Tropical Zoology 13: 239-249, 2000

^ Surface activity in the mudskipper,5 Periophthalmus waHoni Koumans 1941^ in relation to prey activity and environmental factors

D.A. Clayton 1 and R. Snowden 2

1Department of Biology, College of Science, Sultan Qaboos University, P.O. Box 36,123 Al Khod, Sultanate of Oman2 Environmental Sciences Department, Sir William Halcrow & Partners, BurderopPark, Swindon SN4 OQD, Wiltshire, UK

Received 6 July 1999, accepted 18 May 2000

Surface activity and foraging behaviour of the carnivorous mudskipperPeriophthalmus xvaltoni Koumans 1941, was investigated in relation to environmental conditions on the mudflats of Sulaibikhat Bay, Kuwait. Fish occupiedseveral burrows systems within a 2-3 m2 home range. Foraging activity waslargely independent of environmental conditions only being inhibited by highwind speeds and surface temperatures below 15 °C. Hunting forays were longerthan other surface activity, but once prey was caught, the mudskippers quicklyreturned to a pool of water or a burrow. To increase their hunting efficiency,successive hunts were spatially well separated because of the long surface returntimes of the ocypodid crabs following a hunt in their vicinity. For a variety ofphysiological requirements mudskippers exhibit considerable behavioural homeostasis in a harsh environment creating a unique system in which to investigatemechanisms of optimal foraging.

key words: activity, foraging behaviour, Periophthalmus, mudskipper, Ocypodi-dae, crabs, behavioural homeostasis.

Introduction 240Methods 240Results 241

General behaviour 241Environmental correlates of activity 242Crab and fish activity 242Hunting activity 245

Discussion 245Activity and environmental conditions 245Behavioural homeostasis 246Foraging strategies 247

Acknowledgements • 247References 247

240 D.A. Clayton and R. Snowden

INTRODUCTION

Mudskippers have provided a rich source of information of comparative studies in adaptation to the littoral habitat. Many of these studies are physiological, butadditionally the suitability of mudskippers for resolving behavioural issues is beingrealised (Clayton 1993). Recent studies have begun to look in detail at environmental correlates of behaviour (Colombini et al. 1995; Ikebe & Oishi 1996, 1997), orientation (Berti et al. 1992, 1994) and foraging (Colombini et al. 1996). Stomach content analyses (Barak et al. 1994, Colombini et al. 1996, Mhaisen & Al-Maliki 1996)continue to support the fact that species of Periophthalmus have catholic diets.Colombini et al. (1996) further showed that there is considerable tidal and diel variation in prey selection, which are probably related to environmental fluctuationsthat influence the spatial and temporal distribution of the prey. While this stillneeds direct confirmation, it is clear that male and female fish utilize different foraging strategies that could be related to reproduction (Colombini et al. 1995). It isat this level that the study of mudskippers can begin to contribute to the widerdebate on teleost feeding strategies (Hart 1986) or optimal foraging in the inter-tidal environment (Hughes 1988). Even when attempting to limit cost benefitanalyses to temperature and food resource use (Crowder & Magnuson 1983), themulti-dimensional environment (thermal gradients and food patches) inhabited bymost fish complicate the issues. In contrast, mudskippers on exposed mudflatsinhabit a structurally simpler environment where surface water and crab distributions make it easier to identify gradients and patches and predatory behaviour iseasily observed. This makes mudskippers potentially good subjects with which toinvestigate these issues.

Intertidal amphibious fish in general and mudskippers in particular areexposed to one of the greatest ranges of temperature variation met by fish and copewith it by using a number of thermoregulatory mechanisms (Tytler & Vaughan1983, Ikebe & Oishi 1997). This paper represents a preliminary study of the relationship between surface activity, foraging and thermoregulation and suggests waysin which further mudskipper studies could contribute, more directly than they havedone so far, to the wider theoretical issues.

METHODS

The surface activity of the carnivorous mudskipper Periophthalmus waltoni Koumans1941 was observed on a mudflat in Sulaibikhat Bay (29°21.5'N 47°49.25'E) a muddy shoreembayment in Kuwait Bay at the north-western head of the Arabian Gulf. An observationarea of 100 m2 was established on the mudflat just below Mean Low High Water in a regionwhere the low density populations of the herbivorous mudskipper Boleophthalmus dussumeiriCuvier & Valenciennes 1837 (Clayton 1987) and the life cycles of the small (5-10 mm carapace width) ocypodid crabs Tylodiplax indica Alcock 1900, Nasima dotilleformis (Alcock 1900)and Ilyo-plax stevensi (Kemp 1919) (Snowden et al. 1991, 1994; Snowden & Clayton 1995)have pre-viously been studied. Additionally the largest ocypodid, Macrophthalmus dentipesLucas 1836 (60-80 mm carapace width, formerly M. pectinipes Guerin 1838; Holthuis 1995)were frequently found here where they constructed large, water-filled, saucer-shapedentrances to their burrows (Al-Taher 1990). Ropes divided the area into 49 2 x 2 m squares,the central 25 of which comprised the study area. Only mudskippers located within this central area were observed, but as they sometimes travelled outside it, the additional perimeter

Surface activity of Periophthalmus waltoni 241

squares were established to assist in accuracy of reporting movements. The behaviour of thefish was recorded on an OS-3 event recorder (Observational Systems Ltd) and included inactivity, movement, burrow sojourns, burrow maintenance/construction, feeding, fighting andcomfort behaviour and pectoral fin flapping or waving. Behavioural descriptions are takenfrom Harris (1961) and Clayton & Vaughan (1988). The location of all the mudskipper burrows were mapped. Movement routes for the focal animal were plotted onto the maps withposition markers for significant interactions such as fighting and hunting attempts. Observations were made at various states of the tide and under a variety of weather conditions over aperiod of 8 months between September 1989 and April 1990.

During each visit several environmental variables were recorded. A YSI Tele-thermometer,model 44TD equipped with Model 401 thermister probes was used to measure the temperature of the air at a height of 2 cm, the surface mud and standing water, and the mudskipper'sburrow at a depth of 10 cm. The burrow temperature also reflects that experienced by thecrabs since it is common for crab burrows to join those of the fish (Clayton & Vaughan1986). Additionally, wind speed (m/sec) was measured with an Aneno (Casella, London)placed such that the revolving cups were at surface level. The relative humidity also wasrecorded as close to the mudflat as possible. Before the behaviour of the fish was recorded,the number of surface active crabs were calculated by counting those present in a minimumof 6 random squares within the observation grid and are reported as crabs/m2. If the recording session was long all measures were repeated.

A recording session began when the fish and crabs had resumed activity after the disturbance created by the observers arrival. The observation post was about 5 m from the outeredge of the grid, but its position round the grid was varied from visit to visit.

The duration of the surface activity and burrow sojourns of the mudskippers' mainprey {T. indica, N. dotilleformis and /. stevensi) were obtained from video recordings from acamera set up away from the study grid. This near vertical view of a small section (0.20 m2)of mudflat enabled individual crab time schedules to be analysed at a later time. While thevideotapes recorded the passage of P. waltoni, no hunting events occurred within the areacovered by the camera. Consequently crab re-emergence times after a hunting event in theirimmediate vicinity were measured separately. Solitary foraging fish were followed until ahunt occurred and then the area was continuously scanned (with binoculars) until crabsbegan to re-emerge from their burrows.

RESULTS

General behaviour

Each adult fish had a home range of between 2-3 m2 in which were locatedthe main and subsidiary burrows, the main one simply being the most frequentlyused. The burrows were of two types such that the entrance was either a double-turreted one (the 'Y' shaped burrow) or was in a water-filled, saucer-like depression(cf. MacNae 1968). While some fish had a single burrow system of either type, others utilised between two and six different ones. During the period of observation noother P. waltoni were seen to use them.

On several occasions burrow maintenance activities were observed when thefish would deposit mouthfuls of mud away from saucer burrows or onto the rim ofturreted ones. During this activity, fish moved directly, without deviation or pause,between the burrow and the place of deposition several times in succession. Thusthe form and duration [18.49 ± 13.12 (SD), n = 27] of surface activity and burrowsojourns [11.51 ± 9.68 (SD), n = 32] during burrow maintenance was clearly distinct from those occurring during hunting activities and were excluded from thesubsequent analyses.

242 D.A. Clayton and R. Snowden

Additionally within these home ranges there were partially-walled territoriesof B. dussumeiri (Clayton 1987). The territories had pools of water in them intowhich P. waltoni would occasionally enter, but for the most part the two speciesavoided each other. As well as the two mudskipper's pools of water there were alsothose of the mud crab M. dentipes and ephemeral pools on the open mudflat, theoccurrence of which depended on the state of the tide and the time of year. Typically P. waltoni would move about apparently randomly within its home range whereit hunted crabs and avoided, attacked or courted other P. waltoni. During this activity the fish might enter the pools or its own burrow systems along the way.

On 15 occasions there was no crab or fish activity so that mudskipper behaviour was recorded only on 32 of 47 visits for between 24 and 172 min. A total of 78successful crab hunts by P. waltoni were recorded on 25 of these visits duringwhich the number of hunts ranged from 1 to 8 (mean: 3.12 per fish). To avoid statistical pseudo-replication (Hurlbert 1984) only the averaged data for each fishwas analysed.

Environmental correlates of activity

Throughout the study period air temperatures varied between 8.25 °C inDecember and 38.8 °C in October. While winter (December and January) temperatures were clearly lower than at other times of the year, there was considerabledaily variation, such that mid-day temperatures in the cooler months were oftensimilar to early morning or late afternoon ones in the hotter months (Fig. 1A). Airtemperatures were significantly positively correlated with that of the mud surface(Pearson correlation coefficient, r = 0.971, n = 46, P < 0.0001, Bonferroni adjustedprobability), pools of water (r = 0.915) and burrows at a depth of 10 cm (r = 0.877)(Fig. IB). Generally air temperatures were also higher than that of the other locations, except at the lowest values when burrow temperatures were higher. Thuswhile the air temperature at 06:55 on 10 December was 8.25 °C, temperature in theburrows were 13.25 °C. Similarly at 11:30 on 14 November when a 'shamal' windbrought air temperatures to an un-seasonal low of 10.5 °C, burrow temperatureswere 14.25 °C. The negative correlations between relative humidity (r = - 0.384)and wind speed (r = - 0.25) with air temperature were not significant (Fig. 1C).

Crab and fish activity

Surface activity of crabs varied from total inactivity to occasions when densities exceeded 70 crabs/m2. The best environmental predictors of surface density ofcrabs were identified as mud surface temperature and wind speed by a stepwiseregression with low alpha values (Wilkinson 1990) and are shown in Fig. ID. Crabdensity increased with mud surface temperature but decreased with increasingwind speed. At temperatures below 10 °C and wind speeds above 4 m/sec surfaceactivity is all but inhibited (Fig. ID). The state of the tide, as measured by whenthe recording sessions began in relation to the preceding high tide, had no effect oncrab density (r = 0.137, NS).

In general terms, the same conditions promoted the surface activity of bothcrabs and mudskippers. Within the recorded air temperature range of 8.25 to 38.8°C the surface activity of the P. waltoni was only found to be limited at low temper-

Surface activity of Periophthalmus waltoni 243

atures. Records of their behaviour were collected only in air and mud surface temperatures of between 16.5 to 38.8 °C and 15 to 30.25 °C respectively. Activity on thesurface however, did begin at air temperatures below 16.5 °C as observations forthe cloudy and overcast day of 16 January 1989 showed. At 08:45 there was noactivity and the air, mud surface and burrow temperatures were 9, 8 and 7.5 °C

l l l l I I I I I i I I i i i i i I I I I I I

A

i i i i i I • • , • • I • i i i ' i

6 12 18

Time (hr)

J I I I I L

n 1 1 1 1 r

Relative humidity

Wind speed

1

Di i I 1 1

0 .-''

-

; _/

5. ,-' •' ^

10 f .-'

-

_ • i J ^^v^"

i

-~^ .-" 40

0)a>a.

(/>

•oc

5

5 10 15 20 25 30 35 40

Air Temperature (°C)

Fig. 1. — A: seasonal changes in hourly air shade temperatures (data from Al-Kulaib 1975). B-C:correlation of air temperature with that of the mud surface, pool water and deep burrow (B), andwind speed and relative humidity (C). D: a contour plot of the number of emergent small ocypodidcrabs per m2 in relation to the mud surface temperature and wind speed. Isoclines for six levels ofcrab densities are indicated.

244 D.A. Clayton and R. Snowden

respectively. The first crabs and mudskippers were observed at 10:35 at temperatures of 14 °C (air and mud) and 8 °C (burrow). While crabs foraged as usual, mudskipper activity however, was limited to brief appearances from the burrows duringwhich the comfort action of pectoral fin flapping occurred.

By contrast, inhibition of activity could also occur at temperatures within therange in which fish were usually active. As a general observation it was noted thatthere was little activity on dry mud above the level reached by the previous hightide. On 5 December 1989, it was possible to quantify this because only half theobservation grid was wetted by the high tide 3 hr previously. The air and mud andburrow temperatures were 25.5 and 15.25 °C respectively, but there was no crab orfish activity on the dry portion of the grid, while 2 m to the seaward, activity wasnormal with crab densities of 33.6/m2 (± 7.68) and fish actively hunting. That substrate wetness is a necessary prerequisite for crab activity is supported by the factthat their deposit feeding activities are not possible on dry mud.

Periophthalmus waltoni spent more time on the surface (351.6 ± 174.7 sec; seealso Fig. 2) than in their burrows (42.1 ± 56.9 sec). However, within the range oftemperatures acceptable for mudskippers' activity, ambient temperature has noeffect because the fish neither reduced the mean time spent on the surface norincreased that spent in the burrow as the temperature increased. The availability ofsurface water, which the mudskippers often entered, did not increase the time theyspend on the surface at higher ambient temperatures. Wind speed and overall timespent in both the burrow and pools of water, however, were positively correlated (r= 0.503, P = 0.004). The mean times spent in inactivity, movement or in comfortbehaviour were also not affected by the ambient conditions. The only significantrelationship was that the duration of comfort behaviour increased with that ofmovement (r = 0.636, P = 0.001, n = 31), when typically a fish moving by crutching(on pectoral and pelvic fins, cf. Harris 1961) would pause and perform lateral rolls(= turning behaviour, Ip et al. 1991) to one or both sides.

'o Ai

a) 360CO

CD

co 270-

Timeonsu CD00OO

T

-

1

1

CD

£ 4£tob

2

! ! •

B !• • •

•

!

• i • i

r---^-;

•: 1 *•1

•

•

•

*! * !! ! •

1 1

Hunting Hunt to BurrowNo Hunting Burrow to Hunt

0 2 4 6 8

Distance from first to second Hunt

Fig. 2. — Hunting behaviour of Periophthalmus waltoni. A: the duration of inter-burrow intervalswith and without hunts (mean ± SE). Pre- and post-hunt times are also shown. B: scatter-plot ofdistance and direction between successive hunts. The second hunt is plotted relative to the positionof the first, which is indicated by the cross on the 4 m intersection gridlines.

Surface activity of Periophthalmus waltoni 245

Hunting activity

The capture sequence of hunting was easily recognised. Supported on pectoral and pelvic fins, the mudskippers flex their tails to one side forming their bodies into a variably acute T shape. By quickly straightening the tail, the fish leaprapidly at their prey. Hunting, as defined by this event, was not correlated to crabdensity or any environmental variable, including the state of the tide. Furthermore,mudskippers spent significantly longer on the surface when they were hunting thanwhen they were not hunting (Fig. 2A: matched pairs t-test, t = 5.18, df = 24, P <0.001). Following a crab-capture attempt, the fish usually returned quickly to burrows or pools where water was available. This behaviour is reflected in the significantly shorter time spent on the surface after a hunt than before it (Fig 2A: t =4.174, df = 24, P < 0.001).

Except when they moved towards or away from neighbouring fish, the movement of P. waltoni within their home range as they hunted appeared to be random.However, this apparent randomness may simply reflect the difficulty of identifyingeither all instances of stalking behaviour or the fishes' specific target prey. Successive hunting events were both spatially and temporarily separated. The mediandirect distance between one hunt and the next was 2.3 m (range 0.7 to 4.5 m, n =41; Fig. 2B). This often involved circuitous routes in a direction away from the previous capture point and a variable length of time from as short as 107 sec up toover 30 min (maximum 3258 sec; n = 58, median 696.7 sec).

Video analysis showed that undisturbed crabs normally are active on the surface for a median duration of 299 sec (range 178-584 sec, n = 62) and only returnto the burrow for short periods (28.55 sec, 5.5-78.6 sec, n = 26). After being disturbed by a hunt in the immediate vicinity of their burrows, however, theyremained below ground for several minutes (median duration 480 sec, range 77-1088 sec, n = 13; Whitney-Mann z = 5.004, P < 0.001).

DISCUSSION

Activity and environmental conditions

The temperature range to which P. waltoni is exposed in Sulaibikhat Bayexceeds that of most of other mudskippers (Tytler & Vaughan 1983, Clayton 1993,Ikebe & Oishi 1997). The lower limits are well established and the re-emergencedata of P waltoni in the present study are similar to that recorded by Tytler &Vaughan (1983). However, as a maximum surface temperature recorded in boththese studies was below 40 °C, neither study directly established the upper limitsand these have been explored only experimentally. When P. waltoni were kept inaquaria with water at 38-39 °C, most became comatose after 9 min and survivaltime decreased with increasing temperature, until at 42 °C it was only 48 sec (Al-Naqi 1977, El-Zaidy et al. 1979).

For surface water on the mudflat to reach 38 °C would require air temperature to be well in excess of 40 °C. Nevertheless, fish would be able to thermoregu-late either by evaporative cooling or by shuttling back and forth between the openmudflat and their burrows, options not available in the laboratory setting. Since

246 D.A. Clayton and R. Snowden

midday temperatures in October are similar to early morning and evening temperatures in the hottest months (cf. July, Fig. 1), it is also possible that fish may shifttheir activity periods accordingly. Further reduction in the period of exposure isachieved by the migration of P. waltoni to a lower position on the shore during hotmonths (Al-Taher 1990, Clayton 1993). Additionally, the degree of exposure tohigh temperatures is somewhat ameliorated by the local tidal conditions. The diurnal tides are unequal and in the hottest summer months the shorter period (3 hr)of tidal exposure occurs during the day while the longer (7 hr) is at night when thetemperatures are lower (see Fig. 1; Jones & Clayton 1983).

Whatever the accommodations made at high temperatures, the absence ofbehavioural changes (increased inactivity or pool and burrow sojourns at highertemperatures) indicates an apparent disregard in P. waltoni for changing environmental conditions. The preference for spending time on the surface is, however,supported by Gordon et al.'s (1968) comparison with mudflat and mangrovedwelling P. sobrinus (= kolalo Lesson 1830 or argentilineatus Valenciennes 1837).The mudflat specimens preferred to spend the majority of their time out of wateroccasionally seeking brief contact with it at about hourly intervals.

Behavioural homeostasis

Thermoregulatory mechanisms of mudskippers clearly include shuttlingbehaviour and evaporative cooling (Tytler & Vaughan 1983). There is also the general assumption that comfort movements, including rolling (Stebbins & Kalk 1961,Ip et al. 1991) and pectoral fin flapping of the opercular cavity (Stebbins & Kalk1961), may assist in behavioural thermoregulation. Increases in environmental temperatures should then lead to increases in such activities, but in the present study,no correlation between temperature, wind speed or relative humidity and either thenumber or duration of such movements was found. Similarly Yang Ka Yee (1996)reported that the frequency of rolling behaviour in Boleophthalmus pectinirostrisLinneaus 1758 did not change despite a 9 °C change (29-38 °C) in mud surfacetemperature during the day. While some lateral rolls may be considered to be displacement activities (Brillet 1975), the function of others, of longer duration,remains in question. Perhaps, as suggested by Stebbins & Kalk (1961), rolling (andpectoral waving) primarily assist in the mudskippers' respiratory and not its thermoregulatory functions. This reinterpretation is in accordance with Ikebe & Oishi's(1996) claim for mudskippers' clinging behaviour on vertical surfaces subject tosplashing, which Tytler & Vaughan (1983) attributed solely to thermoregulation.Certainly the finding that the duration of burrow and pool sojourns in P. waltoniincreased with increased wind speed, but not temperature, supports the respiratoryfunction. Dry skin is an ineffective respiratory surface and actions like rolling andpectoral waving moisten that portion of the skin identified as being respiratory innature (Schottle 1932). Further support is provided by the demonstration thatBoleophthalmus boddarti Pallas 1770 increased rolling behaviour to the same sideas that to which a drying stream of air was directed (Ip et al. 1991). Observationson rolling behaviour in B. boddarti and Periophthalmodon schlosseri (Pallas 1770)(Swennen et al. 1995) accord with this view. Furthermore, since mudskippers havevery sophisticated behavioural mechanisms for thermoregulation (above) and forosmoregulation (Gordon et al. 1985, Clayton 1993) it is possible that similarbehavioural homeostatic mechanisms also may exist for respiratory requirements.

Surface activity of Periophthalmus waltoni 247

Foraging strategies

As hunting in P. waltoni is not correlated with prey encounter rates as measured by crab density, it seems that a sufficient explanation of when the mudskippers hunt is that both fish and the small ocypode crabs operate within similar environmental temperature ranges. However, fish that are hunting spend longer on thesurface than when not hunting, but then quickly returned to their burrows (orpools) following the hunting event. This rapid transition between activities may bean example of operational behavioural disinhibition (McFarland 1993) where thecessation of one activity (hunting) permits the expression of another (inhibited)one. Without experimental manipulation this remains a moot point, as doeswhether this incompatible activity is thermoregulatory, osmoregulatory or respiratory in nature.

Mudskippers increase their foraging efficiency by conducting successive hunting trips in different areas of the mudflat because their prey remain in their burrows longer than normal following a hunt in their immediate vicinity. Otheraspects of optimal foraging that are amenable to study in carnivorous mudskipperswould include prey and patch selection. For example, it would be expected thatPeriophthalmus waltoni should exhibit different search strategies for prey of different profitability. N. dotilleformis (Snowden & Clayton 1995) and /. stevensi (Snowden et al. 1994) are probably the most and least profitable ocypodids available forthe fish. At spring tide in the Kenyan mangroves female P. sobrinus are more selective than males (Colombini et al. 1996) and an investigation of their foragingbehaviour should show that the strategies adopted by the sexes are very different.

ACKNOWLEDGEMENTS

We thank R. Gibson for comments on an earlier draft. This work was supported byGrant SZ032 from the University of Kuwait.

REFERENCES

Al-Kulaib A.M. 1975. Weather and Climate of Kuwait. Kuwait: Director General of Civil Aviation, Meteorological Section, 82 pp.

Al-Naqi Z.A. 1977. Ecological and physiological studies on the mud-skipper fish, Periophthalmus chrysospilos inhabiting the muddy shores of Kuwait. M.Sc. Thesis, Zoology Department, Kuwait University, Kuwait, 133 pp.

Al-Taher E.Y. 1990. The impact of the Doha West Power Station effluent on the upper eulit-toral benthos of western Sulaibikhat Bay, Kuwait. M.Sc. Thesis, Zoology Department,Kuwait University, Kuwait, 265 pp.

Barak N.A.E., Salman N.A. & Ahmad S.M. 1994. The piscivorous feeding of mudskipper Periophthalmus waltoni Koumans from Khor Al-Zubair, north-west Arabian Gulf. PakistanJournal of Zoology 26: 280-283.

Brillet C. 1975. Relations entre territoire et comportement agressif chez Periophthalmussobrinus Eggert (Pisces, Periophthalmidae) au laboratoire et en milieu naturel.Zeitschrift fiir Tierpsychologie 39: 283-331.

Berti R., Chelazzi L., Colombini I. & Ercolini A. 1992. Direction-finding ability in a mudskipper from the delta of the Tana river (Kenya). Tropical Zoology 5: 219-228.

248 D.A. Clayton and R. Snowden

Berti R., Colombini I., Chelazzi L. & Ercolini A. 1994. Directional orientation in Kenyanpopulations of Periophthalmus sobrinus Eggert: experimental analysis of the operatingmechanisms. Journal of Experimental Marine Biology and Ecology 181: 135-141.

Clayton D.A. 1987. Why mudskippers build walls. Behaviour 102: 185-195.Clayton D.A. 1993. Mudskippers. Oceanography & Marine Biology, An Annual Review 31:

507-577.

Clayton D.A. & Vaughan T.C. 1986. Territorial acquisition in the mudskipper Boleophthalmusboddarti (Pisces: Gobiidae) on the mudflats of Kuwait. Journal of Zoology, London (A)209: 501-519.

Clayton D.A. & Vaughan T.C. 1988. Ethogram of Boleophthalmus boddarti (Teleostei: Gobiidae), a mudskipper found on the mudflats of Kuwait. Journal of the University ofKuwait (Science) 15: 115-138.

Colombini I., Berti R., Ercolini A., Nocita A. & Chelazzi L. 1995. Environmental factors

influencing the zonation and activity patterns of a population of Periophthalmus sobrinus Eggert in a Kenyan mangrove. Journal of Experimental Marine Biology and Ecology190: 135-149.

Colombini I., Berti R., Nocita A. & Chelazzi L. 1996. Foraging strategy of the mudskipperPeriophthalmus sobrinus Eggert in a Kenyan mangrove. Journal of Experimental MarineBiology and Ecology 197: 219-235.

Crowder L.B. & Magnuson J.J. 1983. Cost-benefit analysis of temperature and food resourceuse: a synthesis with examples from the fishes, pp. 189-221. In: Aspey W.P. & LustickS.I., Edits. The cost of survival in vertebrates. Columbus: Ohio State University Press,300 pp.

El-Zaidy S., Eissa S.M. & Al-Naqi Z. 1979. Ecological studies on the mud-skipper fish Periophthalmus chrysospilos (Bleeker) in Kuwait. Bulletin of the Faculty of Science Cairo University 48 (1975): 113-134.

Gordon M.S., Boetius J., Evans D.H. & Oglesby L.C. 1968. Additional observations on thenatural history of the mudskipper, Periophthalmus sobrinus. Copeia (4): 853-857.

Gordon M.S., Gabaldon D.J. & Yip A.Y.-W. 1985. Exploratory observations on microhabitatselection within the intertidal zone by the Chinese mudskipper fish Periophthalmus can-tonensis. Marine Biology 85: 209-215.

Harris V.A. 1961. On the locomotion of the mudskipper Periophthalmus koelreuteri (Pallas)(Gobiidae). Proceedings of the Zoological Society of London 134: 107-135.

Hart P.J.B. 1986. Foraging in teleost fish, pp. 211-235. In: Pitcher T.J., Edit. The behaviour ofteleost fish. London: Croom Helm, 560 pp.

Holthuis L.B. 1995. The identities of Macropththalmus rouxii Lucas, 1836, and M. dentipesLucas, 1836, and the substitution of the latter name for M. pectinipes Guerin, 1838(Decapoda, Brachyura, Ocypodidae). Crustaceana 68 (3): 401-403.

Hughes R.N. 1988. Optimal foraging in the intertidal environment: evidence and constraints,pp. 265-282. In: Chelazzi G. & Vannini M., Edits. Behavioural adaptation to intertidallife. New York: Plenum, 524 pp.

Hurlbert S.H. 1984. Pseudoreplication and the design of ecological field experiments. Ecological Monographs 54 (2): 187-211.

Ikebe Y. & Oishi T. 1996. Correlation between environmental parameters and behaviour during high tides in Periophthalmus modestus. Journal of Fish Biology 49: 139-147.

Ikebe Y & Oishi T. 1997. Relationships between environmental factors and diel and annualchanges of the behaviours during low tides in Periophthalmus modestus. Zoological Science, Tokyo 14: 49-55.

Ip Y.K., Chew S.F. & Ping C.T. 1991. Evaporation and the turning behaviour of the mudskipper Boleophthalmus boddearti. Zoological Science, Tokyo 8 (3): 621-624.

Jones D.A. & Clayton D.A. 1983. The systematics and ecology of crabs belonging to the genera Cleistostoma DeHaan and Paracleistostoma DeMan on Kuwait mudflats. Crustaceana45: 183-199.

MacNae W. 1968. A general account of the fauna and flora of mangrove swamps and forestsin the Indo-West-Pacific region. Advances in Marine Biology 6: 73-270.

Surface activity of Periophthalmus waltoni 249

McFarland D. 1993. Animal behaviour: psychobiology, ethology and evolution, 2nd Edition.Harlow: Longman Scientific and Technical, 585 pp.

Mhaisen F.T. & Al-Maliki N.S. 1996. Parasites, diseases and food of the dark-blotched mudskipper Periophthalmus waltoni (Perciformes: Gobiidae) in the Khor Al-Zubair estuary(Iraq). Zoology in the Middle East 13: 85-87.

Schottle E. 1932. Morphologie und Physiologie der Atmung bei wasser-, schlamm- undlandlebenen Gobiiformes. Zeitschrift fiir Wissenschaftliche Zoologie 140: 1-114.

Snowden R.J., Al-Taher E.Y. & Clayton D.A. 1994. Aspects of the ecology of Tylodiplax indicaAlcock (Brachyura: Ocypodidae) on a Kuwait mudflat. Journal of the University ofKuwait (Science) 21: 219-228.

Snowden R.J. & Clayton D.A. 1995. Aspects of the life history and seasonal ecology of Nasi-ma dotilleformis Alcock (Brachyura: Ocypodidae) on a Kuwait mudflat. Journal of theUniversity of Kuwait (Science) 22: 84-94.

Snowden R.J., Clayton D.A. & Al-Taher E.Y. 1991. Population biology of Ilyoplax stevensi(Kemp) (Brachyura: Ocypodidae) on a Kuwait mudflat. Marine Ecology Progress Series71:219-225.

Stebbins R.C. & Kalk M. 1961. Observations on the natural history of the mud-skipper Periophthalmus sobrinus. Copeia (1): 18-27.

Swennen C, Ruttanadakul N., Haver M., Piummongkol S., Prasertsongskum S., Intanai I.,

Chaipakdi W., Yeesin P., Horpet P. & Detsathit S. 1995. The five sympatric mudskippers (Teleostei: Gobioidea) of Pattani area, southern Thailand. Natural History Bulletinof the Siam Society 43 (1): 109-129.

Tytler P. & Vaughan T. 1983. Thermal ecology of the mudskippers Periophthalmus koelreuteri(Pallas) and Boleophthalmus boddarti (Pallas) of Kuwait Bay. Journal of Fish Biology 23:327-337.

Wilkinson L. 1990. Sygraph: the system for graphics. Evanston, Illinois: SYSTAT Inc., 547 pp.Yang Ka Yee J. 1996. The feeding ecology of the mudskipper Boleophthalmus pectinirostris

(Pisces: Periophthalmidae) at the Mai Po Marches nature reserve, Hong Kong. M.Ph.Thesis, Faculty of Science, University of Hong Kong, 110 pp.