Dissolved oxygen and fish behavior

Synopsis This essay reviews the behavioral responses of fish to reduced levels of dissolved oxygen from the perspective of optimization theory as used in contemporary behavioral ecology. A consideration of oxygen as a resource suggests that net oxygen gain per unit of energy expenditure will be the most useful currency for ecological models of breathing. In the process of oxygen uptake, fish always expend energy on perfusion, usually on ventilation and often on locomotion. These costs, and the risk of predation, will vary with oxygen availability and the type of behavioral response shown. The principal categories of behavioral response to reduced external availability of dissolved oxygen are (1) changes in activity, (2) increased use of air breathing, (3) increased use of aquatic surface respiration, and (4) vertical or horizontal habitat changes. Fish should choose whichever combination of responses minimizes the costs of meeting their oxygen demands. A small number of studies provides qualitative support for this prediction.     

The Effect of Gestational State on Oxygen Consumption and Response to Hypoxia in the Sailfin Molly, Poecilia latipinna

Metabolic activity in livebearing fishes increases with embryonic development so that embryos prior to parturition may have a higher mass-specific oxygen requirement than maternal tissues, temporarily increasing the total routine oxygen requirement of the female. We examined whether females of the livebearing poeciliid Poecilia latipinna (sailfin molly) increase their routine metabolic oxygen consumption during development of their broods. We also quantified effects of gestation on time allocation to aquatic surface respiration (ASR) under hypoxic conditions. Mass-adjusted routine metabolic rate (RMR) of female mollies showed a significant increase during late gestation. The RMR of males did not differ from females that were in their early or mid stage of gestation, but was lower than females in late gestation. Gestating females spent approximately 27% more time conducting ASR than non-gestating females when exposed to chronic hypoxia (1mgl^–1), further supporting a brood-related increase in oxygen demand. Increased time allocation to ASR may directly affect maternal predation risk in low-oxygen conditions.     

Species composition and pattern of fish distribution in Siberia

At the end of the first half of the 20th century, 61 species and subspecies of fish, including one invader (bleak Alburnus alburnus) and 17 species—endemics of Baikal—were reported for Siberia (Berg, 1933, 1949). At the present time, in rivers, lakes, and reservoirs of Siberia, 96 fish species and subspecies are described, of which 80 are aboriginal and 16 are invaders; 33 species are endemics of Baikal. Each landscapegeographic zone of Siberia has its specific ichthyofauna: in rivers and lakes of the south of Siberia, species of boreal piedmont complex dominate; in water bodies of the steppe, forest-steppe, taiga, and southern parts of the forest-steppe zone boreal plain dominates; in the zone of tundra, arctic freshwater dominates; and in Baikal, the most part (35) of species belongs to the Baikal autochtonous complex. Most researchers, as before, distinguish in Siberia two ichthyogeographic sites—West Siberian and East Siberian—that enter the Arctic Province of the Circumpolar subregion of the Holarctic region. Baikal is considered in the rank of the suboblast of the Holarctic.     

Dissolved oxygen and thermal regimes of a Ugandan crater lake

This paper quantifies the temporal pattern of thermal stratification and deoxygenation in Lake Nkuruba, a small (3 ha), deep (maximum depth = 38 m) crater lake in western Uganda. Dissolved oxygen penetrated to an average depth of 9 m and a maximum depth of 15 m below which the lake was permanently anoxic over the 2 years of study. Although surface oxygen levels were correlated with both surface water temperature and rainfall, seasonal cycles of dissolved oxygen were not well-defined and may have been obscured by the high frequency of short-term fluctuations and by inter-annual variations caused by shifts in rainfall. Surface water temperature averaged 23.3±0.7 °C (S.D.) and varied directly with air temperature. Both diurnal changes and top-bottom temperature differentials were small averaging 1.7±0.7 °C and 1.6±0.8 °C, respectively. Thermal stability ranged from 101.3 to 499.9 g-cm cm^-2 and was positively related to surface water temperature suggesting that this small protected lake responds rapidly to short-term meteorological changes. Because contribution to the annual heat exchange cycle was confined to upper waters, the lake's annual heat budget was low, 1,073.8 cal cm^-2 yr^-1. However, net primary productivity was relatively high averaging 1.3 g C m^-2d^-1. The region where Lake Nkuruba is situated experienced a very strong earthquake (6.2 on the Richter scale) on 4 February, 1994. Subsequently, water levels dropped markedly in the lake, falling 3.14 m over a 5-month period. This revised version was published online in September 2006 with corrections to the Cover Date.     

Plankton composition and water quality in a pond of spring origin in Turkey

Phyto/zooplankton composition, chlorophyll a, and some water quality parameters were investigated in a spring-originated pond in Central Anatolia between February 2001 and January 2002. Water temperature, pH, dissolved oxygen, Secchi depth, total and calcium hardness, nitrate-nitrogen, nitrite-nitrogen, ammonia-nitrogen, total phosphorus, and soluble reactive phosphorus levels were analyzed. A total of 49 species belonging to Bacillariophyceae, Chlorophyceae, Cyanophyceae, Cryptophyceae, and Dinophyceae were identified. The highest phytoplankton abundance was found in August, whereas the lowest was determined in January. Phytoplankton abundance increased from February to August and declined in the following months. The Bacillariophyceae were dominant in the phytoplankton community. A total of 21 species of Rotifera, 2 species of Cladocera, and 1 genus of Copepoda were found. The zooplankton community was dominated by Rotifera. The highest abundance of zooplankton was recorded in July and the lowest value in November. The annual mean concentration of chlorophyll a was measured as 1.90 μg l⁻¹. In spite of these eutrophic levels (mean values of total phosphorus and nitrate-nitrogen: 0.069 mg P l⁻¹ and 0.68 mg N l⁻¹), phytoplankton cannot grow satisfactorily because of the short water retention time (0.6 day⁻¹). The shallowness of the pond together with the low phytoplankton biomass and the high concentrations of nutrients are discussed.     

Interaction between female mating preferences and predation may explain the maintenance of rare males in the pentamorphic fish Poecilia parae

Variation in mating preferences coupled with selective predation may allow for the maintenance of alternative mating strategies. Males of the South American live‐bearing fish Poecilia parae fall in one of five discrete morphs: red, yellow, blue, stripe‐coloured tail (parae) and female mimic (immaculata). Field surveys indicate that the red and yellow morphs are the rarest and that their rarity is consistent across years. We explored the role of variable female mating preference and selective predation by visual predators in explaining the rarity of red and yellow males, and more generally, the maintenance of this extreme colour polymorphism. We presented wild‐caught P. parae females and Aequidens tetramerus, the most common cichlid predator, with the five male colour morphs in separate trials to determine mating and prey preferences, respectively. We found that a large proportion of females shared a strong preference for the rare carotenoid‐based red and yellow males, but a distinct group also preferred the blue and parae morphs. The cichlid predator strongly preferred red and yellow males as prey. Together, these results suggest that the interaction between premating sexual selection favouring and predation acting against the red and yellow morphs may explain their rarity in the wild. The trade‐off between sexual and natural selection, accompanied by variation in female mating preferences, may therefore facilitate the maintenance of the striking colour polymorphism in P. parae.     

Long-term cleaner fish presence affects growth of a coral reef fish

Cleaning behaviour is considered to be a classical example of mutualism. However, no studies, to our knowledge, have measured the benefits to clients in terms of growth. In the longest experimental study of its kind, over an 8 year period, cleaner fish Labroides dimidiatus were consistently removed from seven patch reefs (61-285 m(2)) and left undisturbed on nine control reefs, and the growth and parasite load of the damselfish Pomacentrus moluccensis determined. After 8 years, growth was reduced and parasitic copepod abundance was higher on fish from removal reefs compared with controls, but only in larger individuals. Behavioural observations revealed that P. moluccensis cleaned by L. dimidiatus were 27 per cent larger than nearby conspecifics. The selective cleaning by L. dimidiatus probably explains why only larger P. moluccensis individuals benefited from cleaning. This is the first demonstration, to our knowledge, that cleaners affect the growth rate of client individuals; a greater size for a given age should result in increased fecundity at a given time. The effect of the removal of so few small fish on the size of another fish species is unprecedented on coral reefs.     

Disappearance of a spring cohort in a population of the dragonet,Repomucenus valenciennei, with spring and autumn spawning peaks in Tokyo Bay, Japan

The occurrence of eggs, pelagic larvae and juveniles, and settled juveniles of the dragonetRepomucenus valenciennei in Tokyo Bay, Japan, were investigated by plankton net and bottom trawl surveys between September 1990 and September 1991. Eggs, and pelagic larvae and juveniles appeared from April to November (spring to autumn), peaking in both spring and autumn. From the temporal pattern of egg and pelagic fish occurrence, and pelagic duration reported elsewhere (ca. one month), settlement could be predicted as occurring from late spring to autumn. However, settled juveniles appeared from August to December, with an abrupt peak in November. Aging from daily increments in the otoliths of settled recruits in 1990 indicated that the latter comprised individuals which had hatched between mid-September and early November (i.e. autumn cohort), implying that individuals which had hatched in spring to summer (April to August) were not recruited. Benthic hypoxia occurs widely in Tokyo Bay, from June to October each year, particularly in the northern part, which is the main nursery area ofR. valenciennei. The timing of dissolved oxygen recovery, and appearance of settled fish coincided closely (i.e. November), indicating that summer hypoxic conditions prevented the settlement of the spring cohort and hence recruitment to the population.     

Ontogenetic niche shifts and resource partitioning in a subarctic piscivore fish guild

The feeding ecology of three piscivorous fish species (perch (Perca fluviatilis), pike (Esox lucius) and burbot (Lota lota)), was studied in the subarctic Pasvik watercourse (69 °N), northern Norway and Russia. All three species primarily occupied the benthic habitats in the watercourse. Perch and burbot exhibited distinct ontogenetic niche shifts in food resource use, perch changing from a dominance of zooplankton to zoobenthos to fish, and burbot from zoobenthos to fish. Fish prey dominated the diet of all the investigated size-classes of pike, but small-sized pike (<20 cm) were not represented in the sample. Fish prey size was positively related to predator size in all three species. Whitefish (Coregonus lavaretus) was the dominant prey of pike and large-sized burbot and perch. Nine-spined sticklebacks (Pungitius pungitius) was also an important prey and appeared to be a dietary stepping-stone enhancing the transition from invertebrate feeding to consumption of large-sized whitefish prey for all three predators. A cluster analysis separated the different size groups of the three predator species into five functional feeding groups, most of them containing two or all three species. Within these feeding groups, and especially among the piscivorous size-classes, there was a strong and significant interspecific overlap in prey selection, and the dietary similarities between the species were in general much larger than the intraspecific similarities between ontogenetic stages. All three piscivorous species are important top predators in the aquatic food web of the watercourse, and their ontogenetic diet shifts and resource partitioning patterns generate a substantial food web complexity in this subarctic ecosystem.     

Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis

Symbiotic bacteria often help their hosts acquire nutrients from their diet, showing trends of co-evolution and independent acquisition by hosts from the same trophic levels. While these trends hint at important roles for biotic factors, the effects of the abiotic environment on symbiotic community composition remain comparably understudied. In this investigation, we examined the influence of abiotic and biotic factors on the gut bacterial communities of fish from different taxa, trophic levels and habitats. Phylogenetic and statistical analyses of 25 16S rRNA libraries revealed that salinity, trophic level and possibly host phylogeny shape the composition of fish gut bacteria. When analysed alongside bacterial communities from other environments, fish gut communities typically clustered with gut communities from mammals and insects. Similar consideration of individual phylotypes (vs. communities) revealed evolutionary ties between fish gut microbes and symbionts of animals, as many of the bacteria from the guts of herbivorous fish were closely related to those from mammals. Our results indicate that fish harbour more specialized gut communities than previously recognized. They also highlight a trend of convergent acquisition of similar bacterial communities by fish and mammals, raising the possibility that fish were the first to evolve symbioses resembling those found among extant gut fermenting mammals.     

Effects of thermal stress on respiratory responses to hypoxia of a South American Prochilodontid fish, Prochilodus scrofa

Oxygen consumption (o₂) and respiratory variables were measured in the Prochilodontid fish, Prochilodus scrofa exposed to graded hypoxia after changes in temperature. The measurements were performed on fish acclimated to 25°C and in four further groups also acclimated to 25°C and then changed to 15, 20, 30 and 35°C. An increase in o₂ occurred with rising temperature, but at each temperature o₂ was kept constant over a wide range of O₂ tensions of inspired water ( Pi o₂). The critical oxygen tensions ( Pc o₂) were Pi o₂= 22 mmHg for 25°C acclimated specimens and after transfer from 25°C to 15, 20, 30 and 35°C the Pc o₂ changed to Pi o₂= 28, 22, 24 and 45 mmHg, respectively. Gill ventilation ( _G ) increased or decreased following the changes in o₂ as the temperature changed and was the result of an accentuated increase in breath frequency. During hypoxia the increases in _G were characterized by larger increases in breath volume. Oxygen extraction was kept almost constant at about 63% regardless of temperature and ambient oxygen tensions in normoxia and moderate hypoxia ( P o₂∼70 mmHg). P. scrofa showed high tolerance to hypoxia after abrupt changes in temperature although its survival upon transfer to 35°C could become limited by the capacity of ventilatory mechanisms to alleviate hypoxic stress.     

Air Breathing and Gill Ventilation Frequencies in Juvenile Tarpon, Megalops atlanticus: Responses to Changes in Dissolved Oxygen, Temperature, Hydrogen Sulfide, and PH

This study quantified the air-breathing frequency (ABf in breaths h^–1) and gill ventilation frequency (Vf in ventilations min^–1) of tarpon Megalops atlanticusas a function of PO₂, temperature, pH, and sulphide concentration. Ten tarpon held at normoxia at 22–33°C without access to atmospheric oxygen survived for eight days, and seven survived for 14 days (at which point the experiment was terminated) suggesting that the species is a facultative, rather than an obligate, air breather. At temperatures of 29°C and below ABf was highest and Vf was lowest at low oxygen partial pressures. Tarpon appear to switch from aquatic respiration to air breathing at PO₂levels of roughly 40 torr. The gills were the primary organ for oxygen uptake in normoxia, and the air-breathing organ the primary mechanism for oxygen uptake in hypoxia. At 33°C, both ABf and Vf were elevated but highly variable, regardless of PO₂. There were no mortalities in tarpon exposed to total H₂S concentrations of 0–232µM (0–150.9µM H₂S); however, high sulfide concentrations resulted in very high ABf and Vf near zero. Vf was reduced when pH was acidic. We conclude that air breathing provides an effective means of coping with the environmental conditions that characterize the eutrophic ponds and sloughs that juvenile tarpon typically inhabit.     

Adaptations of fish species to oxygen depletion in a central Amazonian floodplain lake

Pronounced seasonal and daily oxygen concentration changes are characteristic for Amazonian floodplain lakes. Studies on the fish fauna of the Lago Camaleão, Solimões River, Amazonas, Brazil, showed several fish species which are able to survive prolonged periods of heavy hypoxia. Twenty species belonging to eight families were observed in the laboratory in order to determine their respiratory adaptations to hypoxic conditions and oxygen concentrations at which the fish present respiratory adaptations. Finally, the fish species were distributed throughout the habitats of Lake Camaleão according to their adaptation responses. Ten fish species used the surface water for aquatic surface respiration, four species used atmospheric oxygen for aerial respiration, four species used oxygen supplied by the exudation of the roots of floating macrophytes and two exhibited a high tolerance to hypoxic conditions, and well-developed physiological biochemical mechanisms. The fish fauna is well adapted to low oxygen concentrations. The large variety of morpho-anatomical adaptations associated with biochemical and physiological mechanisms to tolerate hypoxic and anoxic conditions enable the 20 fish species to exploit several habitats of Lago Camaleão, such as floating aquatic macrophyte meadows, open water and near the shoreline.     

Costs and benefits of polyandry in a placental poeciliid fish Heterandria formosa are in accordance with the parent-offspring conflict theory of placentation

In viviparous species, a conflict over maternal resource allocation may arise between mothers and embryos, between siblings, and between maternal and paternal genes within an embryo due to relatedness asymmetries. We performed two experiments to study the effects of polyandry and brood relatedness on offspring growth in a placental fish (Heterandria formosa). Polyandry was beneficial as it increased the probability of pregnancy, possibly to avoid genetic incompatibility. However, females mated to four males produced offspring that had a longer maturation time than those of monandrous females. When within-brood relatedness was manipulated, the size of the newborn offspring decreased with time in low-relatedness treatment, whereas in highly related broods, offspring size was constant. Low within-brood relatedness may lead to less cooperative offspring in terms of resource extraction from the mother, which may lead to impaired development during gestation. Offspring conflict may thus reduce the benefits of polyandry in viviparous species.     

Factors influencing fish distribution in two desert reservoirs,Central Arizona

Fishes introduced into western reservoirs are intrinsically shallow-water, littoral inhabitants and remain so because of inherent limnological factors characteristic of mid-latitude lentic systems. Depth of euphotic zone and thermocline and dissolved oxygen concentrations limited the majority (90%) of fish in two desert reservoirs to the upper 10 m of water.     

Niche diversification follows key innovation in Antarctic fish radiation

Antarctic notothenioid fishes provide a fascinating evolutionary laboratory for the study of adaptive radiation, as their diversification is linked to both isolation in an extreme environment and a key innovation that allows them to exploit it. In this issue of Molecular Ecology, Rutschmann et al. (2011) evaluate how dietary niche differences have evolved in notothenioids: rarely, or repeatedly in multiple lineages. The authors use stable isotopes to measure species’ use of benthic vs. pelagic resources and map resource use onto a molecular phylogeny. Their findings indicate that pelagic diets have evolved in multiple lineages in at least two families, indicating that dietary niche diversification has occurred repeatedly and in parallel.     

Reduced opsin gene expression in a cave-dwelling fish

Regressive evolution of structures associated with vision in cave-dwelling organisms is the focus of intense research. Most work has focused on differences between extreme visual phenotypes: sighted, surface animals and their completely blind, cave-dwelling counterparts. We suggest that troglodytic systems, comprising multiple populations that vary along a gradient of visual function, may prove critical in understanding the mechanisms underlying initial regression in visual pathways. Gene expression assays of natural and laboratory-reared populations of the Atlantic molly (Poecilia mexicana) revealed reduced opsin expression in cave-dwelling populations compared with surface-dwelling conspecifics. Our results suggest that the reduction in opsin expression in cave-dwelling populations is not phenotypically plastic but reflects a hardwired system not rescued by exposure to light during retinal ontogeny. Changes in opsin gene expression may consequently represent a first evolutionary step in the regression of eyes in cave organisms.     

Biodiversity and distribution of water mites (Acari, Hydrachnidia) in spring habitats

1. The distribution, species richness and ecology of spring‐dwelling water mites in Italy were investigated with the aim to better elucidate the role of spring habitats to sustain high levels of biodiversity and their contribution to freshwater biodiversity at a local and regional scale. 2. More than 300 springs in different geographic areas (Alps, Central and Southern Apennines, Sicily and Sardinia), were examined with a total of 163 water mite species recorded. 3. Species richness in each area ranged from 33 species on Sardinia to 77 on Sicily. The highest diversity was found in the Gran Sasso (Central Apennines). The proportion of crenobionts (species strictly bound to this type of habitat) exceeded 50% in almost all the areas investigated. 4. A diverse (up to 20 species per spring) and highly specialised mite fauna was observed in undisturbed rheocrenes and in natural springs of intermediate typology (rheohelocrenes and rheopsammocrenes). In springs subjected to human impacts (pasture, deforestation, alteration and transformation of spring sources) species richness declined and crenobionts were replaced by unspecialised crenoxenes. 5. The zoogeographic importance of spring habitats is confirmed by the presence of 18 endemic species and by members of genera with an interesting disjunct and relict distribution. 6. A comparison with other geographic areas suggests that springs contain a significant fraction of the total number of species found in freshwater habitats and may contribute almost one third of regional freshwater biodiversity. The presence of endemic crenobionts and rare taxa highlights the importance of these habitats in maintaining high levels of biodiversity as well as their contribution to a better understanding of biodiversity patterns in freshwaters.     

Research on fish ecology in Japan: a brief history and selected review

Fish play an important role in the culture of Japan, supplying the primary source of food protein. Research on fish ecology in Japan began developing about 1955, and paralleled that in North America and Europe, but has a number of unique differences. Two main research foci, stream fish ecology and ecology of Lake Biwa, were founded by H. Kawanabe and his colleagues while graduate students in D. Miyadi's laboratory at Kyoto University in the 1950s. The focus on studies of individual differences in ecology, life history, and behavior by direct observation that were developed in this laboratory had a pervasive influence on research that has continued to the present. In the 1980s, Kawanabe, who had succeeded Miyadi as laboratory head, also co-organized a major research project on the complex communities of cichlid fishes in Lake Tanganyika, which has involved nearly every major Japanese investigator in fish ecology since. A review of research conducted by Japanese investigators in stream fish ecology, ecology of fishes in lakes Biwa and Tanganyika, and marine reef fish ecology revealed a wealth of literature of which most English-speaking fish ecologists are unaware. The most striking difference between Western and Japanese research is the focus on detailed observations and experiments in natural habitats of individual differences in behavior, life history, and ecology, and how these ultimately affect processes at the population and community level, as amply demonstrated by Kawanabe's early work on ayu, Plecoglossus altivelis. This approach predated by 20–30 years the current interest in individual differences and individual-based models in North America and Europe.     

Annual reproductive cycle and rate of the spermatogenic process in male mosquitofish <Emphasis Type=Italic>Gambusia affinis</Emphasis>

The present study investigates the relationship between the annual cycle of testicular development and external environment and the rate of spermatogenesis in the mosquitofish Gambusia affinis based on histological observations of testes. The annual reproductive cycle of the mosquitofish was divided into two periods, i.e., the spermatogenic period (May–October) and resting period (October–April). In the spermatogenic period, the transition from spermatogonia to spermatocytes begins and meiosis actively progresses. In the resting period, the transition from spermatogonia to spermatocytes ceases, meiosis of spermatocytes that already shifted by this period gradually progresses, and a considerable number of sperm balls are produced. Onset of spermatogenesis seems to be related to both a rise in water temperature and a prolonged photoperiod. 5-bromo-2-deoxyuridine (BrdU) was a useful in vivo marker of DNA synthesizing spermatogenic cells. The results of immunohistochemical detection of injected BrdU indicated that 5 days are needed for the conversion of spermatocytes to spermatids, 5 days for spermatids to spermatozoa, and 10 days for spermatozoa to sperm balls.