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Marine Biological Laboratory, Woods Hole, Massachusetts 02543
1 Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543.
2 Boston University Marine Program, 7 MBL Street, Woods Hole, MA 02543.
3 Hebrew University of Jerusalem, ESE Department, Interuniversity Institute for Marine Sciences, P.O. Box 469, Eilat 88103, Israel.
4 Department of Life Science, National Tsing-Hua University, 101 Section 2 Kuang Fu Road, Hsinchu 300, Taiwan, R.O.C.
Cuttlefish use body patterns for camouflage on benthic substrata. These body patterns, described by Hanlon and Messenger (1), fall into three broad categories: uniform, in which the whole body of the cuttlefish presents a single design; mottle, in which dark blotches of irregular shapes and sizes cover the body; and disruptive, in which high-contrast features visually disrupt the body outline. The body pattern chosen depends upon the visual input to the cuttlefish and the perception of this input. We can study the animal’s visual perception (1–4) by presenting cuttlefish with various artificial substrate backgrounds and examining the body patterns produced in response.
In this study, a similar behavioral assay was developed as a new tool with which to learn about cuttlefish perception of polarization information. Specifically, we wanted to examine whether cuttlefish discriminate between (i.e., respond differently to) intensity and polarization patterns. In cephalopods, polarization sensitivity (PS) arises from the orthogonal arrangement of microvilli in the retina (5). Although most nerve fibers exiting the eye respond maximally to either vertically or horizontally polarized light (6), the integration of the signals arriving from these PS units is not well understood.
Cuttlefish reared at the National Research Center for Cephalopods in Galveston, Texas, were shipped to the Marine Resources Center at the Marine Biological Laboratory in Woods Hole, Massachusetts. Animals were tested from August 2000 through May 2002, and the experimental procedure followed that of Chiao and Hanlon (3,4). In short, cuttlefish were placed on one of four substrate patterns (illustrated in Fig. 1): (1) black and white checkerboard, (2) polarized checkerboard, (3) digital video image of the polarized checkerboard, or (4) polarized checkerboard but with all filters oriented to polarize the same way. The expected results were to observe disruptive coloration on (1) and (2), and uniform coloration on (3) and (4). In fact, results on the 4th pattern were unexpected, so 5 animals were later examined on a 5th background, a single sheet of continuous linear polarizing filter (Fig. 1, pattern 5). Following Chiao and Hanlon (3), the size of the squares in the checkerboard patterns was determined experimentally for each group of cuttlefish; this was necessary because the size of the checkerboard squares is determined by the size of the "White square" produced on the skin of the cuttlefish (see Fig. 2C). Body pattern definitions follow Hanlon and Messenger (1).
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The patterns were placed underwater in a tank with running seawater. A bottomless PVC box (20 cm x 26 cm) that restricted the animal to the boundaries of the pattern was then placed on top of the pattern. The tank was illuminated evenly from above (at a consistent oblique angle of less than 30°) to minimize shadows by the animals. A digital video camera mounted above the tank recorded a 2-s video clip every minute. Once the video camera was turned on, each session lasted for 30 min, with a total of 60 s recorded. At the beginning of each session, the animal was placed within the PVC box on top of the test substrate pattern and allowed to settle for at least 5 min before recording began. Videotapes were evaluated by assigning a grade (either uniform or disruptive) to each of the 30 two-second video clips. This scoring technique is similar to that used by Chiao and Hanlon (3,4). If the animal was showing a uniform or stipple pattern, it was given a grade of uniform (Fig. 2B). However, if a White square or a White mantle bar was conspicuous, the animal was given a grade of disruptive (Fig. 2C), as were cases in which another conspicuous transverse or bold patterning component was present (see details in ref. 1). Because cuttlefish will only camouflage themselves if they are settled, scores were rejected if the animal was swimming or appeared restless. The grades were used to determine whether an animal showed a uniform or a disruptive body pattern most of the time (Fig. 2D).
Only animals that showed a disruptive body pattern on the black and white checkerboard pattern and a uniform body pattern on the digital video image of the polarized checkerboard were tested. These 16 animals (4 Sepia pharaonis and 12 S. officinalis) did not show a consistent body pattern on any of the polarizing patterns (polarized checkerboard, and all polarized the same way; Fig. 2D). Indeed, of the five animals tested on the uniform polarizing filter, one animal showed a uniform body pattern and four showed a disruptive pattern. Time and other logistical restrictions prevented us from testing more animals on this pattern; this should be a priority in future experimentation.
It is clear from these results that animals showed mixed body patterns (both uniform and disruptive) on all substrates made of polarizing materials (Fig. 2D; Fig. 1, patterns 2, 4, 5). Assuming that intensity and polarization provide equivalent visual information, or that polarization is coded into a type of a gray scale (cuttlefish are color blind, ref. 2), one would predict that cuttlefish would show either a uniform or a disruptive pattern based upon the overall contrast of the backgrounds. The mixed body patterns shown by cuttlefish only on polarized backgrounds indicates that these backgrounds were distinguished from non-polarized ones.
The underwater light environment is partially linearly polarized (7), and polarization underwater also occurs when light hits particles suspended in the water. Cuttlefish use polarization information in predation (8) and could, hypothetically, use polarization sensitivity for navigation because the orientation of partial polarization changes throughout the day. Cuttlefish are also able to produce distinct polarization patterns on their bodies, and these may be used in communication (9). However, despite numerous observations with different types of polarization imaging devices, we detected no evidence that cuttlefish produce polarization body patterns that match or even resemble the polarization of their background. Therefore, cuttlefish probably do not use polarized body patterning for camouflage.
How are polarized backgrounds perceived by cuttlefish, and how is the polarization information linked to body patterning? The animals may have two visual channels, one for polarization information and the other for non-polarization information (such as intensity), and these two channels may interact in higher-order processing. Alternatively, cuttlefish may use opponency processes to extract polarization information (10) by subtracting the responses of units sensitive to vertical e-vectors from ones sensitive to horizontal e-vectors. Since each portion of the animal’s eye has a different field of view, the opponency processing might sometimes enhance the polarization patterns (e.g., subtracting two orthogonal intensities as in the upper circles of Fig. 2A) and at other times reduce the polarization signals (e.g., subtracting two similar intensities as in lower circle of Fig. 2A). Our results do not distinguish these possibilities, yet they do suggest different ways to study how cephalopods perceive polarization signals.
Perception of polarization signals by animals is difficult to study or conceptualize for human investigators, who are mostly polarization insensitive. Body patterning used for camouflage by cuttlefish provides a robust behavioral assay with which to assess visual perception and information processing (2,3,4). The unexpected findings in the report warrant future studies aimed at the interaction between the PS and non-PS channels, and the processing of polarization information.
We thank Janice Hanley and Bill Mebane for help with cuttlefish maintenance, Gabrielle Santore for manuscript preparation, and Bill Saidel and Jean Boal for stimulating discussions. Part of this work was in fulfillment of a Masters Thesis by MMG for Boston University Marine Program. This study was supported by NSF Grant IBN 9729598 to RTH and BSF Grant 1999040 to NS.
Literature Cited
This article has been cited by other articles:
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  C.-C. Chiao, E. J. Kelman, and R. T. Hanlon Disruptive Body Patterning of Cuttlefish (Sepia officinalis) Requires Visual Information Regarding Edges and Contrast of Objects in Natural Substrate Backgrounds Biol. Bull., February 1, 2005; 208(1): 7 - 11. [Full Text] [PDF]
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