Vol.

10: 21–27 ENDANGERED SPECIES RESEARCH

Published online April 27, 2009
doi: 10.3354/esr00188 Endang Species Res

Contribution to the Theme Section ‘Biologging technologies: new tools for conservation’
OPEN
ACCESS
REVIEW

Diving into the world of biologging

Yan Ropert-Coudert1,*, Michael Beaulieu1, Nicolas Hanuise1, 2, Akiko Kato1
1
Institut Pluridisciplinaire Hubert Curien, Departement Ecologie, Physiologie and Ethologie, 23 rue Becquerel,
67087 Strasbourg Cedex, France
2
Centre d’Etudes Biologiques de Chizé, Villiers-en-Bois, 79360 Beauvoir-sur-Niort, France

ABSTRACT: On the occasion of the publication of the proceedings of the Third International Biolog-
ging Science Symposium, we present a summary of the incidence of biologging in studies of animal
behaviour. Studies investigating diving activity were used as a proxy to examine the use of a biolog-
ging technology. Specifically, studies referenced in the Penguiness Book, an internet-based diving
database, were used to examine: (1) on which taxa of diving animals biologging is principally used;
(2) which countries are the principal users and producers of biologging technology; and (3) the inci-
dence of this approach in peer-reviewed publications. Each of these items is discussed in the light of
the intrinsic limitations of biologging approaches.

KEY WORDS: Retrospective study · Diving activity · Manufacturers · Publications · IUCN

Resale or republication not permitted without written consent of the publisher

INTRODUCTION Over the past 20 yr, miniaturization and technologi-

cal innovations have meant that biologging could be
Biologging is the practice of attaching data-record- applied to smaller animals exploiting any type of envi-
ing devices (e.g. biologgers, data storage tags, archival ronment (aquatic, terrestrial or aerial) and at almost all
tags, electronic data recorders) to animals. This defini- latitudes, thus allowing researchers to address an
tion excludes all tracking devices such as radio or increasingly diverse panel of questions. For instance,
satellite tracking devices, although it includes those Ropert-Coudert & Wilson (2005) identified up to 24 dif-
data-recording devices that can transmit their data at ferent types of sensors in use in biologgers (solely or in
intervals. The approach is suggested to have emerged groups). Compiling all biologging studies exhaustively
in the 1940s when a capillary depth gauge was would be a daunting task, if not an impossible one. We
attached by Pers Scholander onto a harpooned whale therefore decided to use a proxy for biologging that
to gather information about the cetacean’s maximum would be easily detectable in the literature but should
diving depth (Naito 2004). In this respect, biologging still be representative of the whole discipline. We
would thus be > 60 yr old, but the technology has chose diving activity studies as a proxy since biolog-
undergone a rapid development in the last 20 yr, ging finds its origin in the marine environment (e.g.
accompanied by an increase and diversification in the Kooyman 2004) and investigations on diving animals
user base, as indicated by the success of the 3 first sym- represent the core of biologging studies, whether or
posia dedicated to this scientific field as well as the not diving activity is the principal focus of the study
increasing number of reviews on the subject (e.g. Wil- (Rutz & Hays 2009). Conveniently, a substantial por-
son et al. 2002, Cooke et al. 2004, 2008, Block 2005, tion of such studies have already been compiled in the
Ropert-Coudert & Wilson 2005, Burger & Shaffer air-breathing divers database (the Penguiness Book,
2008). Furthermore, data from animal-attached Ropert-Coudert et al. 2006), allowing us to access a
devices are now featured widely in the media and large amount of information pertinent to the present
have even been used as tools to garner public support study. The present review is based on the 464 peer-
for the plight of endangered species. reviewed references entered in the database on 5 April

*Email: [email protected] © Inter-Research 2009 · www.int-res.com

22 Endang Species Res 10: 21–27

2008. This database intends to collect as many diving mammals, 43 reptiles). We first looked at the propor-
data on free-ranging animals as exists in the peer- tion of species that have been studied via biologging in
reviewed literature, a source of reliable information. a given taxon (Fig. 1). In terms of the total number of
The major shortcoming in basing the following review studies conducted, seabirds was by far the most inves-
on this database is that a number of references of tigated taxon. Yet the most studied taxon in terms of
biologging applied to captive species or to non air- percentage of species studied within a taxon was that
breathing species (e.g. fish) are not considered, but it of the pinnipeds, followed by seabirds, while the least
would be unrealistic to try and collect all biologging studied taxa were freshwater birds and sea snakes.
papers exhaustively. These latter taxa actually comprise a substantial num-
In the present review, we will use the Penguiness ber of species; for instance, the latest taxonomic agree-
database to examine the following: (1) what and how ment proposes 75 species of sea snakes (Ineich 2004),
often diving species have been studied through a of which only 3 studies investigated diving behaviour,
biologging approach, noting the current limits of none of them using biologgers (but see Brischoux et al.
biologging applications; (2) the geographical distribu- 2007, not compiled into the database). Within a taxon,
tion of producers and end-users of data-recording the situation was also highly contrasted. For instance,
devices; and (3) the incidence of biologging in the sci- seabird studies greatly outnumbered studies on fresh-
entific literature, through a detailed investigation of water birds. Similarly, penguins were overrepresented
the journals in which studies using this approach were (86 studies out of 197 studies on seabirds), while there
published. were almost no studies on Procellariiforms like petrels
and shearwaters. The same situation was found in the
marine mammal taxa, where most pinniped species
BIOLOGGING FOR WHICH SPECIES? were thoroughly investigated (all species of pinnipeds
have been studied with the exception of the Japanese
In the current section we will only consider studies sea lion Zalophus japonicus, considered extinct) while
from the Penguiness Book that used biologging as a biologging was rarely used to investigate cetaceans —
methodology (i.e. excluding all studies based on obser- although 4 cetacean families are overrepresented:
vations). The database recognises and contains data Monodontidae (beluga whales and narwhals), Bala-
from 536 diving species (289 birds, 136 mammals, 111 enopteridae (rorquals), Phocoenidae (porpoises), and
reptiles), of which 130 have diving data documented Physiteridae (sperm whales). Note that some taxa of
(63 birds, 53 mammals, 14 reptiles). This information is diving, air-breathing animals have not yet been listed
contained in 422 diving studies, where species may be in the database (e.g. kingfishers, freshwater snakes,
represented in more than one study (196 birds, 183 hippopotamuses, beavers), but this is mainly because

Fig. 1. Number of species considered in the Penguiness Book database (white bars) and the respective number of species for
which diving activity has been investigated using a biologging approach (grey bars) for each taxon. The proportion that this
latter number represents compared to the total number of species per taxon is written above the bars
 Ropert-Coudert et al.: A retrospective of biologging 23

of the absence of literature on the diving

abilities of these species.
Why are some species are more tar-
geted than others? We presume that good
candidates should be accessible, have a
large body size and be available in
appreciable numbers. All marine species
that breed on land and return perio-
dically ashore will be preferentially
selected for biologging studies. Con-
versely, marine species that spend the
majority of their time submerged are
underrepresented, a situation that will
change if researchers focus on designing Fig. 2. Number of species considered in the Penguiness Book database (white
new techniques for devices attachment bars) and the respective number of species for which diving activity has been
and recovery. Similarly, it is not surpris- investigated using a biologging approach (grey bars) according to conserva-
ing that the most frequently studied spe- tion status, as defined in the 2008 IUCN Red List. CR: Critically Endangered;
EN: Endangered; VU: Vulnerable; NT: Near Threatened, LC: Least Concern;
cies were large, e.g. elephant seals DD: Data Deficient
Mirounga spp., leatherback turtles Der-
mochelys coriacea or narwahls Monodon
monoceros, i.e. animals large enough to accommodate about the sex of the individuals monitored. This pro-
the early devices, which were bulkier than the pre- portion varies within each taxon, being least sex-spe-
sent ones. Yet miniaturization has meant that body cific in birds (90.7% of studies do not distinguish
size becomes less critical. Moreover, preference was between the sexes) where an appreciable number of
historically given to species that breed in large num- species are monomorphic, but appreciable in
bers at the same place, which offered an incompara- cetaceans (76.1%). Conversely, only 32.5% of studies
ble range of potential candidates to biologging inves- on the highly dimorphic pinnipeds did not specify sex
tigations (e.g. penguin colonies where several differences, while virtually 100% of sea turtle studies
thousands of individuals nest in the same bay). defined the sex of the study animals since most deploy-
Finally, species that display extreme abilities are a ments are conducted on females coming ashore to lay
good model since, for instance, the activity of a deep their eggs. In seabirds, the characteristics of targeted
diver will be more conspicuous and thus easier to individuals cannot be deduced from visual examina-
monitor, even with low accuracy devices, than that of tion upon capture (e.g. male and female penguins look
a shallow diver, though the choice of the species extremely alike), and all classes of individuals are not
should solely depend on the question being asked. similarly accessible (e.g. older individuals tend to nest
One important factor in the choice of a target species further inside a colony than younger ones, Ainley
is the conservation status of the animal model (www. 1983). Yet individual-based approaches are important
iucnredlist.org/search). Across all the different IUCN in ecology, as each individual within a population pre-
statuses the proportion of animals investigated via sents specific life-history traits that make it unique and
biologging was fairly constant at ca. 30% (Fig. 2), with will determine a specific physiological and behav-
the exception of Critically Endangered species, for ioural response (Stearns 1992). To remedy this situa-
which this percentage decreased to 16%. Thus biolog- tion, a suite of new methodologies exists: for instance,
ging provides quantitative and reliable data from modern genetic techniques using biological tissues
which relevant conservation and management proce- (e.g. blood, skin, feathers) are affordable and enable
dures can be implemented. In this context, researchers workers to sex individuals reliably (e.g. Griffiths &
are becoming more aware of deleterious effects caused Tiwari 1993, Griffiths et al. 1998). Similarly, if most
by instruments (e.g. McMahon et al. 2008) and have publications with age information only provide an indi-
proposed guidelines to minimize these effects as much cation on the age class (e.g. juveniles, young-of-the-
as possible (for reviews see Hawkins 2004, Wilson & year, or adults) and nothing about the precise age of
McMahon 2006). It is important to note that in this sec- the animal studied, work could be concentrated on
tion we used the 2008 IUCN status which may not known-age animals (e.g. previously marked using
reflect the status of the species when the relevant rings and/or transponders). The next generation of
biologging study was conducted. studies should clearly aim at applying biologging
When all taxa are considered together, 66.4 ± 30.2% approaches onto known individuals so as to demon-
of the studies analysed did not give any information strate the full potential of this discipline.
24 Endang Species Res 10: 21–27

SOCIOECONOMIC CONTEXT OF BIOLOGGING (4.5%), the UK (3.9%) and Italy (2.1%). Because
biologging research is driven by the desire to answer
At the end of the 20th century, the increased need to specific questions rather than simple use of the tech-
monitor animals in the wild has led to the emergence nology and due to the extreme specificity of biolog-
of the biologgers market. New types of applications gers, most producers may have originally been work-
have emerged thanks to a quick development of the ing in close association with, or even be part of,
technology involved. Who took advantage of this new research institutions to develop custom-made tools.
development as a manufacturer or as a user of biolog- The use of these tools would naturally spread through
gers? Note again that only companies that produced collaborations, increasing the range of potential cus-
devices used in studies in the Penguiness database will tomers, to the point when production of biologgers
be considered in the present review (see ‘Intro- would become viable for a company.
duction’). Although we estimated that, to the best of The spectrum of nationalities was wider for users
our knowledge, all companies producing biologgers (n = 24) than for manufacturers (n = 6) of biologgers.
appeared in the analysis, an undefined number of However, the use of biologgers was confined to rich
biologging producers and users will not be mentioned, countries: 36.56% of authors worked in a North Amer-
including, for example, those who study fish behaviour ican laboratory, 35.24% in a European laboratory,
where the usage of such technology is substantial. 15.86% in Oceania or in South Africa, 9.91% in Japan
Articles in the Penguiness Book were first sorted by and 3.08% in South America.
the type of tools used to monitor animals. They were Within rich countries, the US dominated the produc-
then sorted by the nationality of the logger manufac- tion of biologgers and the number of biologging publi-
turer and the nationality of the laboratory of the first cations. In contrast, the number of publications in
author (Fig. 3). A total of 88% of studies used biolog- Europe was comparable but the production of loggers
gers (sensu stricto, including 12% as capillary depth was anecdotal. The large number of publications rela-
gauges) to monitor diving animals. The remaining tive to the level of biotechnology production in Europe
12% of studies reported the use of radio transmitters likely reflects a reliance of European users on technol-
(8.1%) and acoustic material (3.9%). Among the 76% ogy produced in other countries. However, it may also
of studies using solid state devices (i.e. excluding cap- reflect researchers in Europe producing a higher num-
illary depth gauges that are usually custom built), ber of publications per dataset (cf. King 2004). It would
American, European and Asian companies shared the be worthwhile developing further biologging technol-
market of loggers with 56.1% of loggers produced by ogy in Europe in order to diversify trade supply and to
Northern American companies and 13.3 and 11.2% by propose an alternative to purpose-built loggers, which
Japanese and European companies, respectively. In represent a non-negligible part (16.1%) of the devices
fact, the majority of biologgers used in the studies used by research groups. The reliance on home-made
analysed were manufactured in 6 countries: the US biologgers is exacerbated by the fact that biologgers
(51.5%), Japan (13.3%), Germany (5.2%), Canada are a small market, rendering commercial biologgers
expensive or, another consequence of a reduced
demand, produced with limited capacities (e.g. trans-
ducers) that do not always meet the specific needs of
the researchers.
In summary, only rich countries seem able to afford
the luxury of developing and using biologging tech-
nology. For other countries, collaborations are the
principal means by which they can gain access to
biologgers, but this is problematic. Promoting interna-
tional collaboration between biologging users is,
therefore, a necessity for the forthcoming decades. At
a grand scale, we hope that funding agencies from
rich countries sponsoring international projects better
value those projects that propose to develop biolog-
ging tools and to share these tools with less fortunate
countries. This is especially relevant since endan-
gered species, for which information is sometimes
urgently required, are commonly found in those coun-
Fig. 3. Proportion of biologger manufacturers (white bars) tries that do not possess the financial means to pur-
and users (grey bars) chase biologgers.
 Ropert-Coudert et al.: A retrospective of biologging 25

BIOLOGGING IN THE ‘PUBLISH OR PERISH’ studies, could have been published more easily in
WORLD high-profile journals, while this has become much
more difficult nowadays, especially since an increasing
Kooyman’s (2004) review of the origin and develop- number of journals only accept hypothesis-driven
ment of biologging noted that the number of biolog- studies for publication.
ging studies published in peer-reviewed journals was It is interesting to note that diving studies that use
almost non-existent, apart from a few isolated articles visual observations of diving animals (i.e. non-biolog-
during the 1960s and 1970s, most of these produced by ging) have remained relatively constant throughout
Kooyman or members of his team. The number of the years, even though increasing miniaturization of
biologging studies began to rise from the mid-1980s, biologgers should allow researchers to target a greater
increasing drastically until a peak in the year 2000. variety of species, even those of increasingly small
This trend is similar to that reported by Shaffer & Costa sizes. This is presumably because observations still
(2006), who based their study on a regional database of play an important part in understanding the diving
marine mammal diving studies that stopped in 2000. ecology of animals, they are inexpensive, and are a
The decline in the number of publications following logistically feasible option for very small species.
2000 was mirrored by an increase in the impact factors More than 60% of the references compiled in the
of the journals in which such studies were published Penguiness Book were published in only 10 journals
(Fig. 4). In Fig. 4, we used the impact factor of each (out of a total of 68 journals indexed in the database),
journal from the year of publication of the study. We with the Canadian Journal of Zoology, a generalist bio-
could not trace impact factors of journals prior to 1991, logical journal, comprising 13.5% of the total (Fig. 5).
but the small number of publications before this date There was also an interesting dichotomy in the main
would not have yielded representative figures (espe- type of the journals that published biologging works:
cially if one considers that the impact factor of 1965 more than half of the studies were either published in
would be determined by only one publication: Kooy- generalist journals (e.g. Journal of Experimental Biol-
man 1966). Nonetheless, it would be unwise to con- ogy, Journal of Zoology) or in what we defined as
clude that quality has recently replaced quantity in taxon-specific journals (e.g. Ibis or Marine Mammal
biologging studies, not least because journal impact Science). Marine and polar journals were the next
factors tend to increase over time (Fig. 4). Moreover, it most widespread repositories of biologging studies.
is plausible that the first biologging studies, although This was not unexpected, since biologging was ini-
they might have been more descriptive than some later tially developed to help understand animals exploiting

Fig. 4. Annual number of articles using biologging approaches (bars) or simple visual observations (black dots) to investigate div-
ing activity, and mean (± SE) weighed annual impact factor of the journals in which biologging studies were published (line). Note
that impact factors (IF) of journals (at least those of the 10 most represented journals) increase significantly over time (x) following
IF = 0.06x –116.9 (R2 = 0.96, F1,13 = 291.7, p < 0.001)
26 Endang Species Res 10: 21–27

16 General

14 Species-specific

Marine
12
Number of articles

Polar
10

Ecology
8

Behaviour
6
Conservation
4
Physiology
2

0
J Exp Mar Biol Ecol
Can J Zool
Mar Ecol Prog Ser
Polar Biol
J Exp Biol
Mar Mam Sci
J Zool Lond
Mar Biol

Mar Ornith
Waterbirds
Anim Behav
J Anim Ecol
Brit Birds

Rep Int Whaling Com

Wilson Bull

Physiol Biochem Zool

Proc R Soc Lond Ser B
Antarc Sci
Aquatic Mam

Ecology
Emu
Fish Bull
Notornis
Arctic
Ecol Monogr
J Ethol
J Field Ornith
Ostrich
Austr J Zool
CR Acad Sci
Func Ecol
Herpetologica
J Acoust Soc Amer
Comp Biochem Physiol A
J Mar Biol Assoc
Auk
Condor
Ibis

Fig. 5. Distribution of the biologging articles by journals (bars) and by journal category (pie chart). See text for definition of
taxon-specific journals

inaccessible milieu like marine and polar environ- the application of biologging to studies of vulnerable
ments (one of the very first species to be monitored species is non-negligible and we could expect a
using biologging was the Weddell seal Leptonychotes greater representation of this approach in conservation
weddellii, Kooyman 1966). journals. Indeed, data obtained in the wild from
In contrast, journals that cover a specific scientific biologging approaches are extremely valuable to con-
discipline were underrepresented, although there are servationists as they provide real estimates of the situ-
biases in the way these journals are covered in the ation in the environment, information that can be com-
Penguiness Book. Hence, the number of biologging pared to the outcomes of theoretical models.
studies in physiological journals was artificially under- Hopefully, such an approach will become more widely
estimated due to the fact that the Penguiness Book used in the forthcoming years.
only compiles studies that have been conducted in the
wild (see ‘Introduction’). This process retains only the
ecophysiological studies in which diving activity is CONCLUSIONS
measured in a natural setting, including those few
studies that use semi-captive conditions (like the iso- There are a number of limitations to the use of our
lated dive hole in Antarctica, see Ponganis et al. 2003) index to determine the extent of biologging in today’s
and eliminates an appreciable number of laboratory- scientific community. For instance, the Penguiness
based investigation in which biologging tools other Book does not represent an exhaustive compilation of
than depth recorders may have played a crucial role. all diving studies published in peer-reviewed journals,
However, this poor representation was surprising in although it does account for a substantial number of
the case of journals with a conservation-oriented aim, them. In addition, approximately 8% of studies that
since biologging data can provide substantial informa- used biologging for diving studies but did not provide
tion that could help understand and better protect vul- data in a format that could be compiled in the Pengui-
nerable aquatic or semi-aquatic species (see Cooke ness Book (e.g. no explicit values of diving depth or
2008 for review). As mentioned in the ‘Introduction’, duration, or experiments conducted in captivity) were
 Ropert-Coudert et al.: A retrospective of biologging 27

not taken into account. However, these studies were ➤ Cooke SJ (2008) Biotelemetry and biologging in endangered
generally concerned with various species already cov- species research and animal conservation: relevance to
regional, national, and IUCN Red List threat assessments.
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Editorial responsibility: Rory Wilson, Submitted: December 4, 2008; Accepted: February 16, 2009
Swansea, UK Proofs received from author(s): April 17, 2009