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Труды ИБВВ РАН, вып. 78(81), 2017
Transactions of IBIW, issue 78(81), 2017
УДК 597.08-151:574
DEFENSIVE REACTIONS AND SWIMMING ABILITY OF NILE TILAPIA OREOCHROMIS NILOTICUS (L.) (CICHLIDAE) FROM DIFFERENT HABITATS
I. A. Stolbunov1, Nguyen Thi Hai Thanh2
1Papanin Institute for Biology of Inland Waters Russian Academy of Sciences, 152742 Borok, Russia
e-mail: sia@ibiw.yaroslavl.ru 2Marine Division, Russian-Vietnam Tropical Research and Technological Center, Nha Trang, Vietnam
An experimental study of defensive reaction and swimming ability of Nile tilapia from Kamthyong reservoir and its tributary - Suoikok River (Vietnam) was performed. Significant differences in behavioral reactions of fish inhabiting limnic and lotic conditions were found. Nile tilapia from river habitats was characterized by higher swimming ability. Experiments have shown Nile tilapia individuals from the reservoir to possess a more effective defensive reaction compared with fish from the river. Defensive behavior patterns in fish seem to be inherent as fish from contrasting habitats (limnic and lotic conditions) demonstrated different defensive elements in the same model conditions of the experiment. In the presence of predator, Nile tilapia individuals from the reservoir mainly adhered to group defense tactics - collective maneuvering within a large school, while fish from the river usually resorted to individual defensive behavior elements.
Keywords: defensive behavior, swimming ability, habitats, Nile tilapia Oreochromis niloticus (L.)
INTRODUCTION
A certain set of adaptive behavioral traits, skills and stereotypes in formed in fish populations from different habitats in response to ecological factors: biotopic heterogeneity, food objects' diversity, predator press etc. as well as inherited differences [(Pavlov, 1979); (Pavlov et al., 2000); (Gerasimov et al., 2005); (Mikheev, 2006); Magurran, 1993; De Silva et al., 2006; Stolbunov et al., 2011]. The key factor leading to presence of multiple alternative behavior strategies within fish populations is environment heterogeneity [(Mikheev, 2006); (Gerasimov, 2010)]. Peculiarities of predator-prey interactions are among the main forms of fish adaptive behavior in different conditions [(Mikheev, 2006); Fuiman, Magurran, 1994; Reebs, 2001]. The exposure to abiotic and biotic environmental factors (hydrodynamic activity, environment heterogeneity, inter- and intraspecific interactions etc.) leads to formation of different defensive behavior strategies in fish [(Mikheev, 2006); Colgan, 1993; Gerasimov, Stolbunov, 2007].
Intraspecific ecological groups of individuals differing in the adaptive set of morphological and behavior features were found in temperate latitudes' dominant fish species (roach, bream, perch) possessing high plasticity and population polymorphism [(Dgebuadze, 2001); (Gerasimov et al., 2005); Stolbunov, Pavlov, 2006, Stolbunov, Gerasimov, 2008]. Differences in morphotype's adaptive complexes and behavioral reactions in different ecological groups of fishes allow a more effective exploitation of the environment and the most complete utilization of spatial and temporal subniches found within the species' natural range [(Gerasimov et al., 2005); Stolbunov, Gerasimov
2008]. Intraspecific diversity of temperate latitudes' fish is equally important for sustainable functioning of aquatic communities as the interspecific diversity [(Gerasimov et al., 2005); Stolbunov, Gerasimov, 2008].
Freshwater fish fauna in highly diversified in low latitudes [Winemiller et al., 2008; Kottelat,
2009]. Inland waters of South-East Asia are inhabited by nearly 2200 species of freshwater fish species and 680 species of brackish water species found in estuaries [Kottelat, 2009]. Continental and island waters of Vietnam are inhabited by 900 fish species of different ecological groups [(Ecology..., 2014); Froese, Pauly, 2012; Eschmeyer et al., 2017]. However, many waterbodies of Vietnam are presently dominated by invasive fish species with the aborigine (native) fish species number and abundance dwindling [Le Thanh Luu, Nguyen Van Thanh, 2005; Piligrim, Nguyen Duc Tu, 2007].
Nile tilapia (Oreochromis niloticus) is one of the most abundant invasive species of Vietnamese fresh waters. Initially being an object of aquaculture, this species is presently spread in the wild as well. Nile tilapia is found in fish fauna of rivers, lakes and reservoirs of Vietnam.
Considering its wide feeding spectrum [Stolbunov, Gusakov, 2015] and aggressive behavior [Lowe et al., 2004] we may suppose that this invader replaces native species potentially leading to decreased diversity and transformation of fish communities in Vietnam's inland waters. It should be noted that certain island countries of Pacific region (Nauru, Kiribati, Palau, Fiji etc.) perform large-scale fishery measures aiming at lowering the abundance or completely eradicating
Nile tilapia using various ichtyocides, rotenone predominantly [Nico, Walsh, 2011].
In this study, we aimed at performing an experimental survey of behavioral diversity of Nile tilapia Oreochromis niloticus (L.) from
MATERIALS
Fish were caught in the costal shallow of Kamthyong reservoir (N 12°10'52.1'', E 109°08'26.6'') with well-developed macrophyte beds and sandy-silty bottom as well as in its and its tributary - Suoikok River (N 12°10'16.9'', E 109°07'38.5''). River was 60 m wide, 1 m deep with sandy-rocky bottom; current velocity was 0.4 m/s, in the surface layer in the sampling site. Fish were caught using beach seine and Kinalev's net. Studies were performed in February-March of 2011.
Defensive reaction of tilapia from different habitats was studied experimentally. Fish from the river and the reservoir were placed into separate cylindrical tanks (2.8 m3 volume, 3.0 m2 bottom area) equipped with crushed corals' filters. Fish were kept at forced aeration and natural lighting throughout the whole experiment (20 days). Water temperature in the tanks was 27-28°C, oxygen content 5 mg/l. Tilapia were fed dry feed "Premix®" twice a day.
Defensive reaction of tilapia from different habitats was studied in identical model conditions. Groups of individuals (10 fish) from the tanks were put into an experimental aquarium (410 l volume, 0.73 m2 bottom area) equipped with filter, compressor and lighting. Neither bottom substrate nor vegetation was present. Water temperature was 30°C, oxygen content 4.8-5.0 mg/l. Gar Lepisosteus sp. (Lepisosteidae) 285 mm long weighing 380 g, which was not fed for a day prior to the experiment, was used as a model predator. Fish defensive reaction was judged by the time needed for the predator to eat 100% tilapia individuals from each experimental group. Testing was done in two replications for each fish sample from different habitats.
In addition, defensive behavior efficiency was evaluated in a mixed group. Here, ten individuals from each sample were taken. One
different habitats. This work included testing
defensive reaction and swimming ability of fish
from contrasting habitats (limnic and lotic biotopes).
AND METHODS
group was tagged by clipping the anal fin tip. Fish from different habitats were tagged alternately in replications in order to exclude the effect of fin clipping on fish survival. Mixed group of fish (20 ind.) were placed into aquarium with predator. After eating 50% of individuals, remaining individuals were removed and the share of survived fish from different biotopic groups was estimated. Testing was performed in two replications.
Fish swimming ability was performed in a one-meter long hydrodynamic tray, equipped with electric water pump. Water current velocity in the tray was 0.7 m/s. The tray was submersed into aquarium with water. Fish were tested in groups of five. The time from the moment of introducing the fish into the tray to the moment when the last individual drifted towards the rear protective grate was recorded.
Comparison of morphohydrodynamic parameters of fish individuals from different habitats was performed using corpus shape index (Y, relative units) and fish body streamlineness (H/L, %) [Aleev, 1963]. Magnitude of dorsal (sD) and anal (s^) fins were estimated as the product of relative values of base length and fin height. Length of pectoral fins (IP) and caudal peduncle (lpc) in relation to fish total length was calculated.
Defensive behavior of fish was monitored by means of video recording. Image from video camera was output to computer. Video was processed using "Fish Timer" software.
Fish schooling behavior in the presence of predator was viewed as a defensive behavior element and analyzed using video registration. The duration of swimming within a school of ten fish as well as the time spent swimming separately from the moment of entering the aquarium to the first dart of gar (beginning of active attack) were taken into consideration.
RESULTS
Experimental testing of Nile tilapia swimming ability has shown that fish from the river are able to sustain higher hydrodynamic stress comparing with fish from the reservoir. Found differences were significant. River individuals of Oreochromis niloticus resisted 0.7 m/s water current for 78 minutes on average, while fish from the reservoir - for 58 minutes (Table 1). Twenty minutes after the start of testing
in the hydrodynamic tray, average distance between river sample individuals was 60-70 mm (1.3-1.6 body length). Nile tilapia from the reservoir formed a more dense school, with average distance between individuals being 40-45 mm (0.9-1.0 body length).
Comparative analysis of morpho-hydrodynamic parameters of fish from the river and from the reservoir has yielded significant
differences (p<0.05) in a number of characteristics: body streamlineness, size of anal fin and caudal peduncle length (Table 2). Tilapia from the reservoir were deeper-bodied in comparison to river individuals. Values of caudal
peduncle length and anal fin size were higher in river tilapias (Table 2). No significant differences in other morphohydrodynamic parameters were found (Table 2).
Table 1. Comparative characteristics of the swimming ability of Nile tilapia (M ± c) from different habitats
Таблица 1. Сравнительная характеристика плавательной способности нильской тиляпии (М ± о) из разных местообитаний
Characteristics River Reservoir
Характеристики Река Водохранилище
(n=25) (n=25)
Standard length of the fish, mm 44.9±1.2 45.3±1.0
Стандартная длина рыб, мм
Drift time of 100% of individuals, min 78±10* 58±5
Время сноса 100% особей, мин
Note. Here and further: М - arithmetic mean, о - standard deviation, n - number of fish, ind., * - differences are significant according to Mann-Whitney ^/-criterion at p<0.05.
Примечание. Здесь и далее: М- среднее арифметическое, о - среднеквадратическое отклонение, n -число рыб, экз., * - различия достоверны по непараметрическому ^/-критерию Манна-Уитни при p<0.05.
Table 2. Morphohydrodynamic characteristics of Nile tilapia (M ± о)
Таблица 2. Морфогидродинамические характеристики нильской тиляпии (М ± о)
Characteristics Характеристики River Река (n=129) Reservoir Водохранилище (n=321)
Index of body forms (Y) Показатель формы корпуса (Y) 0.42±0.11 0.42±0.05
Index of streamlineness (H/L, %) Показатель обтекаемости тела (H/L, %) 33.2±3.7* 34.5±9.7
Relative value of dorsal fin (sD) Относительная величина спинного плавника (sD) 0.042±0.012 0.043±0.013
Relative value of anal fin (sA) Относительная величина анального плавника (sA) 0.026±0.008* 0.024±0.006
Relative length of pectoral fin (lP) Относительная длина грудного плавника (lP) 0.207±0.032 0.207±0.036
Relative length of caudal peduncle (lpc) Относительная длина хвостового стебля (lpc) 0.122±0.022* 0.117±0.017
Efficiency of fish defensive behavior. Fish from the reservoir were found to possess a more effective defensive reaction than fish from the river. Tilapia from the reservoir has evaded 100% elimination by the predator for longer period, 45 minutes on average (Table 3). These fish have mainly demonstrated schooling defensive behavior manifested in collective maneuvering during predator evasion.
Experimental group of tilapia from the river has shown a more territorial and agonistic behavior in comparison with reservoir fish. Experimental group of fish from the river has also
formed a school in the presence (and attack) of predator, however group maneuvering was less prolonged than in fish from the reservoir. Tilapia from the river stayed in school for 30% of the total time of the experiment, on average. On the contrary, fish from the reservoir spent 65% of time maneuvering within a school.
Testing tilapia's defensive behavior in a mixed group has revealed that after 50% elimination by the predator, reservoir individuals prevailed in the remaining group (Table 3). Found differences in tilapia's defensive reaction were significant (p<0.05).
Table 3. Experimental testing of defensive behavior of Oreochromis niloticus from different habitats (M±o)
Таблица 3. Экспериментальное тестирование оборонительного поведения Oreochromis niloticus из разных местообитаний (М±о)
Characteristics Характеристики River Река (n = 30 экз.) Reservoir Водохранилище (n = 30 экз.)
Time interval of 100% predation of fish, min. Время выедания хищником 100% особей, мин 85±40* 130±30
The share of specimens eaten in a mixed flock,% Доля особей, съеденных в смешанной стае, % 38.5±9.2* 61.5±9.2
Standard length of Nile tilapia, mm Длина тела тиляпии, мм 44.2±0.9 44.5±0.8
DISCUSSION
Cichlids are characterized by a high level of morphological and behavior variability of adaptive value [Winemiller et al., 1995; Barlow, 2000; Montana, Winemiller, 2010; Lopez-Fernandez et al., 2014 etc.]. The diversity and peculiarities of outer morphology forms of cichlids are mainly linked to trophic differentiation as well as foraging and defensive behavior [Reebs, 2001; Waltzek, Wainwright, 2003; Higham et al., 2007; Lopez-Fernandez et al., 2014].
Nile tilapia inhabiting Vietnamese waters is characterized by high trophic plasticity [Stolbunov, Gusakov, 2015]. Stomach contents' examination has revealed components of plant, animal and mineral (sand) origin [Stolbunov, Gusakov, 2015]. On average, plant and other (indeterminate) debris, consisting of detritus-like bits, blue - green algae and higher aquatic plants' fragments, constitute 87% of fish boluses' weight. Lower crustaceans (cladocerans, copepopods and ostracods) constitute the base of animal food, insects' larvae and pupae are present in smaller quantities. Overall contents and the character of distribution of food components inside fish intestines indicate that the majority of fish forage near the bottom, swallowing detritus with blue-green algae sinking after "blooms", sand, bottom and near-bottom organisms. The presence of relatively large (up to 5-10 mm) green macrophyte fragments in single individuals evidences for feeding in coastal macrophyte beds. However, macrophyte fragments in fish feeding are few. Most probably, fish feeding on macrophyte-associated fauna have accidentally taken them. Small (<1 mm) meiobenthos and zooplankton representatives constituted the most of fish boluses. However, particular tilapia individuals were selectively feeding on large animal organisms: chyronomid larvae and pupae,
ostracods, bugs. Intestines of such fish possessed uncharacteristically (comparing with others) high abundance of referred food organisms. Moreover, animal food remains were located in the total mass of plant and other feeding objects in tight clods and not oddly, evidencing for successive ingestion of organisms one after another. The share of animal food in these fish was 22-79% of the total bolus weight. The presence of fish demonstrating selective feeding on animals evidences for intraspecific trophic differentiation [Stolbunov, Gusakov, 2015]. A wide range of variability in mouth apparatus morphometry in Nile tilapia [Stolbunov, 2014] allows effective utilization of various food resources and lowers intra- and interspecific food competition, especially in the dry season when the range of fish feeding organisms narrows significantly.
Size-mass growth of Oreochromis niloticus in Vietnamese waters is of isometric character [Stolbunov, Gusakov, 2015]. Effective reproductive strategy of Nile tilapia (females nurture impregnated eggs in the mouth) and the intensive growth of fry facilitating rapid escape from mass predators' press allows maintaining high abundance of fish populations in native conditions.
It is known that Nile tilapia male growth rate is significantly higher than that of females [El-Sayed, 2006]. That is why, single fish farms undertake measures on direct sex inversion, adding sexual steroid hormones (androgens) to early fry feeding, forming same sex stocks, consisting of males [Beveridge, McAndrew, 2000].
Earlier we have performed field and experimental studies of morphological and behavioral variability of three cyprinid species (sidestripe rasbora Rasbora paviana Tirant, 1885 [syn. Rasbora paviei], puntius Puntius
brevis (Bleeker, 1849), bonylip barb Osteochilus vittatus (Valenciennes, 1842) [syn. Osteochilus hasselti] [Stolbunov, 2014)] native to waters of Vietnam and adjacent countries. It was shown that these cyprinids possess significant phenotypic, morphofunctional and behavioral differences in limnic and lotic conditions. Found differences indicate presence of a different set of adaptive behavioral and morphological features in fish from contrasting habitats [Stolbunov, 2014]. River individuals of studied cyprinids had a more slender body and larger area of dorsal fin indicating advantages in hydrodynamic parameters compared with fish from the reservoir. Fish from lotic habitats demonstrated higher swimming ability and maneuverability and therefore more effective defensive reaction. Reservoir fish had longer paired fins and deeper body, typical for fish inhabiting shallows with macrophyte beds [Webb, 1984; Webb, Weihs, 1986; Ehlinger, Wilson, 1988; Ehlinger, 1990; Schrank, Webb, 1996; Plaut, 2000]. A more effective defensive reaction and better swimming ability was observed in cyprinids inhabiting river conditions [Stolbunov, 2014].
Similar character of morphological adaptations is found in Oreochromis niloticus as well. In limnic conditions (Kamthyong reservoir) Nile tilapia individuals possessed deeper body, than fish from lotic habitats (Suoikok River). Rivers individuals of tilapia had a longer caudal peduncle than fish from the reservoir (see Table 2).
However, unlike the previously studied cyprinids [Stolbunov, 2014] defensive reaction of tilapia from the reservoir was more effective in comparison with river individuals. It is possible that differences in the effectiveness and tactics of defensive behavior found in river and reservoir tilapia groups in the experiment are caused by a different predator press in natural conditions. It is know that individuals from fish populations subject to constant high predator press were more effective in predator evasion in comparison with
individuals from waterbodies with low or absent press [Huntingford, Giles, 1987; Light, 1989].
An experiment had shown that Nile tilapia individuals demonstrate alternative behavior character depending on the aggregation density [Falter, Debacker, 1988]. Tilapia individuals were more aggressive and territorial in low-density groups. On the contrary, schooling behavior prevailed and individual aggression was lowered in tilapia from high-density groups [Falter, Debacker, 1988]. It should be noted that Nile tilapia is one of the abundance-wise dominating species in Kamthyong reservoir. During the period of observations, Nile tilapia fry density was up 20 ind./m2. This may account for a more pronounced schooling behavior of reservoir tilapia in defensive reaction experiment. It seems that tilapia living a highly heterogenetic river environment demonstrate more pronounced hierarchical, territorial and aggressive (agonistic) behavior. Our experimental data indirectly support this hypothesis: tilapia from Suoikok River have mostly demonstrated individual defensive tactics in the presence of predator. Schooling behavior was less pronounced in comparison with reservoir tilapia.
Therefore, our study revealed significant differences in behavior patterns of Oreochromis niloticus from limnic and lotic habitats. Nile tilapia from river habitats was characterized by better swimming ability in comparison with individuals from the reservoir. Defensive reaction tests have shown reservoir tilapia to possess more effective defensive reaction in comparison with river fish. It is possible that defensive behavior skills are inherited, because fish from contrasting habitats demonstrated different defensive elements in identical model conditions. In the presence of predator, Nile tilapia individuals from the reservoir have mainly adhered to group defense tactics - collective maneuvering within school while fish from the river have used elements of individual defensive behavior, predominantly.
The study was supported by the RAS Presidium Program: I.21.P Biodiversity of natural systems. Biological resources of Russia: state evaluation and fundamental bases of monitoring. 2.5. Effect of anthropogenic regulation of water reservoir level regime and temperature on the dynamics of fish. The study was carried out within the scope of scientific program on theme: "Ecolan E-3.2". "Taxonomic diversity, ecology and behavior offreshwater hydrobionts". Section 1: "Study of morphological diversity of Vietnamese freshwater fish. Species diversity and biology offish in waterbodies of different types ".
ACKNOWLEDGEMENTS We are deeply grateful to the administration and technical personnel of joint Russian-Vietnamese Tropical research and technological center for the given opportunity and assistance in carrying out the studies.
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ОБОРОНИТЕЛЬНАЯ РЕАКЦИЯ И ПЛАВАТЕЛЬНАЯ СПОСОБНОСТЬ НИЛЬСКОЙ ТИЛЯПИИ OREOCHROMIS NILOTICUS (L.) (CICHLIDAE) ИЗ РАЗНЫХ МЕСТООБИТАНИЙ
И. А. Столбунов1, Нгуен Тхи Хай Тхань2
'Институт биологии внутренних вод им. И.Д. Папанина РАН, 152742 пос. Борок, Ярославская обл., Некоузский р-н, e-mail: sia@ibiw.yaroslavl.ru 2Приморское отделение Российско-Вьетнамского тропического научно-исследовательского и технологического центра, Нячанг, Вьетнам
Проведено экспериментальное исследование оборонительного поведения и плавательной способности нильской тиляпии из водохранилища Камтхыонг и его притока - р. Суоикок (Вьетнам). Обнаружены достоверные различия в поведенческих особенностях рыб, обитающих в лимнических и лотических условиях. Нильская тиляпия из речных местообитаний характеризовалась лучшей плавательной способностью по сравнению с особями из водохранилища. В результате экспериментального тестирования оборонительного поведения обнаружено, что особи нильской тиляпии, отловленной в водохранилище, обладали более эффективной оборонительной реакцией по сравнению с речными особями рыб. Навыки оборонительного поведения у рыб, вероятно, закрепляются, так как в одинаковых модельных условиях эксперимента особи из контрастных местообитаний (лимнических и лотических условий) демонстрировали разные элементы защиты. В присутствии хищника особи нильской тиляпии из водохранилища в основном придерживались тактики групповой защиты, выражающейся в коллективном маневрировании рыб в составе общей стаи, в то время как особи из реки преимущественно использовали элементы индивидуального оборонительного поведения.
Ключевые слова: оборонительное поведение, плавательная способность, местообитания, нильская ти-ляпия Oreochromis niloticus (L.).
