https://orcid.org/0000-0001-7287-029X
Figures
Abstract
Although river-crossing structures can have a detrimental effect on the movement and distribution of anguillid eels (genus Anguilla), they have inhabited locations upstream of river-crossing structures in many rivers. However, the growth stage in which the eels start to climb river-crossing structures remains unclear. In this study, we directly observed, using infrared video camera systems, that the Japanese eel (Anguilla japonica) climbs a low-height vertical weir as a migratory barrier, confirming the ability of eels to climb over a low-height weir within a river. All eels climbed the weir at night, between sunset and sunrise. We observed that the total length of Japanese eels that climbed the weir ranged from 60 to 140 mm, suggesting that eels inhabiting the upstream area of a weir climbed it when they were small and then lived and grew upstream. Moreover, the general additive model showed considerable effects of water temperature and precipitation on eel climbing, suggesting that water temperature and precipitation are important for its activation. The results of this study also show the effectiveness of infrared video cameras in monitoring eel climbing, which could be applied to monitor fish migratory behavior through fish passages. The findings of this study are useful for the comprehensive management and conservation of wild eel stocks.
Citation: Kume M, Yoshikawa Y, Tanaka T, Watanabe S, Mitamura H, Yamashita Y (2022) Water temperature and precipitation stimulate small-sized Japanese eels to climb a low-height vertical weir. PLoS ONE 17(12): e0279617. https://doi.org/10.1371/journal.pone.0279617
Editor: Hideyuki Doi, University of Hyogo, JAPAN
Received: May 10, 2022; Accepted: December 12, 2022; Published: December 27, 2022
Copyright: © 2022 Kume et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the paper and its Supporting Information files.
Funding: This study was partly supported by the River Fund of the River Foundation (grant no. 2020-5211-001) to MK. The funder had no role in the study design, data collection and analysis, decision to publish, or manuscript preparation. Competing interests: The authors have declared that no competing interests exist.
Competing interests: The authors have declared that no competing interests exist.
Introduction
River-crossing structures (dams and weirs) have been built on rivers worldwide [1,2]. These structures have serious consequences for adjacent aquatic ecosystems; for instance, they can create physical barriers to the upstream/downstream movement of fish. This has resulted in habitat reduction and fragmentation of freshwater fishes, including diadromous fishes; thus, fish abundance and diversity have decreased, and fish extinction risk has increased [3,4]. Recently, various types of rehabilitation/restoration acts of degraded ecosystems, such as fish ladder installation and dam removal, have been conducted globally to recover longitudinal connectivity throughout watersheds [5,6].
The Japanese eel, Anguilla japonica, also faces such threats. This species is a facultative catadromous fish that spawns in open seas and grows in continental waters [7]. Glass eels enter fresh/brackish waters [8], and elvers disperse in waters with wide ranges of salinity to take advantage of potentially suitable habitats [9]. They then grow as yellow eels and spend several years in these waters [10]. Approximately 78.6% of the effective habitats of Japanese eels have been lost in East Asian rivers [11]. One of the reasons for this is the river-crossing structures, which negatively affect eel movement and distribution even if they are low-rise structures [12–15]. Our previous studies have shown that the upstream migration of small-sized eels (total length, i.e., TL < 200 mm) was negatively influenced by the number of low-height weirs, whereas that of larger-sized eels (TL > 200 mm) was negatively influenced by the maximum weir height [13,14]. Moreover, the cumulative heights of weirs higher than 40 cm and 60 cm have been reported to hinder the upstream migration of Japanese eels by less than and more than 240 mm TL, respectively [15]. However, another study reported that dams shorter than 3.0 m in height did not prevent the upstream migration of the American eel A. rostrata [16]. These studies used a model-based approach to determine the relationships between eel density and dam/weir characteristics (i.e., weir number and/or height) along a river at various scales (reach and unit scales). In these studies, eels were collected upstream of low-height weirs, and although they were less in number compared with those collected downstream of weirs, the data suggested that eels climbed weirs at a certain period during their growth stage. Therefore, it is necessary to examine the exact effects of river-crossing structures on the upstream migration of eels. To undertake effective restoration efforts for the conservation of Japanese eels, we investigated these effects more efficiently by determining the exact stage at which eels start to climb weirs.
Recently, several eel upstream passage solutions have been developed [17]. For example, previous studies have tested a variety of fishways or fish ladders as potential eel upstream passages [18,19]. Additionally, dam/weir removal can aid in better eel upstream movement [20]. Whether such approaches for helping eel upstream migration should be adopted depends on the balance between costs (i.e., time and money) and benefits (i.e., improvement of eel growth and survival and the efficiency of reproductive stock reinforcement). However, river-crossing structures are essential for human well-being and safety (i.e., flood control). Furthermore, there are a huge number of river-crossing structures in Japanese rivers [21]. In small rivers of Japan, several low-height weirs have been constructed to raise water levels for agricultural water use or to stabilize riverbeds, and the mean density of such structures, being larger than 40 cm in height, is 1.6 weirs per km [22]. However, low-height weirs in small rivers generally lack fish passage.
This study used video recording equipment to capture the exact stage in which eels climb weirs and to determine their size, the timing of the climbing, and the effects of environmental conditions on this behavior. Based on a previous study, which suggested that smaller-sized eels were more capable of climbing slopes than larger-sized eels [19], we hypothesized that small-sized yellow Japanese eels climb weirs, whereas large-sized eels do not. Additionally, we explored the environmental factors that stimulate eel climbing. We hypothesized that eels climb weirs at night when water temperature exceeds 13°C. This is because anguillid eels, including Japanese eels, are nocturnal [23,24], and the activity of Japanese eels decreases below 13°C [23].
Materials and methods
Ethics statement
Wakayama Prefecture (#04010003–48) permitted setting two infrared video camera systems under articles 24 and 26 in the River Act.
Study site
Field surveys were conducted in the Akugawa River (~4.3 km long), Wakayama Prefecture, Japan (Fig 1). The lower course of this river (ca. 2.5 km upstream of the river mouth) runs through a lowland mainly consisting of residential areas. The middle and upper courses of this river (2.5–4.3 km from the river mouth) mainly consisted of farmlands and residential areas. In the study area, there was only one vertical concrete weir; it had a height of 165 cm and was located approximately 2.7 km from the river mouth (Fig 1B and 1C). The wall surface of the weir was eroded and crusted with periphyton mats (~2 mm thickness). The area from the river mouth to the weir had concrete banks on both sides and was intruded with saline water, whereas the areas upstream of the weir were entirely freshwater areas as the weir prevented the saline water intrusion. Our previous study showed that a high density of eels (0.67–1.05 eels/m2) with various body lengths (93–641 mm TL) is located in the upper reaches of the Akugawa River [25]. The riverbank of the study area located upstream of the weir mainly consisted of either a masonry revetment on one side and a natural bank on the other side or natural banks on both sides. Areas directly above and below the weir consisted of concrete floors with concrete banks on both sides.
(A) Map showing central Honshu, Japan. The red circle indicates the Akugawa River at Shirahama Town, Wakayama Prefecture. (B) Map of the Akugawa River. The blue square indicates the weir where infrared video camera systems were installed. (C) Photograph of the weir (165 cm height) located at the middle stream of the Akugawa River. The area in the red square indicates the recording angle of the video recorded. Yellow circles with dashed lines indicate infrared video camera systems. The red arrow indicates the flow direction. The white line on the top of the weir was drawn to estimate the TL of eels from the video. (D) Zoom photograph of the infrared video camera system. Yellow arrows indicate infrared lights. Maps were modified using data set (https://geoshape.ex.nii.ac.jp/river/) under CC BY 4.0. Photographs were taken by M.K.
Video survey
To observe the climbing behavior of eels, we set two infrared video camera systems (CSSTC ver.2.21, Tanaka Sanjiro Co., Ltd., Fukuoka, Japan) on the left and right sides of the weir (Fig 1C). Both cameras were installed at a height of 70 cm from the top of the weir and 50 cm downstream from the weir, and at an angle of approximately 45° from the horizontal. The angle of view was approximately 50 cm × 100 cm, and both the upper part and vertical wall of the weir were monitored. We recorded continuously for 24 hours every day from February 13 to May 31, 2021 at a resolution of 1280 × 720 pixels and 30 fps. As anguillid eels are nocturnal [23,24], two infrared lights per camera were lit at night to observe the climbing behavior of eels. To estimate the TL of eels from the video, we painted a white line (AquaCort, HERMETIC, Tokyo, Japan) on top of the weir (Fig 1C and 1D).
In this study, we recorded videos for 5,520 hours. Due to equipment failure, the camera on the left and right sides of the weir did not record from February 15 to 17 and February 13 to 14, respectively. From the video, we counted the number of eels that successfully climbed the weir, confirmed that they could reach the top of a weir, and recorded the date and time of the successful climbing by each eel. It took approximately 200 hours to check the video played at 32x speed. Additionally, the TL of the eels was approximated to the nearest 10 mm using ImageJ ver.1.53k.
Collection of environmental data
Water temperature below the weir was measured every 30 minutes using a data logger (UA-002-64, Onset Computer Corp., Bourne, MA, USA) from February 14 to May 31, 2021. Hourly precipitation data (mm/h) at the “Nanki-Shirahama” observation point (33°39ʹ43ʺN, 135°21ʹ47ʺE), the nearest observation point to the Akugawa River, were downloaded from the database of the Japan Meteorological Agency [26]. Daily moon illumination values, as an index of the moon phase, were obtained using the lunar illumination function in the R “lunar” package [27] and ranged from 0 (new moon) to 1 (full moon).
Statistical analyses
To examine the factors affecting the eel upstream migration timing, we used a general additive model (GAM) with a Tweedie distribution (the gam function in the mgcv package R package [28]) because of the multiple zeros in the dataset. In this analysis, we used the dataset from February 14 to May 31, in which 24-hour videos were recorded. The number of eels that successfully climbed the weir was the dependent variable, and the water temperature, precipitation (mm/d), and lunar illumination were the predictor variables (S1 Data). We used the daily average water temperatures for the analysis because of the time lag between the time it rains and the time the river discharge changes. Furthermore, we used 24-hour precipitation data from 0, 12, and 24 h before precipitation (i.e. precipitationt, precipitationt-12h, and precipitationt-24h, respectively); precipitationt is 24-hour precipitation from 0:00–24:00 on day t; precipitationt-12h is 24 hour-precipitation from 12:00 at one day before day t to 12:00 on day t and precipitationt-24h is 24 hour-precipitation from 0:00–24:00 one day before day t. All analyses used the statistical significance level of 0.05. All statistical tests were performed using R software version 4.1.0 [29].
Results
Environmental variables
During our study period, the daily average water temperature ranged from 6.7 to 21.8°C and gradually increased as the season progressed (Fig 2A); mean values of daily average water temperature were 11.2°C, 13.8°C, 16.0°C, and 18.8°C in February, March, April, and May, respectively. In April and May, water temperatures exceeded 13°C—the threshold at which eel behavioral activity decreases [23]—on all days; however, the water temperatures exceeded 13°C for 4 and 24 days in February and March, respectively, whereas in May, the water temperature exceeded 15°C—the threshold at which the probability of eel climbing increases (see the timing of eel climbing in the results section in this study)—on all days; however, the water temperature exceeded 15°C for 1, 6, and 24 days in February, March, and April, respectively. It rained for 2, 11, 7, and 14 days in February, March, April, and May, respectively (Fig 2C).
(A) average water temperature (black plots and line) with minimum (blue line) and maximum (red line) temperatures. Green and orange dashed lines indicate 13°C—the threshold at which eel behavioral activity decreases [23], and 15°C—the threshold at which the probability of eel climbing increases (see also Fig 5A), respectively. Symbols above the figure indicate the moon phase (open and closed circles indicate full moon and new moon, respectively). (B) the number of eels that successfully climbed the weir (closed bars). (C) daily precipitation (open bars).
Video observations
A total of 102 eels successfully climbed the weir with 165 cm height during our study period, from February 13 to May 30, 2021 (Fig 2B; S2 Data). Within the range of each camera on the left and right bank, all eels were found to climb closer to the edges of the weir (S1 Movie). The number of eels climbing in April (n = 39) and May (n = 38) was higher than that in February (n = 5) and March (n = 20). There were only 3 days in which more than 10 eels climbed in one day throughout our study period: the first one (n = 10; 9.8% of the total number of climbing eels) occurred on March 21, and the second and third ones occurred on April 30 (n = 29; 28.4%) and May 1 (n = 13; 12.7%), 2021. It rained with 31.5 mm/d and 28.5 mm/d precipitation on March 21 and May 1, respectively, and there was a lack of rain on April 30, but precipitationt-12h and precipitationt-24h were 43.0 mm/day and 92.5 mm/day, respectively (Fig 2C). The video observations clearly indicated that the water levels were higher on these three days. The eels climbed up the edge of the weir, where there was little water flowing, wriggling their bodies. They were also observed resting with their bodies hooked on the protrusions of the wall on their way climbing the weir. All eels climbed the weir at night, between sunset (18:00) and sunrise (6:00) (Fig 3). There were two peaks of climbing eel abundance at night: the first peak (n = 17) occurred after sunset (20:00–21:00), and the second peak (n = 8) occurred before sunrise (3:00–4:00). We were able to measure the TL of 68 eels (out of 102), with a mean TL of 95 mm ranging from 60 to 140 mm (Fig 4).
Shaded areas indicate nighttime based on sunrise and sunset times during the study period. Data on sunrise and sunset times were downloaded from the database of the Japan Coast Guard [30].
Timing of eel climbing
The GAM results revealed that the water temperature and precipitation were markedly related to the number of eels climbing the weir (Table 1; Fig 5A–5D). The probability of eel climbing increased as the average water temperature increased (p < 0.05; Table 1), especially when water temperature exceeded approximately 15°C (Fig 5A). There was a different relation between precipitationt and the other precipitation parameters (precipitationt-12h and precipitationt-24h); precipitationt had one peak of eel climbing, ranging between ca. 15–40 mm/d (p < 0.001; Fig 5B), while the probability of eel climbing increased as both precipitationt-12h and precipitationt-24h increased (p < 0.05 for both; Fig 5C and 5D). However, moon illumination tended to affect the number of eels climbing but with no statistical significance (p = 0.052; Table 1; Fig 5E), which implied the weak effect of moon illumination on the eel climbing.
(A) daily average water temperature, (B) precipitationt, (C) precipitationt-12h, (D) precipitationt-24h, and (E) moon illumination. Circles indicate all observations of eel climbing. Lines with shaded areas indicate estimated curves with 95% confidence bands. Tick marks on the x-axes show the location of observations along the range of continuous explanatory variables.
Discussion
Weirs can prevent the upstream migration of anguillid eels, contributing to the loss of longitudinal connectivity within a watershed depending on the relationship between eel density and weir characteristics along the flow direction [12–16,31]. Previous studies have succeeded in collecting eels at the upper reaches of low-height weirs, suggesting that eels can climb a low-height weir, but the growth stage in which they can do so remains unclear. In this study, we directly observed small-sized (60–140 mm TL) Japanese eels successfully climbing a vertical weir (165 cm height) at night. Furthermore, the timing of eel climbing seemed to be influenced by water temperature and precipitation. Previously, we had observed a high eel density (0.67–1.05 eels/m2; TL: 93–641 mm) in the upper reaches of a weir in the Akugawa River [25]. Together, our previous and present findings suggest that eels inhabiting regions upstream of the weir climbed the weir when they were small (60–140 mm TL) and then lived and grew upstream.
The surface of the weir wall in this study was eroded with several protrusions. This surface texture may contribute to the success of eel climbing. In this study, eels were sometimes observed clinging to the rough protrusions of a wall during the process of climbing the weir, possibly to prevent falling. Previous studies have also shown that rough shallow sloping surfaces (e.g., studded plastic, open weave geotextile, and bristle substratum) can help eels climb a weir [17–19,32]. These findings suggest that the roughness of the structural surface is important for eel climbing over natural and artificial barriers. It is also likely that weirs covered with periphyton and plants may help young eels (especially glass eels and elvers) climb weirs [13,14,17]. Matsushige et al. [33] demonstrated that Japanese eels were likely to climb the moss-covered rock wall of a natural waterfall (46 m in height) because eels were collected from an upper reach of the waterfall where they were not stocked. Thus, the surface structure of the weir wall is pertinent for the success of eel climbing.
In this study, Japanese eels with over 150 mm TL were not observed climbing vertical weirs. One hypothesis is that eels have a TL threshold for climbing a weir. Eels over 150 mm TL may fall while trying to climb a weir because they cannot support their own weight. This hypothesis is supported by the experimental study of Lagarde et al. [19], who showed that the probability of climbing experimental slopes decreased for marbled eels Anguilla marmorata with more than 300 mm TL. Another hypothesis is that eels over 150 mm TL did not try to climb a weir. Small-sized eels (glass eels, elvers, and small yellow eels) are in the process of being dispersed over a wide range of habitats, from coastal areas to upstream river basins after they, as glass eels, reach coastal areas [9]. On the other hand, large eels have strong site fidelity and a relatively small home range [23], similar to other anguillid eels [34,35]. In the case of the European eel Anguilla anguilla, small-sized eels (less than 240 mm TL) were observed to migrate upstream, but large-sized eels more than 240 mm TL were not [36]. The body size at which eels begin to exhibit a sedentary lifestyle is likely to vary across rivers [36,37]. If eels inhabiting the Akugawa River begin to show sedentary behavior when they reach TL over 150 mm, the second hypothesis is more likely to be the case. However, we could not test these hypotheses in the present study as further studies are required to confirm them.
In this study, all eels climbed a weir at night, with two peaks just after sunset and before sunrise. Similarly, in previous studies, the behavioral activity of eels increased at night, with two peaks just after sunset and before sunrise in Japanese eels as well as other eel species [23,34,35]. Noda et al. [24] reported the diel movement of yellow Japanese eels; eels move to a river after sunset and return to a brackish lagoon just before sunrise, possibly for foraging purposes [38]. However, the two peaks of eel climbing are unlikely to be explained only by foraging behavior because eel climbing is likely to be an energy- and time-consuming activity. One possible reason for the occurrence of eel climbing at night is to minimize predation risk [39]. In a previous study, Japanese eels seemed to reduce predation risk by potential diurnal predators, such as birds (the grey heron (Ardea cinere) and kingfisher (Alcedo atthis)) [40,41] and fish (the largemouth bass Micropterus salmoides) [42], when they climbed a weir.
Previous studies have revealed that the upstream migratory behavior of anguillid eels appears to be strongly related to water temperature and that the threshold varies across eel species [31,43–46]. In European eels, the upstream locomotor activity at 18°C was higher than that at 10°C [47]. In yellow Japanese eels over 500 mm TL, behavioral activity decreases below approximately 13°C [23]. The threshold water temperature for wall climbing of glass eel, Anguilla spp., from Iceland was between 12°C and 14.5°C [44]. In this study, frequent eel climbing was observed from March to May when water temperature exceeded approximately 13°C, and our GAM results revealed that the probability of eel climbing increased when water temperature exceeded approximately 15°C. Therefore, this study confirms that an increase in water temperature is a key environmental factor in activating upstream migration, including climbing behavior in eels.
Precipitation is an important factor that stimulates upstream migration in several fish species, including anguillid eels [48]. Our GAM results also revealed the positive effects of precipitation on the probability of eel climbing. It was thought that too much rainfall would impede eel climbing because the river discharge would be too strong [43,45,46,49]. A possible explanation for eels climbing the weir during increased river discharge is to avoid predation risk. When it rains, the water level rises, and the river water becomes turbid. In such situations, both bird and fish predators cannot detect aquatic prey, thereby decreasing their feeding rate [41,50]. In this study, we could not use the flow rate as an explanatory variable in GAM. Further study is needed in this area.
Our GAM results revealed that the lunar illumination was ineffectual regarding the probability of eel climbing. Previous studies reported that American eels exhibited high activity of upstream movement under low lunar illumination, that is, a new moon [46,49]. These previous and present studies used cloud cover, lunar phase, and/or lunar illumination as alternative indicators of illumination in a water column [46,49]. The alternative indices of illumination used in these studies may have been insufficient to explain the factors stimulating the upstream migration of eels because illumination in the water column is possibly affected by turbidity in the water column, water level/discharge, weather (i.e., cloudy), moon phase, moon illumination, and its interactions. Therefore, further studies on the relationship between the ambient light environment and eel upstream migration, including eel climbing, are required.
In the present study, all eels were found to climb through the edges of the weir when they were wet during or after rainfall. However, this study had two limitations regarding the visibility of the recorded video. First, it was difficult to confirm the eel climbing through the weir during rainy days because of the surge in water level and water velocity. A previous study revealed that the burst swimming speed of Japanese eel elvers ranged from 36–56 cm/sec [51], which can potentially be slower than the increased river flow after rainy days. In fact, the average current velocity at the center of the river just above the weir measured on September 5, 2022, three days after the rainfall (total 53.0 mm on 30 August 30 to September 2, 2022), was 43.8 cm/sec (range: 43.2–44.4 cm/sec). Therefore, the initial assumption was that the eels could not climb the center of the weir on rainy days since the current speed at the center of the weir exceeded the burst swimming speed of Japanese eels. Our results that eels climbed to areas with less water (less easily washed away) closer to the edges even when water levels were low was supported to this assumption. In addition, the camera’s shooting range could not capture the center of the weir. Thus, we could not discount the possibility that eels climbed the center of the weir on sunny days.
Video imaging is an effective tool for wild animal research, including studies on animal diversity, abundance, and behavior [52]. Being non-invasive, video imaging allows for target species to be studied in their habitats without any disturbance [53,54]. Recently, ecological monitoring using video systems has become more applicable in a broader range of situations owing to the technological developments in cameras, such as extended battery life and increased storage capacity [55,56]. This method has been used in ecological studies of anguillid eels [57,58] and other fish species [59]. However, this monitoring technique has certain disadvantages. It takes a lot of time and effort to manually obtain data from recorded videos [58]. In this study, it took approximately 200 h to check all videos from two cameras that were continuously recording for four months. Provided that better technologies are applied for the automatic or semi-automatic detection of target species (Japanese eels) in recorded videos (i.e., machine learning techniques and models), video surveys will be extensively used in field ecology studies.
Overall, in this study, we recorded Japanese eels climbing a low-height vertical weir using infrared video camera systems. The infrared video camera system used in this study can be used for monitoring activities at the numerous weirs in rivers across Japan. In this study, small-sized Japanese eels ranging from 60 to 140 mm TL could climb a weir (165 cm height) at night. It should be noted that a weir can still act as a physical barrier to the upstream movement of small-sized eels. Some small-sized eels can climb a weir while others cannot climb or stay downstream of a weir, resulting in a reduction in eel density with increasing the number of weirs or their cumulative heights, as shown by previous studies [12–15]. Moreover, the water temperature and precipitation seemed to be important for stimulating the eel’s climbing behavior. However, we used only a limited number of environmental factors for GAM analysis; thus, other abiotic (e.g., illuminance in the water column, tidal phase, and atmospheric pressure) and biotic (e.g., eel and/or predator density, and food and/or shelter availability) factors that we did not use in this study may be complexly related to eel climbing and upstream migration of anguillid eels. Thus, further studies on abiotic and biotic factors that stimulate eel climbing are required. Furthermore, this study could not confirm the success rate of eel climbing and the threshold of weir height that eels could climb. Therefore, further studies on the effects of weirs on eel upstream movement and distribution within a river would help enhance the knowledge required for the comprehensive management and conservation of wild eel stocks.
Supporting information
S1 Movie. Video of the eel that climbed successfully (30 April 2021).
This video was played at an 8x speed. The arrow indicates an eel that climbed successfully.
https://doi.org/10.1371/journal.pone.0279617.s003
(MP4)
Acknowledgments
We thank Satoshi Kameyama for his valuable suggestions and Ayano Medo, Yurika Dantsuji, Shiran Maeno, Yoshimi Itaya, Takumi Honda, and Hiroki Hamanaka for supporting the fieldwork.
References
- 1. Nilsson C, Reidy CA, Dynesius M, Revenga C. Fragmentation and flow regulation of the world’s large river systems. Science. 2005;308: 405–408. pmid:15831757
- 2. Belletti B, Garcia de Leaniz CG, Jones J, Bizzi S, Börger L, Segura G, et al. More than one million barriers fragment Europe’s rivers. Nature. 2020;588: 436–441. pmid:33328667
- 3. Morita K, Yamamoto S. Effects of habitat fragmentation by damming on the persistence of stream-dwelling charr populations. Cons Biol. 2002;16: 1318–1323.
- 4. Jones PE, Champneys T, Vevers J, Börger L, Svendsen JC, Consuegra S, et al. Selective effects of small barriers on river-resident fish. J Appl Ecol. 2021;58: 1487–1498.
- 5.
FAO, DVWK. Fish passes—Design, dimensions and monitoring. Rome, Italy: Food and Agriculture Organization; 2002.
- 6.
Roni P, Pess G, Hanson K, Pearsons M. Selecting appropriate stream and watershed restoration techniques. In: Roni P, Beechie T, editors. Stream and watershed restoration: A guide to restoring riverine processes and habitats. Oxford, UK: Wiley and Blackwell; 2013. pp. 144–188. https://doi.org/10.1111/emr.12142
- 7. Tsukamoto K, Chow S, Otake T, Kurogi H, Mochioka N, Miller MJ, et al. Oceanic spawning ecology of freshwater eels in the western North Pacific. Nat Commun. 2011;2: 179. pmid:21285957
- 8. Kawakami Y, Mochioka N, Nakazono A. Immigration period and age of Anguilla japonica glass eels entering rivers in northern Kyushu, Japan during 1994. Fish Sci. 1998;64: 235–239.
- 9. Kaifu K, Tamura M, Aoyama J, Tsukamoto K. Dispersal of yellow phase Japanese eels Anguilla japonica after recruitment in the Kojima Bay-Asahi River system, Japan. Environ Biol Fish. 2010;88: 273–282.
- 10. Kotake A, Arai T, Okamura A, Yamada Y, Utoh T, Oka HP, et al. Ecological aspects of the Japanese eel, Anguilla japonica, collected from coastal areas of Japan. Zoolg Sci. 2007;24: 1213–1221. pmid:18271637
- 11. Chen J-Z, Huang S-L, Han Y-S. Impact of long-term habitat loss on the Japanese eel Anguilla japonica. Estuar Coast Shelf Sci. 2014;151: 361–369.
- 12. Itakura H, Wakiya R, Yamamoto S, Kaifu K, Sato T, Minamoto T. Environmental DNA analysis reveals the spatial distribution, abundance, and biomass of Japanese eels at the river-basin scale. Aquatic Conserv Mar Freshw Ecosyst. 2019;29: 361–373.
- 13. Kume M, Terashima Y, Wada T, Yamashita Y. Longitudinal distribution and microhabitat use of young Japanese eel Anguilla japonica in a small river flowing through paddy areas. J Appl Ichthyol. 2019;35: 876–883.
- 14. Kume M, Terashima Y, Kawai F, Kutzer A, Wada T, Yamashita Y. Size-dependent changes in habitat use of Japanese eel Anguilla japonica during the river life stage. Environ Biol Fish. 2020;103: 269–281.
- 15. Yokouchi K, Itakura H, Wakiya R, Yoshinaga T, Mochioka N, Kimura S, et al. Cumulative effects of low-height barriers on distributions of catadromous Japanese eels in Japan. Anim Conserv. 2022;25: 137–149.
- 16. Kwak TJ, Engman AC, Lilyestrom CG. Ecology and conservation of the American eel in the Caribbean region. Fish Manag Ecol. 2019;26: 42–52.
- 17.
Solomon DJ, Beach MH. Fish pass design for eel and elver (Anguilla anguilla). Rand Technical Report W2-070/TR. Bristol: UK Environment Agency; 2004.
- 18. Watz J, Nilsson PA, Degerman E, Tamario C, Calles O. Climbing the ladder: An evaluation of three different anguillid eel climbing substrata and placement of upstream passage solutions at migration barriers. Anim Conserv. 2019;22: 452–462.
- 19. Lagarde R, Courret D, Grondin H, Faivre L, Ponton D. Climbing for dummies: Recommendation for multi-specific fishways for the conservation of tropical eels and gobies. Anim Conserv. 2021;24: 970–981.
- 20. Hitt NP, Eyler S, Wofford JEB. Dam removal increases American eel abundance in distant headwater streams. Trans Am Fish Soc. 2012;141: 1171–1179.
- 21. Yoshimura C, Omura T, Furumai H, Tockner K. Present state of rivers and streams in Japan. River Res Applic. 2005;21: 93–112.
- 22.
Nacs J. Report of a civil science project “Shizen Shirabe 2017”; 2017. (in Japanese). Available from: https://www.nacsj.or.jp/shirabe/2017/05/1594/. Tokyo, Japan: Nature Publishing Conservation Society of Japan (NACS-J).
- 23. Itakura H, Miyake Y, Kitagawa T, Kimura S. Site fidelity, diel and seasonal activities of yellow-phase Japanese eels (Anguilla japonica) in a freshwater habitat as inferred from acoustic telemetry. Ecol Freshw Fish. 2018;27: 737–751.
- 24. Noda T, Wada T, Mitamura H, Kume M, Komaki T, Fujita T, et al. Migration, residency and habitat utilisation by wild and cultured Japanese eels (Anguilla japonica) in a shallow brackish lagoon and inflowing rivers using acoustic telemetry. J Fish Biol. 2021;98: 507–525. pmid:33070333
- 25. Kume M, Nakayama N, Iwasaki Y, Hori T, Watanabe S, Terashima Y, et al. River to river: First evidence of eel movement between distant rivers via the sea. Environ Biol Fish. 2021;104: 529–533.
- 26.
Japan Meteorological Agency. Download historical weather data; 2021. (in Japanese). Available from: https://www.data.jma.go.jp/gmd/risk/obsdl/index.php#1. Tokyo, Japan: Japan Meteorological Agency.
- 27.
Lazaridis E. Lunar phase & distance, seasons and other environmental factors; 2015. Available from: https://cran.r-project.org/web/packages/lunar/lunar.pdf.
- 28.
Wood S. Mixed GAM computation vehicle with automatic smoothness estimation; 2018. Available from: https://cran.r-project.org/web/packages/mgcv/mgcv.pdf.
- 29.
R Core Team. R: A language and environment for statistical computing; 2021. Available from: http://www.r-project.org/. Austria: Foundation for Statistical Computing. R Foundation for Statistical Computing.
- 30.
Japan Coast Guard; 2021. Calculate service for sunrise and sunset. Tokyo, Japan: Japan Coast Guard. Available from: https://www1.kaiho.mlit.go.jp/KOHO/automail/sun_form3.html; 2021.
- 31. White EM, Knights B. Dynamics of upstream migration of the European eel, Anguilla anguilla (L.), in the rivers Severn and Avon, England, with special reference to the effects of man-made barriers. Fish Manag Ecol. 1997;4: 311–324.
- 32. Vowles AS, Don AM, Karageorgopoulos P, Worthington TA, Kemp PS. Efficiency of a dual density studded fish pass designed to mitigate for impeded upstream passage of juvenile European eels (Anguilla anguilla) at a model Crump weir. Fish Manag Ecol. 2015;22: 307–316.
- 33. Matsushige K, Hibino Y, Yasutake Y, Mochioka N. Japanese eels, Anguilla japonica, can surmount a 46-m-high natural waterfall of the Amikake River system of Kyushu Island, Japan. Ichthyol Res. 2021;68: 21–31.
- 34. Hedger RD, Dodson JJ, Hatin D, Caron F, Fournier D. River and estuary movements of yellow-stage American eels Anguilla rostrata, using a hydrophone array. J Fish Biol. 2010;76: 1294–1311. pmid:20537015
- 35. Walker AM, Godard MJ, Davison P. The home range and behaviour of yellow-stage European eel Anguilla anguilla in an estuarine environment. Aquat Conserv Mar Freshw Ecosyst. 2014;24: 155–165.
- 36. Imbert H, Labonne J, Rigaud C, Lambert P. Resident and migratory tactics in freshwater European eels are size-dependent. Freshw Biol. 2010;55: 1483–1493.
- 37. Laffaille P, Acou A, Guillouet J. The yellow European eel (Anguilla anguilla L.) may adopt a sedentary lifestyle in inland freshwaters. Ecol Freshw Fish. 2005;14: 191–196.
- 38. Kutzer A, Lavergne E, Kume M, Wada T, Terashima Y, Yamashita Y. Foraging behavior of yellow-phase Japanese eels between connected fresh- and brackish water habitats. Environ Biol Fish. 2020;103: 1061–1077.
- 39. Glova GJ, Jellyman DJ. Size-related differences in diel activity of two species of juvenile eel (Anguilla) in a laboratory stream. Ecol Freshw Fish. 2000;9: 210–218.
- 40. Kameda K, Ishida A, Naruse M. Population increase of the Great cormorant Phalacrocorax carbo hanedae in Japan: Conflicts with fisheries and trees and future. Vogelwelt. 2003;124(Suppl): 27–33.
- 41. Vilches A, Arizaga J, Salvo I, Miranda R. An experimental evaluation of the influence of water depth and bottom color on the Common kingfisher’s foraging performance. Behav Processes. 2013;98: 25–30. pmid:23624098
- 42. Haubrock PJ, Balzani P, Criado A, Inghilesi AF, Tricarico E. Predicting the effects of reintroducing a native predator (European eel, Anguilla anguilla) into a freshwater community dominated by alien species using a multidisciplinary approach. Manag Biol Invas. 2019;10: 171–191.
- 43. Jessop B. Annual variability in the effects of water temperature, discharge, and tidal stage on the migration of American eel elvers from estuary to river. Am Fish Soc Symp. 2003;33: 3–16.
- 44. Linton ED, Jónsson B, Noakes DLG. Effects of water temperature on the swimming and climbing behaviour of glass eels, Anguilla spp. Environ Biol Fish. 2007;78: 189–192.
- 45. August SM, Hicks BJ. Water temperature and upstream migration of glass eels in New Zealand: Implications of climate change. Environ Biol Fish. 2007;81: 195–205.
- 46. Schmidt RE, O’Reilly CM, Miller D. Observations of American eels using an upland passage facility and effects of passage on the population structure. N Am J Fish Manag. 2009;29: 715–720.
- 47. Edeline E, Lambert P, Rigaud C, Elie P. Effects of body condition and water temperature on Anguilla anguilla glass eel migratory behavior. J Exp Mar Biol Ecol. 2006;331: 217–225.
- 48. Jonsson N. Influence of water flow, water temperature and light on fish migration in rivers. Nord J Freshw Res. 1991;66: 20–35.
- 49. Welsh SA, Aldinger JL, Braham MA, Zimmerman JL. Synergistic and singular effects of river discharge and lunar illumination on dam passage of upstream migrant yellow-phase American eels. ICES J Mar Sci. 2016;73: 33–42.
- 50. Higham TE, Stewart WJ, Wainwright PC. Turbulence, temperature, and turbidity: The ecomechanics of predator-prey interactions in fishes. Integr Comp Biol. 2015;55: 6–20. pmid:25980563
- 51. Yataya K, Izumi M, Azuma N, Marui A. Swimming Ability of Japanese Eel (Anguilla japonica) ELVERS. Journal of Japan Society of Civil Engineers, Ser G (Environmental Research). 2020;76: II_109–II_114.
- 52. Brainerd EL, Blob RW, Hedrick TL, Creamer AT, Müller UK. Data management rubric for video data in organismal biology. Integr Comp Biol. 2017;57: 33–47. pmid:28881939
- 53. McIntyre FD, Neat F, Collie N, Stewart M, Fernandes PG. Visual surveys can reveal rather different ’pictures’ of fish densities: Comparison of trawl and video camera surveys in the Rockall Bank, NE Atlantic Ocean. Deep Sea Res I. 2015;95: 67–74.
- 54. Rezzolla D, Boldrocchi G, Storai T. Evaluation of a low-cost, non-invasive survey technique to assess the relative abundance, diversity and behaviour of sharks on Sudanese reefs (southern Red Sea). J Mar Biol Assoc UK. 2014;94: 599–606.
- 55. Mallet D, Pelletier D. Underwater video techniques for observing coastal marine biodiversity: A review of sixty years of publications (1952–2012). Fish Res. 2014;154: 44–62.
- 56. Bicknell AWJ, Godley BJ, Sheehan EV, Votier SC, Witt MJ. Camera technology for monitoring marine biodiversity and human impact. Front Ecol Environ. 2016;14: 424–432.
- 57. Tsukamoto K, Mochioka N, Miller MJ, Koyama S, Watanabe S, Aoyama J. Video observation of an eel in the Anguilla japonica spawning area along the West Mariana Ridge. Fish Sci. 2013;79: 407–416.
- 58. Lenihan ES, McCarthy TK, Lawton C. Use of an acoustic camera to monitor seaward migrating silver-phase eels (Anguilla anguilla) in a regulated river. Ecohydrol Hydrobiol. 2019;19: 289–295.
- 59. Bacheler NM, Gregalis KC, Gillum ZD, Pickett EP, Schobernd CM, Schobernd ZH, et al. Using stationary video data to infer relative abundance and distribution of four Seriola species along the southeast United States Atlantic coast. Fish Res. 2022;249.