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Life histories and evolution: insights from notothenioids (Teleostei, Perciformes)
Full text linkABSTRACT
Organisms show an extraordinary variation in their life history traits, both at inter- and intraspecific level, exhibiting phenotypic variations among populations inhabiting different habitat. The variability in life history traits has been related to environmental conditions, as a result of selective processes or phenotypic response to them. In addition to the huge diversity in life history traits, several trade-offs among them have been recognized. The variability in life history traits and in their trade-offs related to environmental conditions represents a key aspect in the study of evolutionary processes. A wide variation in life history traits is documented among teleost fishes, both among and within species, reflecting the effects of evolutionary forces acting on them over time and across environmental conditions. Several life history traits, such as growth rate, age at sexual maturity, fecundity, reproductive investment, egg size, hatching size, are strongly influenced by temperature and food availability. Notothenioid fish represent a unique example of fish adaptive radiation in marine environment. They dominate the waters surrounding the Antarctic continent both by species number, with over 120 species (47%), and biomass (90-95%). Notothenioids distribution is limited exclusively to the Antarctic and sub-Antarctic regions (South America, New Zealand and South East Australia). Variability in their life history traits at inter- and intra-specific levels has been described, with a latitudinal trends in some reproductive traits. In this framework, despite the availability of recent phylogenies of notothenioids, a comparative analysis aimed at studying habitat dependent evolution of reproductive strategies has not yet been performed. Given the particular characteristics of their habitats and the uniqueness of notothenioid fishes, they can be considered an excellent taxon model to investigate the evolution of life history traits in relation to environmental factors.
The aim of this PhD project was to investigate the evolution of life history traits of notothenioid species in relation to environmental variables (such as sea water temperature, primary productivity and sea ice cover), controlling for phylogenetic relationships. The applied methodology (Independent Contrast Method) represents a key aspect in this study since its robustness can prevent the attribution of correlations between life history traits and environmental variables to evolutionary processes, being instead a consequence of phylogenetic relationships among considered species. Using life history traits estimated from collected species and reported in data available in literature, the study focused the attention on gametogenesis and, gonadal investment, such as fecundity and egg size. Such a comparative study of habitat dependent variation of life history traits is interesting for evolutionary biology, given the extreme adaptations shown by Antarctic fishes to their peculiar environment, as well as for conservation biology, because the knowledge of reproductive traits and of their sensitiveness to environmental changes is recognized as a crucial information for the sustainable management of exploited species and their resilience capacity to overcome current climate change.
In the present research, life history traits of 17 species, belonging the eight notothenioid families were investigated (Papers I, II, III, IV, V, VI), providing original information on their biology and strengthening the reliability of the available literature. Intraspecific variability in life history traits was examined in three species, including in the analyses specimens sampled in different areas (Papers I, III and IV). Unpublished life history traits data of 15 species were included in the interspecific comparison (Paper VI). Species included in this study were collected during two cruises carried out onboard the German R/V Polarstern (ANT-XXVIII/4, 2012 and ANT-XXIX/9, 2014) off the Antarctic Peninsula and in the Weddell Sea. Samples, belonging to four notothenioid species, were provided by partner scientists during past Antarctic expeditions (2009, 2010 and 2011 during the austral summer) in different areas (i.e. South Orkney, South Georgia, Burdwood Bank and Western Antarctic Peninsula).
Comparing the results obtained in studies dealing with individual species, the histological analyses generally indicated some similarities among notothenioids. In all the analysed species, females presented a group synchronous ovarian type, in which two clearly distinct groups of oocytes were visible. The more advanced stage of maturity in maturing or mature females were oocytes at late stage of vitellogenesis, constituting the batch of the current season, while the other group included oocytes at the cortical alveoli or previtellogenic stages, representing the next year batch. The occurrence of late vitellogenic oocytes together with others at the cortical alveoli stage supports a prolonged oogenesis, likely lasting more than one year. Testes were of the unrestricted spermatogonial testicular type. In mature males, testes were completely filled with sperm with few cysts of early-stages of spermatogenesis, indicating that sperm maturation completes before the beginning of the breeding season. Long lasting gametogenesis is likely related to the low temperature and to the high reproductive investment.
The study on individual species provided new data on absolute and relative fecundity, egg size, gonadosomatic index (GSI) and age estimates and therefore information useful for the comparative analyses (Paper VI). By means of age estimates through otolith reading, growth rate, age/length relationship, maximum age and age at sexual maturity were assessed (Papers II, III, IV, V). As expected for cold water fish species, notothenioids exhibit slow growth rate, late sexual maturity (at about 50-87% of maximum size) and long life span (up to 24 years).
The intraspecific comparison highlighted that the observed variation in life history traits could be addressed to local conditions (i.e. local prevailing currents linked to cold water masses and melting ice) and/or be a consequence of the species reproductive habits, including egg type, presence/absence of parental care, adult distribution and mobility. In Chaenocephalus aceratus, a benthic species with demersal eggs and parental care, fecundity was higher in the warmer study area, that is not influenced by cold water masses coming from Weddell Sea, respect to the colder area. In the Antarctic silverfish (Pleuragramma antarctica), the only species lying cryopelagic eggs (i.e. eggs laid to the lower surface of platelet pack ice), and in Notothenia rossii, in which individuals shift from benthic to bentho-pelagic habits achieving the adult phase, no differences emerged between populations, with the exception of some differences in oocyte size and GSI, likely related to temporal differences in sampling periods.
The results of the interspecific comparative analyses highlighted some correlation between environmental factors and life history traits, revealing potential evolutionary forces. Differently from the other biological traits considered in this study, the maximum size did not correlate with any environmental variable. These results support the observation that the Bergmann’s rule, describing the occurrence of a positive relationship between maximum size and latitude, with larger specimens found in colder environments (higher latitudes), does not apply at high latitudes.
In notothenioids egg size was negatively related to primary production. Primary production, in turn, is negatively related to latitude, and general theoretical models and relevant studies indicate a positive relationship between egg size and latitude. Food availability and temperature have been claimed as factors driving the general increasing trend in egg size with latitude. Primary production can be considered a proxy of food availability, therefore in notothenioids food availability appears to be the main factor influencing egg size. A positive relationship between egg and larval size is common, and larger larvae are expected to show enhanced competitive abilities, improved capacity to feed on a wide size range of prey items and enhanced starvation resistance, and ultimately higher survival probabilities in extreme conditions. Egg size is also positively related to the maximum parental body size. Generally, large fishes, as for instance tunas or the Ocean sunfish Mola mola, are not more likely to have large eggs than small ones, nonetheless fish size may indeed constrain, rather than determine, the range of possible egg sizes, as suggested also by the results on notothenioids. Large notothenioids could therefore have a wider range of tactics in the partition of reproductive effort between fecundity and egg size. While Low Antarctic species produce small and large eggs, High Antarctic species present only large eggs. Considering the trade-off between egg size and number, a positive relationship between relative fecundity (i.e. the number of eggs in relation to body weight) and primary production was expected but it was not found. Conversely a positive relationship was observed between relative fecundity and mean water temperature, although it remains an unsolved issue which need to be further investigated. Energetic investment in female reproductive effort, i.e. maximum female GSI, showed a positive relationship with sea ice cover. Seasonal pack ice melting, occurring in summer at intermediate Antarctic latitudes, triggers phytoplankton blooms, resulting in an increased primary production with a cascading effect on the pelagic food web. At higher latitudes, where maximum values of GSI have been detected, the sea ice cover is permanent through the year and the primary production is likely to remain low, being also influenced by the long and dark Antarctic winter. These extreme conditions may therefore trigger a higher investment in reproduction, including the investment in eggs (size and/or number) represented by the female GSI.
The insights provided by this study shed light on the major factors that appear to drive the evolutionary processes occurring in the Antarctic environment. The comparative method proved to be a robust tool in investigating adaptive response to different environmental conditions. Despite notothenioids demonstrated to be an excellent model group to study evolutionary process, further investigations, extending to other taxa and species geographical distributions, are necessary to trace more general and comprehensive patterns in the evolution of life history traits. In any case, shared reproductive features such as low fecundity, large egg size, high reproductive investment in gonads and, in some cases, in parental care, low growth rate and late sexual maturity, depict notothenioids as a taxon highly vulnerable to climate change and fishery re-opening scenarios
The Clodia database: a long time series of fishery data from the Adriatic Sea
Full text linkLong-term time series of species abundances can depict population declines and changes in communities in response to anthropogenic activities, climate changes, alterations of trophic relationships. Here we present a database of historical marine fishery landing data, covering a remarkably long time series (1945–2013) and referring to one of the most exploited areas of the Mediterranean Sea, the Adriatic Sea. The database
includes two time series of landing data, 1945–2013 and 1997–2013, from the official statistics of the fish market of Chioggia, where the major fishing fleet of the area operates. Comparisons between the landing
data of the database and landing data from other fisheries or data from scientific surveys support the reliability of the time series in depicting changes in species abundances. The database is expected to be used by fishery biologists and ecologists interested in depicting and understanding temporal variations in species abundances and community composition, in relation to environmental and anthropogenic factors
Long-term changes in community composition and life-history traits in a highly exploited basin (northern Adriatic Sea): the role of environment and anthropogenic pressures
No full textThe changes in a marine community in the northern Adriatic Sea were explored over a period
of 65 years using landings data from a commercial fishing fleet, and the role of fishing pressure
and environmental variations in driving these changes was investigated. A total of 40 taxonomic
categories, including one or several species, were analysed, representing 93·7% of the total landings.
From 1945 to 2010 a significant decrease in the evenness index was observed, indicating a trend
towards landings dominated by fewer taxa. The composition of the landings showed a temporal shift
during the 1980s; from 1945 to the 1980s a continuous, clear change in composition took place,
probably driven by an increase in fishing pressure as well as riverine nutrient inputs. Since the
1980s, a different trend of changing composition emerged. Among the analysed predictors, fishing
capacity, summer seawater temperature, inflow from the Po River (the major river of the northern
Adriatic Sea) and nutrients were related to the changes in landings. In relation to life-history traits of
the landed species, the community shifted from large, late-maturing species to more fecund, smaller
and earlier-maturing species. A high fishing pressure is probably the major cause of these changes,
possibly acting synergistically with environmental variations
Factors involved in prey resource partitioning in the genus Artedidraco (Notothenioidei, Artedidraconidae) from the western Ross Sea
No full textAntarctic plunderfishes are demersal species inhabiting the continental shelf of the Ross Sea, with sympatric distributions and similar morphology. Assuming these species are potential competitors for food, we aimed to quantify food overlap among them and to test the existence of factors involved in prey resource partitioning. Dietary composition and feeding niche breadth were estimated through stomach contents analysis of some species of Artedidraco sampled in the western Ross Sea. The fish community consisted of a wide range of feeders, from specialists like A. glareobarbatus and A. shackletoni, which fed exclusively on epifaunal polychaetes, to generalists like A. loennbergi and A. skottsbergi, which fed on a variety of prey. Although all species relied exclusively on benthic prey, diet diversity and prey type largely differed from each other, both contributing to reduce prey overlap and food competition. In a few cases, relatively high food overlap was observed between species with different spatial distributions. Based on our data and on previous studies, prey resource partitioning in plunderfishes is therefore established through morphological and behavioural adaptations, either by differential development of sense organs and trophic structures or by different diet composition and spatial distribution within the shared benthic habitat
Fisherman cooperation: the key for a successful conservation
No full textArtisanal fishery often offers the best opportunities for impact mitigation but it’s also the most traditional and difficult to change.
Trap fishery, an artisanal method that targets cuttlefish spawning adults in spring, exploits cuttlefish female attraction to traps for
egg laying. The present study estimated the impact of traps on cuttlefish eggs and tested the efficacy and suitability of a
management measure to mitigate this impact in the Northern Adriatic Sea. Results showed that over 3 millions of eggs, in less than
3 miles of coast, are likely destroyed by this fishery. The use of ropes, attached inside traps, allowed to collect on average 23.7%
of the eggs, without affecting catch rate of adults. The efficacy of this mitigation measure is discussed considering fishermen
attitude towards it
Biological traits and reproductive cycle of smooth hounds (Mustelus spp.) in the northern Adriatic Sea
No full textSperm morphology and size of 15 elasmobranch species: comparing data in the light of phylogenetic relationships
No full text
Life history traits of Notothenia rossii and N. coriiceps along the Southern Scotia Arc.
No full textNotothenia coriiceps and Notothenia rossii are two widespread nototheniid fishes, that live sympatrically along the southern Scotia Arc from South Georgia to the South Shetland Islands. In this sector of the Southern Ocean, they experienced different exploitation rates in the past and exhibit different habitat and food preferences as adult. Aiming to evaluate the influence of these factors in shaping life history traits of these species, we compare the reproductive investment and the age structure between the species and in N. rossii, between populations inhabiting
different areas. Based on histological analyses, the two species share the same pattern of gamete development in both sexes. The potential fecundity was similar and was
positively related to fish size in both species, being relatively high with respect to other notothenioids and in terms of egg size at deposition. Based on sagittal otolith readings,
the growth rate and maximum age recorded differed significantly between the two species. Notothenia rossii exhibited a higher growth rate and a comparatively lower maximum
age than N. coriiceps. Similarly, N. rossii attained sexual maturity at the same age but at a larger size than N. coriiceps. At the intraspecific level, no differences in life history traits were observed between the populations of N. rossii collected from different areas. Consistent with the different levels of fishing pressure exerted on these species and their
low resilience, a recent significant decrease over time in the maximum fish size and related reproductive potential has been observed only in the overexploited populations of N.
rossii
Contrasting life history and reproductive traits in two populations of Scyliorhinus canicula
No full textThe role of natural and sexual selection in generating variability in biological traits between populations represents an intriguing issue in evolutionary biology. Considering their occurrence in different environments and the
extensive incidence of post-copulatory sexual selection, elasmobranchs represent an interesting, yet still poorly investigated group. In this study, the life history and reproductive traits of two populations of Scyliorhinus canicula
from the northern Adriatic Sea and the Strait of Sicily were compared. Differences in maximum size and size at sexual maturity were observed. The two populations also displayed differences in male and female genitalia. Males in
the northern Adriatic Sea presented heavier testes, longer epididymis, seminal vesicles and claspers compared with those in the Strait of Sicily, suggesting the occurrence of stronger sperm competition at the former site. Similarly,
females in the northern Adriatic Sea showed heavier oviducal glands and longer reproductive tracts compared with those in the Strait of Sicily. The coevolution between male and female genitalia suggests the occurrence of stronger sexual conflict and/or cryptic female choice in the population from the northern Adriatic Sea. Therefore, natural selection, represented by the different selective pressures occurring at different latitudes, and sexual selection, represented by potentially differing strengths of post-copulatory sexual selection and sexual conflict, may act individually in driving divergence in life history and reproductive traits in these two populations of S. canicula
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