The Biology of Upogebia pusilla (PETAGNA) (Decapoda, Thalassinidea) : II. Environments and Zonation

P.S.Z.N. I: Marine Ecology, 8 (4): 337-358 (1987) 0 1987 Paul Parey Scientific Publishers, Berlin and Hamburg

Accepted: September 30,1987

ISSN 0173-9565

The Biology of Upogebia pusilla ( PETAGNA) (Decapoda, Thalassinidea) I I . Environments and Zonation PETER C. DWORSCHAK

Institute of Zoology, University of Vienna, AlthanstraRe 14, A-1090 Vienna, Austria.

With 7 figures and 4 tables

Key words: Upogebia piuilla, Decapoda, Thalassinidea, Mediterranean, intertidal, sediments. zonation.

Table of contents 338 Problem 338 Material and Methods 338 1. Study sites 338 a. Lagoon of Grado 340 b. Lido di Staranzano 340 c. Val Saline, Rovinj 341 d. Aurisina 341 341 3. Distribution 342 Results 342 1. Physical parameters 342 a. Lagoon of Grado 344 b. Lido di Staranzano 346 c. Val Saline, Rovinj 346 d. Aurisina 346 2 . Hole densities 346 a. Lagoon of Grado 349 b. Lido di Staranzano 350 c. Vat Saline, Rovinj 350 d. Aurisina 350 Discussion 350 1. Densities 352 2. Zonation patterns 355 Summary 355 Acknowledgements 356 References

2 . Edaphic and climatic parameters

Abstract. The distribution of the thalassinidean shrimp Upogebiapusilla was studied at four sites in the North Adriatic Sea: 1) a tidal flat in the lagoon of Grado, 2) a tidal flat at Lido di Staranzano near the mouth of the Isonzo, 3) a mud flat seawards of a salt marsh in a protected bay north of Rovinj, and 4) a sublittoral station in 6 m depth near Aurisina. Information on grain size distribution, organic content, amount of debris, redox profiles and pH of sediment as well as temperature and salinity is given. Density, as determined by hole counts and a hole :burrow

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338 DWORSCHAK

relationship derived from resin casting, generally increased with increasing water depth in the intertidal. The upper limits ranged between + lOcm (Rovinj) and - 20cm (Grado); densities between mean water and low water level varied strongly due to microtopography and macrophyte cover. Maximum densities in the intertidal ranged from 189 (Grado) to 2420 (Rovinj, juveniles) animals. m-*. Shrimp density at the sublittoral station ranged between 80 and 230. maZ. The zonation of the Upogebiidue and Calliunussidue with respect to environmental parameters is discussed.

Problem

The Thalassinidea (Decupoda) are among the most common burrowing organ- isms in eu- and sublittoral sediments; they are found - sometimes in very high densities - from the intertidal zone down to at least the shelf break and in all types of environments from brackish to euhaline. In the Mediterranean Sea, Upogebia pusilla is the most common member of

the family Upogebiidae. It occurs in the East Atlantic from Mauretania in the south to Brittany in the north (DE SAINT LAURENT & LELOEUFF, 1979), reaching as far north as Norway (PESTA, 1918; BOUVIER, 1940; ZARIQUIEY ALVAREZ, 1968). The species is common all around the Mediterranean including the Black Sea and has been reported from the Red Sea (MONOD, 1930). U. pusilla occurs in high densities, especially in lagoons where its ventilation

activity contributes significantly to the turnover of lagoonal water through the sediment (DWORSCHAK, 1981). In this respect, the knowledge of population density and zonation within these environments is important for quantifying the bioturbation effects of this species.

This study, which is the second of a series dealing with the biology of Upogebia pusilla, describes four environments in the Northern Adriatic Sea populated by this species and investigates the zonation of this shrimp in these environments.

Material and Methods

1. Study sites

a. Lagoon of Grado

The lagoon of Grado is situated in the northernmost part of the Adriatic Sea between the mouths of the rivers Tagliamento and Isonzo (45’40’33” to 45”45’39”N and 13”05‘08” to 3525‘08”E) (Fig. 1). The lagoon was formed 4000 to 5000 years ago by a postglacial sea level rise. Several theories have been forwarded to explain the origin of the littoral belt of islands which separates the lagoon from the open sea (BRAMBATI, 1969; MACHIN, 1979). The lagoon has a length of 32 km, a breadth of 5 km, and covers an area of 16,ooO ha.

BRAMBATX (1969) divided the lagoon morphologically into 3 zones: 1) areas above the mean high water level:. “barene” (marshes), “cordoni litorali” (littoral belt of

2) areas between the mean levels of low and high water: “piani di marea” (tidal flats); 3) areas below the mean water level: “canali” (channels), “bocchi lagunari” (inlets), and “paludi”

DORIGO (1965) separated the lagoon into 5 basins, each of which are in exchange with the open

islands), and “costi” (coasts);

(inner pacts of the lagoon).

sea by a separate mouth. More or less stable water sheds exist between these basins.

Environments and zonation of Upogebia pusilla 339

B

20km - 1:

Northern Adriatic

Sea

0

RatacKrii Uvala Saline

a \

Rovinj

Ratac Kurent

a

A N

Fig. I . Study sites (arrows) in the Northern Adriatic Sea (A); B: detail of area around Rovinj; C: detail showing lagoon of Grado-Marano between Tagliamento (T) and Isonzo (I) with its mouths Lignano (L), Aussa (A), Buso (B), Morgo (M), Grado (G), and Primero (P); Ma: Marano, S: Lido di Staranzano, Mo: Monfalcone, Au: Sorgenti di Aurisina.

The mean tidal range in the lagoon is 65cm; it can reach 105cm at spring tides (DORIGO, 1965). The salinity of the lagoonal water varies according to region and depends mahly on actual water

level, freshwater runoff, and precipitation. FAGANELU (1956) measured salinities between 23 and 33%0. BRECANT & CATALANO (1978) measured a maximum salinity of 36%0 in February at Boccha Fosa (or Grado) and a minimum of 16%0 at Boccha Primero in March; near the mouth of small rivers entering the lagoon in the Marano-part, values of 3.4%0 have been measured.

The pH of the lagoonal water vanes between 7 and 8.5 (FAGANELLI, 1956; BRAMBATI, 1969). pH is lower (mean of 7.65) in the western than in the eastern part (mean 7.9). Here, maximum values of 8.5 due to lack of water exchange have been measured (BRAMBATI, 1969).

The temperature of lagoonal water shows great daily variations due to changing water depth. Fig. 2 presents mean temperature at Boccha Primero as measured by DELPIERO et al. (1978). The maximum temperature was 28°C in July and the minimum temperature 0°C in December. BREGANT & CATALANO (1978) measured maxima between 24 and 27 "C in August and minima of 6 to 7 "C in December at Boccha Fosa and Boccha Primero. In winter, formation of ice may occur below 0°C in regions with low water movements (BRAMBATI, 1969).

The mean precipitation in the lagoonal region is 1084mm per year (GENTILK, 1964). The winds occurring in the lagoonal region include Greco Levante (or Bora) from N and NE,

DWORSCHAK

Fig.2. Temperature course of the lagoonal water at the mouth Primero between November 1975 and Oc- tober 1976. Solid line: mean temperature of 5 days, vertical bars represent ranges (after DEL PIERO et af., 1978). Points indicate temperature values of the author’s measurements at the study site in 1977 and 1978.

340

O C

25.

20.

I5 -

‘ 1 1 ’ 1 2 ’ 1 2 3 ’ 4 5 ’ 6 ’ 7 ’ 8 9 ’ 1 0 ’ tom

Scirocco from SE, Osteo from S. Libbecio from SW, and Ponente from E. Bora has the greatest influence on currents and tidal height (BRAMBATI, 1969).

The sediments of the Grado-Marano lagoon have been investigated in detail by BRAMBAII (1969). Sediment composition vanes according to current regimes: at the mouths, carbonate sand, which becomes finer towards the inner parts, prevail. In the inner parts, sandy to clayey silts dominate. Carbonate content decreases inwards from 90 to 30 %, and the sediment becomes less sorted. Well sorted sediments prevail in regions with uniform water movements such as channels and the inner parts of the lagoon; transitional zones with varying water movements, however, are characterized by poorly sorted sediments. The mineralogical composition and recent sedimentation is mainly influenced by the rivers Tagliamanto and Isonzo.

The present study was undertaken on a tidal flat in the eastern part of the lagoon which is under influence of Boccha Fosa (Fig. 1 C). The flat lies north of the artificial fish pond “Cimitero” and is limited by the Canale “Rio della Parmcca”.

b. Lido di Staranzano

Lido di Staranzano is situated south of Monfalcone just before the mouth of the Isonzo (Fig. 1 C). The tidal flat (0.5 to 2 km wide from HHWL to LLWL) is characterized by numerous patches of Spartinu marifima near the high water level and by a patchy to dense cover of Zosferu noltii around the mean water level. The sediment surface near the low water line shows no vegetation; here ripple marks and sand bars can be observed. Below the low water line, a dense meadow of Cyrnodocea nodosa begins (SIMONETI?, 1973).

The tidal range is 10 % higher than in Grado (ANONYMOUS, 1976). The sediment is muddy fine sand with a carbonate content between 59 and 62% and median

grain sizes between 50 and 100 pm; they originate from recent sedimentation, mainly influenced by the Isonzo (BUMEATI & VENZO, 1967).

c. Val Saline, Rovinj

Val Saline is situated in a protected bay south of the Limski Kana1 (N of Rovinj, Istria, Yugoslavia) (Fig. 1 B). Several deep channels reach into an Arthrocnernum-marsh in the inner part of the bay. Seawards of the marsh lies a small tidal flat which is densely covered by Zostera noltii and Cyrnodocea nodosa. The deeper channels extending into the marsh are also populated by Cy- modocea.

The tidal range is between 0.7 and 1 m (HINZE & MEISCHNER, 1968), being 70 % that of Grado according to ANONYMOUS (1976); On er al. (1976) mention a tidal range of only 0.4m during their investigation period.


The pH of the water ranges between 8.2 and 8.4, that of the sediment between 8.4 and 8.7; deeper sediment layers have a pH of 7.3 to 8.0 (PAUL, 1970).

Water temperature ranges between 7.5 “C in February and 26°C in August, salinities between 36 and 38%0. No freshwater influence other than a yearly precipitation of 1500mm exists (HINZE & MEISCHNER, 1968).

The sediment is a terrigenous red clay with an organic content of 7-9 % ( O n er al., 1976).

d. Aurisina

Aurisina is located 1 km north of the Laboratorio di Biologia Manna between Monfalcone and Trieste (Fig. 1). A zone of boulders reaches from the low water line of the beach to a depth of 4m. A 10 to 20m broad Cymodocea nodosa meadow then extends to a depth of 6m. This is followed by a bare zone populated by U. purilla; it extends 200 m offshore to 9 m depth. In this zone sediment samples were taken in July 1983, holes counted and animals captured with an air lift sampler in August 1984, and resin casts made by P. PERVESLER in July 1983 and August 1984.

2. Edaphic and climatic parameters

Sampling at Grado and Staranzano was carried out along transects perpendicular to the shore-line, reaching from the high to the low water level. Water depth was determined at marked positions at mean water level. The depth of stations outside the transects was estimated in relation to actual water level using the “Previsioni di Marea” (ANONYMOUS, 1976) and that of the marked positions. Two square metres were marked at Grado in May 1977 and April 1978.

At Grado, 250ml of sediment were taken from the surface in December 1977; in April 1978, 2501x11 each from the surface and from 30cm sediment depth were taken in 10 m intervals along the transect. At Staranzano samples were taken along the transect in 100 m intervals in May 1983 using box cores (HERTWECK, 1974). Sediment analysis was performed as outlined by BUCHANAN (1984).

The organic content of the sediment was determined as weight loss on ignition at 450°C for 4 h in a muffle furnace.

Redox profiles in the sediment were measured with a platinum wire electrode against a calomel electrode (Ingold or Seibold CFG) using a KNICK-Portamess 902 or Seibold GPT pH-meter as a millivolt-meter. A combined glass electrode connected to the pH-meter was used for determining the pH of water and sediment. Water and sediment temperature was measured using a calibrated thermometer, salinity determined using a refractometer (American Optical).

Time of exposition during low water was calculated for lOcm depth zones using tide tables (ANONYMOUS, 1976).

3. Distribution

The density of Upogebiapusilla was determined indirectly by counting holes on the sediment surface along or next to transects. Different methods were used: In November 1977 and April 1979 a %6 mz frame was thrown randomly near the marked positions and the holes counted. In December 1977 a 1 m1 frame with 100dm* subdivisions was used and the holes in these subdivisions counted. To minimize working time in siru a camera equipped with a 28 mm wide angle lens was mounted on top of a pyramidal frame. This pyramid, whose base measured 1.1 x 1.1 m, used at Grado in July and October 1978 and at Staranzano in May 1983, yielded overlapping photographs of a 1 m wide strip of the sediment surface from the high water to the low water line.

The number of holes in the 100dmz subdivisions (counted in siru or on photographs) were evaluated in frequency distributions. The variance and mean number of holes were compared using the variance to mean ratio and agreement with a Poisson distribution tested using a Chi-squared test (ELLIOTT, 1977).

The densitiy of juveniles was estimated by taking box cores (HERTWECK, 1974).

342 DWORSCXAK

Results

1. Physical parameters

a. Lagoon of Grado

Table 1 shows the mean and maximum duration of emergence of th.e different depth zones. Whereas the -20 cm zone is exposed every day at least once - with a maximum continuous duration of emergence of 6 h - the -60 cm zone does not fall dry in some months; the maximum duration of emergence in the latter zone is 2.5 h.

Salinity during low water ranges between 24%0 (July) after rain and 36%0 (May), with a mean of 27.7%0. The salinity of the water in the burrows of U.pusilIa does not differ from that of the overlying water, even after longer period of emergence (3 h in summer).

The mean pH of the water is 8.27, that of the sediment surface 8.03. It decreases rapidly to 7.6 in 1 cm sediment depth and fluctuates between 7 and 7.5 down to 5cm. The pH of the burrow water (7.87) is significantly different (p < 0.05, MA"-WHITNEY test) from that of both the overlying water and the sediment surface.

The redox-profiles (Eh between + 222 and + 337mV) show that the sediment is well oxygenated on the surface. There is a rapid decrease down to values between + 74 and + 137 mV in the first 2 cm, followed by a slower drop with increasing sediment depth down to between + 19 and - 1 mV (Fig. 3).

Water temperatures measured at Grado are in good agreement with those observed by DELPIERO et al. (1978). Great daily variations were observed, e. g., in May, when temperatures rose from 17.2 to 21.2"C between 6:OO and 9:00 a. m., and in July when they rose from 22.7 to 25.6"C between 6:OO a. m. and

Table 1. Cumulative monthly (left column), mean daily (right column), and maximum continuous time [h] of emersion during low tide of the 10cm depth zones in 1977 (calculated after ANONYMOUS, 1976).

depth zone 20 cm 30 cm 40 cm 50 cm 60 cm

January 31 4.4 23 4.2 20 3.2 13 2.6 5 1.8 February 37 3.6 19 3.8 14 3.3 11 2.2 1 1.0 March 45 3.7 32 2.9 19 1.9 4 1.4

May 42 3.9 25 3.8 20 3.0 14 2.1 3 1.5 June 29 4.9 23 4.3 20 3.4 15 2.5 7 1.6 July 29 5.0 25 4.2 21 3.3 16 2.5 7 1.7 August 43 4.0 29 3.5 18 2.9 12 1.9 1 1.5

October 44 3.7 30 3.0 15 2.7 8 1.8 November 38 3.9 23 3.9 18 3.2 13 2.2 4 1.7 December 30 5.1 25 4.1 19 3.5 13 2.7 7 1.8

maximum 6.0 5.5 4.5 4.0 2.5

April 45 3.9 30 3.2 15 2.3 5 1.5

September 45 3.9 33 2.9 21 1.8 1 1.0

Environments and zonation of Upogebia purilla 343 Fig. 3. Eh-profiles of sediments. 1: LagoonofGrado,Aprill978;2: Val Saline, Rovinj (after On ef al., 1976); 3: Lido di Staranzano, Apn! 1978 (at = m80); 4: Lido di Staran- zano, May 1985 at m350.

1:OO p. m. In December, the water temperature remained between 6 and 7°C the whole day.

The temperature of the sediment during submergence is between 0.9 and 2.4"C below that of the overlying water. Longer emergence (3h) and sunshine leads to a temperature increase of 2°C.

Data on sediment grain size distribution are summarized in Table 2. Samples taken in December 1977 show small-scale variations: Up to a water depth of 40 cm, fine sand with a sand fraction (> 63 pm) between 87 and 91 % and a silt and clay fraction between 9 and 12.4% is present. The median grain size is 177pm and the sorting is moderate. A t a depth of 49cm the sand fraction decreases to 66 %, the median grain size becomes smaller (144 pm), and the sediment is poorly sorted. At 53cm, the sediment consists to 57% of silt and clay, the median grain size is 38 pm, and the sediment is poorly sorted. Samples taken in April 1978 show less variation with increasing water depth - the sediment is well sorted and consists mainly of fine sand with a median grain size of 176 pm. There is only a slight decrease of the fraction > 500 p m and a slight increase of the silt and clay fraction with increasing water depth. Only in one station (A in April 1978) was the sediment in 30cm different from that of the surface in having twice as much fine fraction (< 63 pm).

The mean organic content of the sediment ranges from 3.5 to 6.4 % (Table 2) and increases slightly with water depth. The mean organic content in 30cm sediment depth is always lower than on the surface.

344 DWORSCHAK

Table 2. Grain size distribution of sediments from the lagoon of Grado and Rovinj as % weight retained on sieve. Median grain size (Md[pm]) and organic content.

Grado Grado Rovinj' December 1977 April 1978 June 1978

Position I I1 111 IV V Ao At Bo Bt Co Ct depth [cm] -21 -32 -41 -49 -53 - 20 - 36 - 50 - 40

> 500 pm 1.1 1.8 1.9 2.3 1.1 0.3 0.1 2.4 2.8 0.8 2.1 0.1 0.1 >250pm 18.1 20.1 18.4 7.2 3.8 20.0 21.1 20.5 19.7 9.8 10.6 1.1 0.7 >125um 69.0 63.6 64.4 49.7 22.1 66.3 57.5 55.5 55.3 63.3 61.8 1.9 1.5 > 63pm 2.8 3.8 3.6 7.5 15.8 5.0 4.9 4.0 5.3 6.1 5.7 6.1 4.4 < 63pm 9.0 10.5 11.7 33.4 57.4 8.4 16.4 17.6 16.8 20.1 19.8 90.7 93.3 Md [pm] 177 177 177 144 38 176 176 176 176 176 176 23 23 org. cont. [%] 3.68 4.09 4.8 3.5 5.5 4.1 6.4 3.9 7-9

I-V: surface sediment, December 1977; Ao, Bo, Co: surface sediment; At, Bt, Ct: sediment in 30cm depth, April 1978. ' After On et al., 1976.


The salinity of the overlying water ranges from 20 to 36700, pH between 7.5 and 8.4.

The redox-profiles show that the sediment is well oxygenated on the surface, with Eh values between f 340 and + 381 mV. At station m80 (80m from HHWL), Eh rapidly falls from + 340mV at the surface to + 177 mV in 1 cm depth, reaching 0 mV in 3.5 cm. At m 350 near the low water line, Eh in 3.5 cm is still + 100mV, steadily dropping to OmV in 7cm.

Table 3. Grain size distribution of sediments from Lido di Staranzano and Aurisina as % weight retained on sieve; median grain size (Md[pm]) and organic content (as % weight loss on ignition).

Staranzano Position HWL m 80

sediment depth [cm] 0-6 6-1 5 15-25 0-10 10-20 20-27

> 8000 fim > 4000 pm 0.249 > 2000 pm 0.011 0.093 0.030 >1000prn 0.043 0.014 0.058 0.053 0.101 0.069 > 500fim 0.092 0.013 0.110 0.046 0.202 0.107 > 250prn 0.156 0.089 0,264 0.808 1.299 0.575 > 125pm 13.520 8.770 15.350 22.880 8.560 5.921 > 6 3 ~ 66.080 70.140 68.380 70.090 45.180 62.140 < 63pm 20.109 20.974 15.828 6.123 44.565 30.909

water depth [cm] + 20 - 2

Median [pm] 91 88 94 101 70 82 org. cont. [%I 1.61 1.20 3.18 0.82 1.61 3.92


Data of sediment analyses are summarized in Table 3. The sediment is medium sand to silty very fine sand with median grain sizes between 70 and 233 pm. From the high water line to the mean water line, the median diameter decreases and the percentage of the subsieve fraction (< 63 pm) increases; the fraction > 63 pm is the major component. Between m250 and m 400 the median diameter of the sediment rapidly increases to 233 pm, the subsieve fraction decreases to 1 %, and the fractions > 125 pm and > 250 pm become the major components. Great variation in grain size exists with respect to sediment depth. At the high water line, sediment in the upper 20 cm is very similar; at 20 cm the subsieve fraction decreases from 20 to 16 %. At m 80 the subsieve fraction increases from 6 to 44 % between 10 and 20 cm, then falls to 30 % below 20 cm. At m 155 and m 250 the subsieve fraction decreases with increasing sediment depth.

The organic content of the sediment ranges between 0.31 and 3.92 %. With one exception (m 155) the organic content at a sediment depth of 20 cm is higher than at lOcm or at the surface. The mean organic content down to 30cm remains relatively constant (1.85-2.11 %) from the high water line to a water depth of 30cm; it then drops rapidly to 0.3 % near the low water line.

Sieving of box-core samples shows that most of the organic material consists of macrophyte debris (mainly Zosreru); this debris (in g[dw] . m-I) increases with increasing water depth from 976 g at m 80 to 1037 g at rn 155 and 1410 g at m 250; at the same time the amount of shell particles decreases from 1026 g (m 80) to 832g (m 155) and 395g (m250). Only little debris and few shell particles (total: 360g. m-?) occur in the first 30cm of the zone near the low water line (m350), which is characterized by ripples and sand bars.

Table 3 . Continued

Staranzano Aurisina m 155 m 250 m -100 - 8 - 31 - 40 - 600 0-10 10-20 20-30 0-10 1&20 20-30 0-10 0-10

0.071 0.053 0.575 1.110 7.290

52.100 38.801 76 2.01

0.044 0.141 0.272 0.640

11.450 64.690 22.764 89 2.33

0.019 0.048 0.118 1.143

13.490 67.990 17.192 93

1.64

0.125 0.226 0.803 0.874 5.350

77.350 15.272 91

1.55

0.035 0.114 0.362 1.758

23.310 63.600 10.818

1.93 101

0.064 0.144 0.418 2.410

29.300 56.820 10.844

2.08 106

0.01 0.49

40.67 50.78 7.06 0.99

0.31 233

1.354 10.200 21.990 14.780 7.491 3.153 6.322

14.260 20.450

888

346 DWORSCHAK


A salinity of 36%0 was measured at this site. The sediment is a red terrigenous clay with a silt and clay fraction of more than 90% (Table 2). The organic content ranges between 7 and 9 % (Om et al., 1976); a box core taken in July 1983 shows 915 g (dw) of macrophyte debris and 527 g (dw) of shell particles per square metre in the ‘upper 30 cm.

d. Aurisina

The sediment analysis (Table 3) shows a very poorly sorted mixture of gravel, sand, silt, and clay, with a median diameter of 888 ym (mean 313 pm).

2. Hole densities

a. Lagoon of Grado

Hole densities (H . m-I) along the transects are presented in Fig. 4. The foliow- ing common trends are evident: The first holes occur at a water depth of about 20 cm and hole density increases rapidly within a few metres to 100 H m-2 in 30 cm. A gradual increase in density with increasing water depth was registered, although the variation was great due to irregularities of the bottom (Figs. 4 and 5 ) . The highest densities can be observed at a depth of 50cm (417H - and in small troughs.

In 82 % of the cases, hole distribution is random (s2 = R) at low (2 I3 * m-2) as well as at high densities. In 10 % , holes are contagious (s2 > R) at hole densities between 2 and 289 H . m2, and in 8 % distribution of holes is regular (s2 < R) at mean densities between 110 and 234H.m-2.

Hole counts in marked square metres showed only small variations. Square metre No. 1 had 83 He m-’ in April 1978, 102 H - m-2 in July 1978, 78 H . m-* in October 1978, and 89 H m-2 in April 1979. Hole densities in square metre No. 2 were 107 H - m-2 in August 1977, 97 H - m-2 in October 1978, and 78 H - m-’ in April 1979. Differences in densities between successive seasons are not significant (p > 0.05, t-test).

The method used for determining interconnection of burrow holes on the sediment surface (DWORSCHAK, 1983) shows that 98 % of the holes attributed to U. pusillu are in fact burrow openings of this species. Thirteen holes counted in the %m2 frame (estimated density 208 H a m-l) before resin casting belonged to 8 burrows with a total of 19 openings (hole : burrow relation 2.25 : 1); this yields an estimated density of 92 animals - m-*.

Counts on photographs show no significant difference (p > 0.05, t-test) in mean hole numbers between %6m2 and 1 m2 frames.

As seasonal variations in hole numbers are low, the different methods of counting are comparable and hole number mainly dependent on water depth.

Environments and zonation of Upogebia pusilla

Fig.4. Water depth (in cm below mean water level) and hole densities (H . m-') along transects in the Lagoon of Grado. (a): November 1977; (b): December 1977; (c) and (d): October 1978; (e): April 1979. Hole densities in (a) and (e) represent means of 10 counts in %6 m2, vertical bars are 95% confidence intervals; (b) densities in 1 m*-frame in situ: (c ) and (d) counts on photographs taken with the pyramid. I through V in (a) show positions of sediment samples shown in Table 2, arrows in (d) indicate position of photographs shown in Fig. 5.

cm

so.

347

H n - 2

200

200

* C

0 0

200 f

2

200

ZOO

Table 4. Minimum (min), maximum (max), and mean hole densities (H. m-') pooled for lOcm depth zones. Population densities (animals. calculated using a mean hole : burrow relationship of 2.2 : 1 (DWORSCHAK, 1983).

water depth min max mean SD animals . m-z

20-30 cm 0 112 38 29.2 17 3C-40 cm 55 181 112 25.6 51 40-50 cm 90 234 167 54.3 76 5 0 4 0 cm 147 417 224 73.4 102

SD: standard deviation.

All data were therefore pooled in lOcm water depth classes. Mean hole numbers of these zones together with mean number of animals - using a mean hole : burrow-relationship of 2.2 : 1 (DWORSCHAK, 1983) - are summarized in Table 4.

Environments and zonation of Upogebia pusitla


349

Hole densities determined with the photopyramid are presented in Fig. 6 together with water depths along the transect of May 1983. The first holes occur around the mid-water level in mean densities of 4 H . m-2 (maximum 60 H - m-*). At a water depth of 20cm hole density increases to a mean of 35H.m-2

100

50

r-- , I rn 100 200 300

distance from HHWL

Fig. 6. Water depth (in relation to mean water level) and hole densities (mean H . m-2 of three successive metres) along the transect at Lido di Staranzano in May 1985. Arrows indicate positions of sediment samples, horizontal bars range of macrophyte cover by Spnrtina (S) and Zostera (Z).

(maximum 161 H . m-2). Great variations are due to changing microtopography: openings of U. pusifla-burrows are more abundant in water-filled troughs and in Zosrera patches than in elevations and macrophyte-free areas. In the zone near the low water line (- 40 cm at m 400), characterized by medium sand and sand bars, overall hole density decreases. From m217 on, a different type of hole occurs. These funnel-shaped structures have a density of up to 8. m-* (photo- graphic evaluation). Such funnels become more frequent near and below the low water line (from m 350 on), especially at the top and on the seaward side of sand bars, whereas U. pusifla burrows dominate in troughs landwards and between bars. The use of a “yabby pump” similar to that described by MANNING (1975) showed that these funnels are the burrow openings of Callianussa

Fig. 5. Single pictures of the phototransect taken at Grado in October 1978. Number in upper left corner indicates number of frame ( X 1.1 = distance from mean water line). Hole densities are shown in Fig.4d. Note surface irregularities (small troughs in frames 20, 22), cover of Ulva or Enterornorpha (frames 20, 33), grazing traces around CJ. pusilia openings (frame 20) and mounds of Callianassa candida (frame 24).

350 DWORSCHAK

fyrrhena. Single frame counts made in April 1979 further south near the mouth of the Isonzo where the tidal flat is wider and densely populated by Zostera showed densities between 211 and 492H.m-z at 30 to 40cm below MWL (Fig. 7A).


On et uf., (1976) reported densities of U. pusiflu-holes between 310 (10-20 cm below HWL) and 1040H-m-2 (40-50cm below HWL) on tidal flats and densities between 130 and 860 H - m-‘ at channel entrances. The present study yielded densities between 295 and 383 H - m-2 in February 1976 (Fig. 7 B). A box core taken in July 1983 in the same zone showed a high density of very small animals (2420 animals * m-*).

d. Aurisina

Hole number in a O.lm’ frame before suction sampling was 46; a total of 23 animals was captured. The estimated density of 460 H * m-’ corresponds to a density of 230 animals - m-’. Resin casting showed that the 10 holes in one %6 mz frame belonged to 5 burrows (July 1983) and that the 33 holes in one %m2 frame belonged to 20 burrows (August 1984). This is equivalent to an estimated density of 160 and 303 H . m-’, respectively.

Discussion

1. Densities

Hole counts often present the only possibility for estimating the population density of deep-burrowing animals such as Upogebia pusilla. Burrow depths of over l m (Om et al., 1976; DWORSCHAK, 1983) make it impossible to capture these shrimps quantitatively by digging or coring and sieving in the intertidal. In the subtidal, sampling devices such as grabs also do not reach deep enough; even an air lift sampler may not give accurate information on density when animals are situated deep in the sediment - e. g., U. deftaura in winter (TUN- BERG, 1986).

In the case of U. pusilla, hole counts give reliable information on population density. A great number of resin casts combined with suction sampling results in a very constant hole : burrow : animal relationship (DWORSCHAK, 1983) and allows the calculation of population density from hole densities. Problems arise in species with unknown hole : burrow : animal relationships or - as in Cal- lianassa californiensis - when the number of burrow openings per burrow changes with sediment type (MILLER, 1984) or season (POSEY, 1986).

Information on population density derived with more or less quantitative sampling methods exists for approximately 26 species of Thalassinidea. The estimated density of juveniles of U. pusilla at Rovinj (2420 m-’) is the highest

Environments and zonation of Upogebia pusilla 35 1

Fig.7. A: 0.38m2 emerged sediment surface at Lido di Staranzano with burrow openings of Upogebia pusilla (435 H * m-z). Note blades of the seagrass Zosteru; boot imprints demonstrate firmness of the sediment. Frame is 10 x 10cm. B: 0.32 m2 submerged sediment surface at the edge of a channel in Uvaia Saline, Rovinj with burrow openings of U. pusilla at a density of 295 H . m-*. Frame is 25 x 25 cm.

352 DWORSCHAK

ever reported; only the maximum density of C. fimosa (approximately lOOO-m-?) lies in the same order of magnitude, followed by C. cafiforniensis with a maximum of 897 * rn-? (POSEY, 1986).

2. Zonation patterns

In the intertidal zone as well as in the upper sublittoral Upogebia pusifla occurs exclusively in protected environments. Of the three intertidal biotopes described in this study Lido di Staranzano shows the strongest water movement. Judging from wave ripples, the maximum velocity is 45 cm - s-l (ALLEN, 1970 after REINECK & SINGH, 1980). In the lagoon of Grado tidal currents prevail; the maximum current velocity at the mouth is 49 cm - s-I (DORIGO, 1965); in the inner part currents are weaker. The water movement in Val Saline is much lower: a mean velocity of 0.2 cm - s-I can be calculated from the mean grain size (HJULSTROM, 1939 after REINECK & SINGH, 1980). U. pusiffa has been mentioned as a characteristic species within the “Biocoen-

ose des sables vaseux superficiel en mode calme” of upper sublittoral mobile bottoms of the Mediterranean by PBRBs & PICARD (1964); this biocoenosis is protected by a natural reef and the sediment is eroded only superficially. HERTWECK (1973) found U. pusiffa below the wave base in 3 m water depth in the foreshore zone in the Gulf of Gaeta. In the Gulf of Trieste U.pusilfa can be found up to a depth of 8m, e .g . , near Aurisina; deeper muddy bottoms are populated by U. tipica (STACHOWITSCH, 1984; DWORSCHAK, unpublished data).

In the intertidal and upper sublittoral all other species of Upogebia are also found exclusively in protected biotopes such as bays, lagoons, and estuaries.

Species of Caflianassa occur in environments similar to those inhabited by Upogebia; some occur in the same biotope, e. g. , C. candida (at Grado and Staranzano near the mean water line) and C. tyrrhena (at Staranzano near the low water line) with U.pusifla (see also LEGALL, 1969 and On et al., 1976), C. cafiforniensis together with U. pugeftensis (STEVENS, 1929; MACGINITIE, 1935), C. krawsi with U. africana (DAY, 1967; MCLACHLAN & GRINDLEY, 1974; SWINBANKS & MURRAY, 198l), and C. japonica with U. major (UTASHIRO et at., 1972). In all these cases the two genera occur - occasionally with some overlap- in different zones (see below). In addition, the above-mentioned Calfianassa species also occur in more exposed biotopes, e. g., C. tyrrhena (PBRBs & PICARD, 1964; On et al., 1976). C. major, for example, inhabits both protected lagoons and moderately exposed beaches (POHL, 1946; RODRIGUES, 1966), while C. filholi lives in relatively strong exposed beaches (DEVINE, 1966).

The sediment data of the four sites described herein show that U.pusilfa burrow in a very wide range of sediment types. Although no clear correlation between density and median grain size or subsieve fraction is evident, U. pusilla seem to prefer muddy sands to muds with a subsieve fraction of more than 10 %. A similar wide range of sediments (mean diameters between 400 and 20 pm) is inhabited by C. armata; with higher densities having been observed in finer sediments (VAUGELAS et a f . , 1986).

The salinity in the habitats of U.pusi f fa ranges from marine (Rovinj) to polymixohaline (Grado and Staranzano); BUSULINI (1955) reported this species

Environments and zonation o f Upogebia pusilla 353

from the lagoon of Grado at a salinity of 9 %o. Several other species of Upogebia have also been recorded from low salinities: U. pugettensk between 22 and 35 %O

(L. C. THOMPSON & PRFTCHARD, 1969), I/.affinis between 25 and 36%0 (FREY & HOWARD, 1975; RABALAIS et al., 1981), and U. africana between 15 and 36%0 (MCLACHLAN & GRINDLEY, 1974). All remaining species are fully marine.

Many Callianassidae also occur in euhaline as well as in poly- to mesomixo- haline waters; C. bjformis between 12 and 36%0 (BIFFAR, 1971; HERTWECK, 1972), C. californiensis between 25 and 36%0 (L. C. THOMPSON & PRITCHARD, 1969), C. filholi between 18.5 and 33%0 (DEVINE, 1966), C. jamaicense between 3 and 36%0 (FELDER, 1978), C. kraussi between 1.2 and 59.5%0 (FORBES, 1974). This list includes the species which occur together with U. pusilla such as C. tyrrhena and C. candida. Most of the species, however, are exclusively marine, e. g., C. major.

Macrophyte cover differs in the four environments investigated: at Grado the “barene” are densely populated by Spartina maritima, whereas the tidal flats and subtidal bottoms show no or only sparse Zostera noltii meadows. A more dense cover is found at the Staranzano flats with very dense meadows at Rovinj. No correlation seems to exist between seagrass cover and hole densities at Staranzano (Fig.6) or when comparing the sites. An influence of dense macrophyte cover on population densities has been mentioned for U.pusilla at Rovinj (Om et al., 1976). A reduction of population density due to Zostera roots was reported for C. australiensis and C. limosa (COLEMAN & POORE, 1980).

The amount of debris on and in the sediment varies due to macrophyte cover; it is negligible at Grado, yet high at both Rovinj and Staranzano. No correlation between shrimp density and debris is apparent when comparing these three sites. In addition, the amount of debris in the sediment is to a great extent influenced by the activity of the burrowing animals (On et af., 1976; DWOR- SCHAK, 1987). A correlation between animal density and debris content has been reported for C. arenosa, C. australiensis, and C. limosa (COLEMAN & POORE, 1980).

In all three environments, the organic content of sediment is roughly corre- lated with water movement. Especially at Grado and Rovinj the organic content is higher than values (0.1-2.9%) reported for lagoons (EMERY & STEVENSON, 1957). No correlation is evident between population density and organic content along the continuous transects or when comparing the three sites. Such a correlation has been reported for U. africana and C. kraussi (MCLACHLAN & GRINDLEY, 1974), although the authors mention that the amount of suspended matter may have been a more important parameter for Upogebia (a supposed suspension feeder).

The amount of suspended material is high at Grado and Staranzano and low at Rovinj; again, no correlation to animal densities could be detected. This demonstrates that several factors must be considered in interpreting the trophic situation of U. pusilla - a viewpoint supported by the different modes of feeding in this species (DWORSCHAK, 1987).

In the intertidal the time of emergence during low water plays an important role in limiting the upper distribution range of U.pusilla. This upper range differs at the three sites. The upper level populated by U.pusilla - the high water line - may be somewhat overestimated in the channels in Rovinj due to

354 DWORSCHAK

overhanging walls (Om et al., 1976); it still lies well above the mean water line and is higher than at the mouth of the channels or at Grado and Staranzano where the first holes occur below mean water level. Emergence times at Rovinj (maximum 15h) are therefore much longer than at Grado and Staranzano (maximum of 6h). As calculated from the oxygen consumption of both the shrimp and the burrow wall (DWORSCHAK, in prep.), the oxygen content of the burrow water of a 10mm individual falls to zero within 0.6h, that of a 60mm specimen within 3.2 h. In the laboratory, however, survival time under anoxic conditions exceeds maximum time of emergence (DWORSCHAK, in prep.). In addition, excretion by the animal and diffusion of solutes from the surrounding sediment change burrow water during low tide emergence (ALLER & YINGST, 1978). This has an additional influence on survival time during low tide conditions.

At Grado, the upper intertidal has a coarser sediment than the lower, whereas at Staranzano and Rovinj the sediments are more similar between the upper and middle intertidal. Laboratory experiments and the presence of U.pusillu at Aurisina show that this species is able to burrow even in coarse sediment. Higher water movement in this zone at Grado, however, may inhibit population of coarse sediments; at Staranzano higher water movement near the low water line lead to a decrease in population density. The finer sediments at Rovinj and at Staranzano are less permeable than those of the upper intertidal at Grado, where the ground water level sinks below the depth which small animals can reach.

The role of several factors determining the upper limit of shrimp distribution in the intertidal is also evident in other Upogebiidae and Culliunassidue. MACGINITIE (1935) reports that U. pugeftensis generally occurs up to the mean water level and discussed an occasional shift to the high water level of neap tides at sites with a higher food supply. For C. californiensk he mentioned a general occurrence below the mean water line. In contrast, R. K. THOMPSON & PRITCH- ARD (1969) report a consistent higher level of C. californiensis, probably due to different sediment types at these sites; THOMPSON (1972) found U. pugerrensis up to 60 cm above mean water level. SWINBANKS & MURRAY (1981) found U. puget- tensis below the mean water level where continuous emergence lasts for a maximum of 0.5 days, and C. californiensis up to mean high water line (maximum emergence 4 days). The authors discuss this zonation in relation to the difference in burrowing behaviour and the different tolerance to anoxic conditions. U. africanu occurs up to the mean water level (DAY, 1967), C . austruliensis up to the high water line of spring tides and locally even higher (HAILSTONE & STEPHENSON, 1961).

The causes for restriction of C. californiensis to the mid-intertidal in many Northwest Pacific tidal flats were investigated by POSEY (1986). Caging and transplantation experiments showed that seasonal predator activity prevents the establishment of dense Callianassu-populations in the lower intertidal and sub tidal.


Summary

Physical parameters of the habitat and the zonation of the thalassinidean shrimp Upogebia pusifla were investigated in four environments in the Northern Adriatic:

(1) A 70 m wide tidal flat in the lagoon of Grado is characterized by muddy sand at the mean water line and becomes a sandy mud (Md 38 pm) near the low water line. The organic content of the sediment ranged from 3.5 to 6.4%; salinity ranged from 24 to 36%0, water temperature from 8 to 26.5”C. The first holes of U. pusilfa-burrows occur at a water depth of - 20cm and increase rapidly to 100 H - m-2 with increasing water depth. Densities of up to 417 H - m-2 could be observed near the low water line. Hole distribution is random in most of the cases, seasonal changes in hole densities are low.

(2) A0.5 to 2 km wide tidal flat at Lido di Staranzano near the mouth of the Isonzo is characterized by stands of Spartina maritima near the high water line and a patchy Zostera noltii cover between the high and the low water line. Salinity ranged from 20 to 36%0; the sediment is a silty very fine to fine sand (Md70-106 pm, subsieve fraction 6-44 %) down to a water depth of - 30cm and becomes a medium sand (Md233 pm, 1 % subsieves) near the low water line. The organic content ranged from 0.33 (low water line) to 4.17 % (mean water line). The first U.pusiflu holes occur around the mean water line with a maximum of 60 H - m-I, increase at a water depth of - 20 cm to a maximum of 161 H * m-*, and vary down to - 30 cm where hole density decreases.

(3) A mud flat seawards of a salt marsh with several deep channels situated in a deep bay on the Istnan coast near Rovinj. The mud flat is densely covered by Zosrera and Cymodocea and consists of red terrigenous clay (Md 23 pm, 90 % subsieves) with an organic content between 7 and 9 %. Hole densities at channel entrances ranged between 295 and 383H.m-*; a box core sample gave an estimated shrimp density of 2420 * m-2 on the tidal flat.

(4) A sublittoral bottom at a depth of 6m in the Gulf of Trieste near Aurisina. The sediment is a mixture of gravel, sand, and mud (Md 888 pm, 20 % subsieves). Hole densities ranged from 160 to 460 H - m-2, which corresponds to an animal density between 80 and 230 - m-* as determined by suction sampling and resin casting.

Acknowledgements

This study was supported by the Hochschuljubilaumsstiftung der Stadt Wien and the projects P5059 and P5915 of the Fonds mr Forderung der wissenschaftlichen Forschung in Osterreich. The author is grateful to the entire staff of the “Laboratorio di Biologia Manna, Sorgenti di Aurisina” for their hospitality and for providing essential facilities. My thanks are due to Dr. P. PERVESLER for help during field work, Dr. R. ROETZEL for sediment analysis, and Drs. J . Orr and M. STACHOWTSCH for critical reading of the manuscript.

356 DWORSCHAK

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Documents

The Biology of Upogebia pusilla (PETAGNA) (Decapoda, Thalassinidea) : II. Environments and Zonation