Testing for Camouflage of the Brazilian Seahorse Hippocampus Reidi (Syngnathidae) Using the Territorial Damselfish Stegastes Fuscus (Cuvier) (Pomacentridae)

aqua, International Journal of Ichthyology

Testing for camouflage of the Brazilian seahorse Hippocampus reidi (Syngnathidae) using the territorial damselfish Stegastes fuscus (Cuvier) (Pomacentridae)

Leonardo de Oliveira Armesto1 and Natalie Villar Freret-Meurer2*

1) Gama Filho, Departamento de Biologia, Rua Manuel Vitorino, 553 – Piedade, Rio de Janeiro, Brasil – CEP: 20748-900. 2) Universidade do Estado do Rio de Janeiro, Instituto de Biologia Roberto Alcântara Gomes, Avenida São Francisco Xavier, 524 – Maracanã, Rio de Janeiro, RJ, Brasil – CEP: 20550-013. *Corresponding Author: [email protected]

Received: 09 December 2010 – Accepted: 20 August 2011

Abstract einen und Größe, Geschlecht und Farbe von Seepferdchen Seahorses present many characteristics such as variable und Haltesubstrat auf der anderen Seite gab es keine Korre- colour, skin fronds and sedentary behaviour that provide lation. Die Seepferdchen, die sich während des Experiments camouflage as a defense mechanism. This study aims to ruhig verhielten (84%), wurden nicht angegriffen; alle, die test seahorse camouflage effectiveness in relation to a terri- sich bewegten, wurden angegriffen (16%). Nach den Ergeb- torial species. Seahorses were translocated into the territory nissen dieser Studie sind weder Farbe noch Größe die of the damselfish Stegastes fuscus (Cuvier) and its aggressive entscheidenden Merkmale für den Tarnungserfolg, sondern behaviour was recorded. Stegastes fuscus was chosen as es sind alle Faktoren zusammen, nicht zuletzt das Verhalten, being a good model of an aggressive fish, probably able to die die Überlebensrate verbessern. detect any transgressor. Seahorse size, sex, colour and mobility were recorded, as was the colour of the substrate Résumé used as holdfast. Eighty-four percent of the translocated Les hippocampes offrent une série de caractéristiques seahorses were not attacked. There was no relation comme la variabilité de la couleur, les excroissances feuil- between number of attacks and size, sex or colour of sea- lues et le comportement sédentaire qui constituent un horse and its holdfast. Seahorses that remained still during mécanisme de défense sous forme da camouflage. Cette the experiment (84%) were not attacked, but those that étude a pour objectif de tester l’efficacité du camouflage moved were attacked (16%). It was observed in this study des hippocampes en présence d’une espèce territoriale. Des that neither seahorse color nor size were relevant characters hippocampes on été délocalisés dans le territoire de Ste- in camouflage fitness, but probably all these together, gastes fuscus (Cuvier) dont le comportement agressif a été including behavior, improved survival fitness. observé. Stegaster fuscus a été choisi pour ses caractéris- tiques de poisson agressif, sans doute capable de détecter Zusammenfassung n’importe quel transgresseur. Taille, sexe, couleur et mobi - Eine Reihe von Merkmalen der Seepferdchen dienen der lité de l’hippocampe ont été notés, tout comme la couleur Tarnung als Verteidigungsmaßnahme, so die variable Fär- du substrat servant d’ancrage. Quatre-vingt-quatre pour bung, Hautanhänge und sesshaftes Verhalten. In dieser cent des hippocampes délocalisés n’étaient pas attaqués. Il Studie sollte die Wirksamkeit der Tarnung gegenüber einer n’y avait pas de relation entre le nombre d’agressions et la Revier bildenden Art untersucht werden. Exemplare von taille, le sexe et la couleur de l’hippocampe ou de son Seepferdchen wurden in das Revier von Vertretern der Riff- ancrage. Les hippocampes qui n’ont pas bougé durant l’ex- barsch-Art Stegastes fuscus (Cuvier) versetzt, deren périence (84%) n’ont pas été attaqués, mais ceux qui ont Angriffsverhalten wurde aufgezeichnet. Stegastes fuscus bougé ont été attaqués (16%). Cette étude a permis d’ob- wurde als günstiges Modell für einen aggressiven Fisch aus- server que ni la couleur ni la taille de l’hippocampe n’ont gewählt, weil die Wahrscheinlichkeit einer Reaktion beson- joué un rôle important dans l’efficacité du camouflage, ders hoch ist. Größe, Geschlecht, Farbe und Bewegungsver- mais il est probable que tous ces facteurs, y compris le halten der Seepferdchen wurden aufgezeichnet, außerdem comportement, améliorent ladite efficacité pour la survie. die Farbe des Substrats, das zum Festhalten diente. 84 Prozent der räumlich versetzten Seepferdchen wurden gar Sommario nicht angegriffen. Zwischen der Zahl der Angriffe auf der I cavallucci marini presentano molte caratteristiche come

165 aqua vol. 18 no. 3 - 15 July 2012 Testing for camouflage of the Brazilian seahorse Hippocampus reidi (Syngnathidae) using the territorial damselfish Stegastes fuscus (Cuvier) (Pomacentridae) colore variabile, fronde della pelle e comportamento habitats is one of the main reasons for such diver- sedentario che forniscono camuffamento come meccan- sity (Sale 1980). This huge diversity improves eco- ismo di difesa. Questo studio mira a testare l'efficacia logical interactions among species, favoring evolu- mimetica del cavalluccio marino in presenza di una specie tion of defense and attack mechanisms (Williams territoriale. I cavallucci marini sono stati trasferiti nel ter- ritorio della castagnola Stegastes fuscus (Cuvier) registran- 1991). done il comportamento aggressivo. Stegastes fuscus è stato Camouflage is a primary defense mechanism scelto poiché è noto essere un buon modello di pesce developed by many species, which allows them to aggressivo, probabilmente in grado di rilevare qualsiasi look like their environment, thereby avoiding intruso. Dimensioni, sesso, colore e mobilità del cavalluc- detection by predators (Merilaita et al. 1999) and cio sono stati registrati, così come il colore del substrato prey (Shine et al. 1998). Camouflage may be utilizzato come sostegno. L’ottantaquattro per cento dei exhibited by a change in body shape and color, and cavallucci marini traslocati non era stato attaccato. Non is more efficient in homogeneous environments c'era alcuna relazione tra il numero di attacchi e le dimensioni, il sesso o il colore del cavalluccio marino o del suo because it increases the degree of crypsis of the ani- sostegno. I cavallucci marini rimasti fermi durante l'esper- mal. Heterogeneous environments, such as coral imento (84%) non sono stati attaccati, ma lo sono stati and rocky reefs, tend to decrease the effectiveness quelli che si muovevano (16%). In questo studio è stato of camouflage due to the presence of numerous osservato che né il colore né le dimensioni erano di per sé microhabitats. However, crypsis might increase caratteristiche rilevanti nel comportamento mimetico, ma with the capacity to change color and low degree of probabilmente sono tutti questi aspetti insieme, compreso displacement (Merilaita et al. 1999). il comportamento, che contribuiscono a salvaguardare la Seahorses present camouflage as predator avoid- sopravvivenza della specie. ance and also as hunting strategy. They are teleost fish that belong to the family Syngnathidae, placed INTRODUCTION in a single genus Hippocampus Rafinesque (Nelson Among all marine ecosystems, coral reefs present 1994; Lourie et al. 1999). Seahorses occur in many the highest diversity of species. They shelter different habitats such as mangroves, seagrasses, around 25% of all marine fishes known to scien- coral and rocky reefs. They present many adapta- tists (Spalding et al. 2001). The great mosaic of tions to benthic life, such as vertical body posture,

Fig. 1. Hippocampus reidi in its natural habitat. Photo by N. V. Freret-Meurer. aqua vol. 18 no. 3 - 15 July 2012 166 Leonardo de Oliveira Armesto and Natalie Villar Freret-Meurer a prehensile tail and highly sedentary behavior divers, but it is not known if their predators have (Schmid & Senn 2002). Besides these adaptations, difficulty in finding them. The aim of this study is they are also capable of changing color, from a dis- to test the crypsis effectiveness of the Brazilian sea- creet base color like black and brown to strong col- horse H. reidi in its natural environment, using an ors like yellow, orange and red (Foster & Vincent aggressive territorial fish species to assess possible 2004) and to develop skin filaments (Lourie et al. differences on crypsis effectiveness between size 1999), allowing the animal to hide itself. All of and mobility and checking if similarity between these adaptations improve fitness in prey capture animal color and substrate color interferes with the and predator defense. It is possible that the ability attack behavior of the territorial fish. As there are to change color and morphology, and similarity to no reported predators of seahorses in Brazil, we its holdfast, may increase crypsis effectiveness. chose an aggressive species as a proxy for this study. Hippocampus reidi (Ginsburg) is the most abundant seahorse species along the Brazilian coast, being MATERIAL AND METHODS frequently observed in rocky reefs and mangroves Study sites: This study was conducted in Arraial (Fig. 1). They usually use sponges, seaweeds, man- do Cabo, Rio de Janeiro State, Brazil. A pilot study grove plant roots and artificial substrates as holdfasts. was undertaken to survey sites with the highest The species is characterized by a long thick snout, densities of seahorses. Six sites were chosen accord- narrow body and the absence of skin filaments in ingly (Fig. 2): 1) Saco do Cardeiro; 2) Ilha de Por- general. The color pattern consists of brown dots, cos – Ponta Sul; 3) Ilha de Porcos – Saltador; many small white dots around the body and stripes 4) Ilha de Cabo Frio – Abobrinha; 5) Ilha de Cabo in the dorsal region (Lourie et al. 1999). This species Frio – Anequin; 6) Forno – Ponta D’água, which is considered “Data Deficient” on the Red List of are part of the Extrativist Marine Reserve of Arra- Threatened Species of the International Union for ial do Cabo (RESEX-MAR). The RESEX-MAR Conservation of Nature – IUCN (IUCN 2006) and controls fisheries, promoting the sustainable use of “Vulnerable” on the List of Threatened Species of natural resources (Lages 2003). Rio de Janeiro State (Mazzoni et al. 2000). Experimental design: This study was carried out Finding seahorses is usually difficult for human at six sites selected according to the presence of

Fig. 2. Study sites in Arraial do Cabo, RJ: 1) Saco do Cardeiro; 2) Ilha de Porcos – Ponta Sul; 3) Ilha de Porcos – Saltador; 4) Ilha de Cabo Frio – Abobrinha; 5) Ilha de Cabo Frio – Anequin; 6) Forno – Ponta D’água.

167 aqua vol. 18 no. 3 - 15 July 2012 Testing for camouflage of the Brazilian seahorse Hippocampus reidi (Syngnathidae) using the territorial damselfish Stegastes fuscus (Cuvier) (Pomacentridae)

H. reidi. The camouflage effectiveness of the sea- experiment were recorded. It is important to high- horse was tested by experiments in situ, with light that no seahorse received any injuries during SCUBA diving equipment. The damselfish Ste- the experiments. gastes fuscus (Cuvier) was used to test the crypsis Control treatment: Aggressive behavior of addi- effectiveness of the seahorse. That species was cho- tional specimens of S. fuscus was also observed in a sen because it was considered a good model for nearby territory without any seahorse within. This detection of other invasive species, especially due was tested to verify the effect of catch and release in to its extremely aggressive and territorial behavior, this environment. The same experimental proce- attacking all fish species which enter its territory dure was used but without the seahorse introduc- (Ferreira et al. 1998; Menegatti et al. 2003). The tion. The number of attacks on other fish species use of an aggressive model efficient in detecting was recorded during a period of 5 minutes intruders is a new method developed specially to (Menegatti et al. 2003) to ensure that damselfish assess the effectiveness of avoiding detection. still presented the same aggressive behaviour. A Identification of Stegastes fuscus territory: The total of 76 experiments were conducted, of which territory occupied by Stegastes fuscus was identified 38 were with seahorse translocations and 38 with in all experiments for each individual. The most controls. frequent area in which the damselfish occurred was Assessment of color and biometry: After the characterized as the nuclear site of the territory and experiment, individuals were measured by height it was used in the experiment. These sites were (HT) according to Lourie (2003), which is repre- established by noting specific characteristics of the sented by the distance between the coronet and the benthic cover (eg. sponge, seaweed) in which the straightened prehensile tail. Seahorse color and its damselfish patrolled and exhibited frequent agonis- holdfast color were also recorded. Similarity tic behavior by attacking other fishes. Limits of the between seahorse and holdfast color was verified by nuclear site of the territory were observed for five a waterproof table containing a color pattern scale minutes. The same territory was only used once in of colors found in available holdfasts and seahorses the study to avoid pseudoreplication. Dives were made specifically for this study. Similarity between made at a distance from each other to prevent sam- seahorse and holdfast was only considered when pling the same territory. the base color of the seahorse was the same as the Experiment of camouflage effectiveness: After holdfast. Dissimilarity was considered when the identification of the S. fuscus territory, each speci- base color of the seahorse was different from the men was collected with a hand net and removed holdfast color. No gradient of similarity was con- from its territory. Afterwards, a specimen of sea- sidered. All experiments were conducted with dif- horse, which had been previously captured and ferent individuals. Seahorses were visually identi- maintained in another hand net, was translocated fied by schematizing and photographing their inside the now-vacated S. fuscus territory. Seahorses coronets according to Freret-Meurer and Andreata were held only a few minutes in the net to avoid (2008) to avoid possible pseudoreplication (Hul- major stress. Distance between the original site of bert 1984). Females were identified by absence of a the seahorse and translocation was about 5 meters. brood pouch and males, by its presence (Lourie et After the seahorse selected the holdfast inside the al. 1999). territory, the damselfish was reintroduced. The Statistical analyses: The number of attacks on holdfast was chosen by the seahorse. In general, individuals similar and dissimilar to the holdfast sponges were used as holdfast as they are the most and the difference between the size of male and abundant substrate at the area. Aggressive behavior female were compared by the Mann-Whitney test, was observed in S. fuscus in relation to the seahorse because data did not follow homoscedasticity. for five minutes (Menegatti et al. 2003) using the Relation between effectiveness and individual size animal focal method (Lehner 1979). The observa- was tested by linear regression (Zar 1999). Mean tion distance was 1.2 m. That distance was selected values were expressed by mean ± standard devia- so as to not interfere with damselfish behavior. tion. This was previously tested with several damselfish before the experiment. The number of attacks on RESULTS the seahorse was quantified and presence or Seahorse translocation experiments showed that absence of attacks on other species during the 15.7% (n = 6) were attacked by S. fuscus and aqua vol. 18 no. 3 - 15 July 2012 168 Leonardo de Oliveira Armesto and Natalie Villar Freret-Meurer

84.3% (n = 32) were not attacked. In the control adapted to several types of environment. In that group all observed S. fuscus (n = 38) attacked other way the species might conceal itself along many fish species, as well as in the treatment group. types of habitat without being detected, optimizing There was no significant difference between its color. The rocky reef is a very heterogeneous attacks on seahorses that were similar or different habitat full of different colors provided by many to their holdfasts (p = 0.531; U = 126; gl = 37). benthic and pelagic species. The ability of the sea- Specimens that had similar color to the holdfast horses to change their base color combined with (n = 18) were attacked by 13% of damselfish in all the habitat structure, turn these animals into cryp- experiments and individuals that had a different tic organisms even when they do not match their color (n = 20) were attacked by 20%. holdfast. In fact, crypsis might be the correct clas- The study seahorses had a mean height of 11.93 sification of the seahorse’s method of avoiding ± 2.94 cm. Males were longer than females, with a detection. Stevens and Merilaita (2009) define mean height of 12.72 ± 3.69 cm and 11.15 ± 1.69 crypsis as “features of physical appearance (e.g. col- cm respectively, although there was no significant oration), but also behavioral traits, or both, to pre- difference between the sexes (p = 0.09; t = 1.69; vent detection”. This definition also fits perfectly n = ). There was no relation between the number with our results in relation to the importance of of attacks and the size of the seahorse (p = 0,406; movement. Our results demonstrate the relevance r = 0,147) and no statistical significance among the of the absence of movement. In general, cryptic size of attacked and not attacked seahorses animals avoid detection by decreasing their move- (p = 0,805; U = 142). ment rates (Edmunds 1974; Sih 1987). These data Seahorse mobility was an important factor to S. are consistent with the experiment of Morey fuscus attack. Individuals that did not move were (1990) who compared vulnerability of the treefrogs not attacked, but all individuals that swam during Pseudacris regilla on matching and non-matching the experiment were attacked. Stegastes fuscus pre- backgrounds. The matching background treefrog sented regular aggressive behavior, attacking other appeared to be as vulnerable as the non-matching fish species in all 76 translocation experiments, treefrog when moving. No specific studies have including the control treatment. A total of 123 been accomplished about seahorse crypsis, but sev- attacks were recorded (3.26 ± 0.714 attacks/ exper- eral authors report the relevance of seahorse move- iment) during the control treatment. ment, color and body shape, such as Lourie et al. (1999) who highlight the small number of seahorse DISCUSSION predators due to the seahorse camouflage, low Seahorses were rarely attacked by the damselfish mobility and bony body shape; Perante et al. in our experiments. The results did not show any (2002) reports that Hippocampus comes Cantor relation between attacks and other physical features develops sedentary behavior as a strategy to make such as seahorse size, sex and color similarity/dis- its camouflage more efficient; and Foster & Vin- similarity to holdfast. Size was expected to have cent. (2004) state that seahorses present efficient some relevance as large animals were supposed to camouflage that improves fitness in prey capture be easier to detect (Kiltie 2000). But in the experi- and escape from predators and that they do not ments, the difference between maximum and min- show territorial defense against other fish species, imum size was not significant, which could explain indicating that color might be a crypsis strategy the absence of relation between both groups and and also a mechanism of communication between the attacks. Color is considered to be an important individuals of the same species. These data are con- feature in the camouflage of several species and sistent with the present study, assigning relevance they usually choose backgrounds upon which they to displacement behavior. will be better concealed (Mercurio et al. 1985; Loss of habitat is one of the major stresses suffered Moey 1990; Steen et al. 1992). However, the by the seahorses, decreasing their populations over experiments showed that it did not matter if sea- time (Foster & Vincent 2004). This habitat change horse color matched the holdfast color. This fact is may lead individuals to die or forces them to probably related to Merilaita et al.’s (1999) hypoth- migrate to other sites (Dulvy et al. 2003). Forced esis on cryptic coloration in heterogeneous habi- displacement implies vulnerability in seahorses, tats. They proposed that heterogeneous habitats making loss of habitat even more dangerous to the tend to shelter species that present color patterns species. Migration has been pointed out as a way

169 aqua vol. 18 no. 3 - 15 July 2012 Testing for camouflage of the Brazilian seahorse Hippocampus reidi (Syngnathidae) using the territorial damselfish Stegastes fuscus (Cuvier) (Pomacentridae) for maintaining stable stocks, but particular atten- MAZZONI, R., BIZERRIL, C. R. S. F., BUCKUP, P. A., CAE- tion should be given to this. More effective man- TANO, M. FILHO O., FIGUEIREDO, C. A., MENEZES, N. agement of coastal areas should be applied to avoid A., NUNAN, G. W. & TANIZAKI-FONSECA, K. 2000. loss of habitat, such as restriction of construction Peixes. In: A Fauna ameaçada de extinção do Estado do Rio de Janeiro (Eds H. G. Bergallo, C. F. D. Da Rocha, M. A. near rocky reefs and mangroves and reduction of Dos Santos Alves & M. Van Sluys): 63-73. Editora da bottom trawling near the coast. Universidade do Estado do Rio de Janeiro, Rio de Janeiro. ACKNOWLEDGEMENTS MENEGATTI, J. V., VESCOVI, D. L. & FLOETER, S. R. 2003. Our thanks to Dive Point for providing all scuba Interações agonísticas e forrageamento do peixe-donzela, diving equipment and the boat; to Gama Filho Stegastes fuscus (Perciformes: Pomacentridae). Natureza on University for providing support to develop the line, 1 (2): 45-50. research; to Viviane Martins, Marcelo Queiroz and MERCURIO, K. S., PALMER, A. R. & LOWELL, R. B. 1985. Predator-mediated microhabitat partitioning by two Roberto de Jesus for their fundamental support species of visually cryptic, intertidal limpets. Ecology 66: during field observations and to Raphael Tubino 1417-1425. and Carlos Augusto Rangel for their comments on MERILAITA, S., TUOMI, J. & JORMALAINEN, V. 1999. Opti- the study. mization of cryptic colouration in heterogeneous habitats. Biological Journal of the Linnean Society 67: 151-161. MOREY, S. R. 1990. Microhabitat selection and predation REFERENCES in the Pacific treefrog, Pseudacris regilla. Journal of Her- DULVY, N. K., SADOVY, Y. & REYNOLDS, J. D. 2003. petology 24: 292-296. Extinction vulnerability in marine populations. Fish and NELSON, J. S. 1994. Fishes of the world. John Wiley & Fishery 4: 25-64. sons, New York, 600 pp. EDMUNDS, M. 1974. Defence in animals: A Survey of Anti- PERANTE, N. C., PAJARO, M. G., MEEUWIG, J. J. & VIN- predator Defenses. Longman Inc., New York, 357 pp. CENT, A. C. J. 2002. Biology of a seahorse species, Hip- FERREIRA, C. E. L., GONCALVES, J. E. A., COUTINHO, R. pocampus comes in the central Philippines. Journal of Fish & PERET, A. C. 1998. Herbivory by the dusky damselfish Biology 60: 821-837. Stegastes fuscus (Cuvier, 1830) in tropical rocky shore: SALE, P. F. 1980. The ecology of fishes on coral reefs. effects on the benthic community. Journal of Experimen- Oceanography and Marine Biology: Annual Review 18: tal Marine Biology and Ecology 229: 241-264. 367-421. FOSTER, S. J. & VINCENT, A. C. J. 2004. Life history and SCHMID, M. S. & SENN, D. G. 2002. Seahorses – masters ecology of seahorses: implications for conservation and of adaptation. Vie et Milieu 52 (4): 201-208. management. Journal of Fish Biology 65: 1-61. SHINE, R., AMBARIYANT, HARLOW, P. S. & MUMPUNI FRERET-MEURIER, N. V. & ANDREATA, J. V. 2008. Field 1998. Ecological divergence among sympatric color studies of a Brazilian seahorse population, Hippocampus morphs in blood pythons, Python brongersmai. Oecologia reidi Ginsburg, 1933. Brazilian Archieves of Biology and 116 (1/2): 113-119. Technology 51 (4): 743-751. SIH, A. 1987. Predators and prey lifestyles: an evolutionary HULBERT, S. H. 1984. Pseudoreplication and the design and ecological overview. In, Predation: direct and indirect ecological field experiments. Ecological Monographs 54: impacts on aquatic communities. (Eds W. C. Kerfoot & A. 187-211. Sih): 203-224. University Press of New England, IUCN 2007. 2007 IUCN Red List of Threatened Species. Hanover. Available at http://www.iucnredlist.org; accessed SPALDING, M. D., RAVILIOUS, C. & GREEN, E. P. 2001. 2008/03/22. World Atlas of Coral Reefs. University of California Press, KILTIE, R. A. 2000. Scaling of visual acuity with body size California, 424 pp. in mammals and birds. Functional Ecology 14: 226-234. STEEN, J. B., ERIKSTAD, K. E. & HOIDAL, K. 1992. Cryp- LAGES, B. G. 2003. Avaliação do potencial invasor do coral tic behaviour in moulting hen willow ptarmigan Lagopus alcionáceo Stereonephthya aff. curvata (Nephtheidae - Alcy- l. lagopus during snow melt. Ornis Scandinavica 23: 101- onacea) na Reserva Extrativista Marinha de Arraial do 104. Cabo (RJ). MSc. Dissertation Universidade Federal Flu- STEVENS, M. & MERILAITA, S. 2009. Animal camouflage: minense. Niterói, 49 pp. current issues and new perspectives. Philosophical Trans- LEHNER, P. N. 1979. Handbook of Ethological Methods. actions of the Royal Society, 364 (B): 423-427. Garland STPM Press, New York, 672 pp. WILLIAMS, D. Mc B. 1991. Patterns and processes in the LOURIE, S. 2003. Measuring seahorses. Project Seahorse distribution of coral reef fishes. In: The Ecology of Fishes Technical Report 4: 15pp. on Coral Reefs. (Ed. P. F. Sale): 437-474. Academic Press, LOURIE, S. A., VINCENT, A. C. J. & HALL, H. 1999. Sea- San Diego. horses: An Identification Guide to the World’s Species and ZAR, J. H. 1999. Biostatistical analysis. Prentice Hall, New their Conservation. Project Seahorse, London, 214pp. Jersey, 663 pp.

aqua vol. 18 no. 3 - 15 July 2012 170