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Determination of tear production and intraocular pressure with rebound tonometry in wild Humboldt penguins (Spheniscus humboldti).

Abstract: Tear production and intraocular pressures (IOPs) were determined in 38 and 102 wild Humboldt penguins (Spheniscus humboldti), respectively, from the Punta San Juan Marine Protected Area in lea, Peru. Tear production was measured by Schirmer tear test, and IOP was measured with a Tono Vet rebound tonometer. Adult (n = 90) and chick (n = 12) penguins were sampled from 2 different beaches (north and south facing) during 2 sampling years (2010 and 2011). Results showed a mean [+ or -] SD (range) of 9 [+ or -] 4 (2-20) mm/min for tear production and 28 [+ or -] 9 (3-49) mm Hg for IOP. Tear production in penguins differed between beach and sex, whereas IOP differed between age, year, and beach. The IOPs were negatively correlated with packed cell volume. Tear production and IOP values had greater variation in this population than it has in other avian species. Previous investigations of IOP and tear production in Spheniscus species were conducted with birds housed under professional care in artificial marine and freshwater environments. This is the first study, to our knowledge, investigating tear production and IOP in wild penguins and establishes valuable reference intervals for this species.

Key words: intraocular pressure, Schirmer tear test, rebound tonometry, avian, Humboldt penguin, Spheniscus humboldti


Although studies of tear production and intraocular pressures of various nondomestic avian species are increasing in the scientific literature, most of the populations studied are under professional care in zoological institutions or wildlife rehabilitation settings. There is limited knowledge of these ocular parameters in free-ranging avian populations.

The Humboldt penguin (HP; Spheniscus humboldti) is endangered throughout its natural range along the Pacific coast of southern South America. The largest Peruvian breeding colony resides within the Punta San Juan Marine Protected Area, a site that is crucial to the conservation of numerous marine species in Peru. This CITES Appendix I species (Convention on International Trade in Endangered Species of Fauna and Flora, Geneva, Switzerland) experienced a severe population decline in the 19th century and remains imperiled today because of threats such as fishing gear entanglements, bycatch issues, competition for prey with industrial fisheries, changes in prey base related to El Nino-Southern Oscillation cycles, human conflict from continued coastal development, and disruption of nesting areas by harvesting of guano. (1,2) Humboldt penguins are well represented in zoos and aquariums worldwide, providing an important role inspiring people to conserve wildlife and marine resources.

The HP is a pelagic visual hunter, possessing unique ocular characteristics. (3) Flat corneas allow for myopic vision in air and emmetropic vision in water, much like other penguin species but unlike most other birds. An accommodating lens makes up for decreased refractive power of the flattened cornea. (3-5) Humboldt penguins also possess a supraorbital gland that excretes salt from the bloodstream into tears. This physiologic adaptation allows consumption of salt water without detrimental effects of dehydration; however, this gland may atrophy in captive penguins living in freshwater habitats. (6,7)

Avian ocular diseases are extensive and commonly encountered; therefore, a thorough ocular examination is vital to any complete medical examination. (8) Tear production and intraocular pressure (IOP) measurements are key diagnostic tools, with many ocular diseases potentially affecting these parameters. Establishing baseline health data is important for maintaining the health of animals under professional care and for monitoring wild population health. Species-specific reference intervals are necessary because of variations among avian species. (9-17)

Applanation tonometry requires topical anesthesia and measures the force required to flatten a constant area of the cornea. This method has been described in ostriches (Struthio camelus), (10) raptors, (9,11,12) and HPs in a zoo setting. (18) Rebound tonometry does not require topical anesthesia and measures the rebound velocity of a small probe's quick and repeated contact with the cornea. (19) This method has been described in domestic chickens, (15) raptors, (11,16,17) flamingos (Plioenicopterus ruber ruber), (14,20) and black-footed penguins (Spheniscus demersus). (13) Intraocular pressure measurements can vary among species and with the device used. Although both methods are widely used, rebound tonometry may be easier to use in health assessments of wild animals because it does not require topical anesthesia of the cornea. It is also reliable in eyes with corneal diameters as small as 1.4 mm, unlike applanation tonometry, which requires a larger corneal surface. (14,17)

The purpose of this study was to establish reference intervals for normal tear production and IOP in wild HPs using the Schirmer tear test and rebound tonometry.

Materials and Methods

Data collection

For this study, 102 HPs from the Punta San Juan Marine Protected Area (lea, Peru; 15[degrees]22'S, 75[degrees]12'W) were included. Penguins were examined in June 2010 (n = 51) and June 2011 (n = 51) as part of an ongoing population health assessment project underway since 2007 (Peruvian permits 09-2010-SERNANP-RNSIIPG and 11-2011-SERNANP-RNSIIPG). In 2010, 12 chicks were included in the sample population, whereas, in 2011, only adults were studied. Adult birds consisted of 41 males and 49 females from both the north (n = 24) and south (n = 66) beaches of the peninsula. Adult penguins were manually removed from nests, which included "burrows" (n = 46) dug into the guano and "crevices" (n = 44) that were surface-based among rocky caves. Eggs were removed from nests via a cupped pole before penguin removal to avoid trauma. Chicks and eggs were provided with supplemental heat during examination of the adult and were returned to the nest just before release of the adult into the burrow. All penguins were released at the site of capture.

All penguins received a complete physical examination. Multiple morphologic measurements and physiologic parameters, including heart rate and respiratory rate, were recorded. Gross examination of the eyelids, nictitating membranes, corneas, and anterior chambers were performed. Metal identification tags and transponder microchips were placed for concurrent projects and served to prevent reexamination of individual birds in the same year. Blood samples were collected from the jugular vein and placed in EDTA or heparinized microhematocrit tubes and centrifuged at 14 800g for 5 min to measure packed cell volume (PCV). Total white blood cell counts were determined by the avian leukopet system (Vetlab Supply, Palmetto Bay, FL, USA), following manufacturer protocols. (21) After centrifugation, plasma samples were analyzed with a VetScan VS2 (Abaxis, Union City, CA, USA).

Measurements of IOP were obtained with a TonoVet rebound tonometer (Jorgensen Laboratories, Loveland, CO, USA) operated by 2 consistent veterinarians. Measurements were obtained on the tonometer's "dog" setting. Birds were manually restrained for the measurements in an upright, vertical position; gentle pressure was applied by the restrainer's knees around the torso and wings of the penguin, whereas the hands were used to hold the penguin's beak and to apply gentle pressure at the occipital base of the skull (Fig 1).

Measurements were obtained by following standard recommendations, with the tonometer held in a horizontal position and the probe starting 4-8 mm from the cornea. Six individual measurements were obtained from the central cornea bilaterally. The average measurement, as calculated by the tonometer (highest and lowest values excluded), was recorded. Results with deviations of [less than or equal to] 1.0 mm Hg and between 1.8-2.5 mm Hg were accepted. Results with a deviation >2.5 mm Hg were repeated.

Measurements by the Schirmer tear test were collected with standardized sterile strips (Merck, Summit, NJ, USA) performed by a single consistent veterinarian following manufacturer instructions. Briefly, the rounded, notched end of the strip was inserted over the central lower eyelid when the nictitans was fully retracted, putting the strip in direct contact with the central cornea. The eyelids were then closed, and the moistened area of the strip was measured in millimeters after 60 seconds (Fig 2). Measurements were collected bilaterally in succession. Dry gauze was used to remove any visible dirt from the periorbital region to prevent contamination of the strip. Care was made to handle the strips only by the sides to avoid contact with any objects or moisture before sampling.

Statistical analysis

The distributions of all continuous variables, including IOP of the right eye (OD), IOP of the left eye (OS), tear production of the OD, and tear production of the OS, were analyzed by the Shapiro-Wilk test. Parametric and nonparametric methods were used to analyze normally and nonnormally distributed data, respectively. Independent sample t tests were performed when a normally distributed independent variable had 2 categories (sex, age, location, year, nest type). If differences were not observed among categories, results were combined for future analysis.

Variables found in the univariate analysis with a P < 0.2 were evaluated further by linear regression. Linear regression models were constructed to include sex (male or female), age (adult or chick), location (north or south beach), year (2010 or 2011), and nest type (crevice or burrow) as independent variables, with the ophthalmological value (IOP or tear production) as the dependent variable. Bivariate correlation was assessed for all ophthalmological variables, total leukocyte count, PCV, body weight, heart rate, respiratory rate, and total calcium values. Statistical software (version 22, SPSS Inc, Chicago, IL, USA) was used to analyze the data, and a P < .05 was used to determine statistical significance.


All birds were considered in normal health based on physical examination findings and blood analyses. No grossly visible abnormalities were present that affected the eyelids, nictitans, cornea, or anterior chamber of any of the examined eyes. Pupils were nearly uniformly miotic because of ambient light conditions, which precluded any evaluation of the posterior chamber of the eye. Chicks weighed an average of 1.16 kg, with a range of 0.92-1.50 kg, consistent with penguins that are 22-35 days old. (22)

For this group of wild HPs, the mean [+ or -] SD (range) of tear production was 9 [+ or -] 4 mm/min (2 20 mm/min), and the mean [+ or -] SD (range) of the IOP was 28 [+ or -] 9 mm Hg (3-49 mm Hg).

Several significant findings were identified on univariate analysis, but multivariate analysis failed to account for a significant amount of the variation. The significant results of the univariate analyses are reported in Table 1. Adults had significantly higher IOP in both eyes than chicks (P < .001). Tear production was measured in 38 birds and was significantly greater in the right eye of adult males than it was for adult females (P = .02). No differences were found between adult males and females for tear production in the left eye (P = .16), IOP of the OD (.P = .49), or IOP of the OS (P = .49). The IOP in each eye differed significantly (P < .001) between years of the study. Between beach location, significant differences were seen in tear production of the OS (P = .006), IOP of the OD (P = .01), IOP of the OS (P = .01) but not in tear production in the OD (P= .18). All birds from north-facing beaches were found in crevice nests, and all birds from south-facing beaches were found in burrow nests; thus, nest type results were identical to beach location results (Table 1). The IOP of the OD (R = -0.337, P = .001) (Fig 3a) and OS (R = -0.398, P < .001) (Fig 3b) both revealed significant negative correlations with PCV. The IOP and tear production data obtained in this study and in other avian studies are presented in Table 2.


This is the first study, to our knowledge, investigating tear production and IOPs in wild penguins and serves as a valuable reference for other wild penguin populations, as well as for penguins under professional care. The results of this study revealed higher mean IOP measurements (28 [+ or -] 9 mm Hg) with a wider range (3-49 mm Hg) than what our group has previously reported for HPs in a zoo setting (20.36 [+ or -] 4.1 mm Hg, range 10-27 mm Hg). (18) This difference and wider range could be caused by higher environmental variability in the wild, animal health status, effects of ocean water compared with filtered freshwater and artificial saltwater, or other unidentified factors. Previous data were also obtained by applanation tonometry because of the unavailability of rebound tonometry at that time. (18) Applanation tonometry has also been shown to consistently underestimate IOP measurements when compared with rebound tonometry in other avian species. (11,16) Mean IOP measurements obtained with rebound tonometry from the closely related black-footed penguins in a zoo setting were similar (28-30 mm Hg) to the wild HPs in this study (29-30 mm Hg). (13)

Compared with other avian species, mean IOP appears greater in wild HPs than in flamingos and most reported raptor species but similar to values in common buzzards (Buteo buteo) and white tailed sea eagles (Haliaeetus albicilla) (Table 2). (11,14,17) The greater IOP in adult penguins has a possible adaptive function for underwater foraging, which can involve dives up to 30 m beneath the ocean surface and significant external pressure on the cornea. (1) Marine mammals have relatively greater mean IOP compared with most terrestrial mammals, with reported means of 33 mm Hg in various cetacean species and 32.8 mm Hg in California sea lions (Zalophus californianus). (23,24) This may reflect a similar marine adaptation with a greater IOP having benefit during underwater diving and foraging behaviors.

Previous investigations of IOP measurements in penguins focused solely on adult animals. The inclusion of chicks in this study revealed that IOP was significantly greater in adult HPs than in chicks. This is consistent with the IOP of adult and juvenile northern goshawks (Accipiter gentilis), common buzzards, and common kestrels (Falco tinnunculus). (17) The IOP in American flamingos increased with increasing body weight; however, all measured animals were adults between 2 and 10 years old. (20) Conversely, IOP did not differ between adults and juveniles in ostriches, Eurasian spar-rowhawks (Accipiter nisus), and tawny owls (Strix aluco). (10,17) This differs from the IOP distribution in people and dogs, in which infants and younger animals have, on average, higher IOP values. (25-28) The cause of some avian species having lower IOP values as chicks compared with adults is not yet understood.

The lack of significant difference in IOP between sexes was expected and consistent with previous studies of IOP in birds. (10,13,14) Unexpectedly, there was a significant difference in IOP between adults in 2010 and those in 2011. Variations in the tonometer, operator technique, animal restraint intensity, elapsed time from capture to assessment, and health status of the eyes are possible explanations.

The significant negative correlation between IOP and PCV is interesting and may be due to relative erythrocytosis caused by dehydration, resulting in lower IOP values. In people, IOP decreases during exercise-induced and nonexercise-induced dehydration.(29,30) Penguin mates alternate caring for their offspring and, with one penguin foraging away from the nest, the attending penguin can be sitting in a nest for several days without access to food or water. Presumably, these animals can develop some degree of subclinical dehydration; however, that is purely speculative, and further studies measuring IOP in confirmed dehydrated animals would be needed.

This study revealed greater mean tear production with a wider range and SD values than those previously reported in HPs in a zoo (Table 2). (18) The clinical significance of that is uncertain, but again, it is most likely attributable to variation between the natural marine environment and a professionally managed zoo/aquarium environment. The significantly greater tear production in the OD of females compared with males is considered clinically irrelevant.

Tear production OS was significantly higher in the north beaches, whereas IOP measurements in both eyes were significantly higher in penguins examined from the south beaches. This may reflect differences in the microclimate or environments between the 2 sides of the reserve. Variation in the health or survival fitness of these 2 subpopulations has not been documented but could also explain these differences. The variations do not appear clinically significant.

There was no correlation between IOP or tear production and heart rate or respiration rate. This is consistent with results from human studies in which there were no linear correlations between blood pressure, heart rate, and IOP after periods of jogging. (31) However, autoregulative mechanisms exist to maintain constant retinal blood flow despite changes in perfusion pressure, which can affect IOP. (32) With variations in elapsed time between capture and measurement, autoregulation may have been able to compensate for changes in IOP that occurred immediately at the time of capture. This suggests that although physiologic stresses associated with capture and restraint of wild penguins did not significantly alter IOP measured in this study, there may have been transient and acute changes that occurred before measurement. Future studies should include IOP measurements taken immediately at time of capture and again after sample collection and examination to determine how autoregulative mechanisms of ocular blood flow may be influencing those data.

Full ophthalmologic examinations and standardized timing of ocular measurements in relation to capture time were not feasible because of field conditions and capture of variable numbers of penguins at one time. This project was incorporated into an established program monitoring population health of wildlife at Punta San Juan Marine Protected Area, meaning that other data and sample collection took priority and limited the time available for ocular assessments of penguins under restraint. Other parameters also dictated selection of the individual penguins and some of the methodology. A limitation of this study is that ocular procedures were not performed at the same time-point during each physical examination. Some animals were handled longer or had to wait before having IOP and tear production measured to facilitate the demands of other concurrent data collection. This could have masked a correlation between ocular parameters and the duration of handling, heart rate, or respiratory rate as stress levels and struggling generally decreased the longer penguins were held. This study was also performed in an outdoor marine environment with significant exposure to dust, ocean spray, and wind, which may have influenced data, unlike studies performed in a controlled indoor environment at a zoological institution.

Julie D. Sheldon, DVM, Michael J. Adkesson, DVM, Dipl ACZM, Matthew C. Allender, DVM, PhD, Dipl ACZM, Gwen Jankowski, DVM, Dipl ACZM, Jennifer Langan, DVM, Dipl ACZM, Marco Cardena, BSc, and Susana Cardenas-Alayza, MSc

Department of Small Animal Clinical Sciences, University of Tennessee College of Veterinary Medicine, 2407 River Dr, Knoxville, TN 37996, USA (Sheldon); Chicago Zoological Society, Veterinary Services Department. Brookfield Zoo, 3300 Golf Rd, Brookfield, IL 60513, USA (Adkesson, Langan, Cardenas-Alayza); Wildlife Epidemiology Laboratory, Department of Comparative Biosciences, College of Veterinary Medicine, University of Illinois, 2001 S Lincoln Ave, Urbana, IL 61802, USA (Allender); Denver Zoo. 2300 Steele St. Denver. CO 80205, USA (Jankowski); Department of Clinical Medicine, College of Veterinary Medicine, University of Illinois. 1008 W Hazelwood Dr, Urbana, IL 61802, USA (Langan); and Universidad Peruana Cayetano Heredia, Av Honorio Delgado 430, Lima 4314, Peru (Cardena, Cardenas-Alayza).

Acknowledgments: We thank all collaborators from the Chicago Zoological Society, St Louis Zoo, and Universidad Peruana Cayetano Heredia that assisted with this project, with special thanks to Mike Macek for his support. Funding for this project was provided by the St Louis Zoo Wild Care Institute and the Chicago Zoological Society.


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Caption: Figure 1. Measuring intraocular pressure with the Tono Vet in a wild Humboldt penguin. Animals were restrained in an upright, vertical position with gentle pressure around their wings, at the base of the skull, and around the beak.

Caption: Figure 2. Measuring tear production by the Schirmer tear test in a wild Humboldt penguin.

Caption: Figure 3. Bivariate correlations between packed cell volume (PCV) and intraocular pressure (IOP) in the right eye (OD) (a), and PCV and IOP in the left eye (OS) of 102 Humboldt penguins, (b), revealing significant negative linear correlations.
Table 1. Significant results (P < .05) from univariate
analyses of intraocular pressure (IOP) and tear
production of the right (OD) and left (OS) eyes in 102
Humboldt penguins (adults and chicks) from north- and
south-facing beaches.

  Variable   n    Mean   95% CI   Minimum-   P value
  Adult      90    30    29-32     14-42      <.001
  Chick      12    13    10-16      8-21
  2010       51    24    22-26      8-41      <.001
  2011       51    34    33-35     25-42
  North      28    26    23-30      8-42       .01
  South      74    31    29-32     14-41
  Adult      90    29    28-31     13-49      <.001
  Chick      12    13     9-16      3-20
  2010       51    21    19-24      3-37      <.001
  2011       51    35    33-36     26-49
  North      28    24    20-29      3-49       .01
  South      74    31    29-32     14-46
Tears OD
  Male       18    10     8-12      5-20       .02
  Female     20    7      6-8       2-15
Tears OS
  North      14    12    10-13      7-18      .006
  South      24    8      7-10      3-15
  Burrow     24    8      7-10      3-15      .006
  Crevice    14    12    10-13      7-18

Table 2. Summary of intraocular pressure (IOP) and tear production
data from studies by rebound (REB) or applanation (APP) tonometry
and the Schirmer tear test in nondomestic avian species.

                             IOP technique, mm Hg,
                             mean [+ or -] SD, range
Species                      (No. of eyes)

American flamingo (14)       REB 11.1 [+ or -] 2.3, 8-21 (28) OS
(Phoenicopterus ruber)
                             REB 10.9 [+ or -] 1.8, 7-15 (28) OD

American flamingo (20)       APP 16.1 [+ or -] 4.2, 7-22

                             REB 9.5 [+ or -] 1.7, 7-13 (34)

Bald eagle (12)              APP 21.5 [+ or -] 1.7, 15-26 (32)
(Haliaeetus leucocephalus)

Barn owl (17) (Tyto alba)    REB 10.8 [+ or -] 3.8, 5-16 (6)

Black-footed penguin (13)    REB 28.1 [+ or -] 6.8, 15-47 (17) OS
(Spheniscus demersus)
                             REB 30.4 [+ or -] 4.3, 21-3 (17) OD

Common buzzard (9)           APP 17.2 [+ or -] 3.5 (40)
(Buteo buteo)

Common kestrel (17)          REB 9.8 [+ or -] 2.5, 4-15 (141)
(Falco tinnunculus)

Eurasian eagle owl (17)      REB 10.5 [+ or -] 1.6, 7-14 (20)
(Bubo bubo)
                             APP 9.4 [+ or -] 1.8, 6-12 (20)

Eurasian sparrowhawk (17)    REB 15.5 [+ or -] 2.5, 10-23 (47)
(Accipiter nisus)

Eurasian tawny owl (9)       APP 11.2 [+ or -] 3.12 (40)
(Strix aluco)

Long-eared owl (17)          REB 7.8 [+ or -] 3.2, 4-13 (21)
(Asio otus)

Humboldt penguin             REB 28 [+ or -] 9, 3-49 (204)
(present study)

Humboldt penguin (18)        APP 20.4 [+ or -] 4.1, 10-27 (48)
(Spheniscus humboldti)

Northern goshawk (17)        REB 18.3 [+ or -] 3.8, 12-29 (58)
(Accipiter gentilis)

Ostrich (10)                 APP 18.8 [+ or -] 3.5, 12-24 (40)
(Struthio camelus)

Peregrine falcon (17)        REB 12.7 [+ or -] 5.8, 5-21 (7)
(Falco peregrinus)

Red kite (17)                REB 13 [+ or -] 5.5, 4-19 (8)
(Milvus milvus)

White-tailed                 REB 26.9 [+ or -] 5.8, 17-1 (29)
sea eagle (17)
(Haliaeetus albicilla)

                             Tear production, mm/min,
                             mean [+ or -] SD, range
Species                      (No. of eyes)

American flamingo (14)       --
(Phoenicopterus ruber)

American flamingo (20)       12.3 [+ or -] 4.5, 4-20 (34)

Bald eagle (12)              14 [+ or -] 2, 8-19 (32)
(Haliaeetus leucocephalus)

Barn owl (17) (Tyto alba)    --

Black-footed penguin (13)    --
(Spheniscus demersus)

Common buzzard (9)           12.5 [+ or -] 2.7 (40)
(Buteo buteo)

Common kestrel (17)          --
(Falco tinnunculus)

Eurasian eagle owl (17)      --
(Bubo bubo)

Eurasian sparrowhawk (17)    --
(Accipiter nisus)

Eurasian tawny owl (9)       3.12 [+ or -] 1.92 (40)
(Strix aluco)

Long-eared owl (17)          --
(Asio otus)

Humboldt penguin             9 [+ or -] 4, 2-20 (76)
(present study)

Humboldt penguin (18)        6.5 [+ or -] 2.9, 1-12 (48)
(Spheniscus humboldti)

Northern goshawk (17)        --
(Accipiter gentilis)

Ostrich (10)                 16.3 [+ or -] 2.5, 13-22.5 (40)
(Struthio camelus)

Peregrine falcon (17)        --
(Falco peregrinus)

Red kite (17)                --
(Milvus milvus)

White-tailed                 --
sea eagle (17)
(Haliaeetus albicilla)

Abbreviations: OD indicates right eye; OS, left eye.
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Article Details
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Author:Sheldon, Julie D.; Adkesson, Michael J.; Allender, Matthew C.; Jankowski, Gwen; Langan, Jennifer; Ca
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Date:Mar 1, 2017
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