Fish Sci (2011) 77:79–85 DOI 10.1007/s12562-010-0313-8
ORIGINAL ARTICLE
Biology
Effect of shelter acclimation on the post-release survival of hatchery-reared black-spot tuskfish Choerodon schoenleinii: laboratory experiments using the reef-resident predator white-streaked grouper Epinephelus ongus Yuuki Kawabata • Kimio Asami • Masato Kobayashi Taku Sato • Koichi Okuzawa • Hideaki Yamada • Kenzo Yoseda • Nobuaki Arai
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Received: 9 October 2010 / Accepted: 14 November 2010 / Published online: 8 December 2010 Ó The Japanese Society of Fisheries Science 2010
Abstract A critical component of many releasing projects is the identification and subsequent implementation of optimal release strategies that can decrease post-release predation mortalities. We performed laboratory experiments to investigate whether acclimation to shelters affects the post-release survival of hatchery-reared black-spot tuskfish Choerodon schoenleinii in the presence of a reefresident predator, the white-streaked grouper Epinephelus ongus. Tuskfish were exposed to groupers under three different experimental conditions/treatments: (1) acclimation of fish to shelters prior to their exposure to groupers; (2) no acclimation of fish to shelters, but with shelters available during their exposure to groupers; (3) fish not acclimated to shelters and no shelters available during their exposure to groupers. Tuskfish that were acclimated to shelters utilized shelters more frequently than did nonacclimated fish, and the survival rate of acclimated fish was
Y. Kawabata (&) N. Arai Graduate School of Informatics, Kyoto University, Sakyo, Kyoto 606-8501, Japan e-mail:
[email protected] K. Asami M. Kobayashi T. Sato K. Okuzawa H. Yamada K. Yoseda Ishigaki Tropical Station, Seikai National Fisheries Research Institute, Fisheries Research Agency, Ishigaki, Okinawa 907-0451, Japan Present Address: K. Asami K. Yoseda National Research Institute of Fisheries and Environment of Inland Sea, Fisheries Research Agency, Hatsukaichi, Hiroshima 739-0452, Japan K. Okuzawa National Research Institute of Aquaculture, Fisheries Research Agency, Minami-ise, Mie 516-0193, Japan
higher than those of fish in the other treatments. These results suggest that pre-release acclimation to shelters improves the post-release survival of hatchery-reared black-spot tuskfish. Keywords Captive-bred Learning Mesocosm Predator–prey interaction Restocking Stock enhancement
Introduction Hatchery-reared fish have been utilized to support sustainable fisheries worldwide. Unfortunately, in some cases, such projects have failed to increase wild population levels [1–3], with many of these failures attributed to predation mortalities during relatively short periods after release [2, 4, 5]. Such results emphasize the necessity of identifying and implementing optimal release strategies that can decrease post-release predation mortality. One possible approach to decreasing post-release predation mortality is to acclimate the fish to wild habitats prior to release. The results from both field and laboratory experiments on flounder species suggest that pre-release habitat acclimation benefits hatchery-reared fish by allowing them to adjust to the wild habitat, thus decreasing postrelease predation mortality [6–8]. However, except for these studies on flounder species, only a few studies have investigated the effects of habitat acclimation on the postrelease survival of fish [9]. The black-spot tuskfish Choerodon schoenleinii is a highly prized commercial fish which has been targeted for stock enhancement in Okinawa Prefecture, Japan [10]. It lives around coral reefs from the Ryukyu Islands to the West Pacific (IUCN red list of threatened species; available
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at: http://www.iucnredlist.org) and is generally territorial, utilizing sandy and gravelly areas near lagoons and seaward reefs [11, 12]. At night or when threatened, the fish rests in a burrow-like shelter which it excavates at the base of hard substrates, such as limestone reefs [11]. In a previous stock enhancement project, hatcheryreared black-spot tuskfish [total length (TL) 50–100 mm] were released into dead coral patches located along the coast of Ishigaki Island in Okinawa Prefecture. Subsequent sampling revealed some of the released fish among the stomach contents of a reef-resident piscivore (white-streaked grouper Epinephelus ongus) and a transient piscivore (brassy trevally Caranx papuensis), and all released fish had disappeared from the release site within 2 weeks of release (Okuzawa et al., unpublished data, 2009). Post-release predation mortality is a plausible cause for this rapid disappearance; therefore, developing release strategies that reduce post-release predation mortality is a priority for ensuring the success of the stock enhancement of this species. The objective of this study was to investigate the effects of acclimation to shelters on the post-release survival of hatchery-reared black-spot tuskfish in the laboratory setting using a reef-resident predator, the white-streaked grouper. As it was necessary to establish a lack of size-related differences in predator avoidance or prey-capture abilities, the effects of prey and predator sizes on the survival rate were determined first. The effects of acclimation to shelters were then examined to determine whether acclimation would enhance the use of shelters by the tuskfish and consequently decrease predation mortality.
Materials and methods Sample fish Immature hatchery-reared black-spot tuskfish Choerodon schoenleinii (size range 60–120 mm TL) were utilized in this study. All individual tuskfish had been reared at Yaeyama Station, Seikai National Fisheries Research Institute, Fisheries Research Agency. As predators, we used the white-streaked grouper Epinephelus ongus (size range 200–280 mm TL) because this species is one of the most abundant piscivores around Ishigaki Island [13], is abundant around the release site of the hatchery-reared tuskfish, and has been found to prey upon released tuskfish (Okuzawa et al., unpublished data, 2009). The size range (200–280 mm TL) used in this study represents the major size range of white-streaked groupers around the release site of black-spot tuskfish (Kawabata et al., unpublished data, 2009). The grouper employs a ‘‘sit-and-wait’’ tactic throughout the day but occasionally employs a ‘‘stalk-andattack’’ tactic during crepuscular periods (Kawabata et al.,
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unpublished data, 2009). The groupers were collected off the coast of Ishigaki Island using a hook-and-line method from April to May 2009. The collected fish were kept in 1000-l black polyethylene tanks for at least 2 weeks before the start of the experiments. They were standardly fed pieces of double-lined fusilier Pterocaesio digramma once every 2 days and occasionally fed hatchery-reared blackspot tuskfish. Effects of size In the case of there being no difference in survival rate among treatments, it was necessary to establish a lack of size-related differences in predator avoidance or prey-capture abilities [14, 15]. Therefore, the effects of prey and predator sizes on the survival rate were determined in a preliminary study performed from 3 to 17 June 2009. Three identical 5000-l rectangular tanks [1.4 (width) 9 3.0 (length) 9 0.8 (depth) m] with the bottom of each covered with an 80-mm-deep layer of sand were used for the experiment. Three shelters for the grouper [constructed of a cylindrical-shaped polyvinyl chloride pipe cut in half lengthwise; inside space: 0.3 (diameter) 9 0.2 (length) m] were deployed on one side of each tank to alleviate stress in the fish (Fig. 1). Water depth was maintained at 0.3 m in each tank. Nine groupers were divided into three size groups [small 208–214 mm (mean ± standard deviation 210 ± 35 mm, n = 3), medium 235–242 mm (239 ± 38 mm, n = 3), and large 268–277 mm (272 ± 46 mm, n = 3)], and three fish from the same group were stocked in the same tanks. The groupers had been starved for 72 h and acclimated to the tank for 24 h prior to the start of the trial. We then measured the TL of the tuskfish and divided them into five different size groups: TL B 80 mm (73 ± 4 mm), 80 mm \ TL B 90 mm (84 ± 3 mm), 90 mm \ TL B 100 mm (96 ± 2 mm), 100 \ TL B 110 mm (105 ± 4 mm), and 110 mm \ TL (115 ± 3 mm). Two fish from each group were introduced into each experimental tank. Therefore, there were ten tuskfish and three groupers in each tank when the experiment started (in total, 30 tuskfish and 9 groupers were used in this experiment). Even though the densities of predators and preys were relatively high (10 tuskfish and 3 groupers in 4.2 m2), similar densities have been reported around the release site following the release of hatchery-reared blackspot tuskfish (Kawabata et al., unpublished data, 2009). After an experimental period of 14 days, surviving tuskfish were captured and their TL measured to identify which tuskfish had been eaten. The difference in TL between any two tuskfish in each tank was at least 3 mm; the fish grew 3 ± 1 mm in TL during the experimental period, the variance of which was relatively small. Therefore, it was possible to identify which tuskfish had been eaten based on the measurement of their TL. During the experiment, the
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Treatment: AS c Partition c Tuskfish Shelters
Groupers G c
Partition
Tuskfish
Treatment: NAS c Partition c Groupers Shelters
c
Partition Treatment: NS c Partition c Tuskfish
Groupers Partition
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Fig. 1 A schematic drawing of the overhead view of the three treatments. NA Black-spot tuskfish (Choerodon schoenleinii) were acclimated to shelters prior to exposure to white-streaked groupers (Epinephelus ongus) (AS, top), not acclimated to shelters but shelters were available during exposure to groupers (NAS, middle), and not acclimated to shelters and no shelters were available during exposure to groupers (NS, bottom). Partitions were removed at the start of the experiment
groupers were starved, but the tuskfish were fed on a commercial diet (Edzuke-ru L; Chubu Shiryo, Chita-city, Japan) twice a day to prevent starvation. Air and water were continuously supplied to the tanks, and water temperature ranged from 25.5 to 27.1°C during the experiment. Light from a nearby window provided the tanks with light under a natural photoperiod. During the experimental period, no tuskfish mortality other than predation mortality occurred. Effects of acclimation to shelters Whether acclimation to shelters would enhance shelter utilization by tuskfish and thus decrease predation mortality by the grouper was investigated in trials conducted from
21 June to 2 August 2009. The same tanks used in the previous experiment were used in this experiment. Since there was no significant effect of grouper size on the predation probability of the tuskfish in the preliminary experiment (see ‘‘Results’’), groupers ranging from 200 to 280 mm TL (233 ± 26 mm) were used in this experiment without any consideration of their sizes. Three groupers were stocked into each tank and starved for 120 h before the start of the experiment. Based on the results of the preliminary experiment (see ‘‘Results’’), black-spot tuskfish which were smaller than 90 mm TL (84 ± 5 mm) were utilized in this experiment to eliminate the effects of tuskfish size on survival. The tuskfish were exposed to the groupers under three different experimental conditions/ treatments: (1) fish acclimated to shelters prior to their exposure to the groupers (AS); (2) fish not acclimated a priori to shelters, but with shelters available during their exposure to the groupers (NAS); (3) fish not acclimated a priori to shelters and with no shelters available during their exposure to the groupers (NS) (Fig. 1). In each treatment, two 0.6 9 0.6 9 0.6-m3 partitions made of plastic mesh, with no bottoms or tops, were set on the side of the tank opposite the grouper shelters (Fig. 1). In treatments AS and NAS, three tunnel-shaped shelters made of brick were provided for the tuskfish in one of the partitioned areas; the space available inside these shelters varied due to differences in height (height 20, 40, or 60 mm; width 80 mm; length 230 mm). No shelters were deployed in treatment NS (Fig. 1). After measuring its TL, we introduced one tuskfish into the partitioned area of each tank: the fish was introduced into the area containing shelters in treatment AS and into the area without shelters in treatments NAS and NS. The tuskfish were introduced at 1200 hours and acclimated for 45 h before the predation trial. During the acclimation period, the tuskfish were fed on commercial diets (Edzuke-ru L; Chubu Shiryo Co.) twice a day to prevent starvation. After the acclimation period, the trial was started by removing the partitions to release the tuskfish at 0900 hours, and the trail was completed 24 h after the release. Survival and shelter utilization of the tuskfish were recorded every 4 h during the trial; ‘‘shelter utilization’’ was defined as the presence of the fish in a shelter or its entering a shelter when the observer approached to the tank for the observation. A hand torch covered by red film was used for nighttime observations to minimize disturbance to both predator and prey. At the end of the trial, we recorded whether the tuskfish had excavated underneath the shelters. The trial was replicated nine times using the same groups of groupers, and then eight and seven additional replications were conduced for AS and NAS trials, respectively, using other groups of groupers. We changed the groupers after the ninth trial because they had become accustomed to the experimental procedure.
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Statistical analyses The object of the ‘‘Effects of size’’ experiment was to investigate whether predation was size dependent. Because the data sets were not normally distributed in all treatments, we compared the sizes of the surviving and preyed tuskfish in each tank (with each size group of grouper) using Mann–Whitney U tests. The effect of size or treatment on survival was examined using logistic regression analysis [16]. The survival and death of the tuskfish were designated as 1 and 0, respectively, and used as the objective variable. In the ‘‘Effects of size’’ experiment, the TL of the tuskfish (tuskfish size), the size group of the grouper (grouper size), and their interaction were first included as explanatory variables. In the ‘‘Effects of acclimation to shelters’’ experiment, the treatment (AS, NAS, and NS) was regarded as an explanatory variable; a blocking variable for different groups of grouper was also included in the model to partition and statistically remove the effects of predator ability. The significance of these explanatory variables was then assessed by progressively removing them from the model and comparing the change in deviance, G, using a G test. In the ‘‘Effects of size’’ experiment, the final model for estimating sizedependent predation probability was also determined by progressively removing the explanatory variables when the variables were not significant in the G test. All statistical analyses were performed using R 2.8.0 (The R Foundation for Statistical Computing, Vienna, Austria).
Results Effects of size Surviving fish were significantly larger than preyed fish in all three treatments (Mann–Whitney U test surviving vs. preyed; predatory grouper size: 81 ± 9 vs. 109 ± 8 mm
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Survival or preyed
Different groupers were not used for each trial, as it would have been difficult to collect sufficient white-streaked groupers for the experiment (e.g., nine trials would have required 81 groupers). Only AS and NAS were replicated further to increase the sample size required for the data analysis of the shelter utilization patterns of the tuskfish. The tanks for the treatments were rotated in each trial to avoid unspecified factors associated with particular tanks. Air and water were continuously supplied to the tanks, and water temperature ranged from 27.4 to 29.6°C during the experiment. Light from a nearby window provided the tanks with a natural photoperiod. During the experimental period, no tuskfish mortality other than predation mortality occurred.
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0.5
0 60
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T Total length of black-spot tuskfish (mm) Fig. 2 Relationship between size and survival of black-spot tuskfish. Survival and death of the fish are plotted as 1 and 0, respectively, and denoted by open circles. The logistic curve for the survival probability in relation to tuskfish size is also shown. The size at 50% survival was estimated to be 98 mm in total length (TL)
(small), 87 ± 13 vs. 109 ± 8 mm (medium), 83 ± 10 vs. 108 ± 8 mm (large), Z = 2.61, 2.17, 2.40, P \ 0.01, \0.05, \0.05, respectively). The sizes of the surviving and preyed black-spot tuskfish are shown in Fig. 2. The smallest surviving fish was 95 mm TL, while the largest preyed fish was 106 mm TL. There was a significant effect of tuskfish size on survival (G test, G1 = 26.9, P \ 0.01); however, the effects of grouper size and the interaction were not significant (G test, G2 = 2.78, G2 = 2.14, P = 0.25, 0.34, respectively). The model composed of the effects of tuskfish size was chosen as the final model, based on the results of the G tests. The survival probability in relation to tuskfish size was drawn by fitting a logistic curve to the final model, as shown in Fig. 2. The size at 50% survival was estimated to be 98 mm TL. Effects of acclimation to shelters Tuskfish under the AS treatment utilized shelters more frequently than those under the NAS treatment until 8 h after release; there were significant effects of treatment on shelter utilization (Fig. 3; 0, 4, 8 h after release, G test; G1 = 36.0, 21.1, 17.7, P \ 0.01, \0.01, \0.01, respectively). There were no significant effects of treatment on shelter utilization from 12 h after release onwards (G test, all G1 = 0, all P = 1) because most of the fish under the NAS treatment were preyed upon and all tuskfish which survived for more than 12 h after release utilized shelters. There were no significant effects of treatment on survival until 8 h after release (4, 8 h after release, G test, G2 = 2.88, 2.72, P = 0.21, 0.26, respectively). From 12 h
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survival in shelter
not in shelter
preyed
Treatment: AS (n=17) 1
NAS fish (50%) survived for 24 h after release, while seven of the 13 AS fish (54%) and one of the two NAS fish (50%) were preyed upon. Of the fish that did not excavate underneath shelters, one of the four AS fish (25%) and none of the 14 NAS fish (0%) survived for 24 h after release, while three of the four AS fish (75%) and all 14 NAS fish (100%) were preyed upon.
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Treatment: NAS (n=16) 1
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Elapsed time after release (hours) Fig. 3 Time-series survival and shelter utilization rates of black-spot tuskfish under each treatment regime. Details of treatments are shown in Fig. 1. White and black bars on the bottom represent daytime and nighttime, respectively. Numbers in parentheses below the elapsed time after release represent times of day. Superscript a denotes a significant treatment effect on shelter utilization (G test, P \ 0.01), superscript b denotes a significant treatment effect on survival (G test, P \ 0.01)
after release onwards, however, the survival rate of fish under the AS treatment was higher than that of fish under the NAS or NS treatment; there were significant effects of treatment on survival (12, 16, 20, 24 h after release, G test, G2 = 13.3, 10.3, 10.3, 10.8, P \ 0.01, \0.01, \0.01, \0.01, respectively). This was due to the sharp declines in the proportion of fish surviving between 8 (1700 hours) and 12 h (2100 hours) after release in treatments NAS and NS. Of the 17 AS fish, 13 (76%) excavated underneath shelters, while two of the 16 NAS fish (13%) excavated underneath shelters. Of the fish that excavated underneath shelters, six of the 13 AS fish (46%) and one of the two
Tuskfish acclimated to shelters utilized shelters more frequently than did non-acclimated fish, and the survival rate of acclimated fish was higher than that of non-acclimated fish or fish without shelters (Fig. 3). In addition, all tuskfish that survived for [12 h after release utilized shelters (Fig. 3). These results strongly suggest that acclimation to shelters enhances shelter utilization by tuskfish, thus decreasing their post-release predation mortality. The black-spot tuskfish is a diurnal coral reef fish: it moves actively during the day and rests in a shelter at night [17]. Diurnal coral reef fishes are reportedly most vulnerable to predators at dusk, and fish which utilize shelters poorly—or not at all—are more likely to be preyed upon by predators during this period [18], most likely because reefresident predators, such as groupers, employ the ‘‘sit-andwait’’ tactic throughout the day but occasionally transition to the ‘‘stalk-and-attack’’ tactic during crepuscular periods (Kawabata et al., unpublished data, 2009). The results from our study are consistent with those reported earlier. Many of the tuskfish that were not acclimated to shelters or not provided with a shelter at all were preyed upon between 1700 and 2100 h (dusk period); in contrast, none of the acclimated fish were preyed upon during this period (Fig. 3). We attributed this difference in final survival rates between the treatments to predation at dusk (Fig. 3). Our results clearly show that shelter utilization is very important for released tuskfish, enhancing their survival from predation at dusk, and that shelter utilization can be enhanced by acclimating hatchery-reared tuskfish to the availability of shelters prior to release. In terms of predator avoidance, the shelters can be considered to have two primary functions, namely, as a visual barrier and as a physical barrier, as suggested by the functions of corals and seagrasses in predator avoidance [19, 20]. In its natural habitat, the black-spot tuskfish excavates underneath a hard substrate to create its own shelter [11]; in our experiment, almost all of the tuskfish that utilized shelters excavated underneath these shelters so that the entrance became narrower and the inside space larger. This excavation would probably enhance both of the aforementioned functions of a shelter because the tuskfish were difficult to observe from the outside and the narrower
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entrance would make it more difficult for predators to enter the shelter. The relative importance of these functions was not clear in this study; however, it is highly likely that these functions associated with the physical presence of the shelter and excavation led to the lower predation rate on the black-spot tuskfish in our experiment. Even though shelter utilization decreased predation mortality, some of the fish that utilized and excavated shelters were preyed upon in this study, especially up to 8 h after release. This predation is likely attributable to the tuskfish’s incautious departure from the shelter and approach to the groupers; we occasionally observed tuskfish incautiously approaching groupers. A combination of the acclimation to shelters conducted in this study and predator-recognition training, as suggested in numerous previous studies [21–23], might lead to more cautious behavior in tuskfish when leaving shelters and encountering predators, thus further decreasing predation mortality. Whether this utilization of shelters (enhanced by acclimation) is useful for enhancing avoidance behavior to other types of predators is uncertain. There have been reports that the habitat complexity of seagrass [24, 25] or burrows [26] reduces predation from one type of predator, but not from other types. The brassy trevally, a diurnal transient piscivore, is a candidate as a major predator of released black-spot tuskfish (Okuzawa et al., unpublished data, 2009) and has been reported to use a different foraging tactic from those employed by reef-resident predators [27]. Thus, research using this species is needed to further elucidate the effects of shelter acclimation on the post-release survival of tuskfish. We observed that shelter acclimation enhanced shelter utilization by black-spot tuskfish and, hence, decreased predation mortality from a reef-resident predator (whitestreaked grouper). Most of the sedentary juvenile fish that are used for stock enhancement utilize habitats for predator avoidance: coral trout hide in small coral spaces [9], red drum and red sea bream are cryptic in seagrass [20, 28], and red tilefish dig hiding burrows in muddy substrates [29]. Based on the results of our study, acclimation to these habitats may be a useful approach for mitigating the postrelease predation mortality of these species. Acknowledgments We thank T. Takebe, N. Hirai, T. Kurihara, A. Nanami, G. Suzuki, S. Arakaki, and other members of the Ishigaki Tropical Station, Seikai National Fisheries Research Institute, Fisheries Research Agency, for research assistance, valuable comments, and encouragement. We also thank I. Ohta at the Okinawa Prefectural Fisheries and Ocean Research Center for providing valuable information on the black-spot tuskfish and white-streaked grouper, and R. Masuda at the Maizuru Fisheries Research Station, Kyoto University, for providing helpful comments on determining experimental procedures. We wish to express appreciation to D. Izumida and S. Katayama at the Institute for East China Sea Research, Nagasaki University, for their help in collecting white-streaked
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