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Low prevalence of visual impairment in a coastal population of gray seals (Halichoerus grypus) in the Gulf of St. Lawrence, Canada

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Aquatic Mammals 2012, 38(4), 423-427, DOI 10.1578/AM.38.4.2012.423
Short Note
Low Prevalence of Visual Impairment in a Coastal Population of
Gray Seals (Halichoerus grypus) in the Gulf of St. Lawrence, Canada
Brian W. Kot,1, 2 Tadamichi Morisaka,3 Richard Sears,2
Don Samuelson,4 and Christopher D. Marshall1, 5
1Department of Marine Biology, Texas A&M University, Galveston, TX 77553, USA
E-mail: kotb@tamug.edu
2Mingan Island Cetacean Study, Inc., Longue-Pointe-de-Mingan, Québec G0G 1V0, Canada
3Wildlife Research Center, Kyoto University, Kyoto 606-8203, Japan
4Department of Small Animal Clinical Sciences, University of Florida, Gainesville, FL 32610, USA
5Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, TX 77843, USA
Visual impairment is common in captive pin-
nipeds (Sweeney, 1974; Ridgway et al., 1975;
Stoskopf et al., 1983; Greenwood, 1985; Colitz
et al., 2010a, 2010b), but its prevalence in the wild
is currently unclear due to the limited number of
published studies and inconsistent information in
the relevant literature (e.g., Griner, 1983; Filer
et al., 2003). Visual impairment is a broad cat-
egory that includes pathological, parasitological,
traumatic, or congenital conditions (e.g., Aguirre,
2004; Dailey et al., 2005). Although the preva-
lence of specific conditions affecting pinniped
vision (e.g., Leptospira pomona infection) may
be under-reported, partly due to the difficulties
of field diagnosis methods, general conditions
(e.g., opacities, lesions, etc.) are reported most
often (Stoskopf et al., 1985; Gerber et al., 1993;
Aguirre, 2004). What is clear is that visual impair-
ment reported in wild pinnipeds is usually associ-
ated with the cornea, anterior chamber, iris, and
lens (e.g., Smith et al., 1977; Stoskopf et al., 1985;
Schoon & Schoon, 1992; Baker et al., 1998).
However, this prevalence is likely because these
are the most conspicuous structures to observers.
Herein, we present results from a series of in-
water marine mammal surveys that included an
investigation of the prevalence of visual impair-
ment in a coastal population of western North
Atlantic gray seals (Halichoerus grypus). We
included behavioral information from individuals
with discernible eye problems and then showed
results from a literature survey to compare the
prevalence in our study area to those in published
studies of pinniped species, including gray seals,
around the world. A total of 23 surveys were con-
ducted from 21 June to 9 August 2011, and they
all were in the Mingan Archipelago of the Gulf
of St. Lawrence, Canada. Depending on weather
and sea conditions, most surveys consisted of four
12-km boat transects that were intermittent with
focal follows when one or more gray seals were
encountered. Observations were conducted with
the naked eye, 7 × 50 binoculars, and digital SLR
cameras (12.1-megapixel) with telephoto lenses
(300 and 600 mm). The total survey effort was
202.1 h with a mean of 8.8 h/d.
Survey results estimated 200 to 300 individ-
ual gray seals in the archipelago throughout the
summer, with highest abundances per survey effort
in three areas near identified haul-out locations
(Figure 1A-C). However, difficulties with identi-
fying and marking individuals likely resulted in
some repeated observations. Throughout our sur-
veys, only one gray seal with a conspicuous visual
impairment was observed, indicating a conserva-
tive prevalence of 1 of 200 (0.5%) gray seals in
the area.
The impaired gray seal was a bull that was
encountered on 22 July 2011 near 50° 09' 46.7" N,
63° 53' 49.2" W in approximately 35 m of water
(Figure 1). Its left eye exhibited a condition resem-
bling endophthalmitis (inflammation of the inter-
nal coats of the eye; Figure 2). The principal cause
of endophthalmitis is penetration of the eye, usu-
ally the cornea, by a sharp foreign body that can
introduce bacteria into the anterior chamber, lens,
and vitreous as well as the cornea. Other causes
include various endogenous systemic infections.
Typically, the entire eye becomes affected, often
filled with pus, and the cornea turns completely
opaque (Samuelson & Brooks, 2011) such as seen
in the impaired gray seal we observed.
424 Kot et al.
A second adult male without a visual impair-
ment was within 100 to 300 m of the first gray seal
throughout our 46-min observation period. Both
bulls were likely part of the herd of approximately
50 gray seals that were 2.3 km away within the
shallow Baie aux Loups Marins (Gray Seal Bay)
along the south shore of Grande Île (Big Island;
Figure 1). Approximately 25 gray seals were
hauled out at La Chaîne de Roches (Chain of
Rocks; H2 in Figure 1) within the bay, and the
other 25 were in adjacent shallow water (< 10 m).
Both gray seals were vigilant at the surface and
watched us for 10 to 30 s at least once before each
dive. The visually impaired gray seal initially
remained beyond 250 m of our 4.3-m boat, but
eventually he approached to within 75 m.
Published information on the prevalence of
visual impairment in the three taxonomic fami-
lies of pinnipeds in the wild is limited. The exist-
ing literature currently encompasses nine spe-
cies that collectively show 185 of 4,244 (4.3%)
individuals with any type of visual impairment
Figure 1. Map of study area (see open rectangle on inset map for a geographic reference) in Quebec, Canada (modified from
Google Earth, Version 6.1). H1: gray seal haul-out areas on Île de la Maison (House Island; left) and Île du Wreck (Wreck
Island; right); H2: La Chaîne de Roches (Chain of Rocks) haul-out area on Grande Île (Big Island; GI), the location near
where the impaired animal was encountered. A through C indicate locations of highest gray seal abundance throughout the
summer of 2011. Parenthetical values indicate estimated number of gray seals encountered per hour of effort in areas A
through C. Dashed lines indicate the four 12-km transect lines used for the surveys.
Figure 2. Photograph of a bull gray seal with visual impairment of its left eye from a condition resembling endophthalmitis
(A), including a close-up (B)
425 Visual Impairment in Gray Seals
(Table 1), although this differs widely among
specific reports. Among otariids, 4 of 765 (0.5%)
California sea lions (Zalophus californianus) had
some form of visual impairment (Gerber et al.,
1993). Likewise, 79 of 1,716 (4.6%) Northern
fur seals (Callorhinus ursinus) were reported
with eye lesions (Stoskopf et al., 1985). An ear-
lier account of northern fur seals showed 3 of 150
(2%) pups with a bacterial infection (Leptospira
pomona), causing dilated and congested vessels of
the iris, and hemorrhaging in the anterior chamber
of the eye (Smith et al., 1977). A report of subant-
arctic fur seals (Arctocephalus tropicalis) showed
1 of 12 (8%) individuals with protruding eyes
and an infected conjunctiva (Velozo et al., 2009).
Finally, a study of juvenile Galapagos sea lions
(Zalophus wollebaeki) showed individuals with
conjunctivae that held up to 47 parasitic eye flukes
(Philophthalmus zalophi; Dailey et al., 2005).
Among phocids, multiple reports of Weddell
seals (Leptonychotes weddellii) showed 14 of
295 (4.7%) seals and 28 of 498 (5.6%) seals with
leukomas (corneal opacities), punctured globes,
mucopurulent discharges, and purulent conjuncti-
vitis (McFarlane, 2009; Yochem et al., 2009). One
study of gray seals showed no visual impairment
in 36 individuals (Baker, 1987). Another showed
none in 33 young pups (< 16 wks) and 20 juve-
niles, but 2 of 50 (4%) older pups (> 16 wks)
with panophthalmitis (inflammation of the entire
eye) and 1 of 38 (2.6%) adults with corneal ulcer-
ations (Baker et al., 1998). Hawaiian monk seals
(Monachus schauinslandi) have been reported
with 21 of 158 (13%) individuals with ocular dis-
charge, “puffy eyes,” diffuse maculae and nebulas,
and leukomas (Aguirre, 2004).
Other reports of phocid visual impairment
include anecdotes of successfully foraging blind
ring seals (Phoca hispida saimensis; Hyvärinen,
1989), a harp seal with bilateral cataracts (Erlacher-
Reid et al., 2011), and a female Northern elephant
seal (Mirounga angustirostris) with a punctured
eye likely caused by male mating aggression
(Le Boeuf & Mesnick, 1991). A similar account of
aggression in Southern elephant seals (M. leonina)
reported 3 of 170 (1.7%) individuals with white
opacities, lacerated corneas, and inflamed nic-
titating membranes (Tierney, 1977). One report
showed 7 of 59 (11.8%) leopard seals (Hydrurga
leptonyx) with discharges and conjunctivitis (Gray
et al., 2009). An unusual case of Lake Baikal seals
(Pusa sibirica) with ophthalmitis was reported in
individuals with a morbillivirus infection similar
to canine distemper virus (CDV) (Grachev et al.,
1989). The highest reported prevalence of visual
impairment in any pinniped species in our lit-
erature survey was 21 of 44 (48%) harbor seals
(Phoca vitulina); bilateral lenticular lesions, len-
ticular malformations, and cataracts were identi-
fied, yet final conclusions about their causes could
not be determined (Schoon & Schoon, 1992).
Reliable estimates of the prevalence of visual
impairment in wild walruses (Odobenus rosmarus)
are not currently possible due to a paucity of pub-
lished reports. However, one investigation of 17
carcasses noted some individuals with prolapsed
Table 1. Low prevalence of visual impairment (% VI = [sum NVI / sum N] × 100 = 4.3%) reported from 16 studies of nine
different species of pinnipeds in the wild; studies with small sample sizes (N < 5) were not included. When considered
independently, the gray seal % VI was 1.6%, which is relatively similar to the 0.5% prevalence in our study area.
Species N NVI References
Callorhinus ursinus
Zalophus californianus
Monachus schauinslandi
Arctocephalus tropicalis
Mirounga leonina
Hydrurga leptonyx
Leptonychotes weddellii
Phoca vitulina
Halichoerus grypus
1,716
150
765
158
12
170
59
295
498
44
36
33
20
50
38
200
79
3
4
21
1
3
7
14
28
21
0
0
0
2
1
1
Stoskopf et al., 1985
Smith et al., 1977
Gerber et al., 1993
Aguirre, 2004
Velozo et al., 2009
Tierney, 1977
Gray et al., 2009
Yochem et al., 2009
McFarlane, 2009
Schoon & Schoon, 1992
Baker, 1987
Baker et al., 1998
Baker et al., 1998
Baker et al., 1998
Baker et al., 1998
Kot et al., this study
Sum 4,244 185
% VI 4.3
426 Kot et al.
eyes (Garlich-Miller et al., 2011), although post-
mortem changes cannot be ruled out. Another
report generalized that walrus eye loss can develop
from dento-alveolar abscesses resulting from
advanced tusk wear (Cornell & Antrim, 1987).
In summary, our study provides evidence that
gray seals in the Mingan Archipelago within the
Gulf of St. Lawrence, Canada, have a low preva-
lence of visual impairment. This is consistent with
results from our literature survey that showed a
similarly low prevalence in nine other pinniped
species from around the world. When considered
independently, the gray seal literature indicated
a low prevalence of 1.6%, which is relatively
similar to the low prevalence in our study area.
Collectively, this study adds to the few published
records of North Atlantic gray seals with ocular
problems and provides information supporting
a low prevalence of visual impairment in wild
pinnipeds.
Acknowledgments
This study was funded as part of a collaborative
program between the National Fish and Wildlife
Foundation and the U.S. Marine Mammal
Commission, and the Department of Marine
Biology at Texas A&M University. Additional
support was provided by Bio-Logging Science,
The University of Tokyo (UTBLS; Investigator:
Katsufumi Sato). We thank Marie-Pierre Maillet
and the Mingan Island Cetacean Study, Inc. for
their logistical support of this work.
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The Weddell seal, Leptonochotes weddelli, is the most southerly breeding of the Antarctic seals. Small groups remain for extended periods over the summer months on the fast-ice of the inlets and shorelines of the Antarctic continent for parturition, lactation and moulting. Those breeding in areas close to Antarctic research stations are uniquely accessible for study, but this may bring them in close contact with human activity and pollution derived from human habitation. Antarctic Treaty nations have undertaken to prevent the accidental introduction of parasites and diseases (Article IX of the Agreed Measures 1964 and The Protocol on Environmental Protection to the Antarctic Treaty, 1991) into Antarctica, but our understanding of existing diseases and their effects are limited. At two sites, the Vestfold Hills, East Antarctica, and at McMurdo Sound, Ross Sea, Weddell seals have been tagged over many years for population and feeding ecology studies. This provides two unparalleled opportunities to investigate health and disease in well-described populations of Antarctic wildlife. Health assessment of the population at McMurdo is reported by Yochem et al. (this volume). It is the population of Weddell seals in the Vestfold Hills that is the subject of this chapter.
Book
This book provides systematic coverage of small animal ophthalmology via randomized self-assessment case presentations: integrated questions, superb illustrations, color photos, imaging, diagrams, tables, and detailed explanatory answers. The authors have emphasize the more common ophthalmic conditions presented to veterinarians in practice with 251 illustrated cases. The differential diagnoses, examination techniques, and therapies for these ocular conditions are discussed within specific cases.
Article
A male yearling harp seal (Phoca groenlandica) stranded and was brought to Mystic Aquarium & Institute for Exploration's Seal Rescue and Rehabilitation Center. The seal presented with a bilateral pendular vertical nystagmus, negative menace response, and a positive palpebral response. Ophthalmological examination by slit lamp biomicroscopy revealed perilimbal corneal edema, excessive iridal surface structures, pupils that appeared to be shaped improperly (dyscoria), and suspected cataracts. Attempts to dilate the pupils with both dark-lighted conditions and repeated dosages of 10% phenylephrine and 1% atropine ophthalmic solution in each eye (OU) were unsuccessful. Ocular ultrasonography findings suggested bilateral cataracts with flattened anterior-posterior (A-P) diameter and possible persistent hyperplastic primary vitreous. It is possible that these structural congenital abnormalities could produce further ocular complications for this seal including uveitis, secondary glaucoma, retinal detachment, and/or vitreal hemorrhage in the future. This case demonstrates the importance of a thorough ophthalmological examination in stranded wild animals, especially if their symptoms appear neurological.
Article
Underwater vocalization and the functional structure of different vibrissae of the ringed seal (Phoca hispida saimensis) of Lake Saimaa, Eastern Finland, were studied. These seals live in darkness under the ice cover for several months during the year. It is known that blind seals are managing well in the lake. Visibility under water in some parts of the area where the seals live is only 2 m. It is suggested that echolocation is used in orientation and feeding. The Saimaa seal has click and click trial underwater vocalizations. However, both the frequency and intensity of the vocalization are low compared with, for example, those of dolphins. The structural adaptations for underwater sound localization are also not well developed. The ringed seal has, however, extremely well-developed vibrissae. The innervation of one vibrissa is more than 10 times greater than normally found in mammals. The main structural deviations from normal mammalian vibrissae are: (1) an upper cavernous sinus, (2) a groove in the wall of the capsule at the level of the lower cavernous sinus, (3) elasticity of the connective tissue bands fixing the hair root to the capsule in the lower cavernous sinus and especially (4) the structure and innervation of the ring sinus area. Sensory elements are situated upon the glassy membrane on the surface of the outer rootsheath and in the basal cell layer of the outer rootsheath which is like a sensory epithelium. Below this epithelium a layer of liquid or gelatinous material and large amounts of glycogen are found. This sensory epithelium is especially well developed in the superciliary vibrissae. These vibrissae are protruded some millimetres when the seals are attentive. It is suggested that the vibrissae also sense sounds, which are transmitted to the sensory elements by tissue conduction through the capsule wall and via the blood sinuses. The seals may possibly detect compressional waves with the vibrissae.