Review Article |
Corresponding author: Alexandra Meira ( alexagmeira@gmail.com ) Academic editor: Eric Larson
© 2024 Alexandra Meira, Francisco Carvalho, Paulo Castro, Ronaldo Sousa.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Meira A, Carvalho F, Castro P, Sousa R (2024) Applications of biosensors in non-native freshwater species: a systematic review. NeoBiota 96: 211-236. https://doi.org/10.3897/neobiota.96.128038
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Technological advances have boosted the ability to obtain large and high-quality ecological data. These new technological tools have the potential to rapidly develop knowledge on how species behave and interact in ecosystems at relevant spatial and temporal scales. Comprehensive time-series datasets on the in situ behaviour and dispersal of wild organisms are essential for addressing fundamental ecological and physiological questions regarding non-native freshwater species. In this review, we address how biosensors, hereby defined as a tool for electronic tagging and tracking, can be useful in assessing movement, internal states and behaviour in non-native freshwater species, plus information about the surrounding environment and discuss possibilities of future research.
We performed a systematic review of the available literature and retrieved a total of 132 scientific studies (from 1996 to 2023) detailing 140 examples of sensor use. Most studies used radio telemetry (40%; n = 53) followed by acoustic telemetry (34%; n = 45) and PIT telemetry (20%; n = 26) to study non-native freshwater species. The taxonomic group most studied was fish (72%; n = 109), followed by crustaceans (14%; n = 21) and amphibians (5%; n = 8). The most addressed topics included species behaviour assessment (72%; n = 101), species physiology (10%; n = 14) and management (9%; n = 12). As expected, the number of studies noticeably increased since 2006, with the majority performed in North America (55%; n = 73), followed by Europe (30%; n = 40) and Oceania (7%; n = 9). Information provided by biosensors can be used to better understand the dynamics and impacts of cryptic non-native species and can be applied in the management of biological invasions.
We also addressed future directions concerning the use of biosensors in non-native freshwater species (e.g. underwater internet systems, artificial intelligence, crittercams). Overall, these technologies provide unique possibilities in the field of biological invasions in freshwater ecosystems and the development of new technologies to address their limitations will increase the amount and reliability of the data gathered to provide information for management actions.
Biologger, biosensor, conservation, freshwater, invasive species, management, telemetry
The introduction of non-native species has dramatically altered terrestrial and aquatic ecosystems and is now an important driver of biodiversity change, requiring enormous resources to manage their impacts (
The growing number of species introduced to freshwater ecosystems and their subsequent establishment highlights the urgent need for more effective measures to monitor and manage these species (
Technology has helped to overcome some of the field monitoring challenges described above by remotely measuring key ecological features of species. Technological advances in the last decade have allowed the development of new tools, enabling us to gather larger amounts and higher-quality data that can accelerate our knowledge of how individuals, populations and communities behave and interact in ecosystems (
New technological solutions are now increasingly available to better understand non-native species ecology and biosensors may be particularly useful (
We reviewed the bibliography available concerning the use of biosensors in non-native freshwater species to assess: i) spatial-temporal patterns of published studies; ii) the breadth of the type of sensors used; iii) and most studied taxonomic groups. We also discussed and provided preliminary insights on the potential application of these devices in advancing our understanding of freshwater biological invasions in the future.
A scientific literature search was conducted using Web of Knowledge (www.webofscience.com) for published research including non-invasive sensors (i.e. sensors that do not impact species’ physiology, behaviour or survival) and non-native species. While our search was conducted using Web of Knowledge (WoS) and different search bases may not cover the same publications, increasing bias, WoS provides various advantages (
Each study was classified by sensor type used (e.g. acoustic telemetry, heart sensor, infrared sensor) and function (i.e. what it had been used for) (Table
List of sensor types and function categories used in the retained studies.
Sensor type | Function |
---|---|
Acoustic telemetry | Behaviour |
Radio telemetry | Interaction |
PIT telemetry | Management |
Hall sensor | Methodology |
Heart sensor | Monitoring |
HPV system | Physiology |
Inductive proximity sensor | |
Infrared sensor | |
Micro acceleration data loggers | |
Pop-off tags | |
Pressure sensitive tags | |
Thermal dissipation sensor | |
Time-depth recorder |
The number of papers published per year on the subject was plotted between 1996 (the year of the first record) and 2023 and a Sankey diagram was generated to illustrate the linkage amongst records on different sensor types, output and functions, based on the taxonomic group, using the R-package “networkD3” (
After excluding records that did not match our criteria (i.e. studies not focusing on freshwater or riparian non-native species using non-invasive attached sensors), the final dataset comprised 132 scientific publications. These corresponded to 140 case studies since six publications used more than one sensor. The studies were mostly conducted in rivers (50%; n = 66), lakes (~ 27%; n = 35) and controlled freshwater environment (e.g. laboratory and mesocosms) (~ 8%; n = 11). A total of 14 different sensor types were identified and comprised acceleration data loggers, acoustic telemetry, hall sensors, heart sensors, Heat Pulse Velocity (HPV) systems, inductive proximity sensors, infrared sensors, PIT telemetry, pop-off tags, pressure sensitive tags, radio telemetry, thermal dissipation sensor, time-depth recorder and ultrasonic telemetry. Telemetry-based sensors that transmit data rather than log it on-board were the most well represented, accounting for 125 (~ 95%) studies (Fig.
Linkage amongst the relative quantity of published records using biosensors for non-native freshwater species research by major taxonomic group, type of biosensors used and functions assessed. NA refers to the Chinook salmon (Oncorhynchus tshawytscha) which, despite being a native species, was used to assess the impacts of a non-native predator (see
Studies included in this review were conducted in 22 countries. Most studies (55%, n = 73) were conducted in North America, the USA being the country that contributed the most with 62 studies. Of the included studies, 40 (30%) were conducted in Europe, followed by Oceania with 9 (~ 7%) (all conducted in Australia), Asia with 5 (~ 4%), Africa (South Africa) with 3 (~ 2%) and lastly, South America with 2 (~ 2%). Aside from the USA, the countries that contributed the most with research using sensors in non-native freshwater species were Canada and United Kingdom (n = 11; 8%, each), Australia (n = 9; ~ 7%, each) and the Czech Republic (n = 8; 6%). The other countries published four (~ 3%) or less studies.
Studies performed in North America focused mostly on non-native fishes (n = 73; ~ 76%; eight of the case studies used more than one species), which follow similar trends as reported in the general results (Fig.
Geographic patterns of published studies using biosensors for aquatic non-native species research displayed by taxonomic groups.
The number of studies generally increased over time, with the earliest published paper found in 1996 (i.e.
Number of publications per year on the use of biosensors to study non-native freshwater species. Milestones represent the first record of the use of each identified sensor in a non-native freshwater species.
Studies from North America encompass a greater diversity of sensor types (n = 11). Acoustic, PIT and radio telemetry were the most frequently applied technologies (n = 33, ~ 42%; n = 21, ~ 27%; n = 16, ~ 21%, respectively). Research in Europe was conducted using seven different sensors, with radio telemetry the most used technique (n = 26; ~ 62%). In Oceania (Australia), studies used acoustic (n = 2; 20%) and/or radio telemetry (n = 8; 80%), while research from Africa (South Africa) used either HPV systems (n = 1; ~ 33%) or acoustic telemetry (n = 2; ~ 67%). Studies from Asia used acoustic telemetry (n = 3; 60%) or acceleration data loggers or radio telemetry (n = 1; ~ 33%, each). Both studies conducted in South America used radio telemetry.
As previously mentioned, species behaviour was the most frequent focus of study (~ 72%; n = 101), whether as a unique application of sensors (n = 83) or jointly with another application (n = 18). This category includes the assessment of natural behaviour and natural movement or changes in movement in response to the environment. It was followed by species physiology (n = 14; 10%), species management (n = 12; ~ 9%), species monitoring (n = 11; ~ 8%), which included dispersal dynamics, the development of methodologies (n = 8; ~ 6%) and species interactions (n = 6; ~ 4%).
Considering the geographical distribution of the studies, some bias could be introduced and so some cautions need to be made when interpreting overall results. In fact, each country contains different environments and may be affected by different non-native species, thus displaying different priorities (
In general, accelerometers record acceleration forces in a continuous manner at a defined frequency or a defined time-average of the acceleration, being the data either stored or transmitted (
Acceleration Data Loggers can be attached to non-native species to monitor their activity levels, swimming behaviour and movement patterns in their new environments (e.g.
Acoustic telemetry involves attaching transmitters to animals that emit acoustic pulses. These signals are detected by receivers within the waterbody. The time and location of each detected pulse allow researchers to track the movements and behaviour of aquatic species, allowing to collect high-resolution data over long time periods (
Acoustic telemetry can be used to track the movement of non-native species within freshwater ecosystems, helping to map their distribution, dispersal patterns and habitat use (e.g.
Hall sensors are capable of detecting magnet‐transducer paired magnetic field properties (
By attaching a magnet to an animal, hall sensors can quantify its amplitude, angular velocity and frequency of limb movements, providing insights into energy‐saving mechanisms (
Heart sensors measure the heart rate of animals, typically using electrocardiography (ECG). These sensors are either implanted or attached to the animal to monitor cardiac activity in real-time (
Heart sensors can provide insights into the physiological responses of non-native species to different environmental conditions, such as temperature changes, pollution levels or interactions with native species (e.g.
HPV systems measure the speed at which heat pulses travel through plant stems, which correlates with sap flow and, by extension, water transport and transpiration rates. A heat pulse is introduced and sensors measure the time it takes for the heat to travel through the stem (
HPV systems could be used to study the water usage and transpiration rates of non-native freshwater plants and plants present in the riparian area, providing data on their impact on water resources in freshwater ecosystems (e.g.
Infrared sensors detect infrared radiation (heat) emitted by objects. These sensors can measure temperature or detect movement, based on changes in the infrared radiation patterns, but also measure heart rates (
Infrared sensors could be used to monitor the presence, activity and physiology of non-native species, particularly in nocturnal or low-visibility conditions. They can also be applied to assess physiological responses (e.g.
PIT (Passive Integrated Transponder) telemetry involves the use of small, implantable tags that emit a unique code when activated by a reader’s electromagnetic field. These tags do not require a battery and are often used for tracking and identifying animals. Thus, PIT telemetry can provide individual identification of tagged animals, but requires close proximity to the reader for detection, being also limited to species that can be tagged.
PIT telemetry can be used to monitor the movement, growth and survival of non-native species in freshwater environments. By tagging individuals, researchers can gather long-term data on the population dynamics, habitat requirements and spread of non-native species (e.g.
Pop-off tags are data-logging devices that attach to an animal and are designed to detach at a predetermined time or under specific conditions. Once released, the tag floats to the surface, where it transmits its stored data via satellite (
Pop-off tags could be used to track the movements of non-native species over long distances or periods. Once the tag detaches, researchers can recover valuable data on the species’ behaviour and habitat use, which is useful for understanding their spread and impact (e.g.
Pressure-sensitive tags measure the pressure exerted by the surrounding environment. These tags can provide data on depth and diving behaviour by recording pressure changes over time. They can also record environmental conditions, such as temperature and can be used on a wide range of species; however, these have to dive or change depth frequently (
Pressure-sensitive tags can be used to study the diving behaviour of non-native species in freshwater ecosystems (e.g.
Radio telemetry involves attaching a transmitter to an animal which then emits radio signals. These signals are detected by a receiver, allowing researchers to track the animal’s location and movement in real-time. This type of telemetry is effective for studying various environments and species, but have a limited range, requiring manual tracking and researchers to be relatively close to the tagged animal (
Radio telemetry can be used can be used to monitor the movement and distribution of non-native species in freshwater ecosystems (e.g.
Thermal dissipation sensors measure heat loss from a surface, often used in plant studies to determine transpiration rates. The sensor measures the temperature difference between a heated probe and its surroundings, which correlates with water movement and transpiration (
Thermal dissipation sensors can be used to study the water use and transpiration of non-native freshwater plants (e.g.
Time-depth recorders (TDRs) log data on the depth and duration of an animal’s dives over time. These devices are attached to the animal and record depth changes, allowing researchers to analyse diving behaviour and habitat use (e.g.
Biosensors used to assess movement have the potential to provide information for population dynamics and support predictions on species dispersal at relevant spatial and temporal scales. Movement of non-native species can change with time, environmental conditions and position (i.e. individuals from the core and front of the invasion), such as in the well-known case of the invasive cane toad (Bufo marinus) (
Non-native species adapt to the new conditions of the invaded habitats, including establishing new biological interactions with co-occurring native species. Sensors can be used to assess these new interactions and, for example,
Predation of native species can also be assessed using telemetry-based tags.
The use of sensors has also been applied to assess intra- and interspecific variation regarding environmental conditions. For example, in the United States of America, the movement of the non-native Silver carp (Hypophthalmichthys molitrix) was assessed regarding phenological and environmental factors (
Given the high ecological and economic impacts mediated by non-native species in freshwater ecosystems with no signs of deceleration in the number of introductions for the near future (
The level of development of biosensors identified throughout the studies included and their potential application in the management of non-native freshwater species. The level of development was classified, based on how much is known about the sensor, its user accessibility and how recurrent its application is in the study and management of non-native species.
Regarding prevention, the use of biosensors could give insights into the physiological tolerances of the species. For example, heart sensors have been used to record crayfish survival and recovery rates when exposed to freezing temperatures, providing insight into crayfish adaptability to different environmental conditions (
Managing the expansion of non-native species and assessing their impacts can be very laborious, expensive and inefficient. The Judas technique can be a reliable and efficient way to control and contain these invasions with cost-effective benefits compared to other ways such as fishing permits.
Many improvements and new approaches could be developed to exploit the full potential of biosensors to study non-native freshwater species. In this section, we share our thoughts about future directions concerning this topic following a hierarchical order, from research studies and management actions that can be implemented without new technological advances to more challenging and ambitious directions that still need further technological developments.
The number of studies published on this topic decreased after 2021. Although it has not been apparent from the last two years, possibly due to the constraints caused by the Covid-19 pandemic, it is possible there will be a significant increase in the number of studies published in the future. Despite the limited number of studies using biosensors in non-native freshwater species research, the results of these studies suggest that the use of these tools could be beneficial to investigate how non-native species interact with other global stressors, such as climate change, habitat loss and fragmentation and pollution. For example: how warming may affect the behaviour and impacts mediated by non-native species, especially those species that are poikilothermic; how the presence of physical obstacles in rivers may affect the dispersal of non-native species; and how pollution or land use may influence the physiology and behaviour of non-native species. Similar studies were conducted with native species (e.g.
There is a clear geographical bias in terms of number of publications using biosensors to investigate non-native freshwater species. As referred before, some regions are under-represented, this lack of research applying biosensors to investigate non-native freshwater species being possibly caused by a lack of investment (
Many biosensors have some combination of the following caveats that restrict their applications, such as size/weight influencing smaller species behaviour, long-distance communication, signal interference, battery life, data storage and processing. Although some recent examples already include invertebrates, such as bivalves, in practice, this technology is mainly applied to larger animals. The current bias towards larger species found in the present review could be mitigated through the development of miniaturised sensors. Recent advancements will make this application possible for very small organisms without impairing their normal behaviour. A recent study with terrestrial gastropods showed how millimetre-sized smart sensors can be used in native and non-native snails (
While some well-known and described examples of the use of biosensors in the control of invasive species exist, this type of application is only possible for the management of gregarious species or populations with low individual behavioural variability. For example, when using radio telemetry to assess the spatial behaviour of the invasive Red swamp crayfish (Procambarus clarkii),
In terms of communication signalling, the information gathered is dependent on the presence of deployed structures and is highly impaired by detrimental environmental conditions. For example, radio frequency transmissions underwater can only work effectively at short distances due to their being highly affected by propagation loss, which is conditioned by salinity and temperature, amongst other environmental characteristics (
Apart from the communication of data, there is also the problem of analysis given the amount of data gathered and stored by biosensors. Artificial intelligence (AI) could be used to support the analysis process by modelling or automatically providing information on non-native species movements and interactions using real-time transmissions with live-buoys or satellites. AI is dependent on machine-learning (ML) and has already been applied in ecological studies, such as behavioural studies (e.g.
The use of animal-mounted cameras (crittercams) for identifying and monitoring non-native species represents a promising path for research and conservation efforts. With the integration of AI and ML, the efficiency and accuracy of species identification from crittercam footage could be greatly enhanced and the development of software capable of real-time identification could facilitate the data analysis process and provide suitable and fast feedback for conservation actions. By combining movement sensors, crittercams and ML to develop a method to automatically detect and geolocate behaviour for the flatback turtle (Natator depressus),
By providing real-time and specific biological data, biosensors can contribute to validating and refining models and predictions related to the species studied. Ground-truthing simulations involve validating SDMs or habitat suitability models, the information gathered by biosensors on the physiology, behaviour and location being used to confirm or refute the model’s predictions (
Biosensors have been applied to detect critical environmental situations, such as pollution peaks, acting as early warning systems. For instance, by monitoring shell movement (i.e. closing time, changes in shell movement pattern and changes in valve gape), it is possible to identify the type of stressor or contaminant that bivalves are exposed to and trigger a warning signal (
The technological developments in biosensors in the last two decades provide unprecedented possibilities in the field of biological invasions in freshwater ecosystems. There is a gap in the application of biosensors to study non-native species between different taxonomic groups and bias towards telemetry-based sensors. This is probably caused by the difficulty to capture and adapt biosensors to organisms other than fishes. The potential data collected is also highly dependent on the sensor used, being unfit to serve studies on all non-native taxonomic groups. As telemetry-based sensors are the most developed and used, it is thus necessary to invest in innovation and the development of other sensors more adapted to other taxonomic groups and goals.
Considering the described limitations that biosensors still have, efforts should be prioritised towards the miniaturisation of the devices and the enhancement of battery life and real-time communication systems. The solutions developed should consider the type of study (i.e. species, environment, data, goals, invasion phase) taking into account that they might be appropriate in certain cases, but not in others. However, given the development of new technologies, including AI, underwater internet and the miniaturisation of many devices, future opportunities to monitor and manage non-native freshwater species are numerous. Nonetheless, several caveats and biases are still to be overcome, which include the study of how environmental factors (e.g. turbidity, depth, salinity) and species characteristics (e.g. size) can impair the efficacy of biosensors.
Lastly, the creation of interdisciplinary working groups involving ecologists, engineers, data scientists and policy-makers could promote the development of biosensors more suitable and effective in their applications for ecological research, enabling efficient management of non-native freshwater species.
We thank the suggestions made by Robert J. Lennox and two anonymous reviewers, which improved the quality of our manuscript.
The authors have declared that no competing interests exist.
No ethical statement was reported.
This work was supported by the Portuguese Foundation for Science and Technology (FCT) and the European Social Fund through the North Portugal Regional Operational Programme through a doctoral grant to A. Meira (SFRH/BD/144570/2019). FCT also supported this research through national funds under the project MULTI-CRASH: Multi-dimensional ecological cascades triggered by an invasive species in pristine habitats (PTDC/CTA-AMB/0510/2021) (https://doi.org/10.54499/PTDC/CTA-AMB/0510/2021).
Conceptualization: AM, RS. Data curation: RS, PC, FC, AM. Formal analysis: AM. Funding acquisition: RS. Investigation: AM, RS, PC, FC. Methodology: FC, RS, AM, PC. Supervision: RS. Validation: RS, AM. Visualization: FC, AM. Writing - original draft: AM. Writing - review and editing: AM, RS, FC, PC.
Alexandra Meira https://orcid.org/0000-0003-1133-0825
Francisco Carvalho https://orcid.org/0000-0002-8414-9587
Paulo Castro https://orcid.org/0000-0001-8637-3075
Ronaldo Sousa https://orcid.org/0000-0002-5961-5515
All of the data that support the findings of this study are available in the main text or Supplementary Information.
Search strategy for ISI-Web of Knowledge database and the list of the invasive species studied with the use of biosensors and respective references
Data type: docx
Explanation note: This list compiles all of the retained research papers used in this review.