See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/297913466 Contingency checking and self-directed behaviors in giant manta rays: Do elasmobranchs have self-awareness? Article in Journal of Ethology · March 2016 DOI: 10.1007/s10164-016-0462-z CITATIONS READS 25 833 2 authors: Csilla Ari Dominic P D'Agostino University of South Florida University of South Florida 55 PUBLICATIONS 735 CITATIONS 106 PUBLICATIONS 2,118 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: Effect of ketone supplementation on CNS diseases View project Non-adenosine nucleosides, LPS and WAG/Rij rats View project All content following this page was uploaded by Csilla Ari on 11 February 2019. The user has requested enhancement of the downloaded file. Contingency checking and self-directed behaviors in giant manta rays: Do elasmobranchs have self-awareness? Csilla Ari & Dominic P. D’Agostino Journal of Ethology ISSN 0289-0771 J Ethol DOI 10.1007/s10164-016-0462-z 1 23 Your article is protected by copyright and all rights are held exclusively by Japan Ethological Society and Springer Japan. This e-offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy J Ethol DOI 10.1007/s10164-016-0462-z ARTICLE Contingency checking and self-directed behaviors in giant manta rays: Do elasmobranchs have self-awareness? 1,2,3 1,2,3 Csilla Ari • Dominic P. D’Agostino Received: 30 November 2015 / Accepted: 20 February 2016 Ó Japan Ethological Society and Springer Japan 2016 Abstract Elaborate cognitive skills arose independently in Introduction different taxonomic groups. Self-recognition is conven- tionally identified by the understanding that one’s own Animal cognition is the process by which animals acquire, mirror reflection does not represent another individual but process, store and act on information gathered from the oneself, which has never been proven in any elasmobranch environment (Shettleworth 2010; Brown 2014). Con- species to date. Manta rays have a high encephalization sciousness includes sentience, intelligence and self- quotient, similar to those species that have passed the mirror awareness (Brown 2014), or, in other words, awareness of self-recognition test, and possess the largest brain of all fish internal and external stimuli, having a sense of self and species. In this study, mirror exposure experiments were some understanding of one’s place in the world (Chandroo conducted on two captive giant manta rays to document their et al. 2004; Bekoff and Sherman 2004; Brown 2014). response to their mirror image. The manta rays did not show Animal consciousness has been a long-time interest and signs of social interaction with their mirror image. However, a debated field among cognitive ethologists (Heyes 1994, frequent unusual and repetitive movements in front of the 1998; Povinelli et al. 1997). The mirror self-recognition mirror suggested contingency checking; in addition, unusual (MSR) test initially developed by Gallup (1970) is con- self-directed behaviors could be identified when the manta sidered to be a reliable behavioral index to show an ani- rays were exposed to the mirror. The present study shows mal’s ability for self-recognition/self-awareness (SA; evidence for behavioral responses to a mirror that are pre- Platek and Levin 2004; Prior et al. 2008). Recognizing requisite of self-awareness and which has been used to oneself in a mirror is a rare capacity among animals (Reiss confirm self-recognition in apes. and Marino 2001), while no species of fish has so far passed this test. There has been only one report on self- Keywords Self-recognition Á Mirror test Á Comparative recognition in fish using chemosensory recognition cognition Á Mobulidae Á Cognition (Thu¨nken et al. 2009). However, studies conducted on other fish species reported that the response to their mirror images differed from responses to conspecifics (Verbeek Electronic supplementary material The online version of this et al. 2007; Desjardins and Fernald 2010; Suddendorf and article (doi:10.1007/s10164-016-0462-z) contains supplementary material, which is available to authorized users. Butler 2013; Balzarini et al. 2014). The only nonhuman species which demonstrated MSR are the great apes (i.e., & Csilla Ari chimpanzees, Pan troglodytes, Pan paniscus; orangutans, [email protected] Pongo pygmaeus; gorilla, Gorilla gorilla), asian elephants 1 Hyperbaric Biomedical Research Laboratory, Department of (Elephas maximus), bottlenose dolphins (Tursiops trunca- Molecular Pharmacology and Physiology, Morsani College tus) and a non-mammal species, the magpie (Pica pica) of Medicine, University of South Florida, 12901 Bruce B. (Gallup 1970; Amsterdam 1972; Lethmate and Ducker Downs Blvd., MDC 8, Tampa, FL 33612, USA 1973; Povinelli et al. 1993; Miles 1994; Patterson and 2 Foundation for the Oceans of the Future, Budapest, Hungary Cohn 1994; Walraven et al. 1995; Prior et al. 2008). 3 Manta Pacific Research Foundation, Kona, HI, USA 123 Author's personal copy J Ethol Those species that passed the MSR test to date share Manta birostris (estimated disc width 4.2 m) which had common characteristics, such as large, complex and highly been living in the exhibit for over 2 years, while the second foliated brain, complex social behavior, cooperative and subject (M2) was a female (estimated disc width 3.3 m) empathic behavior. The largest brain of all fish species is that had been at the Aquarium for 1 year. This individual’s possessed by manta rays with high encephalization quotient taxonomical classification is uncertain to date, because her and highly foliated cerebellum (Ari 2009, 2011), they often characteristics almost completely fulfill the criteria for M. form large feeding aggregations suggesting complex social birostris, except for a white mouth region, brownish back system, and are often referred to as being intelligent; therefore, coloration and the lack of large white shoulder bars. manta rays may be considered the most likely candidates from The two manta rays showed similar responses through- any fish species to pass the MSR test. The universal use of this out the study, and therefore their data were merged in most test has attracted controversy, because it is biased for vision, cases during the representation of the results, unless there but not other sensory modalities. Although it has been sug- was significant difference between their behaviors, in gested that olfactory recognition using chemical cues is more which case their data are presented separately. appropriate for fish (Thu¨nken et al. 2009;Brown2014), this might not be the case for Mobulids. Manta rays have excep- Apparatus and procedure tionally large optic tectum and telencephalon among elas- mobranchs, and the high importance of vision during their The observation area (OA) was selected to be the widest foraging activity has also been recently described (Ari 2009, area in the tank that was free of underwater decoration 2011;AriandCorreia2008), which further supports the obstacles, where the animals were able to turn and possibility that evaluating their self-awareness based on the maneuver comfortably when necessary (Fig. 1). The two MSR test is likely a suitable technique. manta rays’ behavior was documented in a rectangular area The definitive test of MSR is the mark test focusing the of the tank (OA) that was approximately 10 m wide, 15 m animal’s behaviors on the newly marked area of their body long and 5.5 m deep, where the mirror was considered when exposed to a mirror (Sarko et al. 2002). However, visible to the manta rays (Fig. 1). similarly to marine mammals, fish species also have the Three experimental conditions were tested: (1) mirror disadvantage that they are not able to touch the marked placed in the water (MI); (2) control conditions when the area of their body; therefore, it is more challenging to mirror was either removed completely (MO), or (3) a evaluate their behavioral response. Exploratory and social mirror-sized, non-reflective white board was placed in the behavior can be observed at first when animals are exposed water (WB). Seven trials were performed in each experi- to a mirror, which stage is followed by contingency mental condition during 16 days. Each trial was conducted checking when the animals engage in highly repetitive or between feeding times and lasted for 10 min. The test was unusual movements to understand their own image. In the performed with a 0.9 m 9 1.5 m mirror which was tem- next stage, the animals might show self-directed behavior porarily installed in a horizontal orientation on the side of (e.g., dolphins blowing bubbles, chimpanzee picking teeth; Gallup 1970; Reiss 2012; Sarko et al. 2002; de Veer and van den Bos 1999), before the mark test would be initiated. Mirror exposure experiments were conducted on two captive giant manta rays to document their responses to their mirror image in order to predict whether they would be a candidate for the mark test and whether they use a mirror to understand their own image. The present study shows evidence for manta rays’ contingency checking and self-directed behavior when exposed to a mirror, which are the prerequisites of self-awareness. Materials and methods Subjects Fig. 1 The observation area (OA, rectangle) of the tank is presented, Two giant manta ray specimens were exposed to a mirror at where the mirror was considered visible to the manta rays, from dorsal view.