Forage yield and cattle carrying capacity differ by understory type in conifer forest gaps

Author’s Accepted Manuscript Forage Yield and Cattle Carrying Capacity Differ by Understory Type in Conifer Forest Gaps Kesang Wangchuk, Georg Gratzer, Andras Darabant, Maria Wurzinger, Werner Zollitsch www.elsevier.com/locate/livsci

PII: DOI: Reference:

S1871-1413(15)00365-0 http://dx.doi.org/10.1016/j.livsci.2015.08.003 LIVSCI2812

To appear in: Livestock Science Received date: 30 April 2015 Revised date: 1 August 2015 Accepted date: 3 August 2015 Cite this article as: Kesang Wangchuk, Georg Gratzer, Andras Darabant, Maria Wurzinger and Werner Zollitsch, Forage Yield and Cattle Carrying Capacity Differ by Understory Type in Conifer Forest Gaps, Livestock Science, http://dx.doi.org/10.1016/j.livsci.2015.08.003 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Forage Yield and Cattle Carrying Capacity Differ by Understory Type in Conifer Forest Gaps

Kesang Wangchuk1 3*, Georg Gratzer2, Andras Darabant2, Maria Wurzinger1, Werner Zollitsch1 1

Division of Livestock Sciences, Department of Sustainable Agricultural System, BOKU-University of Natural Resources and Life Sciences, Vienna, Austria

2

Institute of Forestry Ecology, Department of Forest and Soil Science, BOKU-University of Natural Resources and Life Sciences, Vienna, Austria

3

Forage and Animal Nutrition Research, Renewable Natural Resources Research Center, Ministry of Agriculture and Forest, Bumthang, 32001, Bhutan. *Corresponding author: [email protected]

Abstract A study was conducted in the Himalayan mixed conifer forests to generate estimates of cattle carrying capacity of logged sites, using consumable forage dry matter and nutrient content. Field samples were collected from four major understory vegetation types dominated by Yushania microphylla (ground cover proportions of 100% and 50%), Rubus nepalensis, Synotis alata and Sambucus adnata. The amount of dry matter, total digestible nutrient and digestible crude protein removed by cattle grazing was highest for the vegetation with 100% Y. microphylla. Vegetation with S. adnata, S. alata and R. nepalensis provided low consumable dry matter yield and nutrient content per hectare area. For vegetation with 100% Y. microphylla, based on consumable dry matter, total digestible nutrients and digestible crude protein, the cattle carrying capacities were estimated at 4.17, 2.27 and 1.27 Livestock Units per Year (LUY) per hectare, respectively. Vegetation with 50% Y. microphylla provided about one LUY per hectare both in terms of consumable DM and nutrient content. Vegetation with S. alata also provided nutritional carrying capacity of about one LUY per hectare but the carrying capacity in terms of consumable dry matter was lower than one LUY per hectare. Cattle carrying capacity, both in terms of dry matter and nutrient content was lower than one LUY per hectare for vegetation with S. adnata and R. nepalensis. We concluded that, depending on the type of understory vegetation, carrying capacity differs within hemlock-dominated mixed conifer forest in the Eastern Himalaya. Forage utilization was higher for S. alata, S. adnata and R. nepalensis vegetation, suggesting the need for vigilance to avoid overgrazing in these vegetation types. The study indicates the opportunity to select appropriate carrying capacities allowing optimum cattle density and providing the required level of nutrition, while avoiding over-grazing. We recommend our estimates to be used as guide to better understand the carrying capacity of logged sites in the Himalayan conifer forest. 1

Keywords: Carrying capacity; Cattle; Dry matter; Forest grazing; Livestock Unit; Nutrient content.

Introduction Ecosystems’ responses to disturbances vary across spatial and temporal scales. The response to anthropogenic disturbances depends on site productivity, with poor sites being less resilient to anthropogenic changes than more productive sites (Larson and Paine, 2007). Herbivory is a key process that determines ecosystems’ resilience (Adam et al., 2011), structure and function (Manier and Hobbs, 2007). In forest ecosystems, the tree-herbivore balance is a fundamental issue and may require certain level of anthropogenic influences for coexistence (Roininen et al., 2007). However, management for harmonious tree-herbivore equilibrium is a challenge (Roder, 2002; Mountford and Peterken, 2003) and often leads to conflicts of interests when deciding on how to manage the system involving livestock and forest. Under such situations, quantitative evaluation of habitat is extremely important to facilitate proper management (Hanley and Rogers, 1989; Mizutani, 1999). Globally, forest ecosystems are subject to recurrent disturbances and resource exploitation, causing radical change. More than natural factors, management methods are driving forest ecosystems (Berg et al., 2008), leading to formation of forest gaps. Forest gaps are characterized by high herbaceous vegetation cover (Modrý et al., 2004) and abundant herbage (Mayer and Stockli, 2005), which are preferentially grazed by cattle (Carman and Briske, 1985) and wild life (Kuijper et al., 2009). Depending on spatial heterogeneity and foraging behavior along the environmental gradient, herbivores have different impacts on ecosystems (Stuart-Hill, 1992). Thus, the effects of ungulate herbivory are reported to be both beneficial (Gratzer et al., 1999; Humprey and Patterson, 2000; Roder, 2002; Luoto et al., 2003; Peco et al., 2006; Casasus et al., 2007; Darabant et al., 2008) and deleterious (Patric and Helvey, 1986; Broersma et al., 2000; Wangda and Ohsawa, 2006). Deleterious effects are often associated with overgrazing by wildlife and domestic herbivores (Mysterud, 2006). Overgrazing is reported to be counterproductive, causing adverse effects on soil (Patric and Helvey, 1986; Broersma et al., 2000; Sharrow, 2007) and vegetation (Haeggstrom, 1990; Broersma et al., 2000; Mayer et al., 2006; Pande and Yamamoto, 2006). While deleterious effects are debated in frequent disputes, management frameworks to address these issues are less emphasized, particularly with reference to logged sites in temperate forest ecosystems. A number of studies suggest measures to counteract the adverse effects of overgrazing such as grazing exclusion (Shrestha and Stahl, 2008; Fernández-Lugo et al., 2009; Li et al., 2012), adjustments in grazing duration (Savadogo et al., 2007), stocking rate (Nomiya et al., 2002), and rotational grazing (Royal Government of Bhutan, 2006). However, these measures are applied widely only on grasslands and less on forest ecosystems. Besides, the measures need to be cost effective, providing opportunities for both resource conservation and utilization. Defining threshold levels for herbivore density which are based on a quantitative assessment of grazing resources might be feasible, without diminishing returns from forest utilization (Jorritsma et al., 1999). Depending on landscape conditions and site productivity, the thresholds of herbivore density vary from one ecosystem to another (Afzal et al., 2007; Chaudhry et al., 2010; Robinson et al., 2010), indicating the need for quantitative assessment of the respective ecosystems. 2

Estimates of animal carrying capacity (Baars and Jeanes, 1997; Afzal et al., 2007; Savadogo et al., 2007; Chaudhry et al., 2010; Robinson et al., 2010; Hajno and Tahiri, 2011) have been successfully used in management decisions and planning (Mayer et al., 2006) and help to achieve sustainable utilization of ecosystems (Stoddart et al., 1975; Kuzyk et al., 2009). Animal carrying capacity is defined as the maximum stocking rate that a certain land area can support on a sustainable basis during a defined grazing season (FAO, 1991). Carrying capacity was estimated using nutritional parameters besides forage biomass in several studies (Hobbs et al., 1982; Thapa and Paudel, 2000; Beck et al., 2006; Das and Shivakoti, 2006). A sound estimate of carrying capacity might promote sustainable management for optimum production of livestock and timber (Roder, 2002; Pollock et al., 2005; Buffum et al., 2009), and may contribute to finding a long term solution to resolving existing conflicts. This paper presents the results of a study conducted on logged sites in the mixed conifer forests of Bhutan, where forest grazing by cattle is perceived to negatively affect tree regeneration and is viewed as a main constraint to good forest management (Roder et al., 2002). The ability to resolve conflicts has been limited by the lack of scientific data on thresholds for cattle density, which would allow for a sustainable forest management. Therefore, our primary objective was to estimate the cattle carrying capacity of logged sites in the mixed conifer forest, using the amount of consumable forage dry matter and its nutrient contents as main parameters. Since mixed conifer forests have different understory vegetation, we aimed to generate estimates of cattle carrying capacity of dominant understory vegetation. The study is an attempt to contribute to a better understanding amongst resource managers on the cattle carrying capacity for sustainable management of logged sites in mixed conifer forests.

2. Materials and methods 2.1. Study sites We selected Gidakom Valley as study site, representing the mixed conifer forests in Bhutan. The forests supply wood and non-wood products to the urban areas and adjacent rural households in the district of Thimphu. Both sedentary and migratory livestock are fully dependent on forest grazing in the study areas. The presence of wildlife based on ocular assessment of droppings seems comparatively negligible. For livestock grazing management, farmers practice deferred grazing of permanent grassland, use of tree fodder species during the dry season and seasonal migration to lower elevations. Forest grazing is one of the main sources of ruminant feed. Fallow land grazing is often practiced after crop harvest where cattle are allowed to graze freely in the crop fields as soon as crops are harvested. The fallow lands are extensively grazed during acute shortages of fodder in winter. Crop residues are used as traditional winter fodder. The Forest Management Unit of Gidakom lies in western Bhutan between Thimphu and Paro valleys with a total area of 13’000 hectares and 115 households (Dhital et al., 1992). The study area (89° 29’N, 27° 27’S; 3220 m elevation) is located in the Forest Management Unit, where commercial harvesting started 20 years ago. Topography is rugged and the mean maximum temperature of 25°C is recorded in the month of July and the mean minimum of 5oC in January. The average annual rainfall is about 622 mm, mostly in the months from June to August (Dorji, 2004). The main tree species include Eastern Spruce (Picea spinulosa), Himalayan Hemlock (Tsuga dumosa) and 3

Brown Oak (Quercus semecarpifolia) mixed with Blue Pine (Pinus wallichiana). The main understory species comprise Yushania microphylla, Synotis alata, Salvia campanulata, Sambucus adnata, Rubus nepalensis and Senecio raphanifolius. Unlike other understory vegetation, Y. microphylla is evergreen but remains dormant in winter.

2.2. Selection of experimental plots We classified the understory vegetation by analysing the plant inventory data of 90 forest openings, using the software CANOCO software. The average size of the forest opening was 0.15 ha. The analysis segregated the logged openings into homogeneous groups of dominant species representing the vegetation of the forests under study. The major species were Yushania microphylla, Rubus nepalensis, Synotis alata and Sambucus adnata. Y. microphylla and S. alata are grazed by cattle; R. nepalensis, although consumable forms a thick mat on the forest floor and is barely grazed and; S. adnata is a non-forage species. Given the varying levels of dominance and patchy occurrence of Y. microphylla in the mixed conifer forests, we purposively sampled two different proportions of vegetation dominated by this species i.e 100 per cent and 50 per cent plant ground cover. Except for Y. microphylla which is evergreen, all dominant vegetation were deciduous in nature. The annual growth cycle of major understory vegetation types except Y. microphylla is generally characterized by bud break in spring and culminating in leaf fall in autumn, followed by dormancy in winter. We selected 10 logged forest openings for field measurement and sampling. Two openings were assigned to each dominant vegetation type. The sample plots were located in the centre of each opening. Each opening constituted one block, consisting of one pair of grazed and ungrazed plot of 2 m × 2 m. The ungrazed plots were fenced after logging.

2.3. Measurement of dry matter yield and estimation of carrying capacity The biomass of consumable plant materials was estimated during the peak growing season, coinciding with optimum yield and quality. The hand clipping method (Catchpole and Wheeler, 1992; ’T Mannetje and Jones, 2000) was employed to determine the plant biomass. Squared quadrats (0.5 m × 0.5 m), reported to be efficient statistically (Brummer et al., 1994) were placed randomly four times avoiding overlap on a plot to obtain fresh biomass yield estimate from a total of one meter square area. Using the expertise of experienced cattle herder, the harvested materials were identified and segregated into consumable and non-consumable plants. The plant materials inside the quadrats which were perceived as being consumable were clipped and weighed. While the dry matter yield of ungrazed plot represented the plant materials untouched by herbivores, the dry matter yield of grazed plot represented whatever plant materials were left after herbivory. The difference between dry matter yields of the two plots was defined as being removed by the animals. Representative sub samples weighing about 300 g were collected and oven dried at 60oC for 48 hours. The dried samples were weighed. The dry matter yield of dominant vegetation types was calculated.

4

Carrying capacities were calculated from consumable dry matter by considering the daily dry matter intake and grazing duration. Feed requirements for livestock were calculated on the basis of feed intake in dry matter (DM) as a % of live weight. Carrying capacity was expressed as the number of standard livestock units (LU) per year per hectare of land. We used the animal body weight of 300 kg as one standard livestock unit for Bhutanese farming systems, with daily dry matter requirement of 2% of body weight (Samdup et al., 2010). Forest grazing was a year round activity, therefore, the grazing period was 365 days. We used the mathematical formula adapted from Gerrish (1998) and calculated annual carrying capacity as;

where Carrying Capacity is expressed in LU ha-1yr-1, EDM = Edible Dry Matter removed by the animals during a grazing period, calculated as difference in EDM yield between ungrazed and grazed plot, DDMI= Daily Dry Matter Intake of one LU, DFP= Days on Forest Pasture. In order to project grazing pressure, we estimated Forage Utilization (FU), which was defined as a measure of the amount of plant dry matter removed by cattle over a year. Forage utilization (FU) was calculated as;

2.4. Measurement of nutrient content and estimation of nutritional carrying capacity The dried samples were processed and analysed for nutrient content. We followed the standard procedure of Ankom’s Filter Bag Technique to determine Acid Detergent Fiber (ADF) and Neutral Detergent Fiber (NDF). Using the values of ADF, we used the mathematical equation of Schroeder (2004) and calculated the TDN as;

The total nitrogen content in the sample was determined with Kjeldahl method (AOAC, 1990) and CP was estimated as % N × 6.25. Finally, we used mathematical equation of Schroeder (2004) and calculated the DCP as;

TDN and DCP were used as the main parameters for estimating the nutritional carrying capacity. The calculation assumed that, a standard Bhutanese livestock unit of 300 kg body weight (Samdup et al., 2010), yielding an average of 2 litres milk with fat content of 5% daily requires 4.74 TDN kg per day or 1730 kg annually and 0.58 DCP kg per day or 212 DCP kg annually (Ibrahim et al., 2008).

2.5. Data analyses

5

The dataset was tested for normal distribution and homogeneity of variance. Where necessary, the dataset was normalized through transformation, however, actual means are reported for easy comprehension. Using the Analysis of Variance, we tested the differences in forage yield and nutritional parameters between grazed and ungrazed plots. Tukey’s LSD test was used to test for significant differences between means. Differences between means were considered significant if p values were less than 0.05. The dataset was analysed in SPSS 19 (Landau and Everitt, 2004).

3.

Results and discussion

3.1. Dry matter production and nutrient content of understory vegetation Our results are confined to four species, Y. microphylla, S. alata, S. adnata and R. nepalensis. There were substantial differences in the aboveground dry matter yields between understory vegetation and between grazed and ungrazed plots. Dry matter yield was substantially higher for understory vegetation with Y. microphylla (Table 1), with yields of ungrazed plots being significantly higher by five folds, as compared with grazed plots. There was no significant yield difference between the other three vegetation types. The high dry matter content of 100% Y. microphylla vegetation was accompanied by low protein content. Conversely, vegetation with 50% Y. microphylla gave low dry matter yield with high protein content. The results demonstrate an inverse relationship between forage abundance and quality (Fig. 1), also reported for semiarid rangeland ((Breman and deWitt, 1983). Irrespective of statistical significance, with exception to the CP content of S. alata, the grazed plots were generally characterized by low fiber, high CP and mineral content (Table 1), which provides valuable insight into the effect of grazing on forage quality. A significantly higher content of CP and P were found in grazed plots of Y. microphylla as compared with ungrazed plots, suggesting that grazed sites offer forage of higher quality. It conforms to reports that grazing enhances the forage quality by maintaining vegetation at a younger phenological stage (Aremu et al., 2007; Casasus et al., 2007; Eilertsen et al., 2000), with significantly higher level of CP (Pavlu et al., 2006), which has been ascribed to high photosynthesis rate and higher concentration of nutrients in young leaves (Zhou and Wu, 1997). Low nutrient content in older leaves is explained by the increasing lignification of cell walls with increasing physiological age and reduced supply of water and nutrients (Kleinhenz and Midmore, 2001). Proper grazing was found essential in maintaining adequate forage condition to meet the nutrient requirement of herbivores (Westenskow-Wall et al., 1994; Clark et al., 1998). Vegetation with S. adnata and R. nepalensis recorded the lowest dry matter yields with no significant difference in nutrient content between grazed and ungrazed plots. The plausible explanation could be that, S. adnata is a non-forage species and usually forms thick layers on the forest floor, and the species was found to be negatively correlated with other plant species (Tshering, 2005). It means, the thick layer of S. adnata restricts growth of other plants, including species consumable, which may explain the low consumable dry matter yield of vegetation dominated by this species. On the other hand, R. nepalensis is consumable but it appears as a thick mat on the forest floor and the species is barely grazed by hervibores (Wangchuk et al., 2014). Furthermore, irrespective of whether or not grazing is present, the thick mat also restricts growth of other plant species, which likely explains the almost 6

similar dry matter yields between grazed and ungrazed sites of R. nepalensis dominated vegetation (Table 1). A closer scrutiny of nutritional parameters of vegetation with S. adnata, S. alata and R. nepalensis revealed higher protein content than the vegetation with Y. microphylla (Table 1) despite the low DM yields. From the forest management perspective, studies (Gratzer et al., 1999; Pollock et al., 2005; Darabant et al., 2007) demonstrate grazed vegetation to offer favorable conditions for forest regeneration, where understory species competing with tree regeneration are palatable. Thus, depending on grazing pressure, cattle grazing serves dual purposes of improving forage quality and enhancing tree regeneration in the conifer forests of Bhutan.

3.2. Cattle carrying capacities of logged sites In Bhutan, carrying capacity has been estimated for natural grasslands using forage dry matter yield (Dorji and Roder, 1980; Roder, 1983; Dorjee, 1986) and through ocular assessments (Singh, 1978; Harris, 1987; Gyamtsho, 1996). Our carrying capacity estimates pertain to village cattle, which is the main livestock in the study area. The estimates are based on important assumptions and the carrying capacity derived in this study depicts the actual feed resource situation at the study site, which is a first estimate only for similar forest ecosystems. Carrying capacity is theoretical (Young, 1998) and the estimates are never precise (Evlagon et al., 2012) as they are found to vary with time (Baars and Jeanes, 1997), vegetation (Robles and Passera, 1995) and site condition (Fritz and Duncan, 1994). This has often resulted in different estimates of carrying capacities from the same resources (Dijkman, 1999). Therefore, estimates reported here are more suited to be used as an indicator for the potential forage resource of the respective understory vegetation. Results for FU ranged from 0.51 for 100% Y. microphylla to 0.62 for S. adnata (Table 2). These values are similar to those estimated for pasturelands of central Asia (Robinson, 2000) and the one used by Chaudhry et al. (2010), but were lower than the values reported for grassland meadows (Hajno and Tahiri, 2011). FU was lowest for vegetation with 100% Y. microphylla and S. alata. Possible explanations include low quality foliage of bamboo (Greenway, 1999) and least cattle preference for S. adnata (pers. commn). Depending on dry matter yield and nutrient content, the cattle carrying capacities ranged from 0.10 to 4.17 -1

LU ha Y-1 (Fig. 2). Carrying capacity is basically a function of understory vegetation (Evlagon et al., 2012). Differences in carrying capacity between different types of vegetation are primarily due to differences in dry matter yields and nutrient content (Robles and Passera (1995). Although this study was unable to ascertain the grazing pressure due to lack of data on number and further details of cattle that graze on logged sites, difference in carrying capacities between plots suggests the necessity for a smart choice of grazing pressure. Despite its lower FU value, vegetation with 100% Y. microphylla provided the highest carrying capacity of 4.17, 2.27 and 1.27 LUY, estimated from consumable dry matter, total digestible nutrients and digestible crude protein, respectively. In terms of digestible crude protein, vegetation with 50% Y. microphylla and S. alata provided carrying capacity of about one LUY (Fig. 2). Understory vegetation with Sambucus adnata and Rubus nepalensis gave the lowest carrying capacities. The relationship between CP content and consumable DM yield displayed a negative trend, and DM yield explained about 68% of variations in CP content (Fig. 1). At vegetation level, it can be 7

interpreted that vegetation (100% Y. microphylla) with high dry matter yield may support more livestock units on a relatively low plane of nutrition, whereas other vegetation with low dry matter yield may support less livestock units but on a high plane of nutrition. Thus, our result further corroborates the inverse relation between abundance and quality of forage (Breman and deWitt, 1983), showing that abundant forage on the logged sites provides low plane of nutrition in the Himalayan conifer forest. Y. microphylla has been found to increase biomass and cover (Gratzer, et al., unpubl.) with increasing light interception in forest gaps, and a positive correlation of bamboo biomass with increased opening sizes has been reported for bamboos (Takatsuki, 1992; Widmer, 1998). In our study, the mono-dominant stands of Y. microphylla were in the small forest openings within a range of 0.065 to 0.204 ha where light could probably have been a factor limiting growth. Therefore, the carrying capacity for Y. microphylla vegetation estimated in this study may be lower than what could be expected for a similar vegetation in large opening. We estimated carrying capacity during the peak growing season, which justifies considering our estimates as ecological carrying capacity (Caughley, 1979), meaning it is the upper limit of cattle density that an area can support. Carrying capacity exceeding the upper limit will not only damage vegetation but could also result in deterioration in the nutritional status of individual animals, even if forage quality is not limiting (Hobbs and Swift, 1985).

3.3. Management implications Our results suggest few but important management implications. Cattle grazing on mono-dominant stands of Y. microphylla might require protein supplements for optimum performance. The low protein content of natural feeds is a limiting factor in cattle production (Ketelaars, 1983) and grazing herds commonly suffer from nutrient deficiency (Ferguson and Chalupa, 1989). The inverse relationship between yield and quality indicates that, either the cattle grazing in low protein vegetation has to be supplemented with a feed rich in protein or cattle must be moved to another vegetation of complementary nutritional value. Thus, the cattle managers can take advantage of the inverse relationship between yield and quality to select appropriate carrying capacity allowing optimum cattle density and at the same time to secure the required level of nutrition (Hobbs and Swift, 1985). The nutrient yield per hectare was generally low for vegetation types with S. adnata, S. alata and R. nepalensis but the protein content per kilogram dry matter was high. This implies that at low stocking rate, these vegetation types could provide high quality forage for a sufficiently high cattle performance. However, the low dry matter yield of these vegetation types would also indicate a greater risk for overgrazing. The possibility of overgrazing cannot be excluded, mainly for two reasons. Firstly, these vegetation types are heterogeneous (Wangchuk et al., 2014) with low forage yields. Vegetative heterogeneity is reported to trigger site selectivity (Vallentine, 1990; Bailey, 1995; Wallis DeVries et al., 1999) and selective grazing leads to higher grazing pressure causing resource deterioration even at low stocking rates (Teague et al., 2011). Secondly, these vegetation types provide low forage yield but of high quality. According to the optimal foraging theory (Stephens and Krebs, 1986), high quality forage results in maximum intake. Cattle have been reported to prefer forage with a high crude protein 8

content (Hirata et al., 2008) and usually consume more amount of feed dry matter than required (Köster et al., 1996; Bailey, 2005). Furthermore, the FU values of these vegetation types exceed 50 per cent, suggesting the likelihood of overgrazing. Studies show that grazing intensity is heavy when utilization of primary forage species exceeds 50 per cent (Holechek et al., 1999; Amezaga et al., 2004). Thus, depending on the herd size, supervised grazing may be necessary in these understory vegetation types. Hence, on logged sites with S. adnata, S. alata and R. nepalensis as dominant vegetation, grazing needs to be regulated. On the contrary, overgrazing is less likely in vegetation with Y. microphylla, probably due to low forage quality, which are less preferred by the cattle (Bailey, 1995).

Conclusions The cattle carrying capacities differ within the mixed conifer forests, depending on the type of understory vegetation, dry matter yield and nutrient content. Vegetation with high dry matter yield will probably provide forage of low nutritional quality. The inverse relation between yield and nutritive value calls for a proper management in order to fulfill the animals' nutritional requirements while at the same time using the feed resources in the forests in a sustainable way. Supplementing the diets of grazing animals and supervised grazing may be necessary in understory vegetation types with S. alata, S. adnata and R. nepalensis. Our results may be applicable in other regions sharing similar management and environmental conditions. Our estimates are normative and suited to be used as guide for enhanced understanding. Although discussed and debated widely, carrying capacity is a parameter less studied in Bhutan, and information on the subject is unusually scarce. The only available information on native grasslands is over two decades old. There is a dire need for a holistic approach to determine the carrying capacities of feed resources in the country. In view of improvement of the socio-economic conditions of herding communities and consequent changes in the traditional herding practices, similar studies need to extend to rangelands and native grasslands. Of immediate need is the study on overtime change in carrying capacities in relation to biotic and abiotic factors and possibly, the development of a model to extrapolate future trends in carrying capacities of forage resources. For reliable estimates, it is vital to update the carrying capacities at regular interval.

Acknowledgements The authors gratefully acknowledge the financial support of the Government of Austria with funds routed through the Österreischer Austauschdienst (OeAD). We also thank Harilal Nirola, Yonten, Karma Dorji, Samten Nidup and Durba Mongar for their valuable assistance during the fieldwork.

References ’T Mannetje, L., Jones, R.M., 2000. Field and Laboratory Methods for Grassland and Animal Production Research. CAB International, Wallingford. Adam, T.C., Schmitt, R.J., Holbrook, S.J., Brooks, A.J., Edmunds, P.J., Carpenter, R.C., Bernardi, G., 2011. Herbivory, connectivity, and ecosystem resilience: response of a coral reef to a large-scale perturbation. PLoS One 6, e23717.

9

Afzal, J., Ullah, M.A., Anwar, M., 2007. Assessing Carrying Capacity of Pabbi Hills Kharian Range. Journal of Animal and Plant Science 17, 27-29. Amezaga, I., Mendarte, S., Albizu, I., Besga, G., Garbisu, C., Onaindia, M., 2004. Grazing Intensity, Aspect, and Slope Effects on Limestone Grassland Structure. Journal of Range Management 57, 606 -612. AOAC, 1990. Official Methods of Chemical Analysis 16th edition. Association of Official Agricultural Chemists, Washington DC, USA. Aremu, O.T., Onadeko, S.A., Inah, E.I., 2007. Impact of Grazing on Forage Quality and Quantity for Ungulates of the Kainji Lake National Park, Nigeria. Journal of Applied Sciences 7, 1800-1804. Baars, R.M.T., Jeanes, K.W., 1997. The grazing capacity of natural grasslands in the western province of Zambia. Tropical Grasslands 31, 8. Bailey, D.W., 1995. Daily selection of feeding areas by cattle in homogeneous and heterogeneous environments. Applied Animal Behavior Science 45, 183-200. Bailey, D.W., 2005. Identification and creation of optimum habitat conditions for livestock. Rangeland Ecology and Management 58, 109-118. Beck, J.L., Peek, J.M., Strand, E.K., 2006. Estimates of Elk Summer Range Nutritional Carrying Capacity Constrained by Probabilities of Habitat Selection. Journal of Wildlife Management 70, 283-294. Berg, A., Östlund, L., Moen, J., Olofsson, J., 2008. A century of logging and forestry in a reindeer herding area in northern Sweden. Forest Ecology and Management 256, 1009-1020. Breman, H., deWitt, C.T., 1983. Rangeland productivity and exploitation in the Sahel. Science 221, 1341-1347. Broersma, K., Krzic, M., Newman, R.F., Bomke, A.A., 2000. Effects of grazing on soil compaction and water infiltration in forest plantations in the interior of British Columbia. In: Hollstedt, C., Sutherland, K., Innes, T. (Eds.), Proceedings: From Science to Management and Back: A Science Forum for Southern Interior Ecosystems of British Columbia. Southern Interior Forest Extension and Research Partnership, pp. 89-92. Brummer, J.E., Nichols, J.T., Engel, R.K., Eskridge, K.M., 1994. Efficiency of different quadrat sizes and shapes for sampling standing crop. Journal of Range Management 47, 84-89. Buffum, B., Gratzer, G., Tenzin, Y., 2009. Forest Grazing and Natural Regeneration in a Late Successional Broadleaved Community Forest in Bhutan. Mountain Research and Development 29, 30-35. Carman, J.G., Briske, D.D., 1985. Morphologic and allozymic variation between long-term grazed and nongrazed populations of the bunchgrass Schizachyrium scoparium var. frequens. . Oecologia 66, 332-337. Casasus, I., Bernues, A., Sanz, A., Villalba, D.L., Riedel, J.L., Revilla, A.R., 2007. Vegetation dynamics in Mediterranean forest pastures as affected by beef cattle grazing. Agriculture, Ecosystems and Environments 121, 365-370. Catchpole, W.R., Wheeler, C.J., 1992. Estimating plant biomass; a review of techniques. Australian Journal of Ecology 17, 121-131. Caughley, G. (Ed.), 1979. North American elk: ecology, behaviour, and management. Laramie. University of Wyoming Press, WY, USA.

10

Chaudhry, A.A., Haider, M.S., Ahsan, J., Fazal, S., 2010. Determining Carrying Capacity of Untreated and Treated Areas of Mari Reserve Forest (Pothwar Tract) after Reseeding with Cenchrus ciliaris. The Journal of Animal and Plant Sciences 20, 103-106. Clark, P.E., Krueger, W.C., Bryany, L.D., Thomas, D.R., 1998. Spring defoliation effects on bluebunch wheatgrass: I. Winter forage quality. Journal of Range Management 51, 519-525. Darabant, A., Rai, P.B., Gratzer, G., 2008. Interactive effects of biotic and abiotic factors on Tsuga dumosa seedling establishment in silvicultural group openings. RNR-RC Jakar, Bumthang, Bhutan, p. 10. Darabant, A., Rai, P.B., Tenzin, K., Roder, W., Gratzer, G., 2007. Cattle grazing facilitates tree regeneration in a conifer forest with palatable bamboo understory. Forest Ecology and Management 252, 73-83. Das, R., Shivakoti, G.P., 2006. Livestock carrying capacity evaluation in an integrated farming system: A case study from the mid-hills of Nepal. International Journal of Sustainable Development and World Ecology 13, 153-163. Dhital, D.B., Pushparajah, M., Maatta, M., 1992. Forest Management Plan (1992-2002). Gidakom Forest Management Unit. Forest Conservation and Management Project FAO/BHU/85/016. Forest Resources and Development Division, Ministry of Agriculture, Thimphu, Bhutan. Dijkman, J., 1999. Carrying capacity: outdated concept or useful livestock management tool? Dorjee, J., 1986. Estimation of Animal Feed Requirement of the Kingdom of Bhutan. Thimphu, Bhutan. Dorji, K., Roder, W., 1980. Experiments in Fodder Development in 1979. Bumthang. Dorji, S., 2004. Natural regeneration at cable crane logged sites in the mixed conifer belt of Gidakom Forest Management Unit, Thimphu, Bhutan. University of Natural Resources and Applied Life Sciences, Vienna, Austria. Eilertsen, S.M., Schjelderup, I., Mathiesen, S.D., 2000. Plant quality and harvest in old meadows grazed by reindeer in spring. Journal of the Science of Food and Agriculture 80 329-334. Evlagon, D., Kommisarchik, S., Gurevich, B., Leinweber, M., Nissan, Y., Seligman, N.G., 2012. Estimating normative grazing capacity of planted Mediterranean forests in a fire-prone environment. Agriculture, Ecosystems and Environment 155, 133-141. FAO, 1991. Guidelines: Land evaluation for extensive grazing. FAO Soils Bulletin, Rome. Ferguson, J.D., Chalupa, W., 1989. Impact of protein nutrition on reproduction in dairy cows. Journal of Dairy Science 72, 746-766. Fernández-Lugo, S., de Nascimento, L., Mellado, M., Bermejo, L.A., Arévalo, J.R., 2009. Vegetation change and chemical soil composition after 4 years of goat grazing exclusion in a Canary Islands pasture. Agriculture, Ecosystems and Environments 132, 276-282. Fritz, H., Duncan, P., 1994. On the carrying capacity for large ungulates of African savanna ecosystems. . Proceedings of Royal Society of London, pp. 77-82. Gerrish, J., 1998. Grazier's Arithmetic. Missouri, USA, p. 1. Gratzer, G., Rai, P.B., Glatzel, G., 1999. The influence of the bamboo Yushania microphylla on regeneration of Abies densa in central Bhutan. Canadian Journal of Forest Research 29, 1518-1527. Greenway, S.L., 1999. Evaluation ofBamboo as Livestock Forage and Applications ofYucca schidigera and Quillaja saponaria Products in Agriculture. Department ofAnimal Sciences. Oregon State University, Oregon, pp. 1-81. 11

Gyamtsho, P., 1996. Assessment of the condition and Potential for Improvement of High Altitude Rangeland of Bhutan, Dissertation No. 11726. Zurich ETH. Haeggstrom, C.A., 1990. The influence of sheep and cattle grazing on wood meadows in Aland, SW Finland. Acta Botanica Fennica 141, 1-28. Hajno, L., Tahiri, F., 2011. Yield and Carrying Capacity of Meadows in Albania. Ratarstvo i Povrtarstvo / Field and Vegetable Crops Research 48, 151-154. Hanley, T.A., Rogers, J.J., 1989. Estimating carrying capacity with simultaneous nutritional constraints Department of Agriculture, Forest Service, Pacific Northwest Research Station, Alaska, USA. Harris, P.S., 1987. Grassland Survey and Integrated Pasture Development in the High Mountain Region of Bhutan (TCP/BHU/4505(A)AHD/FAO). Thimphu. Hirata, M., Sakou, A., Terayama, Y., 2008. Selection of feeding areas by cattle in a spatially heterogeneous environment: selection between two tropical grasses. Journal of Ethology 26, 327-338. Hobbs, N.T., Baker, D.L., Ellis, J.E., Swift, D.M., Green, R.A., 1982. Energy-and Nitrogen-based estimates of Elk Winter-Range Carrying Capacity. Journal of Wildlife management 46, 12-21. Hobbs, N.T., Swift, D.M., 1985. Estimates of habitat carrying capacity incorporating explicit nutritional constraints. Journal of Wildlife Management 49, 814-822. Holechek, R.J., Gomez, H., Molinar, F., Galt, D., 1999. Grazing studies: what’ve we learned? Rangelands 21, 12-16. Humprey, J.W., Patterson, G.S., 2000. Effects of late summer cattle grazing on the diversity of riparian pasture vegetation in an upland conifer forest. Journal of Applied Ecology 37, 986-996. Ibrahim, M.N.M., Gyeltshen, J., Tenzing, K., Dorji, T., 2008. A Practical Guide for Feeding Dairy Cattle in Bhutan (First edition). Ministry of Agriculture, Royal Government of Bhutan, Thimphu, Bhutan. Jorritsma, I.T.M., van Hees, A.F.M., Mohren, G.M.J., 1999. Forest development in relation to ungulate grazing: a modeling approach. Forest Ecology and Management 120, 23-34. Ketelaars, J.J.M.H., 1983. Evaluation of rangeland as a feed resource for livestock production. In: W, S. (Ed.), Workshop on land evaluation for extensive grazing (LEEG) Addis Ababa, Ethiopia. Kleinhenz, V., Midmore, D.J., 2001. Aspects of Bamboo Agronomy. Advances in Agronomy 74, 99-145. Köster, H.H., Cochran, R.C., Titgemeyer, E.C., Vanzant, E.S., Abdelgadir, I., St-Jean, G., 1996. Effect of Increasing Degradable Intake Protein on Intake and Digestion of Low-Quality, Tallgrass-Prairie Forage by Beef Cows. Journal of Animal Science 74, 2473-2481. Kuijper, D.P.J., Cromsigt, J.P.G.M., Churski, M., Adam, B., Jędrzejewska, B., Jędrzejewski, W., 2009. Do ungulates preferentially feed in forest gaps in European temperate forest? Forest Ecology and Management 258, 1528-1535. Kuzyk, G.W., Cool, N.L., Bork, E.W., Bampfylde, C., Franke, A., Hudson, R.J., 2009. Estimating Economic Carrying Capacity for an Ungulate Guild in Western Canada. The Open Conservation Biology Journal 3, 24-35. Landau, S., Everitt, S., 2004. A Handbook of Statistical Analyses using SPSS. CRC Press Company Chapman & Hall/CRC.

12

Larson, A.J., Paine, R.T., 2007. Ungulate herbivory: indirect effects cascade into the treetops. Proc Natl Acad Sci U S A 104, 5-6. Li, Y., Zhou, X., Brandle, J.R., Zhang, T., Chen, Y., Han, J., 2012. Temporal progress in improving carbon and nitrogen storage by grazing exclosure practice in a degraded land area of China's Horqin Sandy Grassland. Agriculture, Ecosystems and Environment 159, 55-61. Luoto, M., Pykala, J., Kuussaari, M., 2003. Decline of landscape scale habitat and species diversity after the end of cattle grazing. Journal of Nature Conservation 11, 171-178. Manier, D.J., Hobbs, N.T., 2007. Large herbivores in sagebrush steppe ecosystems: livestock and wild ungulates influence structure and function. Oecologia 152, 739-750. Mayer, A.C., Stockli, V., 2005. Long term impact of cattle Grazing on subalpine forest development and efficiency of snow avalanche protection. Arctic, Antarctic, and Alpine Research 37, 521-526. Mayer, A.C., Stockli, V., Konold, W., Kreuzer, M., 2006. Influence of cattle stocking rate on browsing of Norway spruce in subalpine wood pastures. Agroforestry Systems 66, 143-149. Mizutani, F., 1999. Biomass density of wild and domestic herbivores and carrying capacity on a working ranch in Laikipia District. African Journal of Ecology 37, 15. Modrý, M., Hubený, D., Rejšek, K., 2004. Differential response of naturally regenerated European shade tolerant tree species to soil type and light availability. Forest Ecology and Management 188, 185-195. Mountford, E.P., Peterken, G.F., 2003. Long-term change and implications for the management of woodpastures: experience over 40 years from Denny Wood New Forest. Forestry 76, 25. Mysterud, A., 2006. The concept of overgrazing and its role in management of large herbivores. Wildlife Biology 12, 129-141. Nomiya, H., Suzuki, W., Kanazashi, T., Shibat, M., Tanaka, H., Nakashizuka, T., 2002. The response of forest floor vegetation and tree regeneration to deer exclusion and disturbance in a riparian deciduous forest, central Japan. Plant Ecology 164, 263-276. Pande, T.N., Yamamoto, H., 2006. Cattle treading effects on plant growth and soil stability in the mountain grassland of Japan. Land Degradation and Development 17, 419-428. Patric, J.H., Helvey, J.D., 1986. Some Effects of Grazing Forest Service on Soil and Water in the Eastern Forest. Department of Agriculture, Northeastern Forest Experiment Station, United States. Pavlu, V., Hejcman, M., Pavlu, L., Gaisler, J., Nezerkova, P., 2006. Effect of continuous grazing on forage quality, quantity and animal performance. Agriculture, Ecosystems and Environment 113, 349-355. Peco, B., Sanchez, A.M., Azcarate, F.M., 2006. Abandonment in grazing systems: Consequences for vegetation and soil. Agriculture, Ecosystems and Environments 113, 284-294. Pollock, M.L., Milner, J.M., Waterhouse, A., Holland, J.P., Legg, C.J., 2005. Impacts of livestock in regenerating upland birch woodlands in Scotland. Biological Conservation 123, 443-452. Robinson, S., 2000. Pastoralism and Land Degradation in Kazakhstan. University of Warwick, UK. Robinson, S., Safaraliev, G., Muzofirshoev, N., 2010. Carrying capacity of pasture and fodder resources in the Tajik Pamirs: A report for the FAO. 13

Robles, A.B., Passera, C.B., 1995. Native forage shrub species in south-eastern Spain: forage species, forage phytomass, nutritive value and carrying capacity. Journal of Arid Environments 30, 191-196. Roder, W., 1983. Agriculture and Animal Husbandry Activities under RDP, Bumthang 1974-83-Final Report. Thimphu. Roder, W., 2002. Grazing management of temperate grasslands and fallows. Journal of Bhutan Studies 7, 44-60. Roder, W., Gratzer, G., Wangdi, K., 2002. Cattle grazing in the conifer forests of Bhutan. Mountain Research and Development 22, 368–374. Roininen, H., Veteli, T.O., Piiroinen, T., 2007. The role of herbivores in the ecosystem and management of miombo woodlands. MITMIOMBO – Management of Indigenous Tree Species for Ecosystem Restoration and Wood Production in Semi-Arid Miombo Woodlands in Eastern Africa. . Working Papers of the Finnish Forest Research Institute : , Morogoro, Tanzania, pp. 107–114. Royal Government of Bhutan, M.o.A., 2006. Forest and Nature Conservation Rules 2006. In: Royal Government of Bhutan, M.o.A. (Ed.). Royal Government of Bhutan, Ministry of Agriculture, Thimphu, p. 180. Samdup, T., Udo, H.M.J., Eilers, C.H.A.M., Ibrahim, M.N.M., VandZijpp, A.J., 2010. Crossbreeding and intensification of smallholder crop-cattle farming systems in Bhutan. Livest. Sci. 132, 126-134. Savadogo, P., Sawadogo, L., Tiveau, D., 2007. Effects of grazing intensity and prescribed fire on soil physical and hydrological properties and pasture yield in the savanna woodlands of Burkina Faso. Agriculture, Ecosystems and Environment 118, 80-92. Schroeder, J.W., 2004. Forage Nutrition for Ruminants. North Dakota State University, North Dakota, pp. 1-22. Sharrow, P.S.H., 2007. Soil compaction by grazing livestock in silvopastures as evidenced by changes in soil physical properties. Agroforestry Systems 71, 215-223. Shrestha, G., Stahl, P.D., 2008. Carbon accumulation and storage in semi-arid sagebrush steppe: Effects of longterm grazing exclusion. Agriculture, Ecosystems and Environment 125, 173-181. Singh, R.P., 1978. Pasture Development in Bhutan (AGOF/BHU/72/010). Thimphu. Stephens, D.W., Krebs, J.R., 1986. Foraging theory. Princeton University Press, Guildford. Stoddart, L.A., Smith, A.D., Box, T.W., 1975. Range Management. McGraw-Hill Book Company, New York, USA. Stuart-Hill, H.C., 1992. Effects of elephants and goats on the Kaffrarian succulent thicket of the eastern Cape, South Africa. Journal of Applied Ecology 29, 699-710. Takatsuki, S., 1992. A case study on the effects of a transmission-line corridor on Sika deer habitat use at the foothills of Mt Goyo, northern Honshu, Japan. Ecological Research 7, 141-146. Teague, W.R., Dowhower, S.L., Baker, S.A., Haile, N., DeLaune, P.B., Conover, D.M., 2011. Grazing management impacts on vegetation, soil biota and soil chemical, physical and hydrological properties in tall grass prairie. Agriculture, Ecosystems and Environment 141, 310-322. Thapa, G.B., Paudel, G.S., 2000. Evaluation of the livestock carrying capacity of land resources in the Hills of Nepal based on total digestive nutrient analysis. Agriculture, Ecosystems and Environment 78, 223-235. Tshering, P., 2005. The Interaction of Grazing and Competition in the Conifer Forest of Bhutan. Institute of Forest Ecology. University of Natural Resources and Life Sciences, Vienna. 14

Vallentine, J.F., 1990. Grazing Management. Academic Press, San Diego, CA. Wallis DeVries, M.F., Laca, E.A., Demment, M.W., 1999. The importance of scale of patchiness for selectivity in grazing herbivores. Oecologia 121, 355-363. Wangchuk, K., Darabant, A., Rai, P.B., Wurzinger, M., Zollitsch, W., Gratzer, G., 2014. Species Richness, Diversity and Density of Understory Vegetation along Disturbance Gradients in the Himalayan Conifer Forest. Journal of Mountain Science 11, 1182-1191. Wangda, P., Ohsawa, M., 2006. Forest Pattern Analysis Along the Topographical and Climatic Gradient of the Dry West and Humid East Slopes of Dochula, Western Bhutan. Journal of Renewable Natural Resources, Bhutan 2, 117. Westenskow-Wall, K.J., Krueger, W.C., Bryant, L.D., Thomas, D.R., 1994. Nutrient quality of bluebunch wheatgrass regrowth on elk winter range in relation to defoliation. Journal of Range Management 47, 240-244. Widmer, Y., 1998. Pattern and performance of understory bamboos (Chusquea sp.) under different canopy closures in old-growth oak forests in Costa Rica. Biotropica 30, 400-415. Young, C.C., 1998. Defining the Range: The Development of Carrying Capacity in Management Practice. Journal of the History of Biology 31, 61-83. Zhou, Y.C., Wu, B.S., 1997. Study on nutrient characteristics of the leaves of Bambusa distegia. Journal of Bamboo Research 16, 13-18.

15

fig 1

16

fig 2

17

highlights 1.

Cattle carrying capacity differed according to understory vegetation types.

2.

Carrying capacities were highest for vegetation with 100% Y. microphylla.

3.

Carrying capacity was about one livestock unit year-1 ha-1 for 50% Y. microphylla.

4.

Carrying capacity was lowest for S. alata, S. adnata and R. nepalensis vegetation.

Table 1 Consumable dry matter yield and nutrient content of plants from grazed and ungrazed plots according to major occurring understory species on logged sites in the mixed conifer forests. Means with different letters are significantly different. Dominant understory vegetation 100% Yushania microphylla

50% Yushania microphylla

Synotis alata

Sambucus adnata

Rubus nepalensis

ɖ

EDMɖ

NDFʓ

ADF£

CP¥

Caπ

P∞

t ha-1yr-1

g kg-1DM

g kg-1DM

g kg-1DM

g kg-1DM

g kg-1DM

Grazed

4.19 b

612.9 b

512.4

70.6 a

64.7

2.30 a

Ungrazed

13.99 a

665.5 a

557.0

40.8 b

61.0

1.70 b

Grazed

0.55 b

456.2 b

322.7 b

133.1 a

31.0 a

1.80 a

Ungrazed

2.93 a

694.9 a

436.9 a

107.1 b

13.8 b

1.30 b

Grazed

0.80

383.1

362.6

143.2

37.0

2.30

Ungrazed

1.78

374.0

424.4

170.1

34.7

2.70

Grazed

0.33

432.9

376.1

178.3

34.1

2.40

Ungrazed

0.99

478.4

337.2

148.8

23.6

2.00

Grazed

0.96

345.7 b

304.1 b

144.1

30.8 a

2.20 a

Ungrazed

1.02

541.2 a

436.2 a

133.6

21.5 b

1.60 b

Plot type

Edible Dry Matter, ʓNeutral Detergent Fiber, £Acid Detergent Fiber, ¥Crude Protein, πCalcium, ∞Phosphorus,

Table 2 Forage utilization (FU) of consumable dry matter according to understory vegetation and offtake of nutrients from logged sites in mixed conifer forests. Means ± SE. Dominant understory vegetation

100% Yushania microphylla

Forage utilization yr-1

Offtake(t ha-1 yr-1)

FU∞

EDM£

TDN┼

DCPβ

0.51 ± 0.03

9.80 ± 0.94

4.37 ± 0.73

0.26 ± 0.05

18

∞

50% Yushania microphylla

0.59 ± 0.06

2.39 ± 0.44

1.22 ± 0.22

0.22 ± 0.05

Synotis alata

0.52 ± 0.05

0.51 ± 0.27

0.55 ± 0.41

0.11 ± 0.03

Sambucus adnata

0.62 ± 0.11

0.67 ± 0.25

0.44 ± 0.16

0.07 ± 0.03

Rubus nepalensis

0.59 ± 0.04

0.98 ± 0.18

0.16 ± 0.07

0.04 ± 0.01

Coefficient of Utilization, £Edible Dry Matter, ┼Total Digestible Nutrients, βDigestible Crude Protein

19