Terrestricythere elisabethae, Horne & Smith & Whittaker & Murray, 2004

Horne, David J., Smith, Robin J., Whittaker, John E. & Murray, John W., 2004, The first British record and a new species of the superfamily Terrestricytheroidea (Crustacea, Ostracoda): morphology, ontogeny, lifestyle and phylogeny, Zoological Journal of the Linnean Society 142 (2), pp. 253-288 : 278-281

A-8 Loxoconcha japonica Ishizaki, 1968

Cytheroidea

An1 A-8 Terrestricythere elisabethae sp. nov. Terr estricytheroidea

Ab 2

100 µm

constant shade at one locality (River Cur), while at the other (Beaulieu River) there are trees close enough to provide shade during much of the day. Specimens were recovered among the reed beds, mostly from the leaf litter (predominantly oak and reed) that covers the surface of the mud, although a few have been found in the top few millimetres of the underlying sediment. The coast has double high tides during each tidal cycle so that there are four high tides a day. At the River Cur, there are approximately 1460 high tides a year, 52% of which are higher than 4.2 m, i.e. cover a significant proportion of the reed banks. There are periods of several days every month when high tides are too low to cover the reeds (neap tides), but the site is covered by brackish water on a regular basis. The salinity of the water in the River Cur ranges from 0 to 12‰. Salinities recorded in creeks on the Beaulieu River Estuary at the time of collection varied between five and 15‰.

Associated Foraminifera

Samples of leaf mould/litter and the underlying sediment from the reed marsh, within the habitat range of Terrestricythere ( Fig. 18 ), were collected from near the highest high water at Curbridge on the River Cur (type locality), and at Jarvis Copse on the Beaulieu Estuary. Leaf mould alone was collected at Bailey’s Hard on the Beaulieu Estuary. Live (stained with an aqueous solution of rose Bengal (1 g /l)) and dead (unstained) Foraminifera were picked separately from the residue using a moist paintbrush (therefore stained forms were clearly recognizable), the results being listed in Table 1 (x = present, xx = abundant) .

Living forms were rare compared with dead forms, so it was not possible to make assemblage counts of>100 living individuals. Nevertheless, there is considerable similarity between the species present living at all localities (see Table 1; two samples were examined from Jarvis Copse, hence the range of values). However, Ammonia limnetes was common at Bailey’s Hard but rare at the other localities. The dead assemblages comprised the same species with the addition of Balticammina pseudomacrescens . A further foraminiferal collection was subsequently undertaken by one of us (RJS) in November 2002, from leaf litter at Curbridge, within the upper range of Terrestricythere (and where the ostracod was particularly numerous). The Foraminifera were not stained so it is not possible to know for certain whether they were alive or dead. For the record, however, from a count of 50 specimens, the fauna comprised: Balticammina pseudomacrescens (17), Trochammina inflata (12), Miliammina fusca (10), Haplophragmoides wilberti (6), Jadammina macrescens (4) and Elphidium williamsoni (1). All these assemblages are typical of middle-high marsh ( Horton, Edwards & Lloyd,1999).

Life cycle

Terrestricythere elisabethae sp. nov. has eight juvenile stages and one adult, a total of nine stages or instars. The high ratio of males to females (approximately 50: 50) and the presence of sperm within some females indicates that it is a fully sexual species. Samples collected in May, June and November all yielded adults and juveniles. The May sample yielded a whole range of juveniles from A-8 to A-1. The later samples contained A-7 to A- 1 juveniles (the A-8 instar was possibly missed in these samples due to its very small size and translucent carapace). Although the sampling is limited, it suggests that this species may reproduce throughout the year. All samples were collected from the leaf litter, which indicates that this species breeds and lives its entire life in this habitat.

Mode of life

Terrestricythere elisabethae sp. nov. moves amongst the wet leaf litter, usually covered in a film of water (so thin as to be visible only under the microscope). Juveniles as young as A-7 also live on the surface of wet leaf litter, the smaller instars often present in between the striations of reed leaves. In the field, since the ostracods are white and the substrate is usually brown, individuals can often be detected with the naked eye and their identification verified with the aid of a 10¥ hand lens. A sample of leaf litter taken at the River Cur locality from a 20 ¥ 20 cm area yielded 84 adults and juveniles, suggesting a population density of 2100 individuals m -2. A laboratory culture has been successfully maintained for over a year in a sample of the habitat cut out with a knife in the field and placed in a plastic box (approx. 25 ¥ 10 cm in plan, 5 cm deep) kept loosely covered with a lid to reduce moisture loss. Although a little water was added to the bottom of the box from time to time to replace loss by evaporation, the mud/leaf surface of the culture remained out of the water at all times and ostracods could frequently be seen crawling on this surface .

The genus Terrestricythere Schornikov, 1969 was so named to reflect the presence of the type species in a terrestrial habitat. However, Schornikov (1980) did not consider any species of ostracod found in terrestrial habitats to be truly terrestrial animals, since they need water to respire. The habitat of T. elisabethae regularly undergoes submersion in brackish water, which strongly indicates that this species requires water to survive and is also not a true terrestrial animal. With each high tide that covers the site, the leaf litter is wetted and small pockets of water are left behind as the tide retreats. These small pockets of water allow tiny aquatic species to survive until the next submersion, including Foraminifera, copepods and the cytheroidean brackish ostracod Loxoconcha elliptica Brady, 1868 .

Only occasional living specimens of L. elliptica have been found with our collections of T. elisabethae ; the former is often extremely abundant in brackish-water salt marshes on British coasts and has an optimum salinity range of approximately 10–20‰ ( Horne & Boomer, 2000); we suspect that higher population densities are likely to occur a little lower in the intertidal zone and further down the estuary in slightly higher salinities (although this has not yet been investigated).

Terrestricythere elisabethae differs from L. elliptica (and indeed all aquatic ostracods) in that it is capable of moving around out of water, with water trapped inside and around its carapace. Specimens placed in a drop of water on a glass slide explore the drop, before sometimes leaving the drop pulling some of the water along with them. As they move the water moves with them, presumably due to the surface tension of the water. The densely spaced ‘shaving brush’ sensilla around the free margins of the valves probably aid in the retention of the water between the ostracod and the substrate and may even draw moisture up into the carapace through capillary action. The very long, stiff sensilla that protrude from the mid-region of the carapace may help to increase drag (or interact in some way with surface tension) so that more water is pulled along with the ostracod, and thus help to maintain the film of water around the ostracod.

As the water evaporates, movement reduces, until the ostracod starts moving in tight circles. When there is no longer water between the ventral margin and the substrate, movement stops altogether and the valves close, but usually with a small gape present. In this semidried state the ostracod can survive for a limited period (approximately 10 min in the laboratory at 15 ∞C). Once replaced in water the ostracod slowly recovers over a period of 5–10 min. The gape of the valves allows for water to enter the carapace and revive the animal and any air bubbles are slowly expelled by the appendages. Specimens in the laboratory that are dried for longer than approximately 10 min perish. It must be noted, however, that the temperature-controlled laboratory environment in which these observations were made has a high evaporation rate (a consequence of the air conditioning system) and specimens therefore probably dried out much more quickly than would normally be the case under natural conditions.

Harding (1955) considered that there are two kinds of organisms that can survive in terrestrial habitats, such as leaf litter. The first live in a film of water, while the second can live out of a film of water and are either dependent on a humid atmosphere or are desiccation-resistant. He suggested that the cypridoidean ostracod Mesocypris terrestris Harding, 1953 was of the second type due to its relatively large size (c. 1 mm in length) and globular shape, which he considered as being inconsistent with a lifestyle adapted to living in a film of water. He suggested that even though M. terrestris has a fully developed maxillular branchial plate (the part of the limb which, in aquatic ostracods, beats regularly to maintain a through-flow of oxygenated water within the carapace), it would not use it, as it is not an aquatic animal (Harding did not, however, study any live specimens).

Terrestricythere elisabethae has a lifestyle that is transitional between the two types of terrestrial lifestyles envisaged by Harding (1955). It needs water to respire and uses its maxillular branchial plate to create a current of water through the carapace (as confirmed by laboratory observations). However, it is not confined to films of water and can move across a dry substrate by taking a supply of water with it, in and around its carapace. Nevertheless, once this water supply is exhausted the ostracod ceases movement and risks death if not covered by water in the very near future. Thus it cannot be considered to belong to Harding’s second group of organisms that can respire in air. The bushy setae of the ventral area of the carapace are probably an adaptation to hold water and reduce water loss as the ostracod transverses dry areas. The length of time that such water will last depends on the air temperature and humidity, and is at its greatest in damp, cool, shaded leaf litter, where this species lives. In conditions with very high levels of humidity we consider it possible that water may condense on the sensilla of the ostracod, replenishing its water supply and thus substantially increasing its survival time away from a body of water. The lifestyle of T. elisabethae could be termed epineustonic (i.e. an organism that lives above the water surface, but is in regular contact with it).

Locomotion

Terrestricythere elisabethae sp. nov. moves using the antennae, sixth and seventh limbs ( Fig. 19 ). The long hooked setae of the antennal exopodite are fanned out in front and are used to help pull the ostracod along the surfaces of the leaves. The sixth limbs are used to push the ostracod along; a significant length of the anterior edge of the endopodite of the sixth limb comes into contact with the substrate during each walking movement, and the claws along this edge increase traction, as reported for T. ivanovae ( Schornikov, 1980) . This is different from the walking movement of other ostracods, for example cypridoideans, in which the long, curved claw of the sixth limb is used to roll the weight of the ostracod forward, so that the anterior edge of the endopodite of the sixth limb does not come into contact with the substrate ( Kesling, 1951). When walking along a flat, horizontal substrate the seventh limbs are usually folded up along the body. However, occasionally the seventh limbs are also used to push the ostracod along in conjunction with the sixth limbs on horizontal surfaces, and on sloping or uneven surfaces the seventh limbs are used for extra grip. Specimens caught in the surface tension of the water use the seventh limbs to try and hook on to an object and pull themselves free.

Figures

Figure 18. Cross-section of the type locality of Terristricythere elisabethae sp. nov. and local tide data for 2002.

Figure 19. Locomotion in Terrestricythere elisabethae sp. nov. Only An2, L6 and L7 drawn for clarity.