Research Progress of Effect of Royal Jelly on Honeybee Learning and Memory
Queen and worker are two castes and have completely different jobs in a honeybee colony. The differences in phenotype and function of this two casts are related to their food royal jelly. Royal jelly from young workers serves as an important food source for lifetime of queens and less than three days old of worker larvae, which also plays a critical role in the healthy development of honeybee colony. However, the effects of royal jelly on the cognitive and behavioral ability of honeybees has not yet been elucidated. Therefore, this paper summarizes the research progress on learning and memory of honeybee itself owing to the royal jelly, in order to provide certain theoretical ideas for the future investigation on honeybee’s cognitive behavior.
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牛每天躺卧10~12 h，在其行为中居于首位[1-2]。躺卧反映了牛床舒适度，躺卧时间与牛床干燥和舒适度有关[3]。不同牛床对牛群体表清洁度和机体健康的影响有较大差异。实心混凝土牛床无尿液渗滤功能，牛床潮湿、泥泞，舒适度差。潮湿牛床易滋生细菌，危害牛群健康[4]；牛蹄长期浸泡在粪尿中，导致肢蹄发病率升高[5]。相比舒适度差的实心混凝土牛床，牛群偏好在舒适度更好的秸秆垫料或橡胶垫上躺卧[6]。垫料可增加躺卧舒适度，但劣质垫料可能含有细菌毒素[7]。稻草、木屑、锯末和木削属于有机垫料，受潮后易滋生细菌；沙子垫料清理困难；未经处理的牛粪作为垫料有生物安全隐患，管理难度也很大。漏缝地板对于提高牛床干燥度有明显优势，但站立和舒适度很差[8]。穿孔混凝土地板容易被粪便堵塞[9]，机械清理难度大。发酵床能较好地改善躺卧舒适度，但因垫料成本高而较难在规模化肉牛育肥场中得到广泛应用[10]。本研究自行设计了一种有粪尿及时分离功能的降污牛床，并对其降污性能进行测试，以期为优化牛床结构提供一定的依据，进而提高育肥肉牛的健康与福利化养殖水平。
1. 材料与方法
1.1 降污牛床结构
图1为降污牛床的结构示意图。降污牛床长2.2 m、宽0.8 m，相邻牛床安装了高1.2 m、长0.8 m的镀锌管隔栏，以明确牛群的躺卧区域。牛床末端埋植2根直径10 cm的PVC管道以模拟尿液暗沟，管道上方有宽3 cm的微缝，2条微缝平行且间隔10 cm。PVC管道沿长度方向有1%的坡度延伸至舍外的粪尿沟，清粪道比牛床末端低10 cm。牛床地板向后设3%的坡度，尿液顺坡流入微缝内。实心混凝土对照牛床除末端无微缝外，其他结构和尺寸均与降污牛床一致。
1.2 试验牛群
在云南省德宏傣族景颇族自治州某牧场选择12头健康、体况一致、平均体质量为482 kg的育肥肉牛(本地黄牛♀×西门塔尔牛♂)，随机平均分配到实心混凝土牛床(对照组)和降污牛床(试验组)上拴系饲养7 d，之后再开展14 d的正式测试。2组牛群的饲养管理措施均一致。
1.3 试验方法
1.3.1 环境温、湿度与肉牛的生理参数采集
在牛床上方1.6 m处悬挂温湿度传感器(±0.2 °C，Testo 175H1)，以1 h为间隔连续记录舍内温、湿度。每天08： 00、13： 00和18： 00，将兽用温度计插入肉牛直肠3 min后读取直肠温度；以秒表记录牛1 min的腹部起伏次数，连续记录3次，取平均值作为呼吸频率。
1.3.2 地板卫生评估
每天08： 00和18： 00对牛床进行清扫，并于08： 00、13： 00和18： 00将1个含有44个网格的栅栏(20 cm×20 cm)平放在牛床上，参照前人的方法[11]，分别计数干净、尿液、干粪和粪尿混合的方格数。针对降污牛床末端微缝内的牛粪数量分别日清理2、3和4次，并以上述方法评估微缝的卫生状况。
1.3.3 牛体表清洁度评分
为避免人为误差，每天由同一观察员在08： 00、13： 00和18： 00对牛群的乳房、腿部、脚部、腹部和尾部的卫生清洁度进行评分。参照前人的4分法[12]对肉牛开展体表清洁度评分(表1)，分值越高，体表清洁度越差。
表 1 育肥肉牛的体表清洁度评分标准[12]Table 1. Scoring standard for body surface cleanliness of fattening beef cattle部位 parts 1 分 one point 2 分 two points 3 分 three points 4 分 four points 尾部 tailhead 
腿部 leg 
脚部 foot 
乳房 udder 
腹部 abdomen 
1.3.4 动物行为监测
在牛舍适当位置安装高清视频摄像头， 通过网络摄像机 [ 海康威视， DS-7804N-K1/4P(D)]、 硬盘录像机(海康威视， DS-2CD3T47EWDV3-L 4 mm)和网络交换机(TP-LINK TL-WDR5620 GB版) 24 h全覆盖记录牛群的各种行为。各种行为的定义为：采食是通过嘴将饲料摄入体内的过程；反刍是在躺卧或站立状态观察到逆呕、咀嚼或吞咽现象；饮水是嘴部接触水槽；躺卧是躯干主体部分与地面接触；站立是躯体由四肢支撑；纯站立是未采食期间的站立；排泄是尾根抬起，拱背，后肢分开稍向前，有粪尿排出。试验结束后，从视频文件中人工提取目标行为数据。
1.4 数据处理与统计分析
采用Excel 2010对数据进行整合；采用SPSS 21.0对数据进行独立样本t检验。数据结果表示为“平均值±标准误”。
2. 结果与分析
2.1 生理参数
试验期间，气温为20.8~28.64 ℃，相对湿度为65%~86%。对照组和试验组牛群的平均直肠温度均为38.5 ℃；呼吸频率分别为22.1次/min和22.7次/min。
2.2 地板卫生
由图2a可知：2种牛床的干净面积占比均最高，尿液污染面积均最小。与对照牛床相比，降污牛床的干净和干粪面积分别增加9.7%和3.29% (P>0.05)，尿液和粪尿混合的污染面积则分别降低1.42%和11.24% (P>0.05)，说明降污牛床更干燥。由图2b可知：每天清理降污牛床末端微缝3~4次时，尿液和粪尿混合污染面积均低于清理2次时，但干粪覆盖面积高于清理2次时；每天清理降污牛床微缝4次时，尿液和粪尿混合的覆盖面积均低于清理3次时，但干粪覆盖面积高于清理3次时。可见，适度增加末端微缝的清理次数，可以减少降污牛床的污染面积。
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图 2 牛床地板的卫生状况注：a) 对照牛床和降污牛床的卫生状况；b) 微缝清理次数对降污牛床卫生的影响。“*”表示差异显著 (P<0.05)，“**”表示差异极显著 (P<0.01)；下同。Figure 2. Hygienic conditions of cattle bedNote: a) hygienic conditions of control cattle bed (Ctrl-bed) and cattle bed with reducing pollution (CBRP-bed); b) effect of micro-crack cleaning times on the hygienic condition of CBRP-bed. “*” indicates significant differences (P<0.05), “**” indicates extremely significant differences (P<0.01); the same as below.2.3 育肥肉牛的体表清洁度
由图3a可知：2类牛床的牛群均是脚部清洁度评分最高，左右腿和腹部的受污染程度较为严重，乳房清洁度评分最低。对照牛床牛群各部位清洁度评分均高于降污牛床牛群；除左腿外，对照组牛群的其他体表部位清洁度评分均显著或极显著高于降污牛床牛群(P<0.05或P<0.01)，表明降污牛床可改善拴系育肥肉牛的体表清洁度。由图3b可知：每天清理降污牛床微缝4次时，牛群左脚清洁度评分显著低于清理2~3次(P<0.05)；其他部位的清洁度评分虽无显著差异，但清理4次均可提高牛群的体表清洁度。
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图 3 牛群体表清洁度注：a) 对照牛床和降污牛床的牛群体表清洁度评分；b) 微缝清理次数对降污牛床牛群体表清洁度的影响。Figure 3. Cleanliness of beef cattle body surfaceNote: a) cleanliness score of beef cattle body surface in Ctrl-bed and CBRP-bed; b) effect of micro-crack cleaning times on the cleanliness score of beef cattle body surface in CBRP-bed.2.4 拴系育肥肉牛的行为
由表2可知：对照和降污牛床牛群的采食和饮水行为均无显著差异(P>0.05)；两类牛群排泄次数虽有显著差异(P<0.05)，但排泄行为的持续时间无显著差异(P>0.05)；站立和躺卧行为也无显著差异(P>0.05)，但降污牛床牛群的躺卧时间更长、站立时间更短；对照和降污牛床牛群的反刍时间有极显著差异(P<0.01)，反刍次数也存在显著差异(P<0.05)。
表 2 对照牛床和降污牛床对育肥肉牛行为的影响Table 2. Effects of control cattle bed (Ctrl-bed) and cattle bed with reducing pollution (CBRP-bed) on the behaviors of fattening beef cattle行为 behaviors 对照牛床 Ctrl-bed 降污牛床 CBRP-bed 采食 feeding 累计时间/min cumulative time 264.81±14.84 275.08±9.89 次数 times 36.57±2.83 29.17±2.41 每次持续时间/min duration each time 11.83±0.73 12.23±0.55 饮水 drinking 累计时间/min cumulative time 17.17±1.93 18.62±2.64 次数 times 15.74±1.80 13.43±1.63 每次持续时间/min duration each time 1.23±0.14 1.55±0.25 站立 standing 累计时间/min cumulative time 528.37±43.40 446.38±60.70 次数 times 9.12±0.99 10.41 ±1.10 每次持续时间/min duration each time 68.99±9.86 65.74 ±11.75 纯站立 stand-only 累计时间/min cumulative time 373.97±26.91 288.66± 31.38 次数 times 50.74±5.08 44.36±1.40 每次持续时间/min duration each time 8.07±1.03 6.64±0.64 躺卧 lying 累计时间/min cumulative time 617.23±33.14 702.70± 45.22 次数 times 9.12±0.99 10.41±1.10 每次持续时间/min duration each time 75.74±5.36 77.38±5.69 反刍 ruminant 累计时间/min cumulative time 426.82±16.93 B 498.13±10.45 A 次数 times 20.00±0.86 b 22.38±0.49 a 每次持续时间/min duration each time 21.74±0.54 23.22±0.62 排泄 excretion 累计时间/min cumulative time 6.64 ± 2.24 5.26±0.56 次数 times 10.26±0.79 b 13.69±0.76 a 每次持续时间/min duration each time 0.75±0.33 0.40±0.04 注：同行不同小写字母表示差异显著 (P<0.05)，不同大写字母表示差异极显著 (P<0.01)。
Note: In the same row, different lowercase letters indicate significant differences (P<0.05), different uppercase letters indicate extremely significant differences (P<0.01).3. 讨 论
3.1 降污牛床的卫生状况
牛床卫生与地板类型和清理次数有关[13]。降污牛床末端的粪污暗沟上设有2条平行微缝，尿液在理论上流动舒畅，能快速实现粪尿分离，提高牛床干燥度和卫生状况。降污牛床的微缝仅将尿液引入下方的粪污暗沟内，多数粪便被截留在牛床上从而实现粪尿分离；降污牛床卫生状况虽不及漏缝地板，但对牛群的肢蹄损伤较小，且有较高的躺卧舒适度。穿孔混凝土地板粪尿分离顺畅[9]，但被牛粪堵塞后的孔洞排尿不顺畅，且清理难度大。“高福利”地板也是通过粪尿及时分离进而改善牛床卫生[14]。排尿顺畅和良好的粪尿分离能力可能是降污牛床干净面积与干粪覆盖面积占比相对较高的主要原因。
3.2 降污牛床对拴系育肥肉牛体表清洁度的影响
牛床对牛群的体表清洁有较大影响[15]，潮湿牛床会降低牛群体表清洁度[16]。与橡胶垫牛床相比，漏缝地板肉牛的体表更干净[17-18]。降污牛床末端的微缝能将尿液及时排出，改善牛床干燥度。尿液在实心地板牛床上流动不畅，牛群体表清洁度低。橡胶垫牛床上尿液流动受阻，牛群体表清洁度比漏缝地板差[19-20]。在进行清洁度评分的7个部位中，有6个部位的清洁度显著优于对照牛床，表明降污牛床有显著改善牛群体表清洁度的功能。
3.3 微缝清理次数对降污牛床卫生和拴系肉牛体表清洁度的影响
增加清理次数能改善牛床清洁度[13]。降污牛床干粪覆盖面积随清理次数的增加而增大，尿液污染面积减少。降污牛床的微缝位于末端，容易被牛粪堵塞；增加微缝清理次数可以缓解堵塞，还能提高地板干燥度和牛群体表清洁度。微缝清理3次时，牛群尾部、腿部和脚部的清洁度较差，这可能是由于微缝3次清理期间，正逢舍外降雨量大，开放式牛舍内的降污牛床潮湿，卫生状况较差。前人也有关于潮湿天气条件下，各类型地板上的动物体表清洁度都降低的报道[21]。降污牛床微缝清理仅将铁钩嵌入微缝内，沿微缝拉动即可，几乎不增加清理难度。因此，适度增加降污牛床微缝的清理次数有利于改善牛群体表清洁度。
3.4 降污牛床对拴系育肥肉牛行为的影响
牛每天有50%~60%的时间处于躺卧状态，躺卧对提高牛群健康和生产性能具有重要意义。降污牛床的牛群躺卧702.70 min/d，高于前人报道的11.0~11.4 h[22-23]，表明降污牛床能较好地满足牛群的躺卧需求。橡胶垫、厚垫料及漏缝地板牛群的躺卧行为无显著差异[24]。橡胶垫和表层铺橡胶垫穿孔地板牛群的躺卧时间比漏缝地板更长[9, 20]，这与牛群偏好在舒适度更高的牛床上躺卧有关。舒适度差的地板有增加肢蹄病的风险[25-26]。已有研究表明：厚垫料牛床可增加牛群的躺卧时间[27]；牛群在垫草牛床上的躺卧时间最长，橡胶垫上次之，混凝土地板上最短[28]。对照牛群的站立时间虽然较长，但与降污牛床牛群相比无显著差异，躺卧时间也无显著差异，但降污牛床牛群每天的躺卧时间比对照牛群多84 min，满足了正常的躺卧需求。降污牛床上尿液流动顺畅，床面干燥，躺卧舒适度高，这可能是牛群躺卧时间增加而站立时间减少的主要原因。与潮湿或覆盖有粪尿混合物的地板相比，牛群偏好在干燥牛床上行走或躺卧[29]，降污牛床能较好地保持干燥，这一特性可能满足了牛群的生理需要，因此其躺卧时间更长。
肉牛偏好在干燥和舒适的牛床上躺卧。反刍行为与地板舒适度有关，降污牛床牛群的反刍时间极显著高于对照牛床，表明舒适的降污牛床有利于育肥肉牛反刍。躺卧状态的反刍行为频繁，夜间牛群大部分躺卧在牛床上，反刍活动也更多[30]。降污牛床牛群的站立反刍和躺卧反刍的时间占比分别为31.6%和68.4%，与前人报道的36.5%和63.4%[31]基本相似。由于采食位固定，拴系肉牛的采食和饮水行为无相互影响[32]，从而无显著差异。与漏缝地板相比，在橡胶垫或垫料牛床[17]、高舒适度牛床[24]的肉牛采食时间和频率无显著差异，这与本研究结果一致。
4. 结 论
降污牛床的干燥度高，卫生状况好，改善了牛群体表清洁度。降污牛床虽然对拴系育肥肉牛的采食和饮水行为无显著影响，但对促进躺卧和反刍行为有积极作用。 此外， 适度增加微缝清理次数有利于提高降污牛床的干燥度和牛群体表清洁度。
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图 1 蜂王浆对蜜蜂学习记忆的总体影响
注：虚线表示尚未得到完全证实的影响。
Figure 1. General effect of royal jelly on the learning and memory of honeybee
Note: The dotted lines are effects that have not well been demonstrated.
表 1 东方蜜蜂与西方蜜蜂的蜂王浆主要成分比较[32]
Table 1 Comparison of the main components of royal jelly between Apis cerana and A. mellifera
% 成分
components东方蜜蜂
A. cerana西方蜜蜂
A. mellifera水分 moisture 65.3±2.5 68.3±1.4 蛋白质 protein 16.4±2.5 12.7±0.8 碳水化合物 carbohydrate 9.4±0.6 11.9±0.7 葡萄糖 fructose 4.8±0.5 5.3±0.5 果糖 glucose 3.6±0.4 5.0±0.5 其他 others 1.3±0.7 1.6±0.4 脂肪 lipid 7.4±0.6 6.1±0.4 10-羟基-2-癸烯酸
10-hydroxy-2-decenoic acid0.9±0.2 2.4±0.2 灰分 ash 1.5±0.2 1.0±0.2 
下载: 导出CSV
表 2 蜜蜂体内王浆主蛋白(MRJPs)的表达及其主要功能
Table 2 Expression of major royal jelly proteins (MRJPs) within honeybees and its main function
王浆主蛋白
MRJPs理化性质
physicochemical property体内表达
expression pattern
within the body预测糖基化位点
predicted
glycosylation sites表达产物糖蛋白含量
在王浆蛋白中的占比/%
proportion of glycoprotein
content in MRJPs已发现在蜜蜂体内的主要功能
identified main functions to honeybee参考文献
references分子质量/ku molecular weight 等电点isoelectric point 氨基酸长度
amino acid length东方蜜蜂
A. cerana西方蜜蜂
A. melliferaMRJP-1 46.86 5.03 413 体内广泛表达
widely expressed in vivo3 37 6 蜜蜂发育与成熟、行为调控、神经系统发育、级型分化、营养等
development and mutation, behavior regulation, nervous system development, caste differentiation, nutrition, and so on[7, 10, 13, 28-29, 33-36] MRJP-2 49.15 6.65 435 蕈形体、咽下腺、脑部
mushroom body,
hypopharyngeal gland, brain2 15 20 卵巢激活、级型决定、社会功能分化、营养等
ovarian activation, caste determination, society function differentiation, nutrition, and so on[8, 10, 13, 29, 35-41] MRJP-3 59.49 6.50 524 体内广泛表达
widely expressed in vivo1 30 40 神经调节、营养等
nervous regulation, nutrition, and so on[10, 29, 33-34, 36, 41-46] MRJP-4 50.67 5.74 444 头部、咽下腺、哺育蜂、蜂王幼虫期
head, hypopharyngeal gland, nurse worker, queen larvae8 5 12 营养等
nutrition, and so on[10, 29, 33, 35-36, 47-49] MRJP-5 68.13 5.95 578 咽下腺、5~26 日龄工蜂
hypopharyngeal gland,
5-26 days old workers4 0 12 促进细胞的生长繁殖、营养等
promote cell growth and reproduction, nutrition, and so on[10, 29-30, 35-37] MRJP-6 47.58 6.01 417 头部、咽下腺、采集蜂
head, hypopharyngeal gland, foragers5 未知
unknown未知
unknown级型分化、营养等
caste differentiation, nutrition, and so on[10, 35, 37, 49-51] MRJP-7 48.66 4.85 426 头部、蕈形体、咽下腺
head, mushroom body, hypopharyngeal gland3 3 0 卵巢激活、营养等
ovarian activation, nutrition, and so on[10, 13, 35-38, 40, 49, 51-52] MRJP-8 45.06 5.81 400 头部、毒囊、胸部、腹部
head, venom, thorax, abdomen6 未知
unknown未知
unknown参与蜂毒引起的过敏反应、营养等
involved in allergic reactions to venom, nutrition, and so on[10, 35, 53-55] MRJP-9 46.27 8.62 403 咽下腺、胸部、腹部、毒囊、触角、受精囊
hypopharyngeal gland, thorax,
abdomen, antenna, spermatheca3 未知
unknown未知
unknown参与蜂毒引起的过敏反应、作为表皮结构成分保护分泌细胞免于蜜蜂毒素引发的损伤、营养等
involved in allergic reactions to venom, acts as a structural component of the epidermis to protect secretory cells from damage caused by toxins, nutrition, and so on[10, 35, 37, 53-56]
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