Tropical coral reefs are among the most diverse ecosystems on the planet. Studying biodiversity in these environments is important not only for gaining knowledge about the variety of organisms present, but also for understanding how the environment shifts and is affected by climate change and anthropogenic stresses. Recent studies show that between 33 and 91 percent of marine species are currently undescribed [1
], making baseline data for studies involving environmental change very difficult to obtain. The majority of these undescribed species are invertebrates from tropical coastal environments [2
Sponges are often dominant members of sessile macrobenthos, but they are also often overlooked in biodiversity studies (or lumped into very coarse taxonomic groups) because they are character-poor and typically require microstructural study for identification, thus are taxonomically challenging [3
]. Nevertheless, sponges serve as one of the most diverse components of reef systems [3
], with their complex structure providing a range of microhabitats for associated epifauna and infauna. Pearse [7
] describes large sponges with substantial internal canals as “veritable living hotels”. Several studies show a positive correlation between sponge volume and macrofaunal abundance or species richness [8
]. Others emphasize morphological features, particularly the importance of large and distinct internal canals [12
]. In many cases, macrofauna take refuge in sponges for protection from predators or for camouflage, thereby increasing their chances of survival [18
]. Some species spend most of their life cycles inside their hosts [19
] and may use them as breeding grounds [11
In addition to protection, many symbionts rely on sponges for food either directly or indirectly. Sponges may provide food indirectly by creating water flow that can be utilized by associated suspension feeders, including some polychaetes, barnacles, porcelain crabs, and brittle stars [20
]. Fish may receive both food and oxygen from water currents [22
]. Sponges are a direct food source for both resident and roving predators, including nudibranchs [23
], various shelled gastropods (e.g., cypraeids, triphorids, pleurotomariids, fissurellids; [24
]), chitons [14
], sea stars [25
], and snapping shrimps [26
], the latter having specialized mouthparts and claws for feeding on their hosts. The regenerative properties of sponges may provide a continual food source for this type of grazing species [26
]. Although most symbiotic relationships with sponges seem to be commensal or parasitic, it is possible for the hosts to benefit as well. For example, in what Swain [27
] suggests is a mutualistic association, zoanthid colonization of some reef sponges increases host growth and function. The bathsponge Spongia
sp. and the bivalve Vulsella vulsella
have what has been termed a “filtering mutualism” during which sponge hosts use the exhaled water of the bivalves to increase their own filtering rates [28
]. Snapping shrimps defend their sponge hosts, as available habitats may be scarce [29
]. However, the nature of most relationships is not fully understood and requires further examination.
The macrofaunal community composition and diversity associated with a single sponge species may change between different sites or reefs of a general region [7
]. Westinga and Hoetjes [8
] showed no difference in the overall number of macrofauna, but did find that the abundances of various taxa changed among locations. Abdo [20
] suggested predator/prey interactions as the cause of macrofaunal composition and density differences while Voultsiadou-Koukoura et al. [30
] suggested the influence of environmental factors such as total vegetation cover and exposure on macrofaunal diversity.
In addition to promoting biodiversity, sponges themselves are diverse and abundant on coral reefs, and important players in space competition. In the Caribbean, sponges may rival coral both in terms of abundance [3
] and biomass [31
]. While coral abundance has been declining through recent decades, the abundance of some sponges has been increasing [32
]. These changes are commonly attributed to high coral mortality due to runoff, overfishing, disease, and bleaching, compared with the release in predation pressure as a result of overfishing and resilience in many sponges (e.g., [35
]). Bell et al. [32
] proposed the potential for sponges to replace coral reefs in some locations as a result of ocean acidification and rising sea surface temperatures. As sponges are an under-appreciated group hosting complex communities of rich biodiversity, it is becoming increasingly important to establish baselines and study the impacts of changing ocean conditions on sponges and their role as habitats to marine communities.
The Red Sea is a region of high biodiversity with levels of endemism recently found to be even higher than previously thought (e.g., [36
]). For fishes, annelids, arthropods, and tunicates, >10% of the Red Sea species are endemic, and more than 60 endemic species have been described in the past two decades [36
]. Increased research efforts in some Red Sea sites, combined with studies utilizing molecular-morphological approaches, are likely responsible for this enhanced understanding of regional biodiversity. The Red Sea is a unique body of water with extremely high temperatures (20–32 °C) and salinity (37–42‰) [38
]. Despite these characteristics, the Red Sea remains an understudied region. The global challenge of the lack of sponge research is only accentuated in the Red Sea. As of 2013, the number of studies conducted on sponges in the Red Sea was approximately four times lower than that in the Great Barrier Reef system and approximately seven times lower than that in the Caribbean [39
]. From those studies in the Red Sea, the majority occurred inside the Gulf of Aqaba, and only two of those outside the gulf involved studies of symbiotic interactions of sponges with associated macrofauna [19
]. Although sponge cover is much lower in the Red Sea and other parts of the world than in the Caribbean (summarized by Pawlik et al. [41
]), sponges play important functional roles in all locations.
The aim of this study is to assess the patterns of community composition of macrofauna associated with Stylissa carteri
in the central Saudi Arabian Red Sea. We use DNA barcoding techniques to estimate the number of symbiotic species in these taxonomically challenging groups. Our study focuses on S
], an abundant and readily-identifiable sponge in coastal waters of the Red Sea, with a complex three-dimensional morphology. Its characteristic folds and ridges form canals and protected areas which, together with its water vascular system, offer a potential habitat for many symbionts. The diversity of epifauna and infauna were examined on a fine scale, across various ecological gradients. We hypothesized a change in the macrofaunal communities of S. carteri
across both a cross-shelf gradient and an even finer-scale difference of wave exposure. Offshore reefs in coastal Red Sea waters are normally characterized by near-vertical reef walls surrounded by deep water (i.e., 100s of meters deep). Some midshelf reefs have a similar structure, but are positioned on the continental shelf and have surrounding water depths ranging from ~30 m to ~80 m. Inshore reefs of the central Red Sea tend to be located in shallower water and may not have prominent wall structures. Inshore reefs, closer to the dry, dusty terrains on the coast, frequently have higher levels of turbidity than the offshore reefs and the oligotrophic waters of the Red Sea. The seaward side of a reef (typically the western side of Saudi Arabian reefs) is more exposed to wave action than the sheltered side. The leeward side of Saudi Arabian reefs may have less vertical reef structures than the windward (i.e., exposed) side, especially on midshelf and inshore reefs. The environmental differences are known to be associated with changes in fish and benthic community composition along this gradient [43
], but the response of communities that live protected on or inside a host has never been investigated. We hypothesize that differences in a combination of factors such as wave energy, turbidity, ecological conditions, and the associated general reef community changes across ecological gradients also affect the distribution of poorly studied host-associated fish and invertebrates. The results of this study provide valuable information concerning the role of S. carteri
as a host and its potential role in promoting or maintaining biodiversity in these coral reef systems.
This study used DNA barcoding techniques to examine the macrofaunal communities associated with Stylissa carteri
in the central Red Sea to gain knowledge of how these communities change at a local scale. The 937 successfully-sequenced macrofauna individuals collected from 99 sponges were clustered into 146 OTUs from eight phyla. While there is no ‘perfect’ barcode marker, COI has proven to be a very valuable marker for a wide range of taxa. The low percentage of OTUs that received a species-level match (6.8%) in GenBank likely indicates the large amount of work still needed to characterize and barcode host-associated macrofauna in the Red Sea and globally [58
]. Significant differences in community composition were found along the cross-shelf gradient, but not the finer difference of exposure to wave action. Inshore reefs seemed particularly different from the other reef classifications, showing a higher relative abundance of macrofauna from Ophiurida, Perciformes, and various Mollusca. S
abundance in the study area generally showed a gradient as well, increasing with proximity to shore.
The changes in the macrofaunal community composition of S. carteri across an inshore–offshore gradient may be attributed to a number of environmental factors. Samples collected from the offshore reefs originated from significantly greater depths on average than those collected from all other sites. However, the largest distinction between shelf positions appears to occur between inshore reefs and the rest, providing some assurance that depth is not the primary cause of macrofaunal community composition shifts reported here. The similar vertical structure of offshore and midshelf reefs may contribute to the close grouping of these samples and similarity in the relative abundance of macrofaunal orders between offshore and midshelf samples. Although some macrofauna are found inside the sponge hosts (e.g., many worms and shrimps), others are found primarily on the outer surface (e.g., many crabs and echinoderms). Therefore, epifauna are subject to surrounding environmental conditions. Infauna which rely on the flow of water through a sponge’s aquiferous system may be affected by these factors as well. The offshore sites are subject to stronger currents and higher wave action because they lack the protection of reef structures farther from shore. Midshelf reefs have some protection from the offshore sites, while inshore reefs have much more protection and the benefits of more horizontal substrates.
The higher abundance of brittle stars and fishes within S. carteri
at inshore sites may be influenced by the more sheltered environment and horizontal substrate, as well as predation, larval supply, and juvenile survival. Perhaps one of the most important factors is the availability of suspended solids and food, which collect much more readily on a flat surface, especially with the lower rate of water flow at inshore sites. Wooster et al. [60
] found a significantly higher level of dissolved organic carbon (DOC), live particulate organic carbon (LPOC), and detritus at inshore reefs than offshore reefs in the central Red Sea. The higher abundance of organic matter inshore [60
] is most likely beneficial to suspension-feeding and deposit-feeding brittle stars and other organisms. The feeding habits and food sources of macrofauna groups have not been examined in this study, but may be a valuable contribution to cross-shelf studies. The trend in fishes associated with S. carteri
is supported by Pearse [7
], who found a greater variety of fishes associated with sponges in a shallow, enclosed sound of Bimini as opposed to the open ocean of the Tortugas. Mollusks (snails, nudibranchs, and a bivalve) were only found associated with sponges on the exposed side of inshore reefs as well as both sites at the intermediate reef (QG). Mastaller et al. [62
] found that gastropods and bivalves, particularly those associated with corals, in the reef zones of Port Sudan showed a lower abundance in areas of low water exchange, high sedimentation, and turbid waters. Qita al-Girsh (QG) is a small reef surrounded by deep water, hence, epifaunal mollusks in this location, as well as on the exposed sides of the inshore reefs, would be subject to a high flow of water with little sedimentation and low turbidity. Biological factors such as predation and larval dispersal may also play a role, although very little is known about larval supply and dispersal within the Red Sea (however, see Reference [63
]). Future studies of invertebrate larval abundances would help to resolve questions of supply vs. survivorship in terms of determining community composition across the cross-shelf gradient.
abundance in the study area generally follows the inshore–offshore gradient as well. As with macrofauna, food availability should be considered a major influence. McClanahan and Obura [64
] found a higher abundance of sponges in areas with more sediment, which generally has a positive correlation with POC and supports the observation of higher numbers of S. carteri
with a closer proximity to shore. Available ambient POC in our study area shows a 42.6% decrease from inshore to offshore reefs (mean 11.5 vs. 6.6 µmol C Lseawater−1
, respectively [60
]). Some studies attribute a lower biomass of sponges offshore to lower levels of organic matter, which may be carried away by the stronger flow of water, and nutrients, which may originate from shore [61
]. Larval supply and patterns of connectivity should also be considered (see Reference [66
]), although sponge communities generally depend most on environmental conditions such as light, currents, turbulence, slope, and suitable substrate availability [67
]. Another influence on S. carteri
abundance patterns could be the Red Sea bleaching event of 2010. Coral bleaching was significantly higher at inshore sites than at midshelf and offshore sites, and was followed by a general decrease in coral cover within the next year [69
]. With a lower abundance of corals, space competition would have decreased and allowed sponges more room to settle and grow, particularly on the more highly affected inshore reefs. A similar pattern has been reported in other locations, such as the Caribbean [70
Mass global bleaching events are becoming more common [71
]. Although studies have been focused on the impacts on coral populations, sponges deserve increased attention. More extensive sampling is required to obtain the baseline data necessary for further studies on how sponges and their associated communities react to such climatic events. This study shows that S. carteri
harbors diverse macrofaunal communities and has the potential to promote or maintain biodiversity as coral reef systems continue to change.