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Urban Evolutionary Biology. Oxford University Press OUP CORRECTED PROOF – FINAL, 20/03/20, SPi CHAPTER 10 Urbanization and Evolution in Aquatic Environments R. Brian Langerhans and Elizabeth M.A. Kern Langerhans, R.B. and Kern, E.M.A., Urbanization and Evolution in Aquatic Environments In: Urban Evolutionary Biology. Edited by Marta Szulkin, Jason Munshi-South and Anne Charmantier, Oxford University Press (2020). © Oxford University Press. DOI: 10.1093/oso/9780198836841.003.0010 OUP CORRECTED PROOF – FINAL, 20/03/20, SPi 158 URBAN EVOLUTIONARY BIOLOGY 10.1 Introduction other systems to outline testable hypotheses about how evolution might be proceeding (Table 10.1). Throughout the history of our species, we have The timescale of urban evolution is typically typically built our settlements, and especially city viewed on the scale of years to decades—indeed, centres, near water—a pattern that persists to this the burgeoning research on the topic has largely day (Kummu et al. 2011). This is because of not only emerged from studies of contemporary evolution. the necessity of freshwater for life, but also the util­ Consequently, most examples comprise such recent ity of water in travel, commerce, food production, evolutionary change. However, cities first began security, power generation, and other human uses. altering aquatic habitats thousands of years ago. Unfortunately, this means that urbanization has For example, cities of Mesopotamia included large­ had a heavy impact on aquatic species (Vörösmarty scale systems of dikes, dams, canals, levees, and et al. 2010). This impact has been well studied from an gated ditches, causing major alterations to river ecological perspective (Paul and Meyer 2001; Wenger environments—modifications occurring as early as et al. 2009), but the effect of urbanization on aquatic 5000 years ago. More recently, the Aztecs built their species’ evolution is just beginning to be recognized. huge city Tenochtitlán on an island in Lake Texcoco, Understanding evolutionary responses to ur ban­ which flourished from 1325 to 1521. The Aztecs iza tion has many practical applications, from human heavily modified the aquatic environment, with a health to pest control to designing sustainable cities large, complex system of canals, causeways, and (Alberti et al. 2017; Johnson and Munshi­South 2017). aqueducts. Thus, city­induced changes to aquatic Contemporary evolution may affect species per­ environments have likely been causing evolution sist ence, inform conservation decisions, interact with in aquatic organisms for longer timescales than the ecological processes and ecosystem services, and past several decades. Nevertheless, we inevitably even alter how human impacts are gauged. For focus on more recent impacts owing to the paucity example, measuring the toxicity of a specific pol lu­ of studies on longer timescales. tant will lead to inaccurate guidelines if the assayed species is from a population with evolved tolerance 10.2 Biotic interactions (Brady et al. 2017). Owing to the ubiquity of cities, urbanization also presents opportunities to explore We begin by briefly reviewing the kinds of evolution­ evolutionary questions using many replicates and a ary changes that can be caused by disruptions in ‘natural experiment’ design (e.g., see Chapter 3). predator–prey dynamics, competition, and resource– Here we discuss how evolution in aquatic systems consumer interactions (diet). Urbanization affects is influenced by four major categories of changes these biotic interactions in a myriad of ways: for that cities can cause: (1) biotic interactions, (2) physic al instance, artificial light can increase night­time pre­ environment, (3) temperature, and (4) pollution. In dation and alter foraging strategies (Dwyer et al. reviewing evolutionary impacts, we focus on 2013); pharmaceuticals in urban wastewater affect selection, but also discuss genetic drift and gene species’ feeding rates (Brodin et al. 2013); and modi­ flow. Along the way, we take into account as many fied structural habitat can alter prey availability and aquatic taxa as possible: plants, algae, invertebrates, foraging efficiency (Smokorowski and Pratt 2007; fish, and other water­associated organisms (e.g., Bulleri and Chapman 2010). More directly, ur ban­ amphibians, reptiles, and insects with an aquatic iza tion alters biotic interactions by causing the decline larval stage), and we consider all types of aquatic or disappearance of sensitive species (especially habitats, from backyard puddles to sweeping coastal benthic macroinvertebrates; Brown et al. 2009), waters. Despite casting this broad net, we find that introducing non­natives, and increasing the abun­ research on evolution in urban aquatic habitats is dance of species that prefer the altered conditions still nascent, with a modest number of truly well­ (e.g., when slow­water species colonize a reservoir) documented cases. We highlight such cases where (Paul and Meyer 2001). possible, but in areas where no research has been How species in aquatic habitats respond evolu­ done, we use theory and empirical studies from tionarily to urban changes in biotic interactions is OUP CORRECTED PROOF – FINAL, 20/03/20, SPi EVOLUTION IN URBAN WATERS 159 Table 10.1 Major impacts of urbanization on evolution in aquatic species reviewed in this chapter. Type of urban impact Types of changes Likely selection targets BIOTIC INTERACTIONS Predation Novel predators Prey life history, morphology, chemical defenses, anti-predator Loss of predators behaviour Changes in predator abundance or behaviour Higher/lower predation pressure Competition Novel competitors Foraging and feeding behaviour, body size, trophic traits, diet Loss of competitors specialization Changes in competitor abundance or behaviour Higher/lower intraspecific competition Diet Changes in abundance and diversity of food, Broader/narrower niche width, gut length, eye position and consumer behaviour, or foraging habitat morph ology, locomotor traits, trophic traits Less terrestrial inputs to streams PHYSICAL ENVIRONMENT Habitat fragmentation Smaller populations Life-history strategies, dispersal traits, body size, locomotor More isolated populations traits, mating system, sexual signals, anti-predator behaviour, Reduced movement distances trophic traits Altered habitat Urban stream flow Increased stream flashiness Body morphology, fin morphology, body size, swimming Higher maximum velocity and variance performance TEMPERATURE Urban heat island Warmer habitat Timing of spring and autumn events, morphology, body size, effect Longer growing seasons pace-of-life syndrome traits, growth rate, thermal tolerance, sex determination POLLUTION Metals/inorganics Higher concentrations of lead, zinc, copper, Resistance/tolerance mechanisms cadmium, chromium, arsenic, nickel, and salt Synthetic organic Presence of PHCs, PAHs, PCBs, endrocrine Resistance/tolerance mechanisms compounds disruptors, antibiotics, and pesticides Altered ecosystem productivity Altered chemical signalling Artificial light at night Altered light intensity and spectra at night Diel behavioural patterns, movement/migration traits, sexual Altered community composition, predator size, signals, phenology, endocrine systems, foraging traits, and behaviour schooling behaviour Disruption of hormone expression Anthropogenic sound Elevated noise levels Acoustic signal and receiver traits, endocrine systems, social Altered frequencies of background sounds behaviours, foraging traits, stress response, schooling behaviour Nutrients and Increased presence of sewage and nitrogen Toxin resistance, body size, oxygen uptake mechanisms, blood suspended particles Increased turbidity pigments, metabolic rate, visual signal traits Lower dissolved oxygen levels Eutrophication Phytoplankton blooms PHCs, petroleum hydrocarbons; PAHs, polycyclic aromatic hydrocarbons; PCBs, polychlorinated biphenyls. OUP CORRECTED PROOF – FINAL, 20/03/20, SPi 160 URBAN EVOLUTIONARY BIOLOGY mostly unknown. However, prior work in urban independently affect vertical migration in zoo­ terrestrial systems and the large body of research on plankton (Gliwicz 1986; Moore et al. 2001). In such evolution in aquatic species allow us to predict how situations, model­selection approaches are useful. urban aquatic species should evolve in response to Research on Bahamian mosquitofish (Gambusia spp.) altered predation, competition, and diet. We will in tidal creeks—where road construction across the refer to mosquitofish (Gambusia spp.) several times creeks has caused dramatic ecological changes that here and throughout the chapter because it has include reduction of predatory fish—has employed become a model genus for studying rapid and model­selection approaches to identify the putative human­induced evolutionary changes. agents underlying phenotypic changes. Changes in predation by piscivorous fishes was found to drive trait changes over ~ 35–50 years in male genital 10.2.1 Predation morphology, muscle mass, and fat content, but not Predation strongly influences evolution, with many male colouration (Heinen­Kay et al. 2014; Giery well­documented examples from aquatic species. et al. 2015; Riesch et al. 2015). To name a few, threespine stickleback, poeciliid live­ bearing fishes, and crustacean zooplankton have all 10.2.2 Competition served as models for how predation drives evolution­ ary divergence. Although there is not yet enough Competition is another strong evolutionary force that research for us to generalize how predation regimes can be disrupted by urbanization. A meta­analysis
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