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Global Ecology and Conservation 3 (2015) 831–838

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Global Ecology and Conservation

journal homepage: www.elsevier.com/locate/gecco

Short communication Shoaling behaviour of Lates japonicus revealed through a digital camera logger

Sara Gonzalvo a,∗, Hideaki Tanoue b, Teruhisa Komatsu a a Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwanoha 5-1-5, Kashiwa, Chiba 277-8564, Japan b National University, Nagata-Honmachi, Shimonoseki, Yamaguchi 759-6595, Japan article info a b s t r a c t

Article history: Protecting endangered species is one of the main targets of conservation biology, but Received 8 February 2015 the study of these species is often a sensitive issue. The need to risk, and often take, Received in revised form 23 April 2015 the life of some specimens during the experiments is not easily justified. Technological Accepted 23 April 2015 advances provide scientists with tools that can reduce damage to studied species, while Available online 4 May 2015 increasing the quality of the data obtained. Here, we analyse the social behaviour of an endangered Japanese , Akame (Lates japonicus), using an attached underwater camera. Keywords: Social behaviour, especially concerning aggregations, is a key factor in conservation plans Lates japonicus Digital still-camera logger and to avoid by-catch and to establish coherent protected areas. In Shoaling behaviour this experiment, a fish-borne underwater still-camera logger was attached to a captured Protected area Akame, recording the individual in its natural environment in July, 2009. The images obtained from the camera revealed several groups of large adults moving together, showing for the first time in this species an aggregative behaviour. This discovery opens the door for initiation of protective measures to preserve these groups, which in turn, can help to ensure continuity of this fish in the Shimanto by protecting the specific areas where these shoals gather. © 2015 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

1. Introduction

Protected areas have emerged as one of the most effective tools for protecting biological and for managing marine and coastal achieving a wide range of conservation objectives (e.g. Al-Abdulrazzak and Trombulak, 2012). Freshwater species and habitats are among the most threatened, which has brought attention to the creation of freshwater protected areas (Saunders et al., 2002). Marine Protected Areas (MPAs), must be created based on the best available scientific knowledge, establishing targets and long-term goals to ensure the preservation of conditions (Angulo-Valdés and Hatcher, 2010), and the same applies to freshwater environments. A comprehensive knowledge of the behaviour of is a key factor for habitat use assessments in conservation (Shumway, 1999), however, endangered species are a particularly complex case, in which the delicate trade-off between the need for information and the risk of harming individuals is always problematic to obtain data. Studying wild in their natural habitat usually provides scientists valuable data on their behaviour, but aquatic systems present intrinsic environmental-related difficulties that make observations difficult to accomplish. Advances in different technologies allow to overcome some of these difficulties and provide new types of data, which would be impossible to acquire otherwise

∗ Correspondence to: Atmosphere and Ocean Research Institute, The University of Tokyo, Behavior, Ecology and Observation Systems, 5-1-5, Kashiwanoha, Kashiwa-shi, Chiba 277-8564 Japan. Tel.: +81 080 4896 2529. E-mail addresses: [email protected] (S. Gonzalvo), [email protected] (H. Tanoue), [email protected] (T. Komatsu). http://dx.doi.org/10.1016/j.gecco.2015.04.009 2351-9894/© 2015 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/ 4.0/). 832 S. Gonzalvo et al. / Global Ecology and Conservation 3 (2015) 831–838

(Heithaus et al., 2002; Cooke, 2008). Especially, developments in digital imaging techniques, give new opportunities to study complex behaviour in fishes (Delcourt et al., 2013). Lates japonicus (Katayama and Taki, 1984) or ‘Akame’ in Japanese, is a large piscivorous fish from the Latidae family. It can reach up to 1.30 m and weigh over 30 kg (IGFA, 2001), being a top predator in their ecosystems. Akame is an endemic fish of Japan, believed to inhabit only the east of the country, mainly from Kagoshima to Tokushima prefectures, living in and big on those areas (Iwatsuki et al., 1993). This rare fish is considered endangered since 1992 (Asahina et al., 1992) but still little is known about it. Their reproduction and life-history are barely understood. The seasonality of occurrence and description of its larvae and juveniles (Kinoshita et al., 1988) and the study of the ovaries of one collected matured female (Iwatsuki et al., 1994), lead the authors to estimate that the spawning season is between late June and early August, probably in estuarine waters. It still remains unclear whether they in the sea (Kinoshita et al., 1988) or in the river (Iwatsuki et al., 1994). Feeding behaviour has also been studied at certain life stages, in both laboratory experiments (Tashiro and Iwatsuki, 1995, in Japanese) and the natural environment (Tanoue et al., 2012), but feeding grounds and prey preference remain unknown. No studies have been conducted to understand the social behaviour of this species nor has a census been performed to estimate its real population size. Although Akame is not a commercially targeted species, the pressure of sport and trading on this species is quite severe. With the exception of the Oyodo river (Miyazaki prefecture), where this species is known to inhabit and fishing is forbidden, Akame remains unprotected from fishing and other threats, and unassessed. Recreational fishing is known to have an impact on fish populations, even inside protected areas (e.g. Bartholomew and Bohnsack, 2005). So it is to be expected that this activity is somehow diminishing the survival of Akame populations in the Shimanto River, as is also probably doing the aquarium trading commerce of its juveniles. Reclamation of the land in the Shimanto River is also an ongoing activity, causing loss of available space, habitats and pollution, adding additional risk factors that contribute to the diminishment of Akame populations. To raise awareness of the situation of this species, some educational programs had already been started. A local aquarium, Tombo Shimantogawa Gakuyukan, is holding educational school activities to teach children about this rare fish and collaborating with researchers to study the species. Additionally, every year an ‘‘Akame Forum’’ is held in Kochi city by sport fishing professionals, where fishermen gather to discuss their techniques and experiences when dealing with this fish. Researchers are welcomed to join this forum, and are able to share their knowledge about this species. When anglers and researchers are joining these sessions together, this forum can be seen as an educational program to promote the sustainable use of this fish. To successfully protect this species, collaboration between stakeholders and scientist is a must. For example, Tanoue et al. (2015) verified in a study in Tokyo Bay when studying Seabass, a cooperative management can help to integrate different potential habitats inside the protection, while increasing the willingness of the stakeholders to follow the restrictions. Opposite to the total closure that is held in Miyazaki, a balance between protection and use can be achieved using information provided by both groups. Researchers can provide a scientific base to define the size of a coherent protected area, large enough to include all the appropriate habitats to provide continued effective protection against fishing activities, even when these activities are happening outside the boundaries of the protection (Meyer, 2007). Fishermen’s associations, on the other hand, can mitigate the mortality caused by sport fishing through regulation of the fishing gears and education of the anglers (Bartholomew and Bohnsack, 2005; Cooke et al., 2006) when targeting this fish, while allowing economic benefits from this activity. To start a better understanding of some aspects of this fish, we studied one part of its social behaviour using digital imaging tools. Unveiling the aggregative behaviour of this fish, we can understand better the type of protection that may be suitable for this species, providing assessments for its conservation. We will present here our results and suggestions of using them as an asset to preserve this species in the Shimanto River.

2. Materials and methods

Previous to the collection of the data used here, also in July of 2009, Tanoue et al.(2012) studied the feeding behaviour of captive and wild Akame in the Shimanto River using accelerometers and tracking devices. In that experiment, he estimated that feeding mainly happened in the deeper area of the bottom part of the Shimanto River. To check if this deeper area is somehow important for Akame, we conducted our experiment there. We attached a digital still-camera logger (DSL, Little Leonardo Ltd., 22 × 133 mm, 82 g in air), to the dorsum of a wild Akame, using a dissolvable suture (Matsuda Medical Kogyo Co.), in front of the first , and released it from the shore of the Shimanto River, Japan. This DSL can store high- resolution photos, and measure also depth and temperature (Kudo et al., 2007; Naito, 2007). The camera logger was included in a floating device equipped with an automatic time-releaser, a 3-axis accelerometer (ORI-380D3GT, Little Leonardo Ltd., 12 × 45 mm, 8 g in air), an acoustic pinger (V13P, Vemco Co., 13 × 44 mm, 12 g in air), and a VHF transmitter (Advanced Telemetry Systems, Inc.) for tracking the fish after release and recovering the package (see further details in Tanoue et al., 2012). The Akame, of 89 cm TL (total length) and 9.4 kg weight, was captured in the Shimanto River using a fishing rod with a line and a hook in the end, by experts of a sports fishing team. A small rubber net was sutured in front of the dorsal fin using S. Gonzalvo et al. / Global Ecology and Conservation 3 (2015) 831–838 833

Fig. 1. Map showing the position of the Shimanto River inside Japan, and a zoomed image showing the release point of the fish inside the river, generated with Google earth. dissolvable silk sutures, and the floater including all the tools, was fixed to the rubber net using a time-release explosive bridle (see details about the release system in Watanabe et al., 2008). After attaching the package, the fish was set free in the lower part of the Shimanto River, close to Shimanto city (Fig. 1). The Shimanto River, with 196 km length and 2270 km2 watershed, is one of the largest rivers of Japan, located in western Kochi¯ Prefecture in Shikoku Island. Along all the length of the river, there are no dams, and the bridges spanning the river have no guardrails, which leads to a pure flow from the beginning to the end (JNTO, 2014). The images obtained were analysed individually and classified according to their contents. Photographs without fish on them where separated from those including any species of fish, and classified according to whether there was any special structure on them, just showing the bottom of the river, or the . The pictures containing fishes were divided in those showing Akame, and those of other species. When applicable, the type of bottom was classified following the definition of Wolman(1954).

3. Results

After releasing the fish, the V13 acoustic pinger (Vemco Co., Canada) included in the package was tracked from a boat using a VR100 tracking system (Vemco Co., Canada). During the entire duration of the experiment, the fish remained nearby the release point, close to the deeper area of the river. The 5 h and 7 min of recording with the DSL provided a total of 4563 pictures between the release of the fish in the river, and the detachment of the camera from dorsum, taken with 4-s intervals. The recorded depth ranged between 1.0 m and 7.9 m, with a mean of 3.90 ± 1.84 m, and a mean temperature of 28.4 ± 0.54 °C, with a minimum of 24.5 °C and a maximum of 28.7 °C. From the 4563 pictures, 496 images (10.8%) contained fish on them. Of those, 472 included Akame (Fig. 2), while 24 were exclusively of other species. Of the images of other fishes species (Fig. 3), 12 corresponded to Sharpnose Tigerfish (Rhynchopelates oxyrhynchus), 7 to Yellowfin Seabream (Acanthopagrus latus), and 5 to Flathead Grey ( cephalus). In the 472 images that corresponded to Akame, the mean depth was 2.90 ± 0.41 m, and the mean temperature 24.9 ± 0.02 °C. The average number of individuals captured together in the same picture was 1.45 ± 0.70, with a maximum number of 4 fishes at the same time. The Akames started to appear in the images of the DSL 31.5 min before the end of the recording. Of the pictures not showing fish, in 1248 (27.4%) of them some structures were identified. Large rocks appeared in 830 pictures, and two types of fishing gears were observed in 418 images (Fig. 3), of which 188 were bottle traps and 230 brushwood traps. When the bottom was visible, the bottom types observed were sand (62%) and gravel (34%). The acceleration logger recorded no feeding event during this time. The depth profile of the diving started with going to a deeper part of the river and then gradually moving to a shallower area, to end in an intermediate depth (around 4 m). The temperature of the water increases in deeper areas where warm is covering the bottom, and decreases at the surface, where cold water coming from the upper flows. 834 S. Gonzalvo et al. / Global Ecology and Conservation 3 (2015) 831–838

Fig. 2. Six captions from the DSL camera showing different shots of Akame shoals. Notice different dispositions of the individuals inside the shoals in the different images, and two types of river bottom.

4. Discussion

4.1. Shoaling behaviour

Several images of Akame showed individuals of this species swimming close to other congeners (Fig. 2). This phenomenon is known to happen in many species of fish and was first defined by Pitcher as shoaling behaviour, referring to fishes remaining in groups for social reasons (Kennedy and Pitcher, 1975; Pitcher, 1983; Pitcher and Parrish, 1993). In a recent review of the terminology, Delcourt and Poncin stated that inside the definition of shoaling behaviour, a gradation of behaviours are included. Without a clear line that defines one of another, in one extreme we have fishes with a tendency for polarized and synchronized swimming, behaviour that remains named as schooling behaviour as it was first understood by Pitcher. S. Gonzalvo et al. / Global Ecology and Conservation 3 (2015) 831–838 835

Fig. 3. Captions from the DSL camera other than Akame. Up, two species of fish: left, Sharpnose tigerfish, and right Yellowfin Seabream. In the middle, two types of traditional fishing gears used in the Shimanto River: left, a bottle trap, and right, a brushwood trap. Down, example of gravel bottom (left) and sand bottom (right).

At the opposite extreme, the ones that tend to form randomly oriented groups that do not maintain a significant degree of polarization, newly termed swarming behaviour (Delcourt and Poncin, 2012). The images of the camera revealed, for the first time in this species, shoaling behaviour. The shoals observed seemed to consist of relatively similar sized individuals, being maybe same age-class individuals that often are blood related (Frommen et al., 2007). The captured Akames were mostly relatively large adults, therefore the maximum number of fish captured at a time was limited by the field of view of the camera. Despite this, we can clearly observe the shoals swimming together in some of the pictures, leading us to believe that often this fish is moving in groups. The benefits obtained from shoaling in fishes have been discussed for a long time, especially in regards to the motivation that leads shoals to happen (e.g. Shaw, 1978 and Partridge, 1982). Some experiments suggested that join, stay, and leave tendencies are dependent on the hunger status of the fish (Robinson and Pitcher, 1989), as well as the different positioning 836 S. Gonzalvo et al. / Global Ecology and Conservation 3 (2015) 831–838 inside the shoal (Robinson, 1991). However, shoals are unlikely to provide any feeding benefits in this top predator, and it can even reduce the amount of prey obtained (Bertram, 1978). As a consequence of this, shoaling may become a disadvantage, since the competition for obtaining food is higher than the profit gained in findings. Also, as top predators of the river, fishes of this size will have virtually no predator to cause them to remain together for protection, or being confined in a specific area of the river. On the other hand, as a rare fish, L. japonicus is likely to have problems finding sexual partners, and shoaling may benefit reproduction success by increasing the access to mates (Nordell and Valone, 1998; Wagner et al., 2000; Ruhl and McRobert, 2005). This study was carried in July, possibly close to the spawning period, believed to happen from late June to early August (Kinoshita et al., 1988; Iwatsuki et al., 1994). Sadly, since the intrinsic motivation for forming these shoals still remains unknown, and because of the limited information available until now, we are not able to define them as either a school or a swarm. We refer to these groups as shoals, in its heuristic sense (Delcourt and Poncin, 2012). Our assumption is that this fish spends most of its time inside shoals, which remain close to other shoals, and during short periods, duly leaves the shoal for hunting prey and before returning to the shoal. But if this behaviour happens only during the spawning season, or if it continues throughout the year is not known. It is also not known if there are night-day differences in forming the shoals.

4.2. Evaluating the threats

Akame is not commercially targeted for being used in cuisine, but other types of fishing pressures can have an impact in its populations. Juveniles of this species are being caught for aquarium trading, and adults are under pressure from sport fishing. Additionally, reclamation and pollution due to the urbanization of the riverside are affecting the environment where this species lives, thus probably having an impact on this species too. The encounter of the study fish with several fishing gears, shows the potential danger that commercial fishing may also be representing for this species. Even when not targeted specifically, the risk of by-catch of small individuals and juveniles, needs to be considered as well. Additionally, changes in prey abundance and distribution can modify the spatial distribution and habitat use of predators (e.g. Wolff et al., 2015) generating survival imbalances at different life stages in Akame. Because shoals provide higher probabilities of getting a profitable catch (Mackinson et al., 1997), they are susceptible to be targeted by recreational fishing, a common practice in our study area. Recreational fishing in this area is mainly a catch-and-release sport fishing, which often does not generate an immediate mortality on the individuals captured (Cooke and Philipp, 2004), but that has been proved to have an impact in fish populations (Westera et al., 2003; Cooke et al., 2006). Management agencies have also pointed out angler pressure as a major factor affecting recreational fisheries in freshwater systems (Mather et al., 1995), thus we may expect recreational fishing is having an impact on this fish.

4.3. Methodology

Digital imaging proved to be a useful technique for studying the aggregative behaviour of Akame, and to first approach the type of habitat this fish is using. Despite the limitations in storage capacity and battery, clear shoals were identified using the DSL (digital still-camera logger), as it were the type of bottom and artificial structures (like fishing gears) that this species might be dealing with frequently. Due to limitations in the weight and volume that can be attached to a fish, only adults could be studied using a DSL. For studying other life stages, bio-telemetry using acoustic pingers or miniaturized loggers are probably better solutions. Nevertheless, bio-logging tools proved again to be an effective method for studying endangered species. More and more, this science is spreading all over the world and reaching a vast amount of species thanks to its adaptation and miniaturization. Protecting endangered species is an important task, and these tools can help us achieve it.

5. Conclusions

The tendency of this species to adopt shoaling behaviours provide useful information for the conservation of the populations of Akame in the Shimanto River. There are potential aggregation areas, where big adults (and therefore potential spawners), may spend most of their time, that can be protected during sensitive times. Since groups of individuals tend to create a cohesive population, we believe that protecting areas where shoals are gathering is a good measure to take. In marine environments, partial MPA effectiveness has being questioned, arguing that they have a limited role in protecting targeted species (e.g. Denny and Babcock, 2004 and Di Franco et al., 2009). Nevertheless, some studies have shown that, especially for recreational angling, they can provide significant benefits to exploited stocks (Bohnsack, 2011; Alós and Arlinghaus, 2013). One of the effects that partial MPAs seem to have in recreational angling is a reduced fishing pressure due to a reduction in the attractiveness of the when it is regulated (e.g. Beardmore et al., 2011 and Johnston et al., 2011). Although freshwater systems present several differences from marine ones, we believe that such differences will not affect significantly the results obtained from a protected area. Catch-and-release is known to have low mortality rates (Alós et al., 2009; Veiga et al., 2011) and, under certain restrictions to ensure that released fishes survive with minimum stress, S. Gonzalvo et al. / Global Ecology and Conservation 3 (2015) 831–838 837 this activity can be compatible with protection objectives. Akame is known to be a ‘‘strong fish’’, able to survive capture and transport (Tashiro and Iwatsuki, 1995), thus this may be a good option to ensure the continuity of this fish in the Shimanto River. Protected Areas (PAs) have proved to be an effective management tool for protecting declining local populations of fishes and biodiversity (e.g. Hilborn et al., 2004), but their success depends on proper implementation. For establishing a coherent and functional PA, a wide range of assessments are necessary, involving not only biological and ecological features, but also the impacts on nearby communities and stakeholders. Sadly, these assessments are out of the scope of the data presented here.

6. Future suggestions

As mentioned above, there is not enough data to make a complete assessment for the protection of this species. We hope that this study encourages other studies to take place and enlighten many aspects that remain unknown of this fish, to be able to establish a comprehensive management plan. We would like to recommend some ideas for following studies as we believe these aspects are essential to create a functional protected area. Following the data of this paper, we propose to find out if there is only one main group or if the population is divided into several groups moving independently, and whether those shoals inhabit a fixed area of the river or they change temporally. An estimation of the population size of Akame is also necessary. Migrations to and from the sea it are still unexplored, therefore, if there is a connexion between populations in the Shimanto River and other nearby different rivers remains unknown. Thus, we suggest to explore these aspects to estimate the size of the populations, and understand if we must think of each river population as an independent group or we must think of the species as a whole population inhabiting different rivers. Also, many aspects of its biology and ecology remain obscure, and are also imperative for protecting this fish. For example, they are supposed to be catandromous and protandrous , but are they really so? If they are, when do they make the shift from male to female? When does it go to the sea? Does it return to the river or go to the sea to live there? If it returns, does it happen seasonally? Spawning area and seasonality should be clearly identified, if we are to understand when this species is more sensitive to fishing pressure. The list of questions and tasks to do can be much longer, but we believe there is enough justification to understand that more research is needed to be able properly comprehend species. Notwithstanding of all the information lacking, we believe that some measures need to be taken as soon as possible to ensure the continuity of the Shimanto River Akame populations, and that these must be made step-by-step together with all interested parties. We believe that the current educational programs to raise awareness about the delicate situation of this fish are a good start that can involve all parties. Yet, this is only the beginning of what should become a larger protection program to ensure that future generations will be able to know this fish. Hopefully, when more information is gathered, new steps can be taken to protect this fish from local extinction.

Acknowledgements

We want to thank all the people that help in obtaining the data and made this project possible. Thanks to T. Tsujino, I. Suzuki, professor N. Miyazaki, and all the researchers and students that collaborated in the project, as well as to Professor Y. Naito of the National Institute of Polar Research for his assistance with the loggers. Also, thanks to all the local people who assisted us: T. Sugimura, S. Nomura, and all the staff of the Shimantogawa Gakuyukan, K. Yamasaki and the staff of the Fisheries Cooperative Association of the Shimanto River, T. Yasumitsu, T. Nishimura, K. Mouri and K. Takimoto of the sport fishing experts team ‘‘Submarine’’, and T. Yamasaki and the staff of the Akamekan. Additionally, thanks to all the people helping in the elaboration of this paper. Special thanks to Takayoshi Otaki, for his constant support and sharing his valuable knowledge of bio-logging tools, and R. Castro, for his help in the edition of this paper. Richard T Corlett, David Bierbach and all the editors and reviewers that patiently gave corrections and more than helpful suggestions. The data used in this paper was obtained under the economic support of the Bio-logging Science program of the University of Tokyo (UTBLS), the Japan Broadcasting Corporation, and Interdisciplinary Collaborative Research of Atmosphere and Ocean Research Institute, the University of Tokyo.

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