Year of Award

2018

Document Type

Dissertation

Degree Type

Doctor of Philosophy (PhD)

Degree Name

Organismal Biology, Ecology, and Evolution

Department or School/College

Division of Biological Sciences

Committee Chair

H. Arthur Woods

Commitee Members

Doug J. Emlen, Scott R. Miller, Amy L. Moran, Bret W. Tobalske

Keywords

Allometry, Metabolism, Oxygen, Pycnogonids, Rate of diffusion

Subject Categories

Ecology and Evolutionary Biology

Abstract

All animals must breathe to survive. The types of primary respiratory structures vary across the metazoa, and the overall size and components of these structures scale with body size. The scaling of respiratory structures has been well studied in vertebrate lungs and gills, but very few, if any studies, have looked at it in terms of cutaneous gas exchange, the process where oxygen moves across the outer integument via diffusion. My dissertation has sought to fill this gap in knowledge by studying animals that use cutaneous respiration, and my work has determined both how the components of their respiratory surfaces function and how they scale with body size. Using sea spiders as a model for cutaneous respiration, I answered these three specific questions: 1) How does a major but poorly studied group of marine arthropods exchange respiratory gases (Ch 1)? 2) How does the physiology and morphology underlying gas exchange scale with body size (Ch 2)? And 3) How do communities of organisms living on the surface of sea spiders (i.e., epibionts) affect their gas exchange and biomechanics (Ch 3 & 4)?

Sea spiders (pycnogonids) are a globally distributed group of marine arthropods that span over five orders of magnitude in body size (Arnaud and Bamber, 1987). They lack gills and rely entirely on cutaneous respiration, which may be facilitated by pores in the cuticle (Davenport et al., 1987). The largest species live in the deep sea and around the poles, which also makes them a common and charismatic example of polar gigantism (Dell 1972), a biogeographic pattern describing the observation that taxa living near the poles often reach unusually large sizes. Sea spiders are an excellent group for studying the scaling of respiratory structures and gas exchange because they have a simple, tractable respiratory system, and there is great variation in body size across the group. Sea spiders have been studied for over a century, yet we still do not know the functional aspects of how they breathe nor how their respiratory surfaces have evolved to allow them to reach such large sizes.

In chapter one, using a combination of empirical measurements and mathematical modeling, I show conclusively that sea spiders take up oxygen across pores in their cuticle. Furthermore, larger species obtain sufficient fluxes of oxygen not by increasing the number of pores in their cuticle, but rather by increasing the total pore volume across their body.

In chapter two, I show that the scaling of respiratory components in sea spiders sets upper limits to body size. Cuticle porosity increases with body size, but it cannot increase indefinitely as a cuticle that is too porous may collapse due to external forces. Additionally, internal oxygen concentration decreases with increasing body size, but this concentration physically cannot go below zero. In addition, when levels of internal oxygen fall low enough, the animal likely fuels metabolism using anaerobic pathways, which is unsustainable for long periods. Therefore, these two variables constrain body size, and the constraints cannot be overcome without some other innovation in the way that sea spiders exchange gases.

Finally, in chapters three and four, I show that the costs and benefits of epibionts vary with ambient conditions. When sea spiders are illuminated by sunlight, photosynthetic epibionts increase external oxygen levels, which may benefit their hosts by increasing the rate of oxygen flux into the sea spider’s body. In the dark, encrusting epibionts reduce external oxygen levels and greatly reduce how quickly oxygen can diffuse into the sea spider, which will reduce the total inward flux of oxygen. These epibionts have no effect on host locomotion, but they increase the drag the animals experience, which likely increases the sea spider’s risk of dislodgement or reduces their behavior during periods of high flow.

The surface of animals that exchange gases across their outer integument often serves two primary functions: gas exchange and structural support. These animals must balance a trade-off in which the integument is thin and porous enough to allow sufficient gas exchange but strong enough to withstand external forces. My dissertation shows that this trade-off can limit the maximum body size of these animals in multiple ways. Additionally, sea spiders are an important part of the Antarctic benthos and a common model for polar gigantism, yet little is known about their physiology and role in the ecosystem. My research provides an important first step in understanding the physiology of these animals that can help explain their role in the Antarctic ecosystem.

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© Copyright 2018 Steven Joseph Lane