Introduction
Determining the drivers of change and natural patterns of environmental variability are critical to support effective marine management, since it enables anthropogenic impacts to be distinguished from natural changes. However, for most marine ecosystems monitoring is either spatially restricted, or has at best only been conducted for decades (e.g. Edwards et al., Reference Edwards, Beaugrand, Hays, Koslow and Richardson2010; Borja et al., Reference Borja, Chust, Rodríguez, Bald, Belzunce-Segarra, Franco, Garmendia, Larreta, Menchaca, Muxika and Solaun2016), and therefore started after the Anthropocene era began around the mid-20th century (Waters and Turner, Reference Waters and Turner2022). This means that it is often very difficult to conclusively identify drivers of change in marine systems and take appropriate management actions, since we have an incomplete picture of patterns of natural variability.
Lough Hyne (LH) Marine Nature Reserve (51o29’N, 9o18’W) is a small, semi-enclosed sea lough on the southwest coast of Ireland, which is known globally as a biodiversity hotspot and has been studied extensively for over 100 years (Minchin, Reference Minchin1991). While in the past the rocky subtidal communities in LH have been considered highly unusual as they differ from those found at corresponding depths on the open Atlantic coast (Bell and Barnes, Reference Bell and Barnes2000a), more recently they have been considered similar to deeper water so-called temperate mesophotic ecosystems found elsewhere (Micaroni, Reference Micaroni2022; Micaroni et al., Reference Micaroni, McAllen, Turner, Strano, Morrow, Picton, Harman and Bellsubmitted). Mesophotic communities are those that exist at the limit of light for photosynthesis and are animal-dominated (see Bell et al., Reference Bell, Micaroni, Harris, Strano, Broadribb and Rogers2022 for review). Therefore, LH represents an opportunity to study mesophotic communities in shallower water.
While many changes have been reported in LH over the last 50 years (e.g. Little et al., Reference Little, Morritt and Stirling1992, Reference Little, Trowbridge, Pilling, Cottrell, Plowman, Stirling, Morritt and Williams2018; Trowbridge et al., Reference Trowbridge, Little, Dlouhy-Massengale, Stirling and Pilling2013, Reference Trowbridge, Little, Plowman, Ferrenburg, Resk, Stirling, Davenport and McAllen2018, Reference Trowbridge, Little, Plowman, Williams, Pilling, Morritt, Vazquez, Dlouhy-Massengale, Cottrell, Stirling, Harman and McAllen2019), most recently there has been a massive loss of sponges (>90% in some locations) on all but one of the subtidal cliffs (Micaroni et al., Reference Micaroni, McAllen, Turner, Strano, Morrow, Picton, Harman and Bell2021). The exact cause of this change remains unknown, but based on long-term casual observations and quantitative data, we know it occurred in one or more events between 2010 and 2015 (Micaroni et al., Reference Micaroni, McAllen, Turner, Strano, Morrow, Picton, Harman and Bell2021). While many species of sponge were impacted during this event, branching, massive and papillate forms declined the most. Prior to this change, direct SCUBA diver observations from various sources (authors observations, personal communication, Bernard Picton, John Turner, Declan O'Donnell) confirm that these sponge assemblages have been stable for many decades and possibly much longer. Importantly, these changes appear to only have occurred in LH and not on the wider Atlantic coast, and only at sites within LH that experience low water currents and high sedimentation rates (Micaroni et al., Reference Micaroni, McAllen, Turner, Strano, Morrow, Picton, Harman and Bell2021).
Several hypotheses have been proposed to explain the sponge loss, including extreme temperature events, disease outbreaks and changes in sedimentation and water quality (see Micaroni et al., Reference Micaroni, McAllen, Turner, Strano, Morrow, Picton, Harman and Bell2021 for a full discussion). However, the cause or causes remain unresolved, and most of potential drivers have low likelihood of being the cause. One of the interesting oceanographic features of LH is a seasonal oxythermocline that forms in the deeper (>50 m) western part of the lough (Kitching et al., Reference Kitching, Ebling, Gamble, Hoare, McLeod and Norton1976; Johnson, Reference Johnson2006). Calm conditions inside LH typically support the development of a colder, oxygen-poor layer in the deeper areas from northern hemisphere spring, with full development by summer, and breakdown during autumn. The low-oxygen layer is thought to have a strong influence on the ecology and biology of organisms in the deeper areas of the lough (Kitching et al., Reference Kitching, Ebling, Gamble, Hoare, McLeod and Norton1976; Ballard and Myers, Reference Ballard and Myers1997), with a marked decline in the biodiversity of sponges and other organisms below approximately 25 m (Bell and Barnes, Reference Bell and Barnes2000a). This deeper layer is also thought to contain hydrogen sulphide, although this has not been explicitly measured to date (authors personal observation). One proposed explanation for the sponge decline could be an unusual or rapid breakdown of this thermocline, effectivity ‘bathing’ sponges in this low oxygen water. However, explicit testing of LH sponge oxygen tolerance found sponges to be resilient to short-term oxygen stress (Micaroni et al., Reference Micaroni, Strano, McAllen, Woods, Turner, Harman and Bell2022), with the focus now being on the presence of hydrogen sulphide as the main driver of change.
In addition to the well-described sponge fauna on the subtidal cliffs at LH, extensive and diverse sponge assemblages can be found on the undersides of boulders in the shallow (<1–3 m) sublittoral zone (Bell and Barnes, Reference Bell and Barnes2003). These boulders are overlying each other and are mostly very stable (Maughan and Barnes, Reference Maughan and Barnes2000), with the sponge assemblages being dominated by low profile encrusting, massive and repent forms, because of the two-dimensional habitat. These boulders also support many sponges, including species that are not common on the deeper subtidal cliffs (Bell and Barnes, Reference Bell and Barnes2003). Although the changes in the LH cliff fauna have been recently described, to date there has been no assessment of whether these shallow subtidal underside boulder sponge assemblages have also changed. Understanding the temporal dynamics of these boulder-associated sponges may provide important insights into the cause of change on the deeper subtidal cliffs, especially if they show different dynamics. Importantly, some recent changes have been reported in the very shallow water communities in LH (<2 m; Trowbridge et al., Reference Trowbridge, Little, Dlouhy-Massengale, Stirling and Pilling2013, Reference Trowbridge, Little, Plowman, Ferrenburg, Resk, Stirling, Davenport and McAllen2018, Reference Trowbridge, Little, Plowman, Williams, Pilling, Morritt, Vazquez, Dlouhy-Massengale, Cottrell, Stirling, Harman and McAllen2019; Little et al., Reference Little, Trowbridge, Pilling, Cottrell, Plowman, Stirling, Morritt and Williams2018), which have been linked to oxygen stress and eutrophication (Trowbridge et al., Reference Trowbridge, Kachmarik, Plowman, Little, Stirling and McAllen2017a, Reference Trowbridge, Davenport, Cottrell, Harman, Plowman, Little and McAllen2017b), but no explicit examination of the sponge fauna has been made. Furthermore, there has been very limited study on the fauna inhabiting the undersides of the boulders more generally and the accessible boulder fields at LH provide a rare opportunity to study changes in under-boulder fauna through time.
The aim of this study was to compare the sponge boulder assemblages at two sites in LH at 1–2 m depth between 2000 and 2022 (incorporating the period when the subtidal sponge assemblages declined) to assess if there is any evidence for change or a decline in sponges. One site was at the entrance to the lough (Whirlpool Cliff), where the deeper (max 18 m) subtidal cliff sponge assemblages have not changed over the last 20 years, and the other at one of the locations where the subtidal cliff sponge fauna has been most impacted (West Cliff). We propose that if the shallow subtidal (<1 m) sponge assemblages have remained stable through time, this lends support to the hypothesis that an unusual breakdown of the thermocline may have caused the change in the deeper subtidal cliff sponge fauna in LH.
Materials and methods
Study sites
LH Marine Nature Reserve is a small semi-enclosed sea lough on the southwest coast of Ireland. LH is characterised by an unusually high number of ecological niches within a localised area (0.5 km2) largely because of flow and sedimentation gradients from east to west (Bell and Barnes, Reference Bell and Barnes2002). LH is extremely sheltered in comparison to the adjacent Atlantic coastline, with slight wave action only being experienced inside the lough during the strongest winds (>50–70 mph). The lough is connected to the Atlantic Ocean by a narrow (25 m wide) tidal rapids that has a raised sill running across it, which leads to an unusual tidal regime (Bassindale et al., Reference Bassindale, Davenport, Ebling, Kitching, Sleigh and Sloane1957). The tidal inflow lasts only 4 h, with currents in the eastern part of the lough being very fast (>200 cm s−1). However, the outflow of water lasts for more than 8 h and the water currents are slight in all parts of the lough, with the exception of the rapids. The sponge fauna on the undersides of boulders was examined: (1) at two sites within LH in 2000 and 2022 (Figure 1) to assess temporal stability in sponge assemblages; and (2) at seven sites in 2018 (Figure 1) to assess spatial variation in sponge species richness. Whirlpool Cliff was the first site sampled in 2000 and 2022, and is characterised by fast (>200 cm s−1 at 0–6 m), unidirectional water flow during the incoming tide. Although sedimentation rates are likely to be high, accumulation rates are negligible as material is moved back into suspension during the incoming tide. West Cliff was the second site sampled in 2000 and 2022. This site experiences only slight currents (5–10 cm s−1) during peak spring tide inflow (lasting only 15–30 min) (Bell and Barnes, Reference Bell and Barnes2002). These conditions result in high rates of sediment settlement and accumulation rates. However, in the first 1–2 m, wind-induced currents are likely to create some water circulation around boulder communities at West Cliff. For the wider species richness survey in 2018, sites that experience a range of different environmental conditions, from high flow in the Rapids to low flow at the North Basin were examined (Figure 1).
Figure 1. Location of Lough Hyne Marine Nature Reserve showing the location of the subtidal cliffs (squares) and the environmental conditions (d = depth, c = current speed, sa = sediment accumulation of rocks, sr = sedimentation settlement rate). Blue circles indicate the sites sampled for sponge boulder assemblages in 2000 and 2022, while the orange circles are the locations where sponge boulder assemblages were sampled in 2018. The numbers in the orange circles are the sponge species richness at each location.
Methods
For the surveys at the two sites sampled in 2000 and 2022, boulders were haphazardly selected for examination in June each year. The surface area of lower boulder surfaces was measured by laying a transparent cloth marked in square centimetres over the boulders in 2000 and by taking a photograph of each boulder with an iPhone 13 with scale in each picture in 2022 followed by image analysis in Image J (Schneider et al., Reference Schneider, Rasband and Eliceiri2012). A total surface area of approximately 35,000 cm2 was examined at each site. All boulders were examined in situ to prevent excessive drying of material in 2000 and to build a visual database of sponge species and from photographs in 2022. The number of each sponge (number of patches) species on each boulder was recorded. Samples were taken for spicule analysis in the laboratory to allow positive identification where necessary. While we would have preferred to have compared the sponge assemblages using both number of patches and area occupied data, only number of patches data were available from previous surveys in 2000 (see Bell et al., Reference Bell, Biggerstaff, Bates, Bennett, Marlow, McGrath and Shaffer2017 for further discussion on the use of number of patches vs area occupied). For the wider survey of sponge species richness in 2018, 20 boulders ranging in size from approximately 50 to 600 cm2 were haphazardly selected at the seven sites and the total species richness across all those boulders recorded.
Analyses
Boulders sampled in 2000 and 2022 were grouped according to size into small (<150 cm2), medium (151–400 cm2), large (401–750 cm2) and very large boulders (>750 cm2), since boulder size has been shown to impact sponge boulder assemblages at LH and elsewhere (Bell and Carballo, Reference Bell and Carballo2008). Thirty boulders of each size class were sampled at each site (120 in total for each site; 240 in total across both sites). Differences in sponge assemblage composition between the two sites, for the 2 years and the different boulder sizes were analysed using permutational multivariate analysis of variance (PERMANOVA). Three-way PERMANOVAs included year (2 levels), site (2 levels) and boulder size (4 levels) as factors. Year and site were treated as random factors, while boulder size was treated as a fixed factor. The analysis was based on Bray–Curtis dissimilarities and models were run using 9999 unrestricted permutations of raw data. Data were log (x + 1) transformed to reduce the influence of the most abundant and rare sponges and standardised based on the overall sponge abundance to account for the different overall numbers of patches on differing boulder sizes. Differences in multivariate assemblages were graphically displayed using non-metric multidimensional scaling based on Bray–Curtis dissimilarities. SIMPER analyses were used to determine which species contributed most to any significant differences observed. All analyses were conducted using PRIMER V6 + PERMANOVA.
Results
In total, we found 43 sponge species (37 Demospongiae, 5 Calcarea and 1 Homosleromorpha) inhabiting the undersides of boulders across 2000 and 2022 (Table 1). These 43 species were represented by a total of 12,011 and 12,770 individual patches in 2000 and 2022, respectively. All species found in 2000 were also found in 2022. There were 38 and 40 unidentified patches in 2000 and 2022 respectively, which may represent some additional species. In 2000, only four of the 43 species (Leuconia nivea, Clathria (Microciona) fallax, Mycale (Aegogropila) contarenii and Mycale (Carmia) macilenta) were exclusively found at West Cliff, while only Grantia compressa was found exclusively at Whirlpool Cliff. In 2022, Grantia compessa, Clathria (Microciona) strepsitoxa and Pseudosuberites sulphureus were exclusively found at Whirlpool Cliff, while Halichondria (Halichondria) bowerbanki, Iophon hyndmani, L. nivea, C. (Microciona) fallax, M. (Aegogropila) contarenii and M. (Carmia) macilenta were only found at West Cliff. However, the abundance of all these exclusive species was low, with abundances less than 0.8% of the total number of sponge patches observed, and often these species were represented by a single patch (see Supplementary Table 1). In both 2000 and 2022, we found that species richness generally increased with boulder size (Table 1), although there was less difference between large and very large boulders, compared to small vs large and very large boulders. For examples of sponge boulder communities, see Supplementary Figure 1.
Table 1. Sponge species reported from the undersides of boulders found at two sites at Lough Hyne for small (S < 150 cm2), medium (M, 151–400 cm2), large (L, 401–750 cm2) and very large boulders (VL > 750 cm2) across both 2000 and 2022
Asterisks (*) represent species found in 2000 and crosses (X) species found in 2001. The overall number of species found in 2000 and 2022 (in brackets) are shown. Sponge morphologies are also shown: EN, encrusting; CL, clathrate; MA, massive; RE, repent; TU, tubular; GL, globulose.
PERMANOVA (Table 2) showed no significant effect of time (P = 0.379) on the sponge boulder assemblages. However, there was a significant effect (P = 0.001 in each case) of both site and boulder size on sponge boulder assemblages, and for the interaction between site and boulder size. These differences between sites and boulder size were also evident from the MDS plot (Figure 2). The significant interaction between site and boulder size was driven by the very large boulders at Whirlpool Cliff in 2022 having more similar sponge assemblages to those on medium and large boulders compared to the pattern in 2000, and for both years at West Cliff. SIMPER analyses found that many species equally contributed to the differences in sponge assemblages between both sites and boulder size (see Supplementary Table 2), with those species absent from any particular boulder size or site (Table 1), unsurprisingly, being the main species driving the differences.
Table 2. PERMANOVA main tests of log x + 1 transformed sponge abundance data for small (<150 cm2), medium (151–400 cm2), large (401–750 cm2) and very large boulders (>750 cm2) in 2000 and 2022
Bray–Curtis similarity was used with 9999 permutations. Significant P-values are in bold.
Figure 2. Non-metric multi-dimensional scaling (data log x + 1 transformed) to compare sponge assemblages found on small (Small, <150 cm2), medium (Medium, 151–400 cm2), large (Large, 401–750 cm2) and very large boulders (VLarge, >750 cm2) in both 2000 and 2022 at two sites, Whirlpool Cliff (WH, red downward-facing) and West Cliff (WC, blue upward-facing) at Lough Hyne Marine Nature Reserve, Ireland.
The wider site survey conducted in 2018 showed some variation in sponge species richness between sites, with all the same species being found as for the 2000 and 2022 surveys (Figure 1). There was generally higher sponge species richness in the eastern parts of the lough, particularly at Whirlpool Cliff.
Discussion
The deeper (>10 m) subtidal communities at LH changed substantially between 2010 and 2015, with a major decline in sponge populations (Micaroni et al., Reference Micaroni, McAllen, Turner, Strano, Morrow, Picton, Harman and Bell2021). Here we aimed to assess whether similar changes had occurred in the sponge assemblages inhabiting the undersides of boulders at LH. While we found differences in the sponge assemblages between the two sites that experience different environmental conditions and for different boulder sizes, there was no significant effect of time. We propose that the boulder sponge assemblages at LH have not been impacted in the same way as the sponges inhabiting the deep-water reefs. This difference may have resulted from the boulder sponges: (1) being more resilient to the impact that the deeper sponges experienced; (2) not having experienced the impact that affected the deeper water sponges; or (3) having recovered since the impact.
Temporal stability in sponge assemblages
Despite the increasing recognition of the importance of sponges in shallow water subtidal ecosystems in temperate regions (Bell et al., Reference Bell, McGrath, Kandler, Marlow, Beepat, Bachtiar, Shaffer, Mortimer, Micaroni, Mobilia and Rovellini2020), and particularly in temperate mesophotic ecosystems (Bell et al., Reference Bell, Micaroni, Harris, Strano, Broadribb and Rogers2022), we still have a very poor understanding of natural patterns of sponge variability. Furthermore, there are no temporal data available for sponges inhabiting the undersides of boulders to compare with the present study. Early reports from the Atlantic region suggested that sponges were generally slow growing and long-lived, with low recruitment rates (Fowler and Laffoley, Reference Fowler and Laffoley1993; Hiscock, Reference Hiscock1994). However, these early studies did not consider entire sponge assemblages, but only selected species (which included some species found at LH).
More recent studies have described variation in entire temperate sponge assemblages, with some finding considerable temporal variability. However, these previous studies have generally had less than 10 years of data. For example, Bell et al. (Reference Bell, Burton, Bullimore, Newman and Lock2006) used a morphological approach to monitor changes in sponge assemblages over a 10-year period at Skomer Island in Wales. These authors found differences in the sponge morphological assemblages and abundance between years, but the sponge assemblages showed rapid recovery (within 1 year) to their original assemblage composition and abundance following declines. These changes were attributed to natural biological variation, rather than any anthropogenic impact as there was no correlation between any of the assemblage changes observed and environmental variables. More recently, Berman et al. (Reference Berman, Burton, Gibbs, Lock, Newman, Jones and Bell2013) examined seasonal and interannual changes at the sponge assemblage level, also at Skomer Island (using different sampling areas to Bell et al., Reference Bell, Burton, Bullimore, Newman and Lock2006), finding evidence for considerable seasonal and inter-annual variation in sponge assemblage composition and abundance. In contrast, Berman and Bell (Reference Berman and Bell2016) examined the temporal variation in sponge assemblages over a 2-year period in New Zealand and found significant seasonal differences in sponge abundance and assemblage composition, but no significant differences between the 2 years for any given season, suggesting the presence of cyclical seasonal variation, but low interannual variability. Combined, these studies suggest that while some sponge species are long-lived with low recruitment rates, others are highly dynamic.
To date, the longest monitoring of any cold-water temperate sponge assemblage has been described by Micaroni et al. (Reference Micaroni, McAllen, Turner, Strano, Morrow, Picton, Harman and Bell2021) from LH, which included quantitative and qualitative observations over a nearly 30-year period (noting the observations are discontinuous across this period). In contrast to the studies by Bell et al. (Reference Bell, Burton, Bullimore, Newman and Lock2006), Berman et al. (Reference Berman, Burton, Gibbs, Lock, Newman, Jones and Bell2013) and Berman and Bell (Reference Berman and Bell2016), these authors found evidence for very stable sponge assemblages prior to the large change that occurred at LH between 2010 and 2015. This difference likely relates to the nature of deeper LH subtidal communities, being more similar to mesophotic communities than typical shallow water assemblages, since mesophotic communities are generally thought to be stable over longer periods of time (decades), although limited data exist to support this (see Bell et al., Reference Bell, Micaroni, Harris, Strano, Broadribb and Rogers2022 for review). However, despite this proposed stability described at LH, one of the sites where sponges declined between 2010 and 2015 has since shown rapid new recruitment of sponges (see Micaroni, Reference Micaroni2022; Micaroni et al., Reference Micaroni, McAllen, Turner, Strano, Morrow, Picton, Harman and Bellsubmitted), suggesting the potential for mesophotic communities to be highly dynamic when recovering from disturbance (noting some of deeper reefs in LH have shown no signs of recovery to date).
Unfortunately, all previous studies on temporal variation in cold-water temperate sponges have focused-on sponges that inhabit open reef areas, with very limited information generally being available for sponges inhabiting the undersides of boulders (but see Bell and Carballo, Reference Bell and Carballo2008). In fact, very few studies have generally considered sponges on the undersides of boulders. Our results suggest that in low-energy environments or predictable flow regimes, such as those found in LH, assemblages may be very stable over time. Importantly, in our study, we only considered two time points, with our second time point occurring at least 7 years after the estimated change that occurred in the deeper subtidal communities (Micaroni et al., Reference Micaroni, McAllen, Turner, Strano, Morrow, Picton, Harman and Bell2021). It is possible that the sponges inhabiting the boulders were also impacted by the same event or events that caused the decline in the deeper sponges, but they have since recovered. While we cannot completely exclude this possibility, we believe it unlikely given the very high similarity between the 2000 and 2022 sponge assemblages, and the very high overall abundance of sponges that we found. Furthermore, the deeper water sponge assemblages at West Cliff have not yet shown any sign of recovery as of 2023 (authors unpublished data).
Spatial variability and boulder size as a driver of sponge assemblage structure
We found a total of 43 sponge species on the undersides of the boulders at LH, which is substantially higher than Trowbridge et al. (Reference Trowbridge, Kachmarik, Plowman, Little, Stirling and McAllen2017a), although this is likely explained by the much larger number of boulders examined in our study. The variation in sponge assemblage structure between sites is perhaps unsurprising given the considerable differences in the environmental conditions at Whirlpool Cliff and West Cliff (Bell and Barnes, Reference Bell and Barnes2002; Figure 1) and is consistent with patterns for deeper subtidal communities (Bell and Barnes, Reference Bell and Barnes2000a, Reference Bell and Barnes2000b; Micaroni et al., Reference Micaroni, McAllen, Turner, Strano, Morrow, Picton, Harman and Bell2021). However, the drivers of deeper water sponge assemblage structure at LH are thought to be the combined effects of sedimentation and flow rates (Bell and Barnes, Reference Bell and Barnes2000a), which are less likely to be an important driver for sponges living on the undersides of boulders. Sponge morphological adaptation is also thought to be an important factor in the differences in sponge assemblages at different sites in LH, with more upright forms in more sedimented areas, which can passively prevent sediment settling on sponge surfaces (Bell and Barnes, Reference Bell and Barnes2000b). However, sponges on the undersides of boulders are not going to experience sediment settlement because of the nature of the habitat. Therefore, other factors must drive the differences between Whirlpool Cliff and West Cliff. Whirlpool Cliff experiences much stronger water currents compared to West Cliff (Figure 1), which is likely to result in greater food availability and also greater scour during the incoming tide. The greater flow rate also has the potential for more frequent disturbance of boulders (Maughan and Barnes, Reference Maughan and Barnes2000). One or a combination of these factors may explain the site differences.
It is also unsurprising that sponge assemblages vary with boulder size, given the area effect created by larger boulders and greater potential for smaller boulders to move (noting data were standardised to account for variation in the number of sponges on smaller compared to larger boulders). Earlier work at LH by Maughan and Barnes (Reference Maughan and Barnes2000) found that small boulders are likely to be moved more at Whirlpool Cliff. Disturbance is a well-known driver of biodiversity patterns (Dayton, Reference Dayton1971; Osman, Reference Osman1977), and smaller boulders are generally more likely to be moved more than larger boulders. However, the specific sites where we sampled in LH are generally stable over time, since the boulders are overlying and subjected to consistent (or very low in the case of West Cliff) flow regimes, so all boulder sizes are likely to see little disturbance irrespective of boulder size. Therefore, species–area relationships most likely explain the differences between sponge assemblages and boulder size at both sites.
Resilience of under-boulder sponge assemblages and implications for the changes at Lough Hyne
Changes have been reported in several components of the shallow subtidal benthic assemblages at LH in recent years (Little et al., Reference Little, Morritt and Stirling1992, Reference Little, Trowbridge, Pilling, Cottrell, Plowman, Stirling, Morritt and Williams2018; Trowbridge et al., Reference Trowbridge, Little, Dlouhy-Massengale, Stirling and Pilling2013, Reference Trowbridge, Little, Plowman, Ferrenburg, Resk, Stirling, Davenport and McAllen2018, Reference Trowbridge, Little, Plowman, Williams, Pilling, Morritt, Vazquez, Dlouhy-Massengale, Cottrell, Stirling, Harman and McAllen2019), and these have been attributed to eutrophication and oxygen depletion, especially during the night (Trowbridge et al., Reference Trowbridge, Davenport, Cottrell, Harman, Plowman, Little and McAllen2017b; Plowman et al., Reference Plowman, Trowbridge, Davenport, Little, Harman and McAllen2020). However, our results suggest sponges on the undersides of boulders have been resilient to these impacts. Recent studies from LH and New Zealand have suggested that sponges are able to tolerate extremely low oxygen levels for days and even weeks (Micaroni et al., Reference Micaroni, Strano, McAllen, Woods, Turner, Harman and Bell2022), which explains why sponges may have been immune to the other impacts reported for communities on the top of boulders. The changes to the subtidal cliffs in the inner parts of LH are specifically restricted to LH, as open coast Atlantic communities had not changed, suggesting the decline in sponges is highly likely a LH phenomenon.
It is also possible that the very sheltered and protected conditions experienced by sponges on the underside of boulders may account for the different response compared to deeper reefs. For example, perhaps sponges on the undersides of boulders have been protected from the impacts of predation or extreme weather events. There is no strong support for this hypothesis at present, although the impacted deep reefs are also very low energy. Predation on sponges has not been explicitly studied in LH despite the potential from the large diversity of nudibranchs (personal communication, Dr Julia Nunn). However, of all the observations made by the authors of sponges over the last 25 + years, nudibranchs have rarely been seen on sponges.
An unusual breakdown of oxythermocline that forms seasonally at LH (Kitching et al., Reference Kitching, Ebling, Gamble, Hoare, McLeod and Norton1976) has been proposed as a potential cause of the changes to the deepwater communities at LH, and the results of present study provide some support for this theory. However, since Micaroni et al. (Reference Micaroni, Strano, McAllen, Woods, Turner, Harman and Bell2022) showed that many LH sponges are tolerant to low oxygen levels, oxygen-stress alone is unlikely to be the driver. The formation of anoxic water masses is also associated with the production of hydrogen sulphide because of anaerobic bacterial respiration (Schunck et al., Reference Schunck, Lavik, Desai, Großkopf, Kalvelage, Löscher, Paulmier, Contreras, Siegel, Holtappels and Rosenstiel2013). A rapid breakdown of the oxythermocline could have ‘bathed’ some of the cliffs in the vicinity in this low-oxygen, hydrogen sulphide-rich water, causing the widespread sponge mortality. In contrast, the sponges living on the underside of the boulders in the immediate shallows are less likely to have been impacted by such an event as a result of the greater water mixing, driven by wind and tidally driven currents in the shallows. This hypothesis is further supported by the lack of change reported for the deeper subtidal cliffs at Whirlpool Cliff (Micaroni et al., Reference Micaroni, McAllen, Turner, Strano, Morrow, Picton, Harman and Bell2021), which receives high water flow from the Atlantic coast twice every day. Whatever, the cause of the change in the deep-water communities in LH, this does not appear to have impacted the very shallow water sponges in the same way.
Conclusions
We found no evidence for changes in the sponge assemblages inhabiting the undersides of shallow water boulders, but did find differences between sites at all sampling times and for different boulder sizes. Our results suggest sponge assemblage composition changes very little for these underside boulder sponge assemblages at LH over the timeframes we considered. The present study has implications for the changes reported in the deeper water communities at LH and supports the implication of the oxythermocline in the deeper water changes to sponge assemblages. Future research should focus on the potential role that hydrogen sulphide may have played in causing the deeper water changes at LH.
Supplementary material
The supplementary material for this article can be found at https://doi.org/10.1017/S0025315424000493.
Data
The data are available from the authors on request.
Acknowledgements
We are grateful to Declan O'Donnell and Patrick Graham from the National Parks and Wildlife Service of Ireland (An tSeirbhís Páirceanna Náisiúnta agus Fiadhúlra) for permission to conduct this work in Lough Hyne Marine Reserve. We also acknowledge the support of Luke Harman in supporting fieldwork at Lough Hyne.
Author contributions
J. J. B., V. M., A. D. and R. M. planned the study. J. J. B., V. M., A. D. and G. W. collected the data. J. J. B. analysed the data, and all authors assisted with manuscript preparation.
Financial support
This work was funded by National Parks and Wildlife Service of Ireland. Valerio Micaroni and Gabriela Wood were supported by Victoria University of Wellington Doctoral Scholarships.
Competing interests
None.
Ethical standards
Not applicable.
Open access
