quantum biology research papers

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The future of quantum biology

Affiliations.

1 Quantum Research Group, School of Chemistry and Physics, University of KwaZulu-Natal, Durban 4001, South Africa.
2 Institute for Lasers, Life and Biophotonics, Faculty of Sciences, VU University Amsterdam, De Boelelaan 1081, 1081 HV Amsterdam, The Netherlands.
3 ARC Centre of Excellence for Engineered Quantum Systems, The University of Queensland, St Lucia 4072, Australia.
4 Cavendish Laboratory, University of Cambridge, Cambridge, UK.
5 National Institute for Theoretical Physics, KwaZulu-Natal, South Africa.
6 Department of Physics, Faculty of Natural and Agricultural Sciences, University of Pretoria, Hatfield, South Africa [email protected].
7 Institute for Lasers, Life and Biophotonics, Faculty of Sciences, VU University Amsterdam, De Boelelaan 1081, 1081 HV Amsterdam, The Netherlands [email protected].
PMID: 30429265
PMCID: PMC6283985
DOI: 10.1098/rsif.2018.0640

Biological systems are dynamical, constantly exchanging energy and matter with the environment in order to maintain the non-equilibrium state synonymous with living. Developments in observational techniques have allowed us to study biological dynamics on increasingly small scales. Such studies have revealed evidence of quantum mechanical effects, which cannot be accounted for by classical physics, in a range of biological processes. Quantum biology is the study of such processes, and here we provide an outline of the current state of the field, as well as insights into future directions.

Keywords: artificial photosynthesis; charge transfer; enzyme catalysis; light harvesting; quantum technology; sensing.

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We declare we have no competing interests.

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Title: quantum biology at the cellular level - elements of the research program.

Abstract: Quantum Biology is emerging as a new field at the intersection between fundamental physics and biology, promising novel insights into the nature and origin of biological order. We discuss several elements of QBCL (Quantum Biology at Cellular Level), a research program designed to extend the reach of quantum concepts to higher than molecular levels of biological organization. Key words. decoherence, macroscopic superpositions, basis-dependence, formal superposition, non-classical correlations, Basis-Dependent Selection (BDS), synthetic biology, evolvability mechanism loophole.

Comments:	53 pages, 8 figures, with 3 open reviews
Subjects:	Other Quantitative Biology (q-bio.OT)
Cite as:	[q-bio.OT]
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The future of quantum biology

A headline review, published in journal of the royal society interface, offers a perspective on the present and future of quantum biology..

A Headline Review , published in Journal of the Royal Society Interface, offers a perspective on the present and future of quantum biology. Quantum biology is the application of quantum theory to aspects of biology that cannot be accurately described by the classical laws of physics, and we spoke with two of the authors, Dr Tjaart Krüger and Professor Rienk van Grondelle, about the field.

What is quantum biology?

Quantum biology is the field of study that investigates processes in living organisms that cannot be accurately described by the classical laws of physics. This means that quantum theory has to be applied to understand those processes.

All matter, including living matter, is subject to the laws of physics. Biology and biological processes often deal with electrons and protons that are continuously being transferred between different parts of a cell or a macromolecular system. These transfer processes can only take place when the system exchanges energy with its environment in the form of molecular vibrations and phonons. Such a system is called an ‘open quantum system’, and special physical laws apply to it.

Good examples of biological processes in which quantum effects are visible are the transport of electrons and protons in photosynthesis, respiration, vision, catalysis, olfaction, and in basically every other biological transport process. Further examples include the transfer of electronic and/or vibrational energy, and magnetic field effects in electron transfer and bird migration.

The quantum effects manifest themselves as long-distance effects (like in electron and proton tunneling) with a characteristic temperature dependence, magnetic field effects, the participation of superposition (or delocalized) states, resonance effects, etc. The aim of quantum biology is to develop a consistent open quantum systems model that explains all these phenomena.

Why is quantum biology an important field?

Electrons, protons, excitations, chemical bonds, and electronic charges are by definition quantum, and an understanding of their dynamics requires quantum mechanics. Furthermore, these basic entities largely determine the properties of the next level of organization in biological systems – that of biomolecular complexes, whose interaction with one another, and with their environment, often cannot be described accurately without considering the laws of quantum biology.

In addition, often in biology, the environment plays an essential role in the outcome of a biomolecular process. Photosynthesis and vision are two prominent examples. Thus, to really understand biology, and the amazing selectivity of biological processes, we need quantum biology.

Quantum biology furthermore can potentially have a huge impact on numerous technologies, including sensing, health, the environment, and information technologies. For example, energy technologies might be revolutionized by bioinspired solar cells, and chemical, magnetic, and biological sensing technologies may be taken to a new level when applying the principles found in natural equivalents.

How did both of you become interested in this field?

Prof van Grondelle: Through my study of energy and electron transfer in photosynthesis. These are ultrafast processes, taking place at a timescale of 10-13–10-11 s, which I studied using ultrashort laser pulses; and already for many years, coherences and delocalized states could be observed.

It was only about a decade ago that I realized that quantum mechanical models are required to understand the observed phenomena, and to explain their high success.

Dr Krüger: I grew up with the idea that the physical and biological sciences are two disparate fields of science until I realised, during my undergraduate studies, that the laws of physics underpin the behaviour of any kind of matter, including animate matter.

The importance of quantum mechanics to understand the fundamental processes of life emerged to me during my PhD under the supervision of Rienk van Grondelle. It was amazing to discover at how many levels quantum mechanics is a very essential ingredient to the process of photosynthesis, and, as a result, to basically all of life.

What is the aim of this Headline Review?

In December 2014, we organized a workshop to discuss quantum biology and where the research field could possibly lead us. There were about 25 participants; half of whom were well-established scientists that, in one way or another, got seriously involved with quantum effects in biological systems, while the other half were students and postdocs of the research groups involved.

For three days we intensely discussed quantum effects in biology via presentations, discussions, questions by the students, and face-to-face discussions. Finally, it was decided that we would write a review article on ‘the future of quantum biology’.

The main outline of the article was to be written by the participating students and, in a follow-up stage, the more senior scientists were expected to get involved. The aim was to produce a manuscript that clearly outlined the current status of quantum biology and how we envision its future development.

In a review like this one, it is impossible to address all aspects of the vast scope covered by quantum biology. We have therefore decided to select topics that we believe, according to current knowledge, show the strongest evidence for non-trivial quantum effects in biology, topics on which current debates in the field are concentrating, and topics that show technological potential.

What is the future of quantum biology?

Scientists will increasingly realize that life and life processes are strongly connected to the physics of open quantum systems.

Without the laws of quantum mechanics, we cannot understand life and life processes. The challenge is to understand how in a wet and noisy environment (such as a protein, a membrane, a cell, and an entire organism) the ‘perfect’ laws of quantum physics survive.

In the near future we will see new experiments that will study, for example, the effects of strong magnetic fields, single molecule/system analysis, and femtosecond coherent microscopy. One challenge is to understand how quantum effects, clearly present at some level of functional description, translate into observations at a higher level of complexity.

We will see new systems being investigated, such as neurons, neural networks, and maybe the entire brain. We will see a closer connection between our further understanding of life, and our understanding of quantum informatics, quantum computing, artificial intelligence, and various other technologies.

Keep up to date with all the latest research and reviews published in Interface by signing up for table of contents alerts .

Anita Kristiansen

Editorial Coordinator, the Royal Society

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It’s Time to Take Quantum Biology Research Seriously

Samueli School of Engineering, University of California, Los Angeles, Los Angeles, CA, US

Imagine healing an injury by applying a tailored magnetic field to a wound. This outcome might sound fantastical, but researchers have shown that cell proliferation and wound healing, among other important biological functions, can be controlled by magnetic fields with strengths on the order of those produced by cell phones. This kind of physiological response is consistent with one caused by quantum effects in electron spin-dependent chemical reactions. However (and it’s a big however), while researchers have unambiguously established such reactions for in vitro experiments, they have not done so for in vivo studies. The barriers to in vivo experiments stem both from the absence of experimental infrastructure to perform true quantum measurements inside biological systems and from a misunderstanding of what quantum behaviors in biology are and why they matter. In my opinion, it is time to set the record straight so that we can legitimize work in this field. Quantum biology findings could enable the development of new drugs and of noninvasive therapeutic devices to heal the human body, as well as provide an opportunity to learn how nature builds its own quantum technologies.

Quantum biology researchers study the inherent quantum degrees of freedom of biological matter with the goal of understanding and controlling these phenomena. To a physicist, I’d describe quantum biology as the study of light–matter interactions, where the matter is living. Quantum biology is not the study of classical biology using quantum tools, nor is it the application of quantum computers or of quantum machine learning to drug discovery or healthcare big data processing, and it definitely has nothing to do with the manipulation of free will, with the origin of consciousness, or with other New Age buzzwords.

Experimental evidence consistent with quantum effects existing in biological systems has been around for more than 50 years. One example is the spin-dependent chemical reaction thought to allow birds to navigate using Earth’s weak magnetic field. Today, there is no doubt that such phenomena play important roles in laboratory biological systems—for example, it is uncontroversial that quantum superpositions can manifest in proteins in solution for long enough that they influence chemical processes. But as yet there is no unambiguous experimental evidence that a single living cell can maintain or utilize quantum superposition states within its molecules, as is required, for example, if birds truly use a quantum process as a compass.

This lack of experimental verification is one of the main reasons that the field is considered inconsequential by funders and by the established quantum and biophysics communities. Yes, sophisticated experiments have been performed with single molecules in solution and with whole organisms (birds and flies, for example). But these experiments only show correlation, not causation, between a molecule’s or an organism’s behavior and quantum physics. Bridging that gap will require performing truly quantum measurements inside biological matter using challenging combinations of quantum instrumentation and wet lab techniques.

Another reason quantum biology is not considered a legitimate field of science is the absence of a cohesive quantum biology community. That deficit is beginning to change, but further efforts are needed in that direction. In early 2020, people in my lab and in the Quantum Biology Doctoral Training Centre at the University of Surrey, UK, started an online seminar series called Big Quantum Biology Meetings. The seminars provide a forum for the more than 600 quantum biology researchers and enthusiasts signed up to our mailing list to meet informally once a week. Other efforts to create a cohesive community include establishing a Gordon Research Conference on Quantum Biology, the first of which happened earlier this year and was attended by 150 people, and the gaining of support from the National Science Foundation for a Research Coordination Network on “Instrumentation for Quantum Biology.”

A point of pride of the Big Quantum Biology Meetings series is the intentional incorporation of inclusive practices in the seminars. For example, each meeting starts with a short presentation from a trainee, which we define as anyone without a permanent position, giving them and their work exposure. The trainee is then the host and mediator for the rest of the meeting. The main speaker also gives a “DEIJ moment”—one slide on anything related to diversity, equity, inclusion, and justice that has impacted their scientific life.

A final reason why quantum biology struggles in being accepted as a stand-alone field is the continued presence of scientific silos at institutions. If cells and organisms are using quantum effects to function optimally, a cohort of interdisciplinary experts is needed to collaboratively explore the problem. In my opinion, this collaboration would ideally take place in a quantum biology-focused institute where scientists can easily and organically work together. Recently, in an example of this idea, Japan unveiled the Institute for Quantum Life Science, which brings chemists, biologists, engineers, clinicians, physicists, and others under one roof to work on quantum biology research questions. The development of a similar institute in the US could help in irrevocably establishing this field—which will have, I believe, radical consequences for the biological, medical, and physical sciences.

About the Author

Clarice Aiello is a quantum engineer interested in how quantum physics informs biology at the nanoscale. She is an expert on nanosensors that harness room-temperature quantum effects in noisy environments. Aiello received a bachelor’s in physics from the Ecole Polytechnique, France; a master’s degree in physics from the University of Cambridge, Trinity College, UK; and a PhD in electrical engineering from the Massachusetts Institute of Technology. She held postdoctoral appointments in bioengineering at Stanford University and in chemistry at the University of California, Berkeley. Two months before the pandemic, she joined the University of California, Los Angeles, where she leads the Quantum Biology Tech (QuBiT) Lab.

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Quantum Physic, Quantum Biology, Quantum Medicine?

29 Pages Posted: 3 Jun 2020

Pedro Bullon

Universidad de Sevilla

Date Written: May 5, 2020

The leading cause and foremost reason for mortality and morbidity in the world is a group known as Noncommunicable Diseases. The best approach to treat them is to evaluate and control the risk factors. There are shared by all these diseases leading to the existence of some meeting points behind all of them. There should be some key to acquire conditions that modify the cells homeostasis and impaired the cell physiology developing different diseases. Physics try to explain the nature of the phenomena that surround us, at first, at the level of our macroscopic perception. Quantum physics studied the atomic and subatomic particles and revolutionized the reality perception with paradoxical and weird concepts. Heisenberg's uncertainty principle established that it is not possible to determine the two characteristic properties of particles with accuracy; measurement affects the system and change it. Subatomic particles have a wave-particle duality that could be in a coherence statement, also can pass through high-energy barriers. Two subatomic particles are entangled, something happening over here can have an instantaneous effect over there, no matter how far away there are. All these concepts have tried to apply to biology and life sciences, especially when classical physics fails to give an accurate description. Quantum biology is behind photosynthesis, mitochondrial respiration, enzyme activity, the sense of smell, animal migration, heredity's fidelity, and consciousness. We can apply all these concepts to diseases pathogeny. So, we describe quantum phenomena in oxidative stress, calcification, signal transduction, vitamin D production, cancer mutations, treatment resistance and metabolism, and microbiome induced pathology. I want to propose that medicine also can be explained by applying quantum physics concepts. It is a new, hard to believe, and an incredible path to be built, but we need to open the treatment options to our patients with new perspectives.

Keywords: Oxidative Stress, Calcification, Signal Transduction, Vitamin D, Cancer Mutations, Cancer Treatment, Cancer Metabolism, Microbiota

JEL Classification: I1

Suggested Citation: Suggested Citation

Pedro Bullon (Contact Author)

Universidad de sevilla ( email ).

Avda. del Cid s/n Sevilla, Sevilla 41004 Spain 0034954481120 (Phone)

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The origins of quantum biology

Johnjoe mcfadden.

1 Department of Microbiology, Faculty of Health and Medical Sciences, University of Surrey, Guildford GU2 7XH, UK

Jim Al-Khalili

2 Department of Physics, University of Surrey, Guildford GU2 7XH, UK

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Quantum biology is usually considered to be a new discipline, arising from recent research that suggests that biological phenomena such as photosynthesis, enzyme catalysis, avian navigation or olfaction may not only operate within the bounds of classical physics but also make use of a number of the non-trivial features of quantum mechanics, such as coherence, tunnelling and, perhaps, entanglement. However, although the most significant findings have emerged in the past two decades, the roots of quantum biology go much deeper—to the quantum pioneers of the early twentieth century. We will argue that some of the insights provided by these pioneering physicists remain relevant to our understanding of quantum biology today.

1. Introduction

There is growing evidence that a number of specific mechanisms within living cells make use of the non-trivial features of quantum mechanics, such as long-lived quantum coherence, superposition, quantum tunnelling and even quantum entanglement—phenomena that were previously thought to be relevant mostly at the level of isolated molecular, atomic and subatomic systems, or at temperatures near absolute zero, and were thereby not thought to be relevant to the mechanisms responsible for life. It is important at the outset of this review, and before we delve into the origins of quantum biology, to make clear that what is currently understood by the term ‘quantum’ in quantum biology does not simply mean quantization: the discretization of electron energies to account for chemical stability, reactivity, bonding and structure within living cells. Clearly, quantization applies to all matter at the microscopic scale and has long been assimilated into standard molecular biology and biochemistry. Today, quantum biology refers to a small, but growing, number of rather more specific phenomena, well known in physics and chemistry, but until recently thought not to play any meaningful role within the complex environment of living cells. For an up-to-date discussion on recent advances in quantum biology and what it means, see for example [ 1 – 3 ].

One of the most celebrated examples of the non-trivial role that quantum mechanics might be playing in biology is the claimed long-lived quantum coherence observed in the transport of exciton energy in photosynthesis [ 4 – 6 ]. While this subject remains controversial, a more established role for quantum mechanics is found in the tunnelling of electrons and protons in enzyme catalysis [ 7 – 9 ]. Beyond these examples of quantum biology, quantum entanglement has been implicated in avian navigation [ 10 – 12 ], while quantum tunnelling has been proposed to be involved in olfaction [ 13 ] and mutation [ 14 , 15 ]. More speculatively, some have suggested a link between quantum coherence and consciousness [ 16 , 17 ], though this view has little support within the neurobiology community.

But while the current interest in quantum biology and the study of the phenomena and mechanisms mentioned above only emerged in the past two decades [ 18 ], the origins of the subject go much further back, to the quantum pioneers of the early twentieth century. We will argue that some of the insights provided by a number of these physicists remain relevant to our understanding of quantum biology today.

Quantum biology's origins are often traced back to 1944 and the publication of Erwin Schrödinger's famous book, What is Life? [ 19 ]. But even before this, several other quantum physicists had already made inroads into biology. For example, the German physicist Pascual Jordan published a book a year before Schrödinger's, entitled Physics and the Secret of Organic Life [ 20 ], in which he had posed the question ‘Sind die Gesetze der Atomphysik und Quantenphysik für die Lebensvorgänge von wesentlicher Bedeutung?’ (‘Are the laws of atomic and quantum physics of essential importance for life?’). In fact, Jordan had been thinking about this question for over a decade and had been using the term Quantenbiologie since the late 1930s. The murky origins that motivated and sustained his interest in quantum biology are inextricably linked to his political sympathies with Nazi Germany and play an important role in explaining why the field did not flourish further after the war ended.

Quantum biology was in fact born shortly after the development of quantum mechanics itself. By 1927, the mathematical framework of the new quantum mechanics was in place, owing to the efforts of Bohr, Heisenberg, Pauli, Schrödinger, Dirac, Born, Jordan, Fermi and others. Flushed with their success at taming the atomic world, and with the arrogance of youth on their side, many quantum pioneers strode out of their physics laboratories and away from their blackboards to seek new areas of science to conquer. Microbiology along with the emerging field of genetics and the chromosome theory of inheritance were still unexplored territories, and a growing number of biophysicists and biochemists began to show more than a passing interest in these subjects. It was only natural therefore for many to ask whether the new atomic physics might also have something to say about the building blocks of life.

Advances in experimental physics around this time were also posing new questions. Just as Robert Hooke's microscope had opened up a new world of the very small in the mid-seventeenth century, so new techniques and key experiments in the decades between the two world wars were helping lay the foundations of an even smaller, molecular, biology. These included the discovery of X-ray mutagenesis by H.J. Muller in 1927, Theodor Svedberg's measurement of the atomic weights of proteins by using his famous ultracentrifuge in the mid-1920s and, later, the crystallization of a virus by W.M. Stanley in 1935. These and other breakthroughs promoted a feeling of optimism that, with the tools of quantum mechanics, the secrets of life could finally be laid bare.

However, not everyone was so confident that the principles of physics and chemistry would be sufficient to explain biology. One such critic was Niels Bohr himself; and yet, as we shall see, it was Bohr's pessimism regarding the importance of quantum mechanics in unlocking the secrets of life that would, paradoxically, influence and inspire the men who would lay the foundations of quantum biology.

At the same time as the quantum revolution was taking place in physics, enormous strides were being made in biology through neo-Darwinian synthesis, which brought together the rediscovered principles of Mendelian heredity with the mutations identified by Hugo de Vries and Thomas Hunt Morgan [ 21 ]. However, many mysteries remained, particularly surrounding the nature of the heritable material. Microscopic studies at the end of the nineteenth century had associated visible chromosome fibres with Mendel's heritable factors, by this time called ‘genes’. Biochemical studies had established that chromosomes consisted of proteins and nucleic acids; but how the genetic information was written into ordinary chemicals and then inherited remained a complete mystery. Moreover, although the idea of vitalism , which maintained that there is some vital ‘life force’ that endows organisms with a special quality absent in inanimate matter, had retreated under the influence of nineteenth century advances, such as Wöhler's synthesis of urea, many scientists and philosophers clung to the belief that some aspects of life required principles outside of classical science. For example, in 1907, the French philosopher Henri Bergson first published his Creative Evolution , in which he argued that heredity and evolution were driven by an ‘élan vital’ or ‘vital impetus’ peculiar to the living [ 22 ]. Many scientists remained similarly unconvinced that the extraordinary dynamics of life and heredity could be accounted for by classical sciences such as thermodynamics, organic chemistry and physics.

2. The organicists

Another factor influencing the birth of quantum biology is more subtle and has to do with the philosophical movement of organicism that was popular with many of the leading scientists of the time. Organicism was a reaction to two opposing schools of thought in biology. The first was mechanism , whose origins go at least as far back as the French Philosopher René Descartes, who maintained that all living organisms 1 are essentially machines, differing in complexity but not in principle from those machines that had driven the Industrial Revolution. The movement tended to be reductionist in the sense that it maintained that in biology, just as in all inorganic phenomena, the whole is no more than the sum of its parts. According to the mechanists, all life should ultimately be explainable in terms of the fundamental building blocks of matter and the forces that connect them, each obeying deterministic physical and chemical laws. The opposing position to this is that of vitalism, which has deep roots in the religions and mythologies of the ancient world.

The organicists sought a middle ground. They accepted that there was something mysterious about life but claimed that the mystery could in principle be explained by the laws of physics and chemistry—it is just that these had to be new laws, as yet undiscovered. One of the early proponents of organicism was Ludwig von Bertalanffy, who is generally accepted to have founded the interdisciplinary field called general systems theory , which has since been applied to everything from biology to cybernetics. His work is considered to be among the forerunners of systems biology. In his 1928 book Kritische Theorie der Formbildung ( Critical Theory of Morphogenesis ) [ 23 ], he claimed that there was a need for new organizational principles to describe life. His ideas influenced many other scientists, including the German physicist Pascual Jordan, who was one of the authors of the famous 1925 Dreimännerwerk (Three-man paper), together with Max Born and Werner Heisenberg. This classic paper introduced the world to matrix mechanics, the mathematical framework on which quantum mechanics is built. The following year, Jordan moved to Copenhagen to work with Niels Bohr.

In 1929, Bohr delivered a lecture to the Scandinavian Meeting of Natural Scientists entitled ‘The atomic theory and the fundamental principles underlying the description of nature’ [ 24 ]. After mainly focusing on the successes of quantum mechanics in describing the nature of the atomic and subatomic world, he moved on to consider whether it might have something to say in biology:

Before I conclude, it would be natural at such a joint meeting of natural scientists to touch upon the question as to what light can be thrown upon the problems regarding living organisms by the latest developments of our knowledge of atomic phenomena which I have here described. [ 24 ]

It was not clear what Bohr was hinting at with his remark about ‘the problems of living organisms'. He was around this time still attempting to clarify his philosophical views, particularly on the measurement problem in quantum mechanics, as well as his ideas on ‘complementarity’, which we discuss further below. Indeed, in his 1929 lecture, he had emphasized in his typically vague way that

… the development of the atomic theory has… first of all given us a recognition of laws which cannot be included within the frame formed by our accustomed modes of perception; the lessons we have learned by the discovery of the quantum of action open up to us new prospects which may perhaps be of decisive importance, particularly in the discussion of the position of living organisms in our picture of the world. [ 24 ]

But, despite the ambiguity of these words, Bohr was nevertheless a hugely charismatic and inspiring figure and his interest in the link between quantum mechanics and life encouraged Pascual Jordan to develop his own ideas further. After returning to Germany, having taken up a post at the University of Rostock, Jordan maintained a regular correspondence with Bohr about the relationship between physics and biology over the next couple of years. Their ideas culminated in what is arguably the first scientific paper on quantum biology. It was written by Jordan in 1932 and appeared in the German journal Die Naturwissenschaften ; the article was entitled ‘Die Quantenmechanik und die Grundprobleme der Biologie und Psychologie’ (‘Quantum mechanics and the fundamental problems of biology and psychology’) [ 25 ].

Jordan incorporated the organicism approach into his thinking by claiming that life's missing laws were the rules of chance and probability (the indeterminism) of the quantum world that were somehow scaled up inside living organisms. He called this his ‘amplifier theory’ and based it on Bohr's notion of the ‘irreversible act of amplification’ that is required in order to bring the fuzzy quantum reality into sharp focus by ‘observing’ it. Jordan believed that living organisms were uniquely able to carry out this amplification in a way that was conspicuously different from inanimate matter, such as a Geiger counter. While this all seems somewhat vague—and it was—the important point is that Jordan was convinced he could extend quantum indeterminism from the subatomic world to macroscopic biology. He even made a connection with free will by suggesting a link between quantum mechanics and psychology.

Jordan's insistence that living organisms have a unique ability to amplify the quantum into the macroscopic world does have a lot of resonance with modern views of quantum biology. However, he went much further and, in doing so, ultimately discredited the entire field by attempting to link his theories to Nazi philosophy in a mutual legitimization. And unlike what was at least claimed by other German scientists, such as Heisenberg, Jordan's political views were not merely those of a man capitulating to the insidiously hostile intellectual climate of 1930s Germany in order to ‘fit in’. Jordan was genuinely sympathetic to fascism and Nazi ideology. Indeed, his biological speculations became increasingly politicized and aligned with Nazi ideology. He even claimed that the concept of a single dictatorial leader (Führer), or guide, was a central principle of life:

We know that there are in a bacterium, among the enormous number of molecules constituting this … creature … a very small number of special molecules endowed with dictatorial authority over the total organism; they form a Steuerungszentrum [steering centre] of the living cell. Absorption of a light quantum anywhere outside of this Steuerungszentrum can kill the cell just as little as a great nation can be annihilated by the killing of a single soldier. But absorption of a light quantum in the Steuerungszentrum of the cell can bring the entire organism to death and dissolution—similar to the way a successfully executed assault against a leading [führenden] statesman can set an entire nature into a profound process of dissolution. [ 25 ]

This attempt to import Nazi ideology into biology is both fascinating and chilling. Yet Jordan correctly pointed out that inanimate objects were governed by the average random motion of millions of particles, such that the motion of a single molecule has no influence whatsoever on the whole object. This insight, as we will see, is usually credited to Erwin Schrödinger, who later claimed that life was different from inorganic chemistry because of its dependence on the dynamics of a small number of molecules. Jordan similarly argued that the few molecules that control the dynamics of living cells within the ‘Steuerungszentrum’ have a dictatorial influence, such that quantum-level events that govern their motion, such as Heisenberg's uncertainty principle, are amplified to influence the entire organism.

In August 1932, the same year that Jordan published his Naturwissenschaften paper, Niels Bohr delivered another key lecture, at the International Congress on Light Therapy in Copenhagen, Denmark [ 26 ]. Like Jordan, he was influenced by the organicists' view that the mysterious ingredient of life was yet to be discovered; but rather than opting for quantum indeterminacy, Bohr claimed that the mystery ingredient was a quantum concept he had helped to conceive: complementarity. Often referred to as wave–particle duality , this was for many of its founding fathers the central tenet of quantum mechanics. Indeed, for Bohr, the notion of complementarity went deeper than merely describing the dual nature of quantum entities, and he would later in life attempt to expand it into a broader philosophical notion. But, in its simplest form, it can be applied, for example, to the nature of light, which can exhibit both wave-like and particle-like properties, but never both at the same time: the properties are complementary. Bohr attempted to extend this notion into biology by arguing that there was an analogous complementarity between the functionality of life and our ability to study it. On a fishing trip in the Baltic around 1932, Werner Heisenberg reports a conversation on Darwinian theory in which Bohr suggests the following: ‘On the one hand, it states that, through the process of heredity, nature tests [every new living form], rejecting the great majority and preserving a few suitable ones. … But there is the second assertion: that the new forms originate through purely accidental disturbances of the gene structure. This claim is much more questionable …’ [ 27 , p. 114]. Several decades and a world war later, in the early 1960s, Heisenberg was considering the same question when, at a meeting on the banks of Lake Starnberg in Germany and listening to a lecture about mutation and selection, he pondered whether, ‘something like intention were associated with Darwinian mutation… We could ask whether the aim to be reached, the possibility to be realised, may not influence the course of events. If we do that, we are almost back with quantum theory. For the wave function represents a possibility and not an actual event. In other words, the kind of accident that plays so important a role in Darwinian theory may be something very much subtler than we think, and this precisely because it agrees with the laws of quantum mechanics’ [ 27 , pp. 242–243].

In 1931, another young German physicist, Max Delbrück, came to Copenhagen to work with, and be inspired by, Bohr. Despite an early interest in nuclear physics, Delbrück became fascinated by biophysics and the emerging field of molecular biology in particular. In 1935, he was one of three authors (the others being the Russian biologist Nikolay Timofeev-Ressovsky and the German biophysicist Karl Zimmer) of the landmark paper [ 28 ] that also became known as the Dreimännerwerk, in which they proposed that the idea of target theory, introduced by Friedrich Dessauer in Germany in the 1920s, could be used to deduce the size of a gene based on its susceptibility to ionizing radiation such as X-rays. They assumed that a quantum of radiation would hit and affect a localized ‘target’ of just a few molecules within the cell. Their paper, ‘Über die Natur der Genmutation und der Genstruktur’ (‘On the Nature of gene mutation and gene structure’) would become the inspirational starting point for Erwin Schrödinger's book, What Is Life? [ 19 ]. Delbrück went on to have a huge influence on molecular genetics. He left Nazi Germany in 1937 and settled in America, where he eventually became a US citizen. He won a Nobel Prize in 1969 for the discovery that bacteria develop resistance to viruses as a result of advantageous genetic mutations.

3. The Cambridge Theoretical Biology Club

The interest in the physical basis of life was not limited to mainland Europe. In the summer of 1932, an interdisciplinary group of scientists at the University of Cambridge set up the Theoretical Biology Club with the ambitious aim of solving ‘the great problem’ of whether life could be explained by the actions of atoms and molecules. The group's aim, like its counterparts in Germany and Austria, was to explore whether the ‘new physics’ (i.e. quantum mechanics) could provide novel laws in biology. It also hoped to merge reductionist biology with an organicist philosophy, though in this case inspired by the thinking of the great twentieth century philosopher Alfred North Whitehead.

Members of the group included some of the most influential scientists in early twentieth century biology, including biochemist Frederick Gowland Hopkins, who was awarded the Nobel Prize in Physiology or Medicine in 1929 (with Christiaan Eijkman for the discovery of vitamins), Joseph Woodger, who had translated Bertalanffy's 1928 book into English, mathematician Dorothy Wrinch, who attempted to deduce protein structure using mathematical principles, developmental biologist Conrad Waddington, along with the great evolutionary biologist and geneticist J.B.S. Haldane. In 1934, Haldane wrote a paper entitled ‘Quantum mechanics as a basis for philosophy’ [ 29 ], which opens arguing that

Biologists have as yet taken but little cognizance of the revolution in human thought which has been inaugurated by physicists in the last five years… . [ 29 , p. 78]

While never advocating vitalism, he goes on to point out that

It has been suggested that while the laws of physics are not violated in living organisms, life takes advantage of the uncertainty principle to make certain events more probable than they would otherwise have been. [ 29 , p. 81]

He clarifies his position by arguing that, at the molecular level, life differs from inanimate matter in that it can be influenced on the macroscale by single events at the quantum level,

If bacteria are heated or poisoned with certain reagents, the number of survivors falls off exponentially. This is taken to mean that the life of the cell depends on a single unstable molecule, whose change involves its death. As the transformation of such a molecule involves the uncertainty principle, this principle plays a large part in the life of bacteria. But higher organisms, even protozoa, behave as if their life depended on a number of similar molecules. The uncertainty principle in this form plays a less important part in their lives. They are protected from it by the laws of statistics, just as are large material particles consisting of many molecules. [ 29 , p. 82]

By the closing years of the 1930s, a number of highly influential scientists on both sides of the Atlantic were examining the implications of the ‘new physics’ for biology, driven by a growing mechanistic picture of biology at the smallest scales, but under the umbrella of organicism. However, the Second World intervened to curtail any further progress.

Meanwhile, Pascual Jordan became increasingly politicized and evermore determined to link his ideas in quantum biology with Nazi ideology, with the conviction that, ‘after the victory, it could stand as a symbol and representation of the unbounded means of power of the new Reich’ [ 32 , p. 270]. In 1941, he published the book Die Physik und das Geheimnis des organischen Lebens ( Physics and the Secret of Life ) [ 20 ], in which he continued to pose the question ‘Are the laws of atomic and quantum physics of essential importance for life?’ However, after Germany's defeat, Jordan's highly politicized ideas became anathema. The other matchmakers of the proposed marriage between biology and fundamental physics were scattered to the four winds in the aftermath of the Second World War; and physics, shaken to its core by the atomic bomb, turned its attention to more traditional problems.

But the plans for a union were not entirely abandoned. One of the pioneers of quantum mechanics, Erwin Schrödinger, had fled Germany when the Nazis gained power. He settled in Ireland, where in 1944 he published a book whose title posed the question ‘What is life?’ [ 19 ], to which we now turn.

4. Order from order

By the 1940s, it was known that heredity was governed by genes, but nobody yet knew what genes were made of. Schrödinger was impressed by the extraordinary high fidelity of genetic inheritance, which had been shown to be associated with mutation rates of less than 10 –8 per gene per generation. He claimed that high fidelity of heredity could not be accounted for by the classical laws, because genes were too small.

Schrödinger's argument starts from a consideration of the laws of classical physics and chemistry, such as those of thermodynamics or the gas laws. He called these ‘order from disorder’ laws to reflect the fact that their orderliness is a product of underlying disorderly molecular dynamics. He pointed out that their accuracy is limited by 1/√ N , where N is the number of particles involved. So, a balloon filled with a trillion particles deviates from the strict behaviour of the gas laws by only one part in 1 million, thereby providing relatively accurate gas laws for such macroscopic systems. However, a balloon filled with only 100 particles will deviate from orderly behaviour by one part in 10 (or 10% accuracy), and will thereby experience significant deviations from the gas laws. For example, all the molecules in the balloon will sometimes, randomly, move towards its centre, causing the balloon to contract while at a constant temperature, thereby violating Boyle's law. This, he argued, created a problem in understanding the physical basis for the fidelity of heredity because genes were known to be too small to be subject to the order from disorder laws. Using target theory, he estimated the size of a gene as no bigger than a cube of sides 300 Å containing a maximum of about 1 million atoms, so the level of noise in heredity if based on the order from disorder principle should be about one in 1000, or 0.1%—clearly much higher than the observed mutation rates. Schrödinger concluded that the accurate laws of heredity could not be founded on these order from disorder classical laws. He argued that genetic information had to be encoded at the molecular level as ‘an unusually large molecule which has to be a masterpiece of highly differentiated order, safeguarded by the conjuring rod of quantum theory’ [ 19 , p. 68]. Schrödinger called this principle on which he claimed life depended ‘order from order’, arguing that ‘incredibly small groups of atoms, much too small to display exact statistical laws, do play a dominating role in the very orderly and lawful events within a living organism’ [ 19 , p. 20]. On the nature of genes, he claimed that genetic information must be encoded by a ‘more complicated organic molecule in which every atom, and every group of atoms, plays an individual role, not entirely equivalent to that of many others (as is the case in a periodic structure). We might quite properly call that an aperiodic crystal or solid … ’ [ 19 , pp. 60–61]. Like Jordan's amplifier principle, Schrödinger claimed that life was sensitive to the dynamics of small numbers of particles, and indeed, its structure and dynamics were encoded at the atomic level. He even suggested that ‘mutations are actually due to quantum jumps in the gene molecule’ [ 19 , p. 34], where here we must be clear that what Schrödinger meant by ‘quantum jumps’ is quantum tunnelling through a finite potential barrier, rather than the old notion of quantum jumps of electrons between energy levels.

Schrödinger's book influenced both James Watson and Francis Crick, the co-discoverers of the DNA double helix, and was a factor in their decision to investigate the nature of genes. According to Watson, ‘this book very elegantly propounded the belief that genes were the key components of living cells and that, to understand what life is, we must know how genes act’ [ 31 , p. 13]. But the years following the publication of Schrödinger's book saw the discovery of the DNA double helix and the meteoric rise of molecular biology, a discipline which developed largely without reference to quantum phenomena. Gene cloning, genetic engineering, genome fingerprinting and genome sequencing were developed by biologists who, by and large, were content to ignore the mathematically challenging quantum world. Physicists similarly dismissed the possibility that quantum effects could play a role in biology, particularly as demonstrating them in inorganic physical systems required an extraordinary level of control that could only be achieved by maintaining systems at temperatures close to absolute zero in a vacuum and shielded from environmental perturbations. Quantum phenomena such as tunnelling or quantum interference effects depend on a system being well isolated from its surroundings . This was considered to be unsustainable for biologically relevant time scales within a hot, wet and complex system such as a living cell.

There were, however, occasional forays into the borderland between biology and quantum mechanics. When Watson and Crick published their structure of DNA they speculated that mutations could be caused by tautomerization of DNA bases from their common imino forms to the rare enol forms, which could produce incorrect base pairs during DNA replication. The idea received a quantum twist from the Swedish physicist Per-Olov Löwdin, who proposed [ 32 ] that quantum tunnelling of protons could generate the tautomeric bases, thereby providing a physical mechanism for Schrödinger's speculation that random point mutations might have a quantum origin. But few geneticists knew of or were influenced by Löwdin's work. Thus, the prevailing view by the 1960s—not only among biologists but among biophysicists and biochemists too—was broadly dismissive of the notion that quantum mechanics played any kind of special role in living systems.

An example of the attitude at the time can be found in the writing of Christopher Longuet-Higgins, a British theoretical chemist who made major contributions to molecular chemistry using mathematical modelling and analysis. In 1962, Longuet-Higgins wrote a paper entitled ‘Quantum mechanics and biology’ [ 33 ], in which he was scathing of attempts to justify the importance of quantum mechanics in biology:

Nowadays, we smile at the concept of a ‘vital force’ governing the growth of living matter, but a few years ago it seemed that this force was coming back into biochemistry under the assumed name [of quantum biology] … One might envisage strange forces of a quantum mechanical nature…where atoms are deftly rearranged by some sort of tunneling effect. But when a biochemist begins to use quantum-mechanical language in this nebulous way, we may justifiably suspect that he is talking nonsense. There was, I remember, some discussion a few years ago about the possible occurrence of long-range quantum-mechanical forces between enzymes and their substrates. It was, however, perfectly right that such a hypothesis should be treated with reserve, not only because of the flimsiness of the experimental evidence but also because of the great difficulty or reconciling such an idea with the general theory of intermolecular forces. [ 33 , p. 209]

Longuet-Higgins’s stance was very typical of the attitude towards quantum biology in the second half of the twentieth century, and, to a large extent, this scepticism was wholly justified.

Let us then summarize the role of the early quantum pioneers. The organicists, such as von Bertalanffy, were convinced that the deterministic classical laws of physics and chemistry were insufficient to account for the phenomena of life and that there was a missing ingredient yet to be discovered. Quantum physicists, such as Bohr, Schrödinger and Jordan, took this as a cue and suggested that quantum physics was that missing ingredient. They seized on the notions of complementarity and the uncertainty principle to claim that measurement and quantum randomness may play a role in evolution, perhaps even providing some directional control to the evolutionary process. However, this claim has largely been discredited and nearly all biologists remain wedded to the notion that there is no directionality in the mutational driver of evolution. What remained were vague ideas about a central role that some physicists such as Eugene Wigner ascribed to life, or rather to consciousness, as the magical ingredient necessary to solve the measurement problem [ 34 ]. This idea has also been largely discredited.

On the other hand, both Jordan and Schrödinger identified a real point of contact between quantum and biological processes that is highly relevant to today's work in quantum biology: macroscopic biological phenomena may be triggered by the dynamics of relatively small numbers of particles whose behaviour will be ruled or at least influenced by the non-trivial quantum phenomena such as uncertainty. Jordan wrote of a ‘very small number of special molecules endowed with dictatorial authority over the total organism’ [ 20 , p. 157]; whereas Schrödinger insisted that ‘incredibly small groups of atoms … play a dominating role in the very orderly and lawful events within a living organism’ [ 19 , p. 20]. Schrödinger went on to point out that this reliance on the dynamics of small numbers of particles separates biological systems with their order from order principle from macroscopic inanimate systems dominated by laws obeying the order from disorder principle. These ideas were picked up by some biologists, such as Haldane, who similarly insisted that ‘higher organisms, even protozoa, behave as if their life depended on a number of similar molecules' [ 31 , p. 82]. Although, reflecting the interests of their times, these quantum pioneers were particularly interested in the role of the uncertainty principle in life, their insights are transferable to the non-trivial quantum mechanical phenomena, such as coherence, tunnelling and entanglement, which are the focus of most modern quantum biology. Also significant is Schrödinger's claim that ‘The living organism seems to be a macroscopic system which in part of its behaviour approaches purely mechanical (as contrasted to thermodynamical) behaviour to which all systems tend, as the temperature approaches the absolute zero and the molecular disorder is removed’ [ 19 , pp. 68–69]’. In this, Schrödinger was essentially pinpointing the role of the randomizing influence of thermal motion, what we refer to today as ‘environmental decoherence’ [ 35 ], which is what separates the quantum from the classical world, an insight that is often traced back to the work of Dieter Zeh [ 36 ]. Schrödinger is essentially claiming that living systems somehow circumvent decoherence, an idea that resonates with modern work on the role that environmental noise may play in maintaining coherence in living cells.

However, by and large, most biologists continued to believe that life is adequately accounted for by all the familiar statistical laws of classical chemistry and physics. In 1993, a collection of eminent scientists from around the world (Steven Jay Gould, Lewis Woolpert, Stuart Kauffman and many others) gathered for a meeting at Trinity College in Dublin, Ireland, to celebrate the half-centenary of his famous 1943 lecture on which the book What is Life? [ 19 ] is based. The book, What is Life: The Next Fifty Years [ 37 ], is a collection of essays written by the participants of the meeting. Yet, in most chapters, quantum mechanics is hardly, if at all, mentioned. Schrödinger's bold proposal for a marriage between the disciplines appeared to have been forgotten.

During the 1960s and 1970s, there remained, however, a few physicists who entertained the possibility that quantum mechanics played a key role in biology. For example, the German-born British physicist Herbert Fröhlich proposed a theory in which quantum mechanical coherence, now known as Fröhlich coherence, plays an important role in biological systems [ 38 -- 40 ]. A biological system that attains such a state of coherence is known as a Fröhlich condensate. He argued that biological organization was facilitated by coherent excited states at the molecular level, driven by the flow of energy provided by metabolic processes that generate molecular vibrations in terahertz range. While highly controversial, there is a current interest in testing this hypothesis experimentally using available sources of intense terahertz radiation [ 41 ].

5. Current thinking

Despite Fröhlich's work, most quantum physicists in the second half of the twentieth century became increasingly sceptical about the possibility of non-trivial quantum effects playing a significant role in biology, particularly from studies of open quantum systems and the role of decoherence in destroying the coherence necessary for non-trivial quantum effects. From a theoretical perspective, a microscopic biological system, such as a biomolecular complex within a cell, must necessarily be treated as an open quantum system in the sense that it is never isolated from its environment. Instead, it must be continuously supplied with energy from its surroundings to maintain its low entropy and out-of-equilibrium state, as well as being subject to the inevitable random thermal noise of its environment. Therefore, it was expected that any delicate quantum effects, such as quantum superposition and coherence, will very rapidly dissipate (decohere), resulting in the suppression of any well-controlled quantum dynamics. These considerations drew physicists and biologists (who considered the question at all) to conclude that quantum phenomena would be unlikely to play a significant role in biology.

Nevertheless, it is being increasingly recognized that, just as Jordan and Schrödinger argued, living systems may after all depend on the dynamics of small numbers of molecules that are extremely well localized (extending across just a few nanometres—the scale of biomolecules such as proteins) and can take place over very short time scales (often of the order of picoseconds). This relative isolation in space, complexity and time could allow non-trivial, purely quantum mechanical processes to play an important role in living systems before decoherence induced by the surrounding environment can wash them away. There is now growing evidence that this is indeed the case.

The status of quantum biology changed dramatically in the last decades of the twentieth and early twenty-first centuries with sound experimental evidence for quantum coherence in photosynthesis and quantum tunnelling in enzyme action, together with strong theoretical arguments and some experimental evidence supporting the role of quantum entanglement in avian navigation and quantum tunnelling in olfaction. Theoretical and experimental approaches have also explored the role of proton tunnelling in the generation of DNA base tautomers [ 14 ]. Figure 1 shows a timeline charting the major discoveries and publications in quantum biology.

An external file that holds a picture, illustration, etc.
Object name is rspa20180674-g1.jpg

Timeline of key landmarks in the development of quantum biology (QB) throughout the twentieth and early twenty-first centuries. The boxes refer to the following sources: 1929 [ 24 ], 1932 [ 25 ], 1941 [ 20 ], 1944 [ 19 ], 1953 [ 42 ], 1963 [ 32 ], 1966 [ 43 ], 1974 [ 44 ], 1976 [ 45 – 48 ], 1989 [ 49 ], 2000 [ 50 ], 2007 [ 4 ]. FMO, Fenna–Matthews–Olson.

The past few years have seen a rapidly growing interest among a still small but expanding group of theoretical quantum physicists and chemists, experimental biochemists and spectroscopists who are carrying out serious theoretical and experimental studies of quantum effects in biology.

In fact, the situation is probably even more interesting than this. Work in quantum information theory has shown that environmental (thermal) noise in stationary non-equilibrium systems may actually support the existence of quantum coherence, allowing, as Schrödinger predicted, the dynamics of living systems to approach those of ‘purely mechanical (as contrasted to thermodynamical) behaviour to which all systems tend, as the temperature approaches the absolute zero and the molecular disorder is removed’ [ 19 , p. 69]. Recent work has demonstrated that the retention of quantum dynamics in biological systems is intricately connected with environmental fluctuations taking place at biologically relevant length and time scales [ 51 – 55 ].

This recent research adds an extra layer to the insight of Jordan and Schrödinger that phenomena involving small numbers of particles subject to biological amplification (such as the hereditary material) were prime candidates for quantum biology. The new research expands the role of quantum biology to more complex systems in which quantum dynamics might be enhanced, rather than washed away, by a finely tuned and constructive interplay between the quantum system and its surroundings.

Quantum biology has come a long way from the insights of the quantum pioneers of the early twentieth century. Phenomena such as quantum tunnelling and quantum coherence are now widely accepted as being involved in vitally important processes for all living cells, such as energy transfer and enzyme action. The debate has now shifted from the question of whether quantum coherence and tunnelling are involved to the role that they play. Other areas of quantum biology, such as olfaction, magnetoreception or mutation, remain more speculative, at least partly because the experimental systems are not as tractable to precise physical measurement.

What remains indisputable is that the quantum dynamics that are undoubtedly taking place within living systems have been subject to 3.5 billion years of optimizing evolution. It is likely that, in that time, life has learned to manipulate quantum systems to its advantage in ways that we do not yet fully understand. They may have had to wait many decades, but the quantum pioneers were indeed right to be excited about the future of quantum biology.

Supplementary Material

Acknowledgements.

The authors are grateful to the five anonymous referees who reviewed and commented on the earlier submission of this review and made a number of suggestions for improving it.

1 In fact, Descartes notoriously excluded humans from his mechanistic philosophy, attributing their mental attributes to the possession of a soul.

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Authors' contributions.

Both authors contributed equally to this article and have read and approved the final submission.

Competing interests

We declare we have no competing interests.

We received no funding for this study.

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Large protected areas safeguard mammalian functional diversity in human-modified landscapes.

1. Introduction

2. materials and methods, 4. discussion, 5. conclusions, supplementary materials, author contributions, data availability statement, acknowledgments, conflicts of interest.

Species	Functional Traits							Trophic Guild	Number of Patches	Number of Records	Threat Categories
	Dietary		Physical			Behavioral					IUCN	BR	SP
	Diet	Foraging Substrate	Locomotion Form	Body Mass (Kg)	Litter Size	Period of Activity	Social Behavior				IUCN	BR	SP
Artiodactyla
Bovidae
Bos taurus *	-	-	-	-	-	-	-	-	1	19	-	-	-
Cervidae
Subulo gouazoubira	Leaves and fruits	Vegetation and soil	Terrestrial	21	1	Diurnal	No	Herbivore	11	228	LC	LC	LC
Suidae
Sus scrofa *	-	-	-	-	-	-	-	-	1	22	-	-	-
Tayassuidae
Dicotyles tajacu	Leaves, invertebrates, and fruits	Vegetation and soil	Terrestrial	26	3	Diurnal and nocturnal	Yes	Frugivore/Herbivore	8	107	LC	LC	NT
Cingulata
Chlamyphoridae
Euphractus sexcinctus	Leaves, vertebrates, invertebrates, and fruits	Vegetation and soil	Semifossorial	5	2	Diurnal	No	Omnivore	3	8	LC	LC	LC
Dasypodidae
Cabassous tatouay	Invertebrates	Soil	Semifossorial	5	1	Nocturnal	No	Insectivore	3	50	LC	DD	DD
Dasypus novemcinctus	Leaves, vertebrates, invertebrates, and fruits	Vegetation and soil	Semifossorial	4	4	Nocturnal and crepuscular	No	Insectivore	14	367	LC	LC	LC
Didelphimorphia
Didelphidae
Didelphis albiventris	Vertebrates, invertebrates, and fruits	Trees and soil	Terrestrial	2	9	Nocturnal and crepuscular	No	Omnivore	17	426	LC	LC	LC
Rodentia
Dasyproctidae
Dasyprocta azarae	Leaves, invertebrates, and fruits	Vegetation and soil	Terrestrial	3	2	Diurnal and crepuscular	No	Frugivore/Herbivore	15	424	DD	LC	NT
Caviidae
Hydrochoerus hydrochaeris	Leaves	Vegetation and soil	Terrestrial	50	5	Nocturnal and crepuscular	Yes	Herbivore	2	3	LC	LC	LC
Cuniculidae
Cuniculus paca	Leaves and fruits	Vegetation and soil	Terrestrial	9	1	Nocturnal	No	Frugivore/Herbivore	4	196	LC	NT	LC
Erethizontidae
Coendou spinosus	Leaves and fruits	Trees	Arboreal	4	1	Nocturnal and crepuscular	No	Herbivore	1	3	LC	LC	DD
Carnivora
Canidae
Canis lupus familiaris *	-	-	-	-	-	-	-	-	8	98	-	-	-
Cerdocyon thous	Vertebrates, invertebrates, and fruits	Vegetation and soil	Terrestrial	7	5	Nocturnal and crepuscular	No	Omnivore	3	77	LC	LC	LC
Chrysocyon brachyurus	Leaves, vertebrates, invertebrates, and fruits	Vegetation and soil	Terrestrial	22	2	Nocturnal and crepuscular	No	Omnivore	4	23	NT	VU	VU
Felidae
Felis silvestris catus *	-	-	-	-	-	-	-	-	4	6	-	-	-
Leopardus pardalis	Vertebrates and invertebrates	Soil	Terrestrial	10	3	Nocturnal	No	Carnivore	7	75	LC	LC	VU
Puma concolor	Vertebrates and invertebrates	Soil	Terrestrial	46	4	Nocturnal	No	Carnivore	9	38	LC	VU	VU
Herpailurus yagouaroundi	Vertebrates and invertebrates	Vegetation and soil	Terrestrial	5	2	Diurnal and nocturnal	No	Carnivore	6	30	LC	VU	LC
Mephitidae
Conepatus semistriatus	Vertebrates, invertebrates, and fruits	Vegetation and soil	Terrestrial	2	5	Nocturnal and crepuscular	No	Omnivore	4	29	LC	LC	DD
Mustelidae
Eira barbara	Vertebrates, invertebrates, and fruits	Vegetation and soil	Terrestrial	7	3	Diurnal	No	Omnivore	8	114	LC	LC	LC
Lontra longicaudis	Vertebrates	Water	Semiaquatic	6	3	Diurnal and nocturnal	No	Carnivore	1	6	NT	NT	NT
Procyonidae
Nasua nasua	Vertebrates, invertebrates, and fruits	Trees and soil	Terrestrial	5	5	Diurnal	Yes	Omnivore	8	47	LC	LC	LC
Procyon cancrivorus	Vertebrates, invertebrates, and fruits	Vegetation and soil	Terrestrial	5	3	Nocturnal	No	Omnivore	2	28	LC	LC	LC
Lagomorpha
Leporidae
Lepus europaeus *	-	-	-	-	-	-	-	-	1	5	-	-	-
Sylvilagus brasiliensis	Leaves	Vegetation and soil	Terrestrial	1	5	Nocturnal and crepuscular	No	Herbivore	7	84	EN	NT	NT
Perissodactyla
Tapiridae
Tapirus terrestris	Leaves and fruits	Vegetation and soil	Terrestrial	260	1	Nocturnal	No	Frugivore/Herbivore	1	1	VU	VU	VU
Pilosa
Myrmecophagidae
Myrmecophaga tridactyla	Invertebrates	Soil	Terrestrial	31	1	Diurnal and nocturnal	No	Insectivore	8	264	VU	VU	VU
Tamandua tetradactyla	Invertebrates	Trees and soil	Terrestrial	5	1	Nocturnal	No	Insectivore	12	51	LC	LC	LC
Primates
Callitrichidae
Callithrix penicillata	Invertebrates and fruits	Trees	Arboreal	0.5	2	Diurnal	Yes	Omnivore	1	6	LC	LC	LC
Cebidae
Sapajus nigritus	Leaves, invertebrates, and fruits	Trees	Arboreal	4	1	Diurnal	Yes	Omnivore	4	27	NT	NT	NT
Total										2862	3	5	5

	Number of Records
Species	BFS	FBJSP	JES	PFSP	ARBR				SBES		SRES			VSP
Species	BFS	FBJSP	JES	PFSP	1	2	3	4	1	2	1	2	3	1	2	3	4	5
Artiodactyla
Bovidae
Bos taurus *	0	0	0	0	0	0	0	0	0	0	0	0	19	0	0	0	0	0
Cervidae
Subulo gouazoubira	0	66	53	12	0	0	0	0	40	24	2	1	1	0	17	0	11	1
Suidae
Sus scrofa *	0	21	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0
Tayassuidae
Dicotyles tajacu	0	0	40	11	0	0	0	0	11	2	0	0	0	0	6	4	15	18
Cingulata
Chlamyphoridae
Euphractus sexcinctus	0	4	1	0	0	0	0	0	3	0	0	0	0	0	0	0	0	0
Dasypodidae
Cabassous tatouay	0	35	14	0	0	0	1	0	0	0	0	0	0	0	0	0	0	0
Dasypus novemcinctus	27	202	45	16	3	5	39	0	8	2	1	14	1	2	2	0	0	0
Didelphimorphia
Didelphidae
Didelphis albiventris	0	200	53	19	11	4	17	8	2	2	18	20	24	7	9	9	17	6
Rodentia
Dasyproctidae
Dasyprocta azarae	13	2	201	18	3	9	16	2	8	0	0	5	0	20	36	31	37	23
Caviidae
Hydrochoerus hydrochaeris	0	2	0	0	0	0	0	0	1	0	0	0	0	0	0	0	0	0
Cuniculidae
Cuniculus paca	0	160	7	0	0	0	0	0	0	0	0	26	0	3	0	0	0	0
Erethizontidae
Coendou spinosus	0	3	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0
Carnivora
Canidae
Canis lupus familiaris *	4	51	1	0	0	0	1	0	0	17	4	10	0	0	0	0	0	0
Cerdocyon thous	0	72	0	3	0	0	0	0	2	0	0	0	0	0	0	0	0	0
Chrysocyon brachyurus	0	5	8	9	0	0	0	0	1	0	0	0	0	0	0	0	0	0
Felidae
Felis silvestris catus *	2	1	0	0	0	0	0	0	1	9	1	0	0	0	0	0	0	0
Leopardus pardalis	0	43	19	1	0	0	0	0	0	0	0	0	0	1	7	1	3	0
Puma concolor	0	9	6	8	0	1	1	2	9	0	0	0	0	0	0	1	1	0
Herpailurus yagouaroundi	0	19	0	4	0	0	0	0	4	1	0	1	0	1	0	0	0	0
Mephitidae
Conepatus semistriatus	0	2	24	0	0	0	0	0	1	0	0	0	0	0	0	0	2	0
Mustelidae
Eira barbara	0	87	14	2	0	0	0	0	3	1	0	0	0	0	2	0	3	2
Lontra longicaudis	0	6	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0
Procyonidae
Nasua nasua	1	15	5	0	0	0	0	0	5	0	2	7	8	0	0	0	0	4
Procyon cancrivorus	0	27	0	0	0	0	0	0	1	0	0	0	0	0	0	0	0	0
Lagomorpha
Leporidae
Lepus europaeus *	0	5	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0
Sylvilagus brasiliensis	0	1	44	20	0	0	0	0	3	0	0	0	0	0	6	0	9	1
Perissodactyla
Tapiridae
Tapirus terrestris	0	0	1	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0
Pilosa
Myrmecophagidae
Myrmecophaga tridactyla	0	155	37	0	0	2	0	0	24	10	0	0	0	0	3	0	30	3
Tamandua tetradactyla	1	14	19	6	1	0	2	1	0	0	0	1	0	1	2	0	1	2
Primates
Callitrichidae
Callithrix penicillata	0	6	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0
Cebidae
Sapajus nigritus	0	22	2	0	0	0	0	2	0	0	0	0	0	0	0	0	0	1
Total records	42	1157	593	129	18	21	76	15	126	42	23	75	34	35	90	46	129	61
Richness (native species)	4	24	19	13	4	5	6	5	17	7	4	8	4	7	10	5	11	10
FD	1.40	6.59	5.29	3.52	1.29	1.53	1.91	1.67	4.50	2.02	1.34	2.51	1.34	2.12	2.81	1.44	2.96	2.99
RAI	0.004	0.120	0.061	0.013	0.002	0.002	0.008	0.001	0.013	0.004	0.002	0.008	0.003	0.004	0.009	0.005	0.013	0.006

Trait Type	Trait	Category		Number of Species
Dietary	Diet	Leaves		12
		Fruits		17
		Vertebrates		13
		Invertebrates		19
	Foraging substrate	Water		1
		Trees		6
		Vegetation		15
		Soil		22
Physical	Locomotion form	Terrestrial		19
		Semifossorial		3
		Semiaquatic		1
		Arboreal		3
Behavioral	Period of activity	Diurnal		11
		Nocturnal		19
		Crepuscular		9
	Social behavior	Social		5
		Non-social		22
		IUCN	Brazil	São Paulo
Threat categories	Data Deficient	1	1	3
	Least Concern	19	16	13
	Near Threatened	3	4	5
	Vulnerable	2	5	5
	Endangered	1	0	0
Trophic guild	Carnivores			4
	Frugivores			4
	Herbivores			8
	Insectivores			4
	Omnivores			10

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Click here to enlarge figure

Protected Area	Classification	Climate	Patch Size (ha)	Fragments	Sampling Points	Sampling Effort (Traps-Day)
Jataí Ecological Station (JES)	Strict protection	Aw	10,285	1	44	2902
Santa Bárbara Ecological Station (SBES)	Strict protection	Cwa	2585	1	19	1309
Santa Bárbara Ecological Station (SBES)	Strict protection		1612	2	8	530
Santa Rita do Passa Quatro Experimental Station (SRES)			9	1	1	78
	Sustainable use	Cwa	19	2	2	156
			51	3	2	156
Bebedouro State Forest (BSF)	Strict protection	Aw	99	1	2	82
Furnas do Bom Jesus State Park (FBJSP)	Strict protection	Cwb	2069	1	25	2021
Porto Ferreira State Park (PFSP)	Strict protection	Cwa	611	1	9	608
Vassununga State Park (VSP)	Strict protection		231	1	2	118
			329	2	5	357
		Cwa	130	3	2	124
			1217	4	13	764
			169	5	3	175
Augusto Ruschi Biological Reserve (ARBR)	Strict protection		115	1	1	38
		Aw	56	2	1	34
			189	3	2	115
			124	4	3	75

Trait Type	Trait	Category	Data Type
Dietary	Diet	Leaves	Percentage
		Fruits	Percentage
		Vertebrates	Percentage
		Invertebrates	Percentage
	Foraging substrate	Water	Binary
		Trees	Binary
		Vegetation	Binary
		Soil	Binary
Physical	Locomotion form	Terrestrial	Binary
		Semifossorial	Binary
		Semiaquatic	Binary
		Arboreal	Binary
	Body mass	Kg	Continuous
	Litter size	Average number of puppies	Continuous
Behavioral	Period of activity	Diurnal	Binary
		Nocturnal	Binary
		Crepuscular	Binary
	Social behavior	Social	Binary
Threat categories	IUCN Brazil São Paulo	Data Deficient	Categorical
		Least Concern	Categorical
		Near Threatened	Categorical
		Vulnerable	Categorical
		Endangered	Categorical

Model	SSQ	RSS	AIC
Start: FD ~ log1p (patch size) + log1p (isolation) + forest + sugarcane
− log1p (isolation)	0.00	106.60	40.02
− Forest	0.74	107.33	40.14
− Sugarcane	0.91	107.50	40.17
No change		106.59	42.02
− log1p (patch size)	36.52	143.11	45.32
Step 1: FD ~ log1p (patch size) + forest + sugarcane
− Forest	0.74	107.33	38.14
− Sugarcane	0.93	107.52	38.17
No change		106.60	40.02
− log1p (patch size)	39.45	146.04	43.68
Step 2: FD ~ log1p (patch size) + sugarcane
− Sugarcane	0.47	107.80	36.22
No change		107.33	38.14
− log1p (patch size)	77.40	184.74	45.91
Step 3 FD ~ log1p (patch size)
No change		107.80	36.22
− log1p (patch size)	146.32	254.12	49.65

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Fornitano, L.; Gouvea, J.A.; Costa, R.T.; Magioli, M.; Bianchi, R. Large Protected Areas Safeguard Mammalian Functional Diversity in Human-Modified Landscapes. Sustainability 2024 , 16 , 5419. https://doi.org/10.3390/su16135419

Fornitano L, Gouvea JA, Costa RT, Magioli M, Bianchi R. Large Protected Areas Safeguard Mammalian Functional Diversity in Human-Modified Landscapes. Sustainability . 2024; 16(13):5419. https://doi.org/10.3390/su16135419

Fornitano, Larissa, Jéssica Abonizio Gouvea, Rômulo Theodoro Costa, Marcelo Magioli, and Rita Bianchi. 2024. "Large Protected Areas Safeguard Mammalian Functional Diversity in Human-Modified Landscapes" Sustainability 16, no. 13: 5419. https://doi.org/10.3390/su16135419

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It's Time to Take Quantum Biology Research Seriously. Clarice Aiello. Samueli School of Engineering, University of California, Los Angeles, Los Angeles, CA, US. May 10, 2023 • Physics 16, 79. Understanding the possible quantum-driven behaviors of biological systems could aid in treating injuries or in developing cures for diseases, but ...
The future of quantum biology
Quantum biology is the study of such processes, and here we provide an outline of the current state of the field, as well as insights into future directions. Keywords: artificial photosynthesis, light harvesting, charge transfer, enzyme catalysis, sensing, quantum technology. Go to: 1. Introduction.
Quantum Physic, Quantum Biology, Quantum Medicine? by Pedro Bullon
Quantum biology is behind photosynthesis, mitochondrial respiration, enzyme activity, the sense of smell, animal migration, heredity's fidelity, and consciousness. We can apply all these concepts to diseases pathogeny. So, we describe quantum phenomena in oxidative stress, calcification, signal transduction, vitamin D production, cancer ...
Physics of life: The dawn of quantum biology
Biology has a knack for using what works, says Seth Lloyd, a physicist at the Massachusetts Institute of Technology in Cambridge. And if that means "quantum hanky-panky", he says, "then quantum ...
Quantum Biology Research Papers
This paper presents a historical perspective on the development and application of quantum physics methodology beyond physics, especially in biology and in the area of consciousness studies. Quantum physics provides a conceptual framework for the structural aspects of biological systems and processes via quantum chemistry.
Quantum Coherence Effect in the Interaction of Light and Molecules
Understanding the quantum coherence effects is crucial for their promising applications, such as engineering artificial photosynthesis, manipulating chemical reactions, and designing coherence‐based functional devices. Considering that a molecule is the smallest unit that can exist independently and maintain its physical and chemical properties, investigating the quantum coherence effects of ...
The origins of quantum biology
The new research expands the role of quantum biology to more complex systems in which quantum dynamics might be enhanced, rather than washed away, by a finely tuned and constructive interplay between the quantum system and its surroundings. Quantum biology has come a long way from the insights of the quantum pioneers of the early twentieth century.
Sustainability
A Feature Paper should be a substantial original Article that involves several techniques or approaches, provides an outlook for future research directions and describes possible research applications. Feature papers are submitted upon individual invitation or recommendation by the scientific editors and must receive positive feedback from the ...

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