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

April 2015
Science 348(6232):333-6

DOI:10.1126/science.1261022

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PubMed

Authors:

Shohei Mitsui

Nobuyo Ohtani

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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.

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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-labile”and “semi-refractory”fractions

(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 rate—because

that would lower their isotopic age—but 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

1. D. A. Hansell, Annu. Rev. Mar. Sci. 5, 421–445 (2013).

2. E. B. Kujawinski, Annu. Rev. Mar. Sci. 3, 567–599 (2011).

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7, 451–459 (2009).

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(2013).

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Oceanography (Wash. D.C.) 22, 202–211 (2009).

12. A. Konopka, Curr. Opin. Microbiol. 3, 244–247 (2000).

13. G. Kattner, M. Simon, B. Koch, in Microbial Carbon Pump in the

Ocean, N. Jiao, F. Azam, S Sanders, Eds. (Science/AAAS,

Washington, DC, 2011), pp. 60–61.

14. T. Dittmar, J. Paeng, Nat. Geosci. 2,175–179 (2009).

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405–408 (1994).

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(2009).

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19. N. Jiao et al., Nat. Rev. Microbiol. 8, 593–599 (2010).

20. R. P. Maharjan, S. Seeto, T. Ferenci, J. Bacteriol. 189,

2350–2358 (2007).

21. R. Stone, Science 328, 1476–1477 (2010).

22. R. Flerus et al., Biogeosciences 9, 1935–1955 (2012).

23. O. J. Lechtenfeld et al., Geochim. Cosmochim. Acta 126,

321–337 (2014).

24. P. M. Williams, E. R. M. Druffel, Nature 330,246–248

(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. 405–453.

26. C. L. Follett, D. J. Repeta, D. H. Rothman, L. Xu, C. Santinelli,

Proc. Natl. Acad. Sci. U.S.A. 111, 16706–16711 (2014).

27. S. D. Copley, Trends Biochem. Sci. 25, 261–265 (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 Community’s 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 (28–35)

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,

Shiori En,

Nobuyo Ohtani,

Mitsuaki Ohta,

Yasuo Sakuma,

Tatsushi Onaka,

Kazutaka Mogi,

Takefumi Kikusui

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.

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 another’s intention but also the

establishment of affiliative relationships with

others. In humans, “mutual gaze”is 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 dog’sgaze

increases urinary oxytocin in the owner, whereas

obstruction of the dog’sgazeinhibitsthisincrease

(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 dog’s 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: “dog’s gaze at owner (dog-to-owner gaze),”

“owner’s talking to dog (dog-talking),”and “own-

er’s 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

Dog or wolf-

to-owner gaze

Dog or wolf-

touching

Dog or wolf-

talking

***

Owner’s oxytocin (pg/mg)

Pre Post

Dog or wolf ’s oxytocin (pg/mg)

300

200

100

Pre Post

*** ***

LG SG Wolf

The change ratio of dog or wolf (%)

200

150

100

The change ratio of owner (%)

LG SG Wolf

500

400

300

200

100

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.

Department of Animal Science and Biotechnology, Azabu

University, Sagamihara, Kanagawa, Japan.

Department of

Physiology, Jichi Medical University, Shimotsuke, Tochigi, Japan.

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)

Pre Post

***

*** ***

The change ratio of owner (%)

Owners of

male dogs Owners of

female dogs

400

300

200

100

Male do

s Female do

The change ratio of dog (%)

200

150

100

Dog’s oxytocin (pg/mg)

150

100

Pre Post

Duration of Gaze (sec)

Duration of Touch (sec)

Duration of Proximity (sec)

400

200

300

100

OW UP OW UP OW UP OW UP OW UP OW UP

Male dogs Female dogs

** ***

150

100

Male dogs Female dogs

1500

1000

500

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 dogs’gaze 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

0.306 0.247

P0.008 0.020

(B) Experiment 2

Oxytocin change ratio

Owners Dogs

Dog’s 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

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 members’faces 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 dogs’gaze (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 humans’oxytocin

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

dog’sgazeandthedurationofdog-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 animals’early-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 dogs’human-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,

Eric W. Seabloom,

Elizabeth T. Borer,

Peter B. Reich

5,6

Human-driven environmental changes may simultaneously affect the biodiversity, productivity,

and stability of Earth’s 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 Earth’s ecosystems,

especially conversion of about half of the

Earth’s 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 (1,3–7). 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.

Association between Pet Ownership and Threatened Abortion in Pregnant Women: The China Birth Cohort Study

Article

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Dec 2022
Int J Environ Res Publ Health

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.

Do children help dogs spontaneously?

Article

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Jan 2023

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.

R E V I E W Dogs functionally respond to and use emotional information from human expressions

Article

Full-text available

Jan 2023

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.

Dogs functionally respond to and use emotional information from human expressions

Article

Full-text available

Dec 2022

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.

Should I pet or should I work? Human-animal interactions and (tele)work engagement: an exploration of the underlying within-level mechanisms

Article

Full-text available

Dec 2022
PERS REV

Ana Junça

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.

Social attention during object engagement: toward a cross-species measure of preferential social orienting

Article

Full-text available

Dec 2022
J NEURODEV DISORD

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.

The role of attachment in children’s relationships with pets: From pet care to animal harm

Article

Full-text available

Dec 2022

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.

One- and Two-Month-Old Dog Puppies Exhibit Behavioural Synchronization with Humans Independently of Familiarity

Article

Full-text available

Nov 2022

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.

Pediatric Dog Bites to the Face May Have Been Less Severe During COVID-19 Pandemic: A Retrospective Cohort Study

Article

Jan 2023

Purpose: Pediatric dog bite injuries are one of the most common nonfatal injuries. During COVID-19 pandemic, children stayed at home more than in the past. The effect of pandemic on severity of dog bites to the face in children has not been examined. The objective of this study was to determine the frequency and severity of dog bite injuries to the face in children during the first year of the COVID-19 pandemic when compared to the previous year. Materials and methods: A retrospective cohort study was conducted for children with dog bite injuries to the head and neck region who presented to the Emergency Department at Children's Healthcare of Atlanta from March 2019 to March 2021. The predictor variable was the time of injury, and this was divided into pre-lockdown [control group (March 15, 2019, to March 15, 2020), ie pre-L] and lockdown (March 15, 2019, to March 15, 2020), ie post-L. The outcome variable was severity of dog bite defined as one or more of the following: 1) patient required sedation or general anesthesia for repair, 2) 3 or more regions in the head and neck were involved, and/or 3) surgical consultation took place. The investigators used a two-sample t-test, multivariable linear regression models, and modified ANOVA/MANOVA tests to analyze the data (P-value < .05 determined significance). Results: 712 children (370 males) with an average age of 6 years old (range, 7 months-18 years) fit the inclusion criteria. There was a total of 381 cases in the pre-L and 331 in the post-L period. There were more cases on average per month pre-L (31.8 cases/month) than post-L (27.6 cases/month) (P-value = .26). There were 183 pre-L surgical consults compared to 75 post-L (48 vs 22.8% of cases, respectively; P-value ≤ .001). There were 52 pre-L cases that had 3 or more sites in the head and neck compared to 28 during the post-L period (P-value = .032). Conclusions: During the COVID-19 pandemic, there may have been a decrease in the severity of the dog bite injuries. This trend may demonstrate a consequence that is not a direct result of the virus.

La relation humain - chat : étude des mécanismes d'une communication interspécifique

Thesis

Jun 2022

Charlotte de Mouzon

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.

The biology of mammalian parenting and its effect on offspring social development

Article

Full-text available

Aug 2014

Parents know the transformative nature of having and caring for a child. Among many mammals, giving birth leads from an aversion to infant stimuli to irresistible attraction. Here, we review the biological mechanisms governing this shift in parental motivation in mammals. Estrogen and progesterone prepare the uterus for embryo implantation and placental development. Prolactin stimulates milk production, whereas oxytocin initiates labor and triggers milk ejection during nursing. These same molecules, interacting with dopamine, also activate specific neural pathways to motivate parents to nurture, bond with, and protect their offspring. Parenting in turn shapes the neural development of the infant social brain. Recent work suggests that many of the principles governing parental behavior and its effect on infant development are conserved from rodent to humans.

Wolves do not join the dance: Sophisticated aggression control by adjusting to human social signals in dogs

Article

Full-text available

May 2013
APPL ANIM BEHAV SCI

Social reward requires coordinated activity of accumbens oxytocin and 5HT

Article

Full-text available

Sep 2013
NATURE

Social behaviours in species as diverse as honey bees and humans promote group survival but often come at some cost to the individual. Although reinforcement of adaptive social interactions is ostensibly required for the evolutionary persistence of these behaviours, the neural mechanisms by which social reward is encoded by the brain are largely unknown. Here we demonstrate that in mice oxytocin acts as a social reinforcement signal within the nucleus accumbens core, where it elicits a presynaptically expressed long-term depression of excitatory synaptic transmission in medium spiny neurons. Although the nucleus accumbens receives oxytocin-receptor-containing inputs from several brain regions, genetic deletion of these receptors specifically from dorsal raphe nucleus, which provides serotonergic (5-hydroxytryptamine; 5-HT) innervation to the nucleus accumbens, abolishes the reinforcing properties of social interaction. Furthermore, oxytocin-induced synaptic plasticity requires activation of nucleus accumbens 5-HT1B receptors, the blockade of which prevents social reward. These results demonstrate that the rewarding properties of social interaction in mice require the coordinated activity of oxytocin and 5-HT in the nucleus accumbens, a mechanistic insight with implications for understanding the pathogenesis of social dysfunction in neuropsychiatric disorders such as autism.

Oxytocin promotes social bonding in dogs

Article

Jun 2014

Significance Although the positive impact of social bonds on individual’s fitness has recently been demonstrated, the mechanisms underlying the motivation to form long-term associations remain largely unknown. Current evidence shows that oxytocin modulates social behavior but evidence of its effects in bond maintenance remains scant, especially in nonreproductive contexts. We provide evidence that in the domestic dog oxytocin enhances social motivation to approach and affiliate with conspecifics and human partners, which constitutes the basis for the formation of any stable social bond. Furthermore, endogenous oxytocin levels increased after dogs engaged in affiliation with their dog partners, indicating a stimulation of the oxytocin system during social interactions. Our findings highlight the important role that oxytocin has in the expression of sociality in mammals.

Maternal Oxytocin Response Predicts Mother-to-Infant Gaze

Article

Oct 2013

The neuropeptide oxytocin is importantly implicated in the emergence and maintenance of maternal behavior that forms the basis of the mother-infant bond. However, no research has yet examined the specific association between maternal oxytocin and maternal gaze, a key modality through which the mother makes social contact and engages with her infant. Furthermore, prior oxytocin studies have assessed maternal engagement primarily during episodes free of infant distress, while maternal engagement during infant distress is considered to be uniquely relevant to the formation of secure mother-infant attachment. Two patterns of maternal gaze, maternal gaze toward and gaze shifts away from the infant, were micro-coded while 50 mothers interacted with their 7-month-old infants during a modified still-face procedure. Maternal oxytocin response was defined as a change in the mother's plasma oxytocin level following interaction with her infant as compared to baseline. The mother's oxytocin response was positively associated with the duration of time her gaze was directed toward her infant, while negatively associated with the frequency with which her gaze shifted away from her infant. Importantly, mothers who showed low/average oxytocin response demonstrated a significant decrease in their gaze toward their infants during periods of infant distress, while such change was not observed in mothers with high oxytocin response. The findings underscore the involvement of oxytocin in regulating the mother's responsive engagement with her infant, particularly in times when the infant's need for access to the mother is greatest.

Sex differences in the neural and behavioral response to intranasal oxytocin and vasopressin during human social interaction

Article

Sep 2013

Growth of Marine Bacteria at Limiting Concentrations of Organic Carbon in Seawater

Article

Apr 1967
LIMNOL OCEANOGR

Holger W. Jannasch

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.

A heat-induced molecular signature in marine dissolved organic matter

Article

Feb 2009

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.

Security of Attachment and the Social Development of Cognition

Article

Jan 1997

E. Meins

A Simple Reason for a Big Difference: Wolves Do not Look Back at Humans, but Dogs Do

Article

Apr 2003
CURR BIOL

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.