Ontogeny of osmoregulation of the Asian shore crab Hemigrapsus sanguineus at an invaded site of Europe

Abstract

We studied the ontogeny of osmoregulation of the Asian shore crab Hemigrapsus sanguineus at an invaded area in the North Sea. H. sanguineus is native to Japan and China but has successfully invaded the Atlantic coast of North America and Europe. In the invaded areas, H. sanguineus is becoming a keystone species as driver of community structure and the adults compete with the shore crab Carcinus maenas. Strong osmoregulatory abilities may confer the potential to use and invade coastal areas already earlier in the life cycle. We reared larvae and first juveniles at 24°C in seawater from hatching to intermoult of each developmental stage (zoea I-V, megalopa, crab I). We exposed each stage to a range of salinities (0-39 ppt) for 24 h, and then we quantified haemolymph osmolality, using nano-osmometry. In addition, we quantified osmolality in field-collected adults after acclimation to the test salinities for 6 days. Larvae of H. sanguineus were able to hyper-osmoregulate at low salinities (15 and 20 ppt) over the complete larval development, although the capacity was reduced at the zoeal stage V; at higher salinities (25-39 ppt), all larval stages were osmoconformers. The capacity to slightly hypo-regulate at high salinity appeared in the first juvenile. Adults were able to hyper-osmoregulate at low salinities and hypo-regulate at concentrated seawater (39 ppt). H. sanguineus showed a strong capacity to osmoregulate as compared to its native competitor C. maenas, which only hyper-regulates at the first and last larval stages and does not hypo-regulate at the juvenile-adult stages. The capacity of H. sanguineus to osmoregulate over most of the life cycle should underpin the potential to invade empty niches in the coastal zone (characterized by low salinity and high temperatures). Osmoregulation abilities over the whole life cycle also constitute a strong competitive advantage over C. maenas.

Keywords: Invasive species; larva; ontogeny; osmoregulation; shore crab.

Figure 1

Hemigrapsus sanguineus. OC change through time. Haemolymph osmolality was measured in zoea V (upper panel) and adults (bottom panel) after transfer from seawater (32.5 ppt) to 20 ppt (blue) and to 15 ppt (red) and 39 ppt (green), respectively. Values are shown as means ± standard error (n = 6–8 for Z V; n = 3–5 for adults for each measurement).

Figure 2

Hemigrapsus sanguineus. Variations in the haemolymph osmolality in different life cycle stages in relation to the osmolality (bottom x axis) and salinity (upper x axis) of the medium at 24°C. Acclimation time was 24 h for larval and crab I stages, and 6 days for adults. Values are shown as average values ± standard error. For zoeal stages I–III: n = 9–10, IV–V: n = 5; for megalopa: n = 6–8, for crab I: n = 4–5; for adults: n = 9–12, except for crabs exposed to < 1 ppt: n = 1, 5 ppt: n = 3 and 10 ppt: n = 6. Zoeal stages are shown in red (Z I: stars, Z II: diamonds, Z III: triangles, Z IV: squares and Z V: circles); megalopa (M) is shown in green squares; first juvenile crab (C I) is shown in light blue circles and adult is shown in dark blue circles. Note that standard errors may be smaller than symbols.

Figure 3

Hemigrapsus sanguineus. Variations in OC at different life cycle stages in relation to the osmolality (bottom x axis) and salinity (upper x axis) of the medium at 24°C. Values are shown as average values ± standard error (replicate numbers as in Fig. 2). Zoeal stages (ZI–ZV): red bars; megalopa (M): green bars; Juvenile I crabs (CI): light blue bars; adults crabs (A): dark blue bars; missing bars at < 15 ppt (434 mOsm kg⁻¹) denote 100% mortality in all larval stages; asterisks instead of bars show salinities not tested for CI.