Climate Change Impacts Beach Microbiota: Comparison
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Please note this is a comparison between Version 3 by Jason Zhu and Version 2 by João Brandão.

Global climate change is affecting beach microbial contamination, via changes to conditions like water temperature, sea level, precipitation, and waves. In addition, the world is changing, and humans travel and relocate, often carrying endemic allochthonous microbiota. 

  • climate change
  • global warming
  • beach sand
  • Microbiota

1. Characterizing Climate Change Impacts on Microbiota

Climate-mediated changes might affect processes controlling inland, estuarine, and coastal concentrations of faecal indicator bacteria (FIB), primarily Escherichia coli (E. coli), enterococci, pathogens, and the frequency and duration of cyanobacterial blooms, including changes in pH, dissolved oxygen (DO) concentration, salinity (S), dissolved organic carbon (DOC), and dissolved organic nitrogen (DON). Nearshore changes in pH and DO have been documented along the west coast of North America due to several chemical contributions, as well as changes in the intensity of upwelling [17][1]. These types of changes can be attributable to changes in water temperature and subsequent alterations to water density and potential stratification regimes. Additional changes in pH and DO may also be associated with eutrophication, as has been observed in the Gulf of Mexico and the South China Sea [18][2]. These two may affect the expected behaviour of FIB in coastal waters and their interactions with sediments, which may be controlled in part by pH. These pH alterations, increases in DOC and DON, and also the increase in water temperature can lead to microbial growth, and changes to some phytoplankton communities (cyanobacteria, diatoms, dinoflagellates, green algae, and chalk-coated Coccolithophores) [19][3]. Subsequently, these changing communities may result in changes to light penetration in the water column, affecting solar-mediated inactivation of indicator organisms and pathogens [20][4], or perhaps their growth.
The case of cyanobacteria and dinoflagellates is of particular concern since these phytoplanktonic groups are able to develop Harmful Algal Blooms (HABs), as some of their species are able to produce diverse types of toxins, thus causing adverse effects [19,21,22][3][5][6]. These toxins may have a nefarious effect on water associated activities and/or ecology. They can also accumulate in the sand and persist for some time [23][7], jeopardizing, for instance, recreational activities taking place at those beach environments.
Consequently, both the presence and persistence of waterborne pathogens and indicator microorganisms will likely change in response to climate change. This could have an impact on the concentration of microbiota in near- and foreshore sands. Deposition and scouring processes associated with waves in the nearshore environment [12,24,25][8][9][10] may intensify due to changes in wave dynamics associated with climate change [8,9][11][12].
Both empirical data collection and mechanistic modelling of FIB are useful tools to help understand the relative importance of the various faecal sources, fate processes, and transport pathways, and for making predictions concerning possible climate change generated phenomena. However, it is important to note that while FIB have been useful to monitor faecal contamination of waterways, there may be differential responses of different microbiota to climate-induced environmental changes. FIB may in fact persist or even multiply in the water–sand interface for a longer time than some faecal pathogens [69][13]. In particular, FIB are unable to predict the growth potential of opportunistic pathogens such as those Vibrio species thriving in the water environments [70,71][14][15]. Accordingly, models also need to incorporate data from specific pathogens likely to cause human illnesses. For example, Topić et al. [72][16] describe an outbreak of impetigo in bathers in 2015, linked to the Croatian Vodice beach, due to Staphylococcus aureus in water, which was not accompanied by an increase in the levels of FIB. 258 locations in Primorje-Gorski Kotar County were investigated for the presence of S. aureus in water, as a follow-up of the outbreak, and the results found were that the bacterium was present in between 2.2 and 36.3% of the 2867 samples collected between mid-May and the end of September. The presence of the bacterium correlates with the intensity of human use of the beach. Croatia has very few beaches with sand, but should that be the case, sand could have added to the intensity of the outbreak. Nonetheless, given incomplete information and knowledge of nearshore systems, both empirical and mechanistic models and analyses are needed to illustrate climate change impacts and inform management decisions in the context of environmental and public health in nearshore zones.

2. Temperature Increases

Rising temperature is a direct response to anthropogenic activities leading to climate change. Moreover, the temperature has a direct effect on the survival and persistence of specific microbial species in both water and sand. Water temperature scenarios are tightly coupled to nearshore hydrodynamics such as stratification, thermal bars, and density-driven currents. An average rise in global atmospheric temperature will result in increases in the temperature of both fresh and marine surface waters, which can directly affect the survival kinetics and growth rates of microbes in both nearshore and upstream tributary environments [73][17]. However, while it is generally thought that increases in temperature enhance microbial growth, many environmental microbes prefer mesophilic growth temperatures, and elevated temperatures may inhibit the growth of many species. Conversely, rising temperatures may also increase the occurrence of other pathogenic microbes which are capable of multiplying in water environments near body temperature [5,6,7,31,32][18][19][20][21][22]. This is especially relevant for fungi when considering the possible selective effect of heatwaves on their potential to infect warm-blooded animals, as described by Casadevall and Kontoyiannis [13][23] on the emerging Candida auris, a multi-resistant yeast of currently high nosocomial impact in multiple regions and whose original habitat is thought to be aquatic [14][24]. Parasitic protozoa may also benefit from rising temperatures, as described in the new WHO guidelines, namely Acanthamoeba and Naegleria fowleri [74][25]. Conversely, the abundance of faecal microbes would decrease in response to many climate change models since faecal microbes generally degrade faster when temperatures increase (i.e., bacterial die-off processes are enhanced) [33,34,35][26][27][28]. For example, Viau et al. [36][29] and Hokajärvi et al. [37][30] reported a negative association of the faecal pathogen Campylobacter with temperature. Rising temperatures may also increase the occurrence of other pathogenic microbes, which are capable of multiplying in water environments, including in sand, potentially changing the local microbial community [5,6,7,31,32][18][19][20][21][22].
Changes in temperature impact physical and biological properties of water in many ways. For example, changing temperatures affect water and contaminant plume buoyancy and dynamics [46][31]. Changes to relative densities of water and contamination plumes, due to temperature changes in the water column, may lead to increases in surface FIB plumes that are susceptible to solar inactivation. Conversely, changes in relative density may lead to increases in sinking or settling plumes that are more resistant to solar inactivation, yielding potentially higher survival and persistence of contaminants in the environment.
The potential for increased microbial proliferation, in combination with the expansion of the geographic range and seasonality of various tropical pathogens, could pose a significant risk of increases in human exposure. For example, the presence of Salmonella spp. in Hawaiian coastal streams has a positive correlation with water temperature [36][29]. Likewise, the presence and persistence of Vibrio spp. is closely and positively correlated with water temperatures [38,39,40][32][33][34]. It has been further suggested that increasing temperatures would allow for increased range and extended seasonality of Leptospira spp. [41,42,43][35][36][37]. The effects of increased temperatures also have the potential to alter the persistence of pathogens in beach sand, including methicillin-resistant Staphylococcus aureus (MRSA) [44][38], allergenic fungi, and antifungal resistant fungal species [16][39].
Another concern is associated with toxic algal blooms, which are also predicted to increase over the next century with the rise of SST and global average lake surface temperature [31,32][21][22]. These blooms, along with any microbes that they may be carrying, may be deposited at the sand–water continuum during high tides and high waves, providing an additional input of contaminants to this continuum [45][40].
In addition to direct changes in the microbial dynamics in the beach ecosystem, temperature rise may have significant indirect effects on environmental conditions and associated microbial loads at beaches. FIB contamination inputs in coastal areas are predicted to change significantly and subsequently may increase adverse health effects for beach users as a result of climate change [75][41]. Changes in human behaviour may thus challenge beach management paradigms. Examples have been reported in shallow freshwater lakes, where norovirus outbreaks have been associated with a sudden increase in the number of beach users [26][42]. High temperatures lead to increased beach use, for heat relief, especially if exceptional or extreme weather events occur [27,28][43][44]. Such contamination events might have a lesser role in riverine and marine conditions with water flow and larger water volume, respectively. There may also be expanded recreational usage as a result of a growing interest in water sports, ranging from triathlon swims to surfing and wind sailing. Expansion of such recreational use may be particularly prominent at those beaches in proximity to large urban centres. Consequently, direct human inputs may temporarily increase via shedding, leading to increased pathogen loading in beach environments [29[45][46],30], or even outbreaks of gastrointestinal illnesses. High temperatures may also attract people to congregate at nearby shores, often at locations that do not comply with recreational water safety standards.
Increased urbanization and climate change may also alter migratory bird patterns, impacting the numbers, species, and behaviour of birds associated with the beach environment. Populations of adaptable bird species, like gulls and Canada geese, have been growing in many urban settings around the world [76][47], and particularly around the Great Lakes [77][48]. Urbanisation has been reported as a factor for the presence of pigeon-borne Cryptococcus spp. both in sand and in water, which are yeasts responsible for fungal meningitis [16][39].
Resident populations of birds, particularly shorebirds, can be expected to continue their role as sources of direct animal faecal deposition in the sand. In fact, their removal leads to a dramatic improvement in water quality, as has been reported for example for gulls [78][49]. Bird population increase in beach settings is expected to lead to a potential increase in human exposure risk to pathogens such as Salmonella, Campylobacter and Chlamydia if populations continue growing in response to climate change [79][50]. These pathogens, in addition to other zoonotic disease-associated microbiota such as West Nile Virus, Aspergillus, Staphylococcus, and a variety of antimicrobial-resistant bacteria have been documented in gulls, terns, and barnacle geese [80,81,82][51][52][53]. These microbiota may be transmitted directly via deposition from the birds to coastal environments (sand and water), where they may accumulate and present human health risks. These risks may further be amplified as human beach usage may increase in response to climate change and increasing air temperatures.

3. Precipitation Increases

Altered precipitation patterns can also greatly influence pathogen exposures at the beach. The intensification of storms, extreme precipitation, and other severe weather events like drought, flooding, storm surge, or even damaging cyclones [1][54] could cause nearshore inundation, coastal erosion and run-off, introducing pathogenic microbes into coastal waters and on beaches [47,48,49,50,51,52,53,54,57,83,84,85][55][56][57][58][59][60][61][62][63][64][65][66]. Heavy precipitation events, predicted to increase in both frequency and intensity, can cause the resuspension of FIB from beach sand into the water column as well as increases in the dissolved organic matter that can influence solar/UV inactivation of microbial contaminants. These impacts may have subsequent effects on water quality lasting up to 5–7 days after the precipitation event [20,49,57][4][57][63]. Changes in global patterns of precipitation are also predicted to amplify existing direct and anthropogenic impacts of microbiota in coastal environments [11,30][67][46]. Increased frequency and intensity of precipitation events can lead to the breakdown of already taxed wastewater infrastructure, resulting in increased point sources of faecal contamination of beaches, such as Combined Sewer Overflow (CSO) events or wastewater effluent [50,58][58][68]. Stormwater outfalls frequently present the greatest direct source of faecal contamination, including pathogens, for adjacent surface waters, even in areas with mixed land use [86,87,88][69][70][71]. Further, runoff from impervious surfaces (such as parking lots), CSO discharge events, and stormwater outfall discharges located at or in proximity to beaches can directly contribute to faecal contamination of beaches [55,56][72][73].

4. Wave Activity and Sea Level Rise

Temperature and precipitation changes are two environmental conditions that have been frequently considered as hallmarks of climate change in the literature. Wave activity is not as commonly explored [90][74] and the effects of waves on the transfer and accumulation of human pathogens in the sand, and their subsequent transfer to recreational water, needs to be studied. wave activity is include d here because the sand–water continuum involves dynamic exchanges of microbes between sand and water [12][8]. Potential climate-induced changes to microbial interactions between water and sand could have important implications on altered exposure conditions [91][75]. Direct faecal deposition from birds or dogs, or direct runoff onto sand may be distributed over a greater area of beach with increased human activity and extreme weather events, including increased wave activity [54,66,67,92,93,94][62][76][77][78][79][80]. Similarly, periodic tidal rewetting enables FIB and pathogens deposited into dry sands to persist for longer periods [54,68][62][81]. Moreover, if ocean depth rises, the tides will edge further inland, allowing for the persistence and exchange of FIB at the sand–water continuum closer to densely populated areas.
Changes in the coastline could also have significant negative impacts on human exposure to pathogens as there has been a global shift towards urbanization with a tendency for cities to develop along coastlines. It has been estimated that nearly half of the world’s population lives within a few hundred kilometres of a coast [95][82]. The combination of rising sea levels, increasing rainfall amounts and intensity, and increasing urbanization means that the risk of exposure to microbial contamination along the coast will continue to rise. An increase in sea level can also lead to the development of new microbial communities in the sand–water continuum of more inland areas [62,63][83][84]. This may precipitate exposure to more diverse microbial contaminants at beaches.

5. Economic Impact

There are both direct and indirect costs associated with climate change-induced increases in the number of harmful bacteria and fungi and resulting exposures to humans. While some are obvious, such as loss of wages due to illness, others are more intangible but no less severe. For example, current costs of recreational waterborne illnesses in the US alone approaches $3 billion annually (range of $2.2–$3.7 billion), with moderate to severe illnesses accounting for ~73% of the economic burden [96][85]. These costs will likely drastically increase due to climate change-induced rises in the number of pathogenic bacteria and fungi present in recreational waters. Moreover, climate-induced increases in temperature, precipitation, sea level, and storm intensities worldwide will likely lead to more disasters and increases in human exposure to pathogens in waterways [12][8], increases in contact of humans and animals, as well as a greater prevalence of antibiotic and heavy metal resistant bacteria and fungi, primarily due to the greater runoff [97][86]. These costs are in addition to those required to maintain and enhance infrastructure in a changing environment [98,99][87][88].

56. Conclusions

Understanding the most critical climatic factors that influence changes in the microbiota of beach sands and recreational water, will aid in recommending best management practices to minimize the exposure risk and illness rates of the millions of individuals, who visit beaches to recreate each year. Some of these visitors may be immunocompromised at some level, which generates higher susceptibility to opportunistic microbes. If this is currently a reality, in a future reshaped by climate change, this type of knowledge may be much more relevant. Planning the future of recreational water use should consider sand and water, as well as the influences of climate changes in their microbiota.

References

  1. Byrne, R.H.; Mecking, S.; Feely, R.A.; Liu, X.W. Direct observations of basin-wide acidification of the North Pacific Ocean. Geophys. Res. Lett. 2010, 37, 5.
  2. Cai, W.J.; Hu, X.P.; Huang, W.J.; Murrell, M.C.; Lehrter, J.C.; Lohrenz, S.E.; Chou, W.C.; Zhai, W.D.; Hollibaugh, J.T.; Wang, Y.C.; et al. Acidification of subsurface coastal waters enhanced by eutrophication. Nat. Geosci. 2011, 4, 766–770.
  3. Henson, S.A.; Cael, B.B.; Allen, S.R.; Dutkiewicz, S. Future phytoplankton diversity in a changing climate. Nat. Commun. 2021, 12, 1–8.
  4. Williamson, C.E.; Madronich, S.; Lal, A.; Zepp, R.G.; Lucas, R.M.; Overholt, E.P.; Rose, K.C.; Schladow, S.G.; Lee-Taylor, J. Climate change-induced increases in precipitation are reducing the potential for solar ultraviolet radiation to inactivate pathogens in surface waters. Sci. Rep. 2017, 7, 12.
  5. United States Environmental Protection Agency. Impacts of Climate Change on the Occurrence of Harmful Algal Blooms. (2013, May). Available online: https://www.epa.gov/sites/default/files/documents/climatehabs.pdf (accessed on 17 November 2021).
  6. Rastogi, R.P.; Madamwar, D.; Incharoensakdi, A. Bloom dynamics of cyanobacteria and their toxins: Environmental health impacts and mitigation strategies. Front. Microbiol. 2015, 6, 1254.
  7. Richer, R.; Banack, S.A.; Metcalf, J.S.; Cox, P.A. The persistence of cyanobacterial toxins in desert soils. J. Arid Environ. 2015, 112, 134–139.
  8. Weiskerger, C.J.; Brandao, J.; Ahmed, W.; Aslan, A.; Avolio, L.; Badgley, B.D.; Boehm, A.B.; Edge, T.A.; Fleisher, J.M.; Heaney, C.D.; et al. Impacts of a changing earth on microbial dynamics and human health risks in the continuum between beach water and sand. Water Res. 2019, 162, 456–470.
  9. Phillips, M.C.; Feng, Z.; Vogel, L.J.; Reniers, A.J.H.M.; Haus, B.K.; Enns, A.A.; Zhang, Y.; Hernandez, D.B.; Solo-Gabriele, H.M. Microbial release from seeded beach sediments during wave conditions. Mar. Pollut. Bull. 2014, 79, 114–122.
  10. Vogel, L.J.; O’Carroll, D.M.; Edge, T.A.; Robinson, C.E. Release of Escherichia coli from foreshore sand and pore water during intensified wave conditions at a recreational beach. Environ. Sci. Technol. 2016, 50, 5676–5684.
  11. Young, I.R.; Zieger, S.; Babanin, A.V. Global trends in wind speed and wave height. Science 2011, 332, 451–455.
  12. Tokinaga, H.; Xie, S.P. Wave and anemometer-based sea surface wind (WASWind) for climate change analysis. J. Clim. 2011, 24, 267–285.
  13. Tiwari, A.; Oliver, D.M.; Bivins, A.; Sherchan, S.P.; Pitkänen, T. Bathing water quality monitoring practices in europe and the United States. Int. J. Environ. Res. Public Health 2021, 18, 5513.
  14. Lutz, C.; Erken, M.; Noorian, P.; Sun, S.; McDougald, D. Environmental reservoirs and mechanisms of persistence of Vibrio cholerae. Front. Microbiol. 2013, 4, 375.
  15. Tiwari, A.; Kauppinen, A.; Pitkänen, T. Decay of Enterococcus faecalis, vibrio cholerae and MS2 coliphage in a laboratory mesocosm under brackish beach conditions. Front. Public Health 2019, 7, 269.
  16. Topić, N.; Cenov, A.; Jozić, S.; Glad, M.; Mance, D.; Lušić, D.; Kapetanović, D.; Mance, D.; Lušić, D.V. Staphylococcus aureus—An additional parameter of bathing water quality for crowded urban beaches. Int. J. Environ. Res. Public Health 2021, 18, 5234.
  17. Liu, L.; Phanikumar, M.S.; Molloy, S.L.; Whitman, R.L.; Shively, D.A.; Nevers, M.B.; Schwab, D.J.; Rose, J.B. Modeling the transport and inactivation of E. coli and enterococci in the near-shore region of Lake Michigan. Environ. Sci. Technol. 2006, 40, 5022–5028.
  18. O’Reilly, C.M.; Sharma, S.; Gray, D.K.; Hampton, S.E.; Read, J.S.; Rowley, R.J.; Schneider, P.; Lenters, J.D.; McIntyre, P.B.; Kraemer, B.M.; et al. Rapid and highly variable warming of lake surface waters around the globe. Geophys. Res. Lett. 2015, 42, 10773–10781.
  19. Sharma, S.; Gray, D.K.; Read, J.S.; O’Reilly, C.M.; Schneider, P.; Qudrat, A.; Gries, C.; Stefanoff, S.; Hampton, S.E.; Hook, S.; et al. A global database of lake surface temperatures collected by in situ and satellite methods from 1985–2009. Sci. Data 2015, 2, 19.
  20. Wu, L.X.; Cai, W.J.; Zhang, L.P.; Nakamura, H.; Timmermann, A.; Joyce, T.; McPhaden, M.J.; Alexander, M.; Qiu, B.; Visbecks, M.; et al. Enhanced warming over the global subtropical western boundary currents. Nat. Clim. Chang. 2012, 2, 161–166.
  21. Brookes, J.D.; Carey, C.C. Resilience to blooms. Science 2011, 334, 46–47.
  22. Rigosi, A.; Hanson, P.; Hamilton, D.P.; Hipsey, M.; Rusak, J.A.; Bois, J.; Sparber, K.; Chorus, I.; Watkinson, A.J.; Qin, B.; et al. Determining the probability of cyanobacterial blooms: The application of Bayesian networks in multiple lake systems. Ecol. Appl. 2015, 25, 186–199.
  23. Casadevall, A.; Kontoyiannis, D.P.; Robert, V. On the emergence of Candida auris: Climate change, azoles, swamps, and birds. mBio 2019, 10, e01397-19.
  24. Arora, P.; Singh, P.; Wang, Y.; Yadav, A.; Pawar, K.; Singh, A.; Padmavati, G.; Xu, J.; Chowdhary, A. Environmental isolation of Candida auris from the coastal wetlands of Andaman Islands, India. mBio 2021, 12, e03181-20.
  25. WHO. WHO Guidelines on Recreational Water Quality: Volume 1: Coastal and Fresh Waters; WHO: Geneva, Switzerland, 2021; Volume 1, ISBN 9789240031302.
  26. Bussi, G.; Whitehead, P.G.; Thomas, A.R.C.; Masante, D.; Jones, L.; Cosby, B.J.; Emmett, B.A.; Malham, S.K.; Prudhomme, C.; Prosser, H. Climate and land-use change impact on faecal indicator bacteria in a temperate maritime catchment (the River Conwy, Wales). J. Hydrol. 2017, 553, 248–261.
  27. Noble, R.T.; Lee, I.M.; Schiff, K.C. Inactivation of indicator micro-organisms from various sources of faecal contamination in seawater and freshwater. J. Appl. Microbiol. 2004, 96, 464–472.
  28. Sokolova, E.; Astrom, J.; Pettersson, T.J.R.; Bergstedt, O.; Hermansson, M. Decay of Bacteroidales genetic markers in relation to traditional fecal indicators for water quality modeling of drinking water sources. Environ. Sci. Technol. 2012, 46, 892–900.
  29. Viau, E.J.; Goodwin, K.D.; Yamahara, K.M.; Layton, B.A.; Sassoubre, L.M.; Burns, S.L.; Tong, H.I.; Wong, S.H.C.; Lu, Y.A.; Boehm, A.B. Bacterial pathogens in Hawaiian coastal streams—Associations with fecal indicators, land cover, and water quality. Water Res. 2011, 45, 3279–3290.
  30. Hokajärvi, A.M.; Pitkanen, T.; Siljanen, H.M.P.; Nakari, U.M.; Torvinen, E.; Siitonen, A.; Miettinen, I.T. Occurrence of thermotolerant Campylobacter spp. and adenoviruses in Finnish bathing waters and purified sewage effluents. J. Water Health 2013, 11, 120–134.
  31. Akar, P.J.; Jirka, G.H. Lateral spreading with ambient current advection: Processus d’étalement en surface dans le transport et le mélange de polluants lere partie: Etalement lateral dans un écoulement ambiant. J. Hydraul. Res. 1994, 32, 815–831.
  32. Baker-Austin, C.; Trinanes, J.A.; Taylor, N.G.H.; Hartnell, R.; Siitonen, A.; Martinez-Urtaza, J. Emerging Vibrio risk at high latitudes in response to ocean warming. Nat. Clim. Chang. 2013, 3, 73–77.
  33. Huehn, S.; Eichhorn, C.; Urmersbach, S.; Breidenbach, J.; Bechlars, S.; Bier, N.; Alter, T.; Bartelt, E.; Frank, C.; Oberheitmann, B.; et al. Pathogenic vibrios in environmental, seafood and clinical sources in Germany. Int. J. Med. Microbiol. 2014, 304, 843–850.
  34. Sterk, A.; Schets, F.M.; Husman, A.M.D.; de Nijs, T.; Schijven, J.F. Effect of climate change on the concentration and associated risks of Vibrio spp. in Dutch recreational waters. Risk Anal. 2015, 35, 1717–1729.
  35. Desvars, A.; Jego, S.; Chiroleu, F.; Bourhy, P.; Cardinale, E.; Michault, A. Seasonality of human Leptospirosis in Reunion Island (Indian Ocean) and its association with meteorological data. PLoS ONE 2011, 6, 10.
  36. Sumi, A.; Telan, E.F.O.; Chagan-Yasutan, H.; Piolo, M.B.; Hattori, T.; Kobayashi, N. Effect of temperature, relative humidity and rainfall on dengue fever and leptospirosis infections in Manila, the Philippines. Epidemiol. Infect. 2017, 145, 78–86.
  37. Zhao, J.; Liao, J.S.; Huang, X.; Wang, Y.P.; Ren, J.H.; Wang, X.Y.; Ding, F. Mapping risk of leptospirosis in China using environmental and socioeconomic data. BMC Infect. Dis. 2016, 16, 10.
  38. Goodwin, K.D.; McNay, M.; Cao, Y.P.; 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.
  39. Brandão, J.; Gangneux, J.P.; Arikan-Akdagli, S.; Barac, A.; Bostanaru, A.C.; Brito, S.; Bull, M.; Çerikçioğlu, N.; Chapman, B.; Efstratiou, M.A.; et al. Mycosands: Fungal diversity and abundance in beach sand and recreational waters—Relevance to human health. Sci. Total Environ. 2021, 781, 146598.
  40. Maghsoudi, E.; Prevost, M.; Duy, S.V.; Sauve, S.; Dorner, S. Adsorption characteristics of multiple microcystins and cylindrospermopsin on sediment: Implications for toxin monitoring and drinking water treatment. Toxicon 2015, 103, 48–54.
  41. Moore, S.K.; Trainer, V.L.; Mantua, N.J.; Parker, M.S.; Laws, E.A.; Backer, L.C.; Fleming, L.E. Impacts of climate variability and future climate change on harmful algal blooms and human health. Environ. Health 2008, 7, 12.
  42. Kauppinen, A.; Al-Hello, H.; Zacheus, O.; Kilponen, J.; Maunula, L.; Huusko, S.; Lappalainen, M.; Miettinen, I.; Blomqvist, S.; Rimhanen-Finne, R. Increase in outbreaks of gastroenteritis linked to bathing water in Finland in summer 2014. Eurosurveillance 2017, 22, 13–20.
  43. Moreno, A.; Amelung, B.; Santamarta, L. Linking beach recreation to weather conditions: A case study in Zandvoort, Netherlands. Tour. Mar. Environ. 2009, 5, 111–119.
  44. Smith, K. The influence of weather and climate on recreation and tourism. Weather 1993, 48, 398–404.
  45. Shuval, H. Estimating the global burden of thalassogenic diseases: Human infectious diseases caused by wastewater pollution of the marine environment. J. Water Health 2003, 1, 53–64.
  46. Perkins, T.L.; Clements, K.; Baas, J.H.; Jago, C.F.; Jones, D.L.; Malham, S.K.; McDonald, J.E. Sediment composition influences spatial variation in the abundance of human pathogen indicator bacteria within an estuarine environment. PLoS ONE 2014, 9, 9.
  47. Tryjanowski, P.; Sparks, T.H.; Kuźniak, S.; Czechowski, P.; Jerzak, L. Bird Migration Advances More Strongly in Urban Environments. PLoS ONE 2013, 8, e63482.
  48. Conover, M.R. Population growth and movements of Canada geese in New Haven County, Connecticut, during a 25-year period. Waterbirds 2011, 34, 412–421.
  49. Converse, R.R.; Kinzelman, J.L.; Sams, E.A.; Hudgens, E.; Dufour, A.P.; Ryu, H.; Santo-Domingo, J.W.; Kelty, C.A.; Shanks, O.C.; Siefring, S.D. Dramatic improvements in beach water quality following gull removal. Environ. Sci. Technol. 2012, 46, 10206–10213.
  50. Navarro, J.; Grémillet, D.; Afán, I.; Miranda, F.; Bouten, W.; Forero, M.G.; Figuerola, J. Pathogen transmission risk by opportunistic gulls moving across human landscapes. Sci. Rep. 2019, 9, 1–5.
  51. Hubálek, Z. Pathogenic microorganisms associated with gulls and terns (Laridae). J. Vertebr. Biol. 2021, 70.
  52. Zeballos-Gross, D.; Rojas-Sereno, Z.; Salgado-Caxito, M.; Poeta, P.; Torres, C.; Benavides, J.A. The Role of Gulls as Reservoirs of Antibiotic Resistance in Aquatic Environments: A Scoping Review. Front. Microbiol. 2021, 12, 1–15.
  53. Kurittu, P.; Khakipoor, B.; Brouwer, M.S.M.; Heikinheimo, A. Plasmids conferring resistance to extended-spectrum beta-lactamases including a rare IncN+IncR multireplicon carrying blaCTX-M-1 in Escherichia coli recovered from migrating barnacle geese (Branta leucopsis). Open Res. Eur. 2021, 1, 46.
  54. IPCC. Climate Change Synthesis Report 2014; Pachauri, R.K., Meyer, L., Eds.; Intergovernmental Panel on Climate Change: New York, NY, USA, 2014.
  55. Hellberg, R.S.; Chu, E. Effects of climate change on the persistence and dispersal of foodborne bacterial pathogens in the outdoor environment: A review. Crit. Rev. Microbiol. 2016, 42, 548–572.
  56. Hofstra, N. Quantifying the impact of climate change on enteric waterborne pathogen concentrations in surface water. Curr. Opin. Environ. Sustain. 2011, 3, 471–479.
  57. Curriero, F.C.; Patz, J.A.; Rose, J.B.; Lele, S. The association between extreme precipitation and waterborne disease outbreaks in the United States, 1948–1994. Am. J. Public Health 2001, 91, 1194–1199.
  58. Patz, J.A.; Vavrus, S.J.; Uejio, C.K.; McLellan, S.L. Climate change and waterborne disease risk in the Great Lakes region of the US. Am. J. Prev. Med. 2008, 35, 451–458.
  59. Mimura, N. Sea-level rise caused by climate change and its implications for society. Proc. Japan Acad. Ser. B-Phys. Biol. Sci. 2013, 89, 281–301.
  60. Steets, B.M.; Holden, P.A. A mechanistic model of runoff-associated fecal coliform fate and transport through a coastal lagoon. Water Res. 2003, 37, 589–608.
  61. Evanson, M.; Ambrose, R.F. Sources and growth dynamics of fecal indicator bacteria in a coastal wetland system and potential impacts to adjacent waters. Water Res. 2006, 40, 475–486.
  62. Halliday, E.; Gast, R.J. Bacteria in beach sands: An emerging challenge in protecting coastal water quality and bather health. Environ. Sci. Technol. 2011, 45, 370–379.
  63. Ackerman, D.; Weisberg, S. Relationship between rainfall and beach bacterial concentrations on Santa Monica Bay beaches. J. Water Health 2003, 1, 85–89.
  64. Fowler, A.M.; Hennessy, K.J. Potential impacts of global warming on the frequency and magnitude of heavy precipitation. Nat. Hazards 1995, 11, 283–303.
  65. Mearns, L.O.; Giorgi, F.; McDaniel, L.; Shields, C. Analysis of daily variability of precipitation in a nested regional climate model-comparison with observations and doubled CO2 results. Glob. Planet. Change 1995, 10, 55–78.
  66. Trenberth, K.E. Conceptual framework for changes of extremes of the hydrological cycle with climate change. Clim. Change 1999, 42, 327–339.
  67. Stewart, J.R.; Gast, R.J.; Fujioka, R.S.; Solo-Gabriele, H.M.; Meschke, J.S.; Amaral-Zettler, L.A.; del Castillo, E.; Polz, M.F.; Collier, T.K.; Strom, M.S.; et al. The coastal environment and human health: Microbial indicators, pathogens, sentinels and reservoirs. Environ. Health 2008, 7, S3.
  68. McLellan, S.L.; Salmore, A.K. Evidence for localized bacterial loading as the cause of chronic beach closings in a freshwater marina. Water Res. 2003, 37, 2700–2708.
  69. McBride, G.B.; Stott, R.; Miller, W.; Bambic, D.; Wuertz, S. Discharge-based QMRA for estimation of public health risks from exposure to stormwater-borne pathogens in recreational waters in the United States. Water Res. 2013, 47, 5282–5297.
  70. Paule-Mercado, M.A.; Ventura, J.S.; Memon, S.A.; Jahng, D.; Kang, J.H.; Lee, C.H. Monitoring and predicting the fecal indicator bacteria concentrations from agricultural, mixed land use and urban stormwater runoff. Sci. Total Environ. 2016, 550, 1171–1181.
  71. Selvakumar, A.; Borst, M. Variation of microorganism concentrations in urban stormwater runoff with land use and seasons. J. Water Health 2006, 4, 109–124.
  72. Rippy, M.A.; Stein, R.; Sanders, B.F.; Davis, K.; McLaughlin, K.; Skinner, J.F.; Kappeler, J.; Grant, S.B. Small drains, big problems: The impact of dry weather runoff on shoreline water quality at enclosed beaches. Environ. Sci. Technol. 2014, 48, 14168–14177.
  73. Edge, T.A.; Crowe, A.; Hill, S.; Seto, P.; Marsalek, J. Surveillance for Potential Sources of E. coli at Toronto’s Bluffer’s Park Beach 2005–2006; Environment Canada: Burlington, ON, Canada, 2007.
  74. Lo Iacono, G.; Armstrong, B.; Fleming, L.E.; Elson, R.; Kovats, S.; Vardoulakis, S.; Nichols, G.L. Challenges in developing methods for quantifying the effects of weather and climate on water-associated diseases: A systematic review. PLoS Negl. Trop. Dis. 2017, 11, 35.
  75. Solo-Gabriele, H.M.; Harwood, V.J.; Kay, D.; Fujioka, R.S.; Sadowsky, M.J.; Whitman, R.L.; Wither, A.; Canica, M.; Da Fonseca, R.C.; Duarte, A.; et al. Beach sand and the potential for infectious disease transmission: Observations and recommendations. J. Mar. Biol. Assoc. UK 2016, 96, 101–120.
  76. Bonilla, T.D.; Nowosielski, K.; Cuvelier, M.; Hartz, A.; Green, M.; Esiobu, N.; McCorquodale, D.S.; Fleisher, J.M.; Rogerson, A. Prevalence and distribution of fecal indicator organisms in South Florida beach sand and preliminary assessment of health effects associated with beach sand exposure. Mar. Pollut. Bull. 2007, 54, 1472–1482.
  77. Heaney, C.D.; Exum, N.G.; Dufour, A.P.; Brenner, K.P.; Haugland, R.A.; Chern, E.; Schwab, K.J.; Love, D.C.; Serre, M.L.; Noble, R.; et al. Water quality, weather and environmental factors associated with fecal indicator organism density in beach sand at two recreational marine beaches. Sci. Total Environ. 2014, 497, 440–447.
  78. Lu, J.R.; Ryu, H.D.; Hill, S.; Schoen, M.; Ashbolt, N.; Edge, T.A.; Domingo, J.S. Distribution and potential significance of a gull fecal marker in urban coastal and riverine areas of southern Ontario, Canada. Water Res. 2011, 45, 3960–3968.
  79. Alm, E.W.; Daniels-Witt, Q.R.; Learman, D.R.; Ryu, H.; Jordan, D.W.; Gehring, T.M.; Santo Domingo, J. Potential for gulls to transport bacteria from human waste sites to beaches. Sci. Total Environ. 2018, 615, 123–130.
  80. Rytkönen, A.; Tiwari, A.; Hokajärvi, A.M.; Uusheimo, S.; Vepsäläinen, A.; Tulonen, T.; Pitkänen, T. The Use of Ribosomal RNA as a Microbial Source Tracking Target Highlights the Assay Host-Specificity Requirement in Water Quality Assessments. Front. Microbiol. 2021, 12, 1–16.
  81. Yamahara, K.M.; Sassoubre, L.M.; Goodwin, K.D.; Boehm, A.B. Occurrence and persistence of bacterial pathogens and indicator organisms in beach sand along the California coast. Appl. Environ. Microbiol. 2012, 78, 1733–1745.
  82. Neumann, B.; Vafeidis, A.T.; Zimmermann, J.; Nicholls, R.J. Future coastal population growth and exposure to sea-level rise and coastal flooding—A global assessment. PLoS ONE 2015, 10, e0131375.
  83. Lemonte, J.J.; Stuckey, J.W.; Sanchez, J.Z.; Tappero, R.; Rinklebe, J.; Sparks, D.L. Sea Level Rise Induced Arsenic Release from Historically Contaminated Coastal Soils. Environ. Sci. Technol. 2017, 51, 5913–5922.
  84. Powers, N.C.; Pinchback, J.; Flores, L.; Huang, Y.; Wetz, M.S.; Turner, J.W. Long-term water quality analysis reveals correlation between bacterial pollution and sea level rise in the northwestern Gulf of Mexico. Mar. Pollut. Bull. 2021, 166, 112231.
  85. DeFlorio-Barker, S.; Wing, C.; Jones, R.M.; Dorevitch, S. Estimate of incidence and cost of recreational waterborne illness on United States surface waters. Environ. Health 2018, 17, 3.
  86. Burnham, J.P. Climate change and antibiotic resistance: A deadly combination. Ther. Adv. Infect. Dis. 2021, 8, 1–7.
  87. Simpkins, G. The costs of infrastructure adaptation. Nat. Rev. Earth Environ. 2021, 2, 661.
  88. Neumann, J.E.; Chinowsky, P.; Helman, J.; Black, M.; Fant, C.; Strzepek, K.; Martinich, J. Climate effects on US infrastructure: The economics of adaptation for rail, roads, and coastal development. Clim. Change 2021, 167, 1–23.
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