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 ^[1][17]. 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 ^[2][18]. 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) ^[3][19]. Subsequently, these changing communities may result in changes to light penetration in the water column, affecting solar-mediated inactivation of indicator organisms and pathogens ^[4][20], 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 ^[3][5][6][19,21,22]. 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 ^[7][23], 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 ^[8][9][10][12,24,25] may intensify due to changes in wave dynamics associated with climate change ^[11][12][8,9].

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 ^[13][69]. In particular, FIB are unable to predict the growth potential of opportunistic pathogens such as those Vibrio species thriving in the water environments ^[14][15][70,71]. Accordingly, models also need to incorporate data from specific pathogens likely to cause human illnesses. For example, Topić et al. ^[16][72] 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.

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 ^[17][73]. 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 ^{[18][19][20][21][22]}[5,6,7,31,32]. 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 ^[23][13] 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 ^[24][14]. Parasitic protozoa may also benefit from rising temperatures, as described in the new WHO guidelines, namely Acanthamoeba and Naegleria fowleri ^[25][74]. 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) ^[26][27][28][33,34,35]. For example, Viau et al. ^[29][36] and Hokajärvi et al. ^[30][37] 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 ^{[18][19][20][21][22]}[5,6,7,31,32].

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 ^[31][46]. 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 ^[29][36]. Likewise, the presence and persistence of Vibrio spp. is closely and positively correlated with water temperatures ^[32][33][34][38,39,40]. It has been further suggested that increasing temperatures would allow for increased range and extended seasonality of Leptospira spp. ^[35][36][37][41,42,43]. The effects of increased temperatures also have the potential to alter the persistence of pathogens in beach sand, including methicillin-resistant Staphylococcus aureus (MRSA) ^[38][44], allergenic fungi, and antifungal resistant fungal species ^[39][16].

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 ^[21][22][31,32]. 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 ^[40][45].

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 ^[41][75]. 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 ^[42][26]. High temperatures lead to increased beach use, for heat relief, especially if exceptional or extreme weather events occur ^[43][44][27,28]. 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 ^[45][46][29,30], 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 ^[47][76], and particularly around the Great Lakes ^[48][77]. 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 ^[39][16].

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 ^[49][78]. 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 ^[50][79]. 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 ^[51][52][53][80,81,82]. 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.

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 ^[54][1] could cause nearshore inundation, coastal erosion and run-off, introducing pathogenic microbes into coastal waters and on beaches ^{[55][56][57][58][59][60][61][62][63][64][65][66]}[47,48,49,50,51,52,53,54,57,83,84,85]. 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 ^[4][57][63][20,49,57]. Changes in global patterns of precipitation are also predicted to amplify existing direct and anthropogenic impacts of microbiota in coastal environments ^[67][46][11,30]. 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 ^[58][68][50,58]. Stormwater outfalls frequently present the greatest direct source of faecal contamination, including pathogens, for adjacent surface waters, even in areas with mixed land use ^[69][70][71][86,87,88]. 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 ^[72][73][55,56].

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 ^[74][90] 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 ^[8][12]. Potential climate-induced changes to microbial interactions between water and sand could have important implications on altered exposure conditions ^[75][91]. 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 ^{[62][76][77][78][79][80]}[54,66,67,92,93,94]. Similarly, periodic tidal rewetting enables FIB and pathogens deposited into dry sands to persist for longer periods ^[62][81][54,68]. 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 ^[82][95]. 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 ^[83][84][62,63]. This may precipitate exposure to more diverse microbial contaminants at beaches.

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 ^[85][96]. 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 ^[8][12], 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 ^[86][97]. These costs are in addition to those required to maintain and enhance infrastructure in a changing environment ^[87][88][98,99].

65. 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.