Adaptive management of sika deer populations in Hokkaido, Japan: theory and practice

We investigated the utility of adaptive management (AM) in wildlife management, reviewing our experiences in applying AM to overabundant sika deer (Cervus nippon) populations in Hokkaido, Japan. The management goals of our program were: (1) to maintain the population at moderate density levels preventing population irruption, (2) to reduce damage to crops and forests, and (3) to sustain a moderate yield of hunting without endangering the population. Because of significant uncertainty in biological and environmental parameters, we designed a “feedback” management program based on controlling hunting pressure. Three threshold levels of relative population size and four levels of hunting pressure were configured, with a choice of four corresponding management actions. Under this program, the Hokkaido Government has been promoting aggressive female culling to reduce the sika deer population since 1998. We devised a harvest-based estimation for population size using relative population size and the number of deer harvested, and found that the 1993 population size (originally estimated by extrapolation of aerial surveys) had been underestimated. To reduce observation errors, a harvest-based Bayesian estimation was developed and the 1993 population estimate was again revised. Analyses of population trends and harvest data demonstrate that hunting is an important large-scale experiment to obtain reliable estimation of population size. A serious side effect of hunting on sika deer was inadvertent lead poisoning of large birds of prey. The prohibition of the use of lead bullets by the Hokkaido Government was successful in reducing the lead poisoning, but the problem still remains. Two case studies on sika population irruption show that the densities set by maximum sustainable yield may be too high to prevent damage to agriculture, forestry, and/or ecosystems. Threshold management based on feedback control is better for ecosystem management. Since volunteer hunters favor higher hunting efficiency in resource management (e.g., venison), it is necessary to support the development of professional hunters for culling operations for ecosystem management, where lower densities of deer should be set for target areas. Hunting as resource management and culling for ecosystem management should be synergistically combined under AM.     

Edge effects created by clear-cutting on habitat use by sika deer on Mt. Goyo,northern Honshu,Japan

Clear-cutting increased the species diversity and amount of undergrowth plants in a habitat of Sika deer (Cervus nippon) on Mt. Goyo, northern Japan. The number of species increased from 15 to 48 as a result of clear-cutting. Among the plants,Sasa nipponica (a dwarf bamboo), an important forage plant for Sika deer, was predominant. Fecal pellets of deer were abundant in the forest and at the “adjacent zone” (from the edge to 150 m out of the forest) and thereafter decreased suddenly. The intensity of utilization ofSasa nipponica was also heavy in the forest, moderate at the adjacent zone and light 200 m from the forest edge. Since the amount of the bamboo in the forest was small, the removal of bamboo was greatest at the adjacent zone. Clear-cutting creates a favorable feeding area for Sika deer in this zone by increasing the available plant production and securing forest cover.     

梅花鹿的微卫星多态性及种群的遗传结构

梅花鹿是我国极度濒危的鹿科动物,其野生种群已濒临灭绝。为了探讨我国野生梅花鹿的保护和管理对策,我们选用了16 个微卫星位点检测来自东北、四川、江西和浙江种群的122 份样品,以此分析我国野生梅花鹿种群的遗传多样性和遗传结构。费希尔确切性检验表明,四个种群中均存在偏离哈迪- 温伯格平衡的现象。与其它的濒危动物相比,中国梅花鹿有着相对较高的遗传多样性:每个位点的平均等位基因数为4 个,平均期望杂合度为0. 559。四个种群中,东北种群拥有最高的平均等位基因数(n = 3. 688),东北种群、四川种群、江西种群以及浙江种群的平均期望杂合度分别为0. 584,0. 477,0. 585 和0.589,它们之间不存在显著的差异。同时,利用逐步突变模型、双相突变模型和无限等位基因突变模型检测了种群的瓶颈效应,结果表明:除四川种群外,其他种群在近期内都经历过遗传瓶颈。费希尔确切性检验及配对样品F ST 的结果均表明:四个梅花鹿种群间存在显著的遗传分化(P < 0. 001)。因此,我们建议将我国梅花鹿的野生种群划分为4 个管理单元进行保护和
管理。     

Summer dietary compositions of sika deer on Yakushima Island,southern Japan

Summer food habits of Sika deer (Cervus nippon yakushimae) on Yakushima Island, southern Japan, were studied focusing in particular onPseudosasa owatarii, a dwarf bamboo native to the island. Fecal analyses showed that the food habit of the Sika deer on Yakushima island was plastic: the dietary composition was dominated by graminoids (ca. 90%), particularlyP. owatarii (50%–60%) in the bamboo grassland of theP. owatarii zone above the timber line, whereas leaves and non-leafy parts of woody plants were important in the crytomeria forest and evergreen broad-leaved forest below the timber line. The maximum culm age ofP. owatarii was 8.5 yr, but the majority of leaves (97.8%) were younger than 2.5 yr. Since the weight contribution of the leaves is great (27.7%) and the turnover rate is high, theP. owatarii grassland affords a good foraging place for the Sika deer on Yakushima Island.     

Genetic variation and population structure of the Japanese sika deer (Cervus nippon) in Hokkaido Island, based on mitochondrial D-loop sequences

Mitochondrial DNA (mtDNA) D -loop region sequences (602 bp) from 141 samples of the sika deer Cervus nippon collected from Hokkaido Island of Japan were investigated to elucidate population genetic structure. All animals possessed seven repeat units (38 or 39 bp each) in the sequences. Comparison of the 602-bp sequences showed four sites of transitional mutations (A↔G or C↔T). Based on combination of the substitutions, six D -loop haplotypes (a–f types) were identified in the Hokkaido population, suggesting the occurrence of at least six maternal lineages. Distribution maps of the haplotypes constructed using the Geographic Information System showed that the distribution patterns differed from haplotype to haplotype. In particular, distribution of the major three types (a-, b-, and c-types) almost overlapped with three main areas of coniferous forests in Hokkaido. These results suggest that expansion of the sika deer population could have occurred through the habitat of coniferous forests after the historical bottleneck in Hokkaido.     

Temporal change in the spatial genetic structure of a sika deer population with an expanding distribution range over a 15-year period

Since the 1980s, the sika deer (Cervus nippon Temminck, 1838) population of Hokkaido, Japan, has grown, resulting in range expansion. To assess the effects of this range expansion on the spatial genetic structure of the population, we compared subpopulation structures during 2 different periods (168 samples for 1991–1996, and 169 samples for 2008–2010), using mitochondrial DNA (mtDNA; D-loop) and microsatellites (9 loci). The number of gene-based subpopulations decreased across the 15-year period; specifically from four to three subpopulations based on mtDNA, and from two to one subpopulation based on microsatellite DNA. The fusion of the two northern subpopulations caused the change to the mtDNA-based structure, which might be explained by the dispersal of females from higher to lower density subpopulations. In comparison, the reason for the change in the microsatellite DNA-based structure was unclear, because no significant genetic differentiation was observed between the two study periods. A stable mtDNA-based structure was maintained in the north and central population separated by a west-to-east boundary, while a north-to-south boundary in eastern Hokkaido maintained stability in the eastern subpopulation versus all other subpopulations. The findings of this study demonstrate the importance of understanding gene flow within a structured population to implement effective management efforts; for instance, the culling of one subpopulation might not affect an adjacent subpopulation, because deer movement is limited between the subpopulations.     

Food habits of sika deer and nutritional value of sika deer diets in eastern Hokkaido, Japan

Rumen content analysis and field observations were used to investigate the food habits and diet quality of sika deer (Cervus nippon yesoensis Heude) from 1991 to 1993 in eastern Hokkaido, Japan. Diets varied seasonally, with deer consuming graminoids and browse in winter, forbs and agricultural crops in spring and summer and all of these plant foods in autumn. Eighty-four plant species with sika deer bite marks were identified and their use also varied seasonally. The diversity of food resources available provided both critical protein and digestible energy, allowing for physiological maintenance and seasonal growth. With these high-quality diets, deer maintained good body condition in eastern Hokkaido, where the population density was relatively low.     

A genetic study of sika (Cervus nippon) in the New Forest and in the Purbeck region, southern England: is there evidence of recent or past hybridization with red deer (Cervus elaphus)?

Sika Cervus nippon are native to Japan and East Asia but are now naturalized in many parks of the world, including Britain. In contrast to the substantial body of research on the extent of hybridization between sika and red deer Cervus elaphus in Scottish populations, there has been little genetic analysis of the English populations of sika. Sika in England still have a patchy and discontinuous distribution; populations are thus still genetically isolated and may be expected to show higher variability in genetic type. The current paper uses DNA-based techniques to explore the genetic composition of sika in the New Forest (Hampshire) and that of sika from the largest population in England, in the Purbeck region (Dorset). The study aims were to determine whether New Forest sika show signs of recent interbreeding with New Forest red deer populations, whether New Forest sika are genetically distinct from Purbeck sika, and whether New Forest and Purbeck sika show evidence of past hybridization or whether they are pure (non-hybrid) strains. Microsatellite analysis was used to compare the genetic profiles of individual deer. Results showed that sika and red deer in the New Forest were genetically distinct, indicating that there is no large-scale in situ hybridization occurring between these feral populations. In terms of overall genetic composition, there was no significant difference between the sika in the New Forest and Purbeck. However, a more detailed analysis found that New Forest sika showed a lower level of introgression with red deer compared with the Purbeck sika. We conclude that, overall, the New Forest sika deer do appear to be more genetically pure bred than the Purbeck sika.     

东北梅花鹿初级卵母细胞的超微结构

研究东北梅花鹿初级卵母细胞发育的超微结构变化,目的是为探索东北梅花鹿初级卵母细胞的发育规律提供组织学和形态学依据。本研究于2003年和2004年的6月初到8月末取3只、9月中旬到10月初取4只,共计7只健康经产2~3胎的成年东北梅花鹿卵巢;卵巢经2·5%戊二醛固定液固定后,切取约1mm3的卵巢皮质和直径0·5~1·5mm及1·5~3mm的卵泡作为电镜观察用材料;该材料经0·1MpH7·2的PBS漂洗、1%锇酸固定、不同浓度乙醇脱水后,再经Epon812和丙酮等量混合液浸透,最后用Epon812包埋制块,并用半薄切片机切成0·5~2μm半薄切片;再经亚甲基兰-天青Ⅱ染色后,在光镜下进行卵泡分类和卵母细胞定位;将经定位的材料用超薄切片机切成厚度为700~800的切片,经醋酸铀和柠檬酸铅双重染色后,用透射电镜观察、记录并照相。观察时将卵泡依其直径大小、透明带的形成、卵泡腔的出现等分为原始卵泡、初级卵泡、次级卵泡和三级卵泡4类。研究结果表明,在原始卵泡阶段,卵母细胞为较规则的圆形,质膜与卵泡细胞膜紧密相贴,有时形成桥粒,细胞器多分布于近核区,高尔基体不典型,线粒体多为圆形,嵴较少;在次级卵泡阶段,2~4层的卵泡细胞局部开始形成透明带,4层以上时形成薄的透明带,微绒毛斜伸入透明带内,方向不规律;在直径为0·5~1·5mm的三级卵泡阶段,卵母细胞的透明带增厚,各种细胞器在皮质区内数量较多,皮质区内高尔基体的数目增多,粗面内质网明显减少;在直径为1·5~3mm的三级卵泡阶段,卵母细胞的透明带继续加厚,微绒毛缩短变弯,开始从透明带退出,许多皮质颗粒开始排列在卵母细胞膜下。     

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

Forage biomass and habitat use of Sika deer (Cervus nippon) at a transmission-line corridor were studied at the foothills of Mt Goyo, northern Japan. Summer forage biomass in the corridor was five times greater than in the adjacentBetula grossa forest. Among the plants that increased in the corridor,Sasa nipponica (a dwarf bamboo), an important forage plant for Sika deer, was predominant. Winter utilization ofS. nipponica by Sika deer was slightly heavier in the corridor, and estimated removal ofSasa leaves was twice as great there as in the forest. However fecal pellets were more prevalent in the adjacent forest in winter. Sika deer seemed to use the transmission-line corridor as a feeding site and the adjacent forest as cover as it reduces wind speed. A transmission-line corridor is more beneficial than a large clear-cut area because it provides more forest edges.     

Evaluation of relative density indices for sika deer in eastern Hokkaido, Japan

We evaluated relative density indices of sika deer (Cervus nippon) to aid in population management. We monitored sika deer population trends from 1992 to 2002 in the eastern part of Hokkaido Island, northern Japan, using spotlight surveys, aerial surveys, catch per unit effort (CPUE), sighting per unit effort (SPUE), and cost of damage to agriculture and forestry. We assumed that the artificial bias in the spotlight index would be lower than in other indices, and compared temporal patterns of other indices to those produced using spotlight surveys using model II regression. There was a significant correlation between the damage cost index and the spotlight index, and both indices indicated consistent population trends. Managers used CPUE as a tool to determine hunting quota efficiency. The SPUE index had the smallest standard error among the indices, and the spotlight survey index had the second smallest standard error. Overall, the spotlight survey was the most useful index because its estimate error was small and it was precise in showing population trends; however, spotlight surveys did lead to underestimation once in 1994. The SPUE index seems to be effective in checking the validity of the spotlight index, but there are so many environmental and demographic uncertainties that several independent indices should be used and crosschecked for accurate evaluation of population trends.     

Variable extent of hybridization between invasive sika (Cervus nippon) and native red deer (C. elaphus) in a small geographical area

Instances of hybridization between endemic and alien species pose a threat to species integrity but also provide us with an opportunity to study the dynamics of gene flow between two species as they first meet. Here, we used variation at 22 highly differentiated microsatellite loci and one mitochondrial DNA (mtDNA) marker in a sample of 735 individuals, to investigate the genetic consequences of an introduction of Japanese sika deer ( Cervus nippon ) for native red deer ( C. elaphus ) on the Kintyre Peninsula in Scotland. We investigated population structure, estimated null-allele frequency and assigned individual hybrid scores using a Bayesian clustering algorithm implemented in structure 2.2. The dataset clearly divided into two clusters and generally, introgression into red and sika was low. However at one site, West Loch Awe, 43% of individuals were hybrids. MtDNA introgression indicated that hybridization was occurring between red-deer hinds and sika-deer stags. We argue that the pattern of differential introgression across the study area is primarily due to the rarity of hybridization events between the two species and the limited time the two species have been in contact (< 120 years). This contrasts with the causes of classic mosaic hybrid zones (selection induced by habitat variability). Currently, it seems possible that, in time, the level of hybridization found at West Loch Awe could also be found across the whole of the peninsula.     

Characteristics of Sasa nipponica grassland as a summer forage resource for sika deer on Mt Ohdaigahara, central Japan

Recently, the sika deer, Cervus nippon Temminck, population has increased on Mt Ohdaigahara, central Japan. The dwarf bamboo, Sasa nipponica Makino et Shibata, is a primary forage plant for sika deer in this area. To demonstrate the characteristics of S. nipponica grassland, especially as summer forage for sika deer, the habitat use intensity of sika deer was estimated by fecal densities, and biomass, growth rate, removal by deer and crude protein content were examined. Sika deer utilized the S.nipponica grassland on Mt Ohdaigahara during summer when the biomass, growth rate and crude protein content of S. nipponica were high. The recent increase in the deer population seems to be partly due to S.nipponica grassland being a favorable summer habitat.     

Food habits of Sika deer on Mt. Goyo,northern Honshu

The food habits of Sika deer (Cervus nippon) on Mt. Goyo, northern Honshu (the main island of Japan), were studied. Among 88 plant species found in surveys, 36 species (40.9%) were eaten by the deer. The percentage frequency of feeding (F) was highest for graminoids (59.6%), followed by browses (16.6%) and ferns (7.7%) and lowest for forbs (5.4%). Though various kinds of plants were eaten, only limited species formed the bulk of the deer dietary composition.Sasa nipponica, in particular, was the most important constituent, ranking highest inF value (80.3%) and being the dominant component of feces. Fecal analyses revealed that, 1) in areas lower than 900 m in altitude,Sasa nipponica accounted for between 20 and 60% of the content and that pasture grasses were also important, and 2)S. nipponica occupied more than 50% in montane areas higher than 900 m, and even more than 80% in winter. The utilization ofS. nipponica as a forage for Sika deer was discussed. This plant can be a key forage species because it meets all the necessary conditions: abundance and stability of supply, palatability, nutritive quality and tolerance to grazing.     

Species diversity and community structure of rove beetles (Coleoptera: Staphylinidae) attracted to dung of sika deer in coniferous forests of southwest Japan

Insect communities of mammal dung have been known as excellent model ecosystems for scientific study. Ecological surveys of diversity and seasonal patterns of coprophilous rove beetles in relation to wild mammals have rarely been conducted, although the high potential species diversity and abundance of the rove beetles are known. In order to investigate biodiversity of these beetles, we analyzed species composition, abundance, feeding guild and seasonality of rove beetles that were attracted to sika deer Cervus nippon dung by using dung‐baited pitfall traps for a 1.5‐year study in two plantations (cypress, cedar) and one secondary natural forest (pine) in Fukuoka Prefecture, southwest Japan. Consequently, saprophagous Anotylus sp. (Oxytelinae) was dominant in all forests. Analyses of feeding guild structure showed the number of individuals were dominated by saprophagous beetles, but the number of species were dominated by predatory beetles. Seasonal effects suggested that the species richness and abundance of rove beetles are possibly regulated by scarabaeoid dung beetles. These findings feature one example of a coprophilous rove beetle community.     

Bottlenecks, drift and differentiation: the population structure and demographic history of sika deer (Cervus nippon) in the Japanese archipelago

We assessed genetic differentiation and diversity in 14 populations of sika deer (Cervus nippon) from Japan and four populations of sika deer introduced to the UK, using nine microsatellite loci. We observed extreme levels of differentiation and significant differences in diversity between populations. Our results do not support morphological subspecies designations, but are consistent with previous mitochondrial DNA analyses which suggest the existence of two genetically distinct lineages of sika deer in Japan. The source of sika introduced to the UK was identified as Kyushu. The underlying structure of Japanese populations probably derives from drift in separate glacial refugia and male dispersal limited by distance. This structure has been perturbed by bottlenecks and habitat fragmentation, resulting from human activity from the mid-nineteenth century. Most current genetic differentiation and differences in diversity among populations probably result from recent drift. Coalescent model analysis suggests sika on each of the main Japanese islands have experienced different recent population histories. Hokkaido, which has large areas of continuous habitat, has maintained high levels of gene flow. In Honshu the population is highly fragmented and is likely to have been evolving by drift alone. In Kyushu there has been a balance between gene flow and drift but all the populations have experienced high levels of drift. Habitat fragment size was not significantly associated with genetic diversity in populations but there was a significant correlation between habitat fragment size and effective population size.     

Seasonal migration patterns of female sika deer in eastern Hokkaido,Japan

Fifty-seven female sika deer (Cervus nippon yesoensis), captured at the wintering area in the Shiranuka Hills in eastern Hokkaido, Japan, were radio-tracked during 1997–2001 to examine the factors affecting seasonal migration at the individual-landscape level. Ten of the 57 deers migrated between low-altitude summer home ranges and intermediate-altitude winter home ranges (the upward migrants). Twenty-nine migrated between high-altitude summer home ranges and intermediate-altitude winter home ranges (the downward migrants). Twelve used the intermediate-altitude home ranges all year round (the non-migrants). The remaining six were unknown. The summer home ranges of deer were widely scattered over an area of 5734km². Migration distances ranged between 7.2 and 101.7km. Deer showed high site fidelities to their seasonal home ranges. The upward migrants wintered in areas of less snow, higher quality of bamboo grass, and more coniferous cover than their summer home ranges. The downward migrants wintered in areas of less snow, higher quality of bamboo grass, higher winter temperature, and more southern slopes, but less coniferous cover than their summer home ranges. The non-migrants used year-round ranges with little snow, high quality of bamboo grass, and sufficient coniferous cover. We suggest that snow cover and bamboo grass are the factors affecting seasonal migration of the population and that coniferous cover is another factor for the upward migration.     

Daily rhythm and seasonal pattern of lick use in sika deer (Cervus nippon) in China

Many ungulates are reported to use natural or artificial licks with seasonal patterns around the world. From December 2016 to August 2017, we used infrared camera to record the use of artificial licks in wild sika deer (Cervus nippon) in Zhejiang Qingliangfeng National Nature Reserve, China. We explored the daily rhythm, seasonal pattern and sex difference in lick utilization. In total, 12,043 videos and 22,901 pictures were collected. Our results showed that: (1) the lick visiting frequency was higher at night than that during daytime; (2) the difference in lick visiting frequency between females and males disappeared after taking into account of sex ratio; (3) the lick duration peaked in April during a year. These findings suggested that there were clear daily rhythm and seasonal pattern of lick use in sika deer. Seasonal change in lick use intensity was consistent with our prediction. These variations in lick use might be driven by both the physiological needs of the mineral elements in different life stages and the seasonal changes in climate and food. The reserve management authority should pay more attention to the supplement of licks in spring and summer to fulfill animal’s physiological needs.     

Seasonal food habits of a sika deer population in the warm temperate forest of the westernmost part of Honshu, Japan

The rumen contents of 63 sika deer (Cervus nippon Temminck) shot in the westernmost part of Honshu were analyzed by the point-frame method. The rumen contents were dominated by forbs and the majority of these were evergreen monocotyledonous plants, probably Ophiopogon spp. Evergreen browse leaves (woody leaves), such as Eurya japonica Thunb., Ilex crenata Thunb. and Trachelospermum asiaticum Nakai, were also important, constituting 20–40% of the rumen contents. Other categories accounted for only small proportions, although in summer, graminoids increased but twigs and bark decreased in importance and in fall and winter, fruits and seeds increased in importance. The diet of the deer was characterized by high-quality foods even in winter and by a stability or less-pronounced seasonality throughout the year than found in the northern deer. These results were compared with those from other populations, including a northern sika deer population in Japan.