Albert Calbet- Institut de Ciències del Mar (ICM-CSIC), Barcelona, Spain
Mixotrophy, the ability to combine photosynthesis with heterotrophic acquisition of carbon or nutrients, is now recognized as a central feature of aquatic microbial food webs and a recurrent strategy in several protist and simple animal lineages. By contrast, terrestrial ecosystems host only a narrow set of mixotrophic plants, and no animal is known to rely substantially on endogenous photosynthesis or plastids over its life cycle. Here I argue that this asymmetry is not paradoxical once mixotrophy is viewed through three coupled filters: ecological state spaces, evolutionary accessibility and physiological feasibility. I outline how these filters differ between water and land, how they jointly compress the adaptive zone for mixotrophy after terrestrialization, and how they generate explicit, testable predictions for future empirical and theoretical work on dual nutritional strategies.
Introduction
In aquatic ecosystems, mixotrophy has shifted from being treated as a minor curiosity to a central organizing principle of plankton ecology. Surveys, experiments and models now show that many marine and freshwater protists combine photosynthesis with prey ingestion, or periodically acquire plastids or phototrophic symbionts, forming a diverse “mixoplankton” guild that blurs the classical autotroph–heterotroph dichotomy (Flynn et al., 2019; Mitra et al., 2014; Millette et al., 2023). These organisms can reallocate effort between light-driven carbon fixation and prey-derived carbon and nutrients, with consequences for microbial loops, bloom dynamics and carbon export (Mitra et al., 2014; Leles et al., 2021).
More broadly, mixotrophy encompasses a spectrum of strategies that combine phototrophy with alternative nutritional pathways, including osmotrophy, symbiotrophy, parasitism, or externalized heterotrophic interfaces (Selosse et al., 2017; Duhamel et al., 2018; Mitra et al., 2016). In this manuscript, however, the focus is deliberately placed on the coupling of photosynthesis and phagotrophy, because this form of mixotrophy shows the strongest contrast between aquatic and terrestrial realms and provides the clearest mechanistic link between resource geometry, evolutionary accessibility, and physiological feasibility (Flynn et al., 2019; Mitra et al., 2023).
This perspective is grounded in ecological stoichiometry, in which mismatches between the supply of carbon, nitrogen, phosphorus and other essential elements constrain growth and shape trophic strategies (Sterner and Elser, 2002). Trait-based and state-space models show that dual nutrition is selectively favored precisely under such stoichiometric and energetic imbalances, for example when light is plentiful but dissolved nitrogen or phosphorus are scarce, or when microbial prey remain available during periods of low light (Berge et al., 2017; Edwards, 2019; Moeller et al., 2024). Under realistic costs and trade-offs, mixotrophs can maintain positive growth where strict phototrophs are nutrient-limited and strict phagotrophs are carbon- or energy-limited, thereby expanding their realized niche and reshaping community structure from the organismal to the community scale (Edwards, 2019; Millette et al., 2023; Mitra et al., 2016; Schenone et al., 2024).
Against this aquatic backdrop, the terrestrial distribution of mixotrophy is strikingly narrow. Land plants have evolved partial heterotrophy repeatedly, but mostly via three externalized routes: mycoheterotrophy or partial mycoheterotrophy, where carbon and nutrients flow through fungal networks; hemiparasitism, where haustoria tap host resources while photosynthesis is retained; and carnivory, where captured prey alleviate nutrient limitation in poor soils (Selosse et al., 2017; Tešitel et al., 2018; Ellison, 2006; Lin et al., 2025). These clades occupy small fractions of plant diversity and are strongly associated with deep shade, nutrient-poor soils or crowded understories (Hynson et al., 2016; Castaldi et al., 2023).
Animals show an even sharper asymmetry. Some aquatic metazoans—most famously corals and other cnidarians—host photosymbionts that provide substantial carbon and nutrient subsidies (Venn et al., 2008; Liao et al., 2025). A few molluscs, notably sacoglossan sea slugs, sequester chloroplasts (“kleptoplasts”) from algae and maintain them for weeks to months (Cartaxana et al., 2017; Cartaxana et al., 2021; Cruz and Cartaxana, 2022). On land, the pea aphid Acyrthosiphon pisum represents an intriguing but limited case: light-dependent electron transfer and ATP synthesis can be mediated by carotenoids in its integument (Valmalette et al., 2012), yet this falls far short of plastid-based photosynthesis and appears to provide at most a modest energetic supplement. No terrestrial animal is known whose energy budget is substantially supported by endogenous photosynthesis over its life cycle.
Selosse et al. (2017) captured part of this contrast in the “grand écart” hypothesis, emphasizing that both realms generate mismatches between light and mineral nutrients, but terrestrial mixotrophy occupies only a few highly constrained niches. Here, I extend that perspective by asking a simple question with broad implications: why did mixotrophy become ubiquitous and functionally central in photic waters, but remain exceptional and small-bodied after terrestrialization?
I argue that the answer lies in three coupled filters:
1. Ecological filter (state space). Water repeatedly decouples light, nutrients and prey in ways that make dual acquisition profitable, whereas on land this kind of decoupling is rarer at the scale of individual organisms.
2. Evolutionary filter (accessibility). Aquatic mixotrophy was repeatedly accessible to phagotrophic protists via plastid acquisition and photosymbiosis. Land plants, having lost phagotrophy early, could re-enter mixotrophy only via externalized heterotrophic interfaces.
3. Physiological filter (volatility and scaling). Terrestrial light and water regimes increase oxidative and desiccation costs of auxiliary photosystems, and in animals surface-area-limited photosynthesis cannot easily meet volume-linked metabolic demand.
Taken together, the ecological state space created by water, the evolutionary accessibility of phagotrophy-based pathways, and the physiological constraints imposed by volatility and scaling act in concert to favor the repeated emergence and persistence of mixotrophy in aquatic systems, while rendering it rare, indirect, or strongly constrained on land, even where ecological opportunity exists. Below, I develop each filter in turn and then discuss how they combine into a cross-realm framework with explicit predictions and open questions.
Ecological filters: resource state spaces in water and on land
Aquatic photic environments place organisms in a resource geometry that repeatedly makes dual acquisition profitable. In the euphotic zone, light, dissolved nutrients and prey biomass are only loosely coupled across depths, seasons and microhabitats. Stratification concentrates light near the surface but traps macronutrients at depth; upwelling and mixing episodically inject nutrients into illuminated layers; and bacteria and small phytoplankton persist as particulate targets even when dissolved nutrients are depleted (Unrein et al., 2014; Berge et al., 2017; Edwards, 2019). The result is a mosaic of “imbalanced regimes” in which strict phototrophs can be carbon-replete yet nutrient-starved, whereas strict heterotrophs can be nutrient-replete but energy-limited when prey encounter or quality declines.
State-space and trait-based models show that mixotrophs gain a selective edge precisely in these regimes because they can substitute between light-driven carbon fixation and prey ingestion for nutrients and, in some cases, carbon (Hartmann et al., 2012; Berge et al., 2017; Edwards, 2019; Moeller et al., 2024). In simulations where trade-offs are imposed between investment in phototrophic and phagotrophic machinery, mixotrophs outperform both specialists across broad swaths of aquatic conditions, especially at intermediate sizes where diffusion, light harvesting and prey encounter are simultaneously feasible (Berge et al., 2017; Moeller et al., 2024). These results echo earlier work on the role of mixotrophic protists in the biological carbon pump, but recast it in a more formal trait-based framework (Mitra et al., 2014).
Field studies broadly corroborate this ecological “wet advantage”. In oligotrophic subtropical gyres and stratified lakes, mixotrophic nanoflagellates and dinoflagellates often dominate where light is sufficient but dissolved inorganic nutrients are low and microbial prey persist (Edwards, 2019; Millette et al., 2023; Figure 1). Comparable dominance and plasticity of mixotrophic protists have been documented in Polar and subpolar waters, where extreme seasonality in light and persistent nutrient–light decoupling favor dual nutritional strategies despite cold temperatures (Norbury et al., 2019; Gast et al., 2007; Søgaard et al., 2021).
Figure 1. Resource state space for aquatic and terrestrial mixotrophs. Conceptual three‐axis diagram showing how light availability, mineral nutrient availability and prey/partner availability shape where different mixotrophic strategies are expected to thrive. Aquatic mixoplankton occupy a broad, mid-light region at low mineral nutrients and moderate to high prey availability, where dual use of photosynthesis and phagotrophy is profitable. Photosymbiotic animals (e.g. corals and sponges with algal symbionts) are placed in similarly high-light, low-nutrient but relatively prey-rich conditions, where symbiont photosynthesis can substantially subsidize heterotrophic feeding. On land, mycoheterotrophic plants occur under low light but relatively high below-ground partner availability, hemiparasites in high-light habitats with reliable host access, and carnivorous plants where light is ample but soils are extremely nutrient-poor and animal prey are available. Together, these distributions illustrate that water offers a wide “plateau” of profitable mixotrophic conditions, whereas terrestrial mixotrophs occupy a few narrow ridges of strong, persistent resource decoupling.
Experiments show rapid plastic shifts toward grazing under nutrient stress and toward photosynthesis under prey scarcity, consistent with optimal switching along a phototrophy–phagotrophy continuum (Millette et al., 2023; González-Olalla et al., 2019). Warming and ultraviolet radiation modulate this balance but generally do not eliminate the advantage of duality under nutrient–light mismatch; instead, they shift mixotrophs along the continuum of reliance (González-Olalla et al., 2019). Evidence from freshwater ecosystems reinforces this view. In stratified lakes, mixotrophic nanoflagellates and dinoflagellates often dominate under conditions of high light availability, low dissolved nutrients and persistent bacterial prey, particularly during summer stratification (Laybourn-Parry et al., 2000; Jones, 2000). Experimental and field studies have repeatedly shown that mixotrophs outcompete strict phototrophs under nutrient limitation and strict heterotrophs under prey or energy limitation, mirroring patterns observed in marine systems (Kamjunke et al., 2006; Katechakis and Stibor, 2006; Princiotta et al., 2023).
On land, comparable three-way decoupling is rarer at the scale of individual plants and animals. Terrestrial primary producers experience chronic nutrient limitation, but potential prey are not a continuously suspended three-dimensional resource; they are localized and patchy. Carbon limitation is often alleviated by atmospheric CO2 diffusion and canopy structure, not by ingesting prey. As a result, heterotrophic supplements tend to be favored only where one resource is both strongly and persistently limiting and where mechanical opportunities exist to tap alternative pools: deep shade with access to fungal carbon networks, highly oligotrophic soils where animal prey can be trapped, or competitive communities where parasitic haustoria can reliably access host tissues (Ellison, 2006; Selosse et al., 2017; Tešitel et al., 2018).
The distribution of terrestrial plant mixotrophs fits this pattern (Figure 1). Mycoheterotrophic and partially mycoheterotrophic orchids and ericaceae are concentrated in shaded forests and nutrient-poor habitats, where stable fungal carbon pools compensate for light limitation (Hynson et al., 2016; Selosse et al., 2017). Hemiparasites often occur in species-rich, high-light communities where host connections alleviate water or nutrient stress rather than carbon limitation (Tešitel et al., 2018). Carnivorous plants are disproportionately found in nutrient-impoverished wetlands, where prey capture relieves nitrogen and phosphorus limitation but typically contributes modestly to total carbon gain (Ellison, 2006; Lin et al., 2025).
Benthic aquatic habitats may appear, at first glance, to be the marine environments most closely resembling terrestrial systems. Although light is spatially structured and often strongly attenuated near the sediment–water interface, benthic environments retain key aquatic features such as persistent hydration, high microbial prey availability, and relatively buffered thermal and irradiance regimes. These conditions sustain dense microbial and protistan communities and favor trophic interactions broadly similar to those of pelagic systems, despite stronger spatial heterogeneity (Fenchel, 1969; Azam and Malfatti, 2007; Glud, 2008). Consequently, the ecological filters acting on benthic mixotrophs more closely resemble those of pelagic environments than those of land (Epstein, 1997; Battin et al., 2016).
In summary, the state space in which internal dual acquisition is profitable is broad, frequently encountered and three-dimensional in the photic ocean, but narrow and habitat-restricted on land. This ecological filter does not make terrestrial mixotrophy impossible, but it confines it to a few “ridges” of strong, persistent resource decoupling, whereas in water the same geometry forms an extensive plateau.
Evolutionary filters: phagotrophic gateways and walled body plans
Ecology sets the stage, but evolutionary history determines which strategies are accessible. In aquatic microbes, the dominant paths to mixotrophy—constitutive phototrophy plus phagotrophy in the same cell, kleptoplasty and stable or semi-stable photosymbioses—are all built on an ancestral capacity to capture and process prey. Phagotrophy is the gateway through which plastids and phototrophic symbionts repeatedly entered eukaryotic cells (Archibald, 2015; Miyagishima, 2023).
Endosymbiotic events and serial plastid acquisitions, largely mediated by phagotrophic hosts, spread photosynthesis across the eukaryotic tree (Archibald, 2015; Mansour and Anestis, 2021). Within these phototrophic lineages, a rich spectrum of mixotrophic strategies evolved as ancestral phagotrophic toolkits were modified rather than abandoned, leading to the modern diversity of mixoplankton (Flynn et al., 2019; Mitra et al., 2023; Mansour and Anestis, 2021). In aquatic settings, high encounter rates with phototrophic prey create many opportunities for selection to favor plastid retention, symbiont management or trophic switching whenever ecological payoffs are positive (Edwards, 2019; Moeller et al., 2024).
Land plants, by contrast, entered terrestrial ecosystems with a very different cellular legacy. The green plant lineage (Streptophyta) derives from algae in which strong cell walls and glucan-rich matrices supported multicellularity and increasing reliance on external nutrient uptake well before full terrestrialization (Bowles et al., 2023). True phagotrophy appears to have been greatly reduced or lost; the ancestral toolkit emphasized photoautotrophy and extracellular interfaces, such as cell walls and symbioses, rather than intracellular prey capture (Bowles et al., 2023). Once multicellular development became organized around walled cells, evolutionary re-entry into intracellular phago-mixotrophy would have required dismantling core developmental and structural constraints.
This history helps explain why terrestrial plant mixotrophy rarely involves reclaiming a protist-like dual nutrition. Later-evolving plant mixotrophs acquire heterotrophic supplements via externalized interfaces that preserve the walled body plan: carbon and nutrients flow through mycorrhizal fungi in mycoheterotrophs (Julou et al., 2005; Hynson et al., 2016; Suetsugu et al., 2020), through haustorial connections in hemiparasites (Tešitel et al., 2018), or via externally digested prey in carnivorous plants (Ellison, 2006; Lin et al., 2025). In many of these species, heterotrophy primarily relieves nutrient limitation while photosynthesis remains essential for reproductive success, consistent with the view that they occupy narrow ridges of state space where one limiting axis is extreme rather than a broad dual-nutritional regime (Tešitel et al., 2018; Castaldi et al., 2023).
Terrestrial animals present a complementary case. They have retained phagotrophy, but multicellularity, differentiated immunity and complex development mean that plastid or algal integration requires stable, regulated endosymbiosis at tissue and organismal scales (Venn et al., 2008; Liao et al., 2025). Aquatic animals have achieved this only in a limited set of lineages, such as cnidarians and sponges with endosymbiotic dinoflagellates, and a few molluscs or simple worms with photosymbionts or kleptoplasts (Venn et al., 2008; Cartaxana et al., 2017; Cruz and Cartaxana, 2022). These partnerships show that animal tissues can host photosynthetic machinery, but they also reveal that maintaining functional photosystems without full access to algal nuclear support is difficult and often transient (Schmitt et al., 2014; Cartaxana et al., 2021; Havurinne et al., 2021).
Physiological filters: volatility, scaling and the cost of duality
Even when ecological payoffs and evolutionary routes align, life on land imposes a fundamentally physiological third filter. Photosynthesis is energetically generous, but it is also intrinsically risky: whenever absorbed light exceeds downstream metabolic use, photosystems generate reactive oxygen species. Aquatic photic environments buffer this risk by keeping cells hydrated, moderating temperature fluctuations and attenuating light with depth, which allows photoprotection and repair to operate continuously (Murchie and Niyogi, 2011; Derks et al., 2015).
Terrestrial environments, by contrast, repeatedly expose phototrophs and any potential hosts of photosymbionts to intense and rapidly fluctuating irradiance, temperature swings and episodic dehydration. Work on terrestrial plants shows that fluctuating light and desiccation amplify oxidative stress, forcing large investments into non-photochemical quenching, antioxidant systems and repair cycles that reduce net carbon gain (Murchie and Niyogi, 2011; Derks et al., 2015; Zhang et al., 2021). Desiccation is especially problematic for intracellular photosymbioses or plastids, because drying disrupts electron transport, concentrates solutes and triggers bursts of reactive oxygen species that can damage both host and symbiont unless elaborate protective systems are in place (Holzinger and Karsten, 2013; Gasulla et al., 2021). Lichen photobionts exemplify how much photoprotective machinery and structural buffering are required to keep photosystems functional under repeated drying and high irradiance (Beckett et al., 2021).
For free-living land plants, these costs are high but manageable because the entire architecture—cuticles, stomata, vascular tissues and growth form—is tuned to water management and photoprotection (Bowles et al., 2023; Chauhan et al., 2023). For a would-be mixotrophic plant or animal attempting to maintain photosystems as an auxiliary module, however, the same volatility can become a disproportionate liability if photosynthesis is not the core metabolic engine. The rarity of stable photosymbioses on land, and their confinement to buffered microhabitats such as lichens, shaded bark surfaces or persistently moist soils, fits this picture (Beckett et al., 2021; Chauhan et al., 2023).
Body-plan scaling sharpens the constraint in animals. Photosynthetic carbon gain scales with exposed surface area, whereas metabolic demand scales with volume and is further elevated on land by locomotion against gravity, thermoregulation and water-balance costs. Biophysical analyses of hypothetical “green animals” and real photosymbiotic metazoans show that even in water, plastid-supported nutrition is only substantial in very thin, low-demand organisms and usually functions as a starvation buffer rather than a primary energy source (Rauch and Redelberger, 2017).
Reef-building corals illustrate how these constraints can be temporarily overcome in aquatic settings. Colonial cnidarians host very high densities of intracellular dinoflagellate symbionts (Symbiodiniaceae) in a thin layer of tissue wrapped around a calcareous skeleton. In clear, warm, oligotrophic waters, translocated photosynthate from the symbionts can meet most of the host’s daily carbon requirements, while nocturnal suspension feeding and dissolved nutrient uptake supply nitrogen and phosphorus that sustain both partners. Corals are therefore strongly mixotrophic: they rely on light for the bulk of their carbon, but heterotrophic feeding is crucial to close nutrient budgets and to buffer short-term light stress (Venn et al., 2008). At the same time, the geometry that makes this strategy feasible—thin tissues with high surface area relative to living biomass and intimate coupling between host and symbiont—also makes it vulnerable: modest increases in temperature or light can destabilize photosystems and trigger bleaching, underlining how narrow the tolerance window is for metazoan mixotrophy. A very similar logic applies to photosymbiotic sponges and other reef holobionts: dense microbial or algal symbionts in thin tissues or canal systems can provide substantial carbon subsidies in clear, oligotrophic, well-flushed waters, while heterotrophic pumping and filtration supply nitrogen and phosphorus. As with corals, these systems are highly productive yet physiologically fragile, with relatively narrow thermal and light tolerance windows.
Kleptoplastic sacoglossan sea slugs make this explicit. Stolen plastids remain photosynthetically active for weeks to months and measurably extend survival during starvation in some species (Cartaxana et al., 2017, Cartaxana et al., 2021). Yet plastids lack access to the algal nucleus and its repair machinery, so their performance decays over time and must be renewed by repeated ingestion of algal prey (Schmitt et al., 2014; Havurinne et al., 2021; Maeda et al., 2021). Genomic and physiological work shows that even in long-term retaining species, plastids are not fully integrated organelles; their persistence depends on plastid-intrinsic resilience and host adaptations that limit oxidative damage (Havurinne et al., 2021; Eastman et al., 2023). Experiments manipulating light and food indicate that photosynthesis can extend survival in the absence of algal prey but rarely supports growth or reproduction on its own (Cartaxana et al., 2017; Laetz and Wägele, 2017; Cartaxana et al., 2021). The geometry of these animals—flat, leaf-like and slow-moving—maximizes surface area relative to volume and keeps demand low, underscoring how tightly their body plan is tuned to the narrow window in which kleptoplasty is worthwhile (Rauch and Redelberger, 2017).
Taking these threads together, aquatic photosymbioses and kleptoplasty suggest that metazoan mixotrophy is already near the edge of feasibility in water (Venn et al., 2008; Cruz and Cartaxana, 2022; Rauch and Redelberger, 2017). Transplanting the same strategies into air would intensify irradiance peaks, introduce frequent dehydration and increase basal metabolic costs, shifting the supply–demand balance further against internal photosynthesis. Under terrestrial conditions, physiological economics tend to favor either full commitment to photosynthesis with robust water management, or full commitment to heterotrophy with no photosystems to protect. Dual strategies persist mainly when heterotrophic supplements are externalized (fungi, haustoria, traps) or when microhabitats remain persistently wet and buffered.
Discussion
The cross-realm asymmetry in mixotrophy is less a paradox than the outcome of three interacting constraints: where organisms sit in resource state space, which trophic tools their lineages bring into that space, and how the physical environment sets the costs of running those tools. In water, light, dissolved nutrients and prey are decoupled often enough—and prey are continuously encounterable—that dual internal acquisition frequently pays off, especially for small and intermediate protists. On land, similar three-way decoupling is rare at the scale of individual plants and animals and tends to be confined to deep shade, nutrient-poor soils or other extreme niches. At the same time, aquatic microbial lineages evolved in the immediate neighborhood of the phagotrophic “gateway” into mixotrophy, whereas land plants committed early to walled multicellularity and externalized uptake interfaces, making re-entry into intracellular mixotrophy highly improbable. Add to this that terrestrial volatility and surface-area/volume scaling make auxiliary photosystems expensive to protect unless they are central to metabolism, and the pattern becomes unsurprising: mixotrophy occupies a wide plateau in the photic ocean but only a few narrow ridges on land (Archibald, 2015; Selosse et al., 2017; Bowles et al., 2023; Tešitel et al., 2018).
Seen this way, terrestrial “exceptions” look less like anomalies and more like expected survivors where these constraints intersect favorably. Mycoheterotrophs, hemiparasites and carnivorous plants sit in habitats with strong resource decoupling and exploit externalized interfaces—fungal networks, haustoria, digestive traps—rather than rebuilding a phagotrophic cell (Julou et al., 2005; Ellison, 2006; Suetsugu et al., 2020). Kleptoplastic sea slugs, photosymbiotic cnidarians and carotenoid-based light-harvesting aphids similarly mark the feasibility edge for animal mixotrophy: they show that animal tissues can host or exploit photosystems for ecologically meaningful benefits, but only under very specific geometries and environmental conditions, and usually as a starvation buffer rather than a primary energy source (Venn et al., 2008; Rauch and Redelberger, 2017; Valmalette et al., 2012; Eastman et al., 2023). In that sense, the question is not why “green animals” failed to spread on land, but why dual strategies did so well in the ocean.
The same framework has clear implications for future change. In the sea, warming and stronger stratification are expected to deepen and prolong nutrient–light decoupling in many regions, expanding the volume of state space where light is available, dissolved nutrients are scarce and microbial prey persist (Leles et al., 2021; Millette et al., 2023; Moeller et al., 2024). Deep lakes further strengthen the analogy with the oceanic case in the context of climate change. Ongoing warming has intensified and prolonged thermal stratification in many deep lakes, increasing the vertical decoupling of light and nutrients and reducing nutrient resupply to surface waters, while episodic mixing events continue to occur seasonally or interannually (Sommer et al., 2012; O’Reilly et al., 2015). At the same time, microbial communities persist throughout the water column and exhibit strong vertical and seasonal structuring, maintaining a continuous pool of potential prey despite enhanced stratification (Salcher, 2014). Together, these climate-driven changes generate recurrent ecological windows in which dual nutritional strategies may be favored, positioning deep lakes as inland analogues of a warming, increasingly stratified ocean.
Supporting this, trait-based and ecosystem models predict that sustained decoupling of light, nutrients and prey will favor organisms that can switch between phototrophy and phagotrophy, with cascading consequences for trophic transfer, mean organism size and vertical carbon flux (Edwards, 2019; Ward and Follows, 2016). Complementary adaptive-evolution and experimental studies show that mixotrophic phytoplankton can respond to warming by shifting their metabolic balance toward greater grazing and reduced photosynthesis, potentially altering their ecological and biogeochemical roles under future climates (Lepori-Bui et al., 2022). Recent theoretical work using adaptive-dynamics and trait-based frameworks further predicts that rising temperatures should, in many cases, select for increased investment in heterotrophy by mixotrophs, amplifying impacts on trophic transfer and carbon cycling unless constrained by prey depletion (Gonzalez et al., 2022; Barbaglia et al., 2024). If these projections hold broadly, the “wet advantage” of mixotrophy could strengthen under climate change, making dual nutrition increasingly central to plankton ecology and biogeochemistry.
On land, many climate scenarios point in the opposite direction for auxiliary photosystems. More frequent and intense droughts, heat waves and light extremes are likely to increase oxidative and desiccation stress on any photosynthetic machinery that is not backed by a fully optimized plant-style water management and photoprotection architecture (Murchie and Niyogi, 2011; Gasulla et al., 2021; Chauhan et al., 2023). This should tighten the physiological filter against internal duality and restrict plant mixotrophy even more strongly to buffered refugia: cool, moist forests with stable mycorrhizal networks; nutrient-poor wetlands where carnivory pays despite volatility; or closed canopies where fungal carbon can reliably substitute for light. Shifts in forest composition, mycorrhizal associations and soil nutrient regimes may redistribute these opportunities geographically, but are unlikely to generate broad new adaptive zones for intracellular mixotrophy in plants or photosymbiosis in terrestrial animals.
Testing and refining this picture will require bringing cross-realm comparisons into the same quantitative frameworks. One priority is “state-space mapping” that couples local measurements of light, inorganic nutrient supply, prey or partner availability and moisture persistence to independent estimates of mixotrophic reliance (for example, stable-isotope–derived carbon fractions or prey uptake rates). Such datasets could reveal whether terrestrial plant mixotrophs truly occupy a narrow, high-decoupling tail of a shared resource geometry, as suggested here, or whether the effective resource axes themselves differ so much between realms that they are only partly comparable (Edwards, 2019; Selosse et al., 2017). A second priority is route-resolved comparative phylogenetics: coding carbon acquisition mechanisms as intracellular versus externalized would allow tests of how irreversible the loss of phagotrophy has been in plants, and whether loss of photosynthesis in both protists and plants is typically preceded by a mixotrophic stage (Bowles et al., 2023; Tešitel et al., 2018).
Finally, physiological experiments that deliberately push the limits of duality will be key. Exposing aquatic mixotrophs or synthetic photosymbioses to controlled “terrestrialized” volatility regimes—fluctuating high light, episodic desiccation, large temperature swings—could quantify when auxiliary photosystems stop paying their way, complementing biophysical models that scale photosynthetic supply and metabolic demand for realistic body plans (Murchie and Niyogi, 2011; Rauch and Redelberger, 2017). Together with climate-aware models of resource state space, such work would turn the question “why did mixotrophy mostly stay wet and small?” into a broader predictive framework—one that not only explains current distributions but also anticipates how dual strategies will respond as oceans stratify, continents dry and the boundaries of habitability shift.
Author contributions
AC: Writing – original draft, Writing – review & editing.
Funding
The author(s) declared that financial support was received for this work and/or its publication. This research was funded by Grant PID2023-150548NB-I00 by MICIU/AEI/10.13039/5011 00011033 and “ERDF/EU. We acknowledge support of the publication fee by the CSIC Open Access Publication Support Initiative (PROA) through its Unit of Information Resources for Research (URICI).
Acknowledgments
This study acknowledges the “Severo Ochoa Centre of Excellence” accreditation (CEX2019-000928.S), and the Marine Plankton Ecology research group (2021 SGR 00427). This article is a contribution from the Marine Zooplankton Ecology Laboratory at the ICM (CSIC). During the preparation of this work, the author used ChatGPT to review and edit the language and style. After using this tool, the author reviewed and edited the content as needed.
Conflict of interest
The author(s) declared that this work was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The author AC declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.
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References
Archibald J. M. (2015). Endosymbiosis and eukaryotic cell evolution. Curr. Biol. 25, R911–R921. doi: 10.1016/j.cub.2015.07.055
Azam F. and Malfatti F. (2007). Microbial structuring of marine ecosystems. Nat. Rev. Microbiol. 5, 782–791. doi: 10.1038/nrmicro1747
Barbaglia G. S., Paight C., Honig M., Johnson M. D., Marczak R., Lepori-Bui M., et al. (2024). Environment-dependent metabolic investments in the mixotrophic chrysophyte Ochromonas. J. Phycol. 60, 170–184. doi: 10.1111/jpy.13418
Battin T. J., Besemer K., Bengtsson M. M., Romani A. M., and Packmann A. I. (2016). The ecology and biogeochemistry of stream biofilms. Nat. Rev. Microbiol. 14, 251–263. doi: 10.1038/nrmicro.2016.15
Beckett R. P., Minibayeva F. V., Solhaug K. A., and Roach T. (2021). Photoprotection in lichens: adaptations of photobionts to high light. Lichenologist 53, 21–33. doi: 10.1017/S0024282920000535
Berge T., Chakraborty S., Hansen P. J., and Andersen K. H. (2017). Modeling succession of key resource-harvesting traits of mixotrophic plankton. ISME J. 11, 212–223. doi: 10.1038/ismej.2016.92
Bowles A. M. C., Williamson C. J., Williams T. A., Lenton T. M., and Donoghue P. C. J. (2023). The origin and early evolution of plants. Trends Plant Sci. 28, 312–329. doi: 10.1016/j.tplants.2022.09.009
Cartaxana P., Rey F., LeKieffre C., Lopes D., and Hubas C. (2021). Photosynthesis from stolen chloroplasts can support sea slug metabolism. Proc. R. Soc B. 288, 20211779. doi: 10.1098/rspb.2021.1779
Cartaxana P., Trampe E., Kühl M., and Cruz S. (2017). Kleptoplast photosynthesis is nutritionally relevant in the sea slug Elysia viridis. Sci. Rep. 7, 7714. doi: 10.1038/s41598-017-08002-0
Castaldi V., Bellino A., and Baldantoni D. (2023). The ecology of bladderworts: The unique hunting–gathering–farming strategy in plants. Food Webs 35, e00273. doi: 10.1016/j.fooweb.2023.e00273
Chauhan J., Singh P., Choyal P., Mishra U., Saha D., Kumar R., et al. (2023). Plant photosynthesis under abiotic stresses: Damages, adaptive, and signaling mechanisms. Plant Stress 10, 100296. doi: 10.1016/j.stress.2023.100296
Cruz S. and Cartaxana P. (2022). Kleptoplasty: getting away with stolen chloroplasts. PloS Biol. 20, e3001857. doi: 10.1371/journal.pbio.3001857
Derks A., Schaven K., and Bruce D. (2015). Diverse mechanisms for photoprotection in photosynthesis. Dynamic regulation of photosystem II excitation in response to rapid environmental change. Biochim. Biophys. Acta 1847, 468–485. doi: 10.1016/j.bbabio.2015.02.008
Duhamel S., Van Wambeke F., Lefèvre D., Benavides M., and Bonnet S. (2018). Mixotrophic metabolism by natural communities of unicellular cyanobacteria in the western tropical South Pacific Ocean. Environ. Microbiol. 20, 2743–2756. doi: 10.1111/1462-2920.14111
Eastman K. E., Pendleton A. L., Shaikh M. A., Suttiyut T., Ogas R., Tomko P., et al. (2023). A reference genome for the long-term kleptoplast-retaining sea slug Elysia crispata morphotype clarki. G3 Genes|Genomes|Genetics 13, jkad234. doi: 10.1093/g3journal/jkad234
Edwards K. F. (2019). Mixotrophy in nanoflagellates across environmental gradients in the ocean. Proc. Natl. Acad. Sci. U.S.A. 116, 6211–6220. doi: 10.1073/pnas.1814860116
Ellison A. M. (2006). Nutrient limitation and stoichiometry of carnivorous plants. Plant Biol. 8, 740–747. doi: 10.1055/s-2006-923956
Epstein S. (1997). Microbial food webs in marine sediments. I. Trophic interactions and grazing rates in two tidal flat communities. Microb. Ecol. 34, 188–198. doi: 10.1007/s002489900048
Fenchel T. (1969). The ecology of marine microbenthos IV. Structure and function of the benthic ecosystem, its chemical and physical factors and the microfauna commuities with special reference to the ciliated protozoa. Ophelia 6, 1–182. doi: 10.1080/00785326.1969.10409647
Flynn K. J., Mitra A., Anestis K., Anschütz A. A., Calbet A., Ferreira G. D., et al. (2019). Mixotrophic protists and a new paradigm for marine ecology: where does plankton research go now? J. Plankton Res. 41, 375–391. doi: 10.1093/plankt/fbz026
Gast R. J., Moran D. M., Dennett M. R., and Caron D. A. (2007). Kleptoplasty in an antarctic dinoflagellate. J. Phycol. 43, 605–613. doi: 10.1111/j.1462-2920.2006.01109.x
Gasulla F., Del Campo E. M., Casano L. M., and Guéra A. (2021). Advances in understanding of desiccation tolerance of lichens and lichen-forming algae. Plants (Basel). 10, 807. doi: 10.3390/plants10040807
Glud R. N. (2008). Oxygen dynamics of marine sediments. Mar. Biol. Res. 4, 243–289. doi: 10.1080/17451000801888726
Gonzalez L. M., Proulx S. R., and Moeller H. V. (2022). Modeling the metabolic evolution of mixotrophic phytoplankton in response to rising ocean surface temperatures. BMC Ecol. Evo. 22, 136. doi: 10.1186/s12862-022-02092-9
González-Olalla J. M., Medina-Sánchez J. M., and Carrillo P. (2019). Mixotrophic trade-off under warming and ultraviolet radiation in a marine and a freshwater alga. J. Phycol. 55, 137–146. doi: 10.1111/jpy.12865
Hartmann M., Grob C., Tarran G. A., Martin A. P., Burkill P. H., Scanlan D. J., et al. (2012). Mixotrophic basis of Atlantic oligotrophic ecosystems. Proc. Natl. Acad. Sci. U.S.A. 109, 5756–5760. doi: 10.1073/pnas.1118179109
Havurinne V., Handrich M., Antinluoma M., Khorobrykh S., Gould S. B., and Tyystjärvi E. (2021). Genetic autonomy and low singlet oxygen yield support kleptoplast functionality in photosynthetic sea slugs. J. Exp. Bot. 72, 5553–5566. doi: 10.1093/jxb/erab216
Holzinger A. and Karsten U. (2013). Desiccation stress and tolerance in green algae: consequences for ultrastructure, physiological and molecular mechanisms. Front. Plant Sci. 4, 327. doi: 10.3389/fpls.2013.00327
Hynson N. A., Schiebold J. M., and Gebauer G. (2016). Plant family identity distinguishes patterns of carbon and nitrogen st able isotope abundance and nitrogen concentration in mycoheterotrophic plants associated with ectomycorrhizal fungi. Ann. Bot. 118, 467–479. doi: 10.1093/aob/mcw119
Jones R. I. (2000). Mixotrophy in planktonic protists: an overview. Freshw. Biol. 45, 219–226. doi: 10.1046/j.1365-2427.2000.00672.x
Julou T., Burghardt B., Gebauer G., Berveiller D., Damesin C., and Selosse M.-A. (2005). Mixotrophy in orchids: insights from a comparative study of green individuals and nonphotosynthetic individuals of Cephalanthera damasonium. New Phytol. 166, 639–653. doi: 10.1111/j.1469-8137.2005.01364.x
Kamjunke N., Henrichs T., and Gaedke U. (2006). Phosphorus gain by bacterivory promotes the mixotrophic flagellate Dinobryon spp. during re-oligotrophication. J. Plankton Res. 29, 39–46. doi: 10.1093/plankt/fbl054
Katechakis A. and Stibor H. (2006). The mixotroph Ochromonas tuberculata may invade and suppress specialist phago- and phototroph plankton communities depending on nutrient conditions. Oecologia. 148, 692–701. doi: 10.1007/s00442-006-0413-4
Laetz E. M. J. and Wägele H. (2017). Chloroplast digestion and the development of functional kleptoplasty in juvenile Elysia timida (Risso 1818) as compared to short-term and non-chloroplast-retaining sacoglossan slugs. PloS One 12, e0182910. doi: 10.1371/journal.pone.0182910
Laybourn-Parry J., Roberts E. C., and Bell E. M. (2000). “Mixotrophy as a survival strategy in Antarctic lakes,” in Antarctic ecosystems. Eds. Davidson W., Howard-Williams C., and Broady P. (The Caxton Press, Christchurch, New Zealand), 33–40.
Leles S. G., Bruggeman J., Polimene L., Blackford J., Flynn K. J., and Mitra A. (2021). Differences in physiology explain succession of mixoplankton functional types and affect carbon fluxes in temperate seas. Progr. Oceanogr. 190, 102481. doi: 10.1016/j.pocean.2020.102481
Lepori-Bui M., Paight C., Eberhard E., Mertz C. M., and Moeller H. V. (2022). Evidence for evolutionary adaptation of mixotrophic nanoflagellates to warmer temperatures. Glob. Change Biol. 28, 7094–7107. doi: 10.1111/gcb.16431
Liao I. J. Y., Sakagami T., Lewin T. D., Bailly X., Hamada M., and Luo Y.-J. (2025). Animal–chlorophyte photosymbioses: evolutionary origins and ecological diversity. Biol. Lett. 21, 20250250. doi: 10.1098/rsbl.2025.0250
Lin Q., Yin S. S., Mata-Rosas M., Ibarra-Laclette E., and Renner T. (2025). Are carnivorous plants mixotrophic? New Phytol. 247, 445–449. doi: 10.1111/nph.70260
Maeda T., Takahashi S., Yoshida T., Shimamura S., Takaki Y., Nagai Y., et al. (2021). Chloroplast acquisition without the gene transfer in kleptoplastic sea slugs, Plakobranchus ocellatus. eLife 10, e60176. doi: 10.7554/eLife.60176
Mansour J. S. and Anestis K. (2021). Eco-evolutionary perspectives on mixoplankton. Front. Mar. Sci. 8, 666160. doi: 10.3389/fmars.2021.666160
Millette N. C., Gast R. J., Luo J. Y., Moeller H. V., Stamieszkin K., Andersen K. H., et al. (2023). Mixoplankton and mixotrophy: future research priorities. J. Plankton Res. 45, 576–596. doi: 10.1093/plankt/fbad020
Mitra A., Caron D. A., Faure E., Flynn K. J., Leles S. G., Hansen P. J., et al. (2023). The Mixoplankton Database (MDB): Diversity of photo-phago-trophic plankton in form, function, and distribution across the global ocean. J. Eukaryot Microbiol. 70, e12972. doi: 10.1111/jeu.12972
Mitra A., Flynn K. J., Burkholder J. M., Berge T., Calbet A., Raven J. A., et al. (2014). The role of mixotrophic protists in the biological carbon pump. Biogeosciences 11, 995–1005. doi: 10.5194/bg-11-995-2014
Mitra A., Flynn K. J., Tillmann U., Raven J. A., Caron D., Stoecker D. K., et al. (2016). Defining planktonic protist functional groups on mechanisms for energy and nutrient acquisition: Incorporation of diverse mixotrophic strategies. Protist 167, 106–120. doi: 10.1016/j.protis.2016.01.003
Miyagishima S.-Y. (2023). Taming the perils of photosynthesis by eukaryotes: constraints on endosymbiotic evolution in aquatic ecosystems. Commun. Biol. 6, 1150. doi: 10.1038/s42003-023-05544-0
Moeller H. V., Archibald K. M., Leles S. G., and Pfab F. (2024). Predicting optimal mixotrophic metabolic strategies in the global ocean. Sci. Adv. 10, eadr0664. doi: 10.1126/sciadv.adr0664
Murchie E. H. and Niyogi K. K. (2011). Manipulation of photoprotection to improve plant photosynthesis. Plant Physiol. 155, 86–92. doi: 10.1104/pp.110.168831
Norbury J., Moroz I. M., and Cropp R. (2019). The role of mixotrophy in southern ocean ecosystems. Environ. Model. Assess. 24, 421–435. doi: 10.1007/s10666-019-09670-0
O’Reilly C. M., Sharma S., Gray D. K., and Hampton S. E. (2015). Rapid and highly variable warming of lake surface waters around the globe. Geophys. Res. Lett. 42, 781. doi: 10.1002/2015GL066235
Princiotta S. D., VanKuren A., Williamson C. E., Sanders R. W., and Valiñas M. S. (2023). Disentangling the role of light and nutrient limitation on bacterivory by mixotrophic nanoflagellates. J. Phycol. 59, 785–790. doi: 10.1111/jpy.13358
Rauch C. and Redelberger T. (2017). On being the right size as an animal with plastids. Front. Plant Sci. 8, 1402. doi: 10.3389/fpls.2017.01402
Salcher M. M. (2014). Same same but different: ecological niche partitioning of planktonic freshwater prokaryotes. J. Limnol. 73(1), 74–87. doi: 10.4081/jlimnol.2014.813
Schenone L., Aarons Z. S., García-Martínez M., Happe A., and Redoglio A. (2024). Mixotrophic protists and ecological stoichiometry: connecting homeostasis and nutrient limitation from organisms to communities. Front. Ecol. Evol. 12, 1505037. doi: 10.3389/fevo.2024.1505037
Schmitt V., Händeler K., Gunkel S., Escande M. L., Menzel D., Gould S. B., et al. (2014). Chloroplast incorporation and long-term photosynthetic performance through the life cycle in laboratory cultures of Elysia timida (Sacoglossa, Heterobranchia). Front. Zool. 11, 5. doi: 10.1186/1742-9994-11-5
Selosse M.-A., Charpin M., and Not F. (2017). Mixotrophy everywhere on land and in water: the grand écart hypothesis. Ecol. Lett. 20, 246–263. doi: 10.1111/ele.12714
Søgaard D. H., Sorrell B. K., Sejr M. K., Andersen P., Rysgaard S., Hansen P. J., et al. (2021). An under-ice bloom of mixotrophic haptophytes in low nutrient and freshwater-influenced Arctic waters. Sci. Rep. 11, 2915. doi: 10.1038/s41598-021-82413-y
Sommer U., Adrian R., de Senerpont Domis L., Elser J. J., Gaedke U., Ibelings B., et al. (2012). Beyond the Plankton Ecology Group (PEG) model: mechanisms driving plankton succession. Annu. Rev. Ecol. Evol. Syst. 43, 429–448. doi: 10.1146/annurev-ecolsys-110411-160251
Sterner R. W. and Elser J. J. (2002). Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere. Princeton University Press. Available online at: http://www.jstor.org/stable/j.ctt1jktrp3.
Suetsugu K., Matsubayashi J., and Tayasu I. (2020). Some mycoheterotrophic orchids depend on carbon from dead wood: novel evidence from a radiocarbon approach. New Phytol. 227, 1519–1529. doi: 10.1111/nph.16409
Tešitel J., Tešitelová T., Minasiewicz J., and Selosse M. A. (2018). Mixotrophy in land plants: Why to stay green? Trends Plant Sci. 23, 656–659. doi: 10.1016/j.tplants.2018.05.010
Unrein F., Gasol J. M., Not F., Forn I., and Massana R. (2014). Mixotrophic haptophytes are key bacterial grazers in oligotrophic coastal waters. ISME J. 8, 164–176. doi: 10.1038/ismej.2013.132
Valmalette J.-C., Dombrovsky A., Brat P., Mertz C., Capovilla M., and Robichon A. (2012). Light-induced electron transfer and ATP synthesis in a carotene-synthesizing insect. Sci. Rep. 2, 579. doi: 10.1038/srep00579
Venn A. A., Loram J. E., and Douglas A. E. (2008). Photosynthetic symbioses in animals. J. Exp. Bot. 59, 1069–1080. doi: 10.1093/jxb/erm328
Ward B. A. and Follows M. J. (2016). Marine mixotrophy increases trophic transfer efficiency, mean organism size, and vertical carbon flux. Proc. Natl. Acad. Sci. U.S.A. 113, 2958–2963. doi: 10.1073/pnas.1517118113
Keywords: kleptoplasty, mixoplankton, mixotrophy, photosymbiosis, terrestrialization
Citation: Calbet A (2026) Why mixotrophy flourished in water but rarely on land. Front. Ecol. Evol. 14:1755631. doi: 10.3389/fevo.2026.1755631
Received: 27 November 2025; Accepted: 07 January 2026; Revised: 02 January 2026;
Published: 04 February 2026.
Edited by:
Nathan Wolf, Alaska Pacific University, United StatesReviewed by:
Luca Schenone, University of Konstanz, GermanyCopyright © 2026 Calbet. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Albert Calbet, YWNhbGJldEBpY20uY3NpYy5lcw==