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Factors Affecting Seed-Selection in the Hazel Dormouse

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Factors Affecting Seed-Selection in the Hazel Dormouse 1 Acorns were good until tannins were found: factors affecting seed-selection 2 in the hazel dormouse (Muscardinus avellanarius) 3 Leonardo Ancillottoa,b, Giulia Sozioa, Alessio Mortellitiac* 4 5 aDepartment of Biology and Biotechnology “Charles Darwin”, University of Rome “La 6 Sapienza”, Viale dell’Università 32, 00185, Rome Italy. 7 b Wildlife Research Unit, Laboratorio di Ecologia Applicata, Dipartimento di Agraria, 8 Università degli Studi di Napoli Federico II, Portici (Napoli), Italy 9 c Fenner School of Environment and Society, Australian Research Council Centre for 10 Environmental Decisions, National Environmental Research Program, The Australian 11 National University, Canberra, ACT 0200. Phone: T: +610261252737 12 13 *corresponding author: [email protected] 14 15 16 1 17 Abstract 18 Seed selection by forest rodents is based on several factors such as seed palatability, 19 manipulation time and caloric content. The final result of this decision-making process has 20 critical consequences on seed predation and dispersal, and thus on tree demography. 21 Previous studies on seed selection have mainly focused on non-hibernating terrestrial rodents. 22 Arboreal rodents may be less adapted to cope with seed defences, usually being more 23 frugivorous. Furthermore, hibernating species need to accumulate fat reserves in autumn, 24 which is when acorns are available and may be the only available resource. We selected the 25 hazel dormouse (Muscardinus avellanarius, an arboreal hibernating rodent) as model species 26 for our study and focused on three seeds which are an important constituent of the hazel 27 dormouse diet and which are characterized by different defensive strategies. 28 We here report the results of a series of experiments targeted towards understanding the 29 effects of manipulation time, energy intake and tannin content on seed selection by the hazel 30 dormouse and the effects of such selection on individuals' body condition. Each of these 31 factors was treated separately through a series of coupled food trials. Our results showed a 32 clear order of consumption with first choice biased towards seeds with lower tannin content 33 (Q. pubescens vs Q. cerris) and/or more caloric seeds (C. avellana vs Q. pubescens) despite 34 the higher degree of mechanical protection of the former. Seeds with high levels of tannins 35 led to weight decrease, despite the large amounts of seed mass ingested by dormice. Our 36 results suggest that seed selection by the hazel dormouse is targeted towards maximising fat 37 storage, which is pursued despite the cost of higher manipulation time. 38 39 Keywords: diet; food choice, Gliridae; Quercus; rodents; cafeteria experiments. 40 2 41 42 Introduction 43 Tree seeds (e.g. acorns, seeds of oaks of the Quercus genus) are a fundamental resource for 44 wildlife, especially for forest-dwelling rodents. Rodents have crucial effects on tree 45 demography by contributing to seed predation and dispersal (Hulme, 1998; Velho et al., 46 2012). Trees need to balance the benefits of dispersal (Steele et al., 2011) with the negative 47 effects of seed loss due to predation (Steele et al., 2005; Zong et al., 2010). As a consequence, 48 many tree species evolved defence mechanisms in order to manipulate rodents’ behaviour and 49 minimize seed predation. Typical seed anti-predatory adaptations consist in harder or thicker 50 pericarps (Zhang and Zhang, 2008), which prolong manipulation time (Jacobs, 1992), and 51 large seed dimensions, which can discourage a rodent to transport the seed (Muñoz and 52 Bonal, 2008). Both these characteristics decrease predation risk by increasing energetic costs 53 for predators. Chemical secondary compounds too can make seeds less palatable, poisonous 54 or at least poorly digestible (Chung-Maccoubrey et al., 1997; Rubino et al., 2012; Shimada 55 and Saitoh, 2003), thus contributing to discourage predation. Acorns in particular are known 56 to have high levels of tannins (Shimada, 2001), a group of polyphenolic molecules which 57 reduce nutrient absorption (Shimada et al., 2006). 58 Previous studies focused on the interactions between rodents and tree seeds have mainly 59 focused on terrestrial or semi-terrestrial (Buesching et al., 2008) rodents (e.g. Apodemus and 60 Mus spp.) whose diet is based on acorns over extended periods and have thus developed 61 several strategies to cope with high levels of tannins (Molinari et al., 2006; Shimada, 2006; 62 Takahashi and Shimada, 2008; Xiao et al., 2008). Little has been done on arboreal rodents 63 (but see Rubino et al., 2012 and Smallwood and Peters, 1986). Arboreal rodents are more 64 capable than terrestrial rodents of exploiting the above-ground availability of fruit (which 65 decays quickly on ground); however, they may still have to rely on acorns for extended 3 66 periods (Juškaitis, 2008; Moller, 1983). Furthermore, no previous study has focused on 67 hibernating rodents, i.e. species that need to accumulate fat reserves in autumn, which is 68 when acorns are abundant and may be the only available resource. Arboreal hibernating seed 69 consumers are able to consume acorns before they are available to terrestrial species, and 70 may significantly increase their seed consumption before hibernation; therefore they may 71 influence the interactions between trees and seed predators at the community level (Muñoz et 72 al., 2009; Sunyer et al., 2013). 73 For this study we conducted a series of experiments targeted towards understanding factors 74 influencing seed predation by the hazel dormouse (Muscardinus avellanarius, an arboreal 75 hibernating rodent) and the effects of seed selection on individuals’ body condition. We 76 focused on three seed defensive elements, which we expected to affect foraging decisions by 77 the hazel dormice: thickness of pericarp (influencing manipulation time), nutritional 78 composition (directly influencing energy intake) and chemical defences (i.e. tannin content, 79 influencing palatability, digestibility and thus indirectly affecting final energy intake). For 80 this purpose we selected three seeds characterised by contrasting degrees of these defensive 81 characteristics. Specifically we designed our experiments to ask the following research 82 questions: 83 1) What is the effect of seed mechanical defence on seed manipulation time? Answering 84 this question would allow us to quantify the actual time required by hazel dormice to 85 access the resource. We expected manipulation time to be significantly higher for 86 seeds with thicker pericarps. Time spent handling a seed is a relevant trait in the 87 decision-making process by rodents (Wang et al., 2013), thus a quantitative 88 assessment of manipulation time of different seeds is a basic pre-requisite for 89 understanding the process of seed predation. 90 2) Which species (and consequently which seed traits) are preferred by hazel dormice for 4 91 foraging? The ability of rodents to select seeds of different species, e.g. according to 92 their nutritional or chemical content before consuming them is a fundamental factor 93 affecting the rodent-trees interactions (Rosalino et al., 2013). Seed traits such as 94 tannin concentration or pericarp thickness are known to alter seed selection by rodents 95 (Wang et al., 2013; Xiao et al., 2008). As seed biochemical and mechanical defences 96 are subject to a trade-off (Chen et al., 2012), seed predators can specialize to overtake 97 one kind of protection or the other. We thus expected dormice to act a selection 98 towards seeds that maximize energy intake, i.e. seeds with low tannin content, short 99 manipulation time and high caloric content. 100 3) What is the effect of seed selection on the body condition of hazel dormice? Different 101 diets can lead to variation in body conditions in rodents (Shimada and Saitoh, 2003). 102 Seeds with different traits can be unevenly available in woodlands, according to tree 103 species composition, relative abundances and masting events (Focardi et al., 2000; 104 Pons and Pausas, 2007). Assessing how diets based on different seeds affect body 105 condition in rodents, particularly in hibernating species, is an important aspect in 106 understanding the relationships between trees and seed consumers. We expected that 107 seeds selected by dormice would lead to a more efficient fat storage and that a tannin- 108 rich diet lead to a weight decrease. 109 Answering to the three questions listed above will allow us to understand factors affecting 110 foraging decisions by the hazel dormice and contribute to untangling the complex decision- 111 making processes involved in seed predation. Such results may help in providing cues on 112 how to interpret habitat choice, e.g. the different demographic performance of dormice 113 populations in habitat types characterised by different acorn availability (Capizzi et al., 2002; 114 Juškaitis, 2008; Mortelliti et al., 2010; Williams et al., 2013) and thus to improve the accurate 115 parameterisation of distribution modelling (Greaves et al., 2006). 5 116 Materials and methods 117 Choice of the target species 118 We chose the hazel dormouse (Muscardinus avellanarius, a strictly arboreal and hibernating 119 rodent) as target species for our study for three reasons: 1) it is a species of conservation 120 concern which is declining in parts of its range due to habitat loss and degradation, thus a 121 deeper understanding of its foraging ecology will help guiding conservation actions such as 122 habitat management and reintroduction programs (Bright and Morris, 1996; Mortelliti et al., 123 2011) ; 2) the quality of habitat (quality and availability of resources) is a key determinant of 124 its survival and distribution (Mortelliti, 2013). The presence of oaks in fact seems an 125 important factor in determining dormouse presence, at least in the UK, as highlighted by 126 Williams et al. (2013). 3) It has been used as model species for other forest dependent 127 vertebrates due to its life-history and ecological traits (Amici and Battisti, 2009; Bright and 128 Morris, 1996; Greaves et al., 2006; Watts et al., 2010).
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