colossoma macropomum

MARINE BIOLOGY

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MARINE BIOLOGY

PHYSIOLOGICAL AND BIOTECHNOLOGICAL APPROACHES OF THE AMAZONIAN TAMBAQUI FISH (COLOSSOMA MACROPOMUM) ELBA V. MATOSO MACIEL DE CARVALHO ROSIELY F. BEZERRA CAIO R. DIAS ASSIS RANILSON S. BEZERRA MARIA TEREZA S. CORREIA AND

LUANA CASSANDRA BREITENBACH BARROSO COELHO

New York

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LIBRARY OF CONGRESS CATALOGING-IN-PUBLICATION DATA ISBN: 978-1-63117-760-6

Published by Nova Science Publishers, Inc. † New York

CONTENTS vii

Preface Chapter 1

Tambaqui Overview

1

Chapter 2

Nutritional Aspects

5

Chapter 3

Hematological Aspects

9

Chapter 4

Hypoxia Tolerance

13

Chapter 5

Lectins

15

Chapter 6

Industrial Enzymes

19

Chapter 7

Enzymatic Biomarkers

21

Chapter 8

Genotoxicity Biomarkers

25

Chapter 9

Final Considerations

27

Acknowledgments

29

References

31

Index

45

PREFACE The tambaqui (Colossoma macropomum) is a fish from the basins of the Amazon and Orinoco Rivers. This species is considered the second largest freshwater scale fish in South America and is the third in the continental aquaculture ranking. The tambaqui have a good pattern of growth and productivity with high quality of meat for tropical aquaculture. It is a rustic species presenting adaptation to adverse environmental conditions. The considerable growth of tambaqui farming promotes studies focusing on nutrition and enzymatic profiles that conducted and have become important tools for productivity. However, little is known about tambaqui nutritional requirements. The fish feeding represents the major portion of production costs; then, one of the factors to have excellent farm productivity is feeding directed to each life stage, as well as feeding rates and water quality. Another factor to succeed in fish farming productivity is monitoring fish health in the management of farms through hematological studies. Thus, it becomes necessary to know different aspects of this species in order to contribute to efforts towards productivity, animal welfare as well as minimize the environmental impacts of farming through reduced waste. Moreover, despite the importance for tropical fish farming, there are few studies on biotechnological applications for C. macropomum. This species presents some biomolecules with features that could suits industrial and environmental demands and can represent a repository of many others. In this book the main approaches on nutrition, enzymatic profile and hematological parameters available in literature are gathered, as well as studies on tambaqui biomolecules of biotechnological interest.

Chapter 1

TAMBAQUI OVERVIEW Colossoma macropomum, popularly known as tambaqui, is a teleost fish belonging to the order Characiformes and the Serrasalmidae family; the genus exists since the Miocene epoch (Figure 1). It is one of the most important fish in Brazilian aquaculture and the second largest scale freshwater fish, only behind the pirarucu fish (Arapaima gigas). Tambaqui is original from South America, basins of the Amazon and Orinoco Rivers, with excellent potential to farming by being rustic, having good growth, high quality meat, gregarious habit, high tolerance to physicochemical changes of water and resistance to low oxygen concentrations (Aride et al., 2004; Val et al., 1998; Goulding and Carvalho, 1982). The successful evolutionary anatomical and physiological adaptations of C. macropomum allow them thriving in a wide range of habitats, reason why it is farmed in different countries (Nelson, 2006; FAO, 2012). This fish is known as black pacu in the United States, as gamitana in Bolivia and Ecuador and Cachama in Colombia and Venezuela. C. macropomum has very fleshy lips, as well as strong and sharp molar teeth allowing its diet to be omnivorous with preferences varying from zooplankton to seeds and fruits as the fish grow. The tambaqui is resistant to abrupt changes of pH and low dissolved oxygen in water; in this case, it shows increased lower lip allowing the animal to capture more oxygen while swimming near the surface (Wood et al., 1998; Val et al., 1998). C. macropomum, in its natural habitat, can reach one meter in length with a total of 30 kg. Adult tambaqui bred in captivity often may

2

E. V. M. M. de Carvalho, R. F. Bezerra, C. R. D. Assis et al.

reach up to about 70 cm of total length with 20 kg in average (Figure 2). Tambaqui, tãba´ki, from the Tupi language (spoken by the native Tupi people of Brazil) means oyster residue (tãba - shell, ki - heap), is a reophilic fish, therefore it does not spawn naturally in captivity and needs to swim against the current of rivers to mature their gonads and procreate. Then, it is a fish of piracema, another term from the Tupi language meaning "exit of fish ".

Figure 1. Taxonomic classification of tambaqui (C. macropomum, Cuvier, 1818).

Figure 2. Adult C. macropomum fish (0.68 m). Photo taken at Continental Aquaculture Station Johei Koike, UFRPE, Recife-State of Pernambuco, Brazil.

Tambaqui is found throughout the Amazon basin and among its tributaries there are rivers of black water, muddy water and clear water.

Tambaqui Overview

3

The black water rivers, such as the Negro River, are those from the sandy tertiary sediments of the Central Amazon. This type of river is characterized by clear brown water with visibility between 1.5 to 2.5 m and pH ranging from 3.5 to 4.0 due to the high amount of humic and fulvic matter they acquire by flooding vegetation. The most notable parameters in these rivers include low pH and low ion concentration (Matsuo and Val, 2002). The muddy water rivers (nutrient-rich waters), such as the Amazon and Juruá Rivers, are those whose headwaters are near the Andean sediments being characterized by high clay content in suspension, 0.1 to 0.5 m visibility and pH between 6.5 and 7.0. The rivers of clear water, such as Xingu and Tapajos, are those originated in the Brazilian Highlands or the Guyana plateau. These waters have very low amount of particulate matter, may present visibility greater than 4 m and can reach slightly alkaline pH (4.5 to 7.8). Daily and seasonal variations in water pH levels affect ion homeostasis in tambaqui, reducing its growth (Aride, 2007), increasing mucus secretion (Wood et al., 1998) and probably affecting the transfer of oxygen to the tissues. The floodplain forests, considered the richest in nutrients, are subject to flooding by the muddy water rivers; wetland forests are also inundated by rivers of clear or black waters. Tambaqui is found preferentially in muddy waters and the species occurrence in clear waters is very low. The tambaqui farming has high mortality during the winter months, particularly where the waters reach temperatures below 15 °C and decrease of growth under 23 °C (Zaniboni Filho and Meurer, 1997). The ideal temperature to the fish is between 25 °C and 30 °C. Thus, the tambaqui farming has been concentrated in the North, Northeast and Center-West Regions of Brazil. Disease prevention is paramount for aquaculture. As far as we know, there is no record of any endemic disease to wild or farmed tambaqui, what favors its reputation as a robust species. Tambaqui infections by microparasites, such as fungi, bacteria and protozoa were less studied. New species of parasites were found at gills, nostrils and intestines of tambaqui captured in the Amazon River and, among these parasites, the species Anacanthorus spathulatus, Notozothecium sp., Neoechinorhynchus butterae and Perulernaea gamitanae showed a good potential as bioindicators for tambaqui health (Malta et al., 2001; Fischer et al., 2003). Myxobolus colossomatis has also been found in the blood of tambaqui farmed in the Amazon Region (Maciel et al., 2011).

4


The great importance of this fish in the tropical aquaculture has put it in focus of researchers such as fishing engineers, biologists and physiologists. On the other hand, there are few data on biomolecules of C. macropomum. Some of these biomolecules present environmental responses whose physicochemical and toxicological properties are unusual and may also be of biotechnological interest. Diet is a factor that ensures excellent productivity in fish farming. The formulation of a diet directed according to the metabolic demand within each fish’s life stage is very important to obtain a good return on the growth, survival and feed conversion. Hematological studies are relevant to physiologically characterize a species in its natural environment as well as to assist the work of farm managements. The tambaqui, according to Kubitza (2012), is one of the most prominent species of Amazonian fish in Latin America. This book aims mainly to describe physiological aspects that support the technology of tambaqui production such as nutrition and hematologic features. Besides, it also gathers information on some C. macropomum biomolecules of biotechnological interest.

Chapter 2

NUTRITIONAL ASPECTS Nutrition and water quality are of great importance for successful fish farming. Therefore, it is paramount the study on feeding strategies, involving the activity of digestive enzymes and their distribution in the digestive tract to get optimum return on the growth, survival and feed conversion. Water quality must be monitored during farming; with farm intensification for higher productivity, higher feeding rates are demanded, worsening water quality, particularly related to dissolved oxygen (Kubitza, 2012). These studies will favor fish farming conditions aiming reducing the environmental impact and water quality, improving aquaculture production chain. According to Chagas and Val (2006), the addition of nutrients to diet follows the manual based on the nutritional requirements for fish from temperate regions - Nutrient Requirements of Fish (National Research Council, NRC, 1993) - and this is due to the lack of studies on tropical species. The practice of using functional food indicates a promising alternative for aquaculture; the food act keeping the organic balance of tropical fishes for every life stage in relation to adverse conditions inherent to intensive farming. It was reported that digestive enzymes have varying patterns among different fish species (Chackrabarti et al., 1995). C. macropomum is an omnivorous fish whose profile of digestive enzymes is similar to that of carnivorous species and the distribution of these enzymes does not seem restricted to specific parts of the tract, except for pepsin (EC 3.4.23.1) restricted to the stomach. Although having a close kinship with

6


Serrasalmus spp. (piranha fish), this distribution of digestive enzymes has also been considered an adaptation to the seasonal variability of the food composition in their natural habitats (Chakrabarti et al., 1995; Silva et al., 2000; Almeida et al., 2006). Therefore, digestive enzymes from C. macropomum are highly responsive to changes in diet. Almeida et al. (2006) observed that digestive protease has increased with dietary protein in stomach with positive correlations between foregut lipase (EC 3.1.1.3) versus dietary lipid and pyloric caecum amylase (EC 3.2.1.1) versus dietary protein. In this study, the metabolic preference for maintenance of energy production processes was lipolytic and such results pointed out that lipids are more efficiently used for storing energy than carbohydrates in this species. Corrêa et al. (2007) evaluated the effect of corn starch in the diet to digestion of polysaccharides and profile of digestive enzymes of tambaqui aiming to optimize the nutritional composition of this species feed. Fish was fed on a diet containing 30, 40 and 50% corn starch and the protein content was kept constant (28%). Amylase and maltase showed similar profiles with increasing levels of corn starch. These enzymes are present in the pyloric caecum and foregut; maltase is generally associated with amylase within the same intestinal section (Sabapathy and Teo, 1993). Alkaline proteases, trypsin and chymotrypsin were insensitive to changes in the corn starch concentration, but the acid protease responded to diet and this was probably due to the fact that the conversion of pepsinogen into pepsin is pH-dependent and H+ secretion is dependent on protein stimulation. Also, this study showed increased concentration of triglycerides in plasma at 40 to 50% of corn starch, with normal glucose and pyruvate; glucose and glycogen increased in the liver. According to the authors, there was lipogenesis with excess glucose from feeding at the level of 40%. Amino acids decreased in plasma and liver and increased in the white muscle thus suggesting that the amino acids have being absorbed by the muscle and spared of degradation by carbohydrates in the diet. Based on the results, the authors suggest feeding tambaqui with formulated diet containing 28% protein and 40% corn starch to prevent lipogenesis enabling protein storage. The nutritional requirements regarding proteins, lipids, vitamins and minerals vary according to the metabolic demand within each fish’s life stage. Proteins are important molecules that promote the normal function

Nutritional Aspects

7

of the body, beyond the supply of essential amino acids. When there is decreased protein concentration in fish diet, the pattern of amino acids must match the ideal pattern of amino acids for each fish’s growth stage (Nwanna et al., 2012). Reduced availability of a specific amino acid results in reduced protein synthesis. Therefore, the protein is essential in the diet for fish growth. The compensatory growth is a strategy that can be used to address the problem of high production cost of fish and may be employed to enhance its growth rate (Hornick et al., 2000) as well as lower costs of production. Ituassú and co-authors (2004) evaluated the effect of food deprivation for 0, 14, 21 and 28 days on the growth and body composition of tambaqui. In the experiment tambaqui showed greater deposition of body protein when fed ad libitum after being subjected to food deprivation. The compensatory growth of C. macropomum was complete after 14 days deprivation. The increased percentage of crude protein in fish that were submitted to food deprivation resulted in increased muscle deposition, which supports the assertion that the increase in mass in response to deprivation is not only caused by the body fat deposition (Dobson and Holmes, 1984). In other words, the protein is directly related to the fish development. Reinforcing the previous data, Santos and co-authors (2010) confirmed that the practice of food deprivation can be used in the farming of this species. They studied the development of tambaqui under different crude protein concentrations (28, 32, 36 and 40%) in the diet and two feeding regimes being a group with food deprivation of 14 days and another without food deprivation. The fish subjected to food deprivation had weight loss compared with those which were not subjected to food deprivation. The essential metabolism is maintained by endogenous reserves (protein, lipid and glycogen) thus justifying weight loss. The specific growth rate, the relative weight gain and feed efficiency of fish subjected to food deprivation were higher compared to the treatment without food deprivation. The best performance was found offering the diet containing 36% crude protein. It was concluded that the fish deprived of food can make better use of the protein in the diet thereby compensating for the lost weight during deprivation of 14 days. According to the authors, after the deprivation period fish revert the mobilization processes of the reserves used to meet vital needs and they

8


prioritize the use of food to overcome energy needs and replenish energy reserves used in catabolism in the feedback phase. Immunostimulants, such as vitamins, have also been used in the diets as strategies for maintaining the health of farmed fish (Maita, 2007). The purpose of administering these immunostimulants is to increase the specific and non-specific animal defense mechanisms (Aride et al., 2010; Sakai, 1999). The nutritional requirements of vitamins for fish are very specific and depend on environmental and physiological factors. Ascorbic acid is not synthesized in teleost fish, such as tambaqui (Fracalossi et al., 2001) due to the absence of the enzyme gulonolactona oxidase (Touhata et al., 1995). Therefore it is very important the supplementation of this vitamin in the diet of these fish since it promotes better growth, reproduction, stress response and disease resistance. Chagas and Val (2003) analyzed that dietary supplementation of ascorbic acid is essential for improving growth, feed conversion and survival; the optimal concentration for this practice is 100 mg/kg. Chagas and Val (2006) studied that diets enriched with ascorbic acid decreases the insults of hypoxia in juvenile C. macropomum. The forest of the Amazon flooded areas, floodplain and wetland, contribute with a large number of fruits and seeds that are used as natural sources of nutrients for fish (Lucas, 2008). Tambaqui can consume fruits and seeds of up to 133 plant species, especially during floods (Silva et al., 2003). This availability offers to tambaqui, in its natural habitat, a mixture of these items achieving better balance in protein, fats and vitamins (Araujo-Lima and Goulding, 1998). Silva and co-authors (2003) studied the effect of including two species of fruits (“embaúba” - Cecropia sp. – “jauari” - Astrocarium jauari) and two species of seeds (“seringa barriguda” - Hevea spruceana, “munguba” - Pseudobombax munguba) from the wetland forest and floodplain of the Amazon in the tambaqui diet aiming to low the production costs of this species in captivity. This study showed that the levels of protein, lipid and gross energy in the experimental diets increased significantly compared to commercial feed/control which uses corn. Thus, the fruits and seeds are important sources of nutrients and energy for C. macropomum and can be used as alternative in the diets by replacing the traditional items, thereby leading to decreased production costs in captivity.

Chapter 3

HEMATOLOGICAL ASPECTS Blood analyses have been used in fish to determine the effects of stress caused by capture, confinement and transport, as well as changes occurring in variations of temperature and dissolved oxygen, disease and other factors (Ranzani-Paiva et al., 2000; Martins et al., 2000; TavaresDias et al., 2001; Bezerra et al., 2013). Some studies relating to hematological parameters of C. macropomum have been performed especially in growing conditions in attempt to establish values that serve as standards for physiological or pathological investigation. Most hematological studies on tambaqui focus on the analysis of hematocrit (Htc) and hemoglobin (Hb). The choice for anticoagulants interferes significantly with the values of Hb and Htc; EDTA was already used as an anticoagulant of choice to tambaqui's blood samples (TavaresDias and Sandrim, 1998). However, a study (Pádua et al., 2012) analyzed heparin and K3EDTA as anticoagulants for tambaqui; heparin as an anticoagulant was more appropriate for tambaqui since it was effective in preventing coagulation for more than 10 h and did not cause hemolysis, changes on hematological parameters or osmotic fragility of erythrocytes. Fish are dependent on aerobic metabolism and Amazonian species are not different; GTP is stronger than ATP in decreasing the Hb-O2 affinity in C. macropomum. This is associated with faster changes of its intra erythrocyte level when animal is exposed to deep hypoxia, which results in an almost immediate adjustment of oxygen transfer to tissues according to environmental oxygen availability (Val, 2000). Tambaqui

10


has high tolerance to hypoxia and sulfide concentrations (LC50 = 34 µM H2S). Juvenile tambaqui exposed to sulfide and hypoxia for 12, 24, 48 and 96 h had increased values of Hb concentrations, red blood cell counts and mean corpuscular hemoglobin cell (MCHC) 12 h after hypoxia; at 96 h after hypoxia and exposure to high sulfide concentrations they showed anemia with low red blood cell count, Hb and Htc. Anaerobic metabolism might play an important adaptive mechanism against hypoxia and exposure to sulfides in tambaqui; also, this fish is able to develop aquatic surface respiration in situations of hypoxia preventing acidosis (Affonso et al., 2002). Mature erythrocytes of fish, unlike mammalian, are nucleated cells having ellipsoid shape and generally have a diameter much larger than the red cells of mammals; thrombocytes also present nucleus (Figure 3). These cells have an important role in the mechanisms of blood coagulation; in fish they also participate in defense mechanisms as defense cells (Gregory, 2001).

Figure 3. Blood withdrawal from tambaqui tail vein (A) and fish blood cells (B). (A) Photo taken at Continental Aquaculture Station Johei Koike. (B) Photomicrograph of erythrocytes measuring 7 - 10 µm, eosinophilic cytoplasm and ovoid nuclei oriented parallel to the long axis of the cell – E; thrombocyte showing hyaline cytoplasm without granulation and fusiform nucleus – T; stained with May Grünwald-Giemsa, bar = 10 µm (1,000 x magnification).

Nitrite (NO2-) is toxic to fish; bioaccumulation of this ion results in methemoglobinemia and hemolytic anemia in tambaqui exposed to nitrite concentrations of up 0.4 mM by 96 h. Also, it was found lack of

Hematological Aspects

11

development of aquatic shallow breathing indicating that the mechanisms involved in nitrite-induced hypoxia differ from those caused by environmental hypoxia (Costa et al., 2004). C. macropomum is known for its high tolerance to water with low pH values; blood shows large variation when exposed to alkaline pH with a significant decrease in the Htc (20%), Hb concentration (8%) and RBC (12%) (Aride et al., 2007). Acute stress, such as capture and management, can lead to decreased total number of erythrocytes, Hb concentration and Htc, with increased mean corpuscular volume, MCV (Tavares-Dias et al., 2001). As mentioned before, the tambaqui is not capable of biosynthesizing ascorbic acid and the absence of this vitamin in the diet causes reduced values of Htc as well as the number of red blood cells, causes increased MCV, mean corpuscular hemoglobin (MCH) and MCHC (Chagas and Val, 2003). Moreover, supplementation with vitamin C, in addition to increasing the Htc, the number of erythrocytes and Hb, also causes better feed conversion rate and better iron absorption (Chagas and Val, 2003; Aride et al., 2010). Regarding the study on white blood cells, four types of distinct leukocytes in the peripheral blood were characterized from C. macropomum kept under intensive monoculture: neutrophils, lymphocytes, special granulocytic cells (SGC) and monocytes; the differential count reveals a greater frequency of neutrophils followed by lymphocytes, monocytes and SGC (Tavares-Dias et al., 1999). Total leukocytes, the number of lymphocytes and neutrophils significantly increases after the stressful stimulus (Tavares-Dias et al., 2001). Also, Tavares-Dias and co-workers (2011) observed a decrease on total leukocytes, lymphocytes, neutrophils and PAS-positive granular leukocytes number when compared to control fish after exposure to 8.75 µg.mL-1 of CuSO4. Hematological parameters are useful tools as bioindicators of health state in fish. C. macropomum exposed at 1,1'-dimethyl-4, 4'-bipyridine dichloride (paraquat), a quaternary ammonium compound used as a herbicide and highly dangerous to humans, showed decreased Hb, MCH and MCHC. The erythrocyte morphology was changed to sickle erythrocytes and the neutrophils counts was also affected (Salazar-Lugo et al., 2009).

Chapter 4

HYPOXIA TOLERANCE C. macropomum is a rustic species presenting high tolerance to hypoxia since their habitat is subjected to seasonal floods and droughts. Under these conditions, this species develops, as well as several characiform species, an enlargement of the lower lip forming a dermal protuberance to act as a channel for the input of only the thin surface layer of oxygen-rich water in a way to improve aquatic surface respiration (ASR) performance (Saint-Paul, 1989; Winemiller, 1989; Scarabotti et al., 2011). In the past such morphological adaptation was believed to make gas exchange but the absence of a higher density or different arrangement of blood vessels in the lower lip corroborates the hypothesis that dermal protuberances perform no direct gas exchange function (Braum and Junk, 1982; Winemiller, 1989). The advanced stage of the protuberance developed in C. macropomum follows a mixture of Triportheus sp. and Astyanax sp. models in which the lip is broadened laterally displaying a not so prolonged dorso-ventrally flattened barbel on each distolateral tip (Figure 4). The main histological modification was an extensive edema in the hypodermal skin layer within the protuberances showing fibroblasts weakly distributed in the mucosa with spaces similar to alveoli while numerous capillaries and lymphocytes are present (Winemiller, 1989; Alves et al., 1999). Braum and Junk (1982) observed the doubling of the surface lip area of this species after 5 h of exposure to oxygen concentrations of 0.4-0.5 ppm in laboratory and a second two-fold increase in lip area after 24 h under the same conditions. Following normoxia, a reduction of 70% was observed in the lip area

14


after 90 min. Concomitantly with such alterations, an increase in hemoglobin levels and erythrocyte count in C. macropomum submitted to hypoxia conditions (lower than 2.0 mg.L-1) were observed due to seasonal changes in their habitat (Saint-Paul, 1984). Machado-Allison (1982) suggested that the ability of develop and absorb the protuberance is lost in adult size fish. However, fish culturists have also reported this feature in adult specimens (Winemiller, 1989).

Figure 4. Demonstration of C. macropomum lower lip increase in lateral (A) and frontal (B) view. When completely developed, the lip is broadened laterally displaying a prolonged dorso-ventrally flattened barbel on each distolateral tip. The main histological modification is, in fact, an extensive edema and no unusual arrangement or density of blood vessels in these protuberances is observed.

Chapter 5

LECTINS Lectins are proteins or glycoproteins of non-immune origin which recognize carbohydrates with high specificity through at least two binding sites, agglutinate cells, precipitate polysaccharides, glycoproteins or glycolipids (Sharon and Lis, 2004). The carbohydrate recognition by lectins is mediated by the carbohydrate recognition domain, CRD. These features allow lectins to participate in some biological processes such as induction of apoptosis (Perillo et al., 1995; Vervecken et al., 2000), cytotoxic activity (Kawsar et al., 2010; Silva et al., 2011), cell-cell interactions (Gabor et al., 2004), antiproliferative activity for cancer cells (Araújo et al., 2011; Bah et al., 2011), mitogenic activity (Maciel et al., 2004; Bah et al., 2011) and antitumor activity (Andrade et al., 2004). The presence of a lectin in a biological sample can be detected by an assay called hemagglutination activity (HA) (Figure 5A), followed by a HA inhibition assay with a solution containing specific carbohydrates or glycoproteins (Figure 5B). Purification is a key step in which are studied the structural and functional aspects of lectins in addition to biotechnological applications (Santos et al., 2013). Lectins have also been used for biotechnological purposes in studies on insect pests (Sá et al., 2009; Lam and Ng, 2011; Araújo et al., 2012), as antitumor drugs (Lam and Ng, 2011) and anti-inflammatory (Araújo et al., 2011), antibacterial, antifungal and termicide activities (Nunes et al., 2011; Souza et al., 2011; Maciel Carvalho et al., 2012; Napoleão et al., 2012), induction of parasites death (Fernandes et al., 2010), isolation of glycoproteins of medical or biotechnological interest (Silva et al., 2011;

16


Coelho et al., 2012), for diagnostics (Andrade et al., 2011, Oliveira et al., 2011), among others. Lectins have been investigated in marine bioresources by their various pharmacological functions in order to develop new potent drugs (Ogawa et al., 2011).

Figure 5. Scheme showing the detection of lectins in a biological sample with hemagglutinating activity (HA) and HA inhibition. (A) The lectin present in the sample induces hemagglutination due to specific binding of the carbohydrate recognition domain (CRD) to erythrocytes specific carbohydrate (ESC) on the surface. (B) Inhibition of HA occurs when sample is incubated with specific carbohydrate (SC) of lectin, before the addition of erythrocytes. No further mesh hemagglutination is performed with CRD.

The number of studies investigating the role of animal lectins using both immunological and molecular biology techniques has growing every year (Shiina et al., 2002; Vasta et al., 2007; Magnadottir et al., 2010; Bah et la., 2011; Kim et al., 2011; Silva et al., 2012). The humoral and membrane-associated lectins from the host are critical in the recognition of molecules that may facilitate the establishment of favorable mutualistic interactions with colonizing microbes, or initiate innate and adaptive responses against potentially pathogenic ones (Vasta et al., 2011). In addition, lectins mediate other functions, such as agglutination, fertilization, immobilization as well as complementmediated opsonization and deaths of pathogens (Ewart et al., 2001, Dong et al., 2004; Russel and Lumsden, 2005; Vasta et al., 2011; Cammarata et al., 2012). One of the events in the innate immune response includes the recognition of microbial target by lectins through CRDs. Lectins recognize foreign cells as "non-self" by the carbohydrates expressed on their surface acting thus as opsonins and stimulating their destruction by

Lectins

17

complement and/or phagocytic cells (Ewart et al. 2001; Fock et al. 2001; Dutta et al., 2005; Gowda et al., 2008; Battison and Summerfield, 2009; Imamichi and Yokoyama, 2010; Vasta et al., 2011). The discovery of these proteins in fish has added a new dimension in the immunology of these animals. Fish lectins may be isolated from serum, plasma, mucus, eggs and gills, such as: serum of Sparus aurata (Cammarata et al., 2007), Oreochromis niloticus (Silva et al., 2012), Clarias batrachus (Dutta et al., 2005) and Morone saxatilis (Odom and Vasta, 2006), plasma of Labeo rohita (Mitra and Das, 2002), skin of Conger myriaster (Nakamura et al., 2001), eggs of Oncorhynchus mykiss (Tateno et al., 2002) and Oncorhynchus keta (Shiina et al., 2002), mucus of Platycephalus indicus (Tsutsui et al., 2011) and gill of Aristichthys nobilis (Pan et al., 2010). The first report of a lectin present in the serum of tambaqui, C. macropomum (ComaSeL), was carried out by Maciel Carvalho and coauthors (2012). This lectin was detected, characterized and its functional property was evaluated against pathogenic bacteria in freshwater fish. ComaSeL recognized the carbohydrates D-galactose, 1-O-methyl-α-Dgalactopyranoside and D-fucose. This protein showed antibacterial activity (Figure 6) against Edwardsiella tarda, E. hydrophila and Aeromonas sobria and proved to be very resistant to changes in pH and temperature. The data confirm the tambaqui robustness by presenting this serum protein with antimicrobial characteristics and resistant to large variations in pH. It was also observed in healthy tambaqui that ComaSeL has seasonal variation, i.e. there is higher concentration during the summer while in winter its concentration in serum is very low. These data corroborate with the observation that tambaqui becomes more susceptible to mortality from diseases caused by bacteria and fungi during the winter. Currently, we are following with lines of research concerning to gene detection, isolation of bacteria from affected tambaqui followed by the challenge in healthy tambaqui in order to determine if ComaSeL concentration, which possesses antibacterial activity, increases with the infection. The approach may help to unravel the role of this lectin in tambaqui immune system contributing to an easier management and ultimately improving the profitability of fish farmers in the North and Northeast of Brazil as well as other South American countries.

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Figure 6. Antibacterial activity of C. macropomum Serum Lectin (ComaSeL) against Gram-negative bacteria. (A) Bacterial growth at zero time of experiment. (B) Presence of ComaSel in the culture medium inhibiting partially bacterial growth; ComaSeL binds to the carbohydrate present in the polysaccharide region triggering mechanisms which reduce bacterial growth. (C) D-fucose carbohydrate linked to ComaSeL blocks the binding of lectin to the carbohydrate surface allowing normal growth of bacteria.

Chapter 6

INDUSTRIAL ENZYMES Catalytic preparations from plants and animals have been used as tools to transform raw materials into end-products since the nature of enzymes and their properties were unknown. In the last decades, with advances in protein technology, food industries are improving the use of enzymes and several sectors of biotechnology are searching for better biocatalysts applying their results in other industries such as pharmaceutical, laundry detergents and leather products. These searches aim to select organisms with enzymes which present operational stability under conditions extremely different from those found in their natural habitat (Porta et al., 2010). The variability of enzymatic behavior in response to sporadic food changes can also be expected as consequences of environmental factors since tambaqui faces varying environments from shallow and warm waters in the dry season to river waters that invade the Amazon floodplain during rainy season with all the changes in temperature, pH, salinity and oxygen. Digestive enzymes with characteristics of biotechnological interest have been discovered from tambaqui. Bezerra and co-authors (2001) purified a 38.5 kDa thermostable trypsin (EC 3.4.21.4) from pyloric caecum of C. macropomum with optimal pH and temperature of 9.5 and 60ºC, respectively; activity did not alter after incubation at 55ºC for 30 min. Marcuschi and co-authors (2010) purified another trypsin with 23.9 kDa and optimum pH between 7.5 to 11.5 (using BapNa as substrate) and 9.0 (using fluorogenic z-FR-MCA substrate) while the optimal

20


temperatures were 70 and 50ºC, respectively for the same substrates. The latter enzyme performed 60% of its activity after incubation at 60ºC during 3 h. The authors have sequenced the N-terminus of the enzyme and determined the substrate specificity which can accelerate further research with this species. The location of optimal temperature in high values is confirmed by limited tolerance to low temperatures in this species (Zaniboni Filho and Meurer, 1997). The stability features of these enzymes could make C. macropomum proteases very attractive to food industry as additive to improve flavor, texture and nutritional value or as exogenous enzymes to increase digestibility of vegetal proteins in animal diet (Ogunkoya et al., 2006; Lin et al., 2007; Porta et al., 2010). The use of exogenous enzymes in fish diet presents additional gain related to the reduction of faecal material minimizing the environmental impacts on land-based and cage culture operations (Ogunkoya et al., 2006). Proteolytic enzymes from aquaculture and fisheries waste are also used in the composition of laundry detergents (Kumar et al., 1998; Gupta et al., 1999). Espósito and co-workers (2009) extracted alkaline proteases from the viscera of C. macropomum as alternative source for detergents and discovered a group of proteases with suitable characteristics for that purpose: thermostability and stability in presence of non-ionic (Tween 20 and Tween 80) and ionic surfactants (saponin and sodium choleate), besides high resistance to hydrogen peroxide (10% H2O2 for 75 min) and commercial detergents. Therefore, C. macropomum proteases have the potential to be used as additive in detergents since their activity is stable in the presence of several surfactants, commercial detergents and hydrogen peroxide, besides having high thermostability.

Chapter 7

ENZYMATIC BIOMARKERS According to estimates, only 0.1% of applied pesticides reach the target pests and the rest of the material containing the active ingredient spreads around, contaminating the air and soil (Hart and Pimentel, 2002). Agrochemicals can reach aquatic ecosystems and groundwater sheets carried by runoff and leaching of rainwater, irrigation and drainage, as well as through spraying (Figure 7). Once present in the aquatic environment, they can join the suspended material, the sediment in the bed of the water body or be absorbed by organisms in which undergo detoxification or bioaccumulation. Due to this environmental fate of agrochemicals and heavy metals from industrial or mining tailings, aquatic organisms have been used as biomonitoring species and despite arthropods and other invertebrates being more susceptible to those compounds, fish are often chosen due to their position in aquatic food chain, liable to higher degree of bioaccumulation (Sturm et al., 1999a and 1999b; Rodríguez-Fuentes and Gold-Bouchot, 2000; Tomita and Beyruth, 2002). Acetylcholinesterase (AChE; EC 3.1.1.7) is an enzyme present in several species including fish which is responsible for modulating nerve impulse transmission through hydrolysis of the ubiquitous neurotransmitter acetylcholine (Figure 8). The AChE extracted from C. macropomum brain seems to have suitable features as biomarker of organophosphate and carbamate pesticides being extracted from a normally discarded part of fish (Assis et al., 2007).

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Figure 7. Pesticides input processes in the aquatic environment. Compounds can reach water bodies in the following sequence: A) drift from spraying that falls on the soil and joins to clouds (gray arrows); B) run off of pesticides ( ) from rain and irrigation waters which can also leach into groundwater before reaching rivers, lakes and reservoirs (gray arrows).

Enzymatic Biomarkers

23

This enzyme from juvenile C. macropomum showed high sensitivity to a commercial formulation of dichlorvos (1.0%) presenting IC50 of 0.36 µM. The same authors (Assis et al., 2010) using organophosphate and carbamate pesticides in analytical grade (> 97% purity) confirmed the sensitivity of the enzyme to dichlorvos (IC50 = 0.04 µM) and found this feature for tetraethyl pyrophosphate (TEPP), chlorpyrifos and carbofuran (IC50 of 3.7, 7.6 and 0.92 µM, respectively). With respect to dichlorvos, this sensitivity was greater than the one found exposing the commercial and purified AChE from Electrophorus electricus, IC50 of 0.16 µM (Assis et al., 2011).

Figure 8. Scheme showing C. macropomum brain as source of acetylcholinesterase and enzyme functioning in the synaptic cleft. Choline acetyl ) transferase from nerve terminal (pre-synaptic neuron) release acetylcholine ( ) activating the sodium channel into the cleft where it can bind to receptors ( ) ( ); the excess of neurotransmitter is hydrolyzed by acetylcholinesterase ( anchored in the post-synaptic membrane which in turn releases choline ( ) and acetate ( ). The choline produced is reabsorbed by pre-synaptic neuron membrane through the choline transporter (

); after, the acetate brought by

coenzyme A ( ) is used in the re-synthesis of acetylcholine by the enzyme choline acetyl transferase stored in vesicle, closing the cycle.

24


Rico and co-workers (2010 and 2011) using C. macropomum fingerlings observed sensitivity to parathion-methyl (LC50-96h of 4.983 µg.L-1) and malathion (LC50-96h of 1.507 µg.L-1) comparable to ornamental fish species which are less rustic and can be more susceptible, but more expensive to be farmed. Thus, C. macropomum AChE could be proposed as a biocomponent of sensors based on enzyme activity inhibition, as described schematically on figure 9, by organophosphate and carbamate pesticides (Marco and Barceló, 1996; Ivanov et al., 2000; Amine et al., 2006). Hence, acetylcholinesterase from tambaqui fish showed high degree of susceptibility to organophosphate and carbamate pesticides without purification.

Figure 9. Representation of a biosensor using acetylcholinesterase immobilized on an electrode modified with nafion-thionine-gold nanoparticles layers. The electrode is covered by a first layer of electroactive polymer nafion ( ) and followed by a mediator thionine ( ) layer. Then, the gold nanoparticles ( ) are added to increase the surface for the acetylcholinesterase ( ) binding. Organophosphorus or carbamates pesticides ( ) present in the sample binds to the active site of the enzyme causing inhibition of its activity and difference in relation to control sample is detected by electrode which sends signal to the potentiostat for its decodification.

Chapter 8

GENOTOXICITY BIOMARKERS Genotoxic alterations on aquatic organisms caused by environmental pollution can be accessed by cytogenetic techniques such as frequency of micronuclei (MN) and other nuclear abnormalities (NA), which detects chromosomal damage, repairs and erroneous repairs in parental cells easily viewable in the daughter cells. Furthermore, it is also used the DNA comet assay (Groff et al., 2010), which in turn detects potentially pre-mutagenic lesions, such as DNA chain ruptures, alkali-labile sites, DNA adducts, base changes, crossed DNA-DNA and DNA-protein links and incomplete DNA repair. Fishes are recommended as models for genotoxicity studies for three reasons: 1) their component cells are very responsive to contaminants even in low concentrations; 2) their erythrocytes have nuclei which streamlines the collection of samples. It is not necessary to collect other tissues; 3) fishes are important sources of nutrients in human diet since food is the most important way of human contamination by water pollutants (Carrasco et al., 1990; Al-Sabti and Metcalfe, 1995; Fontanetti et al., 2010). C. macropomum was exposed to some compounds and physicochemical conditions described below; the responses were evaluated using the markers of MN, NA and DNA comet assay. This species can be considered an appropriate model for evaluation studies of the genotoxic effects of methylmercury and other xenobiotics on aquatic environments. In 2011, two studies evaluated the exposure of tambaqui to methylmercury (2 µg.mL-1) and they found no statistical differences in

26


MN frequencies of erythrocytes in the treated groups compared to the controls. However, erythrocytes NA frequencies were significantly different (ρ < 0.002) between controls and the group exposed to methylmercury for 120 h (Rocha et al., 2011a). The exposure to this heavy metal significantly increased the frequency of tailed nucleoids in the erythrocytes of groups exposed (ρ < 0.0005), indicating DNA damage in comet assay (Rocha et al., 2011b). C. macropomum MN and NA were also used in other studies. Increases in MN frequencies of C. macropomum were observed at concentrations from 10 µg.mL-1 atrazine herbicide (Chapadense et al., 2009). Groff and co-authors (2010) proposed C. macropomum and Arapaima gigas as biomonitoring species of genotoxic effects of UV radiation under normoxia and hypoxia conditions due to the high frequencies observed of MN and class 4 damage of DNA comet assay for both species.

Chapter 9

FINAL CONSIDERATIONS A major constraint in the development of technology in the systematic farming of native species of commercial importance such as C. macropomum in Brazil and elsewhere in South America is the lack of knowledge about its nutritional requirements. The diets available on the market are not balanced for most tropical native fish. Thus, inadequate ratio between the concentration of nutrients in the diets and their feed rates can lead to decreased growth rate and feed conversion, as well as increased costs and mortality. Moreover, the intensification of livestock in search for higher yields requires the use of higher feeding rates, impacting the environment through water quality due to eutrophication and decreasing dissolved oxygen. The tambaqui fish tolerates a wide range of habitats and has a very varied diet. C. macropomum, as an omnivorous fish, has the characteristic to take different sources of nutrients and due to its high adaptability capacity it can modify the enzymatic profile of the gastrointestinal tract according to the quality of ingested nutrients. Since the fish feeding represents approximately 70% of the production costs, it is important for the tambaqui farming the use of an ideal feeding for each life stage as well as feeding rates, ensuring optimum productivity in farms. The fact of tambaqui being tolerant to low dissolved oxygen concentrations in water does not determine that its performance will not be affected. The poor water quality results in stress harming growth favoring the occurrence of diseases (Kubitza, 2012). Moreover, there is

28


no point in making the ideal diet for tambaqui if the feeding management is not correct. The use of a directed diet without losses into the environment will ensure reduction in costs and decreased water pollution due to excessive protein degradation (Dairiki and Silva, 2011). Even tambaqui being resistant to extreme situation that leads to homeostatic imbalances, a pronounced hypoxia, poor water or absence of specific essential nutrient can lead the animal to a disease state and even result in death. The blood physiology works effectively as a biomarker of general health in teleosts and may serve as a diagnostic tool in hostile conditions in the culture systems, thus allowing the choice for the best management techniques and maintenance in fish farming. Lectins from the serum of C. macropomum are pH-stable, thermostable and presented in vitro antibacterial activity, in biochemical level. The lectin concentration in tambaqui fish serum is significantly lower in winter coupled with the fact that tambaqui is more susceptible to disease during this period. Then, it is important to work further in order to unravel the true role of these lectins in the immune system of this species to use them as potential targets for intervention for diseases control. C. macropomum pyloric caecum trypsins are pH-stable and thermostable having the potential to be used in industrial processes such as additive in laundry detergents, for example. The pH-stability and thermostability of lectins and trypsins are a sample of the rusticity of C. macropomum. However, it is a species very sensitive to chemical pollutants such as insecticides: its acetylcholinesterase from brain crude extract presented higher degree of susceptibility to one organophosphorus pesticide (dichlorvos) than the purified commercial AChE from E. electricus. Moreover, tambaqui genetic material was very responsive to other environmental contaminants and physical conditions such as heavy metals, herbicides and UV radiation. Therefore, besides having economic importance, the waste of C. macropomum (blood, brain and intestine) can be used for biotechnological purposes.

ACKNOWLEDGMENTS The authors express their gratitude to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE) for research grants, fellowships (RS Bezerra, MTS Correia, and LCBB Coelho) and postdoctoral fellowship (EVM Maciel Carvalho and CRD Assis). We also thank the Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE) for financial support.

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INDEX A acetylcholine, 21, 23 acetylcholinesterase, 23, 24, 28, 32, 40 acid, 6, 7, 8, 32, 34, 35, 42 acidosis, 10 active site, 24 acute stress, 43 adaptability, 27 adaptation(s), vii, 1, 6, 13, 33, 40, 43 adjustment, 9 adverse conditions, 5 agglutination, 16 alveoli, 13 amino, 6, 7 amino acid(s), 6, 7 amylase, 6 analgesic, 32 anemia, 10 animal welfare, vii anticoagulant, 9, 41 antigen, 36 antitumor, 15, 32 apoptosis, 15, 43 aquaculture, vii, 1, 3, 4, 5, 20 arthropods, 21 ascorbic acid, 8, 11 assessment, 32 ATP, 9

B bacteria, 3, 17, 18 base, 25 Belgium, 41 bioaccumulation, 10, 21 biocatalysts, 19 bioindicators, 3, 11 biological processes, 15 biomarkers, 32 biomolecules, vii, 4 biomonitoring, 21, 26 biosensors, 31, 36, 38 biosynthesis, 35 biotechnological applications, vii, 15 biotechnology, 19, 40 blood, 4, 9, 10, 11, 13, 14, 28, 36, 37, 42 blood vessels, 13, 14 body composition, 7 body fat, 7 Bolivia, 1 brain, 21, 23, 28, 32 Brazil, 2, 3, 17, 27, 39 breathing, 11

C caecum, 6, 19, 28 calcium, 38

Index

46 cancer, 15 cancer cells, 15 candidates, 40 carbohydrate(s), 6, 15, 16, 17, 18, 39 case study, 40 catabolism, 8 catfish, 34, 38 cDNA, 36 cell size, 36 chemical, 28, 33 choline, 23 cholinesterase, 36, 42 chymotrypsin, 6 classification, 2 cloning, 36 coenzyme, 23 Colombia, 1 commercial, 8, 20, 23, 27, 28, 39 complement, 16, 17 composition, 6, 20 compounds, 21, 25 confinement, 9 consumption, 37 contaminant, 33 contamination, 25, 42 Continental, 2, 10 conversion rate, 11 copper, 43 cortisol, 38 cost, 7 costs of production, 7 Croatia, 32, 34 culture, 18, 20, 28, 32, 37, 40, 44 culture medium, 18 cytoplasm, 10

D deaths, 16 defense mechanisms, 8, 10 degradation, 6, 28 dengue, 31, 39 deposition, 7 deprivation, 7, 36, 41

destruction, 16 detection, 16, 17 detergents, 19, 20, 28 detoxification, 21 diet, 1, 4, 5, 6, 7, 8, 11, 20, 25, 27, 28 dietary supplementation, 8 digestibility, 20 digestion, 6 digestive enzymes, 5, 6, 38, 40 diseases, 17, 27, 28 dissolved oxygen, 1, 9, 27 distribution, 5 diversity, 43 DNA, 25 DNA damage, 26 DNA repair, 25 drainage, 21 drug delivery, 35 drugs, 15

E Ecuador, 1 edema, 13, 14 egg, 34, 36 energy, 6, 8, 41 enlargement, 13 environment(s), 4, 19, 21, 22, 25, 27, 28, 43 environmental conditions, vii environmental factors, 19 environmental impact, vii, 5, 20 enzyme(s), 5, 6, 8, 19, 20, 21, 23, 24, 31, 37, 39 erythrocytes, 9, 10, 11, 16, 25, 26 evidence, 43 EVM, 29 exposure, 10, 11, 13, 25, 32, 34

F farmers, 17 farms, vii, 27

Index fauna, 35 fertilization, 16, 34 fibroblasts, 13 financial, 29 financial support, 29 fish, vii, 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 14, 17, 20, 21, 24, 27, 28, 31, 33, 34, 35, 36, 37, 38, 39, 40, 42, 43 fisheries, 20 fishing, 4 flavor, 20 flooding, 3 floods, 8, 13 fluid, 36 food, 5, 6, 7, 19, 20, 21, 25, 31, 34, 36 food chain, 21 food industry, 20 food safety, 31 fragility, 9 freshwater, vii, 1, 17, 34, 39, 40 fruits, 1, 8 functional food, 5 fungi, 3, 17 furunculosis, 37

47

H habitat(s), 1, 8, 13, 19, 27 health, vii, 3, 8, 11, 28, 35 heavy metals, 21, 28 hemagglutinins, 41 hematocrit, 9 hematology, 33 hemoglobin, 9, 10, 11, 14 hemolytic anemia, 10 herbicide, 11, 26, 34 heterogeneity, 40 Highlands, 3 history, 35 homeostasis, 3 host, 16 human, 25, 37 hyaline, 10 hybrid, 31 hydrogen, 20 hydrogen peroxide, 20 hydrolysis, 21 hypothesis, 13 hypoxia, 8, 9, 11, 13, 26, 28, 31, 34, 40, 41

G gastrointestinal tract, 27 genome, 36 genus, 1 gill, 17, 39 glucose, 6 glycogen, 6, 7 glycoproteins, 15 gold nanoparticles, 24 gonads, 2 grants, 29 granules, 34 groundwater, 21, 22 growth, vii, 1, 3, 4, 5, 7, 8, 18, 27, 34, 36, 37 growth rate, 7, 27 Guyana, 3

I ideal, 3, 7, 27, 28 imbalances, 28 immobilization, 16 immune response, 16, 41 immune system, 17, 28, 35 immunity, 43 in vitro, 28, 32, 36, 40, 41 induction, 15 industries, 19 infection, 17, 31, 37 inhibition, 15, 16, 24, 31, 40 innate immunity, 43 intensive farming, 5 intervention, 28 intestine, 28

Index

48 invertebrates, 21, 39 iron, 11, 32 irrigation, 21, 22 isolation, 15, 17

J juveniles, 37, 41

K K+, 38 kinship, 5

metabolism, 7, 9 metabolites, 31 meter, 1 methemoglobinemia, 10 mice, 42 micronucleus, 33 microorganisms, 36 Miocene, 1 models, 13, 25 molecular biology, 16 molecules, 6, 16, 41 morphology, 11 mortality, 3, 17, 27 MTS, 29 mucosa, 13 mucus, 3, 17

L lakes, 22, 41 larvae, 38 Latin America, 4 leaching, 21 lead, 11, 27, 28 lesions, 25 leukocytes, 11 lipids, 6 liposomes, 31 liver, 6 livestock, 27 low temperatures, 20 lower lip, 1, 13, 14 lymphocytes, 11, 13, 37

M macrophages, 33 mammals, 10 management, vii, 11, 17, 28, 35 mass, 7 matrix, 41 matter, 3 meat, vii, 1 medical, 15 Metabolic, 34

N Na+, 38 nafion, 24 nanoparticles, 24 National Research Council, 5, 38 native species, 27 natural food, 41 natural habitats, 6 nerve, 21, 23 neurotransmitter, 21, 23 neutrophils, 11 nitric oxide, 33 nitrite, 10, 34 NRC, 5, 38 nuclei, 10, 25 nucleus, 10 nutrient(s), 3, 5, 8, 25, 27, 28, 41 nutrition, vii, 4

O oocyte, 34 operations, 20 oxygen, 1, 3, 5, 9, 13, 19, 33 oyster, 2

Index

P parallel, 10 parasites, 3, 15, 35 pathogens, 16, 35 pepsin, 5, 6 peripheral blood, 11 peroxide, 20 pesticide, 28, 36 pests, 15, 21, 32 pH, 1, 3, 6, 11, 17, 19, 28, 32, 38, 44 phagocytic cells, 17 pharmaceutical, 19 physical characteristics, 39 Physiological, i, iii, 40, 43, 44 physiological factors, 8 physiology, 28 plants, 19 plasticity, 41 pollutants, 25, 28 pollution, 25, 28 polymer, 24 polysaccharide(s), 6, 15, 18 positive correlation, 6 prevention, 3 production costs, vii, 8, 27 profitability, 17 protection, 35 protein synthesis, 7 proteins, 6, 15, 17, 20 purification, 24, 33 purity, 23 pyrophosphate, 23

Q quaternary ammonium, 11

R raw materials, 19 receptors, 23 recognition, 15, 16, 35, 41, 42, 43

49

red blood cell count, 10 red blood cells, 11, 40 relevance, 35 repair, 36 reproduction, 8 reputation, 3 requirements, vii, 5, 6, 8, 27, 38 researchers, 4 reserves, 7 resistance, 1, 8, 20 resources, 39 respiration, 10, 13, 43 response, 7, 19, 32, 36, 37, 38, 43 roots, 42 runoff, 21

S salinity, 19 salmon, 33, 41 saponin, 20 seasonal changes, 14 secretion, 3, 6 sediment(s), 3, 21 seed, 35, 37, 41 segregation, 34 sensitivity, 23, 24, 39, 40 sensors, 24 serum, 17, 28, 33, 34, 35, 37 shape, 10 showing, 10, 13, 16, 23 skin, 13, 17, 38 snake venom, 39 sodium, 20, 23 solution, 15 South Africa, 43 South America, vii, 1, 17, 27, 43 Spain, 35 species, vii, 3, 4, 5, 6, 7, 8, 9, 13, 20, 21, 24, 25, 28, 34, 38, 39, 40 stability, 19, 20, 28 starch, 6 state, 11, 28 stimulation, 6

Index

50 stimulus, 11 stomach, 5 storage, 6, 42 stress, 8, 9, 11, 27, 33, 38 stress response, 8 structure, 33 substrate(s), 19, 20, 38 sulfate, 43 supplementation, 8, 11, 37 surface layer, 13 surfactants, 20 survival, 4, 5, 8, 38 susceptibility, 24, 28 synthesis, 23

T T cell(s), 39 target, 16, 21 techniques, 16, 25, 28 technology, 4, 19, 27 teeth, 1 temperature, 3, 9, 17, 19, 41, 44 texture, 20 thermostability, 20, 28 thrombocyte, 10 toxicity, 32 transmission, 21 transport, 9 treatment, 7 triglycerides, 6 trypsin, 6, 19, 33, 38 tumor, 33 tumor cells, 33

U UK, 37

United, 1 United States, 1 USA, 33, 38 UV, 26, 28 UV radiation, 26, 28

V variations, 3, 9, 17 vegetation, 3 vein, 10 Venezuela, 1, 37 vertebrates, 36 vesicle, 23 viral infection, 36 viscera, 20 vitamin C, 11, 32, 33 vitamins, 6, 8

W Washington, 38 waste, vii, 20, 28, 35 water, vii, 1, 3, 5, 11, 13, 21, 22, 25, 27, 28, 31, 32, 44 water quality, vii, 5, 27 weight gain, 7 weight loss, 7 white blood cells, 11 withdrawal, 10 workers, 11, 20, 24

Z zooplankton, 1