Mutual Tolerance Ecology is a Key to Future Eco-environmental Science

Frontier of Environmental Science March 2015, Volume 4, Issue 1, PP.1-10

Mutual Tolerance Ecology is a Key to Future Eco-environmental Science Gangcai Liu a,*, Xuemei Wang a,d, Junliang Wu a,d, Yuxiao He a,d, Fuqiang Dai b, Bin Zhang c a

Key Laboratory of Mountain Hazards and Earth Surface Processes, Chinese Academy of Sciences, Institute of Mountain Hazards and Environment, Chinese Academy of Sciences and Ministry of Water Resources, Chengdu 610041, China

b

College of Tourism and Land Resources, Chongqing Technology and Business University, Chongqing 400067, China

c

Land and Resources College, China West Normal University, Nanchong 610000, China

d

University of Chinese Academy of Sciences, Beijing 100039, China

*Corresponding author email: liugc@imde.ac.cn

Abstract With the ongoing increase in global stresses, tolerance studies are becoming more important to eco-environmental science. Based on our citation analysis, mutual tolerance was defined as the capacity of any two biotic and abiotic/environmental systems within an ecosystem to maintain health or stability, while mutually allowing certain disturbances or stress from each other. This definition addresses both abiotic and biotic stresses, unlike the previous tolerances that only addressed either. Mutual tolerance ecology has been defined as the science that studies stress tolerance at a system scale, and particularly focuses on mutual tolerance between a biotic system and an abiotic/environmental system. The framework of mutual tolerance ecology involves three aspects: the features of mutual tolerance; the disciplines of mutual tolerance; and the implications of increasing mutual tolerance. We argue that the sustainable development of an ecosystem involves a process in which there is mutual tolerance between biotic and abiotic/environmental systems, and environmental health refers to the conditions that the biotic system can tolerate. Our perspectives should enhance the practice of these theoretical ideas, as mutual tolerance could be a key to sustainable development.

Keywords: Tolerance; Mutual Tolerance; Environmental Stress; Environmental Health; Sustainable Development; Ecosystem

1 INTRODUCTION Generally, tolerance is the capacity to bear conditions (environment or material) that are painful or stressful for a living being. Usually, tolerance is divided into three groups (Thammavongs et al., 2008): (1) abiotic (physical and chemical) stress tolerance, e.g. tolerance to drought, temperature, shade, radiation, light, salt, heavy metals and nutrition; (2) biotic stress tolerance, e.g. tolerance to bacteria, fungi, insects, nematodes and viruses; and (3) anthropogenic stress tolerance, e.g. tolerance to grazing and chemical fertiliser application. In fact, anthropogenic stresses are embodied in abiotic and biotic stresses; thus, tolerance can simply be grouped into two types: abiotic and biotic stress tolerance.

Commonly, living organisms have a certain tolerance to abiotic and biotic stresses, and different species have different tolerance ranges. Switchgrass (Panicum virgatum L.) has a broad tolerance to moisture availability in soil (Barney et al., 2009). Tropical fern gametophytes have high desiccation tolerance (Watkins et al., 2007); most invading exotic species in forests have high shade tolerance (Martin et al., 2009); smaller fish are more tolerant to hypoxic environments (Robb and Abrahams, 2003); and smaller cladocerans have a higher tolerance to Microcystis than larger ones (Guo and Xie, 2006).

Stress is usually defined as a condition that disturbs the normal function of a biological system, a condition that decreases fitness (Sørensen et al., 2003), or any changes of environmental variable that lead to response by a living being (Thammavongs et al., 2008). It is well known that environmental stress is a fundamental factor shaping 1 http://www.ivypub.org/fes

community structure, biodiversity patterns and levels of ecosystem services. Stressful conditions change the morphological and physiological ecology of organisms, thereby affecting biotic interactions and initiating effects that may cascade throughout the assemblage (Pincebourde et al., 2012). Many reports have shown such effects of stressful environments, and stress damage can even occur in the womb (Vereecken, 2012). Environmental stress can result in effects that cascade through four trophic levels in marsh ecosystems, with stronger effects on the higher trophic levels (Moon and Moon, 2010). Stressful environments are usually shown to enhance inbreeding depression (Plough, 2012) and to decrease the loss and function of biodiversity (Bull et al., 2013; Davidson et al., 2012). In stressful habitats, community-level relationships between non-native invaders and native biodiversity are positive (Von Holle, 2013). However, the increase in environmental stress has relatively strong negative effects on lower-diversity communities (Steudel et al., 2012).

Environmental stresses have existed since antiquity (Vereecken, 2012). As time goes on, global changes and environmental stresses (including those derived anthropogenically) are increasing and becoming stronger – this results in apparent changes in various ecosystems at different scales and induces many new selection pressures (Vereecken, 2012). It is well known that natural selection is ongoing daily and hourly throughout the world, rejecting what is unsuccessful and preserving all that is successful (Vereecken, 2012). Therefore, tolerance is considered an important trait in evaluation of the fitness of a species, and is an important tool for the assessment of ecological risk, in order to detect ecological impacts and to establish causality. In particular, community-level tolerance might be a powerful instrument in ecological risk assessment (Millward and Klerks, 2002; Alla et al., 2006).

Thus, stress tolerance is very important for any living being and its environment. Although we highlighted the importance to extend the soil loss tolerance to other stress tolerance and to develop a new field for eco-environmental science in the past few years (Liu et al., 2009; Li et al., 2009), little research is currently concerned with the tolerance of particular environments to life (activity) stress or the mutual tolerance between life and environmental stresses. To address these problems, based on the analysis of literatures addressing stress tolerance, we aim to (1) develop a novel definition of mutual tolerance ecology and (2) propose a framework of mutual tolerance ecology, suggesting the main aspects for study and content to prioritise.

2 MATERIALS AND METHODS TABLE 1 SUMMARY OF MAJOR INORGANIC ION OR MOLECULE MECHANISMS IN BIOTIC AND ABIOTIC STRESS TOLERANCES (NON-EXHAUSTIVE LIST).

Mechanism Ion or molecule Calcium

Silica (Si)

Nitric oxide (NO)

Number of published articles it is involved in Major

Description Signalling ion in response to both abiotic and biotic stress.

Mediates cell osmotic potential and osmotic adjustment.

Activates and maintains antioxidant and enzyme activities.

Promotes the formation of ABA (Abscisic acid), ethylene, etc.

Induces the expression of related genes.

Signalling ion in response to both abiotic and biotic stress.

Promotes bSiO2 (biogenic silica) accumulation.

Regulates the pH value.

Silicate is the stress element, such as Zn–silicate.

Signalling ion in response to both abiotic and biotic stress.

NO has protective functions against oxidative stress through the (1) reaction with lipid radicals, which stops the propagation of lipid oxidation; (2) scavenging O2– and ONOO–; and (3) activation of antioxidant enzymes.

Initiates signalling pathway.

Interacts with other signalling molecules.

Confirmed by Exogenous applications (such as CaCl2)

Abiotic references (Bowler and Fluhr, 2000) (Jiang and Huang, 2001) (Jiang et al., 2005) (Oh-hora et al., 2008) (Gao et al., 2011)

Biotic

Both

Plant

Animal

183

1

3

116

71

Exogenous applications (such as aerosols)

(Neumann and Nieden, 2001) (Liang et al., 2005) (Querne et al., 2012)

35

-

-

35

-

Exogenous applications (such as sodium nitroprussid e) and transgenic engineering

(Qiao et al., 2009) (Xiong et al., 2009) (Shi et al., 2012) (Yang et al., 2012) (Gill et al., 2013) (Fan et al., 2013)

124

1

-

45

80

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We used the ISI Web of Science database to search literature published between January 1970 and May 2013. Titles were searched using the following keywords that are involved in tolerance mechanisms: tolerance, calcium, silica (i.e. the respective ions), nitric oxide, proline, abscisic acid, salicylic acid, glycine betaine, polyamine (i.e. the respective molecules), heat-shock protein and transcription factor. The search results were further refined by selecting only the titles involved in the tolerance of plants or animals to abiotic, biotic or both stresses, and the final number (Tables 1 and 2, Supplementary Materials) of these stresses were counted for both plants and animals.

Furthermore, we summarised the main mechanisms implicated in tolerance, based on the major referred literatures of the above-searched references (Tables 1 and 2, Supplementary Materials).

TABLE 2 SUMMARY OF MAJOR ORGANIC MOLECULE MECHANISMS IN BIOTIC AND ABIOTIC STRESS TOLERANCES (NON-EXHAUSTIVE LIST) Mechanism Molecule Proline

Abscisic acid (ABA)

Salicylic acid (SA)

Glycine betaine (GB)

Polyamine (PA)

Heat shock protein (HSP) Transcriptio n factor (TF)

Number of published articles it is involved in Major

Description Signalling ion in response to both abiotic and biotic stress.

Modulates the stomatal aperture.

Regulates plant hormones.

Regulates enzyme protein activities.

Modifies the expression of genes.

Signalling ion in response to both abiotic and biotic stress.

Modulates the stomatal aperture.

Regulates (phosphatase and kinase) enzyme activities.

Modifies the expression of genes.

Signalling ion in response to both abiotic and biotic stress.

Activates the activities of antioxidant enzymes.

Induces the expression of tolerance genes.

Signalling ion in response to both abiotic and biotic stress.

Mediates osmotic adjustment.

Regulates enzyme activities.

Protects the photosynthetic apparatus.

Signalling ion in response to both abiotic and biotic stress.

Mediates osmotic adjustment and Ca2+ homeostasis.

Activates the activities of antioxidant enzymes.

Regulates programmed cell death.

Scavenges free radicals.

Modifies the expression of tolerance genes.

Changes the equilibrium in the direction of more functional proteins or degradation of damaged proteins.

Modulates signalling pathways.

Controls the expression of stress-responsive genes.

Confirmed by Exogenous application and transgenic engineering

Abiotic references (Kishor et al., 2005) (Kumar et al., 2010) (Szabados and Savoure, 2010) (Jonytiene et al., 2012)

Biotic

Both

Plant

Animal

154

-

2

154

2

(Li et al., 2003) (Sirichandra et al., 2008) (Cutler et al., 2010) (Farhoudi and Saeedipour, 2011) (Du et al., 2013) (Horvath et al., 2007) (Yang and Sun, 2012) (Bastam et al., 2013)

193

1

1

193

2

48

-

1

49

-

Exogenous application and transgenic engineering

(Ashraf and Foolad, 2007) (Khan et al., 2009) (Wani et al., 2013)

35

-

1

35

1

Exogenous application and transgenic engineering

(Tang et al., 2007) (Duan et al., 2008) (Alcazar et al., 2010) (Gill and Tuteja, 2010) (Tavladoraki et al., 2012)

63

-

1

61

3

Transgenic engineering

(Sørensen et al., 2003) (Sato and Yokoya, 2008) (Padmini and Rani, 2011) (Sun et al., 2012) (Agarwal et al., 2006) (Qiu and Yu, 2009) (Tran et al., 2010) (Golldack et al., 2011) (Khan, 2011) (Sarfraz et al., 2011) (Kim et al., 2012)

112

2

54

60

88

6

Exogenous application

Exogenous application

Transgenic engineering

91

3

3 RESULTS AND DISCUSSION 3.1 Necessities of mutual tolerance ecology Careful reading of the searched reports showed that current studies concerning stress tolerance (Tables 1 and 2, Supplementary Materials) mainly addressed the tolerance of organisms and rarely concerned abiotic systems such as soil, water and air. Most studies were on plants, with some on animals and humans – mainly on individuals and few on communities/systems. The majority concerned abiotic stress tolerance and few were on biotic and anthropogenic stress tolerances. Although many mechanisms of tolerance were confirmed by exogenous application or engineering, or both (Tables 1 and 2, Supplementary Materials), many underlying mechanisms remain to be understood, e.g. the 3 http://www.ivypub.org/fes

connections and differences between stress response elements for abiotic and biotic stresses (Mittler, 2002)). The interactions between species under stressful conditions are not clear (He et al., 2013). Although there is much evidence of the results of anthropogenic stress, there is insufficient understanding of how these stresses influence eco-evolutionary feedback (Bissett et al., 2013). Thus, there is little knowledge of how human societies and nature systems will evolve under both anthropogenic and natural stresses. These science reports implied that new concepts and laws, concerning the tolerance of biotic and abiotic/environmental systems, need to be understood.

Presently, few related mutual tolerances have been reported, such as cross-tolerance (Pastori and Foyer, 2002) or co-tolerance (Millward and Klerks, 2002), meaning acclimation or hardening to one stress may enhance tolerance to other stresses. Mutual reproductive tolerance means individual cooperation with two competitors in some animal systems (Kappeler and Port, 2008; Stiver et al., 2013). Environmental systems also suffer various stresses and have varied tolerances, e.g. to soil loss (Li et al., 2009) and soil fertiliser application (Zhao, 2013). Obviously, the present tolerances only address either biotic or abiotic stresses, not both. Recently, Bissett et al. (2013) suggested that the relationships and feedback between environmental variables (abiotic system) and soil biota (biotic system) should be given increased attention in future studies. We propose that such relationships and feedback should include those of mutual tolerance and mutual tolerance responses. Thus, it is scientifically necessary to extend the content of tolerance to mutual tolerance that can address both biotic and abiotic/environmental stresses.

FIG. 1. TRENDS IN SELECTED NATURAL DISASTERS.

Human activities have led to the degrading of two billion hectares (accounting for 22% of the total) of land (Scherr, 1999). Bekri and Yannopoulos (2012) reported that the Alfeios River system in Greece was degraded mainly by hydrogeological alterations, intensively irrigated agriculture, surface and groundwater overexploitation and infrastructure development. In semi-arid areas in South Africa, landscapes have also been degraded, mainly due to stresses from cultivation, overgrazing and climate variability (Boardman et al., 2010). Various evidence indicates that, through the continuous development of society, humans have deeply affected the natural environment, and that some behaviours of humans have even ‗enraged‘ the natural environment, resulting in disaster (Hanson, 2005; Mann, 2010; Nyssen et al., 2004). Our research has shown that natural disasters show an increasing tendency (Fig. 1) (Liu et al., 2009). It is increasingly convincing that our Earth is now in the Anthropocene epoch (Schimel et al., 2013; Syvitski, 2012), with human actions and behaviours affecting the biosphere both continuously and negatively (Fischer et al., 2012). Social and economic pressures are significantly related to the extinction of plants and animals (Dullinger et al., 2013). The recovery rate of marine environments, in which excessive pollution exists, is slow and most contaminated areas are maintained at a lower biomass level (Neubauer et al., 2013). Human activities have resulted in unprecedented changes of the global nitrogen cycle; in the last century, the total global amount of nitrogen-fixation activity at least doubled. Latin America, in particular, is facing challenges regarding the impact of the nitrogen cycle on human activity (Austin et al., 2013). All of these signals warn that human activity must obey 4 http://www.ivypub.org/fes

the tolerance laws of the natural environment – the impacts or stresses from human activity must not exceed the tolerance of natural environments; otherwise, humans will be ‗punished‘ by nature. Arnold (2006) indicated that the challenge for modern civilisation is to reconcile the demands of human development with the tolerances of nature.

Not only does the life system have a range of tolerance to stresses from environmental systems but environments also have a certain range of tolerance to stresses from the life system, including that of humans. These two systems allow a certain degree of different stresses from each other; however, once exceeding the critical point of the admissible stress, life and/or the environmental system will become unstable or be destroyed.

In addition, under increasingly stressful global conditions, interaction between life and the evolutionary trend of a biotic system is far from clear. Although biotic tolerance significantly reduces the establishment of individual invaders, there is little evidence that species interactions completely repel invasion (Levine et al., 2004). This could contribute towards mutual tolerance between natives and invaders. Although plant interactions change under stress, either by an outright shift to facilitation (survival) or a reduction in competition (growth and reproduction), future studies should apply standardised definitions and protocols in order to better understand how species and communities will respond to environmental changes (He et al., 2013). The environmental forces behind natural selection remain mysterious, particularly in terms of the correlation between environmental stress and the health or behaviour of human beings (Vereecken, 2012). All of this evidence implies that we must develop a broader and more integrative conceptual framework, and including both biotic and abiotic (environmental) systems will greatly enhance our ability to understand, predict and manage critical aspects of biotic and abiotic ecosystems (Bissett et al., 2013). As Mace (2013) demonstrated, serious eco-environmental and social problems such as climate change, loss of ecological services and population growth demand a new type of ecology – one that focuses on how communities of organisms as a whole, at the scale of landscapes or catchments, interact with people and the physical environment.

Thus, it is necessary to practically develop ecology into mutual tolerance ecology.

3.2 Definition and study framework of mutual tolerance ecology According to the above realities, we defined mutual tolerance as the capacity of any two biotic and abiotic/environmental systems within an ecosystem to maintain health or stability, and to mutually allow certain disturbances or stresses from each other. For example, the mutual tolerance between insects (biotic system) tolerating increasing amounts of pesticides (abiotic/environmental stress) and farmland (environmental system) tolerating increasing numbers of insects (biotic stress). This definition addresses both abiotic and biotic stresses, unlike the previous tolerance definitions involved either abiotic or biotic stress.

Mutual tolerance ecology

Subsection

Main contents

1 Tolerance features

 

Range of mutual tolerance; Impact factors of mutual tolerance.

2 Tolerance laws

 

Laws of mutual tolerance dynamics; Mechanisms of mutual tolerance. change.

 

Techniques of increasing mutual tolerance; Management means of increasing mutual tolerance.

3 Means to increase tolerance

FIG. 2. PROPOSED FRAMEWORK FOR MUTUAL TOLERANCE ECOLOGY.

Based on the implications of previous reports, and our understanding of current evidence, we argue that a living system that includes an ecosystem obeys the laws of mutual tolerance: (1) a living system is at least mutually tolerable between individuals or components (including a living being and its environment); (2) a living system can 5 http://www.ivypub.org/fes

be self-restoring or rehabilitating, i.e. it has ‗immune‘ ability when changing conditions do not exceed its tolerance; and (3) living-system evolution (or degradation or recovery) is the essence of the breaks or changes in the various tolerance threshold values. Thus, the range, magnitude, impact factors, mutual relationships and dynamics of these tolerances should be the focus of future eco-environmental science studies. We refer to these related studies as ‗mutual tolerance ecology‘, a science that studies stress tolerance at a system scale, and particularly focuses on mutual tolerance between biotic and abiotic/environmental systems. This not only addresses responses of life systems (including humans) to environmental stresses, but also the responses of environmental systems to life system (including life activity) stresses, particularly the response to mutual stresses between life and the environmental system. Consequently, we propose a framework of mutual tolerance ecology (Fig. 2).

The first point addresses the features of mutual tolerance, particularly regarding mutual tolerance between life and its environmental system; the second concerns the laws of mutual tolerance, mainly the dynamics and the mechanisms; the third includes the means of increasing mutual tolerance, such as the techniques and administration strategies involved. Among these, the mutual tolerance between environments and humans (human activity) is highlighted. It is particularly important to study the theories concerned with eco-environmental tolerances and the acceptable bounds of human activity, including the sub-project of the effects of human activities on eco-environmental tolerances. It should be noted that environmental genomics approaches, such as fish genomics (Cossins and Crawford, 2005), will be highly applicable to mutual tolerance ecology.

3.3 Significance of mutual tolerance ecology In our definition, tolerance can be extended to environmental systems, such as soil, water and air. These tolerances should not only include the tolerance of life to environment stress, but also the tolerance of life-to-life (life activity) stress (e.g. population density tolerance and city-size tolerance), environment-to-environment stress (e.g. soil-loss tolerance) and environment-to-life (life activity) stress (e.g. fertiliser-application tolerance). Mutual tolerances are ubiquitous between individuals in a community (e.g. family) or systems. We argue that mutual tolerance disciplines are basic laws in an ecosystem or a community. In this way, the sustainable development of an ecosystem is a process that is mutually tolerable between components, particularly between life and its environment in the ecosystem, including the sub-processes of mutual responding, mutual adapting and mutual tolerating. In other words, it is only if the ecosystem is mutually tolerable between life and its environment that the ecosystem will be sustainable.

It has now been demonstrated beyond doubt that the environment greatly influences human activity. Our current challenge is not only to work out precisely how the environment affects us (Vereecken, 2012), but also to understand how humans impact on the environment, so that we can tolerate it. We can neither stop the changes of the earth, nor remove the various stresses, but we must make the current changes or stresses tolerable for us and increase our tolerance to these changes and stresses. We can also ensure that the rate of increase in the environmental stress does not exceed that of our increase in tolerance. Thus, environment health dictates the conditions that we can tolerate – only if there is mutual tolerance between humans and the environment will our society be sustainable. If we can tolerate poorer environments, such environments will allow us to increase our activities or population. This is in fact possible, because we have witnessed that, although the environment is being increasingly degraded and 23% of all deaths are attributable to environmental factors (Wu, 2012), there is an increasing population, with health and longevity showing no declining trend. Simultaneously, insects have increased their resistance to the insecticides that are increasingly applied (Millward and Klerks, 2002).

4 CONCLUSIONS We argue that mutual tolerance ecology is one of the most important sciences for sustainable development and constructing an ecological civilisation. This will be a highlight of eco-environmental science in the near future.

Technologies of mutual tolerance are the keys to the sustainable development of ecosystems. We also proposed that in recent future, following interesting fields should be focused on: 1) mutual tolerance between vegetation and soil as well as climate change; 2) mutual tolerance between fishes and water body; 3) mutual tolerance between resident and dwelling environment.

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ACKNOWLEDGEMENTS This work was financially supported by the Natural Science Foundation of China (Grant Nos. 41471232, 41301287, and 41301351).

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AUTHORS Gangcai Liu, Key Laboratory of Mountain Hazards and Earth Surface Processes, Chinese Academy of Sciences, Institute of Mountain Hazards and Environment, Chinese Academy of Sciences and Ministry of Water Resources. Email: liugc@imde.ac.cn

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