Geographic Range and Natural Distribution

C H A P T E R

4 Geographic Range and Natural Distribution Carole J. Lee, Charles R. Tyler, Gregory C. Paull Department of Biosciences, University of Exeter, Exeter, Devon, United Kingdom range of freshwater fish species (Jackson, Peres-Neto & Olden, 2001). Biotic factors, such as predation and competition, are also influential (Gaston, 2003). Determining the geographic range of a species can be tricky. In fact, it is usually impractical, in terms of time and budget, for a single researcher to conduct a complete survey across a large geographical area, and so data from a variety of sources, such as biological surveys, scientific reports, and museum specimens, are often relied on. The accuracy of this information can vary and without careful scrutiny errors in identification or taxonomy may perpetuate over time (Kottelat & Freyhof, 2007).

Geographic range and natural distribution are two of the fundamental characteristics of a species (Gaston, 2003). This chapter provides a broad overview of the range and distribution of zebrafish. It describes the typical habitats of wild zebrafish, the biotic and abiotic factors that determine range limits, and the potential implications of environmental change and human interference. Knowledge on wild zebrafish populations and the environment in which they live is vital for understanding the natural genetic and phenotypic variation, interpreting observations on their morphology, physiology, and behavior in the laboratory, and in designing and refining optimum housing systems and husbandry practices.

Geographic Range of the Zebrafish Geographic Range

The geographic range of the zebrafish extends across much of India, Bangladesh, and Nepal, from the Pakistan border in the west to the Myanmar border in the east, and from the foothills of the Himalaya in the north to the paddy fields of Karnataka in the south (Fig. 4.1; Engeszer, Patterson, Rao & Parichy, 2007). Geographically, this area comprises three major regions: the northern mountains, the Indo-Gangetic Plain, and the Indian peninsula. The northern mountains comprise the Himalaya and Hindu Kush ranges, which run from east to west in an arc across the entire northern boundary of India. South of the mountains, the IndoGangetic Plain encompasses the vast, fertile floodplains of the Indus, Ganges, and Brahmaputra rivers. These floodplains comprise most of northern India and almost all of Bangladesh. To the west lies the desert of Rajasthan, while to the south is the Indian peninsula, an immense plateau flanked by the coastal mountains of the Western and Eastern Ghats, which projects into the Indian Ocean (Thapar, 2004). As with most species, the zebrafish is not evenly distributed throughout its range. Reliable first-hand reports document populations in the streams and

The geographic range of a species comprises the regions in which that species can be found. The geographic ranges of fish species vary in size enormously. At one end of the spectrum are those whose distribution extends the entire world across tropical or temperate waters, such as the swordfish (Xiphias gladius) and the basking shark (Cetorhinus maximus) (Gaither, Bowen, Rocha & Briggs, 2016). At the other end of the spectrum are endemic species confined to a restricted area, such as the gizani (Ladigesocypris ghigii), which lives only in streams on the Greek island of Rhodes (Stoumboudi, Barbieri, Mamuris, Corsini-Foka & Economou, 2002), and the Quitobaquito pupfish (Cyprinodon macularius eremus), which is found in a single spring outflow in the Arizona desert (Douglas, Douglas & Brunner, 2001). The factors that limit geographic ranges are so varied and the interactions among them so complex that they are not fully understood for any single species (Gaston, 2009). Climate (especially temperature) and water chemistry (including levels of dissolved oxygen and acidity) play an important role in determining the geographic The Zebrafish in Biomedical Research https://doi.org/10.1016/B978-0-12-812431-4.00004-X

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4. Geographic Range and Natural Distribution

FIGURE 4.1 The geographic range of the zebrafish comprises the foothills of the northern mountains, the Indo-Gangetic Plain, and the Indian peninsula.

FIGURE 4.2 Wild zebrafish found in Bangladesh. Photo by Gregory Paull.

tributaries of rivers in the Himalaya drainage system of Nepal (Dhital & Jha, 2002), the floodplains of the Ganges and Brahmaputra rivers in India and Bangladesh (Fig. 4.2; Spence et al., 2006; Engeszer et al., 2007; Arunachalam, Raja, Vijayakumar, Malaiammal & Mayden,

2013), and along the Western Ghats (Dahanukar, Raghavan, Ali, Abraham & Shaji, 2011). Compilations of older records report specimens found in Rajasthan (Datta & Majumdar, 1970) and in the peninsula’s southeast region (Menon, 1999). No systematic field studies have mapped the occurrence of the zebrafish throughout its range, and it may be missed from species surveys due to its small size and lack of commercial value (Spence et al., 2008). As a result, zebrafish may be more widely distributed than previously thought. It should be recognized that the geographic range of any species is dynamic. It expands, contracts, or shifts over time in response to changes in climate or physical geography (Thomas, 2010). The ability of the zebrafish to expand or move its range boundaries in response to environmental change is constrained by the physical barriers of the northern mountain ranges to the north, east and west, and by the Indian Ocean to the south. Within its range boundaries, the dispersal of zebrafish to new areas in response to changing conditions is limited to the floodplains and drainage basins that it inhabits and is influenced by interactions with other species (predators and competitors) whose abundance

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Natural Distribution

and diversity are also affected by climate (Thomas, 2010). Human activities, such as farming, flooding arable land to create paddy fields, and connecting previously unconnected water bodies with drainage ditches, may also influence the dispersal of zebrafish.

Home Range Most animals live within a home rangedan area that contains the resources that they need to avoid predation, find food, and reproduce (Welsh, Goatley & Bellwood, 2013). Usually, an animal’s resource requirements change as it grows and matures, and therefore the size of its home range changes with ontogeny. With fish, the smaller the animal, the higher the risk of predation (Miller, Crowder, Rice & Marschall, 1988). A young fish may restrict its home range and avoid risky locations to avoid predators. As it grows, the young fish’s vulnerability to predation decreases and its food requirement increases, allowing it to expand its home range. Finally, as the fish matures, its home range must be big enough to allow it find a mate and reproduce (Welsh et al., 2013). For example, gold-spot mullet (Liza argentea) spawn in coastal waters and the lower reaches of estuaries in tropical and temperate regions (Kendall & Gray, 2008). Larval mullet migrate into the estuaries and seek protection in dense vegetation or in mangrove forests where a labyrinth of tangled roots hampers the movements of large predators (Laegdsgaard & Johnson, 2001). As they grow, juvenile mullet develop greater mobility and can more easily escape from predators. This enables them to move to adjacent habitats, such as seagrass beds or mudflats, and then to open estuarine habitats where they feed on larger prey items before joining adult populations in deep waters (Laegdsgaard & Johnson, 2001). Little is known about the average size of a zebrafish home range. Studying the home range of fish in the low visibility of vegetated habitats or turbid waters is challenging, especially with a diminutive, highly mobile species such as the zebrafish. Tagging individual fish to radiotrack their movements has been used successfully to study larger species (Cooke et al., 2013) but has not been attempted with wild zebrafish. However, recent advances in technology have resulted in smaller, more efficient tags and passive integrated transponders that increase the potential to track smaller fish species and juvenile life stages (Cooke et al., 2016). Innovations continue, and the home range of the zebrafish should soon be testable. As water levels rise at the start of the monsoon, zebrafish are thought to migrate laterally from rivers, streams, and irrigation channels where they spend the dry months to flooded areas such as paddy fields where they spawn in the nutrient-rich waters. When water levels recede at the end of the monsoon, adults and

young-of-the-year migrate out of the floodplains and into rivers, streams, and channels (Engeszer et al., 2007). Little is known about this lateral migration, and the distances covered have not been measured. Zebrafish home range size therefore varies seasonally and may differ in streams versus floodplains due to the correlation of home range size with food supply (Minns, 1995). The spatial behavior of zebrafish at all life stages and throughout the seasons needs to be assessed to understand the extent of their home-ranging behavior.

Natural Distribution The terms geographic range and natural distribution are sometimes used interchangeably, but here we define natural distribution as “the specific areas, within its geographic range, in which a species occurs.” For example, the geographic range of the zebrafish includes the Western Ghats of India. Within the Western Ghats, the natural distribution of the species includes the Thunga River in the state of Karnataka and the Kabini River in the state of Kerala where populations of zebrafish have been found (Arunachalam et al., 2013). A species’ natural distribution may change over time, regardless of whether its geographic range moves, as habitats become more or less favorable due to changes in the physical or biological environment (Lawton, 1996). Much of the zebrafish’s natural distribution lies within the extensive floodplains of the Ganges and Brahmaputra rivers. Indeed, the zebrafish has been described as a “floodplain species” (Spence et al., 2008) and seems well adapted to constantly changing environmental conditions in the floodplains. Typical habitats of zebrafish include streams, drainage ditches, and ponds, often adjacent to rice paddies (McClure, McIntyre & McCune, 2006; Spence et al., 2006). In addition, Engeszer et al. (2007) and Arunachalam et al. (2013) found zebrafish in secondary and tertiary channels of large alluvial rivers. Together, these field studies report a range of habitat features in the specific locations where zebrafish were found. Some areas have still waters while others have slow to medium water flow. Water clarity ranges from clear to muddy, and substrates are recorded from silt at one end of the spectrum, through sand, gravel, pebbles, and boulders, to bedrock at the other end of the spectrum. Vegetation ranges from none at all to an abundance of submerged plants, with or without overhanging canopy. Some of these habitats are permanent while others are transitory and form during the monsoon. In summary, the zebrafish can be found in a diverse array of habitats throughout its huge geographic range; however, the geographic, climatic, and temporal factors that influence the distribution of zebrafish and the endogenous and exogenous pressures that drive them to occupy certain habitats are not well understood.

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4. Geographic Range and Natural Distribution

Floodplains Floodplains are areas that are periodically inundated by the lateral overflow of rivers or lakes and/or by direct precipitation (Junk, Bayley & Sparks, 1989). They contain a medley of habitats and support diverse biotic communities. The floodplains of northern India and Bangladesh flood seasonally from June to October in response to monsoon rains and snow melt (Craig, Halls, Barr & Bean, 2004). Most of this vast region has been converted to agricultural land for the production of rice and other crops while fishing, by professional and subsistence fishers, contributes to floodplain livelihoods (Hoggarth et al., 1999). During monsoon rains, the floodplains are inundated with nutrient-rich waters, causing rapid growth of macrophytes and periphyton, increased concentrations of invertebrates, and an accumulation of detritus from vegetation and phytoplankton. Fish follow the advancing water’s edge and flooded areas become important food-rich nurseries for larval and juvenile fish. When water levels drop, vegetation becomes stranded, the food supply decreases, and surviving adult and young-of-the-year fish of many species migrate from the floodplains to channels, rivers, and other permanent water bodies (Bayley, 1988). Zebrafish are believed to spawn in shallow waters during the monsoon, and their opportunistic life history strategy of small body size, rapid growth, early maturity, and high fecundity allows them to reproduce and disperse while conditions are favorable and food is plentiful. Floodplain fishes rarely survive for more than a year (De Graaf, 2003), and field observations of wild zebrafish support this assumption (Spence, Fatema, Ellis, Ahmed & Smith,2007). Within the floodplains are a mosaic of habitat types, including major rivers and their secondary channels, canals, permanent lakes (baors), floodplain depressions (beels), excavated fish pits (kuas), and household ponds (mathels) (Hoggarth et al., 1999). Field studies have reported populations of zebrafish in most of these habitats.

Rivers The two major floodplain rivers within the zebrafish’s natural distribution are the Ganges and the Brahmaputra. Bedload sediments of sand and silt roll along the bottom of the main channels of both rivers, forming a sequence of dunes up to 6 m high, which slowly move along with the current (Garzanti et al., 2010). These shifting substrates are unfavorable for aquatic plants and invertebrates. As a result, vegetation tends to fringe the main channel borders and side channels where substrates are more stable (De Graaf, 2003). Fish abundance is highest at the channel borders where plant beds create diverse habitats and food is more plentiful (Junk, Bayley & Sparks, 1989).

FIGURE 4.3 Zebrafish have been found in tributaries of major rivers such as the Brahmaputra but have not been reported in the main rivers themselves. Photo by Gregory Paull.

Zebrafish have been captured in the tributaries and drainages of the Ganges and Brahmaputra, but none have been reported in the main rivers themselves (Fig. 4.3). Elsewhere in India, Arunachalam et al. (2013) collected zebrafish in a side channel of the Dikrong River, a major tributary of the Brahmaputra, and in a secondary channel of the Thunga River in the Western Ghats. During a field trip to investigate the habitats of wild zebrafish, Engeszer et al. (2007) traveled to northeast India and found populations in the Ghotimari River and in a tributary of the Jorai River, both in West Bengal, and further populations in the Dukan River in the hills of Meghalaya. The absence of zebrafish in major rivers is likely due to the effects of predation and competition or a lack of suitable food resources or spawning areas. Predators in rivers and streams affect habitat choice of prey species such as zebrafish, which tend to move into shallow waters or complex habitats or leave the site to avoid predators (Jackson, Peres-Neto & Olden, 2001). The effects of interspecific competition on river fish communities may also play a role in the absence of zebrafish from major rivers, although this has not been tested in the field.

Streams Stream types range from perennial snow- or monsoon-fed hill streams that drain the northern mountains and the Western Ghats to seasonal nalas that develop during the monsoon. Zebrafish are absent from fast-flowing hill streams but have been found in slower streams with shallow waters (Fig. 4.4). They appear to have restricted ranges of current velocity and water depth but tolerate variety in other habitat

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Natural Distribution

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FIGURE 4.4 Zebrafish have been found in slow streams with shallow waters and abundant vegetation. Photo by Gregory Paull.

FIGURE 4.5 Sampling zebrafish in a shallow pond in Bangladesh. Photo by Gregory Paull.

features, such as substrate type and the presence or absence of submerged vegetation. A detailed account of the stream habitat preferences of zebrafish is given in a field report by Arunachalam et al. (2013) who collected individuals from 11 streams in the Western Ghats and northern and northeastern states of India. The team found zebrafish in stream areas with overhanging vegetation or undercut banks and in places where alcoves or shallow pools had been created by bedrock or large boulders. Substrates varied from silt and sand to cobbles and bedrock, but all the habitats had low water flow (3.5e13.9 cm/s) and shallow depth (<110 cm). These observations are consistent with other field studies (Engeszer et al., 2007; McClure, McIntyre & McCune, 2006; Spence et al., 2006).

the Indian subcontinent (Gopal, Sengupta, Dalwani & Srivastava, 2010; Hoggarth et al., 1999; Khondoker, Hossain & Moni, 2014). Zebrafish have been found in many wetland habitats. Populations have been recorded in beels and jheels (Arunachalam et al., 2013), in lakes and ponds (Fig. 4.5; Pritchard, 2001; Spence et al., 2006; Spence, Fatema, et al., set link 2007), and in shallow pools and swamps (Engeszer et al., 2007). All the recorded occurrences of zebrafish in wetlands have been in shallow areas, usually with abundant vegetation.

Natural Still Bodies of Water Natural wetlands comprise a variety of lakes, ponds, pools, and marshes. Permanent lakes, or baors, are often large and deep, fed by rivers, streams, or groundwater discharges, supplemented by monsoon rains, and have relatively small changes in water level. Most baors are fringed by marginal plants but contain little aquatic vegetation. In contrast, shallow lakes, or beels, are seasonal with large changes in water level. They form in natural depressions that flood during the monsoon. During the dry season, waters recede leaving small shallow lakes that eventually dry up. Beels support abundant aquatic vegetation and diverse communities of birds, fish, and invertebrates. Oxbow lakes, or jheels, formed by dead arms of rivers, are also seasonal, flooding deeply during the monsoon and drying partially or completely in winter. Isolated ponds, marshes, and swamps also contribute to the extensive wetlands of

Man-Made Habitats In addition to natural wetlands, zebrafish inhabit man-made habitats such as canals, fish pits, household ponds, and, famously, rice fields (Spence et al., 2008). Rice is grown throughout much of the Indian subcontinent. During the rainy season, rice fields flood and become connected to neighboring water courses and wetlands. The floodwater carries aquatic organisms, including fish, into the fields where invertebrates, plants, and microorganisms are a rich food source and rice plants provide hiding places and spawning sites. During the dry season, the water level drops and the fields stagnate and eventually dry, forcing fish to return to the water courses or become trapped in shallow water. Rice fields can be considered as agriculturally managed marshes, and fish harvested from rice fields are an additional source of income for farmers (Das, 2002; Fernando, 1993). Zebrafish are well adapted to conditions in rice fields (Fig. 4.6) and adjacent irrigation and drainage ditches where shallow waters, abundant food, and lack of large predatory fish are ideal for them. They are eurythermal

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4. Geographic Range and Natural Distribution

Temporal Distribution

FIGURE 4.6

Zebrafish are commonly found in rice fields. Photo by

Gregory Paull.

(Cortemeglia & Beitinger, 2005) and tolerate the wideranging temperatures and fluctuating levels of oxygen that result from shallow water depth. Although zebrafish have little commercial value and are caught for food only in rural areas of Bangladesh (Hossain & Afroze, 1991), their presence in rice fields may benefit farmers by reducing the need for pesticides and fertilizers without lowering rice productivity (Lansing & Kremer, 2011).

Connectivity Between Habitats Connectivity refers to the pathways that link habitats and the relative ease with which individuals can move through the landscape between habitat patches (Joint Nature Conservation Committee, 2017). It also refers to linkages between adjacent and distant habitats. The interconnected waterways, drainage ditches, and canals that crisscross much of the zebrafish’s area of natural distribution, together with large-scale flooding during monsoons, create connectivity between populations, despite the movements of individuals being limited by their diminutive size (Gratton et al., 2004). One way to assess connectivity is to measure gene flow (Hedgecock, Barber & Edmands, 2007). A genetic analysis of four zebrafish populations in eastern India from sites 50 or more miles apart suggests that connectivity between the four habitats is continuous and that significant mixing of populations occur (Gratton et al., 2004). Another study found that populations in the Western Ghats, southern Bangladesh, and western and central Nepal are genetically distinct from those in the Ganges and Brahmaputra river basins, indicating that physical barriers exist between regions within the species’ geographic range (Whiteley et al., 2011).

The spacial ecology of zebrafish and how this changes over time is not well understood. Zebrafish are believed to migrate, at the onset of monsoon rains, from rivers, streams, and channels to flooded areas where they breed (Engeszer et al., 2007). However, the factors that influence this temporal distribution and the amount of time that populations spend in these different habitats have not been tested in the field. Similar questions have been addressed in mosquitofish, Gambusia affinis, and other small fishes by using minnow traps to determine their temporal dispersal in rice fields in the United States (Blaustein, 1989; Davey & Meisch, 1977). This simple method could be tested on zebrafish in rice fields and natural habitats. A deeper understanding of the ecology of zebrafish at a variety of spatial and temporal scales can be used to identify critical habitats and inform decisions regarding housing and husbandry methods for the generation and maintenance of laboratory zebrafish.

Climate The Indian subcontinent is a region of extreme climates. In the far north is alpine tundra, in the far south are tropical rainforests, and in between is the wettest place on earth (Mawsynram, in the state of Meghalaya; Guinness World Records, 2018). The climate is influenced by the northern mountains, which prevent frigid air flowing down from central Asia, and by the western desert, which draws moisture-laden winds over the oceans. These monsoon winds dominate the region’s climate and provide most of its rainfall (Fig. 4.7; Krishnamurthy, 2017). The zebrafish’s areas of natural distribution fall within “subtropical humid zones” (the foothills of the northern mountains and the floodplains of the Ganges and Brahmaputra) and “tropical wet and dry zones” (the Western Ghats), according to the Koppen system of climatic classification (Ko¨ppen, 1884).

Seasons The Indian subcontinent has four seasons. January and February, the coldest months, are considered the winter season. From March until May is the summer, or premonsoon season, when temperatures rise and remain high until the start of the monsoon rains in June. The monsoon season lasts until October and is followed by a postmonsoon, or “retreating monsoon” season which continues until the end of the year (Krishnamurthy, 2017). The life cycle and growth of tropical floodplain fish is highly seasonal, with maximum feeding and growth occurring in the

I. Introduction

Seasons

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FIGURE 4.7 Annual rainfall across the Indian subcontinent.

monsoon and postmonsoon seasons (Hoggarth et al., 1999), and this is likely also true of zebrafish.

Winter The relatively cold winter months of January and February are also the driest months throughout much of the subcontinent although there are a few exceptions. Snowfall is common in the northern mountains, and some areas, such as the Coromandel Coast in the east of the peninsula, receive heavy winter rainfall (Krishnamurthy, 2017). Zebrafish adults and young-of-the-year are believed to spend the winter in perennial streams and lakes (Engeszer et al., 2007) as many rice fields and other seasonally flooded areas are partially or completely dry at this time of year (Das, 2002).

Summer The summer months of March, April, and May, also known as the “premonsoon” months, are characterized by rising temperatures and low humidity. Hot, dry winds originate in the western desert and blow over

the Gangetic Plain, creating dust storms and drying vegetation. Violent storms, accompanied by heavy showers of rain or hail, occur in eastern and northeastern parts of the subcontinent, and thunderstorms develop in the far southern peninsula and Western Ghats (Jain, 2017). Summer storms are most intense in Bangladesh, where southerly cyclonic winds may reach speeds of 160 km per hour and cause severe flooding in coastal areas (Karim & Mimura, 2008).

Monsoon The hot air that built up during the summer months creates low-pressure areas in the Gangetic Plains into which moisture-bearing southwestern monsoon winds flow from the Indian Ocean. The monsoon breaks on the west coast of India at the beginning of June, bringing heavy rains and strong winds, and reaches most parts of the subcontinent by the end of June. During July and August, monsoon rains are interspersed with dry spells. This pulsating of the monsoon is irregular and varies across the subcontinent, causing flooding in some areas and droughts in others (Jain, 2017). More than 12% of the

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4. Geographic Range and Natural Distribution

land surface of India is prone to annual flooding (Sharma & Priya, 2001), and in Bangladesh, annual floods submerge 20%e70% of the country (Mirza, 2002). As floodplains are inundated by monsoon rains, the biomass and production of periphyton and invertebrates increase and many fish species migrate from river channels to floodplains to breed and give their offspring the advantage of this timely opportunity to feed and grow (Hoggarth et al., 1999).

(Oncorhynchus kisutch) feed in cold habitats where food is abundant and the move to warmer habitats to assimilate their food (Armstrong et al., 2013). Systematic finescale sampling of water temperature, depth, and vegetation could help identify environmental relationships, investigate microclimate use by zebrafish, and study changes in microclimates over the seasons.

Altitudes Postmonsoon From the middle of September, the southwestern monsoon winds begin to weaken as the trough of low pressure over the Indo-Gangetic plains gradually moves to the Bay of Bengal. The winds then change direction and begin to blow from the northwest, causing the southwestern monsoon to “retreat.” This change from monsoon to postmonsoon or “retreating monsoon” season is gradual and continues until the end of the year. The beginning of the postmonsoon is marked by a return of the intense storms that affect Bangladesh and the southern coast of India during the summer, but eventually, the monsoon recedes, clear skies replace dense clouds, temperatures drop, and the transition to the cooler, drier winter season is complete (Jain, 2017).

Altitude and temperature are strongly correlated. Altitude creates gradients in temperature and precipitation and affects levels of dissolved oxygen in water, all of which impact fish diversity (Boll et al., 2016). Generally, species diversity decreases as altitude increases (Zhao, Fang, Peng, Tang & Piao, 2006). Zebrafish have been recorded at a wide range of altitudes, from 14 m in the coastal region of Orissa province in eastern India (Engeszer et al., 2007) to 1576 m in the hills of Arunachal Pradesh in northeastern India (Arunachalam et al., 2013). Most field reports, however, do not include altitude data, and it is possible that zebrafish occur at higher or lower altitudes than previously reported. In addition, likely differences in abundance and diversity of zebrafish prey and predators at different altitudes remain to be investigated.

Regional Microclimates Individual animals experience a series of fine-scale microclimates rather than the average conditions of their home range (Suggitt et al., 2011). Riparian and aquatic vegetation, water depth and air temperature all affect freshwater microclimates (Welch, Jacoby & May 1998). Increasing temperatures stimulate production of microorganisms and invertebrates and so benefit fish, but effects are negative if temperatures exceed the maximum for optimum fish growth (Welch, Jacoby & May 1998). Riparian vegetation shades the edges of streams and lakes, creating microclimates that provide cooler refuges for fish. This cooling effect decreases with increased water body size (Brazier & Brown, 1973). Small streams and ponds with low flow rates, shallow depth, and overhanging vegetation, as favored by zebrafish, are generally cooler in summer and warmer in winter than similar waters with no vegetative cover (Welch, Jacoby & May 1998). Interestingly, fish may move among habitats to take advantage of thermal diversity. For example, lake-dwelling juvenile sculpin (Cottus extensus) feed at the bottom of the lake during the day and spend the night at warmer temperatures higher in the water column, a behavior which is believed to aid digestion and therefore increase growth (Neverman & Wurtsbaugh, 1994). Similarly, stream-dwelling juvenile coho salmon

Temperatures Temperatures across India vary widely between seasons and across regions (Fig. 4.8). Northern and central areas experience summer temperatures in excess of 45 C, while the west coast and southern parts of the peninsula are generally 5e10 C cooler and temperatures in the far northern mountains rarely exceed 25 C (Jain, 2017). In Bangladesh, summer temperatures range from 38 to 41 C with only slight variations between regions, and daytime winter temperatures are typically 16e20 C (Siddik & Rahman, 2014). Northern parts of India have a mean daytime winter temperature of 20 C, but this may fall to below freezing point at night. Temperatures increase from north to south, with the west coast and southern India having daytime winter temperatures of around 30 C, falling to 20 C at night. In the Western Ghats, night-time winter temperatures may drop to freezing point (Jain, 2017; Jain, Agarwal & Singh, 2007). Zebrafish are eurythermal (Cortemeglia & Beitinger, 2005). Their temperature tolerances in the wild are unknown, but field studies at sites where zebrafish were sampled report temperatures ranging from 12 C in Arunachal Pradesh (Arunachalam et al., 2013) to 39 C in

I. Introduction

Water Conditions

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FIGURE 4.8 Mean annual temperatures across the Indian subcontinent.

Orissa (Engeszer et al., 2007). Laboratory studies suggest that wild-type zebrafish have a lower lethal temperature of 6.2  0.28 C and an upper lethal temperature of 41.7  0.35 C (Cortemeglia & Beitinger, 2005).

environmental variables are regulated by water depth (Miranda, 2011). Overall, the ever-changing quality and mixing of waters creates a diverse floodplain ecosystem (Moyle, Crain & Whitener, 2007).

Depth

Water Conditions Water conditions, including depth, flow, turbidity, pH and salinity, change drastically between wet and dry seasons in floodplains, rice fields, and streams. These variables contribute to the organization of the communities of organisms that occupy these areas. As flood waters rise, seasonally dry areas become colonized by invertebrates and fish that enter the floodplains from the river, forming a complex community in the nutrient-enriched waters. As flood waters recede, microbes in decomposing plant biomass consume large volumes of oxygen and releases carbon dioxide into the water, creating hypoxic conditions (Junk, Bayley & Sparks, 1989) that are intolerable to many species that must return to the rivers or become stranded in increasingly shallow and eutrophic water. Most of these

Zebrafish have been found in water depths from 5 cm (in an irrigation channel; Suriyampola Shelton, Shukla, Roy & Bhat, et al., 2015) to around 1 meter (in a small pond; Spence et al., 2006). Such shallow waters tend to have stronger fluctuations of temperature and dissolved oxygen levels than deeper waters (Miranda, 2011). They have reduced habitat complexity and may be more turbid and eutrophic due to agitation of the benthos by bottom-feeding organisms (Miranda, 2011). For small species such as zebrafish, shallow waters offer protection against larger-bodied fish and piscivores that tend to be intolerant of these conditions (Shields & Knight, 2013), but many avian predators, such as the common kingfisher (Alcedo atthis) and the Indian pond heron (Ardeola grayii), are attracted to shallow waters (Spence et al., 2008).

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4. Geographic Range and Natural Distribution

Flow

Turbidity

Water flow rate is an important component of microhabitat use by zebrafish. As water velocity increases, the metabolic cost to a fish of holding its position and swimming increases while foraging success decreases (Hill & Grossman, 1993). Zooplankton and insects that form a large part of zebrafish diet (McClure, McIntyre & McCune, 2006) may be harder to locate and catch in swiftly flowing water, increasing the energetic cost of foraging. Water flow also affects the survival of eggs and juveniles. Eggs may be swept away, and young fish may have insufficient swimming ability to counteract high velocities (Sukhodolov, Bertoldi, Wolter, Surian & Tubino, 2009). Zebrafish have been found in still waters (Spence et al., 2006) and in waters with flow rates of up to 18 cm per second (Suriyampola et al., 2015). This variation is likely due to the use of different habitats in different seasons, with the high flow rate recorded in a fast-moving river during the postmonsoon season (Suriyampola et al., 2015) when the fish were likely not breeding. Zebrafish have only rarely been found in large river systems where the flow is high. Individuals that respond to the fluctuating benefits and costs of different microhabitats and flow rates may have a survival advantage.

Turbidity is a measure of water clarity (Voichick, Topping & Griffiths, 2017). Dissolved solids and suspended particles in water scatter and absorb light, decreasing the amount of sunlight that penetrates the water column and reducing visibility (Voichick, Topping & Griffiths, 2017). Low visibility reduces the ability of visually foraging fish to detect their prey, but the level of effect depends on the type of prey. In clear waters, piscivorous fish can detect their prey (other fish) at greater distances than planktivorous fish can detect their prey (zooplankton). However, in turbid waters, the hunting ability of piscivores is impaired more than the hunting ability of planktivores (Voichick, Topping & Griffiths, 2017). For a prey species such as zebrafish whose diet consists largely of zooplankton, increasing turbidity reduces not only the hunting ability but also the risk of predation. Studies show that the decrease in predation risk is greater than the decrease in feeding opportunity (Voichick, Topping & Griffiths, 2017), so turbid waters may offer an advantage to zebrafish. Turbidity levels vary among zebrafish habitats (Fig. 4.9) and seasonal changes in turbidity may also occur due to extreme weather patterns, such as monsoon winds and rains. Spence et al. (2006) used a Secchi disk

FIGURE 4.9

(A) Measuring water clarity with a Secchi disk; (BeD) examples of waters with different turbidity levels. Photos by Gregory Paull.

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Vegetation

(Hou, Lee & Weidemann, 2007, Fig. 4.9A) to measure water clarity at several locations where they found zebrafish. The highest clarity was 50 cm in a ditch and the lowest was 15 cm in several ponds. The combination of shallow waters and moderate turbidity may allow zebrafish to decrease predator avoidance behavior and increase feeding opportunities. Turbidity may also lower the predation risk for larval zebrafish.

pH The acidity of water is measured on a potential hydrogen (pH) scale of 0e14. The lower the pH value, the more acidic the water, with 7 representing neutrald neither acidic nor alkaline (Dodds, 2002). Factors that affect the pH in natural freshwaters include the mineral composition of the surrounding rock, acidic precipitation (acid rain), wastewater and other discharges from anthropogenic sources, and photosynthesis by aquatic plants (Alabaster & Lloyd, 1982). The pH of water affects the ability of fish to regulate basic physiological functions such as respiration and the exchange of gasses and salts with the water (Alabaster & Lloyd, 1982). The pH of most natural freshwaters in which fish are found range from about 6 to 9 (Ellis, 1937). Wild zebrafish have been caught in waters with pH values from 5.9 (Engeszer et al., 2007) to 9.8 (Arunachalam et al., 2013), while laboratory zebrafish survive in acidic waters as low as pH 4.0 (Kwong, Kumai & Perry, 2014) although their ability to breed at such low pH values was not tested.

Substrates Substrates are an important component of freshwater habitats. Large diameter substrates provide foraging opportunities, refuge from predators, and shelter from strong currents (Rankin, 1986). Substrate size influences habitat selection by some freshwater fish species (Johnson & Kucera, 1985; Rankin, 1986), and substrate stability affects the diversity and densities of benthic insects (Cobb, Galloway, & Flannagan, 1992) on which fish may prey. Zebrafish are found over substrates ranging from silt, sand, and gravel to pebbles, boulders, and even bedrock (Arunachalam et al., 2013; Engeszer et al., 2007; McClure, McIntyre & McCune, 2006; Spence et al., 2006). Some of this variance may be explained by diel differences in behavior. Zebrafish usually spawn in the early morning, scattering their eggs over the substrate. Although they provide no parental care and may eat their own as well as others’ eggs, zebrafish are selective about oviposition site and prefer to spawn on gravel (Spence, Ashton & Smith, 2007). Egg survival is greatest in graveldthe interstitial spaces within gravel aid oxygenation and protect eggs from predationdand the use of gravel as spawning substrate may be an adaptive strategy (Spence, Ashton et.al., 2007). At other times, when fish are not spawning, choice of substrate may be less important and fish may move to microhabitats that provide better opportunities to forage, shelter, or avoid predation.

Vegetation Salinity As with other water parameters, salinity levels (quantified as mass of salt per unit volume) vary among zebrafish habitats. Spence et al. (2006) measured salinity at nine sites in Bangladesh where zebrafish were present. Their highest recording was 0.6 g per liter in ponds of brackish water in the north of the country, while in the south, salinity levels in a ditch and in an isolated river channel were w0.01 g per liter. Although the zebrafish is generally considered a stenohaline species, tolerant of very low salinities (Craig, Wood & McClelland, 2007), these measurements uphold the suggestion that it may be adapted to osmoregulate under higher salinities (Best, Adatto, Cockington, James & Lawrence, 2010). Some laboratories keep larval zebrafish at salinities of 5 g per liter and culture them together with a food source of live saltwater rotifers (Lawrence et al., 2016).

Submerged, floating, and emergent plants, together with riparian vegetation, increase habitat complexity and play an important role in the ecology of freshwaters. Fish densities are higher in vegetated than in unvegetated areas due mainly to increased food availability and shelter from predation (Rozas & Odum, 1988). Submerged leaves, stems, and roots form large surface areas to which algae can attach and complex structures in which zooplankton and invertebrates can feed and hide (Thomaz & da Cunha, 2010). As a result, these organisms are more diverse and abundant in vegetated habitats (Ganesan & Khan, 2008; Gregg & Rose, 1985). In addition, terrestrial insects falling from riparian vegetation are an important food source for many species (Kawaguchi, Taniguchi & Nakano, 2003), including zebrafish (Arunachalam et al., 2013). In the wild, zebrafish are most often found in habitats associated with aquatic vegetation, such as floating fern (Salvinia natans), swampweed (Hygrophila sp.) and

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FIGURE 4.10 Vegetation typically found in zebrafish habitats (A) include Salvinia natans (B), Hygrophila sp. (C), and invasive plants such as Eichhornia crassipes (D). Photos by Gregory Paull.

duckweed (Lemna sp.), and invasive plants such as water hyacinth (Eichhornia crassipes) (Fig. 4.10). Aquatic vegetation may play a role in the survival of larval zebrafish. Laboratory studies show that newly hatched larvae move along the substrate until they encounter a hard surface, such as a rock or a plant stem or leaf, to which they adhere by means of small secretory cells on their heads (Laale, 1977). Over several hours, the larvae repeatedly release, propel themselves upwards, and reattach at a shallower depth, until they reach the water surface where they inflate their swim bladders to attain buoyancy and become free-swimming (Lindsey, Smith & Croll, 2010). By laying eggs in shallow waters close to vegetation to which larvae may attach, female zebrafish give their offspring the best chance of survival, and thereby increase their own fitness. Thereafter, plants provide shelter and a source of food for larvae and juveniles.

Human Impact Humans have manipulated zebrafish habitat for millennia. The spread of rice cultivation in the Indian subcontinent, since its origins in the Gangetic floodplains over 4000 years ago, is associated with the

development of urbanism, the expansion of laborintensive agriculture, and the creation of major irrigation works (Fuller & Qin, 2009). The subcontinent is now one of the most densely populated regions in the world. It comprises 4% of the world’s landmass and is home to 23% of the world’s population (United Nations, 2017). The increase in population and industrialization has created a demand for water that threatens to outstrip supply and has resulted in a substantial decline of wetland resources in the region (Vass et al., 2011). Major threats to river systems throughout the subcontinent include flow diversion and the alteration of habitats, degradation and siltation of waterways, deforestation of catchments areas, excessive abstraction of groundwater, discharge of untreated domestic and industrial wastes, overexploitation of water resources for hydroelectric purposes, indiscriminate fishing, and the introduction of invasive exotic species (Hoggarth et al., 1999; Prasad et al., 2002; Vass et al., 2011). In addition, the retreat of Himalayan glaciers and a decline in the region’s rainfall have resulted in a reduction in flow of the Ganges, further reducing the supply of water for drinking and irrigation (Vass et al., 2011). To fulfill the growing demand for water and mitigate supply problems, the Indian government has initiated a

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References

huge scheme to connect the major rivers of India and the Himalayas through a system of 30 interlinking canals and tunnels and 3000 dams and reservoirs, to redirect water from areas with “surplus” water to regions that experience a water shortfall (Lakra, Sarkar, Dubey, Sani & Pandey, 2011). The National River Linking Project will move water from Himalayan-fed rivers to droughtprone western states, with further links planned to bring river water to needy areas in the southern peninsula (Bagla, 2014). Such major alterations to water quantity and seasonal flows are likely to have negative consequences for freshwater fish biodiversity due to the loss of wetlands and floodplain habitats, destruction of migration routes, and changes to the physical features of feeding and spawning grounds (Sarkar et al., 2012). Climate change poses an additional threat to freshwater biodiversity. Although the causes of the observed changes in global climate are debated, there is growing consensus that anthropogenic emissions of greenhouse gasses are partially responsible (Stern & Kaufmann, 2014). In the Indian subcontinent, an increase in temperature, the occurrence and severity of storms and droughts, regional variation in monsoons, and the retreat of Himalayan glaciers have been observed (Vass et al., 2011), all of which may directly or indirectly affect the distribution of freshwater fish. When increased water temperature is combined with chemical pollution, the effects can profoundly impact fish populations. For example, the endocrine-disrupting chemical clotrimazole induces male-skewed sex ratios in zebrafish, and this effect is greater at elevated water temperatures (Brown et al., 2015). Such a change can reduce population viability and growth, especially in small populations, leading to an increased risk of extinction (Brown et al., 2015). Chemical pollution is a growing environmental problem in India. Around 70% of all available freshwater in India is polluted, due in part to the manufacture of pharmaceuticals outsourced to India by western countries (Mathew & Unnikrishnan, 2012). Production costs in India are around 50% lower than in industrialized countries, and India is now the world’s biggest exporter of generic prescription drugs, accounting for 40% of the world’s needs (Altstedter, 2017; Mathew & Unnikrishnan, 2012). In addition, wastewater effluents from municipal, industrial, and hospital sources and the disposal of solid wastes without proper treatment have degraded waterways throughout much of the Indian subcontinent (Mathew & Unnikrishnan, 2012; Srivastava, Ismail, Singh & Singh, 2015).

Conclusions The geographic range of the zebrafish includes much of the Indian subcontinent where it occupies a diverse

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range of habitats from hill streams to floodplains and from natural wetlands to man-made ditches. Zebrafish tolerate an equally diverse range of altitudes, temperatures, and water conditions and have been found over different substrates, with or without associated vegetation. Despite the importance of zebrafish to science, surprisingly little is known of the biology and behavior of wild populations. The zebrafish’s natural range boundaries and average home range size are still to be determined, as are its temporal distribution and microhabitat use. Also unknown are the distances traveled by zebrafish when migrating between habitats and the spatial behavior of the species at different life stages. Detailed knowledge of the natural habitat of zebrafish, including water conditions, habitat structure, temperature ranges, and seasonal changes, can be used to inform decisions about how fish can best be maintained and bred in the laboratory and how standards of welfare might be improved. In turn, providing optimum housing conditions for laboratory zebrafish will likely improve the reliability of research data. Wild zebrafish may prove invaluable for studies of adaptive evolution, wild traits, and associations between genotype and phenotype (Whiteley et al., 2011) and for interpreting responses of laboratory zebrafish to experimental manipulation (Suriyampola et al., 2015). However, the survival of natural populations is threatened by habitat degradation and destruction due to the drainage of wetlands for urban or industrial development, pollution of waterways, and an increasingly dry climate. The planned large-scale extraction of water from rivers and its subsequent transfer between regions will likely change the physical characteristics and ecosystems of habitats that zebrafish currently occupy. Geographic barriers prevent zebrafish from extending their range to evade environmental stressors, but within this restricted range, the zebrafish’s natural distribution will likely reduce or change.

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4. Geographic Range and Natural Distribution

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I. Introduction