The Relationship Between Tissue Ultrastructure
Transparency is a remarkable characteristic of many
oceanic zooplankton. Some degree of transparency is found in almost
all pelagic animals that are not camouflaged by small size or mirrored
surfaces, or protected by fast swimming speeds or chemical defenses,
and it is generally accepted that transparency is an important method
of camouflage from visual predators and/or prey in the optically
featureless pelagic environment. Despite this, almost nothing is
known about the physical basis of transparency in these animals.
Using spectroscopy, electron microscopy, and electromagnetic field
modeling, we investigate the relationships between tissue ultrastructure
and transparency work to develop an understanding of the design
principles of transparency in different tissues and species.
Figure 1: Electron micrographs of the cornea
(left) and sclera (right) of the eye of a shark.
Transparency is found in two major types of tissues: 1) ocular
tissues, and 2) the entire bodies of many pelagic animals. Due to
its medical relevance, most research has focused on the former.
Theoretical and experimental research on the physical basis of transparency
in the vertebrate cornea and lens has shown that tissue ultrastructure
and transparency are intimately related. For example, the cornea
and the sclera (white) of the eye are both constructed primarily
of collagen fibers. However, the collagen fibers in the cornea have
a smaller diameter and are more regularly packed, leading to 95-99%
transparency rather than opacity (Figure 1). The enucleation, elongation,
and high protein concentrations of lens cells are additional structural
modifications that are directly related to increased transparency.
These modifications result in tissues that must be metabolically
supported by surrounding tissue and are predisposed to an eventual
decrease or complete loss of transparency over time (e.g. cataracts).
Given the extremity of these modifications, it is likely that equally
novel modifications have evolved in transparent zooplankton.
For a tissue to be transparent, light must pass through it without
being scattered or absorbed. Except in specialized tissues that
contain pigments, scattering is the more significant barrier to
transparency because very few organic molecules absorb light. Scattering
is caused by variations in refractive index. As light passes from
one material to another, a change in refractive index alters the
light's speed and direction. Highly scattering but non-absorbing
substances can be completely opaque (e.g. snow, milk, clouds). Animal
tissue normally has many variations in refractive index, due to
various components required for life (cells, fibers, nuclei, nerves,
etc.). Even gelatinous zooplankton, which contain a relatively large
amount of water, still may have many refractive index variations
(which generally lead to opacity after the animal dies).
Unfortunately, the relationship between refractive index variation
and light scattering is extraordinarily complicated, and details
about the refractive index distribution inside living tissue are
not often known. Our works attempts to overcome these difficulties
in a variety of ways, including electron microscopy, quantitative
phase microscopy, and modeling light scattering using Mie and Fourier
Figure 2. The salp Salpa maxima. Salps
are pelagic tunicates often found in huge abundance.
Figure 3. The heteropod Pterotrachea sp..
These pelagic gastropods are highly visual predators with
very interesting eyes.
Figure 4: Illustration by Hardy showing transparent
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Gilliland, K. O., Freel, C. D., Johnsen, S., Fowler, C., and M. J. Costello (2004). Random distribution of multilamellar bodies in human age-related nuclear cataracts. Experimental Eye Research. 79: 563-576.
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Widder (1999). The physical basis of transparency in biological
tissue: ultrastructure and the minimization of light scattering.
Journal of Theoretical Biology 199: 181-198.
Johnsen, S., and
E. A. Widder (1998). The transparency and visibility of gelatinous
zooplankton from the north west Atlantic and Gulf of Mexico. Biological
Bulletin (Woods Hole) 195: 337-348.
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