FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute Notice: ©2002 Springer‐Verlag. This manuscript is a version of an article with the final publication found online at http://www.springerlink.com and may be cited as: Emson, R. H., D. Morritt, E. B. Andrews and C. M. Young (2002) Life on a hot dry beach: behavioural, physiological, and ultrastructural adaptations of the littorinid gastropod Cenchritis (Tectarius) muricatus, Marine Biology 140: 723–732 DOI 10.1007/s00227‐001‐0738‐9 Marine Biology (2002) 140: 723–732 DOI 10.1007/s00227-001-0738-9 R.H. Emson Æ D. Morritt Æ E.B. Andrews Æ C.M. Young Life on a hot dry beach: behavioural, physiological, and ultrastructural adaptations of the littorinid gastropod Cenchritis (Tectarius) muricatus Received: 15 June 2001 / Accepted: 9 October 2001 / Published online: 8 February 2002 Ó Springer-Verlag 2002 Abstract The distribution and abundance of the littori- haemolymph concentration are greatest in the early pe- nid gastropod Cenchritis (Tectarius) muricatus were de- riod of desiccation. The concentration of the blood after termined on an exposed shore at Lee Stocking Island, 20 weeks is 250% of the original and the water lost is of Bahamas in July/August 1995 and June 1999. Activity the order of 22.5%. After an initial increase there ap- patterns were observed on two occasions shortly before pears to be evidence of regulation of haemolymph con- a hurricane passed near the island in 1995. C. muricatus centration possibly by exchange with free water in the extended from the low water mark to 3.6 m vertical shell itself. The considerable reserve capacity in toler- height above it. Highest densities (20/m2) were found ance is no doubt in part due to the structure and func- just above the high tide mark but the animal remained tioning of the kidney. Adaptive features of the excretory relatively abundant (8/m2) at the highest point. Small system identified from ultrastructural examination in- animals were only found at high shore levels. With the clude the replacement of podocyte-containing filtration exception of animals very near to the water’s edge chambers in the auricle by extracellular tubules perme- C. muricatus was inactive by day and on dry nights. ating the walls of both auricle and ventricle, which Many individuals of the high shore populations became suggests a reduction in the rate of primary urine for- active at night during periods of high humidity and mation. This is also indicated by a reduced surface area rainfall, moving distances of up to 4 m overnight. At of the nephridial gland, which resorbs organic solutes lower levels, extensive pairing and copulation was from the urine. Excretory cells contain single large associated with these periods of rainfall. Abundance vacuoles in which arise large multi-layered concretions changed dramatically after the passage of the hurricane. composed of phospholipids and calcium salts typical of At the level of maximum abundance numbers were re- prosobranchs in which excretory products may be stored duced from 20/m2 to 2.8/m2. Long-term experimental for long periods. studies of water loss rate and haemolymph concentra- tion showed that both water loss rate and increase in Introduction Communicated by J.P. Thorpe, Port Erin The littorinid snail Cenchritis muricatus is a familiar R.H. Emson (&) component of the littoral fauna in the Caribbean, Division of Life Sciences, King’s College London, Franklin-Wilkins Building, 150 Stamford Street, Bahamas and southern Florida, often abundant from London SE1 9NN, UK the waterline to well beyond the highest parts of the E-mail: [email protected] splash zone (Clench and Abbott 1942; Abbott 1954; Fax: +44-020-78484500 Lewis 1960; Borkowski 1971, 1974; Bandel 1974; Bandel and Wedler 1987; Britton 1992; Lang et al. D. Morritt Æ E.B. Andrews School of Biological Sciences, Royal Holloway, 1998). Many individuals near the upper limit of dis- University of London, Egham, tribution are, in dry periods, attached by a mucous Surrey TW20 0EX, UK film to maritime vegetation, often as much as 0.5 m C.M. Young above the adjacent rock surface where they are fully Department of Larval Ecology, exposed to the harsh conditions characteristic of this Harbor Branch Oceanographic Institution, environment. Such individuals appear totally inactive 5600 U.S. Highway 1 N., Fort Pierce, FL 34946, USA in fine weather both by day and night and previous authors (e.g. Bandel 1974) have assumed that they 724 may remain inactive until conditions are suitable for When we returned to the shore after this night of heavy rainfall activity. (29 July 1995) many animals were found to be copulating. We un- dertook a survey relating incidence of association/copulation to A tropical storm that became Hurricane Erin passed height above sea level at six different heights ranging from 0.2 to close to Lee Stocking Island in July/August 1995 and 2.8 m above low water. At each height, we laid out a 30-m tape caused heavy rainfall followed by extremely strong horizontally, at right angles to the original transect line, then winds that generated unusually heavy wave action at the examined 0.5·1 m areas contiguously along the tape, for a distance of 15 m except in a few cases where the end of the transect traversed study site. We were able to establish base-line data about 2 sand. We counted the number of animals/m and noted the number the population before the approach of severe weather; in of animals found singly, in pairs, or associated in larger numbers. addition we were also able both to observe the effects of Periodic (arbitrary) checks of pairs were carried out to confirm that this unusual weather on the behaviour of C. muricatus paired animals were copulating. A similar survey was carried out to and to determine the effects of wave action on the determine abundance and numbers copulating after the wave action generated by the tropical storm/hurricane had subsided. population. The transect described above was re-surveyed in June 1999, Although specimens of C. muricatus removed from size-frequency data obtained for the same levels as in the previous the field are capable of surviving several months of survey, and association levels also recorded. desiccation (Rosewater 1963; Britton 1992) there are no blood osmolality data available for this species. Neither Physiological experiments is there any information as to whether kidney structure reflects the fact that these animals suffer frequent Desiccation and weight loss periods of prolonged dehydration in their natural habitat. An opportunity to re-visit the island in June Inactive animals were individually numbered, weighed to the nearest milligram with a microbalance (Mettler AE166), and then 1999 allowed us to re-survey the population. We also re-hydrated by immersion in fully aerated artificial seawater (Tro- collected animals for an experiment with the objective pic Marine; 34& 1,000 mosmol kg–1) for 1 h. All became active of ascertaining how blood osmolality is affected by during this period. Following immersion, animals were dried with dehydration and for subsequent fixation with the aim tissue paper to remove adherent water, re-weighed, and then placed of studying the adaptive features of the kidney. in a sealed plastic aquarium with three beakers holding saturated MgCl2 solution covered with mesh. Relative humidity was main- tained at 40%. Relative humidity was monitored with a hair hy- grometer that was checked regularly against a calibrated electronic temperature/humidity probe (Vaisala HMP31) connected to a data Materials and methods logger/meter (Squirrel 1250 series). The aquarium was placed in a thermostatically controlled incubator at 35°C. At a series of time Ecological and behavioural observations intervals between 0 h (post-immersion) and the termination of the experiment, 10 snails were removed, weighed, and their haemol- The main distribution and behavioural studies were carried out ymph concentration determined. In parallel with the main experi- over the period 27 July–1 August 1995 on the northeast coast of ment a separate batch of 25 animals was used to monitor rate of Lee Stocking Island, Bahamas (23°46.5¢N, 76°5.5¢W). The study water loss, by weighing at 7-day intervals throughout the experi- site was a small promontory that sloped upwards at an angle of 30° ment. At the end of the experiment the viability of all 25 snails was and had a total height of 3.6 m from the low water mark (LWM) to checked; 2 snails were dead and these were thus excluded from the the ridge crest. subsequent data analysis. A vertical transect was surveyed 3 days before the passage of All water loss data were ultimately expressed as a percentage of Hurrricane Erin and also on the day following the passage of the the initial post-immersion wet weight. These data were transformed hurricane (1 August 1995). A line of contiguous 1 m2 quadrats was (arcsine of the square root of the proportion; Underwood 1997) marked with a tape from the LWM to the crest of the ridge. The prior to analysis. All osmolality and water loss data were tested for number of C. muricatus in each quadrat was recorded, as were the normality and homogeneity of variances prior to analysis. Data vegetation types, the nature of the rock surface, and whether the were analysed using either parametric or non-parametric analysis snails were on the rock or the vegetation. Crevices and the un- of variance as appropriate (SPSS ver. 9.0). derside of loose stones were closely examined for small individuals.