Perceived colors depend on the light absorption by skin pigments, light scattering, or by a combination of both (Shawkey et al., 2009; Cronin et al., 2014). The color of animals responds to selective pressures and mediates the relationship of an organism with the environment in different ways, functioning as social signaling, thermoregulation, UV-protection, mate attraction, intrasexual competition, and camouflage (Cuthill et al., 2017; Marshall, 2000).
The risk of death by predation is one of the main determinants of fitness (Carr, Hixon, 1995). Predation as a selective pressure affects body shape and behavior of organisms (Van Der Laan, Hogeweg, 1995), such as increased physical and chemical defenses by prey and reduced body sizes (Hammerschlag et al., 2018). In addition, prey may escape predation by going unnoticed by predators via camouflage: the set of strategies that reduce the chance of prey being detected or recognized by predators (Stevens, Merilaita, 2008).
Visual camouflage can be divided into several strategies, including background matching, silvery bodies, disruptive patterns, and motion-dazzle (Stevens, Merilaita, 2008). Background matching occurs when the color, brightness, or pattern of the individual resemble the properties of the environment, therefore decreasing the probability of detection by a predator (Merilaita et al., 1999). For fishes that live farther from the bottom and are highly mobile, a symmetrical cylindrical or fusiform silvery body in an underwater light field reflects a region of the water column that corresponds to what is behind the mirror (Ruxton et al., 2004; Johnsen, 2014), making it difficult to detect the animal. Thus, silvering is a case analogous to background matching with the fish matching by reflection the ocean behind it. Either via silvering or coloring, background matching has an implicit cost of restricting an individual to the set of substrates to which their coloration provides effective camouflage (Tyrie et al., 2015), at least if the animal has restricted ability to change colors, as most reef fishes.
An alternative to the dependence of the substrate that background matching demands would be disruptive coloration: a color pattern that makes it difficult to detect the animal by disguising its contour, such as the marine isopods Idotea balthica (Pallas, 1772) (Merilaita, 1998). Disruptive patterns obscure the shape of the animal, mixing it partially in the background, hindering the detection of the contour of its body (Cuthill et al., 2005). In addition to disruptive coloration, stripes may also reduce the risk of predation via motion-dazzle. The combination of high-contrast repetitive stripes makes estimates of speed and trajectory of prey less precise (Hogan et al., 2016; Negro et al., 2020). Similar to disruptive coloration, motion-dazzle may also allow animals to occupy a greater variety of habitats. For instance, striped individuals Hippocampus reidi Ginsburg, 1933 seahorses were found in a greater variety of micro-habitats than individuals with homogenous coloration (Duarte et al., 2019), and in Alpheus Fabricius, 1798 shrimps the evolution of a banded pattern was more frequent in microhabitat generalists than in microhabitat specialist species (Elias et al., 2019). Therefore, for demersal mobile fishes a disruptive or motion-dazzle strategy may be more effective than background matching. The mobility and the greater distance from the substratum may cause the individual to be viewed at a greater variety of habitats than benthic species. However, a motion-dazzle pattern should not be typical in benthic more sedentary fishes because the regularity of the bands may make the fish more detectable than a background matching or disruptive strategy (Stevens et al., 2011).
Reef fishes are vertebrates with the widest variety of known pigment cell types (Schartl et al., 2016), offering diverse color patterns, including dark or evident colors and a combination of stripes, spots, and bands (Salis et al., 2019). Their color patterns may vary according to sex, ecology, and stage of development (Cortesi et al., 2015). Reefs are heterogeneous habitats, full of predators (Mihalitsis, Bellwood, 2019) and are populated by a diversity of fish with different degrees of mobility, being a challenge for animals that camouflage themselves to avoid predation (Dorenbosch et al., 2009). Up to 53% of the reef species are piscivores of greater or lesser voracity (Mihalitsis, Bellwood, 2019). Predation is one of the factors related to mortality and biological limitations in reefs. The species Acanthochromis polyacanthus (Bleeker, 1855), for example, grow larger in environments where there is no predation (Connell, 1998). In another study, relief of predation pressure caused by shark fishing resulted in morphological changes in reef fishes, such as caudal fins shape and relatively smaller eyes (Hammerschlag et al., 2018). Those studies demonstrate the importance of predation in the ecomorphology of reef fishes. In addition, human impacts, such as mining in coral reefs and coral bleaching in response to climate change and the pH of seawater, can have a marked effect on the color of these environments and, consequently, on the survival of the species that inhabit coral reefs (Brown, 1997). This threatens one of the largest sources of biodiversity on the planet (Knowlton et al., 2010).
Thus, the present work investigates habitat use by reef fishes of different color patterns. We seek to understand how reef fishes with varying degrees of mobility and positions in the water column avoid being detected by predators to better comprehend the functioning of these rich environments. We hypothesized that the mobility and stratum of the water column influence the coloration. We predicted that sedentary animals that live close to the substrate take advantage of background matching or disruptive coloration, that more mobile demersal animals apply disruptive coloration or motion-dazzle, while highly mobile pelagic species tend to have silvery bodies.
Material and methods
Our study evaluated the coloration and habitat use of Brazilian reef fishes, both Actinopterygii and Chondrichthyes, with data available on Fishbase (Froese, Pauly, 2019). This is a recognized database among ichthyologists. It was developed by the International Center for Living Aquatic Resources Management (ICLARM) together with the Food and Agriculture Organization of the United Nations (FAO), with support from the Commission of the European Communities (CEC) (Froese, 1991). The data relating to the records of different fish families are curated by a group specialist, giving considerable accuracy to the information presented there. With the data found in FishBase, we collected the following information: scientific name, popular name of the species, family, geographical distribution, and position in the water column it occupies (adults in non-reproductive period).
From the photographs of the species present on the platform, we determined the following aspects of their coloration (Fig. 1): the presence of a moderately homogenous non-silvering color pattern without large contrasting patches (typical of background matching), a relatively homogenous silvery body (typical of silvering), presence of highly contrasting regular stripes (e.g., black and white stripes; typical of motion-dazzle strategy), and presence of contrasting contour breaks patches (typical of disruptive coloration). We also categorized the use of the water column stratum into benthic (species closely related to the bottom, remaining sheltered or propped on the substrate and with less mobility), pelagic (highly mobile species that live at half water or near the surface), and demersal (species that are functionally between benthic and pelagic, living associated to the substrate, but also with good mobility) (Friedman et al., 2020). The photographs were categorized visually by one of us (FMG). Some species may present more than one type of coloration. For instance, the presence of stripes as well as contrasting patches typical of disruptive coloration. In those cases, we classified fishes by the coloration type more readily distinguished.
FIGURE 1| Species exemplifying the color patterns used in this study. A. Large contrasting patterns typical of disruptive coloration in Hippocampus reidi (~ 13 cm of total length, TL); B. Silvery bodies in Haemulon aurolineatum Cuvier, 1830 (~ 18 cm TL); C. Contrasting stripes typical of motion-dazzle in Elacatinus figaro Sazima, Moura & Rosa, 1997(~ 3 cm TL); D. Homogeneous coloration in adult female Parablennius pilicornis (Cuvier, 1829) (~ 6 cm TL). Photographs by Gualter Pedrini.
We analyzed the data in a Bayesian multinomial multilevel model. We present statistical estimates as the mode and credible intervals. In Bayesian analysis the credible intervals are the probability that the true value lies within the interval. In a pairwise comparison, when the 95% credible interval does not cross zero, there is a probability of at least 95% that the difference between estimates is not zero. The color category entered as the response variable (four levels: homogenous non-silvering, contrasting non-striped patches, contrasting stripes, and homogenous silvering) and the position in the water column as the predictor variable (three levels: benthonic, demersal, and pelagic). We included the phylogenetic tree (phylogenetic distances) as a group-level factor (random effects) to model the phylogenetic dependence between fish species. We generated the phylogeny using data from the Open Tree of Life, with the rotl package (Michonneau et al., 2016) of the software R version 4.0.2 (R Development Core Team, 2020). The branch lengths were estimated using the Grafen method (Grafen, 1989) in ape package (Paradis, Schliep, 2019) R version 4.0.2 (R Development Core Team, 2020).
We ran the Bayesian models using the package brms (Bürkner, 2017), which implements Bayesian models in Stan (Bürkner, 2018) in R version 4.0.2 (R Development Core Team, 2020). We set the default weakly informative priors (Tab. S1). We ran four independent chains for 30,000 iterations; 15,000 was a warm-up, in a total of 60,000 sampled iterations. We evaluated model fit by checking chain convergence, the presence of transitions with diverging errors, and visual checks of posterior predictive values.
We analyzed a total of 100 reef fish species (Fig. 2). Thirty-five were classified as benthic, 35 as demersal, and 30 as pelagic. We observed 30 homogeneous species, 31 with contrasting irregular patches, 25 with a silvering coloration, and 14 with contrasting stripes. The data indicated that the benthic stratum is dominated by species with contrasting irregular patches, whereas the pelagic stratum is dominated by species with silvering coloration (Fig. 3). Striped colorations are predominantly found in demersal species (Fig. 3). Contrary to our hypothesis, the proportion of homogenous coloration is similar in benthic, demersal, and pelagic species (Fig. 3).
FIGURE 2| Phylogeny of the 100 species used in this study generated from data in the Open Tree of Life. Branch lengths represent phylogenetic distance and were estimated by the Grafen’s method. Color bars denote the water column use (blue shades) and coloration pattern (red shades) we attributed to them.
FIGURE 3| Coloration of reef fish species by their position in the water column (benthic, n = 35; demersal, n = 35; pelagic, n = 30). Homogeneous refers to the presence of a moderately homogenous non-silvering color pattern without large contrasting patches (typical of background matching); patches refer to the presence of contrasting contour breaks patches (typical of disruptive coloration); stripes refer to the presence of highly contrasting regular stripes (e.g., black and white stripes, typical of motion-dazzle strategy), and silvering to fishes with silvery homogenous body coloration.
Our statistical analysis partially confirmed these trends (Fig. 4; Tab. S2). There was a decrease in the proportion of contrasting patches for demersal and pelagic species in comparison to benthic species; and an increase in the proportion of silvering for pelagic species in comparison to benthic and demersal species (Fig. 4); The data also suggested an increase in the proportion of stripes for demersal species in comparison to benthic and pelagic species but uncertainty around statistical estimates did not confirm this pattern (Fig. 4). The analysis did not show any evident change in homogenous coloration between strata (Fig. 4).
FIGURE 4| Results of the Bayesian statistical analysis showing the difference in the proportion of coloration types between positions in the water column. Points denote the mode; thick and thin lines denote 67% and 95% credible intervals. Comparisons based on the expected values of the posterior predictive distribution. The analysis indicated that presence of contrasting contour breaks patches is more frequent in benthic than in demersal and pelagic species; and that silvering is more frequent in pelagic species than in demersal and benthic species.
Our results support the prediction that animals closely related to the reef bottom take advantage of contrasting irregular patches, while highly mobile pelagic species use to have silvering coloration. However, the statistical analysis did not confirm the predictions of a higher proportion of homogenous coloration in benthic species nor the higher proportion of stripes in demersal fishes.
We observed that fish species with contrasting non-regular patches, typical of disruptive coloration, were more present in the benthic stratum. Disruptive patterns are less background-dependent and may be more frequent in microhabitat generalist species. Nonetheless, disruptive coloration often blends with background matching, being more effective when it involves background-like spots along with disruptive patterns (Thayer, 1909; Poulton, 1940; Stobbe, Schaefer, 2008). When combined with low movement and proximity to the substrate, disruptive coloration and background matching may ensure protection against predators, and may also provide low detectability by prey, since there are many sit-and-wait benthic predators that camouflage efficiently against the substrate (e.g., soles Tyrie et al., 2015; Akkaynak et al., 2017; and groupers Watson et al., 2014).
Silvery species, such as Carax bartholomaei Cuvier, 1833, were more recurrent in the pelagic stratum. This result was already expected due to the non-availability of refuges and the habitat homogeneity in the pelagic stratum. Due to the refraction of light (Denton et al., 1972), in mean waters of the oceans and deep lakes, silvery fishes have the advantage of being less visible, which decreases the detection of possible visual predators. Moreover, silvery fishes present other strategies to pass unnoticed by predators (McFall-Ngai, 1990). The advantage of silvering does not remain when seen directly from above or from below. In these cases, a way to decrease detection is to be flattened laterally (Ruxton et al., 2004). Further, many pelagic species present countershading, another kind of background matching in which animals match their upper dark surface to the dark bottom of the sea, while they also match their light-colored lower surface to coincide with the solar lighting (Archer et al., 1999; e.g., Carcharhinus brachyurus (Günther, 1870)). Therefore, highly mobile pelagic fishes camouflage in such open and unprotected environment by confusing themselves with the ocean around them.
We observed striped coloration, typical of motion-dazzle, in mobile demersal and pelagic species, such as Brachygenys chrysargyrea (Günther, 1859) and Prognathodes guyanensis (Durand, 1960). This raw data agrees with our initial hypothesis that demersal animals apply motion-dazzle and disruptive coloration. The demersal stratum lies between the surface and bottom, so the fishes that inhabit this stratum are expected to be intermediate in swimming abilities and general coloration between pelagic and benthic fishes (Froese, Pauly, 2019). In addition to moving on several types of backgrounds, the distance demersal species maintain from the substrate causes predators at different depths to see demersal fishes against different backgrounds due to the parallax effect (Frost, 2010; Cuthill et al., 2019). Therefore, we expected disruptive coloration and motion-dazzle to be more advantageous than background matching in demersal species (Duarte et al., 2016). However, due to the large credible intervals of the estimates, our statistical analysis did not confirm the trend we found in the raw data (Figs. 2–3).
Contrary to our prediction, fishes with homogeneous coloration were present in the three strata with similar frequencies (Figs. 2–3). We expected homogeneous colored fishes to represent background matching species, but this category included more diverse coloring, such as a body coloration free of a clear pattern but with visible moderately contrasting spots (e.g., Emblemariopsis signifer (Ginsburg, 1942) and Coryphopterus dicrus Böhlke & Robins, 1960)and stripes (e.g., Acanthurus chirurgus (Bloch, 1787)), or species with striking countershading (e.g., Mobula spp., rays and Carcharhinus spp., Sharks), possibly obscuring a distribution pattern. Background matching depends on the substrate against which the animal stands. In this way the individual can go unnoticed in one or few habitats but be quite visible in others (Endler, 1984; Duarte et al., 2018), while it should also remain sedentary (Hall et al., 2013). A wider habitat use may be achieved by color change, such as in Bothus ocellatus (Agassiz, 1831) (Ramachandran et al., 1996). Furthermore, many species with homogeneous coloration are classified as nocturnal, such as batfish (Gibran, Castro, 1999), nurse sharks (Matis et al., 1974), Apogon spp. (Livingston, 1971), Lutjanus spp. and Haemulon spp. (Hitt et al., 2011). In reef there is a dramatic alternation of the diurnal fish fauna with the nocturnal fish fauna. Many of the nocturnal species spend the day in cavities in the reefs (Hobson, 1965), relying less on visual camouflage. Nevertheless, nocturnal fishes can be preyed on during the day or spotted by diurnal predators during turnover, in twilight periods (Hobson, 1979). That is why we included nocturnal species in our analysis.
Fishes with several color patterns, such as silvery, striped, spotted, or homogeneous coloration were present in the demersal stratum. This stratum is intermediate and usually has greater diversity since it receives elements from other strata around. This situation is parallel to the concept of ecotones, in which diversity is higher due to contributions from both the surrounding biomes (Risser, 1995).
The UV reflectance was not addressed in this study as we used photos from standard non-UV sensitivity cameras. However, some species may have UV reflective color patterns that may enhance or reduce the camouflage value for UV sensitive marine organisms (Losey et al., 1999; Marshall et al., 2015). Further, water column causes light polarization that can interfere with the camouflage of pelagic silvery fishes. Light polarization under water is usually at its maximum when looking horizontally through the water and silvering may interfere with this polarization pattern (Johnsen, 2012; Shashar et al., 2000). A predator with visual sensitivity for light polarization could use this cue to find prey (Shashar et al., 2000).
In our study, we categorized the images visually by a human observer. Consequently, we were limited by the human vision. Similarly, habitat categorizations and color patterns are relatively subjective, making room for divergence. Further, we restricted our analysis to Brazilian reef fishes, whose diversity is reasonably divergent from other reef ichthyofaunas (Araújo et al., 2020). Nonetheless, we believe our results should be reproducible in different geographic regions because Brazilian reef fish taxonomic diversity at the family level and functional diversity satisfactorily mirror reefs in other parts of the world (Floeter, Gasparini, 2000). Including species from other regions may increase the accuracy of the analysis.
Our study is the first to correlate reef fishes color and habitat use. A search on Web of Science on September 2021 for the terms “Fish color*” AND “Habitat use” in the topic returned 141 papers, but none specifically tested how fish color influence their water column use. In conclusion, we observed that reef fishes have color patterns that partially reflect the stratum they occupy in the water column. This is particularly clear for benthic and pelagic species, which presented predominantly disruptive patterns and silvering coloration, respectively. Therefore, this study shed light on factors that may affect color and habitat use by reef fishes. The place where a fish dwells may interact not only with its color pattern but also with how much it moves between different reef microhabitats and backgrounds.
The authors would like to thank Fernanda Silva for the critical reading and invaluable comments in a previous version of this text; and Gualter Pedrini for the beautiful images that compose Fig. 1. This study is also part of projects funded by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, process numbers: 408576/2018–9 and 428141/2016–1) and Fundação de Apoio à Pesquisa do Distrito Federal (FAP/DF, process numbers: 24052018 and 00193–00002164/2018–5).
Akkaynak D, Siemann LA, Barbosa A, Mäthger LM. Changeable camouflage: How well can flounder resemble the colour and spatial scale of substrates in their natural habitats? R Soc Open Sci. 2017; 4(3):160824. https://doi.org/10.1098/rsos.160824
Araújo ME, Mattos FMG, Melo FPL, Chaves LCT, Feitosa CV, Lippi DL et al. Diversity patterns of reef fish along the Brazilian tropical coast. Mar Environ Res. 2020; 160:105038. https://doi.org/10.1016/j.marenvres.2020.105038
Archer SN, Djamgoz MBA, Loew ER, Partridge JC, Vallerga S, editors. Adaptative mechanisms in the ecology of vision. Springer Science & Business Media. 1999. https://doi.org/10.1007/978-94-017-0619-3
Brown BE. Coral bleaching: Causes and consequences. Coral Reefs. 1997; 16(1):S129–38. https://doi.org/10.1007/s003380050249
Bürkner PC. brms: An R package for Bayesian multilevel models using Stan. J Stat Softw. 2017; 80(1):01–28. https://doi.org/10.18637/jss.v080.i01
Bürkner PC. Advanced Bayesian multilevel modeling with the R package brms. R J. 2018; 10(1):395–411. https://doi.org/10.32614/rj-2018-017
Carr MH, Hixon MA. Predation effects on early post-settlement survivorship of coral-reef fishes. Mar Ecol Prog Ser. 1995; 124:31–42. https://doi.org/10.3354/meps124031
Connell SD. Effects of predators on growth, mortality and abundance of a juvenile reef-fish: Evidence from manipulations of predator and prey abundance. Mar Ecol Prog Ser. 1998; 169:251–61. https://doi.org/10.3354/meps169251
Cortesi F, Feeney WE, Ferrari MCO, Waldie PA, Phillips GAC, McClure EC et al. Phenotypic plasticity confers multiple fitness benefits to a mimic. Curr Biol. 2015; 25(7):949–54. https://doi.org/10.1016/j.cub.2015.02.013
Cronin TW, Johnsen S, Marshall NJ, Warrant EJ. Visual ecology. Princeton University Press; 2014.
Cuthill IC, Allen WL, Arbuckle K, Caspers B, Chaplin G, Hauber ME et al. The biology of color. Science. 2017; 357(6350):eaan0221. https://doi.org/10.1126/science.aan0221
Cuthill IC, Matchette SR, Scott-Samuel NE. Camouflage in a dynamic world. Curr Opin Behav Sci. 2019; 30:109–15. https://doi.org/10.1016/j.cobeha.2019.07.007
Cuthill IC, Stevens M, Sheppard J, Haddocks T, Párraga CA, Troscianko TS. Disruptive coloration and background pattern matching. Nature. 2005; 434(7029):72–74. https://doi.org/10.1038/nature03312
Denton EJ, Gilpin-Brown JB, Wright PG. The angular distribution of the light produced by some mesopelagic fish in relation to their camouflage. Proc R Soc Lond B Biol Sci. 1972; 182(1067):145–58. https://doi.org/10.1098/rspb.1972.0071
Dorenbosch M, Grol MGG, de Groene A, van der Velde G, Nagelkerken I. Piscivore assemblages and predation pressure affect relative safety of some back-reef habitats for juvenile fish in a Caribbean bay. Mar Ecol Prog Ser. 2009; 379:181–96. https://doi.org/10.3354/meps07896
Duarte M, Gawryszewski FM, Ramineli S, Bessa E. Disruptive coloration and habitat use by seahorses. Neotrop Ichthyol. 2019; 17(4):e190064. https://doi.org/10.1590/1982-0224-20190064
Duarte RC, Stevens M, Flores AAV. Shape, colour plasticity, and habitat use indicate morph-specific camouflage strategies in a marine shrimp. BMC Evol Biol. 2016; 16(1):218. https://doi.org/10.1186/s12862-016-0796-8
Duarte RC, Stevens M, Flores AAV. The adaptive value of camouflage and colour change in a polymorphic prawn. Sci Rep. 2018; 8(1):16028. https://doi.org/10.1038/s41598-018-34470-z
Elias MAM, Anker A, Gawryszewski FM. Microhabitat use and body size drive the evolution of colour patterns in snapping shrimps (Decapoda: Alpheidae: Alpheus). Biol J Linn Soc Lond. 2019; 128(4):806–16. https://doi.org/10.1093/biolinnean/blz152
Endler JA. Progressive background in moths, and a quantitative measure of crypsis. Biol J Linn Soc Lond. 1984; 22(3):187–231. https://doi.org/10.1111/j.1095-8312.1984.tb01677.x
Floeter SR, Gasparini JL. The southwestern Atlantic reef fish fauna: Composition and zoogeographic patterns. J Fish Biol. 2000; 56(5):1099–14. https://doi.org/10.1006/jfbi.2000.1231
Friedman ST, Price SA, Corn KA, Larouche O, Martinez CM, Wainwright PC. Body shape diversification along the benthic–pelagic axis in marine fishes. Proc R Soc Lond B Biol Sci. 2020; 287(1931):20201053. https://doi.org/10.1098/rspb.2020.1053
Froese R. Progress report on FISHBASE the global biological database on living aquatic resources. ICLARM Contribution No. 757. ICES C.M.; 1991.
Froese R, Pauly D, editors. FishBase [Internet]. 2019. Available from: https://www.fishbase.org
Frost BJ. A taxonomy of different forms of visual motion detection and their underlying neural mechanisms. Brain Behav Evol. 2010; 75(3):218–35. https://doi.org/10.1159/000314284
Gibran FZ, Castro RMC. Activity, feeding behaviour and diet of Ogcocephalus vespertilio in southern west Atlantic. J Fish Biol. 1999; 55(3):588–95. https://doi.org/10.1111/j.1095-8649.1999.tb00701.x
Grafen A. The phylogenetic regression. Philos Trans R Soc Lond B Biol Sci. 1989; 326(1233):119–57. https://doi.org/10.1098/rstb.1989.0106
Hall JR, Cuthill IC, Baddeley R, Shohet AJ, Scott-Samuel NE. Camouflage, detection and identification of moving targets. Proc R Soc Lond B Biol Sci. 2013; 280(1758):20130064. https://doi.org/10.1098/rspb.2013.0064
Hammerschlag N, Barley SC, Irschick DJ, Meeuwig JJ, Nelson ER, Meekan MG. Predator declines and morphological changes in prey: Evidence from coral reefs depleted of sharks. Mar Ecol Prog Ser. 2018; 586:127–39. https://doi.org/https://doi.org/10.3354/meps12426
Hitt S, Pittman SJ, Brown KA. Tracking and mapping sun-synchronous migrations and diel space use patterns of Haemulon sciurus and Lutjanus apodus in the U.S. Virgin Islands. Environ Biol Fishes. 2011; 92(4):525–38. https://doi.org/10.1007/s10641-011-9875-2
Hobson ES. Diurnal-nocturnal acrivity of some inshore fishes in the Gulf of California. Copeia. 1965(3):291–302. https://doi.org/10.2307/1440790
Hobson ES. Interactions between piscivorous fishes and their prey. In: Clepper H, editor. Predator-prey systems in fisheries management. Washington (DC): Sport Fishing Institute; 1979. p.231–42.
Hogan BG, Cuthill IC, Scott-Samuel NE. Dazzle camouflage, target tracking, and the confusion effect. Behav Ecol. 2016; 27(5):1547–51. https://doi.org/10.1093/beheco/arw081
Johnsen S. The optics of life: A biologist’s guide to light in nature. Princeton: Princeton University Press; 2012.
Johnsen S. Hide and seek in the open sea: Pelagic camouflage and visual countermeasures. Ann Rev Mar Sci. 2014; 6:369–92. https://doi.org/10.1146/annurev-marine-010213-135018
Knowlton N, Brainard RE, Fisher R, Moews M, Plaisance L, Caley MJ. Coral reef biodiversity. In: McIntyre AD, editor. Life in the World’s oceans: Diversity, distribuition, and abundance. Blackwell Publishing Ltd.; 2010. p.65–78. https://doi.org/10.1002/9781444325508.ch4
Livingston RJ. Circadian rhythms in the respiration of eight species of cardinal fishes (Pisces: Apogonidae): Comparative analysis and adaptive significance. Mar Biol. 1971; 9(3):253–66. https://doi.org/https://doi.org/10.1007/BF00351388
Losey GS, Cronin TW, Goldsmith TH, Hyde D, Marshall NJ, McFarland WN. The UV visual world of fishes: A review. J Fish Biol. 1999; 54(5):921–43. https://doi.org/10.1006/jfbi.1998.0919
Marshall NJ. Communication and camouflage with the same ‘bright’ colours in reef fishes. Philos Trans R Soc Lond B Biol Sci. 2000; 355(1401):1243–48. https://doi.org/10.1098/rstb.2000.0676
Marshall J, Carleton KL, Cronin T. Colour vision in marine organisms. Curr Opin Neurobiol. 2015; 34:86–94. https://doi.org/10.1016/j.conb.2015.02.002
Matis J, Kleerekoper H, Childers D. Cycles in animals: On forecasting the locomotor behavior of the nurse shark, Ginglymostoma cirratum. J Interdiscipl Cycle Res. 1974; 5(3–4):259–66. https://doi.org/10.1080/09291017409359434
McFall-Ngai MJ. Crypsis in the pelagic environment. Am Zoologi. 1990; 30(1):175–88. https://doi.org/10.1093/icb/30.1.175
Merilaita S. Crypsis through disruptive coloration in an isopod. Philos Trans R Soc Lond B Biol Sci. 1998; 265(1401):1059–64. https://doi.org/10.1098/rspb.1998.0399
Merilaita S, Tuomi J, Jormalainen V. Optimization of cryptic coloration in heterogenous habitats. Biol J Linn Soc Lond. 1999; 67(2):151–61. https://doi.org/10.1006/bijl.1998.0298
Michonneau F, Brown JW, Winter DJ. rotl: An R package to interact with the Open Tree of Life data. Methods Ecol Evol. 2016; 7(12):1476–81. https://doi.org/10.1111/2041-210X.12593
Mihalitsis M, Bellwood DR. Morphological and functional diversity of piscivorous fishes on coral reefs. Coral Reefs. 2019; 38(5):945–54. https://doi.org/10.1007/s00338-019-01820-w
Negro JJ, Doña J, Blázquez MC, Rodríguez A, Herbert-Read JE, Brooke ML. Contrasting stripes are a widespread feature of group living in birds, mammals and fishes. Proc R Soc Lond B Biol Sci. 2020; 287(1936):20202021. https://doi.org/10.1098/rspb.2020.2021
Paradis E, Schliep K. ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics. 2019; 35(3):526–28. https://doi.org/10.1093/bioinformatics/bty633
Poulton EB. Adaptive coloration in animals. Nature. 1940; 146(3692):144–45. https://doi.org/10.1038/146144a0
R Development Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2020.
Ramachandran VD, Tyler CW, Gregory RL, Rogers-Ramachandran D, Duensing D, Pillsbury C et al. Rapid adaptive camouflage in tropical flounders. Nature. 1996; 379 (6568):815–18. https://doi.org/https://doi.org/10.1038/379815a0
Risser PG. The status of the science examining Ecotones: A dynamic aspect of landscape is the area of steep gradients between more homogeneous vegetation associations. Bioscience. 1995; 45(5):318–25. https://doi.org/10.2307/1312492
Ruxton GD, Sherratt TN, Speed MP. Avoiding attack: The evolutionary ecology of crypsis, warning signals e mimicry. New York: Oxford University Press; 2004. https://doi.org/10.1093/acprof:oso/9780198528609.001.0001
Salis P, Lorin T, Laudet V, Frédérich B. Magic traits in magic fish: Understanding color pattern evolution using reef fish. Trends Genet. 2019; 35(4):265–78. https://doi.org/10.1016/j.tig.2019.01.006
Schartl M, Larue L, Goda M, Bosenberg MW, Hashimoto H, Kelsh RN. What is a vertebrate pigment cell? Pigment Cell Melanoma Res. 2016; 29(1):8–14. https://doi.org/10.1111/pcmr.12409
Shashar N, Hagan R, Boal JG, Hanlon RT. Cuttlefish use polarization sensitivity in predation on silvery fish. Vision Res. 2000; 40(1):71–75. https://doi.org/10.1016/S0042-6989(99)00158-3
Shawkey MD, Morehouse NI, Vukusic P. A protean palette: Colour materials and mixing in birds and butterflies. J R Soc Interface. 2009; 6(Suppl. 2):S221–31. https://doi.org/10.1098/rsif.2008.0459.focus
Stevens M, Merilaita S. Animal camouflage: Current issues and new perspectives. Philos Trans R Soc Lond B Biol Sci. 2008; 364(1516):423–27. https://doi.org/https://doi.org/10.1098/rstb.2008.0217
Stevens M, Searle WTL, Seymour JE, Marshall KLA, Ruxton GD. Motion dazzle and camouflage as distinct anti-predator defenses. BMC Biol. 2011; 9(1):81. https://doi.org/10.1186/1741-7007-9-81
Stobbe N, Schaefer HM. Enhancement of chromatic contrast increases predation risk for striped butterflies. Proc R Soc Lond B Biol Sci. 2008; 275(1642):1535–41. https://doi.org/10.1098/rspb.2008.0209
Thayer GH. Concealing-coloration in the Animal Kingdom: An exposition of the laws of disguise through color and pattern: Being a summary of Abbott H. Thayer’s Discoveries. New York: The Macmillan Co.; 1909.
Tyrie EK, Hanlon RT, Siemann LA, Uyarra MC. Coral reef flounders, Bothus lunatus, choose substrates on which they can achieve camouflage with their limited body pattern repertoire. Biol J Linn Soc. 2015; 114(3):629–38. https://doi.org/10.1111/bij.12442
Van Der Laan JD, Hogeweg P. Predator–prey coevolution: Interactions across different timescales. Proc R Soc Lond B Biol Sci. 1995; 259(1354):35–42. https://doi.org/10.1098/rspb.1995.0006
Watson AC, Siemann LA, Hanlon RT. Dynamic camouflage by Nassau groupers Epinephelus striatus on a Caribbean coral reef. J Fish Biol. 2014; 85(5):1634–49. https://doi.org/10.1111/jfb.12519
 Programa de Pós-graduação em Ecologia, Universidade de Brasília, Campus Universitário Darcy Ribeiro, Asa Norte 70910-000 Brasília, DF, Brazil. (LEFA) firstname.lastname@example.org, (EB) email@example.com (corresponding author).
 Ciências da Vida e da Terra, Faculdade de Planaltina, Universidade de Brasília, Área Universitária 1, Bairro Nossa Senhora de Fátima, Planaltina, 73345-010 Brasília, DF, Brazil.
Luísa Eduarda Fernandes dos Anjos: Conceptualization, Data curation, Investigation, Methodology, Writing-original draft, Writing-review and editing.
Felipe M. Gawryszewski: Conceptualization, Formal analysis, Funding acquisition, Methodology, Resources, Writing-original draft, Writing-review and editing.
Eduardo Bessa: Conceptualization, Funding acquisition, Funding acquisition, Investigation, Methodology, Resources, Supervision, Writing-original draft, Writing-review and editing.
The authors declare no competing interests.
How to cite this article
Anjos LEF, Gawryszewski FM, Bessa E. Water column use by reef fishes of different color patterns. Neotrop Ichthyol. 2022; 20(1):e210101. https://doi.org/10.1590/1982-0224-2021-0101
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Accepted November 21, 2021 by Fernando Gibran
Submitted June 8, 2021
Epub March 28, 2022