Anthropogenic threats to the reintroduced population of Oriental storks in Japan: analysis of the causes of injury and death of 153 storks from 2005 to 2021

Abstract

After the native population of Oriental stork (Ciconia boyciana) in Japan disappeared, a reintroduction project was implemented in 2005. All released storks and most wild-fledged storks were individually identified using colored rings on their legs. The size of the reintroduced population reached 256 by the end of 2021. In this study, we investigated the causes of stork injury and death in wild populations to clarify important medical issues for successful reintroduction. During the survey, 153 of 412 (78 released and 334 fledged storks) storks were injured or died between 2005 and 2021. At least 49.7% of the injuries and deaths were directly caused by human activities. Entanglement with pest control measures (such as bird- and beast-proofing nets) and accident with electrical and telecommunication equipment are two major causes of injury and death of reintroduced Oriental storks in Japan. It is important to recognize that these anthropogenic threats have a significant impact on the establishment and maintenance of the reintroduced populations of Oriental storks in Japan. Therefore, it is necessary to implement countermeasures against these threats to establish human and Oriental storks coexistence, which is a major goal of reintroduction.

The Oriental stork (Ciconia boyciana) is a large bird belonging to the order Ciconiiform, and is distributed throughout Russia, China, Hong Kong, North and South Korea, Taiwan, and Japan [3]. It is designated as Endangered (EN) on the International Union for Conservation of Nature (IUCN) Red List because it has a small population that has undergone rapid decline, which is projected to continue in the future [3]. Deforestation, wetland reclamation for agriculture, overfishing (overhunting), and habitat disturbance are the main threats to Oriental stork populations [3].

In Japan, the native population of wild Oriental storks disappeared in 1971. After their disappearance, a captive population was established by breeding founders from wild Oriental storks donated to the Hyogo Prefecture by Khabarovsk Krai, former Soviet Union, from storks imported to zoos from China, and from rescued wild storks that had migrated from other countries [32, 35]. Reintroduction aimed at establishing a permanent population in Japan using captive populations began in September 2005 in Hyogo Prefecture, and the first fledgling was recorded in 2007 [10]. The Hyogo Prefectural Government plays an important role in reintroducing storks in Japan [19] and works closely with the Inter-institutional Panel on Population Management of the Oriental White Stork (IPPM-OWS) and their member facilities and organizations.

For individual identification, color rings have been attached to all released storks and most wild fledged storks in Japan since 2005. Information from these rings allows surviving storks from the reintroduced population to be accurately recognized. The size of the reintroduced population reached 256 by the end of 2021; however, many storks have been injured or died since 2005 [30, 31].

Health and mortality monitoring of establishing populations in a reintroduction project enables us to assess the levels of disease and mortality, which impact the translocation success and assist in accurately identifying the causes of death during translocation and identifying the challenges in establishing a new population [21].

Bird mortality owing to human activity is recognized as global issue [9, 27, 29, 39, 44]; thus, many studies on accidents involving birds caused by human activities [5, 11, 25, 28] and on the mortality rate of reintroduced mammals or birds have been conducted [4, 14, 26]. However, to the best of our knowledge, there are no detailed studies on the factors causing injuries and deaths in the reintroduced Oriental stork population.

In this study, to clarify the conservation challenges facing the establishment of the reintroduced Oriental stork population in Japan, we collated all reports on rescued and dead storks in the reintroduced population in Japan from 2005 to 2021 and analyzed the various causes of injury and death, especially those caused by human activity. Finally, we discussed effective countermeasures to reduce human-caused accidents in the reintroduced population in Japan.

MATERIALS AND METHODS

Research period, area, and target

The research period was from September 2005 to December 2021.

The research area encompassed all prefectures in Japan including three, where the storks were initially released, and seven, where the storks fledged in the wild.

We targeted the 412 Oriental storks that were released or fledged in Japan. From 2005 to 2021, 78 storks were released in the Hyogo (Toyooka, Yabu, and Asago City), Fukui (Echizen City), and Chiba Prefectures (Noda City). From 2007 to 2021, 334 Oriental storks fledged in Japan. The stork breeding sites were artificial nest towers, electric poles, or cellular towers in the Tochigi (Oyama City), Fukui (Sakai, Echizen, and Obama City), Kyoto (Kyotango and Ayabe City), Hyogo (Toyooka, Yabu, Asago, and Awaji City), Tottori (Tottori City), Shimane (Unnan City), and Tokushima Prefectures (Naruto City). Seventeen prefledged storks were rescued for various reasons, such as death of a parent stork or falling from the nest. These storks that were raised in captivity and released into the wild are included in the 334 fledged storks. Storks for which ring recovery information could not be obtained for one year were treated as missing individuals.

All released storks had color rings attached to their legs before release. Most wild-fledged storks were captured before fledging and color rings were attached to their legs. The rings consisted of five colors, allowing easy identification of each stork by different color combinations. Each stork was assigned a unique individual identification (ID) number.

Blood and/or feathers samples were collected from each stork upon release or fledging. DNA was extracted from the samples and the sex was identified using a previously reported PCR method [20, 33].

The capture and sample collection of storks were conducted with permission for each year of the study period based on the Law for the Conservation of Endangered Species of Wild Fauna and Flora and the Cultural Properties Protection Law (For example, the license numbers in 2021 are KAN-KIN-CHI-YA-KYO-No.2103314 by the Ministry of Environment and 3-BUN-CHO-No.655 by the Agency for Cultural Affairs).

Analysis of injured and dead storks

Hyogo Park of the Oriental White Stork in Toyooka City, Japan, has been collecting date, location, age, and individual ID number information on injured and dead storks since their initial release in 2005.

We recorded the annual and monthly number of injured and dead storks, the breakdown of released and fledged storks, and the number of years after release or fledging. The annual trends in the number of injured and dead storks were graphically compared with those of the population.

We also recorded medical examination findings of injured and dead storks such as fractures, trauma, feather damage, and electric shock injury. Depending on the body part and severity of the injury, movement of the stork from the accident site by itself was also used as a basis for judging the cause of the accident.

The analysis included the location and surrounding environment of recovery area. In addition, as part of the surrounding environment, we recorded the man-made structures proximal to the recovery area, such as the electrical and telecommunications equipment and roads and railways, which could possibly injure or kill Oriental storks.

Rescued storks were admitted to the Hyogo Park of the Oriental White Stork, zoological gardens, and wildlife rescue centers in several prefectures, and some were returned to the wild on the day they were rescued or, in extreme cases, 525 days after they were rescued.

Storks that died after being rescued or that were found dead already were refrigerated and stored at 4°C and autopsied within a few days. If the stork could not be autopsied within a few days, it was frozen and stored at −20°C and autopsied within a few weeks (up to 159 days). Pathological autopsies of dead storks were performed at the Hyogo Park of the Oriental White Stork, zoological gardens, or veterinary universities. The results of histopathological examinations were not included in this study because histopathological examination was not performed in most cases.

The cause of injury and death was determined and categorized according to criteria created for this study, that is, using the direct observation information, medical examination findings, and surrounding environment and pathological findings (Table 1). The causes of injury and death of storks were classified into three types: human activity, non-human activity, and unknown. Human activity included injury or death by pest control measures, electrical and telecommunications equipment, traffic accidents, hunting equipment, and plastic ingestion. Non-human activity included straying immediately after fledging or release, falling from the nest, injuries by other stork’s attack, falling into waterways, ponds, and pools, disease or weakness, poor growth of wing feathers, death by lightning or predate by other species, and others. “Unknown” included fractures of unknown origin, injuries of unknown origin, and any unidentified cause.

Table 1. The criteria to categorize causes of injury and death of 153 Oriental storks reintroduced in Japan from September 2005 to December 2021.

Human or non-human	Cause of injury and death	Criteria
Human activity	Pest control measures (bird- and beast-proofing equipment)	1. Entangled in bird and beast preventive equipment such as beast-proofing nets, bird-proofing nets, bird-proof fishing lines, electric fences, wires.2. Trapped in a small gap around farmland surrounded by metal fences.
	Electrical and telecommunications equipment	1. Collected under transmission line towers, utility poles, transmission power lines, distribution power lines and mobile phone towers, with fracture(s) or severe internal injuries or wounds from electrical shock, and no paved roads and rails near the collection point that could cause a traffic accident. 2. Witnessed collisions with electrical and telecommunications equipment, or electrocutions on transmission line towers or utility poles.3. One leg trapped in the gap of the frame of the transmission line tower.
	Traffic accident	1. Collected on or near roads or rails, with fracture(s) or severe internal injuries, and no man-made structure (e.g., transmission power lines) above the collection point that could cause a collision.2. Witnessed collision with automobile or train.
	Hunting equipment	1. Observed the bullets from gun shot injury by X-rays.2. Rescued from leg-hold trap.3. Rescued from box traps.
	Ingestion of plastic	1. Observed emaciation and filling of the stomach with plastic.
Non-human activity	Straying immediately after fledging or release, or falling from the nest	1. Strayed into a residential area, a forest or a bush immediately after fledging or release.2. Fell from the nest before fledged.
	Injuries by other stork’s attack	1. Witnessed being attacked by other storks.
	Falling into waterways, ponds and pools	1. Fell into a waterway, pond, pool, etc., without any fracture(s) or injury.
	Illness or weakness	1. Emaciation and visceral disease have been observed without fracture(s) or injuries, or any findings applicable to other categories.
	Poor growth of wing feathers	1. Lost flight feathers before fledging, and fell from the nest with insufficient flight ability. The cause of flight feather loss was unknown.
	Death by lightning	1. Burn marks on the utility pole due to lightning strikes, and observed fracture and severe internal injuries.
	Predate by other species	1. Presence of clear bite mark from a mammal; bleeding was observed near the bite mark during autopsy.
	Other	1. No findings suggestive of human activities, no fractures or injuries, and is not applicable to any other category of non-human activities.
Unknown	Fracture by unknown cause	1. Fractured, and cannot be identified as any of the above causes.
	Injury by unknown cause	1. Injured but not fractured, and cannot be identified as any of the above causes.
	Unidentified	1. Unidentified causes (e.g., skeletonized, found only some parts of the body).

The rate at which injured storks return to the wild after being rescued was analyzed, as well as the elapsed time after fledging or release (e.g., less than one year, and over one year) for human activity, non-human activity, and unknown.

RESULTS

During the survey period, 96 storks were injured and 57 died (153 in total). Of the 96 injured storks, 57 (59.4%) were released back to the wild after recovery (Table 2). Of the 153 storks, 76 storks (49.7%) were injured or died due to human activities, 42 storks (27.5%) were due to non-human activities, and 35 storks (22.9%) were unknown (Table 2).

Table 2. The causes of injury and death of 153 Oriental storks in reintroduced in Japan from September 2005 to December 2021.

Human or non-human	Cause of injury and death							Cases				Subtotal				Breakdown of cause of injury/death in each case
																Death		Injury
Human activity	Pest control measures							35		22.9%		76		49.7%		8		27
	Electrical and telecommunications equipment							31		20.3%						20		11
	Traffic accident							5		3.3%						4		1
	Hunting equipment							4		2.6%						1		3
	Ingestion of plastic							1		0.7%						1		0
Non-human activity	Straying immediately after fledging or release, or falling from the nest							7		4.6%		42		27.5%		0		7
	Injuries by other stork’s attack							7		4.6%						0		7
	Falling into waterways, ponds and pools							7		4.6%						1		6
	Illness or weakness							6		3.9%						3		3
	Poor growth of wing feathers							2		1.3%						0		2
	Death by lightning							1		0.7%						1		0
	Predate by other species							1		0.7%						1		0
	Other							11		7.2%						1		10
Unknown	Fracture by unknown cause							19		12.4%		35		22.9%		6		13
	Injury by unknown cause							8		5.2%						2		6
	Unidentified							8		5.2%						8		0
Total								153		100.0%		153		100.0%		57		96
Human or non-human	Result after rescue in injury cases						Breakdown of age class in each cause
	Died1)	Other2)	Returned to the wild3)	Wild-return rate	Sub-total		less than one year		Sub-total		over one year		Sub-total		Unknown		Sub-total
Human activity	3	1	23	85.2%	28	66.7%	15		43		19		32		1		1
	8	1	2	18.2%			21				10				0
	1	0	0	0.0%			4				1				0
	0	0	3	100.0%			2				2				0
	0	0	0	-			1				0				0
Non-human activity	0	0	7	100.0%	25	71.4%	10		40		9		17		0		0
	4	1	2	28.6%			7				1				0
	0	0	6	100.0%			5				1				0
	3	0	0	0.0%			7				0				0
	0	0	2	100.0%			4				3				0
	0	0	0	-			4				3				0
	0	0	0	-			2				0				0
	1	1	8	80.0%			1				0				0
Unknown	9	4	0	0.0%	4	21.1%	1		10		0		10		0		0
	2	0	4	66.7%			5				6				0
	0	0	0	-			4				4				0
Total	31	8	57	59.4%	57	59.4%	93		93		59		59		1		1

1) Succumbed to injuries resulting from rescue. 2) Kept in captivity or transferred to another facility as an exhibition individual because returning it to the wild was impossible due to the prognostic symptoms. 3) Returned to the wild after recovery from injuries.

The most common cause of injury and death related to human activities was pest control measures installed around farmland to prevent agricultural pest invasion which affected 35 storks (22.9%) (Table 2). Among those 35 storks, 71.4% were entangled in beast-proof netting (Fig. 1), 8.6% were entangled in bird-proof netting, 5.7% were entangled in bird-proof fishing lines, 5.7% were entangled in electric fences, 5.7% were entangled in metal fences, and 2.9% were restrained in wires (considered electric fences for imitation) (Table 3).

Fig. 1.

An Oriental stork entangled in beast-proof netting.

Table 3. Breakdown of injuries or deaths of 35 reintroduced Oriental storks by pest control measures in Japan from September 2005 to December 2021.

Pest control measures materials	Cases
Beast-proofing nets	25	71.4%
Bird-proofing nets	3	8.6%
Bird-proof fishing lines	2	5.7%
Electric fences	2	5.7%
Metal fences	2	5.7%
Wires	1	2.9%
Total	35	100.0%

A total of 31 storks (20.3%) were injured or died due to contact with electrical and telecommunications equipment (Table 2). Among those 31 storks, 61.3% were collisions with transmission, distribution, or telephone lines, 16.1% were electrocuted after contact with transmission or distribution lines when perching on an electric tower (Table 4).

Table 4. Breakdown of injuries and deaths of 31 reintroduced Oriental storks caused by electrical and telecommunication equipment in Japan from September 2005 to December 2021.

Breakdown	Cases
Collisions with transmission, distribution, or telecommunication lines	19	61.3%
Electrocution	5	16.1%
Unknown cause of death under a tower	4	12.9%
Accidents on a tower	1	3.2%
Other	2	6.5%
Total	31	100.0%

A total of five traffic accidents (3.3%) involving storks were caused by stork collisions with trains or automobiles; four storks (2.6%) were injured or died due to hunting equipment, such as guns, leg-hold traps, and box traps, and one (0.7%) was died from ingesting plastic material (Table 2).

The wild-return rate of the rescued storks was 85.2% after entanglement in pest control measures materials and 18.2% after contact with electrical and telecommunications equipment (Table 2).

Injuries and deaths of storks have occurred since 2005 and although there are annual variations, the number of injuries and deaths has gradually increased (Fig. 2).

Fig. 2.

Annual trends in the number of injuries and deaths of Oriental storks and size of the population reintroduced in Japan.

Stork injuries and deaths were recorded throughout the year, and tended to be lower in winter (December to February) and higher in summer (June to August). December had the lowest number with 6 storks, while June, July, and August had the highest number with 21 storks. Thirty seven (48.7%) of 76 storks that were injured or died owing to human activity occurred from June to August (Fig. 3).

Fig. 3.

Monthly trends in the number of injuries and deaths of Oriental storks.

Regarding the elapsed time, 93 of 153 were less than one year and 59 were over one year after fledging or release (Table 2). In 76 human caused cases, storks less than one year were recorded mostly from June to August, and over one year were recorded mostly from April to May (Fig. 4).

Fig. 4.

Monthly trends in the number of injuries and deaths caused by human activity of Oriental storks in less than one year and over one year after fledging or release.

Of the 334 fledglings, 75 were injured (rescued) or died within a year, of which 34 (45.3%) were caused by human factors. Of the 78 storks released into the wild, 13 were injured (rescued) or died within a year, of which four (30.8%) were caused by human factors.

DISCUSSION

There are several studies on the population dynamics or human-caused accidents on other stork species such as White storks (Ciconia. ciconia) [1, 23, 43] and Black storks (Ciconia. nigra) [49], which included ring recovery research, but there are no studies on Oriental storks. Thus, this is the first study that revealed the frequencies of injury and death of Oriental storks due to human-caused accidents in the reintroduced population in Japan. We found that 76 (49.7%) of 153 storks that were injured or died were directly caused by human activities. Of these storks, pest control measures and electrical and telecommunications equipment were the major human causes. We also consider that the rate of human-caused accidents may be maximumly 72.6% because it is possible that human activities may have been the cause of injury in the 35 storks (22.9%) with unknown cause. Our study indicated that most Oriental stork accidents in Japan are caused by human activities. We will continue to collect and analyze data to reveal the influence of human-caused accidents on the sustainable management of the reintroduced Oriental stork population.

Accidents related to pest control measures (including beast-proofing nets, bird-proofing nets, bird-proof fishing lines, electric and metal fences, and wires) were the most common human factors causing injury and death in the reintroduced Oriental stork populations in Japan. Among the pest control measures, beast-proof netting was the most common cause (71.4%). In addition, in recent years, the population and density of Wild boars (Sus scrofa) and Sika deer (Cervus nippon) in several areas in Japan has increased, which significantly increased agricultural damage; thus various pest control measures were installed to deter these animals [17, 41, 47, 48, 53], and this increase in pest control has affected the Oriental stork population. If storks entangled in beast-proofing nets were rescued, the wild-return rate would be higher than that of storks rescued from electrical and telecommunications equipment. Four storks were thought to be eaten by predators before they could be rescued as only an entangled skeleton was found. To the best of our knowledge, there are no studies on beast-proof netting being a major threat to other endangered birds in Japan or to other Ciconiiformes species. In Japan, these accidents occur frequently because storks use rice fields as their main feeding habitat [12, 36].

Oriental storks often use power transmission towers and utility poles as nesting, resting, and roosting sites [3]. Unless safety measures to prevent storks perching and nesting on transmission lines and towers are implemented, these man-made structures will continue to affect the Oriental stork population. Murata [32] identified the need for preventative measures against stork accidents regarding electrical transmission lines. In Toyooka City, where reintroductions began in 2005, some preventative measures have been implemented in electrical transmission lines and steel towers. It is important that effective safety measures are developed in cooperation with electric and telecommunication companies because the wild-return rate after injury caused by transmission lines is quite low compared with other factors.

Studies on the White stork reported many accidents related to electrical and telecommunications equipment such as collision and electrocution [13, 51]; however, research into electrocution prevention measures for the White stork are ongoing [22]. Accidents involving birds and electrical transmission lines are a well-known problem worldwide [2, 45], especially for reintroduced bird species [24, 39, 52], and there are several studies focused on reducing electrical transmission line accidents [8, 15, 22]. Dwyer et al. [8] reported that using a pole-mounted near-ultraviolet light reduced collisions of the Sandhill crane (Grus canadensis). Based on the examination of captive Oriental storks, Ha et al. [15] reported that the installation of bird spikes on top of utility poles may prevent storks from perching on them, which would result in less electrocution accidents in the wild. Kaługa et al. [22] reported that the rate of death by electrocution of the White stork could be reduced by introducing/providing technical modifications such as isolators and disconnectors to particular electricity poles.

Because there are no studies on countermeasures to reduce electrical transmission line accidents involving wild Oriental storks, it is important to conduct research on the reintroduced population in Japan.

There are few studies on cause of death in large bird species in Japan. It has been reported that the death of 63.6% White-naped cranes (Grus vipio) wintering in the Izumi Plain was caused by anthropogenic activity [16]. Although countermeasures, such as installing color markers on transmission lines, to prevent collision accidents with the White-naped crane have been proposed [16], there are no studies on the practicality of such countermeasures. In the case of the White-naped crane, it may be effective to install accident countermeasures in their wintering areas because these areas are limited in Japan. However, because Oriental storks live in various parts of the country throughout the year and have a wide range of activities, it may be difficult to implement efficient accident countermeasures at such a large scale, but if effective countermeasures against human-caused accidents are not implemented, the survival of the reintroduced stork population in Japan will be significantly affected.

There were 4 storks (2.6%) with injuries or deaths caused by illegal hunting equipment. Two storks were injured by leg-hold traps, the details of which were previously reported [30], and one stork (0.7%) was killed by a gun, when a hunter mistakenly identified a stork as a heron (family Ardeidae). In Japan, hunters are permitted to eliminate some heron species and Great cormorants (Phalacrocorax carbo) because of their large populations. Oriental storks forage in rice fields with Great egrets (Ardea alba) and Grey herons (Ardea cinerea), and traverse river environment with Great cormorants. Therefore, hunters must be careful to avoid accidentally shooting storks when hunting herons or cormorants. Currently, the Oriental stork is a special natural monument under the Law for the Protection of Cultural Properties, and a rare wild animal under the Act on Conservation of Endangered Species of Wild Fauna and Flora [18]. Therefore, it is illegal to injure or kill Oriental storks in Japan. As the population of storks increases, similar accidents are likely to occur all over the country. Therefore, it is necessary to raise awareness of the Oriental stork and address the illegal use of leg-hold traps and guns.

One stork (0.7%) was died by ingesting foam rubber; the details of this case were previously reported [31]. At least 1,565 wildlife species are affected by plastic ingestion, including Oriental storks [42].

The causes of illness or weakness for 3.9% of these storks observed in this study remains unknown. Regarding the White stork, there are several studies on infectious diseases that affect them [38, 46, 54]. However, there are few studies focusing on pathogen prevalence in the Oriental stork [55]; therefore, further investigations on the prevalence of infectious diseases must be conducted.

Our findings, seasonal variations observed in the number of stork injuries and deaths, suggest that ecological factors such as behavior patterns in their breeding season are involved in these variations. The breeding season of the stork is from spring to summer. It is considered that adult storks often injured or died in the early part of the breeding season because those adults become active to protect their territory and to forage for their chicks. And it is also considered that young storks often injured or died in the latter part of the breeding season because those juveniles are developing flight ability just after fledging. Although there were annual variations, the number of stork injuries and deaths tended to increase as the population increased. In 2016, only two storks were injured, which was extremely small, and the reason for the decrease is unknown, as there was no change in rescue policy or significant developments in accident countermeasures.

The causes of Oriental stork extinctions in Japan include pesticides [34], feeding habit changes [50], and decreased genetic diversity [19]. There have also been stork injuries and deaths caused by human activities, such as leg-hold traps, collisions with electrical lines, and electrocutions (Matsumoto, unpublished data). These artificial causes previously combined to induce the stork extinction; however, when the reintroduction was conducted in 2005, efforts were made to improve habitats and feeding grounds, including an increase in organic farming and the rehabilitation of wetlands [37, 40] but little has been done to reduce human-caused accidents.

These accidents could also have an adverse effect on population dynamics and genetic diversity in establishing wild populations of Oriental storks in Japan. Therefore, it is necessary to collect further data on injuries and deaths, to develop more effective measures.

The reintroduction project of the Oriental stork in Japan aimed to promote environmentally friendly agriculture to increase the diversity and density of stork prey around farmlands, improve their foraging environment (rivers and wetlands), and provide artificial nest towers as breeding sites. These activities have aided the wild population of storks and gradually increased their numbers since reintroduction began in 2005 [7]. However, this study revealed that human-caused accidents account for approximately half of the injuries and deaths recorded in the reintroduced stork populations in Japan. For the Oriental stork to thrive, their population in Japan must maintain genetic diversity, and the Japanese community must learn to coexist with storks, which was a prominent goal during their reintroduction [19]. Effective measures to prevent human-caused accidents, especially with pest control measures and electrical and telecommunications equipment must be studied further.

The results of histopathological examination are not reflected in the analysis of the causes of death classified in this study. This is because histopathological examination was not performed in many cases due to various constraints such as post-mortem changes and the budget for examination. Therefore, it is possible that histopathological abnormalities in those cases were involved in addition to the causes classified in this study. Globally, it is considered extremely important to comprehensively analyze the causes of death in wildlife from a veterinary forensic perspective using gross autopsies, histopathological examinations, and other methods [6]. However, it is thought that the infrastructure to conducting such surveys is not sufficient in Japan, so it is necessary to develop such infrastructure in Japan as well.

CONFLICT OF INTEREST

The authors declare that there are no conflicts of interest associated with this manuscript.