Mar Biol DOI 10.1007/s00227-007-0777-y
R ES EA R C H A R TI CLE
Larval mortality during export to the sea in the Wddler crab Uca minax Renae J. Brodie · Richard Styles · Stephen Borgianini · Jenice Godley · Khayree Butler
Received: 5 November 2006 © Springer-Verlag 2007
Abstract Dense populations of the Wddler crab Uca minax (Le Conte 1855) are common along tidally inXuenced freshwater rivers and streams >50 km from the sea. Adults do not migrate from inland sites to release larvae, but instead release them directly into an environment where the zoeae cannot survive. Laboratory salinity tolerance experiments were used to determine how long larvae from the inland-most population of U. minax along the Pee Dee River, South Carolina, USA can survive zero salinity compared to larvae from a brackish water population (salinity 5) near the mouth of Winyah Bay in the same estuary. Larvae from the brackish water population were also exposed to a salinity of 5 and their survival tracked. These experiments were conducted from May to August 2004 and 2005. To determine if inland larvae suVered signiWcant mortality in transit due to salinity stress, current proWles were measured in the Weld and used to model the time taken by a larva using ebb-tide transport to travel to permissive salinities. The laboratory tolerance experiments showed that
R. J. Brodie (&) Department of Biology, Mount Holyoke College, 50 College Street, South Hadley, Massachusetts 01075, USA e-mail:
[email protected] R. Styles Department of Geological Sciences and Marine Science Program, University of South Carolina, Columbia, SC 29208, USA S. Borgianini · J. Godley Department of Biological Sciences, University of South Carolina, Columbia, SC 29208, USA K. Butler University of Maryland School of Medicine, 655 W. Baltimore Street, Baltimore, MD 21201, USA
larvae from the inland freshwater population had LT50’s of 4–5 days at 0 salinity, which were signiWcantly longer than those of the brackish water zoeae (2–3 days). Zoeae from the brackish water population survived for at least one larval molt at a salinity of 5 with LT 50’s of »12 days. Estimated travel times to reach permissive salinities from the inland-most population based on current proWles were 3–5 days for larvae using night-time only ebb-tide transport and 1.5–2.5 days for those using ebb-tide transport both day and night. Previously published Weld data indicate that U. minax larvae do use both day- and night-time ebb-tide transport, and are found in high densities in the water column during the day. These results lead to the conclusion that U. minax stage I zoeae do not undergo signiWcant salinity-induced mortality during their 50+ km trip to the sea.
Introduction Decapod crustaceans have complex lifecycles, typically involving a benthic adult stage and planktonic larval stages. In the marine environment, larvae released by benthic adults swim up into the water column and remain there throughout development, returning to the benthos to settle and metamorphose. In some taxa, however, adult stages have invaded non-marine habitats in freshwater or on land, necessitating a potentially hazardous trip between larval and adult habitats. For terrestrial crustaceans with marine planktonic development, adults leave inland habitats and migrate to the shore where larvae are released into the surf zone (De Wilde 1973; Ameyaw-AkumW 1989). In crustaceans occupying freshwater habitats, larvae are hatched in freshwater and migrate down-river to the coastal ocean (Saigusa and Hidaka 1978; Anger et al. 1990), or are
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delivered to the marine plankton by adults that migrate to the mouths of estuaries for larval release (Tankersley et al. 1998; Herborg et al. 2003). In all of these cases, young decapods must Wnd their way back to adult habitats after development, often traveling long distances and through a range of physico-chemical conditions until they encounter the appropriate environmental cues that trigger settlement and metamorphosis (Crisp 1974; Crisp 1976). In this study, we investigated larval mortality due to low salinity stress in newly hatched larvae of the Wddler crab Uca minax. Like other Wddler crabs, U. minax is a euryhaline species; however, dense populations of adults are found more than 50 km from the sea along the banks of tidally inXuenced freshwater streams and rivers at our Weld site in South Carolina (personal observation). This distribution is atypical for Wddler species, which generally prefer brackish or marine salinities (Crane 1975). In South Carolina, larvae are released into the water column in freshwater adult habitats on nocturnal spring tides during the months of May through September. The hatchlings actively swim near the surface during ebb tides to move down-estuary (R. Tankersley, personal observation) and presumably into coastal marine waters where development continues. U. minax larvae pass through Wve zoeal stages, then metamorphose into megalopae, which enter an estuary and actively swim during nocturnal Xood tides to move inland where settlement and a second metamorphosis occurs. Invertebrate larvae face high mortality due to predation, starvation, and transport by ocean currents away from suitable settlement sites (e.g., Thorson 1950; Young and Chia 1987). Additional mortality due to extreme salinity stress in freshwater would impose an even greater burden on the early life stages of U. minax, potentially limiting the range expansion of this species into freshwater systems. We conducted tolerance experiments on newly hatched larvae at 0 and 5 salinity to determine how long they could survive these low salinity conditions. We also measured current proWles and used those data to calculate the time it would take a larva to travel to the sea from the inland-most edge of U. minax’s range along the Great Pee Dee River, South Carolina. By combining the results of the physiological tolerance experiments with the measurements of Xow conditions in the Weld, we tested the hypothesis that larvae of this species hatched into potentially lethal freshwater environments do not suVer additional mortality due to low salinity stress in transit to the coastal ocean.
Materials and methods Salinity tolerance experiments Ovigerous females of Uca minax (Le Conte 1855) were collected during May–August 2004 and 2005 from the
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Bates Hill Plantation (33°34⬘ 26.82⬙ N; 79°09⬘ 58.99⬙ W) and from under the old Hwy 17 bridge (33°22⬘ 12.34⬙ N; 79°16⬘ 00.19⬙ W) on the Great Pee Dee River, South Carolina, USA (Fig. 1). The Bates Hill plantation site is 53 km from the mouth of Winyah Bay when accessed by water and although this area experiences tidal Xuctuations, salinity is 0, year-round. Salinity is generally around 5 at the old Hwy 17 bridge site, but can drop to 0 following rain storms and rise to 10 during dry periods. This site is 18 km from the mouth of Winyah Bay. Populations of adult U. minax exist at both locations, however, the Bates Hill Plantation population is near the end of the inland range and U. minax is rarely seen beyond the oxbow upriver of this site. Hereafter, the Highway 17 Bridge site will be referred to as the “brackish water site” and the population of crabs located there as the “brackish water population”, while the Bates Hill Plantation site and population will be denoted as “freshwater”. Ovigerous females were brought to the Baruch Marine Field Laboratory, Georgetown, South Carolina and placed in pyrex dishes Wlled with water of either 0 or 5 salinity and incubated at 27°C. Beginning 1–2 h before the nocturnal high tide, females were checked every 15 min until they released larvae, which were placed in experimental containers to determine their tolerance of salinities of 0 and 5 (Fig. 2). One hundred actively swimming larvae from the spawn of individual females were assigned to treatment and control groups (N = 50 per group). Within each group, ten larvae were placed into each of Wve pyrex dishes Wlled with 50 ml of water. River water was Wltered through Fisherbrand® 1.6-m glass Wber Wlters to eliminate silt and combined with sand Wltered seawater (to 50-m) to obtain salinities of 0–25. Larvae in the experimental group were given water at the same salinity as that into which they were hatched—either 0 or 5—while larvae in the control group were changed every hour into water with a stepwise salinity increase of 5, until a salinity of 25 was reached. In this way, the control group conditions mimicked the experience of larvae moving from low salinity or freshwater habitats to brackish areas near the mouth of the estuary. Also, a salinity of 25 is within the optimal range for larval development for this species (Morgan 1987). All larvae were kept at 27°C, a temperature well within the range of surface water temperatures at Oyster Landing, North Inlet Estuary, where mean monthly temperatures were 26–29°C during May–August 2004 and 22–29°C during May–August 2005 (North Inlet-Winyah Bay National Estuarine Research Reserve long term data set). The light regime was 12 h light: 12 h dark and the rearing containers were not agitated. Survival in the experimental and control groups were assessed every 6 h in the 0-salinity experiment and every 12 h in the 5-salinity experiment. Larvae were recorded as
Mar Biol Fig. 1 Sampling locations along the Great Pee Dee river in the Winyah Bay Estuary, South Carolina. The freshwater population of U. minax was located at Site A, adjacent to Bates Hill Plantation. The brackish water population of Uca minax was located at Site B, under the old Highway 17 bridge. An acoustic doppler current proWler (ADCP) was also deployed at Site A. The limit of salt intrusion is indicated with a hat symbol near Site B
79°12'0"W 33°36'0"N
33°36'0"N A
B
an
W ac c
At l an t ic
Pe e
Oc e
De
e
am
aw
ck la
33°24'0"N
^_ Sampi t
33°24'0"N
B
North Inlet
W in ya h
Ba y
-
33°12'0"N
33°12'0"N
0 1 2 3 4 Kilometers
79°12'0"W
Newly hatched zoeae from single brood
Experimental
Control Hatch 0
10
10
1-h salinity steps
10
10
10
10
10
10
10
10
5 10 15 20 0 salinity 25
Fig. 2 Experimental design for salinity tolerance experiments. Larvae in low salinity group were left at experimental salinity (either 0 or 5), while control group larva was subjected to salinity increases of 5 per hour until a salinity of 25 was reached. Numbers in circles indicate N’s of larvae in dishes. This schematic shows a 0 salinity experiment
dead if they lay motionless on the bottom and were opaque in appearance. Live saltwater and freshwater rotifers, Brachionus plicatilis and B. calyciXorus (Florida Aqua Farms Inc.), respectively, were used as food for larval U. minax. B. plicatilis were fed to control groups and were
acclimated to 5 for the low salinity experiments. Food was provided ad libitum. Water was changed every 2–3 days for larvae in the experiments (and corresponding controls) started at a salinity of 5 because these experiments ran for a long time. Due to their short duration, water was not changed in the experiments initiated at 0 salinity. For the freshwater population, Wve broods were tested at 0 salinity without rotifer food added and six broods were tested at 0 salinity with food added. For the brackish water population, two broods were tested at 0 salinity without food, three at 0 salinity with food, and Wve broods were tested with food at 5 salinity. Food was added for some of the 0 salinity experiments and not others because the freshwater rotifer, B. calyciXorus, which was used as the food source was not successfully cultured until after several of the U. minax broods had already been tested. Statistics for salinity tolerance experiments Probit analysis (Finney 1947) was used to estimate the time at which 50% of the larvae had died (LT50) in the 0 and 5 salinity experiments. A Kruskal–Wallis One Way Analysis of Variance on Ranks was used to compare the LT50 s of the broods kept at 0 salinity, followed by the Holm-Sidak multiple comparison procedure.
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Physical data and statistics Water column currents were measured using a bottom mounted, 1,200 kHz acoustic doppler current proWler (ADCP). The proWler was deployed in the Pee Dee River adjacent to the Bates Hill Plantation for a period of 7-days spanning a spring tide, beginning June 20, 2005. The ADCP was programmed to record the average current and water elevation at 5-min intervals for the duration of the deployment. The vertical resolution for the current proWle measurements was 0.25 m and the lowest bin was 1.2 m above the bottom. The average channel depth measured by the ADCP pressure sensor was 3.6 m.
Table 2 Kruskal–Wallis one-way ANOVA and post-hoc Holm-Sidak multiple comparison procedure showing signiWcant diVerences in LT50’s in hours between freshwater and brackish water zoeae of Uca minax and also between fed and unfed broods exposed to 0 in the laboratory Source of variation
df
Between Weld sites
2
SS
MS
F
P
4,110
2,055
30.2
