Environmental biology of fishes, tập 91, số 1, 2011

Environ Biol Fish (2011) 91:1–5
DOI 10.1007/s10641-011-9779-1

On our origins
David L. G. Noakes

Received: 13 January 2010 / Accepted: 22 February 2011 / Published online: 10 March 2011
# Springer Science+Business Media B.V. 2011

We marked 2009 devoted to origins. It was our way
of acknowledging the coincidence of 2009 as the
bicentennial of the birth of Charles Darwin, the
sesquicentennial of his publication of The Origin of
Species (Darwin 1859) - and the 170th anniversary of
his marriage. A remarkable number and variety of
books and articles devoted to Darwin were published
to recognize the year (e.g., Quammen 2008; Dawkins
2009; Ruse 2009; van Wyhe 2009). Springer Academic Publishers recognized it as The Year of Darwin
(Fig. 1). It is fitting to add our acknowledgement,
given the importance of evolution to Environmental
Biology of Fishes.
I invited Ian Potter to provide his article on the
origin of Environmental Biology of Fishes (Potter
2010). Ian is in the unique position to provide that
important information, as the only other remaining
active member from the original Editorial Board of
this journal (I was responsible for Notes and
Reviews). Furthermore, he and Bill Beamish were
the origin of the name of our journal! In this Editorial
I will comment more specifically on the origin of

Environmental Biology of Fishes and the development to the current state of our journal.

D. L. G. Noakes (*)
Fisheries & Wildlife Department, Oregon State University,
Room 120 Nash Hall,
Corvallis, OR 97331-3803, USA
e-mail:

Origins, evolution and development are important
to our journal, as they are to all of modern biology.
Perhaps more than some other journals, Environmental Biology of Fishes emphasizes an evolutionary
perspective. Our evolutionary emphasis shows not
only in the articles we publish but also in the interests
and activities of our Editorial Board. Of course we
rely heavily on our external reviewers for their
expertise and advice, and our panel of external
reviewers is critical for reviews of our manuscripts. I
will consider the Editorial Board and our published
articles as the basis for my comments on the origin
and development of Environmental Biology of Fishes.
I have taken the information from the public forum, in
the tables of contents, the lists of Advisory Editors,
the Acknowledgements for Reviewing published in
every volume, and of course most importantly the
articles we publish. In addition, I have drawn upon
the complete editorial files we maintain to provide
critical details on the current status of the journal.
As Ian Potter described in his article (Potter 2010),
our journal originated about 35 years ago, during a
time of rapid growth for science and academia, at

least in North America and Western Europe. Many
changes have taken place over the ensuing quarter
century, including recent economic upheavals, dramatic changes in technology and marked shifts in our
perspectives on the natural world. Certainly the
economic, social and other aspects of the historical
context are important, but they are not the subjects of


2

Fig. 1 The year of Darwin poster, Springer Academic Publishers

my consideration in this editorial. I am concerned
with our science in our research articles and the
affiliations of the authors and reviewers of those
articles as indicators of the nature of our journal. We
have stated from Volume 1, Issue 1 that Environmental Biology of Fishes is an international journal that
publishes original studies on ecology, life history,
epigenetics, behavior, physiology, morphology, systematics and evolution. I will review how we have
accomplished that over our first quarter century.
For my comparison I chose two issues of Environmental Biology of Fishes: Volume 1, Number 1 (30
August 1976), the first issue, and Volume 85, Number
1 (May 2009) from a recent complete volume of the
journal. Volume 1, Number 1 had 14 articles (111
pages) and was the only issue in that year (Volume 1,
Number 2 was published 15 March 1977). Volume
85, Number 1 had 15 articles (88 pages) so it appears
that there might not be much difference in the overall
“package” of the individual issues. Of course we now
publish 12 issues each year so there is an enormous

quantitative difference in the annual output of the

Environ Biol Fish (2011) 91:1–5

journal. That comparison alone documents the very
considerable growth of an order of magnitude in our
journal in both the total content and the production
rate of our journal. So our growth has been very
considerable, but what about the content?
What have we demonstrated in our science, and
how has that developed over time? I will focus my
comparison on these two individual issues of the
journal to judge the content and coverage, recognizing that the first issue represents the production for an
entire year and the recent issue is the production for a
single month. A number of important differences
emerge from this comparison, and they tell us a great
deal about the development of our journal.
I begin with a consideration of the Editorial Board.
The original Editorial Board consisted of 12 individuals, including the Editor-in-Chief and 11 Advisory
Editors (The list of Advisory Editors on the front
cover of the first issue does not agree with the list on
page 2, but the number of Advisory Editors was
stated as 11 in the Preface). Those individuals were
affiliated with academic or other scientific institutions in six countries: Australia, Canada, the USA,
England, Israel and Germany. All but one of the
original Editorial Board were males, the single
exception (and an exceptional individual she
remains) was Eugenie Clark. The Editorial Board
in 2009 consisted of 21 members, including the
Editor-in-Chief and 20 Advisory Editors, 17 male

and four female. The 2009 Advisory Editors were
affiliated with academic or other scientific institutions in eight countries: the USA, Canada, France,
Argentina, Mexico, Japan, Australia and China. The
number of members, the composition, and the international representation of the Editorial Board have all
changed significantly since the founding of the journal
in what must be interpreted as progressive ways.
Volume 1, Number 1 consisted of a Preface, an
Invited Editorial, two Main research articles, three
Notes, three Essays, three Book Reviews and Translation Proposals by authors from Canada, Poland and
the USA. The two Main articles dealt with a study
estimating the fish production of a freshwater lake
in Canada, and the physiology of skipjack tuna
(Katsuwonus pelamis). The three shorter notes dealt
with teleost embryology, fish production, and technical
aspects of rearing fish larvae.
Volume 85, Number 1 included an Editorial, and
14 articles that dealt with threatened fishes of the


Environ Biol Fish (2011) 91:1–5

world, telemetry and behavior, field studies of spawning
behavior, seasonal reproductive physiology, retinal
structure and function, behavior, salinity tolerance,
exotic and invasive species, impacts of habitat change
on fish condition, and conservation of deep-sea fishes.
Authors of the articles were from Canada, the USA,
China, Uganda, Spain, Croatia, Costa Rica, Japan,
Venezuela, New Zealand, Bolivia, and Germany.
The articles published in Volume 1, Number 1

were reviewed by 11 reviewers, 10 from Canada and
1 from Australia. For my comparison to the recent
status of our journal I have chosen the period from 1
May to 31 August 2009 as representative and
comparable to Volume 1, Number 1 (although again
this comparison is 1 year for the first issue and only
4 months for the recent issue). During that period in
2009 we received 126 manuscripts from authors with
affiliations in 13 countries (we had multiple authors
from China for several manuscripts in the special
issue on Chinese fishes), and we solicited reviews
from external reviewers in 31 countries (Table 1). I
repeat my earlier gratitude to this multitude of
external reviewers who contribute so much to the
journal. As we saw with the published articles and the
Editorial Board, the coverage of our journal has
clearly continued to grow not only in volume but
also in scientific breadth and international coverage.
As I have noted in previous Editorials, a number of
independent metrics, including impact factor, also
demonstrate this significant growth in the coverage
and content of our journal.
Environmental Biology of Fishes continues its growth
and development as a truly international journal. The
special issue dedicated to Chinese Fishes (Volume 86,
Number 1) is a recent example of our increasing coverage
and impact. I have given details of the continued
increases in the number and breadth of manuscripts
handled, and the impact factor for the journal in previous
Editorials (Noakes 2003, 2008). Development of the

journal will continue, with special issues forthcoming on otoliths, threatened fishes and fish conservation, elasmobranch feeding behavior, and salmon
biology, in addition to the latest research in
contributed manuscripts. I will continue this series
of Editorials to document those developments.
I conclude this Editorial with some more personal
comments on growth, development and the year
2009. I presented the invited keynote address at the
International Charr Symposium in Sterling, Scotland

3
Table 1 Summary of authors and reviewers of manuscripts
received during the period of 1 May until 31 August 2009,
according to their current affiliation addresses (in addition to
the Advisory Editors who also review manuscripts, and whose
affiliations are provided in the text)
Author affiliation

Reviewer affiliation

Argentina

Brazil

Australia

Canada

Austria

China (multiple)

Brazil

Croatia

Canada

Germany

China (multiple)

Hong Kong

Czech Republic

Japan

Finland

Mexico

France

South Africa

Germany

Spain

Greece

Thailand

Iceland

USA

India

Venezuela

Italy
Japan
Mexico
Mongolia
Nepal
Portugal
Scotland
South Africa
Spain
Sweden
Taiwan
Turkey
United Kingdom
Uruguay
USA
Venezuela

in June 2009, where the focus was on Darwin
(“Charles and Charr: 200 Years On”). During that

address I emphasized the continuity and the connections we all have through our science to Darwin,
his ideas and his influence. It is a relatively simple
exercise to trace our individual scientific genealogies
through our undergraduate and graduate advisors, as
well as our intellectual contacts. For some of us our
scientific heritage will lead, more or less directly, to
Darwin. I hasten to add the obvious point, that


4

Environ Biol Fish (2011) 91:1–5

Fig. 2 The Fitzwilliam
Museum in Cambridge,
England with the special
Darwin exhibition for 2009
(photograph David L. G.
Noakes)

Darwin did not personally supervise any undergraduate or graduate students so our connections cannot
literally lead directly to him. Nonetheless, ideas are as
important to our scientific heritage as are the people,
perhaps more so in many cases. Those ideas will
leave trails as clear as the signatures of our supervisors on academic transcripts. Fortunately, we have
historians and philosophers who seek out and document these connections and academic tracks and trails
in science for us (Ruse 2009).
After my presentation at Stirling University, I revisited Edinburgh University—the site of my first
academic position and coincidentally the location of
Darwin’s first attempt at a university education.

Darwin withdrew from the unsatisfactory experience
of his intended medical education at Edinburgh, but
his biological education clearly benefited from his
contacts there with Professor Robert Grant, his studies
of lumpfish, Cyclopterus lumpus, and other marine
creatures, and perhaps most significantly from his
training in the preparation of study specimens by John
Edmonston, a former slave who had experience in
tropical expeditions (Berra 2009). From Edinburgh I
traveled on to Cambridge, where Darwin had completed his formal university education, and where I
toured a number of the special Darwin exhibitions
staged for the year (Fig. 2). Finally, a visit to Oxford
where I had spent a sabbatical year myself, and where
the famous confrontation took place between Samuel

Wilberforce and Thomas H. Huxley, the great
defender of Darwin after publication of The Origin
of Species. A personal scientific pilgrimage, for sure,
although I had visited all those places, and many of
the other Darwin sites, Shrewsbury, Down House,
Westminster Abbey and the Natural History Museum
many times before. That is a pilgrimage every biologist
should take.

Fig. 3 Annie Proctor Richardson, at 92 years of age, seated in
a chair now in my possession (photograph courtesy of Jean
Noakes Park)


Environ Biol Fish (2011) 91:1–5

My final point is poignant and most personal
(Fig. 3). The lady in the photo is Annie Proctor
Richardson, my paternal great-grandmother. She was
born in 1865, the year Abraham Lincoln died.
Abraham Lincoln was born 12 April 1809, the same
day and the same year as Charles Darwin, as every
biologist should know. Annie was 17 years old when
Charles Darwin died (1882). I was 17 years old the
year Annie died (1959). Of course I had known her
well—she was the matriarch of the family, a tiny little
lady dressed in black most of the time. How sad, I
now realize, that I never talked to her about anything
of substance. Of course there is absolutely no reason
to believe that she had any experience or any opinion
related to Charles Darwin. They certainly had nothing
in common in terms of social or economic status.
Charles and Emma Darwin had as many as 10
servants and staff in Down House. Annie Richardson
worked “in service” as a young girl in England, that is
she was a servant in the house of one of the wealthy
families where she lived near Kendal, England. She
lived the difficult life of a working class family with
little formal education and few opportunities for any
social or economic advancement. No doubt that
grinding poverty and those dreary prospects influenced
her decision to immigrate to Canada with her family
early in the 20th century. Her family included the
daughter (also named Annie) who would become my
grandmother and who lived to visit me as a graduate

student at the University of California at Berkeley and
later read my postcards from Edinburgh and Oxford.
This pilgrimage was thus also intensely personal.

5
Acknowledgements Suzanne Mekking, Lynn Bouvier and
Martine van Bezooijen provided advice, encouragement, data
summaries and constructive comments for this manuscript. Bill
Beamish, Hiroya Kawanabe and Michael Ruse provided the
critical comments and insightful suggestions I needed from
trusted colleagues. Jeff Noakes commented on the historical
aspects of the manuscript and Pat Noakes corrected my
recollections. Jean Noakes Park provided the photo of Annie
Proctor Richardson and reviewed the manuscript for consistency. I
thank Springer Academic Publishers for their continued support
for Environmental Biology of Fishes, and particularly for their
recognition of The Year of Darwin. The Oregon Department of
Fish and Wildlife and the Fisheries and Wildlife Department of
Oregon State University provide my current academic home and
continuing support.

References
Berra TM (2009) Charles Darwin. The concise story of an
extraordinary man. The Johns Hopkins University Press,
New York, p 114
Darwin CR (1859) On the origin of species by natural selection.
John Murray, London, p 502
Dawkins R (2009) The greatest show on earth. The evidence
for evolution. Free Press, New York, 470 pp
Noakes DLG (2003) Changes and continuity. Environ Biol Fish

66:1–2
Noakes DLG (2008) Growth and development. Environ Biol
Fish 85:1–2
Potter IC (2010) On the origin: environmental biology of fishes.
Environ Biol Fish 87:275–276
Quammen D (2008) Charles Darwin on the origin of species.
The illustrated edition. Sterling, New York, p 544
Ruse M (2009) Philosophy after Darwin: classic and contemporary readings. Princeton University Press, Princeton, p
592
van Wyhe J (2009) Darwin in Cambridge. Christ’s College,
Cambridge, p 75


Environ Biol Fish (2011) 91:7–13
DOI 10.1007/s10641-010-9753-3

Sexual dimorphism of drumming muscles in European hake
(Merluccius merluccius)
Anne-Laure Groison & Olav S. Kjesbu &
Marc Suquet

Received: 9 December 2009 / Accepted: 11 November 2010 / Published online: 1 December 2010
# The Author(s) 2010. This article is published with open access at Springerlink.com

Abstract Dissections of mature and non-mature
European hake males and females (N=142) collected
in waters off the western coast of Norway and in the
Bay of Biscay (France) in 2004–2006 demonstrate for
the first time that this gadoid species contains
drumming muscles. There were differences in drumming muscles weight with body length, sex and

maturity stage. This study shows that the difference
between females and males is primarily manifested
during the spawning season, seen both in the French
and Norwegian samples. For the mature females the
drumming muscles dry weight increases only slightly,
if at all, with increase in total length. For mature
males there is a corresponding rapid increase. There
does not seem to be any consistent difference between
the average dry weight of the drumming muscles in
immature male and immature and mature female hake
of the same length, tested on the Norwegian samples.
A.-L. Groison (*)
Department of Biology, University of Bergen,
P.O. Box 7803, Thormøhlensgate 55,
5020 Bergen, Norway
e-mail:
A.-L. Groison : O. S. Kjesbu
Institute of Marine Research,
Nordnesgaten 50, P.O. Box 1870, Nordnes 5817 Bergen,
Norway
M. Suquet
IFREMER, PFOM / ARN,
29840 Argenton, France

Our results suggest that male hake, like the males of
other gadoids studied, may produce sounds in the
context of spawning.
Keywords Drumming muscles . Merluccius
merluccius . Sexual dimorphism . Sound production .
Spawning

Introduction
More than 800 fishes from 109 families are known to
produce sounds, though this is likely to be an
underestimate (Rountree et al. 2003). It is evident
that most of these sounds are deliberate rather than
incidental. These sounds have a role in communication, i.e., are used as exchange of information
between individual fish as part of their social
behaviour (Hawkins and Myrberg 1983). Thus, fish
produce sounds in a variety of contexts. Sounds are
produced by some species when disturbed or when
approached by a predator. Likewise, sounds are also
produced by fish which are competing with one
another for food or space (Ladich and Myrberg 2006).
In many sound-producing fish males produce sounds
during courtship of the female to advertise their nest
sites, to attract the female, and promote courtship and
spawning (Myrberg and Lugli 2006). The gas-filled
swimbladder is a characteristic feature of the viscera
of teleost fish. It contributes to the ability of a fish to
control its buoyancy, and thus to stay at the current


8

water depth without having to waste energy in depthcompensating swimming activity. Another function of
the gas bladder is the use as a resonating chamber to
produce or receive sound and in some species is
equipped with drumming muscles (DM) for sound
production. Sounds are produced by contracting DM

associated with the swimbladder and thereby vibrating
the swimbladder wall (Jones and Marshall 1953; Brawn
1961).
It is known that one particular family, the
Gadidae, includes a number of vocal species
(Hawkins and Rasmussen 1978), including haddock
(Melanogrammus aeglefinus) (Hawkins and Chapman
1966), lythe (Pollachius virens) (Hawkins and
Rasmussen 1978), tadpole fish (Raniceps raninus)
(Hawkins and Rasmussen 1978) and Atlantic cod
(Gadus morhua) (Brawn 1961).
In their work on cod Nordeide et al. (2008)
found that the DM mass was similar in both sexes a
couple of months prior to spawning but became
sexually dimorphic at the onset of spawning and
continued being sexually dimorphic (bigger in
males) for several months after the termination of
spawning.
To date, no studies have investigated whether
European hake (Merluccius merluccius) possess
drumming muscles. This is somewhat surprising in
view of the importance of this species, and the fact
that the presence of drumming muscles have been
reported in other gadoid species.
European hake is a semi-demersal, multiple batch
spawner found in waters from Mauritania to Norway.
It is believed that hake spawning and reproduction
occur at depth ranging 100–200 m (Alvarez et al.
2001; Olivar et al. 2003). The peak spawning time of
hake is in March in waters south of the Bay of Biscay

(France), and occurs progressively later at higher
latitudes (Casey and Pereiro 1995).
In the present study we sampled wild hake males
and females from French (Bay of Biscay) and
Norwegian waters at different times of the year to
search for the presence of drumming muscles and, if
so, to quantify variation among individuals in
drumming muscles size. Specifically, our objectives
were to (a) record differences in drumming muscle
appearance and mass in relation to sex, spawning
status, and body size; and (b) compare hake drumming muscles with what has been observed in other
gadoids.

Environ Biol Fish (2011) 91:7–13

Material and methods
Fish collection
A total of 142 wild European hake were sampled
offshore Western Norway (Nw) (61°34′N, 5° 56′W)
and in the Bay of Biscay, France (Fr) (47°44′N, 4°2′W)
(Table 1). Each fishing trip typically lasted 1–3 days.
Non-mature fish were captured by trawl in Nw waters
while mature fish were captured at both locations by
gillnets set overnight at depths of between 30–180 m
over sandy sea bottom. Recently dead fish (few hours)
were retrieved from the gillnets.
Fish dissection
The fish were transported to laboratory to be dissected
within 12–32 h of sampling, and all showed muscles
attached to the swimbladder on both sides. For each

individual examined we recorded total body length (N=
140; TL to the nearest 0.1 cm was measured for all fish
except for one individual with damaged tail), total (i.e.,
ungutted) body mass (N=138; TW) and gonad mass
(N=61) (to the nearest 0.1 g consulting only gonads
which were not smashed or deteriorated by stripping).
Sex and maturity stage (immature, ripening, ripe/
spawning, and spent) were recorded. Only two groups
of individuals were considered: “spawning” (sp.) for
ripening or ripe/spawning individuals (N=69) and
“non-spawning” (n. sp.) for immature or spent
individuals (N=73). The pair of DM was easily
separated from the surrounding tissue using forceps.
After excision, DM were dried at 65°C for 3 days to
obtain dry weight to the nearest 0.001 mg (N=141).
The following fish characteristics
were calculated:
h
i
condition factor (K ¼ Total weight=ðTLÞ3 Â 100,
N = 138); gonadosomatic index (GSI ¼ ½Gonad
weight=TWŠ  100 in %, N=61), and hepatosomatic
index (HSI ¼ ½Liver weight=TWŠ  100 in%, N=71).
Statistical analysis
Data were presented as means ± SD. Measured and
calculated characteristics of the dissected fish were
combined (Table 2). Statistical analyses were performed using the software SigmaStat 3.1. Statistical
significant difference between two groups were tested
at the probability level 0.05 using Student t-test (when
data were distributed normally and variances were not

Environ Biol Fish (2011) 91:7–13
Table 1 Summary of
spawning and nonspawning European hake
captured in the Bay of
Biscay (France, Fr) and in
waters western Norway
(Nw) at different dates in
2004–2005–2006

9
Spawning fish, N=

Non spawning fish, N=

Date

Origin

Females

Males

Females

Males

20 March 2006

Fr

9

10

0

0

04 April 2006

Fr

6

14

0

0

17 August 2005

Nw

7

6

0

1

22 August 2006

Nw

1

1

0

0

23 August 2004

Nw

0

0

9

6

23 August 2005

Nw

0

1

0

1

01 September 2005

Nw

6

5

1

0

12 September 2006

Nw

1

2

0

0

27 September 2004

Nw

0

0

10

13

12 October 2004

Nw

0

0

14

13

13 October 2006

Nw

0

0

2

2

30 November 2004

Nw

0

0

0

1

15Nw+15Fr

15Nw+24Fr

36Nw

37Nw

Total

significantly different) or Mann-Whitney Rank Sum
test (if one of these two previous conditions, or both,
were invalidated). As the fish dissection resulted in an
uneven number of left (N=141) and right DM (N=
120) a pilot analysis was run to test for any differences
in dry weight between them, which turned out not to
be the case (Mann-Whitney rank sum test, P>0.05).
Therefore, in the following analysis dry weight of the
left DM were used and named DM. ANCOVA with
total length as covariate was used to test for differences
in drumming muscle mass in relation to sex and
spawning status (i.e. “spawning” (sp.) for ripening or
ripe/spawning individuals and “non-spawning” (n. sp.)
for immature or spent individuals). Relationships
between DM dry weight and characteristics of sp.
and n. sp. individuals (TL, TW, K, GSI and HSI) were
investigated with Pearson correlations. Correlations

were investigated separately for Norwegian and French
fish and for males and females.

Table 2 Mean ± SD values of fish characteristics measured on
spawning and non-spawning hake for male and female (Fem.)
captured in the Bay of Biscay (France, Fr) and western Norway

waters (Nw): total length (TL), total weight (TW), dry weight
of the left drumming muscles (DM), gonadosomatic index
(GSI), condition factor (K) and hepatosomatic index (HSI)

Maturation state

Origin

Non-spawning

Nw

Spawning

Nw
Fr

Sex

N

TL (cm)

Results
Fish and observations of drumming muscles
Nw-spawning individuals for both sexes showed
significant higher GSIs compared to Fr-spawning
individuals (Table 2).
The present study showed the presence of DM in
hake: a pair of muscular structures is located at the
anterior end of the swimbladder, close to its ventral
wall (Nw female: Fig. 1a; Nw male: Fig. 1b). Note
that the DM are rounded at the posterior end but

slightly pointed anteriorly and considerably larger in

TW (g)

DM (mg)

GSI (%)

K

HSI (%)

Fem.

37

28.7±15.2

327.2±815.1

3.12±5.41

1.56±2.89

0.57±0.06

2.60±1.58

Male

37

27.1±11.6

143.7±166.1

10.15±23.74

0.17±0.05

0.56±0.05

1.58±0.03

Fem.

15

75.5±7.5

3085.3±1273.1

23.27±8.96

9.38±4.25

0.69±0.08

4.98±5.20

Male

15

69.1±8.7

2477.1±852.2

225.7±123.6

4.12±2.78

0.69±0.06

2.71±1.06

Fem.

15

64.7±13.0

2120.1±1423.1

18.38±9.41

5.10±2.03

0.71±0.06

3.33±0.83

Male

24

45.7±13.4

784.3±690.3

98.75±78.29

1.44±0.88

0.63±0.07

2.20±1.07


10
Fig. 1 Dissection of spawning hake caught on 18
August 2005 in waters off
Western Norway. Total
length (TL), total weight
(TW) and the dry weight of
the left drumming muscles
(DM) are indicated. (a)
Dissection of a spawning
female. TL=83 cm, TW=4
270 g and dry weight of left

drumming muscles=22 mg.
(b) Dissection of a spawning
male. TL=80 cm, TW=3
440 g and dry weight of left
drumming muscles=266 mg

Environ Biol Fish (2011) 91:7–13


Environ Biol Fish (2011) 91:7–13

11

Fig. 2 Variation in left
drumming muscle dry
weight (DM in mg) in
relation to total length (TL
in cm) of European hake for
females (circles) and males
(triangles), split into
non-spawning (open
symbol) and spawning
individuals (filled symbol)
for Norwegian (a) and (b),
and for French samples (c)
and (d)

(ANCOVA). The same result appeared when compared to Nw non-spawning females (Fig. 2a+b) (P<
0.001) and also very much in relation to Nw
spawning females (Fig. 2a+b) (P < 0.01). The

ANCOVA also showed that Fr spawning males had
significantly heavier DM compared to Fr spawning
females (Fig. 2c+d) (P<0.001).

the male than in the female of similar length
(≈80 cm), i.e., in the present example the male DM
dry weight was 12 times larger than in the female.
The DM of the female sits as a flat structure on the
swimbladder wall whereas for the mature male it
appears much thicker. For mature specimens there
was noticed a difference in the colour of the male and
female DM as viewed in situ: the DM of the mature
male for all size classes tends to be reddish fleshcoloured, while light pinkish for females.

Discussion

Relation of drumming muscles dry weight to length,
sex and maturity stage

Observations of the drumming muscles of male
and female hake

There were examples of significant correlations
between DM dry weight and fish total length
(Fig. 2; Table 3). However, for spawning females
the DM dry weight increased only slightly with length
while for spawning males there was a rapid increase
at larger lengths. For the same length, Nw spawning
males had a significantly heavier DM compared to
Nw non-spawning males (Fig. 2b) (P < 0.001)

The present study showed the presence of a sexually
dimorphic muscle in hake males and females. The
main evidence that this fish produce sounds is
provided by the presence of a pair of muscles, one
on either side of the swimbladder, similar to those
found in known vocalists (as e.g., haddock, cod, lythe
(Pollachius pollachius), and tadpole-fish (Raniceps
raninus)) (Sørensen 1884; Hagman 1921; Jones and

Table 3 Regression equations describing left drumming muscle dry weight (y)
as a function of total length
(x) for female and male
hake from Western Norway
(Nw) and France (Fr) (Bay
of Biscay) in non-spawning
and spawning conditions

Maturation state

Origin

Sex

Regression equations

Non-spawning

Nw

Fem.

y ¼ 0:333x À 6:45
y ¼ 1:721x À 36:96
y ¼ 0:833x À 39:65
y ¼ 10:402x À 492:76
y ¼ 0:623x À 21:87
y ¼ 5:264x À 141:55

Male
Spawning

Nw

Fem.
Male

Fr

Fem.
Male

r2

P-values

37

0.937

P<0.001

36

0.835

P<0.001

15

0.701

P<0.01

15

0.734

P<0.01

13

0.864

P<0.001

24

0.904

P<0.001

Sample size


12

Marshall 1953; Templeman and Hodder 1958). In
cod, Delaroche (1809) and Sørensen (1884) describe
the weak, flattened muscles which pass from the sides
of the swimbladder at its anterior end to the ribs of the
anterior vertebrae. Jones and Marshall (1953) label
these external swimbladder muscles of the cod as
drumming muscles (DM). In the European haddock,
special groups of muscles attached to the ventral wall
of the swimbladder defined as well as drumming
muscles were described by Templeman and Hodder
(1958). These anatomical similarities found between
the DM described in cod or in haddock in comparison
with the muscles presently described in hake provide
more circumstantial evidence for the idea that hake
produce sounds. Sound production is caused by rapid
contraction and relaxation of the DM attached to the
swimbladder, as mentioned earlier (Templeman and
Hodder 1958; Brawn 1961; Hawkins and Rasmussen
1978; Hawkins and Amorim 2000).
Relation of drumming muscles dry weight to length,
sex and maturity stage
Presently collected Norwegian (Nw) spawning individuals showed significant higher GSI compare to the
French (Fr) spawning individuals, respectively for

females and for males. The low GSI values for the Fr
samples indicate that the sampling in the Bay of
Biscay was done at the end of the reproductive
season. However, sexual differences in DM were
observed also for spawning Fr individuals. Male hake,
as described for cod, may present sexually dimorphic
DM during and sometime after the termination of
spawning (Nordeide et al. 2008). Non-spawning
individuals could not be captured in French waters
as the two cruises (sampling programmes) were
restrained to the supposed reproductive period. Fortunately, in Nw waters both fish from mid-September
until late November including spawning and non
spawning individuals could be collected.
The drumming muscles of the male hake swimbladder clearly enlarge as the male becomes sexually
mature. In female hake, on the other hand, there is no
increase in the size of the DM with sexual maturity
and no significant increase with increase in the size of
the fish. Similarly, controlling for the influence of
body size, Rowe and Hutchings (2004) found that
male Atlantic cod have larger DM than females and
that among males, DM increase in mass before

Environ Biol Fish (2011) 91:7–13

spawning and decline thereafter. In haddock, which
also belongs to the cod family (Gadidae), the sexually
dimorphic drumming muscles of mature males increase to nearly twice their normal size during the
spawning period (Templeman and Hodder 1958;
Hawkins et al. 1967). Templeman and Hodder
(1958) found no significant difference between the

volumes of the DM of female haddock at different
seasons. This sex-specific developmental pattern may
reflect the important function of the drumming
muscles, and thus of sound production, in the
reproductive behaviour of haddock (Templeman and
Hodder 1958). Both sexes of cod and haddock call
during most of the year, whereas only males seem to
call during the spawning period (Brawn 1961;
Hawkins and Rasmussen 1978; Hawkins and Amorim
2000). Both male and female haddock were observed
in tank to produce short sequences of repeated
‘knocks’ during agonistic encounters. In cod, grunts
are produced during defensive and aggressive behaviour by both sexes when examined in aquarium
tanks in the laboratory and in netting enclosures in the
sea (Hawkins and Rasmussen 1978). During the
spawning season, however, male fish produce sounds
which vary in their characteristics as courtship proceeds (Hawkins and Amorim 2000). Sexual dimorphism and seasonal variation in sound-producing
musculature have been documented for several other
fishes, including weakfish (Connaughton and Taylor
1994), plainfin midshipman (Porichthys notatus)
(Brantley and Bass 1994; Bass 1997) and Opsanus
tau (Gray and Winn 1961). In some members of the
family Sciaenidae only the males possess specially
developed DM, e.g. the gray squeteague Cynoscion
regalis (Fish 1954). For others, both sexes produce
sound, as for the sea horse, Hippocampus brevirostris,
in which both males and females make sounds most
intense and most frequent during the breeding period
(Dufossé 1874).
We suggest that mature male hake use their

drumming muscles more often than either mature
females or immatures of either sex, because these
muscles in mature males are more highly vascularised
(darker red) than those of mature females (light pink).
As well, drumming muscle mass in males and females
is similar prior to spawning, but during the spawning
season it increases significantly in males. According
to Lucio et al. (2000), first maturity is reached in
Merluccius merluccius around 42 cm (both sexes


Environ Biol Fish (2011) 91:7–13

combined). We could therefore expect that hake males
and females do not have significant different DM
until their first maturity.

Conclusion
This study showed for the first time the presence of
drumming muscles in hake. During the spawning
season only drumming muscles from male individuals
are hypertrophied. Based on comparisons established
with other gadoids we can thus suppose that sound
production by adult males is more frequent during the
spawning season than during the rest of the year. It is
suggested that differences in size of the drumming
muscles of male and female hake reflect changes in
sound production with sex, sexual maturity, and season.
Acknowledgements Authors would like to specially thank
fishermen for welcoming us on board to collect the biological

material and Audrey Geffen for financial support (University of
Bergen, Norway). Thanks to Ignacio Serrano for his help in
dissecting fish. Finally thanks to Jon Egil Skjæraasen for his
advices while initiating this study as well to Anne-Christine
Utne Palm (University of Bergen, Norway).
Open Access This article is distributed under the terms of the
Creative Commons Attribution Noncommercial License which
permits any noncommercial use, distribution, and reproduction in
any medium, provided the original author(s) and source are credited.

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Environ Biol Fish (2011) 91:15–25
DOI 10.1007/s10641-010-9754-2

Sex differences in biparental care as offspring develop:
a field study of convict cichlids (Amatitlania siquia)
Jennifer L. Snekser & Nicholas Santangelo &
John Nyby & Murray Itzkowitz

Received: 5 February 2010 / Accepted: 15 November 2010 / Published online: 29 January 2011
# Springer Science+Business Media B.V. 2011

Abstract Parental investment theory states that
parents should contribute more to older offspring.
Differences between the sexes also influence how each
parent contributes to offspring in biparental species.
Here, we examined a naturally occurring population of
biparental convict cichlids in Costa Rica to determine
how each parent cared for offspring during two distinct
offspring development stages. Consistent with the
predictions of the reproductive value hypothesis, we
hypothesized that the levels of parental contribution
would be relative to the value that each parent places
on a brood. We predicted that female parents would
contribute more than male parents because female
convict cichlids have lower future reproductive success

than males. Additionally, we predicted that both
parents should contribute more to older offspring,
either due to the young’s increased susceptibility to
predation (i.e., the vulnerability hypothesis) or because
of the longer period of time parents have been
interacting with older offspring (i.e., feedback hypoth-

eses). This increase in investment by males should
coincide with a change in the coordination of care
between parents. Detailed observations of parental
pairs in their natural habitat supported these predictions. Females contributed more to broods than males
and were relatively unaffected by offspring age while
males spent significantly more time with older, freeswimming fry. Additionally, males tended to leave
younger offspring more than females did, and were
more likely to do so consecutively with younger
offspring. This suggests that the coordination of duties
between parents changes as parental investment
changes. Overall, these data support both the reproductive value and the vulnerability hypotheses, but not
necessarily the feedback hypothesis.
Keywords Amatitlania siquia . Biparental care .
Convict cichlid . Sex differences

Introduction
J. L. Snekser (*) : J. Nyby : M. Itzkowitz
Department of Biological Sciences, Lehigh University,
111 Research Drive,
Bethlehem, PA 18014, USA
e-mail:
e-mail:
N. Santangelo

Department of Biological Sciences,
Eastern Kentucky University,
Moore 235, 521 Lancaster Avenue,
Richmond, KY 40475, USA

Multiple assessments on parental investment theorize
that parents should invest more in older rather than
younger offspring (Williams 1966; Trivers 1972;
Winkler 1987). Many empirical studies of parental
contribution to the care of offspring have shown that
parents provide more care as offspring grow older
(Andersson et al. 1980; Westneat 1988; Brunton
1990; Lavery and Keenleyside 1990; Rytkönen et al.
1990; Lavery and Colgan 1991; Cézilly et al. 1994;
Pavel and Bureš 2001), though a few studies have


16

shown the reverse trend, with parents contributing
less to specific care activities as parents get older
(Dale et al. 1996; Karino 1997; Koskela et al. 2000).
A variety of hypotheses as to the ultimate and
proximate reasons that parents change their contributions as offspring develop have been proposed. These
hypotheses have been explored in a variety of
biparental bird species in which both parents contribute
to the division of labor. The three main hypotheses as
to why parental care increases as offspring age are the
reproductive value hypothesis, the vulnerability hypothesis, and the feedback hypothesis. The reproductive value hypothesis states that parents should
contribute more to older offspring because the reproductive value of offspring increases with age (Barash

1975; Maynard Smith 1977; review by Montgomerie
and Weatherhead 1988). Essentially, older offspring
have a higher probability than younger offspring of
surviving to breeding age, therefore, parents should
contribute more to them. In a study of biparental
magpies (Pica pica), increases in parental defense were
highly correlated with offspring age, but this did not
correspond to increases in predation risk, suggesting
that the reproductive value of the offspring was the
primary influence (Redondo and Carranza 1989). The
vulnerability hypothesis (also referred to as the
predation risk hypothesis) suggests that the increase
in parental contributions with offspring age is due to
the increase in conspicuousness of the young (Harvey
and Greenwood 1978; Andersson et al. 1980; GreigSmith 1980; Onnebrink and Curio 1991). Zenaida
doves (Zenaida aurita) show increases in parental care
that are consistent with changes in the vulnerability of
chicks rather than a linear increase in care as offspring
grow (Burger et al. 1989). However, depending on the
behavioral ecology of the species, the vulnerability
hypothesis could predict an inverse relationship between offspring age and degree of parental care. For
example, if older young are less vulnerable to
predation, they would require less protection from
parents (Galeotti et al. 2000; Koskela et al. 2000).
According to the feedback hypothesis, parental contributions are enhanced as offspring age because of the
parents’ continued exposure to the offspring (McLean
and Rhodes 1992). Specifically, increased stimulation
from offspring as they develop from eggs to active
young continually amplifies parental responses to
young. The feedback hypothesis predicts that, in

species where females build the nest and incubate the

Environ Biol Fish (2011) 91:15–25

eggs, females will initially provide more care than
males and both parents will increase their care as
young grow, as shown in meadow pipits (Anthus
pratensis) (Pavel and Bureš 2001). Of course, these
three hypotheses are not mutually exclusive; all may
be contributing to varying degrees in determining why
levels of care change as offspring age.
Parental contribution levels must also be considered in light of the parents themselves. In species in
which both parents provide offspring care, male and
females typically differ in their contributions to
offspring. Many biparental species do not simply
equally divide each care giving activity, but rather
favor sex-specific roles. In species that show these sex
specific roles, males commonly engage in territorial
defense while females are involved in more direct
care of offspring (birds: Burger 1981; Creelman and
Storey 1991; Fraser et al. 2002; fish: Keenleyside
1991; Lavery and Reebs 1994; Wisenden 1995;
Itzkowitz et al. 2001, 2003, 2005). Such sex differences can be attributed to proximate mechanisms
(such as anatomical, physiological, or behavioral
differences; Lessells 2002) and ultimate mechanisms
(such as differences in potential future reproductive
success; Trivers 1972; Westneat 1988). As such, the
interaction between offspring value based on age and
the care provided based on the sex of the parent can
lead to the complex care giving strategies that we

observe in nature.
An ideal biparental system in which to explore the
dynamic patterns of parental contributions is the
convict cichid (Amatitlania suquia). In the past two
decades, this freshwater system has become a model
species for the study of monogamy and biparental
care. Both parents contribute to extended care of the
offspring for up to 6 weeks but rarely remain together
to jointly raise a second brood (Wisenden 1995).
Together, the male and female find a protected,
smooth substrate on which to lay eggs, which hatch
after approximately 5 days. For five additional days,
the young are non-swimming and remain within the
nest. When the young become free-swimming they
leave the nest and parents swim slowly by the shoal
of young as they feed off the bottom detritus.
Laboratory and field studies have found that females
generally provide more direct care (e.g., spending
time in the nest with offspring) and males provide
more indirect care (e.g., engaging in aggression with
potential brood predators). While this system exhibits


Environ Biol Fish (2011) 91:15–25

sex specific roles, both sexes also have the ability to
undertake the other parent’s roles if required (such as
when one parent is absent; Itzkowitz et al. 2001).
Therefore, pairs show a highly structured coordination of care giving activities (Itzkowitz et al. 2002).
Although the influence of offspring age on these

parental patterns in convict cichlds has been explored,
different trends have been reported. Both field and
laboratory studies show that parental aggression
generally increases as offspring age (Keenleyside et
al. 1990; Lavery and Colgan 1991). These studies did
not reveal many sex differences due to variation in
offspring age. In laboratory and artificial ponds, males
and females only differed in the amount of time spent
near the brood (during the egg and wriggler stages)
with males spending more time away (Keenleyside et
al. 1990; Lavery and Colgan 1991) with no clear
effect of offspring age. This suggests that the brood
value to either parent does not change as offspring
age. In support of this, using a model predator, Lavery
and Colgan (1991) also showed that males and
females do not differ in their aggression across
developmental stages. However, in the field, sex
differences in both aggression levels and time spent
with broods have been observed across developmental
stages. Males increase their time spent with offspring
as the offspring age with females spending a fairly
consistent amount of time across stages, and both
sexes increase their aggression as offspring age, but
chase different types of intruders (Keenleyside et al.
1990). A field study on the Lake Xiloá population of
convict cichlids in Nicaragua showed increases in
parental aggression as offspring developed, with males
showing more aggression than females from the egg
stage until fry were greater than 2 weeks old (Alonzo
et al. 2001). These differences between laboratory and

field studies might suggest that sex differences are
only apparent in complex environments with multiple
predation threats.
In an attempt to resolve these conflicting laboratory
and field data while exploring further the dynamic
patterns of parental contributions as offspring age, we
observed natural convict cichlid pairs during two
distinct stages of parental care. We hypothesized that
the degree of care exhibited by each parent would be
consistent with the value that each parent places on the
brood. We predicted that female parents would
contribute more than male parents based on the
difference in potential reproductive success between

17

males and females in this species. That is, females
typically only breed once per season while males will
breed with up to four different females (Wisenden
1995). To address the degree of parental contributions
more specifically than the studies that have come
before, we recorded a wider variety of behaviors,
including levels of aggression directed at potential
brood predators (chases), the number of times each
parent left the offspring, the amount of time spent
away each time a parent left the brood, the pattern of
leaving that parents exhibited (i.e., the number of
consecutive trips away exhibited by a single parent),
and which parent was present with the offspring across
developmental stages. These additional measures will

reveal more about the continual individual contributions of each parent, as well as the coordination of care
between parents, throughout the growth of their
offspring.

Methods
Field observations
Parental pairs of convict cichlids were observed
within the Lomas Barbudal Biological Reserve,
Guanacaste, Costa Rica (Wisenden and Keenleyside
1994). Data were collected during the dry season in
which the water is clear and pairs can easily be
observed. The 51 pairs were observed during January
1996, December 1999 and January 2000. Pairs were
identified by methodically going through the streams
and looking for a male and a female fish that were
within close proximity. Pairs were observed only once
and were examined to determine the stage of the
offspring for which they were caring.
As in Keenleyside (1991), we define the developmental stages of offspring as follows: the “egg stage”
refers to the 5-day period in which the embryo is
developing within the unhatched egg. Eggs hatch into
free-embryos (eleutheroembryos) that have a large
yolk sac and are unable to swim, which are referred to
as “wrigglers”. These wrigglers develop into freeswimming larvae after an additional 5 days. Freeswimming larvae are cared for by the parents for
approximately 45 days. We use the vernacular term
“fry” to refer to these free-swimming larvae that are
under parental care. These terms are common to
convict cichlid parental care studies (e.g., Keenleyside

18

et al. 1990; Keenleyside 1991; Lavery and Colgan
1991; Wisenden 1995; Alonzo et al. 2001; Wisenden
et al. 2008), but formal definitions and terminology of
ontogenetic stages can be found in Balon (1999).
It was determined if pairs were caring for eggs,
wrigglers or swimming fry. Eggs and wrigglers were
always found within the cave or outcropping “nest”
protected by parents. Pairs were analyzed according to
the stage of their offspring. Eggs and wrigglers were
clumped to represent ‘younger’ offspring (N=12) and
fry represented ‘older’ offspring (N=39). This was
done for two reasons. First, the shortened period of
time that offspring exist as eggs or wrigglers (e.g.,
10 days total) relative to being free swimming fry (e.g.,
14–25; Wisenden 1994b; Wisenden and Keenleyside
1992) make it less likely to find pairs that are within
the egg or wriggler stage. Second, because wrigglers
sit within the rock crevices where eggs are laid, it is
difficult to distinguish the difference between eggs and
wrigglers without completely disturbing the nest.
Multiple observers monitored different nests
throughout the field site, making sure not to sample
the same pair twice. Observers watched pairs and
recorded each parent’s behavior. The total number of
chases exhibited by each parent toward conspecific or
heterospecific intruders was recorded. The species
being chased could not always be identified and
therefore all chases were considered together as a

general measure of parental aggression. Also recorded
was the number of times each parent left the offspring
at a distance of at least five fish lengths. At this
distance, it is common for the leaving parent to
continue swimming away from its offspring and mate.
Additionally, the duration and sequence of each time
the parents left the offspring were also recorded. The
number of times that parents flipped leaves (Wisenden
1995) occurred infrequently and only during the fry
stage and was not included in analyses.
The observation period ranged from 503 s to
1020 s. To account for the variation in observation
time, all behaviors were subsequently calculated as
either a percentage of time or as a rate per 300 s
(5 min) period.
Statistical analysis
Overall time that parents spent with offspring during
each stage (eggs/wrigglers or swimming fry) was
analyzed twice. First, to determine how much time

Environ Biol Fish (2011) 91:15–25

each ‘caring unit’ (i.e., both parents; male only;
female only; or neither parent) was attending the
offspring, a 4×2 repeated measures ANOVA was used
with ‘caring unit’ as a within subjects factor and stage
of offspring as a between subjects factor (eggs/
wrigglers or fry). Second, an additional 2×2 repeated
measures ANOVA was utilized to determine sex
differences in the time spent with the offspring during

each stage, with sex of parent as the within subjects
factor (male or female) and stage of offspring as a
between subjects factor (eggs/wrigglers or fry). Due to
the multiple analyses dealing with time, a Bonferroni
correction was applied and the significance value for
these measures was set at p<0.025.
The number of times each parent left the offspring
(i.e., trips) and the average duration of these trips
were each analyzed using a 2×2 ANOVA with sex of
parent as a within subjects factor (male or female) and
stage of offspring as a between subjects factor (eggs/
wrigglers or swimming fry).
The probability that a parent would leave twice in
succession was determined by the mean percentage of
times the male or female would leave their offspring
immediately following a previous trip away from the
offspring. To determine if males or females were more
likely to leave the offspring twice in succession, a 2×
2 ANOVA was used with sex of the parent that left as
a within subjects factor (MM or FF) and stage of
offspring as a between subjects factor (eggs/wrigglers
or swimming fry) (egg/wrigglers group, N=11; fry
group, N=38).
The number of chases directed toward conspecific
or heterospecific intruders performed by each parent
during each offspring stage was analyzed using a 2×2
ANOVA with sex of parent as a within subjects factor
(male or female) and stage of offspring as a between
subjects factor (eggs/wrigglers or swimming fry).
Most, but not all, pairs of parents chased intruders.

The complete lack of chasing by some pairs was
presumably due to a lack of intruder presence during
the observation period. Given the difficulty in
accurately assessing the number of threatening brood
predators within the winding, wide yet shallow
streams typical of convict cichlid habitat, normalizing
aggression levels for brood predator presence during
observation periods was impossible. Therefore, to
account for the extreme influence that non-chasing
pairs would have on statistical comparisons, only
pairs in which chases occurred (for one or both


Environ Biol Fish (2011) 91:15–25

parents) were included within the analysis (eggs/
wrigglers group, N=6; fry group N=24). This allowed
us to acquire the least biased estimate of natural
aggression levels.

Results
For overall percentage of time spent with offspring,
significant differences were found among the parental ‘care units’ (i.e., both parents present, male only,
female only, or neither parent present) (F3, 147 =
37.66; p<0.001). Additionally, we found a significant interaction of parental category and offspring
stage (F3, 147 = 13.31; p < 0.001). Offspring were
nearly always attended to by some parent, during
both the egg/wriggler stage (99.62±0.24% of the
time) and swimming fry stage (98.90±0.46% of the
time). During the egg/wriggler stage, females were

primarily the sole parent with offspring (67.54±9.02 %
of the time). Both parents, however, were present most
often during the swimming fry stage (56.34±4.67% of
the time; Fig. 1a).
In examination of the total time that each parent is
spending with the offspring, we find a significant
effect of offspring stage (F1, 49 =8.34; p=0.006), a
significant effect of the sex of the parent (F1, 49 =
72.36; p<0.001) and a significant interaction of the
two (F1, 49 =25.28; p<0.001). Females always spent
more time than males with the offspring, but males
spent substantially more time with swimming fry than
with eggs/wrigglers (Fig. 1b).
Parents left swimming fry significantly more often
than they left eggs/wrigglers (F1, 49 =8.48; p=0.005),
but male and female parents left the offspring an
equivalent number of times (F1, 49 =0.57; p=0.45).
There was not a significant interaction of parent sex
and offspring stage (F1, 49 =1.47; p=0.23; Fig. 2a).
Despite the fact that male and female parents left their
offspring a similar number of times at each stage,
males spent significantly more time away from the
offspring than females did per trip (F1, 49 =13.22; p=
0.001). There is a significant interaction of parent sex
and the stage of the offspring (F1, 49 =4.12; p=0.048)
and a very strong trend towards an effect of the
offspring stage (F1, 49 =3.87; p=0.055), with more
time spent away per trip, on average, during the eggs/
wrigglers stage (40.44±3.18 s) compared to when
offspring are swimming fry (15.72±0.98 s; Fig. 2b)

19

and males showing a larger change in the amount of
time spent away than females did.
During the egg/wriggler stage, parents took turns
leaving the offspring 52.81% of the time. During the
swimming fry stage, parents took turns leaving the
offspring 59.74% of the time. That is, when the male
returned from being away, the female would leave
next, and vice versa. In examining the number of
times a parent would leave on two successive trips
away from the offspring, there was no significant
overall effect of the sex of the parent (F1, 47 =1.88; p=
0.18) nor a significant overall effect of the offspring
stage (F1, 47 =1.21; p=0.28). There was, however, a
significant interaction of parent sex and offspring
stage (F1, 47 =4.52; p=0.039). It appears that during
the egg/wriggler stage there is a much greater
difference in the probability of males leaving twice
in succession as compared to females than when
offspring are swimming fry (Fig. 3).
Chases directed toward intruders were not significantly different between males and females (F1, 28 =
2.44; p=0.13), nor between offspring stages (F1, 28 =
2.42; p=0.13), nor was there a significant interaction
of the two (F1, 49 =0.96; p=0.35; Table 1).

Discussion
Within this natural population of convict cichlids, the
age of offspring significantly influenced overall

parental contributions. Parents spent more overall
time with the older, swimming fry than with the
younger, stationary eggs or wrigglers. While parents
did leave the fry more often than they left eggs/
wrigglers, they left for far shorter durations. This
differential contribution to older offspring is in
concordance with many of the results from previous
studies on the convict cichlids in both the laboratory
and field (Keenleyside et al. 1990; Lavery and Colgan
1991; Alonzo et al. 2001) and supports the idea that
parents invest more in older offspring.
While the majority of studies exploring increases
in parental contributions in convict cichlids focus on
aggression and defense (Keenleyside et al. 1990;
Lavery and Colgan 1991; Alonzo et al. 2001), the
pattern by which older offspring received more care
here revealed important sex differences. The change
in the number of times that parents leave the
offspring, the duration of trips away, and the overall


20

Environ Biol Fish (2011) 91:15–25

Fig. 1 a Mean + SE percentage of time that both
parents, the male only, the
female only or neither parent spent with the eggs/
wrigglers or swimming fry
and b the mean + SE percentage of time that each

parent (male or female)
spent with either eggs/wrigglers or swimming fry

pattern of parental leaving as offspring aged demonstrates that it is the male who primarily adjusts his
behavior during offspring development. Overall, and
as predicted, males spent less time with the offspring
at each stage than females did. In fact, during the egg/
wriggler stage, the female was mainly alone with the
young. Although males left the brood as often as
females did during each offspring stage, they left for
significantly longer periods of time. That females are
more attentive to broods than males is not surprising
given previous studies on biparental division of care
in both the laboratory and the field (Smith-Grayton
and Keenleyside 1978; Keenleyside et al. 1990;
Keenleyside 1991; Lavery and Colgan 1991; Lavery
and Reebs 1994; Wisenden 1995; Itzkowitz et al.

2001, 2003, 2005). Males appear to be contributing
less during the egg/wriggler stages and more to the
older swimming fry, while females are relatively
unaffected by offspring age and are consistent in their
level of care. This change in level of attentiveness
indicates a change in offspring investment by only the
males over the course of offspring development. This
increase in investment by only one parent would
predict that a change in the degree of coordination
between parents would be necessary as offspring age.
This might explain the observation that males and
females were equally likely to leave older fry in

succession, yet males were more likely than females
to leave two successive times during the younger egg/
wriggler stage.


Environ Biol Fish (2011) 91:15–25

21

Fig. 2 a Mean + SE number of times that each parent
(male or female) left their
eggs/wrigglers or swimming
fry per 5 min period and b
the mean + SE amount of
time that each parent (male
or female) spent away from
their eggs/wrigglers or
swimming fry per leaving
trip per 5 min period

It is difficult to determine the drive behind this
increase in male parental care across offspring stages.
One possibility is the value he places on the brood (i.e.
the reproductive value hypothesis). Relative to older
offspring, younger offspring represent less in terms of
reproductive success because juvenile mortality generally decreases with increasing age (Clutton-Brock
1991), and older offspring are closer to reproductive
age so are more likely to contribute to parental fitness.
This may be impetus enough for males to place a
higher value on older broods and contribute more to

them. If so, then our data also suggest that females
value offspring of any age rather equally since females

did not alter their brood attention over offspring
stages. This is expected in a system where the female
essentially has only one chance to raise a brood in a
season (Wisenden 1995). In fact, females might be
contributing maximally to young, regardless of fry age
and regardless of level of male contributions (as in the
greater flamingo: Cézilly 1993). This would explain
the lack of female compensation for low levels of male
care during the egg/wriggler stage (as in various
species of burying beetles: Rauter and Moore 2004;
Smiseth et al. 2005; Suzuki and Nagano 2008).
Possibly during early development, eggs and
wrigglers actually require less care being in the cover


22

Environ Biol Fish (2011) 91:15–25

Fig. 3 The probability
(mean percentage + SE)
that one parent would leave
the offspring (eggs/wrigglers or swimming fry) following a previous bout of
being away. MM=male left
the offspring a second time
after he had just previously
been away. FF=female left

the offspring a second time
after she had just previously
been away

of a nest as opposed to being exposed while
swimming. This could explain the change seen in
male care over offspring age; a higher level of defense
is necessary to protect conspicuous, swimming young
(i.e., the vulnerability hypothesis). This could also
explain the lack of female compensation for male care
during young stages; the young simply do not require
additional care at this stage. The increased exposure
to potential predators with age likely increases the
need for parental protection (Skutch 1985). This
might demand that males attend to their swimming
offspring, particularly if females are already investing
their maximum (see above). We recognize the
possibility that, because free swimming fry are always
moving and the location of eggs/wrigglers remains
constant (i.e., in the nest), males attentive behavior
may be based on having to check the location of fry
sooner after leaving in order to be able to keep track
of them. However, using the increase in conspicuousness and the increased movement of the offspring as
the sole explanations for the patterns we observed fail
to explain the female’s lack of change in behavior. If
Table 1 Mean ± SE number of chases exhibited during the
egg/wrigglers (N=6) or swimming fry stages (N=24) by male
and female parents per 5 min observation period. No significant
differences
Behavior

Offspring stage

Male

Female

Chases

Eggs/Wrigglers

0.87±0.25

1.22±0.27

Fry

1.64±0.25

3.07±0.49

it simply were that fry are more conspicuous or move
about more freely, and not about relative investment
based on offspring value, then female behavior should
mimic male behavior. Therefore, a combination of
both increased brood value to the male and increased
need for offspring protection seems the most parsimonious explanation.
The inverse of the vulnerability hypothesis has
also been suggested, where older offspring have a
higher degree of anti-predatory competency and

therefore actually require less parental care (Galeotti
et al. 2000; Koskela et al. 2000), but our data do not
specifically support this idea. It is possible that a
more detailed assessment of older swimming fry
would reveal that parent contributions again decline
as offspring near independence (Montgomerie and
Weatherhead 1988). For example, examination of
brood desertion by male convict cichlids have shown
that broods can be successfully raised by the lone
female, but only when broods are older (Keenleyside
et al. 1990; Keenleyside and Mackereth 1992;
Wisenden 1994a). This may indicate that less care
is required by the offspring as they near independence, thus allowing males to desert and seek a new
mate for a new brood.
While our data show support for both the reproductive value and vulnerability hypotheses, the feedback
hypothesis is not necessarily supported. In biparental
species, the feedback hypothesis predicts that the
parent that has more interactions with the nest should
defend it more vigorously (Hayes and Robertson 1989;


Environ Biol Fish (2011) 91:15–25

Pavel and Bureš 2001). In bird species, it is argued that
because the female initially prepares the nest and tends
to the eggs more, she will garner more overall
stimulation from the offspring and will therefore
provide more early care. The male, who aids little in
the nest preparation, is only continually stimulated as
he provisions more and more as the chicks grow older,

and thus increases his care as the chicks age (Pavel and
Bureš 2001). Therefore, it is expected that female care
will increase with offspring age, but not as much as
male care increases (Hayes and Robertson 1989; Pavel
and Bureš 2001). Convict cichlid pairs jointly excavates a cave for the nest, so both are initially exposed
to the nest itself (Wisenden 1995). If the feedback
hypothesis were supported, this joint nest building
would lead to both parents contributing at similar
levels due to similar exposure to the nest, which is not
apparent here. While it could be argued that convict
cichlid females have more exposure than males to eggs
and wrigglers and therefore more stimulation and
reinforcement, we did not see any increase in female
contributions between offspring stages. It is only the
male that increases his time with offspring and leaves
them less as they age. Thus, it seems unlikely that the
female is influenced by exposure to and reinforcement
from young.
Previous studies regarding convict cichlid parental
contributions also focus on offspring defense as a
measure of parental investment. As the data from
those studies are somewhat conflicting, our data
support some, but not others. Lavery and Colgan
(1991) showed that aggression generally increased as
offspring aged but no difference in aggression
existed between the sexes at any offspring stage.
This lack of a sex difference in aggression supports
our findings in the field. However, Keenleyside et al.
(1990) showed sex differences in the types of
intruders that each parent chased in both artificial

ponds and in the field. Males chased conspecific
adult males more than females did and females
attacked juvenile and female convict cichlids, as well
as non-cichlid intruders, more than males did. In
Nicaragua, there was also a sex difference in chases
directed at specific predators (Alonzo et al. 2001).
Males were generally more aggressive toward five of
eight of the species examined and were more
aggressive than females overall, though females still
showed high levels of aggression, at a rate approximately 70% of the male.

23

We attribute the fact that our study more generally
agrees with Lavery and Colgan’s (1991), rather than
Keenleyside et al.’s (1990) or Alonzo et al.’s (2001),
to offspring threat differences between studies. For
example, Lavery and Colgan (1991) used a model of a
brood predator (thus the threat level from this stimulus
would be static), while within the Keenleyside et al.
(1990) and Alonzo et al. (2001) studies the number of
attacks and threats increased as the brood aged. In our
study, the number of chases toward potential brood
predators did not significantly differ by sex nor
between the developmental stages. Therefore, the
species, age, sex, and number of intruders that
approached broods during observation periods in
Keenleyside et al.’s (1990) study and Alonzo et al.’s
(2001) versus our own likely influenced the resultant
number of chases. In Nicaragua, the threat of

predation to broods is much higher than in our field
conditions. Only 20% of pairs in Lake Xiloá are able
to successfully raise broods (McKaye 1977) (as
compared to 47% success rate in Costa Rican streams;
Wisenden 1994a) and, without parents, no brood
survived more than 6 min (Alonzo et al. 2001). Taken
together, the external environment (specifically predation level) has a strong influence on parental care
decisions and, along with the sex of the parents and
the age of the young, should be taken into consideration when exploring parental behavior.
While there were dissimilarities among all of the
studies on convict cichlid biparental behavior, there
was one obvious similarity: the age of the offspring
influences parental contributions, with more care
being provided to older fry. In this field study, the
higher level of contribution was due primarily to
changes in male contributions, with female parents
remaining relatively consistent in their contributions
to offspring. As total investment in offspring changes,
so does the coordination of caring for offspring
between the parents. Other populations of convict
cichlids that experience different predation threats
may coordinate their care differently (Alonzo et al.
2001). Our field observations provide evidence for the
reproductive value and vulnerability hypotheses of
parental investment, while generally not supporting
the proximate feedback hypothesis. Additional field
and laboratory experiments with strict controls are
necessary to better understand which mechanism or
combination of mechanisms leads to differential
parental contributions in biparental species.

24
Acknowledgements The authors are grateful to B. Wisenden
for advice on field work and locating field locations and to the
Lehigh University Department of Biological Sciences for
support. Thank you to K. McKaye and an anonymous reviewer
for suggestions that strengthened this manuscript.

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Environ Biol Fish (2011) 91:27–38
DOI 10.1007/s10641-010-9755-1

Ontogenetic dietary changes of whitefish larvae: insights
from field and experimental observations
Orlane Anneville & Vincent Berthon &
Olivier Glippa & Mohamed-Sofiane Mahjoub &
Juan Carlos Molinero & Sami Souissi

Received: 19 February 2010 / Accepted: 16 November 2010 / Published online: 1 December 2010
# Springer Science+Business Media B.V. 2010

Abstract Ontogenetic changes in resource use are
widespread in many fish species. This study investigated the feeding habits of whitefish (C. lavaretus L.)
larvae in Lake Annecy (France) coupled with experimental behavioral studies in order to identify the
underlying mechanisms of the ontogenetic shifts in
the diet. The predatory behavior of wild larvae, and
the escape responses of their zooplankton prey were
both videorecorded in experimental tanks under
controlled laboratory conditions. Ontogenetic diet
patterns showed that young whitefish larvae have a
preference for small cyclops, while older larvae
selectively predate cladocerans. Our experimental
O. Anneville : V. Berthon : O. Glippa : J. C. Molinero

observations showed that the capture success rate
also varied in relation to ontogenetic development in

fish. Young larvae were more successful in capturing
small copepods, whereas old larvae were more
successful in capturing Daphnia. In addition, the
larvae were able to adjust their predatory behavior
(speed, pursuit) according to the swimming pattern of
the prey. These observations suggest that the selective
predation on cladocerans observed in old larvae is the
outcome of both active and passive choices depending
on the escape swimming behavior of the prey, and
handling time of the predator.
Keywords Predation . Escape behaviour . Prey
selectivity . Coregonids . Ontogeny

INRA, UMR CARRTEL,
74203 Thonon les Bains, France
O. Glippa : M.-S. Mahjoub : S. Souissi (*)
Université Lille 1 Sciences et Technologies,
CNRS UMR 8187 LOG,
Station Marine, 62930 Wimereux, France
e-mail:
M.-S. Mahjoub
Institute of Marine Biology, National Taiwan Ocean
University,
2 Pei-Ning Road,
20224 Keelung, Taiwan, R. O. C
J. C. Molinero
Leibniz Institute of Marine Sciences, Marine Ecology/
Experimental Ecology,
Düsternbrooker Weg 20,
24105 Kiel, Germany

Introduction
Changes in resource or habitat utilization during
ontogeny are a widespread trait in many sizestructured populations, and evidence of ontogenetic
diet changes in marine and freshwater fishes has been
widely documented. However, the underlying mechanism of dietary shift in relation to ontogenetic
changes in fish has not been understood clearly. In
addition, as these mechanisms are species specific,
they cannot readily be extrapolated to other species.
Several mechanisms have been advanced to explain
changes in diet over time, including, shifts in habitat
use (Nakamura et al. 2008), the growth of morpho-