Multi-Year Mortality Due to Staphylococcal Arthritis and Osteomyelitis with Sandspur-Associated Injury in Juvenile Black Skimmers (Rynchops niger) at Nesting Colonies in Southwest Florida, USA
Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Field and Clinical Observations
2.2. Postmortem Evaluation
2.3. Aerobic Bacterial Culture and Sensitivity Testing
2.4. Additional Laboratory Testing
3. Results
3.1. Demographic, Geographic, and Clinical Observations
3.2. Pathology
3.3. Bacteriology and Antimicrobial Sensitivity Testing
3.4. Other Ancillary Test Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Florida Fish and Wildlife Conservation Commission (FWC). A Species Action Plan for Four Imperiled Species of Beach-Nesting Birds; FWC: Tallahassee, FL, USA, 2013. [Google Scholar]
- Gochfeld, M.; Burger, J.; Lefevre, K.L. Black Skimmer (Rynchops niger), Version 1.0. In Birds of the World; Billerman, S.M., Ed.; Cornell Lab of Ornithology: Ithaca, NY, USA, 2020. [Google Scholar] [CrossRef]
- Rosenberg, K.V.; Dokter, A.M.; Blancher, P.J.; Sauer, J.R.; Smith, A.C.; Smith, P.A.; Stanton, J.C.; Panjabi, A.; Helft, L.; Parr, M.; et al. Decline of the North American avifauna. Science 2019, 366, 120–124. [Google Scholar] [CrossRef] [PubMed]
- Macrotrends, “Florida Population 1900–2023”. Available online: https://www.macrotrends.net/states/florida/population#:~:text=The%20population%20of%20Florida%20in,a%201.9%25%20increase%20from%202021 (accessed on 26 February 2024).
- Florida Fish and Wildlife Conservation Commission (FWC). Biological Status Review Report for the Black Skimmer (Rynchops niger); FWC: Tallahassee, FL, USA, 2011. [Google Scholar]
- Caliendo, V.; Lewis, N.S.; Pohlmann, A.; Baillie, S.R.; Banyard, A.C.; Beer, M.; Brown, I.H.; Fouchier, R.A.M.; Hansen, R.D.E.; Lameris, T.K.; et al. Transatlantic spread of highly pathogenic avian influenza H5N1 by wild birds from Europe to North America in 2021. Sci. Rep. 2022, 12, 11729. [Google Scholar] [CrossRef] [PubMed]
- U.S. Department of Agriculture, Animal and Plant Health Inspection Service. 2024 Detections of Highly Pathogenic Avian Influenza in Wild Birds. Available online: https://www.aphis.usda.gov/aphis/ourfocus/animalhealth/animal-disease-information/avian/avian-influenza/hpai-2022/2022-hpai-wild-birds (accessed on 20 September 2024).
- Shender, L.A.; Cody, T.; Ruder, M.; Fenton, H.; Niedringhaus, K.D.; Blanton, J.; Motes, J.; Schmedes, S.; Forys, E. Heavy rainfall, sewer overflows, and salmonellosis in black skimmers (Rynchops niger). Ecohealth 2022, 19, 203–215. [Google Scholar] [CrossRef]
- Sellers, B.; Smith, H.; Ferrell, J. Document SS-AGR-364. Identification and Control of Southern Sandbur (Cenchrus echinatus L.) in Hayfields. University of Florida, Institute of Food and Agricultural Sciences. 2018 (Revised). Available online: https://edis.ifas.ufl.edu/publication/AG373 (accessed on 27 February 2024).
- Florida Shorebird Alliance. Available online: https://flshorebirdalliance.org/ (accessed on 19 September 2024).
- Allison, A.B.; Mead, D.G.; Gibbs, S.E.; Hoffman, D.M.; Stallknecht, D.E. West Nile virus viremia in wild rock pigeons. Emerg. Infect. Dis. 2004, 10, 2252–2255. [Google Scholar] [CrossRef]
- Youk, S.; Torchetti, M.K.; Lantz, K.; Lenoch, J.B.; Killian, M.L.; Leyson, C.; Bevins, S.N.; Dilione, K.; Ip, H.S.; Stallknecht, D.E.; et al. H5N1 highly pathogenic avian influenza clade 2.3.4.4b in wild and domestic birds: Introductions into the United States and reassortments, December 2021–April 2022. Virology 2023, 587, 109860. [Google Scholar] [CrossRef]
- Kim, L.M.; Suarez, D.L.; Afonso, C.L. Detection of a broad range of class I and II Newcastle disease viruses using a multiplex real-time reverse transcription polymerase chain reaction assay. J. Vet. Diagn. Investig. 2008, 20, 414–425. [Google Scholar] [CrossRef]
- Das, A.; Spackman, E.; Pantin-Jackwood, M.J.; Suarez, D.L. Removal of real-time reverse transcription polymerase chain reaction (RT-PCR) inhibitors associated with cloacal swab samples and tissues for improved diagnosis of avian influenza virus by RT-PCR. J. Vet. Diagn. Investig. 2009, 21, 771–778. [Google Scholar] [CrossRef]
- Rebelo, A.R.; Parker, L.; Cai, H.Y. Use of high-resolution melting curve analysis to identify Mycoplasma species commonly isolated from ruminant, avian, and canine samples. J. Vet. Diagn. Investig. 2011, 23, 932–936. [Google Scholar] [CrossRef]
- Van Deventer, M.; (Florida Fish and Wildlife Conservation Commission [FWC], Naples, FL, USA); Brush, J.M.; (FWC, Fish and Wildlife Research Institute, Gainesville, FL, USA); Cox, A.; (FWC, Gainesville, FL, USA); Hardman, R.; (FWC, Fish and Wildlife Research Institute, St. Petersburg, FL, USA). Personal communication, 2024.
- De Luca, E.; Álvarez-Narváez, S.; Maboni, G.; Baptista, R.P.; Nemeth, N.M.; Niedringhaus, K.D.; Ladner, J.T.; Lorch, J.M.; Koroleva, G.; Lovett, S.; et al. Comparative genomics analyses support the reclassification of Bisgaard taxon 40 as Mergibacter gen. nov., with Mergibacter septicus sp. nov. as type species: Novel insights into the phylogeny and virulence factors of a Pasteurellaceae family member associated with mortality events in seabirds. Front. Microbiol. 2021, 12, 667356. [Google Scholar] [CrossRef]
- Niedringhaus, K.D.; Shender, L.A.; DiNuovo, A.; Flewelling, L.J.; Maboni, G.; Sanchez, S.; Deitschel, P.J.; Fitzgerald, J.; Nemeth, N.M. Mortality in common (Sterna hirundo) and sandwich (Thalasseus sandvicensis) terns associated with Bisgaard Taxon 40 infection on Marco Island, Florida, USA. J. Comp. Pathol. 2021, 184, 12–18. [Google Scholar] [CrossRef]
- Fink, D.; Auer, T.; Johnston, A.; Strimas-Mackey, M.; Ligocki, S.; Robinson, O.; Hochachka, W.; Jaromczyk, L.; Crowley, C.; Dunham, K.; et al. eBird Status and Trends, Data Version: 2022; Cornell Lab of Ornithology: Ithaca, NY, USA, 2023. [Google Scholar]
- Forys, E.A.; Hevesh, A.R. Investigating Black Skimmer Chick Diets Using Citizen Science and Digital Photography. Southeast. Nat. 2017, 16, 317–325. [Google Scholar] [CrossRef]
- Paleczny, M.; Hammill, E.; Karpouzi, V.; Pauly, D. Population trend of the world’s monitored seabirds, 1950–2010. PLoS ONE 2015, 10, e0129342. [Google Scholar] [CrossRef] [PubMed]
- Andreasen, C.B. Staphylococcosis. In Diseases of Poultry, 14th ed.; Swayne, D.E., Ed.; John Wiley & Sons, Inc.: Hoboken, NJ, USA, 2020; pp. 995–1003. [Google Scholar]
- National Oceanic and Atmospheric Administration (NOAA), “ASOS Climate Normals”. Available online: https://www.weather.gov/tbw/newnormals_asos (accessed on 25 July 2024).
- Heaton, C.J.; Gerbig, G.R.; Sensius, L.D.; Patel, V.; Smith, T.C. Staphylococcus aureus epidemiology in wildlife: A systematic review. Antibiotics 2020, 9, 89. [Google Scholar] [CrossRef] [PubMed]
- Topić, N.; Cenov, A.; Jozić, S.; Glad, M.; Mance, D.; Lušić, D.; Kapetanović, D.; Mance, D.; Vukić Lušić, D. Staphylococcus aureus—An additional parameter of bathing water quality for crowded urban beaches. Int. J. Environ. Res. Public Health 2021, 18, 5234. [Google Scholar] [CrossRef]
- Chambers, H.F.; Deleo, F.R. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat. Rev. Microbiol. 2009, 7, 629–641. [Google Scholar] [CrossRef]
- Esiobu, N.; Green, M.; Echeverry, A.; Bonilla, T.D.; Stinson, C.M.; Hartz, A.; Rogerson, A.; McCorquodale, D.S. High numbers of Staphylococcus aureus at three bathing beaches in South Florida. Int. J. Environ. Health Res. 2013, 23, 46–57. [Google Scholar] [CrossRef]
- Ralston, E.P.; Kite-Powell, H.; Beet, A. An estimate of the cost of acute health effects form food- and water-born marine pathogens and toxins in the United States. J. Water Health 2011, 9, 680–694. [Google Scholar] [CrossRef]
- Goodwin, K.D.; McNay, M.; Cao, Y.; Ebentier, D.; Madison, M.; Griffith, J.F. A multi-beach study of Staphylococcus aureus, MRSA, and enterococci in seawater and beach sand. Water Res. 2012, 46, 4195–4207. [Google Scholar] [CrossRef]
- Thapaliya, D.; Hellwig, E.J.; Kadariya, J.; Grenier, D.; Jefferson, A.J.; Dalman, M.; Kennedy, K.; DiPerna, M.; Orihill, A.; Taha, M.; et al. Prevalence and characterization of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus on public recreational beaches in northeast Ohio. Geohealth 2017, 1, 320–332. [Google Scholar] [CrossRef]
- Steele, K.E.; Linn, M.J.; Schoepp, R.J.; Komar, N.; Geisbert, T.W.; Manduca, R.M.; Calle, P.P.; Raphael, B.L.; Clippinger, T.L.; Larsen, T.; et al. Pathology of fatal West Nile virus infections in native and exotic birds during the 1999 outbreak in New York City, New York. Vet. Pathol. 2000, 37, 208–224. [Google Scholar] [CrossRef]
- Nemeth, N.M.; Ruder, M.G.; Poulson, R.L.; Sargent, R.; Breeding, S.; Evans, M.N.; Zimmerman, J.; Hardman, R.; Cunningham, M.; Gibbs, S.; et al. Bald eagle mortality and nest failure due to clade 2.3.4.4 highly pathogenic H5N1 influenza a virus. Sci. Rep. 2023, 13, 191. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Hall, J.S.; Franson, J.C.; Gill, R.E.; Meteyer, C.U.; TeSlaa, J.L.; Nashold, S.; Dusek, R.J.; Ip, H.S. Experimental challenge and pathology of highly pathogenic avian influenza virus H5N1 in dunlin (Calidris alpina), an intercontinental migrant shorebird species. Influenza Other Respir. Viruses 2011, 5, 365–372. [Google Scholar] [CrossRef] [PubMed]
- Pardo-Roa, C.; Nelson, M.I.; Ariyama, N.; Aguayo, C.; Almonacid, L.I.; Munoz, G.; Navarro, C.; Avila, C.; Ulloa, M.; Reyes, R.; et al. Cross-species transmission and PB2 mammalian adaptations of highly pathogenic avian influenza A/H5N1 viruses in Chile. bioRxiv 2023. [Google Scholar] [CrossRef]
- Acevedo-Whitehouse, K.; Duffus, A.L. Effects of environmental change on wildlife health. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2009, 364, 3429–3438. [Google Scholar] [CrossRef]
- Charlton-Howard, H.S.; Bond, A.L.; Rivers-Auty, J.; Lavers, J.L. ‘Plasticosis’: Characterizing macro- and microplastic-associated fibrosis in seabird tissues. J. Hazard. Mater. 2023, 450, 131090. [Google Scholar] [CrossRef]
- Klasing, K.C.; Korver, D.R. Nutritional Diseases. In Diseases of Poultry, 14th ed.; Swayne, D.E., Ed.; John Wiley & Sons, Inc.: Hoboken, NJ, USA, 2020; pp. 1257–1285. [Google Scholar]
- Fauquier, D.A.; Flewelling, L.J.; Maucher, J.M.; Keller, M.; Kinsel, M.J.; Johnson, C.K.; Henry, M.; Gannon, J.G.; Ramsdell, J.S.; Landsberg, J.H. Brevetoxicosis in seabirds naturally exposed to Karenia brevis blooms along the central west coast of Florida. J. Wildl. Dis. 2013, 49, 246–260. [Google Scholar] [CrossRef]
ID | Location, County | Date Died/Euthanized | Age | Sex | General Gross/ Histologic Lesion Pattern 1−3 | Skin Wounds or Sandspurs 5 | S. aureus Cultured from Joint | S. aureus Cultured from Viscera | Brevetoxins (ng/g) (Tissue[s] Tested) 6 |
---|---|---|---|---|---|---|---|---|---|
Colonies affected by staphylococcal arthritis (southwest coast) | |||||||||
W20-456A | Marco Island, Collier | 23 August 2020 | Juvenile | Female | A, D | S | Yes | No (liver) | U (L) |
W20-456B | Marco Island, Collier | 23 August 2020 | Juvenile | Male | A, D | S | Yes | No (liver) | U (L) |
W20-456C | Marco Island, Collier | 23 August 2020 | Juvenile | Male | A, D | P | NT | NT | U (L) |
W20-456D | Marco Island, Collier | 23 August 2020 | Juvenile | Unknown | A, D | S | NT | NT | NT |
W20-456E | Marco Island, Collier | 23 August 2020 | Juvenile | Unknown | A, D | S, P | NT | NT | NT |
W21-481A 3 | Marco Island, Collier | 20 July 2021 | Juvenile | Male | A, D | SS | Yes | NT | U (L, K) |
W21-481B 3 | Marco Island, Collier | 20 July 2021 | Juvenile | Male | A, D | SS | Yes | NT | U (L, K) |
W21-481C | Marco Island, Collier | 22 July 2021 | Juvenile | Male | A, DB | None | Yes | Yes (kidney) | U (L, K) |
W21-481D | Marco Island, Collier | 22 July 2021 | Juvenile | Male | A, D | P | Yes | NT | U (L, K) |
W21-481E 3,7 | Marco Island, Collier | 22 July 2021 | Adult | Male | N | None | NT | NT | NT |
W21-517B 3,7 | Little Estero Island, Fort Myers Beach, Lee | 22 July 2021 | Juvenile | Male | A, D | SS, S, P | Yes | No (lung) | U (L, K) |
W21-517C 3,7 | Little Estero Island, Fort Myers, Lee | 22 July 2021 | Juvenile | Male | A, D | SS, S, P | Yes | Yes (lung) | U (L, K, V) |
W21-673A 3,7,9 | Fort Myers, Lee | 21 September 2021 | Juvenile | Unknown | A, D, DB | SS, S, P | Yes | Yes (lung) | 19.9 (K) |
W21-673B 3,7,9 | Marco Island, Collier | 21 September 2021 | Juvenile | Unknown | A, D, DB | P | Yes | Yes (lung) | NT |
W21-673D 3,7,9 | Marco Island, Collier | 21 September 2021 | Juvenile | Male | A, D | SS, P | Yes | Yes (lung) | NT |
W21-673E 3,7,9 | Marco Island, Collier | 21 September 2021 | Juvenile | Unknown | A, D 4 | None | Yes | NT | U (K) |
W21-673G 3,7,9 | Fort Myers, Lee | 21 September 2021 | Juvenile | Unknown | A, D | SS, S | Yes | Yes (lung) | U (K) |
W21-673H 3,7,9 | Fort Myers, Lee | 21 September 2021 | Juvenile | Male | A, D, DB 4 | SS, S | Yes | Yes (lung) | NT |
W21-673I 3,7,9 | Unknown | 21 September 2021 | Juvenile | Unknown | A, D | S | Yes | Yes (lung) | NT |
W22-520A | Carlos Beach, Lee | 13 July 2022 | Juvenile | Female | A, D, DB | U | Yes | Yes (kidney) | 12 (IC); U (L, K, VC) |
W22-520B | Carlos Beach, Lee | 13 July 2022 | Juvenile | Unknown | A, D | U | Yes | NT | U (L, K, IC, VC) |
W22-520C | Carlos Beach, Lee | 13 July 2022 | Juvenile | Unknown | A, D, DB | P | Yes | Yes (kidney); No (lung) | U (L, K, IC, VC) |
W22-647 | Big Marco Island, Collier | 23 August 2022 | Juvenile | Male | DB | None | NT | NT | NT |
Distant colonies unaffected by staphylococcal arthritis (northwest coast) | |||||||||
W21-673C 3 | Lido Key Beach, Sarasota | 21 September 2021 | Juvenile | Unknown | N | None | NT | Yes (lung) | 41.4 (K) |
W21-673F | Lido Key Beach, Sarasota | 21 September 2021 | Juvenile | Unknown | D | None | No | NT | 22.5 (K) |
W22-410A | Lido Beach, Sarasota | 7 June 2022 | Adult | Female | N | None | NT | No (liver) | U (L, K, IC) 8 |
W22-410B | Lido Beach, Sarasota | 7 June 2022 | Juvenile | Unknown | N | None | NT | NT | NT |
W22-486 | Lido Beach, Sarasota | 1 July 2022 | Juvenile | Female | N | None | NT | NT | NT |
W22-645 3 | Redington Shores, Pinellas | 23 August 2022 | Juvenile | Unknown | N | P | NT | NT | NT |
W23-482A | Lido Key Beach, Sarasota | 12 July 2023 | Juvenile | Female | D | SS, P | NT | No (lung) | U (L, V, I) |
W23-482B | Lido Key Beach, Sarasota | 12 July 2023 | Juvenile | Male | D | P | No | No (liver) | U (L, V, I) |
W23-482C | Lido Key Beach, Sarasota | 12 July 2023 | Juvenile | Male | D | P | NT | No (lung, cloacal bursa) | 8.2 (I); U (L, V) |
W23-482D | Lido Key Beach, Sarasota | 12 July 2023 | Juvenile | Female | D | SS, S, P | NT | No (lung) | 14.2 (L); U (V, I) |
W23-482E | Lido Key Beach, Sarasota | 12 July 2023 | Juvenile | Unknown | N | None | NT | NT | NT |
W23-482F | Lido Key Beach, Sarasota | 12 July 2023 | Juvenile | Unknown | N | S, P | NT | NT | NT |
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Nemeth, N.M.; Brush, J.M.; Cox, W.A.; Hardman, R.; Piersma, B.; Troiano, A.; Barron, H.W.; Kunkel, M.R.; Goodwin, C.C.; Weyna, A.A.W.; et al. Multi-Year Mortality Due to Staphylococcal Arthritis and Osteomyelitis with Sandspur-Associated Injury in Juvenile Black Skimmers (Rynchops niger) at Nesting Colonies in Southwest Florida, USA. Vet. Sci. 2024, 11, 578. https://doi.org/10.3390/vetsci11110578
Nemeth NM, Brush JM, Cox WA, Hardman R, Piersma B, Troiano A, Barron HW, Kunkel MR, Goodwin CC, Weyna AAW, et al. Multi-Year Mortality Due to Staphylococcal Arthritis and Osteomyelitis with Sandspur-Associated Injury in Juvenile Black Skimmers (Rynchops niger) at Nesting Colonies in Southwest Florida, USA. Veterinary Sciences. 2024; 11(11):578. https://doi.org/10.3390/vetsci11110578
Chicago/Turabian StyleNemeth, Nicole M., Janell M. Brush, W. Andrew Cox, Rebecca Hardman, Brittany Piersma, Alexandra Troiano, Heather W. Barron, Melanie R. Kunkel, Chloe C. Goodwin, Alisia A. W. Weyna, and et al. 2024. "Multi-Year Mortality Due to Staphylococcal Arthritis and Osteomyelitis with Sandspur-Associated Injury in Juvenile Black Skimmers (Rynchops niger) at Nesting Colonies in Southwest Florida, USA" Veterinary Sciences 11, no. 11: 578. https://doi.org/10.3390/vetsci11110578
APA StyleNemeth, N. M., Brush, J. M., Cox, W. A., Hardman, R., Piersma, B., Troiano, A., Barron, H. W., Kunkel, M. R., Goodwin, C. C., Weyna, A. A. W., McKinney, A. S., Teo, X. H., Radisic, R., Shender, L. A., Sanchez, S., & van Deventer, M. (2024). Multi-Year Mortality Due to Staphylococcal Arthritis and Osteomyelitis with Sandspur-Associated Injury in Juvenile Black Skimmers (Rynchops niger) at Nesting Colonies in Southwest Florida, USA. Veterinary Sciences, 11(11), 578. https://doi.org/10.3390/vetsci11110578