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Low biomass of macrobenthic fauna at a tropical mudflat:An effect of latitude?

Agus Purwoko a,b, Wim J. Wolff a,*

a Department of Marine Benthic Ecology and Evolution, University of Groningen, P.O. Box 14, 9750 AA Haren, The Netherlandsb Department of Biology, Sriwijaya University, Palembang, Indonesia

Received 22 June 2007; accepted 15 August 2007

Available online 14 September 2007

Abstract

The macrobenthic animal biomass of the intertidal area of the Sembilang peninsula of South Sumatra, Indonesia, has been studied in 2004.Each month (MarcheAugust) 21 core samples were taken at each of six sampling stations. Macrobenthic fauna were identified at the lowesttaxonomical level possible and counted. Biomass was measured as ash-free dry mass (afdm). The average biomass over all stations and monthswas 3.62 g afdm m�2, the highest biomass (47.45 g afdm m�2) found at a station in one month was due to abundant occurrence of the bivalveAnadara granosa. Low biomass of macrobenthic fauna at Sembilang peninsula cannot easily be explained but is in line with low biomasses foundelsewhere in the tropics. For that reason we analyzed a data set of 268 soft-bottom intertidal biomasses collected world-wide to look for a re-lationship with latitude. It was shown that average biomass of intertidal macrobenthic fauna in the tropics was significantly ( p < 0.05) lower thanthat at non-tropical sites. A significant second-order relationship between biomass of macrobenthic fauna and latitude was established.� 2007 Elsevier Ltd. All rights reserved.

Keywords: biomass; macrobenthos; intertidal fauna; tropics; Indonesia; Sembilang

1. Introduction

Warwick and Ruswahyuni (1987) studied the benthic faunaat the northern coast of Central Java, Indonesia, and found lowintertidal biomasses. As an explanation they suggested that intropical waters with more or less continuous phytoplanktonproduction zooplankton grazers are able to remain in phasewith phytoplankton and prevent that a large part of the primaryproduction reaches the bottom as food for benthic fauna. Thisshould be in contrast to temperate latitudes where phytoplank-ton production is highly seasonal and much of the springbloom settles at the bottom before the zooplankton populationhas built up sufficiently to graze it. Hence, they postulated a re-lationship between intertidal benthic biomass and latitudesuggesting this to result in lower biomasses in tropical areascompared to temperate areas.

We studied the benthic fauna of the intertidal flats at Sembi-lang peninsula, South Sumatra, Indonesia, in 2004 and foundlow biomasses as well. Hence, in this paper we report on our re-sults and investigate the possible existence of a positive rela-tionship between latitude and biomass of macrobenthic fauna.

For temperate and subtropical estuaries Kalejta and Hockey(1991) found a negative relationship between estuarine inverte-brate production and distance from the equator and a positiverelationship between production and mean annual ambienttemperature. However, production is not a good predictor ofbiomass, so this paper does not allow generalizations about a re-lationship between benthic biomass and latitude. Reise (1991)compared two temperate mudflats with a tropical one and con-cluded that biomass was lowest at the tropical site, although nobiomass values were given. Piersma et al. (1993) comparedbenthic biomass in 20 estuaries between 57� N and 34� S andconcluded that there was no relationship between biomassand latitude, although their Fig. 2B suggests otherwise. Ric-ciardi and Bourget (1999) analyzed a data set from 245 sedi-mentary shores and found that macro-invertebrate biomass

* Corresponding author.

E-mail addresses: a.purwoko@rug.nl (A. Purwoko), w.j.wolff@rug.nl

(W.J. Wolff).

0272-7714/$ - see front matter � 2007 Elsevier Ltd. All rights reserved.

doi:10.1016/j.ecss.2007.08.013

Available online at www.sciencedirect.com

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for sedimentary shores did not vary linearly with latitude al-though peak values were found for northern and southern tem-perate areas. All analyses suffered from the fact that data fromthe tropics were less abundant than those from higher latitudes(Alongi, 1990). We decided to reanalyze the data sets ofPiersma et al. (1993) and of Ricciardi and Bourget (1999) to in-vestigate if the low biomass at Sembilang tidal flats could beattributed to a biomasselatitude relationship.

2. Methods

2.1. Area description

The Sembilang peninsula (Fig. 1: 1�590 to 2�150 S and104�450 to 104�530 E) is located at the eastern coast of SouthSumatra, Indonesia, and is part of the Sembilang NationalPark. It is influenced by the Musi River, the MusibanyuasinRiver and some smaller tributaries. Originally, the land wascovered by mangrove and swampy forest. The most seawardbelt of the mangrove vegetation is still formed by Sonneratiaand Avicennia where the sediment is sandy; however, wherethe sediment is muddy, Rhizophora occurs. Nypa palms appearwhere the sediment is highly influenced by fresh water. In themangrove area at the Sembilang peninsula, approximately 200to 500 m landward of the outer limit of the mangroves, thereare 4000 ha of shrimp ponds. The coastline of the area facesBangka Strait and the East China Sea.

The area is characterized by a monsoon climate. The annualrainfall is 2000e2500 mm. The maximum rainfall occurs inNovember and December (260e275 mm per month) and the

minimum in July and August (140e200 mm per month). Wehave distinguished a wet season from October to April anda dry season from May to September. Daily temperatureranges between 20 and 32 �C and the humidity varies from70% to 90%t (source: Stasiun Klimatologi Klas I KentenPalembang).

The sediment of the tidal flats ranges from fine to mediumsands to very soft mud with high organic content. Mostly, thesediment is acidic and the C:N ratio is high (Soeroyo andSuryaso, 1999).

There is one high tide and one low tide daily. The tide rea-ches a maximum height of 4 m above low-tide level. Further,the tide is also influenced by the monsoon. During the rainyseason, the height of the high tide will be up to 1e2 m higher.Also, low tide levels are higher in that period, meaning thatthe tidal flats emerge slowly (Tide table from Daftar pasangsurut Sungsang, Computer program TideWizard, and fieldobservation).

Salinity measured at low tidewas 12e13 in the wet season and17e18 in the dry season (Purwoko, unpublished observations).

2.2. Description of sampling stations

We selected 6 sampling stations (Fig. 1) with varyingcharacteristics:

1. Station 1: Tj. (Tanjung) Carat (S: 2�16.3240 and E:104�55.1170 by Gekko 202 Garmin GPS). Located in theestuary of the Musi river; the sediment is sandy, and thestation is strongly influenced by fresh water.

Fig. 1. Sampling stations along the coast of Sembilang peninsula. Each station consists of three transects each with seven sampling points.

870 A. Purwoko, W.J. Wolff / Estuarine, Coastal and Shelf Science 76 (2008) 869e875

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2. Station 2: S. (Sungai) Bungin (S: 2�14.9550 and E:104�50.7140). Located in the estuary of the Musibanyuas-sin river. The surface layer of the sediment is soft and highin organic matter and has a thickness of more than 1 m. Onthe sediment young Avicennia occur.

3. Station 3: Solok Buntu (S: 2�11.0630 and E: 104�54.7640).Located near the estuary of the Musibanyuasin river. Thesurface layer of the sediment is muddy, and reaches 40 cmdepth. Mangrove vegetation consists mainly of Avicennia.

4. Station 4: S. Barong Kecil (S: 2�9.8720 and E: 104�54.5870).The site is near the minor estuary of S. Barong Kecil.The sediment is muddy and the depth of this layer reaches50 cm.

5. Station 5: S. Siput (S: 2�5.8240 and E: 104�54.1020). Thesediment is muddy and the soft layer reaches 40 cm; theadjacent mangrove vegetation is mostly Avicennia; closeto the site young trees grow.

6. Station 6: S. Dinding (S: 2�1.9240 and E: 104�50.5730). Thesediment is muddy and contains many dead shells. Thedepth of the soft layer reaches 40 cm. The site is facing di-rectly the South China Sea, so it is exposed to high waves.

2.3. Sampling procedure

Sampling activities took place during low tide at Sungsangin March, May, June, July and August 2004. Each station con-sisted of 3 parallel line transects each consisting of 7 samplingpoints. The distance between the line transects varied from 5 to10 m; the distance between the sampling points was randomlychosen and varied between 3 and 20 m. The first core sample ofthe first transect was taken at the lowest water level and the sec-ond till the seventh one were at further distance towards themangrove. In the field we could not distinguish beforehand be-tween areas of more or less average density of animals and areasof extremely high density (e.g., beds of bivalve filter feeders).Hence, we could not stratify our samples accordingly. Samples

were taken with a circular corer. Core diameter was 15 cm andthe sampling depth 30 cm. At each sampling point 1 core sam-ple was taken. The core samples directly were extracted by dou-ble layers of 1 mm sieve in the field and the animals werecollected from the sieve by hand.

Sometimes sampling was difficult. Rough seas caused dif-ficulty approaching the sampling sites, whereas big waves dis-turbed sampling activities, especially during sieving of thecore samples. This may have reduced to some extent the num-ber of animals obtained. To overcome this problem, on someoccasions intact core samples have been broken into piecesbefore sieving and animals were collected directly from thecore when we saw them, especially worms.

Macrobenthic fauna collected was preserved in 70% alco-hol mixed with 3% of formalin. The animal fauna in the sam-ples were identified to the lowest taxonomic level possible(Dharma, 1988, 1992; computer program: Poly Key), countedand ash-free dry mass (afdm) (Winberg and Duncan, 1971)was measured at the laboratory at Palembang. The statisticalcalculations were carried out by the Statistics 7 program.

2.4. Reanalysis of literature data

We used the data set collected by Ricciardi and Bourget(1999) and kindly made available by Dr. A. Ricciardi as a start-ing point for our analysis. This data set comprises 245 soft-bottom localities. To these soft-bottom data we added ourown data, in which we treated each of our sampling stationsas one locality, resulting in 6 more locations. Finally, we addedthe data from Table 1 of Piersma et al. (1993) excluding thosealso reported by Ricciardi and Bourget (1999). In total ourdata set consisted of 268 biomass values from soft-bottomtidal flats in tropical, subtropical, temperate and polar areas.To obtain normality we converted our biomass data by log10

(afdm þ 0.1). The Statistics 7 program was used for all dataanalyses.

3. Results

3.1. Biomass at Sembilang

Tables 1 and 2 and Fig. 2 (see also Fig. 1) summarize ourresults for the macrobenthic biomass of the intertidal area atSembilang. The animal biomass averaged over the 6 stationsand the 5 months of sampling at Sembilang amounted to3.62 g afdm m�2. The highest biomass of macrobenthic ani-mals occurred at station 4 in June (47.45 g afdm m�2) andJuly 2004 (17.17 g afdm m�2) and was caused mainly bya high biomass of small individuals of the fast-growing bivalveAnadara granosa (Broom, 1982). The average biomass overall months at station 4 (afdm: 14.09 g m�2) was significantlyhigher than those at the other stations (ANOVA: p < 0.05).Most of the biomass derived from bivalves. Other animals,such as gastropods, crabs and polychaetes reached their high-est biomass level in June (ANOVA: p < 0.05), July and May2004 (ANOVA: p < 0.05), respectively (Table 2).

march may june july august

S1

S3

S5

0

5

10

15

20

25

30

35

40

45

50

gram

afd

m m

-2

months

statio

ns

Fig. 2. Biomass (g afdm m�2) at six different stations over time.

871A. Purwoko, W.J. Wolff / Estuarine, Coastal and Shelf Science 76 (2008) 869e875

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Taxa influenced by place (stations) and time (months) wereTellina remies, Tellina timorensis, Clithon oualaniensis, Nerei-didae, Maldanidae and Lumbrineridae. Their biomasses weresignificantly different between stations and between months,as indicated by the different superscript letters (in parentheses)in Tables 1 and 2.

3.2. Biomasselatitude relationship

The analysis of the Piersma et al. (1993) data set, whilekeeping apart data from northern and southern latitudes, didresult in positive correlations for latitude and biomass butnone was significant (regression analysis: North: R2 ¼ 0.15,p ¼ 0.12; South: R2 ¼ 0.55, p ¼ 0.26). The outcome improvedwhen using absolute values for latitude but also was not signif-icant (R2 ¼ 0.16, p ¼ 0.07).

When we analyzed our main data set of biomasses whilekeeping apart data from northern and southern latitudes, regres-sion analysis and the t-test showed that the mean values of mac-robenthic biomass in tropical and non-tropical areas were notsignificantly different for both northern (R2 ¼ 0.00, p ¼ 0.60;t-test p ¼ 0.13) and southern (R2 ¼ 0.09, p ¼ 0.62; t-testp ¼ 0.32) latitudes. However, when we classified our data with-out differentiating between southern and northern latitudes,Fig. 3 suggests that average biomasses differ by latitude.

Indeed, the mean biomass of tropical (defined as between theTropics of Cancer and Capricorn at 23� N and S) areas wassignificantly (t-test, p ¼ 0.01) different from the biomass ofnon-tropical areas.

Further regression analysis indicated that the hypothesis ofa linear relationship was rejected (R2 ¼ 0.00, p ¼ 0.74). Thebest fitting relationship between biomass of macrobenthicfauna and latitude zone was obtained by polynomial regression(R2 ¼ 0.32, p ¼ 0.03). The equation of the regression islog10(afdm þ 0.1) ¼ 0.2846 þ 0.0241x � 0.0003x2, where xis latitude values (Fig. 4).

As may be expected, in our large data set water temperatureis coupled significantly to latitude (R2 ¼ 0.78, p ¼ 0.00). Bio-mass (as afdm) shows a weak negative linear correlation withwater temperature (R2 ¼ 0.01, p ¼ 0.10) with zero biomass atabout 37 �C.

4. Discussion

4.1. Biomass per station at Sembilang

The highest biomass occurred at station 4 which differed sig-nificantly from all other stations with by far the highest averagevalue (14.09 g m�2) of ash-free dry mass of macrobenthic ani-mals. This is mainly the result of the abundant occurrence of the

Table 1

Average biomass in g ash-free dry mass m�2 of macrobenthic fauna at different stations (see Fig. 1) at Sembilang peninsula from March to August 2004. Different

letters (superscript in parentheses) after biomass values in the same row (species) indicate significant differences (ANOVA: p < 0.05)

Species Average afdm (g m�2) at Sembilang peninsula Average

stationStation 1 Station 2 Station 3 Station 4 Station 5 Station 6

Bivalves

1 Anadara granosa 0.0431 0.0000 1.1113 12.2685 0.0000 0.2047 2.2713

2 Hecuba scortum 0.0122 0.0098 0.0391 0.0095 0.0289 0.0046 0.0173

3 Solen sp. 0.1533 0.0000 0.0000 0.0000 0.0000 0.0000 0.0256

4 Tellina remies 0.0210(a) 0.0892(a) 0.5047(b) 0.8736(c) 0.6869(bc) 0.2765(a) 0.4087

5 Tellina timorensis 0.2631(a) 1.8528(b) 0.0302(a) 0.0841(a) 0.1461(a) 0.0815(a) 0.4096

Total bivalves 0.4927(a) 1.9518(a) 1.6852(a) 13.2357(b) 0.8619(a) 0.5673(a) 3.1324

Gastropods

1 Clithon oualaniensis 0.0350(a) 0.1648(b) 0.0114(a) 0.0734(a) 0.0177(a) 0.0430(a) 0.0575

2 Littorina melanostoma 0.0000 0.0004 0.0000 0.0002 0.0000 0.0005 0.0002

3 Nassa serta 0.0517 0.0637 0.0333 0.0636 0.0337 0.0135 0.0432

4 Thais buccinea 0.0111 0.0151 0.0306 0.0096 0.0038 0.0298 0.0167

Total gastropods 0.0978(bc) 0.2440(c) 0.0753(bc) 0.1467(c) 0.0551(a) 0.0868(bc) 0.1176

Decapods (crabs)

1 Ocypodidae 0.0231 0.0551 0.2012 0.0463 0.2535 0.0350 0.1024

2 Leucociidae 0.0000 0.0116 0.0000 0.0000 0.0493 0.0000 0.0101

Total crabs 0.0231 0.0667 0.2012 0.0463 0.3028 0.0350 0.1125

Polychaetes

1 Nereididae 0.1111(b) 0.1182(b) 0.0609(a) 0.0654(a) 0.0685(a) 0.0721(a) 0.0827

2 Maldanidae 0.0040(a) 0.0103(bc) 0.0060(ab) 0.0250(c) 0.0153(c) 0.0277(d) 0.0147

3 Lumbrineridae 0.0079(a) 0.0230(ab) 0.0288(ab) 0.0553(b) 0.1133(c) 0.0291(ab) 0.0429

4 Capitellidae 0.0027 0.0127 0.0034 0.0071 0.0064 0.0092 0.0069

5 Sternaspidae 0.0124 0.0111 0.0527 0.5013 0.0042 0.0075 0.0982

6 Unidentified worms 0.0085 0.0082 0.0142 0.0089 0.0000 0.0240 0.0106

Total worms 0.1465(a) 0.1835(a) 0.1660(a) 0.6629(b) 0.2077(a) 0.1698(a) 0.2561

Total all species 0.7601(a) 2.4460(a) 2.1278(a) 14.0915(b) 1.4275(a) 0.8590(a) 3.62

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bivalve Anadara granosa, which was rare or lacking at the otherstations. Anadara granosa is a fast-growing species occurringin dense beds (Broom, 1982; Ng Fong Oon, 1986). We encoun-tered especially 1e1.5 cm sized individuals which according toNg Fong Oon (1986) are less than 1 year old. However, theirgrowth is not fast enough to explain their occurrence in oursamples in June without a previous occurrence in May. Appar-ently, we have missed the A. granosa bed when sampling inMay. This is assumption is supported by the strongly clustereddistribution we observed in June and July. When we omitted the

biomass values of Anadara, statistical analysis showed thatthere were no significant differences among the 6 stations forthe total biomass of the macrobenthic fauna.

Polychaete biomass was significantly different between sta-tions. The highest biomass value was found at station 4. Fur-ther analysis showed that the polychaete families Nereididae,Maldanidae and Lumbrineridae each had their highest biomassat different stations. The highest biomass per polychaetetaxon, such as Nereididae, Maldanidae and Lumbrineridae,occurred at station 2, station 6 and station 5, respectively.

Ricciardi and Bourget (1999) included biomass data fromsites with an average annual salinity over 20 in their dataset. We have no detailed information on salinity of our sam-pling stations, but from the limited data available we assumethat at high tide salinity at our stations will be around 20. Any-how, Fig. 4 suggests that biomass at our 6 stations does notdeviate from the pattern shown by the remaining 262 stations.

4.2. Biomass per month at Sembilang

There was also an influence of the month of sampling on thebiomass of the macrobenthic fauna at Sembilang peninsula.Biomass of the total macrobenthic fauna was not significantlydifferent over the 5-month sampling period. However, bivalves,gastropods and polychaetes showed significant differences. The

Table 2

Average biomass in g ash-free dry mass m�2 of macrobenthic fauna in different months at Sembilang peninsula from March to August 2004. Different letters

(superscript in parentheses) after biomass values in the same row (species) indicate significant differences (ANOVA: p < 0.05)

Species Average afdm (g m�2) at Sembilang peninsula Average months

March May June July August

Bivalves

1 Anadara granosa 0.1706 0.0000 7.7037 3.4820 0.0000 2.2713

2 Hecuba scortum 0.0224 0.0067 0.0269 0.0115 0.0191 0.0173

3 Solen sp. 0.0000 0.0000 0.1278 0.0000 0.0000 0.0256

4 Tellina remies 0.5746(b) 0.5163(b) 0.4092(b) 0.3420(ba) 0.2011(a) 0.4087

5 Tellina timorensis 0.0629(a) 0.1427(a) 0.1996(a) 0.8470(b) 0.7960(b) 0.4096

Total bivalves 0.8305(a) 0.6657(a) 8.4672(b) 4.6824(b) 1.0163(a) 3.1324

Gastropods

1 Clithon oualaniensis 0.0224(a) 0.0673(ab) 0.0673(ab) 0.1115(b) 0.0190(a) 0.0575

2 Littorina melanostoma 0.0000 0.0000 0.0009 0.0000 0.0000 0.0002

3 Nassa serta 0.0853 0.0269 0.0853 0.0075 0.0112 0.0433

4 Thais buccinea 0.0067 0.0125 0.0375 0.0193 0.0072 0.0167

Total gastropods 0.1145(a) 0.1068(a) 0.1911(b) 0.1383(ab) 0.0375(a) 0.1176

Decapods (crabs)

1 Ocypodidae 0.0584 0.0147 0.0640 0.1446 0.0771 0.0718

2 Leucociidae 0.0000 0.0571 0.0213 0.0579 0.0675 0.0408

Total crabs 0.0584 0.0718 0.0853 0.2025 0.1446 0.1126

Polychaetes

1 Nereididae 0.0224(a) 0.0673(b) 0.0494(b) 0.1020(c) 0.1723(d) 0.0827

2 Maldanidae 0.0013(a) 0.0269(bc) 0.0269(c) 0.0062(a) 0.0121(b) 0.0147

3 Lumbrineridae 0.0180(a) 0.0629(b) 0.0269(a) 0.0594(b) 0.0474(b) 0.0429

4 Capitellidae 0.0011 0.0028 0.0180 0.0029 0.0099 0.0069

5 Sternaspidae 0.0016 0.4169 0.0314 0.0253 0.0158 0.0982

6 Unidentified worms 0.0131 0.0196 0.0135 0.0018 0.0053 0.0106

Total worms 0.0575(a) 0.5964(b) 0.1661(a) 0.1976(a) 0.2628(a) 0.2561

Total all species 1.0609 1.4408 8.9097 5.2208 1.4612 3.62

0

5

10

15

20

25

0-9.9 10-19.9 20-29.9 30-39.9 40-49.9 50-59.9 > 60Latitude class

gram

ash

-free d

ry w

eig

ht

Fig. 3. Average biomass (g afdm m�2; black) plus standard error (white) per

10� latitude, northern and southern latitudes combined.

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highest bivalve and gastropod biomass was found in June, andthe highest polychaete biomass in May 2004. Biomass of Tell-ina remies was lowest in August whereas biomass of Tellinatimorensis was highest in July and August 2004. Omitting theAnadara biomass value did not influence the ANOVA resultfor bivalves and total macrobenthic fauna biomass, and therewas no time influence for the Sembilang peninsula tidal flat.Maldanidae and Lumbrineridae had their highest biomass valuein May but Nereididae in August 2004.

4.3. Comparison of Sembilang biomass with otherstudies

We found an average biomass over all stations and all monthsof 3.62 g afdm m�2. Biomass value ranged from 2.95 to 36.31 gafdm at east Java (Erftemeijer and Swennen, 1990) and was2.89 g at central Java (Warwick and Ruswahyuni, 1987). Broom(1981) reported that the biomass value at a Malaysian mudflatwas 23.45 g afdm, so the Sembilang biomass value was almostthe same as the Java values but it was lower than the Malaysianone. Parulekar et al. (1980) reported that the biomass of the mac-robenthic fauna at a tropical estuary in India was 54.2 g m�2 wetweight. However, when it was converted to afdm (Ricciardi andBourget, 1998), it was 3.34 g afdm m�2, being very close to ourSembilang value. In Mauritania (Africa, 20� N), the biomasswas much higher (17.00 g afdm m�2) (Wolff et al., 1993).Ricciardi and Bourget (1999) reviewed a large number of inter-tidal biomass studies and found for tropical sedimentary shoresaverage biomasses of about 7.00 g m�2 ash-free dry mass (0e20� N) and about 8.50 g m�2 (0e20� S). We conclude that thevalue for Sembilang peninsula is on the low side.

Ricciardi and Bourget (1999) suggest also that macro-benthic biomass at soft-sediment shores may be lowered byvery muddy sediment, a high slope of the shore, high exposureto waves, and small waves. The Sembilang tidal flats indeed

are very muddy, but neither shows a high slope of the shore,nor, in most cases, they are highly exposed to waves. Thesame authors also suggest a relationship with latitude (see be-low). They do not consider biological factors which of coursemay be connected to the physical factors mentioned.

Exclusion experiments showed that at Sembilang shorebirdswere important predators of the macrobenthic community (Pur-woko, unpublished observations). Resident birds, mainly storksand herons, prey especially on fish, whereas migratory birds,mainly waders, feed on macrobenthic fauna; however, duringlong drought periods local ducks also searched for food at theSembilang peninsula tidal flats. Nonetheless, shorebird num-bers at Sembilang are not exceptionally high (Purwoko, inpreparation).

Although we have no records on predation by fish, there isevidence that some species prey on macrobenthic fauna. Dur-ing field observations at low tide, we observed tracks of fishdisturbance left on the substrate.

Humans can be important predators as well. However, atSembilang before 2005 Anadara and other shellfish were notharvested. On the other hand shrimps were caught with smalltrawls and standing nets. These activities may have caused dis-turbance of the bottom leading to lower macrobenthic biomass.

4.4. Biomasselatitude study

The mean biomass of macrobenthic fauna in the tropics wasshown to be significantly lower compared to the mean biomassof macrobenthic fauna at non-tropical latitudes. However, wecould not demonstrate a significant linear relationship betweenbenthic biomass and latitude. Instead we established a significantsecond-order relationship with the maximum biomass predictedat 40.17 degrees of latitude. This is in line with our earlier con-clusion of low biomasses in the tropics, but we find it difficult tosuggest a biological explanation for this relationship.

-10 0 10 20 30 40 50 60 70 80

Latitude

-1.6990

-1.3010

-0.9208

-0.5528

-0.2007

0.1399

0.4757

0.8096

1.1490

1.4843

1.8360

2.2788

Lo

g10 (afd

m+

0.1)

y = 0.2846 + 0.0241x - 0.0003x2

oo

o

oo

o

Fig. 4. The relationship between latitude and biomass. The relationship shown fits the equation y ¼ 0.2846 þ 0.0241x � 0.0003x2 (0.95 confidence interval) with

y ¼ log10(afdm þ 0.1). The bold data points denote our stations at Sembilang.

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Tropical beaches and tidal flats are subject to climatic andphysical disturbance (review by Alongi, 1990). Large rainfall, storms, sun exposure, and high temperatures disturb themacrobenthic habitat. However, physical disturbance is alsofound at higher latitudes and it is not immediately clear whyit should have less effect on benthic biomass. Maybe, ourlatitudeebiomass relationship is the result of two stress gradi-ents. One gradient might be related to the occurrence of freezingtemperatures and ice scour, leading to a negative relationshipbetween latitude and biomass from the poles towards temperatelatitudes. The other one could be related to increasing tempera-tures leading to increasing heat stress on intertidal flats goingfrom temperate latitudes to the equator.

Other possible explanations are ecological in nature. Warwickand Ruswahyuni (1987) speculated that in the tropics less ofthe primary production by phytoplankton reaches the bottombecause production is more or less continuous and in phasewith zooplankton grazers. On the other hand, they argue,in temperate regions primary production is highly seasonaland much of the spring bloom settles to the bottom beforethe zooplankton population has built up sufficiently to grazeit. This might be true at Sembilang as well. Phytoplanktonoccurs in low densities at Sembilang (Sutomo, 1999), possi-bly because of the high abundance of zooplankton at thesame time (Romimohtarto, 1999). However, data are lackingto test the generality of this explanation.

Another explanation is related to the share of invertebratepredators in the macrobenthic fauna. A high number of pred-ators may enhance mortality of non-predatory species result-ing in a low total biomass. Wolff et al. (1993) drew attentionto the high number of invertebrate predators at the intertidalflats of the tropical Banc d’Arguin. This may be contrastedto the situation at temperate latitudes where winter tempera-tures determine the abundance of invertebrate predators ontidal flats (see for example Beukema and Dekker, 2005). Yearswith low abundance of predators usually result in high recruit-ment of non-predatory benthos, resulting in strong year-classesdominating the benthic fauna for several years. But again, dataare lacking to test the generality of this explanation.

The same applies to the suggestion that tropical flats aresubjected to higher exploitation pressures by humans. Oneof us (W.J.W.) has seen tidal flats all over the world andobserved that in many developing tropical countries coastalecosystems are exploited very intensively. Although we cannotsupport this observation quantitatively, it might mean thattropical mudflats on average are exploited more heavily thannon-tropical flats.

Acknowledgments

First A.P. would like to thank Sriwijaya University, Palem-bang, Indonesia for sponsoring his study. A.P. thanks Ake andUsup for their assistance during sampling and Ismail for actingas a speedboat driver. He is also glad that Edi P. assisted at mea-suring the afdm. Special thanks are addressed to Dr. Harry tenHove who guided us in identifying the macrobenthic fauna and

Dr. Anthony Ricciardi who supplied his world-wide data set onmacrobenthic biomasses. Finally, we thank two anonymous ref-erees for their valuable comments on the manuscript.

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