 S4 S5 S6 S7 S8
1.62 73.38 ± ± T ± ± ± 7.02 T T ± 6.29 ± ± ± 1.56 ± ± ± ± ± ± ±
42.74 ± 24.52 ± ± ± ± ± ± 1.72 14.60 ± 1.45 ± ± 0.78 ± ± ± 4.05 ± ± ± ± ±
44.91 21.16 10.15 ± ± ± 5.33 ± ± 1.10 1.87 ± ± ± ± ± ± ± ± ± ± ± ± ± ±
49.17 ± 34.82 ± ± T ± ± ± 12.76 T ± ± ± ± ± ± ± ± ± 2.18 ± ± ± ±
8.51 ± 13.41 ± ± ± ± ± ± 1.36 T ± ± ± ± ± ± ± ± ± ± ± ± ± ±
± ± ± ± ± ± ± 57.86 ± ± ± ± ± T ± ± ± ± ± ± ± ± ± ± ±
3.82 ± ± ± 13.56 ± ± ± ± ± ± ± ± 25.07 2.52
FABIANA CASTELLARINI et al.
Cvc1 (10)
94
Table 2. Average percent of food items consumed by rodent species captured in different habitats of agroecosystems in CoÂrdoba, central Argentina. Percentages that where £ 1% are listed as trace (T). Cv: Calomys venustus; Cl: C laucha; Cm: C. musculinus; Ad: Akodon dolores. Letters and numbers accompaning species' names are habitats and localities. Habitats: (c) cropped fields; (b) borders; (g) grasslands. Localities: (1) RõÂo Cuarto; (2) Villa de MarõÂa; (3) Cruz del Eje; (4) Villa Dolores. S: unidentified species. Sample size in brackets.
Table 2. Continued Cvc1 (10)
Clc1 (9)
Cvc2 (7)
Cmc2 (16)
Adc2 (8)
Cvb1a Cvb1b Cmb1b Cmb1a Adb1a Cvg2 (12) (6) (8) (11) (10) (6)
Clematis montevidensis Oxalis crisanta Morrenia brachystephana Descurainia argentina Parietaria debilis Salpichroa origanifolia Passiflora coerulea Lycium australe Celtis iguanae Patenium histerophorus Veronica didyama Sorghum sp. Glandularia sp. Malvaceae 1 Gramineae 1 Gramineae 2 Gramineae 3 Gramineae 4 Gramineae 5 Gramineae 6 Gramineae 7 Gramineae 8 S1 S2 S3 S4 S5 S6
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 5.35 ± ± ± ± ±
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
2.89 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 2.05 ± ± ± ±
T ± ± ± ± ± ± ± ± ± ± ± ± ± T ± ± ± ± ± ± ± ± ± ± ± ± ±
2.85 1.59 ± ± ± ± ± ± ± ± ± ± ± ± 2.65 ± ± ± ± ± ± ± ± ± ± ± ± ±
9.39 ± 1.33 T ± ± ± ± ± ± ± ± ± ± ± 4.14 ± ± ± ± ± ± ± ± ± ± ± ±
± ± ± 1.14 ± ± ± ± ± ± ± ± ± ± ± 1.46 3.60 ± ± ± ± ± ± ± ± ± ± ±
± T ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 1.86 ± ± ± ± ± ± ± ± ± ± ± ± ± 1.77 ± ± ± ± ± ± ±
Arthropods
7.96
40.85 T
8.11
63.83 2.17
3.95
11.62 T
Cvg3 (12)
Cvg4 (8)
Cmg4 (6)
Adg2 (9)
Adg3 (10)
Adg4 (9)
1.09 30.22 29.69 2.38 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 13.46 ± ± ± ± ± ± ± ± 2.33 ± ± ± ± ± ± ± 3.78 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 4.69 ± ± 3.75 ± ± ± ± ± ± ± 6.81 ± ± ± ± ± ± 1.30 ± ± ± ± ± ± 7.76 ± ± ± ±
± ± ± 4.93 ± ± ± 20.77 ± ± 4.36 ± 0.88 7.79 ± ± ± ± ± ± ± ± ± ± ± 14.06 ± ±
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
16.15 ± ± 1.65 ± ± 1.28 ± ± ± ± 2.15 ± ± ± ± ± ± ± ± 1.41 ± ± ± ± ± ± ±
± ± ± ± ± ± ± 1.58 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± T ± ±
63.28 T
T
13.55 38.15 31.17 23.32
Leaves
Feeding habits of small mammals
T
39.43 ± ± ± T 1.47 ± ± 2.53 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 1.97 ±
95
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Table 3. Significant correlations between food items consumed by rodent species of agroecosystems in CoÂrdoba (central Argentina) and dimensions of MDS analysis, using Spearman's coefficient (R). Seeds (s). Leaves (l). Food item species
Crop fields
Borders
Grasslands
R
P
R
P
R
P
0.83 ±0.75 0.41 0.46 ±0.53 ±0.43 ± ± ± ± ± ± ± ± ±
0.000 0.000 0.003 0.001 0.000 0.002 ± ± ± ± ± ± ± ± ±
0.87 ± ±0.61 ± ± ± ±0.33 ±0.40 ±0.34 ± ± ± ± ± ±
0.0000 ± 0.0000 ± ± ± 0.0233 0.0058 0.0203 ± ± ± ± ± ±
± ± ± ± ±0.76 ±0.30 ± ± ± 0.92 0.31 ±0.26 ±0.35 ±0.31 0.26
± ± ± ± 0.0000 0.0195 ± ± ± 0.0000 0.0156 0.0417 0.0054 0.0158 0.0456
±0.41 ±0.43 0.57 0.45 0.31 0.43 ± ± ±
0.004 0.002 0.000 0.001 0.028 0.002 ± ± ±
±0.72 ± 0.52 ± ± ± 0.31 ± ±
0.0000 ± 0.0002 ± ± ± 0.0342 ± ±
± ± 0.78 ± ± ± ± ±0.40 0.48
± ± 0.0000 ± ± ± ± 0.0017 0.0001
± ± ± ± ± ± ±
± ± ± ± ± ± ±
± ± ± ± ± ± ±
± ± ± ± ± ± ±
0.50 ±0.30 0.30 0.27 0.26 0.31 ±0.55
0.0000 0.0200 0.0185 0.0401 0.0485 0.0176 0.0000
Dimension 1 E. indica (s) C. album (s) Arthropods Species 1 (l) Malvaceae (s) Amaranthus sp. (s) O. crysantha (l) Gramineae 6 (s) Gramineae 7 (s) C. montevidensis (l) Sorghum sp. (s) Seteria sp. (s) S. kali (s) L. australe (l) S. eleagnifolium (s) Dimension 2 E. indica (s) C. album (s) Arthropods C. montevidensis (l) Malvaceae (s) Lycium sp. (s) Amaranthus sp. (s) M. albus (s) Gramineae 4 (s) Dimension 3 Sorghum sp. (s) Malvaceae (s) Amaranthus sp. (s) B. subalternans (s) Setaria sp. (s) S. kali (s) S. eleagnifolium (s)
Table 3 shows the food items significantly correlated with each dimension variable. The diet of A. dolores was correlated with the consumption of arthropods and that of C. venustus with consumption of Eleusine indica seed. For both these groups diets of C. laucha were mainly correlated with consumption of arthropods and seed of E. indica. Finally, C. venustus and C. musculinus consumed high proportions of seeds of Chenopodium album. Other food items were correlated with this configuration, but their
relative composition in the small mammal diets was low (Tab. 2). Borders: A close similarity between the diets of C. venustus, C. musculinus and A. dolores was observed in the borders (Fig. 2). The similarity between diets of C. venustus and C. musculinus was due to consumption of seeds of E. indica, C. album and Amaranthus sp., and that between the diets of C. venustus and A. dolores to seeds of C. album (Tab. 2 and 3). The only significant difference between the diets of C. mus-
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Fig. 2. Final 2D configuration in MDS analysis of rodents diets of borders in agroecosystems of CoÂrdoba, central Argentina. Calomys venustus (circles), C. musculinus (squares), C. laucha (asterisks) and A. dolores (triangles). Borders: A (open symbols) and B (closed symbols). Kruskal's stress = 0.18.
culinus and A. dolores was found on dimension 1 (MANOVA test: Wilk's l = 0.63, df1 = 8, df2 = 82, P = 0.01, Tukey's test P = 0.004). The difference was correlated with a high consumption of arthropods by A. dolores and seeds by C. musculinus (Tab. 3). Grasslands: Several groups of diets were recognized in the natural grassland (MANOVA test: Wilk's l = 0.02, df1 = 18, df2 = 144, P = 0.000, Fig. 3). Two groups were identified on dimension 1 showing significant differences between diets of small mammals from the grassland of Villa Dolores and those of Cruz del Eje and Villa de Maria. Seed consumption of a Malvaceous species was correlated with the samples from Villa de Maria and leaves of Clematis montevidensis with samples from the other localities (Tab. 2 and 3). Dimension 2 showed significant differences between the diets of A. dolores and the other two coexisting species, C. venustus and C. musculinus, from Villa Dolores (Tukey's test P < 0.04). These differences were due to the higher relative consumption of arthropods by A. dolores (Tab. 2 and Tab. 3).
Finally, dimension 3 showed significant differences between the diets of the C. musculinus ± C. venustus pair (Tukey's test P = 0.0004) and the C. musculinus ± A. dolores pair (Tukey's test P = 0.01) from the grassland of Villa Dolores. The differences were correlated with seed species consumption (Tab. 2 and 3). Only in this habitat, differences between the diets of C. venustus and C. musculinus were found. Habitat diversity, dietary range and overlap: the mean diversity of plants was highest in the borders and the lowest in the cropped fields (Tab. 4). Considering all the food items, dietary ranges in Calomys species were similar in the cropped fields. C. venustus and C. musculinus had a higher dietary range at the borders than in the cropped fields and grasslands. Dietary range in A. dolores was higher in grasslands than in the cropped fields and borders. Considerable overlap between Calomys diets was observed in cropped fields and borders as compared with the grasslands. The opposite pattern was observed for A. dolores, for which there was more overlap in grasslands than in cropped fields and borders (Tab. 5).
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Fig. 3. Final configuration in MDS analysis of rodents diets of grasslands in agroecosystems of CoÂrdoba, central Argentina. Calomys venustus (circles and crosses), C. musculinus (squares), and A. dolores (triangles and asterisks). Localities: Cruz del Eje (closed symbols), Villa Dolores (open symbols) and Villa de MarõÂa (crosses and asterisk). Kruskal's stress = 0.16. Table 4. Dietary breadth (LEVINS 1968) calculated with major dietary components and Shannon's index per habitat. *Average values. Habitat
C. laucha
C. musculinus
C. venustus
A. dolores
Habitat Diversity
Crop field
1.95*
1.80
2.19*
2.31
0.31*
Border
±
3.14*
3.93*
2.32
0.79*
Grassland
±
2.31
3.66*
3.67
0.57*
Table 5. Dietary overlap for each coexisting rodent species with food items above 1% relative percentage, using the simplified Morisita's index (HORN 1966). * Average values Species pair
Crop field
Border
Grasslands
C. venustus ± C. laucha C. venustus ± C. musculinus C. venustus ± A. dolores C. musculinus ± A. dolores
0.86 0.88 0.21 0.29
± 0.80 0.25 0.22
± 0.47 0.52* 0.71
The feeding relationships for the more abundant small mammal species in the agroecosystems of central Argentina suggest that Calomys species showed feeding habitats within the seed-leaves gradient, C. musculinus being largely granivorous, C. venustus granivorous or folivorous-grani-
vorous, and C. laucha the most omnivorous. Akodon species showed feeding habits within the arthropods-omnivory gradient. At the level of omnivory feeding habits, A. dolores presented similar feeding habits as C. laucha (Fig. 4).
Feeding habits of small mammals
Fig. 4. Feeding relationships between small mammal species in the agroecosystems of central Argentina taking into account the average relative composition of leaves, seed and arthropods. Data sources from: BILENCA et al. (1992); DELLAFIORE and POLOP (1994, 1998); ELLIS et al. (1998) and present study. Aa: Akodon azarae, Ad: A. dolores, Cl: Calomys laucha, Cm: C. musculinus and Cv: C. venustus. Numbers accompanying species' names are habitats: cropped fields (1), borders (2) and grasslands (3).
Discussion Our results support the view that the small mammals of the Argentinian pampas are omnivorous (Martinez et. al 1990; Bilenca et al. 1992; Dellafiore and Polop 1994, 1998; Castellarini et al. 1998; Ellis et al. 1998; Castellarini and Polop 2002). However, we found variation in the relative composition of their diets and propose a relationship between coexisting species, feeding habits and habitat disturbance level. A. dolores was mainly carnivorous in the cropped fields and borders, becoming omnivorous in grasslands, while A. azarae was omnivorous in borders. Nevertheless, this dietary separation could not be important because these pairs of species were not found together and in general A. dolores is dominant in less disturbed habitats, like grasslands, and A. azarae in habitats with intermediate disturbance such as borders (Kravetz and Polop 1983; Bilenca et al. 1992). Considering Calomys species, C. venustus and C. laucha had a high dietary overlap, but only with regard to seed spe-
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cies, because taking into account leaves and arthropods C. laucha was the most omnivorous of the three Calomys species. The differences between our results and those of other authors (Bilenca et al. 1992; Dellafiore and Polop 1998; Ellis et al. 1998), who typified C. laucha as granivorous (seed-eating) -folivorous (leaf-eating) or granivorous, the small size of the species and their presence almost exclusively in cropped fields, suggest that C. laucha could use different food resources in only one habitat as an adaptive response to its competitive exclusion from other habitats by the other larger species (Busch and Kravetz 1992). Thus, C. laucha would be a ªresource generalistº and ªhabitat specialistº (both obligate) living chiefly in the more disturbed habitat, the cropped field, and eating the food available or not consumed by other sympatric species. On the other hand, the high dietary overlap observed between Calomys venustus and C. musculinus in the cropped fields applied to both kinds of food items-individual seed and leaf species and the broad category (arthropods, leaves and seeds) and the low food availability, suggest that food partitioning cannot be important to this pair of species because the periodic disturbance could lead to slow population growth or high dispersal rates, allowing species to coexist (Rosenzweig and Abramsky, 1993). Finally, the contrasting results for A. dolores and Calomys species, i. e. the small overlap in crop fields and large overlap in grassland and the high dietary range in grasslands, could be explained by the generalization-specialization of Robinson and Wilson (1998), which predicts that the diets of coexisting consumer species should broadly overlap, being generalists in resources easily captured, and specialists in the ones that require specialized hunting techniques. While all species share a high proportion of food items, and are thus generalists, A. dolores remains a specialist in arthropods, C. venustus in leaf and seed species, and C. musculinus in seeds, the later being the ªresource specialistº and the ªhabitat generalistº. In summary, we suggest that dietary overlap should be analysed in
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both specific and broad categories, and that the feeding habits of the small mammals of the Argentinian pampas agroecosystems in the more disturbed habitats are highly dependent on disturbance and the capability of the species to be opportunist; while in the less disturbed habitats the feeding habits are more dependent on the specialization of each coexisting species.
Acknowledgements We thank Marcos Torres for assistance in fieldwork and Jutta Wester for her help with the German translation of the abstract. This study was supported by grants from Consejo de Investigaciones Cientificas y Tecnologicas de la Provincia de CoÂrdoba (CONICOR).
Zusammenfassung ErnaÈhrungsgewohnheiten von KleinsaÈugern in AgraroÈkosystemen von Zentralargentinien Die widerspruÈchlichen Resultate, zu denen Studien der ErnaÈhrungsgewohnheiten kleiner SaÈugetiere in zentralargentinischen Úkosystemen gefuÈhrt haben, koÈnnen oft auf unterschiedliche Nahrungsidentifikation, auf die Probennahme der LebensraÈume und auf koexistierende Arten zuruÈckgefuÈhrt werden. In der vorliegenden Untersuchung haben wir analysiert, wie anthropogene StoÈrungen die ErnaÈhrung in kleinen Gemeinschaften von SaÈugetieren der Úkosysteme beeinflussen und zu unterschiedlichen Nahrungsrationierungen fuÈhren koÈnnen. Die Proben wurden drei verschiedenen Landschaftstypen in vier Regionen Zentralargentiniens aufgenommen. Die ErnaÈhrung wurde mittels mikrohistologischer Analysen der Mageninhalte bestimmt, und die Daten wurden durch Indices und multivariate Vergleiche analysiert. GemaÈû unseren Ergebnissen sind die untersuchten kleinen SaÈugetiere Allesfresser, die ihre ErnaÈhrung jedoch entsprechend der IntensitaÈt von anthropogenen StoÈrungen einstellen. Die Calomys Arten zeigten eine hoÈhere NahrungsuÈberlappung in LebensraÈumen mit erheblichen und mittleren menschlichen Beeinflussungen als in LebensraÈumen mit geringer StoÈrung. Bei den Arten von Calomys und Akodon dolores wurde ein umgekehrtes Muster gefunden. Die starke Ûberlappung bei Calomys in LebensraÈumen mit hoher und mittlerer Stellung wurde mit Hilfe der Hypothese der StoÈrung als Chance erklaÈrt. Die starke Ûberlappung bei Calomys und Akodon dolores in LebensraÈumen mit geringer StoÈrung wurde erklaÈrt durch die Hypothese der Generalisierung-Spezialisierung, die geringe Ûberlappung bei allen Arten mittels der klassischen Nahrungsverteilung.
References Bilenca, D.; Kravetz, F.; Zuleta, G. (1992): Food habits of Akodon azarae and Calomys laucha (Cricetidae, Rodentia) in agroecosystems of central Argentina. Mammalia 56, 371±383. Bisquerra Alzina, R. (1989): IntroduccioÂn conceptual al anaÂlisis multivariado. Un enfoque informaÂtico con los paquetes SPSS-X, BMDP, LISREL y SPAD. Vol. I Promociones Universitarias, S. A. Barcelona. Busch, M.; Kravetz, F. (1992): Competititve interactions among rodents (Akodon azarae, Calomys laucha and Oligoryzomys flavescens) in a two habitats system. I. Spatial and numerical relationships. Mammalia 56, 45±56. Braun-Blanquet, J. (1979): FitosociologõÂa. Bases para el estudio de las comunidades vegetales. Madrid: H. Blume ediciones.
Castellarini, F.; Polop, J. (2002) Effects of extra food on population fluctuation pattern of the muroid rodent Calomys venustus. Austral. Ecology 27. (in press). Castellarini, F.; Agnelli, H.; Polop, J. (1998): Study on the diet and feeding preferences of Calomys venustus (Rodentia, Muridae). MastozoologõÂa Neotropical 5, 5±11. Crespo, J.; Sabattini, M.; Piantanida, J.; De VillafanÄe, G. (1970): Estudios ecoloÂgicos sobre roedores silvestres. Observaciones sobre densidad, reproduccioÂn y estructura de comunidades silvestres de roedores del sur de CoÂrdoba. MonografõÂa de la SecretarõÂa de Estado de Salud PuÂblica. Ministerio de Bienestar Social. Buenos Aires. RepuÂblica Argentina, 1±45.
Feeding habits of small mammals Dellafiore, C.; Polop, J. (1994): Feeding habits of Calomys musculinus in the crop fields and its borders. MastozoologõÂa Neotropical 1, 45±50. Dellafiore, C.; Polop, J. (1998): Dieta de Calomys laucha (Rodentia, Muridae) en habitats de cultivos de la provincia de CoÂrdoba. Facena 14, 25±30. Ellis, B.; Mills, J.; Glass, G.; Mckee, JR. K.; Enria, D.; Childs, J. (1998): Dietary habits of the common rodents in an agroecosystem in Argentina. J. Mammalogy 79, 1203±1220. Fracker, S.; Brischle, S.; (1944): Measuring the local distribution on ribes. Ecology 25, 283± 303. Horn, H. (1966): Measurement of ªoverlapº in comparative ecological studies. Am. Nat. 100, 419±424. Johansen, D. (1940): Plant Microtechniques. London: Mc Graw ± Hill Book Co. Kravetz, F.; Polop, J. (1983): Comunidades de roedores en agoecosistemas del Departamento de RõÂo Cuarto, CoÂrdoba. Ecosur 10, 1±18. Krebs, C. J. (1989): Ecological Methodology. New York: Harper Collins Publ. Levins, R. (1968): Evolution in Changing Environments. Princenton, New Jersey: Princenton University Press. MartõÂnez, R.; Bocco, M.; MoÂnaco, L.; Polop, J. (1990): Winter diet in Akodon dolores (Thomas, 1916). Mammalia 54, 197±205. Mills, J.; Ellis, B.; McKee, K.; Maiztegui, J.; Childs, J. (1991) Habitat assocciations and relative densities of rodent populations in cultivated areas of central Argentina. J. Mammalogy 72, 470±479.
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Polop, J.; MartõÂnez, R.; Torres, M. (1985): DistribucioÂn y abundancia de poblaciones de pequenÄos roedores en la zona del embalse de rõÂo tercero, CoÂrdoba. Historia Natural 5, 33± 44. Robinson, B.; Wilson, D. (1998): Optimal foraging, specialization, and a solution to Liem's paradox. Am. Nat. 151, 223±235. Rosenzweig, M. L.; Abramsky, Z. (1993): How are diversity and productivity related? In: Species Diversity in Ecological Communities. Historical and Geographical Perspectives, Ed. by E. Ricklefs and D. Schluter. Chicago: Univ. Chicago Press. Pp. 52±65. Scaglia, O.; VelaÂzquez, C.; CahuepeÂ, M. (1981): TeÂcnica de microanaÂlisis para estudios de dieta de herbõÂvoros. ProduccioÂn Animal 7, 572± 576. Strittmater, C. (1973): Nueva teÂcnica de diafanizacioÂn. Bol. Soc. Argentina Bot. 15, 126±129. Zar, J. (1996): Biostatistical Analysis. New Jersey: Prentice Hall.
Authors' addresses: Fabiana Castellarini, DeÂpartement Dynamique des systeÁmes eÂcologiques, Centre d'Ecologie Fonctionnelle et Evolutive ± CNRS 1919, route de Mende, 34293 Montpellier cedex 5 France (e-mail: [email protected]); Claudia Dellafiore and Jaime Polop, Departamento de CC Naturales, Universidad Nacional de Rio Cuarto, Ag; Postal No 9, 5800 Rio Cuarto, Argentina.
Mamm. biol. 68 (2003) 91±101 ã Urban & Fischer Verlag http://www.urbanfischer.de/journals/mammbiol
Zeitschrift fuÈr SaÈugetierkunde
Original investigation
Feeding habits of small mammals in agroecosystems of central Argentina By FABIANA CASTELLARINI, CLAUDIA DELLAFIORE, and J. POLOP Departmento de Ciencias Naturales, Universidad Nacional de RõÂo Cuarto, RõÂo Cuarto, Argentina Receipt of Ms. 27. 12. 2001 Acceptance of Ms. 13. 06. 2002
Abstract Feeding habits of sympatric species of small mammals in agroecosystems of central Argentina were analysed using micro-histological analysis of stomach contents. All small mammal species were omnivores, but species changed their diets in relation to the habitat disturbance level. Calomys species showed more dietary overlap in greatly and moderately disturbed habitats than in less disturbed habitats. Calomys species and Akodon dolores behaved in opposite ways. The high degree of dietary overlap among Calomys species was explained by the chance disturbance hypothesis, and their low degree of dietary overlap by classical resource partitioning. The high dietary overlap between Calomys species and A. dolores was explained via the generalization-specialization hypothesis. Key words: Rodents, communities, diets, agroecosystems, disturbance
Introduction Small mammal species habitating central pampas of Argentinia show different associations closely related to land use. Calomys species, and especially Calomys laucha, are numerically dominant in crop fields; Calomys musculinus, Calomys venustus and Akodon dolores coexist in the borders and fence rows, and C. venustus and A. dolores are dominant in more stable habitats like natural grasslands (Kravetz and Polop 1983; Polop et al. 1985). Concerning disturbance, cropped fields have the highest disturbance level, and natural grassland represents the least disturbed habitat. The habitats with natural vegetation around the crops, known as borders or fence rows, plus roadsides and railway banks, are considered to be intermediate regarding dis1616-5047/03/68/03-091 $ 15.00/0.
turbance (Crespo et al. 1970; Kravetz and Polop 1983; Mills et al. 1991). Studies of the diet of small mammals of Argentinian pampas showed that all species are largely omnivorous, with seasonal variation in their diets (MartõÂnez et al. 1990; Bilenca et al. 1992; Dellafiore and Polop 1994, 1998; Ellis et al. 1998; Castellarini et al. 1998; Castellarini and Polop 2002). However, these studies are difficult to compare not only for differences in seasons and habitats sampled but also for differences in the category of food item identification. Some studies grouped food items into categories of seed, leaves and arthropods, and others according to genus and species, which led to a misleading interpretation about the
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use of food resource. On the hypothesis that small mammal species of the Argentinian pampas show spatial variations in their feeding habits, with diets that overlap more in more disturbed habitats than in less-disturbed habitats, the aims of this study were to: 1) analyse the food partitioning between coexisting species in habitats with different levels of disturbance and 2) integrate our results with other earlier studies.
Material and methods Study Area This study was carried out in farmlands of four localities of CoÂrdoba Province, in central Argentina: RõÂo Cuarto (33°7'17'' S, 64°21'41'' W), Villa Dolores (31°56'26'' S, 65°14'46''), Cruz del Eje (30°44' S, 64°48' W) and Villa de MarõÂa (29°54' S, 63°43' W). Trapping was conducted during autumn 1991 and 1992, in three landscape units: cropped fields, borders and natural grasslands. Small mammals were trapped by trap-lines 50 m long with two snap-traps per station 5 m apart, set for four consecutive nights in two repeated units per locality. Samples with at least two coexisting species with a minimal size of five individuals were considered. A total of 157 stomach contents was analysed: 61 C. venustus, 46 A. dolores, 41 C. musculinus and 9 C. laucha. The number of stomachs per habitat was 50 in cropped fields, 47 in borders and 60 in grasslands. Diet composition was determined by micro-histological analysis of stomach contents, which were prepared using the Strittmater's technique, modified by Scaglia et al. (1981). Food items were identified by comparison with reference histoepidermic samples prepared with plants collected in each habitat sampled. The seed reference slides were prepared using the Jeffrey technique, modified by Dellafiore and Polop (1994), and the leaf reference slides with the Strittmater's technique, modified by Scaglia et al. (1981). Arthropods were identified at the class taxon because the histological features in the fragments of stomach contents were too small for them to be assigned to a subordinate taxonomic group. Diet quantification was carried out: two slides per animal were analysed, observing 20 random microscopic fields per slide under 100 ´ magnification. Only the fields with recognizable fragments were considered. Frequencies were converted to relative densities using the algorithm of Facker and Brischle (1944).
Plant cover was estimated at each habitat according to the quadrat method (Braun-Blanquet 1979), taking samples over line-traps 10 m apart. Plant reference material was collected in all habitats and prepared using the diaphanization technique (Strittmater 1973). Seed patterns were framed using Jeffrey's technique (Johansen 1940).
Data analysis Dietary composition of small mammals from each landscape unit were compared taking into account food items with mean percentage more than 1%. Similarity between diets was analysed with a multidimensional scaling analysis (MDS) using the simplified Morisita's index in the similitude matrix (Horn 1966): CH = 2SXijXik/[(S Xij2/Nj2) + (S Xik2/Nk2)] NjNk where CH is the Morisita's index, Xij and Xik number of i species in j and k samples; SXij = Nj total of individuals in sample j and SXik = Nk total of individuals in sample k. The estimation of the goodness of fit of results and the number of dimensions to use was determined using Kruskal's stress values (Bisquerra Alzina 1989). The groups in the MDS's configuration were compared using a MANOVA test. Here, each dimension was considered as a new variable. In post hoc comparisons, the Tukey's test for unequalsized samples was used. The importance of each food item in the group ordination was analysed by their correlation to each dimension of MDS, using the Spearman's coefficients (Zar 1996). Dietary range for each species and habitat was determined using Levin's algorithm: B = 1/S(p2), where p is the relative frequency of occurrence of each dietary item (Levins 1968). Finally, to compare our results with earlier studies a triangular plot was performed using other authors' data (Tab. 1) and our own results. The data set consisted of the mean proportions of a broad range of food items, i. e. seeds, leaves and arthropods, consumed only during autumn and from habitats with equal disturbance levels.
Results A total of 54 food items was distinguished: 25 kinds of seed, 26 types of leaves and only one category of arthropods (Tab. 2). According to Kruskal's stress values, two dimensions were selected in the MDS to explain similarities in diets of small mammals from crop fields and borders, and three di-
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Table 1. Summary of mean results of small mammal diets in a pampa agroecosystems of Argentina. (Su = summer, Au = autumn and Wi = winter, OM = omnivorous, GR = granivorous, IN = insectivorous, FO = folivorous. Broad identification category are seeds, leaves and arthropods. Asterisk in identification category means that data format are not available to do comparisons). Species
Habitat
Season
Identification Category
Main Feeding habits
Source
Akodon azarae
Borders Borders
Su±Au All
Broad Species*
OM GR ± IN
BILENCA et al. 1992 ELLIS et al. 1998
Akodon dolores
Railway bank
Wi
Species
OM
MARTINEZ et al. 1990
Calomys laucha
Crops fields Crops fields Crops fields
Su±Au Su±Au All
Broad Species Species*
FO ± GR GR GR
BILENCA et al. 1992 DELLAFIORE and POLOP 1998 ELLIS et al. 1998
Calomys musculinus
Crops fields Border
Su±Au All
Species Species*
GR GR
DELLAFIORE and POLOP 1994 ELLIS et al. 1998
Calomys venustus
Railway bank
All
Species
FO ± GR
CASTELLARINI and POLOP 1998, 2002
mensions to explain similarities of diet in grasslands (Figs. 1, 2 and 3). Crop fields: Three significantly different groups of diets were recognized in the crop fields (Manova test: Wilk's l = 0.08, df1 = 8, df2 = 88, P < 0.000, and Tukey's test P = 0.02). The
first group included diets of A. dolores; the second one, diets of C. venustus; and the third diets overlapping C. venustus and C. musculinus. Diets of C. laucha were an intermediate group between diets of A. dolores and C. venustus in the crop field 1 (Fig. 1).
Fig. 1. Final 2D configuration in MDS analysis of rodents diets of crop fields in agroecosystems of CoÂrdoba, central Argentina. Calomys venustus (circles), C. musculinus (squares), C. laucha (asterisks) and A. dolores (triangles). Localities: RõÂo Cuarto (closed symbols) and Villa de MarõÂa (open symbols). Kruskal's stress = 0.14.
Clc1 (9)
Cvc2 (7)
Cmc2 (16)
Adc2 (8)
Cvb1a Cvb1b Cmb1b Cmb1a Adb1a Cvg2 (12) (6) (8) (11) (10) (6)
Cvg3 (12)
Cvg4 (8)
Cmg4 (6)
Adg2 (9)
Adg3 (10)
Adg4 (9)
83.46 1.72 T T ± ± ± ± ± ± ± ± ± ± T ± ± ± ± ± ± ± ± ± ±
58.73 T T ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
± ± 53.12 ± 4.17 ± ± ± ± ± 17.95 13.78 ± 5.11 T ± ± ± ± ± ± ± ± ± ±
±
± ± 11.60 ± ± ± ± ± ± 2.62 ± 6.61 ± 7.74 T ± ± ± ± ± ± ± ± ± ±
19.26 ± 30.93 ± ± ± ± ± ± 13.54 7.87 ± 3.81 ± ± 1.17 ± ± 5.23 ± ± ± ± ± ±
± ± T ± ± ± ± ± ± ±
± ± ± ± ± ± ± ± ± ± ± T ± 45.77 ± ± ± ± ± ± ± ± ± ± ±
± ± T T ± 1.02 24.75 ± T 19.97 5.78 T 7.09 23.49 ± ± ± ± ± ± ± ± ± ± ±
± ± ± ± ± ± ± 13.52 ± ± ± T ± ± ± ± 4.04 ± ± ± ± ± ± ± ±
± ± 5.45 ± ± ± ± ± ± ± 28.81 ± ± ± ± ± 7.18 ± ± ± ± 2.36 2.40 ± ±
± ± ± ± ± ± 13.42 1.16 ± T ± T ± 45.83 ± ± 14.14 ± ± ± ± ± ± ± ±
Seeds Eleusine indica Zea mays Chenopodium album Melilotus albus Oxalis crysantha Bidens subalternans Salsosla kali Solanum elegnifolium Sphaeralcea bonariensis Amaranthus sp. Sorghum sp. Lycium sp. Setaria sp. Malvaceae Gramineae 1 Gramineae Gramineae 3 S1 S2 S3 S4 S5 S6 S7 S8
1.62 73.38 ± ± T ± ± ± 7.02 T T ± 6.29 ± ± ± 1.56 ± ± ± ± ± ± ±
42.74 ± 24.52 ± ± ± ± ± ± 1.72 14.60 ± 1.45 ± ± 0.78 ± ± ± 4.05 ± ± ± ± ±
44.91 21.16 10.15 ± ± ± 5.33 ± ± 1.10 1.87 ± ± ± ± ± ± ± ± ± ± ± ± ± ±
49.17 ± 34.82 ± ± T ± ± ± 12.76 T ± ± ± ± ± ± ± ± ± 2.18 ± ± ± ±
8.51 ± 13.41 ± ± ± ± ± ± 1.36 T ± ± ± ± ± ± ± ± ± ± ± ± ± ±
± ± ± ± ± ± ± 57.86 ± ± ± ± ± T ± ± ± ± ± ± ± ± ± ± ±
3.82 ± ± ± 13.56 ± ± ± ± ± ± ± ± 25.07 2.52
FABIANA CASTELLARINI et al.
Cvc1 (10)
94
Table 2. Average percent of food items consumed by rodent species captured in different habitats of agroecosystems in CoÂrdoba, central Argentina. Percentages that where £ 1% are listed as trace (T). Cv: Calomys venustus; Cl: C laucha; Cm: C. musculinus; Ad: Akodon dolores. Letters and numbers accompaning species' names are habitats and localities. Habitats: (c) cropped fields; (b) borders; (g) grasslands. Localities: (1) RõÂo Cuarto; (2) Villa de MarõÂa; (3) Cruz del Eje; (4) Villa Dolores. S: unidentified species. Sample size in brackets.
Table 2. Continued Cvc1 (10)
Clc1 (9)
Cvc2 (7)
Cmc2 (16)
Adc2 (8)
Cvb1a Cvb1b Cmb1b Cmb1a Adb1a Cvg2 (12) (6) (8) (11) (10) (6)
Clematis montevidensis Oxalis crisanta Morrenia brachystephana Descurainia argentina Parietaria debilis Salpichroa origanifolia Passiflora coerulea Lycium australe Celtis iguanae Patenium histerophorus Veronica didyama Sorghum sp. Glandularia sp. Malvaceae 1 Gramineae 1 Gramineae 2 Gramineae 3 Gramineae 4 Gramineae 5 Gramineae 6 Gramineae 7 Gramineae 8 S1 S2 S3 S4 S5 S6
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 5.35 ± ± ± ± ±
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
2.89 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 2.05 ± ± ± ±
T ± ± ± ± ± ± ± ± ± ± ± ± ± T ± ± ± ± ± ± ± ± ± ± ± ± ±
2.85 1.59 ± ± ± ± ± ± ± ± ± ± ± ± 2.65 ± ± ± ± ± ± ± ± ± ± ± ± ±
9.39 ± 1.33 T ± ± ± ± ± ± ± ± ± ± ± 4.14 ± ± ± ± ± ± ± ± ± ± ± ±
± ± ± 1.14 ± ± ± ± ± ± ± ± ± ± ± 1.46 3.60 ± ± ± ± ± ± ± ± ± ± ±
± T ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 1.86 ± ± ± ± ± ± ± ± ± ± ± ± ± 1.77 ± ± ± ± ± ± ±
Arthropods
7.96
40.85 T
8.11
63.83 2.17
3.95
11.62 T
Cvg3 (12)
Cvg4 (8)
Cmg4 (6)
Adg2 (9)
Adg3 (10)
Adg4 (9)
1.09 30.22 29.69 2.38 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 13.46 ± ± ± ± ± ± ± ± 2.33 ± ± ± ± ± ± ± 3.78 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 4.69 ± ± 3.75 ± ± ± ± ± ± ± 6.81 ± ± ± ± ± ± 1.30 ± ± ± ± ± ± 7.76 ± ± ± ±
± ± ± 4.93 ± ± ± 20.77 ± ± 4.36 ± 0.88 7.79 ± ± ± ± ± ± ± ± ± ± ± 14.06 ± ±
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
16.15 ± ± 1.65 ± ± 1.28 ± ± ± ± 2.15 ± ± ± ± ± ± ± ± 1.41 ± ± ± ± ± ± ±
± ± ± ± ± ± ± 1.58 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± T ± ±
63.28 T
T
13.55 38.15 31.17 23.32
Leaves
Feeding habits of small mammals
T
39.43 ± ± ± T 1.47 ± ± 2.53 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 1.97 ±
95
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FABIANA CASTELLARINI et al.
Table 3. Significant correlations between food items consumed by rodent species of agroecosystems in CoÂrdoba (central Argentina) and dimensions of MDS analysis, using Spearman's coefficient (R). Seeds (s). Leaves (l). Food item species
Crop fields
Borders
Grasslands
R
P
R
P
R
P
0.83 ±0.75 0.41 0.46 ±0.53 ±0.43 ± ± ± ± ± ± ± ± ±
0.000 0.000 0.003 0.001 0.000 0.002 ± ± ± ± ± ± ± ± ±
0.87 ± ±0.61 ± ± ± ±0.33 ±0.40 ±0.34 ± ± ± ± ± ±
0.0000 ± 0.0000 ± ± ± 0.0233 0.0058 0.0203 ± ± ± ± ± ±
± ± ± ± ±0.76 ±0.30 ± ± ± 0.92 0.31 ±0.26 ±0.35 ±0.31 0.26
± ± ± ± 0.0000 0.0195 ± ± ± 0.0000 0.0156 0.0417 0.0054 0.0158 0.0456
±0.41 ±0.43 0.57 0.45 0.31 0.43 ± ± ±
0.004 0.002 0.000 0.001 0.028 0.002 ± ± ±
±0.72 ± 0.52 ± ± ± 0.31 ± ±
0.0000 ± 0.0002 ± ± ± 0.0342 ± ±
± ± 0.78 ± ± ± ± ±0.40 0.48
± ± 0.0000 ± ± ± ± 0.0017 0.0001
± ± ± ± ± ± ±
± ± ± ± ± ± ±
± ± ± ± ± ± ±
± ± ± ± ± ± ±
0.50 ±0.30 0.30 0.27 0.26 0.31 ±0.55
0.0000 0.0200 0.0185 0.0401 0.0485 0.0176 0.0000
Dimension 1 E. indica (s) C. album (s) Arthropods Species 1 (l) Malvaceae (s) Amaranthus sp. (s) O. crysantha (l) Gramineae 6 (s) Gramineae 7 (s) C. montevidensis (l) Sorghum sp. (s) Seteria sp. (s) S. kali (s) L. australe (l) S. eleagnifolium (s) Dimension 2 E. indica (s) C. album (s) Arthropods C. montevidensis (l) Malvaceae (s) Lycium sp. (s) Amaranthus sp. (s) M. albus (s) Gramineae 4 (s) Dimension 3 Sorghum sp. (s) Malvaceae (s) Amaranthus sp. (s) B. subalternans (s) Setaria sp. (s) S. kali (s) S. eleagnifolium (s)
Table 3 shows the food items significantly correlated with each dimension variable. The diet of A. dolores was correlated with the consumption of arthropods and that of C. venustus with consumption of Eleusine indica seed. For both these groups diets of C. laucha were mainly correlated with consumption of arthropods and seed of E. indica. Finally, C. venustus and C. musculinus consumed high proportions of seeds of Chenopodium album. Other food items were correlated with this configuration, but their
relative composition in the small mammal diets was low (Tab. 2). Borders: A close similarity between the diets of C. venustus, C. musculinus and A. dolores was observed in the borders (Fig. 2). The similarity between diets of C. venustus and C. musculinus was due to consumption of seeds of E. indica, C. album and Amaranthus sp., and that between the diets of C. venustus and A. dolores to seeds of C. album (Tab. 2 and 3). The only significant difference between the diets of C. mus-
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Fig. 2. Final 2D configuration in MDS analysis of rodents diets of borders in agroecosystems of CoÂrdoba, central Argentina. Calomys venustus (circles), C. musculinus (squares), C. laucha (asterisks) and A. dolores (triangles). Borders: A (open symbols) and B (closed symbols). Kruskal's stress = 0.18.
culinus and A. dolores was found on dimension 1 (MANOVA test: Wilk's l = 0.63, df1 = 8, df2 = 82, P = 0.01, Tukey's test P = 0.004). The difference was correlated with a high consumption of arthropods by A. dolores and seeds by C. musculinus (Tab. 3). Grasslands: Several groups of diets were recognized in the natural grassland (MANOVA test: Wilk's l = 0.02, df1 = 18, df2 = 144, P = 0.000, Fig. 3). Two groups were identified on dimension 1 showing significant differences between diets of small mammals from the grassland of Villa Dolores and those of Cruz del Eje and Villa de Maria. Seed consumption of a Malvaceous species was correlated with the samples from Villa de Maria and leaves of Clematis montevidensis with samples from the other localities (Tab. 2 and 3). Dimension 2 showed significant differences between the diets of A. dolores and the other two coexisting species, C. venustus and C. musculinus, from Villa Dolores (Tukey's test P < 0.04). These differences were due to the higher relative consumption of arthropods by A. dolores (Tab. 2 and Tab. 3).
Finally, dimension 3 showed significant differences between the diets of the C. musculinus ± C. venustus pair (Tukey's test P = 0.0004) and the C. musculinus ± A. dolores pair (Tukey's test P = 0.01) from the grassland of Villa Dolores. The differences were correlated with seed species consumption (Tab. 2 and 3). Only in this habitat, differences between the diets of C. venustus and C. musculinus were found. Habitat diversity, dietary range and overlap: the mean diversity of plants was highest in the borders and the lowest in the cropped fields (Tab. 4). Considering all the food items, dietary ranges in Calomys species were similar in the cropped fields. C. venustus and C. musculinus had a higher dietary range at the borders than in the cropped fields and grasslands. Dietary range in A. dolores was higher in grasslands than in the cropped fields and borders. Considerable overlap between Calomys diets was observed in cropped fields and borders as compared with the grasslands. The opposite pattern was observed for A. dolores, for which there was more overlap in grasslands than in cropped fields and borders (Tab. 5).
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FABIANA CASTELLARINI et al.
Fig. 3. Final configuration in MDS analysis of rodents diets of grasslands in agroecosystems of CoÂrdoba, central Argentina. Calomys venustus (circles and crosses), C. musculinus (squares), and A. dolores (triangles and asterisks). Localities: Cruz del Eje (closed symbols), Villa Dolores (open symbols) and Villa de MarõÂa (crosses and asterisk). Kruskal's stress = 0.16. Table 4. Dietary breadth (LEVINS 1968) calculated with major dietary components and Shannon's index per habitat. *Average values. Habitat
C. laucha
C. musculinus
C. venustus
A. dolores
Habitat Diversity
Crop field
1.95*
1.80
2.19*
2.31
0.31*
Border
±
3.14*
3.93*
2.32
0.79*
Grassland
±
2.31
3.66*
3.67
0.57*
Table 5. Dietary overlap for each coexisting rodent species with food items above 1% relative percentage, using the simplified Morisita's index (HORN 1966). * Average values Species pair
Crop field
Border
Grasslands
C. venustus ± C. laucha C. venustus ± C. musculinus C. venustus ± A. dolores C. musculinus ± A. dolores
0.86 0.88 0.21 0.29
± 0.80 0.25 0.22
± 0.47 0.52* 0.71
The feeding relationships for the more abundant small mammal species in the agroecosystems of central Argentina suggest that Calomys species showed feeding habitats within the seed-leaves gradient, C. musculinus being largely granivorous, C. venustus granivorous or folivorous-grani-
vorous, and C. laucha the most omnivorous. Akodon species showed feeding habits within the arthropods-omnivory gradient. At the level of omnivory feeding habits, A. dolores presented similar feeding habits as C. laucha (Fig. 4).
Feeding habits of small mammals
Fig. 4. Feeding relationships between small mammal species in the agroecosystems of central Argentina taking into account the average relative composition of leaves, seed and arthropods. Data sources from: BILENCA et al. (1992); DELLAFIORE and POLOP (1994, 1998); ELLIS et al. (1998) and present study. Aa: Akodon azarae, Ad: A. dolores, Cl: Calomys laucha, Cm: C. musculinus and Cv: C. venustus. Numbers accompanying species' names are habitats: cropped fields (1), borders (2) and grasslands (3).
Discussion Our results support the view that the small mammals of the Argentinian pampas are omnivorous (Martinez et. al 1990; Bilenca et al. 1992; Dellafiore and Polop 1994, 1998; Castellarini et al. 1998; Ellis et al. 1998; Castellarini and Polop 2002). However, we found variation in the relative composition of their diets and propose a relationship between coexisting species, feeding habits and habitat disturbance level. A. dolores was mainly carnivorous in the cropped fields and borders, becoming omnivorous in grasslands, while A. azarae was omnivorous in borders. Nevertheless, this dietary separation could not be important because these pairs of species were not found together and in general A. dolores is dominant in less disturbed habitats, like grasslands, and A. azarae in habitats with intermediate disturbance such as borders (Kravetz and Polop 1983; Bilenca et al. 1992). Considering Calomys species, C. venustus and C. laucha had a high dietary overlap, but only with regard to seed spe-
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cies, because taking into account leaves and arthropods C. laucha was the most omnivorous of the three Calomys species. The differences between our results and those of other authors (Bilenca et al. 1992; Dellafiore and Polop 1998; Ellis et al. 1998), who typified C. laucha as granivorous (seed-eating) -folivorous (leaf-eating) or granivorous, the small size of the species and their presence almost exclusively in cropped fields, suggest that C. laucha could use different food resources in only one habitat as an adaptive response to its competitive exclusion from other habitats by the other larger species (Busch and Kravetz 1992). Thus, C. laucha would be a ªresource generalistº and ªhabitat specialistº (both obligate) living chiefly in the more disturbed habitat, the cropped field, and eating the food available or not consumed by other sympatric species. On the other hand, the high dietary overlap observed between Calomys venustus and C. musculinus in the cropped fields applied to both kinds of food items-individual seed and leaf species and the broad category (arthropods, leaves and seeds) and the low food availability, suggest that food partitioning cannot be important to this pair of species because the periodic disturbance could lead to slow population growth or high dispersal rates, allowing species to coexist (Rosenzweig and Abramsky, 1993). Finally, the contrasting results for A. dolores and Calomys species, i. e. the small overlap in crop fields and large overlap in grassland and the high dietary range in grasslands, could be explained by the generalization-specialization of Robinson and Wilson (1998), which predicts that the diets of coexisting consumer species should broadly overlap, being generalists in resources easily captured, and specialists in the ones that require specialized hunting techniques. While all species share a high proportion of food items, and are thus generalists, A. dolores remains a specialist in arthropods, C. venustus in leaf and seed species, and C. musculinus in seeds, the later being the ªresource specialistº and the ªhabitat generalistº. In summary, we suggest that dietary overlap should be analysed in
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FABIANA CASTELLARINI et al.
both specific and broad categories, and that the feeding habits of the small mammals of the Argentinian pampas agroecosystems in the more disturbed habitats are highly dependent on disturbance and the capability of the species to be opportunist; while in the less disturbed habitats the feeding habits are more dependent on the specialization of each coexisting species.
Acknowledgements We thank Marcos Torres for assistance in fieldwork and Jutta Wester for her help with the German translation of the abstract. This study was supported by grants from Consejo de Investigaciones Cientificas y Tecnologicas de la Provincia de CoÂrdoba (CONICOR).
Zusammenfassung ErnaÈhrungsgewohnheiten von KleinsaÈugern in AgraroÈkosystemen von Zentralargentinien Die widerspruÈchlichen Resultate, zu denen Studien der ErnaÈhrungsgewohnheiten kleiner SaÈugetiere in zentralargentinischen Úkosystemen gefuÈhrt haben, koÈnnen oft auf unterschiedliche Nahrungsidentifikation, auf die Probennahme der LebensraÈume und auf koexistierende Arten zuruÈckgefuÈhrt werden. In der vorliegenden Untersuchung haben wir analysiert, wie anthropogene StoÈrungen die ErnaÈhrung in kleinen Gemeinschaften von SaÈugetieren der Úkosysteme beeinflussen und zu unterschiedlichen Nahrungsrationierungen fuÈhren koÈnnen. Die Proben wurden drei verschiedenen Landschaftstypen in vier Regionen Zentralargentiniens aufgenommen. Die ErnaÈhrung wurde mittels mikrohistologischer Analysen der Mageninhalte bestimmt, und die Daten wurden durch Indices und multivariate Vergleiche analysiert. GemaÈû unseren Ergebnissen sind die untersuchten kleinen SaÈugetiere Allesfresser, die ihre ErnaÈhrung jedoch entsprechend der IntensitaÈt von anthropogenen StoÈrungen einstellen. Die Calomys Arten zeigten eine hoÈhere NahrungsuÈberlappung in LebensraÈumen mit erheblichen und mittleren menschlichen Beeinflussungen als in LebensraÈumen mit geringer StoÈrung. Bei den Arten von Calomys und Akodon dolores wurde ein umgekehrtes Muster gefunden. Die starke Ûberlappung bei Calomys in LebensraÈumen mit hoher und mittlerer Stellung wurde mit Hilfe der Hypothese der StoÈrung als Chance erklaÈrt. Die starke Ûberlappung bei Calomys und Akodon dolores in LebensraÈumen mit geringer StoÈrung wurde erklaÈrt durch die Hypothese der Generalisierung-Spezialisierung, die geringe Ûberlappung bei allen Arten mittels der klassischen Nahrungsverteilung.
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Authors' addresses: Fabiana Castellarini, DeÂpartement Dynamique des systeÁmes eÂcologiques, Centre d'Ecologie Fonctionnelle et Evolutive ± CNRS 1919, route de Mende, 34293 Montpellier cedex 5 France (e-mail: [email protected]); Claudia Dellafiore and Jaime Polop, Departamento de CC Naturales, Universidad Nacional de Rio Cuarto, Ag; Postal No 9, 5800 Rio Cuarto, Argentina.