Crustaceans and the biodiversity crisis: proceedings of the Fourth International Crustacean Congress,

Amsterdam, The Netherlands, July 20-24, 998: vol. 1; p. 458-472

Growth and production of Corophium curvispinum G.O. Sars, 1895 (Amphipoda), an invader in the Lower Rhine

Rajagopal S.1, G. van der Velde1, B.G.P. Paffen1 & A. bij de Vaate2

1) Department of Ecology, Laboratory of Aquatic Ecology, University of Nijmegen, P.O. Box 9010, NL-6500 GL Nijmegen, The Netherlands 2) Institute for Inland Water Management and Waste Water Treatment, P.O. Box 17, NL-8200 AA Lelystad, The Netherlands

ABSTRACT

The tube-building amphipod, Corophium curvispinum was sampled from stones at two locations (Lobith and Nijmegen) on the lower Rhine between March 1992 and February 1994. Highest densities were re-corded from June to September and showed a strong, positive correlation with water temperature. Growth rate was also strongly correlated with water temperature and displayed a distinct seasonal pat-tern, with maximum growth (up to 1.3 mm month-1) in summer months. Seasonal population biomass and production fluctuations were similar to those of density, showing high values during June to September. The annual production and mean biomass ratio varied from 2.7 to 3.5. Population density, biomass, and production were much higher at Nijmegen than at Lobith, possibly due to higher stream velocities at Nij-megen. Our results indicate that water temperature and stream velocity can be regarded as important fac-tors in relation to biomass, growth, and production of C. curvispinum.

INTRODUCTION

Corophium curvispinum G.O. Sars, 1895 was first recorded in the River Rhine in 1987 (Van den Brink et al., 1989; Schöll, 1990). Originating from the Ponto-Caspian region of Eastern Europe, С. curvispinum's westerly range expansion has been aided by shipping traffic and canalization of river systems. Due to their tube building, C. curvispinum changes the settled surface (e.g., stones, wooden piles, and macro-phytes) by introducing mud and thereby prevents the development of other competitors (Van der Velde et al., 1999). It is a filter-feeder and food mainly consists of phytoplankton and detritus (Van den Brink et al., 1993). Even though large numbers of euryoecious and exotic species have invaded the River Rhi-ne, C. curvispinum is more successful than any other invader (Van den Brink et al., 1991; Van der Velde et al., 1998). The success of C. curvispinum has been attributed to increased salinity (annual mean: Cl-: from 13 mg 1-1 in 1900 to 200 mg 1-1 in 1990) and water temperatures (annual mean: from 10.9°C in 1900 to 16.1°C in 1990) of the lower Rhine caused by mining activities and industrial pollution (Den Hartog et al., 1989, 1992). The population densities, reproductive capacity and general ecological impacts of С. curvispinum are much higher in the River Rhine (Van der Velde et al., 1994; Rajagopal et al., 1999) than those reported from elsewhere (Behning, 1925; Sebestyén, 1934; Entz, 1947; Wouters, 1985; Waterstraat & Kohn, 1989; Schöll, 1990; Muskó, 1992). С. curvispinum has also been reported to have had an enormous impact on the River Rhine ecosystem by changing food webs and energy fluxes (Kelleher et al., 1998; Marguillier et al., 1998; Van der Velde et al., 1998).

Despite much literature regarding its extension over Europe (for review see Jazdzewski, 1980; Van der Velde et al., 1999), very little is known of the population ecology of C. curvispinum. The life history of C. curvispinum has been documented by Rajagopal et al. (1999) in the lower Rhine and by Musko (1992)

in Lake Balaton, Hungary. The physiology of С. curvispinum has been studied by Taylor & Harris (1986), Bayliss & Harris (1988), Harris & Bayliss (1990), Musko et al. (1994) and Harris & Aladin (1997). No study of C. curvispinum to date has described the seasonal production of this species. The aim of the present study was to determine seasonal changes and annual values of biomass, growth, and production of С. curvispinum in relation to key environmental conditions.

MATERIALS AND METHODS

S i t e d e s c r i p t i o n

The present investigation was carried out at Lobith and Nijmegen in the lower Rhine from March 1992 to February 1994 (fig. 1). The river bed of the lower Rhine and its branches are generally fixed by groynes, breakwaters which consist of large basalt stones (grauwacke). The river bed largely consists of heavily disturbed shifting sands and small quantities of vegetation are only present in the calmer downstream reaches. Water levels vary annually and seasonally, but are generally lowest in September and October.

H y d r o g r a p h i c c o n d i t i o n s

Data on physico-chemical parameters (temperature and chlorophyll-a) were obtained from Rijkswater-staat/RIZA, Lelystad and from RIWA, Amsterdam, The Netherlands. Stream velocities at Lobith and Nijmegen were measured on 23 October 1995 by a flow meter (TAD-Micro-W 16) for the sake of com-parison.

F i e l d p r o c e d u r e s

The stones from groynes at Lobith and Nijmegen were sampled from a vessel at monthly intervals by means of a polyp-grab operated with a hydraulic crane. Water depth (4 to 5 m) was measured at each sampling location using an Atlas DESO 25/SLS instrument. The various macroinvertebrates were sampled by carefully brushing the collected stones. Per locality, three to five stones were sampled each month. All materials collected from stones were preserved in 70% ethanol for further analysis. The den-

sity per surface area of these stones was estimated by using the following equation of Bij de Vaate & Greijdanus-Klaas (1991):

D = (ΣN /ΣA ) x 1 0 , 0 0 0

where, D = the number of animals m-2, Σ A = the sum of mean surfaces (in cm2) of all sides of stones, Σ N = the sum of animals on all sides of stones and 10,000 = the conversion factor.

L a b o r a t o r y a n a l y s i s

The preserved samples were transported to the laboratory in polyethylene bottles and sieved for the separation of macroinvertebrates. Three mesh sizes viz., 0.5 mm, 1 mm, and 2 mm were used for sieving. The small mesh size of 0.5 mm was chosen since the body length of newly hatched juveniles of С. cur-vispinum is about 550 µm (Rajagopal et al., 1999). The number of C. curvispinum in each sample was counted and calculated for the average numbers per square metre from three to five stones. When samples were very large (> 1000 individuals), a sub-sample was taken for measuring length-frequency distribution. The body length of all specimens was measured to the nearest 0.05 mm from the anterior margin of the rostrum to the posterior margin of the telson using a micrometer mounted on a binocular microscope. The sex of all specimens above a body length of 1.8 mm was recorded using the presence (male) or absence (female) of genital apophyses on the ventral face of peraeon somite VII. Individuals less than 1.8 mm in length were considered as juveniles as it was impossible to determine their sex. The presence of males, ovigerous and pre-ovigerous females, and juveniles was recorded for each sample.

G r o w t h r a t e

The weight/length specific growth rate (Gwp) was obtained using the following equation (Winberg et al., 1971):

G w p = ( l / t ) l n ( B 2 / B 1 )

where, t is the interval between sampling dates in days, B1 is the biomass at the beginning of the samp-ling interval and B2 is the biomass at the end as projected by the growth model.

Mean lengths of different generations of C. curvispinum were also estimated from the length-frequ-ency tables based on the increment of mean length of each cohort between subsequent samples during the months.

B i o m a s s

Biomass of C. curvispinum was calculated from a regression between body length (L) and ash-free dry weight (AFDW). The weights of different size groups (0.5-1.0, 1.5-2.0, 2.5-3.0, 3.5-4.0, 4.5-5.0, 5.5-6.0, and 6.5-7.0 mm) of С. curvispinum were obtained using unpreserved animals (n = 50-100 for each size group), which were dried at 60°C to constant weight for 2 days and ashed at 550°C for 5 hours to calculate the mean weight per individual of that size group. To calculate population biomass, length frequency tables were constructed from the length-percentage frequency (ovigerous females and other individuals) and population density data for each month. Quantitative estimations were made by applying length-weight conversion relations to individuals of all size classes observed for each month.

P r o d u c t i o n

The production of C. curvispinum was estimated according to method 3А in Crisp (1971):

where, n is the number of size classes, fi is the mean number of individuals in the size class i in the time period Δt, wi is the mean weight of individuals belonging to the size class i, and Gi is the weight-specific growth rate of the size class i during Δt.

Production biomass ratio (P/B) was calculated from the annual total production and annual mean biomass.

S t a t i s t i c a l a n a l y s i s

The differences in population density, biomass, growth, and production of С. curvispinum between Lo-bith and Nijmegen were compared by Student's t-tests (Sokal & Rohlf, 1981). Stream velocity data col-lected from Lobith and Nijmegen were compared by using non-parametric Wilcoxon-Signed Rank Test (Zar, 1984). Data from each sample interval at Lobith and Nijmegen were analysed and assigned a rank to make statistical comparison, independent of seasonal variation. The standard regression equation was used to relate density and growth of C. curvispinum with water temperature (Sokal & Rohlf, 1981).

RESULTS AND DISCUSSION

H y d r o g r a p h i c c o n d i t i o n s

During the study period (March 1992-February 1994), temperature and chlorophyll-a values varied bet-ween 5.6°C (February 1994) and 24.0°C (August 1992) and 1 µg 1-1 (January 1994) and 72 µg 1-1 (April 1993), respectively. Stream velocities on 23 October 1995 were 42.5 ±5.1 cm sec-1 (mean ± SD; range = 31 -51, n = 35) at Lobith and 51.3 ± 6.2 cm sec-1 (mean ± SD; range = 39-63, n = 35) at Nijmegen.

P o p u l a t i o n d e n s i t y

The highest Corophium curvispinum densities were observed between June and September and the lo-west densities were recorded between October and March (fig. 2a). Following initial release of young animals in late May, densities increased steadily from May to August. A drastic decline in densities was observed from September to April. Densities of C. curvispinum were strongly correlated with water tem-perature (Lobith: у = 2018.09 e0.148x, r = 0.78, P < 0.0001; Nijmegen: у = 4391.92 e0.127x, r = 0.70, P < 0.0001) (fig. 3).

The highest mean density of 168,100 ± 27,495 individuals m-2 (mean ±SE, n = 5) was recorded at Lo-bith in July 1993 (fig. 2a). The corresponding value for Nijmegen was 146,900 ± 11,826 individuals m-2 in July 1993. However, a significant difference in population densities of C. curvispinum was observed between Lobith and Nijmegen from May 1992 (t-tests, P < 0.05) to August 1992 (t-tests, P < 0.001) and from October 1993 (t-tests, P < 0.001) to December 1993 (t-tests, P < 0.05), with mean densities higher

at Nijmegen than at Lobith. This is possibly related to stream velocities which were significantly higher at Nijmegen than at Lobith (Wilcoxon-Sign, P < 0.05). A high stream velocity favours C. curvispinum by transporting silt and planktonic algae along with oxygen which are necessary means for its meta-bolism (Musko et al., 1994; Van der Velde et al., 1998). The mean density of С. curvispinum was higher in than in 1992. In comparison, chlorophyll-a values were also higher and more long lasting in 1993 than in 1992 (mean values: 14.8 µg 1-1 for 1992 and 19.7 µg 1-1 for 1993).

The present density values of C. curvispinum in the lower Rhine were high when compared to litera-ture values reported from other regions. The population densities of 100,000 individuals m-2 from the Ri-ver Rhine in Germany (Scholl, 1990), 97,552 individuals m-2 from the River Mosel at Grevenmacher in France (Bachmann et al., 1995), 3000 individuals m-2 from the River Ingulez, USSR (Bortkewitch, 1987), 8600 individuals m-2 from Lake Balaton in Hungary (Musko, 1989), 167,640 individuals m-2 from the River Oka (Shadina & Liakhov, 1941), and 10,000 individuals m-2 from the river Don in the USSR

(Harris & Bayliss, 1990) were reported. The differences in population densities of C. curvispinum from various waters might be related to differences in the amount of food availability, salinity, flow velocity, pollution, etc. Food conditions in the heavily eutrophic lower Rhine may be relatively better because of a continuous supply of phytoplankton and suspended organic material provided by the flow of the river to this filter-feeding amphipod.

G r o w t h r a t e

Growth of C. curvispinum was calculated by following the modes of the size-frequency histograms. The first generation of young individuals appeared in the samples during May (fig. 4). These young animals mature rapidly to reproduce in summer, and are responsible for the subsequent generations of July and September (refer to Rajagopal et al., 1999). This conclusion is also supported by the disappearance of the overwintering population in June. However, in July and September, when the second and third generati-ons appeared, some overlap among the three generations occurred. In comparison, the most rapid growth (up to 1.3 mm month-1 during May-July) was recorded in the first generation, which can be explained as a result of prevailing high temperatures and high chlorophyll-a concentrations (fig. 5). At the end of Oc-tober, the mean growth of С. curvispinum slowed down considerably until the following January. The overwintering population (second and third generations) had a maximum mean growth of < 0.1 mm month-1 during November to February (fig. 5). Monthly mean growth rate was positively correlated with water temperature (y = -0.289 + 0.062x. r = 0.88. P < 0.0001) (fig. 6). Chlorophyll-a values were increa-sed from May to June, and coincided with the increasing growth rate (fig. 5). Although perhaps less im-portant than temperature, food may be a significant factor initiating the high growth rate in filter-feeders including С. curvispinum.

B i o m a s s

A linear relationship was found between the body length (mm) and AFDW (µg) of ovigerous females (In AFDW = -4.242 + 0.480 In L, r2 = 0.83, P < 0.001, n = 205, size range = 2.2-7.1 mm, fig. 7) and other individuals (In AFDW = -4.284 + 0.462 In L, r2 = 0.97, P < 0.001, n = 265, size range = 0.8-7.2 mm). No significant difference in AFDW was observed between the males and pre-ovigerous females (t-tests, P > 0.05). However, there was a significant difference in biomass between ovigerous females and other individuals (including males and pre-ovigerous females) (t-tests, P < 0.001, table I). In table I, the read-ings were corrected for uniform body length by excluding juveniles for better comparison.

As with density, biomass was higher in 1993 than in 1992 (table II). Biomass patterns were similar to those of density, showing higher values during June-September (fig. 2b). Monthly biomass values varied from 11 (March 1992) to 13,384 mg AFDW m-2 (July 1993) at Lobith, and from 17 (March 1992) to 11,431 mg AFDW m-2 (July 1993) at Nijmegen. However, annual mean biomass values were higher at Nijmegen (2901 mg AFDW m-2 during March 1992-February 1993 and 4091 mg AFDW m-2 during March 1993-February 1994) than at Lobith (1690 mg AFDW m-2 during March 1992-February 1993 and 3176 mg AFDW m-2 during March 1993-February 1994).

P r o d u c t i o n

The highest production of Corophium curvispinum was recorded between June and October (fig. 2c), when high temperature prevailed. Higher population densities and growth rates (first and second gene-ration individuals) were also noticed during this period. Consequently, the predominant proportion of the annual production (> 85%) occurred from July to September (table II). Production was significantly lo-wer from November to May, accompanied by > 80% decline of summer time densities (July-September). Peer et al. (1986) reported that the proportion of the production contributed by the young of the year did not form a smoothly increasing proportion of the population as a result of frequent death of older animals in a Comphium volutator (Pallas, 1766) population at Chignecto Bay, Canada. Production was estimated from both density and weight-specific growth rate of size classes. These two parameters are generally prone to a lot of spatial variability of environmental factors. Rajagopal et al. (1999) reported that brood size of C. curvispinum was significantly higher at Nijmegen than at Lobith due to higher stream velocity. This may explain the variation in the production of C. curvispinum during different seasons at Lobith and Nijmegen.

Monthly production of C. curvispinum ranged from 1 (January 1993) to 2792 mg AFDW m-2 (August 1993) at Lobith, and from 1 (March 1992) to 3176 mg AFDW m-2 (August 1993) at Nijmegen during March 1992-February 1994 (fig. 2c). Annual production values were always higher at Nijmegen than at Lobith (table II). No significant difference was observed in water temperature and chlorophyll-a values between Lobith and Nijmegen. However, the stream velocity was significantly higher at Nijmegen than at Lobith (Wilcoxon-Sign, P < 0.05).

Annual production and mean biomass ratio (P/B) varied between 2.7 and 3.5. Bortkewitch (1987) re-corded a P/B ratio of 5.2 for C. curvispinum (3 generations per year with maximum density of 3,000 in-dividuals m-2) during the vegetation period in the River Ingulez, USSR. However, no annual P/B ratio was reported. P/B ratios of about 2 to 6 were reported in the literature for Corophium volutator (P/B ratio = 3-4, Birklund, 1977; P/B ratio = 4-6, Peer et al., 1986), Corophium insidiosum Crawford, 1937 (P/B ratio = 3-5, Birklund, 1977) and some other amphipods, Ampelisca brevicornis (Costa, 1853) (P/B ratio = 3-4, Klein et al., 1975) and Hyalella azteca (Saussure, 1858) (P/B ratio = 3.2, Cooper, 1965). The different methods used for calculating production in the different areas and different species make a comparison difficult. However, the present P/B ratio of С. curvispinum was in the same range as found in similar investigations on other Corophium species as well as other amphipod species.

CONCLUSIONS

Corophium curvispinum is highly productive in the lower Rhine, displaying a short life span (about 9 months), rapid growth, early maturity (about 4 weeks), production of several generations per year (3 ge-nerations), and high fecundity (Rajagopal et al., 1999). Population density, growth rate, biomass, and production are highest during June-September. Water temperature seems to be the most important factor in relation to biomass, growth, and production of C. curvispinum in the lower Rhine.

ACKNOWLEDGEMENTS

We are thankful to M. J. E. Orbons, M. G. Versteeg, F. M. J. Oosterbroek, and to students for their assis-tance in the field and the laboratory. Thanks are due to B. Kelleher for useful discussions. This research was financially supported by the Ministry of Transport and Public Works, the Ministry of Physical Plan-ning and Environment Directorate, the Netherlands Organization of the Advancement of Pure Research (BION), and the Beijerinck-Popping Foundation.