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Collective decision‐making in aquatic mammals

August 2023
Mammal Review 53(4)

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Dalhousie University

Collective decision-making is an essential part of day-to-day life for group-living animals. These decisions can be unshared (e.g. leadership) or shared (e.g. consensus). Aquatic mammals face particular challenges when making collective decisions, including a three-dimensional habitat that can make group coordination and collective navigation a challenge. We systematically reviewed literature on decision-making in non-human mammals by examining the types of collective decisions observed and hypotheses used to structure analyses. Most of the current literature was centred around terrestrial species, particularly within primates and artiodactyls. There are no collective decision-making studies on aquatic mammal species outside of cetaceans. Both unshared and shared decision-making have been reported in whales and dolphins, with leadership found in killer whales Orcinus orca and bottlenose dolphins Tursiops sp. and consensus decisions in sperm whales Physeter macrocephalus. Five recommendations for decision-making research include: 1) clearly delineating the temporal components of decision-making, 2) standardising research to allow for comparisons, 3) considering both shared and unshared decision-making, 4) analysing decision-making across behavioural contexts, and 5) avoiding anthropomorphic terminology. Future studies of collective decision-making will help us better understand how non-human mammals overcome environmental and contextual challenges – particularly in the case of aquatic species such as cetaceans, which face challenges related to their aquatic environment and exhibit phenomena such as mass strandings.

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Mammal Review ISSN 0305-1838

REVIEW

Collective decision- making in aquatic mammals

Elizabeth ZWAMBORN*Dalhousie University, 1355 Oxford St., Halifax, Nova Scotia, Canada

B3H4J1. Email: elizabeth.zwamborn@gmail.com

Naomi BOONHakai Institute, PO Box 25039, Campbell River, British Columbia, Canada V9W 0B7.

Email: naomi.boon@hakai.org

Hal WHITEHEADDalhousie University, 1355 Oxford St., Halifax, Nova Scotia, Canada B3H 4J1.

Email: hwhitehe@dal.ca

This is an open access article under the terms of the Creative Commons Attribution License, which permits use,

distribution and reproduction in any medium, provided the original work is properly cited.

ABSTRACT

1. Collective decision- making is an essential part of day- to- day life for group-

living animals. These decisions can be unshared (e.g. leadership) or shared

(e.g. consensus).

2. Aquatic mammals face particular challenges when making collective decisions,

including a three- dimensional habitat that can make group coordination and

collective navigation a challenge.

3. We systematically reviewed literature on decision- making in non- human mam-

mals by examining the types of collective decisions observed and hypotheses

used to structure analyses.

4. Most of the current literature was centred around terrestrial species, particu-

larly within primates and artiodactyls. There are no collective decision- making

studies on aquatic mammal species outside of cetaceans. Both unshared and

shared decision- making have been reported in whales and dolphins, with

leadership found in killer whales Orcinus orca and bottlenose dolphins Tursiops

sp. and consensus decisions in sperm whales Physeter macrocephalus.

5. Five recommendations for decision- making research include: 1) clearly de-

lineating the temporal components of decision- making, 2) standardising re-

search to allow for comparisons, 3) considering both shared and unshared

decision- making, 4) analysing decision- making across behavioural contexts,

and 5) avoiding anthropomorphic terminology.

6. Future studies of collective decision- making will help us better understand

how non- human mammals overcome environmental and contextual challenges

– particularly in the case of aquatic species such as cetaceans, which face

challenges related to their aquatic environment and exhibit phenomena such

as mass strandings.

Keywords

aquatic mammals, cetacean, collective

decision- making, decision- making, global,

leadership, mammals

*Correspondence

Received: 24 October 2022

Accepted: 3 May 2023

Editor: DR

doi: 10.1111/mam.12321

INTRODUCTION

Animals that spend time in groups must align individual

and collective decisions about where to forage, when to

travel, and how to escape predators. It can be argued

that collective decision- making itself is inherent to the

deﬁnition of what a group is (Wilson 2000): ‘any set of

organisms, belonging to the same species, that remain

together for a period of time while interacting with one

another to a greater degree than with other conspeciﬁcs’.

In contrast, an aggregation may be deﬁned as individuals

attracted to the same area at the same time for non- social

reasons such as abundant food or adequate shelter (Plötz

et al. 1991, Heyman et al. 2001).

Within the current literature on collective decision-

making, decisions are often classiﬁed as either unshared

or shared according to the framework set out by Conradt

and Roper (2005). When decisions are unshared there

can be either a single leader (fully unshared) or a few

leaders (partially shared), which may or may not be con-

sistent over time (Conradt & Roper 2005). A leadership

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E. Zwamborn, N. Boon and H. WhiteheadCollective decision- making in aquatic mammals

event can be deﬁned in terms of time (e.g. the ﬁrst

individual(s) to initiate a behavioural change; Krueger

et al. 2014) or space (e.g. the individual(s) physically po-

sitioned in front of a group leading movement; Lewis

et al. 2011). There are many examples of unshared deci-

sions in wild animal populations, such as the leadership

of southern resident killer whale Orcinus orca matriarchs

during times of food scarcity (Brent et al. 2015), distrib-

uted leadership in group recruitment of pavement ants

Tetramorium caespitum (Collignon et al. 2014), and un-

shared leadership seen during chacma baboon Papio ursinus

morning departures from their sleeping sites (Stueckle &

Zinner 2008).

Conversely, collective decisions can be made in a shared

manner with a majority decision made by group members

or by reaching a required threshold – such as a quorum

in human societies (Conradt & Roper 2005). Some examples

include meerkat Suricata suricatta quorum- like decisions of

when to return to their sleeping sites (Gall et al. 2017), as

well as the sneezing of African wild dogs Lycaon pictus as

a voting- like mechanism for decisions on movement (Walker

et al. 2017). Sometimes a consensus cannot be reached,

resulting in inaction or even group ﬁssion. Societies with

ﬁssion- fusion dynamics may avoid conﬂict, as has been

hypothesised in American bison Bison bison (Merkle

et al. 2015), if individuals can leave a group when they

do not agree with the decisions made by others. Fission

decisions have been classiﬁed as ‘combined’ decisions because

animals make their choices individually, such as whether

to stay or leave a given group, in comparison to ‘consensus’

decisions, which are generally undertaken by spatially co-

hesive groups that must make decisions about cooperative

actions such as travel (Conradt & Roper 2005).

Decision- making processes found in mammals are complex

and diverse. Many mammalian species are at least partially

group living, with examples ranging from extremely stable

matrilines to solitary individuals that congregate occasionally

under particular conditions to forage (Bigg et al. 1990, Nowacek

et al. 2011). Mammals are often individually identiﬁable and

make particularly interesting subjects for research on collec-

tive decision- making due to an abundance of dedicated long-

term studies where the temporal consistency of leadership

can be studied (Krueger et al. 2014, Brent et al. 2015). There

have been several reviews of mammalian decision- making

(see Appendix S1). Published literature has assessed focused

subjects, such as leadership in mammalian societies (Smith

et al. 2016, 2020) and collective movement decisions in non-

human primates (Fischer & Zinner 2011, King & Sueur 2011),

but none have looked at collective decision- making across

mammals more broadly.

Collective decisions in aquatic environments can lead to

additional challenges for both the mammals reaching these

decisions and the researchers studying them. Visibility is

often low or non- existent and the environment is frequently

used in a much more three- dimensional way (e.g. deep

diving) in comparison to terrestrial species (Norris &

Schilt 1988, Hindell et al. 2002). One taxon of aquatic

mammals, cetaceans, includes species that live in groups

and frequently make collective deep dives. During these

coordinated dives, they are subject to extreme pressures

and go to places where they cannot simply return from

in a quick manner without serious consequences (e.g. de-

compression sickness; Fernández et al. 2017). Certain cetacean

species are known for common mass strandings (Moore

et al. 2018). In species such as killer whales and sperm

whales Physeter macrocephalus, the groups are highly mobile,

tight- knit and long- term (Bigg et al. 1990, Christal

et al. 1998). How does the different use of space in an

aquatic environment change how they make collective deci-

sions? How are we to understand the best response or

intervention during mass strandings, when we do not un-

derstand how the species involved make such collective

decisions? Part of the difﬁculty of examining decision- making

in aquatic mammals, including cetaceans, is the challenge

of collecting continuous observations for species that spend

the majority of their time underwater. Recent advances in

technology, such as drones (Hartman et al. 2020), have

allowed scientists to acquire the data needed to investigate

questions about decision- making further.

In this review, we consider what is known of collective

decision- making for terrestrial non- human mammalian

species and compare this to what has been learned about

collective decision- making in cetacean species (the only

group of aquatic mammals for which collective decision-

making has been studied). Our goal is to suggest new

research directions in this developing ﬁeld for both aquatic

and terrestrial mammals. Our recommendations will allow

for more focused and comparable studies in future, at

both population and species levels.

We ask the following questions:

1. Which collective decision- making processes are used by

mammals?

2. What hypotheses have been tested in studies of collective

decision- making in mammals?

3. How can our knowledge of the collective decision- making

processes in mammals be used to direct and advance

our understanding of collective decision- making processes

in aquatic mammal species?

METHODS

We used a systematic database search to gather literature

on available collective decision- making in non- human

mammalian species and then ran a second search targeting

decision- making literature in cetacean species. The databases

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Collective decision- making in aquatic mammalsE. Zwamborn, N. Boon and H. Whitehead

Web of Science, Biological Abstracts, ProQuest and Scopus

were searched. Identical terms were used for each database

during the respective searches (see Appendix S2). Only

peer- reviewed articles, books, and theses published up until

March 2020 were kept. All citations were uploaded to a

systematic review manager (Covidence Systematic Review

Software 2021) for analysis. Duplicate literature was re-

moved. Two qualiﬁed reviewers screened abstracts (see

Fig. 1 for ﬂowchart) and excluded any studies that were

not linked to collective decision- making. There was a 94%

proportionate agreement between the two reviewers in the

selection of studies. A consensus was reached for the re-

maining literature via consultation and discussion between

both reviewers. Both reviewers then evaluated the full text

of each article. We excluded studies unrelated to collective

decision- making, such as research on individual decisions

made in a non- group context. We also excluded any theses

for which the relevant chapters had been published. Studies

on both wild and captive animals were considered. However,

as this review focuses on providing suggestions for fur-

thering the ﬁeld of decision- making studies in free- ranging

populations of mammals, particularly cetaceans, experi-

mental studies were excluded. We used a quality assessment

to exclude any studies that had inadequate data (see

Table 1).

We then extracted for each study: (1) the decision-

making hypotheses used, (2) the type of decision- making

found (e.g. unshared, partially shared, shared, mixed, etc.),

and (3) the evolutionary explanations proposed by the

authors. Box 1 provides deﬁnitions for the types of deci-

sions used in this review, based on Conradt and

Roper (2005) with additional clariﬁcations.

RESULTS AND DISCUSSION

Six of the 29 extant mammal orders are represented by

collective decision- making studies. Cetacean decision-

making was better represented than decision- making in

bats, elephants, and carnivorans, but research effort in

mammalian decision- making was predominantly focused

on primates and terrestrial ungulates (see Fig. 2). Many

well- researched groups of mammals (e.g. equids, bats) were

represented by only a few non- experimental studies focus-

ing on how they make their collective decisions.

Within mammalian collective decision- making studies

there was a wide range of species from diverse habitats

and geographical locations. There were several examples

of a species, for example chacma baboons, being studied

on multiple occasions (see Table 2) – sometimes with

different decision- making tactics for different contexts or

Fig. 1. Flowchart for systematic review of collective decision- making studies in mammal species.

E. Zwamborn, N. Boon and H. WhiteheadCollective decision- making in aquatic mammals

populations (Sellers et al. 2007, Stueckle & Zinner 2008),

which is perhaps unsurprising given our knowledge of

the complexity of many animal societies. However, these

discrepant ﬁndings emphasise our limited understanding

of decision- making for species that have only been studied

in one speciﬁc context or for a single population.

The largest representative category of mammalian decision-

making is unshared (single leader) decisions, including ex-

amples from ﬁve of the six orders included in this review

(Penzhorn 1984, Peterson et al. 2002, Barelli et al. 2008, Ihl

& Bowyer 2011, Mizuno et al. 2017). Many of these studies

looked speciﬁcally for physical leadership and individuals who

initiated group movement. The second most prevalent cat-

egory was mixed decision- making, where a combination of

unshared, partially shared, and/or shared decisions were made

to reach a goal such as group movement initiation (Seltmann

et al. 2016, Gall et al. 2017). There were few examples of

species using an entirely shared decision- making process

(Bousquet et al. 2011, Whitehead 2016), and even fewer

examples of partially shared decisions (as deﬁned in Box 1)

(Mech 2000, Lee & Teichroeb 2016). Both shared and par-

tially shared decision types were common components within

the mixed decision category.

Studies of several well- known cetacean populations made

up the entirety of the literature available on collective decision-

making in aquatic mammals. This research covers ﬁve species:

democratic consensus movement decisions in sperm whales

(Whitehead 2016), spatial leadership observed in common

bottlenose dolphins Tursiops truncatus and Indo- Paciﬁc bot-

tlenose dolphins Tursiops aduncus (Lusseau 2007, Lusseau &

Conradt 2009, Lewis et al. 2011, 2013a, b) and killer whales

(Foster 2012, Brent et al. 2015), and leadership potential in

Irrawaddy dolphins Orcaella brevirostris (Liew &

Labadin 2017). Evidence for leadership during synchronous

surfacing was not found in Indo- Paciﬁc bottlenose dolphins

(McCue et al. 2020). There have been suggestions made for

leadership in other species, including long- ﬁnned pilot whales

Globicephala melas and sperm whales, particularly during

stranding events (de Kock 1956, Mazzariol et al. 2018), but

these observations are largely anecdotal, without detailed

explanation or supporting evidence.

Hypotheses of mammalian collective

decision- making

The hypotheses tested in mammalian decision- making

studies were diverse, ranging from predicted drivers of

Table 1. Quality assessment domains for mammalian decision- making systematic review

Quality domain Considerations

Methods Are methods well- described and sufcient for inclusion? This ensures that only repeatable studies are included in this review.

Sample size Is the study based on an adequate sample size to draw the conclusions made? Inadequate sample sizes are more likely to result

in inaccurate conclusions that are not representative.

Quantitative vs.

qualitative?

Is the study of decision- making purely observational or supported by quantitative analyses? How robust is the conclusion about

collective decision- making – is it well supported by quantitative data or just a statement made in a broader study?

Evolutionary

framework

Does the study discuss evolutionary reasons or a functional framework for the observed decision- making? Is there an

evolutionary explanation given for the conclusions of the study?

Study design Is the study experimental or non- experimental? Experimental studies do not always produce results that can be observed in

nature because of the articial environment they take place in.

Other bias Are there any other obvious biases resulting from the study design that should be considered when deciding whether or not to

include this article in this review? Are there funding, professional, environmental, or other considerations that could bias the

outcome of the study?

Box 1. Important denitions for decision-making

SHARED: Equal contribution from all group members

on a given decision (quorum – a majority, sub major-

ity or super majority – or voting) (Conradt &

Roper 2005).

UNSHARED (single leader): A single individual who

makes a given decision (Conradt & Roper 2005). For

addressing the temporal aspect of unshared decisions,

leaders could be:

1. stable – a single individual leads

2. semi- distributed – a subset of individuals who share

leadership over time

3. distributed – all members being able to lead in any

given decision, whether equally or unequally

PARTIALLY SHARED (several leaders): An intermediate

decision between shared and unshared where a subset

of individuals make the decision (Conradt & Roper 2005).

MIXED: Where any combination of shared, unshared,

and partially shared decision- making is used to achieve

an outcome.

For example, where the decision of WHEN to move might

be made separately from the decision of WHERE move-

ment, resulting in a two- part process needed for movement

to take place.

Collective decision- making in aquatic mammalsE. Zwamborn, N. Boon and H. Whitehead

leadership to different decision- making types and the

mechanisms underlying the decision- making process (see

Table 3). Over 25% of studies (n = 30) did not state clear

hypotheses in the introduction or methods sections. Reasons

for lack of stated hypotheses ranged from studies being

purely observational without speciﬁc decision- making goals,

to technical papers where speciﬁc hypotheses were not

tested.

The most common hypotheses proposed centred around

testing the drivers of leadership (57% of hypotheses, n = 90),

with dominance (n = 26), energetics (n = 21), social con-

nectedness (n = 19), and ecological knowledge (n = 16) being

the most frequently proposed explanations. These drivers

were frequently tested in a similar manner, ﬁrst by de-

termining the independent variable(s); e.g. dominance rank,

reproductive status, age, etc., for each individual, followed

by using a statistical model (e.g. Generalised Linear Mixed

Model, Analysis of Variance, etc.) to test which factors

successfully predicted observed leadership (Tecot &

Romine 2012, Fernández et al. 2013, Ceccarelli et al. 2020).

There was a wide variety of statistical methods used. The

most common hypothesis was that dominant individuals

were most likely to be leaders, particularly among primates

where high- ranking individuals often play a key social

role within their groups (Leca et al. 2003, Bonnell

et al. 2017). Examples of dominance- driven leadership can

be found in species such as sheep Ovis aries, chacma ba-

boons, wolves Canis lupus, and cattle Bos taurus (Addison

& Simmel 1980, Mech 2000, Peterson et al. 2002, Šárová

et al. 2007, Romero & Castellanos 2010).

Not all mammalian species exhibit dominance hierar-

chies, and other studies were focused on alternative ex-

planations for successful leadership. The hypothesis that

females would be more likely to lead based on higher

energetic needs when gestating or lactating was proposed

as an explanation for species ranging from plains zebra

Equus burchellii and spotted hyenas Crocuta crocuta to

primates such as vervet monkeys Chlorocebus pygerythrus

and red- fronted lemurs Eulemur ruﬁfrons (Fischhoff

et al. 2007, Smith et al. 2010, Lee & Teichroeb 2016,

Sperber et al. 2019). In species where social connectedness

was an important component of societies, it has been

suggested that more connected individuals are frequent

leaders (Strandburg- Peshkin et al. 2015). Socially central

individuals in common bottlenose dolphins, Tibetan ma-

caques Macaca thibetana and highland cattle have been

observed with more followers and better leadership success

(Lusseau 2007, Wang et al. 2016, Sueur et al. 2018).

The ecological knowledge of an individual was sometimes

proposed to be the driver behind leadership. In killer

whales, post- menopausal females were observed leading,

likely because their age and experience meant that they

held the best knowledge of where to ﬁnd salmon

(Oncorhynchus sp.) when food was scarce (Brent

et al. 2015). Similarly, female Verreaux’s sifakas Propithecus

verreaxi were hypothesised to lead more often because

Fig. 2. Representation of mammalian taxonomic orders from this decision- making review (n = 117), with the percentage of studies for each order.

Cetaceans, part of the order Artiodactyla, make up only 8% of studies overall.

E. Zwamborn, N. Boon and H. WhiteheadCollective decision- making in aquatic mammals

Table 2. Orders and species of mammals according to observed decision types (aquatic mammal species in bold, represented in the literature only by

cetaceans). References are listed in the same order as the species to which they pertain

Decision Type Order Species References

Shared Artiodactyla Moose Alces alces, sheep Ovis aries, sperm whale

Physeter macrocephalus

Geist(1963), Whitehead(2016), Pérez- Barbería and

Walker(2018)

Carnivora Meerkat Suricata suricatta Bousquet et al.(2011)

Chiroptera Leisler’s bat Nyctalus leisleri Naďo and Kaňuch(2015)

Primates Chacma baboon Papio ursinus Sellers et al.(2007)

Partially Shared

(several

leaders)

Primates Chacma baboon, vervet monkey Chrorocebus

pygerythrus

Lee and Teichroeb(2016), Bonnell et al.(2017)

Carnivora Wolf Canis lupis Mech(2000)

Unshared (single

leader)

Artiodactyla Barbary sheep Ammotragus lervia, caribou Rangifer

tarandus, cattle Bos taurus, common bottlenose

dolphin Tursiops truncatus, elk Cervus canadensis,

European bison Bison bonasus, Giraffe Giraffa

camelopardalis, goat Capra aegagrus, horse Equus

ferus, Indo- Pacic bottlenose dolphin Tursiops

aduncus, Irrawaddy dolphin Orcaella brevirostris,

killer whale Orcinus orca, muskox Ovibos

moschatus, Pyrenean chamois Rupicapra pyrenaica,

roe deer Capreolus capreolus, sheep, wild boar Sus

scrofa, zebu Bos indicus

Altmann(1952), Beilharz and Mylrea(1963), Dickson

et al.(1967), Naumov and Baskin(1969),

Tsarev(1980), Funk(1981), Bresiński(1982), Gray

and Simpson(1982), Sato(1982), Jakimchuk and

Carruthers(1983), Reinhardt(1983), Carranza and

de Reyna(1987), Mrlik(1991), Escos et al.(1993),

Gerard et al.(1993), Rowell and Rowell(1993),

Zaitsev(1999), Lusseau(2007), Šárová et al. (2007),

Lusseau and Conradt(2009), Ihl and Bowyer(2011),

Lewis et al.(2011, 2013b), Foster(2012), Berry and

Bercovitch(2014), Wolter et al.(2014), Brent

etal.(2015), Liew and Labadin(2017), Ramos

etal.(2018), Sueur et al. (2018)

Carnivora Domestic dog Canis familiaris, wolf, spotted hyena

Crocuta crocuta

Mech(2000), Peterson et al.(2002), Bonanni et al.

(2010), Smith et al.(2010)

Perissodactyla Horse, zebra Equus zebra Jezierski and Gebler(1984), Penzhorn(1984),

Krueger et al.(2014), Briard et al.(2015)

Primates Bonobo Pan paniscus, chacma baboon, chimpanzee Pan

troglodytes, Columbian white- faced capuchin

monkey Cebus capucinus, diamemed sifaka

Propithecus diadema, red lemur Eulemur rufus,

hamadryas baboon Papio hamadryas, eastern lesser

bamboo lemur Hapalemur griseus, gelada

Theropithecus gelada, Geoffroy’s spider monkey

Atelinae geoffroyi, Guatemalan black howler Alouatta

pigra, Japanese macaque Macaca fuscata, mantled

howler monkey Alouatta palliata, moustached

tamarin Saguinus mystax, northern plains grey langur

Semnopithecus entellus, Panamanian white- faced

capuchin Cebus imitator, red- bellied lemur Elemur

rubriventer, red- fronted lemur Eulemur rufrons,

Spix’s saddle- backed tamarin Leontocebus fuscicollis,

Tana River red colobus Piliocolobus rufomitratus,

Tibetan macaque Macaca thibetana, Verreaux’s sifaka

Propithecus verreauxi, vervet monkey, white- faced

capwhite- handed gibbon Hylobates lar

Struhsaker(1967), Makwana(1979),

Dunbar(1983), Nakagawa(1990), Boinski and

Campbell(1995), Erhart and Overdorff(1999),

Leca et al.(2003), Smith et al.(2003), Trillmich et

al. (2004), Barelli et al.(2008), Stueckle and

Zinner(2008), Romero and Castellanos(2010),

Jacobs et al.(2011), King et al.(2011), Pyritz

etal. (2011), Tecot and Romine(2012), Bonnell

et al. (2013), van Belle et al. (2013), Foreit(2016),

Lee and Teichroeb(2016), Wang et al.(2016),

Tokuyama and Furuichi(2017), Chambers(2019),

Palacios- Romo et al.(2019), Sperber et al.(2019),

Ceccarelli et al.(2020), Rasolonjatovo and

Irwin(2020)

Proboscidea African bush elephant Loxodonta Africana, Asian

elephant Elephas maximus

Lee and Moss(2012), Mizuno et al.(2017)

Mixed Artiodactyla Caribou, cattle, European bison, giraffe, plains bison

Bison bison, Przewalski’s gazelle Procapra przewalskii,

sheep

Innis(1958), Addison and Simmel(1980), Ramseyer

et al.(2009a, b, c), Šárová et al.(2010), You

etal. (2013), Merkle et al.(2015), Ramos et al.

(2015), Lesmerises et al.(2018)

Carnivora African wild dog Lycaon pictus, domestic dog, meerkat Bonanni et al.(2011), Gall et al.(2017), Walker

etal. (2017)

Perissodactyla Horse, plains zebra Equus quagga Fischhoff et al.(2007), Bourjade et al.(2009, 2015),

Ozogány and Vicsek(2014)

(Continues)

Collective decision- making in aquatic mammalsE. Zwamborn, N. Boon and H. Whitehead

they do not disperse from their natal habitats like males

do and, therefore, would have knowledge of where to

ﬁnd food (Trillmich et al. 2004). Kinship and personality

(e.g. bold vs. shy) were also hypothesised to be drivers

of successful leadership (Lee & Moss 2012, Briard

et al. 2015), though far less often.

The second most common type of hypotheses were those

that attempted to determine the mechanisms behind the

decision- making process (12% of hypotheses, n = 19). Almost

half of these were focused on whether signal coordination

was important in decision- making (n = 8). Testing for this

hypothesis mainly occurred in primates (Boinski 1993, Boinski

& Campbell 1995), though there were studies on both spot-

ted hyenas and meerkats that also found vocal signals re-

sponsible for group conﬂict avoidance and group movement

coordination, respectively (Smith et al. 2010, Gall et al. 2017).

Hypotheses in this category also focused on whether

decision- making was spatially driven (n = 3; e.g. whether in-

dividuals in speciﬁc positions within a group consistently

led directional changes) or temporally driven (n = 1; e.g.

whether leadership for direction changes depended upon the

ﬁrst individual to move, regardless of position within the

group); what mechanisms underlay consensus decisions (n = 3),

and even suggested that decision- making in some species

was a process involving multiple decisions (n = 4; Norton 1986,

Petit et al. 2009, Ramseyer et al. 2009a, Seltmann et al. 2013).

The third category of hypotheses tested was composed

of those testing for decision- making type (11% of hypotheses,

n = 18), speciﬁcally if there were consensus decisions being

made (broadly, n = 6), what the type of leadership was being

used (stable vs. distributed, n = 7), whether a quorum de-

termined the decision (n = 2), or whether mimetics played

a role in how groups moved (n = 3). A study on Tibetan

macaques discovered that a quorum system was used if the

initiator had a simple majority of followers, but selective

mimetics also played an important role if less than the

majority initially followed (Wang et al. 2015).

Recommendations

There is great potential for future research to expand our

understanding of leadership and shared decisions in non-

human mammals. We have ﬁve recommendations for

designing a study on collective decision- making or analysing

opportunistic data collected for other studies.

MAKE CLEAR DELINEATIONS BETWEEN TEMPORAL AND

NON- TEMPORAL ASPECTS OF DECISION- MAKING

Like many areas of behavioural research, the literature

available on mammalian collective decision- making suffers

from weak and overlapping deﬁnitions. What is leader-

ship? Does the initiator also count as a leader even if

they do not lead the subsequent movement or only func-

tion in triggering a voting process? Are those pivotal ﬁrst

Decision Type Order Species References

Primates Barbary macaque Macaca sylvanus, black and gold

howler monkey Alouatta caraya, black- and- white

ruffer lemur Varecia variegata, chacma baboon,

Columbian white- faced capuchin monkey, golden

snub- nosed monkey Rhinopithecus roxellana, olive

baboon Papio anubis, Panamanian white- faced

capuchin monkey, red- fronted lemur, rhesus macaque

Macaca mulatta, Tibetan macaque, Tonkean macaque

Macaca tonkeana, yellow baboon Papio cynocephalus

Norton(1986), Boinski(1993), Overdorff et al.

(2005), Sueur and Petit(2008, 2010), King and

Cowlishaw(2009), Petit et al.(2009), Sueur et al.

(2009, 2010a, b, 2011, 2013), Zappala and

Logan(2010), Sueur(2011), Marshall et al.

(2012), Fernández et al.(2013), Seltmann et al.

(2013, 2016), Strandburg- Peshkin et al.(2015),

Wang et al.(2015, 2020), Farine et al.(2016),

Schweitzer et al.(2017), Sperber et al.(2017)

Table 2. (Continued)

Table 3. Hypotheses used in mammalian decision- making studies

Hypothesis category Hypothesis subcategory

Number

of studies

Leadership drivers Dominance 26

Energetics*21

Ecological knowledge*16

Social connectedness*19

Kinship*3

Personality 3

Other traits 2

Decision- making type Consensus*6

Leadership – stable*5

Leadership – distributed 2

Quorum 2

Mimetic 3

Decision- making

mechanism

Signal coordination 8

As a process 4

Consensus mechanisms 3

Spatially driven*3

Temporally driven 1

*Hypotheses presented in cetacean decision- making studies.

E. Zwamborn, N. Boon and H. WhiteheadCollective decision- making in aquatic mammals

followers who are needed to meet a quorum also leaders?

In their framework, Conradt and Roper (2005) deﬁned

unshared decisions as a single dominant individual acting

as leader, which does not consider situations where lead-

ership is not linked to dominance. In aquatic mammals

such as cetaceans, dominance hierarchies are not apparent,

perhaps because a three- dimensional and ﬂuid habitat

limits opportunities for the monopolisation of resources

(Strickland et al. 2017, Rendell et al. 2019). In cetaceans,

social connectedness and ecological knowledge have been

more commonly suggested as drivers of leadership

(Lusseau 2007, Brent et al. 2015).

Conradt and Roper’s (2005) broad deﬁnition of partially

shared leadership as ‘a subset of individuals making a given

decision’ has a wide range of interpretations. Having several

leaders for a speciﬁc decision, in contrast to several leaders

rotating leadership at various times are quite different sce-

narios, although in both cases, the leadership is temporally

stable with the same individual(s) leading across the study

period. It appears that much of the confusion in terminol-

ogy could be avoided if time was considered and incor-

porated into deﬁnitions. Further conﬂating this terminology

is that distributed leadership (temporally unstable), where

all individuals in the group are observed leading, is some-

times also interpreted as ‘partially shared’. An example of

this would be if some individuals (e.g. females) lead more

often than the others, even though everyone takes a turn

at leading (Lee & Teichroeb 2016). Where then do these

complexities ﬁt into our understanding of decision- making?

We propose that a single decision made by one individual

at a speciﬁc point in time to be termed as ‘unshared’,

with a second temporally deﬁned subcategory associated

to capture these nuances (e.g. stable, semi- distributed, dis-

tributed unequally, or distributed equally). Clarifying the

temporal dimension of terminology, as well as the mecha-

nisms of decision- making and potential functions, will not

only help facilitate the comparison of studies but also give

the reader a clear understanding of the goals and scope

of the research.

STANDARDISE METHODS TO ALLOW COMPARISONS

There is a need for more standardised studies to facilitate

comparisons of populations and species. There has been

an attempt to standardise research methods in several cases,

often as the result of researchers being involved in multiple

similar studies or projects across populations or species

(e.g. Sueur & Petit 2008, 2010, Sueur 2011). Much of the

lack of standardisation may result from studies that use

opportunistic data, where understanding decision- making

is a secondary research goal. Targeted data collection may

be necessary for undertaking comparative studies and fur-

thering the ﬁeld of decision- making research.

CONSIDER BOTH SHARED AND UNSHARED DECISION- MAKING

Within mammalian decision- making research, there is also

a need to develop studies, which consider both shared

and unshared decisions. Many of the studies we reviewed

were focused solely on testing a hypothesis for one or

the other. For example, if one is testing speciﬁcally for

physical leadership, the absence of an individual leading

in front would not preclude leadership as it could be

acoustic in nature or conducted from a central position

in the group. The risk of not testing for both shared and

unshared decision- making is that the research will be

limited in what it can say about these decisions and po-

tential process complexities. Researchers have observed

different decision- making types within the same species,

indicating that decision- making may be inﬂuenced by the

context in which it is made. If there is evidence for a

physical leader when group movement begins, it can be

difﬁcult to determine whether this decision is truly un-

shared or whether the observed ‘leader’ is simply initiating

movement in a direction that has already been agreed

upon by the majority of the group through a shared

decision- making process.

That decision- making can be a mix of shared and un-

shared processes is often overlooked. Events, such as group

movement, that are initiated by an individual, who then

triggers a consensus decision on direction by the group,

have been found in several species including Panamanian

white- faced capuchins Cebus imitator, and meerkats

(Boinski 1993, Gall et al. 2017). Thus, shared and unshared

decisions are not mutually exclusive. For example, barbary

macaques Macaca sylvanus have a two- fold process where

the ﬁrst part of the decision to move is shared by group

members who display pre- departure behaviour to signal

a readiness for movement, followed by an unshared deci-

sion when an initiator starts travel (Seltmann et al. 2013).

Fig. 3 outlines a framework for exploring decision- making

as a process.

A decision- making process may be simple or complex – and

may require several hypotheses and analyses to clarify.

Important questions to consider include: is the decision

shared or unshared? If unshared, is there one leader or

several? If leadership, is this leadership temporally consistent?

Does the process start with leadership and result in a shared

decision, or vice versa? If the decision is shared, does it

result in group consensus or ﬁssion into subgroups?

CONSIDER DECISION- MAKING IN CONTEXT

Studies that incorporate decision- making for a population

or species across different contexts are crucial for broader

understanding of how collective decisions are made. This

was done in an observational study of mountain zebras

Equus zebra, where dominant mares led most herd move-

Collective decision- making in aquatic mammalsE. Zwamborn, N. Boon and H. Whitehead

ments, but stallions were observed consistently

taking over leadership when the group went to drink

(Penzhorn 1984). Many studies were focused on speciﬁc

events or choices (Berry & Bercovitch 2014, Gall et al. 2017),

resulting in important ﬁndings, yet a poor understanding

of collective decision- making beyond these behavioural

contexts. If there are older female leaders in an endangered

population who lead groups to food during scarcities

(ecological knowledge), then prohibiting the removal of

these older females and protecting known traditional for-

aging habitat would be important. However, other decisions

within this population (e.g. where they breed, who defends

against predators, etc.) may not use the same decision-

making strategies. Conservation measures based on a single

context or study might be limited in their ability to protect

the population and detrimental if the assumption is made

that the population consistently makes decisions in the

same manner.

How can shifts in behaviour, including those not as-

sociated with the initiation of group movement, tell us

more about how decisions are made? Collecting consistent

temporal (timing) and spatial (position) data, in addition

to information on individual gestures, orientation, and

even acoustic signals associated with group decisions will

be important for facilitating the study of collective decision-

making across contexts.

AVOID ANTHROPOMORPHISING DECISION- MAKING IN NON-

HUMAN MAMMALS

Studies on decision- making often use language that is an-

thropomorphic, implying assumptions about the underlying

drivers of the decisions being made. Examples of these are

words like ‘democratic’, used when referring to shared

decisions, and ‘despotic’ when discussing a leadership or

otherwise unshared decision. Do animals really count, as

is implied when using the term ‘quorum’, or are they more

sensitive to a different sort of threshold? Are the leaders

of groups truly ‘despots’? We should be careful when using

wording that implies the intentions of the decision- makers

in cases where this is still often unknown. Using terms

such as shared and unshared in place of democratic and

despotic, as well as threshold instead of quorum, are less

assumptive and more objective.

Why are continued efforts to study collective

decision- making in aquatic mammals

important?

Perhaps the greatest challenge for aquatic mammals when

it comes to collective decision- making is the environment

in which they live and how they use it. Many cetaceans

have been observed diving to great depths to forage, the

deepest of these being recorded for Cuvier’s beaked whales

Ziphius cavirostris reaching to 2992 m (Schorr et al. 2014).

Even species that are generally thought of as inhabiting

surface waters have been occasionally shown to dive deeper,

such as killer whales, where a 1087 m deep dive was re-

corded for an individual in the Southern Ocean (Towers

et al. 2019). Not only are these species diving to great

depths where low visibility in addition to high- pressure

limit communication options and constrain movement

patterns, but many of these departures and returns to the

surface are also tightly coordinated with other conspeciﬁcs

(Aguilar de Soto et al. 2020). Additionally, ocean environ-

ments are often patchy and unpredictable in resources

(Martin et al. 2002), meaning that collective travel deci-

sions are a critical part of life.

Fig. 3. Decision- making framework for a given collective decision or series of decisions, including consideration of temporal components.

E. Zwamborn, N. Boon and H. WhiteheadCollective decision- making in aquatic mammals

All but one of the studies on cetacean decision- making

found evidence of leadership in collective decisions, with

examples in both long- term stable groups and societies

with ﬁssion- fusion dynamics (Lewis et al. 2011, Brent

et al. 2015). This comes as a bit of a surprise, as mo-

nopolising resources in the ocean is difﬁcult, given its

patchy and unpredictable nature, and the added dimen-

sionality of the habitat. Because of this, both territoriality

and dominance are less commonly observed in cetaceans

(Strickland et al. 2017, Rendell et al. 2019). We would

expect unshared decision- making to be less common than

in terrestrial mammals, as leadership is frequently ob-

served in species with strong dominance hierarchies

(Peterson et al. 2002, Sueur et al. 2013). There are several

possible reasons for the unexpected frequency of leader-

ship in cetaceans. Firstly, in female- centred societies, such

as those found in killer whales, the group may value

the ecological knowledge of certain individuals and fol-

low their lead at times when this information is needed

(Brent et al. 2015). Secondly, several of these studies

looked at small inshore dolphin populations (Lusseau &

Conradt 2009, Lewis et al. 2011), where competition and

potential temporal monopolisation of restricted resources

within a small area may be more common. Thirdly,

shared decisions might be more difﬁcult to detect in

cetaceans, particularly when studies are designed to look

for physical leadership among animals that spend much

of their time underwater.

It is important to consider how space use in three-

dimensional aquatic environments with extreme pressure

gradients and generally low or non- existent visibility impacts

how collective decisions are made. An obvious problem

would be the difﬁculty of maintaining communication

between conspeciﬁcs over large distances and depths (Tyack

& Clark 2000). Groups of sperm whales can spread out

over several kilometres to hunt independently, yet they

must make collective decisions on how to move direction-

ally (Whitehead 2016) and then ﬁnd each other when

they return to the surface. Life in aquatic environments

is compounded by an additional challenge. Light travels

poorly and chemical signals do not function well, meaning

that communication is often limited to acoustic signals

(Tyack & Clark 2000). The use of sound is likely to be

a much more integral element of collective decision- making

in cetaceans than for most terrestrial species (perhaps with

the exceptions of bats and humans). While we know that

cetaceans have developed advanced acoustic abilities to

communicate (as well as forage and navigate in toothed

whales), the importance and function of these signals in

collective decision- making remains largely unknown (Tyack

& Clark 2000). It can be argued that the collection of

acoustic data is just as important or even more critical

than the collection of movement data for studying how

cetaceans make collective decisions, given that this is their

primary means of communication.

Studies of decision- making also have the potential to

contribute valuable insight into cetacean sociality. For

example, ﬁnding a relationship between social connected-

ness in Indo- Paciﬁc bottlenose dolphins, and discovering

who leads within different social contexts (Lusseau 2007),

allows us to address questions about the evolution and

function of their social structure. Decision- making studies

can also help us understand the psychology of individuals.

Research in horses and elephants found that personality

can predict who leads (Lee & Moss 2012, Briard et al. 2015).

While no studies in cetaceans have been focused on how

personality and leadership are connected, a recent study

in wild common bottlenose dolphins that looked at traits

(e.g. shyness, boldness) in individuals showed that this

would be an attainable next step (Díaz López 2020).

Fig. 4. Suggested data collection methods and data types for studying decision- making (including acoustic aspects) in aquatic mammals.

Collective decision- making in aquatic mammalsE. Zwamborn, N. Boon and H. Whitehead

A phenomenon unique to cetaceans that involves

decision- making is mass stranding. Various potential

causes for strandings have been proposed (including

military sonar exposure, navigational errors, and illness),

and in many cases, it can be hard to determine the

exact cause (Moore et al. 2018; see Appendix S3 for

further discussion on the causes of mass strandings).

Sometimes, individuals have been observed close to the

shore in the hours or days before a stranding takes

place (Best & Reeb 2010). The singularity of mass strand-

ings has resulted in much discussion and reporting from

groups dedicated to rescue and response, but there are

few peer- reviewed articles on potential causes. Literature

pertaining to pre- stranding behaviour is even more scarce

(Best & Reeb 2010). This is in part because strandings

are typically identiﬁed as an issue only after they occur.

Current technology and social media sharing means that

access to footage of strandings that are ‘in progress’,

showing behaviour as whales linger in nearshore waters

and swim towards the beach, is more readily available.

Understanding more about day- to- day and pre- stranding

cetacean collective decision- making would likely allow

us to prevent or mitigate some (particularly anthropo-

genically triggered) stranding events.

CONCLUSIONS

Studies of mammalian collective decision- making have

advanced signiﬁcantly in recent years. We have made

ﬁve recommendations to move the study of decision-

making forward: 1) make clear delineations between

temporal and non- temporal aspects of decision- making,

2) standardise methods to allow comparisons, 3) consider

both shared and unshared decision- making, 4) consider

decision- making in context, and 5) avoid anthropomor-

phising decision- making by non- human mammals. While

cetaceans are not the only group of aquatic mammals

that make collective decisions, they represent the entirety

of available literature on decision- making for these ani-

mals. A better understanding of collective decision-

making across species will help us understand how these

mammals have adapted to an environment with unique

challenges not faced by their terrestrial counterparts.

Additionally, research has the potential to provide new

insights into both the function of social structures and

the psychology of individuals (e.g. the role of personal-

ity). With new technology, data needed to answer many

of these research questions are becoming readily available

(Fig. 4). Learning from the successes and challenges in

collective decision- making studies conducted across other

mammalian species is important in advancing the ﬁeld

of aquatic mammal behaviour and maximising future

research opportunities.

ACKNO WLE DGE MENTS

We thank Laura Feyrer, Dara Orbach, and Shelley Adamo

for their helpful comments during manuscript preparation.

Open access was funded and made possible by Dalhousie

University.

FUNDING

We are grateful for the research funding provided by the

Natural Sciences and Engineering Research Council of

Canada (Canadian Graduate Scholarship – Doctoral) and

the Amy R. Samuels Cetacean Behaviour and Conservation

Award (to EZ).

DATA AVAILABILITY STATEMENT

Data from our study are freely available online at Figshare

DOI: 10.6084/m9.ﬁgshare.23661132

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SUPPORTING INFORMATION

Additional supporting information may be found in the

online version of this article at the publisher’s website.

Appendix S1. Further details on past mammalian decision-

making reviews.

Appendix S2. Mammalian collective decision- making lit-

erature search terms.

Appendix S3. Further notes and references on the causes

of mass strandings in cetaceans.

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Full-text available

Jul 2019

Cetaceans are fully aquatic predatory mammals that have successfully colonized virtually all marine habitats. Their adaptation to these habitats, so radically different from those of their terrestrial ancestors, can give us comparative insights into the evolution of female roles and kinship in mammalian societies. We provide a review of the diversity of such roles across the Cetacea, which are unified by some key and apparently invariable life-history features. Mothers are uniparous, while paternal care is completely absent as far as we currently know. Maternal input is extensive, lasting months to many years. Hence, female reproductive rates are low, every cetacean calf is a significant investment, and offspring care is central to female fitness. Here strategies diverge, especially between toothed and baleen whales, in terms of mother–calf association and related social structures, which range from ephemeral grouping patterns to stable, multi-level, societies in which social groups are strongly organized around female kinship. Some species exhibit social and/or spatial philopatry in both sexes, a rare phenomenon in vertebrates. Communal care can be vital, especially among deep-diving species, and can be supported by female kinship. Female-based sociality, in its diverse forms, is therefore a prevailing feature of cetacean societies. Beyond the key role in offspring survival, it provides the substrate for significant vertical and horizontal cultural transmission, as well as the only definitive non-human examples of menopause. This article is part of the theme issue ‘The evolution of female-biased kinship in humans and other mammals’.

Should I stay or should I go? Individual movement decisions during group departures in red-fronted lemurs

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Full-text available

Mar 2019

Collective movements are essential for maintaining group cohesion. However, group members can have different optimal departure times, depending on individual, social and contextual factors whose relative importance remains poorly known. We, therefore, studied collective departures in four groups of red-fronted lemurs (Eulemur rufifrons) in Kirindy Forest, Madagascar, to investigate the influence of an individual's age, sex, their affiliative relationships and their proximity to other group members at the time of departure on their individual departure decision. We recorded behavioural and spatial data on individual departures during 167 group movements and conducted group scans (181-279 per group) to assess affiliative relationships. All factors influenced individual departures. Both affiliation and proximity determined a mimetic joining process in which dyads with stronger affiliative bonds departed in closer succession, and individuals followed the initiator and predecessors more quickly when they were in closer proximity at departure. While the influence of affiliation is common, the effect of inter-individual distance has rarely been considered in groups with heterogeneous social relationships. Although local rules influenced joining, the overall movement pattern was mainly determined by individual traits: juveniles took protected central positions, while females made up the van and males brought up the rear. Individual needs, expressed in the departure order, to an extent overruled the effect of affiliation. These results highlight the importance of considering individual, social and contextual factors collectively in the study of collective movements.

Synchrony, leadership, and association in male Indo‐pacific bottlenose dolphins (Tursiops aduncus)

Article

Mar 2020

Male Indo‐pacific bottlenose dolphins in Shark Bay, Western Australia, have converged with humans in the formation of nested male alliances and the use of synchrony in alliance behavior. Further, the strength of association among allied male dolphins varies and the stability of alliances correlates with the rate that males consort with estrus females (and is thus a possible indicator of dominance). To examine the possibility that synchrony reflects alliance association strength and dominance relationships, we analyzed videotapes from focal follows of two groups of males that reflect the range of alliance size and the strength of association between individuals in the population. We examined two variables: leadership during synchronous behaviors, based on which animal in a synchronously surfacing pair surfaced first, and the degree of synchrony, based on temporal differences in synchronous surfacing. We predicted that closer associates would exhibit a greater degree of synchrony and that one dolphin in a dyad would consistently lead. Contrary to our predictions, the degree of synchrony was inversely related to strength of association within alliances. This surprising result suggests that individuals with less secure bonds may strive more to achieve synchrony. We found no evidence of leadership during synchronous surfacing or between synchrony and other behavioral variables. Proximate mechanisms for synchronous behavior, such as entrainment and mutual motor imitation (“the mirror game” paradigm), may inhibit leadership in this context. Our results show that synchrony during surfacing is not a useful behavior to examine for dominance relationships in wild dolphins but it may be a useful tool to examine variation in alliance relationships.

Sociobiology: The New Synthesis, Twenty-Fifth Anniversary Edition

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