Journal of
Marine Animals &
Their Ecology
Vol 7 Issue 1 July/August 2014
Volume 7, Issue 1, July/August 2014
Journal of Marine Animals and Their Ecology
JMATE
TABLE of CONTENTS
EDITORIAL...................................................................................................................................................... pg 1
ANNOUNCEMENT ………………………………………………………………………………......................…… pg 2a
LETTERS TO THE EDITOR............................................................................................................................ pg 3
Citizen Scientists Playing a Role in Saving Threatened SpeciesScience and Reality Coming Together. Michael Belanger
ORIGINAL MANUSCRIPTS
BRIEF COMMUNICATION:
The mesoparasitic copepod Pennella balaenopterae and its significance as a viable indicator of health
status in dolphins (delphindae).
Vecchione A, Aznar FJ ...................................................................................................................... pg 4-11
SCIENTIFIC:
Case report - Recovery from severe cutaneous injury in two free ranging bottlenose dolphins
(tursiops spp.).
Bossley MI, Woolfall MA .................................................................................................................. pg 12-16
REVIEW ARTICLES
A review of natural milk, commercial replacement formulas and home-made substitutes used in the care
of rescued manatee calves.
Belanger MP, Wittnich C, Askin N .............................................................................................................. pg 17-22
The global distribution of sharks and pinnipeds: overlap in body size, trophic ecology and species
diversity.
Ferguson SH, Higdon JW, Tallman RF, Fisk AT, Hussey NE ............................................................... pg 23-tbd
Vol 7, No 1, 2014
Printed in Canada
Journal of Marine Animals and Their Ecology
Copyright © 2008 Oceanographic Environmental Research Society
Editorial
One health and our oceans - not just idle words !
It has been stated that
".. with 70% of the
oxygen we breathe
produced by marine
plants in the ocean,
every other breath
depends on a healthy
ocean" (2). Part of the
reason for this is that much of the earth's surface is
covered by oceans. If we accept the caveat that we
as humans are dependent on the oceans, then the
animals living within these oceans can serve as
sentinel species for the 'health' of these oceans and
thus potentially human health. Clearly then, humans
have a dependency on the oceans for numerous
reasons which links their health with that of the
species that occupy this environment. So logically,
our environment and the species within it are all
linked forming the basis of the 'one health' concept.
The concept of 'One Health’ has been around for
centuries. However it has been getting more
attention in the health care field of late. The term
has been defined in many ways but essentially it has
at its core the goal to link human, animal and
environmental health. The One Health initiative
website states that "The One Health Initiative is a
movement to forge co-equal, all inclusive
collaborations between physicians, osteopaths,
veterinarians, dentists, nurses and other scientifichealth and environmentally related disciplines" (1).
The concept of a role for environmental factors
impacting on human health is also not new as
Hippocrates stated in his writings that public health
depended on a clean environment (3).
Now you may be asking why bring up this
topic as an editorial for a marine animal journal?
Apart from the key role the oceans and their
inhabitants play in human survival and well being,
these oceans have also become a source of harmful
pathogens and contaminants. As well, viruses and
bacteria exist that transfer between species, either
terrestrial, aquatic or humans. Thus it seems only
prudent to invoke a 'one health' approach. Consider
the following examples: (a) harmful algae blooms
are increasing in severity and frequency causing
health issues to both the marine species and humans
(2, 4); (b) antibiotic resistance is increasing and
being reported in marine species such as dolphins as
well as humans (5); (c) contaminants in our oceans
are becoming more recognized for their long lasting
effects, including suppression of the body's natural
immunity which increases susceptibility to disease
(5, 6).
Contaminants also have negative effects on
other physiological systems such as reproduction
which then impacts on the affected species
population. Neurological effects can lead to
increased strandings and other life threatening
problems. For example, mercury has known
neurological and reproductive effects (6). A review
published in 2004 on global mercury levels in
various marine mammals over a 30 year period
demonstrated that despite legislation, a variety of
species have mercury levels that continued to rise
(6). Recent awareness for the role of multiple
contaminants acting either together or even
compounding their effects on those exposed has
taken on new relevance for aquatic species and, by
inference, humans since both are top predators of
their environment. Contaminated food sources from
our oceans can have devastating consequences for
the human population as well. For example, in
humans, Minimata disease was linked to mercury
poisoning from the consumption of contaminated
seafood, while cases of reported lead poisoning in
humans have also been linked to the consumption of
tainted food from the oceans. Recently reports of a
rare chronic mycotic infection seen only in humans
and dolphins has been reported in dolphins along the
Atlantic coast of the USA, who also had high levels
of mercury. Since this disease can be transferred to
humans, the recent reports of this disease in dolphins
1
JMATE
Vol 7, No 1, 2014
Printed in Canada
The Reasons behind Instructions to Authors
Editorial Cont’d
References
1.
One Health Initiative. http://
www.onehealthinitiative.com/index.php
2.
NOAA's Oceans and human health initiative.
https://www.eol.ucar.edu/projects/ohhi/facts/
ocean_health.html
3.
Wikepedia re one heath history. http://
en.wikipedia.org/wiki/One_Health
4.
Sadchatheeswaran S, Belanger M, Wittnich C.
A comparison of published brevetoxin
tissue levels in West Indian manatee,
bottlenose dolphin and double-crested
cormorants in southwest Florida. Journal of
Marine Animals and Their Environment.
5(1):20-27. 2012.
5.
Bossart GD. Marine mammals as sentinel
species for oceans and human health.
Veterinary Pathology 48(3):676-690. 2011.
6.
Wittnich C, Belanger MP, Askin N, Bandali
K, Wallen WJ. Awash in a sea of heavy
metals; mercury pollution and marine
animals. 2004. Report #01-2004.
ISBN #0-735138-0-2 last accessed
September 19, 2014 at http://www.oers.ca/
research/mercury-report.pdf
could indicate an additional risk to humans and
illustrates the connection between environmental
factors, aquatic and human health (5). Further
examples include protozoal infections that have
been reported in sea otters who ingested infected
shellfish originally contaminated from land animal
waste runoff in coastal regions. This coupled with
the risk to humans of consuming improperly
prepared contaminated seafood illustrates the
linkages with terrestrial animal, aquatic species and
human health.
This editorial cannot do justice to the concept
of "One Health" but is meant to stimulate some
thought and curiosity to explore it further. In
addition to the references sited, there are numerous
well written articles on the general subject. With
the large surface area of our planet occupied by
oceans and our reliance on it, by applying the ‘One
Health' concept to our aquatic environment,
conceivably we not only improve our understanding
of how changes and stressors affect aquatic life but
also how this could potentially affect human health
and their quality of life.
Dr Carin Wittnich
Editor-in-Chief, JMATE
2
JMATE
Vol 7, No 1, 2014
Printed in Canada
Journal of Marine Animals and Their Ecology
Copyright © 2008 Oceanographic Environmental Research Society
ANNOUNCEMENT
JMATE launches new section featuring student manuscripts
JMATE is pleased to launch a new section
under ‘Original Manuscripts’ specifically dedicated
to encourage current students in the field of
marine animal research to publish their work in a
peer review journal. Though the manuscripts will
undergo the same rigorous review afforded all
submissions, consideration will be given that the
first author is a student at the time of submission of
the manuscript, and certain expectations will be
adjusted. It is imperative that the work was done by
a student under the supervision or mentorship of an
active scientist in the field, who should be the senior
author on the paper. Whenever possible, we hope to
include at least one paper by a student with each
issue, assuming the submission meets the
appropriate criteria and standards of the journal.
2a
We would like to encourage students at every
level from undergraduate, masters or PhD training
to consider submitting their work for review. It is
our hope that supervisors/mentors of these future
leaders in the marine animal field will support and
promote this initiative; which will give students at
all levels the opportunity to gain experience in
publishing their research work.
Dr Carin Wittnich
Editor-in-Chief, JMATE
JMATE
Vol 7, No 1, 2014
Printed in Canada
Journal of Marine Animals and Their Ecology
Copyright © 2008 Oceanographic Environmental Research Society
Letter to the Editor
Citizen Scientists Playing a Role in Saving Threatened
Species - Science and Reality Coming Together
Michael Belanger
The Oceanographic Environmental Research Society, Barrie, Ontario, Canada L4N 2R2
I found it interesting and timely to read Dr
Vecchione’s article in the December (2013) issue of
JMATE (volume 6, issue #2) entitled “Prospects and
challenges in monitoring the seahorse
population of South Carolina, USA” where Dr
Vecchione discusses the need for the involvement of
citizen scientists (recreational scuba divers) to assist
with the documentation of seahorse
populations (3). A few months later, after the
JMATE article was published, an article was
published in the Globe & Mail (May 22, 2014) that
described how two citizen scientists (scuba divers)
discovered a rare seahorse in Nova Scotian waters
(2).
Over the past few years in Canada, there has
been an alarming number of cutbacks in monitoring
and research programs resulting in more than 2,000
scientists losing their positions (1). With fewer
scientists working on various projects, these two
publications (one publishing scientific data and the
other reporting on ‘soft’ information) both reveal the
need for collaboration between research and citizen
scientists especially in the area of marine
research which is severely underfunded and often
difficult to perform.
I believe it is admirable and critical that
JMATE continues to publish articles such as Dr
Vecchione’s where reality proves that publishing
research data that is broad and multi-disciplinary
(which is often overlooked) does facilitate the
exchange of essential information.
Received June 7, 2014; Accepted June 9, 2014
Correspondence: Michael Belanger
Phone: 416-565-2277
Email: oersdo@gmail.com
3
References:
1.
CBC News- Science and technology. Research
cutbacks by government alarm scientists.
http://www.cbc.ca/news/technology/researchcutbacks-by-government-alarm-scientists1.2490081. Accessed on May 30, 2014.
2.
Globe & Mail. Two divers praised for rare sea
horse sighting off Nova Scotia. http://
www.theglobeandmail.com/news/national/two
-divers-praised-for-rare-seahorse-sighting-offnova-scotia/article18813125/.
Accessed May 30, 2014.
3.
Vecchione A. Prospects and challenges in
monitoring the seahorse population of South
Carolina, USA. Journal of Marine Animals
and Their Ecology. 6(2):6-11. 2013.
JMATE
Journal of Marine Animals and Their Ecology
Copyright © 2008 Oceanographic Environmental Research Society
Vol 7, No 1, 2014
Printed in Canada
Brief Communication
The mesoparasitic copepod Pennella balaenopterae and its
significance as a visible indicator of health status in dolphins
(Delphinidae): a review
Anna Vecchione1 and Francisco Javier Aznar2
1
Research Director, Sea Life Conservation and Arts, Charleston, South Carolina, USA
Unitat de Zoologia Marina, Institut Cavanilles de Biodiversitat i Biologia Evolutiva,
Universitat de Valencia, PO Box 22085, Valencia 46071, Spain.
2
of other copepods generally involves intermediate hosts,
the intermediate host for P. balaenopterae and the
number of moults required to reach the infective
immature stage are unknown (21). Very little
information is currently available on this parasite,
particularly on its life history traits. It is known to
survive in cold waters and significant information on its
morphometry and anatomy has been published (1, 7,
24).
P. balaenopterae is a sexually dimorphic species
and the female undergoes morphological changes at
different stages of infestation. Only fertilized females
parasitize cetaceans (5). Three main body parts (Figure
1) have been described: the cephalothorax, trunk, and
abdomen (1). However, the morphological
characteristics of the cephalothorax, apical papillae, and
holdfast horns are inconsistent among this species and
can even vary substantially between specimens of a
single species (19). For example, the number of holdfast
horns can be either 2 or 3, with higher numbers
corresponding to greater embedding ability. This
variation in horn number appears to be associated with
the need for greater grip, based on observed differences
in the levels of host penetration (1). Furthermore,
differences in the lengths of the abdomen and trunk vary
depending on the age of the parasite. Adult copepods
have photoreceptors and antennae, or so-called
cephalothoracic papillae, which have different shapes
and outlines at the anterior end (19). The length and
thickness of the first antenna were initially considered
useful characteristics to distinguish between the two
copepod species P. balaenopterae and P. filosa.
However, recent studies have shown results obtained
using these variables as a species indicator may be
ambiguous (19). In the mature parasite, the function of
the second antenna is not clear, although it may be of
use during attachment in the infective stage of the
Abstract
Crustacean species of the genus Pennella (Copepoda,
Siphonostomatoida, Pennellidae) are the largest mesoparasites
known to infest cetaceans and marine bony fishes. Pennella
balaenopterae is the species most commonly found semi-buried in
the integument of members of dolphins (Delphinidae) and baleen
whales (Balaenopteridae). This mesoparasite appears as a tag or
filament hanging from the host’s skin and is detectable even in freeranging cetaceans. Under normal conditions, penellid infestations
are limited to only a few individuals per host. However, increased
numbers of infestations by this epizootic crustacean have been
reported recently. Here, the literature available on this parasite is
reviewed. Since more numerical data are available for dolphins than
the baleen whales, this paper focuses on the significance of Pennella
balaenopterae infection in dolphins, and its possible value as an
indicator of compromised health status. [JMATE. 2014;7(1):4-11]
Keywords: Parasite, Cetacean, Immune System, Infestation,
Contaminant
Introduction
The mesoparasitic copepod Pennella
balaenopterae, identified by Koren & Danielssen in
1877, has a broad biogeographic distribution. It has been
found in the waters of Iceland, the Northeastern Atlantic
Ocean, the Mediterranean Sea, the Antarctic, and the
Northern Pacific (1, 5, 12, 15, 24, 29). The sei whale
(Balaenoptera borealis) and the minke whale
(Balaenoptera acutorostrata) are the most common final
hosts of P. balaenopterae. Nonetheless, infestation can
also occur in dolphins, such as the striped dolphin
(Stenella coeruleoalba), and has been reported in the fin
whale (Balaenoptera physalus) and rarely in pinnipeds
(5, 12, 14). Thus the baleen whales and dolphins are the
most common hosts reported to suffer these infestations.
Pennella balaenopterae (length, 8–32 cm) is the
largest mesoparasite detected in the body tissue of
cetaceans and is the only recorded copepod species that
parasitizes marine mammals (1). Although the life cycle
Received April 28, 2014. Accepted August 31, 2014
Correspondence: Anna Vecchione
Phone: 843-766-4422
Email: anna_vecchione@hotmail.com
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P. balaenopterae as an indicator of dolphin health
P. balaenopterae as a visual indicator of health status
in cetaceans
Monitoring the health of wild, free-ranging
cetacean populations is challenging, particularly when
live-capture options and laboratory resources are not
available or are limited. In contrast, the recording of the
numbers of skin parasites and their marks from a
distance could be a useful and simple tool to obtain a
rapid gross visual appraisal of health in free-ranging
cetaceans if a correlation exists between numbers of
visible parasites and overall health. Studies involving
photographic assessments of skin disorders in cetaceans,
such as common minke whales and white-beaked
dolphins, have demonstrated that the dolphins can
present clearly visible skin tattoos and keloidal lesions
caused by poxviruses and lobomycosis (also known as
lacaziosis) respectively (7, 10, 31).
Determining the biogeographic distribution of
skin diseases can also be achieved with the use of
photography, as revealed in studies conducted along the
west- and east-central coasts of Florida. Photographic
records of dolphins were utilized for health assessment
in certain dolphin populations (10, 23, 31). P.
balaenopterae infestation has the potential to also be
valuable in helping researchers establish dolphin health
status. Long-term, cumulative tendencies of P. balaenopterae infestation can be associated with a challenged
dolphin’s immune system. Under normal conditions,
infestation is represented by only a few parasites (Figure
2). However, research has shown that a large number of
epizootic crustacean infestations (Figure 3a, 3b) may be
associated with debilitating viral infections (4, 5). One
Figure 1: Pennella balaenopterae . A: general view of a
specimen; B: ventral view of the cephalothorax and swimming legs;
C: dorsal view of the cephalothorax showing cuticular
structure (arrow); D: abdominal plumes with different level of
branching (a: abdomen; c: cephalothorax; n: neck; o: ovisacs;
t: trunk). Reproduced with permission.
copepod (1).
When the parasite first attaches to the host, it
undergoes two phases of growth: growth of the anterior
end and growth of the posterior end (used for
reproduction). The posterior loose end of the gravid
female has a visible, long, string-like ovisac (1). In P.
balaenopterae, only the first naupliar stage (i.e. the
free-swimming larval stage) and the adult female stages
have been identified with certainty (24).
Although P. balaenopterae can infect dolphins and
baleen whales, reports of infection in dolphins have
increased in recent years and thus more data are
available for them. Therefore, this review focuses on
Pennella infections in dolphins and their possible utility
as a general indicator of health status.
Figure 2: Common minke whales with few parasites of P.
balaenopterae, identified by red circles. Reproduced with
permission Marie Louis/University of Iceland, Faxafloi Cetacean
Research.
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P. balaenopterae as an indicator of dolphin health
observed, but only in the epizootic sample. Both patterns
are compatible with the hypothesis that there was a short
-term increase in the probability of infestation of these 2
species because of the sudden rise in the population of
susceptible hosts (Table 1). The susceptibility was likely
caused by the immunosuppressive effects of viral
infection and the abnormally heavy loads of
polychlorinated biphenyls which were detected in
debilitated dolphins (5).
Other studies have demonstrated that most of the
cetaceans found stranded on Italian coasts between 1990
and 1997 had skin lesions due to P. balaenopterae
infestation (13, 32). This apparent increased
vulnerability to P. balaenopterae infestation has been
associated with the immunosuppressive effects of viral
infections and the unusual heavy loads of pollutants
found in debilitated dolphins. During the morbillivirus
outbreak, substantial depletion of lymphoid tissue was a
common finding in the analysed specimens (13). Several
dolphin specimens also contained high levels of
polychlorinated biphenyls, which are known to be a
major contributing factor to immunosuppression (2, 5).
During post-mortem visual examination and
surgical removal of the parasite, some characteristics and
morphological variations of the holdfast horns of P.
balaenopterae were representative of resistance
encountered in the host. Specifically, the shape and
length of holdfast horns can vary. When P.
balaenopterae resides in a cetacean’s soft blubber, its
lateral horns are very long, whereas when it is found in
the dense muscular layer below the blubber, its horns are
relatively short (19). It is not clear whether there is a
correlation between the host’s immune reaction to the
parasite and the length of its holdfast horns. However,
successful infestation is an indication of the ability of P.
balaenopterae to bypass the host’s immune system,
thereby embedding the anterior end completely into the
host tissues. The parasite probably perforates the host’s
skin with the second antennae during the copepodid
phase. Infestation progresses and anchorage of the
anterior end is increased through the growth and grip of
the holdfast horns. The cephalothorax of P.
balaenopterae penetrates into the blubber, bypassing the
host innate immune reaction and establishing an
effective infestation. In some stranded cetaceans,
granulomatous processes and secondary infections have
been detected at the site of P. balaenopterae infestation.
a
b
Figure 3: (a) View from lateral aspect of a heavily parasitized
Risso’s dolphin (Grampus griseus) from the Western
Mediterranean; (b) Close-up of in situ individuals of P.
balaenopterae from the heavily parasitized Risso’s dolphin from
the Western Mediterranean. Reproduced with permission from the
Marine Zoology Unit, University of Valencia.
example is the high mortality reported in a cetacean
morbillivirus outbreak in the 1990s in the western
Mediterranean Sea. In the affected species, striped
dolphin infestations of P. balaenopterae, and also those
of the phoront cirriped Xenobalanus globicipitis, were
commonly identified (4, 5). Data were obtained from
records of striped dolphins stranded along the
Mediterranean central coast of Spain from 1981 to 2004
(n = 136) (5). In these dolphins, prevalence, intensity of
infestation, size and reproductive status of the
commensal barnacle Xenobalanus globicipitis and
Pennella balaenopterae were evaluated (Table 1).
Results indicated that a significant increase of
prevalence had occurred in the epizootic dolphin sample
(n= 62), compared with the pre-epizootic (n = 12) and
post-epizootic (n = 62) samples. A significant association
between X. globicipitis and P. balaenopterae was also
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Pre-epizootic (n= 12)
(June-December 1981-1989)
P. balaenopterae as an indicator of dolphin health
Epizootic (n= 62)
(June-December 1990)
Post-epizootic (n= 62)
(June-December 1991-2004)
Pennella balaenopterae
Prevalence=25.0 %
Prevalence=40.3 %
Prevalence=12.9 %
V/M=9.6
V/M=17.7
V/M=18.8
K could not be calculated
k=0.17
k=0.028
Median intensity=4
Median intensity=2
Median intensity=15
Xenobalanus globicipitis
Prevalence=33.3 %
Prevalence=58.1 %
Prevalence=30.6%
V/M=31.7
V/M=22.0
V/M=72.3
k=0.109
k=0.27
k=0.073
Median intensity=6
Median intensity=6
Median intensity=10
n=number of dolphins in each sample, V/M=variance to mean ratio, k=parameter of negative binomial
distribution (Aznar et al., 2005).
Table 1. Infestation parameters of the mesoparasitic copepod Pennella balaenopterae and the phoront barnacle Xenobalanus
globicipitis in striped dolphins (Stenella coeruleoalba) stranded along the Mediterranean coast of Spain in the period 19812004. Dolphins are divided into 3 groups, i.e. those that suffered a viral epizootic disease in 1990, and those stranded before
and after this event. A significant change of prevalence of both species was observed during the epizootic event.
In particular, granulomatous or purulent inflammatory
responses observed around chitinous remnants of the
parasites are occasionally accompanied by opportunistic
fungal and bacterial pathogens (22). During the
development and growth of P. balaenopterae, the host
immune system appears to allow for parasite survival.
However, it remains to be established how the dolphin’s
immune system reacts to infestation and the parasite’s
fast growth rate. These factors may be important aspects
that influence the outcome of the disease.
Detrimental changes in the immuno-physiological
properties of marine mammals caused by environmental
contaminants and the subsequent inefficient immune
responses to pathogens have been demonstrated using
assays for molecular biomarkers and clinical chemical
parameters as well as other laboratory-based methods (6,
18, 20, 34). Inefficient immune responses caused by
substantial depletion of lymphoid tissue have been observed in striped dolphins, bottlenose dolphins (Tursiops
truncatus) and Risso's dolphins (Grampus griseus) with
P. balaenopterae infestation (13). Such lymphoid
depletion might be related to reduced production of
cytokines, which are important for both innate and adaptive immunity. Cytokines such as IL-1, IL-2, IL-4, IL-7,
and IL-9 are responsible for the proliferation and
differentiation of T-cells, B-cells, and macrophages,
which are involved in acquired immunity. IL-3,
granulocyte macrophage colony-stimulating factor,
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P. balaenopterae as an indicator of dolphin health
encounters are a common occurrence during these
expeditions. Some of these organizations are willing to
volunteer and consequently collaborate with local
scientists to report any sighting of Pennella on the
dolphins they encounter. Data obtained by these
collaborations with community-based organizations will
help to establish the prevalence of P. balaenopterae in
local dolphin populations.
In addition to the immunodeficiency caused by
pollutants and morbillivirus, another possible suggested
explanation for the increased P. balaenopterae infection
rate is that sickness-induced lethargy may have impaired
breaching or fast movements that would normally have
shaken off the parasites (4). Abnormal lack of energy is
frequently associated with illnesses. Consequently,
behaviours that allow infestation of a large number of P.
balaenopterae on the host are clearly an indicator of
compromised health.
The presence of a visibly high number of skin
parasites and diseases is a useful signal for a preliminary
health appraisal of wild free-ranging dolphins.
Monitoring the skin health of cetaceans using
photographic identification is feasible, effective, and non
-invasive, despite concerns associated with partial body
exposure, which could impair complete skin evaluation
(7). This concern is dependent on breaching behaviors,
where, for some, full body assessments may be done if
breaching is significant as shown in Figure 4. Visual
surveillance of skin diseases during assessment of
cetacean health is of particular relevance, considering
and IL-5 are involved in the proliferation and
differentiation of neutrophils, eosinophils, macrophages,
and mast cells, which are implicated in innate immunity
(33). As cetaceans share common characteristics in the
structure, and possibly function, of cytokines with those
of other mammals, cetacean exposure to pollutants
probably has the same debilitating effect on cytokine
production and function as observed in other mammalian
species, consequently exerting a negative influence on
the immune reaction to any pathogen (6, 32, 33). Severe
P. balaenopterae infestation (Figure 3a, 3b) can lead to
the death of dolphins due to malnourishment, toxicity
caused by tissue necrosis or secondary infections at the
site of parasite invasion (32). Morbillivirus-infected,
pollutant-immunosuppressed, and heavily
Pennella-infested dolphins predictably have a very small
chance of survival, as evidenced by the dolphins
stranded along the Mediterranean coasts between 1990
and 1991 (2, 5, 11, 13).
Worldwide anthropogenic contaminants are
reaching threshold levels, leading to immunosuppression
in marine mammals. In Atlantic bottlenose dolphins off
the coast of Charleston, South Carolina, USA, chronic
exposure to high levels of perfluoroalkyl compounds
(PFCs) has caused changes in immunological parameters
for both innate and adaptive immunity (17, 18). Visible
skin diseases, such as lobomycosis, have been reported
to be at epidemic proportions in Atlantic Ocean coastal
waters, particularly among dolphins in the Indian River
Lagoon of Florida. Localization of the disease to the
southern portion of the lagoon indicated that exposure to
environmental stressors could be responsible for the high
prevalence of the disease (26). While there are no
published reports of P. balaenopterae infestation in
dolphins inhabiting the coastal waters of the Indian
River Lagoon and Charleston, South Carolina, these
populations of free-ranging dolphins are susceptible to
morbillivirus infection like the dolphin populations of
the Mediterranean Sea (3, 27). Further investigation of
the presence of P. balaenopterae in Atlantic Ocean
coastal waters is needed to understand the life cycle,
ecology, and dynamics of this puzzling parasite, and its
relation to pollutants and viral infections.
Lack of scientific data is most often attributed to
absence of financial resources. However, in Charleston,
South Carolina, several nature-based organizations
provide coastal expeditions for tourists. Dolphin
Figure 4: Risso’s dolphin, Grampus griseus from the Western
Mediterranean showing that even ventral surface parasites can be
identified with breaching behaviors. Reproduced with permission.
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P. balaenopterae as an indicator of dolphin health
the fact that marine mammals are representative
sentinels of the health of oceans (8).
2.
Conclusion
The presence of a large number of epizootic
parasites or mesoparasites such as P. balaenopterae on
dolphins is a possible indicator of biological or
environmental changes in their ecosystem, which are
affecting the dolphins’ immune responses. The body
structure and the typical dorsal or lateral location of P.
balaenopterae are ideal for photographic identification.
To the viewer, the parasite appears as a tag or filament
hanging on the dolphin’s skin. Under normal
circumstances, infestation is limited to only a few
individuals per host. However, an increased number of
P. balaenopterae could serve as a marker for other more
serious health issues such as an imbalanced immune
system and secondary infections at the site of parasitosis,
as shown by events documented during the 1990 dolphin
morbillivirus outbreak in the Mediterranean Sea.
In conclusion, increased parasitosis of P.
balaenopterae represents a significant visible indicator
of dolphin health status. Consequently, the presence of
this parasite should be monitored widely, notably in
areas where dolphin populations have been exposed to
toxic compounds and morbillivirus outbreaks, such as
areas surrounding the Southeast US coast and, in
particular, the coastal waters of South Carolina.
3.
4.
5.
6.
7.
8.
Acknowledgments
We wish to thank Dr Paulo Abaunza Martinez, Chiara Bertulli, Marie Louis, Igor Kiporuk for providing figures and photographs. Also, the first author is grateful to Concetta Dorio Tornincasa for her long-term support, Dr Giannina Convertino and Brian
O’Neal for help in editing the manuscript, and Dr Koen Van Waerebeek for his friendship and constructive criticism. Project funding
was provided by Sea Life Conservation and Arts; Project CGL201239545 from the Ministry of Economy and Competitiveness, Spain;
and Project PROMETEO/2011/040 from the Generalitat Valenciana, Spain. There is no conflict of interest to declare.
9.
10.
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JMATE
Journal of Marine Animals and Their Ecology
Copyright © 2008 Oceanographic Environmental Research Society
Vol 7, No 1, 2014
Printed in Canada
Case Report
Recovery from severe cutaneous injury in two free ranging
bottlenose dolphins (Tursiops spp.)
Michael I Bossley1 & Michelle A Woolfall2
1
2
Whale & Dolphin Conservation, Adelaide, South Australia.
School of Animal & Veterinary Sciences, University of Adelaide, South Australia.
Abstract
Bottlenose dolphins (Tursiops spp.) inhabiting the Port
Adelaide estuary in South Australia have been studied since 1989.
Here we present the cases of a female and calf which sustained
severe localized burn-like injuries of unconfirmed aetiology. The
remarkable recovery of the two dolphins was carefully documented
photographically from the time of first sighting (April 11, 2010)
through to the present (June, 2014). No invasive tissue sampling to
investigate pathology was undertaken, nor was any form of
medication administered. This paper chronologically presents
images and commentary of the phases of wound healing seen in
these two unique cases. The unaided recovery of these dolphins
from severe trauma has implications for evaluating the need for
veterinary intervention in these animals in certain situations. In
addition, the topics of dolphin behaviour and the value of citizen
science in documenting the events are discussed.
[JMATE. 2014;7(1):12-16]
Keywords: Cetacean, injury, integument, intervention, healing,
Tursiops
Introduction
Bottlenose dolphins (Tursiops spp.) inhabit the
Port Adelaide estuary in South Australia. These dolphins
have been studied since 1989 using photo identification
techniques to monitor the behaviour and health of individuals. There are approximately 30 resident dolphins
and numerous others that visit the area, which is close to
a city of a million people and thus subject to numerous
human impacts. These impacts include habitat damage
caused by pollution and direct impacts on the dolphins
from deliberate attack and accidents. In 2005, the South
Australian government declared the waters around the
Port Adelaide estuary a dolphin sanctuary. Two of the
resident dolphins are an adult female (F351, estimated to
have been born in 1992) and her male calf (M501, born
in March 2009). F351 had previously given birth to two
calves (a male in 2002 and a female in 2006) which have
remained in the estuary. F351 is identifiable by the shape
Received February 18, 2014; Accepted September 19, 2014
Correspondence: Michael Bossley
Whale and Dolphin Conservation, PO Box 720, Port Adelaide BC, Port
Adelaide, South Australia, Australia 5015.
Phone: + 61 8 84403700
Email: mike.bossley@whales.org
and configuration of her dorsal fin. F351 is known
locally as “Wave” and her calf (M501) as “Tallula.”
At some time between the 2nd and 11th of April
2010, the two dolphins received severe, burn-like skin
injuries, F351 on her right flank and her calf M501 on
his left flank. The aetiology of these injuries is
unknown, but most marine mammal experts who
viewed photographs of the injuries suggested sunburn
arising from being stranded as the most likely cause. We
have no way of verifying this aetiology but the local
geography includes extensive intertidal mudflats which
could increase the potential for standings.
Communication with port authorities indicated no
evidence of chemical spills or other anthropogenic
incidents which might have caused the injuries. The
recovery of the two dolphins from this severe trauma
was documented photographically from the time of first
sighting (April 11, 2010) through to the present (June
2014). However, no invasive tissue sampling to
investigate pathology was undertaken, nor was any form
of medication administered. This paper documents the
phases of wound healing seen in these dolphins.
Dolphins possess remarkable wound healing
abilities (1, 4). Many sustain large gaping wounds from
boat propeller strikes and predators (1). Nevertheless,
even severe wounds exposing deep muscle tissue have
been observed to heal almost completely within five
months (4). Humans sustaining similar injuries relative
to body size would likely encounter serious
complications without surgical or therapeutic
intervention. The wound healing physiology of the
bottlenose dolphin therefore represents an interesting
area of inquiry.
Case report
The two dolphins were sighted on April 2, 2010
with no abnormal lesions. Nine days later, on April 11,
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Recovery from cutaneous injuries in wild bottlenose dolphins
2010, they were observed with marked epidermal
sloughing, seen on F351’s right flank and on her calf’s
left flank (Figure 1a and 1b).
Figure 2: F351’s lesion on the 13th of April 2010. This figure
depicts the tissue lobulation described. Reproduced with permission.
sloughing from the lesion (Figure 3a). Pink tissue
discoloration could be seen caudally. In addition, the
cranial aspect had a diffusely nodular appearance (Figure
3b, arrow). By April 21, 2010 all areas that initially
appeared necrotizing and pale were now pink, which
was likened to the appearance of granulation tissue.
Lesion borders remained hyper-pigmented and there was
some yellow-brown discolouration to the wound cranially (Figure 3c, arrow).
Figure 1: Lesions on April 11, 2010 of (a) mother F351. (b) calf
M501. Arrows indicate the position of two small areas of
hypopigmentation and thickening on the calf’s dorsal fin.
Reproduced with permission.
F351’s lesions - These appeared more extensive
than her calf’s. At this time, she had a focally extensive,
well demarcated, elliptical lesion that resembled
ulceration and necrosis. This spanned across the dorsal
third of the body wall on the right side of the midline,
and extended cranially to the cervical region, caudally to
the peduncle, and tapered at both ends. The lesion was
widest beneath the dorsal fin. Epidermis at the lesion
borders appeared hyper-pigmented (darkened), and a
white layer of what could have been necrotic epidermis,
dermis or underlying blubber was exposed (Figure 1a).
Two days later, this layer appeared raised and lobulated
(Figure 2), and on April 17, 2010, was seen to be
Figure 3: F351’s lesions (a) on April 17, 2010 showing sloughing of
pale white tissue and caudal granulation. (b) on April 17, 2010 there
was a nodular appearance to the cranial aspect of the lesion (arrow).
(c) on April 21, 2010 lesion displays border hyperpigmentation,
cranial discolouration (arrow), necrotic tissue and granulation.
Reproduced with permission.
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Recovery from cutaneous injuries in wild bottlenose dolphins
F351’s loss of body condition was apparent as
evidenced by prominence of ribs and angular flanks seen
on April 26, 2010. Lesion borders now appeared raised
and pale grey (Figure 4a and 4b). This tissue had
completely extended over the granulation tissue by
August 27, 2010, leaving two distinct white scars
(Figure 5a). Nodules that had been present cranially
completely regressed as the wound contracted (Figure 4c
and 4d). Comparison of the images in Figure 4
demonstrates the progression of re-epithelialization and
wound contraction.
Figure 5: (a) F351 on August 27, 2010 shows two distinct scars
have resulted along the right flank. These have remained similar in
appearance to date (June 2014). (b) A minor injury that F351
sustained in early 2011 (arrow) depicts the relative weakness of the
scar to surrounding normal tissue. Reproduced with permission.
as F351’s. While F351’s dorsal fin appeared normal, the
calf had two small focal areas of hypopigmentation and
thickening (interpreted as dermal sloughing) on his
dorsal fin (Figure 1b, arrows; 6b). Like F351,
hyper-pigmentation was observed along the borders of
sloughed and un-sloughed epidermis (Figures 1b, 6a,
6b), and a yellow-brown discoloration became
progressively evident over the surface of ulcerated tissue
(Figure 6b, arrow). By April 22, 2010, tissue resembling
blubber in the caudal aspect of the lesion was slightly
protruding from the level of surrounding healthy
epidermis and appeared broadly lobular (Figure 6c).
There was also a focal area of papular appearance
cranially (Figure 6c, arrow). By May 22, 2010, the entire
lesion had almost completely contracted, with pale grey
discolouration remaining on the affected regions for the
remainder of the year (Figure 6d). Scarring did not occur
in the same manner as with F351.
Behaviour and reproduction
F351 had regularly exhibited a behaviour known
as “tail walking” since 2008, a behaviour that appears to
have been learned from another local dolphin who had
spent time in a local dolphinarium. This was a high
energy behaviour which involved rising out of the water
until only her flukes were submerged and then crashing
back onto the water surface dorsal side first. She did not
perform this behaviour for three months after acquiring
her injury. While activities such as feeding did not seem
to change, certain social activities may have also been
altered as neither dolphin presented with rakings
(markings from social scraping of the teeth by other
dolphins) throughout the duration of their healing
processes. The minor lesion previously discussed
(Figure 5b) was the first potential raking since the major
injury, which had by then reduced to a scar. There did
not appear to be a change in home range or frequency of
Figure 4: F351’s lesion on (a) April 26, 2010. (b) May 7, 2010.
(c) May 14, 2010. (d) July 30, 2010. Comparison of the four
images demonstrates the progression of re-epithelialization and
wound contraction. Reproduced with permission.
In early 2011, F351 sustained an injury resembling
tooth rakings from another dolphin. In reference to
Figure 5b, the scar tissue appeared to be more readily
damaged than surrounding epidermis. This minor injury
healed without complication. It would appear the
existing scar will remain for the life of the animal.
For one year following the appearance of the
injury, F351’s dorsal fin leaned approximately 10° in the
direction of the wound. The fin has since returned to
normal. The calf did not display this response.
M501’s lesion - The calf was a dependent 13
month-old (born March, 2009) when injured, yet the
stages and timing of wound healing appeared similar to
F351’s. On April 11, 2010, the calf had an irregular
oblong streak resembling ulceration and necrosis
dorsally, spanning from the blowhole to the caudal
insertion of the dorsal fin, situated along the midline
cranially, and curving to the left of the midline caudally
(Figure 6a). This lesion was not as sharply demarcated
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Recovery from cutaneous injuries in wild bottlenose dolphins
granulation tissue gradually begins to fill the wound in
order to aid in volume restoration while reconstructing
the blood supply to the site of injury. Within the first
week of the injury, non-viable tissues, including the
transposed blubber, are naturally debrided (4).
For both dolphins, there was hyper-pigmentation
observed along the borders of sloughed epidermis. In
terrestrial mammals, this is a result of inflammation
involving some degree of chronicity. An abundance of
blubber infiltration into the exposed areas of dermis is
consistent with normal healing, and would have brought
immune mediators to the affected site along with
additional insulation and protection to underlying tissue
(4). Once the underlying granulation bed was complete,
non-viable tissue that had lost vascularity and was
necrotizing, including transposed blubber, would be
passively sloughed. The aetiology of the yellow-brown
discolouration on both dolphins was unknown. It may
have been a result of colonization by environmental
bacteria, protozoa and/or fungi. The nodular appearance
of F351’s lesion (Figure 3b, arrow) was also of unknown
aetiology. The focal area of papular appearance
(Figure 6c, arrow) on M501’s lesion may have signified
a hyperplastic process or simply finer lobulation of the
blubber that appeared broader caudally. Nevertheless,
these lesions proceeded to regress without obvious
complication or human intervention. Despite exposure to
an industrially polluted environment, it appears the
dolphins’ immune mechanisms against environmental
pathogens were adequate.
The lack of pigmentation in F351’s scars may
predispose her to predation, reduced heat absorption in
colder weather, and damaging ultraviolet radiation. Due
to the rarity of depigmentation or albinism in cetaceans,
it is difficult to ascertain the significance of these risks.
The survival of F351 with her dependent calf under the
circumstances was remarkable. Given the stress
associated with attempting to sample and/or treat free
ranging dolphins, these observations suggest close
monitoring of injuries should be undertaken and
intervention only instigated as a last resort. A case of
similar significant skin lesions of unknown aetiology in
a wild bottlenose dolphin calf was studied in Monterey
Bay (U.S.A.) (2). The Monterey Bay dolphin suffered
severe ulcerative tissue necrosis, emaciation and swam
abnormally. The calf survived this condition and
Figure 6: Appearance of M501’s lesion on (a) April 11, 2010. (b)
April 6, 2010 showing hyperpigmentation of lesion borders and
yellow-brown discoloration of ulcerative tissue (arrow).
(c) April 22, 2010 showing an area of papular appearance (arrow)
and protruding blubber. (d) May 22, 2010. Reproduced with
permission.
bow riding associated with the injury.
F351’s first three calves, including M501, survived
to weaning and are regularly sighted in the dolphin
sanctuary today. However, in the years following
F351’s injury, a fourth calf was born in February 2012
and died five days later. On September 22, 2013, F351
was sighted holding a fifth calf that was likely to have
been stillborn or died immediately after birth. It is
unknown whether the deaths of F351’s calves in 2012
and 2013 were related to the injury described in this
paper.
Discussion
This report adds to the small body of literature on
the unassisted recovery from severe trauma of bottlenose
dolphins in the wild. In addition, it highlights the
extraordinary capacity of these animals to not only
recover but also manage the extra energy demands of
providing for a dependent calf at the same time.
Within the first day of a dolphin sustaining
cutaneous injury, blubber from surrounding tissue
migrates over the exposed wound surface (4). The
blubber consists of many collagen bundles, elastic fibres
and adipocytes. It is connected to underlying
musculature by the subcutis, a loose layer of connective
tissue (3). This blubber layer is a complex structure that
undertakes coordinated cellular rearrangements in
healing to form new tissue using adipocytes, collagen
and elastic fibres (4). Two days after injury, pink
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Recovery from cutaneous injuries in wild bottlenose dolphins
appeared to be improving in subsequent sightings,
reinforcing the outstanding healing abilities of these
cetaceans (2).
Subsequent to the events described above, in
December 2013, another dolphin U378, a subadult of
unknown gender presented with a set of lesions visually
similar, but less extensive, to those described for F351
and M501. The recovery process proceeded along
identical lines to that for F351 and M501, and we
assume the same aetiology for all three animals.
The unassisted recovery of these dolphins has
implications for triage decision making in relation to
dolphins suffering natural and anthropogenic injuries
and also for decisions concerning the advisability of
interventions.
Comprehensive monitoring of the healing process
of these dolphins was only possible through the
assistance of a group of dedicated volunteer
photographers (see acknowledgments section). Their
involvement highlights the growing contributions of
citizen scientists armed with sophisticated photographic
equipment to field research.
3.
4.
Rommel SA and Lowenstine LJ. Gross and
microscopic anatomy. In: CRC Handbook of
Marine Mammal Medicine, edited by Dierauf LA
and Gulland FMD. 2nd edition. CRC Press, Boca
Raton pp. 139. 2001.
Zasloff M. Observations on the remarkable (and
mysterious) wound-healing process of the
bottlenose dolphin. Journal of Investigative
Dermatology 131: 2503-2505. 2011.
Acknowledgements
Special thanks to the many biologists and veterinarians who
provided their advice on the possible aetiology of these lesions. In
particular we would like to thank Dr P Duignan and Dr J Geraci for
their very helpful assistance. We are also grateful to the following
photographers for permission to use images in this paper: B
Saberton (Figures 1a, 2, 3a, 4c, 6d, 5a), M Boorman (Figures 1b, 3b,
4a, 6a, 5b), O Wieczorek (Figure 4d) and P & D Huxtable (Figure
4b, 6b, 6c) who were also the first to report the dolphins’ injuries.
Without their assistance the documentation of the recovery of these
dolphins would have been incomplete.
References
1.
2.
Bloom P and Jager M. The injury and subsequent
healing of a serious propeller strike to a wild
bottlenose dolphin (Tursiops truncatus) resident in
cold waters off the Northumberland coast of
England. Aquatic Mammals Journal 20(2): 59-64.
1994.
Riggin JL and Maldini D. Photographic case
studies of skin conditions in wild-ranging
bottlenose dolphin (Tursiops truncatus) calves.
Journal of Marine Animals and Their Ecology
3(1): 5-9. 2010.
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Copyright © 2008 Oceanographic Environmental Research Society
Vol 7, No 1, 2014
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Review Article
A review of natural milk, commercial replacement formulas, and
home-made substitutes used in the care of rescued manatee calves
Nesime Askin1,2, Michael Belanger1, Carin Wittnich1,2,3
1.
The Oceanographic Environmental Research Society, Barrie, Ontario, Canada L4N 2R2
Department of Physiology, University of Toronto, Toronto, Ontario, Canada M5S 1A8
3.
Department of Surgery, University of Toronto, Toronto, Ontario, Canada M5S 1A8
2.
Abstract
In marine animal rehabilitation, people with a wide range
of education and experience must be knowledgeable on the
nutritional requirements of numerous marine species and especially
their young that may become abandoned. The Florida manatee
(Trichechus manatus latirostris) population has on average 10
calves per year requiring rehabilitation in that state alone. A review
was undertaken to evaluate the efficacy of natural manatee milk
(NMM) versus the various milk replacers or ‘home-made’ formulas
fed to rescued manatee calves with respect to maintaining growth
and adequate weight gain. Various databases (PubMed, Web of
Knowledge, Google Scholar, Internet, etc) were searched (19792013) for any literature describing the composition and feeding of
NMM and milk replacers to manatee calves. The Florida Fish and
Wildlife Conservation Commission (FWC) website was used to
identify the number of rescued manatee calves per year (9.67 ± 3.39,
mean ± SD) from 2008 through 2013. Of the 4 research articles
describing manatee milk composition and the use of various
commercial or ‘home-made’ formulas, only 2 articles compared
growth patterns with the type of milk formulas used. This scant
amount of published data alone reveals the need for further research
into the use of milk replacers versus NMM when feeding rescued
manatee calves. The lack of knowledge in the use of milk replacers
or their efficacy in maintaining healthy manatee calves underlines
the need for further scientific studies and published results to clarify
the proper nutritional requirements to successfully rehabilitate
rescued manatee calves and better insure their successful release
back into their natural environment. [JMATE. 2014;7(1):17-22]
Rehabilitation of these unweaned rescued calves would
involve additional specialized care to ensure successful
release (Figure 1). An important part of this involves the
proper feeding of the young manatee calf with some
type of milk replacement to maintain its health, nutritional needs, and growth if it cannot be re-united with
its mother. However, in general, it is often very difficult
to hand-rear rescued marine mammal young due to the
unique composition of their mother’s milk or various
changes of milk composition during lactation (4, 26).
At present, there is no commercial milk
replacement specifically developed for the feeding of
young manatee calves. As a result, numerous ‘home
made’ recipes or commercially available milk replacers
(Esbilac, PetAg, Il, USA, Multi-milk, PetAg, Il, USA)
are used which have not been scientifically validated to
be an acceptable milk replacer for young unweaned
manatee calves. Therefore, a review was undertaken to
compare the effects of feeding rescued manatee calves
commercial replacement or ‘home made’ formulas
versus natural manatee milk (NMM) on maintaining
their growth and weight gain.
Keywords: rehabilitation, weaning, orphans, Trichechus manatus
latirostris
Introduction
The Florida manatee (Trichechus manatus
latirostris) is an endangered marine mammal that is
threatened due to both natural (red-tide blooms, cold
water stress, diseases) and anthropogenic causes (water
craft collisions, net/fishing gear entrapment) (2,5,19).
Any of these causes might result in the death of lactating
female manatees which would necessitate the capture,
care, and weaning of orphaned manatee calves (2, 23).
Received May 19, 2014; Accepted August 18, 2014
Correspondence: Michael Belanger
Phone: 416-565-2277
Email: oersdo@gmail.com
Figure 1: A young unweaned manatee calf. Copyright OERS.
Reproduced with permission.
17
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Natural versus replacement milk in manatee calves
Results
Number of Rescued Manatee Calves
The Florida Fish and Wildlife Conservation
Commission website was searched to identify the
number of rescued manatee calves from 2008 to 2013
(23). The number of rescued manatee calves during that
time period was 44 (9.67 ± 3.39 per year, mean ± SD)
and ranged between 6% to 15% of the total number of
manatees rescued for each year. A large proportion of
rescued manatee calves that were rescued died (24 out of
44 or 55%) and this population illustrated a large
variability in mortality from year to year ranging from
30% to 83%. (Figure 2) There were no specific medical
reasons given for the deaths of these calves, though
cases of malnourishment, cachexia, disease, enteritis,
and anatomical anomalies have been previously
published (8, 13, 16, 24).
Figure 2: A young rescued calf being weighed . Copyright OERS.
Reproduced with permission.
Discussion
Variability Between Natural Milk and ‘Home-made’
Formulas
The health and growth of any species requires that
the specific nutritional needs be met and this is
especially true for their young (17). Specifically, in
manatees, it has been reported that the nutritional needs
of these calves has been challenging to provide and that
the success of the available commercial milk products
varies greatly (7). In mammals, these nutritional needs
are obtained through the suckling and digestion of maternal milk until the young animal is weaned (25). The
composition of maternal milk varies immensely
between species, again largely dependant on the
nutritional requirements of their young. Therefore, it is
not advisable to directly feed the young of one species
with maternal milk from another as this may cause
numerous problems including diarrhea or enteritis (22).
The variability of milk composition between species
(humans, cow, cat, dog, marine mammals, etc) is well
understood (25). Also, milk composition in marine
mammals varies greatly and is unusual in its
composition when compared to other mammalian
species, thus great care must be given when
rehabilitating the young of these species (4). As well, it
has been reported in female polar bears and dolphins
that their milk composition changes (fat, crude protein,
water) over time and seasonally depending on the
Scientific Publications Describing Various Feeding
Regimes
Various databases (PubMed, Web of Knowledge,
Google Scholar, Internet, etc.) were searched between
1979-2013 for research articles that described the
feeding and care of rescued manatee calves using NMM
or some type of milk replacer. Few articles were found
(n= 4) which included 2 articles describing the scientific
analysis and composition of manatee milk and 2 articles
describing the use of NMM versus various ‘home-made’
milk replacement formulas that measured weight gain
and body growth of manatee calves when fed either
NNM or ‘home-made milk replacers (1, 4, 15, 17). In
comparison, there were a minimum of 9 papers
reporting on the components of bottlenose dolphin
(Tursiops truncatus) milk with one paper as far back as
1940 (11, 26).
There were numerous web sites of organizations
that rehabilitate manatee calves which mentioned the use
of artificial milk replacers when feeding and caring for
this species of aquatic mammal. However, most did not
elaborate on the composition of the formulas used, the
specific brand of artificial milk replacers, or just stated
that it was a milk replacer developed within their facility
with no further description (10, 20, 27). These web sites
provided neither useable scientific data with respect to
NMM, artificial milk replacement, nor ‘home-made’
milk formulas and were therefore not used in this study.
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Natural versus replacement milk in manatee calves
activity of the mother, the age of their cubs or calves, or
lactation stage (9, 26).
Attempts to adapt milk from one species (known
as ‘home-made’ formulas) or artificial formulas
(commercially made) to feed the young of another
species have met with variable success (4, 6). In harbor
seals, no statistically significant differences in
survivability was detected between rehabilitated seal
pups that were fed a commercially available formula up
to 4 months of age to that of equivalently aged pups in
the wild (12). However, that same study identified that
rehabilitated pups had a steady decline in survivability
after 4 months of age. Another study that examined twin
gray seal pups that were fed a ‘home-made’ formula
revealed that there was no promotion of normal growth
or incremental weight gain when compared to wild pups
(22).
formula consisting of powdered soyabean milk and
butter, and Group III (n=2) were fed whole powdered
milk, butter including a banana, and all three groups had
access to various soft aquatic vegetation. All of these
calves exhibited an average weekly weight increase of 1
kg and a length growth rate of 1.4 cm which was
comparable to a calf nursing from its mother that was
reported earlier by Odell (14).
In 2012, Borges et al. described feeding 2 groups
of manatee calves the following diets for 24 months:
Group I (rescued calves, n=38) were fed various milk
replacers based on whole milk or soybean protein along
with supplements (vitamins) if required, and Group II
(captive born fed by their mothers, n=9) (6). Both groups
started at similar body weights (Group I- 34.6 kg, Group
II- 34.2 kg). Calves born in captivity alongside their
mothers had greater increases in their weights overall
and at the end of the study, Group I (abandoned calves)
had lower average body weights of 157 kg versus Group
II (with mothers) 218.7 kg. Body length was nonsignificantly different (Group I- 199.1 cm versus Group
II- 220.6 cm).
Composition of Manatee Milk
Since 1979, only 2 studies specifically examined
the composition of manatee milk (1, 17). The results of
those studies revealed that manatee milk had high
protein and lipid (mostly triglycerides) levels and low
levels of lactose which is similar to other marine
mammals. Interestingly, Bachman and Irvine also
reported the salt content of manatee milk and compared
that to bovine milk (1). Manatee milk had higher salt,
sodium, and chloride content, but lower calcium,
potassium and phosphorous concentrations when
compared to bovine milk. All of these manatee milk
components are significantly different from bovine milk
and therefore may play a crucial role on how well a
manatee calf may respond to certain ‘home-made’ milk
replacers or artificial formulas using bovine milk. For
instance, it is well known that manatee calves often suffer from diarrhea or enteritis which may be due to too
much lactose commonly found in ‘home-made’ replacers
which may use bovine milk in their recipes (22).
Various Formulations Unpublished
There are numerous facilities in Florida and
elsewhere (Sea World of Florida, Miami Seaquarium,
Georgia Aquarium, plus others) that have formulated
their own milk replacement formulas to rehabilitate
manatee calves depending upon their experience from
previously treated cases, knowledge/experience of their
staff, and other logistical considerations. As well, each
manatee calf may require a specific milk replacer
formula that has subtle changes made to it depending
upon numerous factors such as the calf’s nutritional
requirements (age, amount of weight loss), causes for
rehabilitation (trauma, hypothermia, etc), any nutritional
challenges the calf may have (cachexia), or available
ingredients. There are in existence many medical files
that are filled with valuable practical experience and
knowledge gained from the treatment of many manatee
calves, however few of these detailed treatments are ever
published. One such publication that contains this type
of information is a Masters thesis written by S.L.
Shapiro, however, it is extremely difficult to find either
online or within any type of depository (21).
There are a few online reports of facilities using
Body Growth and Feeding Rescued Manatee Calves
There are only 2 scientific papers that describe
feeding rescued manatees calves. In 1982, Best et al.
described the artificial feeding of 14 netted or abandoned
manatee calves that required care (4). Three separate
diets were used: Group I (n= 10) were fed using whole
powdered milk with butter, Group II (n=2) were given a
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Natural versus replacement milk in manatee calves
This issue should be addressed as scientific data
points to the possibility of large scale climatic events
(more strong violent storms) having dramatic effects on
certain marine mammal species which could result in
higher numbers of abandoned young or strandings
including manatees (18). Ensuring that abandoned
manatee calves are properly nourished during
rehabilitation through the use of natural milk, or a
scientifically proven milk replacement formula, would
increase the release of healthy fully grown calves back
into their natural environment and improve their natural
populations which play a role in future management
practices and policies.
commercially available milk replacement products (ie
Esbilac, PetAg, Il, USA) or ‘home made’ recipes,
however, they do not report any data such as body
growth or weight gain of the young calves (10, 20. 27).
This lack of information makes it difficult to substantiate
any scientific comparison examining the efficacy of
these products on rescued young manatee calves.
Conclusion
Rehabilitation facilities, aquariums, and zoos who
care for young marine mammals must be knowledgeable
on the unique dietary and nutritional needs of the various
species and this seems especially true for abandoned and
rescued manatee calves. However, the literature is
lacking in scientific studies detailing the nutritional
composition and benefits of using either milk replacers
or natural milk in manatee calve husbandry. Further
research in this area could contribute to better husbandry
practices and thereby help decrease the number of deaths
of abandoned manatee calves. (Figure 3)
Acknowledgments
The authors would like to deeply thank the reviewers for
their thoughtful and constructive criticisms that helped to improve
this manuscript.
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JMATE
Journal of Marine Animals and Their Ecology
Copyright © 2008 Oceanographic Environmental Research Society
Vol 7, No 1, 2014
Printed in Canada
Original Article
The ghosts of competition past: body size, trophic ecology, diversity
and distribution of global shark and pinniped species
Steven H. Ferguson*1, Jeff W. Higdon2, Ross F. Tallman1, Aaron T. Fisk3, Nigel E. Hussey3
1
Fisheries and Oceans Canada, 501 University Crescent, Winnipeg, MB, Canada, R3T 2N6
2
Higdon Wildlife Consulting, 912 Ashburn Street, Winnipeg, MB, Canada, R3G 3C9
3
Great Lakes Institute for Environmental Research, University of Windsor, Windsor, ON, Canada, N9B 3P4
Abstract
Pinnipeds (Carnivora: Mammalia) and sharks
(Elasmobranchii: Chondrichthyes) are both widely distributed
marine top predators that occupy similar ecological niches. We
examined global species diversity patterns of sharks (294 species)
and pinnipeds (34 species) as a function of latitude. We then used
body size and trophic position (TP) to test which relationship best
described the global distributional pattern of species richness
between the two clades: (1) pinniped as predator, (2) pinniped as
competitor, or (3) pinniped as prey. Ecological relationships
between the two species groups were diverse with some larger
sharks actively consuming pinnipeds and some smaller shark
species eaten by pinnipeds. Most sharks (81%) overlaped with
pinnipeds for TP (3.3-4.3), however most sharks are smaller than
pinnipeds (62% less than 128 cm maximum length), and only 8% of
sharks (24) are longer than the largest pinniped. Latitudinal
variation of sharks and pinnipeds indicated that species richness of
pinnipeds was bimodally higher at temperate latitudes and lowest at
equatorial latitudes between +40 and -40, the geographic region
where shark species richness was greatest. A comparison of the
three trophic models indicated that the predation model (sharks eat
pinnipeds) best fit the distributional pattern. Oceanic regions that
supported progressively more than 20 shark species resulted in
progressively fewer pinniped species. Results suggest that sharks
may exclude pinnipeds from much of the warmer oceanic waters
through direct predation. However, an alternate hypothesis that
differing thermal adaptations of the two clades may explain the
observed distributional pattern is not refuted by our results. We
discuss conservation implications associated with ocean warming
assuming shark species distribution will expand to higher latitudes,
likely at the expense of pinnipeds. [JMATE. 2014;7(1):23-39]
Keywords: Competitive exclusion, latitude, predation, seals, trophic
position
Introduction
Species of different taxonomic groups can
co-occur in similar habitats but may differ significantly
in competitive adaptations including morphology, life
history, and behavior (35,65,66). Competition has been
speculated to occur at cellular, individual, population,
species, and clade levels through species sorting (5,12,
Received April 4,, 2014; Accepted August 31, 2014
Correspondence: Steven H. Ferguson
Phone: 1-204-983-5057
Email: steve.ferguson@dfo-mpo.gc.ca
32,41,44,51). A possible example of competition at the
species or clade level would be between sharks
(Elasmobranchii: Chondrichthyes) and pinnipeds
(Carnivora: Mammalia) (10). Mammals, as endothermic
organisms, can occupy broader fundamental climate
niches than ectothermic vertebrates or plants because
they are able to buffer variation in climate (30). Thus,
fundamental niche of mammals is likely wide and less
subject to physiological constraints (18). The majority
of sharks are ectothermic (exception family Lamnidae,
heterothermic) while pinnipeds are endothermic and
therefore it would be expected that mammals are better
adapted to colder waters associated with high latitudes.
Sharks have a long evolutionary history with evidence
for temperature-dependent habitat preferences and more
recent adaptation to high-latitude environments (19).
Pinnipeds likely evolved in high-latitude environments
and subsequently evolved adaptations to warmer
environments (29,64). Sharks evolved adaptations to
estuarine, coastal and pelagic environments (7,11,48). In
contrast, pinnipeds have a much more recent
evolutionary history (17) and yet display a similar
diversity of habitat associations including estuarine
coastal and pelagic (64). Interactions between the two
taxonomic groups include predation by sharks on
pinnipeds (39,50), pinnipeds on sharks (1,16), and
evidence of competition for the same food sources
(2,59). However, little consideration has been given to
clade interactions and whether competitive exclusion
occurs or whether past competition (ghosts) are
responsible for the current distribution (10,14). Have the
two taxonomic groups radiated to occupy all marine
habitats or does one group competitively exclude the
other?
Previous research indicated that pinnipeds are
largely relegated to high-latitude environments
23
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Shark and pinniped latitudinal species diversity
compared to the relatively warm-water habitats of sharks
(10). Here we explore spatial patterns to see whether
they are consistent with a possible competitive
mechanism by first comparing latitudinal species
diversity of sharks and pinnipeds to test whether their
global distribution differs. Next we use trophic position
(TP) and body size (length) to define whether indirect
(competition for the same food) or direct (predation by
sharks on pinnipeds and pinnipeds on sharks)
interactions best fit the global pattern. Latitude is a
robust habitat surrogate since it represents a number of
environmental gradients that change relatively
consistently from equator to pole, including temperature,
primary productivity, seasonality and predictability
(3,23,24,33). Finally, we consider how shark and
pinniped global patterns in species diversity relates to
conservation under a scenario of warming global ocean
temperatures.
female and male/unsexed total length was available for
94 species, and the two measures were significantly
correlated (r = 0.95, n = 94, P < 0.0001). Maximum total
length (male/unsexed) and commonly attained total
length (male/unsexed) was available for 83 species and
the two measures were again highly correlated (r = 0.95,
n = 83, P < 0.0001). Elasmobranch taxonomy is in a
state of constant flux, with > 1,100 species currently
recognized (21). We examined sharks only in the
“superorder” Selachimorpha (8 orders of sharks), and
excluded the superorder Batoidea with greater than 500
described species (3 orders; 17 families; eg skates, rays).
A total of 495 shark species are currently recognized
compared to 494 included in FishBase (21,28).
For pinnipeds, data were compiled from a variety
of sources including Bininda-Emonds & Gittleman for
body length, Pauly et al., for TP, and Higdon and IUCN
for global distribution and are detailed in subsequent
sections (4,18,38,42). Length data available from
Bininda-Emonds and Gittleman includes both male and
female standard length in addition to the species average
values which we used (4). All measures are highly
correlated. For females and males, r = 0.82, n = 34
including the two Pusa species which were excluded
from latitudinal analyses, P < 0.0001. Correlations
between species averages and the male or female length
values were even stronger, with r = 0.97 and r = 0.94,
respectively. Some pinniped species are highly sexually
dimorphic, but using male values instead of species
averages would have had no significant influence on our
classification. For example, if we used male length, the
minimum length would be 129.3 cm, instead of 127.7
using the species average (minimum female standard
length was 120 cm). Our data files are available upon
request to the authors.
Materials and Methods
Data: We collected TP, body size, and range data on
globally distributed shark species from the online
version of Fishbase from data collected between
December 2009 and March 2010 (28). We used the longest of five length measures that are available in
FishBase. Not all measures were available for all species
and no species had more than three length variables
(n = 135). Two variables were available for 140 species,
and 19 species had only a single length variable.
Maximum reported total length for females was
available for 99 species, and this value was used for 63
species (longest length reported). Most species (288 of
294) had data for maximum reported length for male or
unsexed specimens, and we used this value for 223
species. An additional six species had equal values for
both of these variables, that is, both measures were the
same, and this was the length value used. Commonly
attained total length for male or unsexed specimens was
available for 82 species but was only used for one
species. Commonly attained total length for female
specimens was only available for two species and was
not used for any species, as it was not the longest value
available. Standard length of male or unsexed specimens
was reported for a single species only, and this was the
length value used as it was the only one with data. Both
Trophic relations: Sharks were classed as
pinniped-predators, pinniped-prey, or
pinniped-competitors (with some overlap) based on TP
and body size (length). For diet characterization, Cortés
(15) included 17 shark species with marine mammal
remains recorded in their diets, with a calculated
minimum TP of 4.16. Nine of the 17 species overlapped
with pinniped TP (range 3.3-4.3, (61)), and the other
eight were higher than the maximum pinniped TP value
(4.3). Using a TP cutoff of 4.3 (> than maximum
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Shark and pinniped latitudinal species diversity
pinniped TP) would underestimate the number of
pinniped-predators. We used 4.16 as the TP cutoff to
identify pinniped-predators but also examined the effect
of a less conservative threshold by comparing results
with a TP value of 4.0 which was the mean pinniped TP,
as the cutoff. TP assessments for sharks and pinnipeds
likely are underestimated based on coarse scale grouping
of prey items and associated bias in the TP calculation,
but values derived from Pauly et al., and Cortés for both
taxonomic clades were used based on their standardized
calculation and current availability of estimates for all
species (15,35,61).
Body length (see Data above) was also
considered in identifying pinniped-predator sharks. A
large number of shark species have high TP values
(≥ 4.0) despite being small in physical size. For example,
Saldanha catshark (Apristurus saldanha) has a maximum
length of 88 cm and a TP of 4.24. If length were ignored,
this shark species would be classified as a pinnipedpredator, despite being 30-40 cm shorter than the
shortest pinniped species. Of the 17 sharks with marine
mammal diet contributions listed by Cortés, species
range in length from 120 cm to 750 cm maximum length
(15). The shortest species, Portuguese dogfish
(Centroscymnus coelolepis), feeds mainly on fish
including other sharks and cephalopods, but also
gastropods and cetacean meat on occasion (13). They are
not known as a predator of pinnipeds, and are more
likely a scavenger of cetacean carcasses. If Portuguese
dogfish is excluded as a pinniped-predator, the next
smallest species with a marine mammal component to
the diet is 200 cm and is the Australian blacktip shark,
Carcharhinus tilstoni. This is the same as the median
length for pinniped species (200 cm, mean 211 cm) (4).
We therefore used 200 cm minimum length as a factor in
classifying sharks as possible pinniped-predators in
combination with the TP requirements noted above.
TP for 32 pinniped species ranged from a
minimum of 3.3 (Crabeater seal, Lobodon
carcinophagus) to a maximum of 4.3 (both Elephant
seals, Mirounga species) (61). Pinniped-competitor
sharks were all those species that overlapped with
pinnipeds in TP (3.3-4.3), regardless of length
(overlapping with pinniped-predators, as some sharks
could be both). Standard adult length (average of both
sexes) of pinnipeds ranged from 127.7 cm (Ringed seal,
Pusa hispida) to 372.5 cm (Northern elephant seal,
Mirounga angustirostris) (4). We classed sharks with a
maximum length ≤ 100 cm as pinniped-prey and this
also overlapped with the pinniped-competitor category.
Latitudinal distribution: For each shark species,
FishBase provides a link to AquaMaps, including the
point data used to produce the predictive maps (28,45).
AquaMaps uses point data from OBIS-SEAMAP and
GBIF (37, 49). The FishBase database also contains a
link to point data, and also provides locations from OBIS
and GBIF, in addition to other record locations specific
to the FishBase database. We extracted maximum and
minimum latitude, and the total number of point
locations, from both data sets, for all 494 shark species.
Pinniped distributions are better known than for most
shark species, with established distribution maps
(polygons) versus the point data available for sharks. A
number of sources provide distribution maps (38).
Recently, the IUCN produced a GIS dataset (ESRI
ArcView shapefile) of global mammal ranges that
contains distributional polygons for 34 extant pinniped
species (42). We digitized the ranges for two recently
extinct pinnipeds – Japanese sea lion (Zalaphus
japonicus) and Caribbean monk seal (Monachus
tropicalis) based on available historic information and
included them in the analyses (63). Both species are
extinct due to human persecution, and we assumed that
both would still exist in their native range had such
over-exploitation not occurred. Two pinniped species
the Baikal seal (Pusa sibirica) and Caspian seal (P.
caspica) are restricted to inland lakes/seas, where no
sharks are present, and were therefore removed from the
analyses (n = 34 pinnipeds total). For each pinniped
species we calculated the maximum northern and
southern latitudes of their range polygons. Each species
(sharks and pinnipeds) was assigned to 5o degree latitude
bands (n = 36) to plot latitudinal patterns in species
richness.
Testing for competition: Latitudinal variation in shark
and pinniped species diversity was examined via
regression analysis. Analyses using latitudinal bands can
be problematic due to statistical non-independence of
band values because each species often contributes to
more than one latitude band (31). If not addressed with
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the proper analyses methods, this spatial
pseudoreplication increases Type I error rates and
produces artificially small p-values. The band data are
spatially autocorrelated, and we therefore examined
latitudinal diversity patterns using generalized
least-squares (GLS) regressions with an autoregressive
first-order process (gls function in R package 'nlme')
(62). The standard linear model is of the form:
y = X*β + e, where y is the response variable; X is the
explanatory variable; β is the regression coefficient to
estimate; and e is the error term. The generalized-leastsquares (GLS) estimator of β = bGLS = (X'Σ−1X)−1X'Σ−1y,
with covariance matrix V (bGLS) = (X'Σ−1X)−1 and a firstorder auto-regressive process, AR(1), defined as
εt = φεt−1 + νs. The random shocks νs are assumed to be
Gaussian white noise and the covariance of two errors
depends only upon their separation in s space (27). The
models assessed the best fit relationships among the
three shark-pinniped groupings: shark predation on
pinnipeds, pinniped predation on sharks and competitive
interactions.
Results
Trophic relations: Among all 294 shark species, overall
length ranged from 20 to 2,000 cm and TP ranged from
3.06 to 4.6. Box-whisker plots of body length and TP
summarize differences between sharks and pinnipeds
(Figure 1). Body length and TP are both highly variable
in sharks. Some orders, for example the
Heterodontiformes and Pristiophoriformes, show little
variation in total length, while the Carcharhiniformes,
Lamniformes and Squaliformes show large variation.
This variation in body length observed by order equated
to larger variation in TP as would be expected. Pinnipeds
show similarly large variation in TP, but are generally
more similar in body length. Pinnipeds overlap, in both
size (length) and TP, with members of all eight shark
orders. Standard adult length (average of both sexes) of
pinnipeds ranges from a minimum of 127.7 cm to a
maximum of 372.5 cm. Mean average body length
(n = 32) is 210.7 cm, close to the median value of 200.3
cm. Mean TP for pinnipeds was 3.97, with the median
again similar (4.0). There were nine species with TP < 4
and 23 species with TP ≥ 4.
We found correlations between TP and body size
Figure 1: Box-whisker plots summarizing (a) body length;
(b) trophic position; (c) geographic range size of shark orders and
pinnipeds. The lower boundary of the box indicates the 25th
percentile, the line within the box marks the median, and the upper
boundary of the box indicates the 75th percentile. Whiskers above
and below the box indicate the 90th and 10th percentiles, points are
outliers. Body length plot excludes one 2000 cm long shark outlier
(Lamniformes). Order of shark groups (orders) follows that of the
Catalog of Fishes (21). Pinniped N = 32 for trophic position and
length, n = 34 for range size (varying data available from original
sources).
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across all sharks combined, but no correlations within
orders with the exception of Carcharhiniformes. TP and
body size were correlated for all pinnipeds minus three
that primarily consume invertebrates (molluscs, krill)
using 2-tailed test looking for positive or negative values
(Table 1).
In a comparison of sharks and pinnipeds we
observed size and diet overlap with a proportion of
sharks that overlap with pinnipeds for length and TP.
Most sharks (n=237, 81%) overlap with pinnipeds for
TP (3.3-4.3). Some (n=53, 18%) have a higher TP, only
4 species have a lower TP (< 3.3) than any pinniped
species. Despite the overlap in TP, most sharks are
smaller (shorter) than pinnipeds (<128 cm maximum
length) (n=181, 62%). Nearly one third (n = 89, 30%)
overlap in length and only 8% of sharks (n=24) are
longer than the largest pinnipeds (total length > 373 cm).
Due to a lack of field data, we inferred sharks as
pinniped-predators, pinniped-competitors, or pinnipedprey based on the combined metrics of TP and total
length. Using TP ≥ 4.16 and total length ≥ 200 cm as
thresholds, we classified 45 sharks as pinnipedpredators, including all marine mammal eating sharks
identified by Cortés (n = 16), excluding Portuguese
dogfish (C. coelolepis) (28). This included 18 sharks that
were also classed as pinniped-competitors. As a test of
sensitivity, we also used a TP cutoff of 4.0 (mean and
median pinniped TP) that resulted in 51 sharks being
classified as pinniped-predators (including 24 pinnipedcompetitors). A total of 228 shark species were
classified as pinniped-competitors, and 141 classified as
pinniped-prey (with overlap for 124 species in both
categories). If pinniped-prey were classified as those
smaller than 128 cm instead (minimum pinniped adult
length), an additional 40 shark species would be
considered pinniped-prey. Table 2 summarizes the
number of classified sharks by order and family.
Based on our definitions, there were 22 shark
species that were unclassified including Portuguese
dogfish, C. coelolepis. Generally the unclassified shark
species were between 100 and 200 cm, and thus not
classed as prey (> 100 cm), while their TP was too low
or too high to be classed as pinniped-competitors
(< 3.3 or > 4.3). The unclassified sharks were spread
among 11 families in six orders, including two families
(Stegostomatidae [order Orectolobiformes] and
Group
n
r
P
All sharks
294
0.21
< 0.001
Hexanchiformes
5
0.46
0.44
Heterodontiformes
7
-0.40
0.37
Orectolobiformes
21
0.023
0.92
Lamniformes
15
-0.35
0.21
Carcharhiniformes
158
0.39
< 0.001
Squaliformes
73
0.19
0.11
Pristiophoriformes
4
0.91
0.09
Squatiniformes
11
-0.52
0.11
All pinnipeds
31
0.19
0.31
Pinnipeds excluding three species
that mainly consume invertebrates
(TP 3.3-3.4)
28
0.62
< 0.001
Table 1: Correlations between total length and trophic position (TP)
for sharks and pinnipeds.
Cetorhinidae [order Lamniformes]) with only one
species each. Nine of the 22 are > 100 cm but < 128 cm,
the minimum pinniped length (and would be included as
pinniped-prey using an alternative cutoff, above).
Another 11 are 130 to 175 cm, these generally have high
TP, 4.31 to 4.5, except for one with TP = 3.06. One large
species is included, the Basking shark (Cetorhinus
maximus), is 980 cm long but TP = 3.2, and therefore
lower than pinniped minimum. There are two other filter
-feeders that eat zooplankton, the Megamouth shark,
(Megachasma pelagios), (TP = 3.38) and the Whale
shark (Rhincodon typus) (TP = 3.55). Both were classed
as pinniped-competitors because their TP overlapped
with the three pinnipeds with the lowest TP scores
(3.3-3.4) that are planktonic or benthic foraging. These
are the Crabeater seal (Lobodon carcinophagus), Walrus
(Odobenus rosmarus) and Bearded seal (Erignathus
barbatus) that are all limited to high latitudes in both
hemispheres where sharks are unlikely to be abundant.
We nonetheless retained these two species as potential
pinniped-competitors.
Latitudinal distribution: The shark distribution dataset
contained 303 species with at least 10 location points
(range 10-24, 515 points, mean = 577, median = 73,
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Order
Family (n w/ data)
Predators
Competitors
Prey
Hexanchiformes
Pristiophoriformes
Squatiniformes
Hexanchidae (4)
Chlamydoselachidae (1)
Heterodontidae (7)
Rhincodontidae (1)
Parascylliidae (3)
Brachaeluridae (2)
Orectolobidae (4)
Hemiscylliidae (8)
Stegostomatidae (1)
Ginglymostomatidae (2)
Odontaspididae (3)
Mitsukurinidae (1)
Pseudocarchariidae (1)
Lamnidae (5)
Megachasmidae (1)
Cetorhinidae (1)
Alopiidae (3)
Scyliorhinidae (69)
Proscylliidae (4)
Pseudotriakidae (2)
Leptochariidae (1)
Triakidae (26)
Hemigaleidae (4)
Carcharhinidae (44)
Sphyrnidae (8)
Dalatiidae (51)
Centrophoridae (11)
Squalidae (9)
Echinorhinidae (2)
Pristiophoridae (4)
Squatinidae (11)
2
1
0
0
0
0
1
0
0
0
3
0
0
5
0
0
3
0
0
1
0
0
1
21
3
2
0
0
2
0
0
3
1
6
1
3
2
4
8
0
2
1
1
1
0
1
0
0
62
4
1
1
23
3
30
5
41
7
5
0
4
8
0
0
2
0
3
1
2
6
0
0
0
0
0
0
0
0
0
64
3
0
1
5
1
6
0
37
4
4
0
1
1
Total
294
45
228
141
Heterodontiformes
Orectolobiformes
Lamniformes
Carcharhiniformes
Squaliformes
Unclassified*
1
1
1
2
2
1
3
5
2
2
2
22
*Unclassified shark species (incl. Portuguese dogfish, Centroscymnus coelolepis) occurred due to
their size (100 and 200 cm), and thus not classed as prey (> 100 cm), while their TP was too high or
too low to be classed as pinniped-competitors (< 3.3 or > 4.3).
Table 2: Breakdown of sharks classified as pinniped-predator, pinniped-prey or pinniped-competitors, by order and
family.
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Shark and pinniped latitudinal species diversity
Figure 2: Latitudinal variation in species richness of sharks (gray bars, n = 294) and pinnipeds (black bars, n =
34) (36 5o latitude bands). The y-axis shows the percentage of the total examined species (294 sharks, 34
pinnipeds) in each group that occur in the 5o latitude band.
5-95th percentile range 12-2, 458). This distribution
dataset was pruned to include only species with length
data and TP available on FishBase, resulting in a final
shark data set of 294, or 60% of the total recognized
species. Coverage per shark family ranged from 32% to
100% and included 31 families (range 1-146 species per
family) in eight orders (2-270 species per order). We
measured total latitudinal extent (Figure 1c) using
whichever data set included the largest number of
locations (usually FishBase, 290 species; see
Supplementary Material). There was still a significant
relationship between total extent and the number of
location points (linear regression on log10 data, n = 303,
R2 = 0.19, F(1, 301) = 70.84, p < 0.0001). Species are
included from all eight orders (ranging from 50% to
94% of the species per order) (Appendix 3).
Latitudinal variation in species richness of sharks
and pinnipeds was largely reversed with pinnipeds
dominating at high latitudes and sharks dominating at
low latitudes (Figure 2). Pinniped species richness
distribution was bimodal with peaks at temperate
latitudes, whereas shark species richness was normally
distributed with a peak within +40 and -40o latitude, the
area with few pinniped species.
Testing for competition: To explore spatial patterns and
test whether they are consistent with a possible trophic
explanation for the observed pattern, we investigated the
relationship of richness per latitudinal band after
dividing the sharks into pinniped-predator, pinnipedcompetitor, and pinniped-prey groupings. We tested both
methods of classifying sharks as predators but found no
qualitative difference in results; therefore we report only
on pinniped-predators defined as sharks greater than 200
cm in length and having a TP > 4.16. Plots of shark
species richness versus pinniped species richness were
fit to all shark species and three shark groupings using a
second-order polynomial relationship (Figure 3). A
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Figure 3: Plots of shark species richness (n=294) versus pinniped species richness (n=34) per 5o latitude band
(n = 36) (2-order polynomial lines of best fit) according to (a) all sharks, (b) sharks classified as pinnipedpredators (conservative classification), (c) as pinniped-competitors, and (d) pinniped-prey.
significant serial auto correlation existed in the different
classifications of shark and pinniped species richness per
latitude band (smallest first-order correlation coefficient
AR(1) = 0.960). Autoregressive first-order models
indicated a positive autocorrelation among error terms
using first order autocorrelation and Durbin-Watson
statistics. Mixed effects models with an autoregressive
first-order process to control for the non-independence
indicated significant relationships for all sharks and the
pinniped-predator classification, but not for pinnipedcompetitors or pinniped-prey (Table 3). The relationship
is nonlinear with: (1) some latitudinal bands having few
shark and pinniped species, (2) as the number of shark
species increases we initially see an increase in pinniped
species until the species richness of sharks exceeds 20
species, after which (3) a negative relationship occurs
with fewer and fewer pinniped species occurring as
shark diversity increases.
Discussion
We have provided correlative evidence that the
shark clade has competitively excluded the pinniped
clade from much of the world’s marine waters. Shark
species richness was opposite pinnipeds with pinnipeds
dominating at high latitudes and sharks dominating at
low latitudes. Of the various shark groups, sharks
classified as predators of pinnipeds were the only group
with a significant spatial relationship between shark and
pinniped richness by latitude. Here, the pattern was
curvilinear with fewer shark predators in areas with very
few pinnipeds in equatorial regions. The distribution of
pinnipeds is noticeably bimodal with few species
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Shark classification
β
SE
t
P
RSE
Correl
AR(1)
Predators* (n = 45)
Competitors (n = 228)
Prey (n = 141)
2.341
0.977
1.014
0.635
0.831
0.860
3.688
1.176
1.179
< 0.001
0.248
0.247
1.787
2.315
2.222
-0.264
-0.269
-0.309
0.9396
0.9382
0.9279
All sharks (n = 294)
2.489
0.636
3.912
< 0.001
2.082
-0.199
0.9554
Shark predators of pinnipeds defined as having body length > 200 cm and trophic
position (TP) > 4.16 (n = 45). A second classification of predators as TP > 4.0 (n = 51)
was also used but results are not shown.
Table 3. Generalized least squares (GLS) regression fit by maximum likelihood models and with an
autoregressive first-order process (AR(1)), comparing pinniped (n = 34) and shark (various
classifications) diversity (log10 number of species per latitudinal band) across latitude (5-degree latitude
bands, n = 36). Zero-values changed to 0.001 prior to log-10 transformation. For all models, df = 36
total, 34 residual. Regression analysis indicates that predation model is the best fit compared to
competitor and prey models.
associated with diving birds and pinnipeds versus
cetaceans suggests that it is the evolved morphological
ability to escape sharks using their size/speed or defend
using 'weaponry/armor' that is an important factor in
determining the outcome of higher-level competition
selection.
Many pinnipeds are locked into land-use because
of the evolutionary pre-condition that necessitates a need
for land breeding, particularly among otariid seals (46).
During their time on land, pinnipeds mate, give birth,
and care for their dependent young while lactating (6).
Land sites are chosen that have few terrestrial predators.
However, during the period of learning to use water, seal
pups are at a considerable disadvantage to marine
predators, such as sharks and killer whales (8,43).
Evidence of shark predation on seal pups is mostly
reported in temperate waters in agreement with the shark
-pinniped species richness trend (57,58). Future research
on the evolutionary origins of pinnipeds relative to
geography such as ocean temperature and sea ice
distribution may assist in understanding the ghosts of
competition past (14).
The evolutionary time scale of sharks
(neoselachians – sharks, skates and rays) of ~420 million
years (55) considerably predates the first occurrence of
pinnipeds at ~50 million years (17). This long
evolutionary history likely enabled sharks to evolve
superior predatory skills and to diversify to occupy a
broad range of niches within the marine realm prior to
the occurrence and diversification of pinnipeds. The
distributed in low-latitude warm waters, the areas where
sharks thrive. Most pinnipeds occur in high-latitude
regions with relatively few shark predators and most
shark predators occur in temperate water areas. The
divergence occurred in latitudinal regions with greater
than 20 shark species.
Our distributional results are descriptive.
However, we consider the likely mechanism of the
distribution pattern to be superior predatory adaptations
of sharks and inferior pinniped adaptations to minimize
this predation risk. Most sharks (62%) are smaller than
pinnipeds and only 8% of sharks are longer than the
largest pinnipeds. Marine trophic dynamics are
gape-limited and sharks have a larger gape than
pinnipeds relative to body size as an adaptation to
engulfing or biting large prey such as pinnipeds,
particularly small-bodied juveniles (36).
The observed pattern found in pinnipeds is not
evident for other endothermic animals such as cetaceans
that have been shown to display greater biodiversity at
warmer sea surface temperatures (71). Cetaceans are
more evolved swimmers than pinnipeds with greater
speed and include species such as Killer whales (Orcinus
orca) that regularly eat large sharks (26). In contrast,
seals are slower swimmers and generally smaller than
cetaceans. Also, endothermic pursuit-diving sea birds
that are smaller than pinnipeds and cetaceans also show
a similar geographic distribution pattern as pinnipeds
suggesting that their world distribution could also be
limited by shark diversity (9, 10). The differences
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Shark and pinniped latitudinal species diversity
radiation of modern day extant sharks occurred in the
early Jurassic, with most species considered to be small
bodied and oviparous in reproductive mode.
Diversification increased rapidly through the early/
middle Jurassic, while extinction rate was low with peak
diversification occurring in the Taorcian, coincidental
with sea level rise (47,55,67). Sea level rise created
extensive shallow marine and epicontinental
environments and was the precursor event for selection
over evolutionary time favoring larger body size, later
age at maturity, and ability to colonize broader habitat
types including the deep ocean (34). Much of the
distribution patterns of modern day sharks reflect this
geologic phase, with highest species diversity occurring
at intermediate latitudes, on upper continental slopes,
along coastlines and near submerged features (53).
Predation on seals by sharks is postulated from the fossil
record during the Eocene (17). Sharks consequently
gained an evolutionary advantage over pinnipeds in
terms of niche, predatory skill, adaptability and habitat
occurrence; through ‘opportunistic’ radiation events and
possible evolution of novel body plans (47).
Heterothermic (endothermic and ectothermic)
sharks include only a few species within the lamnids, the
Great white (Carcharodon cacharias), Shortfin and
Longfin mako (Isurus oxyrinchus and I. paucus) and the
Salmon shark (Lamna ditropis). These represent large,
fast swimming, agile species that occur in both subtropical and temperate waters and are known to occasionally predate on pinnipeds with the white shark considered to be a specialized seal hunter (57).
Interestingly, the lamnids represent one of the more
recent shark groups in evolutionary history, first
occurring in the Miocene and thought to have evolved
from Isurus sp. in the Eocene (21), coincidental with the
occurrence of Pinnipedia. These heterothermic sharks
may have specifically evolved heat exchange systems,
the rete mirabile, to exploit latitudes where pinniped
diversification occurred. Notably these species that
overlap in latitudinal range are all large bodied animals
with serrated teeth design and gape size capable of
predating and handling seal prey. In polar waters, few
shark species occur and are dominated by one family,
Somniosidae, that is known to feed on seals although
little is known about actual predator-prey interactions
(25,72). The Greenland shark (Somniosus
microcephalus), Pacific sleeper shark (Somniosus
pacificus) and Antarctic sleeper shark (Somniosus
antarcticus) are all very large bodied species that do not
possess heat exchange systems but have physiologically
adapted to cold water environments through increased
lipid levels, thick skin layer, high urea content and likely
very low metabolic rates (54). Thus, sharks of the
Lamnidae and Somniosidae have consequently evolved
adaptations that support predation on seals through
independent evolutionary trajectories.
Considerable research has described sharks as
predators of pinnipeds including a summary by Cortés of
diet composition and TP for 149 species of shark within
eight orders and 23 families (15). Marine mammal prey
(0.1 to 35.5%) was included in the standard diet
composition of 18 species in five families of four orders:
a) Carcharhiniformes (11 species, 10 in family
Carcharhinidae); b) Hexanchiformes (2); c)
Lamniformes (2), and d) Squaliformes (3). Marine
mammal prey was a minor component of the diet of
most of the 18 sharks (< 1% for seven species, < 5% for
12 species). TPs from Cortés are significantly (t-test: t =
6.707, df = 37, P < 0.001) higher for mammal-eating
sharks (n=18; mean 4.26, range 4.2-4.7) compared to
those with no recorded mammal diet (n=131; mean 3.98,
range 3.1-4.4) (15).
However, we recognize the limitations of our
assumptions. For example, the coarse metrics used to
delineate shark species as possible pinniped predators
overlooks the likelihood that most of the sharks with
higher TP may not typically eat pinnipeds. The presence
of remains of prey in the stomachs of a predator species
does not provide information on the intensity of
predation interactions, the dynamics of trophic energy
flow or the population-dynamic effects (60). Although,
we have considered the overlap in trophic position as
evidence for potential interspecific competition, we
encourage future research to more explicitly explore the
nature of species interactions between sharks and
pinnipeds and their differential use of the water column.
Field data is limited but given that these sharks eat
higher order and likely larger prey does at least provide
clues into the possibility that they are capable of
predation on pinnipeds and that there may be ghosts of
past evolutionary processes at play in the background
(14). Other trophic considerations that were not included
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Shark and pinniped latitudinal species diversity
are sharks and pinnipeds that feed on lower trophic food
sources such as krill (see above on planktonivores as
pinniped-competitors) and potential interactions
associated with common predators of both groups, such
as Killer whales, humans and other sharks. Also, the
current distributions provided by Fish Base are likely to
be modified by human pressures (direct hunting and
elimination of food resources) and may not reflect the
ranges in which the sharks naturally occurred.
Alternative explanations to the observed
distributional pattern include the distribution of oceanic
primary productivity and physiological differences
between the two clades. Among marine environments,
temperate latitudes, especially areas of upwelling,
support the highest productivity (56) and therefore, tend
to support higher abundance of large predators than
tropical latitudes (69). Pinnipeds as endotherms are
adapted to maintain high metabolism with a large caloric
intake that is provided by temperate latitude marine
environments. Thus, pinniped latitudinal distribution
may be a direct result of adaptations to feed in areas with
the greatest abundance of food resources that generally
occurs in temperate areas. Ectothermic sharks are limited
in their distribution due to thermal constraints associated
with their physiology. The exceptions are heterothermic
lamnids, well-known active predators of pinnipeds.
Lamnids, because they can take advantage of temperate
waters, also appear to have one of the greatest ranges in
distribution (Appendix 2). As a result, temperate
upwelling areas would be beneficial for both sharks and
pinnipeds to occupy. Therefore, an alternative untested
explanation for the observed distribution reflects thermal
constraints rather than competitive exclusion or
predation risk. Future research should investigate the
lamnid, somniosid, and White shark distribution relative
to seal abundance and primary productivity (68).
There are conservation implications of our
distribution results. An expanding range for the shark
clade towards the poles with warming ocean temperature
may prove problematic for pinnipeds. Many of the
pinnipeds that inhabit temperate marine environments
are at an evolutionary risk of extinction due to warming
waters (22). Here, seals make their home around islands
that are observing more shark predation. For example,
Grey seals (Halichoerus grypus) on Sable Island, Nova
Scotia, Canada (52). Predictions are for the world’s
oceans to continue to warm which would suggest highlatitude areas would become better shark habitat and
poorer environments for pinnipeds. With the accelerated
climate change occurring at higher latitudes, research
into global biogeographic patterns of ecosystem
structure will assist in predicting latitudinal shifts in
species distribution (70). Understanding climate-related
changes in species distribution has conservation
implications and can influence human activities,
including commercial fisheries. Thus, there is a need to
shift some of the current attention on climate-change
impacts on marine predators that emphasizes changes at
species-level ecological scales towards interspecific
effects at global community scales since interspecific
competition has the potential to alter populations,
communities and the evolution of trophic interactions.
Acknowledgments
Funding for the research was provided by Fisheries and
Oceans Canada, ArcticNet Centre of Excellence, and a Natural Sciences and Engineering Research Council (NSERC) Discovery Grant
to SHF and NSERC Ocean Tracking Network to ATF and SHF. We
thank the reviewers and editor for helpful comments.
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Appendix 2 Comparison of subgroup distributions
To compare subgroup patterns, we provide figures of the
two major pinniped subgroups (phocids versus otariids
together with walrus) (Top) and the distribution of
lamnid sharks compared to other sharks (Bottom).
Lamniformes is the order with the highest proportion of
predators; 11 or 12 of 15 species, depending on
classification; followed by Hexanchiformes, with 3 of 5
species classed as predators (both classifications). Three
orders have no species classed as predators:
Heterodontidae, Pristiophoriformes and Squatiniformes,
and the remaining three orders have few species classed
as predators (< 20%). Using ANOVAs, shark families
differed in maximum length (F(7, 286) = 11.527,
P < 0.001), trophic position (F (7, 286) = 8.595, P <
0.001) and global range (F(7, 286) = 8.177, P < 0.001).
On average, Lamniformes (n = 15) are the largest
(longest) of the eight shark families (mean length =
482.7 cm, standard deviation (SD) = 223.3 cm), followed by Hexanchiformes (n = 5, mean length = 260.4
cm, SD = 137.2 cm). Lamnids had the second highest
average trophic position (mean = 4.26, SD = 0.42),
slightly lower than Hexanchiformes (mean = 4.30,
SD = 0.17). Lamnids also had the second greatest global
range (n = 15, mean = 17.9 5 - degree latitude bands,
SD = 5.2), again with Hexanchiformes having the
greatest range (n = 5, mean = 20.2, SD = 5.2).
Additional Supporting Information may be found in
the online version of this article:
Appendix 1 Distribution data
The AquaMaps (see Methods) database included point
data (at least two locations) for 232 shark species (range
2-1,468 locations per species). There was a significant
positive trend between total latitudinal extent (range
size) and the number of locations (both log10transformed) (linear regression, n = 232, R2 = 0.250,
F (1, 230) = 76.75, p < 0.0001). The FishBase (see
Methods) database included 391 shark species with at
least two locations (range 2-24,515). Of these, 13
species (2-4 locations per species) had zero latitude
range (all point locations at same latitude) and were
excluded from further analyses, for a total of 378 species
initially retained. There was again a significant
relationship between the number of point locations and
the total latitudinal extent (n = 378, R2 = 0.349,
F (1, 376) = 201.23, p < 0.0001).
Only two species with AquaMaps data have less than 10
point locations, compared to 80 from the FishBase data
set. When these species are removed, the relationship
between the number of locations and overall extent was
not as strong but was still significant (n = 298, R2 =
0.192, F(1, 296) = 70.363, p < 0.0001). To reduce biases
in shark distribution knowledge we excluded all these
species with < 10 locations. FishBase generally had
more points per species (more points for 219 species,
versus 13 for AquaMaps, in addition to another 146
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Appendix 3. Shark summary data (see Methods)
Order (n)
Hexanchiformes (6)
Heterodontiformes (9)
Orectolobiformes (41)
Lamniformes (16)
Carcharhiniformes (270)
Squaliformes (124)
Pristiophoriformes (6)
Squatiniformes (22)
Total (494)
Family
Hexanchidae (4)
Chlamydoselachidae (2)
Heterodontidae (9)
Rhincodontidae (1)
Parascylliidae (8)
Brachaeluridae (2)
Orectolobidae (11)
Hemiscylliidae (15)
Stegostomatidae (1)
Ginglymostomatidae (3)
Odontaspididae (4)
Mitsukurinidae (1)
Pseudocarchariidae (1)
Lamnidae (5)
Megachasmidae (1)
Cetorhinidae (1)
Alopiidae (3)
Scyliorhinidae (146)
Proscylliidae (7)
Pseudotriakidae (2)
Leptochariidae (1)
Triakidae (45)
Hemigaleidae (8)
Carcharhinidae (52)
Sphyrnidae (9)
Dalatiidae (76)
Centrophoridae (18)
Squalidae (28)
Echinorhinidae (2)
Pristiophoridae (6)
Squatinidae (22)
No. with data
4
1
7
1
3
2
4
8
1
2
3
1
1
5
1
1
3
69
4
2
1
26
4
44
8
51
11
9
2
4
11
294
39
Length (cm)
Minimum Maximum
140
482
200
70
165
2000
80
91
76
122
63
320
46
121
235
320
430
320
410
617
110
305
792
549
980
383
760
28
170
24
200
109
295
82
58
220
114
240
69
750
148
610
20
730
79
164
71
160
310
400
80
170
108
244
Trophic position
Minimum Maximum
4.16
4.6
4.21
3.2
4.15
3.55
3.76
3.79
3.5
3.85
3.91
4.23
3.36
4.06
3.1
3.83
4.1
4.16
4.5
4.14
4.21
4.5
4.53
3.38
3.2
4.5
3.5
4.5
3.83
4.2
4.22
4.34
3.79
3.5
4.5
4.16
4.32
3.8
4.54
3.64
4.5
3.06
4.5
4.06
4.5
3.97
4.5
4.38
4.39
3.88
4.17
3.97
4.49
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