A limited habitable zone for complex life

The habitable zone (HZ) is defined as the range of distances from a host star within which liquid water, a key requirement for life, may exist at a planet's surface. Substantially more CO2 than present in Earth's modern atmosphere is required to maintain clement temperatures for most of the HZ, with concentrations of several bars required at the outer edge. However, most complex aerobic life on Earth is precluded by CO2 concentrations of just a small fraction of a bar. At the same time, most of the HZ volume resides in proximity to K and M dwarfs, which are more numerous than Sun-like G dwarfs but are predicted to promote greater abundances of CO in the atmospheres of orbiting planets, a highly toxic gas for complex aerobic organisms with circulatory systems. Here we show that the HZ for complex aerobic life is significantly limited relative to that for simple microbial life. We use 1-D radiative-convective climate and photochemical models to circumscribe the Habitable Zone for Complex Life (HZCL) based on known toxicity limits for a range of complex organisms. We find that for CO2 tolerances of 0.005-0.05 bar, the HZCL is only ~20-28% as wide as the traditional HZ for a Sun-like star and that CO concentrations may limit complex life throughout the entire HZ of the coolest M dwarfs. These results cast new light on the likely distribution of complex life in the universe and have important practical ramifications for the search for exoplanet biosignatures and technosignatures.


Introduction
The search for habitable environments and life beyond our solar system is a deeply compelling scientific goal, as evidenced by a focus on these areas in the recent National Academies of Sciences report on Exoplanet Science Strategy (National Academies of Sciences, Engineering 2018). To date, over 3,700 exoplanets have been discovered, some of which may possess conditions amendable for the emergence and maintenance of planetary biospheres (e.g., Anglada-Escudé et al. 2016;Gillon et al. 2017;Lincowski et al. 2018;Meadows et al. 2018;Ribas et al. 2016;Turbet et al. 2016;Wolf 2017). Discussions of the search for life beyond the solar system often begin with the circumstellar habitable zone (HZ)-the predicted range of distances from a star within which a planet with an N2-CO2-H2O atmosphere and a climate system stabilized by carbonate-silicate feedbacks can maintain surface temperatures conducive to the presence of liquid water (Kasting et al. 1993;Kopparapu et al. 2013;Walker et al. 1981). As conventionally defined, the inner edge of the HZ (IHZ) is delimited by the incident stellar flux above which a runaway (or moist) greenhouse occurs, while the outer edge of the HZ (OHZ) is determined by the 'maximum greenhouse,' an upper limit on the extent to which additional atmospheric CO2 can compensate for decreasing stellar flux (Figure 1). Figure 1. Estimated atmospheric CO2 at the outer edge of the Habitable Zone (OHZ). Shown in (a) are fits to a series of 1D radiative-convective climate models  in which the effective stellar flux (S/S0) required to maintain a surface temperature of 273 K is computed as a function of atmospheric pCO2 for a range of stellar hosts (with stellar effective temperatures denoted for each curve). The minimum S/S0 value for each curve corresponds to the atmospheric pCO2 at the OHZ for each star. Shown in (b) are atmospheric pCO2 values at the OHZ as a function of stellar effective temperature. The grey curve shows the power fit used to derive the ranges for atmospheric pCO2 at the OHZ shown [pCO2 = aTeff b ; a = 3.1563 x 10 -4 ; b = -0.963; r 2 = 0.997]. Crucially, the HZ is regarded as the future starting point for spectroscopic biosignature searches because habitable surfaces allow for significant exchange of gases between the biosphere and atmosphere Schwieterman et al. 2018). Moreover, potential biosignature yields for future flagship space-telescopes are based on our current understanding of the HZ Stark et al. 2014). However, the basic requirement for surface liquid water is predicated on a subset of the minimum requirements for simple, microbial biosphere, and limited attention has been paid to the conditions that may limit more complex life. For our purposes here, we consider "complex life" as encompassing relatively large (mm-to m-scale), tissue-grade aerobic heterotrophs with blood vascular (circulatory) systems, though some of our results may also be applicable to diploblastic organisms, like sponges, that rely entirely on diffusion of O2.
While some studies have analyzed the potentially impact of temperature on complex life within the HZ (Silva et al. 2016), none have considered the possible roles of CO2 and CO in limiting complex life in the HZ.
Here we explore potential limitations to complex life in the HZ. In Section 2, we compare the predicted CO2 concentrations at the outer edge of the habitable zone for FGKM stars to known physiological limits for complex, aerobic life on Earth. In Section 3, we use a 1-D photochemical model to predict likely CO concentrations for Earth-twins orbiting FGKM stars and compare these to known limits for CO toxicity. In Section 4, we use a 1-D radiative-convective climate model to predict limiting HZ boundaries for (progressively less conservative) CO2 limitations of 0.005, 0.05, and 1 bar and combine this with our results from Section 3 to propose a "Habitable Zone for Complex Life" (HZCL). We conclude with some implications of our results in Section 5.

Requirements of complex life and CO2 levels in the habitable zone
The origin and diversification of complex life on Earth is fundamentally tied to the rise of oxygen (O2) in our atmosphere and oceans (Lyons et al. 2014;Planavsky et al. 2014;Reinhard et al. 2016).
Physical and geochemical evidence for eukaryotes (complex cells with organelles) is absent from the rock record until after the earliest accumulation of free O2 in Earth's atmosphere ~2.3 billion years ago (Ga) (Knoll 2014;Luo et al. 2016), while the first metazoan (animal) life emerged only in the last ~700 million years (Erwin et al. 2011). Later, significant increases in biological complexity on Earth, such as the Cambrian Explosion (~542 Ma; Lee et al. 2013), occurred against the backdrop of a more strongly oxygenated planetary atmosphere. The metabolic oxidation of organic matter with O2 produces significantly more free energy than any other plausible respiratory process, and O2 is the only high-potential oxidant sufficiently stable to accumulate within planetary atmospheres (Catling et al. 2005). As a result, it is likely that the centrality of molecular O2 in the emergence and expansion of a complex biosphere on Earth is a general phenomenon (Catling et al. 2005). However, complex aerobic life can be strongly impacted by CO2 and CO-the latter of which is produced by CO2 photolysis and surface biological activity. Both are expected to be present in various concentrations throughout the HZ.
One of the fundamental assumptions underlying the conventional HZ is that the carbonate-silicate cycle, in which atmospheric CO2 levels are regulated by the effect of temperature on CO2 consumption during rock weathering, will act to modulate atmospheric CO2 concentrations (and thus surface temperatures) as a function of insolation (Walker et al. 1981). Near the inner edge of the habitable zone clement surface temperatures can be maintained at low CO2 concentrations similar to that of the modern Earth (tens to hundreds of ppm), but for the middle and outer regions of the HZ, atmospheric CO2 concentrations need to be much higher in order to maintain temperatures conducive for surface liquid water-up to many bars approaching the outer edge ( Figure 1). For example, coupled orbital and GCM studies of the ostensible HZ planet Kepler 62f have found that 3-5 bars of CO2 would be required to maintain clement surface conditions on the surface of the planet (Shields et al. 2016b), a value that is up to ~1000 times greater than any witnessed during the entire history of complex life on Earth (see Table 1).
However, elevated CO2 levels impose often severe physiological stress on complex aerobic organisms (Pörtner et al. 2004). Physiological responses to elevated CO2 (hypercapnia) can be complex, often interacting across molecular, cellular, and organismal scales (Azzam et al. 2010), but are most often regulated by respiratory acidosis and associated changes to ion buffering in internal fluids (Permentier et al. 2017). Indeed, physiological stress at elevated CO2 has been proposed as a significant causal factor in major mass extinctions on Earth (Knoll et al. 2007). High atmospheric CO2 also alters oceanic chemistry by lowering marine pH, with additional deleterious impacts on calcifying organisms (Bennett et al. 2016;Goodwin et al. 2014). Many of these impacts are predicted to occur as a result of anthropogenic CO2 emissions over the next century, the effects of which are dwarfed by predicted OHZ CO2 abundances.   We estimated the CO2 required at the outer edge of the conventional habitable zone as follows.
First, we calculate the atmospheric CO2 value corresponding to the minimum Seff at stellar effective temperatures of 2600 K, 3800 K, 4800 K, 5800 K, and 7200 K by fitting polynomial expressions to results from an ensemble of 1D radiative-convective climate models as presented in Kopparapu et al. (2013). This value represents the conventional 'maximum greenhouse limit' above which Rayleigh scattering by CO2 will lead to decreasing surface temperatures even as atmospheric CO2 increases. We then fit a power function to these discrete values for atmospheric CO2 at minimum Seff in order to derive a continuous function for the location of the maximum greenhouse limit as a function of stellar effective temperature (Figure 1). We remove the 2600 K result because it is effectively asymptotic at high atmospheric CO2, and because small errors in the polynomial fit at this effective temperature can lead to somewhat spurious results. Finally, we assume a range of effective temperature for each spectral class ( Table 2) and use this range to estimate atmospheric CO2 corresponding to the maximum greenhouse limit for each star. We can translate CO2 levels into estimated marine pH levels, which are also limiting for complex organisms (Bennett et al. 2016;Goodwin et al. 2014). Marine pH values are estimated based on atmospheric pCO2 using the csys3 package (Zeebe & Wolf-Gladrow 2001). We use the total pH scale with refit equilibrium constants from Mehrbach et al. (1973), and all calculations assume T = 25ºC, S = 35‰, and P = 1.01325 bar. We assume that on average the global ocean maintains saturation with respect to calcite (Wcal = 1):  (Zeebe & Wolf-Gladrow 2001). We note that assuming saturation with respect to aragonite (another polymorph of CaCO3) yields a higher estimated pH at a given atmospheric pCO2, but on the scale of our analysis this difference is minor.  Table 1). Grey bar shows the range of atmospheric pCO2 levels during the Phanerozoic (540 million years ago to the present) according to geochemical proxies (solid)) and time-dependent biogeochemical models (dashed). Colored symbols show estimated values for pCO2 at the outer edge of the habitable zone for F-, G-, K-, and M-type (red) stars. Upper scale shows marine pH assuming dissolved Ca 2+ concentrations of 10 and 40 mmol kg -1 .
When we compare the predicted atmospheric CO2 abundances for planets at the outer edge of the HZ for FGKM main-sequence stars (or pH equivalents) to levels of acute lethality in a range of complex organisms on Earth (Figure 2), we find that predicted atmospheric CO2 is over 3-4 orders of magnitude greater than the highest values observed during the last 500 million years on Earth.
The predicted CO2 at the OHZ boundary is also at least two orders of magnitude greater than the upper limits for even the most CO2-tolerant complex organisms known. Commonly proposed alternative greenhouse gases for extending the habitable zone (Pierrehumbert & Gaidos 2011;Ramirez & Kaltenegger 2017;Seager 2013)-CH4 and/or H2-are strongly reducing and thus chemically incompatible at high concentrations with the levels of O2 required for the energyintensive metabolisms of large, complex organisms (Catling et al. 2005). In short, the biological requirements for both high O2 and low CO2 suggests that the potential for the development and

CO toxicity and enhanced photochemical lifetimes for late-type stars
An additional obstacle to complex life may be found in high-O2 atmospheres on planets orbiting late-type stars, where certain photochemical conditions can lead to relatively high atmospheric CO levels (Schwieterman et al. 2019). CO is a highly toxic gas for complex organisms with circulatory systems because oxygen-carrying biomolecules like hemoglobin have orders of magnitude higher affinity for CO than for O2 (Liu et al. 2018;Ryter & Otterbein 2004). To illustrate this problem, we use a 1-D photochemical model to predict the CO concentrations for Earth twins (78% N2, 21% O2, 360 ppm CO2) orbiting FGKM stars and compare them to human toxicity limits. We use the photochemical component of the publicly available Atmos 1 model.
Atmos is derived from the photochemical code originally developed by the Kasting group (Kasting et al. 1979;Pavlov et al. 2001) but with several additions and modifications. More recently, the code has been used to calculate photochemically self-consistent atmospheres for the Archean Earth and hazy planets orbiting other stars (Arney et al. 2016(Arney et al. , 2017 and for calculating self-consistent trace gas abundances in the atmosphere of Proxima Centauri b . We began with a modern Earth converged atmosphere (1 bar, 78% N2, 21% O2 v/v, 360 ppm CO2) and used the model to calculate the CO concentration resulting from a net flux of 3 x 10 11 cm -2 s -1 (equivalent to 1,280 Tg/year). This is the CO flux required by the model to reproduce the empirical CO mixing ratio in Earth's atmosphere (1.1 x 10 -7 v/v). This value compares favorably with the empirically estimated terrestrial CO fluxes (745.67 -1112.80 Tg/year;Zhong et al. 2017), mostly generated by terrestrial biomass burning. The temperature-pressure and water vapor mixing ratio profiles are consistent with a planet with a surface temperature of 288 K. We then alter the input stellar spectrum while maintaining this surface flux to calculate a the resulting CO abundance, a procedure employed by similar studies Rugheimer et al. 2013;Segura et al. 2005). The stellar spectra used by the code are derived from prior studies in the literature (Lincowski et al. 2018;Meadows et al. 2018;Segura et al. 2005Segura et al. , 2003. Our complete list of boundary conditions is given in Table 3. We also calculated the resulting CO concentrations when multiplying this CO flux by factors of 0.1, 0.33, 3, and 10 to circumscribe a range of plausible CO concentrations on a world with a terrestrial biosphere and an oxygen-rich atmosphere (Figure 3; Table 4). Some of these results were previously presented in Schwieterman et al. (2019) in the context of predicting the spectroscopic detectability of CO on inhabited exoplanets. Figure 3. Steady state atmospheric mixing ratios of CO for Earth-like planets around a range of stellar hosts. Open circles show results for the modern net surface CO flux (3´10 11 molecules/cm 2 /s), while ranges show results of increasing/decreasing this flux by a factor of 3 (shaded bars) or 10 (horizontal lines). Also shown is the range between the short-term and long-term permissible exposure limits for humans (NIOSH 2005). Calculations are performed assuming an atmospheric pCO2 of 360 ppm (~3.6 x 10 -4 bar), consistent with CO2 levels predicted for the IHZ (both OHZ CO2 and CO levels may be higher). Note the log scale.
Our results show that CO concentrations on planets in the traditional HZ of FGK stars are unlikely to reach known toxicity limits for humans, at least in oxygen-rich atmospheres. However, for stars with effective temperatures below about 3,200 K-for example Proxima Centauri and TRAPPIST-1-predicted CO concentrations can reach and significantly exceed short and long-term human exposure limits. Because CO lifetimes are driven by destruction timescales set by OH (in O2-rich atmospheres), dry planets orbiting interior to the traditional HZ may be problematic for complex Trappist-1 [M8V] Proxima Centauri [M5V] ε Eridani [K1V] Sun [G2V] 10 -7 10 -5 10 -3 human limit life even around FGK stars (Abe et al. 2011;Gao et al. 2015;Zsom et al. 2013). In addition, cooler worlds with lower tropospheric H2O contents may have even higher CO concentrations than those shown here (Grenfell et al. 2007). Table 3. Boundary conditions for modeling atmospheric CO abundance for HZ planets around a range of stellar hosts in Atmos.

Chemical Species
Deposition velocity (cm s -1 ) Flux (molecules cm -2 s -1 ) profile is fixed to an Earth average **Species included in the photochemical scheme with a deposition velocity and flux of 0 include: C2H6, HS, S, SO, S2, S4, S8, SO3, OCS, S3, N, NO3, and N2O5. Table 4. Estimated atmospheric CO concentrations around select stars as a function of surface CO flux (FCO), scaled to that of the modern Earth (e.g., FCO = 1 for the modern Earth flux of 3 x 10 11 cm -2 s -1 ).

A habitable zone for complex life (HZCL)
Combining the potential impacts of high atmospheric CO2 and the potential for abundant CO around cooler host stars, we use a 1-D radiative-convective climate model, also a component of the Atmos package, to estimate the position of the "Habitable Zone for Complex Life" (HZCL).
For each case, we assume a 1-bar bulk atmosphere composed of 78% N2, 21% O2, and 1% Ar, with additional CO2 pressures (in bar) of 5 x 10 -3 , 5 x 10 -2 , and 1. We consider these CO2 partial pressures to encompass pessimistic and optimistic ranges for CO2 limitation of complex aerobic life (i.e., Figure 2), barring any currently unknown physiological mechanism for mitigating hypercapnia at extremely high CO2. We also assume a saturated troposphere, Earth's modern O3 profile, and a 200 K stratosphere. (Note that the HZ boundaries are dependent on the choice of stratospheric temperatures (Ramirez 2018b) -we use the modern Earth's because this is most consistent with stratospheric heating from ozone.) Assuming these parameters, we use the climate model to calculate the effective stellar flux (Seff) reaching the top of the planet's atmosphere required to warm the planetary surface to 273 K. We further derive a relationship between Seff and stellar effective temperatures, following Kopparapu et al. (2013): where T* = T -5780 K and coefficients for each scenario are listed in Table 5. These Seff values can be converted into distances by using the following equation: where L/L☉ is the bolometric luminosity of the host star normalized by the Sun's bolometric luminosity. Figure 4 compares our analytic fits from Equation 2 to the conservative traditional HZ boundaries, defining the inner habitable zone (IHZ) by the 'moist greenhouse' limit and the outer habitable zone (OHZ) by the 'maximum greenhouse' limit.  Table 5. Also shown for reference are the moist greenhouse and maximum greenhouse limits on the conventional habitable zone from Kopparapu et al. (2013). The polynomial fits to individual model runs are shown in Fig. 5.
We find that the HZCL is significantly restricted relative to the conventional HZ, even assuming an extremely high physiological CO2 limit of 1 bar. Figure 5 illustrates the combined impact of    and the "Habitable Zone for Complex Life (HZCL)" assuming limiting CO2 concentrations of 0.005 bar (dark green), 0.05 bar (lighter green), and 1 bar (lightest green). The red boundary represents stellar Teff < 3200K, where photochemical conditions may enhance CO lifetimes above the short-term permissible limits for humans, assuming a net surface molecular flux of 3´10 11 molecules/cm 2 /s. The positions of several exoplanets within the HZ have also been plotted.

Discussion and Conclusions
Our results have a number of important implications for the search for exoplanet biosignatures and complex life beyond our solar system. For example, our predictions of a more limited zone for complex life place constraints on the planetary environments suitable for the evolution of intelligent life, if it requires free O2 and limited concentrations of CO2 and CO. One implication is that we may not expect to find signs of intelligent life or technosignatures on planets orbiting late M dwarfs or on potentially habitable planets near the outer edge of their HZs. There are other habitability concerns with M dwarfs that may also apply to microbial life, which are summarized in a recent review (Shields et al. 2016a), however this is the first time CO limits have been suggested as an additional constraint. These CO2 and CO limits should be considered in future targeted SETI searches (Tarter 2001;Turnbull & Tarter 2003), at the very least as a prediction that can be tested. In addition, the need for significant greenhouse warming from reduced gases should rule out complex aerobic life, as well as remotely detectable O2 as a biosignature, from a large region of the expanded habitable zone (Ramirez 2018a;Seager 2013). More broadly, limitations on complex life by CO2 and CO may partially address why we find ourselves near the inner edge of the habitable zone of a G-dwarf star rather than near the center or towards the outer edge of the habitable zone around one of the much more numerous M-and K-type stars (Haqq-Misra et al.

2018; Waltham 2017).
Moving forward, it will be critical to use coupled 3-D climate-photochemical models to more accurately circumscribe the HZCL. Estimates of the conventional habitable zone boundaries have been shown to differ between 1-D and 3-D models due to a range of factors, including the impact of spatially variable surface albedo, atmospheric mass, surface gravity, rotation rate, continental area and distribution, and orbital parameters (Kopparapu et al. 2016;Wolf 2017). Nevertheless, our results highlight the importance of stellar environment and atmospheric photochemistry in constraining the planetary potential for complex life, and we suggest that consideration of the physiological impacts of high CO2 and CO should remain central in attempts to search for biological complexity beyond our solar system.