Magnetic field effects on the behavior of the shrimp Litopenaeus vannamei (Penaeidae)

Abstract

It is known that several animals are sensitive to magnetic fields. Magnetoreception in animals is the ability to sense the geomagnetic field of the Earth and to use their vectorial properties for navigation and terrestrial location. Animals can also show magneto-sensitivity, unrelated to navigation and show changes in behavior during the application of magnetic fields. The aim of the present study was to analyze the behavior of the shrimp Litopennaeus vannamei under the presence of artificial magnetic fields of different intensities under laboratory conditions. Shrimps were chosen because of their economic importance and because they have been neglected in the study of magneto-sensitivity in animals. The laboratory experiments were performed with the use of a pair of circular coils and four aquariums (three treatments and a control, with 20 shrimps each). Our results show for the first time that L. vannamei shrimps are magneto-sensitive, showing a preference to swim against the magnetic field lines direction as is done by magnetotactic bacteria from the Southern Hemisphere. Also, it was observed that the shrimps remain still after the application of magnetic field intensities from 44 to 237 µT, which could be useful for maintaining shrimps in their captive areas.

Keywords:
Magneto-biology; magneto-sensitivity; physical oceanography; shrimp behavior; South seeking behavior

The Earth generates its own magnetic field known as the geomagnetic field (GMF). The GMF is an abiotic component that interacts permanently with living organisms (Skiles, 1985). The influence of magnetic fields on the behavior of marine organisms deserves to be researched, as has been done with fishes (Formicki et al., 2019) and the migration and navigation of other marine animals (Johnsen et al., 2020). Studies of the relationship between magnetic fields and living organisms can be applied to biological security in the strong economic sector of aquaculture. Some great environmental, economic and social problems of aquaculture are the introduction and transfer of cultivated species, as well as disease control (FAO, 2018). The aim of the present study was to investigate experimentally the influence of magnetic fields on the behavior of the shrimp Litopenaeus vannamei (Boone, 1931). That influence could be used as an environmental protection tool in aquaculture, e.g., keeping these animals retained in the ponds at the time of harvesting.

The specimens of L. vannamei were obtained from a shrimp farm located in the municipality of Igarassu, Pernambuco, Brazil. These animals were selected to obtain relatively homogeneous groups in terms of developmental stage (individuals between 9 and 10 cm) and good physical condition (absence of parasitosis, damage to limbs, and deformities). All the experiments were performed in Recife, Pernambuco, Brazil (8º03’14’’S 34º52’51’’W) whose GMF parameters are: F = 26 µT, H = 22 µT, Z = -13 µT. The specimens were transported in thermal boxes to the laboratory. Once in the laboratory, the specimens were transferred to aquariums (23 cm × 40 cm × 50 cm) with water from the original nursery and allowed to acclimate for 72 hours before being submitted to the tests. During the acclimatization period, the same feed and feeding times used on the farm were maintained. To analyze the shrimp behavior as a function of the magnetic field, a pair of circular Helmholtz coils were used to generate a magnetic field inside the aquarium (Fig. 1A). In the central region between the coils, the generated magnetic field can be calculated by the equation:

$$\mathrm{B}={\left(4/5\right)}^{3/2}N\left({\mathrm{\mu }}_0\mathrm{i}/\mathrm{R}\right)$$ (1)

where N ( = 46) is the number of wire turns in each coil; i ( = 0.16 A, 0.31 A, 0.78 A and 1.56 A) is the current intensity; R ( = 0.3 m) is the radius of the coil, and μ₀ is the vacuum magnetic permeability constant. The description of the Helmholtz coils used in the present work can be found in Gonçalves et al. (2009). At the midpoint of the pairs of coils, a 50 cm × 40 cm × 2 cm polished granite base covered with a rubber blanket was used to support the aquarium (Fig. 1). The coils were fed with a variable DC current digital source (MINIPA, model MPL 1303). A compass and a multimeter were also used, respectively, to determine the direction of the magnetic field and to measure the current from the source. During the tests, the current source was kept away from the test and control tanks to avoid any kind of electromagnetic interference.

Laboratory tests were conducted in a closed environment under controlled illumination and temperature (20 ºC). In all, 4 groups of 20 shrimps were used, distributed in 4 aquariums, 3 for the tests (groups 1, 2 and 3) and one as a control (Control group). Each of the three experimental groups was subjected to horizontal magnetic fields of 44, 65, 129, and 237 (T, obtained by the addition of the applied magnetic field (Eq. 1) and the GMF horizontal component. Each test consisted of 30 minutes of observation, the first 10 minutes without exposure to a magnetic field, to determine the initial condition, the following 10 minutes with exposure to a magnetic field, and the last 10 minutes again without exposure to a magnetic field, to observe the test subjects' recovery. After an interval of 30 minutes, a new test was performed with the same group of test shrimps, moving onto the next magnetic field value, and so on until completing the exposure to the 4 magnetic field values. That procedure was performed in groups 1, 2 and 3 to obtain 3 replicates. A webcam was fixed over the test aquarium using an aluminum support and at a height of 55 cm to visualize all the aquarium surface. To observe the preferential displacement of individuals, each aquarium was marked with permanent black pens, in order to subdivide its length into 3 regions (north, central and south), relative to the magnetic field polarity. The camera was connected to a laptop, and snapshot photographic records were taken at intervals of 1 minute during tests. At the same time, the behavior of the organisms was continuously monitored online observing the preferential displacement direction, activity level, time spent in an area of ​​the aquarium, symptoms of stunning, and aggressiveness level. The data obtained were written into electronic spreadsheets to enable their treatment and analysis.

Shrimp mortality was not observed during the acclimatization, testing or post-test periods. The results of the control experiments indicate that L. vannamei shrimps not subjected to artificial magnetic fields tend to occupy evenly the various regions of the aquarium (Table 1, Figure 1B). Under applied magnetic fields, L. vannamei shrimps showed a clear preference for occupying the South region of the aquarium for the 4 magnetic field values tested (Figure 1C, Table 1, ANOVA test: p < 0.05). The treatments accounted for 80.4% of the total variability and the position occupied by shrimps during the experiments for 19.4% of the total variability. There are statistical differences between the average occupation for the North and South regions of the aquarium for all the magnetic treatments, with no significant differences between the different magnetic field values (Tukey's test, Table 1). These results showed the displacement of shrimps from the North to the South regions, meaning that the shrimp swim against the direction of the magnetic field lines.

Table 1.
Average occupation considering the 3 experimental replications, for each aquarium area as a function of the magnetic treatment. The statistical comparison was done between the different magnetic treatments for each aquarium area. Different letters in the columns mean statistical differences.

Magnetic treatment	Aquarium Area
	South	Center	North
Control	37.8a	29,8a	32.3a
44 µT	77.6b	16.8ab	5.6b
65 µT	77.6b	12.3b	10.1b
129 µT	66.7b	22.7ab	10.6b
237 µT	71.7b	21.7ab	6.7b

Figure 1.
A. Homemade Helmholtz coils made to generate the applied magnetic field in the experiments. The cylinders of 60 cm diameter are fixed in squares of wood of 80 cm x 80 cm. Each cylinder has a coil of 46 turns of copper wire. The granite base between the cylinders holds the aquariums with the shrimp during all the experiments. B. Shrimp distribution during the control experiment. C. Shrimp distribution 2 minutes after the application of 44 mT magnetic field. The arrow indicates the magnetic field line direction.

In exposures to a magnetic field intensity of 44 µT, L. vannamei specimens showed some symptoms of aggressiveness: sudden movements, zigzagging and jumping. In the 10 minutes before the exposure of shrimps to the 65 µT magnetic field, a low activity level by the organisms was noted, reflected in rare movements and obvious stunning. When the 65 (T magnetic field began to be applied, the animals once again responded with aggressive reactions, short and abrupt movements and jumping. Subsequently, after the 30 min intervals between tests and during the 10 min period before exposure to the 129 µT level, the shrimp showed a low level of activity and very rare static movements. Upon exposure to the 237 (T magnetic field, the shrimps remained paralyzed, unable to move, except for a slight movement of antennae. This situation remained, even after switching off the magnetic field and a rest period of 40 minutes. That inactive behavior was confirmed in all three replica tests.

The penaeid life cycle involves a planktonic-pelagic period during the larval stages of nauplii, protozoe and mysis, followed by a transition period, called the post-larva, also planktonic-pelagic, and a demersal benthic period, with juveniles and adults (Calazans, 1993). Penaeid shrimps are more pelagic than previously thought and may no longer be benthic when searching for food (Kristjonsson, 1968). The demonstrated magneto-sensitivity could be related to magneto-reception abilities used during navigation in the ocean, once L. vannamei shrimps have the capacity to perform complex displacements, inherent to their life cycle. Our results also showed that shrimps swim against the magnetic field lines. This kind of movement polarity has been observed in South-seeking magnetotactic bacteria found in the Southern Hemisphere, moving against the direction of the GMF lines to get deeper in sediments and to find better oxygen conditions to survive (Abreu and Acosta-Avalos, 2018). For L. vannamei shrimps is not clear why they prefer to swim against the magnetic field line direction. Our results show that the immobility response of shrimps to high magnetic fields (237 μT) can be used to retain these organisms in the nurseries during harvesting, and has the potential to be a great tool to minimize environmental impacts.

In conclusion, our results show for the first time that L. vannamei shrimps are magneto-sensitive, showing a preference to swim against the magnetic field line direction, and that the shrimps remain still under the application of higher magnetic field intensities, following the complete sequence from 44 to 237 µT. This behavior may be useful for maintaining the shrimps in their captive areas.

ACKNOWLEDGEMENTS

CGBG has been supported by the Brazilian research agency CAPES.

REFERENCES

• Abreu F and Acosta-Avalos D 2018. Biology and Physics of Magnetotactic Bacteria. pp. 1-19. In: Blumenberg M, Shaaban M, Elgaml A (Eds.). Microorganisms, London, IntechOpen.
• Calazans D 1993. Key to the larvae and Decapoda of genera of the infraorder Penaeidea from the southern Brazilian coast. Nauplius, 1: 45-62.
• FAO 2018. El estado mundial de la pesca y la acuicultura. Roma, Organización de las Naciones Unidas para la Agricultura y la Alimentación. 250p. 10.18356/37c4c7b4-es
  » https://doi.org/10.18356/37c4c7b4-e
• Formicki K, Korselecka-Orkisz A and Tanski A 2019. Magnetoreception in fish. Journal of Fish Biology, 95: 73-91. https://doi.org/10.1111/jfb.13998
  » https://doi.org/10.1111/jfb.13998
• Gonçalves CGB, Medeiros C, Oliveira Junior J and Lima D 2009. Apparatus for the conduction of laboratory experiments on the effects of the magnetic field upon aquatic organisms. Tropical Oceanography, 37 (2): 30-40. https://doi.org/10.5914/tropocean.v37i1-2.5155
  » https://doi.org/10.5914/tropocean.v37i1-2.5155
• Johnsen S, Lohmann KJ and Warrant EJ 2020. Animal navigation: a noisy magnetic sense? Journal of Experimental Biology, 223: jeb164921. https://doi.org/10.1242/jeb.164921
  » https://doi.org/10.1242/jeb.164921
• Kristjonsson H 1968. Técnicas para localizar y capturar camarones en la pesca comercial. Documentos Técnicos Carpas, 2: 1-69.
• Skiles DD 1985. The geomagnetic field: its nature, history, and biological relevance. p. 42- 102. In: Kirschvink JL; Jones DL; MacFaden BJ (Eds.). Magnetite biomineralization and magnetoreception in organisms: a new biomagnetism, New York, Plenum Press

• Zoobank

  http://zoobank.org/urn:lsid:zoobank.98130045-39AB-476E-AA4D-D9CAA9D8E172

ADDITIONAL INFORMATION AND DECLARATIONS

• Consent for publication

  All authors declare that they have reviewed the content of the manuscript and gave their consent to submit the document. Funding and grant disclosures

• Data availability

  The data that support the findings of this study are available from the corresponding author, CGBG, upon reasonable request

• Funding and grant disclosures

  Not applicable

• Study association

  Not applicable

• Study permits

  Not applicable

Edited by

Editor-in-chief

Christopher Tudge

Associate Editor:

Dr. Antonio Leão Castilho

Data availability

The data that support the findings of this study are available from the corresponding author, CGBG, upon reasonable request

Publication Dates

• Publication in this collection
  29 July 2024
• Date of issue
  2024

History

• Received
  22 Nov 2022
• Accepted
  04 Dec 2023
• Accepted
  0000