universidade federal do rio grande do norte … · nikola tesla there are no mistakes. the events...
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UNIVERSIDADE FEDERAL DO RIO GRANDE DO NORTE
CENTRO DE BIOCIÊNCIAS
PROGRAMA DE PÓS-GRADUAÇÃO EM PSICOBIOLOGIA
DANIEL SILVA POLARI
Conscious or Zombies
Self-Perception in Callithrix jacchus & Dinoponera quadriceps
Dissertação apresentada a Universidade
Federal do Rio Grande do Norte, como
cumprimento dos requisitos para a obtenção
do grau de Mestre em Psicobiologia.
NATAL, RN - BRASIL
2016
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DANIEL SILVA POLARI
Conscious or Zombies
Self-Perception in Callithrix jacchus & Dinoponera quadriceps
Dissertação apresentada a Universidade
Federal do Rio Grande do Norte, como
cumprimento dos requisitos para a obtenção
do grau de Mestre em Psicobiologia.
Orientadora: Renata S. Sousa-Lima
Banca de Defesa
Profª Drª Renata S. Sousa-Lima
Profº Drº José Zamorano-Abramson
Profª Drª Maria Emilia Yamamoto
Profº Drº Milton Cezar Ribeiro
NATAL, RN – BRASIL
2016
3
Catalogação da Publicação na Fonte. UFRN / Biblioteca Setorial do Centro
de Biociências
Polari, Daniel Silva.
Conscious or Zombies Self-Perception in Callithrix jacchus &
Dinoponera quadriceps / Daniel Silva Polari. – Natal, RN, 2016.
68 f.: il.
Orientadora: Profa. Dra. Renata S. Sousa-Lima.
Dissertação (Mestrado) – Universidade Federal do Rio Grande do Norte.
Centro de Biociências. Programa de Pós-Graduação em Psicobiologia.
1. Callithrix jacchus. – Dissertação. 2. Dinoponera quadríceps. –
Dissertação. 3. Auto-percepção. – Dissertação. I. Sousa-Lima, Renata S. II.
Universidade Federal do Rio Grande do Norte. III. Título.
RN/UF/BSE-CB CDU
599.821
4
Title: Conscious or Zombies – Self-Perception in Callithrix jacchus & Dinoponera
quadriceps.
Author: Daniel Silva Polari
Defense Date: March 4th 2016.
Defense Committee:
Profª Drª Renata Santoro de Sousa Lima Mobley
Federal University of Rio Grande do Norte – Brazil
Profº Drº José Zamorano Abramson
Complutense University of Madrid – Spain
Profª Drª Maria Emilia Yamamoto
Federal University of Rio Grande do Norte – Brazil
Profº Drº Milton Cezar Ribeiro
Paulista State University – Brazil
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…For a better treatment to humans and non-human individuals around the world…
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EPIGRAPH
“The more you know yourself, the more clarity there is. Self-knowledge has no end,
you don’t’ come to an achievement, you don’t come to a conclusion. It is an endless
river.
Jiddu Krishnamurti
My brain is only a receiver, in the universe there is a core from which we obtain
knowledge, strength, inspiration. I have not penetrated into the secrets of this core, but
I know that it exists.
Nikola Tesla
There are no mistakes. The events we bring upon ourselves, no matter how
unpleasant, are necessary in order to learn what we need to learn; whatever steps we
take, they are necessary to reach the places we’ve chosen to go.
Richard Bach
Man in his arrogance thinks himself a great work, worthy of the interpretation of a deity.
More humble and I think truer to consider him created from animals.
Charles Darwin
A problem cannot be solved by the same consciousness in which it arose.
Albert Einstein
It is just like man’s vanity and impertinence to call an animal dumb because it is dumb
to his dull perceptions.
Mark Twain
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ACKNOWLEDGEMENTS
Tricky... how to put acknowledgments in sentences to such a life creation that
brought me to now? That can be complex. But what isn’t in academy? Really tricky is
the construction of a manuscript: hate and love. Love because you give yourself to it.
Hate because of certain difficulties. But what would be of us without such duality? I
deeply believe that there is a proportional relation between the facts of life, in a way
that, probably, love and hate walk on similar paths. But of which beliefs lives a
scientist? To do science in a precarious country is a work for few. Maybe one day we
will live the Brazilian exuberance hidden by the decay of the political and
socioeconomic systems, which would allow the expansion of the scientific knowledge
with the expected support to all professionals, scientist or not. And to think that it can
get worse… Take care Brazil, you are being consumed and we are already exploited.
Well, revolts apart, I get back to the theme. We should be thankful. I would like to
thanks, from my deepest self, to each one that, in your own singularity, collaborated
directly or indirectly to the 28.25 years of my mind expansion. It was you whom allowed
me to get until today. Above all, I would like to highlight here the tenderness dedicated
to my study theme, which is with me through the last years and probably will be with
me to my whole life. Therefore, in parts, I dedicate and I am thankful.
Initially, to my own self, in his own variations, as the macroscopic being attributed
to Daniel Silva Polari; as to my subjective side, the one that only I feel, which,
independently from its real origins or function, allow me to feel alive, and to be alive.
This is what instigates me. Thank you for allowing me to be.
I also would like to acknowledge my professors, that allowed me the expansion of
my knowledge. Without you my consciousness would have the size of an atom. Thank
you for allowing me, with the right respect and sensitivity, to accomplish my dreams
and objectives beyond life complications. I feel today that my consciousness has
reached the size of a molecule, and that will never see through the eyes of an atom
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again. Specially, I am thankful for the advices during the graduation, to the professor
Renata Sousa-Lima, for the patience to understand concepts sometimes complicated
and for the time spent appraising such a delicate theme. It took us many hours, but I
believe that it resulted in an interesting manuscript, which I present here.
A special thank you to my Family, that since always have supported my dreams and
the achievement of my craziness, sometimes expensive and consequently impossible
by myself. I hope that one day I can retrieve all the costs. I am sorry for the conflicts
and thank you for all.
To my beloved friends, for each second of mind expansion and casualness. Without
you I would be nothing. A kiss in everyone’s heart. I don’t even need to quote names.
You will recognize yourself here!
To my partner for the last 3 years, Agnes Santos da Rosa, for allowing me to live
dreamed moments, sometimes hardly, but always lovely. Without you, I wouldn’t be
here. That your life always be full of accomplishments and success. That you improve
always beautifully and guided to the expansion of this wild world where we are in.
I would like to give a special acknowledgment to my interns, whom with personal
means, offered me all palpable help to the execution of my graduation, giving up on
fun to study and to work, actively participating from the beginning. I know that we have
passed through hard ones, but we have grown and overwhelmed that. The future
promises! A kiss in each of your hearts.
I am very thankful to the marmosets that were part of this study, which surely do not
like to be captive, but it was incredible to be able to know a little bit of each individuality
of these very special beings. That my work can positively affects the life quality of
individuals submitted to captivity conditions
A special thanks to the veterinary Janaína Nitta Figueiredo, who dedicates her days
to the care of more than 150 animals of the primatology centre. Difficulties are extreme,
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however her love for the animals allow them to live healthy and with welfare possible
for Brazilian patterns.
A deep acknowledgment to Science and to all scientist, whom efforts allow us to
understand a little bit of the intriguing phenomenon of consciousness. We are far from
an end, but recent works suggest that we are in the way for better enlightenments.
Not less important, I would like to thanks for the financial support from CAPES,
which even that considered as costs support, in reality was my main income during the
two years of research, together with many of other graduate students around the
country.
I am very thankful to the UFRN, here represented by the graduation program of
Psychobiology. That was the opportunity of a life time; Thank you for believing me and
my project since the first interview. There were many opened doors in my life, that part
of who I am I owe to you: scientist, a little bit crazy, but in love for knowledge and its
expansion.
In the end, I would like to acknowledge the universe for the different wave function
collapses during my life, which allowed me to path the world until the present moment.
Thank You!!!
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AGRADECIMENTOS
Intrigante... como agradecer em palavras a construção de uma vida que me trouxe
ao agora? Isso pode ser algo complexo. Mas o que não é complexo na academia?
Intrigante mesmo é a construção de um manuscrito: ódio e amor. Amor pela entrega
Ódio por certas dificuldades. Mas o que seríamos de nós sem tal dualidade? Acredito
profundamente que há uma relação proporcional entre os fatos da vida, de forma que
o amor e ódio provavelmente caminham juntos. Mas, de que crenças vive um
cientista? Fazer ciência em um país precário é obra para poucos. Quem sabe um dia
vivamos a exuberância brasileira escondida pela podridão dos sistemas políticos e
socioeconômicos, expandindo o conhecimento científico com o suporte imprescindível
aos profissionais, cientistas ou não. E pensar que o que está ruim pode piorar...
Cuidado Brasil, estão lhe consumindo e já estamos explotados!
Mas bem, revoltas à parte, retorno ao tema. Temos que agradecer. Obrigado, do
fundo do meu mais profundo eu, à cada qual que, em sua singularidade, direta ou
indiretamente colaboraram aos 28,25 anos de expansão da minha mente. Foram
vocês que me permitiram chegar ao hoje! Acima de tudo, friso aqui o carinho que
dedico a essa temática, que me acompanha há alguns anos e provável que me
acompanhe por toda a vida. Sendo assim, por partes, dedico e agradeço
Inicial3mente, ao meu próprio eu, em suas diversas vertentes, como ser
macroscópico atribuído ao indivíduo Daniel Silva Polari; não obstante, como ser
subjetivo, aquele que só eu sinto, que independente da sua real origem ou função,
permite-me sentir vivo e ser vivo. É isso que me instiga. Obrigado por me permitir ser.
Agradeço aos mestres, que permearam essa expansão de conhecimento. Sem
vocês minha consciência seria do tamanho de um átomo. Obrigado por permitirem,
com todo o carinho e respeito, a conquista dos meus objetivos e sonhos diante das
complicações da vida. Sinto que hoje minha consciência atingiu o tamanho de uma
molécula que nunca mais verá o mundo com os olhos de um átomo. Em especial,
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agradeço a orientação durante o mestrado, à professora Renata Sousa-Lima, pela
paciência para entender conceitos por vezes complicados e pelo tempo dispendido
numa temática complexa. Foram horas à fio, mas acredito que renderam um
manuscrito interessante, que aqui lhes apresento.
Um obrigado especial aos meus familiares, que desde sempre apoiaram meus
sonhos e a realização das minhas loucuras, por vezes caríssimas e
consequentemente impossíveis sozinho. Espero um dia poder retribuir todo o
dispêndio. Desculpem os conflitos e obrigado por tudo.
Aos meus amigos, por cada segundo de descontração e contração mental! Sem
vocês eu nada seria. Um beijo no coração de todos! Nem preciso citar nomes. Vocês
aqui se reconhecem!
A minha companheira nos últimos 3 anos, Agnes Santos da Rosa, por me permitir
viver momentos sonhados, por vezes difíceis, mas sempre amados. Sem você eu hoje
aqui não estaria! Que sua vida seja sempre repleta de conquistas e sucessos. Que
você cresça sempre linda e encaminhada a expandir o mundo louco no qual estamos
inseridos.
Deixo aqui um muito obrigado especial as minhas estagiárias, que com muita
entrega pessoal, me forneceram todo o auxílio cabível para a execução do meu
mestrado, abrindo mão de diversas horas de diversão para estudar e trabalhar,
participando ativamente desde o princípio. Sei que passamos por situações
absolutamente complicadas, mas crescemos e superamos. O futuro promete! Um
beijo forte no fundo do coração de cada uma.
Um obrigado aos saguis que participaram do trabalho, certeza que eles não
gostariam de estar em cativeiro, mas é incrível poder conhecer um pouco da
individualidade de cada um desses seres especiais. Que meu trabalho possa afetar
positivamente a qualidade de vida de indivíduos submetidos a condições cativas.
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Um agradecimento especial a veterinária Janaína Nitta Figueiredo, que dedica seus
dias ao cuidado de mais de 150 animais do núcleo de primatologia. As dificuldades
são extremas, mas seu amor pelos animais permite que os indivíduos ali presentes
possam vivam com saúde e bem-estar, dentro do possível para os padrões Brasil.
Um profundo agradecimento à ciência e a todos os seus representantes, que com
seus esforços nos permitem hoje entender um pouco mais sobre o intrigante
fenômeno que estudo. Estamos longe de um ponto final, mas os trabalhos recentes
apontam que um caminho promissor.
Não menos importante, agradeço ao suporte financeiro da CAPES, que mesmo que
embutido como auxílio de custo, em realidade foi meu sustento pelos dois anos de
pesquisa, assim como da boa parte dos discentes de pós-graduação espalhados pelo
país.
Sou muito grato a UFRN, aqui representada pelo Programa de Pós-graduação em
Psicobiologia. Essa foi uma oportunidade ímpar na minha vida. Obrigado por
acreditarem em mim e no meu projeto desde a primeira entrevista. Foram tantas as
portas que abriram na minha vida, que a vocês devo parte de quem sou, cientista, um
pouco maluco, mas amante do conhecimento e de sua expansão.
Por fim, agradeço ao universo pelos diversos colapsos da função de onda ao
decorrer da minha vida que me permitiram trilhar o mundo ao meu momento atual.
MUITO OBRIGADO!!!
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RESUMO
Consciência como fenômeno biológico pode consistir de diferentes estados
sensoriais, sentimentos e emoções. Comportamentos especializado, ações
sofisticadas de comunicação, meta-cognição, interação social, orientação especial,
use de mapas mentais para navegação e memória espaciais, apontam para tipos
diferentes de processamentos consciente em gêneros que não o Homo. O presente
trabalho busca identificar a auto-percepção em diferentes espécies, com testes do
espelho em Callithrix jacchus e com testes de auto-localização em Dinoponera
quadriceps. O comportamento de C. jacchus no espelho foi catalogado utilizando dois
protocolos diferentes: com marca e sem marca. A capacidade de navegação de D.
quadriceps durante o forrageio, foi calculada considerando três diferentes categorias:
(1) acesso livre ao ninho/recurso, (2) acesso direto bloqueado por objeto opaco; e 3)
bloqueado por objeto transparente. Nossos resultados apontam para auto-percepção
e mambas as espécies, com C. jacchus apresentando comportamentos de verificação
de contingência, auto-observação, além de utilizar a imagem refletida para observar o
ambiente e reagir a marca. D. quadriceps foram capazes de perceber sua própria
localização no ambiente e calcular caminhos curtos até a colônia após obter o recurso
alimentar, em todos os três tipos de testes. Aqui nós apresentamos evidência de
estados conscientes em outras espécies que não vertebrados.
PALAVRAS-CHAVE: auto-percepção, auto-localização; auto-reconhecimento;
navegação; invertebrados; MSR; teste do espelho; teste da marca; Callithrix jacchus;
Dinoponera quadriceps.
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ABSTRACT
Consciousness, as a biological phenomenon, may consists of states of feeling,
sensation or awareness. Specialized behaviour, sophisticated actions of
communication, metacognition, social interaction, spatial orientation, the use of mental
maps for navigation, and spatial memory, all point to conscious processing in genus
other than Homo. This work aims to identify self-awareness states in two different
species: using mirror self-recognition tests in Callithrix jacchus, and using self-
perception tests in Dinoponera quadriceps. Displays of C. jacchus self-recognition
using a mirror, were appraised with two protocols: no mark and with mark.
D.quadriceps navigational capability displays during foraging trips to food resource,
were appraised considering three different tests categories: (1) free access, (2)
blocked by opaque object; and 3) blocked by clear object. Our results show self-
perception in both studied species. With marmosets displaying contingency check
behaviour to the specular image, self-observation, environmental exploration using the
mirror as a tool and little, but significant mark reactions. Tocandiras were able to
perceive its own location and to calculate short return paths to the colony after
obtaining the food resource in all three types of tests. Here we provide further evidence
of conscious states for species other than vertebrates.
KEYWORDS: self-awareness, self-perception; invertebrate navigation; mirror-self-
recognition; MSR; mirror-test; mark-test; Callithrix jacchus; Dinoponera quadriceps.
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SUMMARY
EPIGRAPH ............................................................................................................. 6
ACKNOWLEDGEMENTS....................................................................................... 7
AGRADECIMENTOS ........................................................................................... 10
RESUMO.............................................................................................................. 13
ABSTRACT .......................................................................................................... 14
SUMMARY ........................................................................................................... 15
GENERAL INTRODUCTION ................................................................................ 16
GENERAL OBJECTIVE ....................................................................................... 24
SPECIFIC OBJECTIVES...................................................................................... 24
HYPHOTESIS ...................................................................................................... 24
CHAPTER ONE ................................................................................................... 25
CHAPTER TWO ................................................................................................... 42
GENERAL DISCUSSION ..................................................................................... 58
BIBLIOGRAPHIC REFERENCES ........................................................................ 62
GLOSSARY .......................................................................................................... 67
ANNEX ................................................................................................................. 68
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GENERAL INTRODUCTION
When we talk about consciousness, there is a lot of discussion about its definition,
significance, and therefore about its existence. Indeed, nowadays theories
interconnect philosophy, physics, chemistry, mathematics, psychology and biology, to
achieve a better understanding of this phenomenon. Cogito ergo sum – I think
therefore I am – from René Descartes (1637) must be the oldest argument in history
that supports the study and interpretation of our reality. Descartes, at that time, related
self-perception to existence, assuming it is impossible to doubt one’s own existence if
one perceives that one exists. Over this perspective, self-perception studies evolved
in new ideas to understand consciousness.
Descartes’ ideas influenced scientists for decades mainly from a dualistic
perspective. His concepts set the stage for contemporary ideas considering
materialism and reductionism. Dennett (1991) argues that consciousness is an
illusionary mechanical neuro system which is an output of unsupervised parallel
processing networks. On the other hand, Searle (1997) suggested that consciousness
should not be a neuro mechanism but a qualitative subjective mental phenomenon, a
biological outcome for all species, proposing that consciousness is present in states of
feeling, sensation or awareness. From phenomenology, Tononi (2004) theorizes that
consciousness is integrated information, assuming that all systems that integrate
information are conscious in different levels. From that we could speculate that not only
living systems but also machines such as computer systems are conscious, which
would provide the foundations of the controversial establishment of artificial
intelligence.
Subject’s conscious perception is a part of the processing of integrated information
of a system, represented by a subject’s feeling of the present moment and of the
behavioural response from the decision making momentum. Apparently, decision
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making takes place before the behaviour response and before conscious perception.
Actually, with up to 10 seconds before the perception of the action itself (SOON et al.
2008), subject’s neural activities are already modulated and it is possible to know ones’
decision just by looking at the brain energy flow. Therefore, decision making and
conscious perception are not exactly happened at the same time. On that perspective,
Dennet’s views has tangible values.
Consequently, we can speculate that consciousness perception would have its
origins late in phylogeny, mainly present in high developed brain systems, thrilling the
assumption that a few species other than humans are conscious. However, different
species with different levels of neurological development displays the ability to
supervise, organize and appraise sensory processes, modulating their own behaviour
and the behaviour of others, directly interfering in the habitat. Therefore, this might be
enough evidence of some level of consciousness and awareness for a diverse range
of species in phylogeny.
Phenomenological interpretation of consciousness might be an assumption of a
phylogenetic approach. We can consider that consciousness may have evolved in
different scales of experience, from first living cells to nowadays species, with different
individuals presenting different stages of experience. However, there is caution about
using phylogenetic distances among species systems as a proxy to consciousness.
Still, all exposed concepts are very controversial, triggering a series of discussions
about what exactly is consciousness. Following that debate I assume: Consciousness
– integrated information which can provide evidence of someone or something for a
specific living system, mixing the interpretation from Searle (1993) and Tononi (2004);
Awareness – the access to processed data without subjective experience. With that in
mind, recent ethological studies provides evidence of the expression of consciousness
and awareness in phylogenetic distant species of vertebrates and invertebrates
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(Edelman et al. 2005; Panksepp, 2005; Mather, 2008; Reiss & Marino, 2001; Polari,
2013). Thus, we can start to ask: Are all vertebrate and invertebrate species
conscious? Could we find evidence of conscious states in simpler organisms?
Tripicchio (2007) suggests that consciousness has its origins in a gradual
evolutionary continuum, from simple cell sensitivity up to higher levels of biological
complexity: 1) insentient, unicellular organisms up to porifera. At this level, answers to
environmental stimuli are derived from the cells, manifesting only by protoplasm
irritability. 2) Proto-sentient, mainly considering Coelenterates, in which cells already
started functional specialization and specimens are able to react to electrical stimuli,
transporting information and providing diffuse responses back to the environment. 3)
Pre-sentient, comprising organisms with ganglionic systems capable of receiving,
processing and sending information. 4) Sentient, grouping species with emergent
levels of consciousness through central nervous systems, which would include all
chordates, until new-born Homo sapiens sapiens or children and adults with some
developmental neuropathology. 5) Conscious stage, referring to the most recently
evolutionary-adaptive phenomenon developed in phylogeny, comprise mainly
humans. 6) Hyperconscious stage, achieved with the use of psycho stimulant drugs.
Tripicchio’s points to a consciousness scale over phylogeny, from which
neurological bases can be distinguished. This approach harbours the ethological
perspective, but presents considerable limitations ignoring evidence from the last
decades about consciousness and awareness expression for species other than
humans. Nonetheless, Tripicchio’s scale provides an interesting suggestion on how to
explore the consciousness spectrum distribution in phylogeny, but still it is far from
being a methodological guideline for the study of the phenomenon of consciousness
in biological systems.
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The absence of neocortex apparently does not inhibit an organism of having the
experience of affective states (LOW et al. 2012). In non-human species, the
somatosensory system is the start point of affective states (BAARS, 1997; EDELMAN
et al. 2005; MICHAEL & PERLIS, 2005; SANT'ANA, 2009). We can speculate about
the biological functions of affective states, as they may be related to life support
purposes, and therefore possibly be present among all life forms. In psychobiology, to
understand consciousness is to address a fifth question about the study of behaviour,
extending Tinbergen’s work (1963) to understand how and why an affective state may
modify and influence a subjects’ behaviour (Bateson & Laland, 2013).
The first biological study about the sense of self, dates back to the IXX century,
conducted by Darwin in orangutans, using a mirror to test for self-recognition. In the
XXth century, Gallup (1970) brought this approach back to the scene. Since, theoretical
and practical issues have arisen while many authors appraised self-awareness and
self-consciousness (DARWIN, 1871 apud 2009; GALLUP, 1970; PETTERSON, 1993;
BAARS, 1997; DELFOUR & MARTEN, 2001; REISS & MARINO, 2001; HOWE et al.
2003; MATTER, 2006; PLOTNIK et al. 2006; PLATEK et al. 2007; CARTER, 2008;
MATHER, 2008; PRIOR et al. 2008; MILLER, 2009; POLARI, 2013). During that time
different cognitive displays were registered for phylogenetically distant species,
demonstrating the presence of conscious and/or aware mental states not only to the
genus Homo. Some interesting examples of such specialized behaviour are
sophisticated actions of communication, metacognition, social interaction, spatial
orientation and the use of mental maps and spatial memory for navigation (SANT'ANA,
2009). The presence of flexible and complex memory, the use of tools and accessories,
simple and complex reasoning have also been considered as traits that suggest
awareness and conscious states in human and non-human animals (COOK, 1993).
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Observe and evaluate behaviour responses allow scientists to hypothesize about
the expression of subjective experience in humans and other animals. In control
conditions, for example, self-recognition test such as those with the use of a mirror,
are important mechanisms to appraise animals’ subjectivity side. When an individual
is capable of examining his own image in a reflection, recognising his own identity and
not another member of the same species, we can speculate about the expression of a
conscious self.
Discussion during the past decades improved mirror test protocols and evaluated if
the analyses of mirror test results would be sufficient to prove conscious states. When
you recognize yourself in front of a mirror, you are the mental object of your own
attention. In addition, when an individual performs contingency check behaviour to the
specular image, there is at least, an agent aware of himself and of his body position in
the environment, while performing its own movements. Therefore, the individual has
an implicit information about his own self. (Gallup, 2002; Reiss & Marino, Delfour &
Marten, 2001).
Hauser and collaborators (1995) suggest that the mirror test might not be sufficient
to verify if an animal is able to recognize himself in a mirror if not properly conducted.
These authors argue that to elicit significant mirror staring, it might be necessary to
impose radical changes to an individual's body, such that the alteration is highly salient
to draw the animal's attention to the mirror image. In their study, cotton-top tamarins
had body parts significantly altered, and self-directed mirror behaviour was verified for
a monkey species for the first time. This evidence had to be dismissed years later due
to alleged data fabrication. To date the only evidence of primates other than man and
apes to display mirror-self-recognition comes from rhesus monkeys (Rajala et al.
2010).
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Mirror self-recognition has been verified in several vertebrate species: gorillas,
Gorilla gorilla (PATTERSON et al. 1993); bottlenose dolphins, Tursiops truncatus,
(REISS & MARINO, 2001); killer whales, Orcinus orca (DELFOUR & MARTEN, 2001);
elephants, Elephas maximus, (PLOTNIK, 2006); human beings, Homo sapiens
sapiens, after 18 months of age (CARTER, 2008); orangutans, Pongo pygmaeus,
(LETHMATE & DÜCKER, 1973); birds, Pica pica, (PRIOR et al. 2008); chimpanzees,
Pan troglodytes, and bonobos, Pan paniscus (GALLUP, 1970; MILLER, 2009); rhesus
monkeys, Macaca mulatta, (RAJALA et al. 2010); pacific walruses, Odobenus
rosmarus, and beluga whales, Delphinapterus leucas (POLARI, 2013).
Many species have not yet been subject to any test for the expression of a conscious
self. Nonetheless, the interpretation of this phenomenon in diverse taxa has a great
biological value. Scientists have shown that environmental restrictions may cause
psychological damage that may lead to behavioural deficit in human and non-human
species. Animals with high cognitive capabilities, such as the capacity of processing
information of self-mental states and that of others, may have a higher risk to develop
psychopathologies and other mental syndromes (Sutker et al. 1991; Ladage et al.
2009; Marino et al. 2007; 2009; 2010; 2011; Grimm, 2011; Mason et al. 2013).
Therefore, specific management and handling techniques should be adopted when
individuals housed in captivity are potentially self-conscious. Animals kept in captivity
should be the prime candidates to serve as subjects for biological consciousness
studies. The results from these could inform specific legislation aiming to reduce the
negative impacts of captivity and/or to restrict the maintenance of species that would
suffer dire psychological consequences. Also it can improve management conditions
of housed species (cognitive enrichment).
Callithrix jacchus (Linnaeus, 1758), are commonly kept in captivity (Rylands et al.
2009) and are good models for cognitive behaviour studies. This species occurs in the
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Brazilian Atlantic forest, in the xerophytic scrub deciduous and semi-deciduous forest
of Northeastern Brazil (Caatinga) and in the Cerrado (Brazilian savannah) of central
Brazil. These marmosets are often found in urban parks, gardens and rural villages
because they are easily kept in captivity and targeted for wildlife traffic, to be sold as
pets. Indeed, given that common marmosets are keeps at the Primatology Center –
UFRN, and that convincing self-directed behavior was not described in front of a mirror
we decided to use them in the present work.
Dinoponera quadriceps are bred in captivity under controlled environmental
conditions and should be a good candidate model species for self-perception analyses,
due to their big body size which makes observation easy from a distance (Paiva &
Brandão, 1995). These ants are not socially dependent on queen castes (Peeters,
1987), and forage alone (Araújo & Rodrigues, 2006). Therefore, tocandiras are good
models to answer questions about the navigation mechanism that these ants use
during their foraging trips.
With well-established methods and protocols, such as the mirror test, and the
evaluation of other cognitive capabilities, and proper human, laboratorial and structural
resources, it is possible to answer questions about consciousness and awareness
expression in nonhuman animals, from invertebrate to vertebrate species. We
performed a series of cognitive tests to evaluate the expression of awareness in
tocandiras and common marmosets considering a constructive ethological approach
interpreting animals like individuals that enact individual worlds. We considered that
these animals occupy the environment not as simple living organisms or objects, but
as subjects that use their own senses to construct relations within the physical and
social environments where they interact (Delfour, 2010). Do marmosets recognize
themselves in the mirror expressing self-perception through self-recognition? Do ants
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know about their own location, taking shortcuts while heading back to the colony?
Answers are provided in the following two chapters.
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GENERAL OBJECTIVE
To evaluate self-perception behaviours in Callithrix jacchus and Dinoponera
quadriceps through different cognitive analyses, appraising conscious states in non-
human animals.
SPECIFIC OBJECTIVES
Evaluate C. jacchus capacity to self-recognition in the mirror;
Verify D. quadriceps capacity to self-perceive in the environment.
HYPHOTESIS
C. jacchus subjects can identify themselves in the mirror.
D. quadriceps are able distinguish their own location in the environment.
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CHAPTER ONE
THE MARMOSET IN THE MIRROR: A PROXY FOR CONSCIOUSNESS STUDIES
IN MONKEYS
POLARI, D.S.1,2; LOPES, L. C. 1; SOUZA, M.G.V. 1; SOUSA-LIMA, R. S. 1,2,3
1 LaB – Laboratory of Bioacoustics, Physiology Department, Biosciences Centre,
Federal University of Rio Grande do Norte, Natal-RN-Brazil.
2 Graduate Program in Psychobiology, Federal University of Rio Grande do Norte,
Natal-RN-Brazil.
3 Bioacoustics Research Program, Laboratory of Ornithology, Cornell University-USA.
Journal – Consciousness and Cognition – Elsevier (Qualis: A2; Impact Factor: 1.941).
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THE MARMOSET IN THE MIRROR: A PROXY FOR CONSCIOUSNESS STUDIES IN MONKEYS
POLARI, Daniel Silvaac*; LOPES, Lara Cunhaab; SOUZA, Marise Guipson ab; SOUSA-LIMA, Renata S.abcd
aLaboratory of Bioacoustics, Physiology Department, Federal University of Rio Grande do Norte, Natal-RN-Brazil.
b Undergraduate Program in Biological Sciences, Federal University of Rio Grande do Norte, Natal-RN-Brazil.
c Graduate Program in Psychobiology, Physiology Department, Federal University of Rio Grande do Norte, Natal-RN-Brazil.
d Bioacoustics Research Program, Laboratory of Ornithology, Cornell University. * Corresponding Author: Tel. +55 84 981611711
E-mail address: [email protected]
ABSTRACT Common marmosets, Callithrix jacchus, can be found in many Brazilian biomes, and also in urban centres across the country, as this species is commonly found in captivity. In this study we evaluated common marmoset capacity to discriminate the origin of the specular image in the mirror, comparing between mirror tests with and without a painted mark on the ear tuffs of the subjects. The mark was made with a non-permanent blue dye, and marking procedures were conducted with animals induced to an unconscious state, following procedures described in earlier studies with primates. Subjects aged between 3 and 6 years old and were born in captivity. Videotaped interactions between subjects and the mirror image were evaluated in two different types of tests: Mirror Test – subjects were exposed to a reflective surface; Mark Test – subjects hear tuffs were marked with blue dye (visualization of the mark was only possible with the help of a reflective surface). Each test type was evaluated in three different categories: category A, as a control trial without any external stimuli such as a mirror or any other object; category B, also a control, with a non-reflexive object of the same size of the test mirror; and category C, the effective trial, with a double-sided mirror. Results reported a series of self-directed behaviours such as contingency check, self-observation, mark reaction and the use of the mirror as a tool. We suggest that common marmosets show evidence of conscious mental states of themselves and thus of others, supporting mirror-self-recognition for non-ape primates.
KEYWORDS: Callithrix jacchus; self-directed behaviour; self; mirror-self-recognition; MSR; mark test; self-awareness; awareness; consciousness; animal consciousness.
HIGHLIGHTS
Self-awareness is proposed for Callithrix jacchus.
Contingency-checking behaviour was observed.
Results support self-awareness for non-ape species.
1. INTRODUCTION
The interpretation of consciousness phenomena in species other than humans can be tricky, since measuring subjective experience could be complicated by the eyes of an outsider. In the past four decades, a rush towards the understanding of consciousness resulted in a boom of studies from different scientific areas. In consonance, ethologists have used an experimental approach to provide conclusive evidence of conscious processing – The Mirror Test (Low et al. 2012). The use of a mirror to evaluate subject’s behaviour allows scientists to interpret how an animal perceives himself in the environment, leading to the identification of self-awareness
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hallmarks in species other than humans. Although, only in the XXI century, evidence of processing self and environmental data consciously from other mammal species became available (Gallup, 1970).
When comparing self-recognition among species, behaviour analyses relies on voluntary use of mirror for different aspects of self-evaluation. The failure of macaque monkeys to demonstrate MSR and the difficulties to replicate results of previously intentional species, suggests that the display of self-directed behaviours are dependent on subjects’ cognitive capacity. Toda & Platt (2015) suggests that macaques show cognitive abilities once thought to be uniquely shared by humans and great apes, such as gaze-following, vicarious reinforcement, hot-hand bias and metacognition. Authors also proposes that macaques failed in the mark test probably because of their performance instead of the absence of self-awareness.
In 1995, cotton-top tamarins, Saguinus oedipus, became the centre of a controversial study, in which Hauser et al. claimed their research subjects could recognize themselves in the mirror. However, Anderson & Gallup (1997) contested the authors’ findings and five years later, Hauser et al. (2001) exposed results of a new replication of their first study, in which different outcomes were found, putting in check their original evidence of mirror-self-recognition (MSR) for primates other than apes.
Other species of monkeys and lesser apes were also tested, but only in 2010 the first clear evidence pointed towards MSR in rhesus monkey, Macaca mulatta (Rajala et al. 2010). In this study five subjects that had contact with a mirror image, during most of their lives while as a tool for environmental enrichment, were confronted with their mirror image after receiving a head implant for behavioural/electrophysiological experiments. Rajala et al. found that those rhesus monkeys displayed mirror self-recognition, using the mirror to groom head implants and to inspect body areas otherwise invisible to them, such as their genitals. Before this study, scientists believed for decades that rhesus monkeys were not able to identify their own specular image, because mainly social behaviour was observed (Suarez & Gallup, 1986; Gallup & Suarez, 1991).
In 2015, Chang et al. was able to demonstrate that rhesus monkeys could acquire MRS behavioural displays following training with visual-somatosensory association. Trained monkeys learned to touch the marked spot in front of a mirror, also showing other self-directed behaviours such as smelling their fingers after touching the mark and exploring normally invisible body parts. The authors suggest a new approach on the study of neural MSR mechanisms, because apparently, the visual-somatosensory system can be trained, therefore multimodal sensory integration plays an important role in the self-recognition performance of a subject.
Common marmosets, Callithrix jacchus, were also tested in their capacity of MSR, but not enough evidence of self-directed behaviours was found (Heschl & Burkart, 2006). Nevertheless, subjects were able to distinguish the mirror as an impenetrable object and to use the reflex image as a tool for reaching hidden stimuli, overcoming the mirror fallacy at the same time as they perceived their own position in the environment. Heschl & Burkart did not evidenced other self-directed behaviours, however, the described action stand as an indicative of self and environmental information processing systems and may be interpreted as consciousness evidence, if we take consciousness as the processing of the information of the ongoing experience.
Considering that behavioural responses may be influenced by physiological, mental and environmental features and by extrapolating the salience hypothesis (Hauser et al. 1995) as proposed by Heschl & Burkart (2006), we appraised C. jacchus behaviour in different mirror conditions. Our study aimed to recognize subject’s capacity to discriminate the origin of the specular image, comparing mirror trials with and without
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a body mark of subjects there were not naïve to mirrors surfaces. For the body mark we have chosen a more conspicuous mark then previously tested (green dye and chocolate cream) and we predict that subjects can identify themselves in the mirror with and without the presence of a body painted mark, displaying different self-directed behaviours.
2. MATERIALS AND METHODS
2.1. Study Site The Project was developed in captivity at the Primatology Centre located in the
Campus of the Federal University of Rio Grande do Norte, Natal, RN, Brazil (Process number 02021000621/88-68 – IBAMA-MMA-BR). The centre is equipped with cages and special structures for the development of different experimental studies with primates, in particular common marmosets, Callithrix jacchus, with around 150 individuals. Animals are kept in social groups or alone, depending on ongoing research projects. Cages of different sizes are naturally enriched with tree branches to stimulate natural behaviour, as well as a small wood nest and sometimes a hammock. Chosen subjects were habituated to visual and tactile isolation and were kept in separate cages from August to December, 2015. Each cage had a glass wall with window tint that reflects the environment but not perfectly as a true mirror. Animals were fed twice a day, before trials, to ensure satiety in order to maintain a comfortable emotional state during the test (Heschl & Burkart, 2006). Trials were conducted in the and in the afternoon and in the morning.
2.2. Study Animals Subjects were captive born and selected between 3 and 6 years old. We evaluated
four different individuals: three males, Antero, born in January 2012, Frevo, born in November 2011 and Ariel, born in January 2012; and one female, Nilda, born in January 2012. To ensure animal welfare regulations were met, the present study was evaluated and approved by the ethics committee (approval number 024/2015 CEUA-UFRN).
2.3. Tests Types Behavioural analyses evaluated the interaction between subjects and the mirror
image. We provided individuals with specific access to different stimuli within a cage with dimensions of 60x100x80cm, made of wood walls and an acrylic ceiling to allow the entrance of light.
We evaluated behaviour in two different types of tests: 1) No Mark – subjects were exposed to a reflective surface without the presence of a body painted mark; 2) Mark – subjects were exposed to a reflective surface after a painted body mark was placed in an area only visible with the help of a mirror.
2.4. Test Categories Each test type was conducted in three different categories (figure 1), in the order
presented below, not randomly. These categories were comprised of three replicates of 10 minutes each, totalizing 30 minutes by category. Category A (empty) was a control trial where individuals were placed inside the experimental box under normal environmental conditions (i.e., without any external stimuli such as a mirror or any other object. Category B (object) was also a control, with individuals exposed to a non-reflexive object of the same size of the mirror used in the category C and at the same location. Category C (mirror) was the effective trial, where individuals had access to a double-sided mirror placed in the centre of the cage, measuring 50x2x60cm. In trials
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B and C, animals could jump back and forth over the top of the stimuli, since we left a gap of around 30 centimetres between the roof and the object/mirror.
2.5. Marking Procedures To avoid the perception of the marking procedure, animals were induced to
unconsciousness with Isoflurane at 3%, oxygenation at 0,8mL/min, in open Baraka circuit system, for 2 to 3 minutes following Ludlage & Mansfield (2003). A veterinarian conducted the marking procedures with the help of project researchers. After marking, individuals were left to recover in 5 to 10 minutes. After recovery, monkeys were then placed inside of the test box for behavioural evaluation.
Individuals were saliently marked in the ear tuffs with non-permanent, non-allergenic, odourless blue pigment used in professional make-up. The blue colour is visible for both genders, since male C. jacchus are dichromatic and females are trichromatic (Pessoa et al. 2005). Blue pigment also added higher contrast between the background and the animal, which may facilitate visual detection of the mark (Freitag & Pessoa, 2012). Besides, blue is a very uncommon colour in the species natural environment.
During trials, animals had both ear tuffs marked, one in white and the other one in blue (figure 2), alternating the coloured side in between trials. The white mark works as a sham mark as we expect that the individual focus his attention to the blue mark instead of to the white one. Both pigments are identical in composition and application, only varying in colour.
Figure 1. Aerial image of the inside of the test box, with different test sets of different
categories. In the photos it is possible to see the tested marmoset in the centre of the
box while interacting with the stimuli in categories B (centre) and C (right). Also, we
can observe the marmoset in the category A, without any stimuli inside of the test box
(Photograph: Daniel Polari).
Figure 2. Common marmoset marked in the
ear tuffs with blue (left) and white dyes (right).
(Photograph: Daniel Polari)
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2.6. Trials Record All trials were recorded with the help of professional audio and image equipment. Sounds were recorded with a Marantz PMD661 MKII Portable Flash Field Recorder and a Sennheiser ME66 Shotgun Microphone. Two different equipment, a GOPRO Hero 2 and a Nikon D7000 recorded video during each trial. After tests, image and audio information were synchronized using the platform Adobe Premiere CC and rendered in high quality for behaviour evaluation.
2.7. Behaviour Analyses To evaluate behaviour events, we have adapted an ethogram (table 1) based in previous MSR tests (Polari, 2013), separating events as effective (α) and control behaviours (β). For the definition of social behaviour events, we followed results published from Boer et al. (2013), together with possible events in which the subject would try to touch or hit the specular image with its own body parts. We assumed that such behaviours only would happen if the animal had the illusion that the reflex image was from another subject separated by an impenetrable transparent object. All trials were examined by three different observers in order to avoid any disparity of a single rater and to minimize data misevaluation. For proper ethological analyses, before the video evaluation, raters had more than 100 hours of direct contact with different monkeys while in social interaction and in isolation. Also to help discriminate between effective and control behaviour events, we evaluated individuals’ acoustic repertoire following the work of Bezerra & Souto (2008).
BEHAVIOUR EVENT DESCRIPTION
α1 - Contingency check
Move body parts subtly, frequently with rhythm, evaluating the contingency of the movement of the specular image.
α2 - Self-observation
Explore visually the specular image orientating body parts, sometimes during the execution of deliberated actions.
α3 - Effective mark
Observe, scratch, shake, touch or scrape the effective mark, before, during or after the visualization of the specular image.
α4 - Environment exploration Visually explore the mirrored surround, after looking to the specular image.
β1 - Interact socially
Interact with the specular image displaying social conducts as: hitting the mirror, approaching the face to the specular image, opening mouth while exposing teeth and arching bristles.
β2 - Mark controls
React to the sham mark observing, scratching, shaking, touching or scraping it, before, during or after the visualization of the specular image; react to the effective mark observing, scratching, shaking, touching or scraping it, without looking to the mirror and to the specular image.
Table 1. Ethogram adapted for Callithrix jacchus, to evaluate mirror tests with and
without a body painted mark. In the left, we have each effective and control behaviours
events, with specific codes and titles, followed by its description in the right.
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2.8. Statistical Analyses When appraising behaviour, each rater evaluated the frequency and the duration of
all behaviour events, by different test types and categories. To verify evaluators data consistency, we have run an inter-rater reliability test (3.1). Since behaviour data distribution was non-normal, non-parametric tests were run using SPSS v.23, considering an alpha ≤ 0.05. To evaluate the difference between effective (3.2) and control (3.3) behaviours, Kruskal-Wallis tests were run followed by Mann-Whitney post-hoc, using proper Bonferroni alpha correction.
3. RESULTS A video example of each reported behaviour is displayed annexed to the
supplemental material of this article. In the mirror category (C), subjects interacted with the specular image in a curious outlook, with all individuals displaying contingency check behaviours mainly in the first minutes of the first trials, reducing its frequency in the following replicates. Some subjects displayed side by side movements for many seconds, jumped from one side to the other while looking to the specular image, moved their heads up and down, in circles and side by side in the same behaviour sequence, moved and stopped abruptly and then moved again, often repeating this behaviour. In control category B (object), due to the similarity between some behavioural events, all raters registered a small number of behaviour similar to contingency check, which were non-legit α1, but was counted in final results. However, this data does not change the final statistical outcome. These events probably happened due to the presence of a new object in the test environment, with animal responding with sudden body movements while evaluating the stimuli.
Besides checking the contingency of the specular image, we also have registered self-observation behaviours such as subjects moving body parts slowly, grooming of its own tail and also defecating while looking to the specular image. In other instances, subjects started to scratch different body parts not looking to the mirror, and then suddenly turned to the mirror and looked directly to the specular image while scratching. Sometimes they also stopped and scratched again as if animals intentionally stopped moving their legs to see the reaction from the marmoset in the mirror. We have also observed events in which individuals would vocalize backwards to the mirror image, and then turned to visualize the specular image while in the middle of the vocalization.
Only phee vocalizations were registered. Since that phee is understood as contact calls, we considered that animals were vocalizing searching for answers of individuals from outside the test room, since that room was not 100% sound restricted and we have often registered concomitant phee calls from outsiders. Also, if an individual looked to the specular image while vocalizing, such behaviour was understood as self-observation, since it was often followed by different self-directed displays. Indeed, no social behaviour was registered simultaneously to a vocalization while looking to the specular image.
We observed a significantly smaller frequency of effective (α) behaviours in test type 1 when compared to test type 2. Therefore, it seems that the body mark may have stimulated self-directed behaviour to the specular image. In the mark test, individuals did not touch the mark with their hands, still, all raters have registered subjects scratching the mark with their legs (α3). These events were not exclusive to the category C (mirror) and were registered as mark control (β2) measures. However, we have observed individuals shaking their heads right after looking to the specular image and direct looks to the mark using the mirror, events considered as effective mark reactions (α3).
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Environment exploration (α4), as opposed to contingency check behaviours, increased in frequency within time. Apparently, animals were able to overcome the mirror fallacy and explore their reflected surroundings as trials progressed. We also observed a series of self-observation (α2) events, which consisted as direct looks to different body areas such as legs, abdomen, arms, back and tail, from all individuals.
Pooling all trials with the mirror, social behaviours were also observed, with animals trying to reach the mirror image with their nose. Also the female subject, Nilda, displayed a sequence of five behaviour events that suggests that it was trying to reach the monkey in the mirror through the gap between the stimuli and the box floor. Also, one male, Frevo, was observed attacking his own reflex in four separate events, hitting the mirror with his hand. In another instance, another male, Antero, while sniffing its own poop, looked to the mirror image and got spooked for a moment, as if it had seen another individual, however, right after that, Antero behaved with a series of contingency check to the mirror.
Also we have observed individuals that reacted by scratching the marks (sham or effective mark) while not interacting with the specular image. Scratching was a frequent event during mark test trials, although this behaviour was also observed in other test categories, however. Scratching is a common behaviour in mammals, normally as a reaction of itching caused by ectoparasites. Additionally, a likely explanation to these observations would be an allergic reaction to the anaesthetic that was only used in the test type 2. Apparently, self-scratching has no clear social function but it is related to individual anxiety (Cilia and Piper, 1997). There is also suggestion that self-scratching may send a negative emotional message to conspecifics (Watson, 2011). Nevertheless, we discard these alternatives explanations as scratching was directed only to the effective (blue) mark and not to the shame mark while looking to the mirror.
3.1. Inter-rater Reliability Test The evaluators data from marmosets’ behaviour reported a positive reliability with
an alpha of .70 for frequency and .70 for duration. In other words, 70% of the observed variance of monkeys’ behaviour was significant and consistent.
3.2. Effective (α) behaviour in test type 1 (no mark) and 2 (mark). Statistical analyses reported significant differences between the category C (mirror)
and both control categories, A (empty) and B (object), in test types 1 (frequency: H2 = 198.969, P = 6.2286 -44; duration: H2 = 200.960, P = 2.3016 -44) and 2 (frequency: H2 = 201.089, P = 2.1584 -44; duration: H2 = 198.969, P = 6.2286 -44). There were no significant differences between categories A and B. Results are detailed in table 2 and displayed in figure 3.
Figure 3. Total time (seconds) of effective behaviours (α) in test types 1 (no mark) and
2 (mark), by frequency and duration. It is possible to visualize the differences between
control categories A (empty) and B (object), with the effective category C (mirror).
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We verified that effective behaviour events, separately, showed significant differences in frequency (H2 = 120.653, P = 6.3169 -27) and duration (H2 = 119.858, P = 9.4025 -27) between category C and controls A and B (table 3). Results are presented in figure 4 and are detailed in table 3.
3.3. Control Behaviour (β) in test types 1(no mark) and 2 (mark)
Significant differences were observed in test type 1 (frequency: H2 = 14.397, P = 0.001; and duration: H2 = 14.397, P = 0.001) between category C (mirror) and controls B (object) and A (empty). No significant differences were verified in test type 2 by frequency (H2 = 2.591, P = .274) and duration (H2 = 2.754, P = .252). Frequency and duration values were similar, because events lasted less than one second. Results are detailed in table 2.
Figure 4. Total time (seconds) of effective behaviours – contingency check (α1), self-directed (α2), effective mark (α3) and environment exploration (α4) – in test types 1 (no mark) and 2 (mark), by frequency and duration.
TYPE 1 (NO MARK)
Mirror Mirror
TYPE 2 (MARK)
Mirror Mirror
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When evaluating each control behaviour separately, significant differences were found for social behaviour (β1), by means of frequency (H2 = 23.107, P = 0.000) and duration (H2 = 22.666, P = 0.000). No significant differences were found for mark controls (β2). Results are presented detailed in table 3.
4. DISCUSSION
Our results showed a different progression pattern of behavioural responses to the specular image from those described by Gallup (1970). That author showed that chimpanzees initially behave socially towards the specular image, but with time, subjects began to respond with self-directed behaviour towards their own image. Gallup describes two stages of mirror responses during the 10 days’ experimental period. Stages were: 1) social behaviours towards the specular image and 2) self-directed behaviour to body parts that are invisible without the help of a mirror. We observed a switched progressive pattern for common marmosets, then what Gallup related for chimpanzees. Animals showed contingency check displays followed by self-observation, and social behaviour was only registered after the mirror fallacy was already overcome. Our results suggest that marmosets possibly can recognize the mirror image as themselves, since we reported a short number of social behaviour towards the specular image. We suggest that their conceptual self-image is not developed enough to trigger ape like behaviour, therefore limiting species performance towards the exploration of its own image. Thus, it is clear to us, that this continued contingency check, followed by significant numbers of self-directed behaviours, is, in itself, evidence of some level of self-awareness.
Also, this is the first evidence of contingency check behaviours to the specular image, data registered for all studied subjects. Heschl & Burkart (2006) did not observe such behaviour at all. For an animal to be able to verify the contingency movement of the specular image, a subject has to understand its own body parts and its positions in the environment, simultaneously while in control of its own body. Such behavioural characteristics are related to a self-processing system as suggested for other species that positively passed the mirror test (Delfour & Marten, 2001; Polari, 2013).
To address this analytical caveat, as proposed by Gallup, we appraised the mark test, but no direct hand-mark touch was observed, differently from apes. However, other reactions to the mark were register, such as scratching it with the feet, directly looking at it and shaking the head after looking to the specular image. Additionally, our study animals were born in captivity and are constantly manipulated by veterinarians and keepers. Therefore, individuals may tend not to overreact to the presence of a painted mark in their bodies, since they are often subjected to different medical procedures that may require the use of different substances in their fur and body parts, habituating them to body mark alterations. Therefore, we suggest that our results may be less than obvious in these habituated subjects. Also previous work points out that, even with the presence of a sticky cream (Nutella®) in their heads, common marmosets do not necessarily use their hands to reach the unusual sticky area. Animals rubbed their heads in different surfaces but did not reach the stick cream with their hands (Heschl & Burkart, 2006).
Our results show that C. jacchus reacts to the mark, although in subtler ways than observed for apes. That leads us to question: why should marmosets scratch the marked area using their hands instead of using their feet? We suggest that the size of marmoset brain may hinder higher body control, triggering reactions to the face not too much differently as if to any other body area. Begun (2015) suggests that apes, with bigger and more complex brains, have developed a fine control of the face and the extremities such as hands and fingers, which would naturally trigger reactions to a facial mark differently from possible reactions of species with a smaller brain size and
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specialization. Our test individuals reacted more objectively towards the mirror, not in a progressively complex behavioural continuum as registered in chimps and dolphins (Reiss & Marino, 2001). Dolphins flip in front of the mirror and open their mouths, as observed in apes (e.g., Gallup 1970). However, our study subjects displayed interesting behaviour in front of the mirror such as scratch and groom body parts looking to the specular image in a very detailed manner and observe their own legs, feet, hands, back and tail. We suggest that the mark test should be better explored in the future, using more salient marks, or marking a larger part of the subjects, in order to promote more specialized behaviour that could help validate our results.
The interpretation of Heschl & Burkart (2006) work with common marmosets marked with Nutella® on their forehead, pointed that individuals could not distinguish the specular image as themselves, because they tried to lick the chocolate cream directly of the reflex. For the authors, this behaviour was a strong evidence that marmosets fail to pass the mark test. However, such interpretation could be argued otherwise. Trying to lick chocolate from any area is only an evidence of a misdirected behaviour motivated by an extremely attractive olfactory clue, probably a matter of self-control. We think that the Nutella® olfactory trigger, led individuals to ignore the specular image while trying to reach the food that was visually available in the first plan. That is possible to interpret while checking authors description of the case: “When approaching the image of their marked forehead, the animals arrived at the upper edge of the mirror where the desired goal, the chocolate spot, suddenly disappeared. They then withdrew slightly, rediscovered the goal in the mirror and tried again in vain to reach the chocolate with their tongue.” (Heschl & Burkart, 2006 - page 195).
Consciousness is directly linked to social awareness, since one’s own perception is the starting point for the awareness of others (Premack, 2007; Graziano, 2013), as one’s perceive itself as a separate entity from others and from objects, as active individuals that modify its own environment. From that we can speculate that self-recognition may be commonly present, specially, in higher social species such as common marmosets. Also, the recognition of others, may be related to the identification of familiar subjects not only by visual and chemical signals, but by using sound as an important mechanism for communication. C. jacchus vocal repertoire comprises of at least 13 different calls (Bezerra & Souto, 2008) and individual vocal signatures, has also been shown for the species (Jones et al. 1993). Future studies may consider looking at other sensory modalities and the development of protocols to address the presence of conscious states, evaluating behavioural traits more specific to each particular species, considering its cognitive capabilities or the lack of it.
Mirror self-recognition was confirmed for apes and possibly for rhesus monkeys, Macaca mulatta (Rajala et al. 2010; Chang et al 2015), although Anderson & Gallup (2015) do not find it convincing enough. Marmoset and tamarins are typically organized in groups with female dominance (Dewey, 2008) and exhibit complex social interactions. Rhesus monkeys belong to the Cercopithecidae family that comprises species also dependent on social behaviour, also presenting more developed facial muscle control than marmosets, which could play an important role in social relations (Myers, 2000). In primates, facial expressions can be an important sign for recognizing self-awareness. However, other animals also with complex social relations, such as different species of dolphins, do not have such controlled facial expressions, which leaves a complicated task for scientists to interpret mirror self-recognition behaviours. Yet, positive results of MSR for other species than monkeys were reported (Delfour & Marten, 2001; Reiss & Marino, 2001; Plotnik et al. 2006; Prior et al. 2008; Polari, 2013). This lead us to question: can self-recognition be present as result of a convergent evolutionary mechanism among different species in the tree of life?
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Here we present additional evidence of mirror self-recognition for a primate species that are more phylogenetically distant from apes. This may be evidence that self-awareness origins in primates, are derived from marmosets’ ancestors. Macaca and Calllithrix are derived from the same ancestor in between the divergence of the parvorder Catarrhini, old world monkeys, and the parvorder Platyrrhini, new world monkeys (Springer et al., 2012). If the evolution of self-awareness can be traced by phylogeny, there is a possibility that the roots of self-recognition may be traced back, at least, to the common ancestors of Catarrhini and Plattyrrhini.
Coming from another perspective, recent studies from phenomenology suggest that consciousness experience is ongoing in forms of integrated information (Tononi, 2004). However, could we observe different types of consciousness expression between different species? Panksepp (2005) suggests that primary consciousness (the feeling of oneself experience as a dynamic proxy in the perceived reality) seems to be a fundamental natural condition rather than a developed expertise, and as an intrinsic function of the brain should be present in all mammal species, at least. Indeed, since self-awareness in marmosets has been shown here and may be used as a cross-validation evidence of a mental attribute of the own self and thus of others (Anderson & Gallup,1997), we conclude that common marmosets are not genuine zombies and probably express conscious mental states.
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39
6. ANEXX
Table 2. Statistical results of effective (alpha) and control behaviours (beta), by means of frequency and duration in different categories and test types (significant values are highlighted in bold letters).
Type Categories Behaviour Frequency Duration
1
Mirror Vs Empty α U = 4076, Z = -10.651, P = 1,7233 -26, r = 0.36 U = 4248, Z = -10.744, P = 6.3296 -27, r = 0.37
β U = 2340, Z = -2.702, P = 0.007, r = 0.02 U = 2340, Z = -2.702, P = 0.007, r = 0.02
Mirror Vs Object α U = 4008, Z = -10.839, P = 2.2426 -27, r = 0.37 U = 4337, Z = -10.505, P = 8.175 -26, r = 0.36
β U = 2340, Z = -2.702, P = 0.007, r = 0.02 U = 2340, Z = -2.702, P = 0.007, r = 0.02
Empty Vs Object α U = 10226, Z = -0.706, P = .480, r = .00 U = 10155, Z = -1.130, P = .259, r = .00
β U = 2592, Z = - 0.000, P = 1.000, r = 0.00 U = 2592, Z = - 0.000, P = 1.000, r = 0.00
2
Mirror Vs Empty
α
U = 4340, Z = -10.502, P = 8.4554 -26, r = 0.36 U = 4337, Z = -10.505, P = 8.175 -26, r = 0.36
Mirror Vs Object U = 4248, Z = -10.746, P = 6.1557 -27, r = 0.37 U = 4248, Z = -10.744, P = 6.3296 -27, r = 0.36
Empty Vs Object U = 10224, Z = -1.417, P = 0.157, r = .00 U = 10224, Z = -1.417, P = 0.157, r = .00
40
Table 3. Statistical results of different behaviour types (effective – α, and control – β), by means of frequency and duration, in different categories.
Categories Behaviour Frequency Duration
Mirror Vs Empty
α1 U = 669, Z = -8.663, P = 4.5774 -18, r = 0.06 U = 678, Z = -8.619, P = 6.7285 -18, r = 0.06
α2 U = 756, Z = -8.583, P = 8.9911 -18, r = 0.06 U = 756, Z = -8.583, P = 9.2554 -18, r = 0.06
α3 U = 2264, Z = -2.841, P = 0.004, r = 0.02 U = 2266, Z = -2.824, P = 0.005, r = 0.02
α4 U = 468, Z = -9.524, P = 1.6725 -21, r = 0.06 U = 468, Z = -9.522, P = 1.6963 -21, r = 0.06
β1 U = 2119, Z = -3.561, P = 0.000, r = 0.02 U = 2124, Z = -3.527, P = 0.000, r = 0.02
β2 U = 2564, Z = -0.190, P = 0.849, r = 0.00 U = 2544, Z = -0.326, P = 0.744, r = 0.00
Mirror Vs Object
α1 U = 698, Z = -8.457, P = 2.7406 -17, r = 0.06 U = 701, Z = -8.441, P = 3.1405 -17, r = 0.06
α2 U = 756, Z = -8.586, P = 8.9911 -18, r = 0.06 U = 756, Z = -8.583, P = 9.2554 -18, r = 0.06
α3 U = 2232, Z = -3.264, P = 0,001, r = 0.02 U = 2232, Z = -3.264, P = 0,001, r = 0.02
α4 U = 468, Z = -9.524, P = 1.6725 -21, r = 0.06 U = 468, Z = -9.522, P = 1.6963 -21, r = 0.06
β1 U = 2119, Z = -3.561, P = 0.000, r = 0.02 U = 2124, Z = -3.527, P = 0.000, r = 0.02
β2 U = 2564, Z = -0.190, P = 0.849, r = 0.00 U = 2544, Z = -0.326, P = 0.744, r = 0.00
Empty Vs Object
α1 U = 2522, Z = -0.705, P = 0.481, r = 0.00 U = 198, Z = -0.690, P = 0.491, r = 0.00
α2 U = 2592, Z = 0.000, P = 1.000, r = 0.00 U = 2592, Z = 0.000, P = 1.000, r = 0.00
α3 U = 2556, Z = -1.000, P = 0.317, r = 0.00 U = 2556, Z = -1.000, P = 0.317, r = 0.00
α4 U = 2592, Z = 0.000, P = 1.000, r = 0.00 U = 2592, Z = 0.000, P = 1.000, r = 0.00
β1 U = 2592, Z = -0.000, P = 1.000, r = 0.00 U = 2591, Z = -0.000, P = 0.992, r = 0.00
β2 U = 2360, Z = -1.429, P = 0.153, r = 0.00 U = 2366, Z = -1.138, P = 0.165, r = 0.00
41
Video 1. Behaviour example of each effective (α), and control (β) behaviour types.
42
CHAPTER TWO
RELIABLE MODEL SPECIES, NOT ZOMBIES: APPROACHING INVERTEBRATE CONSCIOUSNESS USING SELF-REFERENT BEHAVIOUR DURING FORAGING TRIPS
POLARI, D.S.1,2; LOPES, L.C. 1; SOUSA-LIMA, R. S. 1,2,3
1 LaB – Laboratory of Bioacoustics, Physiology Department, Federal University of Rio
Grande do Norte, Natal-RN-Brazil.
2 Graduate Program in Psychobiology, Federal University of Rio Grande do Norte,
Natal-RN-Brazil.
3 Bioacoustics Research Program, Laboratory of Ornithology, Cornell University,
Ithaca-NY- USA.
Journal – Journal of Comparative Psychology– Elsevier (Qualis: B1; Impact Factor:
2.344).
43
RELIABLE MODEL SPECIES, NOT ZOMBIES: APPROACHING INVERTEBRATE
AWARENESS USING SELF-REFERENT BEHAVIOUR DURING FORAGING TRIPS
POLARI, Daniel S.ac*; LOPES, Lara C.ab; SOUSA-LIMA, Renata S.abcd
aLaboratory of Bioacoustics, Physiology Department, Federal University of Rio Grande do Norte, Natal-
RN-Brazil.
b Undergraduate Program in Biological Sciences, Federal University of Rio Grande do Norte, Natal-RN-
Brazil.
c Graduate Program in Psychobiology, Physiology Department, Federal University of Rio Grande do
Norte, Natal-RN-Brazil.
d Bioacoustics Research Program, Laboratory of Ornithology, Cornell University, Ithaca-NY-USA.
* Corresponding Author: Campus Universitário – Centro de Biociências, UFRN, Natal, RN, Brazil | E-
mail address: [email protected] | Tel.: +55 (84) 98161-1711 | Financial support: CAPES –
Education Ministry – Brazil.
ABSTRACT
Different species use different stimuli to navigate. Once awareness arises through an integrated
information processing system, some connected behaviour patterns, used by different species
of insects such as bees and ants while navigating, suggests such mental states for invertebrate
species. Therefore, we explored how individuals of Dinoponera quadriceps returned to the nest
after collecting food, evaluating if individuals took a return path equal or different from the
search path. Also, we measured the relation between the search and return paths with controls
paths linked to the shortest-possible-route between the food and the nest entrance. Tests were
conducted in 3 categories with different stimuli between the food source and the nest: A) no
obstacle; B) opaque obstacle; and C) clear obstacle. Our results suggest that ants were able to
calculate short-paths between the nest entrance and the food source, even in the presence of an
obstacle between the food source and the nest entrance. While returning to the nest with the
resource, individuals moved as if following different routes from those chosen in the search
path. Apparently, subjects can process information from its surrounding while locating itself in
the environment. Therefore, we conclude that D. quadriceps are a reliable model species for
studying consciousness expression and cannot be considered a genuine zombie.
44
KEYWORDS: Animal awareness; Dinoponera quadriceps; self-awareness; self-location;
foraging motion; ant; zombies.
INTRODUCTION
Psychobiology considers that consciousness displays itself during different cognitive
behaviours and it is related to diverse mental states (Hochberg, 1970; Atkinson and Shiffrin,
1971; Shallice, 1972; Posner and Klein, 1973; Mandler, 1975; Searle, 1997; Chalmers, 2013;
Tononi, 2004). However, in the last decade, emerged from phenomenology a theory suggesting
that consciousness is expressed in all integrated information systems, in different scales
(Tononi, 2004). Therefore, to assume that species are unconscious, as a genuine zombie (Tye,
1995; Allen-Hermanson, 2008; Humphrey, 2012), is to accept not only that such organisms are
deprived of perceiving its interaction with the socio-environment, but also to accept their
inability to integrate sensory information. Examples of zombies are not clear in the tree of life,
although there is disagreement and one could argue that tropism reflects zombie like features
(Tye,1995). Contrastingly, even phylogenetically distant species may express conscious states
by: mentally representing self and others; the use of memory for cognitive processing;
conscious judgment; decision making; problem solving; the use of language; and other
cognitive capabilities (Edelman et al. 2005; Panksepp, 2005; Marino et al. 2007; Mather, 2008;
Low et al. 2012; Polari, 2013).
Remarkable behaviours commonly displayed by invertebrate species are not expected from
genuine zombies. Invertebrates not only integrate information but process and respond by
innate and controlled behaviour (Mather, 2008; Low et al. 2012). Since invertebrates largely
lack legal protection actions for management and for conservation of their populations
(Andrews, 2011), carrying out studies that seek to bring to light the knowledge about
consciousness in nonhuman animals will have great impacts in animal welfare.
Some invertebrate species rely on a navigational system that would help them to move across
the environment in two main types of motion, the search and the return to the colony (Araújo
45
& Rodrigues, 2006). That system would help, for example, a subject to choose among different
routes between the resource location and the nest such as shortcuts and new routes. Therefore,
ants and bees navigate using shortest distances between targets (Wehner & Menzel, 1990).
Thus, we can speculate about these species self-awareness capacity. Can we use foraging
motion data as a cross-valid attribute of a self?
Wehner & Menzel (1990) pointsout that in long-distant travels, insects guide their navigation
by integrating information from the environment, which takes into account the celestial cues,
distance estimates between targets and visual memories accessing environmental landmark
images, which would allow it to compute shorter paths. In the other hand, while in short-range
displacement, when an individual is close to the target, it may be able to use different clues
such as the angular position the object, the visual recognition of smaller traces and the
discrimination of patterns from different objects, for example, from flowers (Giurfa & Menzel,
1997). In both cases, it is information processing that enables the efficiency in foraging through
a correct guidance while navigating. Therefore, we think that Dinoponera quadriceps is a good
model species to study such self-reference traits because: they have a large body size which
enables observation from a distance (Paiva & Brandão 1995); they are not socially dependent
on queen castes, enabling flexible behaviour (Peeters, 1987); and individuals do not recruit
others for searching for resource, instead they forage alone (Araújo & Rodrigues, 2006).
Therefore, the present work investigated how individuals of D. quadriceps return to the nest
after collecting food. Do they follow clues from the initial journey, returning to the nest in a
similar way? Or do they follow the shortest-possible-route between the food and nest, by
locating themselves in the environment with clues other than the direct vision of the nest? Are
ants a reliable model to study consciousness expression or are they genuine zombies? We
hypothesise that, when exploring the environment for resources, ants use different routes the
search and the return paths. Also, we expect that the return path will be a shortcut between the
resource and the nest entrance.
46
MATERIALS AND METHODS
STUDY SITE
Tests were conducted at the Laboratory of Behavioural Biology – in the Biosciences Center,
Federal University of Rio Grande do Norte, Natal, RN, Brazil. In the laboratory, D. quadriceps
colonies are kept in captivity under controlled environmental conditions of temperature and
light. Animals are fed with fruits and insects three times a week. The amount of individuals
varies between colonies. Nests are made of wood walls and are covered with a transparent
plastic plate, allowing inside visualization. Each colony is comprised of a foraging arena,
limited by wooden walls and open at the top with the ground covered with sand. This arena is
enriched with natural elements such as rocks, sticks, leaves and seeds. The nest of the studied
colony had, from the colony entrance to the arena wall a rectangle of 50x64cm. The tests were
conducted in the morning, approximately at 10:00 am, when these ants are most active
(Medeiros et al. 2014).
STUDY SPECIES
Dinoponera quadriceps (Kempf, 1971) is a Ponerinae endemic species from Brazil,
occurring within a polygon that encompassed areas of severe droughts in northeast Brazil. The
epithet “quadriceps” was given to differ the species from Dinoponera mutica, as D. quadriceps
possesses a duller abdomen and a petiole with an anterior extremity narrowly rounded and a
posterior extremity widely rounded (Kempf, 1971). Their body size varies from 3 to 4 inches
(Paiva & Brandão, 1995) and the species does not form queen castes; whereas workers, called
“gamergates”, reproduce (Peeters, 1987), nests on the ground and forage alone (Araújo &
Rodrigues, 2006).
The study was developed at the laboratory of Behavioural Studies – Physiology Dept.,
UFRN, Brazil, with one colony of 11 individuals. During our test trials the colony was fed with
fruits mixed with honey, in order to ensure engagement in foraging behaviour, following
laboratory standard routine. Ants colony were fed two to three times a week, therefore been
47
subjected to food restriction for 48 hours. The colony was already habituated to the laboratory
environment and to food restriction. Environmental changes to the nest happened only during
trials, with the adding of a petri dish with the food and of an object that blocked direct access
to the food.
ETHOLOGICAL TESTS
Behavioural analyses consisted in the evaluation of workers, while outside the nest, foraging.
We recorded the route taken by all individuals that searched food and returned to the colony,
however our data did not consider individual separately. Tests were divided into 3 categories
which are detailed in figure 1. Categories differ according to the placement of an obstacles
between the food plate and the nest entrance and were presented in the following order: no
obstacle (A), opaque object (B), and clear object (C). Each category comprehended five
replicates of 30 minutes each, totalizing 150 minutes for each category. The food source and
the object were placed in the arena at the same time. The object consisted of a 500x80x4mm
glass plate. In category B, the glass plate was covered with white paper, in order to block the
direct vision of the nest entrance right from the food. The object and the petri dish with food
was placed in the arena at different locations in each trial.
Figure 1. Virtual scheme, demonstrating the different categories, in which environmental
circumstances differ from the addition of and opaque and a transparent object. In red it is
highlighted the nest entrance (X) and the resource (Y). At the left image (category A), the total
distance between the nest entrance and the left wall of the arena is described.
48
Video images of the colony arena were recorded with a GOPRO Hero 2. Afterwards, video
information was edited and rendered in Adobe Premiere CC platform, where behavioural events
were divided into search (the moment an individual leaves the nest until the moment it reaches
the food source) and return (the moment an ant holds the food until it returns to the nest
entrance). Instances where animals did not find or did not take food were removed from the
analyses.
To evaluate the relation of the return route with short-paths between the food and the nest,
three control return paths were virtually measured by image manipulation. The total distance of
each control path was measured using the arena dimensions’ data. Examples of these paths are
displayed in figure 2. These control paths were created as if individuals were searching for a
shortcut between different points around the food plate. Control 1 was calculated starting from
one of the sides of the food source, concatenating vectors to obstacles in the arena. Control 2
was similarly calculated starting from the opposite side of control 1. Control mean was
calculated averaging the distances of control 1 and 2. We have also calculated the shortest-
path, which was measured using vectors from the middle border of the food plate (Y in figure
2) that targeted obstacles in the arena towards the nest entrance (X in figure 2).
Figure 2. Virtual scheme that demonstrates different
calculated controls examples in an event from the category
A. In the blue color, we can see the control 1 example, the
shortest possible route between the nest entrance (X) and
the resource location (Y). Control 2 can be seen in yellow,
as an example of the vectors that starts from one of the sides
of the food source; Control 3 is represented in purple, as a
possible route taken from the opposite side of control 2.
49
After trials, behavioural events were rendered in separate video files. Individual routes were
automatically calculated with the help of the ZebTrack algorithm (Pinheiro-da-Silva,
submitted), that runs in Matlab environment (The Mathworks). ZebTrack was able to measure
individual paths, calculating the total distance covered by each subject during the events of
search and return.
STATISTICAL ANALYSES
We tested the difference between the total distance of search, return, shortest-path, control
1, control 2 and control mean, between categories no obstacle, opaque and clear using SPSS
v.23. Data distribution was not normal, therefore, non-parametric Kruskal-Wallis and Mann-
Whitney test were run with proper Bonferroni alpha correction.
RESULTS
Examples of some of the paths used by the ants are displayed in figure 3, during categories
A, B and C. Our results suggest that ants used short-paths while returning to the colony after
obtaining food. In all trials, ants went out of the nest and randomly searched around the arena
until finding the food, then took some with their mandible and returned right back to the nest.
While returning, ants used a different path than those used in the search phase. However, a few
times we observed that animals got lost while trying to return to the nest. When lost, these
individuals started a behaviour pattern of moving around the food plate area, as if it was trying
to find the right landmark to return. In those cases, the search path was shorter than the return
path. Even so, the differences between the search and return paths were significant (table 1).
The majority of individuals returned to the nest right after finding the food, however a few
subjects spent time eating the food before heading back to the nest. The mix of fruits and honey,
apparently, elicited the consumption before getting the food to the colony. Even after minutes
eating the food, animals returned straight back to the nest, suggesting that the elapsed time
between the moment of finding the food and the moment of getting back to the colony, do not
influence its ability to navigate. Also, apparently, other ant’s pheromones or the nest odour
50
were not used as indicatives clues of the colony direction. Since search paths were commonly
random, possibly, pheromones were spread all around the arena. Therefore, pheromone clues
seem as a feeble indicative of the direction of the nest from the resource.
Figure 3. Paths of search (black), and return (green)
of one individual of D. quadriceps, generated by
Zebtrack software, in the test categories A (left), B
(centre) and C (right). return route between the nest
entrance (X) and the resource location (Y).
51
When we evaluated the mean distances of the routes taken by ants, we reported significant
differences between search and return by different categories, as displayed in figure 4.
As expected, Mann-Whitney results showed significant differences between control paths
with shortest-route, since controls 1 and 2 tended to have higher distance medians. When we
compared the return path with the shortest route, all categories reported significant differences,
which means, specifically, that individuals did not take the shortest-path between targets. Also,
post-hoc results demonstrates that no obstacle between the resource and the colony, apparently,
did not motivate navigation through the shortest-path, with animals probably using visual
discrepancy of environmental clues for navigation. However, return paths were different from
control 1, control 2 and control mean in categories B and C. It seems that an object blocking
the access of targets, influences ants’ navigation between its location and their goal. Results are
displayed by different categories in the figure 5. Statistical results are available in table 1.
Figure 4. Graphic image with the median distances between search and return behaviour types
in different tested categories.
SEARCH
RETURN
52
DISCUSSION
Our results suggest that Dinoponera quadriceps are able to get straight back to the nest after
collecting food. Results suggest that a blockage to the nest entrance do not prevent an individual
of choosing a return path similar to the shortest-route. Also, direct visual perception of the nest
entrance through a clear object did not seem to interfere in the return path chosen by subjects,
with individuals following shortcuts to the nest. Apparently, the object as enough stimuli to ants
navigate taking shortcuts.
Other behavioural evidence in invertebrates’ species are presented by Whener & Menzel
(1990). The results from these authors shows that, while foraging, bees and ants always know
about their position in relation to the starting point of its navigation. The authors also show that
different species of Hymenoptera uses different mechanisms to process information about an
objective’s direction while navigating. Such mechanisms would be part of an integrating path
system, in which individuals would use different environmental visual clues to navigate, such
as the skylight compasses for measuring directions and the use of visual memory. This memory
would allow the access to snapshots taken of the landmark panorama between the nest entrance
and the food.
Figure 5. Graphic image with the average distances of return and control types, by different
test categories. It is shown higher means in the opaque category, in comparison to
transparent. Empty category presents the smallest distances between 60 to 40 cm.
53
The simple fact that these individuals behave as if they knew where to go in the course of
the return path may be the evidence of a self-information processing system that could trigger
subjects’ behaviour while choosing a route. Therefore, sensory visual system might be engaged
in the path integration processes as proposed by Azevedo et al. (2009). They showed that
individuals of D. quadriceps navigate using vision as an essential source for assessing
environmental clues. In the same work, the authors also showed that individuals use short-paths
while returning to the nest in natural environment.
Other species show different ways to process spatial information. The German wasp Vespula
germanica, uses the sun as a sky compass (Jacobs-Jessen, 1959); the paper wasp, Polistes
gallicus, relies mainly in the precision of the initial orientation at the release point, processing
visual information during displacement. The use of different environmental visual inputs for
navigation demonstrates how flexible invertebrates are when processing interconnected
information (Wehner & Menzel, 1990). From a subject’s point of view, to locate itself, it is
necessary to relate its owns body somatosensory information, as a separate individual in the
environment.
Once awareness arises from an integrated information processing system, the studied species
showed specific behaviour that suggests mental mapping systems, probably with ganglions that
work as processors of signs (Gallistel, 1998). Gronenberg et al. (2008) suggests that other
environmental clues such as air currents, gravity and acceleration, besides the sense of touch,
may play a major role on individual movements. These authors also suggest that the social
context of ants and bees affects not only individuals’ behaviour but the neurobiological bases
of that behaviour, the brain itself, with ants’ functional roles shaping their motor output.
D. quadriceps appear to be a reliable model to study consciousness expression, since they
display interesting cognitive behaviour described in this work and those of others (Gould, 1986;
Wehner & Menzel, 1990; Giurfa & Menzel, 1997). There is evidence that other species of ants,
wasps and bees are able to process information about others, recognizing nest mates (Stuart,
54
2000; Leopold & Rhodes, 2010; Boos and d'Ettorre, 2012; Esponda & Gordon, 2015).
Furthermore, if consciousness is expressed in integrated information systems, we can start to
question how such data is managed? Which kinds of processing are we investigating when
studying invertebrate behaviour? Can invertebrates rationalize about self and others? How is
this hypothesized processing capability distributed along invertebrate phylogeny?
Invertebrate neurological simplicity, compared to bigger and more complex brains of
vertebrates, apparently do not inhibit individuals to handle complex tasks. However, our results
suggest that invertebrates may be self-aware, therefore expressing consciousness states of
perception. That uncovers the importance of rethinking our scientific, ethical, and moral issues
involving invertebrate species.
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57
ANEXX
Table 1. Statistical results of the comparisons between distances of different routes taken by D.
quadriceps, with significant differences in bold letters.
CATEGORY COMPARISON STATISTICAL RESULTS
No obstacle
statistical differences H5 = 83.191, P <<0.001
search vs return U = 8, Z = -5.908, P = 3.4593 -9
return vs shortest-route U = 100, Z = -4.146, P = 0.001
return vs control 1 U = 173, Z = -2.721, P = 0.007
return vs control 2 U = 142, Z = -3.326, P = 0.001
return vs control mean U = 152, Z = -3.131, P = 0.002
Opaque
statistical differences H5 = 45.721, P = 1.035 -8
search vs return U = 4, Z = -4.319, P = 0.001
return vs shortest-route U = 28, Z = -3.241, P = 0.001
return vs control 1 U = 70, Z = -1.297, P = 0.195
return vs control 2 U = 47, Z = -2.361, P = 0.019
return vs control mean U = 48, Z = -2.315, P = 0.021
Clear
statistical differences H5 = 88.697, P = 1.2619 -17
search vs return U = 44, Z = -5.855, P = 4,7683 -9
return vs shortest-route U = 147, Z = -4.275, P = 0.001
return vs control 1 U = 337, Z = -1.305, P = 0.192
return vs control 2 U = 272, Z = -2.321, P = 0.020
return vs control mean U = 292, Z = -2.009, P = 0.045
58
GENERAL DISCUSSION
Comparative neurobiological studies have provided evidence that conscious
perception could be a common aspect of sensorial input to all mammals. It is also
argued that conscious states are a “gift from nature” and not an acquired skill, therefore
not a result of convergent evolution among several species (Panksepp 2005). Our data
suggest that we can rely on vertebrates (Callithrix jacchus) and on in vertebrates
(Dinoponera quadriceps) as study models of consciousness expression.
Evidence of awareness has been shown for ants, which returned home using short-
routes, displaying the capacity of self-reference in the environment and the use of
short-cuts during displacement. In nature, Dinoponera quadriceps are able to travel
long distances between the nest and target areas while searching for resource, with
some individuals travelling more than 150 meters from the nest (Azevedo et al. 2014).
Therefore, returning home with food should be trick. Our results suggest that when
returning home D. quadriceps are able to calculate shortcuts and new routes from
those used for searching for food. Therefore, we consider that the information
processing system of this species passes not only through the awareness of the
individual surroundings, but through individual self-awareness by self-perception/self-
location in the environment. In this context, D. quadriceps is a reliable study model as
a proxy to consciousness.
Marmosets displayed contingency check behaviour, self-observation and
environment exploration, but we did not verify clear direct behaviour to the effective
body painted mark since reaction to the sham mark were also observed. Marmosets
looked directly to inaccessible body parts such as the back and tail, but not to genitalia
or the interior of the mouth. We also registered self-directed behaviour in front of the
mirror, while grooming, pooping and scratching body parts. A progression from
59
contingency check to self-exploration behaviours was also evident. New studies should
be realized in order to better elucidate C. jacchus capability of MSR.
As suggested by Helsch & Bukart (2006) and observed in our trials, common
marmosets are able to distinguish the mirror image from a conspecific and overcome
the mirror fallacy, using the reflected image as a tool to visualize the surroundings.
This observation alone is enough evidence of some level of self-awareness. As
described by Iriki (2006), tools are extensions of the body and its use by primates is
transmitted through social learning. Here, we verify that the tool use can be acquired
not only socially, but through self-experience and individual learning. Iriki also suggests
that tool use is directly linked to object manipulation, with monkeys using the same
neural mechanisms of the visual-tactile brain network while using the tool.
Monkeys subjected to more difficult cognitive tests, should have more complex
behaviour triggered. Maybe the more time a subject is exposed to a mirror image, the
more complex behaviours it displays. Also, complex ape-like behaviour in front of a
mirror might arise within a life time of a marmoset under constant mirror exposition,
with experience and development. Therefore, it seems that a mirror is an
environmental enrichment stimulus that may improve some cognitive capabilities.
Anderson & Gallup (2015) presented a very interesting review over MSR studies in
primates. They called the attention to the lack of convincing examples of spontaneous
mirror-guided self-exploration behaviour in the last decades. Authors suggests that
despite the efforts to demonstrate self-recognition in other primates, no convincing
evidence was found for non-apes’ species. It is interesting to conceive that their
arguments were based in the fact that different authors failed to replicate earlier
outcomes, leaving a gap between the reliability of different studies or study subjects.
Here we provide new evidence of mirror self-recognition in monkeys, looking further
for the replication of such data and for better outcomes in the mark test.
60
Apparently, vertebrates and invertebrates are able to express conscious states.
However, how and why such states were shaped by natural selection? We can start to
answer that questions by understanding that, probably, consciousness provides tools
that supports life maintenance. For example: To a subject, the processing of the
information that he is alive, is a direct tool that helps to keep him alive. This data
influences his behaviour, altering the environment in which he interacts. Therefore, we
can understand that conscious states shape behaviour, probably influencing decision
making and individual life history.
When an organism is exposed to a specific circumstance in which it can gain
something from it, subjects’ behaviours are led by a non-random response system,
which can be affected by individual’s background and personality. This observation,
known as flexible response mechanism (FRM), may perhaps be a combination of
instruments settled to generate responses to novel situations and consciousness may
be the main component of such mechanism (Earl, 2014). In risk circumstances, if an
individual response mechanism is only automatous, it could trigger as response no
response at all, which could lead to death or severe damage.
When we think about consciousness perception in species other than human, a lot
of ideas comes to mind. Our results suggest that, in fact, the absence of complex self-
directed behaviour to the body painted mark, in C. jacchus, do not imply directly in the
absence of self-awareness for the species. Other behaviour readings while individuals
were exposed to the mirror such as contingency check, self-observation and
environment exploration, provide information about similar mental states of those
embodied while in the reaction to a body mark observed with the help of a mirror.
Actually, when evaluating mirror response, it is harder to validate the absence of self-
awareness then to prove its existence. Mental states such as those observed are
directly related to self-information processing systems. Also, we should also expect
61
that different levels of consciousness may lead to different levels of mirror use.
Therefore, more complex brain may provide more complex behaviour response. In
monkeys, the evaluation of such displays probably are not definitive evidence of higher
subjective states of consciousness such as the thinking about a thought, however,
such mental states may be present in animals that, like humans, passes the mark test.
We have also verified self-information processing systems in invertebrates, which
make us think that we are only glimpsing what biology understands of how is that
consciousness shapes species behaviour. Searle (1997) suggests that biology should
consider conscious states as a continuum in phylogeny for better appraisal of these
subjective experiences. For that we should understand that different organisms
experience different conscious states, which are limited to its own sensory input. From
that we can understand, for example, that bacteria that lives in your body cannot
process information about its real environmental complexity, because of its sensory
limitations, which leads to completely ignorance of that actual nature of its own reality
– living in another organism’s body. However, for a human brain apparently there are
also difficulties in discerning between the nature of what we call reality. Could we be
missing other dimension information because of our limited sensory input? Probably.
What about other species? Can ants perceive reality as we do? Do they differ human
body as a full peace? How is that an ant processes the information of other ants?
Together with that, the fact that different species may have conscious states, leads
to reductionist questions: Which are the neural processing bases of self-awareness?
What about the neural networks related to self-directed behaviours? Are those
networks different in each behavioural type? Do neural networks converge in sister
species within different behavioural types? What has driven the evolution of these
neural connections? Can neural plasticity allow the expansion of the self-image-neural-
map in a subject’s lifetime?
62
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GLOSSARY
Affection
the experience of feeling emotional, a key part of an organism response while in
interaction.
Awareness
the state of feeling consciousness; the perception of the stimulus without the subjective
state.
Consciousness
integrated information which can provide evidence of someone or something for a
specific system.
Conscious perception
the processing of integrated information, represented by the feeling of the present
moment of one’s surroundings, on control of its own actions.
Conscious state
The processing of integrated information unveiling in the brain as ongoing experience.
Mental state
the circumstance in which qualitative states are relatively constant.
Self-awareness
to understand yourself recognizing your own knowledge and intention, directly
responding to environmental stimulus.
Self-consciousness
to introspect on your own singularity, with your mind as the object of your own attention,
allowing individual development through experience.
Self-perception
to perceive yourself separated from the environment through somatosensory input.
Self-recognition
to recognize yourself aware of your own existence and of your own body limits.
68
ANNEX
PROTOCOLO N.º 024/2015
Professor/Pesquisador: RENATA SOUSA-LIMA
Natal (RN), 16 de junho 2015.
Certificamos que o projeto intitulado “Auto reconhecimento em sagui-de-tufos brancos
(Callithrix jacchus)”, protocolo 024/2015, sob a responsabilidade de RENATA SANTORO
SOUA-LIMA MOBLEY, que envolve a produção, manutenção e/ou utilização de animais
pertencentes ao filo Chordata, subfilo Vertebrata (exceto o homem), para fins de pesquisa
científica encontra-se de acordo com os preceitos da Lei n.º 11.794, de 8 de outubro de 2008,
do Decreto n.º 6.899, de 15 de julho de 2009, e com as normas editadas pelo Conselho
Nacional de Controle da Experimentação Animal (CONCEA), e foi aprovado pela COMISSÃO
DE ÉTICA NO USO DE ANIMAIS da Universidade Federal do Rio Grande do Norte –
CEUA/UFRN.
Vigência do Projeto FEVEREIRO 2016
Número de Animais 6
Espécie/Linhagem Callithrix jacchus
Peso/Idade 150g / +2,5 anos
Sexo Machos e Fêmeas
Origem Núcleo de Primatologia UFRN
Informamos ainda que, segundo o Cap. 2, Art. 13 do Regimento, é função do
professor/pesquisador responsável pelo projeto a elaboração de relatório de
acompanhamento que deverá ser entregue tão logo a pesquisa for concluída.
Josy Carolina Covan Pontes
Coordenadora da CEUA
UFRN – Campus Universitário – Centro de Biociências, Av. Salgado Filho, S/N – CEP: 59072-970 – Natal RN.
Celular Institucional (Claro): 99229-6491
E-mail: [email protected]
Universidade Federal do Rio Grande do Norte
COMISSÃO DE ÉTICA NO USO DE ANIMAIS (CEUA)