Below is an extremely interesting paper written by Stephanie M.Sabbagh, a PhD student at Stony Brook University and long term friend of ReefCI.
About herself, Stephanie writes;
"I am very passionate about both teaching and research. I have always had a passion for the oceans, since I can remember. I have over 10 years of teaching experience, including academic, but also SCUBA diving, skiing and swimming. I hold a BSc. Biology from McGill University and finished my undergraduate degree during an exchange at the University of Queensland (Australia) in 2004 where I studied the sublethal effects of coral bleaching on Heron Island, Great Barrier Reef. I have worked in Belize as a coral reef biologist, lecturer at the University of Belize and working on a shark population study (2006-present). I completed my Master of Sciences in 2012 on how social factors challenge shark conservation in Belize. I am currently in my PhD at the School of Marine and Atmospheric Sciences, where I continue working with stakeholders in Central America and study shark populations."
Significance of colors and patterns of coral reef fishes: an overview
Context: colors, coral reefs and coral reef fishes
Coral reefs are very colorful ecosystems, probably the most colorful in the oceans, if not the world (Marshall 2000b). The first pioneers had much to say about their beautiful colors. In an expedition around the harbor of Amboyna, Indonesia, Wallace (1886) described: “the clearness of the water afforded me one of the most astonishing and beautiful sights I have ever beheld. The bottom was absolutely hidden by a continuous series of corals, sponges, actinic, and other marine productions of magnificent dimensions, varied forms, and brilliant colours. […] In and out among them, moved numbers of blue and red and yellow fishes, spotted and banded and striped in the most striking manner, while great orange or rosy transparent medusa floated along near surface.” Jacques Yves Cousteau (1971) described the wall of coral from his mask as “a living kaleidoscope of lilac flecks, splashes of gold, reddish streaks and yellows”.
Coral reef species display some of the most original and colorful patterns in the ocean. Coral reef fishes are no exception and most present bold colors and patterns. Some of the earlier scientists used a variety of adjectives to qualify the rich diversity of colors displayed. In his account of Hawaiian reefs, MacCaughey (1918) uses the adjective ‘brilliant’ and the word ‘brilliancy’ seven times, ‘bright’ and ‘brightly’ five times, ‘beautiful’ and ‘beautifully’ eight times, ‘gorgeous’ twice, to describe coral reefs and its inhabitants. His description of Hawaiian coral reef fishes is the following: “Gorgeously colored fishes, small and large, lurked in the shadowy reef pools, and evaded prolonged inspection. It is impossible to describe the profound impression produced by one’s first sight of the strange fascinating reef-world. […] Like the fish of many tropical waters, the Hawaiian species are famous for their brilliant coloration, fantastic patterns, and strange shapes. Many are grotesque; many are exceedingly beautiful; many are consummate embodiment of that riot of gorgeous color that is so characteristic of the reef and its life.” Cheney et al. (2013) refer to coral reefs as “one of the most spectrally diverse environments”. Fishes come second to birds in diversity of their “flamboyant colors or combinations of bright hues and elaborate patterns” (Kodric-Brown 1998). Chaetodontids, or butterflyfishes, are among the most conspicuous reef fishes (Ehrlich 1975; Ehrlich 1977). Similarly, Hiatt and Strasburg (1960) state that “the chaetodontids are brilliantly colored” and “like many coral reef fishes, butterflyfishes are spectacularly colored” (McMillan et al. 1999).
Not only are coral reefs some of the most diverse ecosystems, but the diversity of colors on the reef is just as important (Marshall 1998; Marshall et al. 2003b). This paper explores why some coral reef fishes are so colorful and puts their color behavior into ecological significance. It is odd that fish would be so colorful since as Marshall (1998) mentions, this would make them “an obvious meal”. Reef fish depend on corals for shelter from predators (Ehrlich 1975) so it begs the question as to why many would be so conspicuous. To start their paper, Mallet and Joron (1999) mention that “mimicry and warning colors are highly paradoxical adaptations”. Survival strategies and optics are both important to understand the meaning of color (Marshall 1998).
A brief overview on the importance of optics
An important clue to studying why coral reef fishes appear so ‘colorful’ lies in the fact that fish most likely see colors very differently than humans (Marshall et al. 2003c). Adjectives such as ‘bright’ and ‘colorful’ are not particularly useful in describing coral reef fishes as these are from a human perspective (Siebeck et al. 2007). However, there are ways to quantify fish coloration (Endler 1990). Studying animal color patterns are difficult because of the subjectivity in which we see and the observation of color needs to be made at the time of the display (Crook 1997). With innovative technology such as spot-reflectance spectoradiometer (Marshall 1998) and field spectrophotometry, it is possible to measure color and light objectively (Marshall 2000a).
The color perceived by a viewer depends on the viewer’s visual receptors, the physical attributes of the reflected light and the orientation of the colored structure (Booth 1990). It also depends on the “predator’s vision, hunting tactics, prey behavior, and background color patterns” (Endler 1978). Understanding the optics under water and the receptors of different species (for example, humans looking underwater, predators looking at prey, or species looking at each other) is important when attempting to understand the ecological significance of color in coral reef fishes; for example, humans have 3 color receptors (blue, green and red) while some reef fish have 4 or more color receptors (Marshall 1998). The way fish perceive colors is complex, depends on multiple factors (as mention; see Marshall et al. 2003c for further details and summary) and is dynamic, because it changes according to these factors. Marshall et al. (2003c) explain that fine scale measurements (microhabitat) are highly relevant in such studies for this reason.
Colors and position of fish on the reef have, at least in part, to do with absorption of light incident on the reef and with wavelength of colors. Labroids have some of the most complex colors seen in nature (Marshall 2000b). Many labrid (wrasse) and scarid (parrotfish) fishes are green, and are found in shallower parts of the reef, which happens to match the background color of the water there (Marshall et al. 2003c). This is also explained by the color (green) reflected from the abundance of chlorophyll (from coral’s zooxanthellae) found on the reef (Marshall 2000b). Many reef fish possess both blue and yellow colors, including species in the Chaetodontidae (butterflyfish), Labridae (wrasse), Acanthuridae (surgeonfish), Pomacanthidae (angelfish) and Pomacentridae (permicform fish) families (Marshall and Johnsen 2011); due to their wavelength and reflectance, they travel farthest in the water column and yellow is very conspicuous; they are also complementary and thus create a strong contrast explain Marshall (2000a) which could be used in disruptive patterning (Marshall and Johnsen 2011); he continues to explain that because human receptors and cones get excited by these colors, these appear attractive colors to us. Position in the water column and background have a lot of importance. For example, drummers blend in with the light in the water column when vertical, and thus camouflaged (Marshall 1998).
An overview of the meaning of colors in animals
Attempts at understanding the wide range of colors in reef fishes and whether they have a biological significance have long been debated and a source of controversy (Longley 1917; Ehrlich 1977; Warner 1984) for almost a century now (Ehrlich 1975; Marshall 2000a). Long before however, biologists were studying the meaning of color and patterns in terrestrial organisms. For reef fish, the issue is still unresolved (Marshall 2000b). Part of the debate involves whether colors and patterns are biologically- significant or not. In his review of Poulton’s meaning of colors in animals, Cope (1890) states that colors can be non-significant or significant, the latter being subdivided in “colors of direct physiological value, protective and aggressive resemblance, protective and aggressive mimicry, warning colors, and colors displayed in courtship”.
There are diverse reasons why coral reef fishes are so colorful. These include attracting mates, repelling predators, competing, communicating, finding partners (sexual or mutualistic). According to Endler (1978), color patterns have three functions: to thermoregulate, to communicate within the same species (e.g.: courtship, mating) and at the same time to escape or confuse visual predators. But it can also be for interspecific recognition, such as partners in a mutualistic relationship. Some color patterns are recognized by members of a mutualistic relationship. Whereas recognizing protagonists in a mutualist relationship is chemically-based for man, it is visual in vertebrates (Stummer et al. 2004). For species to communicate or to advertise their distastefulness, colors must be as conspicuous as possible against the background (Endler 1990). Color patterns are the result of various selective pressures such as predators, preys, competitors and potential mates and as a result can be more or less conspicuous, cryptic, but can be balanced by plastic pigment-based color patterns (Price et al. 2008). Patterns can be temporary or permanent (Kodric-Brown 1998). Color pattern changes can be fast and reversible (physiological color patterns) or slow and non-reversible (morphological or ontogenetic color patterns) (Crook 1997). Furthermore, many coral reef fish change in forms and colors throughout their development which complicates their study; they also display such sexual habits that leads them to be mistaken for different species (Ehrlich 1975). Bluehead wrasses, some of the most common fish in the Caribbean, have three phases in which they change in colors through their development, the third being only for males. The wide diversity of colors in reef fish is paralleled by a matching diversity of social behaviors, sexual life histories and functional hermaphrodism (Warner 1984).
To add to the complex nature behind color and function, Stevens and Merilaita (2011) explain that “similar pattern types […] may have entirely different functions in different animals and circumstances, ranging from camouflage to warning and sexual signals”. Gimenez-Casalduero et al. (1999) postulate that this might be a reason why fishes at two different Guam reefs responded differently to colors and chemically-deterred models. Randall and Randall (1960) distinguish between resemblance, where an animal imitates another that is of no interest to its enemy and in doing so is concealed, and mimicry, where an organism imitates one that is toxic to its enemies and in doing so displays conspicuous color, well-known and avoided by its enemies. These fishes are indeed more than just a pretty face.
Color can also be behavioral and signify the quality of a fish (to a predator for instance) or its motivation (to mate for example) (Price et al. 2008) because color pigmentation is controlled by the nervous system. Kodric-Brown (1998) explains that “unlike the colors of other vertebrates, the chromatophores of fishes are under neuroendocrine control, so that colors and patterns can be changed almost instantaneously”. Examples are covered later in the paper, in color changes associated with sex-changes (e.g.: parrotfishes)
The evolution of color and function in coral reef fishes is rather well-thought and very meticulous. It is probably simplistic to assume that colors and patterns observed are the product of one evolutionary pressure, but rather the intertwined habitat, behavior and sexuality of fishes probably acting at once (Marshall 2000a). In fact, these strategies are crucial for survival on the reef (Marshall 1998). There still remains a lot of unresolved explanations to the significance of color in coral reef fishes, as Ehrlich (1977) explains: “The function of color in most coral reef fishes is not well understood”.
In the rest of the paper, I will be presenting various examples of different types of color function and brief explanations on each. I present examples but only in the context in which they apply to ‘bright’ colors and patterns, and group them within the different categories that explain their ecological significance.
Camouflage, furtive behavior
The three-dimensional world in which fishes live along with their limits to visual range influence the camouflage strategies that they use (Marshall and Johnsen 2011). There is an important diversity of camouflage strategies (see Marshall et al. 2003b for background). Endler (1981) differentiates between crypsis, masquerade, Batesism, Mullerism, polymorphism and convergence. He first explains that mimicry is when a species resembles another, and crypsis, when a species resembles its background. Mimicry is one way to camouflage through resemblance to other fish (Marshall et al. 2003). Crypsis can be further subdivided into 8 categories: background matching, self-shadow concealment, obliterative shading, disruptive coloration, flicker-fusion camouflage, distractive markings, transparency and silvering (Stevens and Merilaita 2011). Disruptive camouflage is used along with a species’ complex background to distract and confuse predators so that they do not know where a fish begins or ends (Marshall 1998). Marshall (2000a) found for example that when approached, the royal angelfish, P. diacanthus, hides between coral branches, and when viewed from the side, the background and the fish’s color create a disruptive camouflage. Other furtive behavior strategies in many fishes have vertical stripes that help them blend in with urchins (Ehrlich 1975) as defense mechanism from predation. Direct background matching (Marshall et al. 2003b) is another strategy. Labriforms (e.g.: wrasses and parrotfishes) use complementary colors, more complex patterns than the simple monophasic ones that many reef fish use: blue and yellow (Marshall 2000a).
Intraspecific, intergenerational competition
In some benthic fish, color assists juveniles to settle on benthos, which is usually already occupied by adults and creates intraspecific competition. Fricke (1980) demonstrates that color difference in adult and juvenile emperor angelfish, Pomacanthus imperator, allows both generations of the same species to coexist.
Colors to advertise associations with dangerous animals
When chasing other pilotfish associated with the same or a different shark, Magnuson and Gooding (1971) noticed that pilotfishes’ black stripes faded, and that blue patches appeared on their dorsum. The more intense the chase (usually a larger pilotfish chasing a smaller one) towards another pilotfish, the more dramatic this transient pattern coloration change appeared to be. The authors explained that transient color appeared to be an “aggressive threat display in defense of the shark as a moving territory […] reducing intraspecific competition for the larger dominant pilotfish ”. The same might be true of the orange clownfish, Amphiprion percula, who might use its color as warning for the anemone and its tentacles (Mariscal 1996).
Aposematism, or aposematic display of coloration, are bold and indiscreet colors and behavior. Longley (1917) uses the word aposematic as a synonym for warning coloration and explains the function of color in this context as such. There are many examples on land and in the oceans of organisms that display aposematism. In terrestrial organism, yellows, oranges and reds often with black are used by prey to signal their unprofitability to predators (Endler and Mappes 2004). Such display of bright color signifies toxicity in some organisms and warns the predators not to attack. Hiatt and Strasburg (1960) describe the turkey fish for example as “strikingly-colored, bizarrely-shaped, scorpaenids whose sluggish habits and attractive appearance mask one of the most venomous of coral reef fishes in the Marshall Islands”. Similarly, nudibranch are bright colored (Ehrlich 1975) and soapfish have aposematic colors, or ‘warning’ so that they are not attacked by predators (Tachibana 1988).
Conspicuous display in reef fish however is not necessarily only associated with toxicity. So are there bright coral reef fishes that are not toxic and display aposematic coloration? Aposematism is an example of natural selection favoring visual signals that contrast with their backgrounds (Prudic et al. 2006). Batesian mimicry is an example in which some fish display conspicuous coloration but are not toxic. Rather, these fish evolve to mimic toxic fish to deter predators. These fish species are palatable but essentially display a conspicuous phenotype of unpalatable preys, e.g.: the unpalatable pufferfish Canthigaster valentini and his ‘imposter’ the leatherjacket Paraluteres prionurus (Caley and Schluter 2013). That is not to say that only aposematic-colored fish are displeasing to predators; some prey do not have warning colors, yet are defended (Endler and Mappes 2004).
Color as sexual behavior function: mating and scaring off competitors
Some species present different colors between males and females as well as different color phases as they mature sexually. Patterns of sex and coloration in parrotfish species are complex (Robertson and Warner 1978). In the stoplight parrotfish, color change is associated with hormonal changes and sex change from female to male (Cardwell and Liley 1991). Males tend to be the more-brightly colored, as is the case with parrotfishes, wrasses and blennies (Kodric-Brown 1998). Colors in sexual dimorphic species often have two functions: to attract mates and to intimidate others and result in intrasexual and intersexual selection. Robertson and Warner (1978) studied the sexual patterns in the Scaridae family of the Caribbean (parrotfishes) and noted two subfamilies: Scarinae and Sparisomatinae. For the Scarinae, they found that all females appear to change sex (accompanied by a change in color) if they live long enough; females first turn into a initial male phase and then into a terminal male phase, each with a change in coloration. For the Sparisomatinae, patterns are a lot more diverse, even within the same species they concluded.
Color pattern differences in butterflyfishes explain pairing between intraspecific male and female as well as aggression between some species of butterflyfishes studied (Chaetodon multicinctus - Pebbled butterflyfish) but not in others (such as C. punctatofasciatus – Spotband butterflyfish and C. pelewensis – Sunset buuterflyfish) (McMillan et al. 1999).
Changes in colors and patterns (non-sexual – covered previously)
Dynamic camouflage, whereby colors and patterns change, also falls within camouflage (Marshall et al. 2003b). Butterflyfishes that aggregate in the same coral pen at night are of similar colors (Ehrlich 1977); some adopt nocturnal color patterns, some having their stripes become darker, others having a white stripe appear, others again having a white blotch appear, thought to act as protection against predators, pattern changing back at dawn. Ehrlich (1977) suggests that butterflyfishes might recognize themselves among species by their color patterns.
Color reefs are some of the most diverse ecosystems on the planet, and their fish are equally diverse in colors, patterns, changing in some depending on their life stage, permanent in others, nonetheless all complex. This topic is an ongoing investigation and there is still a lot of research to be done. There can be overlap among the different function, or meaning of colors, such as mimicry, color sexual trait. Categories presented were arbitrarily chosen for the purpose of this paper to facilitate description of color function or meaning. In terms of optics, there is a lot more details involved, but for the purpose of this paper, it was not covered, as we wanted to keep the focus on ecological meaning. Nonetheless, this topic involves in great importance optics.
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