Flamboyant cuttlefish behavior: Camouflage tactics and complex colorful reproductive behavior assessed during field studies at Lembeh Strait, Indonesia

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Highlights

  • The colorful Flamboyant Display is among the most elaborate of cephalopods.

  • The Display is seen only during courtship and mate guarding or very briefly as a startle response to predators.

  • Mating is brief (3 s) and females are very choosy.

  • This cuttlefish has superb camouflage and remains this way the vast majority of time.

Abstract

The flamboyant cuttlefish Metasepia pfefferi is renowned for its bold and colorful body patterns, yet the functions of these displays and other behaviors remain largely unknown. We conducted two field studies in Indonesia using SCUBA and video to record its behavior under natural conditions. Camouflage via background matching and masquerade is the common primary defense against predators, and is also used offensively to approach prey closely. This species rarely uses its “flamboyant” bright conspicuous displays in nature; they were observed only during courtship or as secondary defense when a large fish closely approaches it. Males are only 10–60% the size of females and they court her with a vivid and dynamic Flamboyant Display, which appears to be one of the most elaborate among cephalopods. Conversely, females remain camouflaged and show no conspicuous courtship behaviors. When two males courted or mate-guarded a single female, unilateral signaling of aggression was observed. Twenty matings were recorded among 5 pairs of cuttlefish; they were in the “head-to-head” position and lasted only 3 s. Females were choosy; they required males to court for long periods and rejected 50% of males that attempted to mate with them. Females lay ca. 25 eggs per batch, roughly 6–7 min apart, usually during morning hours and with no male present. They often deposit eggs in coconut shells that occupy this open sandy habitat. This small species is cryptic and spends the vast majority of each day in a variety of highly camouflaged body patterns.

Introduction

The flamboyant cuttlefish is well known to the public because of its “Flamboyant Display,” which is a dynamic body pattern featuring bright yellow, red, white and brown colors accompanied by waves of patterns as well as distinctive arm postures and dynamic skin bumps called papillae (Fig. 1). This exotic body patterning has been popularized by photographers, natural history documentaries and public aquaria yet, curiously, the behavioral functions of this and other body patterns and behaviors remain largely unknown. There are only two scientific journal papers with information on aspects of its biology: a brief lab/field study by Roper and Hochberg at Lizard Island, Australia (Roper and Hochberg, 1988) and a lab study of 5th generation lab-reared flamboyant cuttlefish in a public aquarium (Thomas and MacDonald, 2016). A fundamental question from the viewpoint of behavioral ecology is: how does a small, soft-bodied, solitary animal living in a wide-open sand or mud plain survive predation, find food and find mates? Here we report two intensive field studies of natural behavior of flamboyant cuttlefish to provide a basis for determining its behavioral ecology in natural settings.

Section snippets

Materials and methods

Cuttlefish were studied at Lembeh Strait, North Sulawesi, Indonesia in December 2002 (8 days), and May 2019 (11 days). Nine dive sites were investigated, some several times. Water depths ranged from 4 to 15 m and the habitat was always open sand or sand mixed with mud (commonly called “muck diving” by the diving community; De Brauwer et al., 2017). Local guides and volunteer divers (17 in the first trip; 12 in the second) searched for cuttlefish, and then the authors and volunteers video taped

Results

Courtship, mating, egg laying and various tactics of camouflage were recorded during 400 min of video over the course of 10 days. Eight females and 12 males were studied at Lembeh; these were assumed to be different individuals due to the expansive study sites. Focal animal samples on video ranged from 5 to 60 min. Seven courtship sequences were recorded, each focusing on a single different female; four of these showed a single male courting the female, and the other three showed two males

Discussion

This field study elucidates some of the behavioral adaptations that Metasepia pfefferi has evolved to survive in the unique open sand/mud habits near coral reefs in the Indo-Pacific regions. Our results show that this species is camouflaged nearly all of the time, the main exception being the rare courtship displays by males and the very brief secondary defense responses shown when a threatening organism approaches it closely. The latter two occasions involve the elaborate Flamboyant Display (

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

We are indebted to John Forsythe who helped organize and conduct the 2002 trip, and Susan Sammon of CEDAM who organized the volunteers and their dive protocols for that expedition. The 2002 volunteers performed many dives, collected video, and outlined their findings before leaving the field site; we thank them for their assistance and dedication. Thanks especially to Annie Crawley who helped organize and collect imagery for both expeditions, and to Derya Akkaynak and the volunteer divers who

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