ORIGINAL PAPER

Wildl. Biol. Pract., December 2006 2(2): 63-71DOI:10.2461/wbp.2006.2.8

THE WILD RABBIT (ORYCTOLAGUS CUNICULUS L.) DIET ON A SAND DUNE AREA IN CENTRAL PORTUGAL: A CONTRIBUTION TOWARDS MANAGEMENT.

J. Alves1, J. Vingada2 & P. Rodrigues1

1 Sociedade Portuguesa de Vida Selvagem / Portuguese Wildlife SocietyApartado 16, EC Quiaios, 3081 - 101 Figueira da Foz, PortugalTelephone: +351 936410212; Fax: +351 233 910 670Email: zealves@portugalmail.pt2 Departamento de Biologia - Universidade do Minho / Biology Department – University of Minho

Keywords

Wild rabbit;

diet;

feeding strategies;

micro-histological analysis.

Abstract

The wild rabbit plays a fundamental role on Iberian habitats, not only as a target prey in natural trophic chains but also as an elected game species. Recently and all over the Iberian Peninsula, wild rabbit populations have been decreasing as a result of several adverse conditions. Among other parameters, the wild rabbit feeding behaviour must be understood in order to effectively manage rabbit populations. The main aim of the present study is to describe the wild rabbit diet in a sand dune area in Portugal.Diet composition was obtained by micro-histological analysis of faeces collected over a two-year period on two different landscape units: scrubland and pine forest. Diet data indicated significant differences when comparing Winters and Summers in scrublands, while in pine forest areas diet was similar along seasons. Using a finer scale by comparing plant species or genera, differences were also found in the wild rabbit Winter diet in scrubland areas. With respect to taxa, the wild rabbit diet in scrublands is different from that found in pine forest areas throughout the year.Results emphasise that although lacking some plant species, Pine forest areas allow a seasonal selection of food items. Furthermore, the present study highlights the importance of the preservation of particular habitats that support specific vegetation such as Cyperacea and Juncaceae plants.

Introduction

The wild rabbit (Oryctolagus cuniculus L.) is a keystone species on Mediterranean ecosystems in such a way that specialized predators depend almost completely on this prey [1]. Threatened species such as the Iberian lynx (Lynx pardinus) and the Imperial eagle (Aquila adalberti) will settle territories on areas with high wild rabbit densities [2-4]. However, populations of this herbivore have been declining over the last decades on this region [5-7] mostly due to viral diseases (myxomatosis and viral hemorrhagic disease), but also due to habitat fragmentation and unmanaged game activities [8]. It is thus fundamental to understand the wild rabbit feeding ecology in order to effectively manage wildlife species in these ecosystems.

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Although widely considered as a grazer [9], the wild rabbit is able to adapt its diet according to plant items availability [10,11]. Previous studies focusing on the wild rabbit diet in Portugal [12-14] refer to mountain or savannah-like (“montado”) habitats. With respect to coastal sand dune areas, where digging and burrow-building are common activities, only data referring to Spain, the Netherlands and England is available [11,15,16]. The aim of the present study is to describe the wild rabbit diet in two landscape units (pine forest and scrubland) over a two-year period in a coastal area in Portugal. This information can then be used as a management tool to improve preferential food resources and thus recover the wild rabbit population, contributing to the management of the Natura 2000 site “Dunas de Mira”.

Methods

Study area

The Quiaios National Forest is included in the Natura 2000 network site “Dunas de Mira, Gândara e Gafanhas” (PTCON055), which comprises approximately 22,000 ha. This coastal forest is located to the north of Mondego Cape in the Coimbra District, central Portugal. According to the Habitat Directive (93/43/EEC), this area is located in the Mediterranean climate biogeographic region, and includes twenty important habitats [17]. The Quiaios National Forest (ca. 6,600 ha) is mainly composed by three landscape units: dunes, pine forest and scrublands. The dunar area is currently dealing with aggressive invasion by Acacia longifolia and Carpobrotus edulis, and was not considered for this study. Scrublands hold a great diversity of small shrubs including Corema album, Cytisus spp., Erica spp., Caluna vulgaris, Ulex spp., Cistus spp. and Halimium halimifolium. The pine forest is mainly composed by Pinus pinaster and Pinus pinea, with an understory of Myrica faya, Arbutus unedo and Acacia longifolia.Both pine forest and scrubland areas are interspersed with a habitat of major importance according to the Habitat Directive (93/43/EEC), designated as “Mediterranean amphibian vegetation”. This type of vegetation is characterized by a peculiar set of plants, such as Juncus acutus, Juncus minutulus, Carex arenaria, Eleocharis palustris, among others, usually located around small ephemeral lakes and ponds that form as a result of Winter rainfall and may subsist until early Summer. Grassland areas with aromatic herbaceous plants such as Lavandula stoechas sampaiana and Helichrysum italicum are present in landscape depressions and mainly within scrubland areas.

Sample collection and preparation

Samples were collected in two landscape units (pine forest and scrublands). Fifteen faecal samples were collected seasonally over 4 sampling periods (Summer 2002, Winter 2003, Summer 2003, Winter 2004). Each of these 15 faecal samples was composed by 10 fresh pellets collected from the same pellet group (latrine), and were then frozen until diet analyses [10].

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In order to stratify samples per area and season, 8 pool samples were created for each landscape unit and season. Each of these pooled samples contained at least one pellet from each of the 15 field faecal samples. A total of 64 pool samples was obtained (8 samples in 2 habitat units in each of the 4 seasons). After thawing, samples were heated under pressure up to 115 ºC in water for two hours and left to soak overnight. A sub-sample of 5 g was washed in a Warning blender and strained over a plankton sieve, and finally stored in 70% ethanol.

Diet composition

In order to prepare a reference collection, plant tissues such as leafs, stems and in some cases, flowers and seeds, were firstly soaked in household bleach overnight and rinsed afterwards. The tissue epidermis was then striped off and mounted in glycerol [10,18,19]. Photomicrographs (optical microscope: 40x and 100x) of these slides referring to 30 plant species from the study area constitute the reference collection, which allowed the identification of the cuticle and epidermis fragments obtained from wild rabbit faeces [19].The micro-histological analysis followed the procedure developed by De Jong [20]. Samples were examined by light microscopy and at least 100 fragments of cuticle or epidermis in each sample were identified. These were measured using a grid (0.01 m2) in the microscope eyepiece. Taxa (species or genera) abundance was calculated as the percentage of the total area of measured fragments [10,19].

Diet analysis

The Kulczynski´s similarity index (KSI) was ran on the wild rabbit diet data according to areas and seasons, following De Jong [18]: KSI = (Σ 2C/ Σ [A+B]) x 100, where C is the smallest percentage of a species or category occurring in two data sets, and A and B are the percentages of this species or category found in each of the data sets. At taxon level, diets are similar when the KSI value is equal or higher then 61 and significantly different when the KSI value is below 55. For a first analysis, plant items were grouped into six categories: Graminoids of dry areas, Graminoids of moist areas, Dicot and Monocot herbs, Nitrogen fixers, Pinus sp., Lichens/Fungi/Mosses, and accordingly, similarity occurs at KSI values equal or higher than 77, and significant differences occur at 72 or lower values. KSI results obtained in between these limits are out of the index detection range.

Results

The most important item in the wild rabbit diet in both scrubland and pine forest is “Grasses” (over 35%) (Fig. 1 and 2). However, within the graminoid category there is a clear difference between the consumption of plants from dry or humid areas. Plants from wet areas, mainly Cyperaceae and Juncaceae but also Phragmites australis, are consumed mostly during Summer whereas graminoid plants from dry places represent a higher percentage during Winter periods.

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Fig 1. Wild rabbit diet in scrublands (expressed in terms of percentage of the total area of measured fragments) for the different sampling seasons, based on consumed plant categories.

In scrublands, it is possible to denote a seasonal inverse pattern of consumption between the categories of Nitrogen fixing plants (Ulex sp. , Cytisus grandiflorus, Acacia longifolia and Trifolium sp.) and Dicot and Monocot herbs. In fact, in these areas, the Nitrogen fixing plants present a higher percentage in diet during Summer, whereas Dicot and Monocot herbs present a higher percentage during Winter (Fig. 1).With respect to pine forest, Dicot and Monocot herbs maintain a similar seasonal pattern to that observed in scrublands, while Nitrogen fixers present an inverse pattern revealing a higher consumption during Winter periods (Fig. 2).

Fig 2. Wild rabbit diet in pine forest areas (expressed in terms of percentage of the total area of measured fragments) for the different sampling seasons, based on consumed plant categories.

Graminoids dry areas

Nitrogen fixers

Graminoids moist areas Dicots and Monocot herbs

Pinus sp. Lichens/Fungi/Mosses

Summer 02 Winter 03 Summer 03 Winter 04

Per

cent

age

70

60

50

40

30

20

10

0

Graminoids dry areas

Nitrogen fixers

Graminoids moist areas Dicots and Monocot herbs

Pinus sp. Lichens/Fungi/Mosses

Summer 02 Winter 03 Summer 03 Winter 04

Per

cent

age

70

60

50

40

30

20

10

0

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Minor categories such as Lichens/Fungi/Mosses and Pine leaves are almost absent from the wild rabbit diet in scrublands. In pine forest, Lichens/Fungi/Mosses constitute a basal portion of wild rabbit diet, whereas Pine leaves were only registered during the Winter of 2003 (Fig. 2).Several differences were detected among categories when comparing wild rabbit diet according to seasons both in scrublands and pine forest (Table 1). In scrublands, no differences were found among Winters or among Summers while significant differences were found when comparing Winters to Summers (both in the first and second years). In pine forest areas, no differences were found among Winters and data referring to Summers were outside the test detection limits. Categories in wild rabbit diet from pine forest areas were found to be similar when comparing Winters to Summers (both in first and second years).

Scrubland Pine ForestCategories Taxa Categories Taxa

Summers Similar (79.2)

Not detected (56.3)

Not detected (74.6)

Similar (69.4)

Winters Similar (87.0)

Different (43.9)

Similar (85.4)

Not detected (59.6)

Summer 02 x Winter 03 (1st year) Different (71.9)

Different (47.0)

Similar (86.3)

Similar (62.2)

Summer 03 x Winter 04 (2nd year) Different (69.2)

Different (36.9)

Similar (78.3)

Different (53.9)

Table 1. Seasonal comparisons of wild rabbit diets in terms of categories and taxa according to habitat. KSI values in brackets.

However, when considering species or genera (taxa) in scrublands, differences were found between Winter diets while values for Summer diets were out of the detection range. Furthermore, significant differences were found when comparing Winters to Summers (both in first and second years). With respect to pine forest areas, no differences were found among Summers and the data referring to Winters were out of the detection range. Taxa in wild rabbit diet were found to be similar when comparing Winters to Summers in the first year, while differences were detected in the second year (Table 1). Taxa described in wild rabbit diet in scrublands differs from those found in pine forest areas throughout the year (Table 2). Similarity is found for major plant groups (categories) in Winter of 2003, while in both Summers significant differences were detected among categories.

Categories Taxa

Summer 02 Different (71.3) Different (36.9)Winter 03 Similar (78.1) Different (36.0)

Summer 03 Different (56.8) Different (32.4) Winter 04 Not detected (74.0) Different (45.4)

Table 2. Comparison of seasonal wild rabbit diet between scrubland and pine forest zones in terms of categories and taxa. KSI values in brackets.

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Scrublands Pine forestSummer

02Winter

03Summer

03Winter

04Summer

02Winter

03Summer

03Winter

04Grass ni 2.0 5.7 12.6 17.1 4.5 0.9 4.1 6.4Glumes ni 2.1 4.6 1.5 0.8Poa sp. 2.2 3.8Holcus lanatus 2.5 0.4 9.2 3.5 5.5Elymus farctus 14.1 1.3 4.7 10.2 7.3 11.8 7.6 23.3Corynephorus canescens 18.4 22.1 21.3 6.0 5.2 1.3 0.7 2.2Agrostis sp. 4.2 10.8 8.5 19.1 7.9 18.6 1.2Ammophila arenaria 5.3 5.0 6.9 1.8 1.2 0.2Vulpia sp. 1.9 1.3 1.4Dactylis glomerata 0.3Avena barbata 4.0 0.7 1.5 0.3Festuca sp. 0.3 13.3Phragmites australis 7.3 2.2

Dicots ni 10.9 12.1 3.8 9.2 27.6 35.4 25.2 23.9

Acacia longifolia 1.7 0.2 4.2 3.7Cytisus grandiflorus 19.7 8.7 23.1 1.7 3.7 2.9 6.9 4.0Ulex europaeus 0.8 1.5 5.8 16.1 2.2 10.7

Lavandula sampaiana 4.3 1.1 4.1 0.5 4.6 2.0Corema album 6.5 2.7Trifolium sp. 8.2 0.3 4.1 3.5 0.6 0.3 7.0Cistus crispus 0.6 0.3 0.5 2.2 1.7Cistus salvifolius 1.1 0.5Halimium sp. 8.5Anthirrhinum majus 1.8 3.1 0.6 0.9Seseli tortosum 1.0Chamaemelium nobile 0.2 1.5 1.6Conyza rouyana 1.0 1.0 1.9

Monocot ni (herb) 1.1

Pinus pinaster 2.7

Cyperacea 18.1 1.0 13.2 2.8Juncus sp. 0.3 9.3 0.5Carex sp. 4.8 1.0 1.1 1.7Carex arenaria 4.8 0.6 0.8Helochares sp. 0.9

Lichens/Fungi 1.5 0.5 1.8 2.6Mosses 0.6 0.3 0.7

Fragment ni 0.4 1.4 0.1 2.6 0.8 1.9 2.8

Table 3. Wild rabbit diet in scrublands and pine forest in terms of taxa (expressed as the percentage of the total area of measured fragments) according to season. ni = not identified.

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Discussion

In Dunas de Mira, Grasses compose the bulk of the wild rabbit diet in accordance with rabbit diets described elsewhere [10,11,13,21]. It is noteworthy that the group of graminoid plants from humid areas is highly consumed when available (Summer), which disagrees with findings reported by Drees & Olff [22] in Dutch dunes, where rabbits show preference for plants of dry areas. This behavioural difference is possibly due to the disparity in climatic conditions between these countries. Rabbits in Portugal must struggle to obtain water, which might lead to the selection of plants from humid areas mostly during Summer, when water is scarce and possibly constitutes a limiting factor.The category of Dicot and Monocot herbs presents the same pattern of consumption on both areas along the years. Considering the overall diet, this is the second most consumed category (average value of 17.7% in scrubland and 33.5% in pine forest). These results are in accordance with Soriguer [11], where Compositae plants represented 30% of the wild rabbit diet.Nitrogen fixing plants are selected differently according to areas and seasons mainly because of the existing variability within this category. In scrublands, C. grandiflorus is the driver of the category whereas Ulex sp. is the main item in pine forest areas (Tables 3). Alves [23] has shown that C. grandiflorus is the preferred Nitrogen fixing shrub in scrublands and that it is scarcer in pine forest areas. When available, this shrub represents a high percentage of the wild rabbit diet. Due to its physical characteristics, especially its juicy stem, it becomes an important water source during Summer as observed in scrublands. On the other hand, the woody Ulex sp. is not selected during Summer when it becomes a dry plant, but rather in late Winter as a green shrub, thus explaining the higher values of this category during Winter season in pine forest areas (Tables 3).The KSI diet analysis clearly reveals distinct feeding strategies adopted by wild rabbits living in scrublands or in pine forest areas. In scrublands, wild rabbit shifts its diet seasonally. This selective and opportunistic behaviour has already been described [10,11,13,16] and it depends on plant availability, development and nutritional value [24]. However, in pine forest areas, the wild rabbit diet does not change so significantly throughout the year. In fact, Summer and Winter diets are similar in both years. This different feeding strategy is certainly related to the lower plant diversity present in pine forest areas, as shown by the absence of five plant species from rabbit diet in pine forest. The KSI values obtained when considering taxa, show that diet changes occurring on pine forest the second year (2003) were mostly due to the high Cyperacea consumption during that Summer. This particular season was exceptionally warm and dry thus forcing the wild rabbit to find plants with high water contents. During Summer, C. grandiflorus percentages in wild rabbit diet, both in pine forest and scrublands areas, represent the highest seasonal values, corroborating the search for water sources in this season. Differences found at taxon level between Winters on scrublands, refer mainly to variation within the category “Graminoids of dry areas”. Food selection in such a fine scale is outside the aims of this study, but it might be associated with a higher availability of plant species within this category, during Winter of 2004.

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Finally, the wild rabbit diet comparisons between areas along seasons highlights the different feeding behaviour in each area. All seasons show significantly different diets between areas at taxon level. This indicates a differential consumption of plant species, mainly according to their availability but also in response to environmental conditions. The same analysis referring to categories showed that Winter 2003 diets were similar. This was, however, an exceptional season in pine forest areas where Dicot and Monocot herbs presented the overall highest percentage constituting a result of particularly difficult interpretation.Despite their great adaptability to the available food resources [10,11], in Dunas de Mira the wild rabbit diet data emphasised preferences towards some food items. Areas with small ponds and shallow lakes with Mediterranean amphibian vegetation are of crucial importance both in pine forest and in scrubland zones and should therefore be preserved as such. Cytisus grandiflorus is a key food resource in scrubland zones and future studies should address the influence of invasive alien species on this important native shrub.

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