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Water pH and hardness affect growth of freshwater teleosts
Bernardo Baldisserotto1
1Departamento de Fisiologia e Farmacologia, Universidade Federal de Santa Maria – 97105-900 – Santa Maria, RS, Brazil.
ABSTRACT - The freshwater contains a variable amount of dissolved salts, depending on the soil in which it occurs. Water acidification may occur in places where the soil has acidic cations and water can become alkaline due to phytoplankton and aquatic plants blooms or the presence of carbonate salts. Soft waters have a low content Ca2+ and Mg2+ and hard waters have large amounts of these ions. The aim of the present study is to provide a review regarding the effect of water pH and hardness on freshwater fish growth. Exposure of fish to very acidic or alkaline water is lethal, but survival is higher when fish are in hard water than in soft water. Growth of most species is affected at pH below 6.0 or above 9.0. Apparently, effect of water hardness on growth varies according to life stage, species and water quality. For species which are found in hard or moderately hard water in the natural environment, hard water is needed for good development, while in other it might ameliorates the deleterious effect of non-optimal conditions.
Key Words: acidic water, alkaline water, fish culture, hard water, soft water
Efeito do pH e da dureza da água no crescimento de peixes de água doce
RESUMO - A água doce contém uma quantidade variável de sais dissolvidos, que depende do solo onde ela ocorre. A acidificação da água pode ocorrer em locais onde o solo possui cátions ácidos e pode tornar-se alcalina em decorrência de aumento repentino do fitoplâncton ou plantas aquáticas ou da presença de sais de carbonato. Águas moles têm baixos níveis de Ca2+ e Mg2+ e águas duras, grande quantidade desses íons. O objetivo neste estudo foi fornecer uma revisão sobre o efeito do pH e da dureza da água no crescimento de peixes de água doce. A exposição de peixes a águas muito ácidas ou alcalinas é letal, mas a sobrevivência é maior quando os peixes estão em águas duras do que em águas moles. O crescimento da maioria das espécies é afetado quando são expostas a pH abaixo de 6,0 ou acima de 9,0. Aparentemente o efeito da dureza da água no crescimento varia de acordo com o estágio de vida, espécie e qualidade da água. Para espécies cujo habitat natural possui água dura, esse tipo de água é necessário para um bom desenvolvimento, mas para outras a água dura pode reduzir o impacto negativo de condições não-ótimas.
Palavras-chave: água ácida, água alcalina, água dura, água mole, piscicultura
Introduction
The freshwater contains a variable amount of dissolved substances (salts and organic compounds), depending on the soil in which it occurs. Water acidification may occur in places where the soil contains acidic cations, as Al3+, or iron pyrite, which under oxygenating conditions, forms sulfuric acid (Zweig et al., 1999). Very acidic lakes can be formed by streams with sulfuric and hydrochloric acid of volcanic origin, as Lake Usoriko (Japan) (Takatsu et al., 2000). The presence of humic and fulvic acids, formed in the soil through the decomposition of organic matter, can also reduce water pH down to 3.5, as observed in Amazonian blackwaters (Matsuo & Val, 2003). Phytoplankton or aquatic plants blooms decrease the CO2 available in the water
during daylight, increasing water pH (Wood, 2001). Natural alkaline lakes (pH 9.8-10.0) as Van (Turkey) (Danulat &
Selcuk, 1992) and Magadi (Kenia) (Wilson et al., 2004) present very high levels of carbonate and other ions. Soft waters have a low content of salts, mainly Ca2+ and Mg2+, but if the soil contains limestone, water can dissolve large amounts of Ca2+ and Mg2+ salts and is then termed hard water (Baldisserotto, 2003).
Most teleosts species survive to acute pH changes down to water pH 4.0 – 5.0 or up to 9.0-10.0, but exposure to more acidic or alkaline waters is lethal within a few hours (Zaions & Baldisserotto, 2000; Zaniboni-Filho et al., 2002).
However, species that inhabit acidic waters of the Amazon basin, as cardinal tetra, Paracheirodon axelrodi, can withstand water pH 3.5 indefinitely (Matsuo & Val, 2003).
Corresponding author: bbaldisserotto@hotmail.com
Survival is higher when fishes exposed to very acidic or alkaline waters are in hard water than in soft waters (Freda
& McDonald, 1988; Towsend & Baldisserotto, 2001). For example, the increase of water hardness from 20 up to 300 mg L-1 CaCO3 (using CaCl2) increased survival of silver catfish, Rhamdia quelen juveniles exposed water pH 3.75, 10.0 and 10.5, but did not affect significantly survival (which was 100%) at less extreme pH even at 600 mg L-1 CaCO3 (higher values were not tested) (Townsend &
Baldisserotto, 2001).
Physiological effects of exposure to acidic and alkaline waters
Exposure to very acidic pH increased ion loss (Figure 1) (Baldisserotto et al., 2008, 2009), which provoked a decrease in plasma ions and pH, and body ions (Zaions
& Baldisserotto, 2000; Bolner & Baldisserotto, 2007).
Very acidic water pH increases branchial Na+ efflux due to an opening of tight junctions of gill epithelia, increasing ion loss by a paracellular route (Gonzalez, 1996; Wood, 2001). There is also a decrease on Na+ influx when fishes are exposed to acidic waters, with a blockade of almost 100% at pH 4.0 in rainbow trout, Oncorhynchus mykiss.
The Na+ uptake blockade is caused by inhibition of the apical Na+/H+, NH4+ exchangers by external H+, or by creating a gradient too step for further extrusion of protons (Wood, 2001). Mortality of fishes exposed to acidic soft water seems related to a large decrease of plasma ions (Freda & McDonald, 1988). The rapid ions loss during acid exposure causes increase of hematocrit, hemoglobin and plasma protein and fluid volumes disturbances which kill the fish through circulatory failure (Wood, 1989).
The main problems in alkaline waters are the inhibition of ammonia excretion, which can increase plasma ammonia (Bolner & Baldisserotto, 2007), and increase of CO2 excretion (Wood, 2001). At neutral water pH ammonia leaves the gills by diffusion in the form of NH3, and is converted to NH4+ in the water, maintaining a favorable gradient for NH3 diffusion. When the water is alkaline, there is less H+ available to transform NH3 into NH4+, and the NH3 gradient blood – water decreases. The corresponding decrease in water CO2 creates a higher blood – water gradient, which promotes branchial CO2 losses (Wilkie & Wood, 1996). The resultant respiratory alkalosis increases plasma pH levels (Yesaki & Iwama, 1992; Bolner & Baldisserotto, 2007). In addition, high water pH also inhibits branchial Na+/NH4+, Cl-/HCO3- (Wilkie & Wood, 1996) and Na+/H+ exchangers (the last one due to an internal alkalosis, which decreased
availability of internal H for exchange against Na ) (Wood, 2001), which may led to lower plasma Na+ and Cl- (Yesaki & Iwama, 1992; Bolner & Baldisserotto, 2007).
Physiological effects of exposure to different water hardness
Calcium is important for ion regulation of freshwater fish because it influences the permeability of gill membranes, preventing diffusive ionic loss to water (Flik et al., 1995).
Freshwater fish take up Ca2+ predominantly through the gills, and even those fed a Ca2+ deficient diet grow normally if there is enough waterborne Ca2+ to be absorbed (Flik &
Verbost 1995). However, in low Ca2+ water the relative contribution of calcium ions from food increases as a compensatory mechanism (Steffens, 1997).
Rainbow trout exposed to low waterborne Ca2+
(2.5 mg L-¹ CaCO3) increased the number of chloride cells on lamellae and large apical surfaces to increase ion uptake, and maintain constant plasma Ca2+ irrespective of waterborne Ca2+ (Perry & Wood, 1985). The armored catfish, Hypostomus tietensis, traíra, Hoplias malabaricus, and jejú, Hoplerythrinus unitaeniatus, when transferred from 1.7 mg L-¹ CaCO3 to distilled or deionized water also showed high proliferation of gill chloride cells (Fernandes
& Perna-Martins, 2002; Moron et al., 2003). In addition, in armored catfish kept in distilled water the chloride cells were buried and recessed under adjacent pavement cells and the apical surface was arranged in a sponge-like structure, developing an apical crypt. These modifications may be an adaptation to prevent ion loss and increase ion uptake in very soft water (Fernandes & Perna-Martins, 2002). Lower plasma Na+, Cl- and osmolality and higher activity of branchial and renal Na+/K+ ATPase were observed in goldfish, Carasius auratus exposed to ion- poor water. In addition, in ion-poor water the expression of the tight junction occludin increased in the gills and kidney, which probably reduces the permeability of these epithelia (Chasiotis et al., 2009).
Most Mg2+ uptake is by food intake, but if the water presents an adequate amount of Mg2+, branchial uptake may be enough to compensate a low-Mg2+ diet in some species. High waterborne Mg2+ (up to 50 mmol) did not affect Gasterosteus aculeatus, Mozambique tilapia, Oreochromis mossambicus, and goldfish (Bijvelds et al., 1998).
The protective effect of water hardness against low pH is dependent of the affinity of branchial tight junctions for Ca2+. This ion is important at stabilizing these tight junctions and consequently decreasing gill ion loss by the paracellular route (Wood, 2001). Apparently, one of the mechanisms for
Figure 1 - Net Na+, Cl- and K+ fluxes (A, B and C, respectively) of Hoplosternum littorale and Arapaima gigas transferred from white water (pH 7.0) to black water (pH 5.5) and black water 3.5. Data expressed as mean ± SEM. Positive values indicate net influxes and negative values net effluxes. * significantly different from the same group 2h after transfer (P < 0.05) + significantly different from white water (P < 0.05). From Baldisserotto et al. (2008).
Time after change (h) Na+ flux (μmol.kg-1.h-1)
Time after change (h)
Cl- flux (μmol.kg-1.h-1)K+ flux (μmol.kg-1.h-1) Na+ flux (μmol.kg-1.h-1)Cl- flux (μmol.kg-1.h-1)K+ flux (μmol.kg-1.h-1)
White water
White water - black water White water - black water 3.5
survival of species that live in very soft waters, as those from the rio Negro, is the high branchial affinity for Ca2+, because even water hardness of 0.4 – 2.0 mg L-1 CaCO3 provides enough Ca2+ to saturate tight junctions binding sites (Gonzalez et al., 1998). Yellow perch, Perca flavescens, seems to have transporters with high affinity by Na+, because waterborne Ca2+ levels do not affect Na+ uptake in this species even at water pH 4.0 (Freda &
McDonald, 1988). However, for most studied species the increase of water hardness (waterborne Ca2+) decreases ion loss in acidic pH (Figure 2).
Effect of water pH on hatching and growth
Growth of most fish species is affected at pH below 6.0 or above 9.0 (Parra & Baldisserotto, 2007). Hatching does not occur in grumatã, Prochilodus lineatus (Reynalte- Tataje, 2000), when fertilization is done at pH 5.0, and exposure to pH 5.5-6.0 also reduced length and weight of silver catfish larvae compared to those maintained at pH 8.0-8.5 (Lopes et al., 2001). Exposure of silver catfish juveniles in soft water and pH 5.5 or 9.0 also reduced growth compared
to neutral pH (7.0-7.5) (Copatti et al., in press-a, b).
However, post larvae of grumatã showed better development and survival at pH 6 than at pH 7 and 8 (Reynalte-Tataje, 2000).
Additional studies regarding growth of fish which natural environment is acidic or alkaline are still lacking.
Probably their best pH range for growth is not circumneutral, because the freshwater angelfish, Pterophyllum scalare, from rio Negro, showed better growth in the 6.0-6.9 pH range (Chellappa et al., 2010).
Effect of water hardness on hatching and growth
At low water hardness the increase in egg diameter is greater because the swelling process of flaccid newly shed eggs when they first contact water and absorb water is higher (Gonzal et al., 1987; Spade & Bristow, 1999). Survival of eye-up eggs of rainbow trout, Atlantic salmon and brook trout is higher when eggs are hatched at 139-230 mg L-1 CaCO3 (Ketola et al., 1988), and the recommended range for hatching of silver carp, Hypophthalmicthys molitrix, is 300–500 mg L–1 CaCO3 (Gonzal et al., 1987). However,
Figure 2 - Whole body Na+ and Cl- net fluxes in tambaqui, Colossoma macropomum, exposed to water pH 3.5 and different waterborne Ca2+ levels. From Parra & Baldisserotto (2007), and elaborated with data from Gonzalez et al. (1998) and Wood et al. (1998).
higher larval survival and growth of African catfish, Clarias gariepinus, and silver catfish is in the 60-70 mg L-1 CaCO3 water hardness range (Molokwu & Okpokwasili, 2002; Silva et al., 2003, 2005; Townsend et al., 2003). Best growth of channel catfish, Ictalurus punctatus, larvae is with water hardness between 10-100 mg.L-1 CaCO3) (Tucker & Steeby, 1993). In silver catfish larvae the increase of water hardness from 20 to 70 mg L-1 CaCO3 using either Ca2+ or Mg2+
improved hatch rate, but increase of waterborne Ca+2 above 20 mg.L-1, irrespective of water hardness, is not recommend for incubation of silver catfish eggs because it reduced post-hatch (2 days after hatching) survival and larval weight and length after 21 days (Silva et al., 2003, 2005). Juvenile fathead minnows, Pimephales promelas, reared at around 50 mg L-1 CaCO3 had significantly lower survival but higher whole body mass when compared to their conspecifics raised at around 175 mg L-1 CaCO3 (Blanksma et al., 2009).
However, neither the hatching rate nor the growth of Mozambique tilapia larvae were affected by exposure to waters with 2-3 or 88-96 mg L–1 CaCO3 (using CaCl2 or CaSO4 to increase water hardness) (Hwang et al., 1996).
However, growth of male sex reversed juvenile Nile tilapia, Oreochromis niloticus, was higher at 146 mg L–1 CaCO3 (increased with CaCO3) than at 82 mg L–1 CaCO3 (Cavalcante et al., 2009).
Water hardness from 12.5 to 200 mg L-1 CaCO3 (increased with CaCl2) did not significantly affect final weight, food conversion, condition factor, and plasma Ca2+
levels of sunshine bass after 42 days (Seals et al., 1994).
However, water hardness 200 mg L-1 CaCO3 improved sunshine bass (Morone chrysops female x Morone saxatilis male) postharvest survival compared to lower water hardness (Grizzle et al., 1985). The increase of water hardness with MgSO4 up to 400 mg L-1 CaCO3 (with MgSO4) reduced survival of channel catfish juveniles to 0%, but when CaCO3 was used to increase water hardness survival was higher (95%) (Perschbacher & Wurts, 1999). Water hardness (30 to 180 mg L-1 CaCO3, increased with CaCl2) did not affect growth of silver catfish juveniles in neutral water within 30 days, but juveniles kept at pH 9.0 showed better growth performance in low water hardness (30 mg L-1 CaCO3), while a higher water hardness reduced the deleterious effects of acidity (pH 5.5) on growth in soft waters (Copatti et al., in press-a). The increase of water hardness from 12.5 to 100 mg L-1 CaCO3 did not improve growth of juvenile brook trout reared at pH 5.3, but in those kept at pH 6.5 and water hardness 100 mg L-1 CaCO3 presented higher growth rate than those reared at the same pH and water hardness 12.5 mg L-1 CaCO3 (Rodgers, 1984).
Conclusions
Fish raised in very acidic or alkaline pH presented lower growth, but in general studies exposing species to slightly acidic or alkaline waters are lacking. In addition, there are almost no studies dealing with fish that live in the acidic black waters of the Amazon or in alkaline lakes. Apparently, effect of water hardness on growth varies according to life stage, species and water quality. For some species (those which in the natural environment are found in hard or moderately hard water) hard water is needed for good development, while in other it might ameliorates the deleterious effect of non-optimal conditions.
Acknowledgements
B. Baldisserotto received a CNPq (Conselho Nacional de Desenvolvimento Tecnológico -Brazil) research grant.
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