C THE PATTERN CHANGE OF ACCLIMATION TO NOVEL GRAINED SUBSTRATES OF THE SPECKLED SANDDAB ABSTRACT studied the pattern changing abilities of the Speckled Sanddab by acclimating sandy patterned fish to a rocky substrate and rocky patterned fish to a sandy substrate. Both rocky and sandy fish demonstrated the ability to alter their pattern to match a nove substrate. After 8 days of acclimation, rocky fish matched sand bettet than sandy fish matched rock. Whether this was the result of all fish becoming sandier af ter removal from the field is not certain. There may be a cost to maintaining a rocky morphology. If so, it would be more difficult for a sandy fish to gain a rocky morphology than it would for a rocky fish to gain a sandy morphology. Sandy fish showed a greater fidelity to their original substrate than rocky fish, indicating that a lower ability to effectively match another substrate limits the freedom afish displays in choosing a new substrate. INTRODUCTION Cryptic coloration is an important method of defense for many animals. The ability to match a background effectively in the presence of visual predators can be cructal for survival. Flatfish are among the best camouf laged of all fish, with their ability to lie flat on the ocean floor buried in the sand or mud. Ideally, a species using cryptic coloration as a survival tool should be able to match any substrate on which it is placed, yet most creatures naturally selected to match a certain environment are limited in their abilities to adapt to novel environments while SCUBA diving in the Hopkins Harine Life Refuge, 1 observed that the sanddabs, Citharichthys stigmaeus, on a uniform sand bottom have extremely different pigment patterns than the sanddabs on the adjacent substrate of gravel, broken shells, and algal fragments closer to shore This led me to ask two questions: How well and how quickly can sanddabs match new backgrounds? Do these fish remain on the substrate to which they are best adapted, or do they move about freely between substrates? Research on flatfish coloration shows that most species of flatfish have the ability to change or adjust their color patterns using two methods. There is an instantaneous color change, which is an immediate and temporary lightening or darkening of the fish, and there is a morphological change, which takes place over a longer period of time resulting in a more permanent change in color or pattern. Conditions that cause instantaneous pattern changes eventually lead to morphological pattern changes (Brown, 1957.) Studies on plaice show that the young fish, which are found nearshore, have semi-permanent white spots that are not seen on adults, which live in the muddy bottom. However, when the adult fish are placed on white pebbbles, these spots reappear (Cott,1940.) Work with Paralichthys albiguttus demonstrates that this fish can appear finely mottled when placed on a checkerboard of small black and white squares and coarsely mottled on a checkerboard of large squares (Parker, 1971.) designed a set of experiments to answer my questions about the background matching abilities and substrate fidelity of the Speckled Sanddab. By placing different patterned fish on novel substrates, observed that both rocky and sandy sanddabs possessed the ability to alter their patterns to match new backgrounds, and that sandy fish showed a grester fidelity to their substrate than rocky fish. HATERIALS AND FETHODS Using SCUBA gear and a small handnet, I collected 28 Speckled Sanddabs, Citharichthys stigmaeus, of sizes 6.5 to 11 cm. Fourteen of these fish had sandy patterns and were collected from the sandy substrate in the channel between Hopkins Harine Station and the Monterey Bay Aquarium at a depth of 20 feet. The other 14 fish were collected at a depth of 10 feet from the area between Seal Rock and the railroad tracks off Agassiz Beach, where the substrate consisted of gravel, broken shells, sandy patches, and algae fragments; these fish had speckled morphologies (for map of collection sites, see Figure 1.) Since there was within site vartability of substrate type, especially within my designated type "rocky", I made 10 measurements with a 25 cm x 25 cm transect at each of the two collection sites to quantify the makeup of the substrates. The transect was haphazardly dropped and substrate descriptions were recorded from the four corners and the center. Fish were anesthetized with quinaldine and tagged with a color code of embroidery beads sewed through the posterior dorsal muscle mass with nylon thread. Fish were maintained in two outdoor tanks with equal exposure to sünlight and fresh running seawater, each containing a substrate collected from the two capture sites. Each 1.5 square meter tank contained 7 experimental and 7 control fish. The fish were fed mussels and squid every 4 days. photographed each fish 8 hours after collection to record initial pattern morphology. The fish were then placed in the tanks and photographed 24 hours after initial acclimation and every 48 hours thereafter to document the pattern change as adaptation to a different substrate occurred. For photographing, fish were placed in a dish of seawater with a gray scale and ruler as a background. They were Iluminated with four 300 watt reflector flood lamps and photographed using Agfa Pan 100 speed film in a 35 FM Nikon F2 camera mounted 22 cin above the dish. Photographs were also taken of the two substrates, Fish were tested for substrate preference in an aquarium in which the bottom was half sand and half rock. The substrates in the tank were collected from the fish capture sites. Fish were quided onto the dividing line between rock and sand through a clear cylindrical chute. Each control fish was sent down the chute 3 times and substrate choices were scored. This was repeated for each control fish every day for 17 days. Two methods of analyzing pattern changes were employed: human ranking and digital image processing. A pattern scale of 1 (most rocky) to 5 (most sandy) was established based on five representative photographs of different fish (see Figure 2). 25 photographs of fish at day O and 25 photographs of the same fish acclimated for 8 days were shuffled together and scored on this scale of 1 to 5 by 15 unbjased judges. Three sandy patterned fish acclimating to rock died during the 8 day period and could not be scored. By subtracting the pre-acclimation score from the post-acclimation score for each fish, l obtained a value for the magnitude and direction of pattern change. A positive change indicates the fish became more sandy; a negative change indicates the fish became more rocky. Hean pre- and post-acclimation values, as well as net change values, were obtained for each group of fish (rocky and sandy, controls and experimentals.) he rate of acclimation was determined from 6 photographs taken during the acclimation of 4 fish. The middle 4 photographs in each series were removed and shuffled, leaving the first and last photographs as endpoints. 5 unbiased judges were instructed to place the 4 intermediate photographs from each series in order from initial pattern morphology to final. Each misplaced photograph was assigned a value of to 3, depending on how far from its correct position the photograph was placed (for example; if the series' original order was "ABCD" and the photographs were arranged "BDCA", the A position would be assigned 1. the B position 2, the C position O, and the D position 3.) By observing the time after which visually obvious changes in pattern morphology could no longer be distinguished, I was able to estimate sanddab acclimation rate to a new substrate Digital image processing was used to analyze a few representative photographs as a demonstration that this technology may be applied as a valuable complement to other forms of photographic analysis. The image processing was conducted on the MegaVision 1024-XM computer with input from a video camera. Photographic images were stored in 1024 X 1024 arrays of pixels, with each pixel assigned a gray value from 0 (black) to 255 (white).I selected pre- and post-acclimation photos for one rocky fish placed on sand and for one sandy fish placed on rock (see Figures 4 & 5, respectively), Histograms of the gray scale values for a small area around the same eyespot on each fish were obtained to compare how this specific area changed af ter 8 days of acclimation to a different substrate. Histograms of gray scale values for equal sized areas of sand and rock were also obtained for comparison of the two substrates. The command "scanner" was used to input the video image of the black and white print into one of the temporary memories. "Polygon was used to create a template so that several photographs of the same fish could be aligned. This command was then used to create a sample area for the analysis of gray scale values from an image. "Hpolygon created a histogram of gray scale values from the image within the polygon. "Hlist" was used to obtain the raw data from the histogram, which was stored onto a floppy disc and transferred to Lotus for graphing. To compensate for differences in exposure or development of the photographs, "sample" was used to obtain point readings of gray scale values from the image, and "mapper" was used to equalize existing differences. RESULTS Pre-acclimation rocky fish had an average pattern score of 1.75, whereas pre-acclimation sandy fish had an average pattern score of 4.48. After the 8 day acclimation, rocky fish on rock became sandter by a degree of 1.04; rocky fish on sand became sandier by 2.41 degrees. The sandy fish on sand showed an increase in sandiness of 46 degrees, whereas the sandy fish on rock became rockier by 53 degrees (See Table and Figures 4-8). One-tailed, rank sum two sample tests show that there is a significant difference between the pattern change of experimental and control fish (p-.006 for rocky fish, p-03 for sandy fish, see Table 1.) After 8 days of acclimation, rocky fish matched a sandy substrate better than sandy fish matched a rocky substrate (See Figures 9 & 10.) When given the choice between rocky and sandy substrates, rocky control fish chose the sand 56% of the trials. Sandy control fish demonstrated a greater preference for sand by choosing the sandy substrate 76% of the trials (See Table 2 and Figure 11) A Mann-whitney statistical analysis was performed between the means of percent preference for sandy substrate by rocky and sandy controls to demonstrate that this difference is significant (p-.0025, see Table 2.) Most of the visually obvious pattern changes of sanddabs acclimating to a new substrate took place within the first 3 to 5 days. It was this time range in which it became difficult to distinguish the differences between photographs of the same fish (See Table 3.) At the collection site for the sandy fish, the substrate consisted of 100% sand. However, at the collection site for the rocky fish, the substrate was composed of 488 rocky gravel and broken shells coyered with algae; 428 bare, finer gravel, and 102 sand, which was dispersed in small patches ranging from 5 to 10 inches in diameter. The histogram of rocky substrate shows a much greater spread of gray values than the histogram of sandy substrate. The histograms documenting the change of gray values of the rocky fish before and after acclimation to sand show that the spread of gray values is greatly reduced after 8 days. The histograms of the sandy fish acclimating to rock show little change except a general darkening (see Figures 12-15.) DISCUSSION Flatfish possess a large ability to change their patterns to adapt to new substrates. The pattern is largely determined by the percent cover within independent patch distributions of two different pigment structures found in the speckled sanddab, melanophores and iridophores. The melanophore is a reticulate cell that can disperse or concentrate the dark pigment it contains, quickly varying its contribution to the background shade. The iridophore contains intracellular layers of white quanine crystals which are fixed in position. Iridophores can not quickly vary their contribution to background shade like melanophores, (Hoar, 1969.) In an instantaneous change, the pattern and degree to which existing melanophores are open is varied against the fixed background pattern of tridophores. A morphological pattern change results in a change of the total amount of pigment or net number of pigment cells present. Morphological changes occur within melanophore patterns, but may also occur more slowly with iridophore patterns. Acclimations longer than 8 days would need to be performed to observe changes in the patterns of tridophores. The patterns of rocky and sandy fish are extremely different, yet both types express some aspect of a basic pattern of black eyespots and white dorsal, ventral, and lateral line spots. Observations through a dissecting scope show that the black eyespots are composed mainly of melanophores and the white spots are composed mainly of iridophores. On a rocky fish, tridophores are densely packed to form the characteristic white spots and are sparsely distributed over the rest of the fish. On a sandy fish, these iridophores are much more evenly distributed, with only loose clusters of iridophores at the characteristic spot sites. On the rocky fish, the melanophores highlight the white irridophore spots by being densely packed in the areas between the spots and by being sparsely distributed over the spots. On the sandy fish, the melanophores are evenly distributed among the iridophores. It is not exactly clear whether these areas of densely packed pigment structures contain a high density of cells, a high concentration of pigments, or both. It is also not clear whether areas of sparse distibution of pigment structures contain a low density of cells, a low concentration of pigments, or a combination of the two. When a rocky fish acclimates to sand, it lightens the dark areas of its pattern and darkens the white spots to achieve an even tone. This can be seen in the histograms of the rocky fish before and after acclimation to sand. The histogram before the acclimation shows a wide spread of gray values, whereas the histogram af ter the acclimation shows a much narrower range of values, much like the histogram of the sandy substrate (see Figure 14) The fish, however, does not lose its blotchy pattern, only its contrast. This suggests that the pattern change of the 8 day acclimation was a change in the melanophores, and not a rearrangement of the iridophores. Whether the fish is actually decreasing its total number of melanophores in the dark areas and increasing the number of melanophores over the iridophore spots, or is merely adjusting existing melanophores is not certain. It is also not clear whether the irridophore pattern is completely permanent or if it can show plasticity after acclimation longer than 8 days. Asandy fish acclimating to rock shows the reverse type of response of a rocky fish acclimating to sand. The iridophore spots become lighter and the area between the spots becomes darker. Although contrast was changed, the sandy pattern was never lost, again suggesting a change in the melanophores rather than in the iridophores. However, since fridophores are less densely packed in the pattern spots, the lightened areas are not as large or white as those of a rocky fish. The histograms of the sandy fish acclimating to rock Illustrate this point by showing little change in the spread of gray values af ter the acclimation and show only a general darkening (see Figure 15.) It is interesting that there is a basic pattern expressed by all sanddabs. This pattern, which can be used so effectively to adapt to new substrates by increasing and decreasing contrast, gives any sanddab that lands on a coarse graîned substrate a chance to match adequate ly until the final pattern can be perfected, if the fish remains on that substrate. Also, this pattern does not interfere with matching to a fine grained substrate. The pattern is advantageous for a rocky fish because rocky substrate is not 100% rock; it is composed of rock, gravel, broken shells, and sand patches. Fish that possess this pattern can adapt to all of these quickly as they move about the rocky substrate and are likely to be selected for. Sandy patterned fish possess aspects of this easily adaptible pattern as well, showing that perhaps these fish are migratory and move over a variety of substrates, or that their life cycle may expose them to different grains of substrates at different stages of development. The grain of a sandy substrate to a tiny, newly-settled fish may be relatively large, so the adaptable pattern set on a small scale serves the tiny fish well. Since rocky fish acclimating to sand matched the sand better than sandy fish acclimating to rock matched the rock, it would seem that rocky fish show a much greater ability to change than sandy fish (See Figures 9 ≈ 10) However, there is a general trend for the fish in my experiment to become more sandy. Both control groups displayed an increase in sandiness af ter 8 days. This could be the result of one or a C combination of several factors. Perhaps the substrates in both tanks were actually "sandter" than the substrates in the field. Overcrowding or the dict of oquid and musoclo may have pomchow decreased rocky pattern stability. Since sandy fish were collected 10 feet deeper than the rocky fish, and light decreases with ocean depth, perhaps a decrease in light causes an increase in sandiness. If this were true, and the fish in the tanks recieved less light than fish at 20 feet of depth, sandiness would be increased. Another explanation is that there is some cost involved with possessing a rocky morphology, and that removing these fish from the field somehow reduced the pressure to maintain this morphology, causing the fish to become more sandy. If this is the case, then this cost is most likely the energy spent on maintaining the expression of the highly plastic melanophores in dark bands and patches. Sandy fish, when given the choice between rock and sand, seemed to display a preference for sand by choosing sand 768 of the trials. Rocky fish, when presented with the same choice, displayed little preference for either rock or sand. This correlates well with what has been presented. Sandy fish do not seem able to immediately match a rocky substrate. This could be the result of not having large irridophore spots to higfilighit with melanophore changes and create a high contrast pattern, or it could be that obtaining and maintaining a rocky morphology is too energetically costly. Since sandy fish are not able to bury in the rocky substrate for camof lage, they remain in the sand where they match best. Rocky fish, however, seem to be able to adapt quickly to a sandy substrate. This could be the result of possessing an irridophore pattern with easily reduceable contrast, or it could be energetically favorable to discontinue maintenance of melanophore bands and patches. Fish acclimating to a sandy substrate also have the ability to bury in the sand for added camouf lage during the early stages of adaptation, since it takes 3 to S days to complete the matching. Rocky fish do not seem to be limited by an insbility to background match when choosing between rock and sand. If à cost to maintaining a rocky morphology does exist, then what sort of benefits does a rocky fish recieve to counteract that cost? It allows the fish to to exploit a habitat unavailable to their most efffective competitors, members of the same species adapted to sandy substrate. Perhaps Iiving on a rocky substrate provides access to better food. More or tastier crustaceans may live within the gravel and broken shells than in the sandy bottom. The sanddab may eat the algae that settles or grows only on the rocky substrate. Perhaps the advantage is less exposure to larger open water predators that may not come into the shallow waters nearshore. CONCLUSION Rocky and sandy sanddabs both demonstrated an ability to change their patterns to adapt to novel substrates. Rocky fish matched sand better after 8 days of acclimation than sandy fish matched rock, which was probably the result of the general trend for the fish in the experiment to become more sandy. All fish displayed aspects of the same basic pattern of iridophore spots, although the pattern was more pronounced in the rocky fish. Since it is eastly highlighted or de-accentuated, probably by the action of melanophores, this basic pattern seems to offer a great deal of flexibility to the sanddab in matching many grains of substrates. C Literature Cited Brown, Hargaret E. 1957. The Physiology of Eishes, Volume 111. Academic Press Inc. pp 387-401. Cott, Hugh B. 1940. Adaptive Coloration in Animals. Oxford University Press. pp 27-30. Hoar, W. S. and D. J. Randall. 1969. Fish Physiology, Volume 111. Academic Press Inc. pp 307-313. Parker, George Howard, 1971. Animal Color Changes and Their Neurobumours. Hafner Publishing Co. pp 169-175.0 Pasternak, Dahna. 1987. "Quantitative Analysis of Background Matching of Sepia officinalis" Stanford University Hopkins Marine Station Final Papers Biology 175H. (unpublished.) Zar, Jerrold H. 1974. Biostatistical Analysis. Prentice-Hall Inc. pp 09-12 ACKNOWLEDGEMENTS: Hopkins Marine Station in Pacif ic Grove California is à poem, a stink, à grating noise, a quality of light, a tone, a habit, a nostalgia, a dream. Hopkins Marine Station is the gathered and scattered, the pyrex dish, the plastic bucket, the broken gate and weedy lots and hidden keys, sanddab fishtanks of corrugated iron, honky tonks(Agassiz), restaurants(JC canyon), and whore houses(Hawthorne), and little crowded groceries(Nob Hill), and laboratories(Lily), and flophouses(Fisher). Its inhabitants are, as Chuck Baxter once said, "whores, pimps, gamblers, and sons of bitches, by which he meant the Spring Class. Had the man looked through another peephole he might have said, "Saints and angels and martyrs and holy men of science," and he would have meant the same thing. would like to thank Chuck Baxter, my advisor, for the exchange of ideas, be they in the form of taxonomic loquacities, insightful paper revisions, or hasty pool shooting blather. would like to thank Mark Denny, my secondary advisor, for all of his help, advice, assistance, chicken curry, and fourrier transform explanations. would like to thank Ladd Johnson for taking some large chunks of time to really sit (split infinitive) down and look at the data. l'Il name my first ANOVA after you. Iwould like to thank the Squid Festival for forcing Emily Carrington to seek out strange new buddy forms for some amazing diversions. Here we are on ze Calypso... would like to thank Chris Patton for film, for opening up the door, and for film. And finally, would like to thank the words "rocky", "sandy", "acclimate" and "substrate", without whose existence this paper would not have been possible. O Table Legends Table 1. Mean pattern morphology values for each fish day O day 8, and the net change. Below: one tailed, rank sum two sample statistical sts. Table 2. Percent selection of sandy substrate by rocky and sandy patterned fish. Below: Mann-Whitney statistical test. Table 3. Rate of acclimation determination: values assinged to misplaced photographs. O ROt CONTROL (on reck) ROCKY FISH XFERIMI ENTAL (on sand) SANDY FISI CUNTROL (on sand) SANDY FI RIMENTAL (an reck) (ONE TAILE FIEH ROCI SANDY FISH RAHE TAELE 1. INDIVTDUAL MEAN D.DEV. SAMFLE ERRUR STD.DEV. SAMFLE D.ERROE FEA TD.DE SAMFLE S STD.E FiEAN TD. DEV. SAMFLE SUM TUO CHOMGE CHANG CHANC CHANGE OF SAMFLET CONTRCI EXFERI ENTAL RO XFERIHENTAL FAT Before 1.1 1.6 3 1 4 1.76 O.33 6.27 .1 1. 1.53 1.C 1. 1. O.. O.18 4. 367 4.8 41 4.8 4.41 O.C 0.24 2.6 473 4.73 4.7 0.74 O MORFHOLOE After 93 2.1 87 1.8 3.8 0.77 O.E 3.7. 433 3.6 3.7 3. 74 O. 0.08 4.33 47 4. 4.93 4.87 0. 0,08 3.6 48 4.67 4.O 0.38 N=7 =7 =7 = VALUE Change 6.73 1. 1.6 1 „07 0.54 O6 133 1.04 0.41 O.13 1.8 41 0.6 0. 1. 0.13 O.13 0.2 0.46 O.6 0.2 -04 —1.3 -0.13 -O.26 -O. O.2 Fz00 AELE. Terce Sandy Subs Racky Centrals 7.144 66.67 1.7 7.6 a6 41.6 1.6 3.3 5.41 ear 19 Standard Deviation Sample Size andard MH-WHITNEY STATISTICAL EY COMTROL 7 SAMDY SUESTRATE CHOSEN =18 FOO ROCKY COLOR M=16 SANDV COLORED Sand ant . 0 76.19 76.1. S0 76.17 C71 70.48 71.4 76.19 7.14 17.6 78 77 61.11 18 266 ted O ISFLACEI 50 TRIAL. 1 VALUE ASSICN HOTOS O MISFLALED . 1 1 1 1 1 Figure legends Figure 1. Map of Speckled Sanddab collection sites in Hopkins Marine Life Refuge. Figure 2. Scale of pattern morphology. 1-most rocky, 5-most sandy. Figure 3. Speckled Sanddab pattern of irridophore spots. Circle indicates area sampled by eyespot histograms of gray values. Figure 4. Change in pattern of rocky fish acclimating to sand for 8 days. Figure 5. Change in pattern of sandy fish acclimating to rock for 8 days. Figure 6. Change in pattern of rocky fish acclimating to rock for 8 days. Figure 7. Change in pattern of sandy fish acclimating to sand for 8 days. Figure 8. Quantification of pattern changes of rocky and sandy fish, based on scale in Figure 2. (Error bars indicate +/- one standard error.) Figure 9. Substrate matching of rocky fish acclimated to sand for 12 days compared to sandy fish. Figure 10. Substrate matching of sandy fish acclimated to rock for 12 days compared to rocky fish. Figure 11. Substrate preference of rocky and sandy fish (4/- one standard error.) Figure 12. Histogram of gray scale values of rocky substrate. Figure 13. Histogram of gray scale values of sandy substrate. Figure 14. Histogram of gray scale values of rocky fish eyespot (see figure 3), O days and 8 days acclimation to sand. Figure 15. 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