Behavioural Processes 103 (2014) 28–34

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Why do cervids feed on aquatic vegetation? Francisco Ceacero a,∗ , Tomás Landete-Castillejos b,c,d , María Miranda e , Andrés J. García b,c,d , Alberto Martínez f , Laureano Gallego b,c a Department of Animal Science and Food Processing, Faculty of Tropical AgriSciences, Czech University of Life Sciences, Kam´ ycka 129, 165 21 Prague 6, Suchdol, Czech Republic b Departamento de Ciencia y Tecnología Agroforestal y Genética, Universidad de Castilla-La Mancha (UCLM), 02071 Albacete, Spain c Animal Science Tech. Applied to Wildlife Management Res. Group, IREC Sec. Albacete (UCLM-CSIC-JCCM), 02071 Albacete, Spain d Sección de Recursos Cinegéticos y Ganaderos, Instituto de Desarrollo Regional (IDR), Universidad de Castilla-La Mancha (UCLM), 02071 Albacete, Spain e Centre for African Ecology, School of Animal, Plant & Environmental Sciences, University of the Witwatersrand, Private Bag 3, Wits 2050, South Africa f Laboratorio de Ciencia e Ingeniería de Materiales (CIMA), Instituto de Desarrollo Regional (IDR), Universidad de Castilla-La Mancha (UCLM), 02071 Albacete, Spain

a r t i c l e

i n f o

Article history: Received 8 March 2013 Received in revised form 12 October 2013 Accepted 27 October 2013 Available online 9 November 2013 Keywords: Aquatic vegetation Diet seasonality Minerals Protein Red deer Sodium

a b s t r a c t Consumption of aquatic plants is rare among cervids, despite the common occurrence of this form of vegetation. However, the paucity of literature reporting on this feeding behaviour suggests that Na (but also other minerals), protein, and the ubiquitous availability of aquatic vegetation may play a role in its consumption. We present results quantifying those factors that regulate the consumption of aquatic plants in the Iberian red deer. We focussed our study primarily on two questions: (i) what nutritional values are red deer seeking in the aquatic plants?; and (ii) why do red deer primarily use aquatic plants during the summer? A comparison of the seasonal variations in Na content between terrestrial vs. aquatic vegetation did not fully support the hypothesis that aquatic plants are being consumed more in summer because of any seasonal variation in Na availability. The Na content in the aquatic vegetation was adequate all the year-round; whereas, the Na content in the terrestrial vegetation was consistently deficient. However, a greater summer content of essential minerals and protein in the aquatic vegetation may be the cause for their consumption exclusively during the summer. We suggest that seasonal variations in the consumption of aquatic vegetation by cervids is primarily driven by temporal variations in the nutrient content, combined with seasonal variations in the physiological demands for these nutrients. © 2013 Elsevier B.V. All rights reserved.

1. Introduction Aquatic vegetation is a nutritional resource with high levels of minerals and protein, but a low fibre content (Gortner, 1934; Linn et al., 1975). It is used by a wide range of herbivores (from invertebrates to mammals; Lodge, 1991), including several species of cervids (Nowak, 1999). During the 1970s and 1980s, great interest in the use of aquatic plants by Alces americanus arose (Botkin et al., 1973; Jordan et al., 1973; Belovsky, 1978; Fraser et al., 1980, 1982, 1984; Belovsky and Jordan, 1981; reviewed by Jordan, 1987). Thereafter, aquatic vegetation has scarcely been considered

∗ Corresponding author at: Faculty of Tropical AgriSciences, Czech University of ´ 129, 165 21 Prague 6, Suchdol, Czech Republic. Life Sciences, Kamycka Tel.: +420 733450473. E-mail addresses: [email protected] (F. Ceacero), [email protected] (T. Landete-Castillejos), [email protected] (M. Miranda), [email protected] (A.J. García), [email protected] (A. Martínez), [email protected] (L. Gallego). 0376-6357/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.beproc.2013.10.008

in studies on the diet selection of cervids, even if this behaviour was repeatedly been recorded (usually only as a curiosity) for several other species such as: Alces alces, Blastocerus dichotomus, Ozotozeros bezoarticus, Odocoileus hemionus, Odocoileus virginianus, Dama dama, Elaphurus davidianus, Rucervus duvaucelii, and Hydropotes inermis (Nowak, 1999; Table 1). Similarly, the consumption of seaweeds has been reported in some cervids (Table 1). Thus, most of the better studied cervids have been reported to use aquatic vegetation to some extent, and therefore, the consumption of aquatic vegetation might also be expected in other cervids in which only a few (or no) studies on their diets have been conducted (e.g., Mazama, Axis, Elaphodus, or Muntiacus genera), since most of them inhabit marshy habitats (Nowak, 1999) where aquatic plants comprise a significant portion of the vegetation available. For the European red deer (Cervus elaphus), the review by Gebert and Verheyden-Tixier (2001) did not include any reference to the consumption of aquatic vegetation, only a mention of the consumption of seaweeds on Rhum Island (Clutton-Brock et al., 1982; Conradt, 2000). On the Iberian Peninsula, this behaviour has been reported from the Salburua Wetland Protected Area in North Spain

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Table 1 Published records of consumption of aquatic-marshy vegetation or seaweeds by cervid species. Species

Aquatic plants in diet

Location

Latitudea

Season

Proposed hypotheses?

Reference

Alces alces

Aquatic vegetation

59–60◦ N (HL)

Summer



Faber et al. (1988)

Alces americanus

Aquatic vegetation

Grimsö Wildlife Research Area (Sweden) Isle Royal (Michigan, USA)

47–48◦ N (HL)

Spring–Summer

‘Na’

Aquatic vegetation

Cooke Lake (Ontario, USA)

48◦ N (HL)

Summer

Aquatic vegetation

Copper River Delta (Alaska, USA)

62◦ N (HL)

All year

Aquatic vegetation

Pantanal wetland (Brazil) Pantanal Natural Reserve (Brazil) Southern Vancouver Island (British Columbia, Canada) Queen Charlotte Islands (British Columbia, Canada) Tsongas National Forest (Alaska, USA) San Juan Island (Washington, USA) Bodega Bay (California, USA) Southern Alaska (USA) Upper and Lower Peninsula (Michigan, USA) Tree Islands Everglades (Florida, USA) Pantanal Natural Reserve (Brazil) Nhumirim (Brazil)

19◦ S (T-ST)

All year

‘Na’ + ‘Essential minerals’ (P, Mn, Fe, Ca) + ‘Protein’ ‘Protein’ + Supplement under food restriction –

Belovsky (1978), Belovsky and Jordan (1981), and Franzmann and Schwartz (1997) Fraser et al. (1980, 1982, 1984)

16–17◦ S (T-ST)

All year



48◦ N (HL)

All year

Supplement under food restriction + ‘Availability’

McTaggart (1945)

51–54◦ N (HL)





Carlton and Hodder (2003)

56◦ N (HL)





Carlton and Hodder (2003)

48◦ N (HL)





38◦ N (HL)









45–46 N (HL)



‘Essential minerals’ (I)

Carlton and Hodder (2003) Carlton and Hodder (2003) O’Clair and O’Clair (1998) Watkins and Ullrey (1983)

25◦ N (T-ST)

All year



Labisky et al. (2003)

16–17◦ S (T-ST)

All year



Costa et al. (2006)

19 S (T-ST)

All year



South Georgia Island Svalbard (Norway)

53–54◦ S (HL)

All year

79◦ N (HL)

Late winter

Cambodia

10–14◦ N (T-TS)

Rainy season

Supplement under food restriction Supplement under food restriction ‘Availability’

38 N (HL)





Desbiez et al. (2011) Leader-Williams (1988) Hansen and Aanes (2012) Timmins et al. (2012) Azorit et al. (2012)

42◦ N (HL)





56–57◦ N (HL)

Winter



42–45 N (HL)

All year

Supplement under food restriction ‘Na’

42–45◦ N (HL)



‘Na’

Aramilev (2009)

38◦ N (HL)





Azorit et al. (2012)



Summer



Nowak (1999)

28◦ N (T-ST)

All year

Moe (1994)

25–26◦ N (T-ST)

All year

‘Na’ + ‘Essential minerals’ (K, Ca, Mg) –

Rainy season

‘Availability’

Blastoceros dichotomous

Marshy vegetation Odocoileus hemionus

Aquatic vegetation

Seaweeds

Seaweeds

Seaweeds Seaweeds Seaweeds Odocoileus virginianus

Aquatic vegetation

Marshy and aquatic vegetation Ozotoceros bezoarticus

Marshy vegetation Marshy vegetation

Rangifer tarandus

Seaweeds Seaweeds

Axis porcinus Cervus elaphus

Aquatic vegetation (rice) Aquatic vegetation

Marshy vegetation Seaweeds Cervus nippon

Seaweeds Aquatic vegetation

Dama dama

Aquatic vegetation

Elaphurus davidianus Rucervus duvaucelii

Aquatic vegetation Aquatic vegetation

Aquatic vegetation Rucervus eldii

Aquatic vegetation (rice)

Sierra de Andújar Natural Park (Spain) Salburua Protected Area (Spain) Isle of Rum (Scotland, UK) Primorsky Krai (Russia) Primorsky Krai (Russia) Sierra de Andújar Natural Park (Spain) – Royal Bardia National Park (Nepal) Assam (India) Chatthin Wildlife Sanctuary (Myanmar)









23 N (T-ST)

MacCracken et al. (1993) Tomas and Salis (2000) Costa et al. (2006)

Lobo-Urrutia (2008) Conradt (2000) Makovkin (1999)

Qureshi et al. (1994) McShea et al. (2001)

30

F. Ceacero et al. / Behavioural Processes 103 (2014) 28–34

Table 1 (Continued) Species

Aquatic plants in diet

Location

Latitudea

Season

Proposed hypotheses?

Reference

Rusa timorensis Hydropotes inermis

Seaweeds Marshy vegetation

– –

– –

– All year

– –

Nowak (1999) Nowak (1999)

In all the table: dashes indicate information not provided in the bibliographic source. a Latitudinal regions are indicated in brackets: T-ST indicates tropical and subtropical areas (2 seasons); HL indicates temperate and boreal areas (4 seasons).

(Lobo-Urrutia, 2008) as well as from Sierra de Andújar in SouthEastern Spain (Azorit et al., 2012). This behaviour is also well known among game managers, and has been filmed in the wild from late spring to early autumn (also in Sierra de Andújar; SW Spain: ‘Tesoro del Sur’ – Avatar Producciones, and LM Dominguez, pers. comm., or search for the video ‘ciervos comiendo algas’ on the Internet). Thus, feeding on aquatic vegetation seems to be a rarely studied, but common behaviour in the red deer, at least in the Iberian subspecies (C. e. hispanicus). Several explanations have been suggested for the use of aquatic vegetation by cervids; all them hypothesising that aquatic plants are used as a source of minerals and nutrients (particularly Na; but also Ca, P, K, Mg, Fe, Mn, I, and protein). McTaggart (1945) initially reported avid consumption of aquatic vegetation by O. hemionus all year-round, in proportion to its availability (‘availability hypothesis’). Afterwards, it was suggested that aquatic vegetation is consumed by cervids because it constitutes a Na-rich complement to their terrestrial diet (‘Na-hypothesis’; Belovsky, 1978; Fraser et al., 1982). Other minerals (‘essential minerals hypothesis’; Fraser et al., 1980, 1984; Watkins and Ullrey, 1983; Moe, 1994) and organic components (‘protein hypothesis’; MacCracken et al., 1993) have also been proposed as potential drivers. Most of the studies have principally reported the consumption of aquatic vegetation by cervids during the summer in high latitudes, but year-round in tropical and subtropical regions (Table 1). Those few instances when winter feeding on aquatic vegetation or seaweeds was reported in high latitude temperate forests, it was suggested to be used as a supplement after a temporal restriction in food availability. Therefore, it appears that seasonal variations in the physiological requirements for nutrients could potentially drive the consumption of aquatic vegetation. This ‘seasonally increased requirements hypothesis’ (‘synchronization of life cycles with good food availability’ after White, 1993) is not mutually exclusive with the previous hypothesis regarding the potential nutritional benefits in the aquatic vegetation. To date, exhaustive studies on the use of aquatic vegetation have been restricted to the moose; and even for this well-studied species the results are controversial. In this study we aimed to expand the literature on this topic with a study on the Iberian red deer. We specifically aimed at: (i) evaluating which compounds the red deer are seeking in the aquatic vegetation by comparing the protein, Na, and other mineral contents in both the aquatic and terrestrial vegetation; and (ii) evaluating if seasonal variations in the utilisation of aquatic vegetation are related to seasonal variations in the nutrient contents of the aquatic and terrestrial plants. 2. Materials and methods The aquatic vegetation was collected in two semi-natural ponds, frequently used by red deer. The two study sites are located near Sierra de Andújar (Andalusia, southern Spain), where the consumption of aquatic plants had been previously filmed and reported in faecal samples (Azorit et al., 2012). We also collected (in areas adjacent to the ponds) samples of the most abundant terrestrial plant species, which have previously been found in the diets of red deer in similar habitats (Rodríguez-Berrocal, 1978; Caballero, 1985; Palacios et al., 1989; García-González and Cuartas, 1992;

Soriguer et al., 1994; Alvarez, 1999; Patón et al., 1999; Bugalho and Milne, 2003; Fernández-Olalla et al., 2006; Estévez et al., 2009; Torres-Porras et al., 2010; Olguín, 2011). One of the study sites, ‘Aldeaquemada’ (AL; 38.3◦ N, 3.4◦ W), was seasonally sampled (mid-spring in April, mid-summer in July, mid-autumn in October, and mid-winter in January). The second location, ‘Centenillo’ (CE; 38.3◦ N, 3.7◦ W) was only sampled in mid-summer. The terrestrial species collected at AL were: Quercus suber, Quercus coccifera, Juniperus oxycedrus, Asphodelus sp., Cistus ladanifer, Thymus vulgaris, Phillyrea angustifolia, Rosmarinus officinalis, Daphne gnidium, and a mixture of herbs; the aquatic species collected were: Nitella flexilis, Myriophyllum alterniflorum, and Chara sp. The terrestrial species collected at CE were: R. officinalis, Quercus ilex, C. ladanifer, P. angustifolia, Q. coccifera, Viburnum tinus, Q. suber, Pistacia terebinthus, Olea europaea, Pistacia lentiscus, Brachypodium sp., Avena fatua, and a mixture of herbs; the aquatic species collected were: Lemna gibba, Lemna minor, Callitriche brutia and Rannunculus peltatus. Acorns (with a balanced mixture of oak species present in each location) were also collected when available, as these are an important component of the red deer diet in autumn (Rodríguez-Berrocal, 1978; Azorit et al., 2012). Each plant species studied was sampled in 10 randomly selected plots, in order to get a representative sample (in a radius of 100 m around the ponds for terrestrial vegetation; inside the pond for aquatics); finally, samples of the same species were pooled together for further nutritional analyses. Only the leaves and stems were collected, as these are the parts preferred by red deer (Minson, 1990). The leaves were washed (see Muztar et al., 1978), removed from the branches, air-dried for 2 days in paper bags, and oven-dried at 85 ◦ C for 72 h. Thereafter, the material was ground and stored in sterile and hermetically-sealed bags for further analyses. Crude protein was determined by the Kjeldahl method by a specialised agricultural laboratory (Laboratorio Agrario Regional, Albacete, Spain). Chemical content analyses (see Estévez et al., 2009, 2010, for a detailed explanation of the analytical procedures) were conducted for both macro-minerals (Ca, Mg, P, Na, K, and S) and microminerals (Cu, Fe, Mn, Se, Co, and Zn) in samples of 0.500 g ± 0.001 g (weighed on a GramTM SR-410M scale, Barcelona, Spain). The samples were dissolved with an acid solution (32% HNO3 , 12% HCl, 6% HF, and 50% H2 O). A second wet digestion was carried out in a microwave oven (Perkin-Elmer Multiwave 3000, Boston, USA) under 345 kPa for 30 min. Subsequently, the samples were analysed with an atomic absorption spectrophotometer, Optima 5300 DV (Perkin-Elmer ICP-OES, Boston, USA). Results for the macrominerals are expressed in percentages, whilst the micro-minerals are expressed in ppm. Non-parametric U Mann–Whitney analyses were performed to test for differences in nutritional contents between the available terrestrial and aquatic vegetation in each location and season. The analyses were performed using SPSS 20.0 for Windows (SPSS, Chicago, IL, USA). Red deer diets are not balanced for the studied plant species; furthermore, not for the percentages of grazing and browsing changes among the seasons. In order to show more accurate information about the potential benefits of aquatic vegetation, we estimated the botanical composition of red deer diet in each study site by consulting the available literature for the Southern Iberian Peninsula (areas with similar species composition and availability;

*

**

**

**

**

**

**

**

**

**

**

*

1.19 2.36 0.41 0.65 0.29 0.38 11.65 13.29 1827 5607 8.46 48 16.2 †

**

**

**

**

**



1.03 2.11 0.26 0.51 0.20 0.32 11.60 12.74 798 263 0.16 57 16.7 †

*

*

*

*

*

*

1.67 1.67 0.26 0.65 0.11 0.21 8.44 6.83 1306 434 0.00 38 15.1 **

**

**

**

**

**

**

**





0.84 0.99 0.18 0.03 0.11 0.11 0.39 7.11 48 33 1.11 31 9.8 *

1.39 0.89 0.23 0.68 0.12 0.36 9.08 12.64 1885 316 0.00 42 13.4 **

**

**

**

**

*



0.73 0.62 0.17 0.01 0.07 0.10 1.15 5.47 40 24 0.51 30 6.5 1.17 2.30 0.34 0.50 0.17 0.24 12.25 10.22 910 274 0.28 53 10.6

**

Significance at 0.1. Significance at 0.05. Significance at 0.01. *



Ca (%) K (%) Mg (%) Na (%) P (%) S (%) Co (ppm) Cu (ppm) Fe (ppm) Mn (ppm) Se (ppm) Zn (ppm) Protein (%)

0.30 0.60 0.15 0.06 0.25 0.10 0.10 4.00 30.0 20.0 0.10 25.0

0.89 1.13 0.19 0.02 0.15 0.18 1.43 9.09 71 32 0.73 47 10.6

± ± ± ± ± ± ± ± ± ± ± ± ±

0.24 0.60 0.03 0.02 0.08 0.06 0.40 3.29 70 31 0.06 20 2.3

Aq

± ± ± ± ± ± ± ± ± ± ± ± ±

0.20 0.46 0.10 0.10 0.00 0.02 0.35 0.69 221 51 0.23 3 0.5

P

± ± ± ± ± ± ± ± ± ± ± ± ± Te Te

0.34 0.19 0.05 0.01 0.02 0.03 0.34 1.71 28 22 0.25 16 1.6

Aq

± ± ± ± ± ± ± ± ± ± ± ± ±

0.29 0.05 0.01 0.09 0.04 0.01 0.14 1.22 180 10 0.00 1 0.5

P

Te

± ± ± ± ± ± ± ± ± ± ± ± ±

0.57 0.50 0.08 0.06 0.05 0.04 0.58 2.00 66 50 1.82 13 3.9

Aq

± ± ± ± ± ± ± ± ± ± ± ± ±

0.2 0.5 0.00 0.10 0.02 0.02 1.43 1.09 313 149 0.00 4 1.6

*

0.81 1.18 0.18 0.03 0.17 0.18 0.86 8.84 30 30 0.66 43 10.4

P

Te

± ± ± ± ± ± ± ± ± ± ± ± ±

0.19 1.03 0.06 0.06 0.13 0.07 0.27 4.06 17 32 0.15 21 4.0

Aq

± ± ± ± ± ± ± ± ± ± ± ± ±

0.36 0.86 0.01 0.15 0.07 0.01 2.59 0.83 267 85 0.13 4 1.6

**

0.73 0.89 0.17 0.01 0.13 0.15 0.04 7.11 139 160 7.55 25 10.0

Te

± ± ± ± ± ± ± ± ± ± ± ± ±

0.41 0.30 0.07 0.00 0.04 0.04 0.11 2.10 65 263 2.35 8 3.0

Aq

± ± ± ± ± ± ± ± ± ± ± ± ±

0.20 0.46 0.08 0.23 0.02 0.10 6.19 2.71 873 2699 3.49 5 2.9

P

31

P

CE-summer AL-winter AL-autumn AL-summer

Aquatic vegetation showed greater mineral contents than did the terrestrial vegetation used by red deer in our studied locations, and the differences were greatest (and included more minerals) in summer than during the rest of the year (Table 2 for this and the following results). Only P and Na were under deficiency levels (following McDowell, 2003) in the terrestrial vegetation within our studied locations. This was also true for the P content in aquatic vegetation; while Na content in aquatic plants was adequate to fulfil deer requirements all year-round (according to the requirements suggested by McDowell, 2003). In the case of micro-minerals, the content of most of them was adequate in both terrestrial and aquatic vegetation. This occurred for all minerals except for Se (which was absent in aquatic vegetation in summer and autumn in AL), and Zn (in AL, the content of Zn in terrestrial and aquatic vegetation was similar all year-round). Cobalt was consistently higher in aquatic plants all year-round, but Cu content was only greater in aquatic plants in the summer. Finally, Mn and Fe contents were greater in aquatic plants all yearround, with huge variations between sites. Although both Mn and Fe have been suggested as possible drivers of aquatic plant selection by cervids (Fraser et al., 1984; Moe, 1994), this hypothesis seems improbable since Mn and Fe content are not usually deficient in forages (Suttle, 2010). Nevertheless, Mn cannot be stored, and thus, its high content in aquatics, relative to the estimated diet on terrestrial plants (Table 3), makes this resource interesting for cervids during antler growth, and has the potential for being managed as a food source to reduce the incidence of antler breakage under adverse climatic conditions (Landete-Castillejos et al., 2010). In any case, the great variability in the mineral contents in aquatic plants, especially in their micro-mineral content (see SD values in Table 2, and Fraser et al., 1984 for similar results), necessitates further research with more aquatic species and different habitats and soils, in order to fully understand the reasons underlying the consumption of aquatic vegetation in cervids. The ratios of mineral contents in an exclusively aquatic-based diet vs. the estimated terrestrial diet yielded a pattern similar to the previous raw comparison between aquatic vs. terrestrial vegetation (Table 3 for this and the following results). Mineral contents were greater in an aquatic-based diet across seasons (except Se at AL, Cu in spring at AL, and K and P in winter at AL). Apart from the highly variable Fe and Mn contents (Fraser et al., 1984; Suttle, 2010), Na was the mineral with the highest ratios, especially in summer (68, and 65 times greater in the aquatic-based diet, compared to the terrestrial diet at AL and CE, respectively). However, Na ratios were also high during the rest of the year, and thus, there remains

AL-spring

3. Results and discussion

DL

Rodríguez-Berrocal, 1978; Caballero, 1985; Palacios et al., 1989; García-González and Cuartas, 1992; Soriguer et al., 1994; Alvarez, 1999; Patón et al., 1999; Bugalho and Milne, 2003; Fernández-Olalla et al., 2006; Estévez et al., 2009; Torres-Porras et al., 2010; Olguín, 2011). The frequency of appearances of each plant collected in the aforementioned references were used as an estimator of its relative importance in the diet within our study area. Subsequently, the content of protein and minerals in a diet based only on terrestrial plants was calculated for every site and season, according to the estimated proportion of each plant in the diet, but also considering the variation in the seasonal preferences for fruits, grass, and leaves (based on Rodríguez-Berrocal, 1978). This single diet value per study site and season is presented as the ratio between mineral and protein contents in available aquatic plants vs. the contents in the estimated diet. These ratios accurately show the relative benefits of the aquatic vegetation, but could not be statistically analysed for the differences among them.

Table 2 Mean dry weight mineral and protein values (±SD) for the studied terrestrial (Te) and aquatic (Aq) vegetation. P indicates significant differences in nutritional content values (Mann–Whitney U test using each species as subject). Values under deficiency levels (DL) according to McDowell (2003) are indicated in bold.

F. Ceacero et al. / Behavioural Processes 103 (2014) 28–34

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F. Ceacero et al. / Behavioural Processes 103 (2014) 28–34

Table 3 Ratios of mineral and protein content between aquatic vegetation and the estimated terrestrial diet (see Materials and Methods for further details on this estimation).

Ca K Mg Na P S Co Cu Fe Mn Se Zn Protein

AL-spring

AL-summer

AL-autumn

AL-winter

CE-summer

1.5 1.4 1.7 12.5 1.0 1.1 5.4 0.9 4.2 10.2 0.4 1.2 0.8

2.0 1.5 1.4 68.0 2.0 3.5 7.6 2.2 45.7 12.8 – 1.4 2.0

3.4 1.5 1.7 32.5 1.0 2.1 16.9 1.0 20.4 9.2 – 1.7 1.6

1.6 0.8 1.7 25.5 0.6 1.5 19.3 1.5 35.0 14.8 0.3 1.7 1.0

2.8 3.1 3.7 65.0 2.9 2.9 – 2.4 8.9 62.8 1.4 1.9 2.1

Dashes indicate anomalous values because of the low content of Co in terrestrial vegetation in CE-summer, and Se in aquatic vegetation in AL-summer and AL-autumn.

uncertainty as to why Iberian red deer only (or mainly) use this resource in the summer. Calcium, Cu, and protein ratios were consistently greater in the summer. Fraser et al., 1984 also observed a greater summer protein content in the preferred aquatic plants by A. alces (16.6%) vs. terrestrial vegetation (12.7%). Protein is the most limiting nutrient for all animals. This fact is even more important for herbivores, and specially for females during the lactation period when calves are growing fast (White, 1993). Selection of vegetation with a higher protein content has been reported repeatedly in cervids. C. elaphus selectively feeds on heather with the highest concentration of nitrogen in the Dee Valley of Scotland (Moss et al., 1981), with reproduction and the mortality of calves being influenced by the effects of weather on the protein contents of foods (Albon et al., 1987). Hinds groups on Rhum Island occupying areas fertilised by gulls and preferentially grazing this heavily fertilised (N-rich) vegetation, showed a higher lifetime reproductive success than other groups (Iason et al., 1986). Therefore, protein seems to be an important nutrient, and should be taken into account in future research on this topic, since aquatic vegetation is a great source of it (Boyd, 1968; Bump et al., 2009). In summary, our results show that aquatic vegetation is a good source of Na, Co, Fe, and Mn year round, and also a good source of Ca, Cu, and protein in summer. Therefore, these results do not fully support the ‘Na hypothesis’, the ‘essential mineral hypothesis’, nor the ‘availability hypothesis’, since consumption of aquatic vegetation has been exclusively reported during the summer, and aquatics are a rich source of Na (and several other essential minerals) available all year-round. However, our results do support both the ‘protein hypothesis’ (since peak consumption during summer coincides with the greatest protein content in aquatic plants) and the ‘seasonally increased requirements hypothesis’ (even if this resource is available during the entire year, it is only consumed in the season with the greatest requirements and greatest relative benefits). Several factors could explain the seasonal variations in the nutritional requirements. In cervids: (i) summer is the period of lactation in high latitudes, and thus, the period of maximum need for energy, protein, and minerals (Oftedal, 1985; Gallego et al., 2009; Ceacero et al., 2010); (ii) the males also have an annual cycle of antler growth and casting which requires large amounts of minerals in the late spring and early summer (Gómez et al., 2012); (iii) minerals and protein are frequently scarce in vegetation, which forces cervid to look for extra sources, especially at the end of antler growth, and lactation periods (summer), when the body reserves are depleted; and, (iv) Na requirements are increased in the summer, at least in temperate regions, because of the large losses of Na due to increased sweating. In addition, other mineral seeking behaviours have primarily been reported as occurring during the summer (e.g., osteophagia, Denton et al., 1986; use of mineral licks, Weeks and Kirkpatrick, 1976; Risenhoover and Peterson, 1986; even predation

on birds, apparently seeking the Zn contained in the feathers, but also an important source of protein, Furness, 1988), which further supports the idea that the seasonal variations in the required minerals and protein drives the consumption of aquatic vegetation. Cervids from tropical latitudes also maintain a seasonal antler cycle, but the breeding period is somewhat extended (e.g., O. bezoarticus may breed throughout the year; Ungerfeld et al., 2008). Thus, the extended breeding period and Na loss by sweating may explain the continuous appetite for aquatic vegetation in those cervids from tropical areas. Finally, a new hypothesis arises from our data. Increased production of toxic compounds is a common strategy of plants to avoid herbivore consumption (White, 1993), which up to now has not been considered. Our data also suggests that aquatic vegetation could have been avoided during some periods because of its potential toxicity. Aquatic plants had S contents well above the 2 g/kg recommended maximum value for dietary intake (Zinn et al., 1997). Terrestrial plants also had a high S content, but primarily only in spring and winter. This could result in deer only being able to complement their terrestrial diet with aquatic plants during periods when the S content in terrestrial plants is low (i.e. during summer and autumn). Similar results have been obtained when studying the chemical composition of preferred vs. rejected plants by red deer in Mediterranean ecosystems (Ceacero F. et al., unpublished data). 4. Conclusion Our results suggest that red deer likely feed on aquatic plants because of their high nutritional value, especially in protein, and this is driven by the increased requirements during summer. These requirements correspond to the last stages of lactation and antler growth, combined with increased sweating and food depletion (summer nutritional stress for red deer in Mediterranean ecosystems; Bugalho et al., 2001). However, further research involving more deer species, locations, latitudes, and aquatic plant species is needed to more fully understand the mechanisms regulating the consumption of aquatic vegetation. Detailed studies on the seasonal use of aquatic vegetation by males and females may also reveal the relative importance of mineral (with a greater requirement in males), and protein contents (with a greater requirement in females). Such an understanding could generate novel methods of managing deer populations by providing ponds not only as water points, but also as a source for high quality aquatic vegetation. Acknowledgements This research has been partly funded by MEYC-FEDER project AGL2012-38898. FC was supported by a Czech University of Life

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Sciences Postdoctoral Fellowship (Czech Republic). MM was supported by a NRF Free-standing Postdoctoral Fellowship (South Africa). The authors wish to thank Francisco Selva for his helpful assistance with protein analyses, Dr. Marisa Sicilia for her bibliographical suggestions, and Drs. Fredrik Dalerum and Bronson Strickland for their valuable comments and language corrections.

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Why do cervids feed on aquatic vegetation?

Consumption of aquatic plants is rare among cervids, despite the common occurrence of this form of vegetation. However, the paucity of literature repo...
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