Respiratory System of Fishes

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The respiratory system of fishes is a highly specialized and efficient mechanism that allows them to extract oxygen from water. As aquatic organisms, fish must adapt to the lower oxygen content in water compared to air, and their respiratory systems have evolved to maximize the efficiency of gas exchange. Below is an overview of the key components and mechanisms involved in fish respiration.

  • Gills:
    • Gills are the primary respiratory organs in most fishes. They are composed of gill arches, filaments, and lamellae, which provide a large surface area for oxygen exchange.
    • Water enters through the fish’s mouth and flows over the gills, where oxygen is absorbed into the blood while carbon dioxide is expelled.
    • The arrangement of gill filaments and lamellae ensures a countercurrent exchange mechanism, in which water flows opposite to the direction of blood flow, maximizing oxygen absorption.
  • Gill Covers (Operculum):
    • In bony fishes (Osteichthyes), the gills are covered by a bony structure called the operculum. This protective cover aids in controlling water flow over the gills.
    • Cartilaginous fishes (Chondrichthyes), such as sharks and rays, do not have an operculum, and their gill slits open directly to the environment.
  • Countercurrent Exchange:
    • One of the most effective adaptations in the fish respiratory system is the countercurrent exchange mechanism.
    • In this system, water flows over the gills in the opposite direction of blood flow. This gradient ensures that oxygen is continuously absorbed along the entire length of the gill lamellae, greatly enhancing respiratory efficiency.
  • Spiracles and Gill Slits:
    • Cartilaginous fishes, like sharks, often possess spiracles—small openings behind the eyes that allow water to enter even when the mouth is closed.
    • These fishes also have multiple gill slits, which serve as exit points for water after oxygen exchange has occurred.
  • Accessory Respiratory Structures:
    • Some fish species have developed accessory respiratory organs that allow them to breathe air, especially in environments with low dissolved oxygen.
    • Examples include the labyrinth organ in climbing perch (Anabas), the suprabranchial chambers in catfish (Clarias), and air chambers in mudskippers (Periophthalmus).
  • Air-Breathing Fishes:
    • Certain species are obligate air-breathers, meaning they must regularly surface to breathe air, such as the African lungfish.
    • Facultative air-breathers, like the catfish (Hypostomus), can breathe air when needed but primarily rely on their gills for respiration.
  • Special Adaptations:
    • Fish living in environments with low oxygen or those that frequently leave the water have specialized organs, such as vascularized pouches or sacs, to enhance air respiration.
    • These structures allow for the direct absorption of oxygen from the air, making them critical for survival in extreme environments.
Types of gill in fishes
Types of gill in fishes

General Gill Structure

Gills play a crucial role in the respiratory system of fish, allowing them to extract oxygen from water. They are intricate structures that enable efficient gas exchange and are adapted to various environmental conditions. Understanding the general structure of gills provides insight into their functionality and significance in aquatic life. Below are detailed points on the general structure of gills:

Fish gill structure
Fish gill structure (Користувач:Shao \ Anaxibia, CC BY 3.0, via Wikimedia Commons)
  • Location and Protection: Gills are housed within a gill cavity, which offers protection to these delicate organs while facilitating efficient water flow over them. This structural arrangement is vital for optimal respiratory function.
  • Composition of Gills: Gills consist of multiple gill arches located on either side of the fish. These arches separate the opercular and buccal cavities, forming a framework for the attachment of gill filaments.
  • Gill Filaments: Each gill arch is equipped with two rows of gill filaments. The arrangement of these filaments forms a sieve-like structure that allows water to flow through efficiently. The tips of adjacent filaments interconnect, enhancing the surface area for gas exchange.
  • Surface Area Enhancement: Gill filaments are covered by a thin epidermal membrane that folds to create plate-like structures called lamellae. This folding significantly increases the surface area available for respiration, optimizing the exchange of gases.
  • Counter-Current Exchange Mechanism: Water flows over the gills in a direction opposite to that of blood circulation within the gill filaments. This counter-current exchange mechanism maximizes oxygen uptake and carbon dioxide elimination, facilitating efficient respiration.
  • Variation Among Species: The area of gills varies among different fish species, correlating with their activity levels. More active species tend to have larger gill surfaces, enabling them to meet higher oxygen demands.
  • Respiratory Rate Dependency: The rate of respiration in fish is influenced by the concentration of dissolved oxygen in the surrounding water. Fish inhabiting low-oxygen environments exhibit increased respiratory rates to meet metabolic needs.
  • Types of Gills:
    • External Gills: These structures develop from the integument of branchial or visceral arches and protrude into the surrounding water. They are often branched and filamentous, providing a direct contact surface for oxygen absorption. However, they are susceptible to damage.
    • Internal Gills: Associated with pharyngeal slits and pouches, internal gills consist of parallel gill lamellae that enhance gas exchange. These gills can be found on both sides of the interbranchial septa or on only one side, forming structures known as hemibranchs and holobranchs, respectively.
  • Protective Structures: Internal gills are protected by soft skin folds or firm structures known as opercula. The operculum plays a critical role in gill respiration by regulating water flow over the gills through its opening and closing.
  • Types of Internal Gills:
    • Elasmobranchs: In cartilaginous fish, interbranchial septa are well-developed and extend beyond hemibranchs, providing added protection.
    • Bony Fishes: In teleosts, interbranchial septa are reduced, allowing for the protrusion of hemibranchs into branchial chambers, which are located between the operculum and the gills.
  • Capillary Networks: Gills are rich in capillary beds, bringing blood close to the respiratory surfaces. This anatomical feature facilitates the rapid exchange of gases—oxygen is absorbed while carbon dioxide is expelled.
  • Unidirectional Ventilation: In most fish species, water ventilation is unidirectional. Water enters through the mouth, passes over the gill lamellae, where gas exchange occurs, and exits through gill slits. This streamlined process ensures efficient oxygen uptake and waste removal.
FISH -GAS EXCHANGE
FISH -GAS EXCHANGE (Image Source: https://www.pathwayz.org/Tree/Plain/FISH+-GAS+EXCHANGE)

Respiratory System of Fishes

The respiratory system of fishes is a highly specialized adaptation that allows these aquatic animals to extract dissolved oxygen from water, an essential process for their survival. This system comprises various anatomical structures that work together to facilitate efficient gas exchange. Below is an in-depth exploration of the respiratory system of fishes, highlighting its components and functions.

  • Ventilation Mechanism: Fish respiration operates via a unidirectional flow of water. Water enters through the mouth and pharynx, then exits through external gill slits in elasmobranchs (cartilaginous fishes) and through the operculum in teleosts (bony fishes). This arrangement ensures a continuous flow of oxygenated water over the gills.
  • Countercurrent Exchange System: Gas exchange occurs in the gill lamellae, where water flows in one direction while blood circulates in the opposite direction. This countercurrent flow enhances oxygen extraction; as water rich in oxygen passes over blood with low oxygen levels, a gradient is maintained throughout the exchange process. Consequently, blood leaving the gills can extract more than 80% of the dissolved oxygen from the water.
  • Gill Arches: Fishes possess a series of skeletal gill arches that support the gills. These arches, located between gill clefts, include the mandibular arch, hyoid arch, and additional visceral arches. The gill pouch or cleft between these arches is crucial for the arrangement of gills and varies between species.
  • Types of Fishes:
    • Cartilaginous Fishes (Class Chondrichthyes): This group includes sharks, rays, and skates. They typically possess five to seven gill arches and lack an operculum. In elasmobranchs, breathing involves sucking large volumes of water into the buccal cavity via the mouth and spiracles. As the buccal cavity contracts, water is forced over the gills and expelled through external gill slits. Some species may have additional gill slits, such as Hexanchus, which has six, or Heptanchus, which has seven.
    • Bony Fishes (Class Actinopterygii): These fishes include a diverse range of species characterized by the presence of an operculum, which serves to protect the gills. Water enters the buccal cavity, simultaneously expanding the opercular cavity, which creates a pressure differential that facilitates water flow across the gills. The operculum also assists in expelling water from the gill chamber.
  • Swim Bladder Function: Many bony fishes possess a swim bladder, an air-filled sac that aids in buoyancy. This structure is located between the alimentary canal and vertebral column. It plays a critical role in maintaining the fish’s position in the water column without expending significant energy.
  • Adaptations of Lung Fishes: Lung fishes, such as Polypterus and Lepidosiren, possess both gills and lungs, allowing them to survive in environments with varying oxygen levels. While gills are present, they are often reduced or atrophied in some species. These fishes can extract oxygen from the air when necessary, using a buccal pump to facilitate inhalation and relying on the elasticity of their lungs for expiration.
  • Challenges in Air Exposure: Most fishes are adapted to aquatic environments and face significant challenges when exposed to air. The gills can become damaged due to drying, leading to a decrease in respiratory efficiency. In freshwater species, certain adaptations, such as accessory respiratory structures, have evolved to enable air breathing when water levels drop.
  • Physiological Implications: The effectiveness of the respiratory system in fishes is reflected in the partial pressure of oxygen (pO2) in their blood. This measure indicates the success of their respiratory mechanisms in maintaining adequate oxygen levels for metabolic functions.
Fish gill respiration
Fish gill respiration (Користувач:Shao / Anaxibia, CC BY-SA 3.0, via Wikimedia Commons)

Concurrent Exchange Mechanism

The concurrent exchange mechanism is a vital physiological process observed in fish that significantly enhances the efficiency of gill respiration. By enabling more effective gas exchange, this mechanism allows fish to optimize the extraction of dissolved oxygen from water. Below is a detailed explanation of this process and its components.

a) Concurrent flow: When blood and water move in the same direction, then no further exchange of O2 takes place after equal concentration is reached. In this condition the pO2 in blood reaches the pO2 levels of the out flowing water; b) Countercurrent flow: favours better absorption of oxygen by blood. Blood enters with low pO2 but leaves the lamellae with nearly the same pO2 as water; Counter current flow also reduces the energy cost of pumping water over the gills.
a) Concurrent flow: When blood and water move in the same direction, then no further exchange of O2 takes place after equal concentration is reached. In this condition the pO2 in blood reaches the pO2 levels of the out flowing water; b) Countercurrent flow: favours better absorption of oxygen by blood. Blood enters with low pO2 but leaves the lamellae with nearly the same pO2 as water; Counter current flow also reduces the energy cost of pumping water over the gills.
  • Definition and Mechanism:
    • Concurrent exchange refers to the method by which water and blood flow in opposite directions across the gills. This countercurrent flow maximizes the concentration gradient between the oxygen-rich water and the oxygen-poor blood, facilitating a more efficient transfer of oxygen.
    • Research indicates that this mechanism can enhance gill efficiency by up to 90%, allowing fish to absorb a greater amount of dissolved oxygen.
  • Structure of Gills:
    • Gills are located on either side of the pharynx and are protected by gill covers, known as opercula.
    • In bony fish, there is typically one external gill opening, while other species, such as sharks and lampreys, possess multiple gill slits.
  • Gas Exchange Process:
    • Fish initiate gas exchange by drawing oxygen-rich water into their mouths.
    • This water is then pumped across the gill membranes where oxygen diffuses into the blood vessels.
    • After the oxygen has been absorbed, the remaining water is expelled through the gill openings.
  • Types of Gills:
    • Bony fishes typically have three pairs of gills, while cartilaginous fishes possess between five and seven pairs. Primitive jawless fishes, like lampreys, can have up to seven gills.
  • Breathing Techniques:
    • Fish are categorized based on their respiratory strategies into two groups:
      • Obligate Air Breathers: These species must periodically breathe air to survive, as their gills alone cannot provide sufficient oxygen. An example is the African lungfish, which can suffocate without access to air.
      • Facultative Air Breathers: These fish primarily rely on their gills for oxygen but can resort to air breathing if environmental conditions necessitate it. Catfish, such as Hypostomus plecostomus, exemplify this category.
  • Functional Importance:
    • The countercurrent exchange mechanism not only optimizes oxygen uptake but also helps regulate the fish’s internal environment, allowing for effective physiological functions.
    • This adaptation is particularly crucial in environments where oxygen levels may be low, ensuring that fish can survive and thrive in various aquatic habitats.

Respiration Process in different fish

Below is a comprehensive overview of the respiration processes in bony fish, lampreys and hagfish, and cartilaginous fish.

Respiratory mechanism in bony fish
Respiratory mechanism in bony fish (Cruithne9, CC BY-SA 4.0, via Wikimedia Commons)
  1. Respiration in Bony Fish:
    • Bony fishes possess gills located within a specialized branchial chamber, which is protected by an operculum.
    • The operculum plays a critical role in creating water pressure within the throat, thereby facilitating effective ventilation and continuous water flow over the gills.
    • Unlike some other fish, bony fish gill arches do not have a septum; instead, the gills extend from the arches and are supported by structures known as gill rays.
    • In certain species, external gills may also be present, adding to the complexity of their respiratory system.
    • The respiration process involves the following steps:
      • Fish intake oxygen-rich water through their mouths.
      • This water is actively pumped across the gill membranes, where oxygen diffuses into the bloodstream.
      • Once the oxygen has been absorbed, the remaining water is expelled through gill slits, allowing for continuous breathing.
  2. Respiration in Lampreys and Hagfish:
    • Unlike bony fish, lampreys and hagfish do not possess gill slits; instead, they have spherical pouch-like structures that house their gills.
    • Each pouch typically contains two gills, which are situated alongside a circular external opening.
    • Some species may have these openings covered, functioning similarly to an operculum, although not as fully developed as in bony fish.
    • Hagfish typically possess six to fourteen pairs of these gill pouches, while lampreys have seven pairs.
    • The respiratory process involves:
      • Water enters through the external opening.
      • Oxygen is extracted as the water flows over the gills within the pouches.
      • The remaining water exits through the same orifice, ensuring a steady exchange of gases.
  3. Respiration in Cartilaginous Fish:
    • Cartilaginous fish, such as sharks and rays, feature five pairs of gill slits that open directly to the exterior.
    • Each gill slit is separated by a long septum, resembling a sheet and supported by a complex array of gill structures known as gill lamellae.
    • A unique feature of cartilaginous fish is the presence of spiracles—small openings located behind the eyes—that enable respiration.
    • The respiration process in these fish can be outlined as follows:
      • Water is drawn in through the spiracles instead of the mouth, allowing for simultaneous feeding and breathing.
      • The spiracles contain a small pseudobranch that selectively extracts oxygenated blood from the gills.
      • After gas exchange occurs in the gills, the deoxygenated water is expelled through the gill slits.

Accessory Respiratory Organs in Fishes

Below is an exposition on several key accessory respiratory organs found in fishes, each with distinct structures and functions.

  1. Suprabrachial Organ:
    • Found in species such as Clarias batrachus, the suprabrachial organ consists of a complex tree-like structure arising from the second and fourth gill arches on either side.
    • The organ is composed of numerous terminal knobs, each made of cartilage covered with a vascular membrane. Each knob showcases eight folds, indicating that it is formed by the merging of eight gill filaments.
    • Enclosed within highly vascularized supra-branchial chambers, these structures facilitate air breathing. The inhalant aperture, situated between the second and third gill arches, allows atmospheric air to enter the chamber.
    • Air is expelled through the opercular cavity via the gill slit between the third and fourth gill arches, assisted by the contraction of the chamber walls. The fan-like structures formed by fused gill filaments enhance air intake, thereby functioning analogously to lungs.
  2. Branchial Outgrowths:
    • Observed in the climbing perch (Anabas testudineus), these sac-like outgrowths from the dorsal side of the branchial chambers are lined with highly vascular epithelium, increasing the surface area for gas exchange.
    • The characteristic rosette-like labyrinthine organ, formed from the first epibranchial bone, comprises concentric, shell-like plates covered with vascular gill-like epithelium.
    • Air enters the outgrowth through the buccopharyngeal opening and exits through external gill slits, with the process regulated by valves. This adaptation supports the fish’s ability to migrate across land.
  3. Pharyngeal Diverticula:
    • In species like the snake-headed fish and Cuchia eel, these sac-like diverticula developed from the pharynx enable prolonged air breathing, allowing these fish to survive periods out of water.
    • The air chambers, lined with thickened vascular epithelium, function as lung-like reservoirs for gaseous exchange. In Channa striatus, folds in the vascular epithelium create alveolar structures, enhancing the efficiency of respiration.
  4. Pneumatic Sacs:
    • Found in Heteropneustes fossilis, these tubular sacs extend from the branchial chamber and traverse the body musculature. Their elongated shape allows for increased surface area for gas exchange.
    • Similarly, in Saccobran­chus, the lung-like outgrowths assist in respiration during periods when gills are less effective.
  5. Buccopharyngeal Epithelium:
    • The highly vascularized epithelium in the buccopharyngeal region serves as a site for oxygen absorption in numerous fish.
    • In mudskippers, such as Periophthalmus and Boleophthalmus, this adaptation enables atmospheric oxygen absorption, supporting their unique lifestyle of navigating damp environments.
  6. Integument:
    • Eels, including Anguilla anguilla, demonstrate the capacity for cutaneous respiration, utilizing their skin for gas exchange.
    • In amphibious species like Amphipnous cuchia and mudskippers, moist skin functions as a respiratory surface, facilitating oxygen uptake in both air and water.
  7. Gut Epithelium:
    • In certain species, such as Cobitis and Misgurus fossilis, modifications to the gut lining allow for respiratory functions.
    • Air is ingested and subsequently passed through the gut, with specialized areas serving as reservoirs for gas exchange.
  8. Swim Bladder as Lung:
    • Although primarily a hydrostatic organ, the swim bladder in some species, such as Amia and Lepisosteus, has evolved to serve respiratory functions.
    • In Polypterus, the swim bladder contains pulmonary arteries and alveolar structures, effectively enabling respiration during periods when gills are less functional.

Functions of Accessory Respiratory Organs

Below are the primary functions and characteristics of accessory respiratory organs:

  • Oxygen Absorption: Accessory respiratory organs are specialized structures that facilitate a higher absorption rate of oxygen compared to traditional gill respiration. This adaptation is critical in low-oxygen environments, allowing fish to efficiently extract the oxygen needed for metabolic processes.
  • Air Gulping Behavior: Fish equipped with these organs often exhibit behaviors such as surfacing to gulp air. This action is necessary for them to transport oxygen to the accessory respiratory organs. Such behaviors are adaptations that enable them to survive in aquatic environments where dissolved oxygen is limited.
  • Asphyxiation Risk: If these fish are unable to reach the surface, they face a significant risk of asphyxiation due to a lack of oxygen. This underscores the importance of these organs in their overall respiratory physiology. The ability to access atmospheric oxygen is a crucial survival mechanism.
  • Adaptive Feature: The evolution of accessory respiratory organs is an adaptive response to environmental pressures. These structures provide a necessary function that complements gills, enabling fish to occupy ecological niches where oxygen is scarce.
  • Carbon Dioxide Elimination: The rate of oxygen absorption in accessory respiratory organs is significantly higher than the rate at which carbon dioxide is expelled. This indicates that, while the primary role of these organs is oxygen uptake, they also contribute to the elimination of metabolic waste products, primarily carbon dioxide. However, gills remain the main site for carbon dioxide excretion in these fish.
  • High Oxygen Content: The high concentration of oxygen in these organs enhances their efficiency. This is particularly advantageous in hypoxic conditions, allowing fish to maintain adequate oxygen levels for respiration even when environmental conditions are suboptimal.
  • Physiological Adaptations: The presence of accessory respiratory organs often correlates with specific physiological adaptations. These may include changes in gill morphology, increased vascularization in the accessory organs, and alterations in behavior to optimize oxygen intake.

Significance of Accessory Respiratory Organs

Below are key points highlighting their significance:

  • Adaptation to Low Oxygen Environments: Accessory respiratory organs enable fish to thrive in aquatic habitats where oxygen is scarce, such as shallow water bodies that may dry up or become polluted. This adaptation is essential for their survival in challenging environments.
  • Instinctive Behavior: Some fish exhibit an instinct to occasionally leave the water and access atmospheric air. This behavior is linked to the necessity of developing specialized organs to facilitate air breathing. Such instinctual behavior underscores the evolutionary significance of these adaptations.
  • Response to Hypoxia: Fish may be compelled to utilize their accessory respiratory organs when the oxygen concentration in their aquatic environment decreases significantly. This behavioral adaptation allows them to gulp air from the surface, which is then directed into these specialized organs for respiration.
  • Mechanism of Gulping Air: The act of swallowing air bubbles is particularly prevalent in many bony fish, especially those inhabiting shallow waters that periodically experience low oxygen levels. This adaptation enables these fish to efficiently access atmospheric oxygen.
  • Structure and Functionality: Accessory respiratory organs often take the form of air reservoirs, originating from the pharyngeal or branchial cavities. In some species, these reservoirs may house specialized structures that facilitate gaseous exchange, thereby enhancing respiratory efficiency.
  • Developmental Biology: The formation of accessory respiratory organs is rooted in embryonic development. Specifically, the fifth gill arch, which lacks gill lamellae, contributes to the formation of a ‘gill mass’ from which these organs develop. In some species, other gill arches may also participate in this process.
  • Modification of Gill Structures: In many cases, gill lamellae, which typically serve aquatic respiration, undergo modifications to form the respiratory epithelium of suprabranchial chambers, air sacs, and dendritic organs. This transformation enables efficient air respiration in adapted species.
  • Historical Context: Geological periods such as the Tertiary and Quaternary saw a significant reduction in atmospheric and aquatic oxygen levels. Consequently, various teleostean species developed accessory respiratory organs to compensate for the inadequacies of gills under such conditions.
  • Survival in Deoxygenated Waters: Fish with accessory respiratory organs have been observed successfully inhabiting deoxygenated waters, such as swampy areas and muddy ponds. Their ability to gulp air from the surface and utilize it for respiration is crucial for their survival in these habitats.
  • Primary Functionality: The primary function of accessory respiratory organs is to absorb oxygen, as evidenced by the significantly higher rate of oxygen uptake compared to carbon dioxide excretion. Most of the carbon dioxide produced is eliminated via the gills, illustrating the specialization of these organs for aerial respiration.

Accessory respiratory organs in different fish types

 The labyrinthine organ of Anabas.
The labyrinthine organ of Anabas.
  1. Anabas (Climbing Perch):
    • The climbing perch has two air chambers extending from the branchial cavities, located on either side of its head.
    • These labyrinthine organs consist of concentrically arranged wavy plates covered by a highly vascular membrane.
    • Air enters the chambers through the mouth and exits via the branchial aperture.
    • Anabas can remain out of water for approximately six to seven hours, deriving about 54% of its oxygen from atmospheric air.
  2. Ophiocephalus (Murrel):
    • This species possesses a pair of air chambers arising from the pharynx above the first gill arch, extending to the last gill cleft.
    • Air enters these chambers via the mouth and is expelled through the opercular arch.
    • This adaptation allows for effective air breathing while maintaining aquatic respiration.
  3. Clarias (Indian Catfish):
    • Clarias has highly branched and vascularized accessory respiratory organs known as suprabranchial chambers.
    • The structure includes branching, tree-like organs supported by a cartilaginous internal skeleton.
    • The ends of these branches feature cartilage knobs covered with a vascular membrane.
    • Air is inhaled through the pharynx into the suprabranchial chamber and exhaled via an aperture, allowing Clarias to effectively breathe air.
  4. Amphipnous:
    • In Amphipnous, air chambers develop as saccular outgrowths of the dorsal wall of the pharynx, extending to the third branchial arch.
    • The walls of these sacs are vascular and folded, allowing for increased surface area for gas exchange.
    • Air is drawn in through an opening to the pharynx and exits through the gill slits and opercular openings.
  5. Saccobranchus:
    • This species features tubular sacs arising from the gill chambers, extending to the mid-tail region.
    • The folds within these tubes create air chambers that connect with the buccal cavity through a slit.
    • Air flows in and out of the chamber via this slit, allowing Saccobranchus to supplement its oxygen intake.
  6. Mudskipper (Periophthalmus):
    • Mudskippers possess large opercular cavities that fill with air drawn through the mouth.
    • This adaptation allows them to thrive in brackish environments, as they are capable of living outside of water for extended periods.
    • If kept out of water for too long, mudskippers face the risk of suffocation due to their reliance on these aerial respiratory organs.
The accessory respiratory organ of Ophiocephalus.
The accessory respiratory organ of Ophiocephalus.
The arboriform accessory respiratory organ of Clarias.
The arboriform accessory respiratory organ of Clarias.
The air chamber in Amphipinous.
The air chamber in Amphipinous.
The accessory respiratory organ of Saccobranchus.
The accessory respiratory organ of Saccobranchus.
Reference
  1. https://egyankosh.ac.in/bitstream/123456789/16526/1/Unit-7.pdf
  2. https://www.notesonzoology.com/fish/respiratory-system-of-fishes-zoology/4124
  3. https://openbiologyjournal.com/contents/volumes/V4/TOBIOJ-4-35/TOBIOJ-4-35.pdf
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  6. https://www.biologydiscussion.com/fisheries/fish/accessory-respiratory-organs-in-fishes-phylum-chordata/40801
  7. http://www.lscollege.ac.in/sites/default/files/e-content/Respiratory%20system%20of%20fish%20and%20amphibia.pdf
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  13. http://courseware.cutm.ac.in/wp-content/uploads/2020/06/Gas-Exchange-and-Respiration-in-Fishes-1.pdf

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