Bioadhesive interface for marine sensors on diverse soft fragile species

Domain: earth_science
Published: 2024-04-16
Editorial outcome: minor_revision

Abstract
Marine animals equipped with sensors provide vital information for understanding their ecophysiology and collect oceanographic data on climate change and for resource management. Existing methods for attaching sensors to marine animals mostly rely on invasive physical anchors, suction cups, and rigid glues. These methods can suffer from limitations, particularly for adhering to soft fragile marine species such as squid and jellyfish, including slow complex operations, unreliable fixation, tissue trauma, and behavior changes of the animals. However, soft fragile marine species constitute a significant portion of ocean biomass (>38.3 teragrams of carbon) and global commercial fisheries. Here we introduce a soft hydrogel-based bioadhesive interface for marine sensors that can provide rapid (time < 22 s), robust (interfacial toughness > 160 J m−2), and non-invasive adhesion on various marine animals. Reliable and rapid adhesion enables large-scale, multi-animal sensor deployments to study biomechanics, collective behaviors, interspecific interactions, and concurrent multi-species activity. These findings provide a promising method to expand a burgeoning research field of marine biosensing from large marine mammals and fishes to small, soft, and fragile marine animals.

Introduction
Marine animal-borne sensors serve as an autonomous platform to study movements and behaviors (i.e., predator-prey interactions, habitat, and migration) of marine animals, as well as to collect oceanographic data (i.e., light, temperature, salinity, and oxygen) over large spatial and temporal scales1–4. These data have provided vital insights for understanding marine ecosystems5 and aided the effective management of fisheries6. Electronics sensors such as biotelemetry tags that transmit data to satellites and biologging tags that store data internally have been attached to robust marine vertebrates7 (e.g., marine mammals, seabirds, reptiles, and large fishes) via subcutaneous anchors, suction cups, and/or rigid glues. However, these sizeable and rigid sensors are not applicable for attaching to more fragile marine organisms that may be small or have soft outer protective layers. These marine organisms include many invertebrates such as squid and jellyfish and many small fishes. Soft-bodied marine organisms are highly diverse, abundant (>38.3 teragrams of carbon8), and pervasive in all ocean habitats, as well as provide a key protein source for humans worldwide9 and sequester greenhouse gasses into the deep ocean10. While advances in miniaturized biologging tags show the potential to monitor movements and behaviors of individual small invertebrate animals with high temporal resolution11, physically anchoring or gluing biologging tags on soft, fragile species is invasive, slow, or difficult to properly attach4. Further, the resultant tissue trauma on the epidermal and muscular layers can disturb animal behaviors, have ethical challenges, and even lead to diseases and mortality in some soft-bodied animals12. These challenges hinder the wider use of electronic sensors to study social behaviors, distributions, and interactions of soft, fragile marine species.

Here, we report a bioadhesive interface for marine sensors (BIMS) to achieve rapid non-invasive integration (Fig. 1b) on soft fragile marine species including mollusca (squid, Doryteuthis pealeii) and cnidaria (jellyfish, Aurelia aurita). The BIMS contains a thin layer of a dried-hydrogel adhesive interface that can absorb the seawater from the surface of marine species by hydration and swelling, subsequently adhering to sensors on diverse marine species within 22 s. After adhering to the surface of marine species, the adhesive interface of the BIMS becomes a soft yet robust hydrogel. Owing to its fast non-invasive integration and matched mechanical properties with marine species, the BIMS does not disturb normal animal behaviors upon release and enables a wide suite of eco-physiological measurements and comparisons of the animals. We further demonstrate the BIMS applicability to phylogenetically and morphologically distinct species, including actinopterygii (ray-finned fishes, Salmo salar, Paralichthys dentatus), chondrichthyes (skate, Leucoraja erinacea), and crustacea (lobster, Homarus americanus). The rapid adhesion across species further enables multi-joint and multi-animal sensor deployments to study in situ group behaviors, motion dynamics, and interactions between species.

Results
Design and mechanism of the BIMS
A thin dried-hydrogel adhesive interface (150 µm thickness) on the bottom of the BIMS enabled the rapid and non-invasive attachment of biologging sensors with marine species. This interface consisted of two interpenetrating polymer networks, which are physically crosslinked poly(vinyl alcohol) (PVA) and covalently crosslinked poly(acrylic acid) grafted with N-hydroxysuccinimide ester (PAA-NHS ester) (Fig. 1c). The adhesive interface in the dry state quickly absorbs interfacial water upon contact with marine species due to its hydrophilicity and hygroscopicity13–15. Carboxylic acid groups in the PAA-NHS ester form rapid adhesion through physical crosslinks (e.g., such as hydrogen bonds and electrostatic interactions), and subsequent covalent amide bonds between NHS-ester groups and primary amine groups on the marine animal tissue16 ensured stable adhesion over time. The swollen adhesive interface also showed softness (Young’s modulus of 250 kPa), high stretchability (over 5), and mechanical robustness (fracture toughness of over 1100 J m−2), allowing conformable and imperceptible adhesion on curved tissue surfaces (Supplementary Fig. 1). Through surface chemical treatments, the adhesive interface can be easily coupled to a variety of soft engineering solids (i.e., silicone and urethanes), which can be used as an intermediate layer or an encapsulant for embedding sensors regardless of their material composition17,18 (Supplementary Fig. 2).

To demonstrate the simplicity and quickness of the BIMS application compared to the current methods, we first used squid as a representative model to quantitatively evaluate the total time spent out of the water for tagging animals. The entire application process of the BIMS required an average of 22.3 s (n = 10), which is substantially faster than surgical suturing (8.5 min on average) based on the previously reported results19 (Fig. 1d). Moreover, the simple and rapid application process improves animal welfare and reduces stress on both the operators and the tagged animals. For example, tagging squid via complex and time-consuming surgical suturing requires stress-reducing measures such as covering the eyes20 and constant ventilation of seawater into the mantle cavity21 (Fig. 1a). Marine animals can incur significant physiological and metabolic stress during the tagging process, and behavior disruption can persist for numerous hours or even lead to mortality22. In contrast, the BIMS eliminated the need for ventilation and mitigating measures for prolonged air exposure and allowed all tag procedures to be completed by one person (Fig. 1e and Supplementary Movie 1).

Adhesion performance
To evaluate adhesion performance of the BIMS across multiple marine animals, we first conducted three mechanical tests on ex vivo marine animal tissues, measuring the interfacial toughness, the shear strength, and the tensile strength (according to the following testing standards for tissue adhesives: ASTM F2256 for 90-degree peel tests, ASTM F2255 for lap-shear tests, and ASTM F2258 for tensile tests) (Fig. 2a–c and Supplementary Fig. 3). The adhesive interface of the BIMS formed a rapid and robust bond to various wet tissues with a high interfacial toughness (>160 J m−2 for squid, >130 J m−2 for salmon, >70 J m−2 for skate, and >70 J m−2 for flounder), shear strength (>40 kPa for squid, >40 kPa for salmon, >80 kPa for skate, and >70 kPa for flounder), and tensile strength (>60 kPa for squid, >30 kPa for salmon, >130 kPa for skate, and >70 kPa for flounder). Adhesion stability and swelling behavior were further tested ex-vivo on squid tissue over a 24-hour period and at a wider range of temperatures found in the ocean (4 °C, 20 °C, and 30 °C). The lap shear strength was measured on squid tissue samples after 30 min, 1 h, and 24 h of adhesion. Shear strength on squid decreased an average of 15.6% in 24 h across the three temperatures. Notably, the shear strength was overall higher at 4 °C, likely due to the lower swelling ratio of 1.2 at 4 °C (Supplementary Fig. 4). Note that shear and tensile strength testing led to tissue failures instead of interfacial failures for squid, flounder, and salmon, shown by the detachment of the skin or scales (Supplementary Fig. 5).

For soft and fragile species, tagged sensors should conform with the organism’s body shape. Rigid non-conformal sensors may induce epidermal lesions, which may further cause unmitigated bleeding, bacterial infection, and rapid mortality12. In addition, epidermal lesions could lead to poor data quality due to partially or fully displaced sensors. To evaluate adhesion robustness and non-invasiveness under cyclic body deformations, we applied the BIMS on fresh squid cadavers, and simulated animal respiration and movement by expanding and contracting the mantle cavity via pressurized air inputs in seawater. After 40 cycles of loading and unloading (Fig. 2d–h), the dermal layer around the BIMS application site remained intact with no visible tears or deformations. The elasticity of the swollen adhesive interface provided a medium for energy dissipation between the fragile skin and the rigid sensor as the skin stretches and contracts. Without this energy dissipation, the area immediately around the application site may suffer from stress or fracture, as may be the case with rigid glues such as cyanoacrylates. Therefore, the BIMS minimized potential tearing of surrounding tissue on animals that undergo body deformations while swimming such as squid, which expand their mantle cavity by roughly 41% when jetting23.

Rapid tagging and post-release behavior of live marine species
To assess the potential behavioral disruption by the BIMS, we measured the time taken for tagged squid to return to normal schooling behaviors with untagged animals (i.e., synchronized, directionally polarized groups). Upon release, squid were active and quickly swam towards untagged squid and began schooling (<20 s, n = 5) (Fig. 1e), demonstrating a rapid return to baseline individual and group-level behaviors. Natural, high-speed jet propulsion movements did not lead to adhesion failure, verifying strong resistance to dynamic loads while accelerating (Supplementary Movie 2). Importantly, untagged squid readily synchronized and schooled with the tagged squid without aggressive behaviors aimed toward focal squid, demonstrating that group-level behaviors were not impacted by the BIMS. In contrast, squid tagged via suturing typically need to recover in hyper-aerated coolers for fifteen minutes prior to reintroduction to conspecifics19. Without acclimation in coolers, squid are often lethargic and rest on the bottom for several minutes, which may increase individuals’ susceptibility to predation in the wild.

Tag attachment mechanisms and methods are often species-specific. Such specialization has traditionally hampered method or tool scalability, broad applications to monitor multiple species concurrently, and greatly increases the training time and cost required to affix sensors. In contrast with existing species-specific methods, the simple and rapid features of the BIMS enabled instant tagging across multiple live marine species, including squid, jellyfish, skate, lobster, black sea bass (Centropristis striata), sea robin (Prionotus evolans), and flounder (Fig. 2i, j and Supplementary Fig. 6). We further evaluated the stability of the BIMS in a large tank (8 m in length, 2 m in width, and 0.75 m in depth). Due to the soft and robust characteristics of the adhesive interface, the BIMS can be reliably integrated with fragile aquatic animals, such as squid and jellyfish, for up to 3 days, allowing long-term animal behavior monitoring (Fig. 2k). All tags on live animals were left to fall off on their own, no tags were forcibly removed from live animals. After sensor detachment, individuals exhibited natural behaviors (i.e., schooling) and survived just as long as untagged animals in the experimental environment.

To highlight the rapid and reliable deployment of the BIMS, multiple sensors were adhered across a single animal. Four sensors (L, C, R1, R2) (Supplementary Fig. 7) were placed 100 mm from the anterior tip of an adult male skate. Sensors were spaced by 15 mm from L to R2, where L was placed on the left pectoral fin, C was placed at the centerline, and R1 and R2 divide the right pectoral fin. Surge acceleration for each point was directly measured while the skate swam in a flow tank (1.7 m in length, 0.5 m in width, and 0.6 m in depth) at a constant rate of 20 cm s−1. As expected, due to symmetry, the acceleration signal from L and R1 are nearly identical, however, acceleration amplitude increased at R2. To expand on this, acceleration amplitude was plotted as a function of distance from the center (Supplementary Fig. 7) and fit with an exponential regression to map acceleration across the wing. While developing a full kinematic model is beyond the scope of this work, we show that the BIMS could aid kinematic studies, which currently rely on mathematical models, expensive computational models, and video motion analysis24–26.

BIMS functionality across species
To evaluate the robustness of the BIMS across diverse marine species and study the individual and inter-specific interactions via a series of sensors, we conducted a large-scale multi-species biologging experiment in a large 318,000-liter seawater aquaria (9 m diameter, 5 m height). The consistent application technique regardless of species facilitated tagging of a total of ten animals of four species within 25 min. At the individual level, we monitored ecologically important movement behaviors of squid (Fig. 3a, b), jellyfish (Fig. 3c, d), skate (Fig. 3e, f) and kelp (Supplementary Fig. 8) through three-dimensional acceleration and orientation via the BIMS. The individual data allowed us to identify the representative movement behaviors of specific animals21,27, such as bi-directional swimming in squid, jet propulsion in jellyfish (Fig. 3a–d), and finning rates for squid (1.75 Hz) and skate (2.54 Hz) (Fig. 3a, e). The close contact between sensors and marine animals ensured high data quality and allowed for extracting detailed local motion patterns from diverse animals and movements.

Intraspecific aggregations and coordinated movements are widely observed behaviors across many evolutionary lineages28,29. In many marine species, grouping decreases predation risk30, enables more effective navigation31, and lessens metabolic demands32. Yet, group-level behaviors are rarely measured in situ due to the difficulty of monitoring multiple animals concurrently. Without any behavior disruption of either the focal or untagged animals within the groups for different marine animals (Fig. 4b–d), the BIMS played a pivotal role in collecting schooling data using an animal-borne sensor. The enhanced resolution in the BIMS relative to video analysis revealed the dynamics of coordinated schooling behavior and its evolution through a disruption (Fig. 4e–g). Squid preferentially organized into a highly structured school and individuals oriented mantle-first into the current, leading to strong alignment in both heading and pitch (Supplementary Movie 3). While squid schooled, an interspecific interaction was recorded via the BIMS, leading to decreased coordination demonstrated through increased orientation variance (Fig. 4g).

Community-level assessments of movement are poorly understood yet vital to measure energy flow and interactions within ocean habitats. To quantify and compare species movements (Fig. 4h), we calculated overall dynamic body acceleration (ODBA), which is an effective proxy for activity levels and energy expenditure (Halsey et al., 2009) (Fig. 4g). The BIMS reliability across species facilitated concurrent assessment of movement strategies across multiple (>3) marine species and trophic levels. We found that ODBA levels showed a clear distinction between species with varying movement strategies. Flounder, a sit-and-wait ambush hunter, was largely sedentary and had the lowest average ODBA (0.032 g). The skate and lobster are more mobile benthic species, and their ODBA levels were greater and similar at 0.049 g and 0.052 g, respectively. Lastly, squid, which are muscular active pelagic swimmers, had the highest ODBA values (0.067 g). Such concurrent movement data across species could be calibrated and serve to measure energy flow, biotic interactions, and environmental constraints in dynamic marine communities, particularly in the context of the immense anthropogenic pressures arising from our changing oceans.

BIMS in the field
To further evaluate the efficacy of the BIMS in the field, an ITAG sensor was used with the BIMS, which was adhered on a free-ranging veined squid (Loligo forbesii) in the Azores Islands, Portugal (Fig. 5). Similar to our lab tests, we first removed excess interfacial water using a soft cloth (Fig. 5a). Next, the ITAG was gently pressed onto the squid mantle near the posterior mantle tip. Lastly, we took morphometric measurements and placed the animal immediately back into the water. The entire process was completed within 90 seconds (Supplementary Movie 4). The tagging procedure manifested a 466% enhancement in efficiency compared to traditional suturing methods19. For this field experiment, the adhesive was prepared in the lab and hand-carried to the Azores in bags filled with desiccant. The adhesive was kept protected from water and as dry as possible until use.

Upon release, the squid actively descended to a depth of 288 meters at an average rate of 35 cm s−1 (Fig. 5b). During its descent, it sampled vertical oceanographic gradients, including temperature (Fig. 5c) and luminance of different light wavelengths (Fig. 5d). In addition, inertial measurement unit (IMU) sensors measured the movement dynamics and swimming behaviors while the squid was migrating downward. The squid showed natural swimming behaviors, alternating between periods of low (Fig. 5e, f) and high (Fig. 5g, h) intensity jet propulsion movements. Notably, the high intensity jet propulsion for this species averages 0.70 m/s21 highlighting the robust adhesion capabilities of the BIMS, which can withstand drag induced by mobile species. The tag was released from the animal via a galvanic release system, effectively separating it from its base. Subsequently, it was tracked and recovered through a radio signal output. In this pilot field study, the length of deployment was limited by the timed release mechanism. Notably, the sensor retrieval without its base suggests that the base likely remained attached to the squid via the BIMS at the time of tag release. Based on observations from previous seawater tank experiments, we anticipate the BIMS to remain attached to a squid for a period ranging from 1 to 3 days before detaching on its own. This preliminary trial demonstrated that the BIMS can be suturelessly attached to monitor highly mobile free-ranging species that undergo rapid pressure changes in the field.

Outlook
Despite the impressive miniaturization of marine sensors, flexible attachment technologies have proven challenging4. This study reports a universal platform to rapidly and non-invasively affix sensors on live marine species for studying individual, group, and multi-species behaviors beyond existing tag attachment mechanisms. We demonstrated its efficacy in a large-scale multi-species biologging experiment. The rapid and robust adhesive capability of the BIMS minimized the tagging effort and the need for training in species-specific tagging methods. The non-invasive integration with marine species avoided behavioral disruption for either the focal or untagged animals, facilitating the collection of high-quality data. The approach also offers a promising avenue to expand the burgeoning field of marine animal sensing to small and soft-bodied invertebrates (e.g., squid, jellyfish). While we demonstrated that the BIMS is an effective tool for monitoring diverse marine species, future visions can integrate more sophisticated acoustic or optical sensors33. Additionally, the BIMS may function as a drug delivery or wound protection device34,35 for real-time therapies of injured or sick marine animals. Lastly, the BIMS may create sensor networks throughout the body of a single marine animal for locomotion kinematic studies, which could provide insight to improve the design and control of bio-inspired marine robots36–40.

Methods
Materials
All chemicals were purchased from Sigma-Aldrich and used without further purification unless otherwise mentioned. To synthesize the hydrogel adhesive, acrylic acid (AAc), PVA (Mw = 146,000 to 186,000, 99+% hydrolyzed), α-ketoglutaric acid, N,N’-bis(acryloyl)cystamine and N-acryloxysuccinimide (AAc-NHS) (VWR) were used. To prepare the silicone-encapsulated sensor device, Ecoflex 020 (Smooth-On) and benzophenone were used. To attach the adhesive to the 3D-printed urethane base, hydrophilic polyurethane (PU) (HydroMed D3, AdvanSource Biomaterials) was used.

Preparation of the adhesive interface
To prepare the stock solution for the adhesive, 35 w/w% AAc, 7 w/w% PVA, 0.2 w/w% α-ketoglutaric acid, and 0.05 w/w% N,N’-bis(acryloyl)cystamine was added to a bottle of nitrogen purged deionized water equipped with a stirrer. The stock solution was stirred in a 90 °C water bath until completely dissolved. Once dissolved, this stock solution may be stored in a cool dry place in a UV-resistant glass bottle until use. To polymerize the stock solution and bolster its adhesive properties, 30 mg of AAc-NHS was dissolved for every 1 ml of the stock solution and then degassed to remove air bubbles. To make a thin, tape-like adhesive, two rectangular glass plates were treated with a hydrophobic coating (Rain-X) to allow for easier removal, and equipped with 150 µm spacers. The hydrogel precursor was then poured onto the glass mold between the spacers, clamped to form a seal, and cured in a UV chamber (365 nm, 10 W power) for 30 minutes. Care was taken to properly degass and seal the sample while in the UV chamber, failure to do this could inhibit polymerization. To reduce swelling during use, the hydrogel adhesive was stretched to a length and width equal to its equilibrium swelling ratio at room temperature of approximately 1.5, as shown in Supplementary Fig. 4, held with clamps and dried under continuous air flow for at least 3 h. While pre-stretching is not a requirement for the adhesive to work on tissues, it expedites drying and results in a more pliable film. The dried adhesive was then sealed in a bag with desiccant and stored at −20 °C until used.

Coupling with electronic sensor
The silicone encapsulated sensor device was assembled from two separate parts. First, Ecoflex 020 was mixed for 3 min, degassed for 1 min, and poured onto a rectangular acrylic mold (150 × 180 × 2 mm) and allowed to cure at room temperature for 4 h. Curing in an oven under some heat will expedite curing time. Prior to curing, a flat piece of acrylic was used to scrape any excess silicone and ensure a flat sheet. To achieve a strong bond between the hydrogel adhesive and silicone, the cured silicone sheet was soaked in a solution of 10 w/v% benzophenone in ethanol for 10 min, rinsed with ethanol, and then air dried. The hydrogel adhesive precursor, prepared using the method above, was then poured onto one side of the benzophenone-treated silicone, sandwiched with a glass plate using 150 µm spacers, clamped and cured in a UV chamber for 30 min. Once cured, the silicone sheet with adhesive was air-dried for at least 3 h. For the sensor housing, Ecoflex 020 was prepared and poured onto a 3D printed mold with enough hollow space in the middle to tightly grip the sensor and cured for 4 h at room temperature. To finalize the silicone encapsulated sensor device, the sensor was inserted into the top mold and joined to the flat sheet using Sil-Poxy (Smooth-on). The device was sealed in an air-tight container with desiccant and stored at −20 °C until used.

To couple the dry adhesive layer to a 3D-printed urethane base, a thin layer of polyurethane was brushed onto the base. Then, the dry adhesive layer was pressed onto the wet polyurethane and allowed to dry under airflow for 10 min.

Mechanical tests
All tissues were first soaked in artificial seawater, and prepared by dissolving 3.5 w/v% of sea salt (Sigma-Aldrich) in deionized water. All tissues were adhered to engineering solids using the hydrogel adhesive by pressing for 10 s. Mechanical tests were conducted at room temperature using a mechanical testing machine with a 2.5 kN load cell (Zwick/Roell Z2.5). A stiff nylon membrane, or thin polylactic acid film (Fischer Scientific) backing was applied using cyanoacrylate glue (Krazy Glue) to act as a stiff backing for the adhesive interface and marine animal tissues. Aluminum fixtures were applied using cyanoacrylate glue to provide grips for tensile tests.

To measure interfacial toughness, adhered samples with widths of 15 mm were tested by the standard 90-degree peel test (ASTM D2861). Peeling tests were conducted using a constant peeling speed of 50 mm min−1. Interfacial toughness was determined by dividing the plateau force at a steady state by the adhesion width. Shear strength was measured using the standard lap shear strength test (ASTM F2255) using a constant tensile speed of 50 mm min−1. Shear strength was calculated by dividing the maximum force by the adhesion area, which was approximately 15 mm by 15 mm for each sample. Tensile strength was measured using a constant tensile speed of 50 mm min−1 according to the standard tensile test (ASTM F2258). The tensile strength was calculated by dividing the maximum force by the adhesion area, which was approximately 15 mm by 15 mm for each sample.

Tensile properties and fracture toughness of the swollen adhesive interface were measured using pure-shear tensile tests of rectangular samples (30 mm in width, 10 mm in height, and 0.15 mm in thickness). Samples were equilibrated in seawater for 24 h prior to testing. Fracture toughness was calculated based on tensile tests of notched and unnotched samples of equal dimensions (Supplementary Fig. 1). All tests were done using a constant tensile speed of 50 mm min−1 using a 20 N load cell (Zwick/Roell Z2.5). All data collected from mechanical tests was processed using Matlab 2023b.

In vivo testing
To evaluate the efficacy of the BIMS across numerous species, we conducted a large-scale biologging experiment in a large (9 m diameter, 5 m height) saltwater pool at the Woods Hole Oceanographic Institution’s (WHOI) Environmental Systems Laboratory (ESL). The experiment was conducted on October 19th, 2022 in a large saltwater tank filled with seawater (18 °C) from the nearby Vineyard Sound and was continually UV filtered. Animals were allowed to acclimate to the tank for 24 h prior to testing.

Two sensor packages were used in this study ITAGs contain a triaxial inertial measurement unit (IMU) with an accelerometer, gyroscope, and magnetometer sampled at 100 Hz (TDK Invensense MPU9250), and pressure, temperature (Keller 7LD), and light sensors (Intersil ISL29125) sampled at 1 Hz. The ITag was designed specifically for squid and jellyfish, with a hydrodynamic shape to limit additional lift and drag forces on the tagged animal, and was neutrally buoyant19,41. Secondly, Axy5XS bio-loggers (Technosmart Europe srl, www.technosmart.eu), measure tri-axial acceleration at 100 Hz and magnetic field strength in three axes at 2 Hz.

The tank was rigged with three GoPro Hero 7 Black cameras for visual monitoring. All sensors and underwater cameras were time synchronized to accurately relate video and sensor data. Tags were affixed by removing the animal from the water, quickly patting the area of adhesion to remove any mucus and immediately applying the combined sensor and hydrogel adhesive with gentle pressure for 10 s. After, all animals were immediately released back into the water. The experimental animals were four lobsters (two tagged, total length: 25 cm, 22.5 cm), ten squid (five tagged, mantle length: 20.4 ± 2.6), three skate (two tagged, disc length: 37 cm, 42 cm), and one tagged flounder (total length 26 cm). Untagged and tagged animals were used to visually assess potential behavioral changes from applying the sensor with hydrogel adhesive and monitor interactions between tagged and untagged animals. Control animals were subject to the same tag process; they were removed from the water and handled as if a sensor was being applied, followed by immediate release. Animals for tagging were chosen at random, except for the flounder since only one was available. Sex was not considered in this study as a variable that would affect BIMS performance due to similarities in topological features across sex for the species tested. In addition, most species were not sexually dimorphic. Thus, identifying individual sex would require invasive probing and prolong tagging processes, which opposed a key goal of BIMS to rapidly and non-invasively adhere sensors.

Movement and gait classification
Biologging tags were used to measure the acceleration and pitch of squid, jellyfish, skate, lobster, and flounder. For individual behaviors, raw acceleration (gravitational and dynamic) was reported in all three axes. We used a Fast Fourier Transform on the accelerometer axes to calculate finning rates for squid and skate19. Additionally, pitch was calculated from the accelerometer (A) signal using (A_x / (A_x^2 + A_z^2)^0.5), and was used to measure swim direction of squid and detect water currents in kelp19. To compare movements across species, overall dynamic body acceleration was measured for all species (squid, skate, lobster, flounder, and kelp) in the large-scale marine sensing experiment. ODBA was used to compare movement rates among species and as a general activity metric. To distinguish between high-frequency animal movements (dynamic acceleration) and slower changes in orientation (gravitation acceleration), a low-pass filter (window size = 2.0 s42) was applied to all three axes of the accelerometer data. All data was analyzed using Matlab 2023b.

Ethical statement and animal handling
This study was carried out in accordance with the principles of the Basel Declaration and recommendations and approval of the WHOI’s Institutional Animal Care and Use Committee scientific protocol to TAM, IACUC number: 20811.03. Field testing in the Azores was completed with under the Azorean Regional Government’s International Recognized Compliance Certificate 46/2021/DRCTD for access and use of natural resources for scientific purposes. All animal testing was done in compliance with local and national ethical regulations.

For tank experiments, skate, squid, sea robin, sea bass, and flounder were obtained from the Marine Resources Center at the Marine Biological Laboratory, Woods Hole, MA. Jellyfish were purchased from Sunset Marine Labs (Hillsboro, OR), transported overnight in water bags, and allowed to acclimate for 24 h. Live lobster was purchased from a local fish market. Skate, flounder, sea robin and sea bass were released into the nearby vineyard sound two weeks after testing. Local squid, jellyfish, and lobster were kept in their tanks indefinitely after testing. Squid used for field testing in the Azores was caught by jigging and immediately released upon tagging. Animal tissues for ex-vivo testing were purchased from a local fish market.

Peer review rounds
[{"round": 1, "reviewer_comments": {"reviewer_1": "In this manuscript, the authors developed bioadhesive marine sensor networks to study individual, group, and mulfi-species behaviors. The synergy of water absorpfion, physical crosslinks covalent amide bonds make the developed soft hydrogel-based bioadhesive achieving rapid, robust, and non-invasive integrafion on various marine animals. This work proposes a new axis of the applicafion of soft hydrogel- based bioadhesive, and the reported results are interesfing for the broad readers of Nature Communicafion, including biomaterials researchers, marine biologist, and engineer community. However, some revisions are needed to improve the integrity of the story considering the high impact of this journal.\n1. The main concern is that the key component, namely soft hydrogel-based bioadhesive interface, some similar bioadhesives has been designed and fabricated in the previous study from the same authors (Nat. Mater. 20, 229–236 (2021); Sci Transl Med. 14(630), eabh2857 (2022)). Therefore, the novelty of material design is lacking.\n2. The long-term stability of bioadhesive in various liquid environment need to be invesfigated, e.g., the temperature/salinity related swelling and adhesion properfies of bioadhesive versus fime.\n3. In addifion, the swelling behavior needs to be invesfigated.\n4. Could BAMS be easily detached to avoid marine wear these sensors for life?\n5. Is there any prospect of the developed BAMS being used in divers being used in divers or sailors?\n6. Some demonstrafion experiments in real sea areas will further strengthen this manuscript.", "reviewer_2": "Species natural behaviour is very hard to study in the marine environment. The field relies on methods that document data under natural condifions when the human observer is absent. Tagging and biologging is a field in marine science that is rapidly advancing due to the development of ever smaller tags that can be used to track fish, sharks and cetaceans. However, a missing link in the field of biologging is the use of tags on soft bodied organisms such as molluscs and gelafinous organisms. These are abundant and ecologically pivotal taxa but their delicate bodies make it hard to aftach tags to. Advancing our understanding of these bodied marine species relies on technological developments such as presented by Zhao et al. The authors present a new adhesive methodology which allows rapid and traumaless aftachment of electronic tags on marine invertebrates. The authors describe the tesfing and adhesion procedure in great detail and even present very interesfing preliminary data obtained by tagging various organisms in tank tests, to guide future research. I find the study very interesfing, well prepared, well wriften, detailed and it surely breaks new ground in the field of biologging.\nA major problem is that the authors do not explain how they obtain the tags or remove the tags from the animals to obtain the data. Do the animals survive after removal? Also I would like to have seen a discussion or an example set up how this new technology could be used in nature. Or if it is not possible to apply this technique it in nature, the authors should explicitedly state so.\nIn general, the authors do a great job lisfing the advantages of this approach, but they do not present a realisfic view on the real applicafion and its limitafions. Therefore the manuscript is incomplete.", "reviewer_3": "Overall comments\nFor the marine biologging community this is a very important manuscript as it demonstrates a proof of concept for a new way forward for tagging soft fragile marine animals (invertebrates or but also smaller fragile vertebrates) which unfil now have largely been ignored because of the difficulty in aftaching devices to their soft fissues. The authors demonstrate how a new type of bioadhesive can be used to aftach tags to soft and fragile marine animals. The new adhesive is a hydrogel that is dried and then upon contact with the soft fissue of a marine animal absorbs water and starts to form a bond that aftaches the tag to the animal. Very neat. This bond forms within 20 seconds or even less and so the animal can be placed back in the water and do not require venfilafion or surgical procedures. The authors used 3 different mechanical tests to measure adhesive performance. The authors then demonstrate how mulfiple tags can be deployed on many individuals (across many species) so that schooling behaviour can be observed. The authors also discuss how mulfiple sensors can be deployed on a single individual to examine quesfions on ecophysiology. Overall it is an excellent manuscript with very important applicafions in the field of biologging. However, before it can be published I would like some structural changes/or concerns addressed and some further clarity on the wrifing of the manuscript. The authors should be congratulated on this work. I can’t wait to use the adhesive!!!\nKey comments: I find the use of term ‘bioadhesive marine sensor networks’ confusing throughout the manuscript. This stems from the fact that the authors have tagged both invertebrates and vertebrates but also a seaweed, so they need this wordy phrase to describe it. Messy. Why not drop the seaweed and perhaps just menfion in a throwaway comment that adhesive also works on seaweeds etc.? Also, the most important finding from this study for me is the hydrogel and how easy it is to sfick tags onto animals. This is publishable in itself with all the mechanical tests etc. and mulfiple species you tested it on. But this finding is muddled (in fitle and abstract) when the authors also discuss how mulfiple sensors can be deployed across many individuals and even species. So now the fitle becomes adhesive marine ‘sensor network’ (rather than “novel adhesive for aftaching sensors/tags to soft and fragile marine animals”) but I’m not sure how it is a network as individuals of a network communicate with each other and the sensors used in this study do not (I think but this is not clear to me)? Then finally the authors say they can aftach mulfiple sensors to one animal. again this detracts from the main finding. I would prefer the authors just present findings on the adhesive and then say something like the speed (and non-invasiveness of procedure) at which tags can be deployed means that mulfiple tags can be deployed on one animal (maybe show this in supplementary material). I would remove the sensors aftached to many individuals/species showing schooling behaviour. This is a worthy finding of itself but needs further expansion and detail as hugely important work – how marine invertebrates aggregate/school, but it is lost in this new method manuscript.\nSee aftached edited PDF with further comments.\nTom Doyle"}, "author_response": "Response to Reviewer #1\nComment 1. In this manuscript, the authors developed bioadhesive marine sensor networks to\nstudy individual, group, and multi-species behaviors. The synergy of water absorption, physical\ncrosslinks covalent amide bonds make the developed soft hydrogel-based bioadhesive\nachieving rapid, robust, and non-invasive integration on various marine animals. This work\nproposes a new axis of the application of soft hydrogel-based bioadhesive, and the reported\nresults are interesting for the broad readers of Nature Communication, including biomaterials\nresearchers, marine biologist, and engineer community. However, some revisions are needed to\nimprove the integrity of the story considering the high impact of this journal.\nResponse 1. Thank you for your insightful and constructive comments. We greatly appreciate\nyour recognition of the novelty and importance of our work. In the following paragraphs, we\nwill address your comments point-by-point. The new sentences in the manuscript and\nsupplementary information are marked in red.\nComment 2. The main concern is that the key component, namely soft hydrogel-based\nbioadhesive interface, some similar bioadhesives has been designed and fabricated in the\nprevious study from the same authors (Nat. Mater. 20, 229–236 (2021); Sci Transl Med. 14(630),\neabh2857 (2022)). Therefore, the novelty of material design is lacking.\nResponse 2. Thank you for the feedback. While the bioadhesive material compositions are\nadopted from the strategy previously developed in this lab group, we presented several\nimprovements and insights in this work from material perspective. 1) We translate the adhesive\nhydrogel from biomedical applications to an entirely new field – marine animal biologging\napplications. The robust and ease of hydrogel adhesive technology is systematically evaluated\nin the marine environments, which have not been covered previously and will boost the\napplications of biologging. 2) We modified the adhesive hydrogel to be ready integrated with a\nvariety of marine sensors, showing how this material could be widely integrated with existing\nsystems.\nComment 3. The long-term stability of bioadhesive in various liquid environment need to be\ninvestigated, e.g., the temperature/salinity related swelling and adhesion properties of\nbioadhesive versus time. In addition, the swelling behavior needs to be investigated.\nResponse 3. Thank you for your insightful comments. As suggested, the swelling and adhesion\nwere systematically investigated ex vivo over a 24-hour time period at three different\ntemperatures (4°C, 20°C and 30°C). Considering the degradation of squid tissue soaked in\nwater and the subsequent influence on the experiment results, the time of observation is no\nlonger than 24 hours. Results show that the shear strength of the adhesive on squid tissue begins\nto decrease after 24 hours. Results on live animals also show that the adhesion to squid is stable\nfor 24 hours. The adhesion strength is stronger overall at the lower temperatures due to the\nlower swelling ratio. The adhesion strength shows high stability over 24 hours at three different\ntemperatures. We have added Fig. R1 (added as Supplementary Fig. 4) and the following\nparagraph in the revised manuscript and supplementary information.\n“Adhesion stability and swelling behavior were further investigated ex vivo on squid over a 24-\nhour period and at three temperatures (4°C, 20°C, and 30°C). The lap shear strength was\nmeasured on squid samples after 30 minutes, 1 hour and 24 hours. Shear strength on squid\ndecreased an average of 15.6% in 24 hours across the three temperatures. Notably, the shear\nstrength was overall higher at 4°C, likely due to the lower swelling ratio of 1.2 (Supplementary\nFig. 4).”\nFig. R1 | Swelling and adhesion stability at different temperatures. a,b, shear strength of\nthe BAMS on squid tissue over 24 hours at three representative temperatures. c, Adhesive\nswelling ratio at three different temperatures. Values in a,b, and c are mean and standard\ndeviation where error bars are present (n = 3 individual samples).\nComment 4. Could BAMS be easily detached to avoid marine wear these sensors for life?\nResponse 4. Based on our previous works (Nat. Mater. 20, 229 (2021); PNAS 117, 15497\n(2020)), the covalent bonds and physical bonds (e.g., electrostatic interactions) in the adhesive\ninterface can be easily cleaved via an aqueous biocompatible triggering solution (0.5 M sodium\nbicarbonate and 50 mM glutathione). While we did not include the benign detachment of the\nadhesive interface in this study, the sensors are able to detach from marine animals via galvanic\nrelease systems, leaving the adhesive base behind. In these set ups, an intermediary ‘base’ is\nplaced between the sensors and the animal. Instead of sensors being directly attached to the\nanimal, only the base is affixed. Then, a nichrome wire is used to connect sensors to the\nintermediary base. Because nichrome de-ionizes in seawater when an electrical current is\napplied, users can program specific ‘release times’ for on-demand detachment of sensors from\nthe animals. The related schematic illustration and images have been added in the new Fig. 5.\nComment 5. Is there any prospect of the developed BAMS being used in divers or sailors?\nResponse 5. Thank you for your thoughtful feedbacks. As for now, BAMS cannot be employed\nunderwater by divers or sailor. Nevertheless, the potential for underwater applications is\ndefinitely interesting. They could further decrease the out-of-water time for improved animal\nwelfare and simplify the process of tagging marine animals that are challenging to capture\nfrom a boat. There is an ongoing project focused on the development of new BAMS for\nunderwater applications, but this falls outside the scope of this work.\nComment 6. Some demonstration experiments in real sea areas will further strengthen this\nmanuscript.\nResponse 6. BAMS was tested in real sea areas at the Azores, Portugal. In the Fig. R2 (added\nas Fig. 5 in the manuscript). we demonstrate that the squid was successfully tagged using\nBAMS in the field on the side of a boat and then released. The squid was observed diving to\n300 meters under sea level with the sensor attached. Migrating squids autonomously sample\nvertical gradients of temperature and luminance.\nFig. R2 | BAMS application in the field. a, Representative images of the BAMS application\nin wild field, showing (left to right) drying, application, maneuvering, releasing, and tag\nrecovery via radio signal. b, The depth of the squid actively descends immediately after release\nas a function of time. c,d, Adhered environmental sensors sampled the temperature (c) and\nluminance of RGB light (d) as a function of depth (b). e, Schematic illustration of tag recovery\nvia programable galvanic release and radio signal. f-i, Accelerometer, and gyroscope data for\ntwo ecologically important movement behaviors captured by the IMU. Gliding (g and f)\nrepresents a low-activity movement where the negatively buoyant animal descends in the water\ncolumn. Jet propulsion (h and i) represents a high-activity movement and is often employed in\nseries. Colors in f-i, represent direction, where blue is forward motion (surge, or x), orange is\nlateral motion (sway, or y), and yellow is vertical motion (heave, or z).\nResponse to Reviewer #2:\nComment 1. Species natural behaviour is very hard to study in the marine environment. The\nfield relies on methods that document data under natural conditions when the human observer\nis absent. Tagging and biologging is a field in marine science that is rapidly advancing due to\nthe development of ever smaller tags that can be used to track fish, sharks and cetaceans.\nHowever, a missing link in the field of biologging is the use of tags on soft bodied organisms\nsuch as molluscs and gelatinous organisms. These are abundant and ecologically pivotal taxa\nbut their delicate bodies make it hard to attach tags to. Advancing our understanding of these\nbodied marine species relies on technological developments such as presented by Zhao et al.\nThe authors present a new adhesive methodology which allows rapid and traumaless attachment\nof electronic tags on marine invertebrates. The authors describe the testing and adhesion\nprocedure in great detail and even present very interesting preliminary data obtained by tagging\nvarious organisms in tank tests, to guide future research. I find the study very interesting, well\nprepared, well written, detailed and it surely breaks new ground in the field of biologging.\nResponse 1. Thank you for the valuable feedback and interest in our project! We greatly\nappreciate your recognition of the novelty and importance of our work. In the following\nparagraphs, we will address your comments point-by-point. The new sentences in the\nmanuscript and supplementary information are marked in red.\nComment 2. A major problem is that the authors do not explain how they obtain the tags or\nremove the tags from the animals to obtain the data. Do the animals survive after removal?\nResponse 2. BAMS was tested in real sea areas at the Azores. In the new Figure 5, we\ndemonstrate that the squid was successfully tagged using BAMS and then released to sample\nvertical gradients of temperature and luminance autonomously. The sensors with obtained data\nare able to detach from marine animals via galvanic release systems. Specifically, the field tags\nare attached to a base plate which remains on the animal1. The sensor itself is set to release after\na pre-determined time, at which point the sensor separates from the base plate and floats to the\nsurface. When surfaced, the sensor emits frequent pings on a known frequency (VHF) which\nallows for surface tracking and retrieval.\nExperiments in enclosed tanks are employed to evaluate the animal's survivability after tag\nremoval. The animals do survive after BAMS detaches. For example, multiple skate and black\nsea bass were tagged with BAMS and remained healthy over 1 month after BAMS detachment.\nSquid were observed swimming normally a few days after BAMS detachment. However, it was\nnot possible to monitor squids for longer time periods due to the inherent issues with squid\nhusbandry and other complications.\nComment 3. Also I would like to have seen a discussion or an example set up how this new\ntechnology could be used in nature. Or if it is not possible to apply this technique it in nature,\nthe authors should explicitedly state so. In general, the authors do a great job listing the\nadvantages of this approach, but they do not present a realistic view on the real application and\nits limitations. Therefore the manuscript is incomplete.\nResponse 3. BAMS was tested in real sea areas at the Azores. In the Fig. R3 (added as Fig. 5\nin the manuscript) and Supplementary Video 4, we demonstrate that the squid was\nsuccessfully tagged using BAMS in the field on the side of a boat and then released. The squid\nwas observed diving to 300 meters under sea level with the sensor attached. Migrating squids\nautonomously sample vertical gradients of temperature and luminance.\nFig. R3 | BAMS application in the field. a, Representative images of the BAMS application\nin wild field, showing (left to right) drying, application, maneuvering, releasing, and tag\nrecovery via radio signal. b, The depth of the squid actively descends immediately after release\nas a function of time. c,d, Adhered environmental sensors sampled the temperature (c) and\nluminance of RGB light (d) as a function of depth (b). e, Schematic illustration of tag recovery\nvia programable galvanic release and radio signal. f-i, Accelerometer, and gyroscope data for\ntwo ecologically important movement behaviors captured by the IMU. Gliding (g and f)\nrepresents a low-activity movement where the negatively buoyant animal descends in the water\ncolumn. Jet propulsion (h and i) represents a high-activity movement and is often employed in\nseries. Colors in f-i, represent direction, where blue is forward motion (surge, or x), orange is\nlateral motion (sway, or y), and yellow is vertical motion (heave, or z).\nResponse to Reviewer #3:\nComment 1. For the marine biologging community this is a very important manuscript as it\ndemonstrates a proof of concept for a new way forward for tagging soft fragile marine animals\n(invertebrates or but also smaller fragile vertebrates) which until now have largely been ignored\nbecause of the difficulty in attaching devices to their soft tissues. The authors demonstrate how\na new type of bioadhesive can be used to attach tags to soft and fragile marine animals. The\nnew adhesive is a hydrogel that is dried and then upon contact with the soft tissue of a marine\nanimal absorbs water and starts to form a bond that attaches the tag to the animal. Very neat.\nThis bond forms within 20 seconds or even less and so the animal can be placed back in the\nwater and do not require ventilation or surgical procedures. The authors used 3 different\nmechanical tests to measure adhesive performance. The authors then demonstrate how multiple\ntags can be deployed on many individuals (across many species) so that schooling behaviour\ncan be observed. The authors also discuss how multiple sensors can be deployed on a single\nindividual to examine questions on ecophysiology. Overall it is an excellent manuscript with\nvery important applications in the field of biologging. However, before it can be published I\nwould like some structural changes/or concerns addressed and some further clarity on the\nwriting of the manuscript. The authors should be congratulated on this work. I can’t wait to use\nthe adhesive!!!\nResponse 1. Thank you for the valuable feedback and interest in our project! We greatly\nappreciate your recognition of the novelty and importance of our work. In the following\nparagraphs, we will address your comments point-by-point. The new sentences in the\nmanuscript and supplementary information are marked in red.\nComment 2. I find the use of term ‘bioadhesive marine sensor networks’ confusing throughout\nthe manuscript. This stems from the fact that the authors have tagged both invertebrates and\nvertebrates but also a seaweed, so they need this wordy phrase to describe it. Messy. Why not\ndrop the seaweed and perhaps just mention in a throwaway comment that adhesive also works\non seaweeds etc.?\nResponse 2. Thank you for the feedback. We replace the term “bioadhesive marine sensor\nnetworks” into “bioadhesive for marine sensors” to avoid confusion. We simplify the discussion\nabout seaweed and put the figures into supplementary information as Supplementary Fig. 8.\nComment 3. Also, the most important finding from this study for me is the hydrogel and how\neasy it is to stick tags onto animals. This is publishable in itself with all the mechanical tests\netc. and multiple species you tested it on. But this finding is muddled (in title and abstract)\nwhen the authors also discuss how multiple sensors can be deployed across many individuals\nand even species. So now the title becomes adhesive marine ‘sensor network’ (rather than\n“novel adhesive for attaching sensors/tags to soft and fragile marine animals”) but I’m not sure\nhow it is a network as individuals of a network communicate with each other and the sensors\nused in this study do not (I think but this is not clear to me)?\nResponse 3. Thank you for your constructive feedback. We revise the title from “Bioadhesive\nmarine sensor networks on Diverse Soft Fragile Species” to “Bioadhesive for Marine Sensors\non Diverse Soft Fragile Species”. The use of the word sensor network throughout this\nmanuscript is in the context of having groups of sensors from different species collecting data\nthat would be retrieved and analyzed afterwards to inform individual, group, and community\ninteractions. Although we wanted to highlight how this bioadhesive could facilitate studying\nmarine ecosystems in a “sensor network” style as a big picture, we agree that may take away\nfrom the main finding, and have adjusted overall language throughout the manuscript.\nComment 4. Then finally the authors say they can attach multiple sensors to one animal. again\nthis detracts from the main finding. I would prefer the authors just present findings on the\nadhesive and then say something like the speed (and non-invasiveness of procedure) at which\ntags can be deployed means that multiple tags can be deployed on one animal (maybe show this\nin supplementary material). I would remove the sensors attached to many individuals/species\nshowing schooling behaviour. This is a worthy finding of itself but needs further expansion and\ndetail as hugely important work – how marine invertebrates aggregate/school, but it is lost in\nthis new method manuscript.\nResponse 4. We agree that the key finding of this work is the robust and rapid adhesive for\ntagging on marine species. To highlight this, we have moved the figure of multiple sensors on\none animal to supplementary information as Supplementary Fig. 7. In addition to the exhaustive\nlab mechanical tests, the employment on more than one species also highlights the robustness\nof BAMS in large seawater environments where animals ‘interact’ with conspecifics, other\nspecies, and currents. The attachment to many individuals in a short time period also served as\na showcase for the rapidness of employment. Therefore, it is important to keep the Figure which\nshows individual and group level behaviors from experiments in a 318000 liter seawater pool.\nMoreover, it is important to show the efficacy of this technology in the field. So, we developed\na new figure showing a BAMS field test. The data presented in the Fig. R4 (added as Fig. 5 in\nthe manuscript) and Supplementary Video 4 is a brief summary of the field application\ndemonstrating the ease of use in the field.\nFig. R4 | BAMS application in the field. a, Representative images of the BAMS application\nin wild field, showing (left to right) drying, application, maneuvering, releasing, and tag\nrecovery via radio signal. b, The depth of the squid actively descends immediately after release\nas a function of time. c,d, Adhered environmental sensors sampled the temperature (c) and\nluminance of RGB light (d) as a function of depth (b). e, Schematic illustration of tag recovery\nvia programable galvanic release and radio signal. f-i, Accelerometer, and gyroscope data for\ntwo ecologically important movement behaviors captured by the IMU. Gliding (g and f)\nrepresents a low-activity movement where the negatively buoyant animal descends in the water\ncolumn. Jet propulsion (h and i) represents a high-activity movement and is often employed in\nseries. Colors in f-i, represent direction, where blue is forward motion (surge, or x), orange is\nlateral motion (sway, or y), and yellow is vertical motion (heave, or z).\nComments in the annotated manuscript\nComment 5. This title is overly complicated. better to just say - A hydrogel adhesive for\nattaching sensors on soft fragile marine species.\nResponse 5. We revise the title from “Bioadhesive marine sensor networks on Diverse Soft\nFragile Species” to “Bioadhesive Marine Sensors on Diverse Soft Fragile Species”.\nComment 6. In the previous manuscript, “These methods can suffer from severe limitations,\nparticularly for adhering on soft fragile marine species such as squid and jellyfish…”. not\nalways severe. dont think you need to say severe as not always. just delete severe./ enough to\nsay these methods can suffer from limitations such as...\nResponse 6. The word “severe” has been deleted.\nComment 7. In the previous manuscript, “Reliable and rapid adhesion of deployments multi-\nanimal sensor-network to study biomechanics…” it is not exactly clear what this means.\nsuggest you make this very clear in abstract and methods and manuscript as currently not clear.\nso 1) you have tested a new hydrogel for attaching tags to animals and 2) you have\ndemonstrated that this adhesive can be used to attach multiple tags to many different species\nBUT to me it is not clear if these tags communicate or if it is from video analysis and analysis\nof tag data that you gain insights?\nResponse 7. We revise this sentence into “Reliable and rapid adhesion enables large scale,\nmulti-animal sensor deployments to study biomechanics…” to highlight the key finding and\navoid confusion.\nComment 8. In the previous manuscript, “However, these sizeable and rigid sensors are not\napplicable to small fragile organisms, which are highly diverse, abundant (> 38.3 teragrams\nof carbon) and pervasive in all ocean habitats, as well as provide a key protein source for\nhumans worldwide and sequester greenhouse gasses into the deep ocean.” not all are small.\nsome are just soft or fragile and lack hard carapaces of tough robust skin. replace with ' not\napplicable to attach to more fragile marine organisms that may have soft integuments, and/or\nmay be very small e.g. many invertebrates such as squid and jellyfish but also many smaller\nfish species such as xx and xx.\nResponse 8. As suggested, we revised the sentence to provide a more exact description.\n“However, these sizeable and rigid sensors are not applicable to attach to more fragile\nmarine organisms that may be small or have soft outer protective layers as is true for\nmany invertebrates such as squid and jellyfish, but also many small fish. Soft-bodied\nmarine organisms are highly diverse, abundant (> 38.3 teragrams of carbon) and\npervasive in all ocean habitats, as well as provide a key protein source for humans\nworldwide2 and sequester greenhouse gasses into the deep ocean.”\nComment 9. In the previous manuscript, “The BAMS contains a thin layer of a dried-hydrogel\nadhesive interface that can absorb the seawater from the surface of marine species by hydration\nand swelling, on diverse marine species within 22 s. After adhering to the surface of marine\nspecies, the adhesive interface of the BAMS becomes a soft yet robust hydrogel.” keep language\nsimple. so once the dried hydrogel adhesive absorbs water from the surface of the marine\nspecies it sticks to the animal? no need to say subsequently integrating sensors??\nResponse 9. As suggested, we simplify this sentence. “The BAMS contains a thin layer of a\ndried-hydrogel adhesive interface that can absorb the seawater from the surface of marine\nspecies by hydration and swelling, subsequently adhering sensors on diverse marine species\nwithin 22 s”\nComment 10. In the previous manuscript, “A thin dried-hydrogel adhesive interface (150 µm\nthickness) on the bottom of the BAMS enable the rapid and non-invasive integration of\nbiologging sensors with marine species.” replace integration with 'attachment'?? integration\nmeans that the tags is now part of the animal???\nResponse 10. As suggested, we replace “integration” with “attachment” in the revised\nmanuscript.\nComment 11. In the previous manuscript, “The adhesive interface can be easily coupled to a\nvariety of soft engineering solids (i.e., silicone and polyurethane) and embedded with different\nsensors to be a universal BAMS” not fully clear how sensors are inserted into hydrogel? do you\ninsert sensors in the same way you 'stick' to animal i.e. just wet the top and attach sensor to wet\npart of hydrogel???? again language here is over complicated. the adhesive can be easily\n'attached' to a variety of different materials such as silcone and polyurethane and then embedded\nwith different sensors?\nResponse 11. We revise the sentence to avoid confusion. “Through surface chemical treatments,\nthe adhesive interface can be easily coupled to a variety of soft engineering solids (i.e., silicone\nand urethanes), which can be used as an intermediate layer or an encapsulant for embedding\nsensors regardless of their material composition, to be a universal BAMS.”\nComment 12. In the previous manuscript, “The adhesive interface of the BAMS forms a rapid\nand robust bond to various wet tissues with a high interfacial toughness (>160 J m-2 for\nsquid, >130 J m-2 for salmon, >70 J m-2 for skate, and >70 J m-2 for flounder), shear strength\n(>40 kPa for squid, >40 kPa for salmon, >80 kPa for skate, and >70 kPa for flounder), and\ntensile strength (>60 kPa for squid, >30 kPa for salmon, >130 kPa for skate, and >70 kPa for\nflounder).”no mention of jellyfish here? yet mentioned in next sentence.\nResponse 12. Mechanical tests on jellyfish tissue were not possible due to difficulty reliably\nfixing the gelatinous underside of the tissue to the testing device. Jellyfish in the next sentence\nis deleted.\nComment 13. In the previous manuscript, “In addition to facilitating multi-animal sensor\nnetwork deployment, the BAMS allows for rapid and reliable adhesion of multiple sensors\nacross a single animal.” this is possible with many different tags so not sure what the message\nis here?\nResponse 13. We simplify this sentence. “To highlight rapid and reliable deployment of BAMS,\nmultiple sensors are adhered across a single animal.” The figure associated to this paragraph is\nmoved to Supplementary Information.\nComment 14. In the previous manuscript, “To evaluate the robustness of the BAMS across\ndiverse marine species and study the individual, group, and community behaviors via a sensor\nnetwork”. You do not explain what you mean by a sensor network? do the tags communicate\nwith each other or simply is it lots of tags on many different animals in the same place?\nResponse 14. The tags do not communicate with each other in this work. To avoid any potential\nconfusion, we have replaced the term “a sensor network” into “a series of sensors.”\nComment 15. What does Fig. 2k show? time tag remained on animal in water? not clear.\nResponse 15. Fig. 2k shows “the duration of biologging” on squid and jellyfish via BAMS. We\nrevise the figure accordingly.\nComment 16. In Figure 4. need to explain different colours in caption too. not enough to have\nlittle figure of jellyfish showing x, y and z and spiral?\nResponse 16. The explanation of different color has been added in caption. “Colors in a,c,e,g,\nrepresent direction, where blue is forward motion (surge, or x), orange is lateral motion (sway, or y)\nand yellow is vertical motion (heave, or z).”"}, {"round": 2, "reviewer_comments": {"reviewer_1": "My concerns have been addressed by the authors. An acceptance for publicafion of this paper is thus\nrecommended.", "reviewer_3": "I am very happy that the authors have addressed all my comments and I am happy for this to be\npublished. I very much look forward to seeing this published.", "reviewer_4": "Bio adhesive review NCOMMS-23-19712A\nI was asked by the editor to comment on the author’s responses to Reviewer 2 to see if I thought they\nadequately dealt with the reviewer’s concerns. The reviewer produced 3 comments. The first was a\nstatement praising the work. It required no significant reply and the authors express thanks for the\npraise.\nThe second raised two quesfions: They pointed out that the authors did not explain how they “obtained\nthe tag”s or removed the tags from the animals to recover the data. Im was not certain if the review\nwant to know the source of the electronic s they used, i.e commercially sourced or specially custom built\nin houseI to on not certain but is seems that the answer might be some of both. . I am aware of several\nsuppliers of similar recording instruments.\nThe authors responded to this comment by adding a significant new subsecfion to the paper that\nexplains the field procedure in more detail and that included an informafive short video of the animal\nbeing tagged and released. They explained that the tag (which record, rather than transmit, the data\nthey collect) was “released from the animal via a galvanic release system, and that they “recovered the\ntag via a radio signal output”. They also added a new figure that provides a pictorial schemafic of the\nfield process as well as the informafive video. I expect that this might safisfy the reviewer but, if it were\nme, I would like to have a bit more detail, parficularly on the detail of the preparafion of the adhesive.\nThe secfion of the paper capfioned “Preparafion of the adhesive interface” is key to enabling\npracfifioners to use the aftachment approach. It is brief and, as someone not schooled in such\nengineering, I would need some further discussion about the process, the rafionale for the various steps\nand potenfial piffalls and crificalifies before I aftempted to use it.\nReviewer 2 also asks, “Do the animals survive after removal”. The authors suggest that they do, in the\nshort term. There is no data on long term effects, if any. This would of course be very useful, if available.\nOne thing that was not made clear is whether, after release of the recording package, what remains on\nthe animal. If so, how long will it remain aftached and how might it affect the fissue during that fime. I\nwould have liked more detailed info on the removal of the adhesive as tghey aftempted to show in Sup.\nFog. 6. I did not find the images very helpful so perhaps they could provide some clearer images or some\ndiagnosfic discussion of any apparent injury that might have resulted from pressure, shear or necrofic\nfissue under the aftachment.\nThe 3rd comment I guess was driven by a lack of any field study in the original manuscript so this whole\nnew study and the associated text and figure should make it clear that the use of the aftachment\nmethod is feasible in the field.\nSome gratuitous comments from my own reading of the paper. For me, the key aspect of this paper is\nthe report on a potenfially very useful adhesive. I don’t view that data collected on the animals as\nparficularly useful. To me, Its funcfion in the paper is simply an example of how the adhesive might be\nused for aftachment of instruments using the adhesive on animals with a variety of integuments.\nThe adhesive seems similar to some that has been developed and used previously in surgical\nintervenfions on wet, soft fissues and that have advantages over convenfional suturing and other\ntissue glues like cyanoacrylates e.g. DOI: 10.1126/science.abo2542; doi: 10.1016/j.bioactmat.2021.10.001;\nhftps://sanaheal.com/ .\nHere the authors show it is also suitable for aftachment of instruments to soft bodied marine animals.\nThe limitafions of exisfing methods and the importance of finding befter aftachment methods is\nappreciated by the biologists studying such creatures and this is an important new applicafion of the\nmedical methodology in this new realm.\nBut the paper seems to conflate two objecfives. One is the descripfion of the adhesive, its preparafion\nand mechanical tesfing via actual applicafion to a set of animals in the lab where they can be observed\nfor a fime to assess the efficacy of the aftachment; the other is to demonstrate that the methodology is\napplicable in the field by providing an example of how it might be used on a soft-bodied animal, a squid,\nwith a parficular data recording device that records data on depth, accelerafion and light level. (Such\ndevices are now often used and I believe are commercially available so this aspect is not novel.)\nThe fitle reads, “Bioadhesive Marine Sensors on Diverse Soft Fragile Species”. They say, “Here we\nintroduce a soft hydrogel-based bioadhesive marine sensor (BAMS)….” The original fitle probably\nobscured the contents even more in that a reviewer asked, “ In this manuscript, the authors developed\nbioadhesive marine sensor networks [italics mine] to study individual, group, and mulfi-species\nbehaviors.” The importance of the paper is the adhesive. The sensor is independent of the glue. There is\nno network involved, let alone data on group behaviours. They seem to be suggesfing some sort of tags\nthat communicate with each other. It could be any sort of tag.\nIt seems to me that the authors are combining a number of different objecfives in the fitle and the\nintroducfion in a way that I think will be confusing to the reader. What they are predominantly doing is\ncalling aftenfion to a type of surgical adhesive developed to join or repair soft fissues in a medical\ncontext that may also provide an effecfive way of aftaching things to slippery, flexible, animals.\nImportantly, this adhesive is both stretchy and will bond to wet surfaces. This is a very important\nadvance. Because the glue is stretchy, the animals don’t suffer so much from the compliance mismatch\nbetween the sfiff instruments being aftached and therefore deforming the living fissue causing injury as\nthat animals bend and move. This mismatch can also cause instruments to drop off sooner than they\notherwise would.\nThis could is important advance, well worthy of prominent publicafion. (They perhaps should note that\nthis compliance mismatch is also an important constraint in large, robust animals like dolphins and even\nin seals, where tags can be glued to hair. In such animals, a good compliant, fast sefting glue would really\nuseful too. Big animals bend at scales where larger tags can pull away from the skin or fur causing them\nto come away prematurely. Parenthefically, there are people trying to actually produce flexible\nelectronics that will themselves bend and stretch e.g. . “Flexible Bioelectronic Tag with a Kirigami-Based\nDesign for Crosstalk Suppression in Mulfimodal Sensing”, Qipei He, et al,\nhftps://doi.org/10.1002/admt.202300982)\nBut glue is not the “sensor”; nor is it a “network”. Why conflate these disparate things? This derails a\npotenfially clear simple report of an important idea.\nI think the paper would benefit from being reorganized on the basis of its 3 parts. They should just follow\nthe thought process that must have gone on. Firstly, menfion the surgical glue (and reference that\noriginal paper), then discuss the general characterisfics that make it effecfive in soft fissue repair. Then\nthey should note that these characterisfics are useful for an applicafion in an enfirely different realm, i.e.\nanimal biotelemetry, where its use for aftachment to soft bodied animals will make possible studies that\nare presently very difficult or unfeasible. Then descripfion of the glue and its characterisfics including its\ncompliance and the tesfing of mechanical properfies should follow in turn followed by, a descripfion of\nthe laboratory tank tesfing on a variety of animals. This secfion should provide more informafion,\nincluding a clear description of the esfimated how long the tags would stay on the animals. After all, this\nis the first quesfion someone designing a sturdy using the glue would ask.\nThey say, “Due to the soft and robust characterisfics of the adhesive interface, the “BAMS” can be\nreliably integrated with fragile aquafic animals, such as squid and jellyfish, for up to 3 days,\nallowing long-term animal behavior monitoring (Fig. 2k). Does this mean that 3 days is the\nmaximum fime the bond will last? How about the actual data on aftachment fime on the different\nanimals. This is what pracfifioners will want to know, not the data on ODBA etc. In general, the data from\nthe tags a is not the important part of the paper, only serving as an example of potenfial uses. Anyway, it\nis not presented in a biologically meaningful way. It is just an anecdotal account of what tags might record\nif used with this attachment method. I guess reporfing the ODBA results shows that the mounfi8ng is not\nso compliant that it damps out the accelerafion signal to a degree that obscures indicafions of animal\nacfivity but that is not the point that the text makes. It suggests different animals wiggle in different\nways, not much more than that.\nFigures 3 and 4 serve to show how tags might be used. The authors say in Fig 4. , “Group and\ncommunity behavior for marine animals equipped with the BAMS. a, Schemafic illustrafion of large-scale\nmulfi-species biologging experiment. Skate, squid, lobster, and flounder were placed in a large saltwater\ntank (318,100 liters), and roughly half of the individuals of each species were equipped with the BAMS”.\nAgain, this is not really a bi logging experiment to study animal behavior, rather it is an example of the\nsorts of animals on which that the aftachment adhesive might be used. The value of the detailed data\nserve only that the aftachment works. There is not natural community to study here.\nAnd finally, Fig 5 provides a short descripfion of the field test, and its value is primarily to show that the\nadhesive can be used in the field. It would have been useful to go into a bit more detail of exactly where,\nwhen and how the adhesive was prepared, stored and transported to where the animals were caught.\nThe details of the data obtained during this test is of liftle relevance to the main value of the paper,\nwhich is purely the development and tesfing of the glue. The tag could just as well been a mock up. A\nsingle depth profile of light level and associated accelerafion is of liftle significance in its own right. Here,\nthe figure simply provides an example of how the aftachment might be used.\nThere should be more discussion of the mechanics of the bond as it decays over fime due to\nbiodegradafion. The most important thing missing for me was missing for me was the detail on how long\nthe tags would have stayed on of they were not acfively removed and the state of the fissue after the\naftachment falls or is pulled off. In the tanks, were the tags acfively removed or left on unfil they\ndropped off? I understand that there was an issue with maintenance of the squid in capfivity, but how\nlong were tags left aftached? Were they acfively removed? Were the mechanical properfies of the glue\nchanged by longer exposure to sea water? What did the scales or skin of the animals look like after\nforced or “eventual” detachment? These are the sort of details that I think the bio-logging community\nwould like to hear more about so they could befter understand what sorts of studies the glue would\nfacilitate.", "reviewer_4_followup": "Comment 1. I was asked by the editor to comment on the author’s responses to Reviewer 2 to\nsee if I thought they adequately dealt with the reviewer’s concerns. The reviewer produced 3\ncomments. The first was a statement praising the work. It required no significant reply and the\nauthors express thanks for the praise.\nComment 1 from initial Reviewer 2. Species natural behaviour is very hard to study in the\nmarine environment. The field relies on methods that document data under natural conditions\nwhen the human observer is absent. Tagging and biologging is a field in marine science that is\nrapidly advancing due to the development of ever smaller tags that can be used to track fish,\nsharks and cetaceans. However, a missing link in the field of biologging is the use of tags on\nsoft bodied organisms such as molluscs and gelatinous organisms. These are abundant and\necologically pivotal taxa but their delicate bodies make it hard to attach tags to. Advancing our\nunderstanding of these bodied marine species relies on technological developments such as\npresented by Zhao et al. The authors present a new adhesive methodology which allows rapid\nand traumaless attachment of electronic tags on marine invertebrates. The authors describe the\ntesting and adhesion procedure in great detail and even present very interesting preliminary\ndata obtained by tagging various organisms in tank tests, to guide future research. I find the\nstudy very interesting, well prepared, well written, detailed and it surely breaks new ground in\nthe field of biologging.\nResponse 1. Thank you for your time to review our revision manuscript and supplementary\ninformation and confirming that we address Comment 1 from initial reviewer 2\nComment 2. The second raised two questions: They pointed out that the authors did not explain\nhow they “obtained the tag”s or removed the tags from the animals to recover the data. Im was\nnot certain if the review want to know the source of the electronic s they used, i.e commercially\nsourced or specially custom built in houseI to on not certain but is seems that the answer might\nbe some of both. . I am aware of several suppliers of similar recording instruments.\nThe authors responded to this comment by adding a significant new subsection to the paper that\nexplains the field procedure in more detail and that included an informative short video of the\nanimal being tagged and released. They explained that the tag (which record, rather than\ntransmit, the data they collect) was “released from the animal via a galvanic release system, and\nthat they “recovered the tag via a radio signal output”. They also added a new figure that\nprovides a pictorial schematic of the field process as well as the informative video. I expect that\nthis might satisfy the reviewer.\nComment 2 from initial Reviewer 2. A major problem is that the authors do not explain how\nthey obtain the tags or remove the tags from the animals to obtain the data. Do the animals\nsurvive after removal?\nResponse 2. Thank you so much to confirm our newly added experimental data and video,\nwhich might satisfy the Comment 2 from the initial reviewer 2.\nComment 3. but, if it were me, I would like to have a bit more detail, particularly on the detail\nof the preparation of the adhesive. The section of the paper captioned “Preparation of the\nadhesive interface” is key to enabling practitioners to use the attachment approach. It is brief\nand, as someone not schooled in such engineering, I would need some further discussion about\nthe process, the rationale for the various steps and potential pitfalls and criticalities before I\nattempted to use it.\nResponse 3. The particular part of the methods section was enhanced with more detail on the\npreparation of the hydrogel adhesive. Explanations and potential pitfalls for some of the key\nsteps were also included.\nComment 4. Reviewer 2 also asks, “Do the animals survive after removal”. The authors suggest\nthat they do, in the short term. There is no data on long term effects, if any. This would of course\nbe very useful, if available. One thing that was not made clear is whether, after release of the\nrecording package, what remains on the animal. If so, how long will it remain attached and how\nmight it affect the tissue during that time. I would have liked more detailed info on the removal\nof the adhesive as tghey attempted to show in Sup. Fog. 6. I did not find the images very helpful\nso perhaps they could provide some clearer images or some diagnostic discussion of any\napparent injury that might have resulted from pressure, shear or necrotic tissue under the\nattachment.\nThe 3rd comment I guess was driven by a lack of any field study in the original manuscript so\nthis whole new study and the associated text and figure should make it clear that the use of the\nattachment method is feasible in the field.\nComment 3 from initial Reviewer 2. Also I would like to have seen a discussion or an example\nset up how this new technology could be used in nature. Or if it is not possible to apply this\ntechnique it in nature, the authors should explicitedly state so. In general, the authors do a\ngreat job listing the advantages of this approach, but they do not present a realistic view on the\nreal application and its limitations. Therefore the manuscript is incomplete\nResponse 4. Thank you for confirming that the newly added field study makes the Comment\n3 from initial reviewer 2 clear.\nIn terms of the survivability after removal, marine animals survive and behave normally\nafter detachment, and no adhesive remains on the animal after detachment. Tagged and tag-\ndetached animals survived just as long as untagged animals, and showed no noticeable change\nin behaviors. Squid continued to school with untagged animals and fishes continued to swim,\nfeed, and hide in shelters. Note that squid caught from sea and farmed in experimental\nenvironments typically survive for roughly 7 days, due to the inherent issues and complications\n(i.e., skin damage from swimming into tank walls). The attachment and detachment of the\nsensors via bioadhesive interface does not reduce squid survival time. The adhesive interface\nallows 3-day attachment on live squid. In our experiments, we did not attempt to remove the\nadhesive from a live animal, all samples were left to detach on their own. In the field study, the\nsensor detached from a base with a programmed time release. Although not possible to observe\nin the wild, based on our evidence, the base would have remained on the animal until the\nadhesive failed, at which point the base would fall off the squid with the adhesive on it.\nComment 5. Some gratuitous comments from my own reading of the paper. For me, the key\naspect of this paper is the report on a potentially very useful adhesive. I don’t view that data\ncollected on the animals as particularly useful. To me, Its function in the paper is simply an\nexample of how the adhesive might be used for attachment of instruments using the adhesive\non animals with a variety of integuments.\nThe adhesive seems similar to some that has been developed and used previously in surgical\ninterventions on wet, soft tissues and that have advantages over conventional suturing and other\ntissue glues like cyanoacrylates e.g. DOI: 10.1126/science.abo2542; doi:\n10.1016/j.bioactmat.2021.10.001; https://sanaheal.com/ .\nHere the authors show it is also suitable for attachment of instruments to soft bodied marine\nanimals. The limitations of existing methods and the importance of finding better attachment\nmethods is appreciated by the biologists studying such creatures and this is an important new\napplication of the medical methodology in this new realm.\nResponse 5. Thank you for the feedback. While the bioadhesive material compositions are\nadopted from the strategy previously developed in this lab group, we presented several\nimprovements and insights in this work from a material perspective. 1) We translate the\nadhesive hydrogel from biomedical applications to an entirely new field – marine animal\nbiologging applications. The robust and ease of hydrogel adhesive technology is systematically\nevaluated in the marine environments, which have not been covered previously and will boost\nthe applications of biologging. 2) We modified the adhesive hydrogel to be ready integrated\nwith a variety of marine sensors, showing how this material could be widely integrated with\nexisting systems.\nAs suggested, we revise the title and manuscript accordingly to highlight the novelty of\nbioadhesive interface instead of marine sensors. We also respectively point out that real-time\nsensing data collected from various marine species provide representative examples and more\nopportunities for future researchers in the field of biologging and beyond to 1) identify animal\nbehaviors, 2) estimating orientation, and 3) collect environmental data to contextualize\nbehaviors. Therefore, seamlessly and easily collecting various data from soft marine animals\nhighlights the novelty and importance of this work.\nComment 6. But the paper seems to conflate two objectives. One is the description of the\nadhesive, its preparation and mechanical testing via actual application to a set of animals in the\nlab where they can be observed for a time to assess the efficacy of the attachment; the other is\nto demonstrate that the methodology is applicable in the field by providing an example of how\nit might be used on a soft-bodied animal, a squid, with a particular data recording device that\nrecords data on depth, acceleration and light level. (Such devices are now often used and I\nbelieve are commercially available so this aspect is not novel.)\nThe title reads, “Bioadhesive Marine Sensors on Diverse Soft Fragile Species”. They say, “Here\nwe introduce a soft hydrogel-based bioadhesive marine sensor (BAMS)….” The original title\nprobably obscured the contents even more in that a reviewer asked, “ In this manuscript, the\nauthors developed bioadhesive marine sensor networks [italics mine] to study individual, group,\nand multi-species behaviors.” The importance of the paper is the adhesive. The sensor is\nindependent of the glue. There is no network involved, let alone data on group behaviours. They\nseem to be suggesting some sort of tags that communicate with each other. It could be any sort\nof tag.\nIt seems to me that the authors are combining a number of different objectives in the title and\nthe introduction in a way that I think will be confusing to the reader. What they are\npredominantly doing is calling attention to a type of surgical adhesive developed to join or\nrepair soft tissues in a medical context that may also provide an effective way of attaching\nthings to slippery, flexible, animals. Importantly, this adhesive is both stretchy and will bond to\nwet surfaces. This is a very important advance. Because the glue is stretchy, the animals don’t\nsuffer so much from the compliance mismatch between the stiff instruments being attached and\ntherefore deforming the living tissue causing injury as that animals bend and move. This\nmismatch can also cause instruments to drop off sooner than they otherwise would.\nThis could is important advance, well worthy of prominent publication. (They perhaps should\nnote that this compliance mismatch is also an important constraint in large, robust animals like\ndolphins and even in seals, where tags can be glued to hair. In such animals, a good compliant,\nfast setting glue would really useful too. Big animals bend at scales where larger tags can pull\naway from the skin or fur causing them to come away prematurely. Parenthetically, there are\npeople trying to actually produce flexible electronics that will themselves bend and stretch e.g. .\n“Flexible Bioelectronic Tag with a Kirigami-Based Design for Crosstalk Suppression in\nMultimodal Sensing”, Qipei He, et al"}, "author_response": ""}]

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