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Oxytocin-Gaze Positive Loop and the Coevolution of Human-Dog Bonds

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Abstract

Human-like modes of communication, including mutual gaze, in dogs may have been acquired during domestication with humans. We show that gazing behavior from dogs, but not wolves, increased urinary oxytocin concentrations in owners, which consequently facilitated owners' affiliation and increased oxytocin concentration in dogs. Further, nasally administered oxytocin increased gazing behavior in dogs, which in turn increased urinary oxytocin concentrations in owners. These findings support the existence of an interspecies oxytocin-mediated positive loop facilitated and modulated by gazing, which may have supported the coevolution of human-dog bonding by engaging common modes of communicating social attachment. Copyright © 2015, American Association for the Advancement of Science.
The dilution hypothesis provides an alternative
framework with which to explain observations of
the apparent recalcitrance of DOC and lends a
physiological meaning to the operationally de-
fined semi-labileand semi-refractoryfractions
(16,17). We hypothesize that under the dilution
hypothesis, very heterogeneous mixtures of labile
compounds appear semirefractory, whereas in-
creasingly less diverse DOM assemblages con-
taining larger concentrations of some substrates
will present higher microbial growth and DOC
turnover rates, resulting in increasing degrees of
apparent lability. The microbial generation of ap-
parently recalcitrant material (18) from labile
substrates in a process recently dubbed the mi-
crobial carbon pump(19) can also be explained
with the dilution hypothesis. Microbial utilization
of abundant, labile compounds results in hundreds
of different metabolites (20), which are subse-
quently consumed down to the lowest utilizable
concentration. This mechanism explains observa-
tions of relatively concentrated, labile materials
being transformed into apparently recalcitrant
matter through microbial consumption (18)but
does not necessarily imply the formation of struc-
turally recalcitrant molecules. Indeed, recalcitrant
DOC is not defined structurally, but operationally,
as the DOC pool remaining after long experimen-
tal incubations or as the fraction transported in
an apparently conservative manner with the
ocean circulation (1). Thus, the dilution hypothesis
severely limits the feasibility of geoengineering
efforts to enhance carbon storage in the deep
ocean (21)byusingthemicrobialcarbonpump.
FT-ICR-MS characterization of DOC from dif-
ferent oceans (13,14,22,23)andalsofromthis
study (fig. S5) shows no indication of prevalent,
intrinsically recalcitrant compounds accumulat-
ing in substantial amounts. Conversely, FT-ICR-
MS data show that oceanic DOC is a complex
mixture of minute quantities of thousands of or-
ganic molecules, which is in good agreement with
the dilution hypothesis. Mean radiocarbon ages
of deep oceanic DOC in the range of 4000 to 6000
years have been considered as evidence for its re-
calcitrant nature (24,25). However, these are aver-
age ages of a pool containing a mixture of very
old molecules >12,000 years old but also featuring
a large proportion of contemporary materials (26).
Moreover, elevated radiocarbon ages only dem-
onstrate that these old molecules are not being
newly produced at any appreciable ratebecause
that would lower their isotopic agebut does not
necessarily imply that they are structurally recal-
citrant. Furthermore, it is unlikely that natural
organic molecules can accumulate in the ocean in
substantial concentrations and remain recalcitrant
or be preserved for millennia when degradation
pathways for novel synthetic pollutants evolve soon
after these compounds are released in nature (27).
Although there might be a truly recalcitrant com-
ponent in deep oceanic DOC, our results clearly
show that the concentration of individual labile
molecules is a major factor limiting the utiliza-
tion of a substantial fraction of deep oceanic DOC.
These results provide, therefore, a robust and
parsimonious explanation for the long-term pre-
servation of labile DOC into one of the largest
reservoirs of organic carbon on Earth, opening a
new avenue in our understanding of the global
carbon cycle.
REFERENCES AND NOTES
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13. G. Kattner, M. Simon, B. Koch, in Microbial Carbon Pump in the
Ocean, N. Jiao, F. Azam, S Sanders, Eds. (Science/AAAS,
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20. R. P. Maharjan, S. Seeto, T. Ferenci, J. Bacteriol. 189,
23502358 (2007).
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22. R. Flerus et al., Biogeosciences 9, 19351955 (2012).
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321337 (2014).
24. P. M. Williams, E. R. M. Druffel, Nature 330,246248
(1987).
25. J. E. Bauer, in Biogeochemistry of Marine Dissolved Organic
Matter, D. A. Hansell, C. A. Carlson, Eds. (Academic Press, San
Diego, CA, 2002), pp. 405453.
26. C. L. Follett, D. J. Repeta, D. H. Rothman, L. Xu, C. Santinelli,
Proc. Natl. Acad. Sci. U.S.A. 111, 1670616711 (2014).
27. S. D. Copley, Trends Biochem. Sci. 25, 261265 (2000).
ACKNO WLED GME NTS
This is a contribution to the Malaspina 2010 Expedition project,
funded by the CONSOLIDER-Ingenio 2010 program of the from
the Spanish Ministry of Economy and Competitiveness (Ref.
CSD2008-00077). J.M.A. was supported by a Ramón y Cajal
research fellowship from the Spanish Ministry of Economy and
Competitiveness. E.M. was supported by a fellowship from the Junta
para la Ampliación de Estudios program of CSIC. G.J.H. and R.L.H.
were supported by the Austrian Science Fund (FWF) projects I486-
B09 and P23234-B11 and by the European Research Council (ERC)
under the European Communitys Seventh Framework Programme
(FP7/2007-2013)/ERC grant agreement 268595 (MEDEA project).
We thank A. Dorsett for assistance with DOC analyses, participants in
the Malaspina Expedition and the crews of the BIO Hespérides, and
RV Pelagia and the personnel of the Marine Technology Unit of CSIC
for their invaluable support. Original data sets are available online at
http://digital.csic.es/handle/10261/111563. J.M.A. designed the
experimental setup, carried out part of the experiments, measured
prokaryotic abundance, analyzed the data, and wrote the manuscript.
E.M. carried out part of the experiments and data analysis. C.M.D.
designed the Malaspina 2010 Expedition, was responsible for DOC
analyses, and together with G.J.H. contributed to the design of the
experiments and discussion of results. R.L.H. and T.D. analyzed the
FT-ICR-MS samples. All authors discussed the results and contributed
to the manuscript.
SUPPLEMENTARY MATERIALS
www.sciencemag.org/content/348/6232/331/suppl/DC1
Materials and Methods
Figs. S1 to S9
Tables S1 and S2
References (2835)
18 July 2014; accepted 4 March 2015
Published online 19 March 2015;
10.1126/science.1258955
SOCIAL EVOLUTION
Oxytocin-gaze positive loop and the
coevolution of human-dog bonds
Miho Nagasawa,
1,2
Shouhei Mitsui,
1
Shiori En,
1
Nobuyo Ohtani,
1
Mitsuaki Ohta,
1
Yasuo Sakuma,
3
Tatsushi Onaka,
2
Kazutaka Mogi,
1
Takefumi Kikusui
1
*
Human-like modes of communication, including mutual gaze, in dogs may have been
acquired during domestication with humans. We show that gazing behavior from dogs,
but not wolves, increased urinary oxytocin concentrations in owners, which consequently
facilitated ownersaffiliation and increased oxytocin concentration in dogs. Further, nasally
administered oxytocin increased gazing behavior in dogs, which in turn increased urinary
oxytocin concentrations in owners. These findings support the existence of an interspecies
oxytocin-mediated positive loop facilitated and modulated by gazing, which may have
supported the coevolution of human-dog bonding by engaging common modes of
communicating social attachment.
Dogs are more skillful than wolves and
chimpanzees, the closest respective rel-
atives of dogs and humans, at using human
social communicative behaviors (1). More
specifically, dogs are able to use mutual
gaze as a communication tool in the context of
needs of affiliative help from others (2). Conver-
gent evolution between humans and dogs may
have led to the acquisition of human-like com-
munication modes in dogs, possibly as a by-
product of temperament changes, such as reduced
fear and aggression (1). This idea yields interesting
implications that dogs were domesticated by
coopting social cognitive systems in humans that
SCIENCE sciencemag.org 17 APRIL 201 5 VOL 348 ISSUE 6232 333
RESEARCH |REPORTS
Corrected 12 June 2015; see full text.
are involved in social attachment. The devel-
opment of human-unique social cognitive modes
may depend on specific temperament and social
affiliation changes and may have consequently
evolved differently from those of chimpanzees
and bonobos (3). Thus, although humans and
dogs exist on different branches of the evolu-
tionary tree, both may have independently ac-
quired tolerance of one another because of
alterations in neural systems that mediate af-
filiation (1). These alterations may be related
to paedomorphic characteristics in dogs, which
enabled them to retain a degree of social flexi-
bility and tolerance similar to that of humans
(4,5); therefore, it is plausible that a specific af-
filiative relationship developed between humans
and dogs despite interspecies differences. This
common social relationship change may have
enabled cohabitation between humans and dogs
and the eventual development of human-like
modes of social communication in dogs.
Gaze plays an important role in human com-
munication. Gaze not only facilitates the under-
standing of anothers intention but also the
establishment of affiliative relationships with
others. In humans, mutual gazeis the most
fundamental manifestation of social attachment
between a mother and infant (6), and maternal
oxytocin is positively associated with the dura-
tion of mother-to-infant gaze (7). Oxytocin plays
a primary role in regulating social bonding be-
tween mother and infants and between sexual
partners in monogamous species (8,9). More-
over, activation of the oxytocin system enhances
social reward (10) and inhibits stress-induced
activity of the hypothalamic-pituitary-adrenal
axis (11). It has therefore been suggested that
these functions may facilitate dyadic interaction,
such as an oxytocin-mediated positive loop of
attachment and maternal behaviors between
mother and infant (12,13): Maternal nurturing
activates the oxytocinergic system in the infant,
thus enhancing attachment; this attachment then
stimulates oxytocinergic activity in the mother,
which facilitates further maternal behavior (9).
Because the establishment of such an oxytocin-
mediated positive loop requires the sharing of
social cues and recognition of a particular part-
ner, the study of oxytocin-mediated bonding has
been restricted to intraspecies relationships.
The human-dog relationship is exceptional
because it is an interspecies form of attachment.
Dogs can discriminate individual humans (14,15).
Furthermore, dogs show distinctly different be-
havior toward caregivers as compared with hand-
raised wolves (14), and interaction with dogs
confers a social buffering effect to humans. Like-
wise, dogs also receive more social buffering
effects from interacting with humans than from
conspecifics (16). Tactile interaction between
humans and dogs increases peripheral oxytocin
concentrations in both humans and dogs (17,18).
Further, social interaction initiated by a dogsgaze
increases urinary oxytocin in the owner, whereas
obstruction of the dogsgazeinhibitsthisincrease
(19). These results demonstrate that the acquisi-
tion of human-like social communication improves
the quality of human-dog affiliative interactions,
leading to the establishment of a human-dog
bond that is similar to a mother-infant relation-
ship. We hypothesized that an oxytocin-mediated
positive loop, which originated in the intraspe-
cies exchange of social affiliation cues, acts on
both humans and dogs, is coevolved in humans
and dogs, and facilitates human-dog bonding.
However, it is not known whether an oxytocin-
mediated positive loop exists between humans
and dogs as has been postulated between mother
and infants, and whether this positive loop emerged
during domestication.
We tested the hypothesis that an oxytocin-
mediated positive loop exists between humans
anddogsthatismediatedbygaze.First,we
examined whether a dogs gazing behavior af-
fected urinary oxytocin concentrations in dogs
and owners during a 30-min interaction. We
also conducted the same experiment using hand-
raised wolves, in order to determine whether this
positive loop has been acquired by coevolution
with humans. Second, we determined whether
manipulating oxytocin in dogs through intra-
nasal administration would enhance their gazing
behavior toward their owners and whether this
gazing behavior affected oxytocin concentrations
in owners.
In experiment 1, urine was collected from the
dogs and owners right before and 30 min after
the interaction, and the duration of the follow-
ing behaviors was measured during the interac-
tion: dogs gaze at owner (dog-to-owner gaze),
owners talking to dog (dog-talking),and own-
ers touching of dog (dog-touching).Dog owners
were assigned to one of two groups: long gaze
or short gaze (fig. S1). Wolves were tested with
thesameprocedureandwerecomparedwith
thetwodoggroups.Dogsinthelong-gazegroup
gazed most at their owners among the three
groups. In contrast, wolves rarely showed mutual
gazing to their owners (Fig. 1A and fig. S2). After
a 30-min interaction, only owners in the long-
gaze group showed a significant increase in
urinary oxytocin concentrations and the highest
change ratio of oxytocin (Fig. 1, B and C). The
oxytocin change ratio in owners correlated sig-
nificantly with that of dogs, the duration of dog-
to-owner gaze, and dog-touching. Moreover, the
duration of the dog-to-owner gaze correlated
with dog-talking and dog-touching (table S2A);
however, through multiple linear regression anal-
ysis, we found that only the duration of dog-to-
owner gaze significantly explained the oxytocin
changeratioinowners.Thedurationofdog-
touching showed a trend toward explaining
oxytocin concentrations in owners (Table 1A).
Similarly, a significantly higher oxytocin change
ratio was observed in the dogs of the long-gaze
group than in those of the short-gaze group
(Fig. 1, D and E). The duration of dog-to-owner
gaze also significantly explained the oxytocin
change ratio in dogs, and the duration of dog-
touching showed a trend toward explaining
oxytocin concentrations in dogs by multiple lin-
ear regression analysis (Table 1A). In wolves, in
contrast, the duration of wolf-to-owner gaze did
334 17 APRIL 2015 VOL 348 ISSUE 6232 sciencemag.org SCIENCE
Duration (s)
120
140
100
80
60
40
20
0
Dog or wolf-
to-owner gaze
Dog or wolf-
touching
Dog or wolf-
talking
***
**
*
***
***
Owner’s oxytocin (pg/mg)
60
40
20
0
Pre Post
**
Dog or wolf ’s oxytocin (pg/mg)
300
200
100
0
Pre Post
*** ***
LG SG Wolf
The change ratio of dog or wolf (%)
200
150
100
50
0
**
The change ratio of owner (%)
LG SG Wolf
500
400
300
200
100
0
**
Fig. 1. Comparisons of behavior and uri-
nary oxytocin change among long gaze
dogs (LG, n= 8, black bars and circles),
short gaze dogs (SG, n= 22, white bars
and circles), and wolves (wolf, n= 11, gray bars and square).(A) Behavior during the first 5-min
interaction. (B)and(D) Changes of urinary oxytocin concentrations after a 30-min interaction.
Urinary oxytocin concentrations in owners (B) and dogs or wolves (D) collected before and after a
30-min interaction are shown. (C)and(E) Comparisons of the change ratio of urinary oxytocin
among LG, SG, and wolf for owners (C) and dogs or wolves (E). The results of (A), (B), and (D) are
expressed as mean TSE. (C) and (E) reflect median Tquartile. ***P< 0.001, **P< 0.01, *P< 0.05.
1
Department of Animal Science and Biotechnology, Azabu
University, Sagamihara, Kanagawa, Japan.
2
Department of
Physiology, Jichi Medical University, Shimotsuke, Tochigi, Japan.
3
University of Tokyo Health Sciences, Tama, Tokyo, Japan.
*Corresponding author. E-mail: kikusui@azabu-u.ac.jp
RESEARCH |REPORTS
Corrected 12 June 2015; see full text.
not correlate with the oxytocin change ratio in
either owners or wolves, and wolf-to-owner gaze
did not explain the oxytocin change ratio in
owners and wolves (tables S2B and S3). These
results suggest that wolves do not use mutual
gaze as a form of social communication with
humans, which might be expected because wolves
tend to use eye contact as a threat among con-
specifics (20) and avoid human eye contact (21).
Thus, dog-to-owner gaze as a form of social com-
munications probably evolved during domesti-
cation and triggers oxytocin release in the owner,
facilitating mutual interaction and affiliative
communication and consequently activation of
oxytocin systems in both humans and dogs in a
positive loop.
In experiment 2, we evaluated the direct evi-
dence of whether oxytocin administration en-
hanced dog gazing behavior and the subsequent
increase in urinary oxytocin concentration in
owners. This experiment involved 27 volunteers
and their dogs, and participants unfamiliar to
the dogs. A solution containing oxytocin or saline
was administered to the dog and the dog then
entered the experimental room, where the owner
and two unfamiliar people were seated (fig. S4).
Human behavior toward dogs was restricted to
prevent the influence of extraneous stimuli on dog
behavior and/or urinary oxytocin concentration.
They were forbidden to talk to each other or to
touch the dog voluntarily. Urine samples from
the owner and the dog were collected before and
after the interaction and were later compared.
The total amount of time that the dog gazed at,
touched, and was close to the owner and the
unfamiliar participants was also measured.
Oxytocin administration to dogs significantly
increased the duration that the dog gazed at the
owner in female dogs but not male dogs (Fig.
2A). Further, urinary oxytocin concentration sig-
nificantly increased in the owners of female dogs
that received oxytocin versus saline, even though
oxytocin was not administered to the owners (Fig.
2D). No significant effect of oxytocin administra-
tion was observed in the other measured dog
behaviors (Fig. 2, B and C). Furthermore, multi-
ple linear regression analysis revealed that the
duration of gazing behavior significantly ex-
plained the oxytocin change ratio in owners
(Table 1B). Thus, oxytocin administration en-
hances the gazing behavior of female dogs, which
stimulates oxytocin secretion in their owners.
Conversely, when interaction from humans was
limited, no significant difference in urinary oxy-
tocin concentrations in dogs was observed after
the interaction in either the oxytocin or the
saline conditions, and no significant oxytocin
change ratio was found in dogs (Fig. 2, F and
G). These results thus suggest that, although
oxytocin administration may enhance dog gazing
behavior and lead to an oxytocin increase in
owners, limited owner-to-dog interaction may
prevent the increased oxytocin secretion in dogs
by breaking the oxytocin-mediated positive loop.
SCIENCE sciencemag.org 17 APRIL 2015 VOL 348 ISSUE 6232 335
Owners of female dogs / oxytocin
Owners of female dogs / saline
Owners of male dogs / oxytocin
Owners of male dogs / saline
Female dog / oxytocin
Female dog / saline
Male dog / oxytocin
Male dog / saline
Owner’s oxytocin (pg/mg)
80
60
40
20
0
Pre Post
***
*** ***
*
The change ratio of owner (%)
Owners of
male dogs Owners of
female dogs
400
300
200
100
0
Male do
g
s Female do
g
s
The change ratio of dog (%)
200
150
100
50
0
Dog’s oxytocin (pg/mg)
150
100
50
0
Pre Post
Duration of Gaze (sec)
Duration of Touch (sec)
Duration of Proximity (sec)
400
200
300
100
0
OW UP OW UP OW UP OW UP OW UP OW UP
Male dogs Female dogs
** ***
**
**
150
100
50
0
Male dogs Female dogs
1500
1000
500
0
Male dogs Female dogs
Fig. 2. Comparisons of behavior and urinary oxytocin between oxytocin and saline treatment
conditions. (A) to (C) The effects of oxytocin administration on dog behaviors. Panels show the mean
duration of dogsgaze at participants (A), touching participants (B), and time spent in the proximity of
less than 1 m from each participant (C). Black and white bars indicate, respectively, oxytocin- and saline
treatment conditions. OW, owner; UP, unfamiliar person. (D) to (G) Change in urinary oxytocin con-
centrations after a 30-min interaction after oxytocin or saline administration. Urinary oxytocin con-
centrations of owners (D)anddogs(F) before and after a 30-min interaction are shown for oxytocin and
saline groups. The change ratio of urinary oxytocin in owners (E)anddogs(G) is compared between
male and female dogs. ***P< 0.001, **P<0.01,*P< 0.05. The results of (A) to (D) and (F) are
expressed as mean TSE. (E) and (G) reflect median Tquartile.
RESEARCH |REPORTS
Table 1. Results of multiple linear regression
analysis of oxytocin change ratio and behav-
ioral variables in owners and dogs.*P< 0.05,
P<0.1;R, multiple correlation coefficient;
**, P<0.01.
(A) Experiment 1
Oxytocin change ratio
Owners Dogs
Owner talking
to dog 0.107 0.264
Owner
touching dog 0.321
0.335
Dog-to-owner gaze 0.458* 0.388*
R0.619 0.575
Adjusted R
2
0.306 0.247
P0.008 0.020
(B) Experiment 2
Oxytocin change ratio
Owners Dogs
Dogs sex 0.090 0.138
Oxytocin
administration 0.202 0.234
Dog-to-owner gaze 0.458** 0.030
Dog touching owner 0.040 0.054
Proximity to owner 0.048 0.023
R0.574 0.275
Adjusted R
2
0.248 0.046
P0.005 0.686
Sex: Female = 1, male = 0; oxytocin administration:
oxytocin = 1, saline = 0.
Corrected 12 June 2015; see full text.
Interestingly, oxytocin administration only
increased mutual gaze duration in female dogs,
whereas sex differences were not observed in
experiment 1, which did not include unfamiliar
individuals. Sex differences in the effects of in-
tranasal oxytocin have been reported in humans
as well (22), and it is possible that females are
more sensitive to the affiliative effects of oxytocin
or that exogenous oxytocin may also be activat-
ing the vasopressin receptor system preferentially
in males. Oxytocin and the structurally related
vasopressin affect social bonding and aggression
in sexually dimorphic manners in monogamous
voles (8,9), and oxytocin possibly increases ag-
gression (23,24). Therefore, the results of experi-
ment 2 may indicate that male dogs were attending
to both their owners and to unfamiliar people
as a form of vigilance. The current study, despite
its small sample size, implies a complicated role
for oxytocin in social roles and contexts in dogs.
In human infants, mutual gaze represents
healthy attachment behavior (25). Human func-
tional magnetic resonance imaging studies show
that the presentation of human and canine fam-
ily membersfaces activated the anterior cin-
gulate cortex, a region strongly acted upon by
oxytocin systems (26). Urinary oxytocin varia-
tionindogownersishighlycorrelatedwiththe
frequency of behavioral exchanges initiated by
the dogsgaze (19). These results suggest that
humans may feel affection for their companion
dogs similar to that felt toward human family
members and that dog-associated visual stimuli,
such as eye-gaze contact, from their dogs activate
oxytocin systems. Thus, during dog domestica-
tion, neural systems implementing gaze communi -
cations evolved that activate the humansoxytocin
attachment system, as did gaze-mediated oxyto-
cin release, resulting in an interspecies oxytocin-
mediated positive loop to facilitate human-dog
bonding. This system is not present in the closest
living relative of the domesticated dog.
In the present study, urinary oxytocin concen-
trations in owners and dogs were affected by the
dogsgazeandthedurationofdog-touching.In
contrast, mutual gaze between hand-raised wolves
and their owners was not detected, nor was there
an increase of urinary oxytocin in either wolves or
their owners after a 30-min experimental interac-
tion (experiment 1). Moreover, the nasal adminis-
tration of oxytocin increased the total amount of
time that female dogs gazed at their owners and,
in turn, urinary oxytocin concentrations in owners
(experiment 2). We examined the association be-
tween our results and early-life experience with
humans in dogs and wolves in order to test the
possibility that our results were due to differences
in early-life experience with humans. The results
did not indicate a significant association between
the animalsearly-life experiences with humans
and the findings of the current study (see the
supplementary methods). Moreover, there were
no significant differences between dogs in the
long-gaze group and wolves in either the duration
of dog/wolf-touching and dog/wolf-talking, sug-
gesting that the shorter gaze of the wolves was
not due to an unstable relationship. These re-
sul ts support the existence of a self-perpetuating
oxytocin-mediated positive loop in human-dog
relationships that is similar to that of human
mother-infant relations. Human-dog interaction
by dogshuman-like gazing behavior brought on
social rewarding effects due to oxytocin release
in both humans and dogs and followed the
deepening of mutual relationships, which led to
interspecies bonding.
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ACKNO WLED GME NTS
This study was supported in part by the Grant-in-Aid for Scientific
Research on Innovative Areas (No. 4501) from the Japan Society for
the Promotion of Science, in Japan. We thank all human and canine
participants, Howlin' Ks Nature School, U.S. Kennel, R. Ooyama and
N. Yoshida-Tsuchihashi from Azabu University, and Drs. Kato and
Takeda from University of Tokyo Health Sciences. We are also grateful
to Cody and Charley for their significant contributions. The analyzed
data are included in the supplementary materials.
SUPPLEMENTARY MATERIALS
www.sciencemag.org/content/348/6232/333/suppl/DC1
Materials and Methods
Figs. S1 to S5
Tables S1 to S4
References (27 30)
Movies S1 to S3
Data Tables 1 and 2
9 September 2014; accepted 3 March 2015
10.1126/science.1261022
PLANT ECOLOGY
Anthropogenic environmental
changes affect ecosystem
stability via biodiversity
Yann Hautier,
1,2,3
*David Tilman,
2,4
Forest Isbell,
2
Eric W. Seabloom,
2
Elizabeth T. Borer,
2
Peter B. Reich
5,6
Human-driven environmental changes may simultaneously affect the biodiversity, productivity,
and stability of Earths ecosystems, but there is no consensus on the causal relationships
linking these variables. Data from 12 multiyear experiments that manipulate important
anthropogenic drivers, including plant diversity, nitrogen, carbon dioxide, fire, herbivory, and
water, show that each driver influences ecosystem productivity. However, the stability of
ecosystem productivity is only changed by those drivers that alter biodiversity, with a given
decrease in plant species numbers leading to a quantitatively similar decrease in ecosystem
stability regardless of which driver caused the biodiversity loss. These results suggest
that changes in biodiversity caused by drivers of environmental change may be a major factor
determining how global environmental changes affect ecosystem stability.
Human domination of Earths ecosystems,
especially conversion of about half of the
Earths ice-free terrestrial ecosystems into
cropland and pasture, is simplifying eco-
systems via the local loss of biodiversity
(1,2). Other major global anthropogenic changes
include nutrient eutrophication, fire suppression
and elevated fire frequencies, predator decima-
tion, climate warming, and drought, which likely
affect many aspects of ecosystem functioning,
especially ecosystem productivity, stability, and
biodiversity (1,37). However, to date there has
been little evidence showing whether or how these
three ecosystem responses may be mechanistically
336 17 APRIL 2015 VOL 348 ISSUE 6232 sciencemag.org SCIENCE
RESEARCH |REPORTS
Corrected 12 June 2015; see full text.
... Domestic pets can also leave their owners, especially those in close contact with pets, at increased risk of bacterial or parasitic infections [20], some of which (e.g., Helicobacter pylori) may affect the development of spontaneous abortion [21]. Additionally, an experimental study suggested that gazing behaviour from dogs increased urinary oxytocin concentrations in owners, which is typically interpreted as calming and stress-reducing [22]. Oxytocin is also involved in the initiation and promotion of uterine contractions during delivery. ...
... Despite limited evidence from human populations, animal studies have indicated a link between endotoxin exposure and adverse pregnancy outcomes [39,40]. Most importantly, pet exposure may increase oxytocin concentrations in owners and alter the gut flora, which may further cause TA [22,41]. ...
... On the one hand, cat allergens, rather than dog allergens, can induce the production of tumour necrosis factor and interleukin-6 [44], which are inflammatory cytokines associated with adverse pregnancy outcomes [45]. Another study showed that the gazing behaviour of dogs increased urinary oxytocin concentrations in owners; cats were not mentioned in this study [22]. On the other hand, both cats and dogs can increase the concentrations of indoor allergens and house dust endotoxins [38] and alter the gut flora [41,46]. ...
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Background: The aim of this study was to assess the association between pet ownership and threatened abortion (TA) in pregnant Chinese women. Materials and methods: We enrolled pregnant women from 18 provinces and autonomous regions across China between November 2017 and December 2020. Participants were grouped based on the presence or absence of pet ownership. Pet owners were further sub-grouped based on the presence or absence of close contact with their pets. Pet species included cats, dogs, and both. Generalised linear mixed models, with province as a random effect, were used to estimate the associations between pet ownership and TA. Results: Pet ownership, whether or not one had close contact with pets, was associated with greater odds of TA (OR: 1.30, 95% CI: 1.21, 1.40). Keeping pet cats (OR: 1.24, 95% CI: 1.11, 1.40), dogs (OR: 1.29, 95% CI: 1.18, 1.41), or both cats and dogs (OR: 1.36, 95% CI: 1.04, 1.68) during pregnancy were all risk factors for TA. We observed significant group differences (p for difference < 0.05) in pre-pregnancy body mass index, education levels, and annual household income. Conclusions: Cat or dog ownership during pregnancy was associated with an increased risk of TA, especially among overweight, less educated, or lower-income participants.
... We chose to work with dogs as an initial study species for this inter-species helping investigation for two main reasons. First, dogs have a unique coevolutionary history with humans as they are by far the earliest known domesticated species (appearing genetically distinct from wolves as early as 23,000 years ago; Nagasawa et al., 2015;Perri et al., 2021). Second, dogs have evolved to read human social cues (Hare and Tomasello, 1999) and naturally seek out human help when they encounter problems: Dogs' help-seeking behaviors such as reaching and 'begging' for items they cannot access (Marshall-Pescini et al., 2017) resemble the actions of human experimenters in a classic experimental helping paradigm (Warneken and Tomasello, 2006). ...
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Two capacities considered foundational in human cooperation are prosocial motivation and goal-reading abilities that enable helping. Children exhibit both proclivities by age 2 in interactions with other humans, but interactions with nonhuman species on whom we have been interdependent for millennia are unstudied. We tested the hypothesis that children’s goal-reading and prosocial propensities extend to other animals. We predicted children would help pet dogs access objects that dogs attempted to reach but could not reach themselves. We studied 97 children between 2 and 3 years of age living in a small mid-western US city, 44 of whom had dogs as household pets. In a quasi-naturalistic setting, we introduced children to 1 of 3 friendly pet dogs who remained within a small, porous enclosure while a treat or toy was placed outside it. Dogs reacted naturally, either showing interest in accessing the item (e.g., pawing, begging) or ignoring it. Measures of dog and child behavior during sessions were coded blindly with high reliability. Children provided dogs with out-of-reach items twice as often when dogs showed interest rather than ignored items, indicating sensitivity to the dog’s goals. Additionally, children were more generally likely to provide dogs with items if children lived with pet dogs, if dogs were more lively and engaged rather than subdued and if the item was a treat rather than a toy. These findings lend support to our hypothesis that children’s early-developing proclivities for goal-reading and prosociality extend beyond humans to other animals.
... During this shared evolutionary history, dogs may have been selected, probably unintentionally, for handling the complexities of heterospecific social relationships, with evidence supporting the hypothesis that they have developed different mechanisms to facilitate interaction with people (e.g. Nagasawa et al., 2015). The interspecific relationship between dogs and humans seems to be unique within the animal kingdom, with no other domestic animal having shared more of their evolutionary history in close contact with humans (Pendleton et al., 2018), and its benefits are of great social, health and economic relevance (e.g. ...
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Emotions are critical for humans, not only feeling and expressing them, but also reading the emotional expressions of others. For a long time, this ability was thought to be exclusive to people; however, there is now evidence that other animals also rely on emotion perception to guide their behaviour and to adjust their actions in such way as to guarantee success in their social groups. This is the case for domestic dogs, who have tremendously complex abilities to perceive the emotional expressions not only of their conspecifics but also of human beings. In this paper we discuss dogs' capacities to read human emotions. More than perception, though, are dogs able to use this emotional information in a functional way? Does reading emotional expressions allow them to live functional social lives? Dogs can respond functionally to emotional expressions and can use the emotional information they obtain from others during problem-solving, that is, acquiring information from faces and body postures allows them to make decisions. Here, we tackle questions related to the abilities of responding to and using emotional information from human expressions in a functional way and discuss how far dogs can go when reading our emotions. Social media summary: dogs recognise and infer emotional information from humans and use this information to regulate their own behaviour.
... During this shared evolutionary history, dogs may have been selected, probably unintentionally, for handling the complexities of heterospecific social relationships, with evidence supporting the hypothesis that they have developed different mechanisms to facilitate interaction with people (e.g. Nagasawa et al., 2015). The interspecific relationship between dogs and humans seems to be unique within the animal kingdom, with no other domestic animal having shared more of their evolutionary history in close contact with humans (Pendleton et al., 2018), and its benefits are of great social, health and economic relevance (e.g. ...
Article
Full-text available
Emotions are critical for humans, not only feeling and expressing them, but also reading the emotional expressions of others. For a long time, this ability was thought to be exclusive to people; however, there is now evidence that other animals also rely on emotion perception to guide their behaviour and to adjust their actions in such way as to guarantee success in their social groups. This is the case for domestic dogs, who have tremendously complex abilities to perceive the emotional expressions not only of their conspecifics but also of human beings. In this paper we discuss dogs’ capacities to read human emotions. More than perception, though, are dogs able to use this emotional information in a functional way? Does reading emotional expressions allow them to live functional social lives? Dogs can respond functionally to emotional expressions and can use the emotional information they obtain from others during problem-solving, that is, acquiring information from faces and body postures allows them to make decisions. Here, we tackle questions related to the abilities of responding to and using emotional information from human expressions in a functional way and discuss how far dogs can go when reading our emotions.
... In this case, these individuals may not be completely immersed in an innovationseeking-implementation process, but they may be focused on what is occurring to them (the interaction with their pet). In addition, these effects may be explained by the strength of human-animal bonds (Barker and Barker, 1988;Nagasawa et al., 2015), which makes the individual become immersed in the pet and the interaction itself. Thus, this may explain why these individuals are the ones that see the relationship between HAIs and work engagement (directly and indirectly) become stronger. ...
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Purpose Human–animal interactions (HAIs) have been found to have an extensive and significant influence on individuals' well-being and health-related outcomes. However, there are few studies that examine this influence on work-related contexts, such as teleworking. In this study, the author relied on the affective events theory to examine the effect of daily HAI on employees’ daily work engagement and the underlying mechanisms (daily affect ratio and state mindfulness), by resorting to a daily diary study. Design/methodology/approach To test the hypotheses, the author collected daily data during five consecutive working days with pet owners ( N = 400 × 5 = 2,000). Findings Multilevel results showed that interacting with pets during the working day was positively associated with daily work engagement, but this positive relationship was stronger for individuals with lower levels of mindfulness. Further analyses showed that the daily affect ratio mediated the moderating effect of mindfulness on the relationship between daily interactions with pets and daily work engagement. Practical implications These findings provide strong support for the proposed mediated moderation model; indeed, positive affect and mindfulness help to explain the positive effect of HAIs on work engagement. Hence, managers may consider the adoption of teleworking, even in a hybrid format for those workers who own pets, because interacting with pets may be a strategy to make them feel more positive and, in turn, more enthusiastic, dedicated and absorbed in their work. Originality/value This study is one of the first studies to demonstrate the importance of adopting pet-friendly practices, such as allowing pet owners to telework, as a way to promote daily work engagement.
... For example, the amygdala and insula, substrates of affective processing in humans, have been implicated in neural responses to salient human social stimuli in domestic dogs [55]. Like humans, dogs demonstrate increased social responsiveness to humans when exposed to oxytocin, a neuropeptide hormone that enhances affiliative behavior in vertebrates [56]. Increased DNA methylation of the oxytocin receptor gene has been associated with ASD [57] and lower neural responsiveness to social stimuli in humans [29], as well as reduced approach towards unfamiliar humans in dogs [58]. ...
Article
Full-text available
Background A central challenge in preclinical research investigating the biology of autism spectrum disorder (ASD) is the translation of ASD-related social phenotypes across humans and animal models. Social orienting, an observable, evolutionarily conserved behavior, represents a promising cross-species ASD phenotype given that disrupted social orienting is an early-emerging ASD feature with evidence for predicting familial recurrence. Here, we adapt a competing-stimulus social orienting task from domesticated dogs to naturalistic play behavior in human toddlers and test whether this approach indexes decreased social orienting in ASD. Methods Play behavior was coded from the Autism Diagnostic Observation Schedule (ADOS) in two samples of toddlers, each with and without ASD. Sample 1 ( n = 16) consisted of community-ascertained research participants, while Sample 2 involved a prospective study of infants at a high or low familial liability for ASD ( n = 67). Coding quantified the child’s looks towards the experimenter and caregiver, a social stimulus, while playing with high-interest toys, a non-social stimulus. A competing-stimulus measure of “Social Attention During Object Engagement” (SADOE) was calculated by dividing the number of social looks by total time spent playing with toys. SADOE was compared based on ASD diagnosis and differing familial liability for ASD. Results In both samples, toddlers with ASD exhibited significantly lower SADOE compared to toddlers without ASD, with large effect sizes (Hedges’ g ≥ 0.92) driven by a lower frequency of child-initiated spontaneous looks. Among toddlers at high familial likelihood of ASD, toddlers with ASD showed lower SADOE than toddlers without ASD, while SADOE did not differ based on presence or absence of familial ASD risk alone. SADOE correlated negatively with ADOS social affect calibrated severity scores and positively with the Communication and Symbolic Behavior Scales social subscale. In a binary logistic regression model, SADOE alone correctly classified 74.1% of cases, which rose to 85.2% when combined with cognitive development. Conclusions This work suggests that a brief behavioral measure pitting a high-interest nonsocial stimulus against the innate draw of social partners can serve as a feasible cross-species measure of social orienting, with implications for genetically informative behavioral phenotyping of social deficits in ASD and other neurodevelopmental disorders.
... Julius et al. (2013) argue that relationships with pets can qualify as an attachment when they meet the following four criteria (Ainsworth, 1991): (1) they act as a secure base for exploration, (2) they are a haven of safety in times of stress, (3) they are associated with maintenance of proximity and (4) separation is associated with separation distress. Julius et al. suggest that attachment to pets operates through the same physiological pathways as human attachment relationships, including reduction in cortisol during interactions (Polheber and Matchock, 2014) and increase in oxytocin during mutual gazing (Nagasawa et al., 2015). Although this is a promising start, the focus in Julius et al.'s study is on adulthood and there is no discussion of the specific features of attachment to pets in childhood. ...
Article
Full-text available
Relatively little is known about how attachment influences children’s relationships to pets or mediates positive and negative interaction outcomes. We carried out in-depth interviews with 27 children, including nine children at high-risk for animal harm and 18 matched controls. We used the Child Attachment Play Assessment (CAPA), a drawing task and self-report measures including the Short Attachment to Pets Scale (SAPS) and Children’s Animal Harm Behaviours (CAHB). We also designed a novel measure, the ‘Pets In Children’s Attachment Stories’ (PICAS), to probe children’s mentalising about pets, caregiving-behaviours, comfort from pet and parental help. Children at high risk of animal harm were more likely to be classified as insecure (p = 0.002). Drawings indicated secure children tended to feel closer to mothers (p = 0.014) and siblings (p = 0.007), while pets’ proximity did not vary according to attachment strategy. Although insecure children scored lower on mentalising (p = 0.013), caregiving behaviour (p = 0.028) and parental help (p = 0.002), both groups similarly used pets as sources of comfort. There were no differences between attachment patterns on SAPS but there were differences for CAHB scores (p = 0.048). Thus, although insecure attachment was an important risk factor for harming animals, secure and insecure children had similar capacity for bonding with their pets. These results have implications both for how we treat cases of childhood animal harm and for how we understand the supportive role pets can play in children’s lives.
... It has indeed been suggested that dogs' general ability to engage in activity synchrony involving movement, such as following humans when they move from camp to camp, or during hunting sessions, has been selected through their evolution for living together with humans [11,13,26]. It is acknowledged that domestication has affected dogs' human-directed social behaviors [27,28]; we thus hypothesize that dogs' behavioural synchronization with humans is also applicable. This would be plausible with one of our previous hypotheses suggesting that behavioural synchronization has been selected early in the domestication history of the species as it is adaptive and found in all dogs [13]. ...
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Behavioural synchronization is a widespread skill in social species as it helps increase group cohesion among individuals. Such a phenomenon is involved in social interactions between conspecifics as well as between individuals from different species. Most importantly, familiarity and affiliation between interacting partners influence the degree of behavioural synchronization they would exhibit with each other. For example, in human–dog dyads, the more a dog is affiliated with its human partner, the more it behaves in a synchronous way with them. However, little is known about the ontogeny of such a behaviour, especially from an interspecific perspective. The aim of the present study was thus to investigate the existence and modalities of activity synchrony, a type of behavioural synchronization, between humans and puppies. To do so, we observed 29 dog puppies interacting with two different humans (familiar and unfamiliar experimenters). Puppy movements and general activity in relation to the human ones were observed. Results evidenced that puppies did exhibit locomotor synchrony with humans, but familiarity did not affect its degree. It is the first time that activity synchrony with human walk is evidenced in puppies, highly suggesting that dogs’ ability to behave in synchronization with humans seems to be genetically selected through the process of domestication, while the effect of familiarity on it might develop later during the individual ontogeny.
Article
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Thesis
Dans une société où les animaux compagnons sont intégrés au cercle familial, beaucoup d’humains les considèrent comme des membres de la famille à part entière. La recherche doit suivre cette tendance et s’attacher à appréhender les mécanismes de relations qui se construisent entre différentes espèces amenées à cohabiter. L’objectif de cette thèse est d’enrichir et d’approfondir les connaissances scientifiques sur l’éthologie du chat compagnon (Felis catus), afin de mieux appréhender ses besoins et réponses comportementales, au sein d’un environnement souvent imposé par l’humain. Les travaux restitués sont principalement centrés sur la communication interspécifique entre l’humain et le chat. Soucieux d’explorer aussi bien la perspective de l’humain que celle du chat, nous avons étudié la façon dont chacun s’exprime et décode les messages de l’autre. Ainsi, nous nous sommes intéressés à la communication vocale et visuelle entre ces deux espèces différentes qui partagent un même milieu - et doivent apprendre à communiquer efficacement pour cohabiter sereinement. Nos études ont mis en évidence que les humains utilisaient un discours spécifique pour s’adresser à leur compagnons félins, caractérisé par l’utilisation d’une voix plus aiguë. Nous avons également rapporté que les chats étaient plus attentifs à ce type de discours, mais seulement lorsqu’il était prononcé par leur compagnon humain et non par un étranger. Dans une troisième étude, nous avons observé que les chats venaient plus volontiers au contact d’un humain peu familier si celui-ci proposait un contact bimodal ou visuel, plutôt que vocal. Enfin, nous avons vu que les humains comprenaient mieux les chats dans leurs expressions bimodales et visuelles que vocales. Ainsi, bien que communément utilisée par chaque émetteur de cette communication interspécifique, la modalité vocale ne semble pas être suffisante pour la transmission et la réception d’un signal clair. Ces résultats sont discutés à la lumière des notions d’attachement, d’anthropomorphisme et de bien-être animal.
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Growth responses of several species of heterotrophic marine bacteria to limiting con- ccntrations of lactate, glycerol, and glucose in seawater were determined in a chemostat. In all casts, threshold concentrations of the limiting substrates were found below which the organisms were unable to grow. This phenomenon is explained on the basis of a positive feedback mechanism, which is abolished below a certain minimum population density. The resulting inhibitory effect on growth leaves a corresponding concentration of the limiting substrate unattacked. According to their growth parameters, two types of spccics could bc distinguished, one adapted to the marine environment by its ability to grow at low substrate concentrations and one inactive in natural seawater but surviving. The implications of these results on the rates of microbial transformations and on the occurrence and concentrations OF dissolved organic material in the sea are discussed.
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The bulk of sea water is an aqueous solution of inorganic salts and gases. However, if it was just this, life as we know it would not exist. In addition to this inorganic component, at least tens of thousands of organic molecules - collectively known as dissolved organic matter - exist in picomole amounts in each litre of sea water. Dissolved organic matter is important for aquatic food webs and, integrated over the entire volume of the world's oceans, contains roughly as much carbon as all living biota on land and in the ocean combined. Yet, the cycling of dissolved organic matter in the ocean is not well understood. Recent progress in analytical chemistry has allowed the characterization of dissolved organic matter at the molecular level in unprecedented detail, revealing that a significant proportion has been thermally altered, either in deep sediments or through combustion on land with later delivery to the sea. Thermal alteration may explain, at least in part, the resistance of oceanic dissolved organic matter to microbial decomposition.
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The present investigations were undertaken to compare interspecific communicative abilities of dogs and wolves, which were socialized to humans at comparable levels. The first study demonstrated that socialized wolves were able to locate the place of hidden food indicated by the touching and, to some extent, pointing cues provided by the familiar human experimenter, but their performance remained inferior to that of dogs. In the second study, we have found that, after undergoing training to solve a simple manipulation task, dogs that are faced with an insoluble version of the same problem look/gaze at the human, while socialized wolves do not. Based on these observations, we suggest that the key difference between dog and wolf behavior is the dogs' ability to look at the human's face. Since looking behavior has an important function in initializing and maintaining communicative interaction in human communication systems, we suppose that by positive feedback processes (both evolutionary and ontogenetically) the readiness of dogs to look at the human face has lead to complex forms of dog-human communication that cannot be achieved in wolves even after extended socialization.