VOL. 5, NO. 4, APRIL 2021
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Sensor systems
An Accelerometer-Based Sensing System to Study the Valve-Gaping
Behavior of Bivalves
Parvez Ahmmed1*
, James Reynolds1*
, Jay F. Levine2 , and Alper Bozkurt1**
Department of Electrical and Computer Engineering, North Carolina State University, Raleigh, NC 27695-7911 USA
Department of Marine, Earth, and Atmospheric Sciences, North Carolina State University, Raleigh, NC 27695-8208 USA
∗ Student Member, IEEE
∗∗ Senior Member, IEEE
Manuscript received December 3, 2020; accepted March 2, 2021. Date of publication March 19, 2021; date of current version April 15, 2021.
Abstract—Bivalves are extremely sensitive to environmental conditions. The movement of their shells and the gap inbetween the valves can serve as indicators of water pollutants entering surface water bodies. This letter proposes a
novel sensing system to accurately calculate the valve-gaping angle in bivalves. The sensor unit is comprised of two
inertial measurement units for each bivalve to estimate the angle between the two valves. Monitoring of multiple bivalves
is possible with several water-insulated sensor units tethered with flexible cables to a central base station housing the
processing unit. Miniaturization of the sensor packaging and flexibility of the wires ensured minimum hindrance to the
animals’ natural behavior. The precision and accuracy of the angle measurement were tested with a benchtop servo
motor setup simulating the gaping behavior. The standard deviation of measurements at a steady state was 0.78◦ , and the
average change in measurement during a 10◦ step was 9.98◦ . Over 250 h of in vivo validation experiments demonstrated
the consistency of the angle measurements using the presented method alongside a magnetic alternative, which had
an average correlation coefficient of −0.89. The sensor system provides an accurate study of bivalve gaping behavior
and facilitates the potential use of bivalves as environmental sentinels due to their valve-gaping being a biomarker for
monitoring water pollution.
Index Terms—Sensor systems, accelerometers, angle measurement, biomarkers, bivalves, freshwater mussels, gaping.
I. INTRODUCTION
Bivalves are indispensable keystone species in aquatic environments. They feed by extracting suspended food particles from the
water column, including algae, bacteria, and detritus. Shell movement
or valve-gape, as controlled by the anterior and posterior abductor
muscles, reflects the natural filtration behavior of freshwater bivalves.
Water enters the mantle cavity of the bivalve through an inhalant
(incurrent) siphon, and crosses the gills where particles are removed by
cilia and transitioned to the stomach. The water moving over the gills
is also used for oxygen uptake and respiration. Finally, the water leaves
the body through a second exhalant (excurrent) siphon. The opening
and closing of the valves mainly occur for the purpose of water intake,
feeding, and reproduction. However, noxious chemicals in the water
column may prompt valve closure and changes in the valve-gaping can
serve as a suitable biomarker for ecotoxicological research [1].
As natural filter feeders, bivalves play a significant role in maintaining the ecological balance, but their filtration makes them vulnerable
to health effects associated with ingested water pollutants. North
America’s diverse freshwater mussel (Bivalvia: Unionidae) fauna are
imperiled throughout much of their natural range. Changes in riparian
land-use, erosion (resulting in sedimentation), and chemical contamination have driven the decline of freshwater mussels. Their global
Corresponding author: Alper Bozkurt (e-mail: aybozkur@ncsu.edu).
(Parvez Ahmmed and James Reynolds contributed equally to this work.) Associate Editor: G. Langfelder.
This work was supported in part by the National Science Foundation under Grant
ECC-1160483 and Grant CCSS-1554367 and in part by the U.S. Fish and Wildlife
Service under Grant 2018-0535/F18AC00237.
Digital Object Identifier 10.1109/LSENS.2021.3067506
decline has prompted active conservation measures [2], [3]. Moreover,
continuous monitoring of their behavior has proven to be a useful
means of detecting the presence of contaminants in surface waters
and, thus, has prompted their use as environmental sentinels [4]–[6].
Previously studied physiological indicators for monitoring bivalve
behavior include cardiac activity [7], [8], estimated filtration volume [9], [10], and gaping behavior [11]–[15]. Among these, the
valve-gaping behavior is responsive to chemical contaminants and
environmental parameters [16]. Bivalves in surface waters feed asynchronously. However, they generally close their valves when a noxious
event or chemical is impacting their stream habitat and the valve
closure due to these events may be synchronous among individuals.
Valve-gape measurement provides an opportunity to identify these
habitat-altering events, potentially serving as an early-warning indicator [17], [18]. At least three different methods for direct registration of
the gaping angle exist in the literature. First, electromagnetic induction
has been used for estimating the gaping angle [11], [12] by attaching a
coil structure on each side of the valve and using the induced voltage
to indicate the distance between the valves. Alternatively, Hall effect
based sensors have measured the magnetic field strength to estimate
the gaping through the placement of a magnet on one valve and a
magnetometer either on the other side or above the shell [13]–[15]. A
method using optical fibers has also been demonstrated with limited
use in a laboratory setting [19].
Both the electromagnetic induction and the Hall effect based sensors
provide limited accuracy for monitoring the gaping angle. These
methods estimate the separation between the valves by measuring
a parameter related to the opening distance. The related conversion
schemes are often nonlinear and require polynomial fitting [20]. These
measurements also depend on the consistent positioning of the devices
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VOL. 5, NO. 4, APRIL 2021
Fig. 2. Illustration of two reference frames measuring the same physical quantity and the subsequent calculation of the angle between the
two frames.
Fig. 1. (a) Block diagram showing the connection of four sensor nodes
in relation to the data collection system. (b) Picture of a freshwater
mussel with the sensors and a magnet attached on the shell using the
custom adhesive. The inset shows the dimension of the board housing
the accelerometer.
on the shell (i.e., distance from the hinge) and require calibration for an
accurate angle estimation. Some of the earlier approaches required the
mussels to be fixed in place on a pedestal located below the sensor [11],
[14]. Magnetometer-based gap readings can also be affected by natural
magnetic fields that are unique to a geographical location and require
further calibration.
Here, we describe a new method using two accelerometers to
estimate the gaping angles while mitigating the aforementioned measurement limitations. The advantage of using accelerometers lies in
their ease-of-use and the universality of the measurement. We also
present a novel system implementing this method to facilitate valvegaping monitoring in the field. We evaluated the precision, accuracy,
and durability of the system in simulated field conditions. In vivo
experiments with freshwater mussels show the comparison between
various inertial measurement (i.e., magnetometer and accelerometer)
based gaping estimations.
II. SYSTEM OVERVIEW
The overall system is comprised of four sensor nodes connected to a
base station enabling the recording of gaping data from four bivalves in
parallel [see Fig. 1(a)]. The tethered system facilitates in situ monitoring of bivalves in their native habitat. The core of the system is a single
board microcontroller (Adalogger, Adafruit Industries, New York,
NY, USA) with micro-SD card storage. Each sensor node contains
two triaxial accelerometers (LSM303, STMicroelectronics, Geneva,
Switzerland) that are attach to the two shells of a bivalve. A 28-gauge
multistranded cable (up to 10 m long) connects the accelerometer pair
of each sensor node to the base station. Each accelerometer board,
measuring 4 × 5 mm2 , is connected through four wires (two for power
supply and two for I2 C communication). The LSM303 was the smallest
commercially available inertial measurement unit when the system was
designed. It has a triaxial magnetometer along with the accelerometer,
enabling us to perform a comparative study with the same device.
While the chip has SPI capabilities, the system uses I2 C because of
the reduced number of cables required and the better reliability of
I2 C for communicating over long cable lengths. However, the device
has a fixed I2 C address, requiring an I2 C multiplexer (PCA9547, NXP
Semiconductors N.V., Eindhoven, The Netherlands) at the base station.
Although the current prototype contains one multiplexer, the base
station can have up to eight multiplexers, each of which can connect to
eight accelerometers (i.e., four nodes). The embedded program polls
the sensor nodes sequentially to collect raw sensor data periodically. It
then calculates and stores the gaping angle for each mussel connected
to the system.
The sensor board along with the electronics is insulated for underwater operation, utilizing a layer of synthetic rubber (GB Liquid Tape,
Power Products, LLC, Menomonee Falls, WI, USA) and polyurethane
(Seal Coat Clear Urethane Coating, CRC Industries, Horsham, PA,
USA) to form a thick encapsulating layer. After curing, the encapsulated boards are sealed with heat shrink to protect the devices from
abrasion. This readily-available and low-cost solution strengthens the
wire connections to the board and reduces the probability of mechanical failure while retaining its overall flexibility.
We evaluated two materials for attaching the sensor node to the
shell of the bivalve. Initially, an off-the-shelf adhesive (i.e., ethyl-2cyanoacrylate as a fast setting and water-resistant material) provided a
simple means of attaching the sensors to the shell. However, the layer
formed by the adhesive made sensor removal difficult and damaged
the shell surface. Although acetone could be used for dissolving and
weakening the glue, it would also expose the mussel shell to the solvent.
Alternatively, we used a custom adhesive by mixing silicone (GE
Silicone 1, General Electric Company, Boston, MA, USA) and corn
starch [see Fig. 1(b)]. The corn starch reduces the curing duration to
approximately 5 min. This mixture bonded to the shell with enough
strength to resist environmental forces and withstand natural mussel
movement. During detachment, it came off of the shell easily without
leaving any residue or effects. The mixture can also be dyed to match
the color of the shell for a more natural appearance during field
experiments.
III. EXPERIMENTAL METHODS
Triaxial accelerometers measure the acceleration due to gravity in
steady state and express it as a 3-D vector. Two accelerometers placed
on the two shells of a bivalve measure the same vector from different
frames of reference, as shown in Fig. 2. Thus, the angle (θ) between
those two vectors (g1 and g2 ), which is related to their dot product by
(1), is the same as the angle between the two reference frames, therefore
the two shells. Hence, the gaping angle can easily be calculated using
(2)
cos θ =
g1 · g2
|g1 ||g2 |
θ = cos−1 (1)
g2x1
gx1 gx2 + gy1 gy2 + gz1 gz2
.
+ g2y1 + g2z1 g2x2 + g2y2 + g2z2
(2)
We tested the precision and accuracy of this calculation in two ways.
First, the accelerometer pair was positioned at an angle of 60◦ on a
stationary mount. The resulting measurements determine the inherent
variation in the system due to noise. Second, a servo motor with a
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VOL. 5, NO. 4, APRIL 2021
Fig. 3. Tethered mussels in a large tank with an aquatic environment
similar to that of its natural habitat.
positional accuracy of 0.14 ± 0.42◦ (DS3218MG, DSSERVO, China)
varied the angle between the two accelerometers from 0◦ to 180◦ in 10◦
increments to mimic the gaping behavior. These in vitro measurements
simulating bivalve gaping determined the overall accuracy of the
system.
To test the underwater longevity of the devices, we subjected
four systems to an accelerated aging testing with harsher conditions.
This accelerated aging process, based upon industry standards [21],
involved immersing the devices in a saline solution at 60 °C. The
real-time equivalent is estimated with a Q10 of 2 and an ambient
temperature of 25 °C.
For the in vivo validation, we attached the sensors and magnets
on the freshwater mussels (Elliptio complanata) as a model bivalve
and left them in a 150-gal (0.57 m3 ) tank of municipal water (see
Fig. 3) containing sodium thiosulfate as a nephroprotective agent and
an antifungal drug (invertebrates are exempt from animal welfare
regulations). Data from two accelerometers and one magnetometer
were collected from each mussel. The data were recorded every 60 s
and stored in the micro-SD memory card. These measurements reflect
the natural gaping behavior (shell valve movement) of the mussels.
We also implemented an additional test to compare the
accelerometer-based measurement with magnetic field measurement
as it was previously reported in the literature. We performed simultaneous gaping estimations using both the accelerometer and magnetometer housed in the same inertial measurement unit. For this, a small
magnet was placed on one of the shells [see Fig. 1(b)], whereas the
magnetic field was measured from the LSM303 on the opposite side.
IV. RESULTS AND DISCUSSION
On the stationary mount and with the servo motor, the angle measurement had a standard deviation of 0.78◦ and a range of 4.27◦ with a
sample size of 200. A four-sample moving average applied to the data
resulted in a typical error due to random noise of 0.39◦ . This drops to
0.20◦ with a 16-sample average. When adjusted by 10◦ increments, the
average incremental difference across 537 averages (i.e., 16 samples
each for a total of 9129 samples) was 9.98 ± 1.11◦ . The maximum
and minimum average differences between the measured and actual
angles were 1.89◦ and −1.74◦ , respectively (see Fig. 4).
Four of the encapsulated accelerometers were subjected to 72 h
of accelerated aging, which is a real-time equivalent of one month,
representative of a typical experiment duration. All four of the devices continued to function as expected. The polyurethane lost its
5500404
Fig. 4. (a) Distribution of 200 measurements at a fixed angle relative
to the mean, demonstrating the precision of the system. (b) Accuracy
of the system shown by the difference between the measured angles
and the actual angle set using a servo motor.
Fig. 5. Experimental data showing measured angles from each of the
accelerometer pairs.
transparency and had a white sheen to it, but the overall integrity of
the encapsulation was visually and functionally unaffected. Although
the equivalent duration of one month is sufficient for our targeted
application, we continued the aging experiment beyond the initial 72 h.
The first device errors began after a real-time equivalent of 42 days.
For extended deployments, the devices can be coated with a thin layer
of poly-monochloro(para-xylylene) or Parylene-C through vacuum
deposition. This optional step reinforces the electrical insulation and
moisture isolation but increases the fabrication steps and costs.
We performed eight experiments for gape measurements in the
laboratory setting with an average recording time of 2.4 days. The
gape angle corresponding to the initial state of the mussels when they
were immersed into the water was adjusted to 0◦ . A four-measurement
average followed by a 60-point mean window function removed noise
from the signal. The minimum angle was −3.6◦ , and the maximum was
33.6◦ . The average angle was 4.5 ± 3.86◦ (N = 8), which is highlighted
in Fig. 5. The data demonstrated the mussels opening up their shells
within the first 6 h of being immersed. Baseline data collected from
individual animals indicated that the feeding behavior would typically
be asynchronous. Although further investigation of mussel behavior
is beyond the scope of this letter presenting the sensor system, a
single noxious event would potentially prompt synchronous closure by
multiple animals. In this manner, the accelerometer-based valve-gape
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VOL. 5, NO. 4, APRIL 2021
REFERENCES
Fig. 6. Representative data showing a comparison between the magnetic field strength and the angle calculated by the accelerometers.
monitoring system may serve as a nonspecific indicator of chemical
and other pollutant inputs.
The theoretical advantage of the accelerometers over magnetic sensors is also demonstrated by the experimental accuracy and precision
of the system. Across over 250 h of data, the correlation coefficient was
−0.89 ± 0.11 (Pearson, N = 6, robust linear regression smoothing).
The negative correlation, seen in Fig. 6, reflects the inverse relationship
between the two parameters. As the gape angle increases, the magnetic
field strength decreases. The differences between the two can be the
result of a variety of factors. The change in field intensity may not
be linear, so the magnetometer is less sensitive to changes at larger
angles. The magnetometer is also susceptible to external interference
from electronics, the environment, and the magnets on neighboring
mussels.
V. CONCLUSION
An accelerometer-based angle measurement provided a useful alternative to previously reported methods for registering the shell valve
movement (gaping) of a bivalve. We demonstrated a tethered sensing
system that can monitor multiple bivalves with a standard deviation
of 0.78◦ and 1.11◦ during the steady-state and step-change scenarios,
respectively. The current packaging of the system allows for more than
a month of operation, which can be further extended by the deposition
of extra insulation materials. In vivo measurements on freshwater
mussels indicated both the practical functionality of the system as
well as its superior performance with respect to magnetic-field-based
measurements. This system thus allows for more extensive studies of
bivalves to better understand their behavior and possibly the factors
contributing to the decline of freshwater mussels in nature.
ACKNOWLEDGMENT
The authors would like to thank C. Eads for arranging the in vivo experiments and M.
Yokus for helping in encapsulating the boards.
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