This is the accepted version of the article: Peñuelas, Josep; Baldocchi, Dennis. Life and the five biological laws. Lessons for global change models and sustainability. DOI 10.1016/j.ecocom.2019.02.001 This version is avaible at https://ddd.uab.cat/record/203311 under the terms of the license 1 Life and the five biological laws. Lessons for global change 2 models and sustainability. 3 4 5 Josep Penuelas1,2 and Dennis Baldocchi3 1 6 CSIC, Global Ecology Unit CREAF-CSIC-UAB, Bellaterra (Catalonia) E-08193, Spain; 2 7 CREAF, Cerdanyola del Vallès (Catalonia) E-08193, Spain; 3 8 Department of Environmental Science, Policy and Management, 130 Mulford Hall, 9 University of California, Berkeley, CA, 94720, United states 10 11 12 13 Life on Earth is the result of a continuous accumulation of information by 14 combination and innovation using endo- (inside the organism) and exosomatic 15 (outside the organism) energy. Sustenance occurs through cycles of life and death. 16 We here define five life laws for these vital processes. These processes cannot exceed 17 natural limits of size and rates because they are constrained by space, matter and 18 energy; biology builds on what is possible within these physicochemical limits. 19 Learning from the way nature deals with the accumulation of information, the limits 20 of size and the rates at which life can acquire and expend energy and resources for 21 maintenance, growth and competition will help us to model and manage our 22 environmental future and sustainability. 23 24 25 Key words: Physical ecology, information, combination, innovation, endosomatic energy, 26 exosomatic energy, discontinuous destruction, energy flow, natural limits, learning from 27 nature, environmental management. 28 29 30 31 32 33 1 34 Life is a ride on matter and energy through space subject to selective pressure 35 Earth’s life is complex and diverse. Life on Earth consists of discontinuous individuals 36 belonging to millions of species. Life is the result of evolutionary processes acting on a 37 continuous accumulation of structural and functional information by combination and 38 innovation in the use of matter and endo- and exosomatic energy and on discontinuous 39 processes of death and destruction that recycle the materials that form structure, 40 information and energy compounds, such as proteins, DNA and ATP, respectively. 41 Combination builds atoms from elementary particles, molecules from atoms, 42 polymers from monomers, tissues from polymers, organs from tissues, organisms from 43 organs, populations from organisms and communities from populations. Pre-existing 44 pieces in the environment or even other organisms are thus assembled into larger 45 structures1. Enormous complexity and diversity can be attained from a relatively small 46 number of elements by assembling them in different ways, e.g. at the molecular level 47 alone, a few chemical elements such as C, N, P, S, H, O, K or Ca can combine to form 48 ensembles that, ordered or interacting in different ways, produce unimaginable numbers 49 of possibilities2, or at the polymeric level, around 20 amino acids provide building blocks 50 for multiple proteins, enzymes and other structures. 51 Living organisms store and cheaply copy and combine these pieces together with 52 the implicit information they carry. The copied pieces are modified by mutation and other 53 genetic mechanisms in an additional process of innovation. DNA and RNA have this 54 ability. Interestingly, life is over 3 billion years old and has produced a large diversity of 55 forms, shapes and species, but DNA remains the only form of information transfer within 56 the history of life on Earth. Dawkins3, in a particularly extreme but appealing point of 57 view, argues that life is just the competition among genes, a dynamic change of genetic 58 structure favoring the most adequate information for the continuous improvement of the 59 interactions of organisms with the environment. ‘Life is nothing but the maximization of 60 DNA survival’ a merciless contest among genes where DNA neither cares nor knows. 61 DNA just is. 62 The living individuals produced by combination and innovation are open systems 63 that import energy and materials to be used by their cells. They use chemical compounds 64 such as ATP and NADPH to transfer energy and use RUBP to fix carbon. Photosynthesis 65 by autotrophs, self-feeders such as plants and cyanobacteria, dominates the biosphere. 66 They absorb solar energy (photons) leading to (1) photo-oxidation of water and 67 production of oxygen, and (2) formation of electrochemical potential on biological 2 68 membranes, ATP and NADPH, and finally CO2 assimilation and biosynthesis of 69 carbohydrates. This is an amazing feature of biological membranes enabling the 70 transformation of solar energy to chemical energy. The chemical energy stored in 71 carbohydrates is the prime energy source, or food, for the majority of life on Earth. The 72 subsequent extraction of chemical energy from carbohydrates is associated with a variety 73 of heterotrophic or chemo-autotrophic metabolisms that use a hierarchy of 74 biogeochemical redox reactions. This energy is used to fuel various forms of work 75 (chemical, osmotic, mechanical) that sustain life. The redox ladder determines the amount 76 of energy extracted, which depends on the terminal electron acceptor. If there is energy 77 to extract along the redox ladder, there is always a distinct microbial group that has 78 evolved to extract that energy. Organisms must work to acquire matter to grow, acquire 79 additional resources, out-compete their neighbors, move, avoid predators and ultimately 80 reproduce, thereby passing their genes to the next generation. 81 Life thus depends on the flow of energy to sustain metabolism: plants use solar 82 energy, animals and fungi use organic matter and bacteria and archaea can use a variety 83 of chemical energy sources. Ecosystems consist of very complex networks of interacting 84 species (at different levels of space and time) and a physicochemical environment. These 85 networks are hierarchical, organized under the flow of energy, in a stepwise process, as 86 it is dissipated to heat. Because of this link between life and the dissipation of energy, life 87 can be seen as a manifestation of the second law of thermodynamics 4–7. 88 Organisms and ecosystems depend in many ways on high amounts of exosomatic 89 energy (outside the organism) jointly with this relatively weak endosomatic (inside the 90 organism) flow of energy that permits metabolism7. Evapotranspiration lifts water and 91 nutrients from soil to the leaves in plants while also providing turgidity for cell growth. 92 This transport is possible thanks to solar radiation. Many species benefit from wind or 93 water transport to disperse, hunt or find reproductive partners. Some are especially 94 effective in using exosomatic energies for their own benefit. In aquatic ecosystems, 95 movements of water are subsidies of energy for organisms. In the case of mankind, this 96 trend has been much promoted by the advantage of cultural transmission of knowledge 97 and rapid communication. The enormous cultural development of the use of exosomatic 98 energy by mankind is an extreme case of a more general trend in the evolution of life. 99 This cultural development allows a continuously increasing use and control of space and 100 resources that have never been exploited before and feeds back cultural evolution and 3 101 population growth, but it also involves an increasing danger of climatic disturbance, loss 102 of biodiversity and exhaustion of resources. 103 In this biological ride on energy and matter: 1) reproductive success passes on 104 genes for successful organismic traits to those who ride the best, given the available 105 resources and the organisms’ ability to extract and use them, 2) species differentiation 106 (via evolution, competition and selective winnowing) produces the traits that define the 107 structure and function of microbes, plants and animals, 3) structure and function provide 108 the mechanisms for competing for and capturing light energy, acquiring water and 109 nutrients, modulating the diffusion of gases in and out of plant stomata, plant feeding by 110 herbivores and herbivore hunting by carnivores, and 4) bacteria, fungi and other 111 microorganisms recycle material by exploiting differences in redox potential associated 112 with the chemical energy in carbohydrates and the available electron acceptor, whether it 113 is oxygen, nitrate, sulfate, ferric iron (Fe3+) or carbon dioxide. 114 Schrödinger (1944)8 proposed the idea that life implies less entropy, which comes 115 from the ability of life to extract energy from the environment. The second law of 116 thermodynamics establishes that the total entropy of any system cannot decrease unless 117 by increasing the entropy of some other system (“drawing energy from the environment”). 118 Organisms can only stay alive by continually drawing energy from their environment, 119 avoiding decay by eating, drinking, breathing and, in the case of plants, assimilating8. The 120 technical term is metabolism. Without this ability to acquire energy, organisms die. Death 121 is therefore the result of not acquiring energy and resources but is useful and necessary 122 when thinking about life as an interconnected system. When organisms die and cease 123 assimilating the products of photosynthesis, the transition toward greater entropy is 124 inevitable, leading to bodily decay, decomposition and the recycling of matter for the next 125 generation of life. 126 127 …but life is also a continuous asymmetric accumulation of information 128 Ecology has been especially interested in these flows and budgets of energy and matter 129 since the late nineteenth century8–11, understanding ecology as the study of flows of 130 energy and matter, which is why “physics sets the limits on life but biology is how it is 131 done”. Some researchers such as Margalef (1997)7, however, highlighted in the 1960s the 132 importance of the third Aristotelian principle: form, or structure, reinterpreted as 133 information. This information not only regulates the building of structure but also 134 function and metabolism. Information content thus increases faster than the material size 4 135 of its store, i.e. information content is not simply proportional to the material size of its 136 store, but rather a power with an exponent larger than one: 137 𝐼𝑛𝑓𝑜𝑟𝑚𝑎𝑡𝑖𝑜𝑛 = 𝑓(𝑆𝑡𝑜𝑟𝑒 𝑠𝑖𝑧𝑒 >1 ) 138 The result of most events in life is a gradual increase in the complexity of nature. This 139 increase, though, cannot continue forever. Changes leading to simplification occasionally 140 occur discontinuously and apparently randomly, erasing large stores of information. The 141 acquisition of information is historical and cannot be run in reverse; it cannot be played 142 back to dismantle each block of added information in an inversely valid way. 143 Asymmetry thus rules this acquisition of information by life relative to individual 144 birth, growth and death, ecosystem succession and its catastrophic destruction and even 145 the deployment and collapse of human cultures: there is hysteresis from the fact that 146 construction is slow, whereas destruction can be very fast. Changes toward simplification 147 occur discontinuously, apparently distributed at random, similar to punctuated 148 equilibrium and evolution13, but it is impossible to orderly extract the pieces that came 149 with successive inputs and interactions in biological evolution, one after another. The 150 inclusion of death as a normal event in life’s program is very efficient and cheap, because 151 the mechanisms of genetic copying and reproduction of the organisms work so well and 152 are thermodynamically cheap. 153 Ecosystems are also cyclically destroyed by fire, wind throw, flooding, landslides 154 or other disturbances, although in cases with components that are less integrated, some 155 manipulation and restoration are possible. After a large collapse (e.g. a wildfire), the 156 system is rebuilt mostly from the remaining pieces, such as seeds and spores that were 157 protected or buried. Space and resources in Earth’s history were conquered by the 158 survivors that quickly evolved and diversified (adaptive radiations) to use the empty 159 niches after the mass extinctions, i.e. to form a new hierarchical network of energy paths; 160 mammals diversified from surviving species and filled the gap after dinosaurs became 161 extinct. Life amazingly fills all gaps nearly everywhere on Earth: below the ice in 162 Antarctica, in the deep ocean vents, in the driest deserts, … 163 All life and ecological processes are thus built in a thermodynamic continuum 164 where joining an existing store of information is more effective (the winning strategy in 165 a selective game) than starting a new one. Maybe this is why DNA formed only once. 166 Information accumulates easily and faster when there is already a large core. Information 167 growth is allometric, as are most processes concerning life. Saint Matthew’s principle, 168 that those who already have more get more due to the advantage of previous organization, 5 169 applies here. The compound-interest effect also applies here. Time thus offers the 170 possibility for life systems to enlarge and produce complicated structures, but keeping 171 them functionally coherent, up to a limit imposed by the distance between potential 172 reactants. More complex systems may appear as time flows and history accumulates. 173 Basic mechanisms such as natural selection, self-organization and random processes not 174 driven by selection are particularly useful for understanding this huge complexity of 175 organisms and ecosystems and this huge accumulation of evolutionary biological 176 information through combination, innovation and death while cycling matter and energy. 177 Natural selection and random processes not driven by selection operate on individuals 178 (genotypes), governing the traits that influence fitness and how they vary with the 179 environment. Although still under debate14, self-organization operates on communities 180 and ecosystems, governing the interactions of system components. These mechanisms 181 explain how life on Earth generates its huge complexity, a complexity and heterogeneity 182 that can be seen as noise in physics or as the magic of life in ecology, a complexity that 183 we humans are intentionally or unintentionally affecting in the most recent history of 184 Earth. The more complex and diverse a system is, the more information it contains. This 185 principle applies to biological systems as well as physical or cultural systems. 186 Understanding and modeling the accumulation of information in organisms and 187 ecosystems are the main challenges for biology and ecology. 188 189 Life laws 190 Physics has universal laws. Biology is envious because it is perceived not to have 191 universal laws. They just seem to be overlooked. Very few laws may in fact explain life 192 on Earth. The five most prominent laws pertinent to life and ecology (Fig. 1) are: 193 1-the law of mass conservation (introduced by Lomonosov and Lavoisier) 194 2-the first law of thermodynamics, energy cannot be created or destroyed in an isolated 195 system 196 3-the second law of thermodynamics, the entropy of any isolated system always increases. 197 4-information content is a power of the material size of its store with an exponent larger 198 than one and 199 5-basic mechanisms such as natural selection, self-organization and random processes not 200 driven by selection drive evolution, generating the huge complexity of organisms and 201 ecosystems. 6 202 These five laws of nature translate into mostly “principles of limits”, e.g. two 203 things cannot be present simultaneously in the same place, or the same energy cannot be 204 used twice in continuity and in the same way. Life needs to acquire energy to do work 205 and matter to work with in a region of space. The amounts of solar energy and matter per 206 square meter of soil or cubic meter of water are limited, so the number and size of plants, 207 animals and microbes, and the metabolism of an ecosystem have an upper limit. These 208 five laws thus also lead to particular, more focused field laws, e.g. a forest can sustain 209 many small trees or a few big trees but not many big trees. 210 Life is a space-filling system, so power-law exponents characterize the 211 relationship between energy and mass. The metabolic energy of an organism, ME, needed 212 to sustain metabolism scales with the mass of the organism, M, to the ¾ power (Kleiber’s 213 Law): 214 ME ≈ M3/4 215 This law has been challenged by studies of plants showing that this law works 216 only if plant nitrogen mass is used instead of the total plant mass15,16. This can have some 217 important consequences. For example, if the CO2 fertilization of the future world will 218 lead to nitrogen dilution in plant tissues it can have an important consequence for 219 modelling of future ecosystems16. 220 The number of individuals scales with mass to the -¾ power (modified Yoda’s 221 Law): 𝑀−3/4 222 𝑁 ≈ 𝑎 223 The energy/metabolism of the system is thus scale-invariant with mass; the 224 exponent equals zero: 225 E = N ME ≈ M-3/4 M3/4 ~ M0 226 Physical laws set the limits, and biology adapts to what is available, recycles 227 material and extracts energy from the environment while evolving to develop structures 228 and functions optimized for their environment. Due to the accumulation of information 229 in organisms and ecosystems, joining an existing store of information is more effective 230 (the winning strategy in a selective game) than starting a new store. The physical laws 231 and limits make some forms and functions inviable. A 100-m tree does not grow in the 232 desert, nor can ecosystems evaporate more water than is available from rainfall or 233 groundwater, nor can a CO2 fertilization period like the one Earth has lived in the past 234 decades be expected to last long since other resources take over the limits7. 7 235 236 Lessons for life modeling and sustainability 237 These laws and principles suggest Bayesian priors and relationships for traits, structure 238 and function of organisms and ecosystems, and thus put us closer to what model 239 parameters may and may not be. Both Earth system and integrated assessment models 240 (ESMs and IAMs) should take these general ecological laws into account, mostly as 241 principles that set the limits of space, matter, and energy, and the evolution of the 242 asymmetrical accumulation of information through “compound-interest” principles. Most 243 models are already successful because they implicitly apply these laws. ESMs and IAMs 244 must, moreover, consider that basic mechanisms such as natural and intended selection, 245 but also random processes not driven by selection, drive the evolution of species, and 246 self-organization drives the evolution of semi-natural and agricultural ecosystems, which 247 together generate the highly complex feedback processes in organisms, communities and 248 ecosystems. 249 These ecological principles also apply to human activities, including landscape 250 architecture and design, economics or urban transport systems of water and vehicles. 251 Even though our species has acquired increasing abilities to use matter, exosomatic 252 energy and information, thanks to the industrial and technological revolutions, the limits 253 of space, matter and energy and the asymmetric accumulation of information, which 254 depends on the size of its storage, still hold, with multiple and complex feedbacks, often 255 unexpected. For example, when we try to geo-engineer CO2 uptake by plants, these limits 256 and multiple feedbacks lead to ecosystem responses that may have counteracting effects 257 on the original objective17. CO2 uptake is accompanied by undesired changes in albedo 258 and latent and sensible heat, and desiccation of streams, among other energetic and 259 environmental costs to soil, water, air and land-use change and societal and ethical costs. 260 The actual solution to avoid increasing atmospheric CO2 concentrations is to reduce 261 carbon emissions. Other examples involve the availability and use of water or the design 262 and expansion of cities. As a city continues to grow, moving resources to the interior 263 becomes increasingly congested. Additional examples can come even from the 264 economical and societal worlds. These laws also apply to money to fund societal projects. 265 One cannot expect success by spending huge or unlimited amounts of money on a 266 problem. It takes time to build the infrastructure to use resources. 267 Life has adapted to these ecological laws and physical limits for billions of years, 268 and if we humans want to develop a sustainable world, we would do well to not forget 8 269 them in our use of space, matter and energy. In the end, we are only another biological 270 species among millions on Earth and are living in a very short period of Earth’s history. 271 We must also subscribe to the same rules and limits as all other forms of life. Management 272 strategies for sustainability must learn from living systems, such as trees or coral how to 273 deal with the ecological laws and principles. They have become structures and functions 274 optimized for their environments; they have learned how to adapt to what is available, to 275 recycle material and to extract energy from the environment in a sustainable way. We 276 should listen and learn lessons from nature that has had several billion years to evolve 277 and get it as right as possible. 278 279 280 281 Acknowledgments 282 The authors’ research is funded by the European Research Council Synergy grant SyG- 283 2013-610028 IMBALANCE-P, the Spanish Government project CGL2016-79835-P, the 284 Catalan Government project SGR 2017-1005, and the AmeriFlux Management Project of 285 the U.S. Department of Energy’s Office of Science under Contract No. DE-AC02- 286 05CH11231. 287 288 DATA ACCESSIBLITY 289 No data was used in the preparation of this essay manuscript 290 291 References 292 1. Terradas, J. & Penuelas, J. Evolution: Much More than Genetics. The Need for a 293 Holistic View. Open Evol. J. 3, 38–45 (2009). 294 2. Peñuelas, J. et al. The bioelements, the elementome and the “biogeochemical 295 niche”. Ecology in press (2019). 296 3. Dawkins, R. Selfish Gene. (Oxford University Press, New York, 1976). 297 4. Schneider, E. D. & Kay, J. J. 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