Evaporative water loss under desiccation stress in semiterrestrial and terrestrial amphipods (Crustacea: Amphipoda: Talitridae)

145

J. Exp. Mar. Biol. Ecol., 1987, Vol. 111, pp. 145-157

Elsevier

JEM 00928

Evaporative water loss under desiccation stress in semiterrestrial and terrestrial amphipods (Crustacea : Amphipoda : Talitridae) David Morritt Severn Estuary Research Group, Department of Zoology, University of Bristol, Bristol. U.K.

(Received 3 February 1987; revision received 4 May 1987; accepted 4 May 1987) Abstract:

Transpiration rates were measured in both still and moving air systems in three talitrid amphipods, Orchestiu gammarellus (Pallas), Tulimts saltator (Montagu), and Arcitalitrus dorrieni (Hunt). Significant differences were demonstrated between the rates ofwater loss in the three species. The terrestrial A. dorrieni exhibited much higher rates than the supralittoral species. In still air at 15 “C and 75% r.h., for example, the mean rate in A. dorrieni was 0.183 f 0.008 mg. h- ’ ‘rng wet wt- ’ compared with 0.111 f 0.003 for Orchestia gummareNus and 0.106 f 0.003 for Talitrus saltutor. In moving air, regression lines plotting weight-specific rates of water loss against saturation deficit were significantly different between the three species in their slope. The regression line for Arcitalitrus dorrieni (R = - 0.0514 + 0.04814) was much steeper than that for Orchestia gammareBus (R = 0.0465 + 0.0187$~) and for Tulitrus saltutor (R = 0.033 + 0.01284). Arcitalitrus domenitherefore showed the highest rates ofwater loss, under conditions of high desiccation stress, but there was no clear difference between the species at low values of saturation deficit. Mean calculated permeabilities reflect this trend: A. domeni, 0.0403 + 0.0009 mg . h - ’ mg wet wt-‘, mm Hg-‘; Orchestiu gammareBus, 0.0247 f 0.0008; and Talitrus saltator, 0.0188 + 0.0006. Juvenile supralittoral talitrids of approximately the same body size as Arcitalitrus domeni consistently showed higher weight-specific rates of water loss in still air than adults of their own species, but the rates were usually lower than those of adult A. donieni. The very high rates of transpiration in A. dorrieni are not explicable by purely allometric considerations. The results are discussed with reference to the ecology and natural habitats of the species investigated and in relation to the colonization of the terrestrial habitat. Key words: Amphipod; Water loss; Land colonization; Orchestia gammarellus; Talitrus saltator; Arcitalitrus dorrieni

INTRODUCTION

The Amphipoda are one of three groups of Crustacea (along with Isopoda and Decapoda) which can be said to have colonized land with any degree of success (Little, 1983). Within the Amphipoda the fully terrestrial (euterrestrial) forms are restricted to a single family, Talitridae, which also includes many supralittoral species from both marine and freshwater habitats. Whilst much attention has been given to their morphology and systematics (Hurley, 1968; Bouslield, 1984) and the reproductive and developmental implications of the terrestrial mode of life (Williamson, 1951a; Hurley, Correspondence address: D. Morritt, Severn Estuary Research Group, Department University of Bristol, Woodland Road, Bristol BS8 lUG, U.K. 0022-0981/87/$03.50 0 1987 Elsevier Science Publishers B.V. (Biomedical Division)

of Zoology,

146

D.MORRIPIT

1968 ; Williams, 1978 ; Wildish, 1979), little is known about the basic ecophysiological processes of these animals. Occasional studies have looked at excretory characteristics (Dresel & Moyle, 1950), copper metabolism (Wieser, 1967) and more recently some studies on water balance, osmoregulation, and environmental tolerances (Lazo-Wasem, 1984; Moore & Francis, 1985, 1986) and also oxygen-transporting properties of the blood (Taylor & Spicer, 1986). The present study forms part of a comparative investigation into the ecophysiological processes in a range of talitrid amphipods, analogous to those in isopods (e.g., Horowitz, 1970; Lindqvist, 1972). Reported here is a comparison of the rates of evaporative water loss during desiccation stress in an ecological series of talitrids. Talitrid amphipods exhibit few apparent morphological or physiological adaptations to cope with the problems of desiccation stress presented by life on land (Backlund, 1945; Williamson, 1951b; Little, 1983) and the experiments described provide a test of the original hypothesis of Edney (1954) (later elaborated upon by Hurley, 1968) that these animals are adapted to life on land more by behavioural than specific physiological mechanisms. In his discussion of landhopper systematics and phylogeny, Bousfield (1984) subdivided the family Talitridae into four ecomorphological groups: (1) palustral talitrids, (2) nonsubstratum modifying beachfleas, (3) substratum modifying (fossorial) sandhoppers, and (4) landhoppers. For the purposes of this investigation representatives of the last three groups were used, Bousfield’s Group 1 not having representatives in the British fauna. The beachflea Orchestia gammarellus (Pallas) is one of the most abundant detritivores in marine and estuarine strandlines and saltmarshes, whilst the sandhopper Talitrus saltator (Montagu) commonly occurs in the suprahttoral zone of sandy beaches where it inhabits a transient burrow zone by day and forages nocturnally on strandline algae. The representative of Group 4 is the simplidactylate landhopper Arcitalinus dorrieni (Hunt, 1925), an antipodean species now well established in leaf-litter in various parts of the British Isles (Lincoln, 1979) where the climatic conditions, particularly temperature minima, are not too harsh.

MATERIALS

AND

METHODS

The supralittoral talitrids were collected from sites on the Sevem Estuary; Orchestia gammarellus were collected by hand from Chittening Warth saltmarsh, near Avonmouth (ST 532826), and Talitrus saltator using pitfall traps from Sand Bay, near WestonSuper-Mare (ST 329628). The euterrestrial landhopper, Arcitalitnu domkni, was collected by hand from leaf-litter in Penlee Gardens, Penzance, Cornwall (SW 468302). All experimental animals were maintained at 17-20 “C in aquaria containing fucoid algal debris or leaf-titter from the natural habitat as appropriate. A high humidity was ensured in the aquaria using paper towelling soaked in water of an appropriate salinity, either 20 (supralittoral) or Ox, (terrestrial). Animals were maintained for 2 24 h under these conditions (but not for > 2 wk) prior to experimentation, and were held overnight

WATER LOSS IN TALITRID AMPHIPODS

147

in damp (100% r.h.) containers without food sedately before experiments to allow voidance of gut contents. Each animal was tissue-dried to remove excess water before being placed in the experimental chamber. Except where stated the data refer to adult, intermoult (Charniaux-Legrand, 1952) amphipods. At the end of experimentation animals were killed and not used for further experiments. Experiments were carried out between April and November 1986. The rate of water loss from experimental animals was measured independently under contrasting conditions: in still air and in moving air. STILL AIR

Animals were restrained in small pl~kton-mesh envelopes and weighed to the nearest 0.01 mg using a C-1. Electronics Microforce microbalance Mk IIB. The envelope was then placed in an experimental chamber constructed from plastic drinkmg cups in which the animal was held by a plastic mesh platform over an appropriate saturated salt solution or water, the lid being tightly sealed with petroleum jelly. To avoid repeated disturbance of the vapour pressure gradients in the chambers each animal was placed in a separate identical chamber. After 1 h the animals and envelopes were reweighed and the weight loss determined; control bags were also included to control for the hydration of the plastic mesh. Sixteen replicates were performed for each species, at each different ~omb~ation of temperature and relative hu~dity. Temperature control was achieved by i~ers~g the chambers iu a water-bath with a Grant cooling unit which was maintained ~e~ostatic~y at the experimental temperature; either 5, 15, or 25 + 0.5 “C. Relative humidity was controlled using saturated salt solutions (Winston & Bates, 1960): sodium chloride for 75% r.h. and potassium chloride for 85 % r.h. with distilled water used for the highest humidity chambers (z 100% r.h.). The humidity of the chambers was regularly checked using humidity-sensitive cobalt thiocyanate paper with the Lovibond Comparator technique, the validity of these values being checked periodically against measurements in the same chambers performed with a Kane-May portable temperature-humidity probe KM 8004 and a modified lid attachment. Animals which escaped from the mesh envelope were not included in the data for analyses. MOVING AIR

As was first pointed out by Ramsay (1935) and subsequently shown by several other authors (see Beament, 1961), measurement of water loss in still air, particularly with live, moving animals, has several drawbacks. First, an animal, even if partially restrained in a mesh envelope, will by its movements set up a series of small air currents which will upset the vapour pressure gradients around the animals and consequently greatly influence the rates of evaporative water loss through the cuticle and into the air. Secondly, if one wishes to investigate the properties of arthropod cuticle one needs to study what Beament (1961) terms the “membr~e”l~ted system” in which the cuticle

148

D. MORRI-M-

and not the su~oun~g air layer provides the greatest resistance to the diffusion of water vapour. This means that one has to overcome the boundary-layer resistance of the cuticular surface and in practice means that evaporation from the cuticle must take place into a constant moving air stream, sufficient to negate this resistance (Loveridge, 1980). It is thus valid to measure rates of water loss under such conditions for the comparative purposes of the present study, although it is appreciated that the conditions are not strictly relevant from an ecological viewpoint. An apparatus was thus designed to make continuous measurements of weight loss whilst also making simultaneous recordings of temperature and relative humidity of the air flowing over the animal. The animal was suspended, inside a small pl~kton-mesh envelope, from one arm of a Beckman LM-500 ~crob~~ce and hung down into the experimental chamber which was insulated with expanded polyst~ene. A Unicam chart recorder was connected to the microbalance output together with a timer in such a way as to make a recording of the weight of the animal every 1 min throughout the duration of the experimental run (usually 1 h). Rate of water loss over this period was approximately linear. A constant flow of air (11 min - ‘) was passed through a flowmeter (Rotameter Ltd.), through a copper preheating-cooling coil and bubbled through two bottles containing saturated salt solutions or water, the emerging air passing into the experimental chamber via an insulated rubber tube and vapour trap. The copper coil and bottles were immersed in a Grant water bath with Grant cooling unit which was ~~mostatic~ly controlled and maintained at a preset temperat~e k 0.5 “C. All the apparatus was situated in a const~t-temperature cubicIe (w 19 “C). The ambient and dew-point vapour pressures and temperature of the air ffow were measured using a YSI Series 700 ThermiIinear temperature probe and a YSI Model 9103 Dew-Point probe connected to a YSI Model 91HC Dew Point Hygrometer, the outputs of which were connected to an Anaspec Labwriter two-track chart recorder. From the chart recorder traces a constant measure of temperature and relative humidity could be made. Data were obtained for 80 individual Talitms saltator, 75 Orchestia gammarellus, and 66 Arcitaiitms dorrieni over a range of temperature and humidity combinations with saturation-de~cit values ranging from 2-14 mm Hg. RESULTS WATERLOSS IN STILL AIR Data for all the species under all the experimental conditions are shown in Table I. The results are expressed as weight-specific rates of water loss (mg water lost - h - ’ . mg wet wt-‘). Effect of temperature In the majority of cases increased temperature at a controlled humidity (75% or 85 % r.h.) caused an increase in the weight-specific rate of water loss from the ~phipod

WATER LOSS IN TALITRID

149

AMPHIPODS

species examined (Table I). The same relationship was not demonstrated in the high humidity chambers. Here the measured relative humidity changed appreciably with temperature: at 5 ‘C it was 90-95%, whereas at 25 “C it was z 100%. This probably produced anomalies in the consideration of temperature effects. TABLE I Weight-specific rates ofwater loss in still air for talitrid amphipods in different combinations of temperature and relative humidity: means of 16 replicates f SE; Fratios for ANOVA also shown. Levels of significance: *** = P < 0.001, ** = P < 0.01, * = P < 0.05. 5°C

15 “C

25°C

0.105 + 0.006 0.066 f 0.005 0.041 k 0.008 F = 25.36***

0.183 f 0.008 0.124 f 0.009 0.019 f 0.013 F = 62.21***

0.263 + 0.008 0.171 f 0.011 0.059 f 0.018 F = 62.42***

F = 111.53*** F = 37.80*** F= 2.13ns

0.111 * 0.003 0.076 + 0.003 0.012 f 0.002 F = 343.6***

0.110 * 0.005 0.091 f 0.002 0.030 f 0.003 F = 109.2***

F = 3.93* F = 44.27*** F = 14.18***

0.144 + 0.006 0.091 + 0.008 0.020 f 0.008 F = 71.26***

0.221 * 0.007 0.157 + 0.008 0.052 ?r 0.008 F = 122.5***

F = F = F =

88.54*** 38.77*** 6.44**

0.063 & 0.004 0.048 + 0.003 0.020 * 0.002 F = 50.68***

0.106 + 0.003 0.058 f 0.003 0.016 f 0.003 F = 200.6***

0.131 + 0.005 0.079 f 0.004 0.010 + 0.002 F = 246.6***

F = F = F =

82.44*** 18.97*** 4.26*

Talitrus juv. (15-40 mg) 75 0.121 + 0.005 85 0.115 f 0.008 * (1test)

0.160 + 0.006 0.117 f 0.008 *

0.225 f 0.009 0.146 + 0.005 *

F = F =

53.43*** 5.90**

r.h. (%I Arcitalitrus (19-40 mg) 15 85 100

Orchestia (40-80 mg) 15 85 100

0.096 + 0.003 0.056 + 0.003 0.021 * 0.001 F = 190.6***

Orchestia juv. (15-30 mg) 15 85 100

0.118 k 0.004 0.066 f 0.007 0.016 f 0.007 F = 73.65***

Talitrus (40-l 10 mg) 75 85 100

Effect of relative humidity With the exception of juvenile Talitrus saltator at 5 “C, there were consistently significant trends in the weight-specific rates of water loss when considering the series 75-85-100% r.h. at any specified experimental temperature for each species. From 75 to z 100% the rates dropped markedly. Thus at a given environmental temperature water loss was highly dependent on the relative humidity of the surrounding air.

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D. MORRITT

Compa&on of rates of water ioss between species Comparisons were therefore made between the three species under identical conditions of temperature and relative humidity. Adult Orchestia gammardus and Talitrus saltator arc appreciably huger than Arcitalitnts dorrkni and so differences in rates of water loss due to purely allometric factors may be expected. To control for this, the rates of water loss from small (juvenile) Orchestiu gammarellus and Talitras saltator of approximately the same size range as the Arcitali~ dorrkni were also included in the comparison. The comparisons are summarized in Table II. A. do&& consistently had TARLE II Comparisons between rates of

waterloss of talitrid amphipods at different temperature-humidity

combinations. A = Arcikdinw dmrieni; Qj = juvenile Orchestia gammoreUus; 0 = Orchesrio gammnrellus; Tj = juvenile Talitrw salrator; T = T&rus saltalar. * = No data for juvenile Tolirnr at 100% r.h. > = All groups to the IeR of the symbol have significantly greater rates of water loss than those to the right of it; where two groups are underlined these are also signilicantly different from each other at P = 0.05. Groups connected by the symbol * = ” are not signi.hcantIy different from each other at P = 0.05. C0nditions

ANOVA

T (“C)

r.h. (%)

5 5 5 15 15 15 23 25 25

75 85 = 100 75 85 ZIOO 75 85 alOO

the

F = 27.53 (P < 0.001) F=M79(P~o.oal) F = 4.46 (P < 0.01) P=34.X2(P<5.001) P- 19.09(P<0.001) F= 0.24 (P’O.1) ns F= 83.68(P
Student-Newman-Keuls test for signilicance between means

Oj=Tj>A=O>T Tj>A=O=T=Oj A>O=T=Oj A>Tj>Ojz#=T A=Tj>Gj=G=T -

*

A > Tj = Oj z T z=-0 A=Oj=TjrG=T A=Oj>b=T

*

*

weight-specific rates of water loss. These values were significantly greater donienithan for Talitrus sakator and Orchestiagammarellus at higher temperatures (15 and 25 “C) and highest desiccation stress conditions (75% r.h.). In conditions of reduced desiccation stress (85 and z 100% r.h.), Arc&&tis dom’eni again consistently had the highest rates of loss, but these rates did not differ significantly from rates measured for small (juvenile) suprahttoral t&rids of the same size range. Thus, although part of the difference in rates of water loss between A. dorrieni and the suprahttoral tahtrids may be attributed to simple allometric considerations, there is good evidence to suggest that the euterres?rial landhoppers genuinely do have higher weightspecific rates of water toss and as such are more susceptible to desiccation stress than the supratittoral forms. highest

for A.

WATER LOSS IN MOVING AIR

The data are again expressed as weight-specific rates of water loss (mg water lost. h-’ ’ . mg wet wt “~‘). Recordings from the dew-point and ambient temperature/

WATER LOSS IN TALITRID AMPHIPODS 0.6

151

gammarellus

0-n

W= 0.0465 + 0.0187@

r = 0.704 l

..++++ l.

I

I

I

I

l

I

I

I

I

I

I

I

I

I

I

I

Talitrus saltator W=O.O33+ 0.0128@ r= 0.834

A&

Arcitalitrusdorrieni w=-0~0514+0~0481@

.

r=O+l6

Y

.

-

I

I

I

I

I

I

1

2

3

4

5

6

I

7 Saturation deficit (mm.Hg

I

I

I

8

9

10

I H

1

Fig. 1. Graphs plotting weight-specific rates of water loss in a moving air current (1 1. min - ’ ) against the saturation deficit of the air for three talitrid amphipod species. Regression equations are given for each species; W = weight specific rate of water loss and + = the saturation deficit of air. Wet weight ranges of experimental animals as follows: T. sukzfor, 50-150 mg; 0. gammarehs, 35-85 mg; and A. dotieni, 15-40mg.

152

D. MORRITT

humidity probes were used to calculate the saturation deficit of the air flowing over the experimental animal. The measurements for each animal represent one point on the graph (Fig. 1) which plots weight-specific rate of water loss against saturation deficit. The regression lines for the three species were compared by analysis of covariance; the slopes of the regression lines differ significantly between the three species (F = 177.3, df 2,217, P < 0.001). The comparisons between pairs of species were as follows: Orchestia-Tab-us (F = 5.42, df 1,151, P < 0.025), Orchestia-Arcitalitrus (F = 69.21, df 1,137, P < 0.005) and Talitrus-Arcitalitnts (F = 188.16, df 1,142, P < 0.005). These data corroborate the previous results obtained in still air, showing that A. dorrieni had the highest weight-specific rate of water loss in moving air with lower rates in Orchestia gammarellus and the lowest in Talitrus saltator. The sequence is particularly evident at high saturation-deficit values, but due to the differences in slope nonexistent under conditions of low desiccation stress. Finally, to give some idea of the relative permeabilities of the cuticle of these species under these conditions, a term was derived whereby the rate of water loss from the animal was expressed as weight-specific rate of water loss per unit saturation deficit (mg water lost. h- ’ * mg wet wt - ’ * mm Hg - I). A value was thus calculated for each individual animal and the data for each species used to calculate a mean value for that species. In spite of great variability, these values serve to illustrate the marked differences in water loss between the three species examined (Table III). TABLE III

Calculated mean permeabilities for talitrid amphipod species in moving air (1 1.min - ‘). Species

Mean permeability + SE (mgwater*.h-‘.mgwetwt-‘.mmHg-‘)

Talitrus saltator Orchestia gammarellus Arcitalitrus dorrieni

0.0188 + 0.0006 0.0247 ; 0.0008 0.0403 + 0.0009

Wet weight range (mg) 50-150 35-85

15-40

DISCUSSION TEMPERATURE

EFFECTS

A marked effect of temperature and relative humidity on the rates of water loss was observed in all the species examined. This is hardly surprising and has been described in Orchestia gammarellus (Moore & Francis, 1985) and Arcitalitrus sylvaticus (Laze-Wasem, 1984). An increase in temperature at a given relative humidity will effectively increase the saturation deficit of the air while simultaneously increasing the temperature of the evaporating surface, i.e., the cuticle. Both are important factors in determining the evaporative water loss across the integument into the surrounding air (Edney, 1977) which is consequently higher at higher temperatures. Furthermore, the

WATER LOSS IN TALITRID AMPHIPODS

153

basal metabolism has been shown to be dependent on both temperature and body weight (see later) to differing degrees in the beachhopper Chroestiu lotu (Marsden, 1985) the sandhoppers Talitrus saltator (Williams, 1981), Talorchestia margaritae (Venables, 198 l), Trunsorchestiu chiliensis (Marsden, 1984), and Talorchestia cupensis (Van Senus, 1985) and the landhopper Tulitrus sylvuticus (Clark, 1955). It is possible that changes in the basal metabolic rate induced by such increases in temperature may also increase the rate at which evaporative water loss occurs. As the existence of “active” and “basal” rates have been shown in at least one talitrid, Tulitrus saltator (Williams, 1982), animals in their quiescent “basal” phase (i.e., during the L : D daytime period) were used wherever possible for experimental purposes. EFFECTS

OF SIZE

When compared with adults of their species, juvenile T. saltator and Orchestia gammarellus showed significantly higher rates of water loss in all but the lowest temperature experiments. This is attributable to the much smaller size and concomitant increase in surface area to volume ratio in juveniles. Although the high transpiration rates of euterrestrial landhoppers can be partly explained by similar allometric considerations and possibly by their higher relative rates of respiration (Clark, 1955) the data presented here suggest that the basic size difference only provides a partial explanation. Some of the possible implications of, and constraints on, body size in terrestrial amphipods were discussed by Richardson 8z Devitt (1984). They suggested that larger body size in these animals might be advantageous to a mobile species within certain limits. Applying this line of thought to the supralittoral talitrid Talitrus saltator, it is evident that this species attains a larger size than many other talitrids, has lower transpiration rates and hence greater desiccation tolerance and also has reduced weight-specific gill areas. All these interrelated factors may be highly advantageous to a species which undergoes extensive nocturnal migrations (Bregazzi & Naylor, 1972) during which it is inevitably exposed to considerable desiccation stress compared with the optimal burrow conditions (Williams, 1983). The much smaller juvenile talitrids showed far higher rates of water loss and certainly in T. saltutor this is reflected in the ecology and behaviour of the juveniles. Williams (1983) described how recently hatched juveniles (3-5 mm) were recorded only in the top 5 cm of substratum, usually superficially burrowed beneath the algal debris deposited by the previous nocturnal tide thereby maintaining an optimal local r.h. > 80% (Williamson, 1951b). INTERSPECIFIC

COMPARISON

Previous studies have suggested that not only were terrestrial landhoppers unable to control their water loss effectively but they lost water at higher rates than other talitrids. The present results confirm this suggestion and show the euterrestrial Arcitalitrus dorrieni to have the highest rates of water loss, Orchestia gammarellus the next lower,

154

D. MORRITT

T. saltator having the lowest rates of all. The relationships described between water loss

in the three groups are supported by isolated reports in the literature. In Arcitalitrus sylvaticus the measured rates of water loss, depending on temperature, of between 0.420-0.705 mg water * mg wet wt- ’ - h- ’ in 20% r.h. and 0.010-0.300 in 100% r.h.

(Lazo-Wasem, 1984) agree well with the present data. The susceptibility of the landhoppers to reduced humidities is confirmed by the tolerance experiments performed with Talitrus vulgaris and Talks sp. (Richardson & Devitt, 1984) and T. vulgaris and T. angulosus (Friend & Richardson, 1977). Likewise, similar tolerance experiments in the supralittoral species have demonstrated that the sandburrowing form Talorchestia megalophthalma has greater tolerance to desiccation than the beachflea Orchestia agilis (Platzman, 1960). The sandhopper studied here, Talitrus saltator, was shown to survive appreciably longer under conditions of desiccation stress than Orchestia gammarellus and Talorchestia deshayesii (Williamson, 1951b). The only measurements made of the actual rates of water loss in supralittoral species support the measurements made here for Orchestia gammarellus (Moore & Francis, 1985). IMPLICATIONS FOR THE COLONIZATION

OF LAND

Overall the results from the still and moving air experiments provide conclusive evidence that the euterrestrial talitrids have no physiological ability (when compared with semiterrestrial species) to control evaporative water loss through their integument. Talitrid amphipods are thus presumably adapted to life on land (as far as water balance is concerned) by behavioural mechanisms, supporting the original hypotheses of Edney (1954) and Hurley (1968). An active choice of optimal humidity conditions has been demonstrated for intertidal gammarid amphipods (Lagerspetz, 1963), supralittoral talitrids (Williamson, 195 lb) and a euterrestrial landhopper (Lazo-Wasem, 1984). More pertinent to Talitrus is the ability to maintain an optimal relative humidity in the sand burrow and it has been demonstrated that this species is able to regulate its burrow depth and maintain contact with a 22.0% water content in the surrounding sand (Williams, 1983). The rates of water loss reported here and elsewhere, together with the desiccation tolerance results are apparently correlated with the weight-specific gill areas of the species concerned (Spicer & Taylor, 1986). Arcitalitrus dorrieni has a very large gill area, comparable with that of the aquatic littoral amphipod Echinogammarus pirloti (Moore & Taylor, 1984), whereas the other talitrid species investigated had significantly smaller gill areas than the aquatic gammarids, with Talitrus saltator having the smallest weight-specific gill area of all. The question, however, arises as to how important is the reduction in area of highly permeable gill tissue in these animals, in which the whole cuticular surface is somewhat permeable. Although certain parts of the cuticle are more permeable than others, particularly the gills, arthrodial membranes and limb coxae and bases (see Moore & Francis, 1985), oxygen uptake has been shown to occur over the whole body surface in Orchestia and other amphipods (Graf & Magniez, 1969) which

WATERLOSS

INTALITRIDAMPHIPODS

155

is presumably therefore quite permeable. It has been suggested (Spicer & Taylor, 1986) that the levels of gill reduction in the supralittoral talitrids are adaptive to the conditions of desiccation stress presented by the transition from an aquatic to a terrestrial mode of life, while the retention of an almost “aquatic” gill area in the euterrestrial landhoppers can be explained by the absence of any such desiccation stress. This stress may have been lacking because the simplidactylate landhoppers typified by Arcitalitw dorrieni evolved from palustral ancestors in the coastal regions of Gondwanaland (Boustield, 1984) and subsequently colonized land directly via the leaf-litter of the rain forest bordering onto the coastal margins. Such species, therefore, may never in their evolutionary history have encountered marked desiccation stress. Considering the conditions encountered by terrestrial talitrids it is perhaps not surprising that they have not subsequently evolved specific adaptations to combat the stress of water loss. Generally speaking, the habitats utilized by euterrestrial amphipods (Friend & Richardson, 1986) pose few problems of desiccation stress and the small body size facilitates burrowing and retreat to small interstitial cavities in the soil/litter structure which maintain high local humidities. For example, A. dorrieni in the British Isles has been reported as burrowing in damp soil, under various shelter-giving structures and particularly under the cushion-forming plant Helixine (Murphy, 1974), and amonst various types of leaf-litter (Richardson, 1980; Moore & Spicer, 1986). Thus, the high humidities retained in these “leaf-litter” type habitats may render any specific adaptations to desiccation totally unnecessary in Arcitalitm dorrieni and other landhoppers (Hurley, 1968). In contrast, the lower rates of water loss and increased desiccation tolerances of the beach-hoppers may be an adaptation to the supralittoral strandline habitat. Whilst the depths of wrack piles retain relative humidities > 85% (Backlund, 1945; Williamson, 1951b; Moore & Francis, 1985), the surface layers are certainly exposed to significant desiccation, e.g., down to a value of ~50% r.h. (Backlund, 1945), particularly during hot periods in neap tide cycles. It is thus not paradoxical to state that the semiterrestrial, supralittoral habitat may present a harsher environment (in terms of water balance) to talitrid amphipods than does the fully terrestrial “leaf-litter” habitat. As such it is not surprising that the semiterrestrial species show a greater degree of adaptation to short-term desiccation, whether it be physiological, morphological or behavioural, than do their terrestrial counterparts.

ACKNOWLEDGEMENTS

The author would like to thank Drs. C. Little and L. Strong for their constructive comments on the manuscript and Mr. G. B. Miller and Mr. E. Cock for their help in the collection of Arcitalitrus dorrieni. Invaluable technical assistance in the design and manufacture of apparatus was given by Mr. N. Ablett. This work was carried out whilst the author was in receipt of a Science and Engineering Research Council Studentship.

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