Cuticular gas exchange by Antarctic sea spiders

Abstract

Many marine organisms and life stages lack specialized respiratory structures, like gills, and rely instead on cutaneous respiration, which they facilitate by having thin integuments. This respiratory mode may limit body size, especially if the integument also functions in support or locomotion. Pycnogonids, or sea spiders, are marine arthropods that lack gills and rely on cutaneous respiration but still grow to large sizes. Their cuticle contains pores, which may play a role in gas exchange. Here, we examined alternative paths of gas exchange in sea spiders: (1) oxygen diffuses across pores in the cuticle, a common mechanism in terrestrial eggshells, (2) oxygen diffuses directly across the cuticle, a common mechanism in small aquatic insects, or (3) oxygen diffuses across both pores and cuticle. We examined these possibilities by modeling diffusive oxygen fluxes across all pores in the body of sea spiders and asking whether those fluxes differed from measured metabolic rates. We estimated fluxes across pores using Fick's law parameterized with measurements of pore morphology and oxygen gradients. Modeled oxygen fluxes through pores closely matched oxygen consumption across a range of body sizes, which means the pores facilitate oxygen diffusion. Furthermore, pore volume scaled hypermetrically with body size, which helps larger species facilitate greater diffusive oxygen fluxes across their cuticle. This likely presents a functional trade-off between gas exchange and structural support, in which the cuticle must be thick enough to prevent buckling due to external forces but porous enough to allow sufficient gas exchange.

Body Size of Temperate Sea Spiders: No Evidence of Oxygen-Temperature Limitations

“…As expected from prior research (Gillooly et al, 2001;reviewed in Glazier, 2005reviewed in Glazier, , 2018Lane et al, 2018), the respiration rate of both Achelia chelata and Achelia gracilipes increased with body size and with temperature. However, counter to the predictions of the oxygentemperature hypothesis, we did not find a significant interaction between temperature and body size in either species; temperature affected aerobic metabolic rate similarly across body sizes.…”

“…Last, pycnogonids have relatively simple gas exchange systems. They lack specialized respiratory structures (Redmond and Swanson, 1968;Markl, 1986) and instead obtain oxygen through diffusion either directly across the cuticle or through cuticular pores (Douglas et al, 1969;Davenport et al, 1987;Lane et al, 2018). Respiratory pigments are also lacking (Redmond and Swanson, 1968;Markl, 1986;Rehm et al, 2012), and oxygen is distributed through the simple open circulatory system by contractions of a weak dorsal heart in the trunk (Tjonneland et al, 1985) and peristaltic contractions of the gut (Woods et al, 2017).…”

Anatomical changes in postembryonic development of Pycnogonum litorale

“…Clusters of epidermal glands may also facilitate gas exchange, especially in species with massive cuticle, since sea spiders do not have dedicated respiratory organs (see Lane et al, 2017, 2018).…”

Phylogenomic resolution of sea spider diversification through integration of multiple data classes

“…Pycnogonids typically have four pairs of walking legs attached to the small body; the cephalon bears an anterior triradiate proboscis, and three pairs of cephalic appendages, the chelifores, palps, and ovigers. Extant Pycnogonida lack both a segmented opisthosoma (abdomen or posterior tagma) and thus, the segmentally iterated opisthosomal respiratory organs that are found in other chelicerates; sea spiders respire instead via cuticular gas exchange, with peristaltic contractions of the gut facilitating oxygen transport through the body [3,4]. Ovigers, a type of modified leg unique to Pycnogonida, are used for grooming and by the males to carry egg masses (figure 1m) [1].…”