Effects of Callianassa kraussi on microbial biofilms and recruitment of macrofauna: a novel hypothesis for adultjuvenile interactions

Self Cite

Starfish are significant determinants of community structure in marine ecosystems. The starfish Parvulastra (Patiriella) exigua is normally found on intertidal rocky shores. We examined a major outbreak of this species in Langebaan Lagoon, a marine embayment on the west coast of South Africa, and the only known soft-sediment ecosystem where P. exigua flourishes. We document this outbreak and describe subsequent field caging experiments testing the influence of this starfish on soft-sediment community structure. Grazing by P. exigua resulted in a reduction in microalgal biomass that was linearly related to starfish density, but it promoted bacterial density. Macrofaunal communities at intermediate densities of P. exigua were different and more diverse to those at high and low starfish densities, with Shannon-Wiener and Fischer's α indices peaking at intermediate density of P. exigua. It is possible that P. exigua at intermediate densities promotes co-existence of macrofauna by reducing the competitive edge held by dominant species. However, this effect may also be due to the balance between (1) negative effects of microalgal depletion and incidental grazing on invertebrate recruits at high densities of P. exigua, and (2) enhancement of bacteria by P. exigua leading to increased biofilm coverage on the sediment, which promotes macrofaunal recruit diversity in soft sediments. We suggest a need for caution when citing results from marine soft sediments as evidence for the intermediate disturbance hypothesis without knowledge of the promotive and inhibitory effects of the target organism.KEY WORDS: Population outbreak · Disturbance · Recruitment · Biofilms · Macrofauna · Promotive effects · Inhibitory effects Resale or republication not permitted without written consent of the publisherMar Ecol Prog Ser 398: [173][174][175][176][177][178][179][180][181][182] 2010 Lagoon on the west coast of South Africa between 1975 and1983. We also present results from a manipulative field experiment testing the effects of this starfish on community structure at more natural densities following the outbreak. P. exigua is relatively small (5 cm in diameter) and is very common on intertidal rocky shores in South Africa and Australia (Branch & Branch 1980, Jackson et al. 2009). It rarely occurs in intertidal lagoonal sandflats or other soft-sediment ecosystems, although the population in Langebaan Lagoon has been established there for at least the last 50 yr (Day 1959).Starfish are important structuring agents of invertebrate communities in rocky and coral reef ecosystems. Paine (1974) identified the keystone role of the starfish Pisaster ochraceus in intertidal rocky communities, demonstrating that its predation on mussels reduces their competitive edge, leading to increased diversity of co-occurring rock-occupying species. The coraleating crown-of-thorns starfish Acanthaster planci is a major determinant of coral reef community structure in the Indo-Pacific notorious for its devastating effects, and is regarded as a gre...

mentioning

confidence: 99%

Unexpected effects of starfish grazing on sandflat communities following an outbreak

Pillay

Branch²,

Steyn³

2010

Self Cite

“…Under natural conditions, sediments lacking C. kraussi usually have microalgal biomasses 2-to 4-fold greater than those in areas occupied by this sandprawn, while experimental manipulations of C. kraussi densities resulted in 2-to 3-fold reductions in microalgal biomass in the presence of C. kraussi (Pillay et al 2007c). Ecosystem engineering in the form of sediment turnover by other burrowing marine shrimps and prawns also reduce the microalgal biomass of surface sediments (Contessa & Bird 2004, Webb & Eyre 2004.…”

Section: Discussionmentioning

confidence: 99%

“…Sediment turnover by C. kraussi most likely buries microalgae, thus, starving them of light and nutrients required for photosynthesis (Branch & Pringle 1987, Pillay et al 2007a. Alternatively, sediment turnover may prevent the development of microbial biofilms that bind sediments, thereby enhancing sediment erodability (Pater son & Hagerthey 2001) and resulting in microalgae that were attached to the sediment being washed into the water column (Pillay et al 2007c). Under natural and experimental conditions, sediment erodability is 2-to 3-fold greater in areas with dense beds of C. kraussi relative to sediments lacking this sandprawn (Pillay et al 2007a).…”

Section: Discussionmentioning

confidence: 99%

Indirect effects of bioturbation by the burrowing sandprawn Callichirus kraussi on a benthic foraging fish, Liza richardsonii

Pillay¹,

Williams²,

Whitfield³

2012

Self Cite

The alteration of sediments by bioturbating organisms plays a major role in aquatic ecosystems, from both ecological and evolutionary perspectives. Several studies have highlighted the ability of bioturbators to alter sedimentary biogeochemical processes and community structure, but the potential influence of bioturbators on pelagic species is unexplored in marine ecology. In the present study, we investigated the direct effects of bioturbation by a southern African burrowing sandprawn, Callichirus kraussi, on primary producers (benthic microalgae) and the indirect effects on the growth of a fish (grey mullet Liza richardsonii) that consumes microalgae. A mesocosm experiment was undertaken in which similar-sized L. richardsonii at 2 densities were exposed to 3 increasing densities of C. kraussi. After 3 wk of exposure to the effects of C. kraussi, the fish were weighed and their lengths measured to calculate their physical condition and growth rates. At the termination of the experiment, the microalgal biomass and sediment turnover were measured in each mesocosm. Higher C. kraussi densities resulted in an increase in sediment turnover and caused reductions in microalgal biomass, which in turn led to a reduction of the biomass and lengths of L. richardsonii. Increasing densities of C. kraussi evidently enhance sediment turnover from burrows to the sediment surface, leading to the burial of microalgae and indirect reductions in food availability to L. richardsonii. This reduction in turn leads to metabolic losses and reductions in the growth of this fish species. These results indicate that benthic bioturbators can have strong effects on aquatic ecosystems, especially by modulating energy flow to nektonic species. KEY WORDS: Bioturbation · Food webs · Marine benthos · Sediment turnover · Benthic-pelagic coupling Resale or republication not permitted without written consent of the publisherMar Ecol Prog Ser 453: 151-158, 2012, Pillay & Branch 2011. Bioturbating organisms feature prominently in driving changes at both evolutionary and ecological scales. At the evolutionary level, burrowing species and bioturbation have been implicated in the Cambrian-substrate revolution, in which burrowers are thought to have contributed to the transition between pre-and postCambrian animal life in marine sediments (Meysman et al. 2006). Burrowing species, through their bioturbative activities, can also indirectly drive microevolutionary change that ultimately influences the evolution of novel morphology, behaviour and social interactions (Pillay 2010).At the ecological level, bioturbation influences a number of processes and properties, including nutrient fluxes, sediment granulometry and pore-water characteristics (Suchanek 1983, Lohrer et al. 2004, Meysman et al. 2006). These modifications translate into significant effects on the associated softsediment communities. Bioturbators have been shown to influence the community structure, abundance and distribution of the major benthic biotic components (Suchanek 1983, Flach...

“…EPS also facilitate trapping and retention of nutrients and organic material from the water column (van Loosdrecht et al 1990, Wotton 2004b. Substrate-associated EPS in turn play important ecological roles; they are food for invertebrates (Decho 1990), stabilise sediments, promote laminar flow of over-lying water (Paterson & Hagerthey 2001) and are important in the settlement and recruitment of benthic species (Lam et al 2005, Pillay et al 2007). All of these effects have important implications for the structuring of soft-sediment assemblages.…”

mentioning

confidence: 99%

Influence of starfish grazing on lagoonal microalgal communities: non-competitive mechanisms for unimodal effects on diversity

Dawson

Pillay²

2011

Self Cite

We quantified the effects of grazing by the starfish Parvulastra (=Patiriella) exigua on microalgal assemblages in a lagoon on the South African west coast. This starfish is common on rocky shores in South Africa and Australia, but rarely occurs on soft sediments. Although grazing is well known to be a dominant structuring agent of marine systems, the influence of grazing starfish is poorly documented. Our results indicate that at natural densities, P. exigua plays an important role in structuring soft-sediment microalgal assemblages, having no significant effect on microalgal biomass, but reducing microalgal abundance probably through consumption. Interestingly, concentrations of extracellular polymeric substances (EPS) increased with densities of P. exigua, indicating a potentially important ecological role of this starfish in enhancing carbohydrate levels on the sediment either through mucus addition or stimulation of bacterial biomass. Taxonomic richness and diversity of microalgae showed classical hump-shaped responses to increasing starfish density. Our findings are discussed in the context of the intermediate disturbance hypothesis, which proposes that disturbance promotes diversity at intermediate intensities by eliminating dominant species and allowing poor competitors to co-exist. We also present evidence for a mechanism based on non-competitive interactions to explain the promotive effects of this starfish on microalgal diversity, arising from the ability of this species to enhance sedimentary EPS levels. Our results collectively indicate that P. exigua plays an important role in regulating diversity and richness of microalgal assemblages and concur with previous assertions that this starfish plays an underestimated role in structuring intertidal systems. KEY WORDS: Extracellular polymeric substances · EPS · Diversity · Microalgae · Competition · Plant -animal interaction Resale or republication not permitted without written consent of the publisherMar Ecol Prog Ser 435: [75][76][77][78][79][80][81][82] 2011 Lubchenco & Gaines 1981). Through consumption, grazers remove competitively dominant species that monopolise habitats, thereby allowing sub-dominants to establish. However, the role of non-competitive mechanisms by which grazers promote diversity are poorly understood and reported in the literature, even though such pathways are potentially significant (Pillay et al. 2010a).From a benthic perspective, non-competitive interactions are likely to be of importance in promoting diversity in aquatic soft-sediment ecosystems, as competition and competitive exclusion have rarely been shown to be important structuring forces in these habitats (Peterson 1979, Wilson 1990. Soft sediments are 3-dimensional ecosystems, allowing organisms to partition space vertically, by burrowing, thereby potentially minimising competition for space and food (Wilson 1990, Seitz 1998, Little 2000. This is in stark contrast to the situation on hard substrata, which are 2-dimensional systems, in which competition fo...