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Ontogenetic behavior of farm-bred Russian sturgeon (Acipenser gueldenstaedtii) prelarvae in a diel photoperiodic cycle: behavioral modifications in response to light intensity

Ontogenetic behavior of farm-bred Russian sturgeon (Acipenser gueldenstaedtii) prelarvae in a... Russian sturgeon (Acipenser gueldenstaedtii) is commercially important in Korea because its caviar is highly prized. Although the early ontogeny of the species has been described, behavioral modifications in response to various light intensities or diel photoperiodicity patterns have not been studied extensively. The objective of the present study was to examine the behavioral characteristics of hatchery-produced A. gueldenstaedtii prelarvae over a diel photoperiodic cycle. During a diel light cycle comprising 16 h of daylight (450 lx), 4 h of dim light (10 lx), and 4 h of darkness (< 1 lx), newly hatched A. gueldenstaedtii prelarvae exhibited negative phototaxis in daylight (day 0–day 2), and this early behavior was not significantly affected by changes of light intensities. Rheotactic and non-rheotactic aggregation into schools was typical between days 3 and 6. Under the diel light cycle conditions described, rheotaxis was not influenced by environmental light intensity as much as non-rheotactic schooling behavior. Post-schooling behavior, which progressed from day 7 to day 8, did not change significantly during the diel light cycle. The data from the present study could be of practical value in developing a visual guide for assessing the fitness and quality of Russian sturgeon prelarvae under diel light cycle conditions in hatcheries. Keywords: Russian sturgeon Acipenser gueldenstaedtii, Phototaxis, Ontogeny, Behavioral modifications Background Light-dependent behavior in sturgeon prelarvae is Sturgeon, which are extant primitive fish of the order established as early as the mass hatching stage (Dettlaff Acipenseriformes, are highly valued as a source of caviar et al. 1993), but this innate trait differs considerably among (LeBreton et al. 2006). However, because almost all wild Acipenser species. During early life, sturgeons exhibit posi- sturgeon populations are threatened or endangered, the tive, negative, or no phototactic characteristics depending artificial propagation of sturgeon has become important on species-specific adaptation to the natural habitat for the sustainable production of caviar and for restock- (Chebanov and Galich 2011; Zhuang et al. 2002;Gisbert ing natural populations (Doukakis et al. 2012; Johnson and Ruban 2003; Williot et al. 2009). and Iyengar 2015). Light is a critical factor that influ- In the context of aquaculture, species-specific light- ences the behavior and other physiological characteris- dependent behaviors are important for enabling hatchery tics of sturgeons, especially during their prelarval and managers to define visual criteria for the ontogenetic larval stages (Dettlaff et al. 1993; Loew and Sillman development of prelarvae and to explicitly evaluate the 1998;Chebanov and Galich 2011; Zaheh et al. 2013). fitness and physiological state of the prelarvae. It is therefore helpful to develop optimal illumination re- * Correspondence: yoonknam@pknu.ac.kr gimes for prelarval nurseries of target sturgeon species Department of Marine Bio-Materials and Aquaculture, Pukyong National (Gisbert and Solovyev 2018). Most sturgeon species are University, Busan 48513, Republic of Korea characterized by a lengthy period of prelarval development Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Kim et al. Fisheries and Aquatic Sciences (2019) 22:4 Page 2 of 10 (usually more than 1 week) and undergo dynamic changes the incidence of abnormality in 240 embryos and 360 to their ontogenetic behavior during that period (Gisbert hatchlings, respectively. et al. 1999a; Gisbert and Nam 2018). Usually, hatcheries apply a photoperiod regime during the prelarval rearing Prelarval rearing and sampling period. Therefore, the behavioral characteristics of the We transferred newly hatched prelarvae (n = 4500) col- sturgeon are potentially influenced by the diel photo- lected within 4-h intervals to one of three replicate tanks periodicity of the hatchery. (width × depth × height = 1.2 m × 2 m × 0.25 m), each con- The Russian sturgeon (Acipenser gueldenstaedtii)is taining approximately 300 L of 1-μm filtered groundwater. one of the most commercially important Acipenser Each replicate tank was equipped with a custom-designed species—mainly because its caviar (“Ossetra caviar”)is filter unit (200 L volume) and water was re-circulated highly prized—and is now an important candidate species through the filter unit at a flow rate of 8 L/min using a in Korean aquaculture (Kim et al. 2018;Park 2018). The submersible circulation pump. Throughout the experi- ontogeny and general behavioral patterns of artificially ment, we maintained the water temperature at 20 ± 0.5 °C produced Russian sturgeon have been described by several using automatic thermostat-assisted heaters and the dis- research groups (Dettlaff et al. 1993; Chebanov and Galich solved oxygen content at 8.0 ± 0.5 ppm using air diffusers 2011;Kynard etal. 2002). However, previous studies on connected to an electric air pump. The pH of the in-tank farm-bred Russian sturgeon have mainly described the water ranged from 7.2 to 7.4 during the experiment. We behavioral patterns observed during daylight hours only immediately removed and counted dead or apparently (Chebanov and Galich 2011;Kynard et al. 2002). In con- malformed individuals. Every day, we sampled 12 prelar- trast to the relative abundance of information on daylight vae from each tank replicate (i.e., 36 fish) to determine behavior, behavioral modification patterns in response to growth and morphological differentiation. We measured various light intensities, or during a diel photoperiodic the total length and body weight of each prelarvae to the cycle, have not been extensively explored. Such a paucity nearest 0.1 mm and 0.1 mg, respectively. We recorded limits the visual criteria-based evaluation of prelarval the morphological development of the prelarvae with ontogeny to daylight hours, and may also hinder a full an AZ100 microscope (Nikon, Tokyo, Japan) and NIS- comprehension of the diel patterns of the activities and Elements basic research image analysis software. We behaviors in hatcheries. Therefore, the objective of the provided the first exogenous feed (100 μm-sized powder present study was to examine the behavioral character- for flounder larvae; Woosung Corp., Republic of Korea) istics of hatchery-produced Russian sturgeon prelarvae on day 9. during a diel photoperiodic cycle consisting of three different light intensity conditions (i.e., daylight, dim Setting the experimental diel light cycle light, and darkness). We reared the prelarvae in an experimental room (located on the first basement floor), which was covered in blinders to exclude external light. To assess the onto- Methods genetic behavior of the sturgeon prelarvae in a diel light Hormone-induced spawning and artificial fertilization cycle, we set a photoperiod cycle in the following order We obtained the Russian sturgeon (Acipenser guelden- of precedence: light (L) for 16 h, dim light (DL) for 4 h, staedtii) used in the present study from Dinoville and darkness (D) for 4 h. The illumination conditions Sturgeon Aquafarm, Hamyang, Kyoung-nam, Republic for each interval were as follows: (1) L, the light inten- of Korea. We injected luteinizing hormone-releasing sities across the experimental tanks averaged 450 lx sup- hormone analog (LHRH-a; Sigma-Aldrich, St. Louis, plied by white light-emitting diode (LED) lamps (23 W) MO, USA) into the muscles of mature female (n =2) enclosed in translucent plastic covers and installed on and male (n = 3) broodfish at dose levels of 80 μg/kg for the ceiling approximately 3 m above the tanks; (2) DL, females and 20 μg/kg for males to obtain eggs and milt all the white LED lamps were turned off, and translucent (Kim et al. 2018;Park 2018). We used the wet method glass-covered incandescent lightbulbs (7 W; 6500 K) pro- for artificial fertilization and treated the fertilized eggs vided 10 lx across the experimental tanks; (3) D, an in- with anti-adhesive agent (Fuller’s earth; Sigma-Aldrich), frared (IR) LED spotlight (10 W; 730 nm) was set to as described by Kim et al. (Kim et al. 2018). shine toward the wall, which was more than 8 m away We maintained the water temperature of the hatching from the experimental tanks, and the light intensity was incubator at 20 ± 0.5 °C until hatching commenced using less than 1 lx. We monitored transitions in diel behav- thermostat-assisted submergible aquarium heaters (300 ioral patterns—including negative geotaxis (also called W). We estimated the fertilization rate in three random swimming-up), rheotaxis, schooling, and post-schooling samples each consisting of 120 embryos at 2 h post- behavior—under the diel light cycle from day 0 to day 9. fertilization (HPF). We estimated hatching success and We examined ontogenetic diel behavior patterns at 1 h Kim et al. Fisheries and Aquatic Sciences (2019) 22:4 Page 3 of 10 before the end of the L-phase, 1 h after the DL-phase, by two observers per replicate tank, and the observers and 1 h after the D-phase. We also made random exami- were randomly assigned to each replicate tank for every nations when we observed typical transitions and/or observation time. Under L and DL conditions, each ob- modifications of behavior. server took at least six snapshots and taped a movie video using a digital camera equipped with an iPhone Behavioral criteria (version later than 7; Apple Inc., USA). Each observa- Based on previous reports on the behavioral ontogeny of tion lasted 15 min. We analyzed the selected photo- Acipenser species (Gisbert and Solovyev 2018; Park 2018), graphs and videos using Photoshop (Adobe Inc., USA). we applied seven main criteria to define and evaluate However, we recorded behavioral patterns under D potential modifications to behavioral characteristics of conditions using an IR light illuminator (850 nm; Fenix, Russian sturgeon during the prelarval period from days USA) and/or an IR night vision camera (Ancter, USA). 0 to 9. The criteria included negative geotaxis and passive We carried out quantitative assessments on day 0 on a drift, pelagic swimming in the upper water column, small number of newly hatched prelarvae (n = 120/tank) benthic swimming, early corner-gathering, rheotactic assigned to three small rectangular tanks (30 cm × 60 schooling, non-rheotactic schooling, and post-schooling cm × 25 cm) with white bottoms. We counted the num- behavior (Table 1). bers of prelarvae at least six times for each replicate tank. During day 1 to day 3, we determined the propor- Observation regimes tion of early corner-gathering prelarvae in the rearing According to our principal objective to provide hatchery tanks. Some early prelarvae gathered at a corner of each managers with a visual guide for ontogenetic modifications tank, and we trapped those prelarvae inside acryl bar- of prelarval behaviors in response to a diel photoperiodi- framed 500-μm mesh screens (50 cm × 50 cm square). city, the present study essentially included observational The observers counted the number of prelarvae inside data based on prelarval rearing conditions that were simi- or outside the square area at least three times and took lar to those conventionally used in Korean sturgeon pictures to determine the percentage of early corner- hatcheries. For this reason, the statistical evaluation of gathering prelarvae out of the total number of fishes behavioral patterns with accurate counting of prelarvae per tank. When the schools formed at the corners and/ belonging to a particular behavioral criterion might not or water-inlet sites (days 3 to 5), we calculated the be relevant in all aspects of analysis. Therefore, we only number of prelarvae participating in schooling in each obtained numerical data addressing behavioral patterns replicate tank using an acryl bar-framed screen identi- and/or responses at several detection time-points. cal to that described above. On day 8, we installed three All observers had experience of at least three other square frames (30 cm × 30 cm) in each replicate tank to sturgeon-breeding experiments from the preceding 5 estimate the proportion of prelarvae exhibiting typical years. Evaluation of prelarval behavior was carried out post-schooling behavior inside the frame. Table 1 Main behavioral criteria of Russian sturgeon Acipenser gueldenstaedtii prelarvae assessed in this study Behavioral criteria Behavioral characteristics in tank Negative geotaxis and drifting behavior Upward movement toward water surface by active propelling of the posterior body trunk and tail, and then passive settlement to the bottom; prelarvae rest on their side or yolk sac before active swimming-up starts again Pelagic swimming Swimming at water surface or upper water column for a long time in a certain direction Benthic swimming Free swimming for a short or long distance along the bottom of the tank, without displaying other behavioral types Early corner-gathering Approaching the corner(s) of the tank; hatchlings and early prelarvae gather and aggregate loosely into a “school-like” appearance at the corner(s) Rheotactic schooling Aggregation of large number of positively rheotactic prelarvae into a school-shaped group on the bottom of the tank; prelarvae swim against water current with active propelling movement Non-rheotactic schooling Dense aggregation of large number of prelarvae into schools, usually at the corner(s) of the tank where no significant water current exists; prelarvae approach the center of the corner with active propelling of posterior body trunk and tail Post-schooling behavior Non-locomotory, inactive, being dispersed or scattered over the bottom of the tank; prelarvae represent a sign of the initiation of the post-schooling behavior as a slow-wagging motion without locomotory activity Behavioral criteria were compiled from previous literatures with Acipenser species (Gisbert and Ruban 2003; Gisbert and Solovyev 2018; Gisbert et al. 1999a; Park 2018 Kim et al. Fisheries and Aquatic Sciences (2019) 22:4 Page 4 of 10 Results vale shape, and swimming structures including various Prelarval viability, growth, and morphological fins had developed by day 4. Almost the entire body development had become darkly pigmented and dorsal scute rudi- We obtained approximately 110,000 fertilized eggs. The ments had begun to appear by day 8 (Additional file 1: fertilization rate averaged 95 ± 2%. The mean hatching Figure S1). successes (%) and incidence of abnormality (%) were 77 ± 9% and 2.1 ± 0.8%, respectively. There was no signifi- cant mortality during the prelarval period up to and in- Movement of newly hatched prelarvae and early cluding day 9. Prelarval survival averaged 98.4%. The swimming behavior average total length and body weight of the newly The light-dependent behavioral characteristics of A. guel- hatched larvae at 0 days post-hatch (DPH) were 10.2 ± denstaedtii prelarvae examined in the present study are 0.2 mm and 14.5 ± 0.7 mg, respectively. During the pre- summarized in Fig. 1. Upon hatching (day 0), only a small larval period up to 10 DPH, the average total lengths portion of the prelarvae exhibited negative geotactic be- and weights increased to 20.5 ± 0.4 mm and 40.5 ± 2.5 havior and passive drift under L conditions (less than 5% mg, respectively (Additional file 1:FigureS1).The on average), whereas the majority of the remaining indi- Russiansturgeonprelarvae hadanexternalmorphology viduals exhibited sedentary behavior (Fig. 2a). The move- that is typical of Acipenser species, characterized by a ment distance increased on days 1 and 2. However, the pair of pronounced pronephric wings, an oval-shaped prelarvae preferred to remain near the bottom without yolk, and a yolk plug. We observed the beginning of any clear signs of pelagic swimming into the upper yolk invagination and initial development of the exter- water column. Under DL conditions, the newly hatched nal gills on day 2. On day 4, well-structured eyes were prelarvae exhibited no significant behavioral alterations observable and melanin pigmentation was pronounced, compared to those under L conditions (Fig. 2b). When particularly in the craniofacial, posterior body trunk, and the prelarvae were exposed to further reduced light in- caudal regions. The yolk plug had condensed into a spiral tensity (i.e., D conditions), negative geotaxis almost Fig. 1 Schematic summary of the behavioral modifications of Acipenser gueldenstaedtii during the prelarval period from day 0 to day 9 under an experimentally set diel light cycle (16 h of 450-lx daylight, 4 h of 10-lx dim light, and 4 h of < 1-lx darkness). Within a given behavioral criterion, ontogenetic intervals representing more pronounced and distinctive patterns are marked with darker colors. Two different onset patterns of rheotactic and non-rheotactic schooling are noted in pattern I and pattern II (for representative images, refer to Fig. 4). Pelagic swimming in the upper water column was not noted. Total length, body weight, and morphological development of the prelarvae during this period are referred to in Additional file 1: Figure S1 Kim et al. Fisheries and Aquatic Sciences (2019) 22:4 Page 5 of 10 A) B) C) Fig. 2 Behavioral patterns of newly hatched (day 0) Acipenser gueldenstaedtii prelarvae under light (L; 450 lx on average; a), dim light (DL; 10 lx; b), and dark (D; < 1 lx; c) conditions. Behavioral patterns are categorized into negative geotaxis with passive drift (I), non-locomotory stay on the bottom (II), moving across the bottom of the tank (III), moving along the walls of the tank (IV), and gathering at the corners of the tank (V). Means ± SDs are based on three replicate tanks. Significant differences were found only under D conditions based on analysis of variance (ANOVA) followed by Duncan’s multiple range tests (P < 0.05; indicated by asterisks). Representative images showing sedentary behavior and the onset of early corner-gathering behavior of the hatched prelarvae are provided in Additional file 2:Figure S2 disappeared and the prelarvae moved across the bottom rheotactic schools moved to the region around the water and walls of the tank (Fig. 2c). Bottom-swimming be- inlet and formed a rheotactic school. The co-existence havior was more rapid under D conditions than under of both rheotactic and non-rheotactic schools continued L/DL conditions. until the commencement of post-schooling behavior. We noticed that small numbers of prelarvae began to The pattern of school formation was different from that gather at the tank corners from day 0 under L condi- described above in the other two replicate tanks (tank tions (Additional file 2: Figure S2), and the number of II and tank III). Although the prelarvae in these tanks corner-gathering prelarvae gradually increased with age. also exhibited early corner-gathering behavior—which Early corner-gathering behavior was not significantly began on day 0 and increased until day 3—most of the modified under DL conditions compared to L condi- prelarvae at the corners moved to the regions around tions. However, such behavior was much reduced under the water inlets on day 4 and formed large rheotactic D conditions (Fig. 3; Additional file 3:FigureS3). schools. Soon after, rheotactic schooling reached a peak, and the majority of individuals belonged to these Rheotactic and non-rheotactic schooling schools. On day 5, non-rheotactic schools formed at Under L conditions, onset patterns of rheotactic school- the corners. However, there were fewer individuals in ing (at the water inlet in the tank with a water current of the non-rheotactic schools than in the rheotactic schools 8 L/min) and post-rheotaxis schooling (at the corners of (Fig. 4). the tank without significant water current) differed de- Under DL conditions, schooling patterns were not dis- pending on the replicate tanks. In one of the three repli- similar from those under L conditions. Considerable cate tanks (tank I), the number of early corner-gathering numbers of rheotactic prelarvae remained in schools prelarvae (first seen on day 0) continuously and progres- under D conditions, although the participating num- sively increased with age and the prelarvae formed large bers were reduced relative to those observed during the non-rheotactic schools directly at the corners on day 3. DL or L intervals. However, unlike the rheotactic schools, The schools at the corners became more robust by day the non-rheotactic schools were unstable during the D 4, and the size of the non-rheotactic schools—compris- phase. In all the three replicate tanks, the non-rheotac- ing almost all the prelarvae in the tank—peaked on day tic schools were either significantly reduced in size or 5 (Fig. 4). In that tank, we did not observe significant almost completely dispersed under D conditions. The rheotactic schooling behavior until the late phase of day prelarvae besides those in the non-rheotactic schools 5. On day 6, considerable numbers (approximately one exhibited benthic behavior across the bottom of the third) of the prelarvae that had participated in non- tank (Fig. 5). Kim et al. Fisheries and Aquatic Sciences (2019) 22:4 Page 6 of 10 Fig. 3 Proportion of Acipenser gueldenstaedtii prelarvae exhibiting corner-gathering behavior under light (L), dim light (DL), and dark (D) conditions between day 1 and day 3. For each experimental tank (tank I, II, or III), prelarval numbers were averaged based on at least three counts by two observers (see the “Methods” section). There was a significant reduction of the proportion under D conditions (indicated by asterisks; P < 0.05), whereas there was no significant difference between the L and DL conditions (P > 0.05) based on analysis of variance (ANOVA) followed by Duncan’s multiple range tests. A statistical evaluation according to prelarval age (day 1 to day 3) within a given light intensity (L, DL, and D) in each tank is provided in Additional file 3:Figure S3 Post-schooling behavior those previously described (Dettlaff et al. 1993;Chebanov The compact schooling behavior of both rheotactic and and Galich 2011), although the speed of development did non-rheotactic schools began to diminish, with some not exactly match previous descriptions. This was prelarvae exhibiting post-schooling behavior (from the probably due to the difference in incubation temperature early phase of day 7). The number of prelarvae exhibit- (20 °C in the present study versus 16–18 °C in previous ing post-schooling behavior increased continuously studies). Compared to other related sturgeon species, during the DL and D phases (days 7 to 8) (Fig. 6). The Russian sturgeon belong to the sturgeon group showing majority of prelarvae exhibited post-schooling behavior the darkest pigmentation during the prelarval period. In (i.e., non-locomotory, scattering over the tank bottom) the context of hatcheries, the body coloration pattern on day 8 (Additional file 4:FigureS4). The larvae began could be considered a criterion for the evaluation of the to resume their locomotory activity and moved slowly developmental or physiological state of prelarvae, as across the tank bottom after their first feed (day 9). evidenced by previous findings that certain waterborne pollutant (e.g., phenol) markedly inhibit prelarval pigmen- Discussion tation (Dettlaff et al. 1993). The scores for fertilization, hatching, abnormality, via- The findings from the present study indicate that newly bility, and prelarval growth determined in the present hatched Russian sturgeon prelarvae do not exhibit positive study were comparable to those reported by other re- phototaxis, based on their preference for the bottom of searchers studying the artificial propagation of A. guel- the tank under L conditions. No significant negative geo- denstaedtii (Chebanov and Galich 2011; Nathanailides taxis was reported in the hatchling of other sturgeon spe- et al. 2002;Memiş et al. 2009). The development patterns cies (e.g., Acipenser transmontanus and A. brevirostrum) observed in the present study also broadly corroborated exhibiting negative phototactic characteristics (Loew and Kim et al. Fisheries and Aquatic Sciences (2019) 22:4 Page 7 of 10 Fig. 4 Representative photographs showing the progressive increase in the corner-gathering behavior of Acipenser gueldenstaedtii prelarvae with age, followed by aggregation into schools. Two different patterns were observable under the present examination conditions. In pattern I (upper), early corner-gathering prelarvae (day 0–day 2) formed directly non-rheotactic schools at the corners (day 3–day 5). Two large schools on day 5 are indicated by arrows. In contrast, in pattern II (lower), the corner-gathering behavior of the prelarvae (day 0–day 3) shifted to rheotactic prelarval aggregation into a rheotactic school (day 4). A non-rheotactic school developed at a corner on day 5, as indicated by an arrow. Temporal patterns for the two patterns in the diel photoperiodicity of the present study are referred to in Fig. 1 Sillman 1998; Richmond and Kynard 1995). Negative geo- 1993; Gisbert and Solovyev 2018). The prelarvae of tactic behavior has been considered as a characteristic several sturgeon species that exhibit positive phototaxis strategy of the prelarvae of many sturgeon species for (particularly exemplified by the Siberian sturgeon Acipenser early dispersal and predator avoidance. However, this baerii) are reported to actively swim toward the water movement is also related to phototaxis (Dettlaff et al. surface, driven by their intrinsic tendency to approach Fig. 5 Proportion of Acipenser gueldenstaedtii prelarvae engaged in non-rheotactic schools (NRS) and/or rheotactic schools (RS) under light (L), dim light (DL), and dark (D) conditions between day 3 and day 5. Quantitative assessment was carried out with only two tanks (tank 1 and tank 2). Under D conditions, prelarval counts without typical signs of schooling behavior are indicated by dots (day 3/day 4 in tank I and day 3 in tank II). There was no significant difference in the proportions of the prelarvae exhibiting schooling behavior between L and DL conditions in both tanks, irrespective of prelarval age (P > 0.05). Schooling behavior was significantly weakened under D conditions (indicated by asterisks; P < 0.05). However, though they exhibited weakened schooling behavior, a considerable number of prelarvae participated in rheotactic schools under D conditions, whereas non-rheotactic schools almost disappeared. Each mean ± SD is based on at least triplicate counting by two observers, and statistical evaluation was carried out by analysis of variance (ANOVA) followed by Duncan’s multiple range tests Kim et al. Fisheries and Aquatic Sciences (2019) 22:4 Page 8 of 10 Fig. 6 Representative images showing the progressive development of the post-schooling behavior of Acipenser gueldenstaedtii prelarvae from day 6 to day 8, followed by entry into the larval stage on day 9 the light during daylight hours (Gisbert et al. 1999a), unpublished observation), which is highly suggestive which was not clearly seen in the prelarvae of the Russian of negative phototaxis. However, our findings contradict sturgeon. Under DL conditions, the behavior of the previous results in which the 0–5-day-old prelarvae Russian sturgeon at this earliest stage of development was of Russian sturgeon (a Volga River population of A. similar to that under L conditions. Although the behav- gueldenstaedtii) significantly preferred bright illumination ior of the Russian sturgeon prelarvae under D condi- (Kynard et al. 2002). Although such inconsistent results tions differed quantitatively from that under brighter require further investigation, Russiansturgeonprelarvae illumination, a fundamental transition or change in be- have been reported to exhibit a population-dependent havior was not obvious. This differed from the findings variation in phototaxis: positive phototaxis in the Volga reported for other positively phototactic sturgeon River population and negative phototaxis in the Azov species that exhibit a dramatic change in swimming Sea population (Chebanov and Galich 2011;Podushka behavior during the transition from day to night. For 2003). Dettlaff et al. (Dettlaff et al. 1993)reported example, Siberian sturgeon (A. baerii) prelarvae do not that prelarvae of a subspecies of Russian sturgeon swim upwards during darkness, and pelagic swimming (A. gueldenstaedtii colchicus) may not exhibit any photo- at the water surface during the day quickly shifts to taxis during the prelarval stage. benthic movement at night, although the exact light in- Under DL conditions, the Russian sturgeon prelarvae tensity at which this shift occurs has not been reported readily maintained rheotactic and non-rheotactic school- (Gisbert and Ruban 2003; Gisbert et al. 1999a). ing similar to that observed under L conditions (days 4– Onset appearance and development of rheotactic and 6). This suggests that Russian sturgeon prelarvae may be non-rheotactic schooling in the Russian sturgeon prelar- able to sense weak light. Accordingly, the reduction of vae were not uniform among the replicate tanks under L light intensity during DL conditions (10 lx) in the conditions. Increased numbers of prelarvae gathered at present study may have been insufficient to trigger or the tank corners during the early prelarval period (days elicit any significant modifications in schooling behav- 0–3) and were capable of forming large non-rheotactic ior. This finding is different from previous observations schools directly at the corners or alternatively became made with photopositive sturgeon species (A. baerii), rheotactic during day 4. Unfortunately, we were unable in which active schooling behavior under L conditions to identify any potential causative biotic factors (e.g., disappeared when the environmental light intensity was survival and fish size) or abiotic factors (e.g., tank condi- markedly reduced (Chebanov and Galich 2011;Gisbert tions) that were responsible for this non-uniformity. It is et al. 1999a; Rodriguez and Gisbert 2002). therefore clear that further extensive tests are needed to Under the present D conditions (< 1 lx), the Russian determine whether such different schooling patterns are sturgeon prelarvae exhibited a difference in their ability reproducible under various prelarval rearing conditions to maintain rheotactic and post-rheotaxis schooling be- (e.g., density, illumination, tank shape). Nevertheless, havior. Though weakened, the rheotactic schools per- our findings indicate that early corner-gathering school- sisted under dark conditions, whereas the non-rheotactic ing is itself closely related to negative phototactic behav- schools almost disappeared. This observation suggests ior under L conditions. We also found that such corner- that Russian sturgeon prelarvae at these stages may use vi- gathering prelarvae moved actively to avoid an artificial sion as the principal means of determining non-rheotactic spotlight (a 3 W white LED flashlight) (tested on day 1; schooling behavior, whereas their rheotactic behavior may Kim et al. Fisheries and Aquatic Sciences (2019) 22:4 Page 9 of 10 be governed more by an innately established ontogenetic Abbreviations DPH: Days post-hatching; HPF: Hours post-fertilization; HPH: Hours post-hatching; timetable that is less influenced by environmental light LHRH-a: Luteinizing hormone-releasing hormone analogue intensity. In the present study, the post-schooling behavior of the Acknowledgments The authors wish to thank the technical staff at the Experimental Fish Research Russian sturgeon prelarvae did not differ significantly ac- Center, Pukyong National University, who provided the raw observational data. cording to the lighting conditions (L, DL, or D). The post- schooling behavior of the sturgeon prelarvae commenced Funding This study was supported by the grant from KIMST, Ministry of Oceans and with a decrease in prelarval activity in the rheotactic and/ Fisheries of Korea (Grant #20170327). or non-rheotactic schools, typically in the prelarvae at the outer boundary of the schools. As post-schooling behavior Availability of data and materials progressed (days 7–9), compact schools were no longer Not applicable. maintained. The prelarvae were only loosely aggregated Authors’ contributions and eventually became dispersed, non-locomotory, and EJK analyzed the behavior of the sturgeon and prepared the images. CHP scattered over the bottom of the tank (Gisbert et al. bred the sturgeon and co-evaluated the data. NYK designed the study, evaluated the data, and drafted the manuscript. All authors read and approved 1999a). This behavior signals the termination of the pre- the final manuscript. larval phase; the prelarvae are ready to evacuate the yolk plug and finalize the functional development of various di- Ethics approval and consent to participate We followed the experimental protocols described in the guidelines provided gestive organs to ingest exogenous foods (Babaei et al. by the Animal Care and Use Committee of Pukyong National University. 2011; Gisbert et al. 1999b). Therefore, this characteristic behavior reflects the ability of the prelarvae to divert Consent for publication energy to the final preparation for the transition from an Not applicable. endogenous to an exogenous nutrition system (Chebanov Competing interests and Galich 2011;GisbertandWilliot 1997). The authors declare that they have no competing interests. In summary, the results from the present study indi- cate that A. gueldenstaedtii prelarvae essentially exhibit Publisher’sNote negative phototaxis under L conditions during their Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. earliest life stages, and this behavior is not significantly modified under DL or D conditions. During rheotactic Author details and non-rheotactic schooling behaviors, rheotaxis was Department of Marine Bio-Materials and Aquaculture, Pukyong National University, Busan 48513, Republic of Korea. Dinoville Sturgeon Aquafarm, less influenced by environmental light intensity than Hamyang, Kyoung-nam 50027, Republic of Korea. non-rheotactic schooling behavior. Post-schooling be- havior was not significantly affected by light intensity Received: 6 August 2018 Accepted: 10 January 2019 (< 1–450 lx) during a diel light cycle. The results of the present study could be used to scrutinize the light- References dependent physiology of Russian sturgeon prelarvae Babaei SS, Kenari AA, Nazari R, Gisbert E. Developmental changes of digestive enzymes and to develop a practical visual guide for assessing the in Persian sturgeon (Acipenser persicus) during larval ontogeny. Aquaculture. 2011; 318:138–44. https://doi.org/10.1016/j.aquaculture.2011.04.032. health and quality of hatchery-propagated prelarvae Chebanov MS, Galich EV. Sturgeon hatchery manual. FAO Fisheries and Aquaculture under various illumination intensities and/or diel cycle Technical Paper. No. 558. Ankara, FAO; 2011. conditions. The present findings should be used to Dettlaff TA, Ginsburg AS, Schmalhausen OI. Sturgeon fishes: developmental biology and aquaculture. New York: Springer-Verlag; 1993. develop an optimal illumination regime for Russian Doukakis P, Pikitch EK, Rothschild A, DeSalle R, Amato G, Kolokotronis S. Testing sturgeon prelarvae under hatchery conditions. the effectiveness of an international conservation agreement: marketplace forensics and CITES caviar trade regulation. PLoS One. 2012;7:e40907. https:// doi.org/10.1371/journal.pone.0040907. Additional files Gisbert E, Nam YK. Early ontogeny in the Siberian sturgeon. In: Williot P, Nonnotte G, Vizziano-Cantonnet D, Chebanov M, editors. The Siberian sturgeon (Acipenser baerii, Brandt, 1869) Vol. 1 - biology. Cham: Springer Additional file 1: Figure S1. Information on prelarval development of International Publishing; 2018. p. 131–57. Russian sturgeon (Acipenser gueldenstaedtii) used in the present study. Gisbert E, Ruban GI. Ontogenetic behavior of Siberian sturgeon, Acipenser (PDF 381 kb) baerii: a synthesis between laboratory tests and field data. Environ Biol Additional file 2: Figure S2. Representative photographs showing the Fish. 2003;67(3):311–9. https://doi.org/10.1023/A:1025851502232. early behavior of Acipenser gueldenstaedtii hatchlings under L conditions. Gisbert E, Sarasquete MC, Williot P, Castelló-Orvay F. Histochemistry of the (PDF 50 kb) development of the digestive system of Siberian sturgeon during early ontogeny. J Fish Biol. 1999b;55:596–616. https://doi.org/10.1111/j.1095- Additional file 3: Figure S3. Patterns of early corner-gathering behavior 8649.1999.tb00702.x. under light (L), dim light (DL), and dark (D) conditions during the prelarval Gisbert E, Solovyev M. Behaviour of early life stages in the Siberian sturgeon. In: period from day 1 to day 3. (PDF 65 kb) Williot P, Nonnotte G, Vizziano-Cantonnet D, Chebanov M, editors. The Additional file 4: Figure S4. Proportion of prelarvae exhibiting typical Siberian sturgeon (Acipenser baerii, Brandt, 1869) Vol. 1 – biology. Cham: post-schooling behavior on day 8. (PDF 38 kb) Springer International Publishing; 2018. p. 159–72. Kim et al. Fisheries and Aquatic Sciences (2019) 22:4 Page 10 of 10 Gisbert E, Williot P. Larval behavior and effect of the timing of initial feeding on growth and survival of Siberian sturgeon (Acipenser baerii) larvae under small scale hatchery production. Aquaculture 1997;15:663–676. https://doi.org/10. 1016/S0044-8486(97)00086-0 Gisbert E, Williot P, Castelló-Orvay F. Behavioural modifications in the early life stages of Siberian sturgeon (Acipenser baerii, Brandt). J Appl Ichthyol. 1999a; 15(4–5):237–42. https://doi.org/10.1111/j.1439-0426.1999.tb00242.x. Johnson TA, Iyengar A. Phylogenetic evidence for a case of misleading rather than mislabeling in caviar in the United Kingdom. J Forensic Sci. 2015;60: S248–53. https://doi.org/10.1111/1556-4029.12583. Kim EJ, Park CH, Nam YK. Effects of incubation temperature on the embryonic viability and hatching time in Russian sturgeon (Acipenser gueldenstaedtii). Fish Aquat Sci. 2018; in press. Kynard B, Zhuang P, Zhang L, Zhang T, Zhang Z. Ontogenetic behavior and migration of Volga River Russian sturgeon, Acipenser gueldenstaedtii, with a note on adaptive significance of body color. Environ Biol Fish. 2002;65(4): 411–21. https://doi.org/10.1023/A:1021121900207. LeBreton GT, Beamish FWH, McKinley SR. Sturgeons and paddlefish of North America. Dordrecht: Kluwer Academic Publishers; 2006. Loew ER, Sillman AJ. An action spectrum for the light-dependent inhibition of swimming behavior in newly hatched white sturgeon, Acipenser transmontanus. Vis Res. 1998;38(1):111–4. https://doi.org/10.1016/S0042-6989(97)00163-6. Memiş D, Ercan E, Celikkale MS, Timur M, Zarkua Z. Growth and survival rate of Russian sturgeon (Acipenser gueldenstaedtii) larvae from fertilized eggs to artificial feeding. Turk J Fish Aquat Sci. 2009;9:47–52. Nathanailides C, Tsoumani M, Papazogloy A, Paschos I. Hatching time and post- hatch growth in Russian sturgeon Acipenser gueldenstaedtii. J Appl Ichthyol. 2002;18:651–4. https://doi.org/10.1046/j.1439-0426.2002.00399.x. Park CH. Artificial seedling propagation and caviar production in farmed Siberian sturgeon (Acipenser baerii) and Russian sturgeon (A. gueldenstaedtii). PhD. Thesis. Busan: Pukyong National University; 2018. Podushka SB. On the systematics of Russian sturgeon from the Azov Sea. Nauchno-Tehnicheskii Byulleten Laboratorii Ikhtiologii INENKO. 2003;7:19–44. Richmond AM, Kynard B. Ontogenetic behavior of shortnose sturgeon Acipenser brevirostrum. Copeia. 1995;1995(1):172–82. https://doi.org/10.2307/1446812. Rodriguez A, Gisbert E. Eye development and the role of vision during Siberian sturgeon early ontogeny. J Appl Ichthyol. 2002;18(4–6):280–5. https://doi.org/ 10.1046/j.1439-0426.2002.00406.x. Williot P, Rouault T, Pelard M, Mercier D, Jacobs L. Artificial reproduction and larval rearing of captive endangered Atlantic sturgeon Acipenser sturio. Endanger Species Res. 2009;6:251–7. https://doi.org/10.3354/esr00174. Zaheh HE, Rafiee G, Eagderi S, Kazemi R, Poorbagher H. Effects of different photoperiods on the survival and growth of beluga sturgeon (Huso huso) larvae. Intl J Aquat Biol. 2013;1(1):36–41. Zhuang P, Kynard B, Zhang L, Zhang T, Cao W. Ontogenetic behavior and migration of Chinese sturgeon. Environ Biol Fish. 2002;65(1):83–97. https:// doi.org/10.1023/A:1019621501672. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Fisheries and Aquatic Sciences Springer Journals

Ontogenetic behavior of farm-bred Russian sturgeon (Acipenser gueldenstaedtii) prelarvae in a diel photoperiodic cycle: behavioral modifications in response to light intensity

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Life Sciences; Fish & Wildlife Biology & Management; Marine & Freshwater Sciences; Zoology; Animal Ecology
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Abstract

Russian sturgeon (Acipenser gueldenstaedtii) is commercially important in Korea because its caviar is highly prized. Although the early ontogeny of the species has been described, behavioral modifications in response to various light intensities or diel photoperiodicity patterns have not been studied extensively. The objective of the present study was to examine the behavioral characteristics of hatchery-produced A. gueldenstaedtii prelarvae over a diel photoperiodic cycle. During a diel light cycle comprising 16 h of daylight (450 lx), 4 h of dim light (10 lx), and 4 h of darkness (< 1 lx), newly hatched A. gueldenstaedtii prelarvae exhibited negative phototaxis in daylight (day 0–day 2), and this early behavior was not significantly affected by changes of light intensities. Rheotactic and non-rheotactic aggregation into schools was typical between days 3 and 6. Under the diel light cycle conditions described, rheotaxis was not influenced by environmental light intensity as much as non-rheotactic schooling behavior. Post-schooling behavior, which progressed from day 7 to day 8, did not change significantly during the diel light cycle. The data from the present study could be of practical value in developing a visual guide for assessing the fitness and quality of Russian sturgeon prelarvae under diel light cycle conditions in hatcheries. Keywords: Russian sturgeon Acipenser gueldenstaedtii, Phototaxis, Ontogeny, Behavioral modifications Background Light-dependent behavior in sturgeon prelarvae is Sturgeon, which are extant primitive fish of the order established as early as the mass hatching stage (Dettlaff Acipenseriformes, are highly valued as a source of caviar et al. 1993), but this innate trait differs considerably among (LeBreton et al. 2006). However, because almost all wild Acipenser species. During early life, sturgeons exhibit posi- sturgeon populations are threatened or endangered, the tive, negative, or no phototactic characteristics depending artificial propagation of sturgeon has become important on species-specific adaptation to the natural habitat for the sustainable production of caviar and for restock- (Chebanov and Galich 2011; Zhuang et al. 2002;Gisbert ing natural populations (Doukakis et al. 2012; Johnson and Ruban 2003; Williot et al. 2009). and Iyengar 2015). Light is a critical factor that influ- In the context of aquaculture, species-specific light- ences the behavior and other physiological characteris- dependent behaviors are important for enabling hatchery tics of sturgeons, especially during their prelarval and managers to define visual criteria for the ontogenetic larval stages (Dettlaff et al. 1993; Loew and Sillman development of prelarvae and to explicitly evaluate the 1998;Chebanov and Galich 2011; Zaheh et al. 2013). fitness and physiological state of the prelarvae. It is therefore helpful to develop optimal illumination re- * Correspondence: yoonknam@pknu.ac.kr gimes for prelarval nurseries of target sturgeon species Department of Marine Bio-Materials and Aquaculture, Pukyong National (Gisbert and Solovyev 2018). Most sturgeon species are University, Busan 48513, Republic of Korea characterized by a lengthy period of prelarval development Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Kim et al. Fisheries and Aquatic Sciences (2019) 22:4 Page 2 of 10 (usually more than 1 week) and undergo dynamic changes the incidence of abnormality in 240 embryos and 360 to their ontogenetic behavior during that period (Gisbert hatchlings, respectively. et al. 1999a; Gisbert and Nam 2018). Usually, hatcheries apply a photoperiod regime during the prelarval rearing Prelarval rearing and sampling period. Therefore, the behavioral characteristics of the We transferred newly hatched prelarvae (n = 4500) col- sturgeon are potentially influenced by the diel photo- lected within 4-h intervals to one of three replicate tanks periodicity of the hatchery. (width × depth × height = 1.2 m × 2 m × 0.25 m), each con- The Russian sturgeon (Acipenser gueldenstaedtii)is taining approximately 300 L of 1-μm filtered groundwater. one of the most commercially important Acipenser Each replicate tank was equipped with a custom-designed species—mainly because its caviar (“Ossetra caviar”)is filter unit (200 L volume) and water was re-circulated highly prized—and is now an important candidate species through the filter unit at a flow rate of 8 L/min using a in Korean aquaculture (Kim et al. 2018;Park 2018). The submersible circulation pump. Throughout the experi- ontogeny and general behavioral patterns of artificially ment, we maintained the water temperature at 20 ± 0.5 °C produced Russian sturgeon have been described by several using automatic thermostat-assisted heaters and the dis- research groups (Dettlaff et al. 1993; Chebanov and Galich solved oxygen content at 8.0 ± 0.5 ppm using air diffusers 2011;Kynard etal. 2002). However, previous studies on connected to an electric air pump. The pH of the in-tank farm-bred Russian sturgeon have mainly described the water ranged from 7.2 to 7.4 during the experiment. We behavioral patterns observed during daylight hours only immediately removed and counted dead or apparently (Chebanov and Galich 2011;Kynard et al. 2002). In con- malformed individuals. Every day, we sampled 12 prelar- trast to the relative abundance of information on daylight vae from each tank replicate (i.e., 36 fish) to determine behavior, behavioral modification patterns in response to growth and morphological differentiation. We measured various light intensities, or during a diel photoperiodic the total length and body weight of each prelarvae to the cycle, have not been extensively explored. Such a paucity nearest 0.1 mm and 0.1 mg, respectively. We recorded limits the visual criteria-based evaluation of prelarval the morphological development of the prelarvae with ontogeny to daylight hours, and may also hinder a full an AZ100 microscope (Nikon, Tokyo, Japan) and NIS- comprehension of the diel patterns of the activities and Elements basic research image analysis software. We behaviors in hatcheries. Therefore, the objective of the provided the first exogenous feed (100 μm-sized powder present study was to examine the behavioral character- for flounder larvae; Woosung Corp., Republic of Korea) istics of hatchery-produced Russian sturgeon prelarvae on day 9. during a diel photoperiodic cycle consisting of three different light intensity conditions (i.e., daylight, dim Setting the experimental diel light cycle light, and darkness). We reared the prelarvae in an experimental room (located on the first basement floor), which was covered in blinders to exclude external light. To assess the onto- Methods genetic behavior of the sturgeon prelarvae in a diel light Hormone-induced spawning and artificial fertilization cycle, we set a photoperiod cycle in the following order We obtained the Russian sturgeon (Acipenser guelden- of precedence: light (L) for 16 h, dim light (DL) for 4 h, staedtii) used in the present study from Dinoville and darkness (D) for 4 h. The illumination conditions Sturgeon Aquafarm, Hamyang, Kyoung-nam, Republic for each interval were as follows: (1) L, the light inten- of Korea. We injected luteinizing hormone-releasing sities across the experimental tanks averaged 450 lx sup- hormone analog (LHRH-a; Sigma-Aldrich, St. Louis, plied by white light-emitting diode (LED) lamps (23 W) MO, USA) into the muscles of mature female (n =2) enclosed in translucent plastic covers and installed on and male (n = 3) broodfish at dose levels of 80 μg/kg for the ceiling approximately 3 m above the tanks; (2) DL, females and 20 μg/kg for males to obtain eggs and milt all the white LED lamps were turned off, and translucent (Kim et al. 2018;Park 2018). We used the wet method glass-covered incandescent lightbulbs (7 W; 6500 K) pro- for artificial fertilization and treated the fertilized eggs vided 10 lx across the experimental tanks; (3) D, an in- with anti-adhesive agent (Fuller’s earth; Sigma-Aldrich), frared (IR) LED spotlight (10 W; 730 nm) was set to as described by Kim et al. (Kim et al. 2018). shine toward the wall, which was more than 8 m away We maintained the water temperature of the hatching from the experimental tanks, and the light intensity was incubator at 20 ± 0.5 °C until hatching commenced using less than 1 lx. We monitored transitions in diel behav- thermostat-assisted submergible aquarium heaters (300 ioral patterns—including negative geotaxis (also called W). We estimated the fertilization rate in three random swimming-up), rheotaxis, schooling, and post-schooling samples each consisting of 120 embryos at 2 h post- behavior—under the diel light cycle from day 0 to day 9. fertilization (HPF). We estimated hatching success and We examined ontogenetic diel behavior patterns at 1 h Kim et al. Fisheries and Aquatic Sciences (2019) 22:4 Page 3 of 10 before the end of the L-phase, 1 h after the DL-phase, by two observers per replicate tank, and the observers and 1 h after the D-phase. We also made random exami- were randomly assigned to each replicate tank for every nations when we observed typical transitions and/or observation time. Under L and DL conditions, each ob- modifications of behavior. server took at least six snapshots and taped a movie video using a digital camera equipped with an iPhone Behavioral criteria (version later than 7; Apple Inc., USA). Each observa- Based on previous reports on the behavioral ontogeny of tion lasted 15 min. We analyzed the selected photo- Acipenser species (Gisbert and Solovyev 2018; Park 2018), graphs and videos using Photoshop (Adobe Inc., USA). we applied seven main criteria to define and evaluate However, we recorded behavioral patterns under D potential modifications to behavioral characteristics of conditions using an IR light illuminator (850 nm; Fenix, Russian sturgeon during the prelarval period from days USA) and/or an IR night vision camera (Ancter, USA). 0 to 9. The criteria included negative geotaxis and passive We carried out quantitative assessments on day 0 on a drift, pelagic swimming in the upper water column, small number of newly hatched prelarvae (n = 120/tank) benthic swimming, early corner-gathering, rheotactic assigned to three small rectangular tanks (30 cm × 60 schooling, non-rheotactic schooling, and post-schooling cm × 25 cm) with white bottoms. We counted the num- behavior (Table 1). bers of prelarvae at least six times for each replicate tank. During day 1 to day 3, we determined the propor- Observation regimes tion of early corner-gathering prelarvae in the rearing According to our principal objective to provide hatchery tanks. Some early prelarvae gathered at a corner of each managers with a visual guide for ontogenetic modifications tank, and we trapped those prelarvae inside acryl bar- of prelarval behaviors in response to a diel photoperiodi- framed 500-μm mesh screens (50 cm × 50 cm square). city, the present study essentially included observational The observers counted the number of prelarvae inside data based on prelarval rearing conditions that were simi- or outside the square area at least three times and took lar to those conventionally used in Korean sturgeon pictures to determine the percentage of early corner- hatcheries. For this reason, the statistical evaluation of gathering prelarvae out of the total number of fishes behavioral patterns with accurate counting of prelarvae per tank. When the schools formed at the corners and/ belonging to a particular behavioral criterion might not or water-inlet sites (days 3 to 5), we calculated the be relevant in all aspects of analysis. Therefore, we only number of prelarvae participating in schooling in each obtained numerical data addressing behavioral patterns replicate tank using an acryl bar-framed screen identi- and/or responses at several detection time-points. cal to that described above. On day 8, we installed three All observers had experience of at least three other square frames (30 cm × 30 cm) in each replicate tank to sturgeon-breeding experiments from the preceding 5 estimate the proportion of prelarvae exhibiting typical years. Evaluation of prelarval behavior was carried out post-schooling behavior inside the frame. Table 1 Main behavioral criteria of Russian sturgeon Acipenser gueldenstaedtii prelarvae assessed in this study Behavioral criteria Behavioral characteristics in tank Negative geotaxis and drifting behavior Upward movement toward water surface by active propelling of the posterior body trunk and tail, and then passive settlement to the bottom; prelarvae rest on their side or yolk sac before active swimming-up starts again Pelagic swimming Swimming at water surface or upper water column for a long time in a certain direction Benthic swimming Free swimming for a short or long distance along the bottom of the tank, without displaying other behavioral types Early corner-gathering Approaching the corner(s) of the tank; hatchlings and early prelarvae gather and aggregate loosely into a “school-like” appearance at the corner(s) Rheotactic schooling Aggregation of large number of positively rheotactic prelarvae into a school-shaped group on the bottom of the tank; prelarvae swim against water current with active propelling movement Non-rheotactic schooling Dense aggregation of large number of prelarvae into schools, usually at the corner(s) of the tank where no significant water current exists; prelarvae approach the center of the corner with active propelling of posterior body trunk and tail Post-schooling behavior Non-locomotory, inactive, being dispersed or scattered over the bottom of the tank; prelarvae represent a sign of the initiation of the post-schooling behavior as a slow-wagging motion without locomotory activity Behavioral criteria were compiled from previous literatures with Acipenser species (Gisbert and Ruban 2003; Gisbert and Solovyev 2018; Gisbert et al. 1999a; Park 2018 Kim et al. Fisheries and Aquatic Sciences (2019) 22:4 Page 4 of 10 Results vale shape, and swimming structures including various Prelarval viability, growth, and morphological fins had developed by day 4. Almost the entire body development had become darkly pigmented and dorsal scute rudi- We obtained approximately 110,000 fertilized eggs. The ments had begun to appear by day 8 (Additional file 1: fertilization rate averaged 95 ± 2%. The mean hatching Figure S1). successes (%) and incidence of abnormality (%) were 77 ± 9% and 2.1 ± 0.8%, respectively. There was no signifi- cant mortality during the prelarval period up to and in- Movement of newly hatched prelarvae and early cluding day 9. Prelarval survival averaged 98.4%. The swimming behavior average total length and body weight of the newly The light-dependent behavioral characteristics of A. guel- hatched larvae at 0 days post-hatch (DPH) were 10.2 ± denstaedtii prelarvae examined in the present study are 0.2 mm and 14.5 ± 0.7 mg, respectively. During the pre- summarized in Fig. 1. Upon hatching (day 0), only a small larval period up to 10 DPH, the average total lengths portion of the prelarvae exhibited negative geotactic be- and weights increased to 20.5 ± 0.4 mm and 40.5 ± 2.5 havior and passive drift under L conditions (less than 5% mg, respectively (Additional file 1:FigureS1).The on average), whereas the majority of the remaining indi- Russiansturgeonprelarvae hadanexternalmorphology viduals exhibited sedentary behavior (Fig. 2a). The move- that is typical of Acipenser species, characterized by a ment distance increased on days 1 and 2. However, the pair of pronounced pronephric wings, an oval-shaped prelarvae preferred to remain near the bottom without yolk, and a yolk plug. We observed the beginning of any clear signs of pelagic swimming into the upper yolk invagination and initial development of the exter- water column. Under DL conditions, the newly hatched nal gills on day 2. On day 4, well-structured eyes were prelarvae exhibited no significant behavioral alterations observable and melanin pigmentation was pronounced, compared to those under L conditions (Fig. 2b). When particularly in the craniofacial, posterior body trunk, and the prelarvae were exposed to further reduced light in- caudal regions. The yolk plug had condensed into a spiral tensity (i.e., D conditions), negative geotaxis almost Fig. 1 Schematic summary of the behavioral modifications of Acipenser gueldenstaedtii during the prelarval period from day 0 to day 9 under an experimentally set diel light cycle (16 h of 450-lx daylight, 4 h of 10-lx dim light, and 4 h of < 1-lx darkness). Within a given behavioral criterion, ontogenetic intervals representing more pronounced and distinctive patterns are marked with darker colors. Two different onset patterns of rheotactic and non-rheotactic schooling are noted in pattern I and pattern II (for representative images, refer to Fig. 4). Pelagic swimming in the upper water column was not noted. Total length, body weight, and morphological development of the prelarvae during this period are referred to in Additional file 1: Figure S1 Kim et al. Fisheries and Aquatic Sciences (2019) 22:4 Page 5 of 10 A) B) C) Fig. 2 Behavioral patterns of newly hatched (day 0) Acipenser gueldenstaedtii prelarvae under light (L; 450 lx on average; a), dim light (DL; 10 lx; b), and dark (D; < 1 lx; c) conditions. Behavioral patterns are categorized into negative geotaxis with passive drift (I), non-locomotory stay on the bottom (II), moving across the bottom of the tank (III), moving along the walls of the tank (IV), and gathering at the corners of the tank (V). Means ± SDs are based on three replicate tanks. Significant differences were found only under D conditions based on analysis of variance (ANOVA) followed by Duncan’s multiple range tests (P < 0.05; indicated by asterisks). Representative images showing sedentary behavior and the onset of early corner-gathering behavior of the hatched prelarvae are provided in Additional file 2:Figure S2 disappeared and the prelarvae moved across the bottom rheotactic schools moved to the region around the water and walls of the tank (Fig. 2c). Bottom-swimming be- inlet and formed a rheotactic school. The co-existence havior was more rapid under D conditions than under of both rheotactic and non-rheotactic schools continued L/DL conditions. until the commencement of post-schooling behavior. We noticed that small numbers of prelarvae began to The pattern of school formation was different from that gather at the tank corners from day 0 under L condi- described above in the other two replicate tanks (tank tions (Additional file 2: Figure S2), and the number of II and tank III). Although the prelarvae in these tanks corner-gathering prelarvae gradually increased with age. also exhibited early corner-gathering behavior—which Early corner-gathering behavior was not significantly began on day 0 and increased until day 3—most of the modified under DL conditions compared to L condi- prelarvae at the corners moved to the regions around tions. However, such behavior was much reduced under the water inlets on day 4 and formed large rheotactic D conditions (Fig. 3; Additional file 3:FigureS3). schools. Soon after, rheotactic schooling reached a peak, and the majority of individuals belonged to these Rheotactic and non-rheotactic schooling schools. On day 5, non-rheotactic schools formed at Under L conditions, onset patterns of rheotactic school- the corners. However, there were fewer individuals in ing (at the water inlet in the tank with a water current of the non-rheotactic schools than in the rheotactic schools 8 L/min) and post-rheotaxis schooling (at the corners of (Fig. 4). the tank without significant water current) differed de- Under DL conditions, schooling patterns were not dis- pending on the replicate tanks. In one of the three repli- similar from those under L conditions. Considerable cate tanks (tank I), the number of early corner-gathering numbers of rheotactic prelarvae remained in schools prelarvae (first seen on day 0) continuously and progres- under D conditions, although the participating num- sively increased with age and the prelarvae formed large bers were reduced relative to those observed during the non-rheotactic schools directly at the corners on day 3. DL or L intervals. However, unlike the rheotactic schools, The schools at the corners became more robust by day the non-rheotactic schools were unstable during the D 4, and the size of the non-rheotactic schools—compris- phase. In all the three replicate tanks, the non-rheotac- ing almost all the prelarvae in the tank—peaked on day tic schools were either significantly reduced in size or 5 (Fig. 4). In that tank, we did not observe significant almost completely dispersed under D conditions. The rheotactic schooling behavior until the late phase of day prelarvae besides those in the non-rheotactic schools 5. On day 6, considerable numbers (approximately one exhibited benthic behavior across the bottom of the third) of the prelarvae that had participated in non- tank (Fig. 5). Kim et al. Fisheries and Aquatic Sciences (2019) 22:4 Page 6 of 10 Fig. 3 Proportion of Acipenser gueldenstaedtii prelarvae exhibiting corner-gathering behavior under light (L), dim light (DL), and dark (D) conditions between day 1 and day 3. For each experimental tank (tank I, II, or III), prelarval numbers were averaged based on at least three counts by two observers (see the “Methods” section). There was a significant reduction of the proportion under D conditions (indicated by asterisks; P < 0.05), whereas there was no significant difference between the L and DL conditions (P > 0.05) based on analysis of variance (ANOVA) followed by Duncan’s multiple range tests. A statistical evaluation according to prelarval age (day 1 to day 3) within a given light intensity (L, DL, and D) in each tank is provided in Additional file 3:Figure S3 Post-schooling behavior those previously described (Dettlaff et al. 1993;Chebanov The compact schooling behavior of both rheotactic and and Galich 2011), although the speed of development did non-rheotactic schools began to diminish, with some not exactly match previous descriptions. This was prelarvae exhibiting post-schooling behavior (from the probably due to the difference in incubation temperature early phase of day 7). The number of prelarvae exhibit- (20 °C in the present study versus 16–18 °C in previous ing post-schooling behavior increased continuously studies). Compared to other related sturgeon species, during the DL and D phases (days 7 to 8) (Fig. 6). The Russian sturgeon belong to the sturgeon group showing majority of prelarvae exhibited post-schooling behavior the darkest pigmentation during the prelarval period. In (i.e., non-locomotory, scattering over the tank bottom) the context of hatcheries, the body coloration pattern on day 8 (Additional file 4:FigureS4). The larvae began could be considered a criterion for the evaluation of the to resume their locomotory activity and moved slowly developmental or physiological state of prelarvae, as across the tank bottom after their first feed (day 9). evidenced by previous findings that certain waterborne pollutant (e.g., phenol) markedly inhibit prelarval pigmen- Discussion tation (Dettlaff et al. 1993). The scores for fertilization, hatching, abnormality, via- The findings from the present study indicate that newly bility, and prelarval growth determined in the present hatched Russian sturgeon prelarvae do not exhibit positive study were comparable to those reported by other re- phototaxis, based on their preference for the bottom of searchers studying the artificial propagation of A. guel- the tank under L conditions. No significant negative geo- denstaedtii (Chebanov and Galich 2011; Nathanailides taxis was reported in the hatchling of other sturgeon spe- et al. 2002;Memiş et al. 2009). The development patterns cies (e.g., Acipenser transmontanus and A. brevirostrum) observed in the present study also broadly corroborated exhibiting negative phototactic characteristics (Loew and Kim et al. Fisheries and Aquatic Sciences (2019) 22:4 Page 7 of 10 Fig. 4 Representative photographs showing the progressive increase in the corner-gathering behavior of Acipenser gueldenstaedtii prelarvae with age, followed by aggregation into schools. Two different patterns were observable under the present examination conditions. In pattern I (upper), early corner-gathering prelarvae (day 0–day 2) formed directly non-rheotactic schools at the corners (day 3–day 5). Two large schools on day 5 are indicated by arrows. In contrast, in pattern II (lower), the corner-gathering behavior of the prelarvae (day 0–day 3) shifted to rheotactic prelarval aggregation into a rheotactic school (day 4). A non-rheotactic school developed at a corner on day 5, as indicated by an arrow. Temporal patterns for the two patterns in the diel photoperiodicity of the present study are referred to in Fig. 1 Sillman 1998; Richmond and Kynard 1995). Negative geo- 1993; Gisbert and Solovyev 2018). The prelarvae of tactic behavior has been considered as a characteristic several sturgeon species that exhibit positive phototaxis strategy of the prelarvae of many sturgeon species for (particularly exemplified by the Siberian sturgeon Acipenser early dispersal and predator avoidance. However, this baerii) are reported to actively swim toward the water movement is also related to phototaxis (Dettlaff et al. surface, driven by their intrinsic tendency to approach Fig. 5 Proportion of Acipenser gueldenstaedtii prelarvae engaged in non-rheotactic schools (NRS) and/or rheotactic schools (RS) under light (L), dim light (DL), and dark (D) conditions between day 3 and day 5. Quantitative assessment was carried out with only two tanks (tank 1 and tank 2). Under D conditions, prelarval counts without typical signs of schooling behavior are indicated by dots (day 3/day 4 in tank I and day 3 in tank II). There was no significant difference in the proportions of the prelarvae exhibiting schooling behavior between L and DL conditions in both tanks, irrespective of prelarval age (P > 0.05). Schooling behavior was significantly weakened under D conditions (indicated by asterisks; P < 0.05). However, though they exhibited weakened schooling behavior, a considerable number of prelarvae participated in rheotactic schools under D conditions, whereas non-rheotactic schools almost disappeared. Each mean ± SD is based on at least triplicate counting by two observers, and statistical evaluation was carried out by analysis of variance (ANOVA) followed by Duncan’s multiple range tests Kim et al. Fisheries and Aquatic Sciences (2019) 22:4 Page 8 of 10 Fig. 6 Representative images showing the progressive development of the post-schooling behavior of Acipenser gueldenstaedtii prelarvae from day 6 to day 8, followed by entry into the larval stage on day 9 the light during daylight hours (Gisbert et al. 1999a), unpublished observation), which is highly suggestive which was not clearly seen in the prelarvae of the Russian of negative phototaxis. However, our findings contradict sturgeon. Under DL conditions, the behavior of the previous results in which the 0–5-day-old prelarvae Russian sturgeon at this earliest stage of development was of Russian sturgeon (a Volga River population of A. similar to that under L conditions. Although the behav- gueldenstaedtii) significantly preferred bright illumination ior of the Russian sturgeon prelarvae under D condi- (Kynard et al. 2002). Although such inconsistent results tions differed quantitatively from that under brighter require further investigation, Russiansturgeonprelarvae illumination, a fundamental transition or change in be- have been reported to exhibit a population-dependent havior was not obvious. This differed from the findings variation in phototaxis: positive phototaxis in the Volga reported for other positively phototactic sturgeon River population and negative phototaxis in the Azov species that exhibit a dramatic change in swimming Sea population (Chebanov and Galich 2011;Podushka behavior during the transition from day to night. For 2003). Dettlaff et al. (Dettlaff et al. 1993)reported example, Siberian sturgeon (A. baerii) prelarvae do not that prelarvae of a subspecies of Russian sturgeon swim upwards during darkness, and pelagic swimming (A. gueldenstaedtii colchicus) may not exhibit any photo- at the water surface during the day quickly shifts to taxis during the prelarval stage. benthic movement at night, although the exact light in- Under DL conditions, the Russian sturgeon prelarvae tensity at which this shift occurs has not been reported readily maintained rheotactic and non-rheotactic school- (Gisbert and Ruban 2003; Gisbert et al. 1999a). ing similar to that observed under L conditions (days 4– Onset appearance and development of rheotactic and 6). This suggests that Russian sturgeon prelarvae may be non-rheotactic schooling in the Russian sturgeon prelar- able to sense weak light. Accordingly, the reduction of vae were not uniform among the replicate tanks under L light intensity during DL conditions (10 lx) in the conditions. Increased numbers of prelarvae gathered at present study may have been insufficient to trigger or the tank corners during the early prelarval period (days elicit any significant modifications in schooling behav- 0–3) and were capable of forming large non-rheotactic ior. This finding is different from previous observations schools directly at the corners or alternatively became made with photopositive sturgeon species (A. baerii), rheotactic during day 4. Unfortunately, we were unable in which active schooling behavior under L conditions to identify any potential causative biotic factors (e.g., disappeared when the environmental light intensity was survival and fish size) or abiotic factors (e.g., tank condi- markedly reduced (Chebanov and Galich 2011;Gisbert tions) that were responsible for this non-uniformity. It is et al. 1999a; Rodriguez and Gisbert 2002). therefore clear that further extensive tests are needed to Under the present D conditions (< 1 lx), the Russian determine whether such different schooling patterns are sturgeon prelarvae exhibited a difference in their ability reproducible under various prelarval rearing conditions to maintain rheotactic and post-rheotaxis schooling be- (e.g., density, illumination, tank shape). Nevertheless, havior. Though weakened, the rheotactic schools per- our findings indicate that early corner-gathering school- sisted under dark conditions, whereas the non-rheotactic ing is itself closely related to negative phototactic behav- schools almost disappeared. This observation suggests ior under L conditions. We also found that such corner- that Russian sturgeon prelarvae at these stages may use vi- gathering prelarvae moved actively to avoid an artificial sion as the principal means of determining non-rheotactic spotlight (a 3 W white LED flashlight) (tested on day 1; schooling behavior, whereas their rheotactic behavior may Kim et al. Fisheries and Aquatic Sciences (2019) 22:4 Page 9 of 10 be governed more by an innately established ontogenetic Abbreviations DPH: Days post-hatching; HPF: Hours post-fertilization; HPH: Hours post-hatching; timetable that is less influenced by environmental light LHRH-a: Luteinizing hormone-releasing hormone analogue intensity. In the present study, the post-schooling behavior of the Acknowledgments The authors wish to thank the technical staff at the Experimental Fish Research Russian sturgeon prelarvae did not differ significantly ac- Center, Pukyong National University, who provided the raw observational data. cording to the lighting conditions (L, DL, or D). The post- schooling behavior of the sturgeon prelarvae commenced Funding This study was supported by the grant from KIMST, Ministry of Oceans and with a decrease in prelarval activity in the rheotactic and/ Fisheries of Korea (Grant #20170327). or non-rheotactic schools, typically in the prelarvae at the outer boundary of the schools. As post-schooling behavior Availability of data and materials progressed (days 7–9), compact schools were no longer Not applicable. maintained. The prelarvae were only loosely aggregated Authors’ contributions and eventually became dispersed, non-locomotory, and EJK analyzed the behavior of the sturgeon and prepared the images. CHP scattered over the bottom of the tank (Gisbert et al. bred the sturgeon and co-evaluated the data. NYK designed the study, evaluated the data, and drafted the manuscript. All authors read and approved 1999a). This behavior signals the termination of the pre- the final manuscript. larval phase; the prelarvae are ready to evacuate the yolk plug and finalize the functional development of various di- Ethics approval and consent to participate We followed the experimental protocols described in the guidelines provided gestive organs to ingest exogenous foods (Babaei et al. by the Animal Care and Use Committee of Pukyong National University. 2011; Gisbert et al. 1999b). Therefore, this characteristic behavior reflects the ability of the prelarvae to divert Consent for publication energy to the final preparation for the transition from an Not applicable. endogenous to an exogenous nutrition system (Chebanov Competing interests and Galich 2011;GisbertandWilliot 1997). The authors declare that they have no competing interests. In summary, the results from the present study indi- cate that A. gueldenstaedtii prelarvae essentially exhibit Publisher’sNote negative phototaxis under L conditions during their Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. earliest life stages, and this behavior is not significantly modified under DL or D conditions. During rheotactic Author details and non-rheotactic schooling behaviors, rheotaxis was Department of Marine Bio-Materials and Aquaculture, Pukyong National University, Busan 48513, Republic of Korea. Dinoville Sturgeon Aquafarm, less influenced by environmental light intensity than Hamyang, Kyoung-nam 50027, Republic of Korea. non-rheotactic schooling behavior. Post-schooling be- havior was not significantly affected by light intensity Received: 6 August 2018 Accepted: 10 January 2019 (< 1–450 lx) during a diel light cycle. The results of the present study could be used to scrutinize the light- References dependent physiology of Russian sturgeon prelarvae Babaei SS, Kenari AA, Nazari R, Gisbert E. Developmental changes of digestive enzymes and to develop a practical visual guide for assessing the in Persian sturgeon (Acipenser persicus) during larval ontogeny. Aquaculture. 2011; 318:138–44. https://doi.org/10.1016/j.aquaculture.2011.04.032. health and quality of hatchery-propagated prelarvae Chebanov MS, Galich EV. Sturgeon hatchery manual. FAO Fisheries and Aquaculture under various illumination intensities and/or diel cycle Technical Paper. No. 558. 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Published: Jan 31, 2019

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