Seasonal Changes in the Macro- Zoobenthos of a Tropical Mudflat

Seasonal changes in the macrozoobenthos of a tropical mudflat

Report on MONROEB – MONitoring ROEbuck Bay Benthos, 1996-2001

Petra de Goeij1, Marc Lavaleye1, Grant B. Pearson2,3 & Theunis Piersma1,4

1Department of Marine Ecology & Evolution, Royal Netherlands Institute for Sea Research (NIOZ), P.O. Box 59, 1790 AB Den Burg, Texel, The Netherlands

2Western Australian Department of Conservation and Land Management (DCLM), WA Wildlife Research Centre, P.O. Box 51, Wanneroo, WA 6065, Australia

3Broome Bird Observatory, Crab Creek Road, P.O. Box 1313, Broome, WA 6725, Australia

4Animal Ecology Group, Centre for Ecological and Evolutionary Studies (CEES), University of Groningen, P.O. Box 14, 9750 AA Haren, The Netherlands

The analyses presented in, and publication of, this report were made possible with funding from the National Heritage Trust through Environs Kimberley

NIOZ-Report 2003-4

ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH (NIOZ), TEXEL W.A. DEPARTMENT OF CONSERVATION AND LAND MANAGEMENT, PERTH

TABLE OF CONTENTS

ABSTRACT

SAMENVATTING

1. INTRODUCTION ...... 1

2. STUDY SITES AND METHODS ...... 5 2.1. Study sites ...... 5 2.2. Methods ...... 5

3. RESULTS AND DISCUSSION...... 9 3.1. Tropical seasons ...... 9 3.2. Overall biodiversity ...... 9 3.3. Seasonal changes in abundance...... 13 3.4. Recruitment patterns ...... 22 3.5. Optimizing future benthic monitoring ...... 31

4. GENERAL DISCUSSION ...... 35

5. ACKNOWLEDGEMENTS ...... 39

6. REFERENCES ...... 47

ABSTRACT were directly sorted in trays with salt water. All animals were conserved in forma- Roebuck Bay in the Kimberley region of lin, stored in ethanol and sent to the northwest Australia is especially famous Royal Netherlands Institute for Sea for the tens of thousands of shorebirds Research (NIOZ) for identification. The that spent the tropical winter here. sampling programme is still continuing, Shorebirds are attracted to the richness but the analysis includes samples up to of benthic invertebrates living in and on May 2001. the intertidal flats. In the laboratory, all molluscs and crabs To find out which benthic animals are (to species level), the polychaete tube- present throughout the year, and from worms Oweniidae and Chaetopteridae year to year, a benthic monitoring pro- (to family level), the ostracods (three gramme was started in 1997. The aim of taxa), the brachiopods (one species MONROEB (MONitoring ROEbuck Bay Lingula), the echinoderms, the pygnogo- Benthos) was to unravel the seasonality nids (sea spiders), anemones, tunicates of the benthic life on a tropical intertidal and fish were distinguished, counted flat in order to compare this to the better and, if possible, their lengths measured studied intertidal flats of temperate north- to the nearest mm. The remaining poly- west Europe. To the best of our know- chaetes were not analysed yet. ledge this is the first long-term study of the seasonal dynamics of intertidal ben- In the process almost 23,000 macro- thos in the tropics. zoobenthic animals were sorted and assigned names. A total of 139 different From March 1996 two sites in the bay taxa were encountered, including 40 dif- were sampled almost monthly. One site ferent species of bivalve, 26 gastropods, is a sandy place off ‘Fall Point’, the other 2 scaphopods, 7 echinoderms and 17 is a very muddy place off ‘One Tree’, at crab species. The total number of the eastern end of Crab Creek Road. At species was much higher in the sands off these two sites the benthic invertebrates Fall Point than in the soft mud off One were monitored at two stations, respec- Tree. There were hardly any differences tively 150 m and 250 m offshore. The between the relatively nearshore and off- sampling was carried out by the Broome shore stations. Bird Observatory wardens assisted by volunteers. At each of the four stations At Fall Point the most common species (two sites with two stations each), four were the bivalves Anodontia omissa, samples each consisting of six cores of Divaricella ornata and Tellina piratica, the 83 cm2 to a depth of 20 cm were taken. gastropods Vexillum radix and Eulimidae Each sample was sieved over a 1-mm spec., the scaphopod Laevidentalium cf. mesh, which thus yielded the ‘macro- lubricatum, the crab taxon Macro- zoobenthic animals’. The sieved samples phtalmus spec., the ‘spidercrab’ Halicarcinus cf. australis, the crabs the monitoring programme, with quite low Hexapus spec. and Myrodes eudactylus, numbers from 1999 onwards. the polychaete tubeworms Chaetopteridae and Oweniidae, an ostra- The Ingrid-eating snail Nassarius dorsa- cod, hermit crabs, the brachiopod tus showed repeated peak numbers after Lingula spec., brittlestar Amphiura tenuis the cold (dry) seasons. Neither of the and starfish Astropecten granulatus. At tusk shells showed any sign of regular One Tree the most common species circannual changes in numbers, nor did were the bivalves Tellina cf. exotica and the tubeworms Chaetopteridae and Siliqua pulchella, the gastropods Oweniidae. Of the two crab taxa that Tornatina spec., Salinator cf. burmana could be examined, Halicarcinus cf. aus- and the small Nassarius spec., the tralis peaked four times in the middle of scaphopod Dentalium cf. bartonae, her- the year, whereas Macropthalmus spec. mit crabs and mudskippers peaked three times in the middle of the Periophthalmidae. year. The brittlestar Amphiura tenuis showed no large changes over time. Of the 15 numerically dominant taxa, most of which were bivalves, the season- For the seven most abundant bivalves al changes are given. In contrast to the and one gastropod, aspects of settle- clear and regular annual rhythmicity in ment of new cohorts and the possibility the numbers of most species on temper- of movements of animals over the inter- ate intertidal flats, the species in tidal flats were examined by looking at Roebuck Bay show a great variety of the size-frequency distributions. Unlike density changes, with little evidence for the temperate species, there is no single clear circannual cycles. Bloody cockles time period of settlement. Settlement of Anadara granosa had the highest densi- the different species in the Bay took ties from early to mid 1997 with lower place at different times of the year. numbers since. The lucinid bivalve Anadara granosa settled in the course of Anodontia omissa reached peak densi- some of the wet seasons. Both lucinids, ties in late 1997 and again in late 1999. Anodontia omissa and Divaricella irpex Another lucinid bivalve, Divaricella irpex, settled early in the wet, Siliqua pulchella showed peaked numbers every two probably settled late in the wet. The years. The razorclam-like Siliqua pulchel- tellinids settled in the middle of the wet la peaked in mid 1997, with a gradual de- (Tellina capsoides), after the wet (Tellina cline in numbers since. The tellinid piratica) or at the beginning and the end Tellina capsoides peaked in late 1996- of the wet season (Tellina “exotica”). 1997 and also declined since. In contrast, Tellina piratica peaked three times For one bivalve species, Siliqua over the six year of study. Tellina ‘exoti- pulchella, there were clear indications ca’ has been in decline since the start of that these animals make movements over the intertidal flats after settlement. SAMENVATTING een 1 mm zeef. Dat wat op de zeef achterblijft is het ‘macrozoobenthos’. De Roebuck Bay, gelegen in noord-west gezeefde monsters werden direct uitge- Australië vlakbij Broome, is vooral be- zocht in bakken met zout water. Alle die- roemd om de tienduizenden wadvogels ren werden geconserveerd in formaline, die daar de tropische winter doorbren- opgeslagen in ethanol en ter identificatie gen. De wadvogels worden aangetrok- opgestuurd naar het Koninklijk ken door de rijkdom aan voedsel: de Nederlands Instituut voor Onderzoek der benthische bodemdieren die in en op het Zee (NIOZ). Het bemonsteringsprogram- wad leven. ma gaat nog steeds door. In dit verslag worden de resultaten gepresenteerd van Om uit te vinden hoeveel en welke bo- de monsters die tot en met mei 2001 zijn demdieren er door het jaar heen aanwe- verzameld. zig zijn en hoe de aantallen en van jaar op jaar verschillen, zijn we in 1997 ge- In het laboratorium werden de volgende start met een onderzoeksprogramma soorten en groepen onderscheiden: alle waarin de aanwezigheid en aantallen schelpdieren en krabben (tot op soortni- van bodemdieren op een viertal plekken veau), de borstelwormen Oweniidae en werd gevolgd. Het doel van MONROEB Chaetopteridae (tot op familieniveau), de (MONitoring ROEbuck Bay Benthos) was ostracoden (drie typen), de brachiopoden om een vergelijking te maken tussen de (één soort, Lingula), de stekelhuidigen, seizoenscycli van bodemdieren in en op zeespinnen, anemonen, manteldieren en een tropisch wad en die van de bodem- vissen. Alle dieren werden geteld en in- dieren in de uitvoerig bestudeerde wad- dien mogelijk opgemeten tot op een milli- dengebieden in noord-west Europa. meter nauwkeurig. De overgebleven Voorzover ons bekend, is dit is de eerste wormpjes en kleine kreeftachtigen zijn langdurig volgehouden studie van het nog niet geteld, gemeten en op naam ge- benthos van een getijdegebied in de bracht. tropen. Bijna 23.000 dieren werden gesorteerd Vanaf maart 1996 zijn bijna iedere en van een werknaam voorzien. In totaal maand op twee locaties in de baai mon- werden er 139 ‘soorten’ onderscheiden, sters genomen. De ene locatie is een waarvan 40 verschillende soorten twee- zandige plek bij ‘Fall Point’, vlakbij het kleppige schelpdieren, 26 slakken, 2 oli- Broome Bird Observatory (BBO). De an- fantstanden, 7 stekelhuidigen, en 17 dere locatie betreft twee hele modderige krabben. Het totaal aantal soorten was plekken bij ‘One Tree’, aan het oosteinde veel hoger op de zandige locaties van van de ‘Crab Creek road’. Op deze twee Fall Point dan op de modderige locaties locaties werden de benthische bodem- van One Tree. Er waren nauwelijks ver- dieren gemonsterd op twee plekken, schillen tussen de plekken die 150 m en respectievelijk 150 en 250 meter vanaf 250 m van het strand lagen. het zandstrand. De bemonsteringen werd uitgevoerd door de beheerders van De meest algemene soorten van Fall BBO met hulp van vele vrijwilligers. Op Point waren de tweekleppige schelpdie- elk van de vier stations (twee locaties, ie- ren Anodontia omissa, Divaricella ornata der twee plekken) werden vier monsters en Tellina piratica, de slak Vexillum radix van de wadbodem genomen. Ieder mon- en Eulimidae spec., de olifantstand ster bestond uit zes steken met een Laevidentalium cf. lubricatum, de krab- steekbuis van 83 cm2 tot een diepte van ben Macrophtalmus spec., Halicarcinus 20 cm. Ieder monster werd gezeefd over cf. australis, Hexapus spec., het solda- tenkrabje Myrodes eudactylus, de koker- De ‘Ingrid-etende slak’, Nassarius dorsa- wormen Chaetopteridae and Oweniidae, tus, vertoonde ieder jaar piekaantallen een roeipootkreeftje of ostracode, here- na het koude (droge) seizoen. Geen van mietkreeften, de brachiopode Lingula de twee olifantstanden (scaphopoda) spec., de brokkelster Amphiura tenuis en toonde een teken van regelmatige jaar- de zeester Astropecten granulatus. De lijkse veranderingen in aantallen, en dat meest algemene soorten van One Tree geldt ook voor de kokerwormen waren de tweekleppigen Tellina cf. exoti- Chaetopteridae en Oweniidae. Van de ca en Siliqua pulchella, de slakken twee krabben die in voldoende aantallen Tornatina spec., Salinator cf. burmana en voorkwamen, piekte Halicarcinus cf. Nassarius spec., de olifantstand australis vier keer midden in het jaar en Dentalium cf. bartonae, heremietkreeften Macropthalmus spec. drie keer. De brok- en slijkspringers Periophthalmidae. kelster Amphiura tenuis vertoonde geen grote veranderingen in aantallen. Van de 15 meest voorkomende taxa, met name tweekleppige schelpdieren, zijn de Voor de zeven meest voorkomende seizoensveranderingen weergegeven. In tweekleppigen en de slak Nassarius dor- tegenstelling tot de duidelijke en regel- satus is de vestiging van nieuwe jaar- matige jaarlijkse ritmiek in de aantallen klassen, de groei en de mogelijkheid van van de meeste soorten bodemdieren van migratie van dieren over de wadplaten gematigde getijdegebieden zoals de onderzocht door naar de lengteverdelin- Waddenzee, vertonen de soorten in gen van die dieren over de jaren te kij- Roebuck Bay een grote variatie aan ken. In tegenstelling tot de soorten uit dichtheidsveranderingen. Er zijn weinig gematigde streken, is er niet één speci- aanwijzingen voor het bestaan van dui- fiek moment waarop de jonge dieren zich delijke jaarcycli. De bloedkokkel, vestigen. In Roebuck Bay vestigde het Anadara granosa, kwam in de hoogste broed van de verschillende soorten zich dichtheden voor van begin tot halverwe- op verschillende momenten van het jaar. ge 1997 en daarna alleen in lage aantal- De bloedkokkel Anadara granosa vestig- len. De tweekleppige Anodontia omissa, de zich in de loop van enkele van de een ‘oogje’, vertoonde piekdichtheden ‘natte’ seizoenen. De beide ‘oogjes, aan het eind van zowel 1997 en 1999. Anodontia omissa en Divaricella irpex, Een ander ‘oogje’, Divaricella irpex, ver- vestigden zich vroeg in het ‘natte’ sei- toonde iedere twee jaar een piek in aan- zoen. Siliqua pulchella vestigde zich tallen. De op een kleine mesheft lijkende hoogstwaarschijnlijk laat in het natte sei- Siliqua pulchella piekte halverwege 1997 zoen. De nonnetjesachtigen vestigden en nam daarna geleidelijk in aantallen af. zich midden in (Tellina capsoides), net na De nonnetjesachtige Tellina capsoides (Tellina piratica) of zowel aan het begin piekte aan het einde van 1996 en begin als aan het einde van het natte seizoen 1997 en is sindsdien eveneens afgeno- (Tellina ‘exotica’). men. In tegenstelling hiertoe vertoonde een ander soort nonnetje, Tellina piratica, Alleen voor de mesheftachtige tweeklep- in de zes jaar van het onderzoek, drie pige Siliqua pulchella waren er duidelijke keer een piek. De platschelp Tellina “exo- aanwijzingen dat deze dieren over de tica” is sinds de start van het monitor- wadplaten migreren nadat ze zich als programma in aantal afgenomen en jong dier ergens gevestigd hadden. kwam na 1999 nog slechts in zeer lage aantallen voor. Study sites and methods 5

2. STUDY SITES AND METHODS 1999) both indicated that the benthic life of Roebuck Bay is very diverse and rich. 2.1. STUDY SITES In March 1996 two sites were selected (called ‘Fall Point’ and ‘One Tree’, near Roebuck Bay is a marine embayment Crab Creek, Fig. 4), and at each of these with a fringe of mudflats in the north, and sites two sampling stations were posi- with extensive intertidal mudflats in the tioned approximately 150 m and 250 m east and south (Fig. 4). The bay regularly offshore (perpendicular to the beach, supports over 100,000 shorebirds, which more or less directed due south), named makes it one of the most important inter- A and B (Fig. 5). The approximate geo- tidal areas in Australia (Watkins 1993). graphical position of the Fall Point sta- All these birds depend on the benthic an- tions is 17º59’S, 122º21’E and for the imals living on and in the mud. A study of One Tree stations 17º60’S, 122º22’E. the food of Great Knots Calidris The One Tree site is slightly longer ex- tenuirostris (Tulp & de Goeij 1994) and a posed per tidal cycle than the Fall Point study mapping the intertidal benthos of site, especially during neap tides. the north-shore mudflats (Pepping et al. 2.2. METHODS

122.2 122.3 122.4

Dampier Creek The two sites (= four stations) were sam-

Fall Point pled almost every month in the period Crab Creek March 1996 to May 2001. At each station

-18.0 4 samples were taken, each consisting of 6 standard cores with a diameter of 10.3 cm and a surface of 1/120 m² (= 0.083 m² = 83 cm²), taken to a depth of 20 cm.

-18.1 Each sample was sieved on location over a sieve with a mesh-size of 1 mm. Each sample thus represented a mud- surface of 6*1/120 = 1/20 m², and each station represented a sampled surface of Bush Point -18.2 4*1/20 = 1/5 m²; to obtain a density per m², the number of animals per station was multiplied by 5. To obtain overall densities per sampling date, the average Figure 4. Location of Roebuck Bay and the town of of the station-specific densities was cal- Broome on the Dampier Peninsula on the Australian culated. continent (inset) and map of Roebuck Bay with the area of intertidal flat mapped by Pepping et al. (1999) The sieved samples were transferred outlined in grey and the core sites where the benthic to the Broome Bird Observatory where monitoring took place from 1996-2001 indicated by the short sides of the rectangle between Fall Point and they were sorted in trays with salt water, Crab Creek (see Fig. 5). 6 Methods

were then sent to the Royal Netherlands Institute of Sea Research (NIOZ) for de- * tailed analysis. To prevent both leakage FP-B * N FP-A and the dehydration of specimens, before the samples were packed and sent the ethanol was removed and replaced BBO by ethanol-saturated paper tissue. After arrival in the Netherlands the vials were filled again with 70% ethanol. In our laboratory analyses so far we have distinguished (and counted!) all molluscs and crabs (to species level), other crustacean groups to order level but sometimes to species level, the polychaete tubeworms Oweniidae and Chaetopteridae (to family level), the ostracods (three taxa), the brachiopods (one species of Lingula), the echinoderms, pygnogonids (sea spiders), anemones, tunicates and fish. This * leaves the many families of polychaete OT-B * OT-A worms and an assortment of small crustacean forms. The sorted, counted and measured animals have been kept for further study and so have the unsorted animals. All specimens were counted and their length was measured with cal- lipers to the nearest 0.5 mm. The length of bivalves is defined as the length of the anterior-posterior axis, the length of the Figure 5. Composite of two aerial photo’s showing the gastropods as the distance between the study area, the two sites (FP = Fall Point and OT = One Tree) and the four sampling stations (A and B at apex and the tip of the anterior (siphonal) each site) in the northeastern corner of Roebuck Bay canal (when present) or to the farthest (see Fig. 4 for orientation). BBO = Broome Bird Observatory. edge of the aperture, and the length of the scaphopods as the length of the on most occasions on the day of sam- straight line between both tips of the pling. All animals were picked out and shell. The size of the crabs was defined fixed with 4% formaldehyde. After a few as their carapace width. The length of all days the formaldehyde was removed and other specimens is given by the longest replaced by 70% ethanol. The samples body length. Methods 7

Identifications were made with the help (see Table 1). Note that these field of a stereo-microscope, using among names are not intended to be used in the other sources Edgar (1997), Faucauld nomenclature within the meaning of (1977), Janssen (1995), Jones & Morgan International Committee of Zoological (1994), Lamprell & Whitehead 1992, Nomenclature (ICZN). In the process we Lamprell & Healy 1998, Shepherd & have so far sorted and assigned names Thomas (1989) and Wilson (1993, 1994). to 22,946 macrozoobenthic animals of at Although it was possible to assign some least 144 species. Given the taxonomic species a proper scientific name (mainly gaps, true diversity is likely to be much the bivalves), for many specimens a higher. ‘field name’ was given for preliminary use 8

Plate 2 (A, B and C). Early efforts at monitoring the benthos of Roebuck Bay. Sampling at the One Tree stations in March 1996 when we found a yellow sea snake in one of the mudskipper burrows! Photo's by Theunis Piersma. Results and discussion 9

3. RESULTS AND DISCUSSION seagrass cover on the northern shore of Roebuck Bay (D.I. Rogers pers. comm.). 3.1. TROPICAL SEASONS 3.2. OVERALL BIODIVERSITY The intertidal macrozoobenthic animals of Roebuck Bay (as well as the birds, the Excluding the polychaetes (except two wallabies and the people) encounter taxa), a total of 139 different taxa were strong seasonal changes in rainfall and encountered among the 23,000 animals air temperature (Fig. 6). Rainfall peaks in retrieved from the core-samples taken at January, February or March, with two of the One Tree and Fall Point stations the six years (1996 and 2000) showing a single peak and the other four a second period with rain in either May or June. 1996199719981999 2000 2001 1000 Although monthly average maximum air 900 temperatures varied with 7ºC only from 800 28 to 35ºC, there were brief excursions 700 to the lowest part of the temperature 600 500 range during the middle of each year, 400 with broader bands of higher tempera- 300 tures from October through April. The precipitationmmin 200 monthly average minimum air tempera- 100 40

tures varied twice as much, with lows °C down to 12ºC in June and highs of up to 27ºC in December or January. During 35 these five years Roebuck Bay was visit-

daytemp ed by a cyclone one time. In late January 30 1998 a category 1 cyclone had some striking effects on some of the outlets of 25 Crab Creek whereas in April 2000 the cyclone ‘Rosita’ passed 40 km south of max average 30 Broome, coming on land between Bush °C Point and the Ecobeach tourist resort (which was completely destroyed). The 25 latter cyclone is thought to be responsi- ble for the disappearance of most of the 20

15 Figure 6. Seasonal patterns of rainfall, average maximum and average minimum air temperature at Broome over the entire period of study, 1996-2001. average min daytemp daytemp min average 10 The data are presented as monthly sums (precipita- 0 12 24 36 48 60 72 tion) or averages (temperature), and were kindly made months from January 1996 available by the Bureau of Meteorology in Perth. 10 Overall biodiversity

Table 1. For all different macrozoobenthic taxa found during MONROEB the numbers are given per site (Sum) and over all sites (Total sum). FP-A= Fall Point-A, FP-B= Fall Point-B, OT-A= One Tree-A, OT-B= One Tree-B

Species name Group Sum Sum Sum Sum Total sum FP-A FP-B OT-A OT-B juvenile bivalve Bivalvia 2 1 4 2 9 Nucula cf. astricta Bivalvia 36 18 2 56 Ledella spec. Bivalvia 4 1 3 8 Solemya cf. terraereginae Bivalvia 14 24 38 Anadara granosa Bivalvia 1 39 47 87 Modiolus micropterus Bivalvia 1 2 3 Atrina spec. Bivalvia 1 1 Anodontia omissa Bivalvia 184 398 1 583 Divaricella irpex Bivalvia 280 208 1 4 493 Ctena "rough" Bivalvia 49 61 110 Ctena "smooth" Bivalvia 1 1 Montacuta spec. Bivalvia 1 2 3 Mysella "curva" Bivalvia 3 1 4 Pseudopythina macrophthalmensis Bivalvia 7 5 3 7 22 Scintilla spec. Bivalvia 2 22 2 26 Heterocardia gibbosula Bivalvia 3 15 21 39 Mactra spec. 1 Bivalvia 1 1 Mactra? Bivalvia 1 4 4 7 16 Mactra grandis Bivalvia 2 2 1 5 Raeta spec. Bivalvia 2 2 Cultellus cultellus Bivalvia 15 2 17 Siliqua pulchella Bivalvia 22 6 138 137 303 Tellina capsoides Bivalvia 141 140 281 Tellina piratica Bivalvia 236 188 5 7 436 Tellina inflata Bivalvia 3 2 5 Tellina amboynensis Bivalvia 18 2 1 2 23 Tellina oval Bivalvia 1 1 Tellina pointed Bivalvia 7 1 8 Tellina cf remies Bivalvia 1 1 Mud Tellina Bivalvia 1 9 10 Tellina "mysia" Bivalvia 1 12 13 Tellina “exotica” Bivalvia 39 48 110 117 314 Tellina "exotica rose" Bivalvia 15 5 20 Gari lessoni Bivalvia 3 3 1 7 Solen spec. Bivalvia 1 2 1 4 Anomalocardia squamosa Bivalvia 4 2 1 7 Veneridae spec. Bivalvia 1 2 3 Placamen gravescens Bivalvia 2 2 Tapes spec. Bivalvia 1 1 Laternula creccina Bivalvia 6 6 Stenothyra spec. Gastropoda 7 7 Vitrinellidae spec. Gastropoda 1 1 Nerita spec. Gastropoda 1 3 4 Epitoniidae spec. Gastropoda 3 2 8 13 Cerithidea cingulata Gastropoda 1 8 9 Eulimidae spec. Gastropoda 19 40 59 Polinices conicus Gastropoda 21 14 3 6 44 Natica "dull colored" Gastropoda 2 2 4 Natica "with brown band" Gastropoda 4 4 Columbellidae spec. Gastropoda 1 1 Nitidella essingtonensis Gastropoda 3 7 2 12 Nassarius dorsatus Gastropoda 14 21 364 323 722 Nassarius "small Ingrid" Gastropoda 1 22 21 44 Vexillum radix Gastropoda 33 54 87 Turridae spec. Gastropoda 2 4 6 Terebridae spec. Gastropoda 3 3 Haminoae "green" Gastropoda 7 7 Acteon spec. Gastropoda 1 1 Overall biodiversity 11

Tornatina spec. Gastropoda 4 1 40 42 87 Salinator cf. burmana Gastropoda 1 32 24 57 Pyramidellidae spec. Gastropoda 2 1 3 Leucotina spec. Gastropoda 1 4 5 Chrysallida spec. Gastropoda 6 5 11 Syrnola spec. Gastropoda 3 2 5 Odostomia spec. Gastropoda 1 1 Tiberia spec. Gastropoda 1 1 Laevidentalium cf. lubricatum Scaphopoda 57 74 8 22 161 Dentalium cf. bartonae Scaphopoda 2 114 131 247 Chaetopteridae spec. Polychaeta 2426 2450 4876 Oweniidae spec. Polychaeta 3433 771 16 26 4246 Ostracoda "oval, smooth" Crustacea 489 565 10 7 1071 Ostracoda "square, sculptured" Crustacea 26 61 87 Ostracoda "denticulated" Crustacea 63 59 2 1 125 Gam mariidae spec. Crustac ea 11 41 3 1 56 Anthura spec. Crustac ea 4 12 16 Tanaidacea spec. Crustac ea 34 22 56 Cumacea spec. Crustacea 1 2 3 Mantis Shrimp (Squillidae) Crustacea 6 8 4 1 19 Caridae (shrimp) Crustacea 11 23 15 33 82 Gourretia coolibas Crustacea 2 1 2 5 Callianassa spec. Crustacea 2 2 hermit crab Crustac ea 108 44 13 18 183 Dorippe cf. australiensis Crustacea 4 4 8 Raninidae spec. Crustacea 1 1 Matuta planipes Crustac ea 10 3 13 cf. Myrodes eudacty lus Crustac ea 3 14 3 2 22 Nursia abbreviata Crustacea 9 1 2 1 13 Ebalia spec. Crustacea 3 3 Leucosia spec.D Crustacea 2 2 Portunidae spec. Crustacea 4 5 9 Halicarcinus cf. australis Crustac ea 278 286 2 1 567 Mictyris longicarpus Crustac ea 5 5 1 11 Pinnotheres cf cardii Crustacea 3 2 1 3 9 Pilumnidae spec. Crustacea 2 2 Hairy crab (Pilumnidae) Crustacea 2 3 1 6 Hexapus spec. Crustacea 12 13 1 4 30 Macrophthalmus spec. Crustac ea 170 217 230 256 873 Uca spec. Crustacea 1 1 Edwardsia spec. Anthozoa 2 4 2 1 9 Shell anemone Anthozoa 2 1 3 Pycnogonida spec. Pycnogonida 4 6 10 Lingula spec. Brachiopoda 118 80 1 199 Amphiura (Ophiopeltis) tenuis Ophiuroidea 1882 1742 6 6 3636 Astropecten granulatus Asteroidea 83 7 90 Peronella tuberculata Echinoidea 1 1 2 Holothuroidea spec. Holothuroidea 2 2 Leptopentacta grisea Holothuroidea 1 5 6 Holothuria A Holothuroidea 5 2 5 1 13 Stolus buccalis Holothuroidea 2 2 Rooted Tunicate Tunicata 46 46 Sandy Colonial Tunicate Tunicata 52 751 803 Mudskipper (Periophthalmidae) Pisces 9 9 57 60 135 Fish (Gobiidae) Pisces 12 20 17 54 103 12 Overall biodiversity

(Table 1). The taxon-list includes 40 dif- mals in total), which occurred most abun- ferent bivalves, 26 gastropods, 2 dantly at the One Tree stations. Other scaphopods, 7 echinoderms and 17 abundant gastropods were Vexillum radix crabs. The total number of macrozooben- (87; Fall Point only), Tornatina spec. (87; thic species is much higher in the sands One Tree only), Eulimidae spec. (59; Fall off Fall Point than in the blue muds off Point only) and Salinator cf. burmana One Tree (Fig. 7), and this is true also for (57; One Tree only), Polinices conicus the diversity of bivalves, gastropods and (44), and Nassarius “small Ingrid” (44; crabs. It is also clear that there are hard- One Tree only). Two different ly any differences between the relatively scaphopods were found: Dentalium cf. nearshore station and the one further off, bartonae (247 animals in total) that was at both sites the station further offshore only found at the One Tree stations and accumulated a few more species (Fig. 7). Laevidentalium cf. lubricatum (161) that Among the bivalves the most common was most abundant at the Fall Point sta- species at the Fall Point stations were tions but was also occasionally found at Anodontia omissa (583 animals were One Tree. found in total, Table 1), Divaricella irpex The most common crab taxon, found at (493) and Tellina piratica (436). The most all stations in almost equal numbers, common bivalves at the One Tree sta- were sentinel crabs Macrophthalmus tions were Tellina “exotica” (227), Tellina spec. (873 animals in total). It is likely capsoides (281) and Siliqua pulchella that this taxon comprises different (275). Tellina “exotica” and Siliqua pul- species of Macrophthalmus. Another chella were also found in fair numbers at abundant crab near Fall Point was the the Fall Point stations, but by and large spider crab Halicarcinus cf. australis each bivalve species occurred at one of (567). Two other crabs from the Fall the two sites rather than both (Table 1). Point stations found in reasonable num- The most common gastropod was the bers were Hexapus spec. (30; mostly scavenger Nassarius dorsatus (722 ani- Fall Point) and cf. Myrodes eudactylus

120 (22). Of the polychaete worms we sorted 100 and counted, the two most obvious 80 all species groups were the Chaetopteridae and bivalves 60 gastropods Oweniidae. A total of 4876 40 crabs Chaetopteridae were found at Fall Point. number of species Most of the 4246 Oweniidae were also 20 found at Fall Point, but lower numbers 0 occurred at the One Tree stations. Three FP-A FP-B OT-A OT-B different Ostracoda were found, with the Figure 7. Total number of taxa (here called ‘species’) smooth form from Fall Point being the encountered during the MONROEB-sampling and sorting efforts between 1996 and 2001, with separate most common. Hermit crabs (183) oc- columns for the bivalves, gastropods and crabs. Seasonal changes in abundance 13 curred at both the Fall Point and One 1998, with a second smaller peak in late Tree stations, but species identity might 1999. Another Lucinid, Divaricella irpex differ between the two sites. Some 10 (Fig. 10), showed clear cyclicity, but on a times a seaspider Pycnogonida was bi-annual rather than an annual basis. found in the Fall Point samples. The bra- Over the time series, peak densities chiopod Lingula spec. (199) occurred on- were reached three time, in late 1996, ly at Fall Point. The brittlestar Amphiura early 1998 and early 2000. The thin- tenuis was very common (3636) and al- shelled Siliqua pulchella which mostly most completely restricted to Fall Point. occurred in the soft deep mud off One The starfish Astropecten granulatus (90) Tree, showed a single peak density in was only found at Fall Point. Two tuni- mid 1997 (at the time of the mapping ef- cates were found, again at the Fall Point fort by Pepping et al. 1999) and has stations. Mudskippers Periophtalmidae been in decline since with no outspoken (135) ended up mostly in some of the rhythmicity (Fig. 11). samples taken near One Tree. Gobiid A similar pattern to Siliqua was found in fishes (103) came from all stations. the Tellinid bivalve Tellina capsoides which occurred in the muds off One Tree 3.3. SEASONAL CHANGES IN ABUN- rather than the sands off Fall Point (Fig. DANCE 12). After a single peak in late 1996- early 1997, the species went into decline In a series of figures (Fig. 8 to Fig. 22) and had completely disappeared by late we will now present the seasonal 1999. Again, there was no evidence for changes in average densities (per m²) any kind of circannual ryhthmicity in over all four stations of the 15 numerical- numbers. Just as Divaricella irpex (Fig. ly dominant taxa, most of which are bi- 10), the second Tellinid, Tellina piratica, valves. Densities are plotted as date- occurred in peak numbers three times specific average densities over time, over the six years of this study (Fig. 13). through which a kind of running average The timing of the peaks also coincided (the LOWESS routine of SYSTAT, ten- with those of Divaricella, with high num- sion 0.2) was fitted to lead the eye in our bers in late 1996, mid 1998 and early to search for evidence for seasonal cyclicity mid 2000. The third Tellinid was Tellina (also called circannual rhythmicity). “exotica”, which occurred at both the Figure 8 shows the density changes of sandy and the muddy site (Fig. 14). From the bloody cockle Anadara granosa. the very start of the study in early 1996, it Highest densities were found in early to went into decline to reach a level of low mid 1997, with little evidence of clearly numbers from 1999 onwards. This pat- repeated circannual variations. Apart tern resembles the numerical changes in from two high values in late 1996 that do Tellina capsoides (Fig. 12). not show up in the LOWESS routine, the The single gastropod that occurred in Lucinid ‘eye-shell’ Anodontia omissa large enough numbers to examine sea- (Fig. 9) peaked in late 1997 and early sonality was the ‘Ingrid-eating snail’ 14 Seasonal changes in abundance

Anadara granosa

1996 1997 1998 1999 2000 2001 30

numbers/m² 10

0 0 12 24 36 48 60 72 months from January 1996

Figure 8. Changes in average density of Anadara granosa from early 1996 to mid 2001.

Anodontia omissa

1996 1997 1998 1999 2000 2001 100 90 80 70

2 60 50 40

numbers/m 30 20 10 0 0 12 24 36 48 60 72 months from January 1996

Figure 9. Changes in average density of Anodontia omissa from early 1996 to mid 2001. Seasonal changes in abundance 15

Divaricella irpex

1996 1997 1998 1999 2000 2001 40

2 30

numbers/m

0 0 12 24 36 48 60 72

months from January 1996

Figure 10. Changes in average density of Divaricella irpex from early 1996 to mid 2001.

Siliqua pulchella

1996 1997 1998 1999 2000 2001 40

30 2

20 numbers/m

0 0 12 24 36 48 60 72

months from January 1996

Figure 11. Changes in average density of Siliqua pulchella from early 1996 to mid 2001. 16 Seasonal changes in abundance

Tellina capsoides

1996 1997 19981999 2000 2001 40

30 2 20

numbers/m 10

0 0 12 24 36 48 60 72

Figure 12. Changes in average density of Tellina capsoides from early 1996 to mid 2001.

Tellina piratica

1996 1997 1998 1999 2000 2001 40

30 2

20 numbers/m

0 0 12 24 36 48 60 72

Figure 13. Changes in average density of Tellina piratica from early 1996 to mid 2001. Seasonal changes in abundance 17

Tellina cf. exotica

1996 1997 1998 1999 2000 2001 25

20 2 15

10 numbers/m

0 0 12 24 36 48 60 72 months from January 1996

Figure 14. Changes in average density of Tellina “exotica” from early 1996 to mid 2001.

Nassarius dorsatus

1996 1997 1998 1999 2000 2001 80 70 60

2 50 40

numbers/m 30

10 0 0 12 24 36 48 60 72

months from January 1996

Figure 15. Changes in average density of Nassarius dorsatus from early 1996 to mid 2001. 18 Seasonal changes in abundance

Nassarius dorsatus (Fig. 15). Apart from June 1997 (Pepping et al. 1999), now a decline in the last two years of obser- appear to only have been that abundant vation this species showed peak num- in mid 1997, being absent before and af- bers repeatedly after the cold season, in ter that year (Fig. 18)! The tubeworms mid 1996, 1997, 1998 and 1999, sug- Oweniidae peaked in early 1997, again gesting repeated settlements of new co- almost a year later in December 1997 horts. and once more in October 2000 (Fig. The first tusk-shell or scaphopod, the 19). Both these polycheate worm taxa smoothly textured Laevidentalium cf. lu- therefore had strong and erratic occur- bricatum had a rather indistinct pattern of rences, where high numbers alternate numerical abundance, with high numbers with period of absence. In neither case in 1996 and 1997 and again in late 2000 was there any evidence for a seasonal (Fig. 16). The second, grooved, tusk- effect. shell Dentalium cf. bartonae started off The two crab taxa that can be exam- with low numbers and ended with low ined, the tiny ‘spider crab’ Halicarnus cf. numbers as well, and peaked in 1998 australis (Fig. 20) and the sentinel crabs (Fig. 17). In neither of the tusk-shells was belonging to the genus Macrophthalmus there any sign of circannual rhythmicity. (Fig. 21) both showed great variations The abundant ‘plastic tubeworms’ between successive sampling dates, but Chaetopteridae that were such a sorting quite clear seasonal patterns of numeri- problem during the mapping effort in cal change. Halicarcinus peaked four

Laevidentalium cf. lubricatum

1996 1997 1998 1999 2000 2001 30

2 20

numbers/m 10

0 0 12 24 36 48 60 72

months from January 1996

Figure 16. Changes in average density of Laevidentalium cf. lubricatum from early 1996 to mid 2001. Seasonal changes in abundance 19

Dentalium cf. bartonae

1996 1997 1998 1999 2000 2001 40

numbers/m 10

0 0 12 24 36 48 60 72

months from January 1996

Figure 17. Changes in average density of Dentalium cf. bartonae from early 1996 to mid 2001.

Chaetopteridae

1996 1997 1998 1999 2000 2001 2000

1500 2

1000 numbers/m 500

0 0 12 24 36 48 60 72

months from January 1996

Figure 18. Changes in average density of plastic tubeworms Chaetopteridae from early 1996 to mid 2001. 20 Seasonal changes in abundance

Oweniidae

1996 1997 1998 1999 2000 2001 800 700

600 500 2 400 300

numbers/m 200 100 0 0 12 24 36 48 60 72

months from January 1996

Figure 19. Changes in average density of tubeworms Oweniidae from early 1996 to mid 2001.

Halicarcinus cf. australis

1996 1997 1998 1999 2000 2001 70

50 2 40

30 numbers/m 20

0 0 12 24 36 48 60 72

months from January 1996

Figure 20. Changes in average density of the crab Halicarninus cf. australis from early 1996 to mid 2001. Seasonal changes in abundance 21

Macrophtalmus spec.

1996 1997 1998 1999 2000 2001 60

2 30

numbers/m 10

0 0 12 24 36 48 60 72 months from January 1996

Figure 21. Changes in average density of sentinel crabs Macrophthalmus spec. from early 1996 to mid 2001.

Amphiura tenuis 1996 1997 1998 1999 2000 2001 300

2 200

numbers/m 100

0 0 12 24 36 48 60 72 months from January 1996

Figure 22. Changes in average density of the brittle star Amphiura tenuis from early 1996 to mid 2001. 22 Recruitment patterns times in the middle of the year (1996, function of time of a single cohort, and 1997, 1999 and 2000), whereas the size-frequency distribution over the Macrophthalmus peaked three times in entire study period of this particular co- the middle of the year (1996, 1998 and hort assuming that they stay put (Fig. 1999). The abundant brittle star of Fall 23). If the size-frequency distributions Point Amphiura tenuis, showed a gradual that we generate on the basis of the 6 increase in numbers over the study peri- years of monitoring data roughly conform od, with peak numbers in late 2000 (Fig. to the pattern given there (i.e. peak num- 22). bers at small body size and a gradual decline with a long tails thereafter), under 3.4. RECRUITMENT PATTERNS the assumption that we have fairly sampled one or more cohorts over their en- To generate some insight into aspects of tire lifetime, we can conclude that this in- settlement of new cohorts and the possi- dicates a stationary, growing population bility of movements by larger macro- that is unlikely to exhibit mass movement zoobenthic animals we have constructed over the mud- and sandflats later in life. hypothetical (but roughly realistic; see The right panel of Fig. 23 thus gives us a e.g. van der Meer et al. 2000) curves for shape that we can compare our data the density and body size changes as a with.

1200

1000

800

600 1200

DENSITY 400 1000

200 800

0 600 11

10 DENSITY 400 9 8 200 7 0 6 1 2 3 4 5 6 7 8 9 10 11 SIZE 5 SIZE 4 3 2 1 0 1 2 3 4 5 6 7 YEAR

Figure 23. Hypothetical changes in the density and body size (left two panels) of a macrozoobenthic animal that settles in a density of 1000/m² at a body size of 2 mm, incurs an annual survival of 40% and shows a logistic type growth over its lifetime. The expected size-frequency distribution is given in the right panel and shows a density peak at small sizes and increasingly gradual disappearance thereafter. Recruitment patterns 23

As a second step, at a (somewhat arbi- 1997, after the wet season (Fig. 25). A trary) value in the size distribution we smaller settlement of Anadara may have made cut-off to examine if there exist any taken place after the wet of 2000. There differences in changes in numerical is much variation in the density of larger abundance of the smallest and larger an- Anadara, with the decline over the years imals in the population. This exercise probably reflecting the disappearance of may tell us when settlement took place, the strong 1997 cohort. and whether these settlement patterns bear any resemblance to seasonal (cli- matic) factors. The bloody cockle Anadara granosa beautifully obeyed the size-frequency distribution expected from single settle- Anadara granosa ment and growth (Fig. 24). Particularly 30 large numbers occurred in early and mid small

2 Anadara granosa small large 0 15 6 large

numbers/m 5

10 4

3 numbers 5 2

0 0 0 10 20 30 40 50 0 12 24 36 48 60 72 months from January 1996 size (mm) Figure 25. Changes in the densities of small and large Figure 24. Size-frequency distribution of Anadara gra- Anadara granosa (as based on the size-frequency dis- nosa on the basis of animals found in the monitoring tribution of Fig. 24) from early 1996 to mid 2001. samples between 1996 and 2001. 24 Recruitment patterns

The deeply buried and small-footed lu- 1999 (Fig. 27). In fact, the three clear cinid Anodontia omissa also showed the peaks in the density of small Anodontia expected size-frequency distribution for a were all followed by peaks in the density sedentary species (Fig. 26). There ap- of larger Anodontia, suggesting fast peared to have been recruitment events growth and a life span that is little longer late in most years, but these events were than a year. most pronounced in 1996, 1997 and

Anodontia omissa 90 small 80 70 60 50 40 30 20 Anodontia omissa 10

2 small large 0 100 60 large 90 50 80

numbers/m 70 40 60 50 30

numbers 40 20 30

20 10 10 0 0 0 4 8 12 16 0 12 24 36 48 60 72 months from January 1996 size (mm)

Figure 27. Changes in the densities of small and large Figure 26. Size-frequency distribution of Anodontia Anodontia omissa (as based on the size-frequency dis- omissa on the basis of animals found in the monitoring tribution of Fig. 26) from early 1996 to mid 2001. samples between 1996 and 2001. Recruitment patterns 25

The size-frequency distribution of the and especially in 1996, 1997, 1999 and second lucinid, Divaricella irpex (Fig. 28), 2000. Each of these recruitment events resembles that of Anodontia omissa but appears to have been followed by an in- shows more irregularity. Despite this ir- crease in the population of larger-sized regularity, the picture appears consistent Divaricella. Both species of Lucinidae with what we would expect of a seden- settled late in the year (i.e. just before tary species. The density figures are also the wet season) with growth during the more irregular (Fig. 29), but nevertheless subsequent wet season and little survival suggest that recruitment occurred some- beyond one year of life. what later than Anodontia in most years

Divaricella irpex 15 small

Divaricella irpex 2 small large 0 70 30 large

60 numbers/m

50 20 40

30 numbers 10 20

0 0 0 5 10 15 20 0 12 24 36 48 60 72 size (mm) months from January 1996 Figure 29. Changes in the densities of small and large Figure 28. Size-frequency distribution of Divericella Divaricella irpex (as based on the size-frequency dis- irpex on the basis of animals found in the monitoring tribution of Fig. 28) from early 1996 to mid 2001. samples between 1996 and 2001. 26 Recruitment patterns

The size-frequency distribution of early 1998. Nevertheless, the size-fre- Siliqua pulchella (Fig.30) bears little re- quency distribution does suggest move- semblance to the hypothetical size-fre- ments of larger individuals over the area quency distribution of a resident species of intertidal flats, and the fact that the (Fig. 23). Although this could be due to densities of larger-sized Siliqua are much the presence, at the start of the study, of higher than the densities of small-sized a strong cohort of individuals with body Siliqua is consistent with this. Thus, sizes that were not subsequently Siliqua settled early in the calendar-year achieved again (see below for Tellina (late in the wet season), showed massive capsoides), this does not seem to be the movements after settlement and did not case as Siliqua is probably a rather become much older than 1.5 to 2 years. short-lived species (Fig. 31). The latter is suggested by the presence of a strong Siliqua pulchella 15 cohort of small-sized animals in early small 1997 followed by a similarly strong cohort of larger animals later that year, which then declined and disappeared in 10

2 Siliqua pulchella 0 small large 35 30 large

numbers/m 30

25 20 20

15 numbers 10 10

0 0 0 10 20 30 0 12 24 36 48 60 72 months from January 1996 size (mm) Figure 31. Changes in the densities of small and large Figure 30. Size-frequency distribution of Siliqua pul- Siliqua pulchella (as based on the size-frequency dis- chella on the basis of animals found in the monitoring tribution of Fig. 30) from early 1996 to mid 2001. samples between 1996 and 2001. Recruitment patterns 27

Although the size-frequency distribu- late in 1996, a recruitment event which tion of Tellina capsoides at first sight sug- translated in increasing densities of larg- gests massive movement at large size er specimens early in 1997 (Fig. 33), the (Fig. 32), the high frequency of bivalves strong cohort of older animals present in longer than 35 mm is due to a large co- early 1996 was never replaced and hort of old animals being present in our Tellina capsoides thus gradually disap- study area (offshore from One Tree) in peared from the One Tree stations (see early 1996, at the beginning of our study. Fig. 12). Tellina capsoides probably can Although there was some recruitment live some 2-3 years.

Tellina capsoides 12 small 10

Tellina capsoides 2 small large 0 20 30 large

numbers/m 15 20

10 numbers 10 5

0 0 0 10 20 30 40 50 0 12 24 36 48 60 72 size (mm) months from January 1996

Figure 32. Size-frequency distribution of Tellina cap- Figure 33. Changes in the densities of small and large soides on the basis of animals found in the monitoring Tellina capsoides (as based on the size-frequency dis- samples between 1996 and 2001. tribution of Fig. 32) from early 1996 to mid 2001. 28 Recruitment patterns

The size-frequency distribution of in the middle of the year (i.e. after the Tellina piratica (Fig. 34) is consistent with wet season), with reasonable recruitment a sedentary life-style (i.e. no movements in 1997 leading to a build-up of larger an- after settlement) and a lifespan some- imals in early and mid 1998. The subse- what longer than 2 years. This fact and quent collapse is a bit strange as it is not their low densities overall may be the preceded by a similar low in the densities reason that it is hard to interpret the nu- of small animals. A recruitment-peak in merical changes over time (Fig. 35). mid 2000 to some extent restored the Recruitment appeared to have occurred population of Tellina piratica.

Tellina piratica 20 small

2 Tellina piratica 0 small large 25 40 large

numbers/m 20 30

15 20

numbers 10

10 5

0 0 0 10 20 30 40 0 12 24 36 48 60 72 size (mm) months from January 1996

Figure 34. Size-frequency distribution of Tellina pirati- Figure 35. Changes in the densities of small and large ca on the basis of animals found in the monitoring Tellina piratica (as based on the size-frequency distri- samples between 1996 and 2001. bution of Fig. 34) from early 1996 to mid 2001. Recruitment patterns 29

Tellina “exotica” is a small (Fig. 36) and 1997, but this cohort disappeared rapidly probably short-lived species that showed to be replaced immediately by a new co- increases in densities of small animals hort that settled in late 1997. The latter both early and late in the year (i.e. at the cohort disappeared in the course of beginning ánd the end of the wet season; 1998. Since, recruitment of Tellina “exoti- Fig. 37). Good recruitment in 1996 led to ca” has been low, so that total densities a build-up of larger animals in early have remained low as well (see Fig. 14).

Tellina cf. exotica 20 small

Tellina cf. exotica 2 0 small large 20 40 large

numbers/m 30 15

20 10 numbers

10 5

0 0 0 5 10 15 20 25 0 12 24 36 48 60 72 months from January 1996 size (mm) Figure 36. Size-frequency distribution of Tellina “exoti- Figure 37. Changes in the densities of small and large ca” on the basis of animals found in the monitoring Tellina “exotica” (as based on the size-frequency distri- samples between 1996 and 2001. bution of Fig. 36) from early 1996 to mid 2001. 30 Recruitment patterns

The scavenging and predatory gastro- mid 1997 (Fig. 39) was immediately fol- pod Nassarius dorsatus (Ingrid-eating lowed by increased densities of the larg- snail) has all the characteristics of er animals. Recruitment has been some- sedentary species (Fig. 38), with recruit- what lower in 1998 and 1999 and was ment taking place in the middle of the virtually absent in 2000 (even though year (the cold season; Fig. 39), rapid densities of large animals were good in growth and a life span little longer than a January 2001: displacement of older indi- year. Peak recuitment in mid 1996 and viduals from elsewhere?).

Nassarius dorsatus 60 small 50

Nassarius dorsatus 0 small large 20 150 large

numbers/m²

100 10 numbers

50 5

0 0 0 10 20 30 40 0 12 24 36 48 60 72 months from January 1996 size (mm)

Figure 39. Changes in the densities of small and large Figure 38. Size-frequency distribution of Nassarius Nassarius dorsatus (as based on the size-frequency dorsatus on the basis of animals found in the monitor- distribution of Fig. 36) from early 1996 to mid 2001. ing samples between 1996 and 2001. Optimizing future benthic monitoring 31

3.5. OPTIMIZING FUTURE BENTHIC ties over time for the nearshore and off- MONITORING shore stations for the sites where the seven most numerous species selected From 1996 to 2001 the BBO-wardens were most common (Figs. 40-46). We al- and the volunteers helping with MON- so calculated the correlations between ROEB not only visited the two sites (Fall the numbers found at each of the sites. Point and One Tree) in the course of The result is that samples taken at the each sampling day, at each of the sites relatively nearshore and offshore stations they also went to two stations, a relative- give very similar answers. Figures 40 to ly nearshore and a relatively offshore 46 show that the patterns are clearly one. On the sandy sediment off Fall comparable and all correlations are posi- Point this is not a big issue, but at One tive. In 5 of the 7 cases the r-value is al- Tree it does take a lot of effort to get to so significantly greater than zero (Table the second station at 250 m from the 2). The correlations are highest for the shoreline. Table 1 and Fig. 7 already One Tree stations, which in our experi- showed the congruence in species diver- ence is a particularly homogenous area sity and total numbers of animals collect- of mud. ed among the two stations at each of the This means that in the future we can site. Here we have made a further com- do with a single station at each of the two parison among the data for bivalves to sites. The general congruence also see whether changes in densities over means that the precise location of this time are also comparable between sites. site is not very important, and that it can In order to do so we have plotted densi- be in the vicinity of the nearshore sites,

Anadara granosa Anodontia omissa 15 100 OT-A 90 FP-A OT-B 80 FP-B

2 10 70 2 60 50 40

numbers/m

5 numbers/m 30 20 10 0 0 0 12 24 36 48 60 72 0 12 24 36 48 60 72 months from January 1996 months from January 1996

Figure 40. Comparison of the changes in density of Figure 41. Comparison of the changes in density of Anadara granosa at the nearshore (A) and offshore Anodontia omissa at the nearshore (A) and offshore (B) stations off One Tree. (B) stations off Fall Point. 32 Optimizing future benthic monitoring to reduce workload. Nevertheless, the same total of 8 samples consisting of 6 (1/120 m²) cores should be taken, as re- ductions in the number of individuals col- lected per date would lead to less interpretable results (i.e. less interpretable results for more taxa than at present).

Table 2. Pearson product-moment correlations between the densities measured on different occasions during MONROEB (n indicating the number of comparisons) on the nearshore (A) and offshore (B) sites.

Species Pearsons r p n Site Anadara granosa 0.568 <0.005 45 One Tree Anodontia omissa 0.237 >0.5 48 Fall Point Divaricella irpex 0.368 <0.01 48 Fall Point Siliqua pulchella 0.549 <0.005 45 One Tree Tellina piratica 0.238 >0.5 48 Fall Point Tellina capsoides 0.679 <0.005 45 One Tree Tellina “exotica” 0.415 <0.005 48 One Tree

Divaricella irpex Siliqua pulchella 30 25 FP-A OT-A FP-B 20 OT-B 2 20 2 15

10 numbers/m 10 numbers/m

0 0 0 12 24 36 48 60 72 0 12 24 36 48 60 72 months from January 1996 months from January 1996

Figure 42. Comparison of the changes in density of Figure 43. Comparison of the changes in density of Divaricella irpex at the nearshore (A) and offshore (B) Siliqua pulchella at the nearshore (A) and offshore (B) stations off Fall Point. stations off One Tree. Optimizing future benthic monitoring 33

Tellina capsoides Tellina piratica 25 25 OT-A FP-A 20 OT-B 20 FP-B

2 2 15 15

10 10

numbers/m numbers/m

5 5

0 0 0 12 24 36 48 60 72 0 12 24 36 48 60 72 months from January 1996 months from January 1996

Figure 44. Comparison of the changes in density of Figure 45. Comparison of the changes in density of Tellina capsoides at the nearshore (A) and offshore Tellina piratica at the nearshore (A) and offshore (B) (B) stations off One Tree. stations off One Tree.

Tellina cf. exotica 16 OT-A OT-B 12 2

8 numbers/m 4

0 0 12 24 36 48 60 72 months from January 1996

Figure 46. Comparison of the changes in density of Tellina “exotica” at the nearshore (A) and offshore (B) stations off One Tree. 34 Optimizing future benthic monitoring

Plate 3. The pindan cliffs near the One Tree stations after a rainstorm in March 1996. Photograph by Theunis Piersma. General discussion 35

4. GENERAL DISCUSSION MONROEB. For a start, there is the great abundance of plastic tubeworms A reasonable concern shared by several Chaetopteridae that made life so difficult people repeatedly involved in the month- during ROEBIM-97 (Pepping et al. 1999); ly mudsampling was whether the repeat- plastic tubeworms were absent during ed sampling effort would disturb the local both the March 2000 and the June 2002 sediments so much that this would have efforts, a picture fully consistent with the reduced numbers of macrozoobenthic MONROEB results. Then there is the rel- animals in the course of the years. We ative abundance of Siliqua pulchella on would expect fragile sedentary species to the soft muds of Kraken Corner in June be most easily affected. That one such 1997 and the near-absence there in both species, the brittle star Amphiura tenuis, March 2000 and June 2002 (Rogers & together with the lucinid bivalve Taylor 2002). Again this is consistent with Divaricella irpex, were the only taxa that the results of MONROEB. The relative showed a steady increase over time scarcity of Ingrid-eating snails Nassarius since early 1996, suggests that the role dorsatus reported during June 2002 was of disturbance could only have been a reflected well by the MONROEB results. minor factor. We also like to note that the We conclude that the monitoring has precision with which the stations were lo- done a fine job in generating inter- cated (counting steps by different team pretable seasonality data for about 15 leaders, rather than the consistent use of different taxa. modern, high precision GPS) was not This bring us back to the questions we very high, which would have been a con- set out to answer with MONROEB: to cern in itself was it not for the fantastic which extent are settlement and growth congruence in species composition and seasonally structured and is the level of densities among the two stations at each seasonality comparable to what we find site. Thus, we believe that the area over at well-studied north temperate mud- which the monitoring samples were col- flats? To structure the discussion, we lected was perfectly able to cope with the have prepared a summary table (Table 3) disturbance inflicted by the human ob- outlining the basic biological features for servers. 7 bivalves and 1 gastropod as discov- In fact, it is rather gratifying to see that ered during this study. Half of the species trend apparent from other mudsampling are particularly short-lived, with the oth- efforts, notably the repeated mapping ef- ers having lifespans typical of mollusks forts of the northern shores in June 1996 from north temperate mudflats. Like the (Pepping et al. 1999), March 2000 north temperate situation, recruitment is (Rogers et al. 2000) and June 2002 highly seasonal with a tendency for one (SROEBIM, report in prep.) came up with recruitment period to occur within each similar impressions on the abundance of year (two events in the case of the small various macrozoobenthic taxa as did tellinid bivalve Tellina “exotica”). 36 General discussion

Table 3. Summary of the traits of 7 bivalve and 1 gastropod species as derived from the MONROEB observations.

Species Max shell Approximate Timing of settlement Move ment a fter length lifespan settlement? Anadara granosa 50 mm 3-4 yrs Late or just after the wet season No Anodontia omissa 15 mm 1 yr Early in the wet season No Divaricella irpex 18 mm 1 yr Before the wet season No Siliqua pulchella 28 mm 1.5-2 yrs Late in the wet season Yes Tellina capsoides 46 mm 2-3 yrs Early in the wet season? No Tellina piratica 38 mm 2 yrs After the wet, in the cold season No Tellina “exotica” 20 mm 1 yr Beginning ánd end of wet season No Nassarius dorsatus 32 mm 2 yrs? After the wet, in the cold season No

However, unlike the north temperate situ- staple in the diet of great and red knots. ation, there is little correspondence be- Unpredictability in species presence also tween species in when recruitment takes explains the observations of Tulp & de place. In fact, recruitment takes place Goeij (1994) who in February-April 1991 year-round, with some species settling found that a mussel species Modiolus (or appearing in our samples) before the micropterus then was both abundant and wet, others in the early wet, yet others in an important food item for great knots. the late wet and some after the wet in the We have only found a few large speci- cold season (Table 3). Only for the highly mens in surveys since, indicating that mobile species Siliqua pulchella is there Tulp & de Goeij (1994) observed what evidence for large-scale movement of may have been a one-off heavy spatfall older animals, with large animals turning of Modiolus. up in fair numbers at the One Tree sta- Of course the Yawuru are right when tions especially in late 1997 and early they tell us that during willburu 1998 (Fig. 31). (September) shellfish are getting fat and In summary, in a sense, the mudflats of that during larja (October-November, just Roebuck Bay as a larder for migratory before the wet) the shellfish are fat. As shorebirds is less dependable than the we have seen, the first small bloody mudflats of the Wadden Sea (Zwarts & cockles Anadara granosa turn up in our Wanink 1993). Timing of settlement is samples just after the wet, and by then much more variable, and what is more they have experienced a time as a free- important, there is great temporal vari- swimming pelagic larva and a time of ability in the presence/absence of poten- early growth as a tiny settled shell on the tial prey species. For example, Siliqua sediment. If ‘fat shellfish’ indicate cockles pulchella were so abundant in June 1997 that are ready to spawn, and spawning is that we thought them to comprise the triggered by the fresh water running over General discussion 37 the intertidal flats after the first big rainstorm in December or early January (brackish water is known to trigger spawning in the long-lived estuarine West-African species Anadara senilis; Wolff et al. 1987), then there would be 2- 3 months left for the pelagic and early settlement phases before we would find them in our sieves. This seems perfectly reasonable.

Plate 4. Innovation on the deep blue mud near the One Tree stations in 1997: the first and last use of skis! Photograph by Grant Pearson. 38 Acknowledgements 39

5. ACKNOWLEDGEMENTS Dermott and Tracy Stolman, André Joubert, Paula and Bill Rutherford. It happened during a tropical downpour Special thanks to Phil Joy for his extraor- in mid March 1996: GBP and TP were dinary fill-in role between wardens that crawling on their knees in the mud, kept the process rolling. amazed at the variety of creeping Special thanks also to the many offi- crawlies and realizing how little we know cers from the West Kimberley Branch of about what was out there. This was the The Department of Conservation and incentive to start a monitoring scheme of Land Management, especially Allen macrobenthic animals of the intertidal flat Grosse, Mike Lapwood, Tim Willing, of Roebuck Bay on 24 March 1996, Kingsley Miller and Jill Green. It is impor- which was to be run by wardens and vol- tant to note that West Kimberley District unteers from the Broome Bird through the then District Manager, Allen Observatory (BBO) with in-kind and lo- Grosse, contributed the initial seed capi- gistic support from the Western tal that enabled the monitoring to begin. Australian Department of Conservation Environs Kimberley provided ongoing and Land Management (CALM) and the support for the project and assisted from (now Royal) Netherlands Institute for Sea time to time with collections and process- Research (NIOZ). The monitoring ing of samples. It was not an easy task scheme was named MONROEB. BBO to get volunteers in the mud every and its wardens have played a major role month, especially not the mud of One in continuing this sampling programme. Tree. It is peculiar kind of enjoyment to Due to the immense effort of many par- go over your knees in the soft mud! Lots ticipants over five years now, a truly of people tried once. Sorting the samples unique record of temporal and seasonal as soon as they got back from the field changes on a tropical mudflat could now was another onerous job which require- be presented in this report. ment a kind of determination. The follow- A huge number of people (at least 126) ing list gives the names of all people who have been involved in this project in one helped in one way or another to get the way or another. During the first 18 poor benthic creatures from the mud into months, Ali Pentelow from Broome took the vials. Some names are incomplete, the lead and provided a solid foundation as some helpers were passing through that established the monitoring program BBO too quickly to get their names prop- during the first difficult months . From erly registered. However, they have to be that time on the Broome Bird thanked too! Observatory (BBO) wardens took the re- In chronological order: Ali Pentelow, sponsibility for carrying out the pro- Becky Hayward, Jon Fallaw, Janet gramme: thanks a million Becky Sparrow, Chris Hassell, Sheila Foster- Hayward and John Fallaw, Janet Nixon, Claas, Tim Willing, Kathryn from Sparrow and Chris Hassell, Alistair CALM, Jenny Noble, Janet Lankester, 40 Acknowledgements

Helen MacArthur, Rosemary MacArthur, eight Australian Wader Study Group Robert Kirwan, Heather Beswick, John members, A. Mayer, Adrian Boyle, Al Curran, Phil Joy, Robert Van Leeuwen, Dermer, Yus Rusila Noor, H. Rambiak, David Baker-Gabb, Peter West, Raoul W. Gebse, Susan, Tracey Stolman, P. Broughton, Christine McNamara, Michele, Cass Hutton, S. Hartvigsen, D. Shapelle McNee, Ray Lyons, Oliver Secombe, Jacquie Cochran, Ruth Vachez, Kathy Fletcher, Mavis Russell, Bonser, Maria Pedersen, Jan Lewis, Darlene, Sarah and Tim Cantrill and their Astrid and Guido Gomes, Liz Cochran, children, Shirley Cook, Barbara Lake, Persine Ayersberg, André Joubert, M. Mary Councillor, Ian Snadden, Paul and Slattery, Terry Strong, Jaenet, Peter Jake Botwell, Brenda, Michelle Tucker, Jun Matsui, Michael Curran, McDonald, Jean, Mike, Dick and Pam Jane Rusden, John Peterson, Diane Smith, Jeromy, Danny Rogers, Kerry Sherman, Sharin Mullaly, Magie Kurcz, Duff, Sharon, J. Woods, Clare Howard, Josh van Dijke, Melinda Glace, Andrea Magnolia Howard, Wilyarti Howard, Matt Feldpausch, Kelly Millenbah, Max Tishler, Gillis, Jacquie and Nigel Clark, B. Hart, and 15 other anonymous BBO-guests. A. Hart, M. Tarry, C. Tarry, A. Dunn, Rob Van Leeuwen of the Met-station at Nicole Grenfell, Sandie McCaig, Broome helped in the mud as well as be- Macafee, Julie Deleyev, Hunter, Blyth, hind the computer by regularly sending Shirley Slack-Smith, Pieter Honkoop, us weather data reports.

Plate 5. The second time monitoring at the Fall Point stations in April 1996: instructions by Theunis Piersma before entering the flats, with the Russian shorebird scientist Pavel Tomkovich on the right. Photograph by Petra de Goeij. Acknowledgements 41

In The Netherlands, especially in the The analysis of the data of this project lab, Pieter Honkoop had great input dur- was funded by the National Heritage ing the first year. Later we received help Trust through Environs Kimberley. from Mavis Russell and Danny Rogers Nelleke Krijgsman of the Royal during occasional visits to The Netherlands Institute for Sea Research Netherlands. Danny also read the draft (NIOZ) made the final lay-out of this re- report and made many useful sugges- port and Henk Hobbelink prepared the tions. cover and some figures.

Plate 6. Sorting the samples outside the Pearson Laboratory at Broome Bird Observatory in July 2002. Helen MacArthur on the left and Mavis Russell on the right, share the table with mollusk-specialist Shirley Slack- Smith. Photograph by Petra de Goeij. 42

Plate 7. Identification of invertebrates in the Pearson Laboratory at Broome Bird Observatory in July 2002, with Petra de Goeij on the left, and Pieter Honkoop on the right. Photograph by Theunis Piersma.

Plate 8. Pleasurable monitoring on the go at Fall Point, July 2002. Photograph by Theunis Piersma. 43

Plate 9. The chal- lenges of monitoring the benthos at the One Tree Stations: an adventure with the Police Cadets in July 2002. Photographs by Theunis Piersma.

A: inaugural photograph, everybody opti- mistic and clean,

B: off we go!,

C: some are faster than others, 44

D: first problems, but Grant is chatting up the strugglers,

E: first samples, first fun,

F: mothers of invention: the breast crawl works!, 45

G: steady progress at the nearest station,

H: I am greyer than you,

I: wrestling and sampling, it all happens at the same time, 46

J: the crawl back to the beach,

K: we have achieved!,

L: carted off for a good rinse. References 47

Kenneally, F.F., D.C. Edinger & T. Willing. 1996. Broome and beyond. Plants and 6. REFERENCES people of the Dampier Peninsula, Kimberley, Western Australia. CALM, Alongi, D.M. 1990. The ecology of tropi- Como. cal soft-bottom benthic ecosystems. Lane, B. 1987. Shorebirds in Australia. Ann. Rev. Oceanogr. Mar. Biol. 28: Nelson, Melbourne. 381-496. Pepping, M., T. Piersma, G. Pearson & Beukema, J.J. 1974. Seasonal changes M. Lavaleye. 1999. Intertidal sedi- in the biomass of the macrobenthos of ments and benthic animals of Roebuck a tidal flat area in the Dutch Wadden Bay, Western Australia. NIOZ-report Sea. Neth. J. Sea Res. 8: 94-107. 1999-3, Texel. Broom, M.J. 1982. Structure and season- Piersma, T. 1980. Macrobenthic fauna of ality in a Malaysian mudflat community. the interidal flats. Pp. 50-66 in W. Estuar. Coast. Shelf Sci. 15: 135-150. Altenburg, M. Engelmoer, R. Mes & T. Clayton, H.H. & F.L. Clayton. 1947. Piersma (eds.). Wintering waders on World weather records 1931-1940. the Banc d’Arguin, Mauritania. Smithson. Misc. Coll. 105: 1-646. Stichting Veth tot steun aan Dittmann, S. 2002. Benthic fauna in tropi- Waddenonderzoek, Leiden. cal tidal flats of Hitchinbrook Channel, Piersma, T. 1994. Close to the edge. NE Australia: diversity, abundance and Energetic bottlenecks and the evolu- their spatial and temporal variation. tion of migratory pathways in Knots. Wetlands Ecol. Manag. 10: 323-333. Uitgeverij Het Open Boek, Den Burg, Edgar, G. 1997. Australian marine life. Texel. Reed Books, Kew, Victoria. Ricklefs, R.E. 1990. Ecology, Third Fauchald, K. 1977. The polychaete Edition. Freeman, New York. worms. Natural History Museum of Los Rogers, D., P. Battley & T. Piersma. Angeles County, Los Angeles. 2000. Tracking 2000: radio-telemetry Janssen, P. 1995. Seashells of Central and other studies of Great Knots in New South Wales. Published by the Roebuck Bay, March-April 2000. author, Townsville. Progress Report, NIOZ, Texel. Jones, D.S. & G.J. Morgan. 1994. A field Rogers, D.I. & I. Taylor. 2002. guide to crustaceans of Australian wa- Conservation and ecology of migratory ters. Reed Books, Kew, Vic. shorebirds in Roebuck Bay, north- Lamprell, K. & T Whitehead. 1992. western Australia. Final Report for the Bivalves of Australia, Vol.1. Crawford Wetlands Unit, Environment Australia. House Press, Bathurst. Report Charles Sturt University, Albury. Lamprell, K. & J. Healy. 1998. Bivalves of Shepherd, S.A. & I.M. Thomas. 1989. Australia, Vol. 2. Backhuys Publishers, Marine invertebrates of Southern Leiden. Australia. South Australian 48 References

Government Printing Division, poral intercomparisons. Olsen & Adelaide. Olsen, Fredensborg. Tulp, I. & P. de Goeij. 1994. Evaluating Wolff, W.J., A. Gueye, A. Meijboom, T. wader habitats in Roebuck Bay (North- Piersma & M.A. Sall. 1987. western Australia) as a springboard for Distribution, biomass, recruitment and northbound migration in waders, with a productivity of Anadara senilis (L.) focus on Great Knots. Emu 94: 78-95. (Mollusca, Bivalvia) on the Banc Van de Kam, J., B.J. Ens, T. Piersma & d’Arguin, Mauritania. Neth. J. Sea Res. L. Zwarts. 1999. Ecologische Atlas van 21: 243-253. de Nederlandse Wadvogels. Schuyt & Zwarts, L. & J.H. Wanink. 1993. How the Co, Haarlem. food supply harvestable by waders in Van der Meer, T. Piersma & J.J. the Wadden Sea depends on the varia- Beukema. 2000. Population dynamics tion in energy density, body weight, of benthic species on tidal flats: the biomass, burying depth and behaviour possible roles of shorebird predation. of tidal-flat invertebrates. Neth. J. Sea Pp. 317-335 in K. Reise (ed.). Res. 31: 441-476. Ecological comparisons of sedimentary shores. Springer, Berlin Vargas, J.A. 1989. Seasonal abundance of Coricuma nicoyensis Watling and Breedy, 1988 (Crustacea: Cumacea) on a tropical mud flat. Rev. Biol. Trop. 31: 207-211. Watkins, D. 1993. A national plan for shorebird conservation in Australia. RAOU-Report 90, Melbourne. Wilson, B. 1993. Australian Marine Shells. Vol. 1. Odyssey Publishing, Kallaroo, WA. Wilson, B. 1994. Australian Marine Shells. Vol. 2. Odyssey Publishing. Kallaroo, WA. Wolff, W.J. 1991. The interaction of benthic macrofauna and birds in tidal flat estuaries: a comparison of the Banc d’Arguin, Mauritania, and some estuaries in the Netherlands. Pp. 299-306 in M. Elliott & J.-P. Ducrotoy (eds.). Estuaries and coasts: spatial and tem- 49

Plate 10. A potential new monitoring site? Dampier Flats in the Rain, March 2000. Photograph by Theunis Piersma