Biodiversity and functioning of polychaetesin benthic sediments

PAT HUTCHINGSThe Australian Museum, 6 College Street, Sydney, NSW 2000, Australia

Received 10 January 1998; accepted 26 March 1998

Polychaetes are well represented in most marine and estuarine environments, both in terms of

number of individuals and species, and they typically contribute a signi®cant percentage of the totalmacrofaunal diversity. They exhibit considerable variations in recruitment in both time and space,which is then often re¯ected in adult distributions. Whilst families and genera of polychaetes havewide distributions, normally species have discrete distributions. Polychaetes are often classi®ed

according to their diverse feeding guilds. They play a major role in the functioning of benthiccommunities, in terms of recycling and reworking of benthic sediments, bioturbating sediments andin the burial of organic matter. Some species form dense tubiculous colonies which can radically

change recruitment patterns of other infaunal organisms. Polychaetes, by their burrowing andfeeding activity, may considerably enhance various sedimentary processes. However, much remainsto be learnt as to how benthic communities function, and how they may change in function as they

are increasingly being impacted especially in coastal waters adjacent to centres of population.

Keywords: polychaetes; biodiversity; marine sediments; role of polychaetes; recruitment

Introduction

Polychaetes occur in almost all benthic marine and estuarine sediments (Fauchald, 1977)and are often the dominant component of the macrobenthos both in terms of number ofspecies and individuals (Grassle and Maciolek, 1992; Ward and Hutchings, 1996). Over10,000 species have been described to date (Minelli, 1993), belonging to 83 families, andvarious estimates have been made as to the total polychaete fauna ranging from 25,000 to30,000 (Snelgrove et al., 1997). The ratio of described to undescribed species varies ac-cording to habitat and biogeographical region, with intertidal and shallow subtidalcommunities best known in Northern Europe (Fauvel, 1923, 1927; Hartmann-SchroÈ der,1971), and North America (Hartman, 1968, 1969; Pettibone, 1963; Blake et al., 1996, andearlier volumes). Many other regions of the world rely on monographs produced forEurope (Fauvel, 1923, 1927), North America (Hartman, 1968, 1969) and South Africa(Day, 1967) to identify their fauna. This has led to many species being categorised as``cosmopolitan'' or at least being assumed to have very wide distributions. However, asregional family revisions are undertaken many of these species are being found to havebeen misidenti®ed. For example, Day and Hutchings (1979) recorded 32 species of thefamily Terebellidae as occurring in Australian waters, virtually all having been describedfrom European waters. After a revision of the family by Hutchings and Glasby (1991, andrefs therein) only one of these species is now known to occur in Australian waters and thecurrent terebellid fauna is over 90 species (Hutchings, 1997, and refs therein). A similarpattern is expected to be found in South America, New Zealand and much of the South

0960-3115 Ó 1998 Chapman & Hall

Biodiversity and Conservation 7, 1133±1145 (1998)

Paci®c at least. The majority of polychaete families occur world-wide and many generahave wide distributions, and increasingly it is at the species level that discrete distributionalpatterns are being found. This widespread distribution of families and genera may bea re¯ection of the age of the group (Fauchald, 1974; Conway-Morris, 1979; Butter®eld,1990), suggesting that rapid radiation of the group took place in Pre-Cambrian toCambrian times as many current families are recognisable from these deposits (Fauchald,1984).

Accepting that a percentage of the polychaete fauna remains to be identi®ed or to becorrectly identi®ed, there is no debate that they are a highly diverse group. In Table 1a selected number of recent macrobenthic benthic studies are shown which illustrate thebiodiversity of polychaetes in a wide variety of habitats and geographical regions (seeKnox, 1977, for additional earlier studies). Comparing such data sets is di�cult for manyreasons. Sampling techniques, mesh size used, and the size and number of replicatescollected and over what time period, will greatly in¯uence the number of species andindividuals found. Mackie and Oliver (1996) discuss these problems in some detail and thesampling strategy employed will obviously be determined by the questions being asked ofthe data as well as by funding and logistical restrictions. Also, factors such as sedimenttype (Etter and Grassle, 1992), salinity regimes (Stephenson et al., 1979), historicaldisturbances (Gray, 1997), organic content, microbial associations and food availability(see review by Snelgrove and Butman, 1994) will greatly in¯uence the total number ofspecies and individuals present as well as the species composition. In most cases selectionof habitat will occur at the time of larval settlement (Butman and Grassle, 1992; Grassleet al., 1992; Wu and Shin, 1997).

Most polychaetes occur in the upper 5±10 cm of the sediment. In addition typically alarge percentage of species are represented by few individuals and with a few speciesdominating. Hutchings et al. (1993), working in Upper Spencer Gulf, South Australia,recorded 372 species of macrofauna, represented by 12,396 individuals. Of these 372species, 26 were represented by 100 individuals or more, and represented 64% of the totalfauna collected. Of these dominant species, 18 were polychaetes and they represented 77%of the dominant fauna. Species composition often changes over time at the same site(Buchanan and Warwick, 1974; Poore and Rainer, 1979; Hutchings and Jacoby, 1994),especially of species with short life cycles which die after breeding, and recruitment of thatspecies may not re-occur at that site for several years.

Some data has suggested that there are distinct latitudinal gradients, with diversityincreasing towards the tropics (Rex et al., 1995). However the data presented by Rex et al.exhibits much scatter, and if the data from the Norwegian Sea which has low diversity dueto recent glaciation events is removed, then the trends are less clear (Gray, 1997). In theSouthern Hemisphere, such a gradient has also been questioned, in part because of thehigh diversity recorded in the Antarctic for many groups including polychaetes. Hartman(1966) recorded 457 species of polychaetes from the Antarctic, although she indicated thatthe best known areas were from between the sub-Antarctic to the Antarctic Convergence,with other regions far less well known, suggesting that the ®nal polychaete diversity for theentire Antarctic will be much higher. Some of the highest values for soft sediments havebeen recorded from southern Australia (Poore and Wilson, 1993). Colman et al. (1997)found 800 species of macrofauna (of which 24.4% were polychaetes) in just 10 m2 ofsediment in Bass Strait, and 700 species (of which 33% were polychaetes) have beenrecorded from the sediments of nearby Port Phillip Bay (Poore et al., 1975).

1134 Hutchings

Table 1. Selected benthic studies, to illustrate the dominance of polychaetes in macrofaunal assemblages in a variety of habitats

Habitat

Total nos.of individualsof macrofauna

collected

Total nos.of macrofaunalspecies

recorded

Total nos.of individualsof polychaetes

collected

Total nos.of polychaete

species Comments

Upper Spencer Gulf, S.Australia, shallow protected,hypersaline, muddy sediments

and seagrass beds depth 1±10 m(Hutchings et al., 1993)

12,396 372 4834 148 Polychaetes represented 39%of all individuals collectedand had a density of 626 per

m2, 2 sets of samples, 1 mmmesh used.

Jervis Bay, NSW, Australia,

protected, fully marinevegetated and unvegetatedsediments depth 6±20 m

(Hutchings & Jacoby, 1994)

630 171 Polychaetes represented 27%

of the total macrofaunalspecies collected. Samplingat 3 monthly intervals over

3 years, 0.5 mm sieve.Bass Strait, SouthernAustralia depths of 11±51 m

(Coleman et al., 1997)

800 196 Sampled 10 m2, polychaetesrepresented 24.4% of the

total nos of species ofmacrofauna, 0.5 mm sieve.

Port Phillip Bay ± largelyenclosed marine bay, average

depth 13.7 m (Poore et al.,1975)

731 233 Polychaetes represented 32%of macrofaunal species

collected, replicate samplescollected over a largenumber of stations through-

out the bay over 3 years,0.5 mm sieve.

Hong Kong Harbour, Tolo

Channel, heavily impacted,sampled in 1986 (Shin 1990)

3,540 79 37 One-o� sampling at 58 sites,

0.5 mm sieve.

b. Study repeated 1989,

(Mackie and Oliver, 1993)

11,608 147 8351 96 Polychaetes represented 63%

of species and 73% ofindividuals collected.).Replicate samples collectedat 10 stations, 0.5 mm sieve.

Biodiversity

andfunctio

ningofpolychaetes

1135

Table 1. (Continued)

Habitat

Total nos.

of individualsof macrofaunacollected

Total nos.

of macrofaunalspeciesrecorded

Total nos.

of individualsof polychaetescollected

Total nos.of polychaetespecies Comments

North Atlantic Ocean in

1502±2509 m (Grassle andMaciolek, 1992)

90,677 798 367 Polychaetes represented

46% of species collected.3 replicate samples, takenat 14 stations, 3x a year

for 2 yrs, 0.5 mm sieve.Continental Shelf o�North Carolina 0±200 m(Day et al., 1971)

15,000 619 6384 229 Polychaetes represented 40% oftotal fauna. Replicate samplescollected 5 times, 1 mm sieve.

Ria de Muros, N.Spain (Lopez-Jamar,1981)

109 62 Polychaetes represented 57%of the species collected. 5replicates at 5 stations,

0.5 mm sieve.Delaware Bay,northeastern coast of

USA (Maureret al. 1978)

Averagedensity

of indscollected722 m2

169 69 Polychaetes represented 40.8%of species collected. 207

samples collected over2 years, 1 mm sieve.

Block Island, NewEngland, averagedepth 33±97 m.(Steimle, 1982)

224 104 Polychaetes represented46% of species collected.9 stations, replicate samplesin 2 seasons, 1 mm sieve.

1136

Hutch

ings

Other workers have suggested that benthic macroinvertebrate diversity increases fromshallow areas to the deep sea (Sanders, 1968; Grassle and Maciolek, 1992), based largelyon data from the Northern Hemisphere. (Polychaetes represent a very large proportion ofthis biodiversity (see Table 1). Data from the Norwegian continental shelf (Gray, 1994)and southern Australia (Poore and Wilson, 1993) somewhat contradicts this hypothesis.Indeed, the Australian data reveals that some coastal regions exhibit patterns of benthicmacroinvertebrate biodiversity as high as those which have been recorded from the deepsea. Gray (1997) suggests that more quantitative comparable data is needed from tropicalareas and the Southern Hemisphere to prove or disprove the generality of this hypothesis,and some of this is presented in Gray et al. (1997). In addition, there is the problem of thevalidity of extrapolating from a few small, deep sea samples to larger areas especially whenmany species are represented by a single or few individuals. So at this stage, perhaps allone can say is that the presence or absence of gradients of diversity may only be ofimportance regionally.

Many factors in¯uence the distribution and abundance of polychaetes, including sed-iment structure and organic content, depth, salinity, and temperature. In consequence,probably only the most basic predictions can be made, such as ``polychaete densities arelower in exposed sandy beaches and in coarser subtidal sediments than in ®ner sediments''(Knox, 1977). More recently, Etter and Grassle (1992) have shown that in the deep seathat species diversity is signi®cantly correlated with sediment particle diversity. As well assediment being important, most polychaete species are restricted to fully saline waters. Butcertainly it does appear that some regions are more diverse than others, and this maybe related to the geological history of the area, ocean currents, and organic content ofsediments. Poore (1995) evokes these reasons for the very high benthic infaunal biodi-versity found in southern Australia.

So although there are many regions of the world where our knowledge of the diversityof polychaetes is poor, there is no doubt from the currently available data that polychaetesare ubiquitous in virtually all marine sediments and are typically present in high numbersand represented by many species. Thus, benthic polychaetes exhibit high biodiversity,which is continuing to be documented, often as part of an environmental monitoringprogram. In many ways it is probably easier to continue to document polychaete biodi-versity or changes in it, than it is to try and understand the role of this biodiverse group oforganisms in the ecological functioning of benthic sediments. However, I have attemptedto draw together the limited data which does exist, on the roles which polychaetes play inbenthic sediments in the following sections.

Role in the food chain

Polychaetes exhibit a wide variety of feeding methods ranging from surface deposit, sus-pension, mud swallowing, carnivory and herbivory to in a few species even parasitism(Fauchald and Jumars, 1979). Species are typically assigned to a feeding group based uponthe morphology of the mouth parts, rather than on laboratory observations. Although allnereidids and onuphids have well developed sets of jaws, some species in these families aregrazers and others feed on drift algae, and probably many other species regarded ascarnivores are in reality opportunistic feeders. But even allowing for some ¯exibility,polychaetes in any benthic community exhibit a wide range of feeding types, although inmost soft bottom communities, suspension and deposit feeders dominate (Snelgrove et al.,

Biodiversity and functioning of polychaetes 1137

1997). However, polychaetes have representatives at all levels in the food chain; some arepredators on other polychaetes and macroinvertebrates as well as components of themeiofauna, others graze on algae, and many recycle and break down organic matter withinthe sediments. Polychaetes in turn are eaten by a variety of organisms within the sedimentas well as by epifaunal and pelagic species such as ®sh, molluscs and crustaceans.

Within a polychaete assemblage many species of suspension, surface deposit feeders ormud swallowers may co-occur, and it has been shown (Fauchald and Jumars, 1979) thatspecies can sort particles once they are collected according to size, and then ingest them,use them for tube construction, or reject them (Dales, 1955). Increasingly it is beingdemonstrated in a wide range of polychaete species that species can be very selective in theparticles which they collect and that they can respond to variability in food concentrationand its composition (Cammen, 1989; Bock and Miller, 1997, and references therein) andperhaps increase their acquisition of nutritionally important organic compounds.

Productivity of polychaetes

Polychaetes exhibit a wide range of reproductive strategies (for reviews see Olive, 1984;Bentley and Pacey, 1992, and references therein) ranging from broadcast spawners tobrooders. Both sexual and asexual reproduction occurs within the group. Some speciesbreed annually for several years, whereas others breed once and then die, and yet othersbreed almost continuously over many months. Even within a family or a genus severalmethods of reproduction may occur. Thus we have species which produce large numbersof gametes of which relatively few are fertilised to produce pelagic larvae and survive tosettlement, to species which produce few gametes which are brooded within protectivechambers and where virtually all gametes survive to produce viable adults (Rouse andFitzhugh, 1994).

Few studies have attempted to measure the productivity of benthic communities overlong periods. Two studies conducted over a 12 month period, in which polychaetesdominated the communities were carried out by Warwick and Price (1975) in the Lynherestuary in south-west England and by Buchanan and Warwick (1974) in deeper water o�the Northumberland coast of north-east England. Although the total production wasmuch greater in the estuary than in the o�shore study, the percentage contribution to thisproductivity by the polychaetes was similar in both cases, being 72.55% and 73.13%respectively of the total productivity. Buchanan and Warwick (1974) found that ninespecies accounted for 86.2% of the total production estimates, of which six were poly-chaetes, including the ®rst four top-ranked species. However, they suggested that theirtotal estimates of total production were likely to be underestimates as it was probablya year or so before the smaller polychaetes reached a su�cient size to be retained ona 0.5 mm screen. Most of their common species fell into this category and had completeda year's growth before being retained on the sampling screens. Thus the estimates ofproduction could be underestimates as the level of ®rst year mortality for these species isnot known.

Another study, but carried out over a shorter time period, was conducted by Rainer(1982) in a temperate Australian estuary, and he found that again polychaetes dominatedproduction providing over 45% of the total. More often the productivity of a single specieshas been studied (Estcourt, 1974). However, all these community production ®gures areestimates as our knowledge of life cycles and the rates of larval settlement and subsequent

1138 Hutchings

survival to maturity and reproductive status is poor for most polychaetes. Levin (1984,1986) recorded signi®cant variations in larval density of spionids over a mud ¯at on asingle tidal cycle as well as variations on an annual and seasonal basis. To compound thesedi�erences the species she studied also had multiple patterns of reproduction depending ontheir location on the Paci®c, Gulf of Mexico or Atlantic estuaries (Levin, 1984). Woodin(1974) showed that mortality after spawning and variable larval settlement success ex-plained much of the variation in adult densities of common intertidal polychaetes.

More often benthic studies measure the biomass of the various invertebrate groupspresent, as well as the number of species and individuals, and assign them to variousfeeding groups in an attempt to characterise the community (Hutchings et al., 1991, 1993)± primarily because of the di�culty in measuring or estimating productivity and secondlybecause relatively few long term studies are carried out.

The majority of polychaetes are small and typically exhibit a low biomass and yet weknow that large numbers are often present, so that collectively they may form a substantialpart of the ash free dry weight (AFDW) of a sample (Brown, 1991). Recruitment studies(Grassle and Morse-Porteous, 1987; Wu and Shin, 1997, Butman, 1987) show that poly-chaetes rapidly recruit to new sediment or disturbed areas. Often polychaetes are amongstthe ®rst group of macroinvertebrates to settle in recruitment studies regardless of habitat(Shull, 1997, intertidal; Wu and Shin, 1997, shallow coastal waters; Hewitt et al., 1997,estuarine areas; Grassle and Morse-Porteous, 1987, deep sea). Grassle and Grassle (1974)found that some polychaete species were highly opportunistic and responded rapidly toenvironmental perturbations. They also discuss the reproductive strategies employed bysuch species to enable them to build up large populations over very short time periods. Sobiomass per se may not be a very useful indicator of rates of turnover as many species haveshort life spans. Studies by Hutchings and Jacoby (1994) who sampled benthic commu-nities at three monthly intervals over three years, showed that polychaetes recruitthroughout the year, and also that species composition changes throughout the year, withmany species present during only one or two sampling periods, suggesting high rates ofturnover at least for many species. It should also be remembered that as polychaetes aretypically soft bodied, other organisms preying on them can digest all, without having todiscard shells or heavy exoskeletons.

Bioturbation and sediment reworking

Many polychaetes burrow into the sediment both for protection against predation andalso in search of food, and others actively swallow mud and deposited particulate matter(Taghon and Greene, 1992) in order to obtain their nutrition. Such bioturbation may havemajor impacts on the redistribution on organic matter and stimulate sediment metabolism(Lopez and Levinton, 1987), improve the ventilation of the sediments (Aller, 1982; Kris-tensen, 1988), and increase animal respiration (Kristensen et al., 1992).

Recent studies by Levin et al. (1997), working on the North Carolina continental slope,found that maldanid tube building worms can without ingestion, rapidly subduct freshlydeposited algal carbon and inorganic materials to depths of 10 cm or more within thesediment column over 1.5 days. They further suggest that such pulses of organic matteroccur frequently (Smith et al., 1994; Gehlin et al., 1996) and such burrowing species playan important role in rapidly distributing labile organic matter within the seabed.

Biodiversity and functioning of polychaetes 1139

Production of 3-dimensional structures

Many polychaetes are tubiculous and some of these species are highly gregarious, such asspionids (Levin, 1982; Dauer and Ewing, 1991), fabriciinid sabellids (Levin, 1982; Rouse,1993), onuphids (Woodin, 1981), chaetopterids and eunicids (Jacoby et al., 1995). Woodin(1981) has shown that infaunal abundances are highest around the tubes of the onuphidDiopatra, and suggested that the tubes provide protection to the infauna from predationby several species of crabs. However, in some cases it appears that this impact may benegative. A recent invasion of Sabella spallanzanii, a large ®lter feeding sabellid, into partsof Port Phillip Bay, Victoria, Australia which has formed dense colonies, has changed thelocal water ¯ow patterns and the amount of suspended matter which settles on the sedi-ment interface; it seems likely that this polychaete has modi®ed the benthic communitywhich originally existed in the area (Wilson et al., 1996).

Interactions within the macrobenthos

While we can assign some roles to this diverse polychaete community, we still know little ifanything about the interactions of these polychaetes between each other or with othermembers of the macrofauna. Such interactions may vary between adult and larval stagesand between species. One suspects that many larvae are predated upon as they try to settle,perhaps even by other polychaetes, although in some cases larvae are attracted to settle bythe presence of adults of the same species in which dense colonies of a single species maybe formed. By necessity most of these studies have been carried out on intertidal species,but presumably must also occur in many benthic communities where dense concentrationsof adults occur (Pawlik, 1990; Woodin, 1974, and references therein).

Interactions between macrofauna and microfauna

Polychaetes of the genus Capitella are often present in high numbers in organic richsediments which may be polluted with oil products. Holmer et al. (1997) compared mi-crobial and sediment characteristics in cores of harbour sediments and ¯ouranthenecontaminated sediments with and without Capitella, a relatively small species (5±10 mm inlength). After 6 days, cores without Capitella were less oxidised than those with the worms.They found that the polychaete had a stimulatory e�ect on the total microcosm metab-olism and the enhancement of O2 and CO2 ¯ux, and this was not measurably in¯uenced bythe ¯uoranthene contamination. Anaerobic microbial metabolism was reduced by 20±36%in the presence of the worms. They suggest that these studies show the potential impor-tance of macrofaunal-microbe interactions on key decomposition processes and the fate ofpollutants in sediments. This may be the result of enhanced irrigation of porewaters, thusoxidising the deeper sediments and introducing favoured electronic receptors to theselayers. Hansen and Blackburn (1992) found that populations of the polychaete Nephtys inmicrocosms enhanced the sulphur reduction rate, and they suggest that this was caused bythe worms transporting reactive organic matter to the deeper layers. This is obviously anarea where much work remains to be done to fully understand these interactions.

1140 Hutchings

Summary

Repetitive sampling of benthic communities has shown the variation in species compo-sition over time (Stephenson, 1980) in what are regarded as ``healthy'' relatively unpol-luted environments, i.e. the natural situation. Does this mean that components of suites ofspecies can perform the various tasks necessary to be undertaken within that benthicsystem in order for it to function? One must assume so, as it appears impossible to predictwhich species will recruit this year versus the next year. All we can say perhaps is that thespecies will belong to a group of species which have previously been recorded from thathabitat. Does this imply functional redundancy within benthic sediments (di Castri andYouneÁ s, 1990; Walker, 1991)? It is too early to say; we need more information about howthe structure and functioning of communities change over time. Obviously changes inspecies composition and abundance are important, and I suggest that we need additionalinformation, but what sort? Probably just classifying the polychaetes by feeding guilds isnot adequate, should we be looking at reproductive patterns as well as feeding rates, andlife spans as well as their interactions with other components on the benthic fauna? Weneed to urgently understand the functioning of benthic sediments which cover the majorityof the ocean ¯oor, and which are increasingly being impacted, especially those in coastalwaters adjacent to centres of population. It is these benthic communities which are criticalto the survival of the marine ecosystem, and if we are to manage them, we must under-stand how they function.

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