Morphology,performance, fitness: functional insight into a post-Pleistocene radiation of mosquitofish

Bahamas mosquitofish (Gambusia hubbsi) colonized blue holes during the past approximately 15 000 years and exhibit relatively larger caudal regions in blue holes that contain piscivorous fish. It is hypothesized that larger caudal regions enhance fast-start escape performance and thus reflect an adaptation for avoiding predation. Here I test this hypothesis using a three-pronged, experimental approach. First, G. hubbsi from blue holes with predators were found to possess both greater fast-start performance and greater survivorship in the presence of predatory fish. Second, using individual-level data to investigate the morphology–performance–fitness pathway, I found that (i) fish with larger caudal regions produced higher fast-start performance and (ii) fish with higher fast-start performance enjoyed greater survivorship in the presence of fish predators—trends consistently observed across both predator regimes. Finally, I found that morphological divergence between predator regimes at least partially reflects genetic differentiation, as differences were retained in fish raised in a common laboratory environment. These results suggest that natural selection favours increased fast-start performance in the presence of piscivorous fish, consequently driving the evolution of larger caudal regions. Combined with previous work, this provides functional insight into body shape divergence and ecological speciation among Bahamian blue holes.     

Environmental regulation of annual reproductive cycle in the mosquitofish, Gambusia affinis

To clarify the environmental factors regulating the annual reproductive cycle of the female mosquitofish, Gambusia affinis, a viviparous teleost, histological changes of the ovary in natural population, and laboratory experiments were examined. The results, extending over two years, suggested that ovarian recrudescence is initiated by the rise in temperature during spring and that ovarian regression is caused by the shorter daylength during late summer. The first rearing experiments using four photoperiod-temperature groups to investigate the factors triggering the onset of reproduction revealed that females with regressing ovaries began reproduction with the rise of temperature regardless of the photoperiod during spring. The results of the second experiment using three different temperature groups indicated that vitellogenesis occurred at over 14 degrees C and pregnancy at over 18 degrees C. The third experiment with four photoperiod-temperature groups was arranged to investigate the factors in the cessation of reproduction. Sexually active females ceased vitellogenesis of the next clutch of oocytes due to the shorter daylength regardless of temperatures during late summer; however, temperature seemed to influence the rate of embryo development. The critical photoperiod is estimated at about 12.5 hr. In nature, it is supposed that vitellogenesis starts when the temperature rises to about 14 degrees C, and final maturation of oocytes occurs when the temperature reaches about 18 degrees C during spring. Then, vitellogenesis of the next clutch of oocytes ceases when the daylength becomes shorter than 12.5 hr during late summer; the last gestation proceeds at a rate dependent on the temperature, and finally reproduction ends by the last parturition. J. Exp. Zool. 286:204-211, 2000.     

Impacts of mosquitofish (Gambusia affinis) predation on plankton communities

An investigation of the effects of mosquitofish (Gambusia affinis) predation was conducted in 12 experimental ponds in southern California over a period of 10 months.Gambusia essentially eliminatedDaphnia pulex andCeriodaphnia sp. populations, reducedDiaptomus pallidus andKeratella quadrata populations, had little impact onCyclops vernalis, and caused large increases inK. cochlearis, Polyarthra sp.,Synchaeta sp., andTrichocerca spp. populations and in total phytoplankton.Gambusia caused a decrease in the PIE (probability of interspecific encounter) of the planktonic crustaceans and an increase in the PIE of the planktonic rotifers. Hemiptera, such as neustonicMicrovelia sp. and nektonicBuenoa sp. andNotonecta sp., andHyla regilla tadpoles were absent from fish ponds but sometimes abundant in control ponds.Gambusia caused higher pH and oxygen levels, presumably via its effect on the phytoplankton. The impact ofGambusia on the pond ecosystems was less in winter, when fish numbers and feeding rates were low, than in summer. Results of other fish-plankton studies are summarized in tabular form. A model is proposed to account for variation in the calanoid/cyclopoid ratio; evidence is summarized suggesting that in general calanoids are more susceptible to predation by predaceous zooplankters while cyclopoids are more susceptible to fish predation. Some parallels are drawn between the effects ofGambusia predation and those of insecticide treatments.     

Predation and the persistence of melanic male mosquitofish (Gambusia holbrooki)

The empirical reasons for the persistent rarity of a genotype are typically complex and tedious to identify, particularly in nature. Yet rare morphs occur in a substantial fraction of phenotypic polymorphisms. A colour polymorphism has persisted for decades in the eastern mosquitofish, yet why this is so remains obscure. Here, I report the results of (1) intensive sampling at 45 natural sites to obtain the frequency distribution of the melanic (black) mosquitofish morph in Florida, (2) predation trials, conducted independently in mesocosms, with three different predatory species and (3) two mark-recapture studies, conducted in nature. This work (1) documents the rarity of melanic mosquitofish in nature, (2) demonstrates that melanic males experience a selective advantage over silver males in the presence of predators, (3) indicates no difference in the colour morphs' survival at a natural site essentially devoid of these predators, although suggesting a higher rate of recapture for melanic males at a site rife with predators. Overall, selective predation appears to contribute to the persistence of the melanic morph, despite its rarity in nature.     

Life history and parasites of the invasive mosquitofish (Gambusia holbrooki) along a latitudinal gradient

The eastern mosquitofish (Gambusia holbrooki) is among the most invasive fish worldwide and yet, while very abundant in most Mediterranean countries, it is unable to tolerate the colder winters of northern and central Europe. Understanding the effects of latitude on its life-history traits is essential to predict the potential for its invasion of central Europe in current scenarios of climate change. We studied the variation of life-history traits and parasite load in the eastern mosquitofish along a latitudinal gradient from southern France to southern Spain, sampling mosquitofish populations in eight Mediterranean river mouths ranging 5° in latitude. Southern mosquitofish populations displayed higher catch rates, allocated more energy to reproduction (gonadosomatic index and gonadal weight after accounting for fish size) and had a lower condition (total weight and eviscerated weight after accounting for fish size) than in northern populations. Despite variability among populations, size-at-maturity (L₅₀) significantly varied with latitude and northern individuals matured at smaller size (lower L₅₀). Parasite prevalence ranged from 0.0 to 26.7% but parasite richness was very low; all the parasites identified were larvae of pleurocercoid cestodes belonging to the order Pseudophyllidea. The abundance of mosquitofish parasites decreased with latitude and the presence and number of parasites infecting the mosquitofish had a significant negative effect on fish condition. The significant effects of latitude on the catch rates, life history and parasites of mosquitofish highlight the importance of latitudinal studies of invasive species to understand the interactive mechanisms of climate change and biological invasions.     

Behavioral constraints for the spread of the eastern mosquitofish, Gambusia holbrooki (Poeciliidae)

Eastern mosquitofish (Gambusia holbrooki) are native to the southeastern United States but notoriously invasive elsewhere, and are aggressive predators in ecosystems they inhabit. Information on dispersal behavior is needed to better understand mosquitofish spread upon introduction and potential means to mitigate that spread. We experimentally tested the effects of shallow water depths (3–24 mm) and obstacles (leaf litter) on mosquitofish dispersal behavior, plus a range of conditions relevant to field situations. Mosquitofish dispersed significantly faster in deeper water (p < 0.001) but some dispersed in only 3 mm water depth (i.e., one-half average body depth). Wetland and upland leaf litter at natural densities strongly interfered with mosquitofish dispersal behavior. Based on our results, introduced mosquitofish spread rapidly given unimpeded dispersal corridors (e.g., mowed ditches), and may do so at rates >800 m/day. Also, consistent lack of sexual dimorphism in dispersal behavior indicates that mosquitofish spread is not strongly dependent on female poeciliid reproductive biology. Our results support designation of mosquitofish as highly invasive and suggest that barriers to mosquitofish spread must obstruct dispersal pathways as shallow as 3 mm depth.     

Characterization and use of the total head soluble cholinesterases from mosquitofish (Gambusia holbrooki) for screening of anticholinesterase activity

Inhibition of cholinesterases (ChE) has been widely used as an environmental biomarker of exposure to organophosphates (OP) and carbamate (CB) pesticides. Different ChE isoforms may be present in the same tissue and may present distinct sensitivities towards environmental contaminants. The present work characterises the soluble ChE present in mosquitofish (Gambusia holbrooki) total head homogenates, through the use of different substrates and selective inhibitors of cholinesterasic activity. Furthermore, the effects of sodium dodecylsulphate (SDS) on the enzymatic activity were investigated, both in vivo and in vitro. These results showed that acetylcholinesterase (AChE) seemed to be the predominant form present in head homogenates of G. holbrooki, despite the inhibition by tetraisopropylpyrophosphoramide (iso-OMPA) found at high concentrations. SDS was responsible for in vitro, but not in vivo, inhibitory effects. The in vitro AChE inhibitory effects of SDS was partially prevented by the use of increasing amounts of ethanol, suggesting that the inhibition was induced by an emulsion effect, which may explain the lack of effect in vivo.     

Polymorphism and pair formation in the mosquitofish Gambusia holbrooki (Pisces: Poeciliidae)

Synopsis Pair formation was studied in a polymorphic population of Gambusia holbrooki in a brackish drainage canal in Southern Florida. All females and the majority of males were gray colored and only 5% of the males were black spotted. A small fraction of the population formed pairs, composed of a female and a male that swam synchronously and close together for several minutes. During pairing the male often achieved gonopodial contact with the female. Black spotted males occurred in pairs ten fold more frequently than expected under random pairing. The major behavioral mechanism accounting for the disproportionate occurrence of spotted males in pairs is, probably, the preference of females for these males.     

Fat cycling in the mosquitofish (Gambusia affinis): fat storage as a reproductive adaptation

Summary We argue, based on reviewed literature covering reptiles, amphibians, birds, and fish, that fat storage may represent a life history adaptation because it enables an organism to shift in time when resources are allocated to reproduction. We applied these arguments to fat and population cycles in three populations of the mosquito fish, Gambusia affinis. For males, there appeared to be a constant size at maturation during the reproductive season. Mature males became scarce late in the summer. At the same time, immature males delayed maturity and attained much larger sizes; they matured in large numbers in the fall. The amount of stored fat tended to be equal for immature and mature males at all times except in the late summer. In the August samples, when mature males were relatively rare, they also had the lowest level of fat reserves. It appears that the older generation of mature males did not store fat and did not overwinter. At the same time, immature males registered a two to three fold increase in fat reserves. These differences in fat content between mature and immature males disappeared by September, probably because of the recruitment of a new generation of mature males. The reserves were gradually utilized during the winter. Females reproduced from the late spring through mid- to late-summer. They stopped reproducing in the late summer, when there was ample time to produce an additional litter of young. There was an inverse relationship between resources devoted to reproduction and fat reserves. As reproductive allotment decreased in the late summer, fat reserves increased. The magnitude of the change in fat reserves was similar to that displayed by males. The reserves were depleted over the winter. Significant reserves remained at the beginning of the reproductive season the following spring. Reproducing females utilized the remaining reserves significantly more rapidly than non-reproducing females. An analysis of resource availability revealed an overall decrease in food availability in the late summer, coincident with the increase in fat reserves. These cycles are therefore not attributable to changes in resource availability. They instead indicate a change in how resources are allocated by the fish. The trends in the data indicate that fat reserves are used to shift investment in reproduction from the late summer to the following spring. In males, deferring maturity, rather than maturing in August, allows them to store the necessary reserves to survive the winter so that they can mate the following spring. In females, a subset of the fat reserves is intended for producing the first clutch of eggs the following spring. The female pattern corresponds to those reported for a diversity of organisms. The possible advantages of shifting reproductive effort from the fall to the following spring include higher fecundity and higher offspring fitness. The limitations of the methodology and potential directions for future research are discussed.     

Effects of 17alpha-ethynylestradiol on sexual development of male western mosquitofish (Gambusia affinis)

Juvenile male western mosquitofish (Gambusia affinis) were exposed to different concentrations of 17alpha-ethynyl estradiol (EE2) in the diet during the period of sexual maturation. A clear inhibiting influence of EE2 on sexual development was apparent. The proportion of males in each treatment group that failed to complete gonopodial development during the 150-day observation period increased significantly with EE2 concentration. There were significant nonlinear trends toward shorter gonopodia in groups exposed to higher EE2 concentrations. Vitellogenin (VTG) was detectable in the blood of all fish exposed to 1.0 or more micro/g food and the concentration increased dramatically with increasing EE2 exposure. A significant negative association was seen between EE2 concentration and spermatophore counts. This study has demonstrated deleterious effects of EE2 exposure on sexual maturation and several indirect measures of reproductive fitness. It supports the biological relevance of vitellogenin in the blood and reduced gonopodium length as biomarkers for estrogen exposure and endocrine disruption in mosquitofish.     

Tolerance of low oxygen stress in insecticide-resistant and susceptible populations of mosquitofish (Gambusia affinis)

The tolerance of low oxygen stress in insecticide-resistant and susceptible populations of mosquitofish ($\text{Gambusia}$$\text{affinis}$) was investigated. Dissolved oxygen was reduced chemically with formaldehyde and sodium sulfite treatment. Available oxygen was reduced physically through barriers, both by preventing oxygen exchange at the air-water interface and by preventing the fish from contacting the surface of the water. In all cases, the tolerance to low oxygen stress was reduced in the insecticide-resistant population compared to the susceptible population. The results indicate that although tolerance of pesticides in the resistant population has been dramatically increased by environmental selective pressures, tolerance to other stresses has not been concomitantly increased.     

Mechanisms of sexual selection operating on body size in the mosquitofish (Gambusia holbrooki)

Collections in two natural populations of the mosquitofish,Gambusia holbrooki, were made to determine whether the sexesassociated nonrandomly based on body size, and laboratory experimentswere performed to identify mechanisms that could generate theobserved field patterns of association. In both populationslarger females were associated with larger males. However, thesize distributions of males caught with and without femaleswere not different. Both gravid females and females that hadreleased broods within the previous 24 h spent more time nearlarger males in laboratory choice experiments. In contrast,males did not discriminate between females on the basis of sizeor reproductive status in laboratory choice experiments, andmales did not attempt relatively more copulations with largerfemales when one male was allowed to freely interact with twofemales. Body size differences and aggressive interactions betweenmales did influence the access of males to females, with largermales attempting more copulations with females when two maleswere allowed to freely interact with one female: aggressiveinteractions between males were frequent when males differedby < 1.0 mm standard length but were rare when males differedby>5.0 mm standard length. These results indicate that femalechoice for larger males could contribute to generating the nonrandomassociations between the sexes that were observed in these twopopulations and that interactions between males in the vicinityof females may additionally increase the mating advantages oflarger males.     

Consistency of leadership in shoals of mosquitofish (Gambusia holbrooki) in novel and in familiar environments

In social animal groups, an individual's spatial position is a major determinant of both predation risk and foraging rewards. Additionally, the occupation of positions in the front of moving groups is generally assumed to correlate with the initiation of group movements. However, whether some individuals are predisposed to consistently occupy certain positions and, in some instances, to consistently lead groups over time is as yet unresolved in many species. Using the mosquitofish (Gambusia holbrooki), we examined the consistency of individuals' spatial positions within a moving group over successive trials. We found that certain individuals consistently occupied front positions in moving groups and also that it was typically these individuals that initiated group decisions. The number of individuals involved in leading the group varied according to the amount of information held by group members, with a greater number of changes in leadership in a novel compared to a relatively familiar environment. Finally, our results show that the occupation of lead positions in moving groups was not explained by characteristics such as dominance, size or sex, suggesting that certain individuals are predisposed to leadership roles. This suggests that being a leader or a follower may to some extent be an intrinsic property of the individual.     

Effect of mosquitofish (Gambusia affinis) and sestonic food abundance on the invertebrate community within a constructed treatment wetland

1. The effect of mosquitofish (Gambusia affinis) predation on the invertebrate community in a hypereutrophic constructed treatment wetland in southern California was investigated at two nutrient levels that influenced sestonic food abundance. 2. Gambusia affinis and insect predators in the wetland had a significant impact on larval mosquito density in the wetland irrespective of nutrient level. At the end of the 5‐month study, cladoceran abundance in predator exclusion enclosures was 2–3 orders of magnitude greater than in the treatments that allowed access by planktivores. Chironomids were the most abundant insect group collected in emergence traps, and midge production from the high nutrient location of the wetland was greater than from the low nutrient location, but was not affected significantly by G. affinis. The presence of abundant alternative prey in this highly enriched wetland may have weakened the predation impact of G. affinis on mosquitoes. 3. The abundances of six invertebrate groups in dipper samples and of four insect groups in emergence trap collections were analysed using a multivariate distance‐based linear model. Fish treatment and location interactions with sampling date explained significant amounts of the variation in the abundance of invertebrate groups. 4. Multivariate multiple regression analysis showed that chlorophyll‐a concentration explained a large portion of the variability in non‐predatory insect and zooplankton abundance at the high nutrient location, whereas bacterial density explained a large portion of the variability in the abundances of these taxa at the low nutrient location. Predatory insects were not directly coupled to the bottom‐up influence of bacterial abundance and chlorophyll‐a.     

Melanic body colour and aggressive mating behaviour are correlated traits in male mosquitofish (Gambusia holbrooki)

Correlated traits are important from an evolutionary perspective as natural selection acting on one trait may indirectly affect other traits. Further, the response to selection can be constrained or hastened as a result of correlations. Because mating behaviour and body colour can dramatically affect fitness, a correlation between them can have important fitness ramifications. In this work, melanic (black) male mosquitofishes (Gambusia holbrooki) with temperature-sensitive body-colour expression are bred in captivity. Half of the sons of each melanic sire are reared at 19 degrees C (and express a black body colour) and half are reared at 31 degrees C (and express a silver body colour). The two colour morphs are placed in the same social setting and monitored for behavioural differences. Mating behaviour and colour are correlated traits. Mating behaviour differs markedly between the two phenotypes, despite high genetic relatedness. Melanic (black) phenotypes are more aggressive towards females, chasing them and attempting more matings than their silver siblings. Females avoid melanic-male mating attempts more than silver-male mating attempts. When males with temperature-sensitive colour expression are melanic and aggressive, they probably experience a very different selective regime in nature from when they are silver and less aggressive. Under some conditions (e.g. predation), melanic coloration and/or aggression is advantageous compared with silver coloration and/or less aggressive behaviour. However, under different conditions (e.g. high-frequency melanism), melanism and/or aggression appears to be disadvantageous and melanic males have reduced survival and reproduction. Selective advantages to each morph under different conditions may enable the long-term persistence of this temperature-sensitive genotype.     

Allometric relationship between oxygen consumption and body weight of mosquitofish,Gambusia affinis

Synopsis The allometric relationship between body size and oxygen consumption of Gambusia affinis at 28° C was determined under controlled experimental conditions, using a manometric respirometer. The allometric exponent (b-value) was 0.64 ± 0.02 S.E. (n = 51). Oxygen consumption was not influenced by any time-related factors during the 17 days of measurements. Variance between replicated oxygen consumption trials on individual fish was negligible. Specific oxygen consumption rates of several G. affinis at 28° C that were determined by using a sealed vessel and O₂ electrode respirometry method were similar to the rates measured by the manometric respirometry method in similar-sized G. affinis.     

Beta-naphthoflavone inhibits the induction of hepatic oestrogen-dependent proteins by 17alpha-ethynylestradiol in mosquitofish (Gambusia holbrooki)

The interactive effects of an aryl hydrocarbon receptor (AhR) agonist and of a xenoestrogen on biomarker responses were studied in the liver of male mosquitofish (Gambusia holbrooki). Hepatic 7-ethoxyresorufin O-deethylase (EROD) enzymatic activity was measured as a biomarker of exposure to the model AhR agonist beta-naphthoflavone (bNF). Hepatic proteins indicating the exposure of males to the synthetic oestrogen 17alpha-ethynylestradiol (EE2) were monitored by Western blot analysis using immunoserum prepared for this study. After a semi-static exposure only to waterborne EE2, Western blot analysis of liver homogenate revealed the induction of two protein bands (a double band at 205 kDa and a single band at 125 kDa). The interaction between bNF and EE2 was investigated by analysing, on the one hand, EROD activity and, on the other hand, immunoreactivity corresponding to the two oestrogen-dependent protein bands in the liver of fish exposed to different concentrations of bNF for 2 days, then to the same concentrations of bNF plus 0.1 µg l^-1 EE2 for 5 days. EE2 changed neither the basal activity of EROD nor its rate of induction with 1.0 and 4.0 µg l^-1 bNF. On the other hand, the induction of oestrogen-dependent proteins with 0.1 µg l^-1 EE2 was inhibited by exposure to 4.0 µg l^-1 bNF. These results together with literature data suggest that field monitoring of xenoestrogen contamination through the analysis of oestrogen-dependent protein in male fish as a biomarker should take into account the possible negative interference of AhR agonists.