Chemistry of Cohesion and Communication in Fish Schools

Keywords: Fish, Shoal, School, Olfaction, Chemosensory, Pheromones, Ocean acidification, Pollution

Abstract

Over a quarter of the world’s fish school at some point in their life; many spend most of their lives apart of these groups. Fish rely on several different sensory systems to communicate and school, including bioluminescence, osmoregulatory, olfactory, gustatory, and chemosensory systems. These sensory approaches are crucial for survival and social interaction; for instance, bioluminescence can attract mates or deter predators, while the olfactory and chemosensory systems are essential for detecting pheromones and environmental cues. Ecological changes caused by heavy metal, pesticide, and many other forms of pollution interfere with the communication pathways required for fish to school and are thus detrimental to their survival. Examining the physiology, communication, and responses of fish to environmental stressors may lead to a better understanding of some of the complex mechanisms behind schooling.

Introduction

Schooling is a distinctive social behavior that first evolved in teleosts (bony fish). It is a type of shoal, defined as an aggregation of fish, but is unique in that fish traveling in a school must do so parallel to each other and at a certain distance apart (Pavlov & Kasumyan, 2000). This structured behaviour allows fish to achieve numerous benefits that are often crucial for the survival of these fish.

Fish in a school learn advantageous reflexes from their schoolmates through imitation and gain greater swimming efficiency by swimming in the vortices created by their neighbours. They are also able to achieve higher defence, better nutrition, and safer migration; the increased number of individuals in a school provides advantages over solitary living. In addition to using pressure waves and electrical signals to detect their neighbors, fish are equipped with many other methods of communication which they rely on to school (readers are referred to Nature’s Aquatic Ballet: The Physics and Synchronization of Schooling Fish for more detail on the advantages of schooling).

To join a school, a fish must be able to identify other schooling fish that are phenotypically similar to itself. For a school to remain cohesive, all individuals must be able to adjust to changes in the movement of their neighbors (Pavlov & Kasumyan, 2000). The mechanisms by which fish detect and respond to these changes are diverse and range from an instinctual attraction based on sight to other similar fish (typically of the same species), to sense of smell and taste to detect chemical signals such as pheromones released by others in the school.

The ability of fish to communicate and receive these chemical signals is largely dependent on the environment. In fact, schooling behavior as a whole is largely influenced by ecological context. Environmental factors are considered to be more significant in the development of schooling behaviors than ancestry (Pavlov & Kasumyan, 2000), and sudden changes to these environments may have negative impacts on the health of fish and their ability to coordinate with their neighbors. 

Physiology

Fish physiology—including the gills, swim bladder, and osmoregulatory and chemosensory systems—is highly adapted to the diverse environments they inhabit. Among these systems, respiration is particularly important as it enables fish to harness energy from their surroundings.

Respiration

Respiration in fish is a complex process facilitated by gills which are crucial to the absorption of oxygen and in supporting cellular respiration. The function of gills along with the metabolic processes involved in cellular respiration enable efficient energy production in fish, powering many other physiological processes necessary for the fish’s survival.

The energy currency of eukaryotic cells, including those in shoaling fish, is Adenosine Triphosphate (ATP), a nucleic acid. Organisms must be able to synthesize the glucose in the food they digest. The chemical equation for cellular respiration is noted below in Figure 1 (Kahwaty & Kahwaty, 2021).

Fig. 1. Chemical reaction for Cellular Respiration (Kahwaty & Kahwaty, 2021).

The first step in cellular respiration is glycolysis which occurs in the cytoplasm of eukaryotic cells. It is an anaerobic process which converts a single glucose molecule into two pyruvates, two ATPs molecules, and two NADH. The pyruvate then goes through an intermediate step while being transported to the mitochondria of the cell. There, it is converted into acetyl CoA and a CO₂ molecule is emitted (Kahwaty & Kahwaty, 2021).

In the mitochondrial matrix, the second step of cellular respiration occurs: the Kreb’s Cycle. This aerobic process releases a CO₂ while synthesizing two ATP, six NADH, and two FADH₂. These compounds are necessary in the third step of the process: the electron transport chain.

Using the inner mitochondrial membrane as a barrier, the electrons from NADH and FADH₂ are used to generate a proton gradient by pumping H⁺ ions into the intermembrane space of the mitochondria. ATP synthase uses this proton gradient to add a phosphate to ADP to make ATP as the H⁺ enters back across the membrane (Fig. 2). Finally, oxygen acts as the last electron acceptor, producing H₂O. Overall, cellular respiration generates about 30 ATP molecules per glucose, contributing to the energy currency cells need to survive.

Though many organisms utilize this evolutionarily conserved process, fish are unique in that they use it while living in an underwater environment. To undergo cellular respiration, they have found a way to obtain oxygen using their innovative gills.

Fig. 2. The electron transport chain and ATP synthase (Kahwaty & Kahwaty, 2021).

Gills

Oxygen is relatively insoluble in water and thus respiration under water requires a much greater amount of energy than respiration in air. As such, fish have evolved a unique system to increase the efficiency of gas exchange under water.

Gills are thin layers of thin, capillary-filled tissue primarily responsible for gas exchange. Water flows in through the fish’s mouth and passes over the surface of the gills as it leaves, allowing oxygen to diffuse into the bloodstream, and waste to diffuse back into the environment (Fig. 3) (Parenti & Weitzman, 2024a).

In order to increase the overall rate of diffusion, thin layers of tissue called lamella are evenly distributed across the gill filaments. Gill filaments are also covered by epithelial pavement cells with microvilli and microplicae structures. In combination, lamellae and pavement cells increase the surface area of the gills (the mean scaling exponent of gill area being 0.76) (Palzenberger & Pohla, 1992) allowing a higher overall rate of diffusion and increasing the efficiency of the gas exchange in gills (Baker et al., 2019; Evans et al., 2005). The rate of diffusion is defined by (Baker et al., 2019):

rate of diffusion = (amount of gas passing through an area) / time (1)

Fig. 3. The water flows through the gills for respiration to occur (Evans et al., 2005).

Bony fish and cartilaginous fish use different methods to pass water over their gills. Cartilaginous fish use ram ventilation, the opening of their mouths during swimming to let water pass (Evans et al., 2005). Cartilaginous fish must be constantly moving for enough water to flow over their gills for them to respire. Bony fish, on the other hand, have evolved the operculum, a special bone that covers the fish’s gills. The operculum allows bony fish to use buccal pumping, meaning that fish actively swallow water in order to push water through its gills. Thus, teleosts do not need to be moving to respire (Parenti & Weitzman, 2024b; Ferry & Hernandez, 2011; U.S. Department of the Interior, n.d.).

In addition to being the site for respiration, fish gills are also a site for metabolism. Toxins, in addition to certain wastes, are also excreted at the gills. Thus, environmental pollutants, such as the 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD), often significantly damage the gills (Evans et al., 2005).

Swim bladder

Fish rely on gas absorption not only for respiration, but also for movement. The swim bladder is a hydrostatic organ found in most modern fish, which allows them to control their depth in water. Special glands release gas, mostly oxygen, into the bladder, which increases the buoyancy of the fish and decreases its depth. When the fish wants to increase its depth in water, the gas is absorbed into the bloodstream, decreasing the buoyancy of the fish (Parenti & Weitzman, 2024a).

Osmoregulation

Fish have adapted to live between opposite extremes of habitat osmodiversity, ranging from desert pools with concentration quadruple that of the ocean (128 ppt) to freshwater pools with nearly no ion concentration at all (Greenwell et al., 2003). Living cells require a constant osmotic environment to function and maintain their structure. While most of the fish is covered in scales and a thin mucus that renders it impermeable to water, the gills of the fish are semipermeable, thin, exposed to the environment, and designed to maximize the area over which gas exchange can occur. The semipermeable nature of gills also allows the transport of water across their membranes (Greenwell et al., 2003).  

The greatest challenge to fish is therefore the regulation of internal water and electrolyte homeostasis in the face of extremely hypo- and hyper- osmotic environments (compared to the bodily fluids of the fish). Marine teleosts reside in hyperosmotic environments which contain a concentration of salt 2-4 times that of the bodily fluids of the fish (1000 mOsm/kg and 250-500 mOsm/kg, respectively). The higher concentration of salt in the environment poses chronic risk of dehydration and salt loading. Conversely, freshwater teleosts, which live in hypoosmotic environments (< 1mM as compared with 150 mM in their bodily fluids), are faced with constant challenges of volume loading, strain caused by excess fluid volume within the fish due to over-absorption of water and salt depletion (Greenwell et al., 2003). The differences in the respective osmoregulatory physiologies of marine and freshwater teleosts help highlight their specialized adaptations in response to their contrasting environmental challenges.

The main purpose of osmotic mechanisms in marine fish is to minimize dehydration through the constant intake of sodium chloride. This is primarily done by drinking seawater (Greenwell et al., 2003). Marine fish typically drink 10-20% of their body weight in sea water per day, though some may drink up to 35-40% of their weight in more saline environments. The ions are then absorbed, transported in a series of ion exchanges, and excreted, allowing for a net gain in total body water but generally no net gain in ions. The absorption and excretion of ions is primarily through the gills, gastrointestinal system, and urinary tract. Approximately 80% of sodium and chloride ions consumed are absorbed in the esophagus, which is impermeable to water, and the gut lumen, which is permeable to both water and monovalent ions, via diffusion along the concentration gradient. Other monovalent and divalent ions such as potassium, magnesium, and sulfate are also absorbed in the gut lumen via Na⁺ -K⁺ ATPase-driven basal membrane pumps and a Na⁺ -K⁺ -2Cl^- cotransporter system. Any excess of sodium, chloride, and potassium ions are excreted via a combination of active transport, cotransport and passive diffusion by mitochondria-rich chloride cells in the fish’s gills. Absorbed divalent ions are excreted by kidneys into the urine, though 80% of divalent ions are not absorbed and are simply excreted in the feces. Urine flow rates in marine fish are low (approximately 1-2% of their body weight) as the water is reabsorbed by the urinary bladder (Greenwell et al., 2003).

The osmoregulation in freshwater fish is designed to prevent overhydration. Due to the hypotonic environmental conditions, a large amount of water is absorbed through the gills—the influx of water may reach roughly 50% of the fish’s body mass per hour. To compensate, freshwater fish drink very little and excrete large amounts of dilute urine, facilitated by the kidneys which rely on high glomerular filtration rates to eliminate large volumes of water. Sodium and chloride ions are completely reabsorbed, facilitated by Cl^- exchange with HCO₃^- in chloride cells and conductive channels driven by proton pumps in the outer cells of the gills. The chloride cells in freshwater fish are also located deeper in the gill tissues than in marine fish, which results in lower ion absorption in freshwater fish, making them more suitable to their hypoosmotic environment (Greenwell et al., 2003).

These adaptive osmoregulatory strategies are vital for the physiological stability and cellular function across a diverse set of aquatic environments. In addition to osmoregulation, fish have evolved various sensory tools to aid in navigating their environment, helping fish to school, even under less favourable conditions.

Flashlight fish and bioluminescence

Vision is the primary sensory basis for schooling; fish rely on vision to imitate the behaviors of their neighbors and respond to predators. In low light, the distance between fish gradually increases and the school eventually loses its structure, and thus schools often dissipate in low light to decrease the risk of predation (Pavlov & Kasumyan, 2000). Flashlight fish (Anomalopidae) are a family of fish that rely on bioluminescence as a light source to remain a school at night (Gruber et. al, 2019). 

Bioluminescence is the emission of visible light by an organism via a chemical reaction (chemiluminescence). The energy released by the oxidation of a luciferin substrate by a luciferase enzyme is emitted as visible light as opposed to heat. Depending on the bioluminescent organism, the luciferin and luciferase involved may differ (Herring & Widder, 2001).

In flashlight fish, a symbiotic bioluminescent bacterium of the genus Vibrio is responsible for the light emitted by the fish. In these bacteria, luciferase is a heterodimer composed of alpha and beta subunits that catalyzes the oxidation of long-chain aldehydes (RCOH) and reduced flavin mononucleotides (FMNH2). The alpha and beta subunits of luciferase are encoded by luxA and luxB genes, respectively. Other luxCDABEG genes encode various proteins that catalyze different steps in the chemical pathways responsible for producing long-chain aldehydes and flavin mononucleotides. These pathways also include the production and recycling of fatty acids and the activation of AMP, an intermediate in ATP synthesis (Fig. 4) (Miyashiro & Ruby, 2013).

Fig. 4. (A) Genes involved in the production (luxA-G) and (B) regulation (luxR and luxL) of luminescence in Vibrio bacteria (Miyashiro & Ruby, 2013).

Vibrio bacteria grow within masses of parallel, specialized tubules in the subocular bioluminescent organs of flashlight fish. These masses of tubules align at right angles to each other and run along the surface of the fish’s light organs (Fig. 5). Stacks of guanine crystals parallel to the surface of the organ are attached to the base of the tubules and act to reflect the light generated by the bacteria (Gruber et. al, 2019). Flashlight fish rotate or cover their light organ (depending on the species) in order to reduce the light output. They frequently rotate or cover and uncover their light organs to expose and hide the bioluminescent bacteria to create brief flashes of light that they use for defense, feeding, communication, and schooling (Gruber et. al, 2019).

Fig. 5. (A) An adult Anomalops katoptron and (B) a macro image of its bioluminescent organ (Gruber et al., 2019).

Chemosensory system

As water is a good solvent, the aquatic environment serves as a perfect medium for the dispersion of chemicals (Ward et al., 2008). Fish can detect minute concentrations of environmental chemicals, such as pheromones, through their chemosensory system, which consists of various types of chemoreceptors. The detection of chemical signals plays a crucial role in the behavior and survival of schooling fish (Sorensen, 1992). There are two major systems for detecting chemical signals, the olfactory and the gustatory systems.

Olfactory and gustatory systems

The olfactory system in fish is primarily responsible for detecting volatile substances in the environment, including those dissolved in water (Jónsson, 1980). While olfaction is generally concerned with the detection of food, it is also important for the detection of chemical signals by conspecifics (Liley, 1982). Fish typically possess paired nasal cavities located near the dorsal surface of the head (Fig. 6). However, some species, such as lampreys and hagfish, have only a single nostril and nasal cavity (Daghfous et al., 2012). The olfactory chambers (rosettes) in these cavities contain folds or lamellae lined with olfactory sensory neurons (Fig. 7) (Jónsson, 1980). The surface area and layout of these lamellae differ between species, and it was once thought they affected the sense of smell. However, new studies have shown that fluid flow and how odors move are more important for smell sensitivity (Daghfous et al., 2012).

Fig. 6. Olfactory pathway of a goldfish. Odors enter the nasal cavity and reach the olfactory epithelium. The olfactory information is then transmitted from the olfactory nerve to the bulbs. The bulbs transmit action potentials via the olfactory tracts to the telencephalon, where the behavioral control center is located (Kobayashi, 2020).

Fig. 7. Overview of the peripheral zebrafish olfactory system. A) Adult zebra fish B) View of the peripheral olfactory organ and connectivity to the brain. The olfactory system consists of two olfactory epithelia located on each side of the head. Each olfactory epithelium extends a short nerve, composed of olfactory sensory neuron (OSN) axons, to the olfactory bulb. C) Composition of olfactory rosette (chambers). D) A single lamella, Olfactory sensory neurons occupy the inner sensory region of each lamella. E) Different olfactory sensory neurons present in zebrafish (Calvo-Ochoa et al., 2020).

Olfaction refers to the chemical information detected through the specific chemoreceptors located in the olfactory epithelium, a sensitive tissue inside the nasal cavity (Sorensen, 1992). Inside the nasal cavity, ligands – specific stimulus molecule that can be bind to specific membrane receptors- bind to the chemoreceptors, activating the G proteins (proteins that can bind to guanosine triphosphate and guanosine diphosphate) on the cell membrane (Hara, 1994; Rehman et al., 2023). The activated G proteins in turn activate adenylyl cyclase or phospholipase C to produce secondary messengers. The secondary messengers activate the opening of ion channels, leading to the generation of an action potential across the olfactory tracts. Ions can also be directly transported across the membrane without involving the second messengers, leading to the generation of electrical signals to the central nervous system. By recording the generation of action potentials by different chemical stimuli, the electro-olfactogram (EOG) can be obtained (Fig. 8) (Hara, 1994).

Fig. 8. The electro-olfactogram of cichlid with different odorants. OB stands for olfactory bulb, OE stands for olfactory epithelium, and Vv stands for ventral telencephalon. Through the recording electrode and the reference electrode, the electric field and the action potentials can be recorded (Nikonov & Maruska, 2019).

While the olfactory neurons are more sensitive to several compounds—such as amino acids, sex steroids, bile acids/salts, and prostaglandins—they are less sensitive to alcohols, carboxylic acids, amines, and aromatic hydrocarbons (Hara, 1994). The highly complex olfactory systems help fish to distinguish between different types of pheromones, each eliciting specific behaviors (Stacey & Sorensen, 2002).

In addition to the olfactory system, fish also rely on the gustatory system to detect chemical compounds in water. Gustatory system is composed of epithelial gustatory cells. Different species are more sensitive to different amino acids. A fish’s gustatory system is also sensitive to carbon dioxide and certain toxins. Gustatory system might aid the fish to avoid poisons and dangerous environments in water (Hara, 1994).

Olfactory signals are one of the main determinants of whether a fish will join and remain in a shoal or school. For example, focal fish will stay in conspecific shoals even if they lack their vision, however, they do not when they lack on olfactory stimulus (Ward et al., 2002). Moreover, fish can also compare its own chemical signals from those of the other fish. Through this “self-reference”, it can find conspecific fish with size similar to itself. It is hypothesized that ontogenetic changes with respect to size produce chemical cues, aiding fish in finding conspecific fish with similar size and to form a more uniform school (Ward & Currie, 2013). Other chemical signals are used for communication and help schools remain cohesive and respond to external stimuli.

Pheromones

Pheromones are chemical signals released by fish as a form of communication that trigger behavioral or physiological responses in others of the same species (Stacey & Sorensen, 2002; Liley 1982). They can be in the form of amines, amino acids, prostaglandins, bile acids, and steroids (Fig. 9) (Bowers et al., 2023), compounds that the olfactory system is sensitive to (Hara, 1994). These chemicals are crucial in regulating key behaviors such as reproduction, migration, predator avoidance, and the maintenance of social hierarchies (Sorensen & Stacey, 2004). Pheromones are species-specific, meaning they affect only members of the same species, ensuring targeted communication (Liley, 1982).

Fig. 9. Chemical structure of different pheromones. For each chemical, the general structure is given followed by an example of fish pheromone (Chung-Davidson et al., 2011).

Reproductive pheromones

In some fish species, reproductive pheromones are essential for ensuring synchronized mating and reproductive success (Stacey & Sorensen, 2002). One of the most studied fish pheromones is prostaglandin, which functions as a sex pheromone in various species. Ovulating females release prostaglandin, and this chemical signal stimulates male courtship behavior, which increases the likelihood of successful reproduction (Fig. 10). Different species show unique responses to reproductive pheromones, with some fish relying heavily on these chemical cues to coordinate mating (Sorensen & Stacey, 2004).

Fig. 10. Female releases sex pheromones to find a male of the same species to mate with. (Wyatt, 2015).

Alarm pheromones

In fish, pheromones also play an important role in group behaviors, especially in species that form schools or shoals (Stacey & Sorensen, 2002). Alarm pheromones are released when a fish is injured or under stress, signalling danger to nearby fish (Chung-Davidson et al., 2011). This triggers an immediate group response aimed at enhancing the survival of individuals (Fig. 11). For example, the release of these alarm pheromones can cause the group to scatter or adopt defensive behaviors, such as darting, when faced with a predator (Sorensen, 1992; Masuda et al., 2024).

Fig. 11. (A) Fish uses reproductive pheromones to enable mating, (B) to senses alarm pheromones from predators, (C) to detects food pheromones, and (D) senses alarm pheromones from pollutants (Korsching, 2020).

In certain fish, such as those in the ostariophysan group (which includes minnows), injury causes the release of a chemical alarm signal from specialized skin cells called club cells. These cells store the alarm substance, which is released into the water when the fish is injured. Nearby fish detect this cue and react quickly, often by swimming away or forming tighter groups for protection (Daghfous et al., 2012).

Other fish species like gobies, salmon, cichlids, and perch also release alarm substances when injured, but the reactions differ between species. For instance, minnows respond by swimming faster, tightening their school, or freezing in place to avoid detection, while Crucian carp react by swimming down to the bottom and stirring up mud to hide (Daghfous et al., 2012). Although the specific behaviors vary, the common response across fish species is to avoid areas where alarm pheromones are present, thus reducing the risk of predation (Stacey & Sorensen, 2002).

Two specific molecules have been identified as the alarm pheromones in zebrafish: daniol sulfate, a sulfated bile alcohol with the molecular formula C₂₇H₄₆O₇S ; and the ostariopterin, a pterin derivative with a molecular formula C₁₁H₁₃N₅O₅. These molecular signals are perceived by the olfactory receptors on the fish’s cilia or microvilli. A signal is then transmitted to the olfactory bulb composed by glomeruli. The daniol sulfate activates the part of the glomeruli called dorsal glomerular cluster(dGa) and the ostariopterin activates the lateral glomerulus 4 (IG4) (Fig. 12). When the two substances are released together in the water, they activate the telencephalon, similar to mammalian amygdaloid nuclei, and trigger the panic reactions in zebrafish (Masuda et al., 2024).

Fig. 12. Daniol sulfate and ostariopterin are released by an injured fish and act as the dangers and conspecifics signals to alert the shoal of the potential dangers (Masuda et al., 2024).

Social and territorial pheromones

Pheromones are also used by fish for migration, to establish social hierarchies, and to defend territories. It is widely accepted that migratory fish “imprint their odor” onto their environment by the release of population-specific pheromone trails, which later provide information to the fish on the location of their return destination (Hasler, 1966; Liley, 1982). Furthermore, in schools with dominant fish, the dominant fish release pheromones that suppress reproductive activities in subordinates, ensuring only the strongest individuals have the chance to reproduce. This hierarchical control helps maintain balance within the population. In species like tilapia, pheromones play a role in defending nesting sites and establishing breeding territories, ensuring that individuals can successfully reproduce and defend their young (Stacey & Sorensen, 2002).

Food pheromones

For fish that do not rely on vision for hunting or foraging, chemosensory systems are crucial for locating food, capturing prey, and avoiding harmful substances. Fish detect amino acids released by prey and use them to initiate species-specific search behaviors. For example, in zebrafish, the amino acids trigger an appetitive swimming behavior, characterized by an increased number of turns as they search for food. However, in rainbow trout, amino acids induce bottom-searching behaviors (Daghfous et al., 2012).

Fish can detect amino acids at very low concentrations, from micro-molar to nanomolar levels, which are commonly found in natural waters. However, environmental pollutants can interfere with these olfactory-mediated behaviors. Fish may be attracted to contaminated areas due to the presence of amino acid-like substances, which could lead them into harmful environments. This highlights the importance of the chemical senses in fish survival and the potential risks posed by water contamination (Daghfous et al., 2012).

Environment chemistry and fish health

The presence of certain chemicals in the water is integral for fish survival while other elements act as toxins, detrimental to fish health. Each of these factors not only impact the survival of each individual fish but the ecosystem as a whole. Pollution, whether caused by human activities or natural disasters, leads to fundamental changes in aquatic environments. These include decreases in the amount of dissolved oxygen, changes in water pH, and the introduction of toxic chemicals, impacting the health of fish and their ability to osmoregulate and communicate (Mustafa et al., 2024).

Heavy metals

Human activities such as smelting, mining, manufacturing, urbanization, and agriculture have led to the contamination of heavy metals in aquatic environments (Mustafa et al., 2024). Heavy metals such as mercury, lead, cadmium, and arsenic, accumulate within aquatic organisms, impacting many of their biological functions. Fish absorb heavy metals as part of ion exchange in their gills, skin and tissues, through osmoregulation and the consumption of contaminated food. These heavy metals are then carried through the bloodstream, spreading to vital organs where they bind to metal binding proteins. As the heavy metals accumulate, they damage tissues, organs, and cells. Some of these detrimental impacts include reduced reproductive capabilities, endocrine disruption, neurological disorders, and death (Mustafa et al., 2024). Such effects, especially endocrine disruption and neurological disorders, have severe impacts on the health of individual fish, carrying implications for the overall cohesion of shoals and schools.

Another impact of high levels of heavy metals is oxidative stress. Heavy metals generate free radicals and reactive oxygen species within cells. These highly reactive molecules cause damage to vital cellular structures such as proteins, lipids, and DNA, known as oxidative stress. Furthermore, these molecules may activate redox-sensitive transcription factors which affect DNA repair, apoptosis, cell growth, and cell differentiation (Mustafa et al., 2024).

Pesticides

Agriculture commonly uses pesticides, including fungicides, insecticides, and herbicides, to maximize crop output. However, runoff from farms contaminates waters, leads to changes in pH, nutrient content, and oxygen levels. These changes can negatively impact a fish’s ability to breathe and may also destroy their bodies on a cellular level.

Some pesticides are known to be toxic to fish. For example, acrolein, a well-known herbicide, is a highly toxic algaecide that causes severe damage to fish gills which are vital for respiration. Other pesticides introduce high amounts of plant nutrients. The runoff assists the growth of algae in aquatic environments, leading to eutrophication. Chemicals containing high amounts of nitrogen and phosphorus saturate the aquatic environment, creating a prime habitat for large algae blooms. This surplus in algae depletes the oxygen levels as well as blocks sunlight from reaching inhabitants below the surface. These impacts of eutrophication impact fish and their ability to survive such chemical changes (Mustafa et al., 2024).

Nanoparticles

Nanoparticles are molecules that can pollute the environment through waste discharge, runoff, and leaching (Mustafa et al., 2024). They are responsible for leading to oxidative stress, inflammatory responses, and tissue damage through bioaccumulation, direct toxicity, and interfering with biological process.

Endocrine disrupting compounds

Endocrine Disrupting Compounds (EDCs) are chemicals that interfere with typical function of the endocrine system, impacting the creation and release of hormones in an organism. Some examples of such chemicals include phenols, estrogens, heavy metals, industrial intermediates, PAHs, pesticides, dioxins, and polychlorinated biphenyls (Mustafa et al., 2024). For example, the release of harmful EDCs in a phenomenon called red tide has serious implications for water chemistry and fish health.

Red tide: A case study

Red tide is a term for harmful algal blooms (US Department of Commerce, NOAA, 2019). As mentioned before, changes in water chemistry resulting from pollution may lead to eutrophication from algae blooms. Red tide releases neurotoxins into the surrounding environment, resulting in massive fish kills. Not only that, but the algae also deplete the oxygen supply in the water, further leading to death resulting from changes in water chemistry (Howard, 2023). With the pollution of aquatic environments and climate change, waters have become more susceptible to longer and more destructive red tides, indicating the delicate balance between habitat chemistry and the survival of different organisms, including fish.

For example, in recent years, Florida has been dealing with increasingly larger and longer lasting blooms of a toxic alga called Karenia brevis. These algae release toxins that accumulate in shellfish, causing a condition called neurotoxic shellfish poisoning, leading to death. These toxins not only impact the predators that eat these organisms but also those living in the surrounding waters, including shoaling fish. Together, these lead to massive kills of wildlife as well as disrupting the Florida ecosystem (Fig. 13) (Rose, 2023).

Fig. 13. Red Tide Algae Blooms lead to massive fish kills in Florida (Jacobo, n.d.).

Surfactants

Surfactants are known to disrupt the function of important receptors involved in chemical communication, affecting a fish’s ability to school (Ward et al., 2008). Surfactants are components with an amphiphilic structure (Fig. 14), their amphiphilic properties cause them to assemble at interfaces between two phases or two substances, reducing the surface tension at the interphase (Unal et al., 2023).

Fig. 14. Structure of a surfactant molecule (Unal et al., 2023).

When juvenile Arctic charr (Salvelinus alpinus) are exposed to surfactants, they are less attracted to conspecific chemical cues. One vastly used surfactant in industrial and sewage processes is 4-Nonylphenol (4-NP). The levels of 4-NP near outflows across the world is currently around 1 to 2 μg 1^-1. Under these concentrations, shoaling killifish (Fundulus diaphanus) avoided the odor of their conspecifics and maintained a greater distance from its neighbors, compared to fish in an environment without 4-NP. The exposure to 4-NP thus affects the chemical signal of fish and impedes social recognition, this might be detrimental to the formation of a shoal if fish are no longer attracted to their conspecifics (Ward et al., 2008).

Carbon dioxide and ocean acidification

The current carbon dioxide concentration is the highest since the last 800 000 years and is projected to double by 2100 (Nadler et al., 2016). This drastic change in CO₂ levels may carry serious implications for fish, including impaired neurotransmission in fish, resulting in behavioral changes such as an inability to recognize predators. Certain neurotransmitters rely on the function of GABA-A receptors, which are linked to chloride and bicarbonate ion channels. Changes in the concentration of these ions within cells, potentially caused by elevated carbon dioxide levels in the water, can affect receptor function. Research has shown that gabazine, an inhibitory neurotransmitter of the GABA-A receptor, can treat the behavioral changes in fish being exposed to elevated concentrated CO₂ water (Chivers et al., 2013).

Under the projected future CO₂ concentration, the ability of fish to recognize olfactory cues will also be negatively affected. Increased CO₂levels lead to decreased shoaling instinct. It is postulated that the decrease in shoaling instinct is a result of elevated CO₂ concentration damaging the fish’s ability to detect olfactory social cues, and interfering with memory and the ability to learn (Nadler et al., 2016). Increased CO₂ concentration may also impact behavioral traits such as boldness, which may be fatal in the face of threats such as predators (Nadler et al., 2016).

Carbon dioxide reacts with water to form carbonic acid which can dissociate to produce hydrogen atoms and increase the acidity of water (Fig. 15). As CO₂ concentration increases, more carbonic acid can be produced, leading to ocean acidification (Doney et al., 2009).

Fig. 15. The reaction that CO₂ undergoes in water (Doney et al., 2009).

Ocean acidification affects fish lateralization. Lateralization describes the “handedness” of fish which affects the ability of fish to move in certain directions. At a lower pH, fish move randomly to the left or right when encountering a wall, and lateralization decreases. This can cause the schools to lose cohesion when making rapid maneuvers (such as when changing direction in response to predators).

Furthermore, increasing ocean temperature increases the boldness of temperate fish, so they only start escaping when they are at a closer distance to the predators (Fig. 15) (Mitchell et al., 2022).

These changes in behaviors due to ocean acidification can be detrimental to fish cohesion and the survival of shoaling fish, as shown in the figure 16.

Fig. 16. Shoaling behaviors are expected to change with the predicted carbon dioxide levels of the year 2100. Lateralization in fish will decrease and so fish will no longer turn in the same direction, will become bolder, and therefore will only escape predators when they are much closer (Mitchell et al., 2022).

Conclusion

Living in water is different from living on land. Water is much denser than air, and it transmits chemical information differently.  

To live in water, even breathing becomes a difficulty due to the insolubility of oxygen in water. To obtain enough oxygen, fish use the gills with a high surface area for gas diffusion, and they use their swimming movements or swallowing of water to pass enough water through their gills. Moreover, fish need to adapt to osmodiverse environments with different ion concentrations. Marine fish consume high amounts of seawater to take in enough sodium chloride to avoid dehydration, while freshwater fish excrete dilute urine to avoid being overhydrated.  

In addition to these basic survival strategies in water, fish rely on chemistry to cooperate with each other. At night, when lack of light becomes a problem, flashlight fish use bioluminescence to maintain their school structure in the dark. On the other side, water can easily disperse chemical particles. The fish’s olfactory and gustatory systems allow them to communicate, mate, and alert each other by releasing different pheromones.

Since fish rely heavily on their aquatic environment to survive, changes in the water compositions and the water pH can have a great impact on the health of individual fish, their behaviors and affect the shoal’s formation and cohesiveness.  

Fish use a variety of chemical strategies and adaptations to ensure they survive and thrive in diverse waters. Any environmental change will not only impact the land and oceans but also has the potential to disrupt the balance that fish and their shoals maintain within their ecosystem, negatively affecting their survival. Given the complex and interconnected nature of the chemical strategies fish employ for survival, further research is needed to determine the future sustainability of fish and other aquatic animals under the growing uncertainties and threats of climate change.