Elsevier

Zoology

Volume 123, August 2017, Pages 16-29
Zoology

The Ebbinghaus illusion in the gray bamboo shark (Chiloscyllium griseum) in comparison to the teleost damselfish (Chromis chromis)

https://doi.org/10.1016/j.zool.2017.05.006Get rights and content

Highlights

  • We tested the visual perception of Ebbinghaus circles in an elasmobranch and a teleost.

  • C. chromis succumbed to the illusion, similar to humans or dolphins (contrast effect).

  • In contrast, sharks were not deceived by the illusion (assimilation effect).

  • These contrasting responses point towards potential differences in perceptual processing mechanisms.

Abstract

This is the first study to comparatively assess the perception of the Ebbinghaus-Titchener circles and variations of the Delboeuf illusion in four juvenile bamboo sharks (Chiloscyllium griseum) and five damselfish (Chromis chromis) using identical training paradigms. We aimed to investigate whether these two species show similarities in the perceptual integration of local elements into the global context. The Ebbinghaus-Titchener circles consist of two equally sized central test circles surrounded by smaller or larger circles of different size, number and/or distance. During training, sharks and damselfish learned to distinguish a large circle from a small circle, regardless (i) of its gray level and (ii) of the presence of surrounding circles arranged along an outer semi-circle. During the subsequent transfer period, individuals were presented with variations of the Ebbinghaus-Titchener circles and the Delboeuf illusion. Similar to adult humans, dolphins, or some birds, damselfish tended to judge the test circle surrounded by smaller inducers as larger than the one surrounded by larger inducers (contrast effect). However, sharks significantly preferred the overall larger figure or chose indifferently between both alternatives (assimilation effect). These contrasting responses point towards potential differences in perceptual processing mechanisms, such as ‘filling-in’ or ‘(a)modal completion’, ‘perceptual grouping’, and ‘local’ or ‘global’ visual perception. The present study provides intriguing insights into the perceptual abilities of phylogenetically distant taxa separated in evolutionary time by 200 million years.

Introduction

Size, shape, and distance perception are not mere objective translations of images received by the eyes, because retinal images are typically ambiguous and thus subjective for every individual. Although early visual processing is an integral part of perceptual processing, the visual image depends not just on the properties of one single element (e.g., of the actually and ‘physically present’ visual information), but also on its contextual interaction and on the attributes of other features which may be present in the same image (Kandel et al., 2000, Macknik and Martinez-Conde, 2004, Troncoso et al., 2005, Troncoso et al., 2007, Macknik, 2006). Beyond early visual processing, this contextual interaction can cause optical illusions which generate a somehow altered impression of objectively measurable visual conditions (Pylyshyn, 1999, Kandel and Wurtz, 2000, Macknik et al., 2000, Macknik et al., 2008, Eagleman, 2001). Perceptual mechanisms that enable animals to perceive figures and forms instead of a collection of lines, curves or circles can be subject to cognitive functions, which are known to be closely related to areas of the dorsal pallium, i.e. the mammalian neocortex, or their equivalent areas in the pallium of birds and possibly even fishes (e.g., Mishkin, 1978, Murray and Mishkin, 1984, Zola-Morgan and Squire, 1985, Shapiro and Olton, 1994, Hampton and Shettleworth, 1996, Kandel et al., 2000, Berryhill and Olson, 2008, Agrillo et al., 2013). Some optical illusions are elicited in every individual with normal sight and appear not to depend on individual experience, but are consistently present and thus reflect the properties of the systematic processing of visual information (for review see Macknik et al., 2008). Others – for instance, cognitive illusions such as the Ebbinghaus circles or the Müller-Lyer deception – can be caused by systematic perceptual errors or the ‘rules’ of object organization in subsequent (“higher”) levels of sensory processing (‘inattentional blindness’) (Coren and Girgus, 1978, Macknik et al., 2008, Kelley and Kelley, 2014).

However, visual sensory information is processed and perceived differently across human and non-human species. On the one hand, this is due to evolutionary differences in the vertebrate eye itself such as spatial or temporal sampling or resolving power (e.g., mammals: Hughes, 1977, Coimbra et al., 2013, Mengual et al., 2015; birds: Fite and Rosenfield-Wessels, 1975, Hodos and Weibowitz, 1977, Coimbra et al., 2012; elasmobranchs: Hueter, 1990, Lisney and Collin, 2007, Lisney and Collin, 2008, Theiss et al., 2010), photoreceptor topography (Collin, 1999, Collin, 2008), cone monochromacy or multichromacy (for review see Osorio and Vorobyev, 2008, Marshall et al., 2015; mammals: Jacobs, 1993, Ahnelt and Kolb, 2000, Griebel and Peichl, 2003, Marshall et al., 2015; birds: for review see Bennett and Cuthill, 1994, Finger and Burkhardt, 1994; elasmobranchs: Hart et al., 2004, Hart et al., 2006, Hart et al., 2011, Van-Eyk et al., 2011, Bedore et al., 2013, Schluessel et al., 2014), or the composition of the dioptric system (e.g., elasmobranchs: Sivak, 1990, Collin and Collin, 2001, Hueter et al., 2001). On the other hand, there are differences in the neural processing of information in the brain: for instance, the pallial cortex of mammals devotes large areas to the processing of visual information (for review see Grill-Spector and Malach, 2004, Logothetis and Sheinberg, 1996), while fish, even though possessing a dorsal pallium, are thought to perform the vast majority of visual processing in the optic tectum of the midbrain (e.g., Wullimann and Meyer, 1990, Ebbesson, 1970, Smeets, 1983). Hence, optical illusions can help (i) to dissociate the neural activity that matches the perception of a stimulus from the neuronal activity that matches the physical reality and (ii) to reveal hidden constraints of the perceptual system and allow the investigation of the neuro-cognitive mechanisms and principles underlying visual perception in many different animal species (Macknik et al., 2008, Agrillo et al., 2013).

The question how different species – both vertebrates and invertebrates – respond to optical illusions in a way different than would be predicted based on physical parameters alone presents an interesting research topic that has recently claimed a lot of attention in a wide variety of species. Evaluations of different illusions have now been demonstrated in mammals (e.g., Von der Heydt et al., 1984, Bravo et al., 1988, Nieder, 2002, Scarpi, 2011, Murayama et al., 2012), birds (e.g., Nieder and Wagner, 1999, Bateson, 2002, Nieder, 2002, Morgan et al., 2012, Salva et al., 2013, Nakamura et al., 2008, Nakamura et al., 2014), teleosts (e.g., Wyzisk, 2005, Wyzisk and Neumeyer, 2007, Sovrano and Bisazza, 2008, Sovrano and Bisazza, 2009, Darmaillacq et al., 2011, Agrillo et al., 2013, Salva et al., 2014, Sovrano et al., 2014, Sovrano et al., 2016) and even invertebrates such as honey bees (Horridge et al., 1992, Shafir et al., 2002) or European cuttlefish (Zylinski et al., 2012).

Bamboo sharks (Chiloscyllium griseum) were previously tested for their response to optical illusions and their ability to perceive Kanizsa figures, subjective contours (induced by grating gaps or phase-shifted abutting gratings) and the Müller-Lyer size illusion in two-alternative forced choice experiments (Fuss et al., 2014a). In a series of transfer tests, sharks were able to discriminate successfully between various sets of Kanizsa figures in comparison to randomized Pacmen figures as well as between subjective contours resembling a square or a rhomboid. Also, the sharks did not succumb to the Müller-Lyer illusion, which consists of two center lines of equal length that are set between two arrowheads or tails. Similar to goldfish (Wyzisk, 2005), sharks seem to be able to identify the lengths of the center lines as being equal, irrespective of the surrounding elements. In contrast, the line featuring two arrowtails appears to be longer than the line featuring arrowheads to most humans (e.g., Tausch, 1954, Gregory, 1966a, Pressey, 1967, Warren and Bashford, 1977, Müller and O’Grady, 2000, Millar and Al-Attar, 2002), primates (e.g., rhesus macaques: Tudusciuc and Nieder, 2010; capuchin monkeys: Suganuma et al., 2007), birds (gray parrots: Pepperberg et al., 2008; pigeons: Nakamura et al., 2006; ring doves: Warden and Baar, 1929; chickens: Winslow, 1933) and teleosts (redtail splitfins: Sovrano et al., 2016).

Another well-known geometric size illusion is the Ebbinghaus illusion (also referred to as ‘Ebbinghaus-Titchener circles’). The Ebbinghaus size illusion displays two center circles (‘central target circles’) of equal diameter, which are surrounded by ‘inducer circles’ of different size, number and/or distance. Ebbinghaus circles have already been tested in several vertebrate groups. In adult humans (De Fockert et al., 2007) and children over ten years of age (Doherty et al., 2010), bottlenose dolphins (Tursiops truncatus, Murayama et al., 2012), 4-day-old chicks (Gallus gallus, Salva et al., 2013) and redtail splitfins (Xenotoca eisenii, Sovrano et al., 2014) larger surrounding (inducer) circles tend to decrease the size estimation of the central circle and vice versa (Murayama et al., 2012, Salva et al., 2013). Baboons (Papio papio, Parron and Fagot, 2007) were not affected by the Ebbinghaus illusion at all and continued to accurately judge the size of the central target regardless of the surrounding elements. Children under seven (Happé, 1996, Kaldy and Kovacs, 2003, Phillips et al., 2004, Doherty et al., 2010), pigeons (Columba livia, Nakamura et al., 2008), and bantams (Gallus gallus domesticus, Nakamura et al., 2014) perceive the Ebbinghaus-Titchener circles in a way opposite to older humans, chicks or teleosts, with larger inducer objects increasing the size estimate of the central target (Parron and Fagot, 2007, Nakamura et al., 2008, Nakamura et al., 2014).

Among the principles that are used to explain the differences in susceptibility to certain illusions in different vertebrate groups are metric aspects such as assimilation and/or contrast effects or orientation aspects such as regression to right angles or orthogonal expansion (Ninio, 2014). Situational and/or depending on an animal’s way of life, its visual attention can be distributed homogeneously over the entire visual field or focused on single or very few features of a scene or a set of stimuli (Posner et al., 1980, Duncan, 1984). These features would be emphasized while features beyond the focus would be neglected (Posner et al., 1980, Duncan, 1984). Thus, a size illusion may be caused when the visual point of focus is either shifted towards the surrounding context (size-assimilation illusion) or away from it (size-contrast illusion) (Girgus and Coren, 1982). However, it would be far too simple to draw a solid line between species prone to contrast effects and others prone to assimilation effects, since species may vary in their experience of these effects. In both humans and non-human species, the level of processing to be applied in a certain situation is highly flexible and influenced by context and task demands (Fremouw et al., 1998, Kimchi, 1992). For instance, pigeons or bantams can experience assimilation effects but not contrast effects, whereas humans experience both assimilation and contrast effects, depending on the magnitude of an illusion, their focal attention and previous experiences (Girgus and Coren, 1982, Nakamura et al., 2008).

Moreover, perceptual information processing mechanisms (e.g., perceptual grouping, filling-in etc.) that have evolved in different vertebrate groups have to be taken into account. For instance, humans (Treisman, 1982, Grossberg et al., 1997, Blake and Logothetis, 2002; for review see Wagemans et al., 2012), rats (e.g., Kurylo et al., 1997), monkeys (e.g., Spinozzi et al., 2006), pigeons (e.g., Cavoto and Cook, 2001, Nagasaka et al., 2005) and teleosts (e.g., Appelle, 1972, Truppa et al., 2010) use ‘perceptual grouping’; i.e., the neural substrates underlying visual discrimination and/or interpretation tend to group several elements of one stimulus together to form ‘a big picture’ (Treisman, 1982, Grossberg and Mignolla, 1985, Fang et al., 2008). This grouping helps to better interpret various stimuli or a complete scene. Perceptual grouping comprises different aspects: similar objects and objects close to each other tend to be grouped into one context or one stimulus perception. Moreover, connected and/or continuous figures are favored over non-continuous ones and incomplete shapes are preferentially completed or merged into whole figures (Grossberg and Mignolla, 1985, Fang et al., 2008). Other mechanisms underlying visual perception such as ‘filling-in’ (Kandel et al., 2000), ‘(a)modal completion’ (Michotte et al., 1964, Kanizsa et al., 1993, Singh, 2004) or the complementing of subjective contours assist the organization of contextual interactions of different object features such as shape, color, luminance, distance or movement (Kandel et al., 2000, Singh, 2004) and have been found in several vertebrate groups (mammals: Bertenthal et al., 1980, Bravo et al., 1988, De Weerd et al., 1990, Vallortigara, 2004, Vallortigara, 2009, Nielsen et al., 2006, Nielsen et al., 2008; birds: Nieder and Wagner, 1999, Nieder, 2002, Vallortigara, 2006, Wede, 2008; teleosts: e.g., Schuster and Amtsfeld, 2002, Wyzisk and Neumeyer, 2007, Sovrano and Bisazza, 2008, Sovrano and Bisazza, 2009; Siebeck et al., 2009; elasmobranchs: Fuss et al., 2014a).

Recently, the teleost redtail splitfin (Xenotoca eiseni) was shown to succumb to two size illusions (Müller-Lyer deception: Sovrano et al., 2016; Ebbinghaus illusion: Sovrano et al., 2014) in a way similar to humans. Teleosts belong to the ray-finned fishes (Actinopterygii) within the bony fishes (Osteichthyes), which evolved in the Triassic period about 250 million years ago (Kardong, 2012). In contrast, sharks, rays and chimeras belong to the cartilaginous fishes (Chondrichthyes) and represent one of the oldest extant jawed vertebrate groups that first arose some 450 million years ago (Compagno, 2001, Kardong, 2012). To meet the sharks’ requirements especially regarding position and size of presented stimuli, experiments in the present study were performed using a different training paradigm and experimental setup than used by Sovrano et al. (2014) to train redtail splitfins. Thus, parallel experiments with the saltwater teleost damselfish Chromis chromis were performed in the present study in order (i) to confirm, and facilitate comparison with, the results found by Sovrano et al., 2014, Sovrano et al., 2016, but using a different training paradigm and experimental setup and, thus, (ii) to rule out a possible bias for any aspect of paradigm and setup. C. chromis is a common indicator species for marine aquaria housing elasmobranchs and teleosts. It generally lives in small shoals above or near rocky reefs or above seagrass meadows (Quignard and Pras, 1986). Thus, they share important habitat properties and conditions with bamboo sharks used in the present study. In order to further investigate how juvenile bamboo sharks (Chiloscyllium griseum), as representatives of this vertebrate group, perceive geometrical size illusions, we tested in the present study how they react to contextual changes that influence the magnitude of the illusion and variations of the Ebbinghaus-Titchener circles (including the Delboeuf illusion). To study potential differences in the perceptual integration of visual size information in two species reflecting a phylogenetic distance of about 200 million years, the results obtained from bamboo sharks were compared to those obtained from damselfish.

Section snippets

Animals and housing facilities

Four experimentally naïve female juvenile bamboo sharks (Chiloscyllium griseum, head tail length: 25–40 cm) and five naïve juvenile damselfish (Chromis chromis, TL = 5–7 cm) were kept in three aquaria (two shark aquaria: 1.80 m × 0.5 m × 0.5 m; one damselfish aquarium: 1.00 m × 0.5 m × 0.5 m) filled with aerated, filtered salt water (ca. 1.0217 kg/dm3, conductance: about 50 mS) at 26 ± 2 °C, providing constant environmental conditions (conductivity, temperature, and pH). There was a 12 h light: 12 h dark cycle; all

Results

Four sharks and five damselfish started and finished the experimental training procedure. The following sections will summarize individual as well as group results.

Discussion

The present study investigated how juvenile bamboo sharks (C. griseum) and juvenile damselfish (C. chromis) perceive the Ebbinghaus-Titchener circles and variations of the Delboeuf illusion and how they react to contextual changes.

Sharks needed 13–22 sessions to distinguish a large circle from a small circle, regardless of (i) whether it was dark gray or light gray and (ii) the presence of surrounding circles arranged along an outer semi-circle (Table 1, Figs. 2 and 3a). Damselfish learned

Acknowledgments

We are specifically grateful to the “Haus des Meeres” in Vienna, Austria and the Frankfurt Zoo, Germany for supplying the animals used during this study. We would like to thank Max Müllender and Karsten Stehr for conducting experiments during the transfer phase, Slawa Braun for animal caretaking, maintenance and repairs and Horst Bleckmann for providing laboratory space and support. This study was funded by a DFG Grant (SCHL1919/4-1) to V.S. The research reported herein was performed under the

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