The evolution of air-breathing in crustaceans: A functional analysis of branchial, cutaneous and pulmonary gas exchange

Abstract

1. 1. The evolution of aerial gas exchange in land crabs is correlated with a transition from diffusion limited gills (L diff, 0.88–0.92), via a bimodal, diffusion limited “skin” (vascularized branchial chamber epithelium)/gill system (L diff, 0.53–0.63), to the perfusion limited, invaginated lung of the mountain crab Pseudothelphusa (L diff, 0.008–0.145) (L diff, is used as an index of diffusion limitation); a glossary of terms is presented at the end of the Abstract. 2. 2. The reduction in diffusion limitation with the evolution of the lung in land crabs reduces the mean oxygen diffusion gradient (ΔPgO2) required to generate gas transfer at the exchange surface (gill and “skin”, 86–108 mmHg; lung, 59–69 mmHg). 3. 3. The reduction in (ΔPgO2) and concomitant elevation in (PaO2) (gill, 14–19 mmHg; “skin”/gill, 50–100 mmHg; lung, 120–140 mmHg) and PvO2) (gill, 7–8 mmHg; “skin”, 7–25 mmHg, lung, 20–28 mmHg) facilitates oxygen diffusion to the tissues (i.e. potential for large ΔPvO2—PcellO2). 4. 4. The elevation of mean blood oxygen tension at the gas exchange surface (PaO2 + PvO2/2) with the evolution of the land crab lung is matched by a decrease in the in vivo blood oxygen affinity (i.e. elevated blood P50: gill, 10 mmHg; “skin”/gill, 13–21 mmHg; lung, 26–28 mmHg) which ensures 100% O2 saturation at the gas exchange organ and 40–60% O2 delivery to the tissues. 5. 5. The low ventilation requirement of air-ventilated “cutaneous” and invaginated lungs, compared to water-ventilated gills, leads to an elevation in pulmonary air PMCO2) (i.e. PACO2 3–7 mmHg at PAO2 140–154 mmHg) and a concomitant increase in blood P,CO2 levels in land crabs (P,CO2: gill, 3.6–4.1 (< 5) mmHg; “skin”/gill, 7.5–15 mmHg; lung, 8–12.5 mmHg) (c.f. aquatic gill breather, PaCO2, 2–3 mmHg). 6. 6. A potential respiratory acidosis associated with elevated air and blood P,CO2 levels in the intermittently ventilated lungs of land crabs is compensated by an elevation in blood bicarbonate levels (CaCO2: gill, 8–12 mM/1; “skin”/gill, 8–19 mM/1; lung 14.5–25 mM/1) (c.f. aquatic gill breather, CaCO2 = 4–8 mM/1). At the pH of crab blood the directly measured variable C,CO2 is almost exclusively in the form of the bicarbonate ion. 7. 7. The evolution of air-breathing in land crabs leaves them poorly equipped for secondary water breathing via reduced gills as (a) gas transfer is impaired at the exchange surface (i.e. low PaO2, 17–27mmHg/high PaCO2, 5–6.5 (> 5) mmHg; L diff, 0.91–0.95, indicating predominant diffusion limitation) compared to primary water breathing crabs (PaO2, 50–100mmHg/PaCO2 2–3 mmHg; L diff, 0.45–0.48) and, (b) blood oxygen loading at the gills is impaired (48–52% of “air-breathing” C,O2) at the low post branchial oxygen tensions (17–27 mmHg) generated during submergence as a consequence of the evolution of a high “air-breathing” blood P50. 8. 8. The evolution of air-breathing in crustaceans described above closely parallels that of the vertebrates, but all land crabs retain gills and the potential for bimodal respiration if water is available. By the vertebrate analogy land crabs appear to have reached the lungfish stage of evolution into the terrestrial environment. 9. 9. Land crabs differ fundamentally from vertebrates in maintaining blood PaCO2 < 15 mmHg (c.f. mammals, birds, PaCO2, 30–40 mmHg) either (a) by CO2 excretion via the branchial aquatic route when water is available or, (b) in the instance of the “lung crab” Pseudothelphusa, by elevating blood PaO2 to exceptionally high levels (120–140 mmHg) thus “blowing off” CO2 (PaCO2 < 12.5 mmHg) across the perfusion limited lung. 10. 10. The maintenance of low P,CO2 levels in crustaceans may be associated with a limited capacity for extracellular acid-base regulation and the necessity to maintain the functional integrity of haemocyanin in the face of a potential Root effect at high P,CO2 levels. This appears to be a principal factor in limiting the terrestrial diversity of the Crustacea. 11. 11. Extending the lungfish analogy, the “lung crab” Pseudothelphusa also survives prolonged droughts (desiccation) during the dry season by virtue of having evolved a perfusion limited lung with a low ventilation requirement which enables it to limit convective and evaporative respiratory water loss. The perfusion limited lungs of crustaceans and vertebrates appear to have evolved primarily as an adaptation to conserve water at depressed levels of activity (aestivation) during the tropical dry season. The vertebrates have subsequently exploited the potential endowed by a large pulmonary diffusing capacity to elevate V,O2MAX) and diversify into a wide array of terrestrial habitats.