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Natural environments, nature relatedness and the ecological theater: Connecting satellites and sequencing to Shinrin-yoku

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Abstract

Recent advances in research concerning the public health value of natural environments have been remarkable. The growing interest in this topic (often housed under terms such as green and/or blue space) has been occurring in parallel with the microbiome revolution and an increased use of remote sensing technology in public health. In the context of biodiversity loss, rapid urbanization, and alarming rates of global non-communicable diseases (many associated with chronic, low-grade inflammation), discussions of natural vis-a-vis built environments are not merely fodder for intellectual curiosity. Here, we argue for increased interdisciplinary collaboration with the aim of better understanding the mechanisms—including aerobiological and epigenetic—that might help explain some of the noted positive health outcomes. It is our contention that some of these mechanisms are related to ecodiversity (i.e., the sum of biodiversity and geodiversity, including biotic and abiotic constituents). We also encourage researchers to more closely examine individual nature relatedness and how it might influence many outcomes that are at the interface of lifestyle habits and contact with ecodiversity.
REVIE W Open Access
Natural environments, nature relatedness
and the ecological theater: connecting
satellites and sequencing to shinrin-yoku
Jeffrey M. Craig
1,4*
, Alan C. Logan
2,4
and Susan L. Prescott
3,4
Abstract
Recent advances in research concerning the public health value of natural environments have been remarkable.
The growing interest in this topic (often housed under terms such as green and/or blue space) has been occurring
in parallel with the microbiome revolution and an increased use of remote sensing technology in public health. In
the context of biodiversity loss, rapid urbanization, and alarming rates of global non-communicable diseases (many
associated with chronic, low-grade inflammation), discussions of natural vis-a-vis built environments are not merely
fodder for intellectual curiosity. Here, we argue for increased interdisciplinary collaboration with the aim of better
understanding the mechanismsincluding aerobiological and epigeneticthat might help explain some of the
noted positive health outcomes. It is o ur contenti on that some of th ese mechanisms are related to ecodiversity
(i.e., the sum of biodiversity and geodiversity, including biotic and abi otic con stituents). W e also enco urage
researchers to more closely examine ind ividual nature r elatedness and ho w it might in fluence many outcomes
that are at the interface of lifestyle habits and contact with ecodiversity.
Viewpoint
The study of physiological anthropology concerns it self
with understanding the ways in which the modern en-
vironment exert s selective pressures on humans and to
what extent those pressures influence physiology. As
such, physiological anthropology is ultimately a study
of health and well-being and enjoys a spe cial place a s a
central hub between countless branches of science and
medicine. At times, some of the research developed
throu gh other disciplinespublic health, psychology,
environmental sciences, and ecology to name but a
fewmay seem disconnected from physiological an-
thropology. Conversely, some of the research produced
by experts in physiological anthropology may not be
immediately apparent to those in other isolated fields.
Here, in this invited Viewpoint, we will att empt to
sew together some of the rapidly acc umulating resea rch
on natural environments and identify ways in which
biodiversity (and products of biodiversity) interact with
psychological constructs (under the rubric of nature
relatedness or an individuals c onne ction to nature).
The aim of this effort is to highlight that there are
many potential linkages between psychology and physi-
ologyinthemodernenvironmentthathaveyettobe
married. As described below, an individualsconnection
to na ture is associated with health and w ell-being. We
wonder, what are the physiological conne ctions be-
tween the two? These have not been explored. Could it
be that physiological changes in a certain environment
impact on nature relatedness?
Moreover, a growing body of research utilizing satellite
technology has demonstrated clear associations between
natural environments and a wide variety of positive
health outcomes. Yet, the interpretations of such re-
search remain limited because mechanismsincluding
those pertaining to physiology and psychologyremain
largely unexplored. Finally, a third area of research mov-
ing at a brisk pace is that pertaining to the microbiome.
Thanks in large part to advances in high throughput
sequencing and other methods, we can now study hu-
man and environmental bacterial communities with
* Correspondence: jeff.craig@mcri.edu.au
1
Murdoch Childrens Research Institute; Department of Paediatrics, University
of Melbourne, The Royal Childrens Hospital, Flemington Road, Parkville,
Victoria 3052, Australia
4
International Inflammation (in-FLAME) Network, Worldwide Universities
Network (WUN), Perth, Australia
Full list of author information is available at the end of the article
© 2016 Craig et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
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reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Craig et al. Journal of Physiological Anthropology (2016) 35:1
DOI 10.1186/s40101-016-0083-9
unprecedented pre cision. Again, we highlight that these
advances are of great relevance to physiological anthropol-
ogy because the microbiome research may also explain
much about physiology in the modern environment. How-
ever, this too may be a product of individual relationships
to the modern environment.
Here, we will examine some important history and use
research advances (starting in the Advances in research
section) to highlight that there are potentially fruitful
lines of research that could link what is already known
concerning in vivo research on natural environments
(exemplified by Japanese shinrin-yoku), publ ic health
data gathered from satellites, microb es (and products of
biodiversity), and individual connection to the environ-
mentall with an eye toward expanding what is known
on the physiological plane. We do so by acknowledging
at the outset that some of the connections are specula-
tive. Some have only limited research to support them.
Yet, in a rapidly changing, urbanizing world, we suspect
that the study of these potential interconnections is an
urgent task not only for physiological anthropology but
also for science an d medicine.
Forests and physiology
When the giant of the forest dies and falls to the
ground, it is by the action of the bacteria that the
tree trunk gradually disappears from viewthis is
the secret of natures eternal freshnessdissipated in
the air or into simple compounds which sink into the
Earth. Red Cross Notes on Useful Bacteria, 1900 [1]
Twenty-five years ago, Japanese scientists traveled t o
Yaku island (Yakushima; shima = island in Japanese) to
determine if spending time in a forest environment
might influence mood and markers of stress physiology.
Althoughapreliminarystudybasedonaverysmall
sample, the results indicated that walking in a forest
environment could provide a lift in mood and reduce
objective markers of stress physiology [2]. The first
small step toward proper in vivo investigation of natural
environments was taken; Yakushima as a location to take
that giant leap for humankind was highly appropriate.
Yakushima includes a 19,000-ha area designated as a
biosphere reserve. Sitting at a biogeographic boundary be-
tween tropical and temperate regions, the island contains
a remarkably rich variety of flora. Walking on this small
island translates into visual encounters with evergreen
broadleaf forests, conifer, 2000-year-old cedar trees, and
nearly 2000 different plant species [3]. Pioneering re-
searchers exploring the effects of the forest on mood and
stress were not merely interested in the visual.
Throughout the 1990s, Japanese researchers started
asking fundamental questions. Does walking in a forest
influence mood state and stress physiology? And if so,
might the forest environment specifically amplify the
benefits of generalized physical activity? Could the forest
environment influence stress physiology by olfactory or
other non-visual pathways?
Researchers set their sights on phytoncides, a gene ral-
ized term for natural chemicals released by plant s into
the environment. It was theorized that these chemicals
could influence stress physiology through inhalation.
Preliminary findings were published in an English-
language textbook [2], and work on forest-based exer-
cise therapy in patients with diabetes wa s reported in
the International Journ al of Biometeorology (IJB) in
1998marking the first time that the Japanese term
shinrin-yoku would be uploaded to PubMed [4].
The t e rm shinr i n-y ok u struck a chord. More than a
visual (e sthetica lly pleasing ) experience in nat ure,
shinrin-yoku was described a s forest-air bathing , with
an empha sis on what wa s encountered during bre ath-
ing.Theshin rin - y o k u experience allowed an individual
to literally take in the component s emitted from the
forest [4]. Since forest air i s rich in volatile and non-
volatile components and other unseen constituents
that might be absent (or found in lower quantities) in
urban built environments, shinrin-yoku was not merely an
escape from toxic urban air [2, 4]. Walking through for-
ests on Yakushima, therefore, was an opportunity to
visualize, touch, listen to, and inhale nature. It meant
bathing in biodiversity.
Aerobiology and the hygiene hypothesis
At the same time and along somewhat related lines, ex-
perts in aerobiology were also beginning to turn their
attention to the health implications of natural air con-
stituents. This new research direct ion involved environ-
mental biodiversity and the microbial constituent s that
mayormaynotbeencounteredbyhumansinthe
near-surface atmosphere of various settings. Writing in
the textbook Perspective s in Env ironment (1998), r e-
searchers highlighted the health implications of air-
borne biodiversity in the context of allergic disease:
In recent years, special attention has been given to
the biodiversity of airborne biocomponents. These bio-
component s are present in the air in the form of pollen
grains, fungal spores, bacteria, mycelium, cysts, algal fila-
ments and spores, lichens, insects and their parts, plants
and animal tissues, and several other microorganisms.
The presence of such biomatter in the air depends upon
the occurrence of diversity of flora and fauna in the sur-
roundings. [5]
This interest was undoubtedly fueled, at least in part,
by the so-called hygiene hypothesis. The generalize d idea
of the original hypothesis and its variants is that the glo-
bal rise in allergic disease could be related to diminished
Craig et al. Journal of Physiological Anthropology (2016) 35:1 Page 2 of 10
opportunity for early-life exposure to pathogenic (and
diverse commensal) microbe exposure via increased hy-
giene, antibiotic use, smaller family sizes and lower ex-
posure to bacteria in foods, and the overall environment
[6, 7]. The end result of altere d microbial contact in
modern environme nts was an abnormally stable micro-
flora [7]. It has been theorized that this new normal
creeping into developed, urbanized, industrial nations, a
microbiota of modernity, might not be in the best inter-
est of health promotion.
Eye in the sky
As international researchers toiled away at identifying
airborne biocomponents (still largely reliant upon cul-
ture technique for microbial evaluation), and while the
first Japanese research subjects walked through forests,
earth observation satellites were in orbit several hundred
miles above them. Among other things, the satellites dedi-
cated to earth science were measuring different wave-
lengths and intensities of visible and near-infrared light
reflected by the land surface. This allowed for a normal-
ized difference vegetation index (NDVI) of greenness or
vegetative vigor [8].
In the late 1990s, the utility of satellite technology to
assist in land-based ecological assessmentsmeasures of
biodiversitywas beginning to take shape [9]. However,
the initial public health application of NDVI was under-
standably in priority orderassessments and modeling
of drought, disease ve ctors, threats to food supply, envir-
onmental contamination, and so on. It would take a bit
of time before remote sensing would break through a s
an important tool to examine broad health and well-
being endpoints.
Advances in research
The application of remote sensing as a means to link
residential proximity to green natural environments and
risk of chronic, non-communicable diseases, socioeco-
nomic disparities, and other public health outcomes has
witnessed tremendo us growth. Layered upon large co-
hort data and the results in favor of a green spa ce bene-
fit are literally visible in the health outcome statistics
[1015]. Of course, the NDVI does not tell us whether
or not a person actually uses natural environments for
physical activity and social engagement. Furthermore,
emerging studies are indicating that access to natural en-
vironments and public open spaces may be intertwined
with complex non-communicable diseases (NCDs) de-
terminants such as dietary patterns [1620]; however,
there are likely to be unt old benefits of simply having
good quality green space in the residential proximity
[21]. The most obvious might be clean air [22].
Field research involving natural environments has also
grown. While still requiring larger sample sizes and
replication of existing work, studies involving shinrin-
yoku (now generally referred to in Japanese studies as
simply forest medicine or forest therapy) have grown
in sophistication. Spending time in a forest environment
has been linked with decreased cortisol, inflammatory
cytokine (and chemokine) production, lowered blood
pressure, improved heart rate variability, and elevations
in natural killer cell activity [2329].
These outcomes are highly relevant to the current epi-
demic of chronic, inflammatory NCDs. In addition, re-
search designs now involve urban built environment
(control) exposure, gender differences, personality fea-
tures, seasonal influences on foliage, and experimentation
with forest components such as sounds and airborne phy-
toncides [3033]. The studies in natural environments
have also enjoyed technological advances that allow for
more convenient in-field assessments (e.g., electroenceph-
alogram, cortisol).
Then we have the so-called microbiome revolution.
Discussions of the possible use of beneficial microbes
for NCD prevention and/or treatment, including mental
health, are no longer met with blank stares and yawns.
Advances in culture-independent, high-throughput se-
quencing technology have woken the disinterested from
their slumber. Microbes matter. Although there are far
more questions than answers, the relevancy of indoor
and outdoor microbial contact to health has now moved
closer to center stage [3437].
In sum, the early origins of each section of primary
research discussed thus farin vivo experiments on
natural environments, the use of remote satellite technol-
ogy to access greenness in public health, and examination
of airborne (including living constituents)have grown
leaps and bounds. Largely, they have developed apart from
one another. Now, we will attempt to reconcile some of
this research, or at least its possibilities, in ways that might
benefit the stimulation of future research ideas.
Microbes, phytoncides, ionsair to brain?
Microbes are a less obvious part of the biodiversity en-
countered on walks through natural environments. We
know with a greater degree of certainty that the bark of
trees , the stems, leaves , and needles of forested and
vegetation-rich areas are teeming with microbial diver-
sity [3840]. Forest soils are also incredibly rich sources
of microbial diversity [41]. We know that microbes, in-
cluding those from the soils and leaf/needle surfaces of
forests, are readily dispersed in the air [4244], and we
also know that Yakushima has some very interesting soil
microbes [45]!
Microbes also interact with two other unseen con-
stituents of the near-surface atmosphere in natural
environmentsphytoncides and air ions. Numerous
studies have found a relatively higher concentration of
Craig et al. Journal of Physiological Anthropology (2016) 35:1 Page 3 of 10
negatively charged ions within natural environment s ,
especially within forest s and area s close to bodies of
water [ 25, 46, 47]. Waves, whitecaps, and waterfalls can
producearelativeincreaseinnegativeions[48]and
also promote t he eje ction of microbes into the atmos -
phere [49].
Research concerning negative ions has been clouded
by marketing overreach associated with commercial ion-
generating machines. However, evidence does point to
beneficial effects on mood and inflammation [50, 51].
Phytoncides and negative ions enjoy a bi-directional re-
lationship in natural environments, with higher concen-
trations of one influencing the other [52]. Of course,
phytoncides are a product of plant interaction with mi-
crobes, and both phytoncides and negative ions may
dictate the microbial makeup in the air within a natural
environment. Dubos cites older research wherein the
relative ly h igh concentration of p ositive air ions was as-
sociated with dec reased intestinal lactobacilli in infants
[53]. Examining interactions between phytoncides, mi-
crobes (skin, intes tinal, lung), and air ions with more
sophisticated modern te chniques is an area ripe for re-
search in physiological anthropology.
In the meantime, it would seem obvious that microbes
are part of a complex discussion concerning what might
(or might not be) inhaled within differing environments.
The field of microbiome research is sufficiently advanced
to put forward a theoretical framework of how airborne
microbiotaboth directly and indirectlycan influence
the human brain and behavior. Skin microbiota, no lon-
ger viewed as an external entity, are capable of influen-
cing systemic immune function [54, 55]. Research shows
marked differences in the skin microbiota or rural and
urban residents [56]. The intra-nasal administration of
non-harmful microbe s can also influence systemic im-
mune signaling [5759].
The inhalation of phytoncide is known to reduce
physiological stress [60], and how that might impact in-
testinal microbiota in the context of the emerging gut-
brain-microbe research is unclear. Given the detrimental
influence of stress on the microbiome [61], it would be
easy to spe culate t hat stress reduction could temper
dysbiosis. Animal research involving the oral adminis-
tration of very minor amounts of phytonc ides der ived
from Korean pine (a mere 0.2 % of total dietary
intake)hasshownthatphytoncidecanimprove
gastrointestinal microbiota profile and nutrient digest-
ibility [62].
Reviewed in detail elsewhere [63], pathwa ys connect-
ing intestinal microbes to brain include communication
via the vagus nerve, immune-mediated pathways (in-
cluding microglia [64]), intestinal barrier maintenance,
limitation of oxidative stress, enhancement of nutrient
bioavailability, and neurotransmitter precursors. Current
evidence also suggest s that changes to the microbiome
results in widespread changes to gene expression in af-
fected organs and in organs such as the brain. Such
changes have been shown to be mediated by epigenetic
factors which can lead to long-term changes in gene
expression without a change in DNA sequence [65]. Epi-
genetic mechanisms involv e the binding of small mole-
cules to DNA and the histone proteins responsible for
packaging and thereby regulating DNA. Such mecha-
nisms include methylation of the CpG dinucleotide in
DNA, acetylation and methylation of histones, and the
binding to DNA of small non-coding RNAs.
Although diet has been the primary research focus
concerning intestinal microbial diversity, we take this
opportunity to highlight that other external environmen-
tal factors also seem to play a role in how intestinal mi-
crobial communities take their shape [6670]. In other
words , it is entirely possible that natural environments
can impact upon all human-associated microbial com-
munities, which in turn could influence nerve cell com-
munication. Taken together, the above evidence provides
plausible mechanisms by which externa l environmental
(including airborne) microbiota can bring about feelings
of pleasure and change our mental and physical health
for the better.
Vis medicatrix naturae
Although it has taken quite a few years, t hese seemingly
disparate areas of rese archforest walking, exploration
of the unseen components of air within natural envi-
ronments, and green s pace epidemiolo gy via remote
sensinghave begun to interse ct. In their own w ays,
each area of research has been e va luating the extent to
which natural environments might work toward health
promotion [71, 72]. The available e vidence suggests that
natural environments might influence mood and stress
physiology. A buffering of allostatic loadreduction of
the destructive tandem of low-grade chronic inflamma-
tion and oxidative stresscan provide a potential
mechanistic link to both healthy birth outcomes and
mortality reduction rel ated to NCDs [73].
We began our viewpoint discussions with Yakushima
not simply because it was the birthplace of the scientific
investigation of shinrin-yoku. Islands are hotbeds of
plant diversity20 % of the world s plant species are
found only on islands. Yakushima, with its various cli-
mate zones and rich geological history, represents the
need to bring the natural environments-public health re-
search trail toward the question of diversity.
There are hints that the value of natural environments
in relation to complex non-communicable diseases
(mental health in particular) may be a by-product of bio-
diversity [7479]. What sort of diversity is the que stion?
It could be diversity in species of trees and/or vegetation
Craig et al. Journal of Physiological Anthropology (2016) 35:1 Page 4 of 10
and birds (and the audible sounds of diversity). It might
be encounters with non-harmful environmental mi-
crobes (especially those encountered in less urbanized,
traditional societies) and/or the natural airborne chemi-
cals that are a product of biodiversity (e.g., phytoncides)
secreted from trees and other plants [80, 81], or it could
be a synergistic combination of the lot?
Of course, natural environments are so much more
than their biotic components. A century ago, biologist
Sir John Arthur Thompson proposed that human evolu-
tionary connections to natural environments were being
eroded by urbanization. In his keynote address to physi-
cians of the British Medical Association, he focused on
vis medicatrix naturae (the healing power of nature) and
interpreted it to be clinically relevant, mindful contact
with the biotic and abiotic elements of nature. As he
said: We have put ourselves beyond a very potent vis
medicatrix if we cease to be able to wond er at the grand-
eur of the star-strewn sky, the mystery of the mountains,
the sea eternally new…” [82].
Philia overload: ecodiversity and human health
The study of plants and animals carries an impressive
lesson as to the unity prevailing amid all the diversity
of Naturethe grand outcome of geological study is
that it brings vividly before the mind the immen sity
of timethe contemplation of past geological ages,
reckoned by millions of years, the fact that our Earth
is coeval with the sun in age - all these considerations
tend to immeasurably expand our mental horizon,
and thus to react in a way to broaden the mind.
Alpheus S. Packard, Brown University, 1892 [83]
Although biologist Edward O. Wilson did not coin the
term biophilia (see [71] for its historical use), in 1979, he
argued that it is the rich, natural pleasure that comes
from being surrounded by living organisms, not just
other human beings but a diversity of plant s and ani-
mals [84]. Almost two decades earlier, geographer Yi-Fu
Tuan introduced the term topophila, originally defining
it as a love of nature [85] and subsequently as the
affective bond between people and place or setting [86].
Landscape architect Robert Thayer suggested that geo-
philia or gaiaphilia might be more appropriate terms for
a generalized love of the land and the Earth , including
its abiotic parts [ 87].
It is not our desire to introdu ce yet another philia
into the natural environments discussion. However, it is
becoming increasingly clear that geodiversitythe vari-
ability of the Earths surface materials, landf orms (e.g.,
mountains, bodies of water) and physical processesis
highly relevant to biodiversity, ecosystem ser vices, and
conservation [88, 89]. It is interesting to note that in
human research directed at the e valuation of the pri-
mary domains underlying Tuans topophilia, only the
ecodiversity category emerged a s significantly and posi-
tively correlated to respondents qualityoflife[90].
Areas with noted plant spe cies diversity, including
forests , are often at the rich end of geodiversity. They
are typically mountainous and sitting on a steep climate
gradient (Yakushima ha s both of these attributes) or
areas such a s Southwestern Australia , California, and
other world regions that enjoy a Mediterranean climate
[91]. Throughout histor y, our ge nus has been evolving
at the genetic and epigenetic level be cause living organ-
isms,asJohnArthurThompsonstated,enter into s ub-
tle inter-relations with their inanimate environment,
whence also new complexities spring [92]. G eodiver-
sity is not only part of those complexities; in the con-
text of ecosystem ser vices, it is also a matter of human
health and well-being.
In 1996, the biotic and abiotic environmental terms
were incorporated into a simple concept of ecodiversity.
As defined by Barthlott, ecodiversity is the total diversity
of a region, including the sum of its biodiversity and
geodiversity [93]. It also considers the highly relevant
factor of climate. Natural environments and human
health, particularly mental health, are obviously discus-
sions involving natural light, temperature, and weather
[94, 95]. Weather-related factors may also determine the
microbiota with which one may make contact [96]. As
such, ecodiversity underscores that biodiversity is
dependent upon a host of abiotic factor sconsiderations
of which pass through the expertise of many scientific
disciplines.
If we truly seek to encourage interdisciplinary dialogue
and liberate silo-sequestered research related to public
and planetary health, then perhaps adoption of the term
ecodiversity is not merely name-game semantics. The bio-
philia hypothesis posits that humans have an innate need
for affiliation with other forms of life, most notably the
visible portions of life such as savannah-like trees. It was
an extension of JA Thompsons1914vis medicatrix
naturae hypothesis. Rene Dubos continued the theme of
universal fellowship with all other human beings and
even with other forms of life
[97] in his biological joie de
vivre hypothesis described elsewhere [71].
As a microbiologist, Dubos also forewarned (nearly five
decades ago) of the NCD epidemic that might precipitate
via a disconnection from the microbes with which we co-
evolved. The recent biodiversity hypothesis further pro-
poses that loss of biodiversity at the level of macrobiota
will translate into loss of contact with microbiotic diver-
sity. Specifically, biodiversity loss leads to reduced inter-
action between environmental and human microbiotas.
This in turn may lead to immune dysfunction and
impaired tolerance mechanisms in humans [98].
Craig et al. Journal of Physiological Anthropology (2016) 35:1 Page 5 of 10
If only for convenience, it might be helpful to ro ll
these and other overlapping hypotheses related to
modern lifestyle mismatches into a universal e vol ution-
ary health concept that considers contextual biotic and
the abiotic determinants of the so-called disea ses of
civilization. Famed e cologist G. Evelyn Hutchinson
folded the abio tic/biotic into the metaphor of an eco-
logical theater in which an evolutionary play is tak-
ing p lace [99]. For the better part o f three mill ion
years, our genus has been a player on that stage, in
many ways like actors in a long-running Broadway
play. The stage and the production of the play have, of
course, changed to some degree over space and time.
However, modern human lifestyles have rapidly chan-
ged both the theater and the play.
Diminished contact with e volutionary-rooted ecodi-
versity appears to be a product of modernity. This can
be extended to inclusion of those aspects of the modern
landscap e and lifestyle that are incompatible with levels
of adequate natural daylight and very low levels of light at
night under which humans evolved. However, at this
point, lack of contact with ecodiversity is not well estab-
lished in its linkage to NCDs vs. other lifestyle contribu-
tors, such as higher consumption of ultra-processed foods
and sedentary behavior. The role of urbaniz ation on
biodiversity is complex and may, in certain cases, actu-
ally increa se species richness at t he cost of native spe-
cies [100].
At present, there is little evidence to show that the
promotion of human health, reduction of NCD risk, and
the minimization of psychological distress are sitting
along a neatly defined and universal continuum in favor
of the countryside and biodiversity [101, 102]. The role
of biodiversit y loss in elevated communicable disease
risk is becoming more clear [103]. As yet, early life ex-
perience with microbial exposure via traditional lifestyles
has not been proven to differentially alter later-life im-
mune responses in complex mental disorders such as de-
pression [104]. Moreover, urbanization does not appear to
automatically translate into significant differences in dom-
inant microbial communities in the outdoor air, at least
not in North America [105].
Many unanswered questions
Despite recent advances, and much needed convergence
of research pathways, there are many unanswered ques-
tions concerning natural environments and their utility
in policy and practice. Basic questions are now obvious,
including those related to dose. For example, how
often and for how long does one have to visit a natural
environment in order to enjoy meaningful health-related
benefits? Does the type of natural environmentits
physical features, spatial arrangement, biodiversity, geo-
diversity, climate, weather, density of trees, sounds,
smells, microbiota, natural light, air ions, soils, and
sandmatter to health outcomes?
It also seems reasonable to ask if time of day matters,
or if an optimal time to spend time in natural environ-
ments might exist? We would speculate that such a time
might be early morning. There are several features of
natural environments in the morning that could differ-
entiate mood and/or physiological outcomes vs. after-
noon. First, the mood-regulating [106] blue portion of
the natural light spectrum is highest in the morning
[107, 108]. Second, phytoncides are more abundant in
the morning [109]. Third, culture-based techniques
show that certain airborne microbes in forests and other
natural environments (coastal, rural) are also signifi-
cantly higher before noon [43]. And four th, negative ions
may also be relatively higher in the morning [110, 111].
There are also required discussions concerning the
dangers that might e xist in natural environmentsin-
cluding but not limited to disease-carrying vectors ,
predators, allergens , and excess exposure to ultraviolet
radiation. We ne ed to learn more concerning the phys -
ical aspe ct s of natural environment s that might actually
induce fear and compromise t he endgame o f outcomes
such as stress reduction and improved vitality [112].
Not e very study has found natural environments to be
associated wit h positive health outcomes [113, 114],
and these negative studies may provide essential in-
formation concerning the limitations of green space
relative to other biopsychosocial factors.
Connection to nature
It seems evident that not every person who lives close to
natural environments, or walks through a lush forest, is
going to receive the same benefits. To what extent are
previous experience with and perceptions of nature
guiding those differences? Nature relatedness (NR) (and
similar psychological con structs such as nature connect-
ivity, nature connectedness) have been connected to
mental well-being [115, 116]. Briefly, the NR and other
such scales can measure an individua l s fascination with,
interest in, and desire for nature contact. Moreover, the
measurements go beyond superficial love of nature;
they can also tap into awareness and understanding of
the natural world, including the bits of ecodiversity that
might not be aesthetically pleasing.
We would encourage researchers to incorporate vali-
dated nature connectivity scales into research protocols.
For convenience only, we point toward the validated six-
question short form (nature relatedness-6; NR-6) that can
rapidly capture an individuals orientation to nature [117].
The NR-6 (and other scales) could be folded into a variety
of studies that could provide critical unifying information;
these findings could link many aspects of seemingly
Craig et al. Journal of Physiological Anthropology (2016) 35:1 Page 6 of 10
disconnected research. Here, we provide ten examples of
what we consider to be worthwhile questions:
1. Is NR connected to healthier lifestyle habits?
Dietary patterns? Fermented food consumption?
Physical activity?
2. Is NR associated with differing skin, oral, or
intestinal microbiota/microbiome?
3. Is NR associated with risk of NCDs? Is it connected
to physiological markers of allostatic load? Could
subgroups in epidemiological studies be evaluated
for NR? Given the emerging studies on green space
and healthy birth outcomes [118] and inverse
associations between surrounding greenness and
incident asthma development [119], we wonder
how maternal NR might mediate these findings?
4. Is NR associated with prescription drug use,
including psychotropics and antibiotics?
5. Is NR linked to genetics and/or epi genetics?
6. Is NR associated with screen time or time spent
indoors? Is it connected to vitamin D levels?
7. Is NR associated with neighborhood features,
perceptions of pollutants, and/or local biodiversity?
Does NR place a higher burden on stress physiology
while encountering human generated noise? For
example, residential traffic noise is associated with
increased risk of depression [120], and we wonder
if those scoring high on NR may experience traffic
noise as more of an irritant?
8. Is NR associated with disgust sensitivity, fear of
microbes, aspects of hygiene?
9. Is NR related to brain activity while viewing nature
vs. urban scenes?
10. Does NR influence outcomes of intervention
studies involving prescription medications and/or
eco-psychotropic agents such as aromatic chemicals
(phytoncides), beneficial microbes, etc.?
Answers to these and other questions could provide an
entirely new direction to research endeavors. If NR is so
valuable to well-beingand numerous studies indicate that
it isthen how do we cultivate it? Application of the NR
scale in studies involving twins would provide tremendous
insight. T hus, as far as learning more about the ways in
which natural environments can influence health, the NR-
6 could provide a research conduit between unseen satel-
lites in space and invisible microbes on Yakushima island.
Finally, and by no means least important, we should
strive to further our understanding of the ways in which
natural environments might foster human interconnected-
ness. As mentioned earlier, natural environments are often
places where the development of social capital can be fos-
tered [121]. Community gardens might represent a prime
example of this phenomenon.
However, it has been shown that NR is associated with
empathy, and images of natural environments (as well as
the presence of plants) can foster pro-social actions, in-
cluding resource sharing [122124]. Moreover, when re-
searchers induce awe via nature scenes, subjects are
more likely to report increased oneness to other human
beings and a more pronounced willingness to do volun-
teer activities [125, 126]. Perhaps ecodiversity may play a
role in connecting humans in as yet untold ways. Vital to
the study of physiological anthropology, we can make at-
tempts to understand how social gains may be manifested
in physiological endpoints.
Call to action
Remote sensing and land-based ecological assessments ,
along with more detailed examinations of just what, pre-
cisely, someone is breathing in while spending time in a
forest or other natural environment [127], can be layered
into experimental outcomes. We can further examine if
the inherent value of physical activity and social engage-
ment is amplified by environments rich in ecodiversity. Of
course, such work can also help to strike the appropriate
balance between health-promoting access to nature and
essential conservation needs [128, 129].
Twenty-five years on, interdisciplinary collaboration
can help bring the discipline of forest medicine (and
more broadly, the therapeutic potential of natural envi-
ronments) into a more prominent place within discus-
sions of preventive medicine and public health. Much has
changed in the last quarter century, especially concerning
the tandem juggernaut of chronic inflammatory NCDs
and climate change. Their collective force is already bear-
ing down upon us [130132], and as such, research
exploring natural and built environments from a psycho-
logical and physiological perspective is not merely a mat-
ter of intellectual fancy. Personal, public, and planetary
health is on the line.
Competing interests
The authors declare that they have no competing interests.
Authors contributions
All authors contributed equally to the intellectual content. They have read
and approved the final manuscript.
Acknowledgements
JMC is supported by the Australian National Health and Medical Research
Council (Grant numbers 437015 and 607358) and the Financial Markets
Foundation for Children (Grant number 032-2007) and the Murdoch
Childrens Research Institute, which is supported in part by Victorian
Government's Operational Infrastructure Support program. All authors are
members of the World University Network's International Inflammation
Network (in-FLAME)
Author details
1
Murdoch Childrens Research Institute; Department of Paediatrics, University
of Melbourne, The Royal Childrens Hospital, Flemington Road, Parkville,
Victoria 3052, Australia.
2
CAMNR, 23679 Calabassas Road, Suite 542,
Craig et al. Journal of Physiological Anthropology (2016) 35:1 Page 7 of 10
Calabassas, CA 91302, USA.
3
School of Paediatrics and Child Health, Princess
Margaret Hospital for Children, University of Western Australia, GPO Box D
184, Perth, WA 6840, Australia.
4
International Inflammation (in-FLAME)
Network, Worldwide Universities Network (WUN), Perth, Australia.
Received: 29 July 2015 Accepted: 7 January 2016
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Craig et al. Journal of Physiological Anthropology (2016) 35:1 Page 10 of 10
... Restoring human connections to nature may therefore provide a critical common pathway to mitigate adversity and promote the physical [34][35][36][37] and spiritual well-being of individuals [30,35,38,39] and communities [40,41], as well as personal and collective social and environmental responsibility [42][43][44]. ...
... Restoring human connections to nature may therefore provide a critical common pathway to mitigate adversity and promote the physical [34][35][36][37] and spiritual well-being of individuals [30,35,38,39] and communities [40,41], as well as personal and collective social and environmental responsibility [42][43][44]. ...
... A connection to nature is also linked to health behaviors, including physical activity, coping with stress, social behaviors, and even dietary choices [35,55,56]. For example, NR was positively associated with dietary diversity and fruit and vegetable intake in an urban population [57]. ...
Conference Paper
Full-text available
The vast and growing challenges for human health and all life on Earth require urgent and deep structural changes to the way in which we live. Broken relationships with nature are at the core of both the modern health crisis and the erosion of planetary health. A declining connection to nature has been implicated in the exploitative attitudes that underpin the degradation of both physical and social environments and almost all aspects of personal physical, mental, and spiritual health. It is increasingly clear that the entwined challenges of biodiversity loss, climate change, and human health cannot be addressed without addressing selfishness, greed, apathy, and the value systems that created these global problems. Calls for a spiritual and cultural transformation recognize that “inner” development is important and necessary for meaningful “outward” transitions with a shared purpose for wiser, more sustainable societies. Many of these emotional and spiritual assets appear to be facilitated by a connection to nature, which is also strongly associated with community cohesion, prosocial attitudes, and pro-environmental actions. Restoring the human connection to nature may therefore provide a critical common pathway to promote the physical and spiritual wellbeing of individuals and communities as well as personal and social environmental responsibility. In this paper, we summarize and reflect on the discussions of the Nova Network planetary health community with respect to nature-based solutions as pathways to promote both personal and planetary health with a more mutualistic mindset. These discussions spanned biological to psychological interactions with nature—including the critical relationships with environmental microbes that influence the physical, emotional, and behavioral aspects of health. We consider the ways in which stronger relationships with nature promote “inner assets” to support “outward actions” for personal and planetary health.
... Notably, stronger relationships with nature through contact with green space also increases pro-environmental attitudes and actions [59,60]. Restoring these crucial connections may therefore provide a critical common pathway to mitigate adversity and promote the physical [61][62][63][64] and spiritual well-being of individuals [62,[65][66][67] and communities [27,68]. It also enhances personal (and collective) social and environmental responsibility [69][70][71]. ...
... Notably, stronger relationships with nature through contact with green space also increases pro-environmental attitudes and actions [59,60]. Restoring these crucial connections may therefore provide a critical common pathway to mitigate adversity and promote the physical [61][62][63][64] and spiritual well-being of individuals [62,[65][66][67] and communities [27,68]. It also enhances personal (and collective) social and environmental responsibility [69][70][71]. ...
Article
Full-text available
Healthy social connections—belongingness and relatedness to others—are considered to be basic human needs [...]
... For example, the volatile organic compounds present in forests have positive effects on health [56][57][58], and studies have investigated the beneficial effects of the presence of birds [59][60][61]. The richness of biodiversity in an urban forest ecosystem may have psychological benefits [62][63][64], but a "wild" forest ecosystem would be more beneficial to health than would a managed urban forest [65]. Although health benefits may vary according to the type of environment [66][67][68], not all forest ecosystems are conducive to resourcing [12]. ...
Article
Full-text available
Forest frequentation is associated with benefits for human health, warranting the importance of forest-based health practices. These practices can be classified into four categories: connection with nature (e.g., Shinrin-Yoku, yoga, and meditation); sports, outdoor, and adventure activities; Indigenous health practices on the land; and professional consultations in a natural environment. The aim of this research was to better understand the social representations of the forest supporting these practices and the environmental characteristics that are favorable to them, as well as to examine the effects of these practices on the forests. We interviewed 28 forest-based health practitioners in Quebec and conducted four participant observation activities. Data analysis led us to five forest representations: an entity in its own self, an unfamiliar area, a place of attachment, a land at the heart of Indigenous cultures, and a tool to improve health. The results showed that favorable environmental characteristics varied according to the type of health practice. The presence of water (e.g., drinking water, lakes, and rivers) is favorable to all forest-based health practices and access to nature seems to be an issue for many practitioners. We also found that forest-based health practices were leaving traces in the forest and attempting to redefine the place of humans in nature.
... (Barbiero, 2021, 51). In fact, we suggest that an expansion of biophilia toward geophilia is not only possible, but even necessary to fully comprehend the multifaceted emotional connections humans have with ecological systems (see Thayer, 1989;Faulstich, 2006;Craig et al., 2016). The intermediate concept of "topophilia," which Yi Fu Tuan introduced in the 1970s (Tuan, 1974), refers to the human "sense of place," or the feeling of connection to a specific milieu (usually a socio-natural one). ...
... Such applied studies have investigated factors including temperature, light, sound [30], odors [31], and textures of materials [32][33][34]. There are studies not only on negative effects but also on positive effects such as the ability to recover from problems and to be comfortable without invisible stresses [35,36]. ...
Article
Full-text available
... Investigaciones han demostrado que las personas, al vivir o frecuentar espacios verdes, presentan mejor salud física y mental, así como menos complicaciones que aquellas personas que viven en zonas con pocas AVU (de Vries et al., 2003); además, un metaestudio encontró una correlación positiva entre la cantidad de AVU y la percepción de la salud mental (van den Berg et al., 2015). Un modelo considera que la naturaleza promueve la salud en general a través de los siguientes factores: (1) la calidad del aire, pues se cree que la respiración en las AVU puede tener efectos beneficiosos para la fisiología humana y la salud mental (Craig et al., 2016); (2) la actividad física, porque se evidenció que en las AVU las personas experimentan mayores emociones positivas y menos fatiga al realizar ejercicios (Bowler et al., 2010); (3) la cohesión y el contacto social, debido a que son espacios donde los vecinos se encuentran y socializan (de Vries et al., 2013); y (4) la reducción del estrés, debido a que los espacios naturales promueven una restauración más rápida y completa de síntomas físicos y mentales (estrés) que los ambientes construidos (de Vries et al., 2013;Collado et al., 2017). Por lo tanto, observamos que la naturaleza en espacios urbanos genera un beneficio en la salud que no podemos ignorar, y más bien nos invita a reflexionar de su prioridad al planificar ciudades, pero no nos deja en claro cómo beneficia al rendimiento académico. ...
Article
Full-text available
Las áreas verdes urbanas son conocidas por transmitir paz y bienestar a las personas expuestas a ellas. Debido a ello, las políticas públicas consideran que las áreas verdes deben estar incluidas en la planeación urbana; sin embargo, la evidencia indica que no muchos centros urbanos tienen a su disposición dichas áreas; es decir, hay personas que, por vivir en ciertos distritos, se beneficiarían más de los efectos positivos de la naturaleza que otros. ¿Cómo se daría en el caso de los estudiantes durante la pandemia? Este ensayo presenta evidencia acerca de cómo la naturaleza nos mejora la calidad de vida y las repercusiones que nos produce al no estar expuestos a ella. Especialmente en estos tiempos de pandemia, porque en Lima no todos los distritos tienen el mismo acceso a dichas áreas.
... Forest air is refreshing because trees clean the air of pollutants such as nitrogen oxides and sulfur oxides, produce oxygen, and release volatile bioactive terpenes into the air [1]. Research from Japan [1], South Korea [2], China [3], Taiwan [4], Australia [5], the United States [6], Italy [7], Denmark [8], Norway [9], the United Kingdom [10], Luxembourg [11], Iceland [11], Finland [12], Sweden [13], Hungary [14], Germany [9] and Austria [15] suggests that spending time in the forest promotes relaxation, lowers stress hormones and blood pressure [16] and strengthens the immune system [17]. Most studies compared stays in the forest to stays in the city. ...
Article
Full-text available
Research suggests that stays in a forest promote relaxation and reduce stress compared to spending time in a city. The aim of this study was to compare stays in a forest with another natural environment, a cultivated field. Healthy, highly sensitive persons (HSP, SV12 score > 18) aged between 18 and 70 years spent one hour in the forest and in the field at intervals of one week. The primary outcome was measured using the Change in Subjective Self-Perception (CSP-14) questionnaire. Secondary outcomes were measured using the Profile Of Mood States (POMS) questionnaire and by analyzing salivary cortisol. We randomized 43 participants. Thirty-nine were allocated and included in the intention-to-treat analysis (90% female, mean age 45 years). CSP-14 in part showed significant differences—total score (p = 0.054, Cohen’s d = 0.319), item “integration” (p = 0.028, Cohen’s d = 0.365)—favoring the effects of the forest. These effects were more pronounced in summer (August). In October, during rainfall, we detected no relevant differences. POMS only showed a significant difference in the subcategory “depression/anxiety” in favor of the field. The amount of cortisol in saliva was not different between the groups. A short-term stay in a forest in summer caused a greater improvement in mood and well-being in HSP than in a field. This effect was not detectable during bad weather in the fall.
Article
Full-text available
Background: Mental well-being plays a pivotal role within the broader spectrum of health and illness, encompassing factors such as stress, depression, and anxiety. Nature-based therapeutic interventions have emerged as a promising approach to addressing these mental health challenges. This study seeks to assess the impact of these interventions on stress, depression, and anxiety levels. Methods: We conducted an extensive search for randomized clinical trials that examined stress, anxiety, and depression levels. The selected studies underwent a rigorous risk-of-bias assessment following the guidelines outlined in the Cochrane Handbook for Systematic Reviews. Results: Our review encompassed findings from eight publications. Among them, two studies measuring cortisol levels revealed significant differences between the pre-test and post-test measurements within the intervention groups. In two studies that employed the Stress Response Inventory, a significant decrease in stress levels was observed within the intervention groups in contrast to the control groups. However, no significant differences were noted in studies that utilized the Restorative Outcome Scale. In the assessment of anxiety and depression levels, three studies employed the Positive and Negative Affect Schedule, while four studies utilized The Profile of Mood States scale; none of these studies demonstrated significant differences. Conclusions: The current body of evidence offers limited support for advocating nature-based therapeutic interventions as a primary approach to reducing stress, depression, and anxiety.
Article
Full-text available
Shift work is increasingly common in health services, subjecting healthcare professionals to work schedules that can alter circadian rhythms and eating habits with consequent repercussions for the intestinal homeostasis. The objective of this study was to describe the relationship of rotating work shifts with the intestinal health, sleep quality, and emotional dimension of nursing professionals. In March and May 2019, an observational and comparative study was conducted among 380 nursing professionals from different Spanish cities and divided into fixed shift (n = 159) and rotating shift (n = 221). To carry out the present work, the variables measured were gastrointestinal symptoms, stool consistency and shape, anxiety, depression, sleep, as well as stress and work environment. Nurses with rotating shifts reported more abdominal pain and symptoms of depersonalization, as well as worse sleep efficiency and worse nursing practice environment. In addition, overall scores of the Gastrointestinal Symptom Rating Scale and Hospital Anxiety and Depression Scale were found to be significantly worse in nurses with these shifts. Rotating shift work by nursing staff may be associated with the occurrence of gastrointestinal and anxiety-related symptoms. These findings, together with the presence of negative and insensitive attitudes towards patients by nurses on rotating shifts, should be considered to maintain the quality of healthcare.
Article
Full-text available
Background: Traffic noise affects a large number of people especially in urbanized areas. Noise causes stress and annoyance, but less is known about the relationship between noise and depression. Objective: To investigate the association of residential road traffic noise and depressive symptoms using five-year follow-up data from a German population-based study. Methods: We analyzed data from 3,300 participants of the Heinz Nixdorf Recall study, aged 45-75 years and without depressive symptoms at baseline (2000-2003). Depressive symptoms were defined based on the CES-D 15-item questionnaire (total score ≥17) and antidepressant medication intake. Road traffic noise was modeled per European Parliament/Council Directive 2002/49/EC. High noise exposure was defined as annual mean 24-hour noise levels >55dB(A). Poisson regression with robust variance was used to estimate relative risks (RR), adjusting for the potential confounders 1) age, sex, socioeconomic status (SES), neighborhood-level SES, traffic proximity, 2) additionally adjusting for body mass index and smoking, and 3) additionally adjusting for the potential confounders/intermediates co-morbidities and insomnia. Results: Overall 35.7% of the participants were exposed to high residential road traffic noise levels. At follow-up (mean = 5.1 years after baseline), 302 participants were classified as having high depressive symptoms, corresponding to an adjusted RR of 1.29 (95% confidence interval 1.03, 1.62; model 1) for exposure to >55 versus ≤55 dB(A). Adjustment for potential confounders/intermediates did not substantially alter the results. Associations were stronger among those who reported insomnia at baseline (RR = 1.62; 1.10, 2.59 vs. RR = 1.21; 0.94, 1.57) and appeared to be limited to those with ≤13 years of education (RR = 1.43; 1.10, 1.85 vs. 0.92; 0.56, 1.53 for >13 years). Conclusion: Our results suggest that residential road traffic noise exposure increases the risk of depressive symptoms.
Article
This study investigated the influence of forest walking on blood pressure (BP), profile of mood states (POMS) and salivary cortisol in both young and aged people. Twenty-three young people (Men=11, Women=12) with a mean age of 22 yrs and twenty-five aged people (M=10, W=15) with a mean age of 59 yrs participated in this study voluntarily. Each participant walked about three hours in the forest according to their comfortable walking pace. After forest walking, systolic BP (SBP) and mean BP (MAP) had significantly decreased in aged people (-10±3 mmHg in SBP, and -5±2 mmHg in MBP, P<0.05, respectively) while remained unchanged in young people. The scores for the “tension-anxiety” and “confusion” subscales of POMS were significantly improved in both young and aged people; moreover, the score for the “anger–hostility” subscale in aged people was also improved significantly. Salivary cortisol significantly decreased in young people (-0.22±0.03?g/dl, P<0.05) and had a tendency to decrease in aged people (-0.05±0.03?g/dl, P=0.099). BP variables at baseline were associated with the changes in BP variables (r=0.575 in systolic BP, r=0.581 in diastolic BP, r=0.582 in MAP, and r=0.582 in pulse pressure), respectively. Furthermore, the baseline salivary cortisol was also related to the forest walking-induced changes in that value (r=0.882). Thus, people with higher BP and higher stress markers may show greater effects from forest walking. Collectively, these results suggested that forest walking may have the possibility to reduce resting BP, mental stress and stress markers in both young and aged people; moreover, significant deceases in BP of aged people indicate that forest walking can be an important and novel exercise therapy if undertaken at a comfortable pace.