Divergent respiratory modes drive differences in heat tolerance and habitat use among tropical intertidal crabs

Abstract

Physiological adaptations for amphibious living underpin successful sea-to-land transitions and shape thermal tolerance. Intertidal brachyurans crabs independently evolved contrasting respiratory strategies: air-breathing lungs in fiddler crabs (Gelasiminae) and water-dependent gill respiration in sentinel crabs (Macrophthalmidae). How these strategies influence thermal performance, vulnerability to climate change, and habitat use remains poorly understood. We examined whether air- versus water-breathing strategies affect the oxygen delivery and upper thermal limits in closely related intertidal species, Macrophthalmus tomentosus (Macrophthalmidae) and Tubuca arcuata (Ocypodidae). We measured cardiac performance, oxygen consumption (ṀO2) and haemolymph oxygen partial pressure (PO2) across 25-40°C in both air and water. The air-breathing T. arcuata exhibited higher upper lethal temperatures (mean±s.e.m.: 42.2±0.4°C versus 41.65±0.6°C) and maintained exponential increases in ṀO2 when breathing air, despite inhabiting a cooler microhabitat. Additionally, T. arcuata sustained higher arterial and venous PO2 during aerial heating, indicating efficient oxygen delivery near their thermal limits. In contrast, M. tomentosus was severely oxygen-limited during emersion, with 90% impaired recovery, and exhibited oxygen deficits under present-day warm habitat conditions, implying that extant populations operate near their physiological thresholds with minimal thermal safety margins. Both species showed constrained performance when submerged at high temperatures, indicating universal oxygen limitation in water. Our findings show that the evolution of air breathing improves oxygen delivery across environmental stressors, thereby enhancing aerobic scope and thermal resilience. Our approach provides a mechanistic explanation for both current habitat partitioning and differences in climate vulnerability among tropical intertidal crabs.