Preliminary Examination of Skin Lesions on Bottlenose...

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Preliminary Examination of Skin Lesions on Bottlenose Dolphins (Tursiops truncatus) in the Outer Banks, North Carolina Jessica Taylor 1 , Leslie Hart 2 , Holly Krumsick 1 , and Jeff Adams 3 1 Outer Banks Center for Dolphin Research, 2 NOAA/NOS/NCCOS, 3 National Marine Fisheries Service ABSTRACT Bottlenose dolphins (Tursiops truncatus) are sentinels of environmental health. Monitoring the health of dolphin populations provides insight into local environmental conditions. Skin lesions, which can be observed through photo-identification, can indicate viral, bacterial, or fungal disease and may be linked to contaminant exposure and used to infer population health. This study presents a preliminary examination of skin lesion prevalence and classification of estuarine bottlenose dolphins in the Outer Banks, NC using photo-identification. Dedicated boat-based transect surveys were conducted monthly in Roanoke Sound from April through October 2012, using standardized photo-identification techniques. Sighting data and dorsal fin images were processed using FinBase. High quality images of distinctive fins were examined for the presence and type of skin lesions. A minimum estimate revealed that 44% of the animals screened (n=83) exhibited at least one of 7 different types of skin lesions, with pale lesions being the most common type observed (P=0.46). At least 1/3 of the animals screened presented multiple types of lesions. The greatest prevalence of lesions occurred in the spring (P=0.75; p<0.001). A residency analysis revealed 83% of the seasonal residents (n=5) and 71% of the transients (n=10) observed in the spring exhibited lesions, suggesting residency does not contribute to seasonal lesion presence. The skin lesions occurring on Roanoke Sound dolphins are similar in frequency and type to those observed on other east coast populations. The methods used in this study are suitable for further examination of skin lesions on dolphins in this area. Seasonal occurrence of lesions observed may result from the influence of lower water temperature in the spring. Future studies should focus on expanding the current dataset to further examine the seasonal prevalence of lesions, relationship between residency and lesions, and correlations between lesion presence and environmental factors. Figure 1: Roanoke Sound Study Area INTRODUCTION As long-lived top predators, bottlenose dolphins are key indicators of marine environmental health (Wells et al. 2004). Skin lesions have been identified on various species of cetaceans (Hart et al. 2012; Van Bressem et al. 2007); these lesions may provide evidence of bacterial, viral, or fungal disease within individuals (Hart et al. 2012) or the effects of local environmental contaminants (Wilson et al. 1999). This study represents a preliminary examination of skin lesions on bottlenose dolphins in Roanoke Sound, North Carolina. Insight into the health of these dolphins and their environment aids in further understanding stock status and designing appropriate conservation measures. OBJECTIVES 1) Use photo-identification data to estimate the prevalence of skin lesions that occur on bottlenose dolphins in the Outer Banks and compare seasonal estimates 2) Classify the types of skin lesions observed on bottlenose dolphins in the Outer Banks 3) Compare the prevalence of lesions between dolphins of different residency patterns in this area STUDY AREA The study area encompassed the entirety of Roanoke Sound, approximately 41 square miles from the northern tip of Roanoke Island south to Oregon Inlet (Figure 1). Roanoke Sound separates Roanoke Island from Nags Head and is heavily used for recreational fishing, boating, and swimming. METHODS Conducted monthly transect surveys from a 16’ outboard vessel from April through October 2012. Used standard photo-identification techniques for photographing dorsal fins (Wϋrsig and Wϋrsig 1977). Seasons determined based upon water temperature: Spring (April, May), Summer (June, July, August), Fall (September, October). Used FinBase (Adams et al. 2006) for storage, management, and analysis of sighting data and dorsal fin images. Visually screened original images for lesions. Scored each image for photo quality and rated the distinctiveness of each dorsal fin (Urian et al. 1999). Excluded poor quality images and low/not distinct fins from analysis Calculated overall and seasonal lesion prevalence (P) using the equation: P = (# individuals with lesions)/(# total individuals examined). Classified lesion types according to Hart (2011). Defined major lesion types as prevalence greater than 0.15 (Hart et al. 2012). Seasonal residents were sighted in the study area across years during one or more seasons. Transients were sighted in the study area during only one season (Zolman 2002). Calculated overall and seasonal prevalence for both residency patterns. Compared seasonal prevalence estimates using a Fisher’s Exact Test with a Bonferroni correction for multiple comparisons (α=0.0167). Compared major lesion types using a Fisher’s Exact Test with a Bonferroni correction for multiple comparisons (α=0.0167). RESULTS We screened 240 digital images of 83 distinct individuals for the presence of skin lesions. Of these individuals, 37 (P=0.45; 95% CI: 0.34-0.55) were observed with visible lesions. Skin lesions were most prevalent in the spring (P=0.75) and least prevalent during the summer (P=0.15; p<0.001) (Figure 2). 35% of the individuals identified within this study (n=29) were classified as seasonal residents and 52% (n=43) as transients. A subset of individuals (13%; n=11) did not fit within either of these categories and were excluded from this analysis. Skin lesion prevalence of seasonal residents and transients varied by season as did composition of residency patterns (Figure 3). Seven different types of lesions were observed, with 3 representing major lesion types (Figure 4). These major lesion types included black lesions (n=11; P=0.30), dark-fringed lesions (n=10; P=0.27), and pale lesions (n=17; P=0.46) (Figures 5a-5c). Approximately 1/3 of individuals observed with lesions presented more than one type. DISCUSSION This preliminary study represents the first formal examination of residency patterns in the Outer Banks. Anecdotal evidence suggests long term site fidelity of individuals to this area. Further investigation should examine residency across years and relationships between residency patterns and lesion occurrence. Seasonal differences in lesion prevalence suggest an environmental influence on their occurrence. This influence is supported by lack of significant difference in lesion prevalence be- tween seasonal residents and transients within seasons. Previous studies (Hart et al. 2012; Wilson et al. 1999) found the presence of lesions to be associated with lower water temper- ature and salinity. Future studies should focus on expanding the current dataset to further examine seasonal prevalence of lesions, the relationship between lesions and seasonal changes in water temperature and salinity, and other potential influences on lesion occurrence in the Outer Banks. Skin lesions were comparable in type and prevalence to occurrences observed in other areas of the East Coast (Hart et al. 2012; Wilson et al. 1999). Dolphins examined in this study are included in the Northern North Carolina estuarine system stock (NNCES), which was affected by the Unusual Mortality Event (UME) of 2013. A greater understanding of popula- tion health and residency patterns in this area aids in stock conservation. ACKNOWLEDGEMENTS We would like to thank OBXCDR volunteers and interns for assistance with field surveys, Todd Speakman for aid in creating transect survey routes, Jay Taylor for assistance in creating graphs and dorsal fin matching, John Kerner for assistance with boat maintenance, and Eric Zolman for advice on defining residency patterns. Funding was provided by fundraisers and private donations of the Outer Banks Center for Dolphin Research. Field research was conducted under a GA permit awarded to J. Taylor (LOC#13416). LITERATURE CITED Adams, J.D., T. Speakman, E. Zolman, and L.H. Schwacke. 2006. Automating image matching, cataloging, and analysis for photo-identification research. Aquatic Mammals 32(3): 374-384. Hart, L.B. 2011. The use of longitudinal and cross-sectional photographic data to study skin disease in wild bottlenose dolphins (Tursiops truncatus). Doctor of Philosophy, Medical University of South Carolina, Charleston, SC Hart, L.B., D.S. Rotstein, R.S. Wells, J. Allen, A. Barleycorn, B.C. Balmer, S.M. Lane, T. Speakman, E.S. Zolman, M. Stolen, W. McFee, T. Goldstein, T.K. Rowles, and L.H. Schwacke. 2012. Skin lesions on common bottlenose dolphins (Tursiops truncatus) from three sites in the northwest Atlantic, USA. PLoS One 7(3): e33081. doi:10.1371/journal.pone.0033081. Van Bressem, M., K.V. Waerebeek, J.C. Reyes, F. Felix, M. Echegaray, S. Siciliano, A.P. Di Beneditto, L. Flach, F. Viddi, I.C. Avila, J.C. Herrera, I.C. Tobόn, J. Bolaños-Jiménez, I.B. Moreno, P.H. Ott, G.P. Sanino, E. Castineira, D. Montes, E. Crespo, P.A.C. Flores, B. Haase, S.M.F Mendonça de Souza, M. Laeta, and A.B. Fragoso. 2007. A preliminary overview of skin and skeletal diseases and traumata in small cetaceans from South American waters. Lajam 6(1): 7-42. Urian, K.W., A.A. Hohn, and L.J. Hansen. 1999. Status of the photo-identification catalog of coastal bottlenose dolphins of the Western North Atlantic. Report of a workshop of catalog contributors. NOAA Administrative Re- port NMFS-SEFSC-425, 22pp. Wells, R.S., Rhinehart, H.L., Hansen, L.J., Sweeney, J.C., Townsend, F.I., Stone, R., Casper, D.R., Scott, M.D., Hohn, A.A., and T.K. Rowles. 2004. Bottlenose dolphins as marine ecosystem sentinels: Developing a health moni- toring system. EcoHealth 1:246-254. Wilson, B., H. Arnold, G. Bearzi, C.M. Fortuna, R. Gaspar, S. Ingram, C. Liret, S. Pribanić, A.J. Read, V. Ridoux, K. Schneider, K.W. Urian, R.S. Wells, C. Wood, P.M. Thompson, and P.S. Hammond. 1999. Epidermal diseases in bottlenose dolphins: impacts of natural and anthropogenic factors. Proc. R. Soc. Lond. B 266:1077-1083. Würsig, B. and M. Würsig. 1977. The photographic determination of group size, composition and stability of coastal porpoises, Tursiops truncatus. Science 198:755756. Zolman, E.S. 2002. Residence patterns of bottlenose dolphins (Tursiops truncatus) in the Stono River Estuary, Charleston County, South Carolina, U.S.A. Marine Mammal Science 18(4): 879-892. Figure 5a: Black Lesion Figure 5b: Dark Fringed Lesion Figure 5c: Pale Lesion Figure 2: Seasonal Lesion Prevalence 0.75 0.15 0.42 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 Spring Summer Fall Lesion Prevalence Seasonal Lesion Prevalence p < 0.001 Figure 4: Prevalence of Major Lesion Types 0.30 0.27 0.46 0 0.05 0.1 0.15 0.2 0.25 0.3 0.35 0.4 0.45 0.5 Black Dark-fringed Pale Lesion Prevalence Prevalence of Major Lesion Types Figure 3: Seasonal Lesion Prevalence of Residents and Transients

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Preliminary Examination of Skin Lesions on Bottlenose Dolphins (Tursiops

truncatus) in the Outer Banks, North Carolina

Jessica Taylor1, Leslie Hart2, Holly Krumsick1, and Jeff Adams3

1Outer Banks Center for Dolphin Research, 2NOAA/NOS/NCCOS, 3National Marine Fisheries Service

ABSTRACT

Bottlenose dolphins (Tursiops truncatus) are sentinels of environmental health. Monitoring the health of dolphin populations provides insight into local environmental conditions. Skin lesions, which

can be observed through photo-identification, can indicate viral, bacterial, or fungal disease and may be linked to contaminant exposure and used to infer population health. This study presents a

preliminary examination of skin lesion prevalence and classification of estuarine bottlenose dolphins in the Outer Banks, NC using photo-identification. Dedicated boat-based transect surveys were

conducted monthly in Roanoke Sound from April through October 2012, using standardized photo-identification techniques. Sighting data and dorsal fin images were processed using FinBase. High

quality images of distinctive fins were examined for the presence and type of skin lesions. A minimum estimate revealed that 44% of the animals screened (n=83) exhibited at least one of 7 different

types of skin lesions, with pale lesions being the most common type observed (P=0.46). At least 1/3 of the animals screened presented multiple types of lesions. The greatest prevalence of lesions

occurred in the spring (P=0.75; p<0.001). A residency analysis revealed 83% of the seasonal residents (n=5) and 71% of the transients (n=10) observed in the spring exhibited lesions, suggesting

residency does not contribute to seasonal lesion presence. The skin lesions occurring on Roanoke Sound dolphins are similar in frequency and type to those observed on other east coast populations.

The methods used in this study are suitable for further examination of skin lesions on dolphins in this area. Seasonal occurrence of lesions observed may result from the influence of lower water

temperature in the spring. Future studies should focus on expanding the current dataset to further examine the seasonal prevalence of lesions, relationship between residency and lesions, and

correlations between lesion presence and environmental factors.

Figure 1: Roanoke Sound Study Area

INTRODUCTION

As long-lived top predators, bottlenose dolphins are key indicators of marine environmental health (Wells et al.

2004).

Skin lesions have been identified on various species of cetaceans (Hart et al. 2012; Van Bressem et al. 2007); these

lesions may provide evidence of bacterial, viral, or fungal disease within individuals (Hart et al. 2012) or the effects

of local environmental contaminants (Wilson et al. 1999).

This study represents a preliminary examination of skin lesions on bottlenose dolphins in Roanoke Sound, North

Carolina.

Insight into the health of these dolphins and their environment aids in further understanding stock status and

designing appropriate conservation measures.

OBJECTIVES

1) Use photo-identification data to estimate the prevalence of skin lesions that occur on bottlenose dolphins in the

Outer Banks and compare seasonal estimates

2) Classify the types of skin lesions observed on bottlenose dolphins in the Outer Banks

3) Compare the prevalence of lesions between dolphins of different residency patterns in this area

STUDY AREA

The study area encompassed the entirety of Roanoke Sound, approximately 41 square miles from the northern tip

of Roanoke Island south to Oregon Inlet (Figure 1).

Roanoke Sound separates Roanoke Island from Nags Head and is heavily used for recreational fishing, boating,

and swimming.

METHODS

Conducted monthly transect surveys from a 16’ outboard vessel from

April through October 2012. Used standard photo-identification

techniques for photographing dorsal fins (Wϋrsig and Wϋrsig 1977).

Seasons determined based upon water temperature: Spring (April,

May), Summer (June, July, August), Fall (September, October).

Used FinBase (Adams et al. 2006) for storage, management, and

analysis of sighting data and dorsal fin images.

Visually screened original images for lesions. Scored each image for

photo quality and rated the distinctiveness of each dorsal fin (Urian

et al. 1999). Excluded poor quality images and low/not distinct fins

from analysis

Calculated overall and seasonal lesion prevalence (P) using the

equation: P = (# individuals with lesions)/(# total individuals

examined). Classified lesion types according to Hart (2011). Defined

major lesion types as prevalence greater than 0.15 (Hart et al. 2012).

Seasonal residents were sighted in the study area across years during

one or more seasons. Transients were sighted in the study area

during only one season (Zolman 2002). Calculated overall and

seasonal prevalence for both residency patterns.

Compared seasonal prevalence estimates using a Fisher’s Exact Test

with a Bonferroni correction for multiple comparisons (α=0.0167).

Compared major lesion types using a Fisher’s Exact Test with a

Bonferroni correction for multiple comparisons (α=0.0167).

RESULTS

We screened 240 digital images of 83 distinct individuals for the presence of skin lesions. Of these individuals, 37 (P=0.45; 95% CI: 0.34-0.55) were observed with visible lesions.

Skin lesions were most prevalent in the spring (P=0.75) and least prevalent during the summer (P=0.15; p<0.001) (Figure 2).

35% of the individuals identified within this study (n=29) were classified as seasonal residents and 52% (n=43) as transients. A subset of individuals (13%; n=11) did not fit within either of

these categories and were excluded from this analysis.

Skin lesion prevalence of seasonal residents and transients varied by season as did composition of residency patterns (Figure 3).

Seven different types of lesions were observed, with 3 representing major lesion types (Figure 4). These major lesion types included black lesions (n=11; P=0.30), dark-fringed lesions

(n=10; P=0.27), and pale lesions (n=17; P=0.46) (Figures 5a-5c). Approximately 1/3 of individuals observed with lesions presented more than one type.

DISCUSSION

This preliminary study represents the first formal examination of residency patterns in the Outer Banks. Anecdotal evidence suggests long term site fidelity of individuals to this area.

Further investigation should examine residency across years and relationships between residency patterns and lesion occurrence.

Seasonal differences in lesion prevalence suggest an environmental influence on their occurrence. This influence is supported by lack of significant difference in lesion prevalence be-

tween seasonal residents and transients within seasons. Previous studies (Hart et al. 2012; Wilson et al. 1999) found the presence of lesions to be associated with lower water temper-

ature and salinity. Future studies should focus on expanding the current dataset to further examine seasonal prevalence of lesions, the relationship between lesions and seasonal

changes in water temperature and salinity, and other potential influences on lesion occurrence in the Outer Banks.

Skin lesions were comparable in type and prevalence to occurrences observed in other areas of the East Coast (Hart et al. 2012; Wilson et al. 1999). Dolphins examined in this study

are included in the Northern North Carolina estuarine system stock (NNCES), which was affected by the Unusual Mortality Event (UME) of 2013. A greater understanding of popula-

tion health and residency patterns in this area aids in stock conservation.

ACKNOWLEDGEMENTS

We would like to thank OBXCDR volunteers

and interns for assistance with field surveys,

Todd Speakman for aid in creating transect

survey routes, Jay Taylor for assistance in

creating graphs and dorsal fin matching, John

Kerner for assistance with boat maintenance,

and Eric Zolman for advice on defining

residency patterns. Funding was provided by

fundraisers and private donations of the Outer

Banks Center for Dolphin Research. Field

research was conducted under a GA permit

awarded to J. Taylor (LOC#13416).

LITERATURE CITED

Adams, J.D., T. Speakman, E. Zolman, and L.H. Schwacke. 2006. Automating image matching, cataloging, and analysis for photo-identification research. Aquatic Mammals 32(3): 374-384.

Hart, L.B. 2011. The use of longitudinal and cross-sectional photographic data to study skin disease in wild bottlenose dolphins (Tursiops truncatus). Doctor of Philosophy, Medical University of South Carolina, Charleston, SC

Hart, L.B., D.S. Rotstein, R.S. Wells, J. Allen, A. Barleycorn, B.C. Balmer, S.M. Lane, T. Speakman, E.S. Zolman, M. Stolen, W. McFee, T. Goldstein, T.K. Rowles, and L.H. Schwacke. 2012. Skin lesions on common bottlenose

dolphins (Tursiops truncatus) from three sites in the northwest Atlantic, USA. PLoS One 7(3): e33081. doi:10.1371/journal.pone.0033081.

Van Bressem, M., K.V. Waerebeek, J.C. Reyes, F. Felix, M. Echegaray, S. Siciliano, A.P. Di Beneditto, L. Flach, F. Viddi, I.C. Avila, J.C. Herrera, I.C. Tobόn, J. Bolaños-Jiménez, I.B. Moreno, P.H. Ott, G.P. Sanino, E. Castineira,

D. Montes, E. Crespo, P.A.C. Flores, B. Haase, S.M.F Mendonça de Souza, M. Laeta, and A.B. Fragoso. 2007. A preliminary overview of skin and skeletal diseases and traumata in small cetaceans from South American waters.

Lajam 6(1): 7-42.

Urian, K.W., A.A. Hohn, and L.J. Hansen. 1999. Status of the photo-identification catalog of coastal bottlenose dolphins of the Western North Atlantic. Report of a workshop of catalog contributors. NOAA Administrative Re-

port NMFS-SEFSC-425, 22pp.

Wells, R.S., Rhinehart, H.L., Hansen, L.J., Sweeney, J.C., Townsend, F.I., Stone, R., Casper, D.R., Scott, M.D., Hohn, A.A., and T.K. Rowles. 2004. Bottlenose dolphins as marine ecosystem sentinels: Developing a health moni-

toring system. EcoHealth 1:246-254.

Wilson, B., H. Arnold, G. Bearzi, C.M. Fortuna, R. Gaspar, S. Ingram, C. Liret, S. Pribanić, A.J. Read, V. Ridoux, K. Schneider, K.W. Urian, R.S. Wells, C. Wood, P.M. Thompson, and P.S. Hammond. 1999. Epidermal diseases in

bottlenose dolphins: impacts of natural and anthropogenic factors. Proc. R. Soc. Lond. B 266:1077-1083.

Würsig, B. and M. Würsig. 1977. The photographic determination of group size, composition and stability of coastal porpoises, Tursiops truncatus. Science 198:755‑756.

Zolman, E.S. 2002. Residence patterns of bottlenose dolphins (Tursiops truncatus) in the Stono River Estuary, Charleston County, South Carolina, U.S.A. Marine Mammal Science 18(4): 879-892.

Figure 5a: Black Lesion Figure 5b: Dark Fringed Lesion Figure 5c: Pale Lesion

Figure 2: Seasonal Lesion Prevalence

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Figure 4: Prevalence of Major Lesion Types

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Figure 3: Seasonal Lesion Prevalence of Residents and Transients