Biol Invasions (2009) 11:2055–2066 DOI 10.1007/s10530-009-9496-2

ORIGINAL PAPER

Reproductive biology of Dikerogammarus haemobaphes: an invasive gammarid (Crustacea: Amphipoda) colonizing running waters in Central Europe Karolina Bacela Æ Alicja Konopacka Æ Michal Grabowski

Received: 17 January 2008 / Accepted: 12 August 2008 / Published online: 25 June 2009 Ó Springer Science+Business Media B.V. 2009

Abstract 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 8 months from April till October in both sites. Three generations per 1 year 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

K. Bacela (&)
A. Konopacka
M. Grabowski Department of Invertebrate Zoology and Hydrobiology, University of Lodz, Banacha 12/16, 90-237 Lodz, Poland e-mail: [email protected] A. Konopacka e-mail: [email protected] M. Grabowski e-mail: [email protected]

was 0.430 ± 0.029 mm 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. Keywords Life history
Fecundity
Alien species
Ponto-Caspian species
Freshwater bodies

Introduction Dikerogammarus haemobaphes (Eichwald, 1841) is one of five invasive gammarid species of PontoCaspian origin occurring in Polish fresh waters (Grabowski et al. 2007a). Its expansion in European rivers started in 1950s via the southern migration corridor (Bij de Vaate et al. 2002) going up the Danube (Strasˇkraba 1962; Nesemann et al. 1995) and reaching the River Rhine in 1995 (Scho¨ll et al. 1995). Simultaneously, it has reached the Baltic Sea drainage area via the central migration corridor (Grabowski et al. 2007a). It was recorded for the first time in Poland in the lower Vistula River by Konopacka in 1996 (Konopacka 1998). Further research of Polish running waters showed that the

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species dominated amphipod communities in all the middle and the lower Vistula flow including its deltaic system (Jazdzewski et al. 2002, 2004; Grabowski et al. 2006). It was recorded in other large rivers: Oder with its delta, Bug, Notec and Warta (Jazdzewski and Konopacka 2000, 2002; Jazdzewski et al. 2002) where it has become very abundant nowadays (Jazdzewski et al. 2004). It is also present in the Great Masurian Lakes (Jazdzewski 2003) and in a small mesotrophic lake in the Vistula valley (Grabowski and Bacela 2005). While the geographical distribution of the species is well studied, there is only few data published concerning its biology. Ponomareva (1975) and Kiticyna (1980) stated that the species is very tolerant to some ecological parameters such as salinity and temperature. Reproductive biology was partly studied by Kurandina (1975), Kiticyna (1975) and Musko´ (1993), however, the complete life cycle was almost unknown, especially for the populations invading new territories. Detailed data on the biological features of the species are crucial to understand its place in functional structure of invaded ecosystems. It constitutes a food base for local fish particularly those belonging to the Percidae, Gobiidae and Anguillidae (Kelleher et al. 1998, 2000; Kostrzewa and Grabowski 2003; Grabowska and Grabowski 2005), and it is also known as a vector of parasites such as gregarines (Codreanu-Balcescu 1995). The aim of our study was to describe the life history of D. haemobaphes by estimating its fecundity, reproductive period and population demography. We studied the population inhabiting the lower Vistula River. The results were compared to data available for populations inhabiting different geographical regions as well as for other gammarid species in order to reveal the role of life history traits in promoting the species invasion in European rivers.

K. Bacela et al.

In the first site, Nieszawa, placed on 695 km on the Vistula flow (N52°500 ; E18°540 ) the river is around 500 m wide (Fig. 1). According to Donderski and Wilk (2002) the Vistula River undergoes an intense self-purification in that section. Samples were taken from the shallow littoral zone where current was relatively fast (ca. 0.214 m s-1). The substrate consisted of stones covered with tubes of another invasive amphipod Chelicorophium curvispinum (G.O. Sars, 1895) that occurred in very high densities, periphyton and mud. Occasionally grass roots, Potamogeton pectinatus L. and Elodea canadensis Michx. were also found at that site. The second study site was Murzynowo (N52°350 ; E19°300 ) on 642 km of the river flow, in the Wloclawski Reservoir built in 1970s between ca. 618 and 675 km from the source of the Vistula River (Fig. 1). This water reservoir is the largest artificial lake in Poland. Its area is ca. 70 km2, the length 55– 58 km, width 0.5–2.5 km, maximal and mean depth 15 and 5.5 m, respectively (Glogowska 2000). The reservoir is not a typical ‘‘dam reservoir’’ since the retention time is only 5 days, and there is a total replacement of water 70 times per year. Gizinski (2000) suggested that the proper name for this kind of system is a ‘‘run-off-river reservoir’’. Animals were gathered from the shallow littoral zone of the reservoir where the water was almost still and the current was 0.009 ± 0.005 m s-1. The sediment consisted of gravel and shells of Viviparus

Materials and methods Study sites The research was carried out at two sites on the lower Vistula River differing in hydrological characteristics.

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Fig. 1 Localisation of sampling sites

Reproductive biology of Dikerogammarus haemobaphes

viviparus (Linnaeus, 1758). The roots of white willow (Salix alba L.) were also present in the site. Sampling gammarids In Nieszawa samples were gathered once a month during winter and twice a month during spring, summer and autumn from October 2003 till November 2004 and from April till October 2005. Sampling in Murzynowo was carried out from April to August 2004 because only few individuals of D. haemobaphes were found in the site outside that period. All samples were collected with a fine-meshed net and preserved in formalin. At every occasion the water temperature was measured and presence of pair in prae-copula was notified. In the laboratory samples were sorted and gammarids were transferred into 75% ethanol. Measurements and indices used to qualify the reproductive biology of D. haemobaphes Each individual was measured under stereomicroscope with ocular micrometer from the anterior margin of a head to the posterior margin of the telson with an accuracy of 0.5 mm. Sex was identified by presence of penes on the male pereon VIIth sternite and presence of oostegites in females. Individuals without penes or oostegites were classified as juveniles. Females were classified based on stage of development of oostegites (Fig. 2): o1—small oostegites, o2—large oostegites without setae,

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o3—large oostegites with setae forming the brood pouch (modified after Zielinski 1995). Ovigerous females were classified according to presence of eggs or juveniles in brood pouch. Different stages of embryonic development were identified: s2—the second stage of development according to classification by Weygoldt (1924) and Skadsheim (1982); s3—egg enlarged, advanced embryological development visible through outer layer; the third, fourth and fifth stage according to Weygoldt (1924) and Skadsheim (1982); s4—the last stage before releasing, eye of progeny well visible; stage sixth according to Weygoldt (1924) and Skadsheim (1982); s5—juveniles released from the egg membrane. In order to determine the female fecundity and the relationship between its size and brood size, the number of eggs in developmental stage 2 was counted in 136 females that had undamaged brood pouches. Additionally 2,347 stage 2 eggs in 88 females were measured to the nearest 0.001 mm with stereoscopic microscope with Lucia 5.0 software (Laboratory Imaging Ltd, Prague, The Czech Republic). An average length and width of egg was used as a measurement of its size (Steele and Steele 1969; Sainte-Marie 1991; Maranhao et al. 2001). To estimate the role of life history traits in the species invasion success several other parameters were obtained: 1. 2.

3. 4. 5.

number of generations per year; number of cohorts per year—estimated with Bhattacharya (1967) method: cohorts could be followed from one sample to another (see Piscart et al. 2003), separation of cohorts was done using FiSAT II 1.2.0.software (2005, FAO, Rome, Italy); length of reproductive period; partial fecundity index (PF)—defined as mean brood size/mean breeding female size; relative size when reaching maturity (Mind— maturity index)—defined as minimal/mean breeding female size.

Results Fig. 2 Stages of oostegite developments used for female classification

Dikerogammarus haemobaphes was very abundant in the first site (Nieszawa). It co-occurred with numerous

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C. curvispinum, less numerous Chaetogammarus ischnus (Stebbing, 1899) and scarce Pontogammarus robustoides (G.O Sars, 1894). Other invertebrates, such as larvae of caddisflies and dragonflies, oligochaetes and gastropods were also present. In the second site (Murzynowo) P. robustoides dominated in all seasons. D. haemobaphes was much less numerous, but its density was higher than C. ischnus also present in the site. Among other invertebrates chironomid larvae and oligochaetes were the most abundant.

K. Bacela et al.

The population structure of D. haemobaphes collected in Nieszawa is shown with histograms (Fig. 3a, b). The breeding period lasted 8 months from April to October, when gravid females were observed. However, first pairs in prae-copula were recorded already in March. The highest numbers of ovigerous females was observed in April, when 75% (in 2004) and 57% (in 2005) of all females carried eggs (Fig. 4). In May the second peak in reproduction was noted (49% of all females), and the third one at the end of July (50%).

Fig. 3 a Population structure of D. haemobaphes in subsequent sampling dates (2003/2004). b Population structure of D. haemobaphes in subsequent sampling dates (2005)

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Fig. 3 continued

The data analysis showed that three generations appeared during 1 year: spring, summer and autumn generation. The autumn generation matured quite slowly during winter and in March its growth rate was the highest (t = -10.54, df = 111, P \ 0.0001). That overwintering generation started to reproduce at the beginning of April. Its progeny (spring

generation) appeared in the middle of May and population size structure was strongly bimodal because of the presence of a parental generation. The autumn generation died of at the end of June what is confirmed by the size structure analysis of following samples (t = 4.93, df = 81, P \ 0.0001). The spring generation started to reproduce in June

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Fig. 4 Proportion of breeding versus non-breeding females of D. haemobaphes in subsequent sampling dates

and at the beginning of July the summer generation was released. Individuals of summer generation mature relatively quickly and during the same reproductive season they reproduced and gave rise to the next autumn generation. The analysis of data presented in Fig. 5 allowed us to estimate the length of egg development time. It took around 3 weeks from fertilization of the egg to release of juvenile in raising temperature from 10°C (12.04.2005) to 13°C (30.04.2005). The Bhattacharya method allowed us to distinguish 10 cohorts that appeared during 1 year (Fig. 6). The male/female sex ratio was generally close to 1:1 (v2 = 26.65, df = 24, P = 0.01; Fig. 7). Significantly more males were in October 2003 and February 2004, in contrast to June and November

Fig. 5 Proportion of females of D. haemobaphes carrying embryos in different developmental stages (s2–s4), juveniles (s5) and with empty brood pouch (o3) in subsequent sampling dates

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2004 when females were the most abundant in the population. It is worth to be added that during studies several intersexes were found: 11 individuals in Nieszawa (from 1522 individuals examined) and 10 in Murzynowo (from 964). Their body length ranged from 9 to 15 mm. Three of these specimens were able to lay eggs in brood pouch. Moreover, those eggs were in stage 2 and 3 of embryonic development, which means that they had been fertilized. Body length of gravid females ranged from 7 to 14.5 mm, with a mean of 10.5 mm. The maturity index (minimal size/mean size of gravid females) was low (0.67) that can be interpreted as reaching the maturity at relatively young age. The mean brood size was 35 and ranged from 5 to 98 eggs per brood. Partial fecundity gained relatively high value of 3.2. It has to be stressed that breeding females from the summer generation were the smallest in comparison with the autumn and spring generations (F2.75 = 36.68, P \ 0.0001) and had about twice smaller mean clutch size (20 eggs) per brood in comparison with other generations (F2.75 = 36.68, P \ 0.0001) (Fig. 8a, b). As a strong correlation between the length of ovigerous females and their brood sizes was observed (Fig. 9) there were no differences between generations in the regression indices observed (Table 1). There was no possibility to study the whole life cycle of D. haemobaphes in the Wloclawski Reservoir in Murzynowo. However, differences in size of individuals and in the clutch size were found between both sites if the animals from the same months (April, May, June and July 2004) were compared (Table 2). All mature individuals inhabiting the reservoir were much bigger than those from the river (t = 9.48, df = 1297, P \ 0.0001). In both populations no size differences between sexes were observed. The mean size of breeding females significantly differed between those two populations. Females from the artificial reservoir were bigger than that from the river (t = 2.58, df = 111, P \ 0.005). The analysis of the clutch size and partial fecundity showed that the reservoir population is also more fecund (t = 2.93, df = 92, P \ 0.002; t = 2.75, df = 96, P \ 0.003, respectively), but the analysis of covariance did not show any differences between both populations (Table 3; Fig. 10).

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Fig. 6 Number and estimated growth of cohorts of D. haemobaphes over the entire sampling period

Fig. 7 Sex ratio in studied populations of D. haemobaphes over the entire sampling period

It is worth to mention that there was no difference in the size of eggs between both populations studied (t = -0.05, df = 84, P = 0.96) as well as comparing among different months. Mean size of eggs was 0.430 ± 0.029 mm.

Discussion The life cycle of D. haemobaphes studied in the Vistula River was semi-annual and multivoltine based on classification by Steele and Steele (1986) and Sainte-Marie (1991). Three generations: spring, summer and autumn appeared in 1 year. Similar results came from Kurandina (1975) and Kiticyna (1980) who had studied populations from Ukraine. Also the reproductive periods were similar in all

cases despite the population inhabiting heated waters described by Kiticyna (1980). Both populations inhabiting the Vistula River, especially the one from the artificial reservoir, were very fecund comparing to populations from Ukraine. In our case the mean brood size was 36 (females inhabiting river) and 52 (females from the reservoir) while the mean brood size from literature ranged from 28 to 39 eggs (Briskina 1950; Gudkova and Melnikova 1969; Kurandina 1975; Kiticyna 1980). Musko´ (1993), who studied D. haemobaphes from the littoral zone of Lake Balaton (Hungary), got very different results. She found only 17 eggs in brood pouch as a mean value. She also notified the smallest females (the biggest female size was 10.3 mm) in comparison with other data. It has to be stressed that in all cases the correlation between the brood size and

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Fig. 8 Differences in body lengths and brood sizes among three generations of D. haemobaphes Table 1 Covariance analysis of three generations of breeding females of D. haemobaphes Generation

a (SE)

b (SE)

n

R2

P

Autumn (A) -2.684 (0.392) 4.059 (0.372) 42 0.75 0.0001 Spring (S)

-2.219 (1.297) 3.700 (1.276) 10 0.51 0.02

Summer (SU)

-1.467 (0.551) 2.852 (0.578) 26 0.50 0.0001

ANCOVA

F2.72 = 1.518, P = 0.226 =[ bA = bS = bSU F2.74 = 1.419, P = 0.248 =[ aA = aS = aSU

a, b constants, SE standard error, n sample size, R2 coefficient of correlation, P probability

Fig. 9 Correlation between female body length and brood size in three generations of D. haemobaphes

the female size was found. Concerning that, quite small size of females resulted in small number of laid eggs. A significant difference in size of individuals inhabiting river and water reservoir was indicated in our study. Mature specimens from the reservoir were much bigger and more fecund than those studied in the river. This could be a result of differences in predation pressure and and/or differences in hydrological conditions, i.e. water velocity (Adams et al. 1989). Moreover, we cannot exclude that those two sites may differ in nutrition level, which may

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influence the growth of individuals. Thermal conditions did not differ between both sites in all year round (own data). In our study we observe a decrease in the mean size of mature individuals and in the mean size of breeding females as well as theirs fecundity in subsequent generations from autumn (that overwinter and reproduce in early spring) through spring to summer. The same phenomenon was noticed by Kurandina (1975) and Musko´ (1993) and was also observed for other Ponto-Caspian gammarid species such as P. robustoides (Kasymov 1960; Bacela and Konopacka 2005), C. ischnus, Obesogammarus crassus (G.O. Sars, 1894), Obesogammarus obesus (G. O. Sars, 1894) (Kurandina 1975) and D. villosus (Sowinsky, 1894) (Po¨ckl 2007).

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Table 2 Fecundity and size of breeding females and all mature individuals of D. haemobaphes in two sites studied Site

Mean size of mature individuals ± SD (mm)

Mean size of breeding females ± SD (mm)

Mean brood size (min–max)

Partial fecundity (PF)

9.9 ± 7.2

10.7 ± 2.3

37 (5–98)

3.29

11.2 ± 5.7

11.4 ± 3.4

52 (7–128)

4.26

Nieszawa Murzynowo

SD standard deviation Table 3 Covariance analysis of breeding females of D. haemobaphes inhabiting two sites R2

P

Site

a (SE)

b (SE)

n

Nieszawa (N)

-2.325 (0.257)

3.732 (0.251)

68 0.77 0.0001

Murzynowo (M)

-2.709 (0.266)

4.109 (0.252)

57 0.83 0.0001

ANCOVA

F2.123 = 0.429, P = 0.514 =[ bN = bM F2.124 = 0.429, P = 0.652 =[ aN = aM

a, b constants, SE standard error, n sample size, R2 coefficient of correlation, P probability

Fig. 10 Correlation between female body length and brood size of D. haemobaphes in both sampling localities

The autumn overwintering generation seems to be not only the biggest and the most fecund, but also semelparous in contrast to spring and summer generations which produced three or even four broods. In general all gammarid species studied are known to be iteroparous (Sainte-Marie 1991) so every female can produce few broods in its life. Mordukhai-Boltovskoi (1949), who did some

laboratory experiments on D. villosus and C. ischnus showed that one female can produce three to four broods in its life-time. However, the analysis of population size structure in subsequent samples and the analysis of cohorts’ appearance showed that the overwintering females produced only one brood. This phenomenon was also observed for P. robustoides (Bacela and Konopacka 2005) as well as for some other invertebrates that overwinter as larvae or mature individuals (Steele and Steele 1986). In our study the presence of intersexes in D. haemobaphes were noticed for the first time ever. In general, the phenomenon is not unusual for gammarids and it was noticed in several freshwater ¨ kland 1969; Zielinski species before (Hynes 1955; O 1998). This can be induced by several causes: parasites (Dunn and Hatcher 1997), temperature and light conditions (Dunn et al. 1996) or/and water pollution (Ladewig et al. 2002; Jungmann et al. 2004). In our study three intersexes had eggs in their marsupium and the brood size was twice smaller than observed in females of the same size. The much lower fecundity had been already observed by Dunn et al. (1990) and Ford et al. (2003). We can expect that increasing number of intersexes in population can strongly influence the reproductive effectiveness of the population. However, very few specimens with both female and male secondary sexual features were observed in our investigation and in general it did not have any influence on the population structure. Dikerogammarus haemobaphes inhabiting the Vistula River has a life history typical to gammarids from Ponto-Caspian complex (as defined by Stock 1974) with 2–3 generations per year, each of 3–5 cohorts with mean broods of 20–50 eggs (Mordukhai-Boltovskoi 1949). D. villosus, P. robustoides, C. ischnus and C. curvispinum are also members of that complex. Moreover, all the above mentioned species are nowadays invasive in central and western Europe.

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2064 Table 4 Partial fecundity (PF) and maturity index (Mind) for native, alien and alien invasive species of gammarids occurring in European fresh waters (modified after Grabowski et al. 2007a, b)

K. Bacela et al.

Species

PF

Mind

Source

Gammarus fossarum

1.66

0.79

Brzezinska-Blaszczyk and Jazdzewski (1980)

1.85

0.72

Ladewig et al. (2006)

1.41

0.73

Bacela (2007)

Gammarus varsoviensis

1.86

0.74

Konopacka (1988)

Gammarus balcanicus

0.87

0.84

Zielinski (1995)

Gammarus pulex

1.66

0.88

Hynes (1955)

Gammarus lacustris

1.66

0.71

Hynes (1955)

Gammarus leopoliensis Gammarus roeseliia

1.78 2.10

0.79 0.68

Zielinski (1998) Bacela (2007)

4.42

0.50

Chambers (1977)

Gammarus tigrinusb Dikerogammarus villosus

a b

b

4.45

0.57

3.87

–

Mordukhai-Boltovskoi (1949), Kley and Maier (2003), Devin et al. (2004), Po¨ckl (2007)

Obesogammarus crassusb

2.87

0.68

Kurandina (1975)

Chaetogammarus ischnusb

2.56

0.64

Mordukhai-Boltovskoi (1949), Kurandina (1975), Konopacka and Jesionowska (1995)

Pontogammarus robustoidesb

5.10

0.63

Dikerogammarus haemobaphesb

3.90

0.57

3.21

0.67

4.57

0.70

Dedju (1967), Kasymov (1960), Bacela and Konopacka (2005) Kurandina (1975), Musko´ (1993), own data (Nieszawa), own data (Murzynowo)

Alien species Alien invasive species

In comparison to natives all those invasive species are characterised by very high fecundity (in some cases even three times higher than in natives), fast growth of individuals and attaining the maturity early in the life-span (Table 4). Such features may promote the invasion. Additionally, D. haemobaphes has a relative short time of embryonic development. At temperatures ranging from 10 to 13°C it took around 3 weeks since fertilisation of eggs to leave the brood pouch by offspring. Po¨ckl (2007) got similar results for D. villosus in a similar thermal regime. It has to be stressed that embryological development time of native G. fossarum at the same temperatures is around 40 days (Po¨ckl and Humpesch 1990). Comparing D. haemobaphes to other invasive species such as D. villosus and P. robustoides, reproductive performance of the former species is moderate. However, it should be stressed that fecundity and size of mature individuals may differ largely among sites. It suggests high plasticity of the species

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reproductive strategy. In favourable conditions D. haemobaphes may fully use its reproductive potential and be an efficient competitor for the local gammarid fauna as well as colonise quickly new areas. Van der Velde et al. (2000) defined the traits important for the success of crustacean invaders. According to these criteria, along with other invasive gammarid species, D. haemobaphes shows early sexual maturity, very high fecundity and short generation time. This may to large extent explain the rapid expansion and high abundance of the species in many European rivers. However, another important factor may be potential environmental and feeding plasticity of the species that should be a subject for future studies. Acknowledgments This research was supported by Polish Ministry of Science and Higher Education grant no. 2 P04C 090 029 and by the internal funds of the University of Lodz. We thank Professor Krzysztof Jazdzewski for his suggestions during collecting and analysing data and Professor Miroslaw Przybylski for his help in statistical analysis. We also thank Karolina Chaniecka for her help in measuring embryos.

Reproductive biology of Dikerogammarus haemobaphes

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