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Reproductive biology of Dikerogammarus haemobaphes: an invasive gammarid (Crustacea: Amphipoda) colonizing running waters in Central Europe

DOI:10.1007/s10530-009-9496-2
Authors:
Karolina Bacela-Spychalska at University of Lodz
Karolina Bacela-Spychalska
Alicja Konopacka
Alicja Konopacka
Alicja Konopacka
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Michal Grabowski at University of Lodz
Michal Grabowski
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Dikerogammarus haemobaphes is a Ponto-Caspian gammarid that has invaded vast areas in Central and Western Europe. Our paper is a first presentation of its life history features in an invaded region. The study was conducted in the Vistula River in Poland from autumn 2003 to autumn 2005 in two sites differing in hydrological conditions with one being water reservoir. The results showed that the reproductive period lasted 8months from April till October in both sites. Three generations per 1year were observed: autumn (overwintering), spring and summer. Ten cohorts per year were distinguished. The individuals from the reservoir were much bigger than those from the other site. The fecundity of those specimens was also higher and they laid 52 eggs per clutch in average in comparison with 37 eggs in the river itself. The strong relationship between the number of embryos (in developmental stage 2) per clutch and the length of females was noticed. The overall mean egg size of stage 2 of D. haemobaphes was 0.430±0.029mm which is smaller than noted for native species such as Gammarus fossarum. A potentially high reproductive capacity, comparatively small eggs, short time of eggs’ development, fast reaching sexual maturation, short life span, tolerance to a wide range of environmental conditions, all promote the invasion of this Ponto-Caspian gammarid in freshwater ecosystems of the temperate climate zone.
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... For example, juveniles' dominance indicates rapid growth of the population (Dobrzycka-Krahel et al. 2019). The reproductive potential of amphipods is related to body size, the number and size of eggs and embryos, the length of the reproductive period, the time of maturation and voltinism (San Vicente 2018; Bacela et al. 2009;Grabowski et al. 2007a;Bacela, Konopacka 2005;Sainte-Marie 1991). Life history traits are also dependent on other biological (competition and predation) and environmental factors (temperature, food, habitat, water quality and geographical location) (Poznańska-Kakareko et al. 2021;Grabowski et al. 2007a;2007b;Pöckl 2007;Kley, Maier 2006;Panov, McQueen 1998;Sutcliffe 1993;Sainte-Marie 1991;Welton, Clarke 1980;Nilsson 1977;Hynes 1955). ...
... Females prevailed, especially in the reproductive period (Figure 5,7,9), thus indicating a high potential to increase the population in a short time, as has been observed in studies on alien species. For example, in the aggressive alien species Dikerogammarus villosus in the Moselle River, France, D. haemobaphes in the Vistula River, Poland and P. robustoides in the Gulf of Finland (Neva estuary) in north-western Russia, females were more prevalent during the reproductive period, making a significant contribution to the development of the population with a large number of eggs and juveniles in the spring generation (Berezina 2016;Bacela et al. 2009;Devin et al. 2004). ...
... Other invasive alien species in freshwaters are also characterized by a high number of eggs per brood. The size and number of eggs will also depend on the life strategy of the species (Kurina 2017;Bacela et al. 2009;Grabowski et al. 2007a;Kley, Maier 2006;Pöckl 2007;Nelson 1980). ...
The Ponto-Caspian and native amphipod life history in the Daugava River, Latvia
Article
Full-text available
  • Sep 2022
Population structure, reproductive parameters and other life history traits are among the main preconditions for alien amphipods’ successful invasion. In the freshwaters of Northern Europe, i.e. Latvia, the overall life history of alien Ponto-Caspian amphipods is little known. Furthermore, the population structure and reproductivity of native Gammarus pulex have not been studied in Latvian freshwaters. The aim of the study was to describe the life history of Gammarus varsoviensis, Pontogammarus robustoides and the coexistent G. pulex. Their population structure, reproductive period and fecundity in the Daugava River were evaluated as part of this study from 2017 to 2019. The results revealed that the reproductive period of G. varsoviensis and P. robustoides lasted from four to five months, with up to three generations per year and a high proportion of juveniles. The average number of eggs for G. varsoviensis was 31 (maximum: 69) and for P. robustoides 28 (maximum: 81), with ovigerous females of both species being an average of 11.3 mm. Gammarus pulex had one generation per year with a high proportion of juveniles. The average number of eggs per brood was 27 (maximum: 41) with the average size of ovigerous females being 10.7 mm.
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... In our study, the maximum TBL of females and males were higher at the Medsave site than at the Jarun site. It was suggested that the significant differences in the length of individuals of Dikerogammarus haemobaphes (Eichwald, 1841) (Amphipoda) inhabiting two sites with different hydrological characteristics could be due to different hydrological conditions and different predation pressures [81]. In our study, the water levels and discharges of the Sava River were similar at the two sampling sites. ...
... When we observed only sexually mature individuals, the lowest mean TBL was in autumn for most age groups (females at the Medsave site and males at the Medsave and Jarun sites). The opposite pattern was observed in the study on adult individuals of the amphipod Dikerogammarus haemobaphes, who had the lowest size in summer and the highest size in autumn [81]. ...
Life History Traits of the Stygophilous Amphipod Synurella ambulans in the Hyporheic Zone of the Lower Reaches of the Upper Sava River (Croatia)
Article
Full-text available
  • Sep 2023
Estimating the growth and population dynamics of crustaceans is important for understanding the role of species in ecosystems and for conservation and monitoring purposes. This study investigated temporal and spatial variation in population dynamics (growth rate, instantaneous mortality rates, and longevity) of the stygophilous freshwater amphipod Synurella ambulans (F. Müller, 1846), and influencing environmental factors. Seasonal sampling was conducted from December 2018 to October 2019 at two sampling sites (Jarun and Medsave) along the Sava River in northwestern Croatia. A Bhattacharya cohort analysis was applied to the length-frequency data using the FISAT software package. At least four cohorts were distinguished during the year. The possible influence of environmental factors on growth parameters was investigated using Canonical Correspondence Analysis (CCA), which revealed that the important environmental factors influencing S. ambulans abundance were water temperature and dissolved oxygen concentration. The average total body length (TBL) of females was 4.25 mm, while the TBL of males was 3.34 mm. The asymptotic length (L∞) and growth coefficient (K) were estimated to be 6.30 mm and 0.92 year−1 for females and 5.40 mm and 0.59 year−1 for males, respectively, at the Jarun site. L∞ and K were estimated to be 7.20 mm and 0.34 year−1, respectively, for females and 4.00 mm and 1.20 year−1, respectively, for males at the Medsave site. Estimated total mortality (Z) for each sex had higher values for males than females at both sampling sites. The lack of ecological knowledge on S. ambulans populations and relationships with invertebrate communities in the hyporheic zone of the large river ecosystems emphasises the importance of a detailed study for protecting this species and its vulnerable ecotonal groundwater-connected environment.
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... Only June of all summer months was the hottest (Fig. 2, Tab. 2) (Latvian Environment, Geology and Meteorology Centre 2020). It has been shown that the life history traits of various species of amphipod (induction of reproduction, size of body, number of generations per year, number of eggs, maturation time, and choice or migration of habitat) depend on the water temperature and food (Berezina 2016, Bacela et al. 2009, Bacela & Konopacka 2005, Pöckl et al. 2003, Panov & McQueen 1998, Sutcliffe 1993, Sainte-Marie 1991. ...
... As similar to G. varsoviensis the population structure and breeding of P. robustoides during the study can explain by the water temperature. For example, in the population of alien amphipod Dikerogammarus haemobaphes in the Vistula River, from egg fertilization to release of juveniles took around three weeks from 10°C to 13°C in April (Bacela et al. 2009). But in our study, the average water temperature was from 8.2°C in April to 11.5°C in May, and only at the beginning of June it was 14.4°C. ...
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... The demon shrimp has a high potential for invasion (Grabowski et al. 2007a;Bacela et al. 2009;Bacela-Spychalska and Van der Velde 2013). However, another invasive species of the genus Dikerogammarus, the so-called killer shrimp D. villosus, was often considered a more successful invader (Dick et al. 2002;Rewicz et al. 2015;Kobak et al. 2016), attracting more scientific attention than D. haemobaphes. ...
Cryptic diversity and mtDNA phylogeography of the invasive demon shrimp, Dikerogammarus haemobaphes (Eichwald, 1841), in Europe
Article
Full-text available
  • May 2020
The region of the Black, Caspian, and Azov seas are known both as (i) the place of extensive crustacean radiation dated to the times of Paratethys and Sarmatian basins, and (ii) present donor of alien and invasive taxa to many areas worldwide. One amphipod morphospecies, Dikerogammarus haemobaphes, is known both as native to rivers draining to the Black and Caspian seas as well as a successful invader (nicknamed demon shrimp) in Central and Western European rivers. Based on mitochondrial (COI and 16S) and nuclear (28S) datasets and 41 sampling sites, representing both the native (19) and the invaded (22) range, we assessed cryptic diversity, phylogeography and population genetics of this taxon. First, we revealed the presence of two divergent lineages supported by all markers and all species delimitation methods. The divergence between the lineages was high (18.3% Kimura 2-parameter distance for COI) and old (ca. 5.1 Ma), suggesting the presence of two cryptic species within D. haemobaphes. Lineage A was found only in a few localities in the native range, while lineage B was widespread both in the native and in the invaded range. Although genetic divergence within lineage B was shallow, geographic distribution of 16S and COI haplotypes was highly heterogeneous, leading us to the definition of four Geo-Demographic Units (GDUs). Two GDUs were restricted to the native range: GDU-B1 was endemic for the Durugöl (aka Duruşu) Liman in Turkey, whereas GDU-B2 occurred only in the Dniester River. GDU-B3 was both present in several localities in the native range in the Black Sea drainage area and widespread in Central and Western Europe. The GDU-B4 was found exclusively in the Moskva River in Russia. Extended Bayesian Skyline Plot indicated steady growth of GDU-B3 population size since 30 ka, pointing to the rather old history of its expansion, first in the late Pleistocene in the native range and nowadays in Central and Western Europe. The analysis of haplotype distribution across the present distribution range clearly showed two invasion routes to Central and Western Europe. The first one originating from the lower Dnieper allowed the demon shrimp to colonize Polish rivers and the Mittellandkanal in Germany. The second one, originating from the Danube delta, allowed to colonize the water bodies in the upper Danube basin. The UK population has originated from the Central Corridor, as only a haplotype found exclusively along this route was recorded in the UK. Population genetics analysis showed that the invasion of the demon shrimp along the Central Corridor was not associated with the loss of genetic diversity, which might contribute to the success of this invader in the newly colonized areas.
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... One example of just such an invader is Dikerogammarus haemobaphes (Eichwald, 1841), also referred to as the "demon shrimp". D. haemobaphes originates from the Ponto-Caspian region, however the species has been documented to progressively move across much of Central and Western Europe over recent years ( Bacela et al. 2009). In the United Kingdom, it was first recorded in 2012 in the river Severn ( Constable and Birkby 2016;Aldridge 2018), and has since spread rapidly through many canal and river networks across the country (Constable and Birkby 2016). ...
The development of an eDNA based detection method for the invasive shrimp Dikerogammarus haemobaphes
Article
Full-text available
  • Mar 2019
Dikerogammarus haemobaphes is a freshwater gammarid crustacean native to the Ponto-Caspian region. However, the species is rapidly spreading throughout Western Europe and is classed as a highly invasive species. Here we present a novel eDNA assay aimed at detecting D. haemobaphes and demonstrate its suitability with validation steps conducted in-silico (computer simulations), ex-situ (test of specificity using closely related species) and in-situ (within the field). A survey of freshwater systems in the West-Midlands, United Kingdom, highlighted that D. haemobaphes was present in 26 out of the 39 sites assessed. We conclude that eDNA detection for D. haemobaphes is a promising tool for assessing and mapping the presence/distribution of this invasive amphipod.
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Contribution of alien peracarid crustaceans to the biocontamination of benthic macroinvertebrate assemblages in Croatian large rivers
Article
Full-text available
  • Mar 2022
Contribution of alien peracarid crustaceans to the biocontamination of benthic macroinvertebrate assemblages in Croatian large rivers Peracarid crustaceans (orders Amphipoda, Isopoda and Mysida) are one of the most important groups of invaders in fresh and brackish waters. Although large rivers in Croatia have been heavily invaded by peracarid crustaceans, little is known about their impact on local benthic macroinvertebrate assemblages. The main aim of this study was to investigate the contribution of alien Peracarida to the biocontamination of macroinvertebrate assemblages in Croatian large rivers as a proxy measure of their impact. Quantitative sampling was conducted twice (2015 and 2016/2017), at 48 sites on four large rivers (Danube-4, Sava-21, Drava-20, Mura-3). Physicochemical parameters were measured eight times during 2015 and 2016. In total, 16 species were recorded, five native and 11 alien species. The highest number (10 alien species, most from genus Dikerogammarus and Chelicorophium) were found in the Danube River, while subsets of alien species were found in the Sava (5 spp.) and Drava Rivers (6 spp.), and no alien species were found in the Mura River. The most upstream reaches of the Mura, Drava, and Sava Rivers in Croatia have not yet been colonized by invasive peracarids and the native peracarids are still abundant there. In the Drava River, alien Peracarida had the highest densities. Significant negative correlations were established between the number of native taxa and alien Peracarida species. Proportions of alien peracarids in the total density of benthic macroinvertebrates were spatially variable, the highest average values in the Drava River (24.4 %), and lower in the Danube (20 %) and the Sava (17.7 %) Rivers. Alien Peracarida had the most important contribution to the richness and abundance contamination of macro-invertebrate assemblages. The upstream spread of invasive peracarids will increase biocontamination and could cause a decline of native species richness and abundance in the most upstream reaches of the Sava and Drava Rivers. To prevent further upstream spread of alien Peracarida, "check, clean and dry" protocols should be included in the national regulations.
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Pronounced and prevalent intersexuality does not impede the ‘Demon Shrimp’ invasion
Preprint
Full-text available
  • Jan 2015
Crustacean intersexuality is widespread and often linked to infection by sex-distorting parasites. However, unlike vertebrate intersexuality, its association with sexual dysfunction is unclear and remains a matter of debate. The ‘Demon Shrimp’, Dikerogammarus haemobaphes , an amphipod that has invaded continental waterways, has recently become widespread in Britain. Intersexuality has been noted in D. haemobaphes but not investigated further. We hypothesise that a successful invasive population should not display a high prevalence of intersexuality if this condition represents a truly dysfunctional phenotype. In addition, experiments have indicated that particular parasite burdens in amphipods may facilitate invasions. The rapid and ongoing invasion of British waterways represents an opportunity to determine whether these hypotheses are consistent with field observations. This study investigates the parasites and sexual phenotypes of D. haemobaphes in British waterways, characterising parasite burdens using molecular screening, and make comparisons with the threatened Gammarus pulex natives. We reveal that invasive and native populations have distinct parasitic profiles, suggesting the loss of G. pulex may have parasite-mediated eco-system impacts. Furthermore, the parasite burdens are consistent with those previously proposed to facilitate biological invasions. Our study also indicates that while no intersexuality occurs in the native G. pulex , approximately 50% of D. haemobaphes males present pronounced intersexuality associated with infection by the microsporidian Dictyocoela berillonum . This unambiguously successful invasive population presents, to our knowledge, the highest reported prevalence of male intersexuality. This is the clearest evidence to date that such intersexuality does not represent a form of debilitating sexual dysfunction that negatively impacts amphipod populations.
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Features of the reproduction processes of amphipods (Crustacea, Amphipoda) alien species in the conditions of Belarus watercourses
Article
Full-text available
  • Feb 2019
For the first time in Belarus, reproduction features of 6 mass alien Amphipodae species have been established: C. curvispinum, D. villosus, O. crassus, O. obesus, E. ischnus, and D. haemobaphes. The data on the monthly changes in their density and biomass have been given, as well as the species these changes are most pronounced in. The range in temperature conditions, the reproduction processes are observed under, is determined. These conditions are mostly confined to the warm season: all species start reproduction in spring at a temperature of 7.9–11.9 °C and end it in autumn at a temperature of 9.7 °C. Based on changes in the age composition, the main parameters of the life cycle are determined. The reproduction period was established for 5 studied alien species, 2 to 3 generations were observed during a year, the sex ration is determined (the prevalence of females in the species represented indicates the populations stability). The obtained research results, in comparison with the literature data for other parts of the area with similar climatic conditions, mostly coincide, the differences are mainly determined by the temperature and environmental conditions of watercourses. Compared with populations from other parts of the species distribution that have a longer reproduction period, the same number of generations with a shorter reproductive period is observed in Belarus conditions for 5 species of Gammaridae, which indicates the wide adaptive capabilities of these species.
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PARAMETERS OF THE FECUNDITY OF AMPHIPOD CRUSTACEAN ALIEN SPECIES (CRUSTACEA, AMPHIPODA) FROM WATERCOURSES OF BELARUS
Article
Full-text available
  • Aug 2018
For the first time for water bodies of Belarus, based on studies (2008–2015), the main fertility parameters for eight alien species of amphipods were established . The minimum sizes of individuals for which identification of sex and the size of sexual maturation is possible are presented. The ranges of the body length of the egg-bearing females and the average sizes of the breeding individuals were determinate. The sizes and number of eggs are given at three stages of development for females of different age groups. Absolute and relative fertility were revealed. It is established that the number of eggs in the brood bag correlates with the size and weight of the female; the dependences of fecundity on the length and weight of the female were calculated. The theoretical possible number of litters in the period of reproduction of animals in the conditions of the obtained range was determined. The obtained results differed insignificantly with the literature data from regions with similar climatic conditions, that was determined mainly by various ecological conditions.
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Importance of Gammarus in aquaculture
Article
Full-text available
In recent years, there have been significant increases in the production and breeding of aquaculture species; for example, the gilt-head (sea) bream and seabass in salt water and trout, carp, and tilapia in fresh water., Amphipods in the genus Gammarus are used as a rich source of protein to feed various pet animals such as aquarium fish, lizards, and turtles, as well as in aquatic ecotoxicology and water quality assessment. Gammarus meal is used as a partial replacement (10–20%) of fish meal. However, the reproduction and rearing of Gammarus in intensive or semi-intensive conditions has not yet been carried out. Gammarus products (live, dried flakes, or powdered) transported to the markets are constituted from wild caught Gammarus. Due to the high price of these products, Gammarus aquaculture potentially has great economic benefits. Therefore, there is a need to focus on the importance of Gammarus in aquaculture. In the present review, the ecology and distribution of Gammarus, its importance in aquatic ecotoxicology and water quality assessment, the chemical analysis of Gammarus and factors affecting chemical composition of it, and the importance of Gammarus in fish nutrition are discussed. In addition, the economic importance and culture methods of Gammarus are also reviewed. This review will be beneficial for scientific investigators and fish-crustacean farmers.
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Distribution of epigean Malacostraca in the middle and upper Danube (Hungary, Austria, Germany)
Article
  • Jan 1995
The Danube between Harta (rkm 1549) and Kehlheim (rkm 2410) was sampled qualitatively in 1985-1995 at all seasons. Eighteen epigean species of Malacostraca (Janiridae, Asellidae, Gammaridae, Talitridae, Corophiidae, Mysidae, Astacidae, Cambaridae) were recorded. The malacostracan fauna shows a distinct longitudinal zonation in the River Danube. At least nine species are of Ponto-Caspian origin. The actual distribution patterns were analyzed with respect to former studies. At least six species were strongly expansive during the last few decades. Navigation appears to be among the crucial factors for this dispersion.
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Invasive Ponto-Caspian Species in Waters of the Vistula and Oder Basins and the Southern Baltic Sea
Article
  • Jan 2002
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