ArticlePublisher preview available

Oxygen stress and reproduction do not impede aerobic performance in adult eastern mosquitofish (Gambusia holbrooki)

Authors:
To read the full-text of this research, you can request a copy directly from the authors.

Abstract and Figures

Physiological traits are key determinants of species success in any given environment. Competing metabolic demands can influence success by limiting the available scope for aerobically-demanding activities, including reproduction and dispersal. The present study investigated whether the aerobic performance of Gambusia holbrooki, one of the most invasive species in the world, was affected by the embryonic demands of pregnancy and whether these demands were compounded in a hypoxic environment. To quantify these effects, we measured the resting metabolic rate (RMR) and critical swimming speed (Ucrit) of wild-caught adult mosquitofish in saturated oxygen conditions, and following chronic exposure to hypoxic or hyperoxic water. Contrary to expectations, the RMR and Ucrit of gravid females was equal to that of non-gravid females and males, once the significant effects of body mass on these traits was accounted for. Whilst the exposure studies demonstrated that RMR changes subject to oxygen availability, overall aerobic performance does not. These findings suggest that mosquitofish metabolism is adapted for continued reproductive function and dispersal in low oxygen environments, which are essential for establishing and replenishment of populations. The ability of this species to tolerate hypoxia may confer a competitive advantage relative to native species, especially in disturbed lentic environments where prolonged periods of hypoxia are more common. Given their live-bearing mode of reproduction and resilience to the metabolic demands of reproduction, even in low oxygen conditions, we suggest that the physiology of female mosquitofish is a significant contributor to the invasion success and persistence of the species.
This content is subject to copyright. Terms and conditions apply.
Oxygen stress and reproduction do not impede aerobic
performance in adult eastern mosquitofish (Gambusia
holbrooki)
Thomas J. Callaghan &Craig R. White &Mischa P. Turschwell
Received: 6 September 2020 /Accepted: 31 January 2021 /Published online: 8 February 2021
Abstract Physiological traits are key determinants of
species success in any given environment. Competing
metabolic demands can influence success by limiting
the available scope for aerobically-demanding activities,
including reproduction and dispersal. The present study
investigated whether the aerobic performance of Gam-
busia holbrooki, one of the most invasive species in the
world, was affected by the embryonic demands of preg-
nancy and whether these demands were compounded in
a hypoxic environment. To quantify these effects, we
measured the resting metabolic rate (RMR) and critical
swimming speed (U
crit
) of wild-caught adult
mosquitofish in saturated oxygen conditions, and fol-
lowing chronic exposureto hypoxic or hyperoxic water.
Contrary to expectations, the RMR and U
crit
of gravid
females was equal to that of non-gravid females and
males, once the significant effects of body mass on these
traits was accounted for. Whilst the exposure studies
demonstrated that RMR changes subject to oxygen
availability, overall aerobic performance does not.
These findings suggest that mosquitofish metabolism
is adapted for continued reproductive function and dis-
persal in low oxygen environments, which are essential
for establishing and replenishment of populations. The
ability of this species to tolerate hypoxia may confer a
competitive advantage relative to native species, espe-
cially in disturbed lentic environments where prolonged
periods of hypoxia are more common. Given their live-
bearing mode of reproduction and resilience to the met-
abolic demands of reproduction, even in low oxygen
conditions, we suggest that the physiology of female
mosquitofish is a significant contributor to the invasion
success and persistence of the species.
Keywords Invasive species .Aerobic metabolism .
Swimming performance .Pregnancy .Mosquitofish
Introduction
Invasive alien species are a key driver of global biodi-
versity decline and ecosystem degradation (Wilcove
et al. 1998; Pejchar and Mooney 2009). These species
generally exhibit advantageous physiological traits or
phenotypic differences, increasing the probability of
establishment and success relative to native species
(Crawley et al. 1986;MoyleandMarchetti2006). Un-
derstanding the biological mechanisms that contribute
to the success of invasive species is important to ensure
appropriate management strategies are developed to
minimise present and future impacts.
Freshwater ecosystems and fish are particularly vul-
nerable to the effects of alien species introductions
(García-Berthou et al. 2005). For example, the introduc-
tion of Nile Perch (Lates niloticus)intoLakeVictoria
led to the decline and extinction of endemic
Environ Biol Fish (2021) 104:143154
https://doi.org/10.1007/s10641-021-01065-z
T. J. Callaghan (*):C. R. White
School of Biological Sciences, University of Queensland,
Brisbane, Queensland, Australia
e-mail: thomas.callaghan@uqconnect.edu.au
M. P. Turschwell
Australian Rivers Institute, Griffith University, Brisbane,
Queensland, Australia
#The Author(s), under exclusive licence to Springer Nature B.V. part of Springer Nature 2021
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
ResearchGate has not been able to resolve any citations for this publication.
Preprint
Full-text available
Freshwater ecosystems have been severely fragmented by artificial in-stream structures designed to manage water for human use. Significant efforts have been made to reconnect freshwater systems for fish movement, through the design and installation of dedicated fish passage structures (fishways) and by incorporating fish-sensitive design features into conventional infrastructure (e.g. culverts). Key to the success of these structures is making sure that the water velocities within them do not exceed the swimming capacities of the local fish species. Swimming performance data is scarce for Australian fish, which have a reduced swimming capacity when compared to many North American and European species. To help close this knowledge gap and assist fisheries management and civil engineering, we report the swimming performance capacities of twenty-one small-bodied fish and juveniles (< 10 cm) of large bodied species native to Australia as measured by critical swimming speed (Ucrit) and burst swimming speed (Usprint) in a recirculating flume. This data is complemented by endurance swim trials in a 12-meter hydraulic flume channel, and by measures of flume traverse success. Building on the utility of this dataset, we used a panel of morphological, behavioural and ecological traits to first assess their relative contributions to the observed swimming performance data, and second, to determine if they could be used to predict swimming performance capacity; a useful tool to assist in the management of species of conservation concern where access to swimming performance data may be limited. We found that body length combined with depth station (benthic, pelagic or surface) explained most of the interspecific variation in observed swimming performance data, followed by body shape and tail shape. These three traits were the most effective at predicting swimming performance in a model/unknown fish. This data will assist civil engineers and fisheries managers in Australia to mitigate the impact of in-stream structures on local fish populations.
Article
Full-text available
Swimming performance of pregnant live-bearing fish is presumably con- strained by the additional drag associated with the reproductive burden. Yet, it is still unclear how and to what extent the reproductive investment affects body drag of the females. We examined the effect of different levels of reproductive investment on body drag. The biggest measured increase in body volume due to pregnancy was about 43%, linked to a wetted area increase of about 16% and 69% for the frontal area. We printed three-dimen- sional models of live-bearing fish in a straight body posture representing different reproductive allocation (RA) levels. We measured the drag and visu- alized the flow around these models in a flow tunnel at different speeds. Drag grewin a power fashion with speed and exponentially with the increase of RA, thus drag penalty for becoming thicker was relatively low for low speeds com- pared to high ones. We show that the drag increase with increasing RA was most probably due to bigger regions of flow separation behind the enlarged belly. We suggest that the rising drag penalty with an increasing RA, possibly together with pregnancy-related negative effects on muscle- and abdominal bending performance, will reduce the maximum swimming speed.
Article
Full-text available
Synopsis: Arnold's 1983 path-analytic paradigm, considering "morphology, performance, and fitness," has been elaborated in several ways. For example, current versions recognize the level of "behavior" (including aspects of motivation) as a filter between performance abilities (only measurable if motivation is maximal) and fitness components. Performance abilities constrain behavior, but behavioral choices may shield performance from selection. Conceptual and empirical issues remain, such as the extent to which individual variation in lower-level subordinate traits (e.g., circulating hormone concentrations) might directly affect behavior, growth rates, sexual maturation, etc., rather than having effects only through paths involving some aspect of performance. Moreover, empirical studies have yet to encompass more than a few possible paths in a given system, in part because life-history researchers rarely communicate with those focused on performance. Most life-history studies ponder trade-offs associated with reproductive effort, but studies of locomotor performance (e.g., maximal sprint speed) have rarely considered trade-offs with reproduction. This lack of connection is surprising because both life history (e.g., clutch size) and locomotor performance (e.g., locomotor stamina) traits require allocation of energy and other resources, so trade-offs between these trait types may be expected. These perspectives and cultures could be bridged by a focus on the ability of organisms to perform components of reproductive biology (e.g., lactation performance could be studied in animals maximally "motivated" by manipulation of litter size or endocrine function). Alternatively, one could study impacts of reproduction on performance, as when bats and live-bearing fishes lose maneuverability during gestation. We also consider sperm performance in the context of the paradigm and illustrate that the paradigm can easily be utilized as a frame-work within which to consider key aspects of sperm biology.
Article
Full-text available
Deciphering the mechanisms by which climate change interacts with invasive species to affect biodiversity is a major challenge of global change biology. We conducted experiments to determine whether the global invader, Gambusia holbrooki, was more resistant to high water temperature (heat) and low dissolved oxygen (hypoxia) than a threatened native fish, Nannoperca australis. Metabolic experiments conducted at 25 and 29 °C showed that G. holbrooki had at least four times the capacity for metabolic depression during hypoxia than N. australis. An increase in environmental temperature from 25 to 29 °C had no significant impact on the critical oxygen tension, Pcrit, of G. holbrooki, but significantly and strongly increased Pcrit of N. australis. Gambusia holbrooki also had a lower Q10 of standard metabolic rate than N. australis. Our results indicate that G. holbrooki have physiological traits conferring greater resistance to hypoxia than N. australis, and as temperature increases, the resistance of N. australis to hypoxia was more eroded than that of G. holbrooki. Intensive monitoring of the temperature and dissolved oxygen dynamics of wetlands showed that contemporary heat waves are already causing conditions that might give G. holbrooki the edge over N. australis on Australian floodplains. Our study adds weight to recent anecdotal reports of drought and heat waves causing localised extinction of N. australis, but the proliferation of G. holbrooki.
Article
Full-text available
This review and data analysis outline how fish biologists should most reliably estimate the minimal amount of oxygen needed by a fish to support its aerobic metabolic rate (termed standard metabolic rate; SMR). By reviewing key literature, it explains the theory, terminology and challenges underlying SMR measurements in fishes, which are almost always made using respirometry (which measures oxygen uptake, ṀO2). Then, the practical difficulties of measuring SMR when activity of the fish is not quantitatively evaluated are comprehensively explored using 85 examples of ṀO2 data from different fishes and one crustacean, an analysis that goes well beyond any previous attempt. The main objective was to compare eight methods to estimate SMR. The methods were: average of the lowest 10 values (low10) and average of the 10% lowest ṀO2 values, after removing the five lowest ones as outliers (low10%), mean of the lowest normal distribution (MLND) and quantiles that assign from 10 to 30% of the data below SMR (q0·1, q0·15, q0·2, q0·25 and q0·3). The eight methods yielded significantly different SMR estimates, as expected. While the differences were small when the variability was low amongst the ṀO2 values, they were important (>20%) for several cases. The degree of agreement between the methods was related to the c.v. of the observations that were classified into the lowest normal distribution, the c.v. MLND (C.V.MLND). When this indicator was low (≤5·4), it was advantageous to use the MLND, otherwise, one of the q0·2 or q0·25 should be used. The second objective was to assess if the data recorded during the initial recovery period in the respirometer should be included or excluded, and the recommendation is to exclude them. The final objective was to determine the minimal duration of experiments aiming to estimate SMR. The results show that 12 h is insufficient but 24 h is adequate. A list of basic recommendations for practitioners who use respirometry to measure SMR in fishes is provided.
Article
Nile perch were secretly introduced into Lake Victoria in the 1950s, and officially in the 1960s, amid unresolved controversy. Proponents were of the view that the introduction would improve fisheries production and sport fishing. Although the former objective was achieved, the side effects were dire, including extinction of many native species, especially the ecologically important haplochromines, because of predation. The introduction also changed the habitat, trophic dynamics and water clarity. The change in water clarity is thought to be responsible for hybridization of haplochromines, further contributing to the loss of species diversity among cichlids. The establishment and expansion of the Nile perch also altered the fishery and socio-economic settings characterizing the lake. A local economy which, until the early 1980s, was based on native fish species has been replaced by an export-oriented exotic fish processing industry that destroyed the once-cherished traditional resource. Other socio-economic issues associated with Nile perch include the high HIV/AIDS prevalence among fishers, and border conflicts attributable to the migratory and transboundary nature of the fishery resource. Conservation measures for the fishery should include establishment of co-management units that have so far registered both successes and challenges. Other efforts include establishment of the Nile perch Fisheries Management Plans that focus on curbing overfishing and eradicating illegal fishing.
Article
Little is known about levels of dissolved oxygen fish are exposed to daily in typical urbanised tropical wetlands found along the Great Barrier Reef coastline. This study investigates diel dissolved oxygen (DO) dynamics in one of these typical urbanised wetlands, in tropical North Queensland, Australia. High frequency data loggers (DO, temperature, depth) were deployed for several days over the summer months in different tidal pools and channels that fish use as temporal or permanent refuges. DO was extremely variable over a 24 h cycle, and across the small-scale wetland. The high spatial and temporal DO variability measured was affected by time of day and tidal factors, namely water depth, tidal range and tidal direction (flood vs ebb). For the duration of the logging time, DO was mainly above the adopted threshold for hypoxia (50% saturation), however, for around 11% of the time, and on almost every logging day, DO values fell below the threshold, including a severe hypoxic event (<5% saturation) that continued for several hours. Fish still use this wetland intensively, so must be able to cope with low DO periods. Despite the ability of fish to tolerate extreme conditions, continuing urban expansion is likely to lead to further water quality degradation and so potential loss of nursery ground value. There is a substantial discontinuity between the recommended DO values in the Australian and New Zealand Guidelines for Fresh and Marine Water Quality and the values observed in this wetland, highlighting the limited value of these guidelines for management purposes. Local and regional high frequency data monitoring programs, in conjunction with local exposure risk studies are needed to underpin the development of the management that will ensure the sustainability of coastal wetlands.
Article
In freshwater ecosystems, abiotic factors such as flow regime and water quality are considered important predictors of ecosystem invasibility. The aim of this study was to investigate the critical swimming capacity and metabolism of the eastern mosquitofish, Gambusia holbrooki, focusing on sex and size effects, to evaluate the influence of water flow on its invasive success. Specimens of mosquitofish were captured from the Ter Vell lagoon (L'Estartit, north-eastern Spain) in July 2014, and we measured the critical swimming speed (Ucrit) and oxygen consumption of individual fish (30 females and 30 males) using a mini swim tunnel. The mean Ucrit of this poeciliid fish was estimated at 14.11 cm·s-1 (range = 4.85-22.26), which is lower than that of many other fishes of similar size and confirms that this species is limnophilic and its invasive success might be partially explained by hydrologic alterations. However, the Ucrit and maximal metabolic rate vary markedly with fish size and sex, with males having much higher values for the same body mass, and thus probably being more resistant to strong water flows. Multiple regression models illustrate that multivariate analyses might increase the predictive power and understanding of swimming performance and metabolic traits, compared to results from conventional simple regressions.