Ancestral form and function of larval feeding structures are retained during the development of non-planktotrophic gastropods.

Mode of development (MOD) is a key feature that influences the rate and direction of evolution of marine invertebrates. Although many groups include species with different MODs, the evolutionary loss of feeding larvae is thought to be irreversible, as the complex structures used for larval feeding and swimming are lost, reduced, or modified in many species lacking feeding larvae. This view is largely based on observations of echinoderms. Phylogenetic analysis suggests that feeding larvae have been re-gained in at least one species of calyptraeid gastropod. Further, its sister species has retained the velum, the structure used for larval feeding and swimming. Here, we document velar morphology and function in calyptraeids with 4 different MODs. Embryos of Crepidula navicella, Crepidula atrasolea, Bostrycapulus aculeatus, Bostrycapulus odites, Bostrycapulus urraca, Crepipatella dilatata, Crepipatella occulta, Crucibulum quiriquinae and Crepidula coquimbensis all hatch as crawling juveniles, yet only Crepidula coquimbensis does not make a well-formed velum during intracapsular development. The velar dimensions of 6 species with non-planktotrophic development were similar to those of planktotrophic species, while the body sizes were significantly larger. All of the species studied were able to capture and ingest particles from suspension, but several non-planktotrophic species may ingest captured particles only occasionally. Video footage suggests that some species with adelphophagic direct development capture but frequently fail to ingest particles compared to species with the other MODs. Together these lines of evidence show that, among calyptraeids at least, species that lack planktotrophic larvae often retain the structures and functions necessary to successfully capture and ingest particles, reducing the barriers to the re-evolution of planktotrophy.

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

AbstractOxygen limitation has been proposed as one of the key factors that limits body size at high temperatures (the oxygen-temperature hypothesis). Geographic patterns in body size are thought to be driven in part by the effects of temperature on oxygen supply and demand, particularly when the increased oxygen demand of tissues at higher temperatures outpaces the ability of large organisms to supply internal tissues with oxygen. We tested the effects of temperature on the rate of oxygen consumption of two temperate sea spider (Pycnogonida) species, Achelia chelata and Achelia gracilipes, across a range of body sizes. We measured oxygen consumption at 5 temperatures: 12, 16, 20, 24, and 28 °C. Oxygen consumption of both species increased significantly with temperature, but the effect did not depend on body size; thus, we found no evidence to support the oxygen-temperature hypothesis. While previous interspecific studies on Antarctic pycnogonids have found that larger-bodied animals have more porous cuticles, thus potentially offsetting their higher aerobic metabolic demand by increasing oxygen diffusivity, the pore area of the cuticle of the two temperate species did not change with body size. This suggests that the generally small size of warm-water sea spiders may be due to selective factors other than oxygen limitation.

Polar gigantism and the oxygen-temperature hypothesis: a test of upper thermal limits to body size in Antarctic pycnogonids.

The extreme and constant cold of the Southern Ocean has led to many unusual features of the Antarctic fauna. One of these, polar gigantism, is thought to have arisen from a combination of cold-driven low metabolic rates and high oxygen availability in the polar oceans (the 'oxygen-temperature hypothesis'). If the oxygen-temperature hypothesis indeed underlies polar gigantism, then polar giants may be particularly susceptible to warming temperatures. We tested the effects of temperature on performance using two genera of giant Antarctic sea spiders (Pycnogonida), Colossendeis and Ammothea, across a range of body sizes. We tested performance at four temperatures spanning ambient (-1.8°C) to 9°C. Individuals from both genera were highly sensitive to elevated temperature, but we found no evidence that large-bodied pycnogonids were more affected by elevated temperatures than small individuals; thus, these results do not support the predictions of the oxygen-temperature hypothesis. When we compared two species, Colossendeis megalonyx and Ammothea glacialis, C. megalonyx maintained performance at considerably higher temperatures. Analysis of the cuticle showed that as body size increases, porosity increases as well, especially in C. megalonyx, which may compensate for the increasing metabolic demand and longer diffusion distances of larger animals by facilitating diffusive oxygen supply.

Cuticular gas exchange by Antarctic sea spiders.

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.

Upper limits to body size imposed by respiratory-structural trade-offs in Antarctic pycnogonids.

Across metazoa, surfaces for respiratory gas exchange are diverse, and the size of those surfaces scales with body size. In vertebrates with lungs and gills, surface area and thickness of the respiratory barrier set upper limits to rates of metabolism. Conversely, some organisms and life stages rely on cutaneous respiration, where the respiratory surface (skin, cuticle, eggshell) serves two primary functions: gas exchange and structural support. The surface must be thin and porous enough to transport gases but strong enough to withstand external forces. Here, we measured the scaling of surface area and cuticle thickness in Antarctic pycnogonids, a group that relies on cutaneous respiration. Surface area and cuticle thickness scaled isometrically, which may reflect the dual roles of cuticle in gas exchange and structural support. Unlike in vertebrates, the combined scaling of these variables did not match the scaling of metabolism. To resolve this mismatch, larger pycnogonids maintain steeper oxygen gradients and higher effective diffusion coefficients of oxygen in the cuticle. Interactions among scaling components lead to hard upper limits in body size, which pycnogonids could evade only with some other evolutionary innovation in how they exchange gases.

No Effects and No Control of Epibionts in Two Species of Temperate Pycnogonids.

Essentially all surfaces of marine plants and animals host epibionts. These organisms may harm their hosts in a number of ways, including impeding gas exchange or increasing the costs of locomotion. Epibionts can also be beneficial. For example, they may camouflage their hosts, and photosynthetic epibionts can produce oxygen. In general, however, the costs of epibionts appear to outweigh their benefits. Many organisms, therefore, shed epibionts by grooming, molting, or preventing them from initially attaching, using surface waxes and cuticular structures. In this study, we examined how epibionts affect local oxygen supply to temperate species of pycnogonids (sea spiders). We also tested the effectiveness of different methods that pycnogonids may use to control epibionts (grooming, cuticle wettability, and cuticular waxes). In two temperate species: Achelia chelata and Achelia gracilipes, epibionts consisted primarily of algae and diatoms, formed layers approximately 0.25-mm thick, and they colonized at least 75% of available surface area. We used microelectrodes to measure oxygen levels in and under the layers of epibionts. In bright light, these organisms produced high levels of oxygen; in the dark, they had no negative effect on local oxygen supply. We tested mechanisms of control of epibionts by pycnogonids in three ways: disabling their ovigers to prevent grooming, extracting wax layers from the cuticle, and measuring the wettability of the cuticle; however, none of these experiments affected epibiont coverage. These findings indicate that in temperate environments, epibionts are not costly to pycnogonids and, in some circumstances, they may be beneficial.