FRAGMENTA THERIOLOGICA
Acta Theriologica 48 (2): 283–288, 2003. PL ISSN 0001–7051
Food digestibility of an Eurasian badger Meles meles with special reference to the Mediterranean region Luís M. ROSALINO, Filipa LOUREIRO, David W. MACDONALD and Margarida SANTOS-REIS
Rosalino L. M., Loureiro F., Macdonald D. W. and Santos-Reis M. 2003. Food digestibility of an Eurasian badger Meles meles with special reference to the Mediterranean region. Acta Theriologica 48: 283–288. Feeding trials were carried out with a captive adult badger Meles meles (Linnaeus, 1758) to establish relationships (digestibility coefficients) between the biomass of freshly consumed food and the dry undigested remnants recovered from scats (bone, teeth, hair, feathers, exoskeleton parts, seeds, etc). The foods studied were those revealed by our research to be the principal components of badger diet in a Mediterranean environment, and the values of the digestibility coefficients (DC) were: 24.74 for rabbits Oryctolagus cuniculus, 21.72 for rodents, 19.81 for pigeons Columba sp., 99.50 for amphibians, 32.35 for arthropods imago, 44.39 for insect larvae, 18.45 for earthworms Lumbricus rubellus, 2.75 for acorns Quercus sp., 9.19 for arbutus Arbutus unedo, 12.25 for blackberries Rubus ulmifolius, 46.12 for figs Ficus carica, 34.87 for loquats Eriobotrya japonica, 10.94 for olives Olea europaea, and 12.02 for pears Pyrus bourgaeana. The variability of DC values was measured, and attributed to the heterogeneity of constituents of the selected food types. There was no statistically significant correlation between the average weight of consumed food and the digestibility coefficients, confirming the expectation that such coefficients must be derived empirically for each food type. Centro de Biologia Ambiental, Departamento de Biologia Animal da Faculdade de Ciências da Universidade de Lisboa, Ed. C2 Campo Grande 1749-016 Lisboa, Portugal, e-mail:
[email protected] (LMR, FL, MS-R); Wildlife Conservation Research Unit, Department of Zoology, Oxford University, OX1 3PS, UK (DWM) Key words: Meles meles, digestibility coefficients, diet, Mediterranean environments
Introduction Diet is a fundamental and widely studied aspect of carnivore ecology, and is commonly studied through the analysis of undigested faecal remains (eg Roper and Mickevicius 1995, Virgos et al. 1999). Results of scat analysis can be expressed in various ways, of which common examples are frequency of occurrence [(number of scats containing food itemi/total number of scats) ´ 100] or as percentage of occurrence [(number of occurrences of food itemi/total number of food item occurrences) ´ 100] (Lockie 1959). However, these approaches usually lead to an overestimation of small prey, which may dominate in number but when converted to biomass actually represent a less important food (Goszczyñski 1974, Floyd et al. 1978). One way of overcoming this problem is to present data as percentage of [283]
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consumed biomass. This necessitates the use of correction factors (digestibility coefficients) that quantify the relationship between dry weight of undigested remains of prey in scats and fresh weight of the consumed prey (Fairley et al. 1987). Digestibility coefficients based on feeding tests have been published already for various carnivore species (eg red foxes Vulpes vulpes – Lockie 1959, wolves Canis lupus – Floyd et al. 1978, coyotes Canis latrans – Meriwether and Johnson 1980, side-striped jackals Canis adustus – Atkinson et al. 2002, domestic cats Felis catus – Liberg 1982, American mink Mustela vison – Fairley et al. 1987, common genets Genetta genetta and Egyptian mongooses Herpestes ichneumon – Palomares and Delibes 1990, and wildcats Felis silvestris – Sarmento 1996). However, none of these species’ diets closely approximates that of European badgers Meles meles. Indeed, most concern large vertebrate prey (eg Lodé 1993, Sarmento 1996, O’Donoghue et al. 1998, Vos 2000, Rosalino and Santos-Reis 2002). Additionally, none of these species is phylogenetically close to the Eurasian badger (Macdonald 1992). The diet of Eurasian badgers Meles meles (Linnaeus, 1758) has been rather widely studied, but there are no published data on the digestibility coefficients of their prey apart from some values recently given by Revilla and Palomares (2002). As Kruuk (1978) illustrated in his revealing isocline plots (frequency of occurrence versus volume of undigested prey in badger faeces), this is a species whose diet contains both large and small foods, of diverse categories, and doubtless radically different digestibilities. Feeding habits of this mustelid vary greatly across geographical regions. In northwest and eastern Europe, badgers specialize in the consumption of earthworms (eg Kruuk 1978, Goszczyñski et al. 2000), but in Mediterranean areas the distinct climatic and landcover characteristics are associated with a much more diverse diet. In western Italy, fruit and insects are the main categories consumed (Pigozzi 1991), whereas in southern Spain, Martín et al. (1995) and Revilla (1998) reported a substantial proportion of European rabbits Oryctolagus cunuculus in the diet. In Portugal, we studied the diet of badgers in an area of cork oak Quercus suber woodland, where their feeding ecology was revealed to be broadly similar to that reported in western Italy (L. M. Rosalino, unpubl.). We undertook this study to determine digestibility coefficients for the main foods consumed by badgers, focusing particularly on those which emerged as important in our cork-wood Mediterranean study area. Material and methods Feeding trials involved an adult male badger (weighing 9 kg), held at the Lisbon Zoological Garden, in an 8 m2 cage. Before each trial, the badger was fasted for 48 hours, during which all scats were removed from the enclosure (Floyd et al. 1978). During the following 3 days the animal was fed with specific food items, which were previously weighed. The weight of each food category given per day varied (Table 1), but was never less than 0.5 kg, a value suggested by Hewson and Kolb (1976) and Henry (1983) as the average daily food requirement of a medium-sized adult badger. For arthropods (imagos and larvae) feeding trials, due to the low weight of these prey and the difficulty in getting the number needed, a complement of apple pulp (without any seed or peel) was used to achieve the requested amount 0.5 kg per day (Table 1). Non-consumed food and remains (hair, feathers, seeds, etc) were collected, and their weight subtracted from the initial amount given.
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No further food was provided until faeces production ceased (less than 48 hours) (Goszczyñski 1974). All scats were collected and analysed using standard procedures (eg Rosalino and Santos-Reis 2002). As correction factors were assumed to be independent (irrespective of how prey may be mixed within a given meal) (Lockie 1959), all food categories considered were tested separately. To confirm DC’s independence a mixed feeding trial (that included the main food categories in Mediterranean environments: arthropods imagos, beetles larvae and fruit) was also performed. Selection of the different trophic resources to be tested was based partly on the results of our analysis of 450 badger scats collected at Grândola hills, SW Portugal (L. M. Rosalino, unpubl.): fruit (acorns, blackberries, figs, loquats, olives, strawberry tree fruit, and pears), arthropods, amphibians, birds, and mammals, as well as other foods known to be important for badgers elsewhere (Kruuk and Parish 1981, Fedriani et al. 1998, Revilla 1998) and for other meso-carnivore species in southern Iberia (eg Gil-Sanchez et al. 1999). Badgers are known to eat both Lumbricus terrestris and L. rubellus (see review by Macdonald 1983), both of which have been shown to have similar nutritional characteristics (French et al. 1957, Kruuk 1978). For our trials we used only L. rubellus. The weight of earthworm’s undigested remains was calculated by subtracting the weight of secretions, soil and other prey remains to the total weight of the badger’s scat. Correction factors (Digestibility coefficients – DC) were calculated using the following equation: DCi = Fi – NCRi / URi where Fi is the weight of a given food item i, NCRi the weight of the non-consumed remnants of item i and URi the weight of undigested remnants of item i found in scats. Correlation between the mean weight of each item and the respective DC value was tested using Spearman’s rank correlation coefficient (rS) to avoid normality constraints (Zar 1999). Coefficients obtained from feeding experiments that involved each food were compared separately with those obtained from the mixed feeding trial. This comparison was performed using the t-score (Fowler and Cohen 1990). For each food item, at least three replicates were made at different times of year in order to minimize any bias associated with the animal’s body condition.
Results and discussion The majority of the food categories analysed expressed low variability of DC (SE proportion of DC ranges from 3.69 to 18.12%); however, arthropod imagos and blackberries categories showed considerable variation (Table 1). The former is a heterogeneous group (scorpions, spiders, crickets and beetles). However, distinguishing their remains in faeces is extremely laborious and therefore a combined value for their digestibility seemed a more useful measure than species-specific coefficients. Variation in the coefficient for blackberries is attributable to variation in the number of seeds per fruit (Herrera 1987, L. M. Rosalino, pers.obs.). We detected no correlation (p > 0.05) between DC value and food mean weight in any of the main categories: fruits, invertebrates and vertebrates. However, a non-significant trend for a positive association was found in fruit (rS = 0.750, p > 0.05). These results differ from those of Fairley et al. (1987), who described a positive relation between food item mass and the DC value. Palomares and Delibes (1990) also reported such a correlation, and ascribed it to the negative correlation between body volume and surface area in the foods they tested. However, the particular types of food that we tested (and that are represented in the badger’s diet) are so different that we had no a priori expectation of any such correlation. The comparison between DC values obtained with feeding trials per item and the mixed trial revealed no statistical difference (for arthropods: t = 0.212, larvae: t = 1.424, blackberries: t = 2.836, acorns: t = 3.747, arbutus: t = 2.517, olives:
Insect larvae Amphibians Pigeon Rodents Rabbits
Acorns Blackberries Figs Loquats Olives Pears Strawberry tree fruit Earthworms Arthropod imagos
Category
Quercus sp. Rubus ulmifolius Ficus carica Eriobotrya japonica Olea europaea Pyrus bourgaeana Arbutus unedo Lumbricus rubellus Order Coleoptera Order Orthoptera Classis Chilopoda Order Scorpionida Order Coleoptera Rana perezi Columba sp. Mus musculus Oryctolagus cuniculus
Species
4 4 3 3 4
3 4 4 3 3 3 3 3 4
n
264.88 803.72 2653.10 768.27 3429.68
5.17 1.11 46.83 39.55 2.34 39.50 4.12 0.69 1.27 0.43 2.57 1.88 0.66 26.45 421.80 23.79 2215.94
(g)
trial (g) 2467.60 1919.37 2258.98 2850.28 2678.93 2834.71 2212.73 606.10 180.90
Prey-item mean weight
Mean total weight given per
44.39 ± 8.05 99.50 ± 16.90 19.81 ± 1.15 21.72 ± 0.80 25.74 ± 4.39
2.75 ± 0.46 12.25 ± 3.33 46.12 ± 5.98 34.87 ± 5.48 10.94 ± 1.49 12.02 ± 1.28 9.19 ± 1.47 18.45 ± 2.14 32.35 ± 8.10
x ± SE
31.02 67.60 17.90 20.29 14.03
1.88 7.75 34.20 24.35 8.27 9.89 6.63 15.65 12.79
Min
66.54 157.17 21.86 23.03 33.50
3.40 22.01 57.63 42.77 13.41 14.31 11.70 22.64 50.40
Max
Digestibility coefficients
Exoskeleton fragments Bones Bones and feathers Bones, teeth and hair Bones and hair
Peel and pulp Seeds Seeds and peel Seeds and peel Seeds and peel Seeds and peel Seeds Chaetae and gizzards Exoskeleton fragments
Undigested remnants
Table 1. Mean weights and digestibility coefficients of Mediterranean types of food in feeding experiments with an Eurasian badger. n – number of trials.
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t = 0.876, pears: t = –2.041; all p > 0.05). This is an important result since the majority of scats analysed (L. M. Rosalino, unpubl.) reveal that badgers have mixed meals and only rarely eat a single type of food. While our focus has been on badgers in Mediterranean environments, many of the food items (or at least similar ones) represented in our trials occur in the recorded diets of badgers in other regions. Due to sample size (one badger), variation associated with sex, reproductive stage, health and age are not accounted for in our results, and values obtained should therefore be used with due caution. Moreover, some discrepancy was found between our results and correction factors given by other authors (eg Revilla and Palomares 2002), but this probably originates from differences in methodology. In the absence of other published data on badger digestibility and considering the correlation reported here between the results of isolated and mixed feeding trials, we believe, our results may be useful for dietary studies of badgers in other areas of the species’ range. Certainly, analysis of diet as disclosed by faecal remains can be greatly advanced when DC values are used to complement other measures, such as frequency and volume of undigested remains. Acknowledgements: We wish to acknowledge the kind co-operation of the Lisbon Zoological Garden and the staff responsible for feeding the badger between experiments. We also thank all our colleagues that occasionally helped during feeding experiments. Two anonymous reviewers improved the content of the previous draft. Funding for this research was provided by FCT and FSE (III Quadro Comunitário de Apoio) (PRAXIS XXI/BD/15842/98; SFRH/BD/5162/2001, PRAXIS/PCNA/C/BIA/105/96).
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