短嘴金丝燕洞穴生活适应机制研究
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摘要
短嘴金丝燕属雨燕目(Apodiformes)、雨燕科(Apodidae),全世界共有三个亚种,在我国均有分布。分布于湖南省石门县壶瓶山国家级自然保护区的为短嘴金丝燕四川亚种(A.b.innominata),该区是短嘴金丝燕在湖南省内已知的唯一分布区,上海、四川、贵州、湖北、广西和香港也有分布。由于其种群数量少,栖息地狭窄且偏远,人迹罕至,加上其生活习性极为特殊：营巢于黑暗的洞穴,飞行速度快,飞行能力强,活动范围广。因此研究的难度较大,国内外的研究极少,尤其是洞穴生活适应机制与繁殖生态研究,至今尚无系统的报道。
本项研究从1994年至2012年,以壶瓶山自然保护区核心区内神景洞哨所为工作据点,采用逐日连续定点观察、野外调查、声波特征分析、环志标记、摄影摄像、红外线无人值守监测、形态结构解剖、分子系统进化学分析等多种研究手段,对神景洞内的短嘴金丝燕种群的回声定位机制、洞穴巢址选择机制、洞穴繁殖生态行为、昼夜活动规律、适应洞穴生活的生物学特征、迁徙行为等作了较为系统的研究,结果表明：
1、壶瓶山短嘴金丝燕种群数量少,分布狭窄。全区仅有2个溶洞有其分布,其中神景洞1000余巢,2000余个体；鹰子尖溶洞60余巢,120余只个体。环志与个体标记结果说明：该种群的性比为1：1,神景洞种群分为两个“家族”,它们在空间分布上处于不同的洞段。
2、根据短嘴金丝燕的鸣声与其行为的关系,将其分为定位、报警、嬉戏、幼鸟鸣声。2012年6月,使用Avisoft-UltraSoundGate116(e)录音设备对短嘴金丝燕在山洞内自由飞行状态进行实时声音的录制,然后利用声音软件(BatSound software, release1, Pettersson Elektronik AB,瑞典)对其进行分析,结果显示：其回声定位叫声为调频的双脉冲组,组内脉冲间隔很短(6.6+0.42ms),组间脉冲间隔较长(99.3±3.86ms),两者差异显著(t-test：t=-23.888,P<0.01)；对比第一与第二脉冲的声音参数发现,主频和脉冲时程差异不显著,第一和第二脉冲的主频分别为6.2±0.08kHz和6.2±0.10kHz(t=0.572,P>0.05),脉冲时程分别为2.9±0.12ms和3.2±0.17ms(t=.1.550,P>0.05),两者的最高频率(20.1±1.10kHz,15.4±0.98kHz,t=3.239,P<0.01)和最低频率(3.7±0.12kHz,4.0±0.09kHz,t=.2.316,P<0.05)差异显著,第一脉冲的频宽(16.5±1.17kHz)比第二脉冲的(11.4±1.01kHz)要宽(t=3.303,P<0.01)；此外,第一脉冲的能量(.32.5±0.60dB)比第二脉冲的(.35.2±0.94dB)高(t=.2.463,P<0.05)。通过分析还发现,短嘴金丝燕在黑暗的山洞内的回声定位叫声还包含了部分超声波,最高频率可达33.2kHz。
3、营巢洞穴选择机制分析采用SPSS11.5统计软件对神景洞鸟巢的生境选择因子进行聚类分析,结果显示：巢址一般具备四个安全条件,一是高度条件,巢址一般高于地面3m(实际测量最低2.5m),为人和其他动物所不及,从而免遭破坏；二是“孤岛条件”,即巢址与地面之间没有其他动物攀援的通道；三是光线条件,在黑暗的洞穴中(照度小于0.01Lx),短嘴金丝燕可以凭借回声定位能力活动自如,而其他动物则可能活动受限；四是湿度条件,足够的湿度能使巢的唾液成分不会失水而保持良好的粘性,从而保持巢结构的稳定性。
4、短嘴金丝燕洞穴繁殖生态行为研究结果表明：其求偶过程可能在越冬地就已完成,婚配形式为“一夫一妻”的单配制,交配行为可在空中或巢中进行；旧巢利用率100%,仅在产卵前加以修补,无巢的新鸟或巢被破坏的老鸟另建新巢；巢址一般选在既安全、又适于群居的黑暗洞壁上；巢材主要为唾液和苔藓,间杂有少量自身的羽毛和草尖,量度为：巢重17.84+4.18g,外径(88±7.78)×(78.75±8.43)mm内径(71.83±7.95)×(66.91±8.40)mm,巢深25.25±8.10mm。筑巢期长达60d左右。卵长椭圆形,白色无斑,大小为21.3×12.lmm,重量为2.7g；最早产卵于5月31日,最迟为7月20日左右；筑新巢的鸟产卵较晚,最早见于6月26日。大部分产卵2枚,少数产1枚,平均窝卵数为1.7g,一般为连续产卵,偶有间隙1-2d。第一枚卵产出后立即坐巢孵化；雌雄共同孵卵,但以雌鸟为主。孵卵温度为37.28+1.02℃；孵化期为27.85+3.39d；孵出顺序与产卵顺序一致,相差1-3d,孵化率为71.43%。雏鸟晚成性,体重1.68+0.08g,刚出壳时,全身粉红色,裸露无羽,眼未睁开。喂雏的任务主要由雄鸟承担；先出壳的个体始终保持生长优势。育雏期27d左右；雏鸟在洞内学飞,学飞后3-4d后出洞；雏鸟离巢时个体重甚至超过成鸟,离巢后体重有减轻现象。
短嘴金丝燕洞穴内的天敌目前仅发现有白腹巨鼠(Rattus edwardsi),偶有危害鸟蛋、幼鸟、甚至成鸟的现象,但危害不大；洞外的天敌主要是松雀鹰(Accipiter virgatus offinis)、普通鵟(Buteo buteo burmanicu)等猛禽。
昼夜活动规律：早晚离归巢、白天返巢频率、在巢率、集群行为与季节变化、繁殖行为规律相适应。基本上是日出而作,日落而息；繁殖前期,白天在巢率、返巢率逐渐升高,到繁殖中期达到高峰。集群情况在繁殖前、后期较为明显。
5、短嘴金丝燕适应洞穴生活的的生物学特征：前趾型足、四趾末端均具有发达的爪,与柔软而富有弹性的尾羽相互配合,适宜其在洞穴石壁上停歇。体型小,飞行动作快速灵敏,适合在狭窄曲折的洞穴内穿行；呼吸系统鸣肌粗壮,与定位回声发声有关；消化系统具有能分泌粘性唾液的唾液腺,其粘性分泌物是洞穴筑巢的必备物质；食道没有嗉囊,但弹性较大,可以将野外捕获的昆虫粘成食团储存其中,带回洞穴喂饲尚未离巢的雏鸟；循环系统中心脏较一般鸟类发达,其重量可达自身比重的2%；骨骼系统中尤以后肢骨骼特征与洞穴行为最为适应,耻骨末端比坐骨长出约1/3,能更好地起到对盆腔的保护作用,跗跖骨其远端由位于同一平面位置的第2、3、4跖骨滑车组成典型的“滚轴”关节模式,从数据上显示,短嘴金丝燕的后肢骨骼中胫跗骨的长度最长,股骨的长度要长于跗跖骨,并且其股骨、胫跗骨、跗跖骨三段骨骼的比例为1：1.57：0.75,类似如其他雨燕目物种而有别于其他树栖类物种。这些形态结构特点反映了短嘴金丝燕的结构和功能与洞穴生活行为相适应。
分子系统进化分析实验结果显示,短嘴金丝燕与同样具有回声定位能力的爪哇金丝燕(Aerodraus fuciphagus germanni)有较为接近的亲缘关系,其洞穴生活习性有着共同的遗传学基础。
6、短嘴金丝燕为夏候鸟,4月初迁来,11月初迁走；迁离方式为整群一次性；迁入方式为分群体,多次性,居留期为209.1±1.4d(207.213,n=9),迁徙明显与气候、食物因子有关。
The Himalayan Swiftlets (Aerodramus brevirostris), subordinate to Apodidae family and Apodiformes order, comprises three subspecies and can be found in China. The Sichuan subspecies (A.b. innominata) is distributed in Hupingshan National Nature Reserve (NNR) in Shimen County, where it is by far the only distribution area known in Hunan. And the species is also distributed in Shanghai, Sichuan, Guizhou, Hubei, Guangxi and Hongkong SAR in China. The study is a tough one due to certain features of the species, such as small population size, secluded and narrow habitat environment, and particular life habit including nesting in dark caves, rapid flight speed, strong flight performance, as well as wide sphere of activities. Thus domestic and international researches are rare, especially the research on the adaptation mechanism of its cave life and breeding ecology.
The study started in1994and ended in2012, choosing the Shenjing Post for work strongholds, which is located in the core area of Hupingshan NNR. Diverse research methods were adopted, such as day by day consecutive point observation, field survey, morphological structure anatomy, sound wave characteristics analysis, bird banding mark, film and video, infrared unattended monitoring, etc. A certain level of systematic studies have been conducted, mainly on the species selection mechanism of nesting site, echolocation mechanism, breeding ecology behavior, migration behavior, day and night activity rule, and molecular system evolution, etc, with the findings shown as follows:
1. The species has a small population and is only distributed in a very narrow region. There are only two distribution areas found in karst caves within the study area, among which there are about1000nests with2000individuals in Shenjing karst cave, while approximately60nests and120individuals in Yingzijian karst cave. The bird banding and individual mark indicates this species is monogamous with a sex ratio of about1:1. The nest and its location are exclusive with no sign of fights and invasion. The species in Shenging Cave has been separated into two "families", which settle in different sections of the cave in terms of spatial distribution.
2. Based on the relationship of its chirping and the behavior, the chirping of Himalayan Swiftlets can be categorized into:positioning, alarming, playing, and nestling's chirping. In June2012in Shenjing Cave, the free-flying echolocation calls were recorded with Avisoft-UltraSoundGate116(e), and the results were analyzed by certain sound software (BatSound software, release1, Pettersson Elektronik AB, Sweden). The results suggested that the echolocation sounds of Himalayan swiftlets are broadband double FM clicks, separated by a short pause, and the inter-pulse intervals between double clicks (99.3±3.86ms) were longer than those within double clicks (6.6±0.42ms)(t-test:t=-23.888, P<0.01). Except the peak frequency (6.2±0.08kHz,6.2±0.10kHz, respectively; t=0.572, P>0.05) and pulse duration (2.9±0.12ms,3.2±0.17ms; t=-1.550, P>0.05), others (maximum frequency, minimum frequency, frequency bandwidth, and power) were significantly different between the first and second click. The maximum frequency of the first pulse (20.1±1.10kHz) was higher than that of second (15.4±0.98kHz)(t=3.239, P<0.01), while the minimum frequency of the first pulse (3.7±0.12kHz) was lower than that of second (4.0±0.09kHz)(t=-2.316, P<0.05); resulting in the frequency bandwidth of the first pulse (16.5±1.17kHz) was longer than that of second (11.4±1.01kHz)(t=3.303, P<0.01). The power of the first pulse (-32.5±0.60dB) was higher than that of second (-35.2±0.94dB)(t=-2.463, P<0.05). More important, we found that Himalayan swiftlets emitted echolocation pulses including ultrasonic sound, that the maximum frequency reached33.2kHz.
3. Analysis of nesting cave selection mechanism. The clustering analysis concerning habitat selection impact factors in Shenging Cave has been conducted by SPSS11.5. Findings indicate that four safety conditions are required for the nesting selection. The first is the height of the nest, which requires3m higher above the ground (the actual measurement is at least2.5m), often beyond man or other animals'reach so as to keep the nest from being damaged. The second is the "islet condition", referring to the passageway between the nest and the ground to prevent other animal from climbing to the nest. The third is the light condition, for Himalayan Swiftlets can move flexibly by echolocation capability while other animals' movement may be confined in dark caves. And the Fourth is the humidity, which means sufficient humidity may help maintain good stickiness of saliva and thus keep stable structure of the nest.
4. Breeding ecology behavior of Himalayan Swiftlets. The courtship process may be fulfilled in wintering ground on the basis of monogamy, with mating conducted in the air or in the nest. The old nest can be fully reused, only mended before hatching. For those with no nest or the nest destroyed, they have to build new ones, which are usually on secure cave walls suitable for living in groups. The nests are primarily composed of saliva and mosses, mixed with a little feather and grasses. The nest weights17.84±4.18; in terms of nest measurement, the external and internal diameter as well as the depth are (88±7.78)×(78.75±8.43),(71.83±7.95)×(66.91±8.40) and25.25±8.10respectively. Nest construction can take up to60days. The eggs are oblong, white, unspotted, with a size of21.3×12.1mm and a weight of2.7g. The earliest egg laying starts on31May, while the latest on around20July. If nest building is ongoing, the egg laying is often delayed, with the earliest date known on26June. In most cases, two eggs can be found for each couple each reproductive season, yet one egg per couple is also occasionally observed, thus the average amount for each couple is1.7eggs. The egg laying usually goes on continually, occasionally ceasing for just one day or two. And egg hatching starts immediately after the laying of the first egg. Both males and females are involved in hatching but females invest more time in it. The hatching temperature is37.28±1.02℃, the duration is27.85±3.39days, and the hatching rate is71.43%. The brooding sequence conforms to the hatching sequence, difference in1-3days. Nestlings usually weigh1.68±0.08g, with little body totally pink, covered with no feather and eyes yet not open when just getting out of shells. Nestlings are altricial brooding, and are fed by parents for about27days. After that, they spend some extra3or4days learning flying in the cave before turning into fledglings. Fledglings gain substantial weight before leaving parents'nests which could be even more than that of an adult. They will then lose some weight before getting fully mature.
It has also been found that the natural enemy of Himalayan Swiftlets in caves is mainly the Rattus edwards, which occasionally threatens the eggs, nestlings and even adult birds, however with minor danger to Himalayan Swiftlets; while the natural enemies outside caves primarily are raptorial birds like Accipiter virgatus offinis and Buteo buteo burmanicu, etc.
Day and night activity rules. Certain monitoring indexes, such as morning-evening leaving and homing status, frequency of homing at day, rate of staying at nest, and birds clustering behavior etc, have indicated that they are sufficiently in line with seasonal change and species' breeding behavior rules. Basically the species repeat their behavior model, which can be called "with the lamb, and stopped work at sunset". That is, at early days of breeding, the rate of staying at nest at day and the rate of homing at evening are increasing, which generally reach the peak at the middle period of breeding. And the birds clustering often occurs at the early and the late period of breeding.
5. The morphological characteristics:The Himalayan Swiftlets weighs19.29±1.41g and the body length is130±3.69mm. Its beak is flat and of short width, with the width of beak base almost equal to the length of culmem. The upper part of its body is infuscate, with light-colored waist feather decorated with crineous scapus texture; the lower part of the body is taupe with distinct scapus texture. The length of the wing is larger than or equal to the body length, exceeding tail end when folding. The scape of the tail feather is of high resilience; four toes onward suitable for perching on cave wall; and the tarsometatarsus covered with feather, whose rear side has a blanket of thin callus due to the long-time supporting itself against the cliff. Other morphological features include:the front toe and the four toe tips have well developed claws; the flexible tail feather helps it rest on cave walls; small body type and swift flight make it appropriate for pass through narrow and zigzag caves freely.
The internal structure adapts it to dark cave life. In regard of alimentary system, the salivary gland is capable of secreting viscous saliva, and the elastic esophagus without craw can reserve food bolus made by captured insects for nestlings. Additionally, the species has a well functioning digestion system with gastric emptying time for about6hours. As to its circulating system, the cardiac is more powerful than the common birds, with the weight accounting for2%of its body weight. When discussing the skeletal system of Himalayan Swiftlets, the skeleton of the posterior limbs is particularly suitable for cave behavior, for the tail tip of the pubis is1/3longer than the ischium, which can better protect its pelvic cavity; and the far end of metatarsal bones is formed into a typical "roller" joint mode, composed of the2nd,3rd and4th trochlea metatarsus at the same level. Data show that the length of tibiotarsus of the posterior limb bone is the longest, with the femora longer than the metatarsal bones, and the length ratio among the femora, tibiotarsus and metatarsal bones is1:1.57:0.75, similar to other species of Apodiformes order while different from other arboreal species. All those morphological structure features have reflected that the structure and functions of Himalayan Swiftlets conform well to its cave life behavior.
The experimental results of molecular system evolution analysis indicate that the Himalayan Swiftlets may have a relatively close genetic relationship with Edible-nest Swiftlet (Aerodramus fuciphagus), both of which have the capability of echolocation.
6. The Himalayan Swiftlets is the summer residents, coming at early April and leaving at early November. The way of its emigration is one-time clustering, while the way of immigration is divided into several groups with more than once activities, with resident period for209.4±1.4(207-213,n=9) days. The migration activity is closely linked to climate and food factors.
本项研究从1994年至2012年,以壶瓶山自然保护区核心区内神景洞哨所为工作据点,采用逐日连续定点观察、野外调查、声波特征分析、环志标记、摄影摄像、红外线无人值守监测、形态结构解剖、分子系统进化学分析等多种研究手段,对神景洞内的短嘴金丝燕种群的回声定位机制、洞穴巢址选择机制、洞穴繁殖生态行为、昼夜活动规律、适应洞穴生活的生物学特征、迁徙行为等作了较为系统的研究,结果表明：
1、壶瓶山短嘴金丝燕种群数量少,分布狭窄。全区仅有2个溶洞有其分布,其中神景洞1000余巢,2000余个体；鹰子尖溶洞60余巢,120余只个体。环志与个体标记结果说明：该种群的性比为1：1,神景洞种群分为两个“家族”,它们在空间分布上处于不同的洞段。
2、根据短嘴金丝燕的鸣声与其行为的关系,将其分为定位、报警、嬉戏、幼鸟鸣声。2012年6月,使用Avisoft-UltraSoundGate116(e)录音设备对短嘴金丝燕在山洞内自由飞行状态进行实时声音的录制,然后利用声音软件(BatSound software, release1, Pettersson Elektronik AB,瑞典)对其进行分析,结果显示：其回声定位叫声为调频的双脉冲组,组内脉冲间隔很短(6.6+0.42ms),组间脉冲间隔较长(99.3±3.86ms),两者差异显著(t-test：t=-23.888,P<0.01)；对比第一与第二脉冲的声音参数发现,主频和脉冲时程差异不显著,第一和第二脉冲的主频分别为6.2±0.08kHz和6.2±0.10kHz(t=0.572,P>0.05),脉冲时程分别为2.9±0.12ms和3.2±0.17ms(t=.1.550,P>0.05),两者的最高频率(20.1±1.10kHz,15.4±0.98kHz,t=3.239,P<0.01)和最低频率(3.7±0.12kHz,4.0±0.09kHz,t=.2.316,P<0.05)差异显著,第一脉冲的频宽(16.5±1.17kHz)比第二脉冲的(11.4±1.01kHz)要宽(t=3.303,P<0.01)；此外,第一脉冲的能量(.32.5±0.60dB)比第二脉冲的(.35.2±0.94dB)高(t=.2.463,P<0.05)。通过分析还发现,短嘴金丝燕在黑暗的山洞内的回声定位叫声还包含了部分超声波,最高频率可达33.2kHz。
3、营巢洞穴选择机制分析采用SPSS11.5统计软件对神景洞鸟巢的生境选择因子进行聚类分析,结果显示：巢址一般具备四个安全条件,一是高度条件,巢址一般高于地面3m(实际测量最低2.5m),为人和其他动物所不及,从而免遭破坏；二是“孤岛条件”,即巢址与地面之间没有其他动物攀援的通道；三是光线条件,在黑暗的洞穴中(照度小于0.01Lx),短嘴金丝燕可以凭借回声定位能力活动自如,而其他动物则可能活动受限；四是湿度条件,足够的湿度能使巢的唾液成分不会失水而保持良好的粘性,从而保持巢结构的稳定性。
4、短嘴金丝燕洞穴繁殖生态行为研究结果表明：其求偶过程可能在越冬地就已完成,婚配形式为“一夫一妻”的单配制,交配行为可在空中或巢中进行；旧巢利用率100%,仅在产卵前加以修补,无巢的新鸟或巢被破坏的老鸟另建新巢；巢址一般选在既安全、又适于群居的黑暗洞壁上；巢材主要为唾液和苔藓,间杂有少量自身的羽毛和草尖,量度为：巢重17.84+4.18g,外径(88±7.78)×(78.75±8.43)mm内径(71.83±7.95)×(66.91±8.40)mm,巢深25.25±8.10mm。筑巢期长达60d左右。卵长椭圆形,白色无斑,大小为21.3×12.lmm,重量为2.7g；最早产卵于5月31日,最迟为7月20日左右；筑新巢的鸟产卵较晚,最早见于6月26日。大部分产卵2枚,少数产1枚,平均窝卵数为1.7g,一般为连续产卵,偶有间隙1-2d。第一枚卵产出后立即坐巢孵化；雌雄共同孵卵,但以雌鸟为主。孵卵温度为37.28+1.02℃；孵化期为27.85+3.39d；孵出顺序与产卵顺序一致,相差1-3d,孵化率为71.43%。雏鸟晚成性,体重1.68+0.08g,刚出壳时,全身粉红色,裸露无羽,眼未睁开。喂雏的任务主要由雄鸟承担；先出壳的个体始终保持生长优势。育雏期27d左右；雏鸟在洞内学飞,学飞后3-4d后出洞；雏鸟离巢时个体重甚至超过成鸟,离巢后体重有减轻现象。
短嘴金丝燕洞穴内的天敌目前仅发现有白腹巨鼠(Rattus edwardsi),偶有危害鸟蛋、幼鸟、甚至成鸟的现象,但危害不大；洞外的天敌主要是松雀鹰(Accipiter virgatus offinis)、普通鵟(Buteo buteo burmanicu)等猛禽。
昼夜活动规律：早晚离归巢、白天返巢频率、在巢率、集群行为与季节变化、繁殖行为规律相适应。基本上是日出而作,日落而息；繁殖前期,白天在巢率、返巢率逐渐升高,到繁殖中期达到高峰。集群情况在繁殖前、后期较为明显。
5、短嘴金丝燕适应洞穴生活的的生物学特征：前趾型足、四趾末端均具有发达的爪,与柔软而富有弹性的尾羽相互配合,适宜其在洞穴石壁上停歇。体型小,飞行动作快速灵敏,适合在狭窄曲折的洞穴内穿行；呼吸系统鸣肌粗壮,与定位回声发声有关；消化系统具有能分泌粘性唾液的唾液腺,其粘性分泌物是洞穴筑巢的必备物质；食道没有嗉囊,但弹性较大,可以将野外捕获的昆虫粘成食团储存其中,带回洞穴喂饲尚未离巢的雏鸟；循环系统中心脏较一般鸟类发达,其重量可达自身比重的2%；骨骼系统中尤以后肢骨骼特征与洞穴行为最为适应,耻骨末端比坐骨长出约1/3,能更好地起到对盆腔的保护作用,跗跖骨其远端由位于同一平面位置的第2、3、4跖骨滑车组成典型的“滚轴”关节模式,从数据上显示,短嘴金丝燕的后肢骨骼中胫跗骨的长度最长,股骨的长度要长于跗跖骨,并且其股骨、胫跗骨、跗跖骨三段骨骼的比例为1：1.57：0.75,类似如其他雨燕目物种而有别于其他树栖类物种。这些形态结构特点反映了短嘴金丝燕的结构和功能与洞穴生活行为相适应。
分子系统进化分析实验结果显示,短嘴金丝燕与同样具有回声定位能力的爪哇金丝燕(Aerodraus fuciphagus germanni)有较为接近的亲缘关系,其洞穴生活习性有着共同的遗传学基础。
6、短嘴金丝燕为夏候鸟,4月初迁来,11月初迁走；迁离方式为整群一次性；迁入方式为分群体,多次性,居留期为209.1±1.4d(207.213,n=9),迁徙明显与气候、食物因子有关。
The Himalayan Swiftlets (Aerodramus brevirostris), subordinate to Apodidae family and Apodiformes order, comprises three subspecies and can be found in China. The Sichuan subspecies (A.b. innominata) is distributed in Hupingshan National Nature Reserve (NNR) in Shimen County, where it is by far the only distribution area known in Hunan. And the species is also distributed in Shanghai, Sichuan, Guizhou, Hubei, Guangxi and Hongkong SAR in China. The study is a tough one due to certain features of the species, such as small population size, secluded and narrow habitat environment, and particular life habit including nesting in dark caves, rapid flight speed, strong flight performance, as well as wide sphere of activities. Thus domestic and international researches are rare, especially the research on the adaptation mechanism of its cave life and breeding ecology.
The study started in1994and ended in2012, choosing the Shenjing Post for work strongholds, which is located in the core area of Hupingshan NNR. Diverse research methods were adopted, such as day by day consecutive point observation, field survey, morphological structure anatomy, sound wave characteristics analysis, bird banding mark, film and video, infrared unattended monitoring, etc. A certain level of systematic studies have been conducted, mainly on the species selection mechanism of nesting site, echolocation mechanism, breeding ecology behavior, migration behavior, day and night activity rule, and molecular system evolution, etc, with the findings shown as follows:
1. The species has a small population and is only distributed in a very narrow region. There are only two distribution areas found in karst caves within the study area, among which there are about1000nests with2000individuals in Shenjing karst cave, while approximately60nests and120individuals in Yingzijian karst cave. The bird banding and individual mark indicates this species is monogamous with a sex ratio of about1:1. The nest and its location are exclusive with no sign of fights and invasion. The species in Shenging Cave has been separated into two "families", which settle in different sections of the cave in terms of spatial distribution.
2. Based on the relationship of its chirping and the behavior, the chirping of Himalayan Swiftlets can be categorized into:positioning, alarming, playing, and nestling's chirping. In June2012in Shenjing Cave, the free-flying echolocation calls were recorded with Avisoft-UltraSoundGate116(e), and the results were analyzed by certain sound software (BatSound software, release1, Pettersson Elektronik AB, Sweden). The results suggested that the echolocation sounds of Himalayan swiftlets are broadband double FM clicks, separated by a short pause, and the inter-pulse intervals between double clicks (99.3±3.86ms) were longer than those within double clicks (6.6±0.42ms)(t-test:t=-23.888, P<0.01). Except the peak frequency (6.2±0.08kHz,6.2±0.10kHz, respectively; t=0.572, P>0.05) and pulse duration (2.9±0.12ms,3.2±0.17ms; t=-1.550, P>0.05), others (maximum frequency, minimum frequency, frequency bandwidth, and power) were significantly different between the first and second click. The maximum frequency of the first pulse (20.1±1.10kHz) was higher than that of second (15.4±0.98kHz)(t=3.239, P<0.01), while the minimum frequency of the first pulse (3.7±0.12kHz) was lower than that of second (4.0±0.09kHz)(t=-2.316, P<0.05); resulting in the frequency bandwidth of the first pulse (16.5±1.17kHz) was longer than that of second (11.4±1.01kHz)(t=3.303, P<0.01). The power of the first pulse (-32.5±0.60dB) was higher than that of second (-35.2±0.94dB)(t=-2.463, P<0.05). More important, we found that Himalayan swiftlets emitted echolocation pulses including ultrasonic sound, that the maximum frequency reached33.2kHz.
3. Analysis of nesting cave selection mechanism. The clustering analysis concerning habitat selection impact factors in Shenging Cave has been conducted by SPSS11.5. Findings indicate that four safety conditions are required for the nesting selection. The first is the height of the nest, which requires3m higher above the ground (the actual measurement is at least2.5m), often beyond man or other animals'reach so as to keep the nest from being damaged. The second is the "islet condition", referring to the passageway between the nest and the ground to prevent other animal from climbing to the nest. The third is the light condition, for Himalayan Swiftlets can move flexibly by echolocation capability while other animals' movement may be confined in dark caves. And the Fourth is the humidity, which means sufficient humidity may help maintain good stickiness of saliva and thus keep stable structure of the nest.
4. Breeding ecology behavior of Himalayan Swiftlets. The courtship process may be fulfilled in wintering ground on the basis of monogamy, with mating conducted in the air or in the nest. The old nest can be fully reused, only mended before hatching. For those with no nest or the nest destroyed, they have to build new ones, which are usually on secure cave walls suitable for living in groups. The nests are primarily composed of saliva and mosses, mixed with a little feather and grasses. The nest weights17.84±4.18; in terms of nest measurement, the external and internal diameter as well as the depth are (88±7.78)×(78.75±8.43),(71.83±7.95)×(66.91±8.40) and25.25±8.10respectively. Nest construction can take up to60days. The eggs are oblong, white, unspotted, with a size of21.3×12.1mm and a weight of2.7g. The earliest egg laying starts on31May, while the latest on around20July. If nest building is ongoing, the egg laying is often delayed, with the earliest date known on26June. In most cases, two eggs can be found for each couple each reproductive season, yet one egg per couple is also occasionally observed, thus the average amount for each couple is1.7eggs. The egg laying usually goes on continually, occasionally ceasing for just one day or two. And egg hatching starts immediately after the laying of the first egg. Both males and females are involved in hatching but females invest more time in it. The hatching temperature is37.28±1.02℃, the duration is27.85±3.39days, and the hatching rate is71.43%. The brooding sequence conforms to the hatching sequence, difference in1-3days. Nestlings usually weigh1.68±0.08g, with little body totally pink, covered with no feather and eyes yet not open when just getting out of shells. Nestlings are altricial brooding, and are fed by parents for about27days. After that, they spend some extra3or4days learning flying in the cave before turning into fledglings. Fledglings gain substantial weight before leaving parents'nests which could be even more than that of an adult. They will then lose some weight before getting fully mature.
It has also been found that the natural enemy of Himalayan Swiftlets in caves is mainly the Rattus edwards, which occasionally threatens the eggs, nestlings and even adult birds, however with minor danger to Himalayan Swiftlets; while the natural enemies outside caves primarily are raptorial birds like Accipiter virgatus offinis and Buteo buteo burmanicu, etc.
Day and night activity rules. Certain monitoring indexes, such as morning-evening leaving and homing status, frequency of homing at day, rate of staying at nest, and birds clustering behavior etc, have indicated that they are sufficiently in line with seasonal change and species' breeding behavior rules. Basically the species repeat their behavior model, which can be called "with the lamb, and stopped work at sunset". That is, at early days of breeding, the rate of staying at nest at day and the rate of homing at evening are increasing, which generally reach the peak at the middle period of breeding. And the birds clustering often occurs at the early and the late period of breeding.
5. The morphological characteristics:The Himalayan Swiftlets weighs19.29±1.41g and the body length is130±3.69mm. Its beak is flat and of short width, with the width of beak base almost equal to the length of culmem. The upper part of its body is infuscate, with light-colored waist feather decorated with crineous scapus texture; the lower part of the body is taupe with distinct scapus texture. The length of the wing is larger than or equal to the body length, exceeding tail end when folding. The scape of the tail feather is of high resilience; four toes onward suitable for perching on cave wall; and the tarsometatarsus covered with feather, whose rear side has a blanket of thin callus due to the long-time supporting itself against the cliff. Other morphological features include:the front toe and the four toe tips have well developed claws; the flexible tail feather helps it rest on cave walls; small body type and swift flight make it appropriate for pass through narrow and zigzag caves freely.
The internal structure adapts it to dark cave life. In regard of alimentary system, the salivary gland is capable of secreting viscous saliva, and the elastic esophagus without craw can reserve food bolus made by captured insects for nestlings. Additionally, the species has a well functioning digestion system with gastric emptying time for about6hours. As to its circulating system, the cardiac is more powerful than the common birds, with the weight accounting for2%of its body weight. When discussing the skeletal system of Himalayan Swiftlets, the skeleton of the posterior limbs is particularly suitable for cave behavior, for the tail tip of the pubis is1/3longer than the ischium, which can better protect its pelvic cavity; and the far end of metatarsal bones is formed into a typical "roller" joint mode, composed of the2nd,3rd and4th trochlea metatarsus at the same level. Data show that the length of tibiotarsus of the posterior limb bone is the longest, with the femora longer than the metatarsal bones, and the length ratio among the femora, tibiotarsus and metatarsal bones is1:1.57:0.75, similar to other species of Apodiformes order while different from other arboreal species. All those morphological structure features have reflected that the structure and functions of Himalayan Swiftlets conform well to its cave life behavior.
The experimental results of molecular system evolution analysis indicate that the Himalayan Swiftlets may have a relatively close genetic relationship with Edible-nest Swiftlet (Aerodramus fuciphagus), both of which have the capability of echolocation.
6. The Himalayan Swiftlets is the summer residents, coming at early April and leaving at early November. The way of its emigration is one-time clustering, while the way of immigration is divided into several groups with more than once activities, with resident period for209.4±1.4(207-213,n=9) days. The migration activity is closely linked to climate and food factors.
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Del Hoyo, J., Elliott A., Sargatal J. Handbook of the Birds of the World,1999. vol.5: Barn-owls to Hummingbirds. Lynx Edicions, Barcelona, Spain.1999,425-434.
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Fullard JH, Barclay RMR, Thomas DW. Echolocation in free-flying Atiu swiftlets (Aerodramus sawtelli). Biotropica,1993,25:334-339.
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Griffin DR, Suthers RA. Sensitivity of echolocation in cave swiftlets. Biol Bull,1970,139: 495-501.
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Griffin DR. Acoustic orientation in the oil bird, Steatornis. Proc Natl Acad Sci, USA,1954, 39:884-893.
Griffin DR. Listening in the Dark [M]. New Haven, Conn:Yale University Press,1958.
Hay ami J, Kase T. Characteristics of submarine cave bravalves in the northwestern Pacific. American Malacological Bulletin,1996,12:59-65.
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James D.Reichel, Charles T.Collins, Derek W.Stinson, Visente A.Camacho. Growth and Development of the Mariana Swiftlet.The Wilson Journal of Ornithology,2007, 119(4):686-692.
JKonishi M, Knudsen EI. The oilbird:hearing and echolocation. Science,1979,204:425-427.
Jordan Price J, Kevin P.Johnson, Sarah E.Bush, Dale H.Clayton. Phylogenetic relationships of the Papuan Swiftlet Aerodramus papuensis and implications for the evolution of avian echolocation.Ibis,2005,147:790-796.
Langham N. Breeding biology of the Edbile-nest Swiftlet Aerodramus fuciphagus. Ibis,1980, 122:447-461.
Lee PG, Kang N. The Reproductive Strategies of Edible-Nest Swiftlets(Aerodramus spp). Bull.B.O.C.,1994,114(2):107-113.
Lee PLM, Clayton DH, Griffiths R, Page RDM. Does behavior reflect phylogeny in swiftlets (Aves:Apodidae)? A test using cytochrome b mitochondrial DNA sequences. Proc Natl Acad Sci, USA,1996,93:7091-7096.
Lim Chan Koon. Opportunity and Sustainability of Swiftlet Farming in Malasia. ICOTOS, 2011:1-16.
Malacarne.G.M. Cucco.GOrecchia. Nest Attendance,Parental Roles and Breeding Success in the Pallid Swift(Apus pallidus)Die. Vogelwarte,1992,36:203-210.
Mauro P. The Influence of Clutch and Brood Size on Nesting Success of the Biscutate Swift, Streptoprocne Biscutata(Aves:Apodidae). Zoologia,2011,28(2):186-192
Medway L. Echo-location among Collocalia. Nature,1959,184:1352-1353.
Medway Lord. The Swiftlets(Collocalia) of Niah Cave,Sarawak.part 1.Breeding Biology. Ibis, 1962,104:45-66.
Medway L. The swiftlets (Collocalia) of Niah cave, Sarawak. Par 2. Ecology and the regulation of breeding. Ibis,1962,104:228-245.
Medway L. The function of echonavigation among swiftlets. Anim Behav,1967,15:416-420.
Medway L. Studies on the biology of the Edible-nest swiftlets of South-East Asia. Mala Nat J, 1969,22:57-63.
Medway L, Pye JD. Echolocation and the systematics of swiftlets, Chap.19 [M]//Stonehouse B, Perrins C. Evolutionary Ecology. Baltimore:University Park Press,1977,225-238.
Nakagawa H, Hama Y, Sumi T. Occurrence of a nonsulfated Chondroitin proteoglycan in the dried saliva of collocalia swiftlets. Glycobiology,2007,17(2):157-164.
Nguyen QP. Discovery of the Black-nest Swiftlet Collocallia (Aerodramus) Maxima Hume in Vietnam and Preliminary Observations on its Biology. Bulletin du Museum National d'Histoire Naturelle,Section A,1996, n 1-2:3-12.
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