Hydrobiologia (2007) 590:43–46 DOI 10.1007/s10750-007-0755-x
I N V A S I V E C RU S T A C E A
Invasive zebra mussel colonisation of invasive crayfish: a case study ˇ urisˇ Æ Ivona Horka´ Æ Adam Petrusek Zdeneˇk D
Springer Science+Business Media B.V. 2007 Abstract We investigated the interaction between two invasive invertebrate species in a shallow Central European flooded sandpit: the epibiosis of Ponto-Caspian zebra mussels Dreissena polymorpha on the American crayfish Orconectes limosus. Between 2004 and 2005, we followed the seasonal variation in number and size of the mussels attached to crayfish bodies, and microhabitats preferred by mussels. The proportion of crayfish colonised by mussels varied seasonally: in spring and early summer it was
consistently over 75%, afterwards it dropped temporarily due to loss of bivalves during the crayfish moult, and later increased again due to re-colonisation by often relatively large juvenile mussels. Three different pathways of mussel settlement on crayfish hosts are likely: (1) primary settlement of free-swimming pediveliger larvae; (2) secondary settlement of plantigrade mussels and juveniles; (3) active re-attachment of grown mussels from the substrate to crayfish. This epibiosis was promoted by lack of suitable substrates at the studied locality.
Guest editors: Elizabeth J. Cook and Paul F. Clark Invasive Crustacea
Keywords Zebra mussel Dreissena polymorpha Spiny-cheek crayfish Orconectes limosus Body colonisation Epibiosis
Electronic supplementary material The online version of this article (doi: 10.1007/s10750-007-755-x) contains supplementary material, which is available to authorised users. ˇ urisˇ (&) I. Horka´ Z. D Department of Biology, University of Ostrava, Chittussiho 10, Ostrava 710 00, Czech Republic e-mail:
[email protected] A. Petrusek Charles University in Prague, Faculty of Science, Department of Ecology, Vinicˇna´ 7, Prague 2 12844, Czech Republic A. Petrusek ˇ eske´ Budeˇjovice, University of South Bohemia in C Research Institute of Fish Culture and Hydrobiology at Vodnˇany, Za´tisˇı´ 728/II, Vodnˇany, CZ-38925, Czech Republic
The zebra mussel Dreissena polymorpha (Pallas, 1771) is a bivalve mollusc of Ponto-Caspian origin. During the last two centuries it has invaded large regions of Europe through rivers and artificial channels (Bij de Vaate et al., 2002), and since the end of the 1980s also North America (Johnson et al., 2006). Dispersal of zebra mussels is greatly facilitated by their life cycle, which contains planktonic stages—trochophora and veligers. The last free-swimming stage, pediveliger, actively selects a suitable hard substrate and metamorphoses into a postlarva—plantigrade mussel (Ackerman et al., 1994; Brazner & Jensen, 2000). Although shells of older zebra
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mussels or their close proximity are the most preferred locations for mussel settlement (Mo¨rtl & Rothhaupt, 2003), limited availability of substrates in habitats with dense populations of D. polymorpha leads to colonisation of alternative substrates, including mobile hard-shelled animals. During our recent (2003–2005) survey of the distribution of American spiny-cheek crayfish Orconectes limosus (Petrusek et al., 2006), we sampled approx. 60 locations in the Czech Republic. Among other cases of epibioses of invertebrates on crayfish bodies, colonisation by zebra mussels was regularly observed in the flooded sandpit Lhota (5015¢ N, 1440¢ E) but not in other localities where these two species ˇ urisˇ et al., 2006). Here we present data coexist (D on seasonal changes in quantity, size and spatial distribution of juvenile zebra mussels on the crayfish body surface and discuss possible pathways by which crayfish are colonised. We sampled crayfish eight times between June 2004 and August 2005, and noted the presence of zebra mussels on their bodies. In 2005, we focused further on the size of mussels (Table 1) and their microhabitats on crayfish. In total, we examined 108 crayfish specimens, 47 in 2004 and 61 in 2005. The frequency of colonised crayfish was strongly dependent on season in both years, exceeding 75% in spring and early summer but sharply dropping to 0–20% in August, after the crayfish moult. In August 2004, no mussel life stages were
recorded on 25 examined crayfish, but by the end of September and in October 2004, some specimens of plantigrade stage (0.33–0.41 mm of the longest shell axis) and early juveniles (0.65– 1.40 mm long) were already found on the crayfish. In April 2005, we observed a higher level of mussel infestation (15 out of 16 examined crayfish colonised, carrying up to 33 mussels per host), which lasted until July (11 out of 14 crayfish colonised, up to 37 mussels per host). The particularly high variability in the mean number of mussels per host in July 2005 (Table 1) was caused by the coexistence of heavily infested and freshly moulted crayfish. The seasonality in the zebra mussel epibiosis may at least partly explain the high variation of colonisation frequency in previous causal reports of this phenomenon (see online supplementary table). Although zebra mussels were occasionally found on most parts of crayfish bodies, the most preferred microhabitats for their attachment were (1) the ventral surface of the abdomen, especially the hollows under abdominal pleurae (35–45% of mussel individuals in April to July), (2) the anterior dorsal region of the carapace among spines and in the cervical groove (20–24%), and to a lesser extent (3) the ventral cephalothorax including the mouth region (19% in April and 17% in July) and (4) chelipeds (18% in June). In general, microhabitats on the ventral side of crayfish were slightly more preferred over the dorsal surface (Table 1).
Table 1 Number and sizes of zebra mussels attached to crayfish collected in 2005. Variability is expressed as mean ± SD
No of crayfish examined Proportion of colonised crayfish Total no of mussels Mean no of mussels per host Mussels on dorsal side of the host Mussels on ventral side of the host Size classes of mussels [n] S (10 mm) Mean mussel length [mm] Total On dorsal side On ventral side
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April 28
June 09
July 16
August 18
16 94% 157 9.81 ± 10.5 35% 65%
13 83% 55 4.23 ± 4.35 41% 59%
14 79% 84 5.07 ± 9.26 37% 63%
18 17% 3 0.17 ± 0.37 100% –
40 116 0 1
8 40 4 3
15 40 15 1
0 0 3 0
2.11 ± 1.27 2.13 ± 0.72 2.09 ± 1.5
3.8 ± 3.06 4.82 ± 3.89 2.78 ± 1.16
3.47 ± 2.31 4.58 ± 2.06 2.86 ± 2.23
2.56 ± 0.6 2.56 ± 0.6 –
Hydrobiologia (2007) 590:43–46
Median Median 25%-75% 25%-75% 25%-75% Non-Outlier Non-outlierRange Range Range Outliers Outliersand and extremes extremes
16 16 14 14
mussel shell length [mm]
Fig. 1 Length of zebra mussels attached to collected crayfish in 2005. Results for all measured mussels and partitioning between the dorsal and ventral host body surfaces is shown. Bars on the right indicate the size classes of attached mussels
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XL
12 12 10 10 88
L 66
44
M 22
S 00 total total
April
June
The majority of zebra mussels attached to crayfish were small, below 5 mm long; this corresponds to juveniles less than one year old (Ackerman et al., 1994; Garton & Johnson, 2000). However, some specimens were much larger, reaching a shell length over 10 mm (up to 16 mm in June 2005; Fig. 1); these represented older individuals, which must have actively reattached to crayfish from other substrates. Nevertheless, this large size class of attached mussels was mostly smaller than the typical size of 1-yearold mussels, 15–17 mm, reported by Garton & Johnson (2000). This might have been caused either by a prolonged period of pediveliger settlement or by generally slower mussel growth rates in the Lhota sandpit (due to, e.g., inadequate food supply). The average length of all specimens, excluding the largest ones over 10 mm long, was 2.1 mm in April, 3.1 in June and 3.5 in July; this increase in size suggests the successful growth of mussels carried by crayfish hosts. However, we also observed an increasing tendency for size differences between mussels attached to dorsal and ventral sides of crayfish during the 2005 season (April: means 2.13 and 2.09 mm, respectively; P = 0.44; June: 4.82 vs. 2.78 mm, P = 0.037; July: 4.58 vs. 2.86 mm, P < 0.001; all P-values determined by the Mann–Whitney U test). This
July
dorsal ventral dorsal dorsal ventral ventral April
dorsal dorsal dorsal ventral ventral ventral
June
dorsal dorsal dorsal ventral ventral ventral
July
significant difference in summer may reflect crayfish cleaning behaviour, possibly leading to more efficient selective removal of larger epibionts from the host’s ventral side. Alternatively, faster growth of mussels on the dorsal crayfish side may have been caused by better exposure of the filter-feeding mussels to water with their phytoplankton food. The main pathway by which the crayfish bodies are first colonised by zebra mussels is the settlement of planktonic larvae (postlarvae were found on crayfish caught in autumn 2004 as well as in summer 2005). However, as the postlarvae are lost during the summer crayfish moult, the translocation of larger juveniles from the substrate (Toomey et al., 2002) likely plays a significant role (mussels several mm long were found on a few recently moulted crayfish in July 2005). The grown mussels’ ability to actively detach from the original substrate and re-attach to the host body was clearly demonstrated by records of large specimens, e.g., in April or June 2005. The colonisation of crayfish bodies by zebra mussels is certainly an unusual phenomenon, although it has been occasionally recorded (see online appendix). To occur more generally, a combination of two conditions is needed: syntopy of the two species, and a strong limitation in other, more preferred, types of hard substrates.
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If such conditions are fulfilled, the proportion of affected hosts may be very high, and in case of heavy infestations, (e.g., Sebestye´n, 1938; Brazner & Jensen, 2000), adverse effects of epibiotic mussels on the crayfish hosts are possible. Acknowledgements Our research was supported by the Czech Science Foundation (project GACˇR 206/03/0532) and the Czech Ministry of Education (MSM0021620828 and MSM6007665809). We thank Jirˇı´ Kristian, Tereza Petruskova´ and Lenka Filipova´ for field assistance.
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Hydrobiologia (2007) 590:43–46 Orconectes limosus in the Czech Republic. Bulletin Franc¸ais de la Peˆche et de la Pisciculture 380–381: 1325–1337. Garton, D. W. & L. E. Johnson, 2000. Variation in growth rates of the zebra mussel, Dreissena polymorpha, within Lake Wawasee. Freshwater Biology 45: 443– 451. Johnson, L. E., J. M. Bossenbroek & C. E. Kraft, 2006. Patterns and pathways in the post-establishment spread of non-indigenous aquatic species: the slowing invasion of North American inland lakes by the zebra mussel. Biological Invasions, 8: 475–489. Mo¨rtl, M. & K.-O. Rothhaupt, 2003. Effects of adult Dreissena polymorpha on settling juveniles and associated macroinvertebrates. International Review of Hydrobiology 88: 561–569. ˇ urisˇ, I. Horka´, P. Koza´k, T. Petrusek, A., L. Filipova´, Z. D Policar, M. sˇtambergova´ & Z. Kucˇera, 2006. Distribution of the invasive spiny-cheek crayfish (Orconectes limosus) in the Czech Republic—past and present. Bulletin Franc¸ais de la Peˆche et de la Pisciculture 380–381: 903–918. Sebestye´n, O., 1938. Colonization of two new fauna-elements of Pontus-origin (Dreissensia polymorpha Pall. and Corophium curvispinum G. O. Sars forma devium Wundsch) in Lake Balaton. Verhandelungen der Internationalen Vereinigung fu¨r theoretische und angewandte Limnologie 8: 169–182. Toomey, M. B., D. Mccabe & J. E. Marsden, 2002. Factors affecting the movement of adult zebra mussels (Dreissena polymorpha). Journal of the North American Benthological Society 21: 468–475.
