adaptation of mesocarnivores (mammalia: carnivora) to agricultural landscapes of mediterranean...

In: Middle-Sized Carnivores in Agricultural Landscapes ISBN: 978-1-61122-033-9 Editor: L. M. Rosalino and C. Gheler-Costa, pp. 1-38 © 2011 Nova Science Publishers, Inc.

Chapter 1

ADAPTATION OF MESOCARNIVORES (MAMMALIA:

CARNIVORA) TO AGRICULTURAL LANDSCAPES IN

MEDITERRANEAN EUROPE AND SOUTHEASTERN

BRAZIL: A TROPHIC PERSPECTIVE

Luciano M. Verdade¹, Luis Miguel Rosalino², Carla Gheler-Costa¹, Nuno M. Pedroso² and Maria Carolina Lyra-Jorge1

¹ Laboratório de Ecologia Isotópica, CENA / Universidade de São Paulo, Caixa Postal 96, Piracicaba, SP 13400-970, BRASIL

² Centro de Biologia Ambiental, Faculdade de Ciências da Universidade de Lisboa, Ed. C2, Campo Grande, 1749-016 Lisboa, PORTUGAL

ABSTRACT

The conversion of natural ecosystems into silvo/agriculture systems has been occurring for millennia or centuries throughout our planet. While for many carnivores species this landscape transformation can have negative conservation consequences, for others it could represent a window of opportunity. Therefore, we aimed to review the use of agricultural ecosystems of Mediterranean Europe and Southeastern Brazil by carnivores, as well as how these predators use the surplus of food available in those men-shaped environments. Our review shows that most of these studies were carried out in mono-silvicultural landscapes of Southeastern Brazil and in mixed-agricultural landscapes of Southern Europe. Moreover, while Neotropical species prey more upon small vertebrates, Mediterranean species tend to consume more often invertebrates and fruits. We discuss the possible role of this increase in habitat carrying capacity on the enhancement in numbers of these carnivores in opposition to the mesopredator release hypothesis. We believe that mesocarnivores are adapting to take advantage of a trophic resource enhancement opportunity window created by agro-systems practices, which increase the overall landscape carrying capacity as agriculture is re-shaping the landscape for thousands of years. Finally, we discuss the possible conservation value of agricultural landscapes

Luciano M. Verdade, Luis Miguel Rosalino, Carla Gheler-Costa et al. 2

1. INTRODUCTION Large-sized carnivores experienced massive population declines due to habitat

destruction and human hunting pressure (Crooks, 2002). The former is predominantly associated with agriculture expansion (Marino, 2003), whereas the second is mostly related with livestock depredation (Blanco and Cortés, 2007) and illegal trade of skin or other body parts (e.g., Shepherd and Nijman, 2008). Large home ranges, naturally low population densities and a low intrinsic growth rate make large carnivores more prone to these anthropogenic impacts (Crooks, 2002; Caughey, 1977, 1994). This is the case of large felids such as the tiger (Seidensticker et al., 1999), the African and the Asian lion (Chardonnet, 2002) and the jaguar (Hoogesteijn and Mondolfi, 1992), as well as other large carnivores like the brown bear (e.g., Palomero et al., 1997) and the wolf (Mech, 1970).

There are evidences that the extinction of top predators can have an indirect and negative effect on prey species, by increasing the presence of other smaller predators (Wright et al., 1994; Palomares et al., 1995; Palomares et al., 1996; Crooks and Soulé, 1999; Terborgh, 2000; Gehrt and Clark, 2003), which were no longer subjected to a predatory/competition constrain by larger carnivores. However, this interpretation has been subjected to some criticisms (e.g., Litvaitis and Villafuerte, 1996), and other alternative hypotheses have also been proposed. Some authors have argued that more generalist predators are favoured when natural landscapes are fragmented by agriculture, even in the secular absence of larger predators due to an increase in food resources which they can use (Oehler, 1995; Morán-López et al., 2006; McDougall et al., 2006; Sánchez-Hernandéz et al., 2001; Tabeni and Ojeda, 2005).

Agricultural landscapes are mostly mosaics formed by a matrix of an agroecosystem (the landscape element with a high connectivity whose area exceeds the area of all other elements combined – Forman, 1995) permeated by remnant patches of native vegetation. Agroecosystems are cultivated areas of domestic plant species for economic purposes. The permanence of wild species in agricultural landscapes depends basically on the matrix permeability and on the resources available, both in the agroecosystems and in the remnant patches of native vegetation (Gascón et al., 1999). In general, the displacement of native ecosystems by agriculture affects species composition and consequently the ecosystem structure and functioning (Oehler and Litvaitis, 1996). However, some species – in especial mesocarnivores (intermediate body-size mammalian carnivores – Buskirk and Zielinski, 2003) – apparently benefit from this land use change (e.g., Laurance, 1994; Litvaitis and Villafuerte, 1996; Chiarello, 1999; Gehring and Swihart, 2003; Dotta and Verdade, 2007) due to a possible increase in their food resources (Moguel and Toledo, 1999; Faria et al., 2006; Acharya, 2006).

Agriculture has been developed for the last thousands of years (Diamond, 1997, 2005), affecting not only the spatial structure of the landscape but also inducing temporal heterogeneity (Wiens, 2000). Time scale should then be considered in order to evaluate the effects of agriculture on the patterns of abundance and distribution of biodiversity (Balée, 2006). In this study we review the use of food resources by mesopredators in agricultural landscapes from Mediterranean Europe and Southeastern Brazil, as a way to address adaptive processes of mesopredators to Human changes in the landscapes. Agriculture based on deforestation has been implemented in both regions but in different time scales. In southern

Adaptation of Mesocarnivores… 3

Europe this landscape shaping activities induced by man started some millenniums ago. For example, in the island of Crete (Greece - Eastern Mediterranean) 4000-3000 BC the landscapes nearby the city of Kommos already consisted of a intricate mosaic of cultivated fields and orchards interspersed with semi-natural woodlands (Blondel and Aronson, 1999). In Southeastern Brazil, agriculture transformation started only recently (in the last 200 to 300 years – Dean, 1995). Although such a different time scale could act as a diversion variable, this agricultural transformation of the landscape in both geographical regions have similarities: the type of agriculture, together with its management schemes, implemented in Southern America have a southern European origin, since they were introduced in the New World by European colonial settlers and immigrants. Moreover, ecologically similar species of mesopredators are found in both (Jaksić and Delibes, 1987).

Although sharing a common set of evolutionary features the families herein considered vary considerably in their life history strategies. Felids are highly efficient solitary predators hunting mostly on vertebrate prey by ambush. On the other hand, herpestids and canids developed well structured social systems. Ursids, procyonids and viverrids developed three-climb abilities. However, the former are large-sized omnivores, the intermediate are middle-sized omnivores and the later are middle-sized carnivores. At last, mustelids have a slender body shape with a relatively high metabolic rate and a great variation in body size and food habits (García-Perea et al., 1996; Macdonald, 2001; Nowak, 2005).

2. STUDY AREAS

2.1. Mediterranean Region The Mediterranean region is defined by the Mediterranean Sea basin. It’s delimited by

the Euro-Siberian region to the north (with the Palaeartic deciduous and coniferous forests interspersed with steppes), the Saharo-Arabian in the south (influenced by the Sahara desert) and the Irano-Turanian region on the east, which includes high steppes (Blondel and Aronson, 1999). It is composed by diverse ecosystems, adapted to the transitional regime between cold temperate and dry tropical climates that, in a geological scale, can be considered young due to the relatively recent appearance of a Mediterranean climate (Suc, 1984). This climate, characterized by hot, dry summers and cool humid winters, has one defining trait: unpredictability.

The Mediterranean region’s current biodiversity also comprises species whose core distribution is located in the other biogeographical regions, which led to its inclusion in the list of the world’s 25 biodiversity hotspots for conservation priorities (Myers et al., 2000). This rich species diversity and high number of endemisms are a result of the conjunction action of three factors: biogeography, geology and history (Blondel and Aronson, 1999). Although the first two shaped biodiversity and the species natural history, the long lasting Human history in the region seems to be the most important constraining/facilitating factor. Its continuum contact with the vast land of Eurasia and Africa promoted species contact and interaction with a strong influence on species evolution. In addition, its climatic unpredictability created opportunities for specializations (Blondel and Aronson, 1999). However, the Human factor is a constant since the end of the late Pleistocene, with the region


being the birth place of the largest and most powerful civilizations of the Old World (e.g., Sumerians, Phoenicians, Greeks, Romans, Ottomansand Sarrasins) and the focus of northern invaders (e.g. Vandals and Visigoths), who have impacted ecosystems everywhere in the basin leading some authors to consider that a ‘coevolution’ has shaped the interactions between Mediterranean ecosystems and humans through constantly evolving land use practices (di Castri, 1981 in Blondel, 2006).

Naveh and Dan (1993 in Blondel and Aronson, 1999) suggested that humans have a direct impact in the Mediterranean landscape for at least 50.000 years leading to an intensive landscape redesign. However, the most intense ecosystem transformation occurred 10.000 years ago, when hunters/collectors began the domestication of animals and cultivation of plants to survive. Since then, pastoralists and agriculturalists were responsible for major deforestation and soil erosion (Blondel and Aronson, 1999). Nowadays, agro-silvo-pastoral Mediterranean landscapes include orchards, fruit farms, olive yards (intensive and extensive), cereal fields, pastures for cattle breeding, or production forests (e.g., Eucalyptus and Pinus), among others. Nevertheless remnants of deciduous (e.g., Quercus spp.), conifers (e.g., Pinus spp.) and riverine (e.g., Populus spp.) forests, matorral (e.g., Erica spp., Cistus spp., Arbutus spp.), tomillares and Phyrgana patches (e.g., Thymus spp., Genista spp.), steppes, grasslands and wetlands can still be found throughout the Mediterranean basin (Blondel and Aronson, 1999).

This long lasting landscape shaping has produced intense modifications in the ecosystems with the transformation of native communities, including the extinction or declining of several species (e.g. Brown bear Ursus arctos and Iberian-lynx, Lynx pardinus populations in Portugal, respectively – Cabral et al., 2005), the invasion of some (e.g., Egyptian mongoose Herpestes ichneumon – Delibes, 1982) and the adaptation of others (e.g., Eurasian badger, Meles meles - Rosalino et al. 2005). Many species with high conservation profiles are associated with traditional land uses and with the human-maintained semi-natural habitats, what can be considered extreme cases of adaptation (Sirami et al., 2008). For example, great bustard Otis tarda, a globally threatened species (Alonso et al., 2003), depends greatly on agricultural areas for survival in the Iberian Peninsula (Lane et al, 2001). Other examples of the importance of man-shaped landscapes are the oak forests (cork and holm), typical Mediterranean forests and the major remaining wood-pasture systems of Europe. They represent a sustainable agro-silvo-pastoral system well adapted to the environmental restrictions of the Mediterranean region (low edaphic and climatic potential) (Pinto-Correia, 2000), important to wildlife conservation (Diáz et al., 1997; Cabral et al., 2005), including endangered species such as the polecat (Mustela putorius) (Santos-Reis et al., 1999) and the wildcat (Felis silvestris) (Virgós et al., 2002).

2.2. Southeastern Brazil The Southeast is the most populated and developed region of Brazil. As a consequence,

this region presents the most dramatic environmental problems of this country including a massive deforestation of its major original biomes, the Atlantic Forest and the Cerrado. The former originally covered 12% of the country from 3º S to 31º S, and from 35º W to 60º W, mainly extending along the Brazilian coast (92%), but also reaching into Paraguay (Cartes and Yanosky, 2003; Huang et al., 2007) and Argentina (Giraudo, 2003).


Possibly due to its large latitudinal range, the Atlantic Forest has a high number of endemic species even higher than some parts of the Amazon Forest (Silva and Leitão Filho, 1982; Peixoto and Gentry, 1990; Barros et al., 1991; Joly et al., 1991; Brown Jr. and Brown, 1992). For this reason, the Atlantic Forest is considered prioritary for conservation among tropical forests (Conservation International, 2008a). According to Joly et al. (1991), the Atlantic Forest is composed by three distinct formations: coastal lowland, steep and plateau forests. In Southeastern Brazil the steep forest formation is predominant.

The Cerrado lato sensu varies from savanna to forest formation due to the physical-chemical characteristics of the soil and the frequency of natural fire (Coutinho, 2002; Ruggiero, 2002). Possibly due to its continental location in South America, the Cerrado has a high diversity of fauna and flora including species from the Amazon and the Atlantic forest as well as from the semi-arid Caatinga at its northeast and the Pantanal at its southwest. However, it has a relatively smaller number of endemic species (Durigan et al., 2007).

Both biomes are characterized the typical climate of Southeastern Brazil which varies from humid subtropical (> 1,200 mm, 20ºC in Southern São Paulo) to semi-arid tropical (< 900 mm, 24ºC in Northern Minas Gerais) (Projeto Cactáceas do Brasil, 2010). The Atlantic Forest tends to cover the more humid areas closer to the seashore, whereas the Cerrado tends to cover the drier continental plateau (Huber, 1987).

Although native South Americans used to make slash-and-burn agriculture in areas of the Atlantic Forest, only after the arrival of the first Europeans in the 1,500’s deforestation became dramatic (Dean, 1995). By its turn, the Cerrado used to be predominantly inhabited by native hunters and gatherers and suffered a massive deforestation only in the late 20th Century due to the expansion of agroindustry in Brazil which also affected the remaining parts of the Atlantic Forest (Dean, 1995). As a result, there is currently only 12% of the Atlantic Forest (Ribeiro et al., 2009) and 20% of the Cerrado remaining in Brazil (Conservation International, 2008b).

3. METHODS In this study we reviewed the diet of species of the order Carnivora from the

Mediterranean Europe (six families, 17 species) and the Southeastern Brazil (four families, 21 species), with special reference to mesocarnivores. Reviewed studies were divided into five silvo-agricultural landscapes types: intensive and extensive exotic pasture, mono- and mixed-agriculture and mono-silviculture. We considered mono-cultures those where an agricultural or silvicultural matrix covers at least 75% of the landscape. Mixed-cultures were defined as those below landscape composition percentage (Agnelli and de Marinis, 1995).We calculated the percentage of diet studies implemented in each of the landscapes units considered in our review.

In order to gather prey items presence/absence data on carnivores diet in a systematic approach, we clustered data into 12 food items categories: fruits, other plant materials, microinvertebrates, macroinvertebrates, fish, amphibians, reptiles, passerine- and non-passerine birds, small, middle and large-sized mammals. Again, we calculated the percentage of diet studies mentioning the consumption of these 12 prey items by carnivores in the silvo-agriculture landscapes of Southwestern Brazil (A) and Mediterranean Europe.

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Table 1. Diet and habitat use by Carnivora (Mammalia) in Mediterranean Europe and Southern South America

Taxon Conserv. status

Diet Environments

REGION / Taxon IUCN Fru Opm Ima Imi Fis Amp Rep Apa Anp Msm Mme Mla MAg MSi Mal Pin Pex

SOUTHERN BRAZIL

Felidae

Panthera onca NT 1 2 3

1 2 1 2 3

2 3

1 3 4 5

Puma concolor NT 2 2 2 1 6

2 2 6

1 2 6 7

8 9

6 8 9 10 11 12 13 14 15

16 17

Leopardus pardalis LC 18 19 23

6 20

1 6 8 18 20 21 23 24

8 21 23

9 6 9 10 11 12 13 14 25

22

Puma yagouaroundi LC 10 11

16

Leopardus tigrinus NT 23 23 10 11 14

16

Leopadus weidii LC 26 26 26 21 23 26 16

Canidae


Diet Environments


Chrysocyon brachyurus

NT 27 27 27 6 27

6 27

6 27

27 9 6 9 10 11 13 14 15

27

Cerdocyon thous LC 28 28 28 29

28 28 28 28 28 9 30 31

9 10 11 12 13 14 15 29

28 16

Lycalopex vetulus DD 32 32 32 32 32 14 32

Mustelidae

Eira barbara LC 31 10 11 12 13 14

16

Conepatus semistriatus

LC 9 9 10 11 14 15

Galioctis vittata LC 31 16

Table 1. (continued)


Diet Environments


Galictis cuja LC 9 9 10 11 12 14

Lontra longicaudis DD 33 33 33 33 33 33 33 9 9 10 11 13

33

Ptenoura brasiliensis EN

Procionidae

Procyon cancrivorus LC 27 27 27 27 27 27 27 27 9 31 9 10 11 12 13 14 15

27 16

Nasua nasua LC 9 30 31

9 10 11 12 13 14

16

MEDITERRANEAN

EUROPE

Felidae


Diet Environments


Lynx pardinus CR C2a(i)

135 125 130 131 135

130 131 135

124 125 128 129 130 131 135 21

125 130 131 135

129 133 134

Lynx lynx NT 63A 23 63A

19 20 23 24 178 63A

178

Felis silvestris LC 51 52

75

116 51 52 70 75 82 106

115 116 117 51 52 70 75 82 96 106

70 82

115 116 117 51 52 70 75 82 96 106

115 116 117 51 52 70 75 82 96 106

115 116 117 51 52 70 75 82 106

82 114 51 52 70

Canidae

Canis lupus LR/cd 96 112

68 96 49 50 68 81 99

50 68 99

49 50 73 68 81 99 112

41 50 81

Table 1. (continued)


Diet Environments


Vulpes vulpes LC 43 45 47 48 51 52 54 58 64 65 83 87 90 94 96 100 105 107 124

43 45 54 64 83 87 90 94 100 107

65 89

43 45 47 48 51 52 54 58 64 65 83 87 89 90 94 96 100 105 107 124

90

45 51 52 65 83 90 96 100 107

47 48 58 64 65 83 87 90 94 96 105

45 48 51 52 54 58 64 65 83 87 90 94 96 100 105 107

43 45 47 48 51 52 54 58 64 65 83 90 94 96 100 105 107

43 45 47 48 51 52 58 64 65 83 87 90 94 100 105 124

45 48 58 64 65 83 90 105 107

58

45 51 52 94 105 107 113

Mustelidade

Mustela nivalis LR/lc 67 96 67 67 96

67 67 96

67 96

67 67

Mustela erminea LR/lc 79 158

162 79 162

79 79 44 41 42 43 45

160 79 53 160


Diet Environments


Mustela putorius LR/lc 93 179

93 179

144 184

93 144 145 151 179 184

93 144 179

93 144 179 184

93 144 179 184

93 144 151 179 184

93 144 151 179 184

150 182

93 148 149 152 179 119

Mustela vison LR/lc* 143 143 144

121 126 127 139 143 183 184

121 126 127 139 143 184

121 126 139 143 144 184

121 126 127 139 183

121 126 127 139 143 144 183 184

121 127 139 143 144 183 184

121 126 127 139 143 144 183 184

143 144 184

119

Mustela lutreola EN A1ace 118 121 120 182 119

Martes foina LR/lc 35 40 45 69 78 83 88 104 105 107 108

35 45 78 83 107

35 40 45 69 78 83 104 105 107 108

69 104

35 35 40 45 69 83 104 107 108

35 40 69 83 104 107

35 40 45 69 78 83 104 105 107 108

35 40 45 69 78 83 104 105 107 108

35 40 45 69 78 83 104 105 108

35 45 69 83 107

35 40 69 80 98 104 105 107

Martes martes LR/lc 34 39 55 57 96

39 55

34 39 55 57 96

55 96

34 39 55 96

34 39 55 57 96

55

55

55

Table 1. (Continued)

Taxon Conserv. Status

Diet Environments

REGION / Taxon IUCN Fru Opm Ima Imi Fis Amp Rep Apa Anp Msm Mme Mla MAg MSi Mal Pin Pex Lutra lutra NT 153

154 155 157 165 166 168 171 172 173 174 175 176 177

153 154 155 157 161 163 165 166 168 169 171 172 173 174 175 176 177

96 153 154 155 157 161 163 165 166 168 169 171 172 173 174 175 176 177

153 154 155 157 161 163 165 166 168 169 171 172 173 174 175 176 177

96 153 154 155 157 161 163 165 166 168 169 171 172 173 174 175 176 177

155 157 161 165 166 171 172 173 174 175 177

155 157 161 165 166 168 171 172 173 174 175 177

96 155 157 161 163 165 166 168 173 174 175 176 177

164


Diet Environments

REGION / Taxon IUCN Fru Opm Ima Imi Fis Amp Rep Apa Anp Msm Mme Mla MAg MSi Mal Pin Pex Meles meles LR/lc 36

38 42 47 54 59 66 71 74 76 77 91 95 96 97 101 124

36 54 59 74 76 77 97

36 38 42 47 54 59 66 71 74 76 77 91 95 96 97 101 124

36

36 42 47 66 77 91 95 97 101

36 42 54 59 66 71 77 95 96 97 101

36 47 59 71 77 91 101

36 38 42 59 66 71 74 76 91 95 96 97 101

36 38 42 47 59 66 71 74 76 77 91 95 96 101

36 38 59 66 71 76 77 91 95 97 101 124

36 74 91

36 38 42 47 71 76 101

Ursidade Ursus arctos LR/lc 72 72 72 72 92 Viverridae Genetta genetta LR/lc 37

46 51 52 55 56 60 62 96 102 103 105 109 110

37 55 60 85 86 102

85 86 102 103

37 46 51 52 55 56 60 62 70 85 86 96 102 103 105 109 110 111

46 56 103

46 56 60 85 86 103 110 111

37 46 51 52 55 56 60 62 70 85 86 96 102 103 109 110 111

37 46 56 60 70 102

37 46 51 52 55 56 60 62 70 85 86 96 102 103 105 109 110 111

37 46 51 52 55 56 60 62 70 85 86 96 102 103 105 109 110 111

37 46 51 52 55 56 60 70 86 105 102 103 111

46 55 56 102

46 51 52 55 70 102 103 105

Table 1. (Continued)


Diet Environments


Herpestidae Herpestes ichneumon LR/lc 105 61

63 86

84 86

61 63 85 86 105

63 63 84 85 86

61 63 84 85 86 105

61 84 86 105

61 63 85 105

61 63 84 85 86 105

61 63 84 85 86 105

84 105

Fru: Fruits; Opm: Other plant materials; Ima: Macro invertebrates (> 10g), Imi: Micro invertebrates (< 10g); Fis: Fish; Amp: Amphibians; Rep: Reptiles; Apa: Passerine birds; Anp: Non-passerine birds; Msm: Small-sized mammals (< 500g); Mme: Medium-sized mammals (500 - 5,000g); Mla: Large sized mammals (> 5,000g); MAg: Agricultural monocultures (> 75% of the landscape matrix); MSi (Silvicultural monocultures (> 75% of the landscape matrix); Mal (Mixed agricultural landscapes (< 75% of the landscape matrix); Pin: Intensive exotic pastures (> 75% of the landscape matrix); Pex: Extensive exotic pastures (> 75% of the landscape matrix). 1 Taber et al., 1997; 2 Leite and Galvão, 2002; 3 Crawshaw, 2007; 4 Conforti and Azevedo, 2003; 5 Soisalo and Cavalcanti, 2006; 6 Mantovani, 2001; 7 Hass and Valenzuela, 2002; 8 Mazzolli, 2000; 9 Dotta, 2005; 10 Gargaglioni et al., 1998; 11 Talamoni et al., 2000; 12

Silva, 2002; 13 Tozetti, 2002; 14 Lyra-Jorge et al., 2008; 15 Hulle, 2006; 16 Chiarello, 1999; 17 Mazzolli et al., 2002; 18Sunquist et al., 1989; 19 Murray and Gardner, 1997; 20 Chinchila, 1997; 21 Miranda et al., 2005; 22 Trolle and Kéry, 2003; 23 Wang, 2002; 24 Meza et al., 2002; 25 Lopes and Mantovani, 2005; 26

Azevedo, 1996; 27 Motta-Júnior et al., 1996; 28 Gatti et al., 2006; 29 Beisiegel, 1999;3 0 Gheler-Costa et al., 2002; 31 Briani et al., 2001; 32 Dalponte, 1997; 33

Pardini, 1998;34 Agnelli and de Marinis, 1995; 35 Alegre et al., 1991; 36 Balestrieri et al., 2004; 37 Ballesteros et al., 2000; 38 Barea-Azcón et al., 2001; 39 Bermejo and Guita, 1996; 40 Bertolino and Dore, 1995 ; 41 Blanco and Cortés 2007; 42 Boesi and Biancardi, 2002 ; 43 Boldreghini and Pandolfi, 1991; 44 Bounous et al., 1995 ; 45 Brangi, 1995 ; 46 Calviño et al., 1984; 47 Canova and Rosa, 1993; 48 Cantini, 1991 ; 49 Capitani et al., 2004 ; 50 Carreira and Petrucci-Fonseca, 2000; 51 Carvalho and Gomes, 2001; 52 Carvalho and Gomes, 2004 ; 53 Ceña and Ceña, 2000; 54 Ciampalini and Lovari, 1985; 55

Clevenger, 1995 ; 56 Cugnasse and Riols, 1984; 57 de Marinis and Massetti, 1995; 58 Debernardi et al., 1991 ; 59 del Bove and Isotti, 2001 ; 60 Delibes, 1974; 61 Delibes, 1976; 62 Delibes, 1977; 63 Delibes et al., 1984; 63A Jobin et al., 2000; 64 Fais et al., 1991 ; 65 Fedriani, 1996; 66 Fedriani et al., 1998 ; 67 Fragoso and Santos-Reis, 2000; 68 Gazzola et al., 2005; 69 Gil-Sánchez, 1996; 70 Gil-Sánchez, 1998; 71 Kruuk and de Kock 1981; 72 Lagalisse et al., 2003; 73 Llaneza et al., 2000; 74 Lucherini and Crema 1995; 75 Malo et al., 2004.; 76 Marassi and Biancardi, 2002; 77 Martín et al., 1995; 78 Martinoli and Preatoni 1995 ; 79 Martinoli et al., 2001 ; 80 Masseti, 1995; 81 Mattioli et al., 2004;82 Moleón and Gil-Sánchez, 2003; 83 Padial et al., 2002; 84 Palomares, 1993; 85 Palomares and Delibes, 1991a; 86 Palomares and Delibes, 1991b; 87 Pandolfi and Bonacoscia, 1991 ; 88 Pandolfi et al., 1996 ; 89 Pandolfi et al., 1991 ; 90 Papageorgiou et al., 1988; 91

Pigozzi, 1991; 92 Posillico et al., 2004 ; 93 Prigioni and de Marinis, 1995; 94 Prigioni and Tacchi, 1991; 95 Revilla and Palomares, 2002; 96 Rivera and Rey, 1983 ; 97 Rodríguez and Delibes, 1992; 98 Rondinini and Boitani, 2002; 99 Roque et al., 2001; 100 Rosa et al., 1991; 101 Rosalino et al., 2005; 102 Rosalino and Santos-Reis, 2002; 103 Ruiz-Olmo and López-Martín, 1993; 104 Ruiz-Olmo and Palazon, 1993; 105 Santos et al., 2007; 106 Sarmento, 1996; 107 Serafini and

Lovari, 1993; 108 Such and Calabuig, 2003 ; 109 Torre et al., 2003; 110 Virgós et al., 1996 ; 111 Virgós et al., 1999 ; 112 Vos, 2000; 113 Yom-Tov et al., 2007; 114 Lozano et al., 2003; 115 Aymerich, 1982; 116 Ragni, 1981 ; 117 Gil-Sánchez et al., 1999; 118 Bonesi and Palazon, 2007; 119 Ceña et al., 2003; 120 Bravo and Bueno, 1999; 121 Vidal-Figueroa and Delibes, 1987; 124 Fedriani et al., 1999; 125 Delibes et al., 2000; 126 Bueno and Bravo, 1985; 127 Palazón and Ruiz-Olmo, 1997; 128 Palma, 1980; 129 ICN, 2003 ; 130 Calzada, 2000; 131 Beltrán and Delibes, 1991; 133 Castro and Palma, 1996; 134 Fernández et al., 2006 ; 135 Gil-Sánchez et al., 2006; 136 Stahl et al., 2002 ; 137 Stahl et al., 2001a; 139 Bueno, 1994; 140 Molinari et al., 2001; 143 Bravo, 2002; 144 Lodé, 1999; 145 Lodé, 2000; 148 Marcelli et al., 2003; 149 Rondinini et al., 2006 ; 150 Zabala et al., 2005; 151 Virgós, 2002; 152 Mestre et al., 2007; 153 Clavero et al., 2005 ; 154 Clavero et al., 2006 ; 155 Pedroso and Santos-Reis, 2006; 158 Remonti et al., 2006; 160 Azcón and Duperon, 1999; 161 Sales-Luís et al., (2007); 162 Ruiz-Olmo et al., 1997; 163 Beja, 1991; 164 Bifolchi and Lodé, 2005; 165 Prigioni et al., 2006a; 166 Prigioni et al., 2006b; 168 Clavero et al., 2004; 169 Ruiz-Olmo, 2006; 171 Beja, 1996; 172

Adrián and Moreno, 1986; 173 Adrián and Delibes, 1987 ; 174 Callejo and Delibes, 1987; 175 Ruiz-Olmo et al., 1989 ; 176 Arcá and Prigioni, 1987; 177 Prigioni et al., 1991; 178 Stahl et al., 2001b; 179 Prigioni and De Marinis, 1995; 182 Fournier et al., 2007; 183 Ruiz-Olmo 1987; 184 Lodé 1993.

Luciano M. Verdade¹, Luis Miguel Rosalino², Carla Gheler-Costa 18

While canids (Chrysocyon brachyurus, Cerdocyon thous and Lycalopex vetulus) are the most generalist species in Southeastern Brazil (Figure 2), in the Mediterranean Region mustelids, viverrids and herpestids, share this generalist trophic behavior with canids (Table 1). Large-sized carnivores such as jaguars, pumas and wolves are frequently associated with large-sized livestock depredation (i.e., cattle and sheep). Nevertheless, smaller species can also be associated with small-sized livestock (i.e., chicken and fish) depredation (Table 1) (e.g., Genet consumption of ducks - Rosalino and Santos-Reis, 2002; Eurasian otter consumption of stocked fish – Freitas et al., 2007).

4. DISCUSSION

4.1. Mesopredator Release The present results suggest a possible competition between large- and middle-sized

Carnivora species as both have small-sized mammals as preys. In addition, there seems to be some consumption of middle-sized mammals (including carnivores) by large-sized species in Brazil, and by many species in Europe. In such circumstance the local extinction of top predators could decrease competition for food items concurrently as it also decreases predation pressure over medium-sized carnivores. These two processes combined could result on an increase in the fitness of mesopredators, due mainly to an increment in the natality rate (as a result of higher food resource availability) as well as a decrease on mortality rate as a consequence of absence of top predators. These two aspects corroborate the mesopredator release hypothesis (Wright et al., 1994; Palomares et al., 1995, 1996; Crooks and Soulé, 1999; Terborgh, 2000; Gehrt and Clark, 2003), which was defined by Prugh et al. (2008) as “the expansion in density or distribution, or the change in behavior of a middle-ranked predator, resulting from a decline in the density or distribution of an apex predator”. However, the actual ecological relevance of these aspects is not clear, especially in man-altered and fragmented landscapes. In these environments mesopredator outbreaks can be the result of the disappearing of top predators, due to their need of wider areas, some of which not fragmented, and their higher probability of conflict with man (use of similar resources – e.g. livestock depredation by wolves and jaguars) leading to a higher persecution levels (Prugh et al., 2008). However, fragmentation can also enhance the resources available to mesopredators, especially those directly related with human activities such as pet food, crops and crop pests.

4.1. Increase in Carrying Capacity Some evidences of the increase food availability in agro-forest systems are already

available. For example, Silva et al. (2008) showed that agricultural units of a Mediterranean cork-oak landscape recorded the highest abundance and richness levels of ground beetles, which are regularly included in the diet of southern European mesocarnivores (e.g., Rosalino et al., 2005; Santos et al., 2007). Moreover, in southeastern Brazil, sugarcane plantations also support higher densities of rodents than pristine landscapes (Gheler-Costa, 2006). Such


rodents are an important resource for many carnivores (Rocha et al., 2004; Tófoli et al., 2009). Furthermore, the simple existence of agricultural patches, specially those devoted to fruit production, increase the environmental carrying capacity, in particular to those species highly adaptable in using fruits as a trophic resource, often highly energetic (e.g., olives). For example, a study reviewing fruit consumption by carnivores in Mediterranean Europe showed that more than 20% of fruits eaten by predators such as the red fox, stone marten, pine marten, Eurasian badger and the common genet where originated in orchard or fruit trees plantations (e.g., grapevine Vitis vinifera, loquats Eriobotrya japonica, persimmon Diospyros sp.) (Rosalino and Santos-Reis, 2009).

These evidences seem to point out that human altered landscapes (by agriculture or forestry) can be an important food source for more generalist species per se, allowing more foraging opportunities, due to higher trophic resources availability (increasing the landscape carrying capacity), even in the presence of top predators, when comparing with some type of more natural habitats. Actually, the simple fact that most of the studied species use, at least, one type of agro/forest system (see figure 1) seems to indicate that they are using available resources present in those areas, most likely as surplus of food resources. This ecological adaptation can develop in short/medium time scale, with species starting to use new resources made available by human activities. For example, since the beginning of the 1980’ fish farming has been implemented as an important industry in Portuguese estuaries, producing fish species which are not naturally abundant in those areas (Freitas et al., 2007). Recent studies have determined that 60% of prey consumed by otters in fish farming areas are produced marine fish species (Freitas et al., 2007), and that fish farms had a 76% visiting rate by otters, indicating that otters are using a surplus food resource, nowadays highly available, but probably less common 30 years ago.

We thus believe that mesocarnivores are adapting to take advantage of a trophic resource enhancement opportunity window created by agro-systems practices, which increase the overall landscape carrying capacity, some of which are shaping the landscape for thousands of years (e.g., Mediterranean Region) (Pinto-Correia and Vos ,2004).

4.3. Conservation Value of Agricultural Landscapes It is possible and necessary to promote good management practice that allows a balanced

promotion of biodiversity and maintenance of production, integrating conservation with production objectives. This can be achieved through several approaches. For example, the main problem when dealing with monocultures is the habitat homogeneity. Maintaining landscape connectivity is difficult when dealing with agricultural landscapes, especially in intensive management schemes. The presence of water courses (rivers and streams) with riparian vegetation, constitute areas of high biodiversity (Naiman et al., 2005), including not only typical aquatic species (e.g. Eurasian otter and European mink in Europe; neotropical otter in Brasil), but also more terrestrial carnivores that use these corridors as refuge, access to prey (e.g. fish, crayfish, birds), routes for juvenil dispersion, and often as the only habitats that enable successful reproduction in a intensive agriculture landscape (e.g., Virgós, 2001; Matos et al., 2009). Therefore, the maintenance of an ecological flow and improvement of the riparian vegetation in this water courses constitute an important contribute to improve biodiversity. The example of the legal obligation regarding maintaining buffers of vegetation


(30m) along the water courses in Brazil is, therefore, one to maintain and promote (Metzger et al., 2010).

Another example is based on the fact that ecological corridors can be accomplished by the conservation or reimplementation of patches of adequate habitat for certain species, or species guilds. This can be achieved by maintaining or creating hedges or walls for smaller carnivores (Macdonald et al. 2007), or larger patches of favorable habitat for all carnivores, in general. Traditionally, hedgerows are part of agricultural landscape in Europe, as well as a cultural element of the landscape structure and diversity. Therefore, these structures may act as important commuting and hunting routes, allowing the survival of some species which use these areas as refuges while feeding on the contiguous agricultural fields. In some cases the fields' boundary areas comprise the most species-rich prey community (Tattersall et al., 2002) resulting in ideal hunting grounds for carnivores, where protective cover is associated to higher prey density. Often, these corridors do not have to be prime habitats. Regarding the Iberian lynx, a species considered highly specialist in habitat requirements (and prey), Palomares et al. (1991) stated that these corridors can even support moderate habitat degradation due to human activity. However, this species uses mixed landscapes, with Mediterranean woods and scrubland, and avoids intensive plantations and agriculture (Rodríguez and Delibes, 1990).

Agricultural landscapes are also commonly used as grazing pastures. The establishment of areas without pasture, mainly in extensive exploration schemes, allows the growth of grasslands and scrubland mosaic, which could promote some prey species availability (e.g., wild rabbit – Monzón et al., 2004), and consequently be used by several carnivore species that exploit those food resources (Verdú et al., 2000; Ferrer and Negro, 2004).

The importance of this mosaic is well expressed in the Iberian cork and oak woodland (Quercus suber and Quercus rotundifolia), the “montado” in Portugal and “Dehesa” in Spain. These are mixed farming landscapes around extensive woodlands, interspersed with patches of scrubland, grassland and cultivated fields. The montado/dehesa is one of the best examples for the balance between biodiversity and human activity (Pinto-Correia and Vos, 2004), providing both economic value (from the extensive cattle raising, the cork extraction of the Q. suber, mushrooms collecting, ecotourism) and natural value (which encompass a wide range of carnivores, including the wildcat, polecat, genet, stone marten and Iberian lynx).

Another important aspect regarding increasing carrying capacity for biodiversity is the presence of small and medium-sized water reservoirs. These aquatic systems, common in the Mediterranean region, where river flows are irregular and many dry out during summer, constitute a water source for cattle and, sometimes, irrigation for agriculture. The role of these systems in the ecology and conservation of carnivores is still somewhat unknown. However, it is obvious that they constitute resources for mammalian carnivores (among others), namely water and prey availability. For example, Basto et al. (in press) detected that the abundance of American crayfish (Procambarus clarkii) was one of the most important variables positively associated with the Eurasian otter’s use of these smaller reservoirs. Moreover, in more open agriculture landscapes, such as arable steppes or pasturelands, the vegetation developing in these reservoirs margins can also provide some refuge for mesocarnivores. The positive association of the reservoirs’ use with the availability of refuges was already referred in other studies (e.g. Elliot, 1983; Prenda et al., 2001). Ideally, the maintenance or creation of these water bodies, usually associated with livestock production, should be accompanied by a moderate/low use by cattle, which is rather difficult. Higher cattle pressure promotes a high


disturbance around the reservoir and reduces cover, and consequently refuges, for carnivore species.

Conservation of pristine habitats, still occurring in agriculture landscapes, is also an important way of ensuring the maintenance of biodiversity in these human altered habitats, especially because they can offer protective cover which is often lacking in the agricultural fields. Most of these patches remain in the agricultural landscape due to difficulty of implementing agriculture practices in those terrains. Valleys and steep slopes are among these areas. However, they have been greatly reduced in the last decades (Tscharntke et al., 2005), maybe due to the increase of machinery capability and pressure for soil use.

Presently, in some countries where intensive agriculture has led to an alarming level of ecological degradation, an increasing number of efforts are now being made to restore agricultural landscapes and enhance biodiversity by implementing agro-environmental programs, such as introducing semi-natural habitats and field margins into farmland (Jeanneret et al., 2003).

4.4. Adaptive Processes of Mesopredators to Agricultural Landscapes Time in evolutionary processes should be counted in number of generations of the

population in question and not in years (Simpson, 1949). In addition, genetic adaptive changes tend to be faster in changing environments (Levins, 1968). Alterations in food resources availability and spatial-temporal heterogeneity tend to act as selection forces towards individuals. On a single generation time scale, individuals tend to respond to such alterations by behavioural changes (Tuyttens and Macdonald, 2000) which can be called “acclamation”. Individuals’ success in such circumstance depends basically upon their phenotypic plasticity (Relya, 2004). On the other hand, along a certain number of generations a population tends to respond to environmental changes by genetic changes (Dobzhansky, 1970). Populations’ success in such circumstance depends basically upon their genetic variability (Sinclair et al., 2006). Both acclamation and adaptation to agricultural landscapes should involve changes in two basic behavioural-ecological processes: feeding ecology and use of space. The former is related to changes in food resources availability whereas the later is related to the land use change in spatial terms where, for instance, shelters quality and availability may alter. Mesocarnivores seem extremely plastic both in terms of diet and space use. The present results (high number of generalist species in both European and South American carnivore guilds) corroborate the former whereas their apparently higher abundance in agricultural landscapes (e.g., Dotta and Verdade, 2007) corroborates the later. The extinction or absence of top predators – usual in agricultural landscapes – may potentiate these characteristics. The present results suggest that mesocarnivores may benefit from agricultural landscapes: directly by the increase in the abundance of fruits (Rosalino et al., 2009) or indirectly by the increase in the abundance of seeds or green matter (plant biomass) and consequent increase in rodents’ abundance (Gheler-Costa, 2006). Systematized studies about the use of space by mesocarnivores in agricultural landscapes should be prioritized as information about it is still scarce. We need to better understand the possible impact of land shaping mechanisms associated with Human activities (e.g. agro-environmental schemes, habitat management) in order to promote the increase of conservation value of agricultural landscapes, namely regarding carnivores.


4.5. Possible Ecological Imbalances and the Domestication of Nature The extinction of top predators and consequent “mesopredator release” has been

considered to result on an increase in bird predation and their consequent population decline (e.g., Soulé et al., 1988; Crooks and Soulé, 1999; Galetti et al., 2009). Although the present results indicate a consistent consumption of birds by middle-sized carnivores there is no evidence that this consumption is higher in agricultural landscapes and/or in the absence of top predators. However, in general these studies are based on short-term surveys where both dependent and independent variables are circumscribed on a smashed time frame. Thus, there is not enough information available about the possible consequences of mesopredator release on a long-term basis. Middle-sized carnivores are also considered as reservoir for pathogens that can cause diseases in domestic carnivores (i.e., dogs and cats) as well as in humans (Whiteman et al., 2007). There seems to be indeed a lot of contact between domestic and wild carnivores (e.g., predation, physical contact with urine and feces etc, hybridization) (Oliveira et al., 2008). It is possible that such contact increase in the absence of top predator as they prey on both domestic and wild smaller carnivores. However, in this case domestic animals should be excluded from conservation units and even from unprotected natural areas as they compete with wild carnivores for food resources (Lepczyk et al., 2003; Bonnaud et al., 2007; Campos et al., 2007). As small-sized carnivores adapt to anthropogenic environments we might expect a certain process of domestication occurring in agricultural landscapes. The concept of domestic or domesticated nature depends on the human perception of nature (Descola, 1986). However, no matter how subjective the concept of nature and natural can be, the fact that small-sized carnivores may depend on anthropogenic habitats to succeed may become their – and ours - most complex conservation problem.

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