Christine H. L. Schönberg

Ocean acidification accelerates reef bioerosion

In the recent discussion how biotic systems may react to ocean acidification caused by the rapid rise in carbon dioxide partial pressure (pCO2) in the marine realm, substantial research is devoted to calcifiers such as stony corals. The antagonistic process – biologically induced carbonate dissolution via bioerosion – has largely been neglected. Unlike skeletal growth, we expect bioerosion by chemical means to be facilitated in a high-CO2 world. This study focuses on one of the most detrimental bioeroders, the sponge Cliona orientalis, which attacks and kills live corals on Australia’s Great Barrier Reef. Experimental exposure to lowered and elevated levels of pCO2 confirms a significant enforcement of the sponges’ bioerosion capacity with increasing pCO2 under more acidic conditions. Considering the substantial contribution of sponges to carbonate bioerosion, this finding implies that tropical reef ecosystems are facing the combined effects of weakened coral calcification and accelerated bioerosion, resulting in critical pressure on the dynamic balance between biogenic carbonate build-up and degradation.

Bioeroding sponges common to the central Australian Great Barrier Reef: Descriptions of three new species, two new records, and additions to two previously described species

A large collection of bioeroding sponges was obtained from the following reefs of the Central Great Barrier Reef (GBR), Australia: Myrmidon, John Brewer, Rib and Pandora Reefs, and Pelorus, Orpheus, Fantôme, Great Palm, Acheron and Magnetic Islands. As many descriptive characters as possible were used including skeleton and tissue characters, but also field observationsin situ and bioerosion traces. Bioerosion traces are very similar between species; nevertheless, they yield extra information on genus level. The following sponges are described in detail:Cliona tinctoria sp. nov.,Cliona orientalis, new record for the GBR,Pione caesia sp. nov., incertae sedis,Cliothosa hancocki, new record for the GBR,Zyzzya criceta sp. nov. Descriptions of selected characters of two previously described GBR bioeroding sponges,Cliona celata andAka mucosa, are amended.C. orientalis belongs into a species group previously named as “Cliona viridis complex”, species of which are difficult to discern from each other.C. orientalis can be recognized by its spiraster morphology, i.e. by their multisplit actines along the convex side of a spiraling spiraster shaft. Summarizing tables with descriptive characters for all described species and for species of the “Cliona viridis complex” are given.

A Standardised Vocabulary for Identifying Benthic Biota and Substrata from Underwater Imagery: The CATAMI Classification Scheme

Imagery collected by still and video cameras is an increasingly important tool for minimal impact, repeatable observations in the marine environment. Data generated from imagery includes identification, annotation and quantification of biological subjects and environmental features within an image. To be long-lived and useful beyond their project-specific initial purpose, and to maximize their utility across studies and disciplines, marine imagery data should use a standardised vocabulary of defined terms. This would enable the compilation of regional, national and/or global data sets from multiple sources, contributing to broad-scale management studies and development of automated annotation algorithms. The classification scheme developed under the Collaborative and Automated Tools for Analysis of Marine Imagery (CATAMI) project provides such a vocabulary. The CATAMI classification scheme introduces Australian-wide acknowledged, standardised terminology for annotating benthic substrates and biota in marine imagery. It combines coarse-level taxonomy and morphology, and is a flexible, hierarchical classification that bridges the gap between habitat/biotope characterisation and taxonomy, acknowledging limitations when describing biological taxa through imagery. It is fully described, documented, and maintained through curated online databases, and can be applied across benthic image collection methods, annotation platforms and scoring methods. Following release in 2013, the CATAMI classification scheme was taken up by a wide variety of users, including government, academia and industry. This rapid acceptance highlights the scheme’s utility and the potential to facilitate broad-scale multidisciplinary studies of marine ecosystems when applied globally. Here we present the CATAMI classification scheme, describe its conception and features, and discuss its utility and the opportunities as well as challenges arising from its use.

The sponge gardens of Ningaloo Reef, Western Australia

Preliminary results from biodiversity surveys in the deeper waters of Ningaloo Marine Park, Western Australia revealed that while much of the area is composed of sediments and rhodolith fields with low densities of macro- epibenthos, locally dense and extensive filter feeding communities exist. They were distinctly dominated by demosponges, both in biomass and diversity. A subsample of dominant taxa determined by fresh weight yielded 155 different demosponge species from over 350 transects between 18-102 m depth. Data from three successive years of sampling indicated that only a few species were ubiquitous, suggesting that as minor species are identified the cumulative species list will significantly exceed the present species record. This implies greatly enhanced biodiversity values associated with Ningaloo Marine Park, complementing records attributed to the shallow coral reef environment. The richness of the observed filter feeding communities adds additional weight to the increasing perception of Australia as a global hotspot for Porifera biodiversity.

Estimating the extent of endolithic tissue of a great barrier reef clionid sponge

Data from two studies of growth and bioerosion of the Australian spongeCliona orientalis were used to investigate methods to quantify endolithic clionid sponge tissue in experimental blocks made from 8 massive Great Barrier Reef coral species and fromTridacna squamosa shells. Three radiography techniques were tried: conventional X-radiography, phase-contrast radiography, and computer tomography. Radiographs were compared to images of sponge tissue manually traced onto transparent sheets: endolithic sponge tissue in 1 cm thick blocks was made visible by fixing the blocks in front of strong light for tracing. None of the three radiography techniques were found to be satisfactory to estimate the extent of endolithic clionid tissue, unless the substrate was very dense and its structure comparatively homogeneous. Otherwise, delicate sponge tissue strands were often obscured by substrate structures. This was especially the case around the margins of the sponge colony, which were not clearly resolvable. Additionally, at all radiography settings tried, sponge tissue had very little attenuation so that it could not be distinguished from empty pores in coral skeleton. Radiography was thus found to be largely unsuitable for studying endolithic tissue of Clionidae excavating small pores. Computer tomography may have considerable significance in qualitative studies, however, as this technique lowers ambiguity by permitting several observations with smaller slice thickness. Manual tracing of endolithic tissue worked surprisingly well and provided data of about 90% accuracy. Tracing is more work-intensive than radiography, but low in cost and does not require specific technology. Given a material thickness of 1 cm or less, it is non-intrusive, i.e. studied material will not be lost. Areas of superficial and endolithic sponge tissue were highly significantly proportional to each other. Hence, at least for C.orientalis, the areas of superficial tissue can be used to estimate endolithic extent without damaging the substrate. Calculation models are given. It is likely that such a correlation is a general phenomenon for clionid sponges. Use in the field is restricted by problems with species identification.

Bioerosion: the other ocean acidification problem

&NA; Bioerosion of calcium carbonate is the natural counterpart of biogenic calcification. Both are affected by ocean acidification (OA). We summarize definitions and concepts in bioerosion research and knowledge in the context of OA, providing case examples and meta‐analyses. Chemically mediated bioerosion relies on energy demanding, biologically controlled undersaturation or acid regulation and increases with simulated OA, as does passive dissolution. Through substrate weakening both processes can indirectly enhance mechanical bioerosion, which is not directly affected by OA. The low attention and expert knowledge on bioerosion produced some ambiguous views and approaches, and limitations to experimental studies restricted opportunities to generalize. Comparability of various bioerosion and calcification rates remains difficult. Physiological responses of bioeroders or interactions of environmental factors are insufficiently studied. We stress the importance to foster and advance high quality bioerosion research as global trends suggest the following: (i) growing environmental change (eutrophication, coral mortality, OA) is expected to elevate bioerosion in the near future; (ii) changes harmful to calcifiers may not be as severe for bioeroders (e.g. warming); and (iii) factors facilitating bioerosion often reduce calcification rates (e.g. OA). The combined result means that the natural process bioerosion has itself become a “stress factor” for reef health and resilience.

Happy relationships between marine sponges and sediments – a review and some observations from Australia

Being sessile filter feeders, sponges may be disadvantaged by sediments in many ways, e.g. through clogging and burial. However, in order to correctly recognize negative effects of sediments in the field, natural relationships of sponge taxa adapted to a life with sediments need to be understood. The present publication reviews available literature and provides observations on natural and beneficial interactions of sponges with sediments, distinguishing several strategies: (1) Saving energy through sediment incorporation, reducing or replacing spicule production commonly occurs in keratose, verongimorph, tethyid and poecilosclerid sponges, which often received scientific names referring to sediments. (2) Forming sediment crusts externally or embedded in surface tissues reinforces outer layers, provides shade, and for external crusts camouflage and shelter from spongivory and desiccation. External crusts often occur in the tethyids and axinellids, while surface armour is most common in keratose sponges. (3) Anchoring in soft sediments provides a selective advantage for space colonization. This is mainly achieved in the hexactinellid, polymastiid and spirophorine sponges by using spicules (predominantly in deeper water), commonly in endopsammic sponges by rootlets, basal agglutination and basal incorporation of particles, and in various groups by attachment to buried materials (shallow water). (4) Living at least partially embedded in sediments (psammobiosis) appears to be best developed in Oceanapia spp. and bioeroding sponges, generates shelter from various external conditions and reduces the risk of spongivory. Typical morphological characters of sediment-adapted sponges are thus sediment skeletons and surface crusts (reinforcement), stalks and fistules (elevation above sediments), spicule tufts and root-systems (anchoring).

Monitoring Bioeroding Sponges: Using Rubble, Quadrat, or Intercept Surveys?

Relating to recent environmental changes, bioerosion rates of calcium carbonate materials appear to be increasing worldwide, often driven by sponges that cause bioerosion and are recognized bioindicators for coral reef health. Various field methods were compared to encourage more vigorous research on bioeroding sponges and their inclusion in major monitoring projects. The rubble technique developed by Holmes et al. (2000) had drawbacks often due to small specimen sizes: it was time-costly, generated large variation, and created a biased impression about dominant species. Quadrat surveys were most rapid but overestimated cover of small specimens. Line intercepts are recommended as easiest, least spatially biased, and most accurate, especially when comparing results from different observers. Intercepts required fewer samples and provided the best statistical efficiency, evidenced by better significances and test power. Bioeroding sponge abundances and biodiversities are influenced by water depth, sediment quality, and most importantly by availability of suitable attached substrate. Any related data should thus be standardized to amount of suitable substrate to allow comparison between different environments, concentrating on dominant, easily recognized species to avoid bias due to experience of observers.

Self-cleaning surfaces in sponges

As filter feeders, sponges are thought to be at risk in high sediment environments, but many species can tolerate exposure to sediments or benefit from it (Cerrano et al. 2007). Some sponges can maintain clean surfaces even in intensive sedimentation (Fig. 1A–D). Apart from descriptions of active cleaning processes, almost nothing has yet been published to explain this, but clean sponges are often densely ‘microhispid’ (Boury-Esnault 2002; Bell 2004). ‘Hispidity’ occurs when spicules project from the surface, macroscopically giving the sponge either a velvety or a bristly appearance (Fig. 1E–I). Depending on the arrangement, this may create a ‘lotus effect’ through surface roughness that prevents adherence of dirt and induces passive self-cleaning, not requiring energy expenditure (e.g., Blossey 2003). According to present observations, this apparently works best where spicules are densely set and only protrude from the surface for a short distance (≤ 100 μm; fakir’s carpet; Fig. 1E–G). The opposite effect results when hispidity is pronounced, with spicules emerging far from the surface, or where hispidity is widely spaced, trapping debris as external crusts (commonly 1–2 mm; pin cushion; Fig. 1H–I). The effect may be changed by contraction of the sponge tissues, during which the protruding spicules may be flattened against the surface. Clionaid species such as Cliona orientalis can alternatively appear clean (expanded) or ‘dusty’ (contracted). As some clionaid species harbour photosynthetic symbionts, regulating the sediment cover may be important to optimise irradiation (Schönberg and Suwa 2007). In moderate sedimentation, sponges with self-cleaning surfaces will have a selective advantage compared to other species. However, passive self-cleaning may quickly fail in settings of intensive sediment deposition, such as in dredging plumes. C. H. L. Schönberg Australian Institute of Marine Science, 39 Fairway, Crawley, WA 6009, Australia

Coral bleaching in turbid waters of north-western Australia

We report severe bleaching in a turbid water coral community in north-western Australia. Towed still imagery was used for a benthic survey near Onslow in March 2013 to assess thermal stress in hard and soft corals, finding 51–68% of all corals fully bleached in 10–15-m water depth. Tabulate or foliaceous Turbinaria was the locally most abundant hard coral (46%), followed by massives such as faviids and poritids (25%) and encrusting coral (12%), thus over 80% of the local corals could be considered to be bleaching resistant. All coral groups were bleached in similar proportions (massive hard corals 51%<soft corals 60%<encrusting hard corals 62%<Turbinaria 62%<‘others’ 68%). NOAA data and environmental assessments suggest previous recurrent thermal stress throughout the last 10 years in the study area. On the basis of these records this stress apparently changed the community structure from bleaching vulnerable species such as Acropora, leaving more tolerant species, and reduced coral cover. We could see no evidence for adaptation or acclimation of corals in this area. Towed still imagery was found to be a suitable means for rapid and large-scale bleaching studies in shallow, turbid areas where diving can be difficult or impossible.