{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T21:14:43Z","timestamp":1792790083421,"version":"4.5.0"},"reference-count":38,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2024,11,18]],"date-time":"2024-11-18T00:00:00Z","timestamp":1731888000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"State of Florida\u2019s Nongame Trust Fund Conserve Wildlife","award":["23-04"],"award-info":[{"award-number":["23-04"]}]},{"name":"State of Florida\u2019s Nongame Trust Fund Conserve Wildlife","award":["F23AP00163"],"award-info":[{"award-number":["F23AP00163"]}]},{"name":"Fish and Wildlife Foundation of Florida","award":["23-04"],"award-info":[{"award-number":["23-04"]}]},{"name":"Fish and Wildlife Foundation of Florida","award":["F23AP00163"],"award-info":[{"award-number":["F23AP00163"]}]},{"name":"USFWS Zoonotic Disease Initiative","award":["23-04"],"award-info":[{"award-number":["23-04"]}]},{"name":"USFWS Zoonotic Disease Initiative","award":["F23AP00163"],"award-info":[{"award-number":["F23AP00163"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Veterinary Sciences"],"abstract":"<jats:p>The black skimmer (Rynchops niger) is a state-threatened, colonially nesting seabird in Florida, USA. Conservation threats include habitat alteration, human disturbances, severe weather, and predation. During nest monitoring (May\u2013September, 2020\u20132022), black skimmer juveniles at colonies on Fort Myers Beach and Marco Island, Florida, had polyarthritis and died or were euthanized due to severe illness. Similarly-aged skimmers from geographically distant (considered unaffected) colonies were evaluated for comparison (2021\u20132023). We documented field, clinical, radiographical, and pathological findings to characterize disease and purported pathogenesis. The majority were lame and lethargic, in poor nutritional condition, and dehydrated. Additionally, 8\/23 of the skimmers with dermatitis and arthritis from affected colonies also had penetrating sandspurs associated with skin ulceration, scabbing, and\/or hemorrhage. The affected joints were often in limbs (interphalangeal and hock; less commonly stifle, elbow, carpus). A postmortem evaluation and bacteriology revealed Staphylococcal aureus-associated dermatitis, arthritis, tenosynovitis, and\/or osteomyelitis in 21\/22 of the juvenile skimmers from southwestern nest colonies. Staphylococcus aureus dissemination to internal organs occurred in 10\/13 of the skimmers tested. Among skimmers evaluated from distant colonies, 5\/10 that were examined histologically had skin crusting and inflammation but lacked arthritis. Occasional coinfections were documented (e.g., West Nile virus, Gram-negative bacilli). The results suggest that staphylococcal joint disease originated from sandspur-induced skin damage, followed by hematogenous dissemination to the joints and, occasionally, the internal organs. Additional nest sites should be tested to evaluate disease risk and potentially contributing environmental factors. We recommend that site managers employ techniques that reduce the risk of skimmer interactions with sandspurs.<\/jats:p>","DOI":"10.3390\/vetsci11110578","type":"journal-article","created":{"date-parts":[[2024,11,19]],"date-time":"2024-11-19T10:44:37Z","timestamp":1732013077000},"page":"578","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["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"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5931-175X","authenticated-orcid":false,"given":"Nicole M.","family":"Nemeth","sequence":"first","affiliation":[{"name":"Southeastern Cooperative Wildlife Disease Study, University of Georgia, Athens, GA 30602, USA"},{"name":"Department of Pathology, University of Georgia, Athens, GA 30602, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Janell M.","family":"Brush","sequence":"additional","affiliation":[{"name":"Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, Gainesville, FL 32611, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"W. Andrew","family":"Cox","sequence":"additional","affiliation":[{"name":"Florida Fish and Wildlife Conservation Commission, Gainesville, FL 32601, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9083-8525","authenticated-orcid":false,"given":"Rebecca","family":"Hardman","sequence":"additional","affiliation":[{"name":"Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, St. Petersburg, FL 33701, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brittany","family":"Piersma","sequence":"additional","affiliation":[{"name":"Florida Fish and Wildlife Conservation Commission, Naples, FL 32601, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexandra","family":"Troiano","sequence":"additional","affiliation":[{"name":"Clinic for the Rehabilitation of Wildlife, Sanibel, FL 33957, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Heather W.","family":"Barron","sequence":"additional","affiliation":[{"name":"Clinic for the Rehabilitation of Wildlife, Sanibel, FL 33957, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Melanie R.","family":"Kunkel","sequence":"additional","affiliation":[{"name":"Southeastern Cooperative Wildlife Disease Study, University of Georgia, Athens, GA 30602, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2181-018X","authenticated-orcid":false,"given":"Chloe C.","family":"Goodwin","sequence":"additional","affiliation":[{"name":"Southeastern Cooperative Wildlife Disease Study, University of Georgia, Athens, GA 30602, USA"},{"name":"Department of Pathology, University of Georgia, Athens, GA 30602, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alisia A. W.","family":"Weyna","sequence":"additional","affiliation":[{"name":"Southeastern Cooperative Wildlife Disease Study, University of Georgia, Athens, GA 30602, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amy S.","family":"McKinney","sequence":"additional","affiliation":[{"name":"Athens Veterinary Diagnostic Laboratory, University of Georgia, Athens, GA 30602, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xuan Hui","family":"Teo","sequence":"additional","affiliation":[{"name":"Southeastern Cooperative Wildlife Disease Study, University of Georgia, Athens, GA 30602, USA"},{"name":"Department of Pathology, University of Georgia, Athens, GA 30602, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rebecca","family":"Radisic","sequence":"additional","affiliation":[{"name":"Southeastern Cooperative Wildlife Disease Study, University of Georgia, Athens, GA 30602, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lisa A.","family":"Shender","sequence":"additional","affiliation":[{"name":"Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, St. Petersburg, FL 33701, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2438-5983","authenticated-orcid":false,"given":"Susan","family":"Sanchez","sequence":"additional","affiliation":[{"name":"Athens Veterinary Diagnostic Laboratory, University of Georgia, Athens, GA 30602, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michelle","family":"van Deventer","sequence":"additional","affiliation":[{"name":"Florida Fish and Wildlife Conservation Commission, Naples, FL 32601, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,11,18]]},"reference":[{"key":"ref_1","unstructured":"Florida Fish and Wildlife Conservation Commission (FWC) (2013). A Species Action Plan for Four Imperiled Species of Beach-Nesting Birds, FWC."},{"key":"ref_2","unstructured":"Billerman, S.M. (2020). Black Skimmer (Rynchops niger), Version 1.0. Birds of the World, Cornell Lab of Ornithology."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1126\/science.aaw1313","article-title":"Decline of the North American avifauna","volume":"366","author":"Rosenberg","year":"2019","journal-title":"Science"},{"key":"ref_4","unstructured":"(2024, February 26). Macrotrends, \u201cFlorida Population 1900\u20132023\u201d. Available online: https:\/\/www.macrotrends.net\/states\/florida\/population#:~:text=The%20population%20of%20Florida%20in,a%201.9%25%20increase%20from%202021."},{"key":"ref_5","unstructured":"Florida Fish and Wildlife Conservation Commission (FWC) (2011). Biological Status Review Report for the Black Skimmer (Rynchops niger), FWC."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"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., and Lameris, T.K. (2022). Transatlantic spread of highly pathogenic avian influenza H5N1 by wild birds from Europe to North America in 2021. Sci. Rep., 12.","DOI":"10.1038\/s41598-022-13447-z"},{"key":"ref_7","unstructured":"U.S. Department of Agriculture, Animal and Plant Health Inspection Service (2024, September 20). 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."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1007\/s10393-022-01596-6","article-title":"Heavy rainfall, sewer overflows, and salmonellosis in black skimmers (Rynchops niger)","volume":"19","author":"Shender","year":"2022","journal-title":"Ecohealth"},{"key":"ref_9","unstructured":"Sellers, B., Smith, H., and Ferrell, J. (2024, February 27). 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."},{"key":"ref_10","unstructured":"(2024, September 19). Florida Shorebird Alliance. Available online: https:\/\/flshorebirdalliance.org\/."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"2252","DOI":"10.3201\/eid1012.040511","article-title":"West Nile virus viremia in wild rock pigeons","volume":"10","author":"Allison","year":"2004","journal-title":"Emerg. Infect. Dis."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"109860","DOI":"10.1016\/j.virol.2023.109860","article-title":"H5N1 highly pathogenic avian influenza clade 2.3.4.4b in wild and domestic birds: Introductions into the United States and reassortments, December 2021\u2013April 2022","volume":"587","author":"Youk","year":"2023","journal-title":"Virology"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"414","DOI":"10.1177\/104063870802000402","article-title":"Detection of a broad range of class I and II Newcastle disease viruses using a multiplex real-time reverse transcription polymerase chain reaction assay","volume":"20","author":"Kim","year":"2008","journal-title":"J. Vet. Diagn. Investig."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"771","DOI":"10.1177\/104063870902100603","article-title":"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","volume":"21","author":"Das","year":"2009","journal-title":"J. Vet. Diagn. Investig."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"932","DOI":"10.1177\/1040638711416846","article-title":"Use of high-resolution melting curve analysis to identify Mycoplasma species commonly isolated from ruminant, avian, and canine samples","volume":"23","author":"Rebelo","year":"2011","journal-title":"J. Vet. Diagn. Investig."},{"key":"ref_16","unstructured":"Van Deventer, M., Brush, J.M., Cox, A., and Hardman, R. Personal communication."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"De Luca, E., \u00c1lvarez-Narv\u00e1ez, S., Maboni, G., Baptista, R.P., Nemeth, N.M., Niedringhaus, K.D., Ladner, J.T., Lorch, J.M., Koroleva, G., and Lovett, S. (2021). 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., 12.","DOI":"10.3389\/fmicb.2021.667356"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1016\/j.jcpa.2021.01.009","article-title":"Mortality in common (Sterna hirundo) and sandwich (Thalasseus sandvicensis) terns associated with Bisgaard Taxon 40 infection on Marco Island, Florida, USA","volume":"184","author":"Niedringhaus","year":"2021","journal-title":"J. Comp. Pathol."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Fink, D., Auer, T., Johnston, A., Strimas-Mackey, M., Ligocki, S., Robinson, O., Hochachka, W., Jaromczyk, L., Crowley, C., and Dunham, K. (2023). eBird Status and Trends, Data Version: 2022, Cornell Lab of Ornithology.","DOI":"10.2173\/ebirdst.2022"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1656\/058.016.0301","article-title":"Investigating Black Skimmer Chick Diets Using Citizen Science and Digital Photography","volume":"16","author":"Forys","year":"2017","journal-title":"Southeast. Nat."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Paleczny, M., Hammill, E., Karpouzi, V., and Pauly, D. (2015). Population trend of the world\u2019s monitored seabirds, 1950\u20132010. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0129342"},{"key":"ref_22","unstructured":"Swayne, D.E. (2020). Staphylococcosis. Diseases of Poultry, John Wiley & Sons, Inc.. [14th ed.]."},{"key":"ref_23","unstructured":"(2024, July 25). National Oceanic and Atmospheric Administration (NOAA), \u201cASOS Climate Normals\u201d, Available online: https:\/\/www.weather.gov\/tbw\/newnormals_asos."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Heaton, C.J., Gerbig, G.R., Sensius, L.D., Patel, V., and Smith, T.C. (2020). Staphylococcus aureus epidemiology in wildlife: A systematic review. Antibiotics, 9.","DOI":"10.3390\/antibiotics9020089"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Topi\u0107, N., Cenov, A., Jozi\u0107, S., Glad, M., Mance, D., Lu\u0161i\u0107, D., Kapetanovi\u0107, D., Mance, D., and Vuki\u0107 Lu\u0161i\u0107, D. (2021). Staphylococcus aureus\u2014An additional parameter of bathing water quality for crowded urban beaches. Int. J. Environ. Res. Public Health, 18.","DOI":"10.3390\/ijerph18105234"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1038\/nrmicro2200","article-title":"Waves of resistance: Staphylococcus aureus in the antibiotic era","volume":"7","author":"Chambers","year":"2009","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1080\/09603123.2012.699027","article-title":"High numbers of Staphylococcus aureus at three bathing beaches in South Florida","volume":"23","author":"Esiobu","year":"2013","journal-title":"Int. J. Environ. Health Res."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"680","DOI":"10.2166\/wh.2011.157","article-title":"An estimate of the cost of acute health effects form food- and water-born marine pathogens and toxins in the United States","volume":"9","author":"Ralston","year":"2011","journal-title":"J. Water Health"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"4195","DOI":"10.1016\/j.watres.2012.04.001","article-title":"A multi-beach study of Staphylococcus aureus, MRSA, and enterococci in seawater and beach sand","volume":"46","author":"Goodwin","year":"2012","journal-title":"Water Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"320","DOI":"10.1002\/2017GH000106","article-title":"Prevalence and characterization of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus on public recreational beaches in northeast Ohio","volume":"1","author":"Thapaliya","year":"2017","journal-title":"Geohealth"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1354\/vp.37-3-208","article-title":"Pathology of fatal West Nile virus infections in native and exotic birds during the 1999 outbreak in New York City, New York","volume":"37","author":"Steele","year":"2000","journal-title":"Vet. Pathol."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Nemeth, N.M., Ruder, M.G., Poulson, R.L., Sargent, R., Breeding, S., Evans, M.N., Zimmerman, J., Hardman, R., Cunningham, M., and Gibbs, S. (2023). Bald eagle mortality and nest failure due to clade 2.3.4.4 highly pathogenic H5N1 influenza a virus. Sci. Rep., 13.","DOI":"10.1038\/s41598-023-27446-1"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1111\/j.1750-2659.2011.00238.x","article-title":"Experimental challenge and pathology of highly pathogenic avian influenza virus H5N1 in dunlin (Calidris alpina), an intercontinental migrant shorebird species","volume":"5","author":"Hall","year":"2011","journal-title":"Influenza Other Respir. Viruses"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Pardo-Roa, C., Nelson, M.I., Ariyama, N., Aguayo, C., Almonacid, L.I., Munoz, G., Navarro, C., Avila, C., Ulloa, M., and Reyes, R. (2023). Cross-species transmission and PB2 mammalian adaptations of highly pathogenic avian influenza A\/H5N1 viruses in Chile. bioRxiv.","DOI":"10.1101\/2023.06.30.547205"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"3429","DOI":"10.1098\/rstb.2009.0128","article-title":"Effects of environmental change on wildlife health","volume":"364","author":"Duffus","year":"2009","journal-title":"Philos. Trans. R. Soc. Lond. B Biol. Sci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"131090","DOI":"10.1016\/j.jhazmat.2023.131090","article-title":"\u2018Plasticosis\u2019: Characterizing macro- and microplastic-associated fibrosis in seabird tissues","volume":"450","author":"Bond","year":"2023","journal-title":"J. Hazard. Mater."},{"key":"ref_37","unstructured":"Swayne, D.E. (2020). Nutritional Diseases. Diseases of Poultry, John Wiley & Sons, Inc.. [14th ed.]."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"246","DOI":"10.7589\/2011-09-270","article-title":"Brevetoxicosis in seabirds naturally exposed to Karenia brevis blooms along the central west coast of Florida","volume":"49","author":"Fauquier","year":"2013","journal-title":"J. Wildl. Dis."}],"container-title":["Veterinary Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2306-7381\/11\/11\/578\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:34:45Z","timestamp":1760114085000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2306-7381\/11\/11\/578"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,11,18]]},"references-count":38,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2024,11]]}},"alternative-id":["vetsci11110578"],"URL":"https:\/\/doi.org\/10.3390\/vetsci11110578","relation":{},"ISSN":["2306-7381"],"issn-type":[{"value":"2306-7381","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,11,18]]}}}