Humans have long been part of marine ecosystems worldwide, although the nature of this relationship has changed over time and space. Today many marine ecosystems are deeply threatened, including commercial fish stocks, coral reefs, and polar environments (Bindoff et al., 2019; Worm and Lotze, 2021). The ongoing crisis in the world’s oceans threatens vulnerable species and ecosystems as well as economic stability and food security (FAO, 2018). Further, the world is shifting toward relying even more heavily on the ocean (Costello et al., 2020). From these trends, it is clear that research must address the maintenance of ocean ecosystems. To balance the various needs of all ecosystem actors, both human and non-human, it is crucial that we have language and theory that reflects the dynamic nature of marine ecosystems and our place in them.

Addressing the problem of ocean ecosystem degradation requires enormous interdisciplinary effort. This effort, however, is often stymied by the way in which knowledge creation occurs in marine science. In 1995, Daniel Pauly published a paper on the now-famous phenomenon known as “shifting baselines syndrome (SBS),” in which collective environmental knowledge and memory move forward in time with successive generations, resulting in gradual loss of knowledge regarding the previous state of an ecosystem (Pauly, 1995). Continuous environmental degradation can result in a misinterpretation of changes over time, frequently leading to under-valuation of environmental carrying capacities or species population sizes (Lotze and Worm, 2009; Rodrigues et al., 2019) making researchers ill-equipped to fully understand changing ecosystems. Yet, the environments being studied have been transformed by human actions, often for a much longer time period than is commonly assumed (Lotze and Worm, 2009; Rodrigues et al., 2019).

Although the prevalence of SBS has been clearly demonstrated, the concept itself relies on a problematic ecological assumption: that there is a “baseline” for any one species or ecosystem dynamic. This implies a singular, natural state for any particular ecosystem, which, in practice, becomes fraught with arbitrary decisions regarding how a “baseline” is determined (Lotze and Worm, 2009; Rodrigues et al., 2019). To illustrate this point, Collins et al. (2020) estimated historical population sizes of hunted North American mammals throughout history using two different historical time points as cut-offs for baseline calculation. They found that by pushing the timeline back 100 years, population size estimates increased by over 10%, suggesting the original estimates were likely misleading due to the arbitrary designation of a temporal baseline. Such studies are crucial in illustrating the arbitrary nature of baseline determination while acknowledging the equally important role baseline assumptions play in knowledge creation.

It is clear that humans have had a significant and deleterious effect on our surrounding ecosystems in our more recent history. Yet, it is also important to emphasize that humans have played a role in our environments for the entirety of our evolutionary history, including coastal and marine ecosystems (Rick and Erlandson(eds), 2008; Stringer et al., 2008). This role was neither inherently positive nor inherently negative our long relationship with the marine environment and the increasingly appreciated dynamic nature of ecosystem stability illustrates the fact that the “baseline” concept itself is what should be shifting. Rather than focusing on a baseline, the concept of SBS should be incorporated into a wider theoretical framework of thresholds in marine environments which explicitly incorporates human culture as an integral component of marine ecosystems. As will be discussed below, the concept of the threshold allows conceptual space for the fluid nature of ecosystems throughout time. It also provides markers for establishing baselines and a critical framework for understanding drivers of ecosystem change.

By incorporating SBS into a larger discussion of thresholds, the debate can be shifted back to understanding long-term ecosystem dynamics rather than elucidating concrete baselines. Further, the concept of thresholds expands the timescale further than that of SBS, allowing complete incorporation of ecological and evolutionary dynamics into the discussion of sustainable resource management. Finally, as we will show, SBS can be conceptualized as a key component within the wider threshold structure as a cultural characteristic that facilitates the crossing of a certain type of threshold—the tipping point.

We recognize that some of these concepts have been previously addressed in other studies and reviews (Groffman et al., 2006; Samhouri et al., 2010; Rodrigues et al., 2019). Here, we propose a framework that seeks not to disprove other attempts but to expand and enhance inquiry into past ecosystems. We propose a generalized research approach. We emphasize the way in which recent advances in molecular research can illuminate long-term ecosystem change when they are firmly grounded in theory that explicitly incorporates human society in our understanding of what constitutes an “ecosystem.” We situate this framework within previous theoretical work, including SBS. We then highlight knowledge gaps in ecological and evolutionary thresholds that can be addressed through biomolecular methods that have become increasingly efficient and accessible in recent years, such as genomics and palaeo-/archaeo-genomics and stable isotopes analysis. Finally, we provide suggestions for future research and the impact such studies could have on providing crucial information for future environmental resource management.

The technical definition of a “threshold” in the Oxford English Dictionary is, “[t]he magnitude or intensity that must be exceeded for a certain reaction or phenomenon to occur” (OED, 2021). We use this definition of “threshold” to define various subtypes of threshold that are relevant for understanding marine ecosystems: the magnitude or intensity of some driver increases or decreases to the point that a threshold is crossed. Here we highlight three major threshold categories that pertain to change in marine ecosystems: cultural, ecological, and evolutionary (see Table 1) and discuss various research techniques to identify when a threshold has been crossed, e.g., a certain reaction or phenomenon has occurred. For each category, threshold identification is always dependent on the research question: it relies on the reaction or phenomenon of interest in the study.

When discussing marine resource exploitation, there are several major ways in which a threshold can be identified. The first is to pinpoint times in the past at which human societies experienced a major transition that coincided with changes in relationships to marine ecosystems: thresholds in culture. These thresholds are based on phenomena such as changes in perception of marine environments, technological loss/innovation, economic development, and changes in resource use fall into this category. Thresholds in culture signify a shift in human society that impacts societal-level relationships with the surrounding environment. There are several cultural thresholds that have been identified in human history and are widely known, including the Neolithic and Industrial “revolutions” and the rise of the Information Age. It should be noted, however, that shorter or seemingly less dramatic periods of flux can also be considered cultural thresholds though this is dependent on the scale of the study and the research question. Some examples of cultural thresholds include religious change, technological advance, and political regime changes (including societal collapse). These changes often affect the relationship between humans and their environments, even if indirectly, through changing subsistence patterns, access to novel food sources through trade, and changing economic and political regulations. Cultural thresholds that impact human exploitation in the marine environment are varied and often relate to technological advance (e.g., seafaring technology or improved fishing techniques) (Unger, 1980; Couper, 2009; O’Connor et al., 2011; Montenegro et al., 2016), but can also be linked to cultural mores surrounding seafood consumption, as seen with the arrival of Christianity in northern Europe and the associated increase in fish consumption on religious holidays in lieu of meat (Hoffmann, 2001, 2005; Müldner and Richards, 2005). Although these cultural changes can (and often do) have ecological implications, impacting the ecology is not a requirement for a cultural threshold.

The second category of thresholds characterizes ecosystem boundaries according to species biology or ecological traits. These are thresholds in ecology. Thresholds in ecology encompass relationships between species in an ecosystem (e.g., mutualism, predation, symbiotic relationships, trophic balance, etc.) and can refer to radical shifts in ecosystem dynamics as a whole. Again, the threshold is scalable depending on the research aims. Thresholds in ecology can be linked to anthropogenic impacts but may also occur naturally, such as in the process of ecosystem turnover. Thresholds in ecology can also be driven by abiotic factors, both extrinsic, such as the introduction of pollutants or chemicals, and intrinsic, such as biogeological processes like shifting currents and changes in upwelling. Such ecological thresholds are commonly used in exploitation policies today. For example, fisheries policies are often based on measures of spawning-stock biomass—the number of fish in a species that can reproduce in any given year—requiring that human extraction levels do not cause the population to dip below a certain threshold based on the minimum remaining stock size calculated for sustaining the population (De Lara et al., 2007). We here avoid the terms “ecosystem services” and “ecosystem function” as these have been used in the past to create hierarchies between human societies and their surrounding ecosystems and frame management goals purely in terms of how these ecosystems can benefit humans (de Groot, 1987; de Groot et al., 2002; Costanza et al., 2017). We recognize that the definition of the term “ecosystem function” has been under debate in ecological research for some time (Paterson et al., 2012). As it can be used as an underpinning for determining ecosystem services and occasionally synonymously with “ecosystem services” (e.g., Peterson et al., 2010; Oliver et al., 2015; Hillman et al., 2018), we choose to avoid this term altogether.

Finally, there are thresholds in evolution. Evolutionary thresholds are crossed when there is a heritable change in genotype or phenotype in a species. For simplicity’s sake, we here discuss molecular evolution as the main example for crossing and evolutionary threshold. This includes demographic shifts such as bottlenecks and population expansions, selective processes and inbreeding, and other phylogenomic phenomena. Potential drivers of threshold crossing include: species migration, climate change, and abiotic factors such as ocean acidification and temperature changes. In recent history, many of these thresholds are likely reached due to human activity, but may have been non-anthropogenic in the past. In this paper, we focus on human exploitation as a critical example of how anthropogenic change can induce an evolutionary threshold. For example, the concept of fisheries-induced evolution postulates that intensive fishing pressures cause an evolutionary change in fish species, mostly by changing life-history traits for faster maturation (Heino et al., 2015; Pinsky et al., 2021). Fisheries-induced evolution occurs when fishing has reached a scale in which evolution is impacted, which may be temporally decoupled from the ecological or cultural thresholds.

Recent discourse in ecosystem management, on anthropogenic impacts on the environment, and on climate change has revolved around the notion of maintaining human activity and ecosystem dynamics within a set of sustainable boundaries often referred to as “thresholds” or “tipping points” (Lenton and Schellnhuber, 2007; Rockström et al., 2009; Russill and Nyssa, 2009). As these terms are not often concretely distinguished, we suggest a differentiation between them. A threshold is distinct from a “tipping point” in that it does not inherently imply a system that has lost crucial regulatory elements. A tipping point can be a form of a threshold, but thresholds exist which are not “tipping points.” For example, quantification of sprat population size dynamics has revealed distinct thresholds at which the Baltic Sea ecosystem transitions to an alternate stable state (Casini et al., 2009) but the overall ecosystem dynamics remain unchanged. In contrast, extractivist policies based on research generated under SBS is a cultural characteristic that is causing our oceans to hurtle toward global fisheries collapse and near-total ecosystem degradation (Pauly, 1995; Jackson et al., 2001; Roberts, 2007; Bindoff et al., 2019), therefore is key to crossing the tipping point. Crossing this threshold would be nothing short of catastrophic, which only serves to highlight the importance of deepening our understanding of the other three thresholds. Establishing how thresholds in culture, ecology, and evolution are crossed is therefore of crucial importance to better inform ecosystem management efforts and foster novel approaches to avoid tipping points.

Although seemingly straightforward in definition, these thresholds are in practice entwined in complex, interdependent relationships. For example, advances in fishing technology constitute not only a cultural threshold, but also ecological and evolutionary thresholds as selective fishing and its ecological impact will act as new elements in the marine environment, e.g., with the advent of deep-sea trawling. Given the complexity of human behavior, ecosystem dynamics, and species evolution, it is critical to explore these thresholds thoroughly both in conjunction and as separate phenomena. It can be difficult to determine at what point a threshold has been crossed or what should be considered a “threshold.” The threshold concept is not one-size-fits-all, rather it is a flexible approach that can be scaled across time and space.

Here, we lay out the ideal workflow for addressing the issue of identifying thresholds in marine ecosystems in the context of marine resource exploitation. First, context must be grounded in historical, paleontological, archeological, and anthropological research. This includes consultation of historical records, archeological site reports, and, where applicable, ethnographies. Critically, what this means for ecologists is directly searching for answers to ecological/evolutionary questions outside the field of ecology. A strong background in the relevant historical and archeological contexts of the time period and/or biological system in question shifts ecological inquiry away from assumptions that long-term change must be caused by abiotic factors, such as climate, whereas only recent changes can be due to human activity in the ecosystem. Concurrently, a relevant background in the natural history of the biological system in question is crucial for framing the historical and archeological context. Biomolecular analysis can then be carried out. This work must be situated in archeology, history, indigenous knowledge, and ecology in order to interpret results in a nuanced approach based in systems-level thinking.

Archeology, anthropology, and historical research are key methodological approaches with which to explore cultural thresholds. The application of these methods, however, are not stand-alone modes of inquiry into the problem of identifying sustainable practices. Research must be framed in the context of archeology, history and, wherever applicable, indigenous knowledge. Incorporating all types of knowledge is the only way we will be able to balance issues such as food security with the pressing problems of declining biodiversity, climate change, and social justice.

Many studies of marine resource extraction set their baseline as the mid- or early twentieth century, citing a drastic change in technology that allowed for increased fishing capacity in hitherto inaccessible regions of the globe (Pinnegar and Engelhard, 2008). This is, of course, an important cultural threshold in marine resource extraction and one that merits attention. It is likely, however, that industrial-scale exploitation was occurring, for at least some populations, much earlier than the twentieth century. In the Atlantic, archeological and historical research has revealed fisheries on an enormous scale occurring up to 1,000 years ago (Barrett, 2019). Indeed, Barrett et al. (2004) propose that a cultural threshold was crossed at this time in the form of the “Fish Event Horizon,” in which the English proto-industrial fishing operations reached a high enough level that the surrounding North Sea ecosystems were forever changed. These conclusions were reached based on zooarchaeological analysis in combination with analysis of historical documents, suggesting that the mid- or early twentieth century baselines established for many marine populations are again subject to SBS. This illustrates the capacity of archeological and historical research to exhibit thresholds in human culture that indicate likely parallel ecological thresholds. While providing significant insights, these sources remain limited for generating a comprehensive understanding of the marine ecosystem. Archeological and historical research efforts are adept at determining thresholds in human behavior such as major societal changes or shifts in scale of exploitation, yet both are less well-equipped for informing us about species or ecosystem dynamics (Barrett, 2019; Oosting et al., 2019).

Molecular analysis of archeological assemblages, undertaken in collaboration with archeologists and historians, can provide novel insight into broader ecological questions. These approaches include stable isotope analysis, proteomics, and genomics, often in conjunction with archeology and paleontology to form the discipline of biomolecular archaeo/paleontology. The research aims that can be addressed include: species identification (Biard et al., 2017); establishing trade, migration, and population continuity (Star et al., 2017); reconstructing demographic history and evolutionary change (De Bruyn et al., 2009; Foote et al., 2013); and analyzing past ecological and climatic conditions (Gokhman et al., 2017). Recent advances in ancient biomolecular techniques have created a novel arena for investigating thresholds, one that is already beginning to take shape in bioarchaeology and marine ecology (Martínez-García et al., 2021; Ólafsdóttir et al., 2021). By reconstructing past ecosystems using ancient DNA and stable isotope analysis, it may be possible to observe periods of stability and flux, providing a better understanding of what constitutes a balanced and sustainable ecosystem in support of future-oriented conservation efforts. Indeed, ecological principles identified through molecular approaches could provide policymakers and scientists with the knowledge necessary to not only recover damaged ecosystems but to help foster novel ecosystems in the coming years (Alagona et al., 2012; Máñez et al., 2014).

We recognize that such an approach to inquiry requires generalized knowledge and a strong collaborative research network that draws on expertise in each of these fields. In recent years, such networks have been established in marine ecology (e.g. Oceans Past Initiative, 2021; Sea Change Project, 2021; SeaChanges Itn, 2021). We anticipate that as the field turns toward incorporating social science and humanities, we will see an influx of networks of this type increasing.

All of the above analytic capacities of ancient biomolecular research are crucial for understanding our past relationship with the marine environment. To establish future sustainable measures for marine resource exploitation, it is necessary to contextualize today’s sustainability and conservation efforts with knowledge of the long-term relationships between humans and these ecosystems. The data currently available on human impact are typically collected on decades-long bases, and almost never predates the beginning of the twentieth century. As discussed above, there is strong evidence for industrial-scale marine resource extraction that occurred up to 1,000 years ago, at least in the North Atlantic context and likely elsewhere. This understanding is based on historical records and the analysis of archeological sites and remains. These initial research efforts provide a platform for understanding the human relationship with the sea going far back in time. They also provide context for emerging biomolecular techniques and novel applications. The above methodologies should, therefore, always be conducted with as much ecosystem-wide information as is possible, acknowledging the limitations of working with damaged and/or partial datasets. By exploring the past population dynamics of one species, it is possible to gain long-term information on balanced ecosystem dynamics. This will provide us with tools for avoiding the catastrophic threshold in our near future: the tipping point.

It is too often that thresholds identified for sustainable human exploitation fall under the category of the tipping point, pushing population dynamics to the point of collapse. For example, the commonly used notion of “maximum sustainable yield” in many modern fisheries sets catch limits on exploited species based on the amount of spawning stock biomass that can be sustainably removed from the population (Tsikliras and Froese, 2019). In practice, maximum sustainable yield does not take into account ecosystem dynamics and fluidity, rather it is based mainly on the population size of the focal species, allowing extraction up to the point of population collapse (McEvoy, 1986). In the same way, whaling regulative measures, such as the potential biological removal level defined by the U.S. Marine Mammal Protection act, and the Strike Limit Algorithm by the International Whaling Commission, are also based on the minimum population estimates of the stocks and their carrying capacity (Wade, 1998; Givens, 2000). Application of these and similar approaches have led to marine population collapses around the world due to the combined effects of overexploitation and climate change (Guénette and Gascuel, 2012).

The marine historical ecology approach provides ecosystem-based measures for the determination of “sustainable yield” by broadening the definition of the threshold, establishing a conceptual space for ecosystem change that occurs outside of, and prior to, the tipping point. Broadening thresholds allows quantification of population dynamics in focal species that lead to ecosystem perturbation, providing threshold indicators that signal impending population or ecosystem collapse rather than driving the system to the breaking point (Duarte et al., 2020). It has been demonstrated that ecosystem complexity and controlled exploitation measures have overwhelmingly positive impacts on human and societal health, the marine environment, and the health of global fisheries (Hutchinson, 2008; Howarth et al., 2014).

By utilizing thresholds that act as boundaries for ecosystem dynamics rather than bringing the population to the tipping point each year, sustainable management measures are more likely to ensure the ecosystem remains stable. Further, FAO nations have pledged since 2003 to put in place ecosystem-based fisheries management (EBFM) practices in fisheries instead of devising policies that only apply to individual species, as was previously the case (FAO, 2003). In practice, EBFM has been difficult to implement due to the lack of consensus regarding issues of practical application and scale (Trochta et al., 2018), yet is demonstrably crucial to adapting to climate change (Holsman et al., 2020). The threshold concept provides a clear framework for identifying ecosystem, evolutionary, and cultural dynamics that can assist with developing EBFM practices. To effectively enact regulations such as ecosystem-based fisheries management, it is necessary to understand long-term ecosystem dynamics. To do so we must provide space for input from research that emphasizes long timescales and incorporates human society into our understanding of an “ecosystem,” a perspective that has long been held by many indigenous communities (Salomon et al., 2014 and references therein).

To effectively conduct research on changing marine ecosystems, common frameworks and terminology are required. For compelling communication between researchers, this framework must be flexible enough to encompass a myriad of different fields and scales, and requires a shift to incorporate humans and human society into our understanding of the environment. We have introduced a new theoretical language and a generalized approach that incorporates commonly used ecological ideas to address these issues. The thresholds theory is a way to conceptualize ecosystems and ecosystem change that is both flexible and scalable to the research questions being addressed, and lends itself well to practical applications.

We will never return to the oceans of old. It is not the aim of this research to provide pathways for doing so. Rather, it will likely be required to foster new ecosystems as we move forward into the future (Alagona et al., 2012; Duarte et al., 2020), therefore it is crucial to understand what constitutes a balanced ecosystem, the issue of ecosystem complexity, and the role humans might play in these ecosystems. In addition to establishing regulation and oversight to provide future sustainable marine management, consideration must be given to long-term evolution that has occurred between people and marine environments around the globe, such as the interplay between indigenous communities and sea otters in BC during the late Holocene. Funding efforts for marine historical ecology should be directed toward archeology and population genomics analysis for the marine ecosystems on which people most directly depend, including a targeted effort to fund research occurring outside the traditional spheres of Europe and North America. To provide food security in a changing world, the species people depend on need to be understood from an evolutionary standpoint; how have they adapted to past climate change, anthropogenic exploitation, and different actors in their ecosystems? Are balanced ecosystem dynamics in a north Atlantic context the same as in a Pacific island context? What are the local boundaries management programs must navigate to ensure ecosystem balance? Through the thresholds framework, marine historical ecology is poised to answer these questions and provide crucial information for establishing sustainable marine ecosystems for future generations of humans and the species living with them.

The original contributions presented in the study are included in the article/supplementary material, further inquiries can be directed to the corresponding author/s.

LA and MA wrote the manuscript with contributions from FF. All authors contributed to the development of the theory and revised, and accepted the manuscript.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.