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Fine-scale behaviour of the Lusitanian toadfish assessed in situ with the AccelTag

Fine-scale behaviour of the Lusitanian toadfish assessed in situ with the AccelTag Background: Three-axis acceleration sensor acoustic transmitters (AccelTag) programmed to identify specific accel- eration patterns associated with particular behaviours (e.g., burrowing, attack) were used to study some aspects of the ecology of the Lusitanian toadfish Halobatrachus didactylus (Bloch & Schneider 1801). The AccelTag combines the features of archival tags (records acceleration in all three directions measuring also roll-independent pitch/tilt angle and roll around the fish’s axis) and acoustic transmitters. Therefore, this tag can autonomously identify and record specific signatures (i.e., behaviour patterns) of different movements transmitting autonomously and periodically the data to an acoustic biotelemetry receiver. Lusitanian toadfish is a subtropical marine teleost confined to estuaries in its northern limit of distribution due to thermal constraints. During 2010 (August and October), 24 toadfish were cap - tured, tagged with the AccelTag and released in the Mira estuary, SW coast of Portugal, where an array of underwater automatic acoustic biotelemetry receivers was deployed. Results: Around 40% of AccelTag transmissions from tagged fish that stayed in the study area were logged by the acoustic receiver array. The Lusitanian toadfish exhibited low activity during late summer and early autumn (< 3% of time active). The tidal stage and time of day were important factors that influenced the species behaviour and activity. Increased burrowing and re-burrowing movements were registered during spring tides, while attacks prevailed on neap tides and during the night. The tidal cycle only influenced toadfish behaviour and activity in interaction with time of day, with more attacks and higher levels of activity during nocturnal high tides. Conclusions: Higher activity levels and attacks displayed by the Lusitanian toadfish during the night, at high tide periods and during Spring tides are considered to be associated with increased activity and vulnerability of its prey during these periods. The AccelTag proved to be a powerful tool to assess and monitor the activity and fine-scale behaviour of fish in situ. This technology is particularly suited for fish species with biological and ecological features similar to Lusitanian toadfish, i.e., resident species with low activity levels and behaviours with a distinct 3D accelera- tion signature. Keywords: Halobatrachus didactylus, Batrachoididae, Biotelemetry, Accelerometer tag, Biologger, Mira estuary, Portugal Background Understanding fish behaviour and activity patterns is crucial to comprehend the biology and ecology of a fish species or the fish community of a particular ecosystem. In the field, locomotor activity is often inferred from cap - *Correspondence: bsquintella@fc.ul.pt MARE-Centro de Ciências do Mar e do Ambiente, Faculdade de Ciências ture in fishing gear and feeding activity is usually assessed da Universidade de Lisboa, Campo Grande, 1749-016 Lisbon, Portugal from gut fullness at the moment of capture [1]. On the Full list of author information is available at the end of the article © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Pereira et al. Anim Biotelemetry (2021) 9:10 Page 2 of 9 other hand, fish behaviour is often studied by direct Although Lusitanian toadfish is usually considered rela - observations, either on-site or in experimental tanks tively sedentary, using mark–recapture procedures [22], [1–3]. However, with the advancements of fish telemetry it was found that some individuals might perform impor- in the past decade, several behavioural and environmen- tant displacements, which may have feeding or reproduc- tal variables can be monitored remotely [4, 5]. A signifi - tive purposes. In the past, seasonal and daily patterns of cant part of these studies involves archival tags [6, 7], and activity of Lusitanian toadfish were roughly assessed with acoustic transmitters equipped with a three-axis sensor estimates of the yield of captures using trawling nets or [8–11]. feed intake cycles [22, 24]. However, these methodolo- Combining the features of archival tags and acoustic gies showed important limitations because the seasonal transmitters, the AccelTag was successfully developed patterns of activity obtained were fairly masked by the and tested [5]. This acoustic three-axis accelerometer recruitment of young-of-the-year and the differential transmitter measures acceleration in all three directions level of avoidance of the fishing gears by the specimens in (forward, lateral, and vertical). In addition, it also meas- different light (i.e., visibility) and tide conditions, together ures roll-independent pitch/tilt angle and roll around with the differential rate of digestion of the different prey. the fish’s axis. The novelty of the AccelTag is that it has Previous studies tagging toadfish with pressure and tem - the measuring capabilities of an accelerometer archival perature data storage tags (DSTs) and acoustic transmit- tag, but without the necessity of recapture the tagged ters in the Mira estuary (Southwest Portugal) confirmed fish since it has the ability to analyse the logged data that some individuals might perform important displace- (algorithm), extract very detailed species-dependent ments (more than 17  km) and that the species activity information and transmit the relevant processed data is influenced by the circadian cycle, tidal stage and tidal [5]. Therefore, this tag is able to autonomously identify cycle [23]. The study also reinforced the idea that Lusi - and record specific patterns (i.e., signatures) of different tanian toadfish may not exclusively adopt a sit-and-wait movements or behaviours. Due to its proven effective - predation behaviour, but probably undertakes an active ness [5], this technology was selected to study the fine- search for food. However, the DSTs and acoustic trans- scale behaviour of the Lusitanian toadfish Halobatrachus mitters did not allow detecting all the movements per- didactylus (Bloch & Schneider 1801). formed, identify their type and understand which of Lusitanian toadfish reaches over 50 cm in total length, those were related to feeding. Additionally, the effort to and it is one of the biggest members of the Batrachoidi- recapture the tagged individuals to be able to download dae taxonomic Family [12]. The geographical distribution the information recorded by the DSTs was considerable area is vast, encompassing the Central and Northeast [23] and this is a major limitation when working with Atlantic Ocean, from the Gulf of Guinea to the Cen- DSTs particularly when dealing with aquatic animals. tral Iberian Peninsula, and the Western Mediterranean Considering that the species has previous extensive Sea [13, 14]. The species inhabits marine coastal waters, research that also includes the use of biologgers, the estuaries and open littoral lagoons living at depths up to adoption of the AccelTag to comprehend further the 50 m or more, maintaining a benthic behaviour [15]. It is behaviour and trophic ecology of the species offers the mostly found in muddy and sandy bottoms, where it may opportunity to solidify the species knowledge and, at the rest partially buried, but is also found concealed in hard same time, to evaluate in situ the adequacy of the three- substrata, using stones or rock crevices as shelters and axis accelerometer acoustic transmitter. nesting sites [16]. The species is more active in late spring and early sum - Materials and methods mer, concurring with the reproductive period [17, 18]. It Study site and acoustic receiver array occupies a top position on the food web [19] and exhib- The study was carried out in the Mira estuary, a relatively its a high degree of trophic plasticity, adapting its feeding small brackish water system in the southwest coast of habits to prey availability reproductive needs [17, 20, 21]. Portugal (coordinates WGS84: 8º46′19′′W; 37º43′33′′N). The specimens of this species remain most of the time Six biotelemetry acoustic receivers (VR2W, VEMCO) buried or concealed in crevices, adopting a camouflage were deployed ~ 200  m apart from each other, covering and ambush mode of predation [22, 23]. However, in the a distance of ca. 1.5  km, to detect the transmitted codes absence of prey or when the conditions are favourable, (Fig.  1). Every 15  days, the receivers were retrieved for they perform an active search for food by sweeping the data download and deployed again. bottom and the water column, consuming a high per- centage of necktobenthic organisms [22]. Stomach con- AccelTag and fish tagging tents analysis suggested that such variations on activity The AccelTag is an acoustic transmitter with a sen - may be related to temperature, light and tidal cycles [22]. sor (three-axis accelerometer) capable of measuring P ereira et al. Anim Biotelemetry (2021) 9:10 Page 3 of 9 Table 1 Sensor activity codes Code Time of activity (%) 0 0.00–0.99 1 1.00–1.99 2 2.00–2.99 3 3.00–3.99 4 4.00–4.99 5 5.00–5.99 6 6.00–6.99 7 7.00–7.99 8 8.00–12.49 9 12.50–24.99 10 25.00–37.49 11 37.50–49.99 12 50.00–62.49 13 62.50–74.99 14 75.00–87.49 15 87.50–99.99 Each transmitted code corresponds to the percentage of time (interval) during which each toadfish was active in the past hour Fig. 1 Location of the study area and biotelemetry acoustic receivers ( VR2W ) array were reprogrammed by Thelma Biotel. Tagging was external, according to the procedure described in [5]. forward, lateral and vertical accelerations as well as A total of 24 Lusitanian toadfish ranging between tilt and roll angles [5]. The AccelTag was developed to 27.3  cm and 32.6  cm were captured using fish traps on detect particular behaviours of the Lusitanian toadfish. two distinct occasions: 12 specimens in August 2010 The version of the AccelTag that was used is capable of (Group 1) and 12 in October 2010 (Group 2). Group 1 identifying three behavioural signatures: attack towards was tested from August 23 to September 24 and Group 2 a potential prey, burrowing and re-burrowing move- from October 1 to November 3. The considered periods ments. The attack detection feature was tested with dif - allowed to avoid the influence of the reproductive cycle ferent types of prey, but the tag could not distinguish (Spring and beginning of Summer). All Lusitanian toad- them. Moreover, although the behaviour is identified fish were captured and released in Mira estuary within and registered as an attack, the predation’s success rate range of the VR2W array. After capturing, fish were is unknown [5]. immediately tagged with 9-mm versions of the AccelTag The Acceltag detects and counts events for hourly peri - with approximately 1  month of battery life and released ods, after which the data are acoustically transmitted at the capture site. through two consecutive S256 codes and recorded by an acoustic receiver array. The tag could report 0–6 events Data analysis correctly, but if the number of events was 7 or more, the The success rate of transmissions detected by the acoustic number 7 was logged. More than 7 events in one hour receivers array was calculated by dividing the number of were not very likely to happen with this species [23]. The transmissions received by the total number of transmis- AccelTag also comprises an activity meter programmed sions theoretically emitted by the tag. This was only cal - and tested according to Lusitanian toadfish movements culated for the duration of the study period during which that measure the percentage of time the fish are moving. tagged specimen maintained position within range of the The activity data is transmitted as percentage intervals acoustic receiver array. The influence of environmen - (Table 1). tal factors on the activity and behaviour of toadfish was Prior to the field study, a 13-mm AccelTag with the analysed using a factorial ANOVA. The analysed envi - latest version of the “signature” detection software was ronmental factors were tidal stage (spring vs neap), tidal externally implanted in 4 toadfish and tested for accuracy cycle (high vs low) and time of day (day vs night). Also, in a 900-L sand bottom covered trial tank using an iden- the influence of the time of the year was studied com - tical experimental protocol as previously described [5]. paring the differences between Group 1 (summer) and After satisfactory results were obtained, 9-mm AccelTags Pereira et al. Anim Biotelemetry (2021) 9:10 Page 4 of 9 Group 2 (autumn). This procedure allowed to assess each Considering the activity and the number of events factor’s influence or, as an interaction of two or more fac - observed during distinct environmental conditions, tors. The data used in the analysis were expressed as the tidal stage (TS: spring vs neap) and time of day (TD: day total number of events per fish and hour for each behav - vs night) were the most influencing factors (Tables  2, ioural signature. Activity data was converted from per- 3). In fact, tagged Lusitanian toadfish were more active centage to time units (minutes), and the lower limit of and performed significantly more burrowing and re- the activity interval per hour and per fish was used for burrowing movements during spring tides. However, the the analysis. As an example, if the data showed an activity TS did not influence the number of attacks significantly interval of 3 (5%)–3.6 (5.99%) minutes, it was used 3 min (Tables 2, 3). Regarding the influence of time of day, Lusi - of activity for the analysis. Spring tides were defined as tanian toadfish were more active and performed signifi - tides with an amplitude of over 3.2  m and neap tides as cantly more attacks during night-time (Tables 2, 3). tides of amplitude less than 2 m. For tidal cycle analysis, it When evaluating differences in behaviour poten - was considered the transmissions detected 2 h before and tially associated with seasonality, the number of attacks 2  h after low and high tidal peaks. Night-time included and activity revealed no statistical differences between dusk and day-time included dawn. In order to obtain the groups/seasons. However, Group 1 composed by fish most accurate data possible, codes from the first 2 days tracked during the summer performed significantly more and the last day of transmissions were removed from the burrowings and re-burrowings than Group 2 composed analysis [5]. by fish tracked in autumn (Tables 2, 3). Even though tidal cycle (TC: high vs low) alone did not Results significantly influence the behaviour and activity of the Before the field study, the tag and detection software Lusitanian toadfish, factorial ANOVA showed a signifi - were tested for accuracy on four specimens in a labora- cant interaction between this factor and the TD regard- tory trial. Tests resulted in 100% efficiency for detect - ing the number of attacks and fish activity (Table  3). The ing activity, burrowing and re-burrowing movements. analyses of Tables  2 and 3 show that toadfish performed Attacks towards potential prey were registered with 85% more attacks and were more active during high tides that accuracy, increasing 25% when compared with the previ- occurred during night-time. The TS also significantly ous algorithm developed by [5]. influenced toadfish behaviour when interacting with TD. Regarding the field study, of the 24 Lusitanian toad - Indeed, it was during the night-time of spring tides when fish tagged and released in the Mira estuary, only three toadfish were substantially more active (Tables  2, 3). Sig- specimens spent most of the time out of the range of nificant interactions were also found between-group and the acoustic receiver array. The remaining specimens TS, and between-group and TD. During the summer returned to the capture sites within 2 days and remained (Group 1) Lusitanian toadfish were more active and per - most of the time inside a perimeter of 200 m. formed more burrowing and re-burrowing movements A total of 3530 (39.5% of the transmissions) complete during spring tides, along with more attacks during the codes from Group 1 and 3719 (41.7%) from Group 2 were night-time. successfully received, stored, and downloaded from the acoustic telemetry array. Group 1 performed 960 poten- Discussion tial attacks, 202 burrowings and 282 re-burrowings, and The results from this study were obtained using an inno - showed 1.51 min (2.5% of the time) per hour of minimum vative technological approach, the AccelTag, developed mean activity. Group 2 conducted 665 potential attacks, and previously tested in controlled laboratory condi- 120 burrowings and 142 re-burrowings, and had a mini- tions [5]. In the present work, it was used for the first mum mean activity of 1.52 min per h (2.5% of the time). time to obtain in  situ detailed foraging behaviour data By plotting the frequency of each studied behaviour of an aquatic animal. AccelTag proved to be a power- and the percentage of activity against tidal amplitude, ful tool to assess and monitor the fine-scale behaviour it was possible to observe that the frequency of attacks, of a resident estuarine fish. In terms of ecological data burrowing and re-burrowing movements varied along obtained with AccelTag, the main findings are concord - the studied period but without an obvious relation with ant with results obtained with other works that used dis- tidal stage per se (Figs.  2 and 3). Regarding activity pat- tinct methodological approaches to study the Lusitanian terns, Lusitanian toadfish from Group 1 tracked in the toadfish foraging behaviour [21–24]. When comparing summer were more active during spring tides, whereas to other available tools (see [5] for further discussion) fish from Group 2 tracked in autumn did not reveal a such as data storage tags with accelerometer sensors [6, marked activity pattern throughout the study period 7], and even more recent acoustic transmitters equipped (Figs. 2 and 3). with three-axis accelerometer sensors [8–11, 25, 26], the P ereira et al. Anim Biotelemetry (2021) 9:10 Page 5 of 9 Fig. 2 Graphic representation of the studied behaviours as a function of the tidal stage (spring or neap tide) and time of day (day or night) for the toadfish of Group 1 tracked during August–September 2010 AccelTag has the advantage of being able to process the the software accordingly to distinct behaviours, and then fine-scale acceleration information autonomously and implement in situ behaviour studies. acoustically transmit the correspondent behaviour. Sev- With regard to the foraging ecology of the Lusitanian eral authors have identified advantages of data processing toadfish, tides and circadian cycle, together with the time and compression, e.g., increased tag autonomy, reduced of year, seem to play an essential role in the behaviour storage requirements and reduced data analysis time [11, of this species. Notwithstanding being capable of swim- 27]. Moreover, the work previously developed [5], com- ming over relatively large distances [22, 23], specimens bined with the present study corresponds to the antici- typically do not perform significant displacements and pated studies and technological enhancements proposed remain most of the time inactive (97.5% of the time in [11], namely the tagging of captive specimens to calibrate the present study), buried in the sediment or concealed Pereira et al. Anim Biotelemetry (2021) 9:10 Page 6 of 9 Fig. 3 Graphic representation of the studied behaviours as a function of the tidal stage (spring or neap tide) and time of day (day or night) for the toadfish of Group 2 tracked during October–November 2010 in rocky crevices. In fact, the majority of the specimens Tidal stage influenced toadfish behaviour and activ - remained within the study area for almost the entire ity in larger cycles of time. During spring tides of higher study period, some of them returning to the capture site amplitudes, the activity increased and the number of after being tagged and released. However, this sedentary potential attacks diminished. This pattern may be related behaviour was amplified by the time of the year when to strong water currents associated with this period that the study occurred. Moreover, this species is more active force toadfish to actively avoid being dragged away and, during the spawning season, which occurs in late spring consequently, reduce feeding activity. After this period and early summer [17, 18], whereas this study was per- of reduced feeding attempts, during neap tides, attacks formed in late summer and mid-autumn when the speci- considerably increase and activity level decreases. Vari- mens tend to reduce global activity and decrease the ations on tidal stages also explain the marked pattern number of long displacements [22]. of burrowing and re-burrowing movements. These are P ereira et al. Anim Biotelemetry (2021) 9:10 Page 7 of 9 Table 2 Mean number of events and time of activity of the tagged toadfish according to environmental factors Attack Burrowing Re-burrowing Activity N Mean SD N Mean SD N Mean SD Minute Mean SD Group 1 ST 362 0.27 0.73 162 0.12 0.47 204 0.15 0.61 2708.4 2.00 4.29 NT 598 0.27 0.66 40 0.02 0.14 78 0.04 0.25 2631.9 1.21 1.78 LT 493 0.27 0.69 88 0.05 0.27 140 0.08 0.42 2564.1 1.44 2.54 HT 467 0.27 0.68 114 0.06 0.34 142 0.08 0.45 2776.2 1.58 3.44 Da 201 0.13 0.45 98 0.06 0.29 118 0.08 0.41 1264.8 0.79 1.55 Ni 759 0.40 0.81 104 0.05 0.33 164 0.09 0.45 4074.5 0.11 3.73 Group 2 ST 143 0.17 0.49 38 0.05 0.32 45 0.05 0.34 1089.6 1.31 2.09 NT 522 0.18 0.54 82 0.03 0.25 97 0.03 0.25 4594.2 1.59 2.85 LT 267 0.15 0.45 50 0.03 0.28 60 0.03 0.25 2810.7 1.56 3.05 HT 398 0.21 0.59 70 0.04 0.25 82 0.04 0.29 2873.1 1.50 2.32 Da 190 0.11 0.41 51 0.03 0.19 74 0.04 0.24 1764.9 1.04 2.02 Ni 475 0.24 0.60 69 0.03 0.32 68 0.03 0.29 3918.9 1.94 3.10 Total ST 505 0.22 0.61 200 0.09 0.40 249 0.10 0.48 3798.0 1.66 3.19 NT 1120 0.23 0.60 122 0.03 0.20 175 0.05 0.25 7226.1 1.40 2.32 LT 760 0.21 0.57 138 0.04 0.28 200 0.06 0.34 5374.8 1.50 2.80 HT 865 0.24 0.64 184 0.05 0.30 224 0.06 0.37 4649.3 1.54 2.88 Da 391 0.12 0.43 139 0.05 0.24 192 0.06 0.33 3029.7 0.92 1.79 Ni 1234 0.32 0.71 143 0.04 0.33 232 0.06 0.37 7993.4 1.03 3.42 N number of events (attacks, burrowings and re-burrowings) and mean time of activity (minutes) per hour, SD standard deviation, ST spring tides, NT neap tide, LT low tide, HT high tide, Da day, Ni night Table 3 Factorial ANOVA results to  assess the  influence of  environmental factors on  the  activity and  behaviour of the tagged toadfish Factorial ANOVA Attacks Burrowing Re-burrowing Activity Global F = 18.883; d.f. = 15; p < 0.01 F = 9.864; d.f. = 15; p < 0.01 F = 8.370; d.f. = 15; p < 0.01 F = 29.517; d.f. = 15; p < 0.01 TS F = 0.003; d.f. = 1; p = 0.958 F = 61.611; d.f. = 1; p < 0.01 F = 49.191; d.f. = 1; p < 0.01 F = 13.832; d.f. = 1; p < 0.01 TC F = 1.921; d.f. = 1; p = 0.166 F = 1.506; d.f. = 1; p = 0.220 F = 0.583; d.f. = 1; p = 0.445 F = 2.903; d.f. = 1; p = 0.09 TD F = 138.887; d.f. = 1; p < 0.01 F = 0.000; d.f. = 1; p = 0.993 F = 0.195; d.f. = 1; p = 0.658 F = 248.599; d.f. = 1; p < 0.01 G F = 31.572; d.f. = 1; p = 0.05 F = 20.140; d.f. = 1; p < 0.01 F = 27.775; d.f. = 1; p < 0.01 F = 3.744; d.f. = 1; p = 0.05 TS * TC F = 0.042; d.f. = 1; p = 0.838 F = 1.875; d.f. = 1; p = 0.171 F = 0.176; d.f. = 1; p = 0.675 F = 7.131; d.f. = 1; p = 0.08 TS * TD F = 2.657; d.f. = 1; p = 0.103 F = 0.040; d.f. = 1; p = 0.842 F = 1.228; d.f. = 1; p = 0.268 F = 5.539; d.f. = 1; p < 0.05 TS * G F = 0.051; d.f. = 1; p = 0.822 F = 33.601; d.f. = 1; p < 0.01 F = 25.382; d.f. = 1; p < 0.01 F = 53.695; d.f. = 1; p < 0.01 TC * TD F = 4.216; d.f. = 1; p < 0.05 F = 0.103; d.f. = 1; p = 0.748 F = 0.953; d.f. = 1; p = 0.329 F = 12.149; d.f. = 1; p < 0.01 TC * G F = 2.730; d.f. = 1; p = 0.10 F = 0.267; d.f. = 1; p = 0.605 F = 0.465; d.f. = 1; p = 0.495 F = 1.325; d.f. = 1; p = 0.250 G * TD F = 21.913; d.f. = 1; p < 0.01 F = 0.708; d.f. = 1; p = 0.400 F = 2.234; d.f. = 1; p = 0.135 F = 15.885; d.f. = 1; p < 0.01 TS tidal stage, TC tidal cycle, TD time of day, G group Significant differences for p < 0.01 and p < 0.05. more frequent during spring tides, when toadfish need On the other hand, the tidal cycle only influenced toad - to refuge (i.e., remain buried) to avoid being displaced by fish behaviour and activity in interaction with the time strong water currents, and decrease during neap tides. of day. Indeed, the number of attacks and activity were influenced synergistically by those two factors. Toadfish Pereira et al. Anim Biotelemetry (2021) 9:10 Page 8 of 9 were more active during night-time, confirming previ - the Lusitanian toadfish, i.e., resident species with low ous findings in the same estuary [22, 23]. The nocturnal activity levels and behaviours with a distinct three- period is the preferred for engaging feeding activities as axis acceleration signature. Higher activity levels and their prey are also more active. Subsequently, the number attacks displayed by the Lusitanian toadfish during of attacks also increased during the night period. Addi- the night, at high tide periods and during Spring tides tionally, high tide phases considerably improve visibility are considered to be associated with increased activity in the lower Mira Estuary due to the input of more trans- and vulnerability of its prey during these periods. The parent water from the ocean. As previously observed in potentialities of this technology to study aquatic organ- laboratory experiments [5], toadfish is a visual predator isms behaviour are far from being fully explored with attacking its prey mostly based on movement. Therefore, this study. More precise and complete signature detec- the combination of high tide with night-time results in a tion algorithms, together with longer battery life could favourable period for toadfish to feed. As highlighted by offer new possibilities of behavioural studies on the [23] these higher activity periods displayed by the Lusi- Lusitanian toadfish and other fish species. In the future, tanian toadfish are not independent of the activity of it would be interesting to discern between success- its prey, most of them displaying higher activity or vul- ful and unsuccessful attacks or even the type of prey, nerability to predation during the night and at high tide once toadfish may attack and handle distinct preys periods. differently. The influence of the time of year was evident in the dif - Acknowledgements ferences between the two groups of toadfish tagged. The The present study was carried under the project “AccelTag—Development of first group of toadfish was tagged and tested in late sum - an acoustic three-axis accelerometer transmitter for marine species” funded by European Union EUREKA Eurostars Programme and project “COASTNET— mer, close to the end of the spawning season. Moreover, Portuguese Coastal Monitoring Network (PINFRA/22128/2016)” funded by the year of 2010 presented a relatively rainy and cold European Regional Development Fund (FEDER), through LISBOA2020 and spring, which delayed the spawning season of this spe- ALENTEJO2020 regional operational programs, in the framework of the National Roadmap of Research Infrastructures of strategic relevance. cies, which is highly influenced by water temperature [22]. Therefore, global activity is relatively high at the Authors’ contributions beginning of the study, gradually reducing in the follow- PRA, BRQ, AG and JLC conceived and designed the project. TJP and BRQ led the field work. Data analysis was conducted by TJP with help from JLC, PRA ing 12  days. During this period, the tagged toadfish also and BRQ. All authors (JLC, PRA, BRQ, AG, MJC, JPM and JLC) contributed to the performed more attacks, as it is expected at the end of research and writing of the manuscript. All authors read and approved the the reproductive period [22]. Concerning the second final manuscript. group of toadfish, it was monitored in mid-autumn, far Funding from the spawning season and closer to the winter. This Research was funded by European Union EUREKA Eurostars Programme. period corresponds to the time of year when this species Availability of data and materials is less active [22]. This discrepancy between the times of The datasets used and analysed during the current study are available from the year in which the two groups were monitored may the corresponding author on reasonable request. explain detected differences in burrowing and re-burrow - Ethics approval and consent to participate ing movements and activity levels, with toadfish tracked This study was carried out in strict accordance with the recommendations in summer performing more of these behaviours and present in the Guide for the Care and Use of Laboratory Animals of the toadfish tracked in autumn being globally more active. European Union—in Portugal represented by the Decree-Law No. 129/92, Portaria No. 1005/92. Approval by a named review board institution or ethics However, the number of attacks did not significantly dif - committee was not necessary as the final model for ethical experimentation fer between seasons, which may suggest that the higher using fish as biological models was not implemented in Portuguese research activity observed with the toadfish tracked in autumn units at the time of experimentation. may be related to the search for shelters instead of food. Consent for publication Therefore, both groups were influenced by tide and time Not applicable. of day, but differences between groups are probably Competing interests related to the species circannual lifecycle. The authors declare that they have no competing interests. Author details Conclusions MARE-Centro de Ciências do Mar e do Ambiente, Faculdade de Ciências da The behavioural signature capture version of the Accel - Universidade de Lisboa, Campo Grande, 1749-016 Lisbon, Portugal. Depar- tamento de Biologia, Escola de Ciências e Tecnologia, Universidade de Évora, Tag was tested for the first time in  situ to monitor the Évora, Portugal. Departamento de Biologia Animal, Faculdade de Ciências da fine-scale behaviour of aquatic animals. This tech - Universidade de Lisboa, Lisboa, Portugal. Thelma Biotel, Sluppen, Trondheim, nology proved to be particularly suited for fish spe - Norway. cies with biological and ecological features similar to P ereira et al. Anim Biotelemetry (2021) 9:10 Page 9 of 9 Received: 17 September 2020 Accepted: 27 January 2021 15. Roux C. Batrachoididae. In: Fischer W, Bianchi G, Scott WB, editors. Fiches FAO d’identification des espèces pour les besoins de la pêche. Atlantique centreest: zones de pêche 34, 47 (en partie). Vol. I. Canada Fonds de Dépôt, Ottawa, 1981. 16. Muzavor S, Arruda LM, Andrade JP. Roteiro ecológico da Ria Formosa. vol. 2, Peixes. Foco Editora 1993. References 17. Costa JL, Silva G, Almeida PR, Costa MJ. Activity and diet of Halobatrachus 1. Reebs SG. Plasticity of diel and circadian activity rhythms in fishes. Rev didactylus (Bloch & Schneider, 1801) adults in the Tagus estuary. Thalassas. Fish Biol Fisher. 2002;12:349–71. 2000;16:21–5. 2. Martins CIM, Conceição LEC, Schrama JW. Consistency of individual vari- 18. Palazón-Fernández JL, Arias AM, Sarasquete C. Aspects of the reproduc- ation in feeding behaviour and its relationship with performance traits in tive biology of the toadfish, Halobatrachus didactylus (Schneider, 1801) Nile tilapia Oreochromis niloticus. Appl Anim Behav Sci. 2011;133:109–16. (Pisces: Batrachoididae). Scientia Marina. 2001;65(2):131–8. 3. Ramos A, Fonseca PJ, Modesto T, Almada VC, Amorim MPC. Alloparental 19. Costa JL, Domingos I, Almeida AJ, Feunteun E, Costa MJ. The interaction behavior in the highly vocal Lusitanian toadfish. J Exp Mar Biol Ecol. between Halobatrachus didactylus and Anguilla anguilla: what happens 2012;435:58–62. when these species occur in sympatry? Cybium. 2008;32(2):111–7. 4. Hussey NE, Kessel ST, Aarestrup K, Cooke SJ, Cowley PD, Fisk AT, Harcourt 20. Pereira TJ, Silva G, Costa MJ, Costa JL. Life strategies of Halobatrachus RG, Holland KN, Iverson SR, Kocik JF, Flemming JEM, Whoriskey FG. didactylus (Bloch & Schneider, 1801) in the Tagus estuary: comparison Aquatic animal telemetry: a panoramic window into the underwater among different morphotypes. Estuar Coast Shelf Sci. 2011;93(4):328–35. world. Science. 2015;348(6240):1255642. 21. Félix P, Amorim M, Pereira T, Fonseca P, Sousa-Santos C, Costa J. Feeding 5. Almeida PR, Pereira TJ, Quintella BR, Gronningsaeter A, Costa MJ, Costa ecology and life-history strategy of nesting males in a fish with long JL. Testing a 3-axis accelerometer acoustic transmitter (AccelTag) on the parental care, Lusitanian toadfish (Halobatrachus didactylus, Batrachoidi- Lusitanian toadfish. J Exp Mar Biol Ecol. 2013;449:230–8. dae). J Mar Biol Assoc UK. 2016;96(3):657–65. 6. Gleiss AC, Gruber SH, Wilson RP. Multi-channel datalogging: towards 22. Costa JL. A biologia do xarroco, Halobatrachus didactylus (Bloch & Schnei- determination of behaviour and metabolic rate in free-swimming sharks. der, 1801), e o seu papel na estruturação e funcionamento das comuni- In: Nielsen JL, Arrizabalaga H, Fragoso N, Hobday A, Lutcavage M, Sibert J, dades em que se insere; referência especial à população do Estuário do editors. Tagging and tracking of marine animals with electronic devices. Mira. PhD Thesis, University of Lisbon, Lisbon, 2004. Dordrecht: Springer; 2009. p. 211–28. 23. Campos MC, Costa JL, Quintella BR, Costa MJ, Almeida PR. Activity and 7. Ward CRE, Bouyoucos IA, Brooks EJ, O’Shea OR. Novel attachment movement patterns of the Lusitanian toadfish inferred from pressure methods for assessing activity patterns using triaxial accelerometers on sensitive data-loggers in the Mira estuary (Portugal). Fish Manag Ecol. stingrays in the Bahamas. Mar Biol. 2019;166:53. 2008;15(5–6):449–58. 8. Gleiss AC, Dale JJ, Holland KN, Wilson RP. Accelerating estimates of 24. Cotter JC, Pereira TJ, Costa MJ, Costa JL. Distribution, abundance, popula- activity-specific metabolic rate in fishes: testing the applicability of accel- tion structure and activity of Halobatrachus didactylus (Bloch & Schneider, eration data-loggers. J Exp Mar Biol Ecol. 2010;385(1–2):85–91. 1801) in the Tagus estuary and adjacent coastal area. J Mar Biol Assoc. 9. Murchie KJ, Cooke SJ, Danylchukc AJ, Suski CD. Estimates of field activity 2013;93(2):405–12. and metabolic rates of bonefish (Albula vulpes) in coastal marine habitats 25. O’Toole AC, Murchie KJ, Pullen C, Hanson KC, Suski CD, Danylchuk AJ, using acoustic tri-axial accelerometer transmitters and intermittent-flow Cooke SJ. Locomotory activity and depth distribution of adult great bar- respirometry. J Exp Mar Biol Ecol. 2011;396(2):147–55. racuda (Sphyraena barracuda). In: Bahamian coastal habitats determined 10. Nakamura I, Watanabe YY, Papastamatiou YP, Sato K, Meyer CG. Yo–yo ver- using acceleration and pressure biotelemetry transmitter. Mar Freshw Res tical movements suggest a foraging strategy for tiger sharks Galeocerdo 2010;61(12):1446–1456. cuvier. Mar Ecol Prog Ser. 2011;424:237–46. 26. Kneebone J, Winton M, Danylchuk A, Chisholm J, Skomal G. An assess- 11. Nuijten RJM, Gerrits T, Shamoun-Baranes J, Nolet BA. Less is more: on- ment of juvenile sand tiger (Carcharias taurus) activity patterns in a board lossy compression of accelerometer data increases biologging seasonal nursery using accelerometer transmitters. Environ Biol Fish. capacity. J Anim Ecol. 2020;89(1):237–47. 2018;101(8):1739–56. 12. Greenfield DW, Winterbottom R, Collette BB. Review of the toadfish 27. Allen AN, Goldbogen JA, Friedlaender AS, Calambokidis J. Develop- genera ( Teleostei: Batrachoididae). San Francisco, CA, USA: California ment of an automated method of detecting stereotyped feeding Academy of Sciences, Proc; 2008. events in multisensor data from tagged rorqual whales. Ecol Evol. 13. Beauchot ML. Poissons osseux. In: Fischer W, Schneider M, Beauchot M-L, 2019;6(20):7522–35. editors. Fiches FAO d’identification des espèces pour les besoins de la pêche. Mediterranée et Mer Noire (Zone de Pêche 37). Revision 1. Vol. II-Vertebrés. FAO, Rome, 1987. p. 891–1421. Publisher’s Note 14. Costa JL, Costa MJ. Distribution and abundance of the Lusitanian toadfish Springer Nature remains neutral with regard to jurisdictional claims in pub- Halobatrachus didactylus (Bloch & Schneider, 1801) in Portugal with some lished maps and institutional affiliations. remarks on its population fragmentation. Rev Biol. 2002;20:155–67. Re Read ady y to to submit y submit your our re researc search h ? Choose BMC and benefit fr ? Choose BMC and benefit from om: : fast, convenient online submission thorough peer review by experienced researchers in your field rapid publication on acceptance support for research data, including large and complex data types • gold Open Access which fosters wider collaboration and increased citations maximum visibility for your research: over 100M website views per year At BMC, research is always in progress. Learn more biomedcentral.com/submissions http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Animal Biotelemetry Springer Journals

Fine-scale behaviour of the Lusitanian toadfish assessed in situ with the AccelTag

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Abstract

Background: Three-axis acceleration sensor acoustic transmitters (AccelTag) programmed to identify specific accel- eration patterns associated with particular behaviours (e.g., burrowing, attack) were used to study some aspects of the ecology of the Lusitanian toadfish Halobatrachus didactylus (Bloch & Schneider 1801). The AccelTag combines the features of archival tags (records acceleration in all three directions measuring also roll-independent pitch/tilt angle and roll around the fish’s axis) and acoustic transmitters. Therefore, this tag can autonomously identify and record specific signatures (i.e., behaviour patterns) of different movements transmitting autonomously and periodically the data to an acoustic biotelemetry receiver. Lusitanian toadfish is a subtropical marine teleost confined to estuaries in its northern limit of distribution due to thermal constraints. During 2010 (August and October), 24 toadfish were cap - tured, tagged with the AccelTag and released in the Mira estuary, SW coast of Portugal, where an array of underwater automatic acoustic biotelemetry receivers was deployed. Results: Around 40% of AccelTag transmissions from tagged fish that stayed in the study area were logged by the acoustic receiver array. The Lusitanian toadfish exhibited low activity during late summer and early autumn (< 3% of time active). The tidal stage and time of day were important factors that influenced the species behaviour and activity. Increased burrowing and re-burrowing movements were registered during spring tides, while attacks prevailed on neap tides and during the night. The tidal cycle only influenced toadfish behaviour and activity in interaction with time of day, with more attacks and higher levels of activity during nocturnal high tides. Conclusions: Higher activity levels and attacks displayed by the Lusitanian toadfish during the night, at high tide periods and during Spring tides are considered to be associated with increased activity and vulnerability of its prey during these periods. The AccelTag proved to be a powerful tool to assess and monitor the activity and fine-scale behaviour of fish in situ. This technology is particularly suited for fish species with biological and ecological features similar to Lusitanian toadfish, i.e., resident species with low activity levels and behaviours with a distinct 3D accelera- tion signature. Keywords: Halobatrachus didactylus, Batrachoididae, Biotelemetry, Accelerometer tag, Biologger, Mira estuary, Portugal Background Understanding fish behaviour and activity patterns is crucial to comprehend the biology and ecology of a fish species or the fish community of a particular ecosystem. In the field, locomotor activity is often inferred from cap - *Correspondence: bsquintella@fc.ul.pt MARE-Centro de Ciências do Mar e do Ambiente, Faculdade de Ciências ture in fishing gear and feeding activity is usually assessed da Universidade de Lisboa, Campo Grande, 1749-016 Lisbon, Portugal from gut fullness at the moment of capture [1]. On the Full list of author information is available at the end of the article © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Pereira et al. Anim Biotelemetry (2021) 9:10 Page 2 of 9 other hand, fish behaviour is often studied by direct Although Lusitanian toadfish is usually considered rela - observations, either on-site or in experimental tanks tively sedentary, using mark–recapture procedures [22], [1–3]. However, with the advancements of fish telemetry it was found that some individuals might perform impor- in the past decade, several behavioural and environmen- tant displacements, which may have feeding or reproduc- tal variables can be monitored remotely [4, 5]. A signifi - tive purposes. In the past, seasonal and daily patterns of cant part of these studies involves archival tags [6, 7], and activity of Lusitanian toadfish were roughly assessed with acoustic transmitters equipped with a three-axis sensor estimates of the yield of captures using trawling nets or [8–11]. feed intake cycles [22, 24]. However, these methodolo- Combining the features of archival tags and acoustic gies showed important limitations because the seasonal transmitters, the AccelTag was successfully developed patterns of activity obtained were fairly masked by the and tested [5]. This acoustic three-axis accelerometer recruitment of young-of-the-year and the differential transmitter measures acceleration in all three directions level of avoidance of the fishing gears by the specimens in (forward, lateral, and vertical). In addition, it also meas- different light (i.e., visibility) and tide conditions, together ures roll-independent pitch/tilt angle and roll around with the differential rate of digestion of the different prey. the fish’s axis. The novelty of the AccelTag is that it has Previous studies tagging toadfish with pressure and tem - the measuring capabilities of an accelerometer archival perature data storage tags (DSTs) and acoustic transmit- tag, but without the necessity of recapture the tagged ters in the Mira estuary (Southwest Portugal) confirmed fish since it has the ability to analyse the logged data that some individuals might perform important displace- (algorithm), extract very detailed species-dependent ments (more than 17  km) and that the species activity information and transmit the relevant processed data is influenced by the circadian cycle, tidal stage and tidal [5]. Therefore, this tag is able to autonomously identify cycle [23]. The study also reinforced the idea that Lusi - and record specific patterns (i.e., signatures) of different tanian toadfish may not exclusively adopt a sit-and-wait movements or behaviours. Due to its proven effective - predation behaviour, but probably undertakes an active ness [5], this technology was selected to study the fine- search for food. However, the DSTs and acoustic trans- scale behaviour of the Lusitanian toadfish Halobatrachus mitters did not allow detecting all the movements per- didactylus (Bloch & Schneider 1801). formed, identify their type and understand which of Lusitanian toadfish reaches over 50 cm in total length, those were related to feeding. Additionally, the effort to and it is one of the biggest members of the Batrachoidi- recapture the tagged individuals to be able to download dae taxonomic Family [12]. The geographical distribution the information recorded by the DSTs was considerable area is vast, encompassing the Central and Northeast [23] and this is a major limitation when working with Atlantic Ocean, from the Gulf of Guinea to the Cen- DSTs particularly when dealing with aquatic animals. tral Iberian Peninsula, and the Western Mediterranean Considering that the species has previous extensive Sea [13, 14]. The species inhabits marine coastal waters, research that also includes the use of biologgers, the estuaries and open littoral lagoons living at depths up to adoption of the AccelTag to comprehend further the 50 m or more, maintaining a benthic behaviour [15]. It is behaviour and trophic ecology of the species offers the mostly found in muddy and sandy bottoms, where it may opportunity to solidify the species knowledge and, at the rest partially buried, but is also found concealed in hard same time, to evaluate in situ the adequacy of the three- substrata, using stones or rock crevices as shelters and axis accelerometer acoustic transmitter. nesting sites [16]. The species is more active in late spring and early sum - Materials and methods mer, concurring with the reproductive period [17, 18]. It Study site and acoustic receiver array occupies a top position on the food web [19] and exhib- The study was carried out in the Mira estuary, a relatively its a high degree of trophic plasticity, adapting its feeding small brackish water system in the southwest coast of habits to prey availability reproductive needs [17, 20, 21]. Portugal (coordinates WGS84: 8º46′19′′W; 37º43′33′′N). The specimens of this species remain most of the time Six biotelemetry acoustic receivers (VR2W, VEMCO) buried or concealed in crevices, adopting a camouflage were deployed ~ 200  m apart from each other, covering and ambush mode of predation [22, 23]. However, in the a distance of ca. 1.5  km, to detect the transmitted codes absence of prey or when the conditions are favourable, (Fig.  1). Every 15  days, the receivers were retrieved for they perform an active search for food by sweeping the data download and deployed again. bottom and the water column, consuming a high per- centage of necktobenthic organisms [22]. Stomach con- AccelTag and fish tagging tents analysis suggested that such variations on activity The AccelTag is an acoustic transmitter with a sen - may be related to temperature, light and tidal cycles [22]. sor (three-axis accelerometer) capable of measuring P ereira et al. Anim Biotelemetry (2021) 9:10 Page 3 of 9 Table 1 Sensor activity codes Code Time of activity (%) 0 0.00–0.99 1 1.00–1.99 2 2.00–2.99 3 3.00–3.99 4 4.00–4.99 5 5.00–5.99 6 6.00–6.99 7 7.00–7.99 8 8.00–12.49 9 12.50–24.99 10 25.00–37.49 11 37.50–49.99 12 50.00–62.49 13 62.50–74.99 14 75.00–87.49 15 87.50–99.99 Each transmitted code corresponds to the percentage of time (interval) during which each toadfish was active in the past hour Fig. 1 Location of the study area and biotelemetry acoustic receivers ( VR2W ) array were reprogrammed by Thelma Biotel. Tagging was external, according to the procedure described in [5]. forward, lateral and vertical accelerations as well as A total of 24 Lusitanian toadfish ranging between tilt and roll angles [5]. The AccelTag was developed to 27.3  cm and 32.6  cm were captured using fish traps on detect particular behaviours of the Lusitanian toadfish. two distinct occasions: 12 specimens in August 2010 The version of the AccelTag that was used is capable of (Group 1) and 12 in October 2010 (Group 2). Group 1 identifying three behavioural signatures: attack towards was tested from August 23 to September 24 and Group 2 a potential prey, burrowing and re-burrowing move- from October 1 to November 3. The considered periods ments. The attack detection feature was tested with dif - allowed to avoid the influence of the reproductive cycle ferent types of prey, but the tag could not distinguish (Spring and beginning of Summer). All Lusitanian toad- them. Moreover, although the behaviour is identified fish were captured and released in Mira estuary within and registered as an attack, the predation’s success rate range of the VR2W array. After capturing, fish were is unknown [5]. immediately tagged with 9-mm versions of the AccelTag The Acceltag detects and counts events for hourly peri - with approximately 1  month of battery life and released ods, after which the data are acoustically transmitted at the capture site. through two consecutive S256 codes and recorded by an acoustic receiver array. The tag could report 0–6 events Data analysis correctly, but if the number of events was 7 or more, the The success rate of transmissions detected by the acoustic number 7 was logged. More than 7 events in one hour receivers array was calculated by dividing the number of were not very likely to happen with this species [23]. The transmissions received by the total number of transmis- AccelTag also comprises an activity meter programmed sions theoretically emitted by the tag. This was only cal - and tested according to Lusitanian toadfish movements culated for the duration of the study period during which that measure the percentage of time the fish are moving. tagged specimen maintained position within range of the The activity data is transmitted as percentage intervals acoustic receiver array. The influence of environmen - (Table 1). tal factors on the activity and behaviour of toadfish was Prior to the field study, a 13-mm AccelTag with the analysed using a factorial ANOVA. The analysed envi - latest version of the “signature” detection software was ronmental factors were tidal stage (spring vs neap), tidal externally implanted in 4 toadfish and tested for accuracy cycle (high vs low) and time of day (day vs night). Also, in a 900-L sand bottom covered trial tank using an iden- the influence of the time of the year was studied com - tical experimental protocol as previously described [5]. paring the differences between Group 1 (summer) and After satisfactory results were obtained, 9-mm AccelTags Pereira et al. Anim Biotelemetry (2021) 9:10 Page 4 of 9 Group 2 (autumn). This procedure allowed to assess each Considering the activity and the number of events factor’s influence or, as an interaction of two or more fac - observed during distinct environmental conditions, tors. The data used in the analysis were expressed as the tidal stage (TS: spring vs neap) and time of day (TD: day total number of events per fish and hour for each behav - vs night) were the most influencing factors (Tables  2, ioural signature. Activity data was converted from per- 3). In fact, tagged Lusitanian toadfish were more active centage to time units (minutes), and the lower limit of and performed significantly more burrowing and re- the activity interval per hour and per fish was used for burrowing movements during spring tides. However, the the analysis. As an example, if the data showed an activity TS did not influence the number of attacks significantly interval of 3 (5%)–3.6 (5.99%) minutes, it was used 3 min (Tables 2, 3). Regarding the influence of time of day, Lusi - of activity for the analysis. Spring tides were defined as tanian toadfish were more active and performed signifi - tides with an amplitude of over 3.2  m and neap tides as cantly more attacks during night-time (Tables 2, 3). tides of amplitude less than 2 m. For tidal cycle analysis, it When evaluating differences in behaviour poten - was considered the transmissions detected 2 h before and tially associated with seasonality, the number of attacks 2  h after low and high tidal peaks. Night-time included and activity revealed no statistical differences between dusk and day-time included dawn. In order to obtain the groups/seasons. However, Group 1 composed by fish most accurate data possible, codes from the first 2 days tracked during the summer performed significantly more and the last day of transmissions were removed from the burrowings and re-burrowings than Group 2 composed analysis [5]. by fish tracked in autumn (Tables 2, 3). Even though tidal cycle (TC: high vs low) alone did not Results significantly influence the behaviour and activity of the Before the field study, the tag and detection software Lusitanian toadfish, factorial ANOVA showed a signifi - were tested for accuracy on four specimens in a labora- cant interaction between this factor and the TD regard- tory trial. Tests resulted in 100% efficiency for detect - ing the number of attacks and fish activity (Table  3). The ing activity, burrowing and re-burrowing movements. analyses of Tables  2 and 3 show that toadfish performed Attacks towards potential prey were registered with 85% more attacks and were more active during high tides that accuracy, increasing 25% when compared with the previ- occurred during night-time. The TS also significantly ous algorithm developed by [5]. influenced toadfish behaviour when interacting with TD. Regarding the field study, of the 24 Lusitanian toad - Indeed, it was during the night-time of spring tides when fish tagged and released in the Mira estuary, only three toadfish were substantially more active (Tables  2, 3). Sig- specimens spent most of the time out of the range of nificant interactions were also found between-group and the acoustic receiver array. The remaining specimens TS, and between-group and TD. During the summer returned to the capture sites within 2 days and remained (Group 1) Lusitanian toadfish were more active and per - most of the time inside a perimeter of 200 m. formed more burrowing and re-burrowing movements A total of 3530 (39.5% of the transmissions) complete during spring tides, along with more attacks during the codes from Group 1 and 3719 (41.7%) from Group 2 were night-time. successfully received, stored, and downloaded from the acoustic telemetry array. Group 1 performed 960 poten- Discussion tial attacks, 202 burrowings and 282 re-burrowings, and The results from this study were obtained using an inno - showed 1.51 min (2.5% of the time) per hour of minimum vative technological approach, the AccelTag, developed mean activity. Group 2 conducted 665 potential attacks, and previously tested in controlled laboratory condi- 120 burrowings and 142 re-burrowings, and had a mini- tions [5]. In the present work, it was used for the first mum mean activity of 1.52 min per h (2.5% of the time). time to obtain in  situ detailed foraging behaviour data By plotting the frequency of each studied behaviour of an aquatic animal. AccelTag proved to be a power- and the percentage of activity against tidal amplitude, ful tool to assess and monitor the fine-scale behaviour it was possible to observe that the frequency of attacks, of a resident estuarine fish. In terms of ecological data burrowing and re-burrowing movements varied along obtained with AccelTag, the main findings are concord - the studied period but without an obvious relation with ant with results obtained with other works that used dis- tidal stage per se (Figs.  2 and 3). Regarding activity pat- tinct methodological approaches to study the Lusitanian terns, Lusitanian toadfish from Group 1 tracked in the toadfish foraging behaviour [21–24]. When comparing summer were more active during spring tides, whereas to other available tools (see [5] for further discussion) fish from Group 2 tracked in autumn did not reveal a such as data storage tags with accelerometer sensors [6, marked activity pattern throughout the study period 7], and even more recent acoustic transmitters equipped (Figs. 2 and 3). with three-axis accelerometer sensors [8–11, 25, 26], the P ereira et al. Anim Biotelemetry (2021) 9:10 Page 5 of 9 Fig. 2 Graphic representation of the studied behaviours as a function of the tidal stage (spring or neap tide) and time of day (day or night) for the toadfish of Group 1 tracked during August–September 2010 AccelTag has the advantage of being able to process the the software accordingly to distinct behaviours, and then fine-scale acceleration information autonomously and implement in situ behaviour studies. acoustically transmit the correspondent behaviour. Sev- With regard to the foraging ecology of the Lusitanian eral authors have identified advantages of data processing toadfish, tides and circadian cycle, together with the time and compression, e.g., increased tag autonomy, reduced of year, seem to play an essential role in the behaviour storage requirements and reduced data analysis time [11, of this species. Notwithstanding being capable of swim- 27]. Moreover, the work previously developed [5], com- ming over relatively large distances [22, 23], specimens bined with the present study corresponds to the antici- typically do not perform significant displacements and pated studies and technological enhancements proposed remain most of the time inactive (97.5% of the time in [11], namely the tagging of captive specimens to calibrate the present study), buried in the sediment or concealed Pereira et al. Anim Biotelemetry (2021) 9:10 Page 6 of 9 Fig. 3 Graphic representation of the studied behaviours as a function of the tidal stage (spring or neap tide) and time of day (day or night) for the toadfish of Group 2 tracked during October–November 2010 in rocky crevices. In fact, the majority of the specimens Tidal stage influenced toadfish behaviour and activ - remained within the study area for almost the entire ity in larger cycles of time. During spring tides of higher study period, some of them returning to the capture site amplitudes, the activity increased and the number of after being tagged and released. However, this sedentary potential attacks diminished. This pattern may be related behaviour was amplified by the time of the year when to strong water currents associated with this period that the study occurred. Moreover, this species is more active force toadfish to actively avoid being dragged away and, during the spawning season, which occurs in late spring consequently, reduce feeding activity. After this period and early summer [17, 18], whereas this study was per- of reduced feeding attempts, during neap tides, attacks formed in late summer and mid-autumn when the speci- considerably increase and activity level decreases. Vari- mens tend to reduce global activity and decrease the ations on tidal stages also explain the marked pattern number of long displacements [22]. of burrowing and re-burrowing movements. These are P ereira et al. Anim Biotelemetry (2021) 9:10 Page 7 of 9 Table 2 Mean number of events and time of activity of the tagged toadfish according to environmental factors Attack Burrowing Re-burrowing Activity N Mean SD N Mean SD N Mean SD Minute Mean SD Group 1 ST 362 0.27 0.73 162 0.12 0.47 204 0.15 0.61 2708.4 2.00 4.29 NT 598 0.27 0.66 40 0.02 0.14 78 0.04 0.25 2631.9 1.21 1.78 LT 493 0.27 0.69 88 0.05 0.27 140 0.08 0.42 2564.1 1.44 2.54 HT 467 0.27 0.68 114 0.06 0.34 142 0.08 0.45 2776.2 1.58 3.44 Da 201 0.13 0.45 98 0.06 0.29 118 0.08 0.41 1264.8 0.79 1.55 Ni 759 0.40 0.81 104 0.05 0.33 164 0.09 0.45 4074.5 0.11 3.73 Group 2 ST 143 0.17 0.49 38 0.05 0.32 45 0.05 0.34 1089.6 1.31 2.09 NT 522 0.18 0.54 82 0.03 0.25 97 0.03 0.25 4594.2 1.59 2.85 LT 267 0.15 0.45 50 0.03 0.28 60 0.03 0.25 2810.7 1.56 3.05 HT 398 0.21 0.59 70 0.04 0.25 82 0.04 0.29 2873.1 1.50 2.32 Da 190 0.11 0.41 51 0.03 0.19 74 0.04 0.24 1764.9 1.04 2.02 Ni 475 0.24 0.60 69 0.03 0.32 68 0.03 0.29 3918.9 1.94 3.10 Total ST 505 0.22 0.61 200 0.09 0.40 249 0.10 0.48 3798.0 1.66 3.19 NT 1120 0.23 0.60 122 0.03 0.20 175 0.05 0.25 7226.1 1.40 2.32 LT 760 0.21 0.57 138 0.04 0.28 200 0.06 0.34 5374.8 1.50 2.80 HT 865 0.24 0.64 184 0.05 0.30 224 0.06 0.37 4649.3 1.54 2.88 Da 391 0.12 0.43 139 0.05 0.24 192 0.06 0.33 3029.7 0.92 1.79 Ni 1234 0.32 0.71 143 0.04 0.33 232 0.06 0.37 7993.4 1.03 3.42 N number of events (attacks, burrowings and re-burrowings) and mean time of activity (minutes) per hour, SD standard deviation, ST spring tides, NT neap tide, LT low tide, HT high tide, Da day, Ni night Table 3 Factorial ANOVA results to  assess the  influence of  environmental factors on  the  activity and  behaviour of the tagged toadfish Factorial ANOVA Attacks Burrowing Re-burrowing Activity Global F = 18.883; d.f. = 15; p < 0.01 F = 9.864; d.f. = 15; p < 0.01 F = 8.370; d.f. = 15; p < 0.01 F = 29.517; d.f. = 15; p < 0.01 TS F = 0.003; d.f. = 1; p = 0.958 F = 61.611; d.f. = 1; p < 0.01 F = 49.191; d.f. = 1; p < 0.01 F = 13.832; d.f. = 1; p < 0.01 TC F = 1.921; d.f. = 1; p = 0.166 F = 1.506; d.f. = 1; p = 0.220 F = 0.583; d.f. = 1; p = 0.445 F = 2.903; d.f. = 1; p = 0.09 TD F = 138.887; d.f. = 1; p < 0.01 F = 0.000; d.f. = 1; p = 0.993 F = 0.195; d.f. = 1; p = 0.658 F = 248.599; d.f. = 1; p < 0.01 G F = 31.572; d.f. = 1; p = 0.05 F = 20.140; d.f. = 1; p < 0.01 F = 27.775; d.f. = 1; p < 0.01 F = 3.744; d.f. = 1; p = 0.05 TS * TC F = 0.042; d.f. = 1; p = 0.838 F = 1.875; d.f. = 1; p = 0.171 F = 0.176; d.f. = 1; p = 0.675 F = 7.131; d.f. = 1; p = 0.08 TS * TD F = 2.657; d.f. = 1; p = 0.103 F = 0.040; d.f. = 1; p = 0.842 F = 1.228; d.f. = 1; p = 0.268 F = 5.539; d.f. = 1; p < 0.05 TS * G F = 0.051; d.f. = 1; p = 0.822 F = 33.601; d.f. = 1; p < 0.01 F = 25.382; d.f. = 1; p < 0.01 F = 53.695; d.f. = 1; p < 0.01 TC * TD F = 4.216; d.f. = 1; p < 0.05 F = 0.103; d.f. = 1; p = 0.748 F = 0.953; d.f. = 1; p = 0.329 F = 12.149; d.f. = 1; p < 0.01 TC * G F = 2.730; d.f. = 1; p = 0.10 F = 0.267; d.f. = 1; p = 0.605 F = 0.465; d.f. = 1; p = 0.495 F = 1.325; d.f. = 1; p = 0.250 G * TD F = 21.913; d.f. = 1; p < 0.01 F = 0.708; d.f. = 1; p = 0.400 F = 2.234; d.f. = 1; p = 0.135 F = 15.885; d.f. = 1; p < 0.01 TS tidal stage, TC tidal cycle, TD time of day, G group Significant differences for p < 0.01 and p < 0.05. more frequent during spring tides, when toadfish need On the other hand, the tidal cycle only influenced toad - to refuge (i.e., remain buried) to avoid being displaced by fish behaviour and activity in interaction with the time strong water currents, and decrease during neap tides. of day. Indeed, the number of attacks and activity were influenced synergistically by those two factors. Toadfish Pereira et al. Anim Biotelemetry (2021) 9:10 Page 8 of 9 were more active during night-time, confirming previ - the Lusitanian toadfish, i.e., resident species with low ous findings in the same estuary [22, 23]. The nocturnal activity levels and behaviours with a distinct three- period is the preferred for engaging feeding activities as axis acceleration signature. Higher activity levels and their prey are also more active. Subsequently, the number attacks displayed by the Lusitanian toadfish during of attacks also increased during the night period. Addi- the night, at high tide periods and during Spring tides tionally, high tide phases considerably improve visibility are considered to be associated with increased activity in the lower Mira Estuary due to the input of more trans- and vulnerability of its prey during these periods. The parent water from the ocean. As previously observed in potentialities of this technology to study aquatic organ- laboratory experiments [5], toadfish is a visual predator isms behaviour are far from being fully explored with attacking its prey mostly based on movement. Therefore, this study. More precise and complete signature detec- the combination of high tide with night-time results in a tion algorithms, together with longer battery life could favourable period for toadfish to feed. As highlighted by offer new possibilities of behavioural studies on the [23] these higher activity periods displayed by the Lusi- Lusitanian toadfish and other fish species. In the future, tanian toadfish are not independent of the activity of it would be interesting to discern between success- its prey, most of them displaying higher activity or vul- ful and unsuccessful attacks or even the type of prey, nerability to predation during the night and at high tide once toadfish may attack and handle distinct preys periods. differently. The influence of the time of year was evident in the dif - Acknowledgements ferences between the two groups of toadfish tagged. The The present study was carried under the project “AccelTag—Development of first group of toadfish was tagged and tested in late sum - an acoustic three-axis accelerometer transmitter for marine species” funded by European Union EUREKA Eurostars Programme and project “COASTNET— mer, close to the end of the spawning season. Moreover, Portuguese Coastal Monitoring Network (PINFRA/22128/2016)” funded by the year of 2010 presented a relatively rainy and cold European Regional Development Fund (FEDER), through LISBOA2020 and spring, which delayed the spawning season of this spe- ALENTEJO2020 regional operational programs, in the framework of the National Roadmap of Research Infrastructures of strategic relevance. cies, which is highly influenced by water temperature [22]. Therefore, global activity is relatively high at the Authors’ contributions beginning of the study, gradually reducing in the follow- PRA, BRQ, AG and JLC conceived and designed the project. TJP and BRQ led the field work. Data analysis was conducted by TJP with help from JLC, PRA ing 12  days. During this period, the tagged toadfish also and BRQ. All authors (JLC, PRA, BRQ, AG, MJC, JPM and JLC) contributed to the performed more attacks, as it is expected at the end of research and writing of the manuscript. All authors read and approved the the reproductive period [22]. Concerning the second final manuscript. group of toadfish, it was monitored in mid-autumn, far Funding from the spawning season and closer to the winter. This Research was funded by European Union EUREKA Eurostars Programme. period corresponds to the time of year when this species Availability of data and materials is less active [22]. This discrepancy between the times of The datasets used and analysed during the current study are available from the year in which the two groups were monitored may the corresponding author on reasonable request. explain detected differences in burrowing and re-burrow - Ethics approval and consent to participate ing movements and activity levels, with toadfish tracked This study was carried out in strict accordance with the recommendations in summer performing more of these behaviours and present in the Guide for the Care and Use of Laboratory Animals of the toadfish tracked in autumn being globally more active. European Union—in Portugal represented by the Decree-Law No. 129/92, Portaria No. 1005/92. Approval by a named review board institution or ethics However, the number of attacks did not significantly dif - committee was not necessary as the final model for ethical experimentation fer between seasons, which may suggest that the higher using fish as biological models was not implemented in Portuguese research activity observed with the toadfish tracked in autumn units at the time of experimentation. may be related to the search for shelters instead of food. Consent for publication Therefore, both groups were influenced by tide and time Not applicable. of day, but differences between groups are probably Competing interests related to the species circannual lifecycle. The authors declare that they have no competing interests. Author details Conclusions MARE-Centro de Ciências do Mar e do Ambiente, Faculdade de Ciências da The behavioural signature capture version of the Accel - Universidade de Lisboa, Campo Grande, 1749-016 Lisbon, Portugal. Depar- tamento de Biologia, Escola de Ciências e Tecnologia, Universidade de Évora, Tag was tested for the first time in  situ to monitor the Évora, Portugal. Departamento de Biologia Animal, Faculdade de Ciências da fine-scale behaviour of aquatic animals. This tech - Universidade de Lisboa, Lisboa, Portugal. Thelma Biotel, Sluppen, Trondheim, nology proved to be particularly suited for fish spe - Norway. cies with biological and ecological features similar to P ereira et al. Anim Biotelemetry (2021) 9:10 Page 9 of 9 Received: 17 September 2020 Accepted: 27 January 2021 15. Roux C. Batrachoididae. In: Fischer W, Bianchi G, Scott WB, editors. Fiches FAO d’identification des espèces pour les besoins de la pêche. Atlantique centreest: zones de pêche 34, 47 (en partie). Vol. I. Canada Fonds de Dépôt, Ottawa, 1981. 16. Muzavor S, Arruda LM, Andrade JP. Roteiro ecológico da Ria Formosa. vol. 2, Peixes. Foco Editora 1993. References 17. Costa JL, Silva G, Almeida PR, Costa MJ. 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Distribution and abundance of the Lusitanian toadfish Springer Nature remains neutral with regard to jurisdictional claims in pub- Halobatrachus didactylus (Bloch & Schneider, 1801) in Portugal with some lished maps and institutional affiliations. remarks on its population fragmentation. Rev Biol. 2002;20:155–67. Re Read ady y to to submit y submit your our re researc search h ? Choose BMC and benefit fr ? Choose BMC and benefit from om: : fast, convenient online submission thorough peer review by experienced researchers in your field rapid publication on acceptance support for research data, including large and complex data types • gold Open Access which fosters wider collaboration and increased citations maximum visibility for your research: over 100M website views per year At BMC, research is always in progress. Learn more biomedcentral.com/submissions

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