Comprehensive Physiology Wiley Online Library

Mechanisms of Excretion and Ion Transport in Invertebrates

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Ion Transport and Osmoregulation in Invertebrates: Functional Morphology and Cellular Mechanisms
1.1 Water Expulsion Vesicles and Contractile Vacuoles in Protozoans, Sponges, and Cnidarians
1.2 Nephridia and Coelomoducts: Embryology and Terminology
1.3 Nephridia
1.4 Coelomoduct‐Derived Renal Organs
1.5 Gut‐Derived Renal Organs
1.6 Other Ion‐Transporting Structures
2 Excretion in Invertebrates
2.1 Nitrogenous Wastes
2.2 Alkaloids
2.3 Organic Anions
2.4 Organic Cations
2.5 Magnesium and Sulfate
2.6 Storage and Deposit Excretion
2.7 Catabolism of Insect Neurohormones by Malpighian Tubules
2.8 Roles of Arthropod Excretory Systems and Molluscan Mantle in Acid‐Base Regulation
2.9 Active Transport of Sugars
2.10 Transport of Cardiac Glycosides
2.11 Passive Permeability to Metabolites and Toxins
3 Future Research
Figure 1. Figure 1.

Functional model of protonephridial and metanephridial systems. Direction of fluid flow is indicated by arrows. Two designs for filtration nephridia are shown (A, B). Fluid flows from inner to outer compartment when P1 exceeds P2. Fluid composition is adjusted subsequently by the modifier. C: Metanephridium. Transverse section of a generalized coelomate. Contraction of peritoneal musculature elevates blood vascular pressure, thereby filtering fluid across peritoneal podocytes. Coelomic fluid is subsequently modified by metanephridial duct. D: Protonephridium. Schematic transverse section through a generalized metazoan lacking blood vessels. Activity of terminal cilium (or cilia) creates a pressure difference, which drives fluid across terminal weir. Filtration occurs as fluid crosses extracellular matrix of weir, and fluid is subsequently modified by protonephridial duct.

Redrawn from Ruppert and Smith 461
Figure 2. Figure 2.

Summary of ionic compositions of blood and secreted fluid, suggested mechanisms of ionic transport, and electrochemical potentials for secretion of Na+, K+, and Cl by the leech canaliculus. In this and all subsequent figures, ATP‐dependent pumps are indicated by circles labeled +ATP; secondary active transport systems (co‐ or countertransport) by open circles, and passive conductive pathways (for example, channels) by arrows through gaps in plasma membrane.

Figure 3. Figure 3.

Schematic showing routes for ingestion of blood meal and excretion of ions and water by an ixodid tick, Dermacentor andersoni.

Redrawn from Kaufman and Phillips 223
Figure 4. Figure 4.

Schematic summarizing mechanisms of Na+, K+, and Cl secretion by Malpighian tubule cells of the blood‐feeding hemipteran Rhodnius prolixus.

Redrawn from Maddrell and O'Donnell 296
Figure 5. Figure 5.

Summary of mechanisms of ion movement in Malpighian tubule cells of the mosquito Aedes aegypti.

Figure 6. Figure 6.

Summary of ion and acid‐base transport mechanisms in locust rectum. Redrawn from Thomson and Phillips 528 with additions. Diffusional pathways indicated by dashed arrows. Upper cell shows mechanism of rectal lumen acidification; lower cell summarizes transport mechanisms for Na+, K+, Cl, proline, and other amino acids. Values for Va, Vb, and pHi obtained under conditions described by Thomson and Phillips 528, with nominally ‐free saline at pH of 7.0 on both sides of isolated rectum. Net electrochemical potentials determined under open‐circuit conditions 160,529. Favorable gradients for net ion movement from lumen to hemocoel indicated by negative electrochemical potentials; positive values indicate opposing gradients.

Figure 7. Figure 7.

Schematic of excretory system of desert locust. Composition of fluid added to hindgut by Malpighian tubules shown at top of figure. Changes in pH and osmotic concentration during passage through hindgut and final contents of excreta produced by locusts starved for 1 day also indicated. Active fluid reabsorption (Jv), ion transport mechanisms, and control of these processes by first and second messengers shown in middle of figure. Arrows under CONTROL indicate whether increases (upward arrows) or decreases (downward arrows) in indicated mechanisms are produced by ileal transport peptide (ITP), purified chloride transport–stimulating hormone (CTSH), extracts of corpora cardiaca (CC), or cAMP.

Redrawn from Audsley et al. 12
Figure 8. Figure 8.

Pathways for water and ion movement in recta and Malpighian tubules of saline–water mosquito larvae.

Redrawn from Bradley 38
Figure 9. Figure 9.

Schematic longitudinal section through rectal complex of tenebrionid beetle larvae. Proposed routes for ion transport and osmotically coupled water movements are shown. Inset indicates electrical potentials and ion activities in hemolymph, perinephric space, and tubule lumen of Onymacris plana. Details in text.

Figure 10. Figure 10.

Model of NaCl uptake in crustacean gills. ATP‐dependent Na+/K+ or exchange, Na+/H+ exchange, and exchange demonstrated in both vesicle preparations and isolated gills.

Figure 11. Figure 11.

Model proposed to explain functions of carbonic anhydrase (CA) in both respiration and ion regulation in crustacean gills. Both cytoplasmic and membrane‐bound CA is inhibited by acetazolamide (Az) and benzolamide (Bz). Only extracellularly oriented, membrane‐associated CA is inhibited by quaternary ammonium sulfanilamide (QAS) and dextra‐bound inhibitors (DBI).

Redrawn from Henry 179
Figure 12. Figure 12.

Model of NaCl excretion by metepipodites of brine shrimp Artemia salina. Model is comparable to that proposed for gills of marine teleosts. Although chloride cells exist in both cases, there is no evidence in crustacean branchial epithelial cells for the structural equivalent of the apical crypts which characterize teleost chloride cells.

Figure 13. Figure 13.

Model proposed for tertiary coupling of organic anion (p‐aminohippuric acid, PAH) secretion to ATP‐dependent ion transport. Establishment of a sodium graident by Na+, K+‐ATPase is used to drive secondary uptake of α‐ketoglutarate (aKG2−). Efflux of aKG2− is then coupled to uptake of PAH. Transapical movements of PAH are driven by the electrical gradient between cell and lumen.

Redrawn from Pritchard and Miller 408
Figure 14. Figure 14.

Model proposed for excretion of organic cations, including the probe molecule tetraethylammonium (TEA). The basolateral carrier is inhibitable by quinine and driven by the inside‐negative cell potential. TEA+ is exchanged for H+ across apical membrane, and the proton is recycled through an Na+/H+ exchanger.

Redrawn from Pritchard and Miller 408


Figure 1.

Functional model of protonephridial and metanephridial systems. Direction of fluid flow is indicated by arrows. Two designs for filtration nephridia are shown (A, B). Fluid flows from inner to outer compartment when P1 exceeds P2. Fluid composition is adjusted subsequently by the modifier. C: Metanephridium. Transverse section of a generalized coelomate. Contraction of peritoneal musculature elevates blood vascular pressure, thereby filtering fluid across peritoneal podocytes. Coelomic fluid is subsequently modified by metanephridial duct. D: Protonephridium. Schematic transverse section through a generalized metazoan lacking blood vessels. Activity of terminal cilium (or cilia) creates a pressure difference, which drives fluid across terminal weir. Filtration occurs as fluid crosses extracellular matrix of weir, and fluid is subsequently modified by protonephridial duct.

Redrawn from Ruppert and Smith 461


Figure 2.

Summary of ionic compositions of blood and secreted fluid, suggested mechanisms of ionic transport, and electrochemical potentials for secretion of Na+, K+, and Cl by the leech canaliculus. In this and all subsequent figures, ATP‐dependent pumps are indicated by circles labeled +ATP; secondary active transport systems (co‐ or countertransport) by open circles, and passive conductive pathways (for example, channels) by arrows through gaps in plasma membrane.



Figure 3.

Schematic showing routes for ingestion of blood meal and excretion of ions and water by an ixodid tick, Dermacentor andersoni.

Redrawn from Kaufman and Phillips 223


Figure 4.

Schematic summarizing mechanisms of Na+, K+, and Cl secretion by Malpighian tubule cells of the blood‐feeding hemipteran Rhodnius prolixus.

Redrawn from Maddrell and O'Donnell 296


Figure 5.

Summary of mechanisms of ion movement in Malpighian tubule cells of the mosquito Aedes aegypti.



Figure 6.

Summary of ion and acid‐base transport mechanisms in locust rectum. Redrawn from Thomson and Phillips 528 with additions. Diffusional pathways indicated by dashed arrows. Upper cell shows mechanism of rectal lumen acidification; lower cell summarizes transport mechanisms for Na+, K+, Cl, proline, and other amino acids. Values for Va, Vb, and pHi obtained under conditions described by Thomson and Phillips 528, with nominally ‐free saline at pH of 7.0 on both sides of isolated rectum. Net electrochemical potentials determined under open‐circuit conditions 160,529. Favorable gradients for net ion movement from lumen to hemocoel indicated by negative electrochemical potentials; positive values indicate opposing gradients.



Figure 7.

Schematic of excretory system of desert locust. Composition of fluid added to hindgut by Malpighian tubules shown at top of figure. Changes in pH and osmotic concentration during passage through hindgut and final contents of excreta produced by locusts starved for 1 day also indicated. Active fluid reabsorption (Jv), ion transport mechanisms, and control of these processes by first and second messengers shown in middle of figure. Arrows under CONTROL indicate whether increases (upward arrows) or decreases (downward arrows) in indicated mechanisms are produced by ileal transport peptide (ITP), purified chloride transport–stimulating hormone (CTSH), extracts of corpora cardiaca (CC), or cAMP.

Redrawn from Audsley et al. 12


Figure 8.

Pathways for water and ion movement in recta and Malpighian tubules of saline–water mosquito larvae.

Redrawn from Bradley 38


Figure 9.

Schematic longitudinal section through rectal complex of tenebrionid beetle larvae. Proposed routes for ion transport and osmotically coupled water movements are shown. Inset indicates electrical potentials and ion activities in hemolymph, perinephric space, and tubule lumen of Onymacris plana. Details in text.



Figure 10.

Model of NaCl uptake in crustacean gills. ATP‐dependent Na+/K+ or exchange, Na+/H+ exchange, and exchange demonstrated in both vesicle preparations and isolated gills.



Figure 11.

Model proposed to explain functions of carbonic anhydrase (CA) in both respiration and ion regulation in crustacean gills. Both cytoplasmic and membrane‐bound CA is inhibited by acetazolamide (Az) and benzolamide (Bz). Only extracellularly oriented, membrane‐associated CA is inhibited by quaternary ammonium sulfanilamide (QAS) and dextra‐bound inhibitors (DBI).

Redrawn from Henry 179


Figure 12.

Model of NaCl excretion by metepipodites of brine shrimp Artemia salina. Model is comparable to that proposed for gills of marine teleosts. Although chloride cells exist in both cases, there is no evidence in crustacean branchial epithelial cells for the structural equivalent of the apical crypts which characterize teleost chloride cells.



Figure 13.

Model proposed for tertiary coupling of organic anion (p‐aminohippuric acid, PAH) secretion to ATP‐dependent ion transport. Establishment of a sodium graident by Na+, K+‐ATPase is used to drive secondary uptake of α‐ketoglutarate (aKG2−). Efflux of aKG2− is then coupled to uptake of PAH. Transapical movements of PAH are driven by the electrical gradient between cell and lumen.

Redrawn from Pritchard and Miller 408


Figure 14.

Model proposed for excretion of organic cations, including the probe molecule tetraethylammonium (TEA). The basolateral carrier is inhibitable by quinine and driven by the inside‐negative cell potential. TEA+ is exchanged for H+ across apical membrane, and the proton is recycled through an Na+/H+ exchanger.

Redrawn from Pritchard and Miller 408
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M. J. O'Donnell. Mechanisms of Excretion and Ion Transport in Invertebrates. Compr Physiol 2011, Supplement 30: Handbook of Physiology, Comparative Physiology: 1207-1289. First published in print 1997. doi: 10.1002/cphy.cp130217