Interspecific variation in gill size is correlated to ambient dissolved oxygen in the Amazonian electric fish Brachyhypopomus (Gymnotiformes: Hypopomidae)

Gymnotiform electric fish assemblage structure is strongly correlated to dissolved oxygen (DO) availability, which exhibits considerable heterogeneity among Amazonian aquatic systems. DO is known to influence the respiratory morphology of gymnotiform fishes, and yet species-level variation among congeners endemic to alternative DO regimes has not been examined. We describe the DO environment experienced by four congeneric species of gymnotiforms (Brachyhypopomus) and correlate this to quantitative variation in a suite of gill metrics. Whitewater floodplain lakes flanking nutrient-rich whitewater rivers are seasonally hypoxic, exhibiting oxygen concentrations close to 0 mg/l from late April until September. In contrast, DO levels in blackwater floodplain lakes and in terra firme forest stream habitats remain high throughout the year. Two common species of Brachyhypopomus restricted to periodically anoxic whitewater floodplain exhibited a substantially greater gill size than two common species restricted to the perpetually well-oxygenated waters of blackwater floodplain lakes and terra firme stream systems. Discriminant Function Analysis (DFA) based on gill metrics separated the species that live in seasonally anoxic whitewater floodplain species from those that live in perpetually-well oxygenated habitats. Our observations suggest a history of adaptive divergence in the gill morphology of Brachyhypopomus associated with oxygen availability.     

Male colour variation in a eurytopic African cichlid: the role of diet and hypoxia

Species that cross strong environmental gradients are expected to face divergent selective pressures that can act on sexually‐selected traits. In the present study, we examine the role of hypoxia and carotenoid availability in driving divergence in two sexually‐selected traits, male colour and reproductive behaviour, in the African cichlid Pseudocrenilabrus multicolor victoriae. Low‐dissolved oxygen (DO) (hypoxic) environments are expected to be energetically challenging; given that male nuptial colour expression and courtship displays can be costly, we expected fish in low‐DO versus high‐DO environments to differ in these traits. First, a field survey was used to describe natural variation in male nuptial colour patterns and diet across habitats divergent in DO. Next, using wild‐caught fish from a low‐DO and high‐DO habitat, we tested for differences in reproductive behaviour. Finally, a laboratory rearing experiment was used to quantify the interaction of DO and diet (low‐ versus high‐carotenoid availability) on the expression of male colour during development. In energetically challenging low‐DO environments, fish were more red and, in high‐DO environments, fish were typically brighter and more yellow. The frequency of reproductive displays in fish of low‐DO origin was 75% lower, although this had no consequence for brooding frequency (i.e. both populations produced the same number of broods on average). Our laboratory rearing study showed carotenoid availability to be important in colour production with no direct influence of DO on colour. Additionally, weak patterns of diet variation across wild populations suggest that other factors in combination with diet are contributing to colour divergence.     

Hypoxia drives plastic divergence in cichlid body shape

Organisms experience multiple selective agents that can influence phenotypes through heritable and/or plastic changes, often reflecting complex interactions between phenotype and environment. Environmental factors can directly influence phenotypes, but also indirectly affect phenotypic variation when genetic/plastic change in one trait results in correlated genetic/plastic change in another trait. In fishes, body shape is a trait that might be particularly prone to influence from environmental pressures that act on other morphological features. Variation in dissolved oxygen among aquatic environments has a large impact on the size of the gills and brains of fishes. It is likely that dissolved oxygen interacts with other environmental factors to both directly and indirectly influence patterns of body shape variation. We examined effects of dissolved oxygen on body shape variation among populations of an African cichlid fish (Pseudocrenilabrus multicolor) from multiple high- and low-oxygen sites within a single drainage in Uganda. A split-brood laboratory experiment was used to estimate plasticity of gill and brain size, and we used morphometric analyses to identify variation in body shape in F₁ offspring. Several analyses enabled us to identify genetic effects among populations, and effects of oxygen acting either directly on body shape or indirectly through its effects on gill and brain size. A large part of the variation in body shape was due to plastic variation in gill size associated with dissolved oxygen. Fish raised under low oxygen had deeper heads and shorter bodies, and this variation was driven by both direct effects of oxygen and indirect effects of gill size variation. Body shape variation in fishes should reflect interacting effects of multiple environmental factors that act directly or indirectly on morphology. Body shape might be particularly difficult to predict when phenotypes are plastic, because changes among populations would occur rapidly and be unrelated to genetic variation.     

Hierarchical and interactive habitat selection in response to abiotic and biotic factors: The effect of hypoxia on habitat selection of juvenile estuarine fishes

Habitat selection is a shared process among animals where individuals choose areas that differ in biotic and abiotic characteristics to maximize individual fitness. We used manipulative laboratory mesocosm choice experiments to examine hierarchical and interactive relationships influencing this habitat selection process of estuarine fishes. We assessed selection among substrate, dissolved oxygen (DO) concentration, food availability, and predation risk using two common juvenile estuarine fish species, pinfish (Lagodon rhomboides) and Atlantic croaker (Micropogonias undulatus). For both species oxygen concentration greatly influenced selection patterns; fishes strongly avoided low DO conditions, while in higher levels of DO factors such as substrate or food influenced selection patterns. However, both species strongly avoided predators even when alternative habitat was severely oxygen limited. These results suggest that predation risk may be the greatest determinant of habitat selection of the factors considered. Expansion of low DO areas in the world’s oceans is a major anthropogenic disturbance and is rapidly increasing. Assessing impacts of hypoxia on habitat usage of mobile organisms is critical as changes in environmental metrics including predator distribution and DO levels may alter habitat selection patterns disrupting critical ecosystem processes and trophic interactions. Our results indicate that juvenile fishes may forgo emigration from hypoxia due to predation risk. If similar patterns occur for juvenile fishes in estuaries they may potentially suffer from reduced growth, reproductive output, and survivorship.     

Complex phenotype-environment associations revealed in an East African cyprinid

Environmental factors influence phenotypes directly, as well as indirectly via trait correlations and interactions with other environmental variables. Using nine populations of the African cyprinid Barbus neumayeri, we employed path analysis to examine direct, indirect and total effects of two environmental variables, water flow (WF) and dissolved oxygen (DO), on several morphological traits. WF and DO directly influenced relative gill size, body shape and caudal fin shape in manners consistent with a priori predictions. Indirect effects also played an important role in the system: (1) strong, oppositely signed direct and indirect effects of WF on body shape resulted in a nonsignificant total effect; (2) DO had no direct effect on body shape, but a strong total effect via indirect effects on gill size; (3) WF indirectly influenced gill size via effects on DO. Only through examination of multiple environmental parameters and multiple traits can we hope to understand complex relationships between environment and phenotype.     

Hypoxia and life‐history traits in a eurytopic African cichlid

This study quantified variation in key life‐history traits of the widespread African mouth‐brooding cichlid Pseudocrenilabrus multicolor victoriae. Egg size, number, batch reproductive effort, size at maturity and brooding efficiency were compared among field populations across a wide range of dissolved oxygen (DO) concentrations from extreme hypoxia to normoxia. In the laboratory, a similar suite of characters was quantified in F1 of low‐ and high‐DO origin reared under low or high DO. In general, females from low‐DO habitats and females reared under low DO were characterized by a smaller size at maturity and no difference in batch reproductive effort when compared with females from high‐DO habitats or females reared under normoxia. A trade‐off between egg size and number was evident in the field and in the laboratory‐rearing experiment, but the direction of the trade‐off differed. Egg size was negatively correlated with egg number across field populations; females collected from low‐DO sites generally had more, smaller eggs relative to females from high‐DO sites. In the laboratory‐rearing experiment, F1 females of high‐DO origin produced larger, fewer eggs than F1 females of low‐DO origin, lending support to the field results and suggesting a heritable component to these traits. There was also an element of developmental plasticity, F1 females raised under low DO produced larger, fewer eggs compared with F1 females raised under high DO (regardless of population) suggesting that DO may interact with other variables to determine egg size in the field.     

A comparison of the behavioural responses of parasitized and non-parasitized three-spined sticklebacks, Gasterosteus aculeatus L., to progressive hypoxia

Eighty sticklebacks (32 parasitized, 48 uninfected) were subjected to a serial reduction in dissolved oxygen (DO) concentration until they showed continuous aquatic surface respiration for longer than 10s (> 10s ASR). An analysis of results showed that (1) parasitized adult male and female sticklebacks reacted to low DO significantly earlier than non-parasitized controls; (2) severity of parasite infection was significantly correlated with DO at which > 10s ASR occurred; (3) gravid, non-parasitized females show ASR at a relatively high DO, with a threshold response similar to that of parasitized fish.
It is suggested that the metabolic respiratory demand of the parasitic tapeworm larvae causes the stickleback to modify its behaviour at lowered DO. This behavioural modification causes the fish to surface, where they are likely to be at risk from predatory birds. Field data on DO levels at the study site show that environmental conditions in the shallow lake margins approach the range required to affect the behaviour of heavily parasitized sticklebacks.     

Morphology,metabolism and behaviour: responses of three fishes with different lifestyles to acute hypoxia

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Papyrus swamps and the respiratory ecology of Barbus neumayeri

Synopsis In seasonally flooding fresh waters, dissolved oxygen and fluctating water levels combine to create strong seasonal changes in habitat availability and dispersal pathways for fishes. In this study we demonstrate how respiratory mode can affect the use of and dispersal through hypoxic papyrus swamps for a small cyprinid fish, Barbus neumayeri, a species which uses aquatic surface respiration (ASR) in response to severe hypoxia. Monthly records of the distribution and relative abundance of B. neumayeri across 28 stations in a papyrus swamp in Uganda were used to examine seasonal patterns of habitat use and movement. The distribution of B. neumayeri was very restricted during the drier months. Most fish were captured in open pools and channels with large areas of open water surface and higher oxygen. Movement of B. neumayeri was limited to short periods during the wet season when peak water levels produced high levels of oxygen and pathways for movement. Three lines of evidence suggest that these patterns relate to its respiratory mode. These include: the positive :relationship between dissolved oxygen and the number of stations used per month, the positive relationship between fish density at dry season stations and dissolved oxygen, and the absence of fish from stations with. little open water surface area during the dry season. Significant differences in the gill morphology between B. neumayeri from the papyrus swamp and those from the main river suggest that papyrus swamps may contribute to the diversification of B. neumayeri by limiting movement and demanding specialization for extremely hypoxic waters.     

Patterns of variation in life history among South American fishes in seasonal environments

Summary Ten traits related to life history theory were measured or estimated for 71 freshwater fish species from two locations in the Venezuelan llanos. Multivariate statistics and cluster analysis revealed three basic endpoint patterns bounding a two-dimensional continuum. A suite of attributes associated with parental care and aseasonal reproduction appeared to correspond to an equilibrium strategy. A second group of small fishes was distinguished by traits associated with rapid colonizing ability: early maturation, continuous reproduction, and small clutches. The third basic pattern was associated with synchronized reproduction during the early wet season, high fecundity, absence of parental care, and breeding migrations. A subset of mostly small fishes exhibiting little or no parental care, small clutches, and two to four month reproductive seasons was intermediate between the opportunistic (rapidly colonizing) and seasonal strategies. All ten life history variables showed significant effects of phylogeny. The cluster of species corresponding to the equilibrium group was dominated by siluriform fishes and perciforms of the Cichlidae. The opportunistic cluster was dominated by cyprinodontiform and characiform fishes, whereas the seasonal cluster contained primarily characiform and siluriform fishes. Seven of nine traits were significantly correlated with body length. The three reproductive patterns are interpreted as being adaptative with respect to relative intensity and predictability of temporal and spatial variation in abiotic environmental parameters, food availability, and predation pressure.     

Natural selection drives leaf divergence in experimental populations of Senecio lautus under natural conditions

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Oxygen‐mediated plasticity confers hypoxia tolerance in a corallivorous polychaete

There is mounting evidence that the deoxygenation of coastal marine ecosystems has been underestimated, particularly in the tropics. These physical conditions appear to have far‐reaching consequences for marine communities and have been associated with mass mortalities. Yet little is known about hypoxia in tropical habitats or about the effects it has on reef‐associated benthic organisms. We explored patterns of dissolved oxygen (DO) throughout Almirante Bay, Panama and found a hypoxic gradient, with areas closest to the mainland having the largest diel variation in DO, as well as more frequent persistent hypoxia. We then designed a laboratory experiment replicating the most extreme in situ DO regime found on shallow patch reefs (3 m) to assess the response of the corallivorous fireworm, Hermodice carnaculata to hypoxia. Worms were exposed to hypoxic conditions (8 hr ~ 1 mg/L or 3.2 kPa) 16 times over an 8‐week period, and at 4 and 8 weeks, their oxygen consumption (respiration rates) was measured upon reoxygenation, along with regrowth of severed gills. Exposure to low DO resulted in worms regenerating significantly larger gills compared to worms under normoxia. This response to low DO was coupled with an ability to maintain elevated oxygen consumption/respiration rates after low DO exposure. In contrast, worms from the normoxic treatment had significantly depressed respiration rates after being exposed to low DO (week 8). This indicates that oxygen‐mediated plasticity in both gill morphology and physiology may confer tolerance to increasingly frequent and severe hypoxia in one important coral predator associated with reef decline.     

Getting in shape: habitat‐based morphological divergence for two sympatric fishes

Freshwater fishes often show large amounts of body shape variation across divergent habitats and, in most cases, the observed differences have been attributed to the environmental pressures of living in lentic or lotic habitats. Previous studies have suggested a distinct set characters and morphological features for species occupying each habitat under the steady–unsteady swimming performance model. We tested this model and assessed body shape variation using geometric morphometrics for two widespread fishes, Goodea atripinnis (Goodeidae) and Chirostoma jordani (Atherinopsidae), inhabiting lentic and lotic habitats across the Mesa Central of Mexico. These species were previously shown to display little genetic variation across their respective ranges. Our body shape analyses reveal morphometric differentiation along the same axes for both species in each habitat. Both possess a deeper body shape in lentic habitats and a more streamlined body in lotic habitats, although the degree of divergence between habitats was less for C. jordani. Differences in the position of the mouth differed between habitats as well, with both species possessing a more superior mouth in lentic habitats. These recovered patterns are generally consistent with the steady–unsteady swimming model and highlight the significance of environmental forces in driving parallel body shape differences of organisms in divergent habitats. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 114 , 152–162.     

What big lips are good for: on the adaptive function of repeatedly evolved hypertrophied lips of cichlid fishes

Linking phenotypic traits to an adaptive ecological function is a major goal of evolutionary biology. However, this task is challenging and has been accomplished in only a handful of species and ecological model systems. The repeatedly evolved adaptive radiations of cichlid fishes are composed of an enormously diverse set of species that differ in trophic morphology, body shape, coloration, and behaviour. Ecological guilds of species with conspicuously hypertrophied lips have evolved in parallel in all major cichlid radiations and are characterized by large lips and pointed and narrow heads. In the present study, we experimentally tested the adaptive significance of this set of conspicuous traits by comparing the success of hypertrophied‐lipped and closely‐related thin‐lipped endemic Lake Victoria cichlids in a novel foraging assay. The hypertrophied‐lipped species (Haplochromis chilotes) was clearly more successful in exploiting food resources from narrow crevices and the observed difference in foraging success increased more at narrower angles. Furthermore, pronounced differences in exploratory behaviour between the species suggest that the evolution of hypertrophied‐lipped species involved the co‐evolution of a suite of traits that include foraging behaviour. The repeated evolution of hypertrophied‐lip morphology in conjunction with a narrow and pointed head shape in cichlids represents an evolutionary innovation that facilitates foraging in rocky crevices, thus allowing access to a novel niche. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 448–455.     

Brood protection at a cost: mouth brooding under hypoxia in an African cichlid

This study quantifies the behavioral response of the widespread mouth brooding African cichlid Pseudocrenilabrus multicolor victoriae to progressive hypoxia. We exposed four gender/stage classes of P. multicolor (males, brooding females, females that had just released young, and non-brooding females) to progressive hypoxia and recorded the percent time spent using aquatic surface respiration (surface skimming, ASR) and gill ventilation rates. This was done for fish collected from three sites in Uganda (lake, swamp, and river) after long-term acclimation to normoxia. There was no effect of site of origin on response to hypoxia, but ASR thresholds did differ between gender/stage classes. The oxygen level (threshold) at which spent 10, 50, and 90% of their time at the surface using ASR was much higher for brooding females than for males, whereas ASR thresholds did not differ between non-brooding females and males. Similarly, the level at which ASR was initiated was much higher in brooding females than males, but did not differ between males and non-brooders, or between males and females than had just released young. The rate of gill ventilation dropped significantly in males and all stages of females after initiation of ASR, suggesting that surface skimming increases efficiency of oxygen acquisition. These results suggest that mouth brooding in female P. multicolor ASR improves oxygen uptake but imposes a cost in terms of time spent at the water surface, and this may affect maternal predation risk in low-oxygen habitats.     

Physiological (antioxidant) responses of estuarine fishes to variability in dissolved oxygen

Cycles of dissolved oxygen (DO) in estuaries can range from anoxia to various levels of supersaturation (200–300%) over short time periods. Aerobic metabolism causes formation of damaging reactive oxygen species (ROS), a process exacerbated by high or low DO. Fish can generate physiological defenses (e.g. antioxidant enzymes) against ROS, however, there are little data tying this to environmental conditions. We investigated physiological defenses generated by estuarine fishes in response to high DO and various DO cycles. We hypothesized that chemical defenses and/or oxidative damage are related to patterns of DO supersaturation. Specific activities of antioxidants in fish tissues should be positively correlated with increasing levels of DO, if high DO levels are physiologically stressful. We caged common benthic fishes (longjaw mudsucker, Gillichthysmirabilis, and staghorn sculpin, Leptocottusarmatus, in CA and spot, Leiostomusxanthurus and pinfish, Lagodonrhomboides, in NC) during summer 1998 in two estuarine sites in southern North Carolina and two in central California. At each site a water quality meter measured bottom DO, salinity, temperature, depth, pH and turbidity at 30 min intervals throughout the study. These sites exhibited a wide variety of dissolved oxygen patterns. After 2 weeks in the cages, fish gills and livers were analyzed for antioxidant enzymes (glutathione peroxidase, catalase and superoxide dismutase) and the metabolite glutathione. All fish exhibited antioxidant enzyme activity. There was a significant site-dependent effect on all enzyme activities at the NC sites, with the most activity at the site with the highest DO cycling and the most DO supersaturation. There was a trend towards higher enzyme activities under high DO levels at the CA sites.     

Hypoxia tolerance of two centrarchid sunfishes and an introduced cichlid from karstic Everglades wetlands of southern Florida, U.S.A.

In this study, the hypoxia tolerance of three Everglades fishes, two native centrarchids ( Lepomis gulosus and Lepomis marginatus ) and a recently introduced cichlid ( Hemichromis letourneuxi ), were documented. Aquatic surface respiration (ASR) thresholds were lowest for H. letourneuxi , followed by L. gulosus , then L. marginatus . The ASR thresholds for L. marginatus were within ranges reported for small, freshwater tropical fishes, while those for L. gulosus were similar to swamp-adapted fishes. For H. letourneuxi , ASR thresholds were some of the lowest reported. All three species showed excellent tolerance of low dissolved oxygen levels when allowed access to the surface. When denied surface access, L. marginatus lost equilibrium at a higher oxygen tension than the other species. Overall, although all species easily tolerated hypoxia, H. letourneuxi appeared to be best equipped to deal with hypoxia, followed by L. gulosus , then L. marginatus . Hemichromis letourneuxi also exhibited more aggressive behaviours than the centrarchids. These results suggest that hypoxia is not likely to prevent H. letourneuxi from exploiting the seasonally inundated wetlands of south Florida while expanding its range there.     

Comparison of ovarian functions for keeping embryos by measurement of dissolved oxygen concentrations in ovaries of copulatory and non-copulatory oviparous fishes and viviparous fishes

To investigate causes of anomalous development of embryos facultatively fertilized in the ovary of a non-copulatory oviparous fish Hemilepidotus gilberti (Scorpaeniformes: Cottdae), dissolved oxygen (DO) concentrations were measured in ovaries of copulatory oviparous (Alcichthys alcicornis, Bero elegans), non-copulatory oviparous (H. gilberti, Hexagrammus otakii), and viviparous (Sebastes taczanowskii, Zoarces elongatus) fishes. DO concentrations changed during vitellogenesis and ovulation cycles, and also before and after ovulation. DO concentrations in the ovary of H. gilberti and H. otakii at ovulation were 0.27±0.03 and 0.15±0.03 mg O₂ l⁻¹, respectively, whereas in A. alcicornis and B. elegans, the concentrations were 0.47±0.08 and 0.20±0.06 mg O₂ l⁻¹, respectively. In the ovaries of intralumenal gestation viviparous fishes, S. taczanowskii and Z. elongatus, DO concentration was from 0.01 to 0.11 mg O₂ l⁻¹. The average DO concentration during the artificial pregnancy of A. alcicornis was 0.97±0.19 mg O₂ l⁻¹, but all embryos showed deformity. DO concentrations recorded in oviparous fishes in this study were lower than the oxygen level at which most oviparous fish embryos exhibit retardation or death, and it probably caused the anomalous embryonic development. In contrast, the normal development of viviparous fish embryos at low oxygen level was attributed to the specialized structure of ovary, e.g. the dual arterial system to supply the developing embryos with the respiratory demands in Sebastes.     

Plasticity of ontogenetic trajectories in cyprinids: a source of evolutionary novelties

Research in evolutionary developmental (evo‐devo) biology is making an increasingly important contribution to our understanding of the molecular mechanisms underlying the establishment of complex morphological traits. Deciphering the ontogenetic trajectories leading to the differentiation of sister species (and the existence of hybrids) is a new challenge in our understanding of speciation processes. In the present study, we characterized the ontogenetic trajectory of lower lip morphology in two cyprinid species and their hybrids. Chondrostoma toxostoma has an arched lower lip and a generalist diet. Chondrostoma nasus has a straight lower lip and a specialist diet. An analysis of 99 C. toxostoma, 99 C. nasus and 25 first‐generation (F₁) hybrid individuals demonstrated that the difference between arched and straight lip morphology was found to depend strongly on the height/width ratio of the lower lip. A comparison of the ontogenetic trajectories of these morphometric traits showed that the height of the lower lip was isometric to body length in both species, whereas developmental changes involving an acceleration and a hypermorphosis of the widening of the lower lip led to a straight lip morphology in C. nasus. F₁ hybrids were characterized by an extreme phenotype resulting from a rate of lower lip widening slower than that in the two parent species. Therefore, we rejected a codominance hypothesis and concluded that the first stage of hybridization provides the foundations of evolutionary novelty. These results have important evolutionary implications because lower lip shape is linked to dietary behaviour in many fish species. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 342–355.