African Journal of Marine Science 2011, 33(2): 327–332 Copyright © NISC (Pty) Ltd Printed in South Africa — All rights reserved AFRICAN JOURNAL OF MARINE SCIENCE ISSN 1814–232X EISSN 1814–2338 doi: 10.2989/1814232X.2011.600433

Short Communication

Tube-forming enhance invertebrate diversity and abundance in sandy sediments of Mozambique, Africa

MS Thomsen1,2*, MF Muth3 and KJ McGlathery3

1 Marine Department, National Environmental Research Institute, University of Aarhus, PO Box 4000, Roskilde, Denmark 2 School of Plant Biology, University of Western Australia, Crawley 6009 WA, Australia 3 Department of Environmental Sciences, University of Virginia, 291 McCormick Rd, Clark Hall, Charlottesville, VA 22904, USA * Corresponding author, e-mail: [email protected]

Manuscript received March 2011; accepted May 2011

In marine soft-bottom systems, polychaetes can increase complexity by constructing rigid tubes (e.g. several onuphid ) that contrast with surrounding topographically flat sediments. These structures can provide predation refuges and increase larval settlement and thereby increase the richness and abundance of fauna. We collected invertebrate samples from an intertidal flat with low onuphid tube density (2.7 m–2) in Mozambique and document that more organisms (70 times higher mollusc abundances) and more species (15 times more mollusc species) were found associated with solitary tubes of an onuphid compared with surrounding sand . These results are in agreement with tube versus sand comparisons from soft-bottom systems in the North Atlantic where polychaete tube densities are often much higher.

Keywords: habitat formation, onuphid polychaete, species richness, western Indian

Introduction

Species that form or modify habitat, often referred to as (Thomsen et al. 2010), and predation refugia (Woodin 1981, ecosystem engineers (Jones et al. 1997, Berke 2010), can Bell and Woodin 1984). Regardless of the mechanisms of be of fundamental ecological importance in influencing facilitation, these studies suggest that solid polychaete species abundances, community composition and biologi cal tubes that emerge from the sediment enhance diversity, yet diversity (Berke 2010, Thomsen et al. 2010). Numerous tests from other habitats and biogeographical regions would marine habitat-formers build external physical structures be valuable in verifying the generality of this pattern. Here, such as shells or tubes that can provide living space and we test if the faunal richness and abundances are higher shelter from predators. In soft-bottom habitats, tube-building around the tube structures of an onuphid polychaete from polychaetes represent an important group of marine Mozambique, Africa, compared with surrounding barren organisms that build such external structures. Many studies sandy habitats. from the North Atlantic have shown that faunal diversity is higher in the vicinity of polychaete tubes that emerge Material and methods above the sediment, in particular to those belonging to the genera and , compared with sediments Study site lacking large tube structures (Woodin 1978, Bell and Coen The study was conducted on intertidal sand-flats on Inhaca 1982, Luckenbach 1984, Callaway 2003, Van Hoey et Island, Mozambique, in March 2007. Tides are semidiurnal al. 2008). Positive effects of tube-forming polychaetes on (1–4 m) and local populations of an onuphid tube-building faunal communities may be caused by turbulence around polychaete exhibit patchy distributions around the island, the tubes that increase contact between larvae in the being most common on the extensive tidal sand-flats in the water column and physical structures (Luckenbach 1987), sheltered southern bay (Kalk 1995, MFM pers. obs.). This provision of attachment space for settling organisms (Bell species is likely to be D. cuprea (Bosc 1802), but could also and Coen 1982, Bell 1985), bioirrigation or nutritional supply be D. neapolitana Day 1960, D. musseraensis (Audouin (Mayer et al. 1995, Phillips and Lovell 1999), incorporated and Milne-Edwards 1833), Onuphis quinquedens Day 1951 plant material that provides extra habitat for invertebrates or O. holobranchiata Marenzeller 1859. Ultimately, DNA

African Journal of Marine Science is co-published by NISC (Pty) Ltd and Taylor & Francis 328 Thomsen, Muth and McGlathery analysis is needed to verify the species’ identity (Arias top portion of the tube that emerges above the sediment et al. 2010, Pires et al. 2010). We refer here conserva- surface and was ornamented with shell and plant debris tively to the species as an ‘onuphid polychaete’. Data (‘tube-cap alone’) (Brenchley and Tidball 1980, Thomsen were collected from two sandy sites, separated by 1.5 km and McGlathery 2005). The comparison between bare sand (Site 1: 26.054300° S, 32.930390° E; Site 2: 26.061650° S, vs tube-cap + sand represents the total ecological effect 32.919850° E). Temperature loggers recorded an annual associated with the presence of the onuphid polychaete, range of 10.8–46.5 °C on the sediment surface at both whereas the bare sand vs tube-cap alone contrasts how sites, with extreme values recorded during low tides. The fauna associated with a small hard-structure (that increases sediment porosity (g cm–3), bulk density g ml–1) and organic topographic heterogeneity) may differ from the flat sandy contents (% ash-free dry weight [AFDW] ± SD) were habitat. Note that, because the tube-cap densities are relatively similar between the sites (0.38 ± 0.02 vs 0.46 ± low (2.7 m–2), the collection of a solitary tube-cap also 0.01; 1.42 ± 0.02 vs 1.36 ± 0.01; 1.19 ± 0.04 vs 1.44 ± 0.09 represents all tube-cap material that can be found in any respectively; n = 3 randomly collected samples). The tubes 0.005 m2 area (corresponding to the area of the cores, i.e. it at the two sites were well decorated with shell fragments is meaningful to compare tube-cap alone to core samples). (Figure 1), sometimes covering up to 75% of the tube. Small By showing data from the two onuphid habitats, our results amounts of detritus were also found inserted into can also be compared to other studies that have sampled the tubes, with little algae present. These fragments were one or both habitats (e.g. Woodin 1978, Bell and Coen generally inserted edge-wise and embedded in a tough, 1982, Luckenbach 1986, Nyberg et al. 2009, Thomsen leathery parchment. Tubes were largely hook-shaped, with et al. 2009, 2010). We randomly collected 10 tube-caps larger fragments found towards the tip of the tube. The two alone from each site in March 2007 by a swift hand motion, sites had similar tube densities: 2.7 m–2 (SE = 0.4, n = 30, clipping the cap at the sediment surface with the fingers. 0.25 m2 random quadrats collected per site), cap width The cap was immediately transferred to a plastic bag to (inner diameter): 0.72 cm (SE = 0.32, n = 15 randomly minimise the loss of associated motile organisms (Nyberg collected caps per site) and cap length: 4.13 cm (SE = 0.11, et al. 2009). Circular cores (8 cm inner diameter and 10 cm 15 randomly collected caps per site); t-tests, p > 0.13, all depth) were collected from bare sand (n = 5 per site) and measured with calipers. These tubes generally resemble centred on a single tube (tube-cap + sand, n = 5 per site). tubes of Diopatra species. More general information on the Individual samples were separated by >0.5 m, the three location is provided in Kalk (1995). habitats were scattered between each other, and the sites were covered by a minimum of 10 cm water at the time of Sample collections collection. Sand was removed from cores using a 1 mm Sandy habitats (‘bare sand’) were compared to two types sieve. Caps were dissected gently by hand and tweezers. of onuphid habitats; ‘entire’ vs ‘partial’ onuphid habitats. All organisms were immediately transferred into 20 ml glass The entire onuphid habitat included the tube that is buried vials and preserved in a solution of 70% isopropyl alcohol in the sediment, the tube-cap that emerges above the for later analysis. Only a small amount of aquatic plant sediment surface, and the surrounding sandy matrix (‘tube- material was found incorporated into the tubes (g wet weight cap + sand’). The partial habitat only included the 4–5 cm of plant material incorporated per tube ± SE; =

Figure 1: Tube-caps with incorporated shells that protrude above the sediment. The tube-caps provide a topographic contrast to the surrounding flat sediments. The caps resemble those of . The average inner diameter width and length are 0.72 and 4.13 cm respectively African Journal of Marine Science 2011, 33(2): 327–332 329

0.132 ± 0.055 and 0.447 ± 0.095, and macroalgae = 0.010 ± for polychaetes this was only evident at Site 2 (Figure 0.006 and 0.027 ± 0.013, for Sites 1 and 2 respectively, n = 3a–c; 6.1, 71.0 and 1.5 times higher densities of all-fauna, 20 per site). Our focus during this study was on effects on molluscs and polychaetes respectively associated with the fauna; the plant material was therefore excluded from the two onuphid habitats compared to bare sand). The tube-cap data analysis. alone habitat had higher abundances of mollusc and all-faunal groups compared with the tube-cap + sand habitat Data analysis — a counter-intuitive pattern caused by a few tube-cap alone PERMANOVA, a permutation-based analogue to multivar- samples that contained high abundances of bivalves (small iate analysis of variance (MANOVA) (Anderson et al. 2008), juveniles; MFM pers. obs.). There were no significant effects was used to test for effect of habitat (fixed factor) and site of habitat on the abundance of crustaceans or , (random factor) on the multivariate invertebrate assemblage which was in part due to many samples containing no individ- structure. Data were fourth-root transformed to downscale uals. However, inspection of the graphs suggested a trend the importance of highly abundant species, and the sample that followed the other results; higher abundances were resemblance matrix was calculated with the Bray–Curtis observed associated with tube-caps alone and tube-caps + similarity coefficient, based on 4 999 permutations (Anderson sand compared with the bare sand habitat (Figure 3d–e). 2001a, 2001b). Multivariate effect of habitat was visual- This trend was significant using the Mann-Whitney test: ised with a non-metric multidimensional scaling plot (MDS). the combined abundance of echinoderms and crustaceans PERMANOVA and MDS were calculated using the PRIMER was significantly higher when the two onuphid habitats software package (Anderson et al. 2008). Factorial ANOVA were merged and contrasted with the bare sand habitat (p = was used to test for effects on taxonomic richness and the 0.002). The tests of taxonomic richness mirrored the tests total abundances of all fauna. Data were not conducive to of abundances, except that tube-cap alone and tube-cap + ANOVA tests on responses of individual taxa due to high data variability with many zero values. Instead, taxa were analysed for ‘all fauna’ and by major taxonomic groups; Stress = 0.22 Bare sand molluscs, polychaetes, crustaceans and echinoderms Tube-cap alone (the four groups constituted >98% of counted taxa). The Tube-cap + sand univariate test variables were Log (x+1) transformed when necessary to meet ANOVA assumptions of variance hetero- geneity as tested with Cochran’s test. Significant effects of habitat were followed by Student–Newman–Keuls tests (SNK) (Underwood 1997). Echinoderms and crustaceans were uncommon in most samples and these abundance and richness data could therefore not be transformed to variance homogeneity. We therefore also conducted robust Mann-Whitney’s rank tests on combined richness or abundances of echinoderms and crustaceans, pooling site data and regrouping the three habitats into two (two onuphid habitats vs bare sand).

Results Figure 2: Two-dimensional, non-metric, multidimensional scaling

There were significant effects of habitat (F2,34 = 4.72, p = plot showing faunal assemblage relationships between bare sand, tube-cap alone, and tube-cap + sand (three overlapping points are 0.006) and site (F1,34, p = 0.002) on assemblage composi- tion, consistent between sites (habitat × site interaction; denoted as thick arrow and two overlapping points as thin arrow) samples F2,34 = 1.60, p = 0.081). Pairwise comparisons showed that the bare sand habitat was different from both tube-cap alone (p = 0.005) and tube-cap + sand habitats (p = 0.036), Table 1: Summary of p-values from ANOVA tests. Analysis was whereas the two latter habitats did not differ (p = 0.240). The conducted on Log(x+1)-transformed data for organisms marked by *. MDS plot in Figure 2 shows a weak tendency for tube-cap Significant results (p > 0.05) are in bold alone, tube-cap + sand and bare sand samples to cluster in the upper, lower and left sectors of the plot respectively, with a few outliers dispersed in the bottom-right corner Factor Test organism Habitat Site Habitat × Site Abundance All-fauna* 0.045 0.126 0.231 (Figure 2). Representation of the multivariate assemblage Molluscs* 0.018 0.092 0.455 structure in 3-d space was slightly clearer (stress = 0.15). Polychaetes 0.689 0.383 0.011 There were no significant site-effects on any taxonomic Crustaceans 0.242 0.204 0.734 group response (Table 1). However, there were significant Echinoderms 0.296 0.188 0.368 effects of habitat on the abundances of all fauna combined Richness All-fauna 0.049 0.254 0.061 and molluscs, and a significant habitat × site interaction on Molluscs* 0.023 0.115 0.543 polychaete abundances. In each case, there were higher Polychaetes* 0.591 0.417 0.004 abundances associated with tube-cap alone and tube-cap + Crustaceans 0.120 0.404 0.573 sand habitats compared with the bare sand habitat, although Echinoderms 0.250 0.197 0.543 330 Thomsen, Muth and McGlathery

Abundances Richness sand habitats had similar values for all-fauna and molluscs (a) All-fauna (f) All-fauna (Figure 3f, g). Overall, the richness of all-fauna, molluscs a 20 Site 1 a 8 and polychaetes were respectively 2.6, 17.5 and 1.1 times Site 2 higher associated with the two onuphid habitats compared 15 6 to bare sand. Similarly, the Mann-Whitney tests showed that b richness of echinoderms and crustaceans (combined) was 10 4 higher when the two onuphid habitats were merged, and b contrasted with the bare sand habitat (p = 0.002). 5 c 2 Discussion 18 (b) Molluscs (g) Molluscs 3 a a As hypothesised, we found higher faunal abundance and 15 richness associated with the onuphid habitats compared with 12 2 the surrounding sandy habitat. These results were consistent across broad taxonomic groups, including the less common 9 b echinoderms and crustaceans. Similar findings have been 6 1 observed in the North Atlantic for Diopatra cuprea and Lanice b 3 conchilega habitats (Woodin 1978, Bell and Coen 1982,

) c

2 Callaway 2003, Van Hoey et al. 2008, Thomsen et al. 2010). − (c) Polychaetes (h) Polychaetes However, most of these studies compared barren sediments

7 5 ) a 2 to tube aggregations collected from high-density tube flats. 6 a − 4 We found that solitary onuphid tubes from low-density tube 5 flats in Mozambique can also have strong effects on inverte- 4 3 brate communities. Due to the correlative nature of our 3 b b study, it is not possible to identify the specific mechanisms

b 2 no. 0.005 m b ( by which positive effects occur. Likely mechanisms include 2 1 provision of predation refugia, enhanced habitat for larval 1 settlement and recruitment, or, more broadly, provision of a TAXA TAXA (d) Crustaceans (i) Crustaceans general suitable habitat to live in or around for a broad range 4 1.5 of fauna (particularly for molluscs) (Woodin 1978, 1981, Bell DENSITY (individuals 0.005 m DENSITY 1.2 and Woodin 1984, Dudley et al. 1989, Zuhlke 2001). 3 The effects of polychaete tubes will likely vary with tube 0.9 density. Most previous studies have compared barren 2 sediment habitats to habitats composed of dense-tube 0.6 aggregations (e.g. 6–12 tubes in a core) (Luckenbach 1984, 1 0.3 1987, Zuhlke et al. 1998, Callaway 2003). However, the few studies that have tested for density effects have indicated (e) Echinoderms (j) Echinoderms an impact threshold between 1 and 6 tubes for Diopatra 1.8 0.8 cuprea within 0.0014 m2 cores (Woodin 1978, 1981, Bell and 1.6 Woodin 1984). Recent studies (Callaway 2006, Thomsen 0.6 et al. 2010) have shown that solitary tubes can also impact 1.2 invertebrate communities, and our results here support this 0.4 notion. The effect on invertebrates may also vary with tube 0.8 density on larger landscape scales. Only few studies have 0.2 0.4 combined analysis of impacts of tubes with random surveys of tube densities to quantify typical landscape densities — all studies for L. conchilega (Callaway 2006, Rabaut et al. 2007, Van Hoey et al. 2008). However, it is likely that most previous Diopatra studies have been conducted on Tube-capaloneTube-cap Tube-capaloneTube-cap Bare sand + sand Bare sand + sand high-density flats because dense tube aggregations have HABITAT been sampled and because this has been stated in some papers (e.g. Woodin 1981, Luckenbach 1984). Figure 3: Abundances and taxonomic richness of all-fauna, The present results supplement previous studies in showing molluscs, polychaetes, crustaceans and echinoderms associated that solitary onuphid tubes from low-density landscapes can with bare sand, tube-cap alone, and tube-cap + sand habitats respectively. Abundance and richness are shown per core (0.005 m2) also have strong effects on invertebrate communities (as for bare sand and tube-cap + sand samples and per individual cap documented for L. conchilega in Callaway 2006). We did for tube-cap alone samples. Significant effects between habitats are not test for temporal effects of onuphid polychaetes, but marked with different letters (a, b, c; based on SNK-tests). Note that observed that many of the molluscs were small individuals Mann-Whitney tests showed that both the abundance and richness (probably new recruits) (Dudley et al. 1989). To understand of crustaceans and echinoderms combined differed between the two long-term effects, future studies should also quantify faunal onuphid habitats (pooled) and the bare sand habitats size structures, size-dependent survival rates, if fauna African Journal of Marine Science 2011, 33(2): 327–332 331 migrate out to adjacent sediments during ontogenesis, or if Berke SK. 2010. Functional groups of ecosystem engineers: fauna are consumed by predators. Although our results were a proposed classification with comments on current issues. collected from a single point in time, they indicate that tubes Integrative and Comparative Biology 50: 1–11. may drive complicated foodweb processes in sedimentary Berke SK, Woodin SA. 2008. Tube decoration may not be cryptic for Diopatra cuprea (Polychaeta: ). Biological Bulletin systems, e.g. by providing indirect linkages between the 214: 50–56. larvae in the water column and consumption by predators. Brenchley GA, Tidball JG. 1980. Tube cap orientations of Diopatra Our results differ from recent studies from the North Atlantic cuprea Bosc Polychaeta, the compromise between physiology where Diopatra create seaweed gardens around their and foraging. Marine Behaviour Physiology 71: 1–14. tube-caps (e.g. Thomsen 2004, Berke and Woodin 2008). Callaway R. 2003. 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