bioengineering effects of burrowing thalassinidean

Oceanography and Marine Biology: An Annual Review, 2011, 49, 137–192 © R. N. Gibson, R. J. A. Atkinson, J. D. M. Gordon, I. P. Smith and D. J. Hughes, Editors Taylor & Francis

BIOENGINEERING EFFECTS OF BURROWING THALASSINIDEAN SHRIMPS ON MARINE SOFT-BOTTOM ECOSYSTEMS DEENA PILLAY & GEORGE M. BRANCH Marine Research Institute, Zoology Department, University of Cape Town, Private Bag X3, Rondebosch 7701, Cape Town, South Africa E-mail: [email protected], [email protected] Abstract Crustaceans classed as Thalassinidea are shrimp-like marine organisms that burrow predominantly in sediments. They have generated particular interest over the last decade because of their roles as ecosystem engineers that exert major influences over ecosystem processes and community structure. Their sphere of influence is wide as their burrowing activities substantially affect sedimentary and biochemical properties and processes, translating into both positive and negative impacts on co-occurring organisms spanning bacteria, microalgae, meiofauna, macrofauna and seagrasses, and possibly up the food chain to fish and birds. The specific microclimates they create within their burrows are particularly important for microbes and meiofauna, which in turn play important roles in organic and inorganic nutrient cycling. The physical turnover of sediments from burrows to the sediment surface significantly influences macro-invertebrate community structure, generally by negatively affecting surface fauna or organisms such as filter-feeders and epibenthic grazers that are dependent on the interface of sediment and water for feeding. Their burrowing activities increase sediment penetrability and porosity, which can favour burrowing macrofaunal species. Sediment turnover can also reduce recruitment of macro-invertebrates, either indirectly by diminishing microbial biofilms that act as food, sediment stabilizers and biochemical cues for larval settlers or directly by burying recruits. Thalassinidean bioturbation also influences marine vegetation, in some instances excluding seagrasses; together with the ecosystem services these plants provide for co-occurring species. Thalassinideans also affect commercial aquaculture operations for oysters and penaeid shrimps. Sediment turnover by thalassinideans buries adult and juvenile oysters, and their propensity to increase fluxes of toxic nutrients and sulphides, allied with their high oxygen consumption, reduces yields of cultured shrimps, leading to financial losses. Harvesting of thalassinideans for bait has important consequences for soft-sediment ecosystems as the physical disturbance induced by bait-collectors, associated with the removal of the ecosystem services provided by thalassinideans, leads to changes in oxygenation, sediment granulometry and the structure of invertebrate communities. Lastly, ecosystem engineering by thalassinideans acts as a selective agent leading to the evolution of novel morphology, behaviour and social interactions in co-occurring organisms. Most of the effects of thalassinidean shrimps are manifested via their influence on environmental conditions, including the stability, granulometry, turnover and geochemical properties of sediments, all reflecting their powerful ecosystem engineering.

Introduction The central focus of this review is the ‘ecosystem engineering’ role of thalassinidean shrimps via their bioturbation of sediment. To provide context, we first outline the relevant aspects of their 137

DEENA PILLAY & GEORGE M. BRANCH Community Structure Bacteria Microalgae Meiofauna Macrofauna Seagrasses

Sediment Properties

Evolution

Morphology Behaviour Social Interactions

Penetrability Granulometry Organic content Water content Oxygen levels

Figure 1 The threefold influences of ecosystem engineering by burrowing thalassinideans on sediment properties, soft-sediment community structure and the evolution of co-occurring species.

biology before turning to the triad of effects that their activities have on (1) sediment properties, (2) community composition and structure, and (3) the evolution of co-occurring species, as summarized in Figure 1.

Taxonomy and distribution Crustacea falling in the Thalassinidea in the order Decapoda comprise mainly endobenthic or fossorial species that create burrows in marine sediments (Griffis & Suchanek 1991, Coelho et al. 2000a). Thalassinidea are globally distributed (Figure 2) in intertidal and subtidal soft-bottom habitats of tropical and cool temperate marine systems (Coelho 2004 and references cited therein, Dworschak 2004), and frequently attain high densities, approaching 400 m−2 (Nates & Felder 1998). Because thalassinideans occur predominantly in muddy or sandy sediments, they are commonly referred to as mud- or sandshrimps. Other common names include ‘yabby’, ghost shrimps (Australia) or mud- or sandprawns (South Africa). A few species deviate from burrowing in sediments by boring into corals and sponges (Scott et al. 1988), living in fissures between corals (Kensley 1994) or constructing burrows on boulder beaches (MacGinitie 1939) or maerl beds (Hall-Spencer & Atkinson 1999). 138

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Red Sea & Arabian Gulf

Southern Africa

Mediterranean

North Sea

Taiwan

New Zealand

Australia

Japan

Figure 2 The distribution of the major thalassinidean genera on which ecological research has been undertaken. Generic revision is active within the Thalassinidea (Atkinson & Taylor 2005), and we retain here the names best established in each region while recognizing that further revisions have already taken place and that more changes in the allocation of species among genera are likely.

South America

Caribbean

North America

BIOENGINEERING EFFECTS OF BURROWING THALASSINIDEAN SHRIMPS

DEENA PILLAY & GEORGE M. BRANCH

Table 1 Classification of families within the infraorders Gebiidea and Axiidea (sensu Bracken et al. 2009, Robles et al. 2009), previously comprising the infraorder Thalassinidea (sensu Poore 1994, Felder 2001), with a listing of genera commonly mentioned in the ecological literature ‘Thalassinidea’ Infraorder Gebiidea

Infraorder Axiidea

Family Laomediidae Jaxea, Laomedia

Family Axiidae Calaxius, Calocarides, Calocaris, Calastacus, Eiconaxius

Family Thalassinidae Thalassina

Family Callianassidae Biffarius, Callianassa, Callichirus, Calliax, Corallianassa, Corallichirus, Eucalliax, Glypturus, Lepidophthalmus, Neocallichirus, Neotrypaea, Nihonotrypaea, Pestarella, Sergio

Family Upogebiidae Acutigebia, Aethogebia, Austinogebia Potamogebia, Upogebia Family Axianassidae Axianassa

Family Callianideidae Callianidea, Crosniera, Thomassina Family Ctenochelidae Ctenochelas Family Micheleidae Meticonaxius, Michelea Family Strahlaxiidae Neaxius, Strahlaxius

The infraorder Thalassinidea (sensu Poore 1994 and Felder 2001) contains roughly 556 species, spanning 11 families and approximately 96 genera (Dworschak 2005). Bracken et al. (2009) and Robles et al. (2009) have, however, demonstrated that members of the Thalassinidea are paraphyletic and fall into two subclades; consequently they have proposed that two separate infraorders, the Gebiidea and Axiidea, should be erected in the place of this taxon. The proposed classification of current families within these two infraorders is summarized in Table 1. In our review, we continue to refer to the Thalassinidea, partly because the taxon is so established in the literature we cover, but also because members of the two proposed infraorders are functionally equivalent in terms of the ecosystem engineering; we use the term ‘thalassinideans’ as a convenient collective term, while recognizing that the group is paraphyletic. Thalassinidean taxonomy is uncertain, and we follow in this review Manning & Felder (1991), Manning & Tamaki (1998), Tudge et al. (2000) and Ngoc-Ho (2003). The distribution and diversity of thalassinideans have been reviewed by Dworschak (2000, 2005). Species richness increases from higher latitudes to the equator in both hemispheres. Ninety-five per cent of thalassinidean species occur in shallow-water systems spanning 0–200 m, with only three species recorded from depths below 2000 m. The Callianassidae, Upogebiidae, Thalassinidae and Strahlaxiidae are generally recorded at depths between 0 and 20 m, while members of the Axiidae and Calocarididae are predominantly deep-water species occurring at 200–2000 m (Dworschak 2000).

Life cycle Thalassinideans typically have five or six planktonic zoeal larval stages, ending in metamorphosis into a stage that settles and is called either a megalopa or a decapodid larva. Some species show abbreviated larval development with as few as two zoeal stages, including species within the genus 140


Lepidophthalmus (Nates et al. 1997, Felder 2001) and the mudshrimp Austinogebia (as Upogebia) edulis, which completes its development in a few days (Shy & Chan 1996). In Callichirus* (as Callianassa) kraussi there is no planktonic stage, and the juveniles burrow directly off the burrows of adults (Forbes 1973). In other species, although development is more prolonged, the total larval duration is still relatively short, with metamorphosis into the juvenile stage taking place after about 10 days (Abrunhosa et al. 2005). There is some evidence that waterborne cues emanating from adults (in conjunction with the presence of sand) enhance settlement of juveniles by increasing burrowing behaviour, shortening the duration of zoeal stage IV and bypassing stage V to moult directly into the decapodid stage (Strasser & Felder 1999), but the results are ambiguous because of differences among regions. Facilitation of juvenile survival due to bioturbation by adults has been inferred from field observations (Tamaki & Ingole 1993). The relationship between adults and juveniles remains a topic that needs further research as the implications for population dynamics are considerable.

Feeding Knowledge of feeding mechanisms in thalassinideans is based predominantly on the Callianassidae and Upogebiidae, the most comprehensively studied families (MacGinitie 1930, 1934, Pohl 1946, Devine 1966, Scott et al. 1988, Nickell & Atkinson 1995, Coelho et al. 2000a,b, Coelho & Rodrigues 2001a). A few studies have investigated the feeding of the Axiidae, Calocarididae and Laomediidae (Buchanan 1963, Kensley 1980, Nickell & Atkinson 1995, Coelho & Rodrigues 2001b), but the feeding behaviour of the remaining families is largely unknown (Coelho 2004) and represents a major gap in knowledge. Feeding in thalassinidean crustaceans is intimately linked with their burrows, and filter and deposit feeding are the two principle modes of feeding. Those that are filter-feeders draw water through burrows and strain out suspended organic food, while deposit-feeding species consume organic material in the sediment or present along the burrow walls (Coelho 2004). Several types of food are consumed, including bacteria, diatoms, dinoflagellates, microalgal and seagrass fragments, mangrove and saltmarsh debris, meiofauna and, in rare cases, macrofauna (Abed-Navandi & Dworschak 2005, Atkinson & Taylor 2005 and references cited therein, Shimoda et al. 2007). Some species exhibit specialized feeding modes, while others use a combination, depending on resource availability (Nickell & Atkinson 1995). Some deposit-feeding thalassinideans have been described as ‘gardeners’ because they attach plant and other organic material to their burrow walls, enhancing microbial growth and thus their own food availability (Griffis & Chavez 1988). Some collect and store plant debris in specialized chambers, periodically chopping it up and transferring it from one chamber to another (Dworschak 2004). Abed-Navandi et al. (2005) showed that Corallianassa longiventris and Pestarella tyrrhena consume this processed debris directly, and that amino acids commonly deficient in the diet of deposit-feeders are enriched in these burrow chambers. The Callianassidae have generally been classed as deposit-feeders (MacGinitie 1934, Coelho et al. 2000a), with some species considered gardeners (Branch & Pringle 1987); a few show filterfeeding ability (Nickell & Atkinson 1995, Coelho et al. 2000a). The Upogebiidae, on the other hand, have been mostly classed as filter-feeders, but again, variation in feeding mode exists within the group, with some species adept at deposit feeding (Nickell & Atkinson 1995, Coelho et al. 2000a,b). Species within the Laomediidae have been described as deposit-feeders, while members of the Calocarididae use a combination of filter- and deposit-feeding, and some may be carnivorous (Buchanan 1963, Nickell & Atkinson 1995, Coelho & Rodrigues 2001a). One laomediid, Jaxea nocturna, is a resuspension-feeder, flicking up material with its mouthparts and filtering out *

Recent generic revision by Poore (2010): Callianassa kraussi Stebbing, 1900. Available through World Register of Marine Species at http://www.marinespecies.org/aphia.php?p=taxdetails&id=246238 (accessed 24 September 2010).

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the organic components (Pinn et al. 1998). Carnivory has been reported for Axiopsis serratifrons (Axiidae) by Kensley (1980) and for Calocaris macandreae (Calocarididae) by Pinn & Atkinson (2010). Whatever the feeding mode, many thalassinidean species possess unique gut microflora that aids digestion of ingested material, although there are rare instances of species that harbour no gut microflora (Harris et al. 1991, Pinn et al. 1999).

Burrow morphology The burrows produced by thalassinideans are incredibly diverse in morphology and temporal variability (Butler & Bird 2008), and the literature on this subject is extensive. Reviews appear in Coelho (2004) and Atkinson & Taylor (2004, 2005), so we do not attempt to cover the literature dealt with in these reviews but rather summarize the patterns and add literature that has appeared since their reviews. Burrows vary from uncomplicated U- or Y-shaped to extremely complex branching structures with networks of chambers below the sediment surface (Dworschak 1983). The burrows of the Upogebiidae are generally simple (Atkinson & Taylor 2005, Kinoshita & Itani 2005), usually U-shaped with constricted openings. Expansions along the tubes may also be present to facilitate turning or feeding by the shrimp (Li et al. 2008). This burrow design facilitates unidirectional flow, which the shrimps use for filter-feeding (Atkinson & Taylor 2005). Some U-shaped tubes have a vertical extension at the bottom, giving a Y-shaped appearance (Li et al. 2008). The vertical shaft stores material such as shell or stones but may also serve as a refuge from predation or disturbance (Atkinson & Taylor 2005). Deposit-feeding thalassinideans or species that ‘harvest’ seagrasses possess complex branching burrows (Dworschak 2001, 2002, 2008, Dworschak et al. 2006). Most studies examining burrow structure in deposit-feeding thalassinideans have focused on the Callianassidae, with limited information on the Axiidae, Calocarididae, Laomediidae, Axianassidae and Thalassinidae. Little is known of the remaining families (Atkinson & Taylor 2005). Burrow dimensions vary both between and within species, ranging in depth from about 20–30 cm in most of the filter-feeding upogebiids (Coelho et al. 2000a) to 208 cm for Upogebia major (Kinoshita 2002). Burrow depth is generally greater in deposit-feeding callianassids, as deep as 2.5 m (Ziebis et al. 1996a), and up to 3 m in the Axiidae (Pemberton et al. 1976). Berkenbusch & Rowden (2000) showed that the dimensions of the burrows of Biffarius (as Callianassa) filholi are correlated with temperature and inversely related to the organic content of sediments, and Butler & Bird (2008) recorded that burrows of Trypaea australiensis and Biffarius arenosus extend deeper and occupy a greater volume in warmer months. Both studies imply greater burrowing activity at times when food demands rise or food supplies diminish. The link between burrow morphology and feeding behaviour of thalassinideans has generated significant interest (Griffis & Suchanek 1991, Nickell & Atkinson 1995). Griffis & Suchanek (1991) presented evidence for their model that U- or Y-shaped tubes are mainly indicative of filter or suspension feeding in thalassinideans. Nickell & Atkinson (1995), however, argued that different sections of burrows need to be considered separately to infer feeding behaviour. In some U-shaped tubes, for example, a circular burrow cross section indicates filter-feeding, but other structures such as mounds on the surface or subsurface chambers are indicative of deposit-feeding. In this way, combinations of feeding modes may be identified. It should be noted, however, that a major hindrance to such models is the paucity of knowledge about the feeding biology of many thalassinidean species, and studies of burrow morphology substantially outnumber studies of feeding (Coelho 2004). In addition, questions still remain about the role of non-feeding burrow structures used for reproduction or refuge and whether such structures have different functions in different thalassinideans, representing a major gap in knowledge (Coelho et al. 2000a). 142


Adaptations to burrow environments Due to their largely fossorial lifestyles, thalassinideans exhibit a range of adaptations, allowing them to cope with the unique and sometimes extreme conditions prevalent in marine soft-sediment ecosystems, as reviewed by Atkinson & Taylor (2004, 2005). For example, marine sediments, particularly at the depths to which thalassinideans burrow, are characteristically anoxic or hypoxic (Thompson & Pritchard 1969, Witbaard & Duineveld 1989) and may have elevated levels of sulphide (Johns et al. 1997). Thalassinidean burrow waters may also be hypercapnic, that is, enriched in carbon dioxide (Aller et al. 1983, Waslenchuk et al. 1983, Astall et al. 1997b). Several behavioural and physiological adaptations to low oxygen levels exist in thalassinideans. Beating of pleopods, also referred to as irrigation, generally becomes more frequent during periods of hypoxia (Farley & Case 1968, Torres et al. 1977, Felder 1979, Anderson et al. 1991) and is an important behaviour used to overcome low oxygen levels within burrow waters. Most species within the Callianassidae, Calocarididae and Upogebiidae increase pleopod beating only when oxygen partial pressures reach critically low levels (Felder 1979, Anderson et al. 1991, Astall et al. 1997b), but irrigation then declines under extreme hypoxia or anoxia, presumably because the energetic costs of irrigation outweigh the benefits of drawing oxic water into burrows. During anoxic conditions, however, thalassinideans may continue to beat their pleopods, albeit at very low levels, putatively to detect changes in oxygen levels in the water. When the partial pressure of oxygen increases after severely hypoxic or anoxic conditions, irrigation rates usually increase again (Felder 1979, Anderson et al. 1991). Paterson & Thorne (1993) tested the hypothesis that the rate of burrow ventilation is a reflex response to reduction in oxygen level and showed that whereas Biffarius arenosus (as Callianassa arenosa) conforms to this model, Trypaea (as Callianassa) australiensis does not as it increases swimmeret beating under conditions of anoxia. Paterson & Thorne pointed out that ventilation rates should not be expected to be linked solely to oxygenation as ventilation also purges sediments and is linked to feeding, so that differences may arise among species because of differences in environmental conditions, mode of feeding or tolerance to anoxia. In spite of irrigation activities of thalassinideans, hypoxic conditions may still develop in burrows. Thalassinideans are, however, far more tolerant of hypoxic conditions than most other crustaceans and are able to continue aerobic metabolism at very low partial pressures of oxygen (Thompson & Pritchard 1969, Felder 1979, Hanekom & Baird 1987, Anderson et al. 1991, Atkinson & Taylor 2005). The survival times of various thalassinideans under conditions of low oxygen levels have been reviewed by Atkinson & Taylor (2005). Interspecific differences in tolerance to hypoxia in thalassinideans may be due to variations in gill area as species such as Callianassa subterranea and Jaxea nocturna possess larger weight-specific gill areas than upogebiids, which are less tolerant of hypoxic conditions (Astall et al. 1997a). Under extremely low oxygen partial pressure and high sulphide concentrations, thalassinideans may switch from aerobic to anaerobic metabolism, with lactate as the main end product (Pritchard & Eddy 1979, Zebe 1982, Anderson et al. 1994). Thalassinideans may also use air to overcome anoxic conditions (Felder 1979). Neotrypaea californiensis and some species of Upogebia move toward their burrow openings during low tide (Farley & Case 1968). In the case of Upogebia, the anterior portion of the animal can be held above the water surface, allowing partial reoxygenation of the gills (Hill 1981). Sulphide exposure is also a major problem thalassinideans face (Bourgeois & Felder 2001). Sulphide in marine sediments is usually produced by sulphate-reducing bacteria. In the presence of oxygen, sulphide rapidly oxides, and concentrations usually build up only during anoxic conditions. Sulphide is extremely toxic to most organisms, but thalassinideans appear to be more tolerant than most (Atkinson & Taylor 2005). Accumulation of sulphides through passive diffusion in thalassinidean tissue is countered by oxidation to thiosulphate (Johns et al. 1997), thus eliminating the toxic effects of sulphide. Oxidation to thiosulphate rather than sulphate is energetically more efficient as fewer oxygen molecules are required (Jahn et al. 1996). 143


Thalassinideans as ecosystem engineers Research on the effects of burrowing thalassinideans on marine soft-sediment ecosystems has intensified over the last few decades, particularly in terms of the effects they have on sediment biogeochemistry and community structure that arise from their bioturbative activities (Dworschak 2000, Felder 2001). Bioturbation, the process by which organisms disturb sediments, is an established factor influencing marine soft-bottom communities (Cadée 2001, Flach & Tamaki 2001). The term is broad and covers a range of organismal activities such as birds wading through sediments, the movement of meiofauna between sand grains, flatfish burying themselves in sediments or the production of feeding troughs by grey whales. Under this broad definition, diverse organisms function ecologically as bioturbators. For example, while feeding on bivalves living in sediments, the New Zealand eagle ray Myliobatis tenuicaudatus uses a combination of water jets and flapping of pectoral fins to excavate pits that may be up to a metre wide and 30 cm deep (MacGinitie & MacGinitie 1968, Gregory et al. 1979). Other rays (Urobatis (as Urophus) halleri and Myliobatis californica) can rework a sediment layer up to 15 cm thick per year (Cadée 2001). In the Bering Sea, side-scan sonar images of the sediment surface have revealed pits roughly 2 × 4 m and about half a metre deep, which are believed to be produced by grey whales while feeding on benthic bivalves (Johnson & Nelson 1984). The volume of sediment ejected into the water column during pit formation by grey whales is roughly 1.2 × 109 m3 per year in an area of 22,000 km2. Expressed in another way, these feeding activities result in the reworking of an overall sediment layer roughly 5 cm thick. In Puget Sound, grey whales feed on ghost shrimp, and in the process they make pits roughly 10 cm deep and 6 m2 in area (Weitkamp et al. 1992). Walruses feeding on benthic bivalves form pits averaging 47 m in length and 0.5 m deep (Johnson & Nelson 1984). Thalassinidean crustaceans are, however, considered to be among the most influential of bioturbators (Cadée 2001). Most thalassinideans are burrowing species that expel residual sediment from their burrows to the sediment surface, creating volcano-like mounds on the sediment surface (Figure 3). They can burrow to depths greater than 1 m and turn over sediment from burrows to the surface at exceptionally high rates (Cadée 2001). Depending on population densities, thalassinideans can expel a sediment layer averaging the equivalent of 50–100 cm thick annually (Cadée 2001). These estimates are considerably higher than those measured for other bioturbators, such as the

Figure 3 (A) Uneven sediment topography due to mounds produced by (B) the southern African sandprawn Callichirus kraussi (inset). (Photo sources: G.M. Branch, C.L. Griffiths.) 144


rays, grey whales and walruses mentioned. Moreover, the last organisms are mobile or migratory, so their impacts will be temporary or sporadic, offering benthic communities the opportunity to recover between bouts of disturbance. Burrowing callianassids on the other hand are permanent residents of sedimentary habitats, and their bioturbation will be a continuous feature of the habitat. Communities associated with the sediment cannot therefore recover from the bioturbative impacts of sandprawns. Bioturbators have been classified as ‘ecosystem engineers’ (Levinton 1995), that is, organisms that modify resource availability to other species because of the physical changes they induce in the habitat, either because of their activities or the structures they build (Jones et al. 1994). The application of this concept to thalassinideans was initially slow, but they are now formally recognized as among the most important ecosystem engineers in marine soft sediments, where their activities govern a plethora of ecological processes, including nutrient fluxes and cycling, alteration of geochemical and sedimentological properties and modification of community composition across all organismal groups. Jones et al. (1994) identified six criteria by which relative importance of organisms as ecosystem engineers can be adjudged. Under this framework the New Zealand ghost shrimp Biffarius (as Callianassa) filholi (Berkenbusch & Rowden 2003) and the southern African sandprawn Callichirus (as Callianassa) kraussi (Siebert & Branch 2006) have been formally recognized as ecosystem engineers, but many of the criteria are equally applicable to other thalassinidean species. The criteria are listed next in relation to the characteristics of thalassinidean life histories and ecology. 1. Lifetime per capita activity. In terms of sediment reworking, turnover rates for callianassids are the highest of all known marine bioturbators (Rowden & Jones 1993, Cadée 2001). 2. Population density. Thalassinideans often occur in dense assemblages in marine sediments: up to 400 m−2 (Nates & Felder 1998). 3. Spatial distribution. Thalassinideans are globally distributed, being absent only in polar regions (Dworschak 2004). Individual species often have wide geographical ranges. For example, Callichirus (as Callianassa) kraussi is distributed across the entire 3500-km southern African coastline, spanning four biogeographic regions (Branch et al. 2010). 4. Duration of occupation. Geological evidence indicates that thalassinideans have been present on Earth since the Jurassic or even Permian times (Chamberlain & Baer 1973, Thayer 1979, Schram 1986, Bromley 1996). 5. Durability of constructions of ecosystem engineers. The burrows built by thalassinideans are maintained throughout the lifetime of the organism. 6. Number and types of resource flows influenced. Thalassinideans are known to alter the physical and chemical properties of sediments (Koike & Mukai 1983, D’Andrea & DeWitt 2009), as well as the communities inhabiting these sediments, including seagrass beds (Siebert & Branch 2005a,b, 2006, 2007, Berkenbusch & Rowden 2007, Berkenbusch et al. 2007); meiofauna; benthic primary producers and bacteria (Branch & Pringle 1987, Dobbs & Guckert 1988); and macrofauna (Siebert & Branch 2005a, 2006, Pillay et al. 2007a,b,c, 2008).

The influence of burrowing thalassinideans on sediment and porewater properties Burrow construction and maintenance, together with active ventilation by thalassinideans, have a range of effects on sedimentary and porewater properties and processes. In relation to the role of thalassinideans as ecosystem engineers, their influence on biogeochemical processes is by far the most researched area, with the literature on the topic spanning several decades and many species. 145


Sediment processes and properties Transport of sediments by thalassinideans greatly exceeds that ever attained by abiotic burial or diffusion processes (Grigg 2003). In terms of reworking sediment, the general view is that members of the Callianassidae are the most influential of thalassinideans, showing the highest turnover rates of all known bioturbators (Cadée 2001). Sediment turnover estimates for the Callianassidae have been reviewed by Rowden & Jones (1993), but trends are difficult to assess due to differences among studies in methods employed, units reported and environmental conditions. The highest rate of turnover recorded is 12.14 kg m−2 day−1, for Callichirus (as Callianassa) kraussi (Branch & Pringle 1987). Water temperature, organic content, particle size, the position of burrows on the shore and time of sampling have, in particular, been shown to affect turnover estimates significantly (Griffis & Chavez 1988, Berkenbusch & Rowden 1999, 2000). The deposition of residual sediment from burrows to the sediment surface by thalassinideans often creates an uneven sediment topography (Figure 3; see also Rowden et al. 1998) and can increase the total sediment surface area by 1.5 to 15 times (D’Andrea & DeWitt 2009). Sediment mounds produced by Callianassa subterranea in the North Sea are 5.4 cm tall and 11.7 cm wide at the base (Rowden et al. 1998), while mounds 2–3 cm tall and 7–15 cm wide at the base have been recorded for Pestarella (as Callianassa) candida in the Mediterranean (Dworschak 2002). In Enewetak Atoll, individual callianassids generate mounds of up to 1300 cm3 day−1 (Suchanek & Colin 1986). Sediment unevenness created by these thalassinidean mounds enhances resistance to wave action and increases boundary roughness approximately 1000-fold relative to a smooth sediment surface (Rowden et al. 1998). Ziebis et al. (1996b) quantitatively demonstrated that water flow over sediment mounds produced by the burrowing shrimp Necallianassa (as Callianassa) truncata is not uniform. At distances of 10–20 mm upstream of burrows water flow experienced a significant reduction of velocity within 10 mm of the sediment surface, then accelerated directly over mounds; greatest disturbance to flow occurred at the tail end of mounds, where there were significant flow reductions, with almost complete stagnation roughly 40 mm downstream of mounds. Such differences in flow velocities lead to pressure differentials directly above the mound and in areas surrounding mounds, leading to turbulent flow (Ziebis et al. 1996b). The sediments ejected from callianassid burrows are unconsolidated and are highly erodible even at low current speeds (Pillay et al. 2007a). They are therefore more prone to resuspension and lateral transportation and are redeposited in adjacent areas by bottom currents (Rowden et al. 1998). Lateral dry-weight sediment transport reaches 7 kg m−2 mo−1 for Callianassa subterranea in the North Sea and 8 kg m−2 mo−1 for various species of callianassid in the Caribbean (Roberts et al. 1981). During periods of high current velocities, such transport and resuspension can have extreme effects on bottom sediments, principally by elevating turbidity at the sediment-water interface. Rowden et al. (1998) reported that parts of the seabed in the North Sea can become completely obscured by sediments due to resuspension and lateral transportation by waves, making it virtually impossible to discern individual mounds of C. subterranea. The highly unconsolidated nature of sediments ejected from burrows of thalassinideans, together with burrowing activities, can also affect sediment penetrability, porosity and permeability (Katrak & Bird 2003, Siebert & Branch 2005a, Waldbusser & Marinelli 2006, 2009, D’Andrea & DeWitt 2009). These effects occur primarily because the continual reworking and turnover of sediments by callianassids prevent natural accretion processes that would otherwise compact the sediment bed. Reworking of sediments by the ghost shrimp Neotrypaea (as Callianassa) californiensis creates a “fluidized” sediment surface with an “almost quicksand quality” (Posey 1986, p. 16; also see MacGinitie 1934, Roberts et al. 1981, Bird 1982). Bioturbation by callianassid sandprawns also directly influences the composition of sediments surrounding burrows. In a long-term study of changes to the benthos of Ariake Sound in Japan, 146


increases in population size and range of the thalassinidean Nihonotrypaea harmandi led to a reduction in the silt-clay content of the sediment due to the resuspension of finer particles into the water column (Flach & Tamaki 2001). At the same time, large shell fragments were buried deeper in the sediment because of the rapid conveyer belt type of sediment turnover by N. harmandi. Similarly, feeding by Glypturus (as Callianassa) acanthochirus and Neocallichirus maryae (as Callianassa rathbunae) can funnel up to 2.5 kg m−2 day−1 into specialized subsurface compartments (Suchanek 1983). Fine-grained sediments, less than 1.4 mm in particle diameter, are ejected to the sediment surface to form mounds, while coarser grains (>1.4 mm diameter) are retained in the burrow. Sediment cores from areas densely populated by these thalassinideans show a pattern of alternating layers of fine and coarse sediment. In contrast, Upogebia pugettensis retains fine-grained sediments as its burrow walls are coated with fine mud (Swinbanks & Murray 1981), although it is uncertain whether this is a selective process driven by the thalassinideans or an incidental process (D’Andrea & DeWitt 2009). Bird (2004) also indicated that various thalassinideans, particularly Biffarius arenosus and Trypaea australiensis, sort sediments prior to ejecting them from burrow openings, preferentially removing grains with particle diameters between 125 and 250 µm. Various other thalassinideans have also been reported to line their burrows with fine sediment and detritus (MacGinitie 1930, Posey et al. 1991, Pinn et al. 1998, Webb & Eyre 2004). In many cases, the ‘blowing off’ or retention of fine sediments by thalassinideans influences not only particle size but also sediment organic content. Webb and Eyre (2004) reported a 13% decrease in organic content in the upper layers of sediments occupied by Trypaea australiensis, relative to control treatments without them. In contrast, burrow linings and faecal pellets of T. australiensis are richer in organic matter than surrounding sediments (Kerr 2001). An 11- to 17-fold increase in organic matter content in burrow walls of Glypturus (as Callichirus) laurae was recorded by de Vaugelas & Buscail (1990), a finding corroborated by Abu-Hilal et al. (1988), who reported a 2- to 10-fold increase in burrow wall organic content relative to adjacent subsurface sediments. Kerr & Corfield (1998) reported increases in organic content with depth in sediments occupied by Trypaea australiensis relative to controls lacking it. Burrows of the mudshrimp Upogebia major have been suggested to trap organic matter and phytodetritus (Kinoshita et al. 2003, 2008, Wada et al. 2004). This idea is consistent with other studies showing an accumulation of organic material and phytopigments in burrows of thalassinideans (Suchanek 1983, Dobbs & Guckert 1988, Dworschak & Ott 1993). By actively pumping overlying waters though their burrow systems, thalassinideans may enhance the adsorption of organic matter on to burrow walls, thus stimulating microbial abundance around burrow linings. Passive transport of organic material into burrows may also be possible. Not all studies are unanimous in supporting the notion that thalassinidean burrow linings are sites enriched with organic matter. Stamhuis et al. (1997), for example, showed that organic content of burrow linings and expelled sediments was unaffected by processing by Callianassa subterranea. Dworschak (1983) also could not detect differences in organic contents between burrow walls of Upogebia pusilla and surrounding sediments. The contrasting nature of these results is most likely related to interspecific differences in burrow-lining and feeding behaviour of these thalassinideans. There is likely to be a positive feedback between organic content and burrowing activity. Most studies reveal an enhancement of organic material in the burrows of thalassinideans, but Yamasaki et al. (2010) also recorded that organic content of the sediment is correlated with the mean total length of Upogebia yokoyai; greater size will in turn imply larger and more extensive burrows. Organic matter and fine sediments are intimately linked with the distribution of trace and heavy metals in marine sediments (Abu-Hilal et al. 1988). Burrowing thalassinideans can influence both organic content and fine sediment distribution, particularly along their burrow walls, thus potentially affecting the distribution and abundance of trace elements. Abu-Hilal et al. (1988) showed that trace metals were enriched in burrow linings of Glypturus (as Callichirus) laurae, with iron, manganese, chromium and zinc most concentrated relative to surface sediments. Pemberton et al. 147


(1976) similarly reported enrichment of lead, zinc, copper and iron in burrows of the thalassinidean Axius serratus. Aller et al. (1983) and Papaspyrou et al. (2005) recorded greater levels of iron in the burrow walls of Upogebia affinis and Pestarella tyrrhena. Burrow walls of Sergio trilobata and Lepidophthalmus louisianensis were shown to have greater zinc and cadmium levels than surface sediments (Klerks et al. 2007). Suchanek et al. (1986) have raised the spectre that callianassid bioturbation may redistribute highly radioactive layers of sediment deposited during nuclear tests at Enewetak Atoll and reintroduce them to surface layers with the fine-grained particles they deposit at the surface. The shrimps do not themselves accumulate or secrete trace metals, which are most likely concentrated in burrow walls as overlying water containing trace metals and nutrients is pumped through burrow systems. Trace metals may adsorb on to burrows walls by contact through burrow irrigation or as water moves passively into burrows. The final trace metal concentration in burrows is dependent on adsorption on to particulate organic matter, especially reactive humic substances (Abu-Hilal et al. 1988), and the finer the sediment associated with burrows, the greater the opportunity for adsorption.

Effects on porewater biochemistry Burrow construction and ventilation by thalassinideans greatly influence sedimentary biogeochemical processes, thereby creating unique environments in marine soft sediments (Aller et al. 1983, Waslenchuk et al. 1983, Colin et al. 1986, Murphy & Kremer 1992, Ford et al. 1999, Bird et al. 2000, Flach & Tamaki 2001, Jordan et al. 2009). The Upogebiidae and Callianassidae tend to have different ventilation patterns, with the former spending up to 50% of the time on water pumping, which is linked with filter-feeding behaviour (Dworschak 1981), whereas ventilation is far less frequent in the Callianassidae, occupying roughly 8% of the time and serving mainly respiratory purposes (Stamhuis et al. 1996). Ventilation rates of 30–50 ml min−1 have been reported for the upogebiids Upogebia pusilla and U. major (Dworschak 1981, Koike & Mukai 1983), whereas values of 0.6–5.5 ml min−1 are documented for Nihonotrypaea (as Callianassa) japonica (Koike & Mukai 1983, Mukai & Koike 1984). Oxygenation of sediments by thalassinideans is common as they burrow to depths sometimes in excess of a metre, and their ventilation increases oxygen penetration both laterally and vertically into the sediment (Forster & Graf 1992, 1995, Flach & Tamaki 2001, Katrak & Bird 2003, Kinoshita & Furota 2004). Burrowing effectively increases the total area of the sediment-water interface, by up to 400% in some cases (Ziebis et al. 1996a), and ventilation of burrows is responsible for transferring oxygen to deeper sediments (Kinoshita & Furota 2004). Prior to a population increase of the burrowing shrimp Nihonotrypaea harmandi in Japan, the oxic zone in sediments was restricted to the upper 2- to 3-cm layer, but afterwards, sediment oxygenation extended as deep as 60 cm (Flach & Tamaki 2001). Experimental removal of burrowing thalassinideans has been shown to increase the prevalence of sediment anoxia and reduce the depth of the sedimentary oxic layer (Wynberg & Branch 1994, Contessa & Bird 2004). Sediment oxygenation associated with tubes or mounds formed by thalassinideans can also occur passively. The ‘chimney’ effect of burrow openings in assisting flow into burrows is well documented (Vogel 1977, 1994) and has been suggested to reduce the energetic costs of ventilation (Allanson et al. 1992). This effect potentially maintains oxygen transfer into sediments during periods when thalassinideans are not actively pumping water. Sediment mounds produced by thalassinideans also influence small-scale oxygen penetration. Ziebis et al. (1996a) investigated the effects of mound production by the burrowing mudshrimp Necallianassa (as Callianassa) truncata and demonstrated that oxygen penetration into smooth sediments was restricted to the upper 4-mm layer, but that a sediment mound 1 cm tall facilitated penetration to a depth of 44 mm. In effect, mounds increased the oxygenated sediment volume by a factor of 4.8. At natural background mound 148


densities (120 m−2), the total volume of oxic sediment was calculated to be 3.3 times greater than for smooth sediment. The burrow waters of thalassinideans are usually enriched in nutrients compared with overlying water (Koike & Mukai 1983, Waslenchuk et al. 1983, Murphy & Kremer 1992, Hughes et al. 2000). Waslenchuk et al. (1983) recorded greater levels of dissolved phosphate, ammonia and sulphide in burrow waters of various species of callianassid in Bermuda, during both active pumping and inactive phases, with overall concentrations of dissolved organic carbon (DOC) and trivalent arsenic also greater in burrows than in overlying water. Burrow waters of Nihonotrypaea (as Callianassa) japonica and Upogebia major contain levels of ammonium an order of magnitude greater than overlying waters, with nitrate and nitrite levels two to three times greater (Koike & Mukai 1983). Effluent burrow water of Callianassa subterranea also contains higher levels of ammonium and phosphate than ambient water (Hughes et al. 2000). D’Andrea & DeWitt (2009) have shown the far-reaching effects of the mudshrimp Upogebia pugettensis on biogeochemical processes, leading them to label this shrimp a “geochemical ecosystem engineer”. Field incubations indicated that remineralization rates of organic carbon and benthic uptake of oxygen were positively correlated with the density of shrimp burrows. Effects on nitrogen cycles were, however, particularly striking. Ammonification rates were elevated up to seven times, nitrification rates three to four times and denitrification up to four times greater than areas lacking this shrimp. Ventilation by U. pugettensis also leads to an increase in levels of dissolved inorganic nitrogen (DIN); its flux increases exponentially with prawn density, rising to as much as 15 times greater than in areas without U. pugettensis. Effectively, the population of U. pugettensis increased carbon and nitrogen efflux by 1.9 and 3.7 times, respectively. Howe et al. (2004) similarly showed that nitrification was enhanced 2.9 times in the presence of U. deltaura. Webb & Eyre (2004) demonstrating that the Australian ‘yabby’ Trypaea australiensis enhances benthic oxygen demand by 81%, with denitrification rates four times greater in the presence of this shrimp. They estimated that T. australiensis accounts for 76% of total sediment denitrification. Efflux of ammonia was also greater in the presence of T. australiensis. Complex mechanisms are responsible for the effects of thalassinideans on nutrient and gaseous properties of soft sediments. The extensive burrow systems produced by thalassinideans effectively increase the area of oxic surface and the diffusive movement of solutes available to microorganisms. The addition of mucus to burrows by some thalassinideans increases the carbon content available for microbial activity (D’Andrea & DeWitt 2009) and is responsible for trapping phytoplankton cells, with up to 30% sticking to mucous linings during ventilation (Griffen et al. 2004), thus adding to the carbon pool available to bacteria in the burrow wall. Burrow ventilation may also enhance the availability of oxygen and other oxidants to microbes. All of these factors may increase oxygen uptake by microbes (D’Andrea & DeWitt 2009). Most thalassinideans have low metabolic rates relative to other crustaceans (Atkinson & Taylor 2005), and the common view is that enhanced microbial activity is the major reason for elevated oxygen consumption in sediments bioturbated by thalassinideans (Papaspyrou et al. 2004, Webb & Eyre 2004, Kristensen & Kostka 2005). Net fluxes of DIN are dependent on processes that produce and remove sedimentary inorganic nitrogen, as well as transport pathways such as diffusion and bioirrigation (DeWitt et al. 2004, D’Andrea & DeWitt 2009). Of the different DIN species, ammonium is most easily available for exchange across the sediment-water interface. Elevated ammonium flux recorded in the presence of thalassinideans is most likely a function of the increased diffusive surface area associated with thalassinidean burrows but could also be due to increased nitrogen mineralization, caused either directly by bacteria or indirectly because of increased organic content in thalassinidean burrows (Webb & Eyre 2004, D’Andrea & DeWitt 2009). Fluxes of ammonia are also directly affected by thalassinidean excretion or production by burrow microorganisms (Koike & Mukai 1983, D’Andrea & DeWitt 2009). Previous studies have shown that macrofaunal excretion can account for 10–70% of DIN flux (Blackburn & Henrikson 1983, Kristensen 1988), and for Upogebia pugettensis, it 149


was estimated that excretion contributes 5–21% of total ammonium flux in sand flats (D’Andrea & DeWitt 2009). Enhanced rates of nitrification associated with thalassinideans are believed to be related to increased surface areas of burrows for nitrifying bacteria, increased supply of oxygen through bioirrigation, and elevated concentrations of substrate (NH4+) due to excretion and ammonification in burrow walls (D’Andrea & DeWitt 2009). It has, however, been suggested that some bacteria involved in the nitrification cycle benefit from low oxygen content, as occurs in portions of burrows of some thalassinideans (Koike & Mukai 1983). The contribution of thalassinidean faecal pellets to sediment organic content has received little attention in the literature. In one of the few studies of this nature, Frankenberg et al. (1967) demonstrated that populations of Callichirus major in a sandy beach ecosystem could produce as much as 11,700 g of carbon per day in an area of 200,000 m2. Viewed relative to other carbon-producing systems in the region, faecal production by C. major was roughly 2.4–28% of phytoplankton production, 60% of microphytobenthic production, 1.3% of production by Spartina alterniflora beds and 20% of exported marsh detritus (Frankenberg et al. 1967 and references cited therein). A minimum of 70% of faecal matter was exported subtidally where it was fed on or then broken up and transferred by wave action back to intertidal sediments for consumption. Branch & Day (1984) also drew attention to the importance of faecal pellets of Callichirus (as Callianassa) kraussi, indicating that its total faecal production could contribute as much carbon as all other carbon inputs combined in the estuarine ecosystem they studied on the southern coast of South Africa. The carbon and nitrogen content of newly voided faeces of marine invertebrates can increase over time due to colonization by bacteria. Faeces are sometimes reingested by invertebrates to exploit the bacteria that develop on them as a food source. This cycle of voidance, colonization and consumption probably continues until the organic components in faeces are depleted to the point at which consumption is no longer profitable (Newell 1979). In this context, it is likely that the role of thalassinidean faeces in marine soft-sediment ecosystems has been underestimated, as reflected in the sparse literature on the topic. Based on the examples given in this section, it should be apparent that the influence of burrowing thalassinideans on biogeochemical processes in marine soft sediments is immense. This was perhaps best encapsulated by Pemberton et al. (1976), who described one particular thalassinidean, Axius serratus, as a “Supershrimp” in view of its deep burrowing and impacts on sediment geotechnical processes on the seabed. Such impacts of thalassinideans are not only extremely important for ecosystem functioning but also strongly influence co-occurring faunal and floral assemblages, from bacteria to large macrofauna and from microalgae to seagrasses. The following sections continue the theme of ecosystem engineering by burrowing thalassinideans, focusing specifically on their effects on co-occurring communities.

Effects on bacteria, microalgae and meiofauna Bacteria Burrow construction and ventilation by burrowing thalassinideans are clearly important in developing a variety of microclimates within the sediment. This creates diverse niches for microbes, including both aerobic nitrifying species and anaerobic denitrifying and sulphate-reducing groups (Bird et al. 2000, Kinoshita et al. 2003). In addition, the selective retention of fine organically rich sediments by some thalassinideans, or the stabilization of burrow walls by mucopolysaccharides or plant material, may aid microbial activity (Aller & Aller, 1986, Aller, 1988, Reichardt, 1988, Steward et al. 1996). 150


Dobbs & Guckert (1988) showed that bacterial biomass, estimated from phospholipid phosphate and phospholipid fatty acid (PLFA) assays, is roughly four times greater in burrow linings of Sergio (as Callianassa) trilobata than surrounding sediment surfaces. This trend was also mirrored in concentrations of all fatty acids sampled (Dobbs & Guckert 1988). Branch & Pringle (1987), using direct count methods, recorded reductions in bacterial numbers in surface sediments occupied by Callichirus (as Callianassa) kraussi but greater densities of bacteria with depth into the sediment and with proximity to the burrow linings. Dworschak (2001) and Papaspyrou et al. (2005) both demonstrated increased bacterial abundance in burrow walls of the callianassid Pestarella tyrrhena relative to adjacent ambient sediments. In addition, Dworschak (2001) reported greater bacterial abundance in walls of feeding chambers (in which seagrass debris is collected) than in normal burrow walls. Both results corroborate previous assertions that burrows are key microhabitats for microbes, and that ‘interfaces’ support greatest microbial biomass (Dobbs & Guckert 1988). In contrast to these reports, Bird et al. (2000) did not find differences in bacterial abundance or biomass between burrow walls of the callianassid Biffarius arenosus and adjacent sediments. However, they did point out that inadequate replication may underlie the lack of statistically significant differences. Kinoshita et al. (2003) showed a more complex case in which bacterial abundance in burrow walls was similar to surface sediments during winter but then became up to four times greater during summer, indicating strong seasonality and a possible interactive effect of temperature on microbial abundance. Microbial activity, measured by quantifying extracellular enzyme activity using fluorescein diacetate (FDA) hydrolysis, was shown to be three times greater in burrow walls of Biffarius arenosus and surface sediments relative to subsurface sediments (Bird et al. 2000). Thus, thalassinidean burrows conform to the view that burrow walls of invertebrates are hot spots for microbial activity (Aller & Yingst 1978, 1985, Aller & Aller 1986, Reichardt 1988, Köster et al. 1991). Papaspyrou et al. (2005) have shown that the specific microclimates in thalassinidean burrows influence the composition of bacterial assemblages. Bacterial communities in burrow walls of Pestarella tyrrhena are different from those in adjacent ambient sediments. These authors also showed that burrow assemblages are more temporally stable than surface assemblages, concurring with the work of Lucas et al. (2003) on the tube walls of Hediste (as Nereis) diversicolor. Both results confirm current thinking that burrow walls and sediment immediately adjacent to them are more stable than surface sediments, with the latter more prone to both biological and physical disturbances (Kristensen 1988, Papaspyrou et al. 2005). Earlier work by Dobbs & Guckert (1988) and Bird et al. (2000) failed to detect differences in bacterial assemblages between burrow walls of thalassinideans and adjacent unoccupied sediments, but this may simply reflect the fact that the PLFA assay they employed is less sensitive than the denaturing gradient gel electrophoresis (DGGE) used by Papaspyrou et al. (2005). Thalassinideans can influence bacteria around burrow walls for a number of reasons. Firstly, by oxygenating burrows, thalassinideans may promote aerobic metabolism in bacteria. Secondly, accumulation of organic matter, either through the development of a burrow lining or via influx of organic debris, will enhance bacterial abundance (Kinoshita et al. 2003, Wada et al. 2004). Pillay et al. (2007c) reported that bioturbation by Callichirus (as Callianassa) kraussi negatively affects microbial biofilms growing on sediment surfaces, which is in agreement with the findings of Branch and Pringle (1987) for the same species, obtained by direct counts. Biofilms are a complex mixture of bacteria, fungi and microalgae coexisting in a matrix of extracellular polymeric substances (EPSs) they secrete (Underwood & Paterson 1995, Gu et al. 1998). Rapid turnover rate of sediment from burrows to the surface probably curtails surface colonization by bacteria. Sediments with poorly developed biofilms are in turn more erodible and prone to resuspension, thus increasing erosion of bacteria to the water column, further reducing bacterial colonization of sediment (Figure 4; Pillay et al. 2007c). 151


40 µm

40 µm

Figure 4 The influence of burrowing thalassinideans on bacteria and microalgae on sediment surfaces. Bacteria and microalgae form films that stabilize sediment in the absence of thalassinideans (A), promoting laminar flow of water over the sediment surface (B). The negative effect of thalassinideans on surface films promotes turbulent flow over the sediment bed, contributing to erosion of bacteria and microalgae (C). Scanning electron microscopic (SEM) images (t200) contrast the uniform smooth microbial biofilm developing on surfaces of sediments lacking Callichirus kraussi (left) with the irregular, loosely packed sand particles depauperated of a microbial film in the presence of this sandprawn (right). (Adapted from Pillay (2006).)

Microalgae Burrowing thalassinideans can have a range of effects on sediment microalgae, again due to the unique microclimates they produce in sediments as well as their sediment-reworking activities. Most studies have reported negative effects of thalassinideans, particularly the callianassids, on microalgae on the surfaces of sediments (Wynberg & Branch 1994, Contessa & Bird 2004, Pillay et al. 2007a,b,c), but in rare cases callianassids may enhance microalgal levels in sediments (Katrak & Bird 2003). Using field observations, Pillay et al. (2007c) showed that chlorophyll-a (chl-a) concentrations at sites with high densities of the sandprawn Callichirus (as Callianassa) kraussi were up to 10 times lower than at sites where it was rare or absent. These results were supported by field experiments that showed a three- to fourfold decline in chl-a in cages with C. kraussi relative to 152


controls lacking it. Similarly, Webb & Eyre (2004) recorded a twofold decrease in chl-a levels in treatments with Trypaea australiensis relative to controls. Experimental removal of burrowing thalassinideans to simulate the effects of bait harvesting on sandflat ecosystems have been shown to increase benthic chl-a levels (Wynberg & Branch 1994, Contessa & Bird 2004), although Branch & Pringle (1987) did not find any effect of bioturbation by Callichirus (as Callianassa) kraussi on benthic microalgae when they used field caging experiments to manipulate sandprawn densities. They did, however, point out that this outcome was most likely an artefact of the small cages used in the experiment. Reduction of surface microalgal biomass by actively burrowing thalassinideans is due to a number of factors. Firstly, the rapid deposition of sediment from burrows may bury surface microalgae, transporting them deeper into sediments, where they will be deprived of light. Secondly, because of the enhanced erodibility of sediments expelled by thalassinideans (Pillay et al. 2007a), microalgae will be swept more readily into the water column (Figure 4). Bioturbation by several other deposit-feeders is known to enhance sediment erodibility by negatively affecting natural sediment stabilizers such as bacteria and diatoms (Widdows et al. 2000, de Deckere et al. 2001, Paterson & Hagerthey 2001). By binding the topmost sediment layer, such sediment stabilizers promote smooth or laminar flow of water over sediments, as is the case for sediments in which thalassinideans are rare or absent. High densities of thalassinideans deplete surface-binding microorganisms, increasing the chances of microalgae being swept into the water column (Pillay et al. 2007c). The same mechanism could contribute to the scarcity of bacteria on the surface of sediments occupied by thalassinideans (Pillay et al. 2007c). Burrowing thalassinideans can, however, promote microalgae in deep sediments. Papaspyrou et al. (2005), for example, recorded greater chl-a levels in burrow walls of Pestarella tyrrhena than in surface or surrounding sediments, although only differences between burrow walls and surface sediments were statistically significant. Branch & Pringle (1987) documented similar increases in chl-a levels with increasing depth below the sediment surface and distance to burrow walls of Callichirus (as Callianassa) kraussi. In contrast to these studies, Dobbs & Guckert (1988) did not find differences in chl-a levels in burrow walls of Sergio (as Callianassa) trilobata relative to surface sediments, although concentrations of phaeopigments, which are indicative of degraded autotrophic material, were four times more concentrated in burrows than surface sediments. Diatoms and other microalgae were not detected in burrows, and the photopigments recorded there most likely reflect debris derived from vascular plants. Predicting the effects of thalassinideans on microalgae is hindered by the fact that almost all examples explored involve deposit-feeding callianassids. Filter-feeding species, with stable burrows and limited turnover of sediment, may have no effect on benthic microalgae or may even promote them by increasing nutrient flux. So, for example, Kinoshita et al. (2003) detected no differences in chl-a levels in burrows of Upogebia major and surface sediments.

Meiofauna Meiofaunal assemblages have long been considered to be intimately linked to macrofauna, with macrofaunal biogenic structures known to enhance meiofaunal diversity (Bell 1980, Ólafsson 2003). Compared with studies investigating thalassinidean-macrofaunal interactions, studies of thalassinidean-meiofaunal interactions are scarce. Burrowing thalassinideans can have a range of effects on meiofaunal abundance and community composition, but the effects are ambiguous because relevant studies are few and have yielded contrasting results. Branch & Pringle (1987) demonstrated that bioturbation by the southern African sandprawn Callichirus (as Callianassa) kraussi negatively affects meiofaunal numbers on the sediment surface, as well as at depths of 10–20 cm. Nematodes were most affected, with their densities reduced by almost half in the presence of this thalassinidean. Copepods and juvenile polychaetes were less 153


affected or appeared unaffected. Dobbs & Guckert (1988) showed that meiofaunal abundance in burrow walls of Sergio (as Callianassa) trilobata were roughly four times lower than in surrounding sediments, with nematodes in particular following this pattern. These authors did, however, point out that sampling bias, specifically the sorting and fixing protocol, favoured hard-bodied meiofauna, thus potentially missing soft forms. Alongi (1985) similarly showed that meiofaunal densities declined in burrows of various species of callianassid in subtidal lagoonal sediments. In contrast, burrows of Trypaea (as Callianassa) australiensis seem to promote meiofauna, with densities of both permanent and temporary meiofauna greater in its burrows than in adjacent sediments (Dittmann 1996). Because of the limited work on thalassinidean-meiofaunal interactions, it is difficult to generalize about the nature of these interactions or the potential mechanisms involved. This difficulty was raised by Branch & Pringle (1987) when trying to identify mechanisms by which Callichirus (as Callianassa) kraussi influences meiofaunal assemblages and remains true for most other studies of thalassinidean-meiofaunal interactions. Surface meiofaunal densities may be reduced by thalassinideans, especially those that are major sediment reworkers, as the sediment they deposit on the surface may bury the meiofauna. Deeper in sediments, meiofauna may benefit from oxygenation of sediments, greater food availability in the form of organic matter, and possibly enhanced microbial abundance (Dobbs & Guckert 1988, Kinoshita et al. 2003). Understanding why meiofauna numbers tend to decline in burrows of thalassinideans is difficult. The sedimentary environment in burrows of some thalassinideans, especially those that line their burrows, may be unfavourable for meiofauna, principally because the sediments are too fine and poorly sorted and have low porewater content. These factors are hypothesized to influence meiofauna negatively because the limited pore spaces severely limit movement of interstitial organisms (Dobbs & Guckert 1988 and references therein).

Thalassinidean-macrofaunal interactions Adult-adult interactions Several studies throughout the world have shown that thalassinideans exert considerable influence on macrofaunal communities. This is not surprising given the prominent role these ecosystem engineers play in modifying benthic biogeochemical characteristics and processes. Three main types of studies on thalassinidean-macrofaunal interactions are reported in the literature: field observations comparing areas with high versus low densities of thalassinideans, experimental manipulations, and longterm studies of ecosystem changes following natural changes in the abundance of thalassinideans. Long-term studies provide valuable information on the consequences of population expansions or contractions of thalassinideans for ecosystem functioning and community structure. One of the first studies of this kind was made by Tamaki (1994) in the Ariake Sound, Japan, where densities of the callianassid shrimp Nihonotrypaea harmandi increased roughly 10-fold between 1979 and 1998. Associated with this were several changes in sediment characteristics, including alterations in granulometry, oxygen levels and shell content. Importantly, the increase in density of N. harmandi coincided with the local extinction of the grazing gastropod Umbonium moniliferum, which dropped from densities of 2000 m−2 in 1979 to zero in 1986 (Tamaki 1994). In 1995, however, there was evidence of a decline in density of Nihonotrypaea harmandi, which coincided with a partial recovery in Umbonium moniliferum populations (Flach & Tamaki 2001). Other species also appeared to be affected by population fluctuations of Nihonotrypaea harmandi. The tube-building polychaete Pseudopolydora paucibranchiata, which was the most dominant macrobenthic species prior to 1979, underwent major declines during population increases of Nihonotrypaea harmandi—a trend also mirrored by the surface deposit-feeding opheliid polychaete 154


Armandia amakusaensis. Destabilization of sediment due to bioturbation by this burrowing thalassinidean was identified as the mechanism driving these changes (Flach & Tamaki 2001). In the North Sea, similar shifts in the benthos have taken place in parallel with increases in thalassinidean densities. The brittlestar Amphiura filiformis was the dominant benthic macrofaunal species between 1984 and 1992, with densities ranging between 1433 and 1750 individuals (ind.) m−2. After 1992, however, its density declined to less than 10%, coincident with an increase in abundance of the burrowing shrimp Callianassa subterranea from roughly 50 ind. m−2 in 1982 to 200 ind. m−2 in 1992. The highly erodible nature of sediments created by C. subterranea may have hampered recruitment of juvenile Amphiura filiformis and is the likely mechanism responsible for its decline (Amaro et al. 2007, van Nes et al. 2007). The most recent work reporting shifts in benthic communities due to thalassinideans was provided by Pillay et al. (2008). Sand flats in an estuarine embayment in South Africa underwent a major transformation between 1994 and 2002, in which increases in densities of the burrowing thalassinidean sandprawn Callichirus (as Callianassa) kraussi were coincident with changes in sediment granulometry from muddy sand to sand and decreases in abundance of suspension-feeders, depositfeeders and surface grazers. One of the most important changes over this time period was a 25-fold reduction in bivalve abundance. The role of C. kraussi in these changes in the benthos has since been experimentally and observationally evaluated (Pillay et al. 2007a,b,c, 2008). An interesting outcome of the study by Pillay et al. (2008) was the possibility that burrowing thalassinideans may indirectly influence higher trophic groups. In 1994 when C. kraussi densities were low, bottom-feeding fish dominated the ichthyofauna, and bivalve siphons were the main food item in their stomachs, contributing between 10 and 60% to diets. In 2002, when C. kraussi had became established, the fish community changed, with zooplanktivorous species becoming dominant, and bivalve siphons were no longer being recorded in any of the stomachs of the previously numerically dominant bottom-feeding fish. Pillay et al. (2008) noted that waders also declined over the same period and tentatively suggested that this might also be linked to changes in prey availability associated with the ascendancy of C. kraussi, although the evidence for this is weaker than in the case of changes in the fish fauna. While it is impossible to be certain that these cascading changes were due to bioturbation by C. kraussi, the experimental and observational data highlight the prominent role of C. kraussi as an ecosystem engineer and the potential for burrowing thalassinideans in general to influence higher trophic levels by modifying prey abundance and distribution (Pillay et al. 2008). Although challenging, understanding the effects of thalassinideans on higher trophic groups should be an important goal for future research in the field as it represents a major gap in knowledge. Several other detailed field and experimental studies documented the influence of thalassinideans on macrofauna, as summarized in Table 2. All of these studies indicated asymmetric thalassinidean-macrofaunal interactions, with macrofauna being significantly affected by thalassinideans, but not vice versa (Flach & Tamaki 2001). Also noteworthy is that bioturbation by sandprawns can have either positive or negative effects on macrofauna. Negative effects have been recorded on bivalves (Peterson 1977, Murphy 1985, Berkenbusch et al. 2000, Pillay et al. 2007a,b,c, 2008), corals (Aller & Dodge 1974), penaeid shrimps (Nates & Felder 1998), macrofauna with limited mobility such as tanaids, spionid polychaetes (Posey 1986) and filter-feeding gastropods (Flach & Tamaki 2001). Promotive effects of sandprawns have been recorded for mobile taxa such as ostracods (Riddle 1988), bivalves (Aller & Dodge 1974, Tudhope & Scoffin 1984), amphipods (Posey 1986, Riddle 1988) and burrowing infauna (Siebert & Branch 2005a,b, 2006, 2007). In spite of the wealth of literature available on the influence of burrowing thalassinideans on macrofauna, there seems to be no single unifying theory on the mechanism by which community structuring occurs. Much of the initial work was done in the early 1970s and 1980s, with the nowclassical work of Rhoads & Young (1970) and Brenchley (1981). For almost two decades, no new 155


Table 2 Review of studies of thalassinidean-macrofaunal relationships showing the major outcomes Reference

Thalassinidean

Location

Outcome

Aller & Dodge 1974

‘Callianassa’ (before generic revision)

Caribbean

Peterson 1977

Neotrypaea (as Callianassa) californiensis Biffarius ceramicus (as Callianassa ceramica) Upogebia pugettensis and Neotrypaea californiensis ‘Callianassa sp.’ (before generic revision) Neotrypaea (as Callianassa) californiensis Neotrypaea (as Callianassa) californiensis

North America

Negative effects on corals, reduction in settlement and growth of suspensionfeeders Exclusion of filter-feeding bivalves, negative effect on polychaete recruitment Negative effects on spionid polychaetes

Posey et al. 1991

Upogebia pugettensis

North America

Tamaki 1994

Nihonotrypaea harmandi

Japan

Dittmann 1996

Trypaea (as Callianassa) australiensis ‘Callianassa’ (before generic revision) Biffarius (as Callianassa) filholi

Australia

Callichirus (as Callianassa) kraussi Callichirus (as Callianassa) kraussi Callianassa subterranea

South Africa

Dorsey and Synnot 1980 Brenchley 1981 Tudhope & Scoffin 1984 Murphy 1985

Australia North America Australia

South Africa

Negative effects on filter-feeding bivalves through increases in turbidity Negative effect on sedentary deposit-feeders, promotive effect on one mobile suspension-feeder Negative effect on sessile polychaetes and crustaceans Localized extinction of a gastropod and a mobile polychaete Positive effect on amphipods and overall macrofaunal density Positive effects on mobile polychaetes and ostracods Reduction in densities of an amphipod and a bivalve Negative effect on a suspension-feeding thalassinidean Promotion of burrowing infauna

North Sea

Reduction in densities of brittlestars

Callichirus (as Callianassa) kraussi Callichirus (as Callianassa) kraussi

South Africa

Pillay et al. 2007b

Callichirus (as Callianassa) kraussi

South Africa

Pillay et al. 2007c

Callichirus (as Callianassa) kraussi Callichirus (as Callianassa) kraussi

South Africa

Negative effects on an eelgrass limpet, positive effect on burrowing infauna Negative effects on survival, microalgal consumption and physical condition of a filter-feeding bivalve and a grazing gastropod Negative effects on surface grazers, subsurface and filter-feeders, density, richness and diversity of macrofauna Negative effect on macrofaunal recruit abundance and diversity Negative effects on surface grazers, subsurface and filter-feeders, richness and diversity of macrofauna

Posey 1986

Riddle 1988 Berkenbusch et al. 2000 Siebert & Branch 2005a Siebert & Branch 2005b, 2007 van Nes et al. 2007, Amaro et al. 2007 Siebert & Branch 2007 Pillay et al. 2007a

Pillay et al. 2008

North America

Negative effect on surface deposit-feeders and tube builders Positive effects on mobile bivalves

North America

Australia New Zealand

South Africa

South Africa

156


major hypotheses were presented specifically for thalassinidean-macrofaunal interactions until the contribution by Pillay et al. (2007c). Although not directly related to thalassinideans, the work of Rhoads & Young (1970) has often been used to understand the mechanisms by which these bioturbators structure macrofaunal communities. This emanated from observations that suspension- and deposit-feeders are often spatially separated, with suspension-feeders restricted to firm mud bottoms, whereas deposit-feeders tend to occur in soft muddy bottoms. This segregation was believed to have arisen because bioturbation by deposit-feeders creates a ‘fluid’ sediment surface that can readily be resuspended by wave action (even at low velocities), with a range of possible effects, including the clogging of filtering apparatus, burial of larvae, or prevention of settlement of suspension-feeders. This concept was referred to as the ‘trophic group amensalism hypothesis’ (Rhoads &Young 1970) and was supported by transplantation experiments indicating that growth of the suspension-feeding clam Mercenaria mercenaria was reduced when individuals were held in close proximity to bioturbated sediment surfaces, relative to those to held high above it. There has been further support for the trophic amensalism hypothesis from studies of thalassinidean-macrofaunal interactions, with negative effects documented on suspension-feeding bivalves (Peterson 1977, Murphy 1985, Berkenbusch et al. 2000, Pillay et al. 2007a,b,c, 2008), gastropods (Tamaki 1994) and polychaetes (Pillay et al. 2007b,c, 2008). Also supporting the hypothesis, Pillay et al. (2007a) showed that bioturbation by Callichirus (as Callianassa) kraussi significantly reduces the survival, microalgal consumption and condition of the suspension-feeding bivalve Eumarcia paupercula. The amount of microalgae consumed by E. paupercula was halved when it was placed in experimental cages with Callichirus (as Callianassa) kraussi, and this trend was mirrored in comparisons between habitats of high and low densities of C. kraussi. These effects on Eumarcia paupercula may occur through two mechanisms. Firstly, sediment reworking by Callichirus kraussi may physically hinder microalgal ingestion by blocking the filtration apparatus of Eumarcia paupercula. Secondly, if E. paupercula were to switch from filter feeding to deposit feeding, it would encounter the problem of reduced microalgal biomass on the sediment surface as sediment turnover by Callichirus kraussi has been shown by both experimental and field approaches to reduce abundance of surface microalgae, bacteria and the carbohydrates they exude by 50–70% (Pillay et al. 2007c). Further support for the trophic amensalism hypothesis is provided by Pillay et al. (2007a), who demonstrated that the physical condition of Eumarcia paupercula is negatively correlated with sediment erodibility, which is in turn enhanced by Callichirus kraussi bioturbation. The negative influence of bioturbation by C. kraussi on Eumarcia paupercula was also corroborated by field data, as the size of E. paupercula in areas where Callichirus kraussi was abundant was three times smaller than in areas where C. kraussi was rare or absent. These results are similar to those reported by Rhoads & Young (1970), in which sediment reworking by the deposit-feeding bivalves Nucula proxima, Yoldia limulata and Macoma tenta reduced growth of the suspension-feeding bivalve Mercenaria mercenaria. Brenchley (1981) questioned the validity of the trophic amensalism hypothesis and showed from a combination of field and laboratory manipulations that bioturbators may not necessarily target specific trophic groups such as suspension-feeders, as postulated by the trophic group amensalism hypothesis of Rhoads & Young (1970). Instead, she proposed that the mobility of organisms and whether they were surface dwellers or burrowers determined their susceptibility to bioturbation. She demonstrated experimentally that densities of sedentary tube builders, such as the spionid polychaete Rhynchospio arenicola and the tanaid Leptochelia savignyi (as L. dubia), were reduced significantly by the bioturbative activities of the mudshrimp Upogebia pugettensis, the lugworm Arenicola marina and the sand dollar Dendraster excentricus. In contrast, mobile organisms such as surface suspension-feeding and burrowing bivalves and polychaetes were unaffected

157


by bioturbation (Brenchley 1981). This ‘mobility mode hypothesis’ is frequently used to explain the relative effects of bioturbation by burrowing thalassinideans on macrofauna with different mobilities and lifestyles (Posey 1986, Pillay et al. 2007b). Again, there were several studies supportive of the mobility mode hypothesis. Posey (1986) showed from correlative field observations that densities of sedentary tube builders such as the polychaetes Pseudopolydora kempi japonica, Pygospio elegans and Streblospio benedicti were negatively associated with densities of the thalassinidean Neotrypaea (as Callianassa) californiensis. Although the density of one suspension-feeding amphipod was positively influenced by the density of N. californiensis, five other deposit-feeders reached greatest densities outside beds of this thalassinidean. Posey (1986) pointed out that the last result opposes the trophic amensalism hypothesis, which predicts a negative effect of deposit-feeders on suspension-feeders but not negative effects on other deposit-feeders. Posey’s results are more supportive of the mobility mode hypothesis as five of the six sedentary species examined were negatively correlated with N. californiensis density, and the suspension-feeder that was positively affected by N. californiensis was a mobile species. Pillay et al. (2007a) provided supportive evidence for Brenchley’s (1981) mobility mode hypothesis. In experiments testing the effects of bioturbation by Callichirus (as Callianassa) kraussi on survival and feeding by the mobile surface-grazing gastropod Nassarius kraussianus and the sedentary suspension-feeding bivalve Eumarcia paupercula, it was shown that Callichirus kraussi had no effect on the survival of Nassarius kraussianus but increased mortality of Eumarcia paupercula. Microalgal consumption (measured as gut chl-a content) was, however, halved in both species in the presence of Callichirus kraussi. Nassarius kraussianus may survive the effects of Callichirus kraussi due to its mobility, allowing it to escape burial by sediments turned over by C. kraussi. Experiments on another mobile grazing gastropod, Ilyanassa obsoleta, have demonstrated that if these snails are buried by a 10-cm sediment layer, they can actively burrow to the surface within 4–8 hours; for a 15-cm sediment layer, burrowing to the surface took 24 hours, but they did nonetheless survive (Miller et al. 2002). Mobility, however, does not guarantee that organisms will be unaffected by bioturbation as they will likely suffer metabolic costs. Even though survival of Nassarius kraussianus was not affected by Callichirus kraussi bioturbation, its consumption of benthic microalgae was reduced (Pillay et al. 2007a). In the long term, this could translate into a reduction of growth rate and possibly reproduction or lead to emigration to avoid areas bioturbated by C. kraussi. There are two possible mechanisms by which C. kraussi influences gut chl-a levels in Nassarius kraussianus. Firstly, the high sediment turnover rates reported for callianassid sandprawns (Rowden & Jones, 1993), and for Callichirus (as Callianassa) kraussi in particular (Branch & Pringle, 1987), may bury these snails, increasing the amount of time they must spend to reemerge, thereby reducing feeding opportunities. Secondly, reduced gut chl-a levels may simply reflect a scarcity of microalgae in sediments occupied by C. kraussi (Pillay et al. 2007c). Indeed, bioturbation by several thalassinideans does reduce benthic microalgal levels. Thus, the influence of thalassinideans on the food supply of benthic macrofauna is another likely pathway by which they structure communities (Pillay et al. 2007a,b). This mechanism is essentially an extension of the trophic amensalism hypothesis in that any organism whose food source is influenced by sandprawns may be directly or indirectly affected. Using a combination of field observations and experiments, Pillay et al. (2007b, 2008) found that macrofaunal communities in the presence of C. kraussi had statistically lower densities of deposit-feeders, suspension-feeders and grazing gastropods relative to sediments lacking C. kraussi, while burrowing infaunal species were unaffected by C. kraussi bioturbation. The negative effect observed on suspension-feeders is in agreement with the predictions of the trophic amensalism hypothesis, but the reductions in deposit-feeders and grazers by C. kraussi run counter to its predictions. In terms of mobility, the negative effect of C. kraussi on sessile suspension-feeders and the neutral or positive effects on burrowing infauna are in agreement with Brenchley’s (1981) mobility mode hypothesis, but the negative effect on mobile grazers does not conform to those predictions. 158


The lack of a clear consensus on whether thalassinidean-macrofaunal relationships are related to mobility or feeding mechanism is symptomatic of the literature on this topic. The application of the trophic amensalism and mobility mode hypotheses to thalassinideans-macrofaunal interactions has generated significant debate in the search for a unifying mechanism by which thalassinideans structure macrofaunal communities. However, a single unifying mechanism is unlikely, given the range of effects of thalassinideans on sediment biophysical properties, and an interplay between different mechanisms is more plausible. Promoting a single mechanism is perhaps an oversimplification of a complex problem. Also pertinent to the lack of agreement in the literature about mechanisms by which thalassinideans structure macrofaunal communities is the difficulty of categorizing macrofaunal lifestyles (mobility, position in the sediment, etc.) as burrowing makes observational studies tricky, a point raised by both Brenchley (1981) and Posey (1986). It is also difficult to identify the feeding mechanisms of organisms, partly because of the difficulty of observing feeding behaviour, but also because marine invertebrates commonly switch between feeding modes (Reise 1985). Nevertheless, two overall trends appear in studies of thalassinidean-macrofaunal interactions: (1) organisms associated with the sediment surface are negatively affected by thalassinideans, and (2) burrowing deposit-feeding organisms appear unaffected or may even be positively influenced. Pillay et al. (2007b) explained these trends for the specific case of the burrowing sandprawn Callichirus (as Callianassa) kraussi, as summarized in Figure 5, but these mechanisms can be extrapolated to other thalassinideans. The overwhelming majority of studies investigating thalassinidean-macrofaunal relationships have been based on callianassids, with most of their effects originating from their deposition of residual sediment from burrows to the sediment-water interface. As their burrows can extend to depths exceeding 1 m and they can turn over sediment at rates as high as 12 kg m−2 day−1 (Rowden & Jones 1993), this is not surprising. Three possible scenarios may arise from this sediment turnover (Figure 5). Firstly, surface and subsurface fauna may be buried, directly causing mortalities or indirectly leading to metabolic losses due to loss of feeding time or energy spent countering burial. Tube-dwelling, subsurface fauna may be killed by smothering or inhibited by the demands of maintaining burrows. It is also likely that adversely affected organisms may emigrate from heavily bioturbated habitats, potentially increasing their susceptibility to predation in the process. Flach (1993), for instance, demonstrated that burrowing by the lugworm Arenicola marina had no direct effect on the survival of the amphipods Corophium volutator and C. arenarium, but its interference with their tubes led to emigration, and in the process, the amphipods suffered greater mortality due to predation from the crabs and shrimp. Tamaki (1988) similarly showed that bioturbation by Nihonotrypaea harmandi (as Callianassa japonica) increased migration by a mobile polychaete. Secondly, sediment deposition by thalassinideans at the sediment-water interface may negatively influence sediment microbial biofilms, with effects on both adult macrofauna and larval settlers and recruits. In brief, Pillay et al. (2007c) showed that Callichirus (as Callianassa) kraussi retards the growth of surface microalgae and bacteria and consequently reduces the quantities of EPSs they produce. Branch & Pringle (1987) showed a similar effect of this thalassinidean on microalgae and bacteria. As a consequence, organisms such as grazing gastropods and subsurface deposit-feeders that feeding directly on the sediment surface may face a depletion of their food supply in habitats heavily bioturbated by thalassinideans, with resultant metabolic losses and reduction in survival and condition (Ellis et al. 2002, Pillay et al. 2007c). Thirdly, thalassinideans increase erodibility of surface sediments because of their physical manipulation of sediments, accelerating their negative effects on natural biofilms that would otherwise bind sediments (Paterson & Hagerthey 2001, Amaro et al. 2007). Sediments that lack a biofilm and have an uneven topography will in turn increase resistance of water flow over them, leading to turbulent flow and further erosion. For organisms that inhabit surface sediments, this is critical as they will become more prone to being swept into the water column, increasing their exposure 159

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Figure 5 Potential mechanisms for the observed effects of thalassinideans on macrofauna. (Reproduced from Pillay et al. (2007b) with permission from Springer.)

to predators (Flach 1993). This effect is likely to be most severe for small organisms, including larvae and recruits. Potential effects on recruitment are elaborated in the section on adult-juvenile interactions. A secondary outcome of enhanced erodibility of sediments is that resuspended sediments may clog and interfere with the filtration systems of suspension-feeders, as predicted by the trophic amensalism hypothesis (Rhoads & Young 1970). This potential mechanism can also theoretically be extrapolated to subsurface fauna that switch between deposit and filter feeding. Even if suspension-feeders can switch to deposit feeding to counter the effects of highly mobile sediments induced by thalassinidean bioturbation, they will then be likely to suffer reductions in food availability. Thus, sedentary surface and subsurface fauna that are predominantly suspension-feeders, grazers or switchers between deposit and filter feeding may be excluded or negatively affected by thalassinidean bioturbation because (1) species with limited mobility cannot escape sediment disturbance associated with bioturbation, leading to direct mortality (Brenchley 1981); (2) those that are sufficiently mobile can escape smothering but may face reduced food availability because of the scarcity of bacteria, diatoms and EPSs or increased predation as they emigrate; (3) the filtration systems of suspension-feeders may become clogged by expelled sediments (Rhoads and Young 1970); 160


and (4) small organisms may be washed away into the water column because of increased erodibility of sediments. Burrowing infauna are not adversely affected by thalassinidean bioturbation because they do not rely on the sediment surface to feed, their food supply is not reduced, and they are not at risk of being swept away into the water column or being buried by sediments expelled by thalassinideans. Indeed, if anything, they may be promoted by bioturbation because destabilization of the sediment will aid their burrowing activities (Siebert & Branch 2005a,b, 2006, 2007). It needs to be stressed that most studies investigating thalassinidean-macrofaunal interactions have been based on deposit-feeding thalassinideans, with suspension-feeding species underrepresented. Therefore, current perspectives, from a mechanistic point of view, are significantly biased towards the deposit-feeding thalassinideans. In one of the few studies of its kind, Posey et al. (1991) showed that the suspension-feeding mudshrimp Upogebia pugettensis had similar effects on macrofauna to those induced by deposit-feeding thalassinidean Neotrypaea californiensis (Posey 1986), with roughly the same assemblages of sessile polychaetes and crustaceans negatively affected in both cases. This is surprising given the apparent differences in lifestyles and sediment reworking rates between the two thalassinidean species. The possible explanation for the negative effect of Upogebia pugettensis on sessile species is that even the low rate of sediment turnover by this species is sufficient to exclude sessile macrofauna (Posey et al. 1991). Filtration of larvae during suspension feeding could also have been involved, although this mechanism does not fully explain why the negative effect seemed directed specifically at sessile macrofauna. Both mechanisms are unsatisfying, and this particular study raises important questions about the mechanisms by which filter-feeding thalassinideans structure macrofaunal communities and highlights the need for significant clarification in future work.

Adult-juvenile interactions Prior to the work of Pillay et al. (2007c), the majority of studies of thalassinidean-macrofaunal interactions focused on adult stages of macro-invertebrates, skewing perspectives toward adultadult interactions alone, neglecting adult-juvenile interactions and their effects on recruitment and settlement. This was anomalous, given that adult-juvenile interactions in marine ecosystems have been shown for decades to be highly influential in determining adult distributions in both rocky and soft-sediment habitats (Wilson 1955, Gray 1966, Woodin 1976). In linking thalassinidean bioturbation to juvenile processes, Pillay et al. (2007c) provided a novel perspective on the mechanisms by which thalassinideans structure communities. Thalassinideans can substantially influence recruit assemblages by virtue of their sediment turnover to the sediment-water interface. Peterson (1977) showed that elimination of Neotrypaea californiensis resulted in recruitment of the bivalve Sanguinolaria nuttallii, whereas in control areas where the thalassinidean was present, it failed to recruit. Pillay et al. (2007c) demonstrated that sediments in which the thalassinidean Callichirus (as Callianassa) kraussi is naturally absent or rare had densities of macro-invertebrate recruits that were roughly two to four times greater than areas densely populated by C. kraussi. Similar trends were also recorded for recruit richness and diversity. Importantly, the composition of juvenile assemblages in sediments where C. kraussi was rare differed from those in sediments densely populated by C. kraussi. More specifically, juveniles of suspension-feeding taxa such as bivalves and the polychaete Desdemona ornata occurred at higher animal density in sediments where Callichirus kraussi was rare. The same trends emerged from experiments manipulating the density of C. kraussi (Pillay et al. 2007c), increasing confidence that these patterns are attributable to the effects of C. kraussi. One of the major outcomes of the study by Pillay et al. (2007c) was that burrowing thalassinideans can hinder the development of sediment microbial biofilms. Biofilms play key roles in marine sedimentary ecosystems because they (1) bind the topmost sediment layer and promote laminar flow of water over the sediment bed (Paterson & Hagerthey 2001), (2) serve as food sources for adult and 161


juvenile invertebrates (Decho & Lopez 1993), and importantly, (3) provide cues for the settlement and metamorphosis of invertebrate larvae (Gu et al. 1998, Huang & Hadfield 2003). Some research indicates that biofilms can exert a negative influence on the settlement of larvae of particular invertebrates (Wieczorek & Todd 1998, Lau et al. 2003, Dobretsov & Qian 2006), but on the whole, most studies show a promotive effect of biofilms on settlement and metamorphosis (Gu et al. 1998, Hadfield & Paul 2001, Huang & Hadfield 2003). Sediments in which C. kraussi is naturally absent or scarce have been shown to have welldeveloped biofilms, evidenced by the fact that the main components of biofilms (viz. microalgae, bacteria and EPS) are roughly two to four times more abundant in such areas than those with dense populations of C. kraussi (Pillay et al. 2007c). This observation led to the hypothesis that C. kraussi structures macrofaunal communities by modifying biofilms and hence recruitment. Experimental manipulation of sediment biofilms showed that sediments with poorly developed biofilms had recruit densities and richness two to three times less than sediments with well-developed biofilms. Importantly, recruits of suspension-feeders and bivalves were more abundant in biofilmed sediments. The overall picture was that the patterns observed in assemblages of adult macrofauna mirrored the influences of both C. kraussi and biofilms on assemblages of juveniles, leading to the conclusion that C. kraussi structures macrofaunal assemblages partially through its effects on recruitment via its reduction of microbial biofilms. Pillay et al. (2007c) advanced three potential mechanisms by which thalassinideans such as C. kraussi may influence microbial biofilms and recruitment of macrofauna (Figure 6). The first proposes that the high turnover rate of sediment buries larval settlers, bacteria and microalgae, thus preventing their colonization of surface sediments or causing them to lose contact with the water column and become smothered. The second mechanism postulates that sediments expelled by C. kraussi are highly erodible, and that bacteria, diatoms and larvae that settle on the sediment risk being swept away into the water column. The third mechanism is that larvae may preferentially settle at sites of low bioturbation intensities, using microbial biofilms as cue to settlement or using poorly developed biofilms in heavily bioturbated areas as a cue to avoid settlement (Wilson 1955, Gray 1967, Pawlik 1992). The third of these mechanisms is supported by the work of Gray (1967), showing that the distribution of the polychaete Protodrilus rubropharyngeus on sandy beaches is related to the localized presence of biofilms. Gray hypothesized that these biofilms function as settlement cues for larvae of P. rubropharyngeus. Using preference experiments, he showed that when natural sediments were treated with concentrated sulphuric acid, alcohol or formalin or autoclaved to destroy biofilms, the settlement of P. rubropharyngeus larvae was reduced. Isolation of bacteria from natural sediment and their inoculation on to ‘unattractive’ sediment restored larval settlement. Wilson (1955) and Meadows (1964) also showed that bacteria growing on surface sediments stimulate settlement of larvae of the polychaete Ophelia bicornis and of amphipods in the genus Corophium. The hypothesis that the impacts of Callichirus kraussi on microbial biofilms influence recruitment and hence adult assemblages flows from the following lines of reasoning. Firstly, for juveniles to recruit successfully, they must first settle and metamorphose. These processes are often triggered by cues associated with the substratum, which are usually biochemical in nature (Pawlik 1992, Eckman 1996), although other factors play a role, including physical characteristics and the presence or absence of conspecifics and other species. Secondly, the most general sediment-associated settlement cue planktonic larvae are likely to encounter is the presence or absence of microbial biofilms, which are known to influence the settlement of larvae of a number of taxa (Gu et al. 1998, Hadfield & Paul 2001, Huang & Hadfield 2003). Once larvae settle and metamorphose, postsettlement factors such as burial by sediment turnover or loss into the water column due to increased sediment erodibility may then become influential. Therefore, the effect of thalassinideans such as C. kraussi on recruitment of macrofauna is most likely to operate through its influence on settlement, the first step in the successful recruitment of juveniles. Well-developed biofilms associated 162


No C. kraussi

C. kraussi present Planktonic Larvae Selective rejection

Preferential settlement Random settlement Larvae settle and survive due to the stabilising effect of sediment biofilms

Larvae settle on substrate, but are swept into water column, because of sediment erosion Larvae examine substrate, reject it due to poor biofilm coverage, and re-enter plankton

Larvae settle on substrate and metamorphose in response to settlement cues in biofilms

Sediment stable: Larvae not smothered

Sediment Bed

Sediment turned over: Larvae buried

Figure 6 The influence of bioturbation by the southern African sandprawn Callichirus kraussi on sediment microbial biofilms and its effects on recruitment of macrofauna. (Reproduced from Pillay et al. (2007c) with permission from Inter-Research.)

with non-bioturbated sediments may act as a positive settlement cue, while poorly developed biofilms may deter settlement. The three mechanisms postulated by Pillay et al. (2007c) for the effects of C. kraussi on the larvae and recruits of macrofauna are difficult to separate, and it is likely that they will interact. It is also likely that they will be applicable to other thalassinideans that are active bioturbators. Future studies investigating thalassinidean-macrofaunal interactions need to pay more attention to adult-juvenile interactions as they represent a significant gap in knowledge. Indeed, studies of adultjuvenile interactions in relation to thalassinidean effects lag significantly behind studies of other ecosystem engineers in marine soft-sediment and rocky substrata. Linking knowledge of adult-adult interactions with adult-juvenile interactions will be a major step in completing the puzzle surrounding thalassinidean-macrofaunal interactions.

Interactions between thalassinideans and seagrasses Seagrass cover is generally diminished by bioturbation, with a number of bioturbators being influential, including rays and crabs (Townsend & Fonseca 1998) and polychaetes (Reise 1985, Phillipart 163


1994, Luckenbach & Orth 1999). Across the world, seagrasses and bioturbating thalassinideans commonly interact in sheltered soft sediments (Suchanek 1983, Dumbauld & Wyllie-Echeverria 2003, Siebert & Branch 2006, 2007, Berkenbusch et al. 2007, Nacorda 2008). The two groups have contrasting effects on soft-sediment ecosystems and on each other, with the root systems of seagrasses binding the sediment and burrowing by thalassinideans loosening it (Siebert & Branch 2006, 2007, Berkenbusch et al. 2007). Several studies have reported negative effects of bioturbation by burrowing shrimps on seagrasses. In one of the first, Suchanek (1983) showed from field observations that productivity and coverage of the turtle-grass Thalassia testudinum were negatively correlated with mound densities of four species of burrowing shrimp: Glypturus acanthochirus, Corallianassa longiventris, Neocallichirus maryae (as rathbunae) and Eucalliax quadracuta (all as Callianassa spp. in Suchanek’s publication). Growth and survival of Thalassia testudinum were also reduced when it was transplanted into areas with high shrimp densities, suggesting that shrimp bioturbation can exclude T. testudinum. Bioturbation by the Mediterranean ghost shrimp Pestarella (as Callianassa) tyrrhena was shown to increase mortality of the seagrass Posidonia oceanica (Molenaar & Meinesz 1995). When Siebert & Branch (2006) transplanted the seagrass Zostera capensis into sand flats occupied by Callichirus (as Callianassa) kraussi, they found that it survived there provided this sandprawn was eliminated, but not otherwise. In contrast, Bird (2004) did not find any negative effect of thalassinidean bioturbation on the seagrass Heterozostera tasmanica, although design problems render this conclusion tentative. Using the pesticide carbaryl to eliminate the ghost shrimp Neotrypaea californiensis from experimental plots, Dumbauld & Wyllie-Echeverria (2003) also showed a negative effect of thalassinidean bioturbation on the seagrass Zostera japonica. This type of approach deviated from the more traditional method of transplanting seagrass to test its interactions with thalassinideans and relied on colonization by seagrass seeds of experimental plots from which ghost shrimp were removed. It demonstrated that the cumulative proportion of Z. japonica seeds in surface sediments was greater in plots without ghost shrimp. Although no differences were initially detected in emerging seedlings between sediments with and without Neotrypaea californiensis, over time, survival and growth of seedlings were greater in plots lacking ghost shrimps. Some studies have shown two-way antagonistic effects between burrowing thalassinideans and seagrasses. Harrison (1987) reported long-term negative effects of the ghost shrimp N. californiensis on shoot density of the seagrass Zostera japonica, and that during peak recruitment of Z. japonica, population sizes and distribution of Neotrypaea californiensis diminished. Harrison (1987) suggested that because Zostera japonica productivity peaks in spring and that of ghost shrimp occurs in summer, ghost shrimp were outcompeted in spring. In a transcontinental experiment covering New Zealand and the United States, Berkenbusch et al. (2007) also demonstrated that the timing of seagrass growth was important in determining the outcome of interactions between thalassinideans and seagrasses. When Z. japonica was transplanted into areas occupied by the callianassid Neotrypaea californiensis during a spring-summer period in the United States, the seagrass was able to flourish and persist despite bioturbation by N. californiensis. Mound density decreased in response to the presence of seagrasses, indicating a reduction in bioturbation by thalassinideans. In contrast, transplantation of either Biffarius (as Callianassa) filholi into beds of the seagrass Zostera capricorni or vice versa in New Zealand during a summer-winter period resulted in the exclusion of the transplanted organism that is, seagrass shoot density declined when transplanted into beds of Biffarius filholi, and B. filholi density declined when transplanted into seagrass beds. Berkenbusch et al. (2007) argued that since spring is the time of peak growth of Zostera japonica it could overcome the effect of bioturbation by Neotrypaea californiensis during that season. On the other hand, peak biomass and activity of seagrasses and thalassinideans coincided in the summer-winter period in the New Zealand experiment, resulting in the exclusion of whichever species was transplanted. Berkenbusch et al. (2007) pointed out these differences in responses could 164


+

+

+

–

–

+

Figure 7 Effects of thalassinideans and seagrasses on sediment properties and consequences for each other and infaunal assemblages.

simply have been because different species were involved in the two regions. For instance, Zostera japonica is considered to be a ‘superior’ colonizer, and Neotrypaea californiensis an ‘inferior’ bioturbator, reworking sediments at rates that are only 25% of those achieved by Biffarius (as Callianassa) filholi. Siebert & Branch (2006), also using field transplantation experiments, showed that bioturbation by Callichirus (as Callianassa) kraussi can eliminate beds of the eelgrass Zostera capensis, but that the reverse is also true: transplantation of Z. capensis can eliminate Callichirus kraussi, although this effect is relatively short lived, lasting about 4 months. There are many hypothesized mechanisms by which burrowing thalassinideans influence seagrasses (and vice versa), as summarized in Figure 7. Burrowing activities turn over sediments, which can smother seagrasses. Expulsion of fine sediment from burrows adds to this smothering and increases water column turbidity, reducing photosynthetically available radiation and hence seagrass growth (Suchanek 1983). Dumbauld & Wyllie-Echeverria (2003) proposed that sediment reworking by Neotrypaea californiensis buries seeds of Zostera japonica to depths that prevent their sprouting. However, shallow burial of seagrass seeds by species other than thalassinideans may aid seagrass survival by reducing predation (Fishman & Orth 1996), and physical abrasion against sand may enhance sprouting success by incising seed coats (Loques et al. 1990). Conversely, seagrasses may negatively affect burrowing thalassinideans as their root-shoot systems bind the sediment and reduce penetrability, thus hindering burrowing (Siebert & Branch 2006). The nature of seagrass-thalassinidean interactions is, however, dependent on the biology of the species involved. For example, Siebert & Branch (2006) showed strong negative associations between Zostera capensis and the sandprawn Callichirus kraussi but strong positive correlations between the same eelgrass and the mudprawn Upogebia africana. The difference in responses 165


relates to the facts that (1) Callichirus kraussi is a deposit-feeder that turns over sediment far more prodigiously than Upogebia africana, and (2) the latter relies on stable sediment to construct durable U-shaped tubes for filter feeding.

Consequences of thalassinidean-seagrass interactions Seagrasses are important in structuring soft-sediment marine communities and play significant roles in energy transfer between ecosystems (Hemminga & Duarte 2000, Orth et al. 2006, Airoldi et al. 2008, Waycott et al. 2009). Seagrasses can form continuous beds, spanning tens to hundreds of square metres in area, or mosaics of small patches scattered amongst unvegetated sand flats that increase ecosystem heterogeneity and diversity (Hemminga & Duarte 2000). Seagrasses are also ecosystem engineers as their root/rhizome systems stabilize sediments, while their threedimensional leaf canopies modify local hydrodynamics, trapping organic and inorganic nutrients, thus providing nutrient-rich, sheltered habitats for resident biota (Kikuchi & Peres 1977, Hemminga & Duarte 2000, Coleman & Williams 2002, Ward et al. 2003). Seagrasses are also food for megaherbivores, such as manatees, dugongs and turtles, and function as nurseries for many fish and invertebrates (Heck et al. 2003, Orth et al. 2006). All of these features interact in a way that often enhances biomass, richness and abundance of fauna in seagrass beds relative to surrounding bare sand (Hemminga & Duarte 2000, Hughes et al. 2002, Baden et al. 2003). The negative influence of bioturbation by burrowing thalassinideans on seagrasses reduces the ecosystem services provided by these plants, and hence the unique faunal assemblages they support, as evidenced in several transplantation experiments (Angel et al. 2006, Siebert & Branch 2006, 2007, Berkenbusch et al. 2007). Angel et al. (2006) showed that the lower limit of distribution of the eelgrass Zostera capensis in intertidal sand flats is determined by bioturbation by the thalassinidean Callichirus (as Callianassa) kraussi. Beds of Zostera capensis are occupied by the eelgrass limpet Siphonaria compressa, one of South Africa’s most endangered marine invertebrate species. This limpet occurs exclusively on blades of Zostera capensis and is confined to just two localities (Allanson & Herbert 2005). When Angel et al. (2006) transplanted eelgrass lower down into sand flats normally occupied by Callichirus kraussi, the eelgrass flourished only if C. kraussi was experimentally eliminated. Importantly, in such plots, abundance of the eelgrass limpet Siphonaria compressa increased 20-fold relative to control plots of seagrass on the high shore, indicating that its usual restriction to high-shore eelgrass beds confines it to a habitat that is suboptimal. Bioturbation by Callichirus kraussi thus indirectly shifts the distribution of Siphonaria compressa into suboptimal high-shore areas by preventing Zostera capensis from occurring further down the shore. Using field experiments, Siebert & Branch (2006) also showed that bioturbation by Callichirus kraussi negatively affects coverage of Zostera capensis, but that the mudprawn Upogebia capensis becomes more abundant in treatments that contain Zostera capensis. Callichirus kraussi usually occurs predominantly in sandy sediment, whereas Upogebia capensis occurs more commonly in mud. Upogebia capensis requires stable mud to construct the U-shaped tubes it uses for filter feeding, and the root-shoot system of Zostera capensis beds stabilizes sediments and tends to exclude Callichirus kraussi, thus preventing it from undercutting the tubes of Upogebia capensis (Siebert & Branch 2006). Relationships between seagrasses and thalassinideans can also influence the faunal assemblages of soft sediments. Building on the work of Brenchley (1982), Siebert & Branch (2005b, 2007), using both field observations and transplantation experiments, tested the hypothesis that because eelgrass stabilizes sediments, the macrofaunal assemblages in eelgrass beds will be dominated by relatively small, flexible, non-burrowing taxa. Conversely, they hypothesized that assemblages in sandprawn-dominated areas, which are subjected to bioturbation, would predominantly comprise relatively large, inflexible, burrowing taxa. They showed that beds of the eelgrass Zostera capensis and sand flats occupied by Callichirus (as Callianassa) kraussi harbour different macrofaunal assemblages, with species unique to each habitat. However, no evidence emerged that eelgrass beds 166


supported proportionately fewer large or hard-bodied animals than would be expected by chance, contradicting the first two predictions of Brenchley’s hypothesis. The results did, however, support the third prediction, that non-burrowers should be proportionately more abundant in eelgrass beds and burrowers more abundant in areas bioturbated by callianassids. Siebert & Branch (2005b) also demonstrated a significant reduction in burrowing rate of Callichirus kraussi in the presence of seagrass roots, providing empirical evidence that the roots of seagrass hinder burrowing species. Berkenbusch et al. (2007) and Berkenbusch & Rowden (2007) also documented unique macrofaunal assemblages in seagrass beds and sandprawn-dominated sand flats. When they transplanted seagrass plots into sandprawn areas, or vice versa, the communities that developed in the transplanted plots became similar to the respective undisturbed control plots. Taken collectively, these examples therefore constitute strong evidence that seagrass beds and thalassinidean-dominated sand flats support different communities, with burrowing forms disfavoured in the former and favoured in the latter. Engineering of marine soft sediments by both burrowing thalassinideans and seagrasses thus generates antagonistic effects between them via several mechanisms while creating positivefeedback loops that enhance their own survival (Figure 7).

Thalassinideans as pests in mariculture Coastal mariculture operations are multimillion-dollar industries and have been developed in many parts of the world. Penaeid shrimp culture in the Caribbean, for example, was estimated to produce 4314 tons of shrimp valued at US$22.4 million per annum in 1990 (Lemaitre & Rodrigues 1991). There have been reports of the bioturbative activities of thalassinideans having a negative impact on aquaculture operations, leading to these crustaceans being viewed as pests in these operations (Lemaitre & Rodrigues 1991, Dumbauld et al. 1996, 2006, Nates & Felder 1998). Members of the genera Lepidophthalmus, Neotrypaea and Upogebia, for example, negatively influence coastal penaeid shrimp aquaculture in South and Central America (Nates & Felder 1998, Felder 2001) and oyster farming in the United States (Dumbauld et al. 1996, 2006).

Effects on cultured penaeid shrimp The possibility of thalassinideans influencing mariculture was raised when shrimp culture production in the Caribbean declined unexpectedly in 1991, associated with persistent low oxygen levels in pond waters and high numbers of thalassinidean shrimp burrowing in the sediments of artificial culture ponds (Lemaitre & Rodrigues 1991). This fuelled speculation that burrowing thalassinideans were the cause of dwindling shrimp production (Nates & Felder 1998). It is plausible that the artificial pond environments used in shrimp culture operations favour population growth of thalassinideans (Nates & Felder 1998) because (1) pond waters are highly productive due to the artificial feed provided for cultured shrimp; (2) pond sediments are sheltered and protected relative to the natural environments, providing a stable substratum for burrow construction; (3) no predators are present; (4) larval stages of thalassinideans cannot disperse beyond the closed pond environments and (5) thalassinideans can survive periods when the ponds are dried out, by burrowing deeper in sediments (Lemaitre & Rodrigues 1991). These factors lead to greater densities of thalassinideans in culture ponds than are achieved in their natural environments. For upogebiids, only a few natural populations in Europe attain densities equivalent to those reported in culture ponds, and densities of Lepidophthalmus in culture operations far exceed values reported for natural populations (Nates & Felder 1998). There are several mechanisms by which thalassinideans may influence cultured shrimp. Many of these arise from their natural effects on sediment biogeochemical processes that have been highlighted here. Firstly, high densities of burrowing thalassinideans may reduce oxygen availability 167


for the penaeid shrimps farmed in ponds. Secondly, reworking of organic material from prawn feed into sediments by thalassinidean bioturbation, and subsequent decomposition by microbial activity in burrows, will add to oxygen demand and further limit oxygen availability to cultured shrimps (Nates & Felder 1998). Burrowing thalassinideans are renowned for their ability to cope with anoxic sediments (Paterson & Thorne 1995, Atkinson & Taylor 2005). Members of the genus Lepidophthalmus are particularly tolerant of low oxygen levels compared to most other thalassinideans (Thompson & Pritchard 1969, Mukai & Koike 1984, Nates & Felder 1998), with some species capable of anaerobic metabolism and lactate accumulation (Felder 1979, Felder et al. 1995). Thus low-oxygen environments in culture ponds are likely to be more detrimental to cultured penaeid shrimps than to thalassinideans. The third way thalassinideans may affect shrimp culture is through increasing fluxes of organic and nitrogenous compounds from their burrows. This is believed to increase primary production levels in ponds, which increases oxygen demand in confined closed-pond systems. This effect is most severe during the maturation phase of culture, when the cultured prawns reach their greatest biomass and thus have high oxygen requirements (Nates & Felder 1998). Ventilation of burrow waters by thalassinideans, and the associated increase in fluxes of reduced nutrients into pond waters, is the fourth mechanism by which thalassinideans negatively affect cultured shrimps (Nates & Felder 1998). Lepidophthalmus sinuensis, which occurs in dense aggregates in shrimp aquaculture ponds, is much more tolerant of ammonia and nitrite than cultured shrimps (Chen et al. 1990, Chen & Kou 1992, Noor-Hamid et al. 1994, Chen & Lin 1995, Ostrensky & Wasielesky 1995, Nates & Felder 1998). Excessive ammonia and nitrite levels can lead to increased moulting in shrimps, greater metabolic demands, reduced growth rates and greater mortality. In addition, the toxic effects of ammonia are magnified by hypoxic conditions, which is a common feature of culture ponds inhabited by thalassinideans (Merkens & Downing 1957, Nates & Felder 1998). Increased fluxes of sulphides from burrows of thalassinideans into pond waters are also believed to have a negative impact on shrimp growth and production (Nates & Felder 1998). Again, penaeid shrimps are more sensitive to the toxic effects of sulphides than thalassinideans, which further explains the inverse relation observed between thalassinidean and shrimp abundance in aquaculture ponds.

Effects on cultured oysters Burrowing thalassinideans of the genera Neotrypaea and Upogebia are abundant in estuaries on the Pacific coast of North America. Many of these systems are also well suited to oyster aquaculture, and the Pacific oyster Crassostrea gigas was introduced these estuaries in the 1920s for commercial culture (Dumbauld et al. 2001). The burrowing activities of Neotrypaea californiensis and Upogebia pugettensis in particular adversely affect these oyster culture operations, principally because their bioturbation increases turbidity and loosens sediment, causing cultured oysters to sink and become smothered, increasing mortality (Dumbauld et al. 1996, 2006). This is especially problematic for juvenile spat as they are planted on cultch shell, which is buried below the sediment surface together with the attached spat (Dumbauld et al. 1996, 1997, 2001). Of the two species involved, Neotrypaea californiensis is the greater threat. Because it is a deposit-feeder, its burrowing activities are more extensive, and its average turnover of sediment per shrimp is 49.1 g day−1. As a filter-feeder, Upogebia pugettensis has a well-defined mucus-lined burrow, and sediment turnover is only 4.2 g day−1 (Dumbauld et al. 2004). Also related to their respective modes of feeding, Neotrypaea californiensis ventilates its burrows less and digs deeper than Upogebia pugettensis, making it less susceptible to applications of pesticide. Decreasing yields of oysters in North America have been blamed on burrowing thalassinideans since the 1940s (Dumbauld et al. 2006), and the pesticide Carbaryl (1 napthyl-n-methyl carbamate) 168


was applied in the 1960s to control burrowing thalassinideans (Dumbauld et al. 2006 and references cited therein). Carbaryl blocks acetylcholine sterase activity in arthropod synapses, leading to paralysis and death, and has been selected for use because of its effectiveness, low toxicity to mammals, negligible uptake by oysters and absence of bioaccumulation in non-target species (Dumbauld et al. 1996, 2006). In spite of the success of Carbaryl in controlling thalassinidean populations, the practice is controversial because of potentially adverse environmental effects, leading to a ban on its use to control thalassinideans in oyster culture operations in two states in the United States (Dumbauld et al. 2006 and references therein). The adverse effects of thalassinideans on cultured shrimps and oysters all arise from the functions that thalassinideans fulfil in natural soft-sediment ecosystems, including bioturbation of sediments, increasing nutrient flux and oxygen depletion, which in turn are reinforced by bacterial activity in burrows. All these processes are only problematic in artificial culture ponds because (1) conditions favour proliferation of thalassinideans, (2) closed aquaculture systems intensify their effects and (3) the thalassinideans are more tolerant of adverse conditions in ponds, including those they create themselves, than the cultured organisms.

The influence of thalassinidean harvesting on soft-sediment ecosystems Around the world, burrowing thalassinideans are frequently harvested because of their popularity as bait for fishing (Hailstone 1962, Wynberg & Branch 1991, Hodgson et al. 2000a,b, Contessa & Bird 2004, Skilleter et al. 2005, Botter-Carvalho et al. 2007, Chiang et al. 2008, Napier et al. 2009). They are generally collected using handheld prawn pumps or by digging, resulting in significant physical disturbance to the habitat (Contessa & Bird 2004), but the ‘tin-can’ method, in which an inverted tin is plunged downwards over one aperture of upogebiid burrows to expel the prawn, is less destructive. Digging and pumping usually turn over sediments to depths of 30–80 cm, thereby altering physicochemical properties of the sediment. In addition, removal of these ecosystem-engineering thalassinideans will in itself alter soft-sediment ecosystems (Wynberg & Branch 1994, 1997, Contessa & Bird 2004). Indeed, there are several concerns regarding the ecosystem consequences of overexploiting ecosystem engineers such as thalassinideans (Coleman & Williams 2002). In South Africa, Callichirus (= Callianassa) kraussi and Upogebia africana are the main thalassinideans used as bait. Both species can reach densities of 350–400 m−2 in estuaries and lagoons (Hanekom 1980), and concern was raised as long ago as 1967 over the potential ecological consequences of their exploitation (Hill 1967). A parallel situation exists in Australia, where Trypaea (as Callianassa) australiensis is harvested for bait, and concern was raised in 1961 about the sustainability of harvesting (Hailstone & Stephenson 1961).

Effects of harvesting on thalassinidean populations Reductions in densities and sizes of Callichirus major due to harvesting have been reported in South America, where the standing stock is depressed by 10% due to harvesting pressure (Souza & Borzone 2003). Wynberg & Branch (1991) reported from field measurements that the abundance of the sandprawn Callichirus (as Callianassa) kraussi and the mudprawn Upogebia africana were depressed at sites at which harvesting was undertaken, relative to regions of low or no harvesting. There was also evidence that bait collection affected the sizes of Callichirus kraussi, with populations in exploited areas skewed towards smaller individuals, reflecting selective retention of larger individuals by bait collectors. However, potential confounding factors such as water temperature and sediment properties may also have influenced differences in sizes of C. kraussi between exploited and unexploited sites. 169


Subsequent experiments by Wynberg & Branch (1994, 1997) were more conclusive. Experimental plots were either pumped or dug to simulate the effect of harvesting, and abundances of C. kraussi and Upogebia africana were compared between such harvested plots and unmanipulated control sites (Wynberg & Branch 1994). Harvesting depleted stocks of C. kraussi sharply relative to controls, and recovery to densities approaching control levels took at least 18 months. Densities of Upogebia africana were similarly depleted by harvesting, but recovery to control levels took only 4 months (Wynberg & Branch 1994). In a subsequent experiment on Callichirus (as Callianassa) kraussi, plots were pumped at three levels of intensity, but pumped prawns were returned to plots. Another set of plots was trampled only, at levels corresponding to those in pumped plots (Wynberg & Branch 1997). In all cases, numbers of C. kraussi were reduced relative to unmanipulated controls, but pumped and trampled plots were statistically indistinguishable, indicating that trampling has as much of an impact on the sandprawn populations as removal coupled with trampling. This is probably because trampling causes burrows of C. kraussi to collapse, thereby compacting sediments and reducing natural bioturbationinduced oxygenation. Experiments in Australia revealed important effects of harvesting on the abundance of Trypaea (as Callianassa) australiensis (Contessa & Bird 2004). A BACI (before-after, control-impact) design was used in this experiment and was intended to separate the effects of shrimp removal from harvesting disturbance. After harvesting, densities of T. australiensis declined significantly, and while an estimated 10% of thalassinideans was removed via pumping, an additional reduction of 20% was ascribed to the deleterious effects of physical trampling during harvesting, including sediment compaction and burrow destruction. Trampling therefore accounted for twice the mortality attributed to removal of sandprawns. Contessa & Bird (2004) also demonstrated that numbers of T. australiensis remaining after harvesting could not be statistically differentiated between pumped and trampled plots, corroborating the assertions of Wynberg & Branch (1997) that trampling during harvesting causes at least as much impact as removal.

Effects of harvesting on sediment geochemistry Thalassinidean harvesting can have a range of side effects on both the physical environment and other biota, either through physical disturbance or by reducing the ecosystem services provided by thalassinideans. These organisms are renowned for their ability to oxygenate sediments, and their depletion reduces sediment oxygen levels. Wynberg & Branch (1994) reported the appearance of a dark sulphide layer 3 cm below the surface after experimental harvesting of thalassinideans, whereas unmanipulated control plots were characterized by uniformly lighted-coloured sediment down to depths of 50–60 cm. Based on measurements of redox potential (Eh), Contessa & Bird (2004) demonstrated similar reductions in sediment oxygen levels following experimental harvesting of T. australiensis. Where T. australiensis had been removed, Eh levels 5 cm deep were similar to those at a depth of 15 cm in sediments that contained T. australiensis. There are therefore clear indications that the redox potential discontinuity (RPD) shifts upwards if thalassinidean numbers are depleted by harvesting (Contessa & Bird 2004), probably because of the elimination of pumping activities by thalassinideans and the compaction of sediments by trampling during harvesting. Harvesting and associated trampling have strong influences on sediment topography. Harvested areas become depressed and sink below normal sediment levels, partly because of compaction due to trampling but also because of a reduction in turnover of sediments by thalassinideans, which maintains sediment in a ‘loose’ state with a high water content. Wynberg & Branch (1994) also recorded changes in granulometry associated with harvesting. When Callichirus kraussi was harvested, sediments became finer, but when Upogebia africana was harvested, sediments became coarser. Increased proportions of fine sediments were also recorded following harvesting of Trypaea australiensis and persisted for at least 3 months (Contessa & Bird 2004). 170


Sediments from which Callichirus kraussi had been removed became less porous and more compact, but this was not the case following harvesting of Upogebia africana (Wynberg & Branch 1994). This difference is probably related to differences in the sediments where these species occur, as well as differences in burrowing behaviour, with U. africana occurring in naturally compacted mud, whereas Callichirus kraussi is a far more vigorous bioturbator (Branch & Pringle 1987) and occurs predominantly in naturally porous sands. Contessa & Bird (2004) also reported a decrease in sediment porosity following harvesting of the callianassid Trypaea australiensis, which remained evident 3 months after harvesting ceased. Harvesting of Callichirus kraussi also resulted in a decrease in sediment organic content after 18 days, but this trend later reversed, and for up to 4 months, organic content remained greater in harvested plots than in controls. No differences in organic content were recorded between control plots and those in which Upogebia africana was harvested (Wynberg & Branch 1994).

Effects of harvesting on benthic communities Harvesting thalassinideans has complex effects on benthic communities, as highlighted in the early work of Wynberg & Branch (1994) involving experimental removal of Callichirus kraussi, which is a deposit-feeder, and Upogebia africana, a filter-feeder. Differences in the consequences of removing these species would therefore be expected on the grounds of their having different modes of feeding involving quite different rates of sediment turnover. However, experiments of this nature inevitably confound two effects—the removal of prawns per se and the inadvertent but unavoidable disturbance of sediments involved in the process—so the outcomes need to be viewed in this light. One month after experimental harvesting of Callichirus kraussi, chl-a levels increased in harvested plots relative to controls and remained elevated for 4 months (Wynberg & Branch 1994). Contessa & Bird (2004) recorded increases in chl-a levels following harvesting of Trypaea australiensis, which persisted for roughly 3 months. The elevation in chl-a following experimental harvesting of Callichirus kraussi and Trypaea australiensis is probably due to alleviation of the deleterious effects of sediment turnover by these deposit-feeding thalassinideans on benthic microflora and are consistent with other studies reporting negative effects of callianassids on microalgae (Branch & Pringle 1987, Pillay et al. 2007a,b,c). In contrast, in areas where the filter-feeding Upogebia africana was harvested, chl-a concentrations declined relative to control plots, and this situation persisted for 18 months (Wynberg & Branch 1994). Experimental removal of Callichirus kraussi by Wynberg & Branch (1994) did not appear to affect bacterial density, but removal of Upogebia africana caused an initial spike in bacterial densities and then declined relative to controls and remained depressed after 4 months. The physical disturbance associated with bait collecting can also have side effects on co-occurring meiofaunal and macrofaunal invertebrate communities (Wynberg & Branch 1994, 1997, Contessa & Bird 2004). Experimental harvesting of Callichirus kraussi initially led to fluctuations in meiofaunal abundance, but after 2 months the numbers of nematodes, copepods and juvenile polychaetes were depressed and remained so for at least 18 months, whereas turbellarians were positively influenced by harvesting and returned to control levels after 9 months (Wynberg & Branch 1994). Harvesting of Upogebia africana also resulted in a depression of meiofauna numbers. Both outcomes were unexpected, given that thalassinideans generally have negative effects on meiofauna. Wynberg & Branch (1991) showed that 9 of 13 macrofaunal species sampled showed significant reductions in biomass due to incidental turnover of sediment associated with pumping for Callichirus kraussi and subsequent predation by scavenging birds, which appears to be a common phenomenon associated with thalassinidean harvesting (Wynberg & Branch 1991 and references cited therein). It was estimated that an average of 54 g of macrofauna are incidentally turned over by each bait collector during collection of a daily quota, resulting in disturbance of a total of 1300 kg 171


of macrofauna per year, of which 80% is preyed on by birds. Macrofauna may also be affected by mechanical damage and sediment instability during pumping. Further experimental manipulations by Wynberg & Branch (1994) also demonstrated strong effects of thalassinidean harvesting on macrofauna. Recovery times of macrofauna were predictably much greater than those of meiofauna, a finding consistent with other studies examining disturbance effects on these groups (Bell & Woodin 1984). Responses of macrofauna could be separated into three categories: (1) taxa that were unaffected by harvesting, (2) those that were immediately affected and showed a slow recovery and (3) those that had a delayed response. Taxa that were most sensitive to harvesting disturbance were sessile, shallow-dwelling tube builders, which took roughly 9 months to recover. Of all macrofaunal taxa documented, only the hermit crab Diogenes brevirostris was positively affected by thalassinidean harvesting. It aggregated in the depressions created by harvesting and may have taken advantage of increased availability of detritus and microalgae in these depressions (Wynberg & Branch 1994). Similar aggregation in depressions in areas lacking thalassinideans has also been recorded by Walters & Griffiths (1987). The abundance of D. brevirostris declined after 18 months, coincidental with a flattening of harvesting depressions and a recovery of Callichirus kraussi (Wynberg & Branch 1994). In contrast to other studies examining the effects of thalassinidean harvesting on macrofauna, Skilleter et al. (2005) recorded far less of an impact, with the effects subtle and localized. In this case, the abundance of polychaetes, bivalves and gammarid amphipods was more patchy at sites where intense harvesting took place relative to reference sites where harvesting was less severe. One of the major outcomes of studies examining the effects of thalassinideans harvesting on soft-sediment ecosystems is that physical disturbance such as trampling during bait collecting can have as much of an effect as the removal of thalassinideans (Wynberg & Branch 1997, Contessa & Bird 2004). Trampling collapses thalassinidean burrows and compacts sediments, leading to sediment anoxia, low sediment porosity and ‘deflation’ of the sediment surface, and can significantly influence sediment oxygenation, granulometry and organic content, microalgal biomass and invertebrate assemblages (Wynberg & Branch 1997, Contessa & Bird 2004). Three patterns emerge after harvesting of thalassinideans. Firstly, provided harvesting is not maintained, recovery is relatively quick, never exceeding 18 months. Secondly, the effects are attributable more to the physical disruption of sediments by harvesting and associated trampling than to the removal of thalassinideans per se. Thirdly, harvesting profoundly alters all elements of communities via sediment disturbance, increased predation, anoxia and other secondary effects related to the removal of thalassinideans.

Bioturbators as drivers of evolutionary change in soft sediments The emergence of the concept of ecosystem engineers has played an important role in developing ecological theory (Jones et al. 1994), and its application to burrowing thalassinideans has changed perspectives on the ecological processes associated with these organisms. However, thalassinideans, like most ecosystem engineers, have effects that go beyond ecosystem engineering alone; they affect their own evolution as well as that of other co-inhabiting species (Odling-Smee et al. 2003, Pillay 2010). Many ecosystem engineers produce constructions such as burrows, tubes, tunnels or nests, and in the process they define, create and modify their own niches and those of other species (Odling-Smee et al. 1996), influencing the selective pressures that operate on future generations of their own and other co-inhabiting species. This concept is referred to as ‘niche construction’ (Odling-Smee et al. 2003, Laland et al. 2004). 172


Burrowing thalassinideans are prime examples of organisms that modify their ecosystems, through either their physical constructions or their activities, yet their influence on the evolution of other species has been neglected, as is the case with most other bioturbators (Pillay 2010). Significant advances, however, have been made over the last decade, with the role of bioturbation in evolutionary change, especially its postulated link to the Cambrian explosion, generating particular interest. However, this macro-evolutionary link only partially addresses the influence of bioturbators on evolutionary change. At the micro-evolutionary scale, bioturbators can play direct or indirect roles in the evolution of unique morphologies, behaviour and social interactions. Such effects of bioturbating organisms are missing in current thinking but need to be incorporated to reveal their full sphere of influence (Pillay 2010), and the situation surrounding thalassinidean bioturbators is no different. This section highlights the role of bioturbators in general as drivers of micro-evolutionary change in soft-sediment ecosystems. Many of the specific examples involve thalassinideans, thus providing a link between the ecological roles of this group as ecosystem engineers and their influence as agents of evolutionary selection.

The role of bioturbation in macro-evolutionary change The effect of bioturbation at a macro-evolutionary level has specifically been invoked in the context of the ‘Cambrian explosion’ (Meysman et al. 2006). The basic body plans of metazoan life were still evolving between the late Neoproterozoic and early Phanerozoic periods (Bottjer et al. 2000), and two processes are hypothesized to be crucial in the later evolution of metazoan form. The first was the development of predation, which acted in combination with other biological and geological processes to promote the development of biomineralized exoskeletons (Vermeij 1989). The second factor was the advent of bioturbation, the disruption of sediments by burrowing organisms (Droser & Bottjer 1989, Dzik 1994, 2003, Meysman et al. 2006). This was so influential in transforming the early seafloor and metazoan life that it has been termed the ‘agronomic revolution’ (Seilacher & Pflüger 1994). Geological evidence indicates that marine sediments in the Neoproterozoic were coated by well-developed microbial mats, with little or no evidence for bioturbation-induced mixing of the sediment. During this period, sediments below microbial mats had low water content, and the sediment-water interface was distinct and well defined. By the Cambrian period, the evolution of burrowing metazoan species led to the breakdown of these microbial mats, resulting in greater water penetration into the sediment and a comparatively poorly defined sediment-water interface. Microbial mat food sources were uniformly dispersed in the sediment because of bioturbation, in contrast to the previously well-layered distribution characteristic of mat-covered sediments (Bottjer et al. 2000). The changes to the sediment fabric induced by bioturbation, and their subsequent effect on metazoan extinction and evolution, is referred to as the ‘Cambrian substrate revolution’ (Bottjer & Hagedorn 1999), summarized in Figure 8. Seilacher (1999) indicated that the organisms associated with microbial mats were species that (1) encrusted mats, (2) grazed on mats without destroying them, (3) attached to mats and relied on filter feeding, or (4) fed on decaying material beneath mats. One such mat feeder, a type of mat-sticking helicoplacoid echinoderm, was relatively immobile/ sessile and well adapted to ‘mat lifestyles’ of the Neoproterozoic. Increases in bioturbation through the Cambrian, however, and the associated instability imposed on sediments, probably led to the extinction of these organisms (Dornbos & Bottjer 2000). Also associated with increases in bioturbation was the evolution of early Cambrian edrioasteroids and eocrinoids. Both groups lived unattached to sediment mats in the early Cambrian, but by the late Cambrian, edrioasteroids had become attached to hard substrata, and eocrinoids evolved stems that anchored them to hard substrata. Bioturbation probably drove both changes as sediment instability most likely led to the shift 173

DEENA PILLAY & GEORGE M. BRANCH Q

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Figure 8 Hypothesized effect of bioturbation on Precambrian and Cambrian life on the seafloor. The dashed line indicates the redox potential discontinuity. (A) Inaria, (B) Parvancorina, (C) Dickinsonia, (D) Tribrachidium, (E) Charnia, (F) Spriggina, (G) archaeocynathid, (H) mollusc, (I) Ottoia, (J) Anomalocaris, (K) Skolithos, (L) trilobite, (M) Burgessochaeta, (N) Opabinia, (O) diplocraterian, (P) Wiwaxia, (Q) crinoid. (Drawing courtesy of Kelly Vlieghe.)

to hard substrata and the development of stalks in eocrinoids, which elevated them above the bioturbation zone (Bottjer et al. 2000).

The influence of bioturbation on micro-evolutionary change The role of burrowing organisms in the Cambrian explosion is the most established link between bioturbation and evolution, but perspectives on bioturbators need to incorporate their microevolutionary effects. Hansell (1993) hypothesized that burrows in terrestrial ecosystems led to several evolutionary changes in co-occurring species. Burrows offer greater security than surrounding habitats, promoting long-term occupation and increases in social complexity and colony sizes. Specialization of burrow architecture and the development of food storage behaviour favour microhabitat diversification and control of resources around burrows. These effects, in turn, lead to the radiation of species in or around burrows (Hansell 1993, Eisenberg & Kinlaw 1999, Hafner et al. 2000). Given the similarity in ecological functions provided by burrows in both terrestrial and marine ecosystems, it is likely that the hypothesized effects of terrestrial burrowing organisms on the evolution of co-inhabiting species are equally applicable to marine burrowers. The construction of burrows in marine sediments offers several advantages to organisms (Bromley 1996). Firstly, they may allow avoidance of dangers associated with life above the sediment, such as predators, turbulence and periodic exposure during low tides. When burrowing organisms turn over sediment at rapid rates, as is the case with callianassids, burrows may provide a

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refuge for co-occurring species from the adverse effects of sediment turnover. Secondly, water can be circulated relatively easily through burrows without much energy expenditure, making ventilation of the gills and respiratory surfaces comparatively easy, offering an elegant solution to the problem of sediment anoxia. Currents generated in burrows can also be used to aid filter feeding, and burrows may protect the bodies of deposit-feeders that employ specialized appendages to collect organic matter on the sediment surface. Lastly, burrows may allow concentration of organic material and facilitate ‘gardening’ of microbes, enhancing food supplies (Bromley 1996). Given these functions, burrows in marine soft sediments have been described as “elite structures” (Bromley 1996) and attract co-inhabitants from both the pelagic and sedimentary realms, often leading to shared use of burrows. The result is the speciation of burrow associates or symbionts, with varying dependence on hosts and their burrows. Evidence of this is scattered through the literature, often in natural history journals. Species that are completely dependent on hosts and burrows (obligate symbionts) show radical changes in morphology and behaviour, while less-dependent species (facultative symbionts) exhibit more subtle changes. Also evident is the evolution of complex social interactions between hosts and burrow associates as host dependence increases. The influence of thalassinideans specifically on micro-evolutionary change has generally not been intensively or quantitatively pursued in the literature. Most of the work is documented in taxonomic descriptions of symbiotic species that share burrows of thalassinideans and is conspicuously absent from mainstream work on thalassinidean bioturbation. Nevertheless, when the scattered literature is drawn together, burrow symbionts occurring with thalassinidean crustaceans have been well documented (MacGinitie 1934, Itani 2004, Santagata 2004, Atkinson & Taylor 2005, Anker et al. 2006). At least 10 species of alpheid crustaceans are known burrow commensals of thalassinideans spread across the Callianassidae, Upogebiidae and Laomediidae (Anker et al. 2006). Two pinnotherid crabs, Scleroplax granulata and Pinnixa fransiscana, occur in burrows of callianassids and upogebiids (MacGinitie 1934). The bivalve Phacoides pectinata is a burrow associate of Axianassa australis. A polynoid polychaete Harmothoe sp. is commensal with Neotrypaea (= Callianassa) californiensis: juveniles of Harmothoe lie epizoically across the abdomen of ovigerous callianassid females, while the adults live freely in burrows (MacGinitie 1934). It is not the aim of this section to review the symbionts harboured by thalassinideans but rather to comment on the role of thalassinideans in driving micro-evolutionary change, specifically from the perspective of adaptations of morphology, behaviour and social interactions. The association between the blind goby Typhlogobius californiensis and the burrowing shrimp Neotrypaea biffari (as Callianassa affinis) is a prime example of thalassinideans acting as agents of selection in the evolution of novel morphologies in co-inhabiting species (MacGinitie 1939). Typhlogobius californiensis occupies the deeper and darker portions of the burrows of N. biffari and exhibits little activity. Newly hatched gobies have fully developed eyes, but as they grow, their retinas change shape, become withdrawn and are covered by body layers, giving the gobies their eyeless appearance. The gobies cannot burrow by themselves and rely on their hosts to generate currents to bring in food; they are entirely dependent on N. biffari (MacGinitie 1939). Another goby, Gillichthys mirabilis, which is a burrow associate of various species of Upogebia, also has small eyes relative to free-living gobies and seeks out the darker, deeper portions of burrows. MacGinitie (1939, p 492) suggested that Gillichthys mirabilis is “another step to the condition exemplified by Typhlogobius, where the fish remains permanently in the burrow of a particular host”. Another possible example of burrowing thalassinideans influencing the evolution of cooccurring species is provided by Spiroplax (=Thaumastoplax) spiralis (Figure 9), which occurs commensally with Callichirus (as Callianassa) kraussi and Upogebia africana (Branch et al. 2010). It is commonly referred to as the ‘six-legged crab’, being unique in having only six walking legs, whereas most other crabs possess eight. This crab, like most other burrow commensals, is unable

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Figure 9 Dorsal view of the commensal ‘six-legged crab’ Spiroplax spiralis. (Photo: G.M. Branch.)

to burrow by itself, and when it occupies burrows of thalassinideans, it lies flattened against the burrow wall out of the path of the burrow host. It is unclear what factor was responsible for the evolutionary loss of a pair of walking legs, but it may be linked to its commensal nature. An example of burrowing species inducing behavioural changes in burrow associates is provided by the clam Cryptomya californica, which occurs commensally with burrowing thalassinideans and an echiurid worm (MacGinitie 1934). This bivalve is a filter-feeder, but rather than filtering the water column directly, it feeds by inserting its siphons into the burrow of the host, making use of water currents generated by its host (MacGinitie 1934). This has allowed C. californica to live at depths greater than those permitted by the length of its siphons, thereby reducing predation and the frequency with which its siphons are cropped. The bivalve Peregrinamor ohshimai is another example of the evolution of novel behaviour induced by its association with burrowing thalassinideans. Peregrinamor ohshimai is an ectosymbiont associated with six species of Upogebia and Austinogebia narutensis, all of which are filterfeeding thalassinideans. Peregrinamor ohshimai attaches by byssal threads to the ventral surface of the cephalothorax of its thalassinidean hosts, at the base of the second and fourth periopods (Kato & Itani 1995). Its siphons extend into the filtration basket of its host and are used to filter organic material from water currents created by the host. It is intriguing to note that P. ohshimai does not appear to occur with deposit-feeding thalassinideans, suggesting that the selection pressure driving the symbiotic relationship was most likely energy saved from not having to generate its own water currents for filter feeding. The presence of burrow symbionts may also lead to the evolution of novel behaviour by the host. This is evident in the relationship between the goby Typhlogobius californiensis and Neotrypaea biffari (as Callianassa affinis). Typhlogobius californiensis usually feeds on pieces of organic material that enter the burrows of N. biffari but are too large for the host to ingest. On occasion, though, N. biffari may actually collect large pieces of organic debris and ‘dump’ them in front of Typhlogobius californiensis, presumably for consumption (MacGinitie 1939). Although this behaviour needs to be quantified to evaluate its importance, it appears to be an evolved cooperative behaviour that prevents the accumulation of organic debris in the burrow, possibly avoiding localized oxygen depletion through microbial decomposition. 176


Many burrowing species in marine ecosystems display complex social interactions with other burrow associates. The best-known example is the evolution of warning relationships, by which the burrow associate signals inherent danger to the host. Shrimp-goby mutualism is a clear example of such a ‘warning’ association and has been recorded in many parts of the world. Several alpheid shrimps create burrows in sand that are inhabited by gobies that are unable to burrow for themselves but secure protection in the alpheid burrows (Karplus 1987). The gobies in turn act as scouts, signalling to the host the presence of danger in the form of predators or other burrow intruders. A system of interspecific communication must evolve for the relationship to work. This involves rapid flicking of the tail by gobies to signal alarm, and the shrimps place their antennae on the bodies of gobies to receive this signal (Karplus 1987). A similar warning association seems to exist in the relationship between the alpheid shrimp Betaeus jucundus and Callichirus kraussi (D. Pillay personal observation), in which Betaeus jucundus moves up and own the burrow shaft of Callichirus kraussi, often peering out of the burrow opening. This section of the review demonstrates three points. Firstly, intricate associations between burrowing thalassinideans and burrow associates are abundant in the literature. Secondly, many of these accounts are descriptive natural history observations that need quantification and critical evaluation to fully appreciate their evolutionary significance. Thirdly, there is a need to advance recognition of the evolutionary role of bioturbators such as thalassinideans to the level already accorded to their ecological roles to reveal the full importance of thalassinideans in marine softsediment ecosystems.

Conclusion This review has drawn attention to the importance of thalassinideans as ecosystem engineers in marine soft-sediment ecosystems and how they influence a number of important ecological processes in these habitats. There are, however, major gaps in knowledge, and significant opportunities exist for future research to provide new insights into the roles of thalassinideans as ecosystem engineers. Current knowledge in this regard is restricted to relatively few species, with studies of the Callianassidae and Upogebiidae generally dominating (Felder 2001). Given the subtle differences in biology of individual species, it is likely that each species influences soft-sediment ecosystems in different ways. To fully appreciate the effects of thalassinideans in bioengineering marine softsediment systems, further studies on the lesser-known groups are vital. In terms of impacts on soft-sediment community structure, studies of the deposit-feeding thalassinideans dominate, with few studies on the effects of suspension-feeding groups such as the Upogebiidae. To our knowledge, only two studies reported on the effects of filter-feeding thalassinideans on soft-bottom community structure (Brenchley 1981, Posey et al. 1991). Most studies have focused on physical ecosystem engineering in the form of sediment turnover and the consequences for co-occurring communities, but questions remain about the possibility that suspension-feeding thalassinideans structure communities by filtering out larval invertebrates or propagules. Nevertheless, the existing literature does indicate that the sphere of influence of burrowing thalassinideans is enormous (Figure 10), although the nature of their impacts is highly dependent on the biology of the individual species. The prodigious bioturbation caused by thalassinideans transforms the physical properties of marine sediments, fully justifying their classification as ecosystem engineers. In the process, they strongly influence the community composition of associated microorganisms, meiofauna, macrofauna and micro- and macroflora. The conditions they create are likely to have evolutionary consequences, ranging from adaptations of individual species to the functioning of entire ecosystems. Recognition of the far-reaching effects on these processes has transformed our appreciation of thalassinideans in marine soft-bottom ecosystems. 177


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Acknowledgements We are extremely grateful to Professor R.J.A. Atkinson for his useful comments on the manuscript, particularly his assistance with the taxonomy of the Thalassinidea. We are also grateful to the National Research Foundation (NRF) and the Andrew Mellon Foundation for financial support.

References Abed-Navandi, D. & Dworschak, P.C. 2005. Food sources of tropical thalassinidean shrimps: a stable-isotope study. Marine Ecology Progress Series 291, 159–168. Abed-Navandi, D., Koller, H. & Dworschak, P.C. 2005. Nutritional ecology of thalassinidean shrimps constructing burrows with debris chambers: the distribution and use of macronutrients and micronutrients. Marine Biology Research 1, 202–215. Abrunhosa, F.A., Pires, M.A.B., Lima, J.F. & Coelho-Filho, P.A. 2005. Larval development of Lepidophthalmus siriboia Felder and Rodrigues, 1993 (Decapoda: Thalassinidea) from the Amazon region, reared in the laboratory. Acta Amazonica 35, 77–84. Abu-Hilal, A., Badran, M. & de Vaugelas, J. 1988. Distribution of trace elements in Callichirus laurae burrows and nearby sediments in the Gulf of Aqaba, Jordan (Red Sea). Marine Environmental Research 25, 233–248. Airoldi, L., Balata, D. & Beck, M.W. 2008. The Gray Zone: relationships between habitat loss and marine diversity and their applications in conservation. Journal of Experimental Marine Biology and Ecology 366, 8–15. Allanson, B. & Herbert, D.G. 2005. A newly discovered population of the critically endangered false limpet Siphonaria compressa Allanson, 1958 (Pulmonata: Siphonariidae), with observations on its reproductive biology. South African Journal of Science 101, 95–97. 178

BIOENGINEERING EFFECTS OF BURROWING THALASSINIDEAN SHRIMPS Allanson, B.R., Skinner, D. & Imberger, J. 1992. Flow in prawn burrows. Estuarine Coastal Shelf Science 35, 253–266. Aller, J.Y. & Aller, R.C. 1986. Evidence for localized enhancement of biological activity associated with tube and burrow structures in deep-sea sediments at the HEBBLE site, western North Atlantic. Deep-Sea Research 33, 755–790. Aller, R.C. 1988. Benthic fauna and biogeochemical processes in marine sediment: the role of burrow structures. In Nitrogen Cycling in Coastal Marine Environments, T.H. Blackburn & J. Sorensen (eds). New York: Wiley, 301–338. Aller, R.C. & Dodge, R.E. 1974. Animal-sediment relations in a tropical lagoon Discovery Bay, Jamaica. Journal of Marine Research 32, 209–232. Aller, R.C. & Yingst, J.Y. 1978. Biogeochemistry of tube-dwellings: a study of the sedentary polychaete Amphitrite ornata (Leidy). Journal of Marine Research 36, 201–254. Aller, R.C. & Yingst, J.Y. 1985. Effects of the marine deposit feeders Heteromastus filiformis (Polychaeta), Macoma balthica (Bivalvia), and Tellina texana (Bivalvia) on averaged sedimentary solute transport, reaction rates, and microbial distributions. Journal of Marine Research 43, 615–645. Aller, R.C., Yingst, J.Y. & Ullman, W.J. 1983. Comparative biogeochemistry of water in intertidal Onuphis (Polychaeta) and Upogebia (Crustacea) burrows: temporal patterns and causes. Journal of Marine Research 41, 571–604. Alongi, D.M. 1985. Effect of physical disturbance on population dynamics and trophic interactions among microbes and meiofauna. Journal of Marine Research 43, 351–364. Amaro, T.P.F., Duineveld, G.C.A., Bergman, M.J.N., Witbaard, R. & Scheffer, M. 2007. The consequences of changes in abundance of Callianassa subterranea and Amphiura filiformis on sediment erosion at the Frisian Front (south-eastern North Sea). Hydrobiologia 589, 273–285. Anderson, S.J., Atkinson, R.J.A. & Taylor, A.C. 1991. Behavioural and respiratory adaptations of the mudburrowing shrimp Calocaris macandreae Bell (Thalassinidea: Crustacea) to the burrow environment. Ophelia 34, 143–156. Anderson, S.J., Taylor, A.C. & Atkinson, R.J.A. 1994. Anaerobic metabolism during anoxia in the burrowing shrimp Calocaris macandreae Bell (Crustacea: Thalassinidea). Comparative Biochemistry and Physiology 108A, 515–522. Angel, A., Branch, G.M., Wanless, R.M. & Siebert, T. 2006. Causes of rarity and range restriction of an endangered, endemic limpet, Siphonaria compressa. Journal of Experimental Marine Biology and Ecology 330, 245–260. Anker, A., Vera Caripe, J.A. & Lira, C. 2006. Description of a new species of commensal alpheid shrimp (Crustacea, Decapoda) from the southern Caribbean Sea. Zoosystema 28, 683–702. Astall, C.M., Anderson, S.J., Taylor, A.C. & Atkinson, R.J.A. 1997a. Comparative studies of the branchial morphology, gill area and gill ultrastructure of some thalassinidean mud-shrimps (Crustacea: Decapoda: Thalassinidea). Journal of Zoology (London) 241, 665–688. Astall, C.M., Taylor, A.C. & Atkinson, R.J.A. 1997b. Behavioural and physiological implications of a burrow-dwelling lifestyle for two species of upogebiid mud-shrimp (Crustacea: Thalassinidea). Estuarine Coastal and Shelf Science 44, 155–168. Atkinson, R.J.A. & Taylor, A.C. 2004. Aspects of the biology and ecophysiology of thalassinidean shrimps in relation to their burrow environment. In Proceedings of the Symposium on Ecology of Large Bioturbators in Tidal Flats and Shallow Sublittoral Sediments—From Individual Behaviour to Their Role as Ecosystem Engineers, A. Tamaki (ed.). Nagasaki: Nagasaki University, 45–51. Atkinson, R.J.A. & Taylor, A.C. 2005. Aspects of the physiology, biology and ecology of thalassinidean shrimps in relation to their burrow environment. Oceanography and Marine Biology An Annual Review 43, 173–210. Baden, S., Gullström, M., Lundén, B., Pihl, L. & Rosenberg, R. 2003. Vanishing seagrass (Zostera marina, L.) in Swedish coastal waters. Ambio 32, 374–377. Bell, S.S. 1980. Meiofauna-macrofauna interactions in a high salt marsh habitat. Ecological Monographs 50, 487–505. Bell, S.S. & Woodin, S.A. 1984. Community unity: experimental evidence for meiofauna and macrofauna. Journal of Marine Research 42, 605–632. Berkenbusch, K. & Rowden, A.A. 1999. Factors influencing sediment turnover by the burrowing ghost shrimp Callianassa filholi (Decapoda: Thalassinidea). Journal of Experimental Marine Biology and Ecology 238, 283–292. 179

DEENA PILLAY & GEORGE M. BRANCH Berkenbusch, K. & Rowden, A.A. 2000. Intraspecific burrow plasticity on an intertidal population of Calianassa filholi (Crustacea: Decapoda: Thalassinidea) in relation to environmental conditions. New Zealand Journal of Marine and Freshwater Research 34, 397–408. Berkenbusch, K. & Rowden, A.A. 2003. Ecosystem engineering—moving away from ‘just-so’ stories. New Zealand Journal of Ecology 27, 67–73. Berkenbusch, K. & Rowden, A.A. 2007. An examination of the spatial and temporal generality of the influence of ecosystem engineers on the composition of associated assemblages. Aquatic Ecology 41, 129–147. Berkenbusch, K., Rowden, A.A. & Myers, T.E. 2007. Interactions between seagrasses and burrowing ghost shrimps and their influence on infaunal assemblages. Journal of Experimental Marine Biology and Ecology 341, 70–84. Berkenbusch, K., Rowden, A.A. & Probert, P.K. 2000. Temporal and spatial variation in macrofauna community composition imposed by ghost shrimp Callianassa filholi bioturbation. Marine Ecology Progress Series 192, 249–257. Bird, E.M. 1982. Population dynamics of thalassinidean shrimps and community effects through sediment modification. PhD thesis, University of Maryland, College Park, Maryland. Bird, F.L. 2004. The interaction between ghost shrimp activity and seagrass restoration. In Proceedings of the Symposium on Ecology of Large Bioturbators in Tidal Flats and Shallow Sublittoral Sediments— From Individual Behaviour to Their Role as Ecosystem Engineers, A. Tamaki (ed.). Nagasaki: Nagasaki University, 71–75. Bird, F.L., Boon, P.I. & Nichols, P.D. 2000. Physicochemical and microbial properties of burrows of the deposit-feeding thalassinidean ghost shrimp Biffarius arenosus (Decapoda: Callianassidae). Estuarine Coastal Shelf Science 51, 279–291. Blackburn, T.H. & Henrikson, K. 1983. Nitrogen cycling in different types of sediments from Danish waters. Limnology and Oceanography 28, 477–493. Botter-Carvalho, M.L., Santos, P.J.P. & Carvalho, P.V.V.C. 2007. Population dynamics of Callichirus major (Say, 1818) (Crustacea, Thalassinidea) on a beach in northeastern Brazil. Estuarine Coastal and Shelf Science 71, 508–516. Bottjer, D.J. & Hagedorn, J.W. 1999. The Cambrian substrate revolution and evolutionary paleoecology of the Mollusca. Geological Society of America Abstracts with Programs 31, 335. Bottjer, D.J., Hagedorn, J.W. & Dornbos, S.Q. 2000. The Cambrian substrate revolution. GSA Today 10, 1–7. Bourgeois, R.P. & Felder, D.L. 2001. Postexposure metabolic effects of sulfide and evidence of sulfidebased ATP production in callianassid ghost shrimp (Crustacea: Decapoda: Thalassinidea). Journal of Experimental Marine Biology and Ecology 263, 105–121. Bracken, H.D., Toon, A., Felder, D.L., Martin, J.W., Finley, M., Rasmussen, J., Palero, F. & Crandall, K.A. 2009. The decapod tree of life: compiling the data and moving toward a consensus of decapod evolution. Arthropod Systematics and Phylogeny 67, 99–116. Branch, G.M. & Day, J.A. 1984. Ecology of southern African estuaries: part 13. The Palmiet River Estuary in the south-western Cape. South African Journal of Zoology 19, 63–77. Branch, G.M., Griffiths, C.L., Branch, M.L. & Beckley, L.E. 2010. Two Oceans, a Guide to the Marine Life of Southern Africa. Cape Town, South Africa: Struik Nature. Branch, G.M. & Pringle, A. 1987. The impact of the sand prawn Callianassa kraussi Stebbing on sediment turnover and on bacteria, meiofauna, and benthic microflora. Journal of Experimental Marine Biology and Ecology 107, 219–235. Brenchley, G.A. 1981. Disturbance and community structure: an experimental study of bioturbation in marine soft-bottom environments. Journal of Marine Research 39, 767–790. Brenchley, G.A. 1982. Mechanisms of spatial competition in marine soft-bottom communities. Journal of Experimental Marine Biology and Ecology 60, 17–33. Bromley, R.G. 1996. Trace Fossils. Biology, Taphonomy and Applications. 2nd ed. London: Chapman & Hall. Buchanan, J.C.B. 1963. The biology of Calocaris macandreae (Crustacea: Thalassinidae). Journal of the Marine Biological Association of the United Kingdom 43, 729–749. Butler, S.N. & Bird, F.L. 2008. Temporal changes in burrow structure of the thalassinidean ghost shrimps Trypaea australiensis and Biffarius arenosus. Journal of Natural History 42, 2041–2062. Cadée, G.C. 2001. Sediment dynamics by bioturbating organisms. In: Ecological Comparisons of Sedimentary Shores, Ecological Studies 151, K. Reise (ed.). Berlin, Heidelberg: Springer-Verlag, 127–148. 180

BIOENGINEERING EFFECTS OF BURROWING THALASSINIDEAN SHRIMPS Chamberlain, C.K. & Baer, J.L. 1973. Ophiomorpha and a new thalassinid burrow from the Permian of Utah. Brigham Young University Geological Studies 20, 79–94. Chen, J.C. & Kou, Y.Z. 1992. Effects of ammonia on growth and molting of Penaeus japonicus juveniles. Aquaculture 104, 249–260. Chen, J.C. & Lin C.Y. 1995. Responses of oxygen consumption, ammonia-N excretion and urea-N excretion of Penaeus chinensis exposed to ambient ammonia at different salinity and pH levels. Aquaculture 136, 243–255. Chen, J.C., Ting, Y.Y., Lin, J.N. & Lin, M.N. 1990. Lethal effects of ammonia and nitrite on Penaeus chinensis juveniles. Marine Biology 107, 427–431. Chiang, T.Y., Lin, H.D., Chan, T.Y., Hung, C.Y., Lin, F.J. 2008. Isolation and characterization of microsatellite loci in the commercially important mudshrimp Austinogebia edulis (Upogebiidae) using PCR-based isolation of microsatellite arrays (PIMA). Conservation Genetics 9, 1653–1655. Coelho, V.R. 2004. Feeding behaviour, morphological adaptations and burrowing in thalassinidean crustaceans. In Proceedings of the Symposium on Ecology of Large Bioturbators in Tidal Flats and Shallow Sublittoral Sediments—From Individual Behaviour to Their Role as Ecosystem Engineers, A. Tamaki (ed.). Nagasaki: Nagasaki University, 1–6. Coelho, V.R., Cooper, R.C. & Rodrigues, S. 2000a. Burrow morphology and behaviour of the mud shrimp Upogebia omissa (Decapoda: Thalassinidea: Upogebiidae). Marine Ecology Progress Series 200, 229–240. Coelho, V.R. & Rodrigues, S.A. 2001a. Setal diversity, trophic modes and functional morphology of feeding appendages of two callianassid shrimps, Callichirus major and Sergio mirim (Decapoda: Thalassinidea: Callianassidae). Journal of Natural History 35, 1447–1483. Coelho, V.R. & Rodrigues, S.A. 2001b. Trophic behaviour, setal types and functional morphology of the feeding appendages of the laomediid shrimp, Axianassa australis. Journal of the Marine Biological Association of the United Kingdom 81, 441–454. Coelho, V.R., Williams, A.B. & Rodrigues, S. 2000b. Trophic strategies and functional morphology of feeding appendages, with emphasis on setae, of Upogebia omissa and Pomatogebia operculata (Decapoda: Thalassinidea: Upogebiidae). Zoological Journal of the Linnean Society 130, 567–602. Coleman, F.C. & Williams, S.L. 2002. Overexploiting marine ecosystem engineers: potential consequences for biodiversity. Trends in Ecology and Evolution 17, 40–44. Colin, P.L., Suchanek, T.H. & McMurtry, G. 1986. Water pumping and particulate resuspension by callianassids (Crustacea: Thalassinidea) at Enewetak and Bikini Atolls, Marshall Islands. Bulletin of Marine Science 38, 19–24. Contessa, L. & Bird, F.L. 2004. The impact of bait-pumping on populations of the ghost shrimp Trypaea australiensis Dana (Decapoda: Callianassidae) and the sediment environment. Journal of Experimental Marine Biology and Ecology 304, 75–97. D’Andrea, A.F. & DeWitt, T.H. 2009. Geochemical ecosystem engineering by the mud shrimp Upogebia pugettensis (Crustacea: Thalassinidae) in Yaquina Bay, Oregon: density-dependent effects on organic matter remineralization and nutrient cycling. Limnology and Oceanography 54, 1911–1932. Decho, A.W. & Lopez, G.R. 1993. Exopolymer microenvironments of microbial flora: multiple and interactive effects on trophic relationships. Limnology and Oceanography 38, 1633–1645. de Deckere, E.M.G.T., Tolhurst, T.J. & Brouwer, J.F.C. 2001. Destabilization of cohesive intertidal sediments by infauna. Estuarine Coastal and Shelf Science 53, 665–669. de Vaugelas, J. & Buscail, R. 1990. Organic matter distribution in burrows of the thalassinid crustacean Callichirus laurae, Gulf of Aqaba (Red Sea). Hydrobiologia 207, 269–277. Devine, C.E. 1966. Ecology of Callianassa filholi Milne-Edwards 1878 (Crustacea, Thalassinidea). Transactions of the Royal Society of New Zealand 8, 93–110. DeWitt, T.H., D’Andrea, A.F., Brown, C.A., Griffen, B.D., & Eldridge, P.M. 2004. Impact of burrowing shrimp populations on nitrogen cycling and water quality in western North American temperate estuaries. In Proceedings of the Symposium on Ecology of Large Bioturbators in Tidal Flats and Shallow Sublittoral Sediments—From Individual Behaviour to Their Role as Ecosystem Engineers, A. Tamaki (ed.). Nagasaki: Nagasaki University, 107–118. Dittmann, S. 1996. Effects of macrobenthic burrows on infaunal communities in tropical tidal flats. Marine Ecology Progress Series 134, 119–130. 181

DEENA PILLAY & GEORGE M. BRANCH Dobbs, F.C., Guckert, J.B. 1988. Callianassa trilobata (Crustacea: Thalassinidea) influences abundance of meiofauna and biomass, composition, and physiologic state of microbial communities within its burrow. Marine Ecology Progress Series 45, 69–79. Dobretsov, S. & Qian, P.Y. 2006. Facilitation and inhibition of larval attachment of the bryozoan Bugula neritina in association with mono-species and multi-species biofilms. Journal of Experimental Marine Biology and Ecology 333, 263–274. Dornbos, S.Q. & Bottjer, D.J. 2000. Evolutionary paleoecology of the earliest echinoderms. Helicoplacoids and the Cambrian substrate revolution. Geology 28, 839–842. Dorsey, J.H. & Synnot, R.N. 1980. Marine soft-sediment benthic community offshore from the Black Rock sewage outfall, Connewaire, Victoria, Australia. Australian Journal of Marine & Freshwater Research 31, 155–162. Droser, M.L. & Bottjer, D.J. 1989. Ordovician increase in extent and depth of bioturbation: implications for understanding early Paleozoic ecospace utilization. Geology 17, 850–852. Dumbauld, B.R., Armstrong, D.A. & Feldman, K.L. 1996. Life history characteristics of two sympatric thalassinidean shrimps, Neotrypaea californiensis and Upogebia pugettensis, with implications for oyster culture. Journal of Crustacean Biology 16, 689–708. Dumbauld, B.R., Armstrong, D.A. & Skalski, J. 1997. Efficacy of the pesticide carbaryl for thalassinid shrimp control in Washington state oyster (Crassostrea gigas, Thunberg, 1793) aquaculture. Journal of Shellfish Research 16, 503–518. Dumbauld, B.R., Booth, S., Cheney, D., Suhrbier, A. & Beltran, H. 2006. An integrated pest management program for burrowing shrimp control in oyster aquaculture. Aquaculture 261, 976–992. Dumbauld, B.R., Brooks, K.M. & Posey, M.H. 2001. Response of an estuarine benthic community to application of the pesticide carbaryl and cultivation of Pacific oysters (Crassostrea gigas) in Willapa Bay, Washington. Marine Pollution Bulletin 42, 826–844. Dumbauld, B.R., Feldman, K.L. & Armstrong, D.A. 2004. A comparison of the ecology and effects of two species of thalassinidean shrimps on oyster aquaculture operations in the eastern North Pacific. In Proceedings of the Symposium on Ecology of Large Bioturbators in Tidal Flats and Shallow Sublittoral Sediments—From Individual Behaviour to Their Role as Ecosystem Engineers, A. Tamaki (ed.). Nagasaki: Nagasaki University, 53–61. Dumbauld, B.R. & Wyllie-Echeverria, S. 2003. The influence of burrowing thalassinid shrimps on the distribution of intertidal seagrasses in Willapa Bay, Washington, USA. Aquatic Botany 77, 27–42. Dworschak, P.C. 1981. The pumping rates of the burrowing shrimp Upogebia pusilla (Petagna) (Decapoda: Thalassinidea). Journal of Experimental Marine Biology and Ecology 52, 25–35. Dworschak, P.C. 1983. The biology of Upogebia pusilla (Petagna) (Decapoda, Thalassinidea) I. The burrows. Pubblicazioni della Stazione Zoologica di Napoli I: Marine Ecology 4, 19–43. Dworschak, P.C. 2000. Global diversity in the Thalassinidea (Decapoda). Journal of Crustacean Biology 20, 238–245. Dworschak, P.C. 2001. The burrows of Callianassa tyrrhena (Petagna 1792) (Decapoda: Thalassinidea). Pubblicazioni della Stazione Zoologica di Napoli I: Marine Ecology 22, 155–166. Dworschak, P.C. 2002. The burrows of Callianassa candida (Olivi 1792) and C. whitei Sakai 1999 (Crustacea: Decapoda: Thalassinidea). In The Vienna School of Marine Biology, M. Bright, P.C. Dworschak & M.S. Stachowitsch (eds). A tribute to Jörg Ott. Vienna, Austria: Facultas, 63–71. Dworschak, P.C. 2004. Biology of Mediterranean and Caribbean Thalassinidea. In Proceedings of the Symposium on Ecology of Large Bioturbators in Tidal Flats and Shallow Sublittoral Sediments—From Individual Behaviour to Their Role as Ecosystem Engineers, A. Tamaki (ed.). Nagasaki: Nagasaki University, 15–22. Dworschak, P.C. 2005. Global diversity in the Thalassinidea (Decapoda): an update (1998–2004). Nauplius 13, 57–63. Dworschak, P.C. 2008. The burrows of Callianassa tyrrhena (Petagna 1792) (Decapoda: Talassinidea). Marine Ecology 22, 155–166. Dworschak, P.C., Koller, H. & Abed-Navandi, D. 2006. The burrow structure, burrowing and feeding behaviour of Corallianassa longiventris and Pestarella tyrrhena (Crustacea, Thalassinidea, Callianassidae). Marine Biology 148, 1369–1382. Dworschak, P.C. & Ott, J.A. 1993. Decapod burrows in mangrove channel and back-reef environments at the Atlantic Barrier Reef, Belize. Ichnos 2, 277–290. 182

BIOENGINEERING EFFECTS OF BURROWING THALASSINIDEAN SHRIMPS Dzik, J. 1994. Evolution of ‘small shelly fossils’ assemblages of the early Paleozoic. Acta Palaeontologica Polonica 39, 247–313. Dzik, J. 2003. Anatomical information content in the Ediacaran fossils and their possible zoological affinities. Integrative and Comparative Biology 43, 114–126. Eckman, J.E. 1996. Closing the larval loop: linking larval ecology to the population dynamics of marine benthic invertebrates. Journal of Experimental Marine Biology and Ecology 200, 207–237. Eisenberg, J.F. & Kinlaw, A. 1999. Introduction to the special issue: ecological significance of open burrow systems. Journal of Arid Environments 41, 123–125. Ellis, J., Cummings, V., Hewitt, J., Thrush, S. & Norkko, A. 2002. Determining effects of suspended sediment on condition of a suspension feeding bivalve (Atrina zelanica): results from a survey, a laboratory experiment and a field transplant experiment. Journal of Experimental Marine Biology and Ecology 267, 147–174. Farley, R.D. & Case, J.F. 1968. Perception of external oxygen by the burrowing shrimp, Callianassa californiensis Dana and C. affinis Dana. Biological Bulletin 134, 261–265. Felder, D.L. 1979. Respiratory adaptations of the estuarine mud shrimp, Callianassa jamaicense (Schmitt, 1935) (Crustacea, Decapoda, Thalassinidea). Biological Bulletin 157, 125–138. Felder, D.L. 2001. Diversity and ecological significance of deep-burrowing macrocrustaceans in coastal tropical waters of the Americas (Decapoda: Thalassinidea). Intersciencia 26, 440–449. Felder, D.L., Nates, S.F. & Duhon, D.W. 1995. Invasion and colonization of tropical penaeid shrimp farms by thalassinid mudshrimp: the ecological scenario and biogeochemical consequences. In Swimming Through Troubled Waters: Proceedings of the Special Session on Shrimp Farming, Aquaculture ’95, C.L. Browdy & J.S. Hopkins (eds). Baton Rouge, Louisiana: World Aquaculture Society, 240–241. Fishman, J.R. & Orth, R.J. 1996. Effects of predation on Zostera marina L. seed abundance. Journal of Experimental Marine Biology and Ecology 198, 11–26. Flach, E. & Tamaki, A. 2001. Competitive bioturbators on intertidal sand flats in the European Wadden Sea and Ariake Sound in Japan. In Ecological Comparisons of Sedimentary Shores, Ecological Studies 151, K. Reise (ed.). Berlin: Springer-Verlag, 276–293. Flach, E.C. 1993. The distribution of the amphipod Corophium arenarium in the Dutch Wadden Sea: relationships with sediment composition and the presence of cockles and lugworms. Netherlands Journal of Sea Research 31, 281–290. Forbes, A.T. 1973. An unusual abbreviated larval life in the estuarine prawn Callianassa kraussi (Crustacea: Decapoda: Thalassinidea). Marine Biology 22, 361–365. Ford, P.W., Bird, F.L. & Hancock, G.J. 1999. Effect of burrowing macrobenthos on the flux of dissolved substances across the water-sediment interface. Marine and Freshwater Research 50, 523–532. Forster, S. & Graf, G. 1992. Continuously measured changes in redox potential influenced by oxygen penetrating from burrows of Callianassa subterranea. Hydrobiologia 235/236, 527–532. Forster, S. & Graf, G. 1995. Impact of irrigation on oxygen flux into sediment: intermittent pumping by Callianassa subterranean and ‘piston pumping’ by Lanice conchilega. Marine Biology 123, 335–346. Frankenberg, D., Coles, S.L. & Johannes, R.E. 1967. The potential trophic significance of Callianassa major fecal pellets. Limnology & Oceanography 12, 113–120. Gray, J.S. 1966. The attractive factor in intertidal sand to Protodrilus symbioticus. Journal of the Marine Biological Association of the United Kingdom 46, 627–645. Gray, J.S. 1967. Substrate selection by the arachiannelid Protodrilus symbioticus. Helgolander wiss Meeresunters. 46, 253–269 Gregory, M.R., Balance, P.F., Gibson, G.W. & Ayling, A.M. 1979. On how some rays (Elasmobranchia) excavate feeding depressions by jetting water. Journal of Sediment Petrology 49, 1125–1130. Griffen, B.D., DeWitt, T.H. & Langdon, C. 2004. Particle removal rates by the mud shrimp Upogebia pugettensis, its burrow, and a commensal clam: effects on estuarine phytoplankton abundance. Marine Ecology Progress Series 269, 223–236. Griffis, R.B. & Chavez, F.L. 1988. Effects of sediment type on burrows of Callianassa californiensis Dana and C. gigas Dana. Journal of Experimental Marine Biology and Ecology 117, 239–253. Griffis, R.B. & Suchanek, T.H. 1991. A model of burrow architecture and trophic modes in thalassinidean shrimp (Decapoda: Thalassinidea). Marine Ecology Progress Series 79, 171–183. Grigg, N.J. 2003. Benthic bulldozers and pumps: laboratory and modelling studies of bioturbation and bioirrigation. PhD thesis, Australian National University, Canberra, Australia. 183

DEENA PILLAY & GEORGE M. BRANCH Gu, J.D., Maki, J.S. & Mitchell, R. 1998. Microbial biofilms and their role in the induction and inhibition of invertebrate settlement. In Zebra Mussels and Aquatic Nuisance Species, F.M. D’Itri (ed.). Ann Arbor, Michigan: Ann Arbor Press, 343–357. Hadfield, M.G. & Paul, V.J. 2001. Natural chemical cues for settlement and metamorphosis of marine-invertebrate larvae. In Marine Chemical Ecology, J.B. McClintock & B.J. Baker (eds). Boca Raton, Florida: CRC Press, 431–461. Hafner, M.S., Demastes, J.W. & Spradling, T.A. 2000. Co-evolution and subterranean rodents. In Life Underground: The Biology of Subterranean Rodents, E.A. Lacey, J.L. Patton & G.N. Cameron (eds). Chicago: University of Chicago Press, 370–388. Hailstone, T.S. 1962. They’re good bait! Australian Natural History 14, 29–31. Hailstone, T.S. & Stephenson, W. 1961. The biology of Callianassa (Trypaea) australiensis Dana 1852 (Crustacea, Thalassinidea). University of Queensland Papers, Department of Zoology 12, 259–283. Hall-Spencer, J.M. & Atkinson, R.J.A. 1999. Upogebia deltaura (Crustacea: Thalassinidea) in Clyde Sea maerl beds, Scotland. Journal of the Marine Biological Association of the United Kingdom 79, 871–880. Hanekom, N. 1980. A study of two thalassinid prawns in the non-Spartina regions of the Swartkops Estuary. PhD thesis, University of Port Elizabeth, Port Elizabeth, South Africa. Hanekom, N.M. & Baird, D. 1987. Oxygen consumption of Callianassa kraussi Stebbing (Thalassinidea, Decapoda, Crustacea) in relation to various environmental conditions. South African Journal of Zoology 22, 183–189. Hansell, M.H. 1993. The ecological impact of animal nests and burrows. Functional Ecology 7, 5–12. Harris, J.M., Seiderer, L.J. & Lucas, M.I. 1991. Gut microflora of two saltmarsh detritivore thalassinid prawns, Upogebia africana and Callianassa kraussi. Microbial Ecology 21, 277–296. Harrison, P.G. 1987. Natural expansion and experimental manipulation of seagrass Zostera spp. abundance and the response of infaunal invertebrates. Estuarine Coastal and Shelf Science. 24, 799–812. Heck, K.L., Hays, G. & Orth, R.J. 2003. Critical evaluation of the nursery role hypothesis for seagrass meadows. Marine Ecology Progress Series 253, 123–136. Hemminga, M.A. & Duarte, C.M. 2000. Seagrass Ecology. Cambridge, UK: Cambridge University Press. Hill, B.J. 1967. Contribution to the ecology of Upogebia africana (Ortmann). PhD thesis, Rhodes University, Grahamstown, South Africa. Hill, B.J. 1981. Respiratory adaptations of three species of Upogebia (Thalassinidea, Crustacea) with special reference to low tide periods. Biological Bulletin (Woods Hole) 160, 272–279. Hodgson, A.N., Allanson, B.R. & Cretchley, R. 2000a. An estimation of the standing stock and population structure of Upogebia africana (Crustacea: Thalassinidae) in the Knysna Estuary. Transactions of the Royal Society of South Africa 55, 187–196. Hodgson, A.N., Allanson, B.R. & Cretchley, R. 2000b. The exploitation of Upogebia africana (Crustacea: Thalassinidae) for bait in the Knysna Estuary. Transactions of the Royal Society of South Africa 55, 197–204. Howe, R.L., Rees, A.P. & Widdicombe, S. 2004. The impact of two species of bioturbating shrimp (Callianassa subterranea and Upogebia deltaura) on sediment nitrification. Journal of the Marine Biological Association of the United Kingdom 84, 629–632. Huang, S. & Hadfield, M.G. 2003. Composition and density of bacterial biofilms determine larval settlement of the polychaete Hydroides elegans. Marine Ecology Progress Series 260, 161–172. Hughes, D.J., Atkinson, R.J.A. & Ansell, A.D. 2000. A field test of the effects of megafaunal burrows on benthic chamber measurements of sediment-water solute fluxes. Marine Ecology Progress Series 195, 189–199. Hughes, J.E., Deegan, L.A., Wyda, J.C., Weaver, M.J. & Wright, A. 2002. The effect of eelgrass habitat loss on estuarine fish communities of southern New England. Estuaries and Coasts 25, 235–249. Itani, G. 2004. Host specialization in symbiotic animals associated with thalassinidean shrimps in Japan. In Proceedings of the Symposium on Ecology of Large Bioturbators in Tidal Flats and Shallow Sublittoral Sediments—From Individual Behaviour to Their Role as Ecosystem Engineers, A. Tamaki (ed.). Nagasaki: Nagasaki University, 33–43. Jahn, A., Gamenick, I. & Theede, I. 1996. Physiological adaptations of Cyprideis torosa (Crustacea, Ostracoda) to hydrogen sulphide. Marine Ecology Progress Series 142, 215–223. Johns, A.R., Taylor, A.C., Atkinson, R.J.A. & Grieshaber, M.K. 1997. Sulphide metabolism in thalassinidean Crustacea. Journal of the Marine Biological Association of the United Kingdom 77, 127–144. 184

BIOENGINEERING EFFECTS OF BURROWING THALASSINIDEAN SHRIMPS Johnson, K.R. & Nelson, C.H. 1984. Side-scan sonar assessment of gray whale feeding in the Bering Sea. Science 225, 1150–1152. Jones, C.G., Lawton, J.H. & Shackak, M. 1994. Organisms as ecosystem engineers. Oikos 69, 373–386. Jordan, M.A., Welsh, D.T., Dunn, R.J.K., & Teasdale, P.R. 2009. Influence of Trypaea australiensis population density on benthic metabolism and nitrogen dynamics in sandy estuarine sediment: a mesocosm simulation. Journal of Sea Research 61, 144–152. Karplus, I. 1987. The association between gobiid and burrowing alpheid shrimps. Oceanography and Marine Biology An Annual Review 25, 507–562. Kato, M. & Itani, G. 1995. Commensalism of a bivalve, Peregrinamor ohshimai, with a thalassinidean burrowing shrimp, Upogebia major. Journal of the Marine Biological Association of the United Kingdom 75, 941–947. Katrak, G. & Bird, F.L. 2003. Comparative effects of the large bioturbators, Trypaea australiensis and Heloecius cordiformis, on intertidal sediments of Western Port, Victoria, Australia. Marine and Freshwater Research 54, 701–708. Kensley, B. 1980. Notes on Axiopsis serratifrons (A. Milne Edwards) (Crustacea: Decapoda: Thalassinidea). Proceedings of the Biological Society of Washington 93, 1253–1263. Kensley, B. 1994. The genus Coralaxius redefined, with the description of two new species (Crustacea: Decapoda: Axiidae). Journal of Natural History 28, 813–828. Kerr, G. 2001. Ecological aspects of Trypaea australiensis. PhD thesis, Southern Cross University, New South Wales, Australia. Kerr, G. & Corfield, J. 1998. Association between the ghost shrimp Trypaea australis Dana 1852 (Crustacea: Decapoda) and a small deposit-feeding bivalve Mysella vitrae Laserson 1956 (Mollusca: Leptonidae). Marine and Freshwater Research 49, 801–806. Kikuchi, T. & Peres, J.M. 1977. Consumer ecology of seagrass beds, In Seagrass Ecosystems: A Scientific Perspective, C.P. McRoy & C. Helfferich (eds). New York: Dekker, 147–194. Kinoshita, K. 2002. Burrow structure of the mud shrimp Upogebia major (Decapoda: Thalassinidea: Upogebiidae). Journal of Cructacean Biology 22, 474–480. Kinoshita, K. & Furota, T. 2004. Burrow structure and life-history characteristics of the mud shrimp, Upogebia major. In Proceedings of the Symposium on Ecology of Large Bioturbators in Tidal Flats and Shallow Sublittoral Sediments—From Individual Behaviour to Their Role as Ecosystem Engineers, A. Tamaki (ed.). Nagasaki: Nagasaki University, 7–13. Kinoshita, K. & Itani, G. 2005. Interspecific differences in the burrow morphology between the sympatric mud shrimps, Austinogebia narutensis and Upogebia issaeffi (Crustacea: Thalassinidea: Upogebiidae). Journal of the Marine Biological Association of the United Kingdom 85, 943–947. Kinoshita, K., Wada, M., Kogure, K. & Furota, T. 2003. Mud shrimp burrows as dynamic traps and processors of tidal-flat materials. Marine Ecology Progress Series 247, 159–164. Kinoshita, K., Wada, M., Kogure, K. & Furota, T. 2008. Microbial activity and accumulation of organic matter in the burrow of the mud shrimp, Upogebia major (Crustacea: Thalassinidea). Marine Biology 153, 277–283. Klerks, P.L., Felder, D.L., Strasser, K. & Swarzenski, P.W. 2007. Effects of ghost shrimp on zinc and cadmium in sediments from Tampa Bay, FL. Marine Chemistry 104, 17–26. Koike, I. & Mukai, H. 1983. Oxygen and inorganic nitrogen contents and fluxes in burrows of the shrimps Callianassa japonica and Upogebia major. Marine Ecology Progress Series 12, 185–190. Köster, M., Jensen, P. & Meyer-Reil, L.A. 1991. Hydrolytic activities of organisms and biogenic structures in deep-sea sediments. In Microbial Enzymes in Aquatic Environments, R.J. Chróst (ed.). New York: Springer-Verlag, 60–83. Kristensen, E. 1988. Benthic fauna and biogeochemical processes in marine sediments: microbial activities and fluxes. In Nitrogen Cycling in Coastal Marine Environments, T.H. Blackburn & J. Sørensen (eds). Chichester, UK: Wiley, 275–299. Kristensen, E. & Kostka, J.E. 2005. Macrofaunal burrows and irrigation in marine sediment: microbiological and biogeochemical interactions. In Interactions between Macro- and Microorganisms in Marine Sediments, Coastal Estuarine Studies 60, E. Kristensen, J.E. Kostka & R.R. Haese (eds). Washington, DC: American Geophysical Union, 125–157. Laland, K.N., Odling-Smee, F.J. & Feldman, M.W. 2004. Niche construction: do the changes that organisms make to their habitats transform evolution and influence natural selection? Nature 429, 609 only. 185

DEENA PILLAY & GEORGE M. BRANCH Lau, S.K., Thiyagarajan, V. & Qian, P.Y. 2003. The bioactivity of bacterial isolates in Hong Kong waters for the inhibition of barnacle (Balanus amphitrite Darwin) settlement. Journal of Experimental Marine Biology and Ecology 282, 43–60. Lemaitre, R. & Rodrigues, S.D. 1991. Lepidopthalmus sinuensis: a new species of ghost shrimp (Decapoda Thalassinidea: Callianassidae) of importance to the culture of penaeid shrimps on the Caribbean coast of Columbia, with observations on its ecology. Fishery Bulletin 89, 623–630. Levinton, J.S. 1995. Bioturbators as ecosystem engineers: control of the sediment fabric, inter-individual interactions, and material fluxes. In Linking Species and Ecosystems, J.H. Lawton & C.G. Jones (eds). New York: Chapman and Hall, 29–44. Li, H.Y., Lin, F.J. Chan, B.K.K. & Chan, T.T. 2008. Burrow morphology and dynamics of mudshrimp in Asian soft shores. Journal of Zoology 274, 301–311. Loques, F., Caye, G. & Meinesz, A. 1990. Germination in the marine phanerogram Zostera noltii Hornemann at Golfe Juan, French Mediterranean. Aquatic Botany 38, 249–260. Lucas, F.S., Bertru, G. & Höfle, M.G. 2003. Characterization of freeliving and attached bacteria in sediments colonized by Hediste diversicolor. Aquatic Microbial Ecology 32, 165–174. Luckenbach, M.W. & Orth, R.J. 1999. Effects of a deposit-feeding invertebrate on the entrapment of Zostera marina L. seeds. Aquatic Botany 62, 235–247. MacGinitie, G.E. 1930. The natural history of mud shrimp Upogebia pugettensis (Dana). Annals and Magazine of Natural History 6, 36–47. MacGinitie, G.E. 1934. The natural history of Callianassa californiensis Dana. American Midland Naturalist 15, 166–177. MacGinitie, G.E. 1939. The natural history of the blind goby Typhlogobius californiensis Steindachner. American Midland Naturalist 21, 489–505. MacGinitie, G.E. & MacGinitie, N. 1968. Natural History of Marine Animals. New York: McGraw-Hill. Manning, R.B. & Felder, D.L. 1991. Revision of the American Callianassidae (Crustacea: Decapoda: Thalassinidae). Proceedings of the Biological Society of Washington 104, 764–792. Manning, R.B. & Tamaki, A. 1998. A new genus of ghost shrimp from Japan (Crustacea: Decapoda: Callianassidae). Proceedings of the Biological Society of Washington 111, 889–892. Meadows, P.S.M. 1964. Experiments on substrate selection by Corophium species: films and bacteria on sand particles. Journal of Experimental Marine Biology and Ecology 41, 499–512. Merkens, J.C. & Downing, K.M. 1957. The effect of tension of dissolved oxygen on the toxicity of un-ionized ammonia to several species of fish. Annals of Applied Biology 45, 521–527. Meysman, F.J.R., Middelburg, J.J. & Heip, C.H.R. 2006. Bioturbation: a fresh look at Darwin’s last idea. Trends in Ecology and Evolution 21, 688–695. Miller, D.C., Muir, C.L. & Hauser, O.A. 2002. Detrimental effects of sedimentation on marine benthos: what can be learned from natural processes and rates? Ecological Engineering 19, 211–232. Molenaar, H. & Meinesz, A. 1995. Vegetative reproduction in Posidonia oceanica: survival and development of transplanted cuttings according to different spacing, arrangements and substrates. Botanica Marina 38, 313–332. Mukai, H. & Koike, I. 1984. Behaviour and respiration of the burrowing shrimps Upogebia major (De Haan) and Callianassa japonica (De Haan). Journal of Crustacean Biology 4, 191–200. Murphy, R.C. 1985. Factors affecting the distribution of the introduced bivalve, Mercenaria mercenaria, in a California lagoon—the importance of bioturbation. Journal of Marine Research 43, 673–692. Murphy, R.C. & Kremer, J.N. 1992. Benthic community metabolism and the role of deposit-feeding callianassid shrimp. Journal of Marine Research 50, 321–340. Nacorda, H.M. 2008. Burrowing shrimps and seagrass dynamics in shallow-water meadows off Bolonao (NW Philippines). Rotterdam, The Netherlands: CRC Press/Balkema. Napier, V.R., Turpie, J.K. & Clark, B.M. 2009. Value and management of the subsistence fishery at Knysna Estuary, South Africa. African Journal of Marine Science 31, 197–310. Nates, S.F. & Felder, D.L. 1998. Impact of burrowing ghost shrimp, Genus Lepidophthalmus Crustacea: Decapoda: Thalassinidea, on penaeid shrimp culture. Journal of the World Aquaculture Society 29, 188–210. Nates, S.F., Felder, L.D. & Lemaitre, R. 1997. Comparative larval development in two species of the burrowing ghost shrimp genus Lepidophthalmus (Decapoda: Callianassidae). Journal of Crustacean Biology 17, 497–519. 186

BIOENGINEERING EFFECTS OF BURROWING THALASSINIDEAN SHRIMPS Newell, R.C. 1979. Biology of Intertidal Animals. Faversham, UK: Marine Ecological Surveys. Ngoc-Ho, N. 2003. European and Mediterranean Thalassinidea (Crustacea, Decapoda). Zoosystema 25, 439–555. Nickell, L.A. & Atkinson, R.J.A. 1995. Functional morphology of burrows and trophic modes of three thalassinidean shrimp species, and a new approach to the classification of thalassinidean burrow morphology. Marine Ecology Progress Series 128, 181–197. Noor-Hamid, S., Fortes, R.D. & Parado-Estepa, F. 1994. Effect of pH and ammonia on survival and growth of the early larval stages of Penaeus monodon Fabricius. Aquaculture 125, 67–72. Odling-Smee, F.J., Laland, K.N. & Feldman, M.W. 1996. Niche construction. American Naturalist 147, 641–648. Odling-Smee, F.J., Laland, K.N. & Feldman, M.W. 2003. Niche Construction. The Neglected Process in Evolution. Princeton, New Jersey: Princeton University Press. Ólafsson, E. 2003. Do macrofauna structure meiofauna assemblages in marine soft-bottoms? A review of experimental studies. Vie Milieu 53, 249–265. Orth, R.J., Carruthers, T.J.B., Dennison, W.J., Duarte, C.M., Fourqurean, J.W., Heck, K.L., Jr., Hughes, A.R., Kendrick, G.A., Kenworthy, W.J., Olyarnik, S., Short, F.T., Waycott, M. & Williams, S.L. 2006. A global crisis for seagrass ecosystems. Bioscience 56, 987–996. Ostrensky, A. & Wasielesky Jr, W. 1995. Acute toxicity of ammonia to various life stages of the São Paulo shrimp, Penaeus paulensis Pérez-Farfante, 1967. Aquaculture 132, 339–347. Papaspyrou, S., Gregersen, T., Cox, R.P., Thessalou-Legaki, M. & Kristensen, E. 2005. Sediment properties and bacterial community in burrows of the ghost shrimp Pestarella tyrrhena (Decapoda: Thalassinidea). Aquatic Microbial. Ecology 38, 181–190. Papaspyrou, S., Thessalou-Legaki, M. & Kristensen, E. 2004. Impact of Pestarella tyrrhena on benthic metabolism in sediment microcosms enriched with seagrass and macroalgal detritus. Marine Ecology Progress Series 281, 165–179. Paterson, B.D. & Thorne, M.J. 1993. The effect of oxygen tension on the swimmeret rate of Callianassa australiensis and C. arenosa (Crustacea, Decapoda, Thalassinidea). Marine and Freshwater Behaviour and Physiology 24, 15–24. Paterson, B.D. & Thorne, M.J. 1995. Measurements of oxygen uptake, heart and gill bailer rates of the callianassid burrowing shrimp Trypaea australiensis Dana and its responses to low oxygen tensions. Journal of Experimental Marine Biology and Ecology 194, 39–54. Paterson, D.M. & Hagerthey, S.E. 2001. Microphytobenthos in contrasting coastal ecosystems: biology and dynamics. In Ecological Comparisons of Sedimentary Shores, Ecological Studies 151, K. Reise, (ed.). Berlin: Springer-Verlag, 276–293. Pawlik, J.R. 1992. Chemical ecology of the settlement of benthic marine invertebrates. Oceanography and Marine Biology An Annual Review 30, 275–335. Pemberton, G.S., Risk, M.J. & Buckley, D.E. 1976. Supershrimp: deep bioturbation in the Strait of Canso, Nova Scotia. Science 192, 790–790. Peterson, C.H. 1977. Competitive organization of the softbottom macrobenthic communities of Southern California lagoons. Marine Biology 43, 343–359. Phillipart, C.J.M. 1994. Interactions between Arenicola marina and Zostera noltii on a tidal flat in the Wadden Sea. Marine Ecology Progress Series 111, 251–257. Pillay, D. 2006. The influence of bioturbation by the sandprawn Callianassa kraussi Stebbing on macrobenthic assemblages of the Little Lagoon. PhD thesis, University of KwaZulu-Natal, Durban, South Africa. Pillay, D. 2010. Expanding the envelope: linking invertebrate bioturbation with micro-evolutionary change. Marine Ecology Progress Series 409, 301–303. Pillay, D., Branch, G.M. & Forbes, A.T. 2007a. The influence of bioturbation by the sandprawn Callianassa kraussi on feeding and survival of the bivalve Eumarcia paupercula and the gastropod Nassarius kraussianus. Journal of Experimental Marine Biology and Ecology 344, 1–9. Pillay, D., Branch, G.M. & Forbes, A.T. 2007b. Experimental evidence for the effects of the thalassinidean sandprawn Callianassa kraussi on macrobenthic communities. Marine Biology 152, 611–618. Pillay, D., Branch, G.M. & Forbes, A.T. 2007c. Effects of Callianassa kraussi on microbial biofilms and recruitment of macrofauna: a novel hypothesis for adult-juvenile interactions. Marine Ecology Progress Series 347, 1–14. 187

DEENA PILLAY & GEORGE M. BRANCH Pillay, D., Branch, G.M. & Forbes, A.T. 2008. Habitat change in an estuarine embayment: anthropogenic influences and a regime shift in biotic interactions. Marine Ecology Progress Series 370, 19–31. Pinn, E.H. & Atkinson, R.J.A. 2010. Burrow development, nutrient fluxes, carnivory and caching behaviour by Calocaris macandreae (Crustacea: Decapoda: Thalassinidea). Journal of the Marine Biological Association of the United Kingdom 90, 247–253. Pinn, E.H., Atkinson, R.J.A., Rogerson, A. 1998. Particle size selectivity and resource partitioning in five species of Thalassinidea (Crustacea: Decapoda). Marine Ecology Progress Series 169, 243–250. Pinn, E.H., Nickell, L.A., Rogerson, A., Atkinson, R.J.A. 1999. Comparison of gut morphology and gut microflora of seven species of mud shrimp (Crustacea: Decapoda: Thalassinidea). Marine Biology 133, 103–114. Pohl, M.E. 1946. Ecological observations on Callianassa major Say at Beaufort, North Carolina. Ecology 27, 71–80. Poore, G.C.B. 1994. A phylogeny of the families of Thalassinidea (Crustacea: Decapoda) with keys to families and genera. Memoirs of the Museum of Victoria 54, 79–120. Posey, M.H. 1986. Changes in a benthic community associated with dense beds of a burrowing deposit feeder Callianassa californiensis. Marine Ecology Progress Series 31, 15–22. Posey, M.H., Dumbauld, B.R. & Armstrong, D.A. 1991. Effects of a burrowing mud shrimp, Upogebia pugettensis (Dana), on abundances of macro-infauna. Journal of Experimental Marine Biology and Ecology 148, 283–294. Pritchard, A.W. and Eddy, S. 1979. Lactate formation in Callianassa californiensis and Upogebia pugettensis (Crustacea: Thalassinidea). Marine Biology 50, 249–253. Reichardt, W. 1988. Impact of bioturbation by Arenicola marina on microbiological parameters in intertidal sediments. Marine Ecology Progress Series 44, 149–158. Reise, K. 1985. Tidal Flat Ecology. An Experimental Approach to Species Interactions, Ecological Studies, 54. Berlin: Springer-Verlag. Rhoads, D.C. & Young, D.K. 1970. The influence of deposit-feeding organisms on sediment stability and community trophic structure. Journal of Marine Research 28, 150–178. Riddle, M.J. 1988. Cyclone and bioturbation effects on sediments from coral reef lagoons. Estuarine Coastal and Shelf Science 27, 687–695. Roberts, H.H., Wiseman, W.J. & Suchanek, T.H. 1981. Lagoon sediment transport: the significant effect of Callianassa bioturbation. Proceedings of the Fourth International Coral Reef Symposium, Manila 1, 459–465. Robles, R., Tudge, C.C., Dworschak, P.C., Poore, G.C.B. & Felder, D.L. 2009. Molecular phylogeny of the Thalassinidea based on nuclear and mitochondrial genes. In Decapod Crustacean Phylogenetics, Crustacean Issues 18, J.W. Martin, K.A. Crandall & D.L. Felder (eds). Boca Raton, Florida: CRC Press, 309–326. Rowden, A.A. & Jones, M.B. 1993. Critical evaluation of sediment turnover estimates for Callianassidae (Decapoda: Thalassinidea). Journal of Experimental Marine Biology and Ecology 173, 265–272. Rowden, A.A., Jones, M.B. & Morris, A.W. 1998. The role of Callianassa subterranea (Montagu) (Thalassinidea) in sediment resuspension in the North Sea. Continental Shelf Research 18, 1365–1380. Santagata, S. 2004. A waterborne behavioural cue for the Actinotroch larva of Phoronis pallida (Phoronida) produced by Upogebia pugettensis (Decapoda: Thalassinidea). Biological Bulletin 207, 103–115. Schram, F.R. 1986. Crustacea. New York: Oxford University Press. Scott, P.J.B., Reiswig, H.M. & Marcotte, B.M. 1988. Ecology, functional morphology, behaviour, and feeding in coral and sponge-boring species of Upogebia (Crustacea: Decapoda: Thalassinidea). Canadian Journal of Zoology 66, 483–495. Seilacher, A. 1999. Biomat-related lifestyles in the Pre-Cambrian. Palaios 14, 86–93. Seilacher, A. & Pflüger, F. 1994. From biomats to benthic agriculture: a biohistoric revolution. In Biostabilization of Sediments, W.E. Krumbein, D.M. Paterson & L.J. Stal (eds). Oldenberg, Germany: Bibliotheks- und Informationssystem der Universitat Oldenburg, 97–105. Shimoda, K., Aramaki, Y., Nasuda, J., Yokoyama, H., Ishihi, Y. & Tamaki, A. 2007. Food sources for three species of Nihonotrypaea (Decapoda: Thalassinidea: Callianassidae) from western Kyushu, Japan, as determined by carbon and nitrogen stable isotope analysis. Journal of Experimental Marine Biology and Ecology 342, 292–312. Shy, J. & Chan, T. 1996. Complete larval development of the edible mud shrimp Upogebia edulis Ngoc-Ho & Chan, 1992 (Decapoda, Thalassinidea, Upogebiidae) reared in the laboratory. Crustaceana 69, 175–168. 188

BIOENGINEERING EFFECTS OF BURROWING THALASSINIDEAN SHRIMPS Siebert, T. & Branch, G.M. 2005a. Interactions between Zostera capensis and Callianassa kraussi: influences on community composition of eelgrass beds and sandflats. African Journal of Marine Science 27, 357–373. Siebert, T. & Branch, G.M. 2005b. Interactions between Zostera capensis, Callianassa kraussi and Upogebia africana: deductions from field surveys in Langebaan Lagoon, South Africa. African Journal of Marine Science 27, 345–356. Siebert, T. & Branch, G.M. 2006. Ecosystem engineers: interactions between eelgrass Zostera capensis and the sandprawn Callianassa kraussi and their indirect effects on the mudprawn Upogebia africana. Journal of Experimental Marine Biology and Ecology 338, 253–270. Siebert, T. & Branch, G.M. 2007. Influences of biological interactions on community structure within seagrass beds and sandprawn-dominated sandflats. Journal of Experimental Marine Biology and Ecology 340, 11–24. Skilleter, G.A., Zharikov, Y., Cameron, B. & McPhee, D.P. 2005. Effects of harvesting callianassid (ghost) shrimps on subtropical benthic communities. Journal of Experimental Marine Biology and Ecology 320, 133–158. Souza, J.R.B. & Borzone, C.A. 2003. Ghost-shrimp Callichirus major (Say) (Crustacea, Thalssinidea) extraction for bait us in beaches of Paraná’s littoral: the exploited populations. Revista Brasileira de Zoologia 20, 625–630. Stamhuis, E.J., Reede-Dekker, T., van Etten, Y., de Wiljes J.J., & Videler, J.J. 1996. Behaviour and time allocation of the burrowing shrimp Callianassa subterranea (Decapoda, Thalassinidea). Journal of Experimental Marine Biology and Ecology 204, 225–239. Stamhuis, E.J., Schreurs, C.E. & Videler, J.J. 1997. Burrow architecture and turbative activity of the thalassinid shrimp Callianassa subterranea from the central North Sea. Marine Ecology Progress Series 151, 155–163. Steward, C.C., Nold, S.C., Ringelberg, D.B., White, D.C. & Lovell, C.R. 1996. Microbial biomass and community structures in the burrows of bromophenol producing and non-producing marine worms and surrounding sediments. Marine Ecology Progress Series 133, 149–165. Strasser, K.M. & Felder, D.L. 1999. Settlement cues in an Atlantic coast population of the ghost shrimp Callichirus major (Crustacea: Decapoda: Thalassinidea). Marine Ecology Progress Series 183, 217–225. Suchanek, T.H. 1983. Control of seagrass communities and sediment distribution by Callianassa (Crustacea, Thalassinidea) bioturbation. Journal of Marine Research 41, 281–298. Suchanek, T.H. & Colin, P.L. 1986. Rates and effects of bioturbation by invertebrates and fishes at Enewetak and Bikini Atolls. Bulletin of Marine Science 38, 25–35. Suchanek, T.H., Colin, P.L., McMurtry, G.M. & Suchanek, C.S. 1986. Bioturbation and redistribution of sediment radionuclides in Enewetak Atoll lagoon by callianassid shrimp: biological aspects. Bulletin of Marine Science 38, 144–154. Swinbanks, D.D. & Murray, J.W. 1981. Biosedimentological zonation of Boundary Bay tidal flats, Fraser River Delta, British Columbia. Sedimentology 28, 201–237. Tamaki, A. 1988. Effects of the bioturbating activity of the ghost shrimp Callianassa japonica on migration by a mobile polychaete. Journal of Experimental Marine Biology and Ecology 120, 81–95. Tamaki, A. 1994. Extinction of the trochid gastropod, Umbonium (Suchium) moniliferum (Lamark), and associated species on an intertidal sandflat. Researches on Population Ecology 36, 225–236. Tamaki, A. & Ingole, B. 1993. Distribution of juvenile and adult ghost shrimps. Callianassa japonica Ortmann (Thalassinidea), on an intertidal sand flat: intraspecific facilitation as a possible pattern-generating factor. Journal of Crustacean Biology 13, 175–183. Thayer, C.W. 1979. Biological bulldozers and the evolution of marine benthic communities. Science 203, 458–461. Thompson, R.K. & Pritchard, A.W. 1969. Respiratory adaptations of two burrowing crustaceans, Callianassa californiensis and Upogebia pugettensis (Decapoda, Thalassinidea). Biological Bulletin 136, 274–287. Torres, J.J., Gluck, D.L. & Childress, J.J. 1977. Activity and physiological significance of the pleopods in the respiration of Callianassa californiensis (Dana) (Crustacea: Thalassinidea). Biological Bulletin 152, 134–146. Townsend, E.C. & Fonseca, M.S. 1998. Bioturbation as a potential mechanism influencing spatial heterogeneity of North Carolina seagrass beds. Marine Ecology Progress Series 169, 123–132. 189

DEENA PILLAY & GEORGE M. BRANCH Tudge, C.C., Poore, G.C.B. & Lemaitre, R. 2000. Preliminary phylogenetic analysis of genetic relationships within the Callianassidae and Ctenochelidae (Decapoda: Thalassinidea: Callianassoidea). Journal of Crustacean Biology 20, 129–149. Tudhope, A.W. & Scoffin, T.P. 1984. The effects of Callianassa bioturbation of the preservation of carbonate grains in Davies Reef Lagoon, Great Barrier Reef, Australia. Journal of Sediment Petrology 54, 1091–1092. Underwood, G.J.C. & Paterson, D.M. 1995. The measurement of microbial carbohydrate exopolymers from intertidal sediments. Limnology & Oceanography 40, 1243–1253. van Nes, E.H., Amaro, T., Scheffer, M., Duineveld, G.C.A. 2007. Possible mechanisms for a marine benthic regime shift in the North Sea. Marine Ecology Progress Series 330, 39–47. Vermeij, G.J. 1989. The origin of skeletons. Palaios 4, 585–589. Vogel, S. 1977. Flow in organisms induced by movements of the external medium. In Symposium on Scale Effects in Animal Locomotion, T.J. Pedley (ed.). London: Academic Press, 285–297. Vogel, S. 1994. Life in Moving Fluids: The Physical Biology of Flow. Princeton, New Jersey: Princeton University Press. Wada, M., Kinoshita, K. & Kogure, K. 2004. Mud shrimp burrows as traps of tidal-flat organic matters. In Proceedings of the Symposium on Ecology of Large Bioturbators in Tidal Flats and Shallow Sublittoral Sediments—From Individual Behaviour to Their Role as Ecosystem Engineers, A. Tamaki (ed.). Nagasaki: Nagasaki University, 101–106. Waldbusser, G.G. & Marinelli, R.L. 2006. Macrofaunal modification of porewater advection: the role of species function, species interaction, and kinetics. Marine Ecology Progress Series 311, 217–231. Waldbusser, G.G. & Marinelli, R.L. 2009. Evidence of infaunal effects on porewater advection and geochemistry in permable sediments: a proposed infaunal functional-group framework. Journal of Marine Reseach 67, 503–532. Walters, W.L. & Griffiths, C.L. (1987) Patterns of distribution, abundance and shell utilization amongst hermit crabs, Diogenes brevirostris. South African Journal of Zoology 22, 269–277. Ward, D.H., Morton, A., Tibbitts, T.L., Douglas, D.C. & Carrera-González, E. 2003. Long-term change in eelgrass distribution at Bahía San Quintín, Baja California, Mexico, using satellite imagery. Estuaries 26, 1529–1539. Waslenchuk, D.G., Matson, E.A., Zajak, R.N., Dobbs, F.C. & Tramontano, J.M. 1983. Geochemistry of burrow waters vented by a bioturbating shrimp in Bermudian sediments. Marine Biology 72, 219–225. Waycott, M., Duarte, C.M., Carruthers, T.J.B., Orth, R.J., Dennison, W.C., Olyarnik, S., Calladine, A., Fourqurean, J.W., Heck, K.L., Hughes, A.R., Kendrick, G.A., Kenworthy, W.J., Short, F.T. & Williams, S.L. 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Science of the United States of America 106, 12377–12381. Webb, A.P. & Eyre, B.D. 2004. Effect of natural populations of burrowing thalassinidean shrimp on sediment irrigation, benthic metabolism, nutrient fluxes and denitrification. Marine Ecology Progress Series 268, 205–220. Weitkamp, L.A., Wissmar, R.C., Simenstad, C.A., Fresh, K.L. & Odell, J.G. 1992. Gray whale foraging on ghost shrimp (Callianassa californiensis) in littoral sand flats of Puget Sound, USA. Canadian Journal of Zoology 70, 2275–2280. Widdows, J., Brinsley, M.D., Salkeld, P.N., Lucas, C.H. 2000. Influences of biota on spatial and temporal variations in sediment erodibility and material flux on a tidal flat (Westerchelde, the Netherlands). Marine Ecology Progress Series 194, 23–37. Wieczorek, S.K. & Todd, C.D. 1998. Inhibition and facilitation of settlement of epifaunal marine invertebrate larvae by microbial biofilm cues. Biofouling 12, 81–118. Wilson, D.P. 1955. The role of micro-organisms in the settlement of Ophelia bicornis Savigny. Journal of the Marine Biological Association of the United Kingdom 34, 531–543. Witbaard, R. & Duineveld, G.C.A. 1989. Some aspects of the biology and ecology of the burrowing shrimp Callianassa subterranea (Montagu) (Thalassinidea) from the southern North Sea. Sarsia 74, 209–219. Woodin, S.A. 1976. Adult-larval interactions in dense infaunal assemblages: patterns of abundance. Journal of Marine Research 34, 25–41. Wynberg, R.P. & Branch, G.M. 1991. An assessment of bait-collecting for Callianassa kraussi Stebbing in Langebaan Lagoon, and of associated avian predation. South African Journal of Marine Science 11, 141–152. 190

BIOENGINEERING EFFECTS OF BURROWING THALASSINIDEAN SHRIMPS Wynberg, R.P. & Branch, G.M. 1994. Disturbance associated with bait-collection for sandprawns (Callianassa kraussi) and mudprawns (Upogebia africana) long-term effects on the biota of intertidal sandflats. Journal of Marine Research 52, 523–558. Wynberg, R.P. & Branch, G.M. 1997. Trampling associated with bait-collection for sandprawns Callianassa kraussi Stebbing: effects on the biota of an intertidal sandflat. Environmental Conservation 24, 139–148. Yamasaki, M., Nanri, T., Taguchi, S., Takada, Y. & Saigusa, M. 2010. Latitudinal and local variations of the life history characteristics of the thalassinidean decapod, Upogebia yokoyai: a hypothesis based on trophic conditions. Estuarine Coastal and Shelf Science 87, 346–356. Zebe, E. 1982. Anaerobic metabolism in Upogebia pugettensis and Callianassa californiensis (Crustacea: Thalassinidea). Comparative Biochemistry and Physiology 72B, 613–617. Ziebis, W., Forster, S., Huettel, M. & Jørgensen, B.B. 1996a. Complex burrows of the mud shrimp Callianassa truncata and their geochemical impact in the sea bed. Nature 382, 619–622. Ziebis, W., Huettel, J. & Forster, S. 1996b. Impact of biogenic sediment topography on oxygen fluxes in permeable seabeds. Marine Ecology Progress Series 140, 227–237.

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