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Article

Colonial Ascidian Populations at Inshore Coral Reefs of Norfolk Island, South Pacific

by
Shannon Eckhardt
1,
Tracy D. Ainsworth
1,
William Leggat
2 and
Charlotte E. Page
1,2,*
1
Centre for Marine Science and Innovation, School of Biological, Earth and Environmental Sciences (BEES), UNSW, Kensington, NSW 2033, Australia
2
School of Environmental and Life Sciences, University of Newcastle, University Drive, Callaghan, NSW 2308, Australia
*
Author to whom correspondence should be addressed.
Diversity 2024, 16(7), 384; https://doi.org/10.3390/d16070384
Submission received: 5 June 2024 / Revised: 26 June 2024 / Accepted: 26 June 2024 / Published: 30 June 2024
(This article belongs to the Special Issue Patterns Of Marine Benthic Biodiversity)
Browse Figures
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Abstract

:
Subtropical coral reefs such as the lagoonal reefs of Norfolk Island in the remote South Pacific are vastly understudied, with many benthic species unrecorded in the scientific literature. Here we report on ascidian populations from 2021 to 2023 at Norfolk Islands inshore reefs. Quantitative assessments spanning that period were conducted to assess ascidian presence, cover, and benthic interactions. We show ascidian cover remained persistently low and stable across the lagoonal reefs during the study period. We find adjacent reef site, Cemetery Bay showed variation in ascidian cover over time, where we measure a 3.2-fold increase in cover over 2 years. Ascidians were associated primarily with sand and sediment substrates at all reef locations. Recorded interactions between hard corals and ascidians were low. This study provides valuable insights into the population dynamics of ascidians within subtropical reef ecosystems. Ongoing ascidian population monitoring can provide a comprehensive understanding of ascidian dynamics whilst also providing insight of theimpact of anthropogenic stressors on benthic communities. Together, this can aid in informing management and conservation strategies for subtropical reefs.

1. Introduction

Coral reefs are the most biologically diverse marine ecosystems in the world providing vital habitats and substrates for marine life including fish, sessile and free-living invertebrates, algae, and microorganisms [1,2,3]. In recent decades, disturbance and degradation events on coral reefs have led to declines in reef cover and changes in population structure on reefs globally [4,5,6,7,8,9,10,11]. Reductions in coral cover have been associated with an increase in available space on reefs which can be rapidly colonized by other benthic organisms, contributing to population changes on coral reefs [12,13,14,15].
Organisms that rapidly invade open spaces on coral reefs include macroalgae, turf algae, cyanobacteria, urchins, anemones, zoanthids, and ascidians [12,13,15,16,17,18,19]. These species invasions and population shifts have also been linked to reduced coral recruitment and the establishment of phase shifts on reefs [8,16,17,20,21,22]. Phase shifts from coral- to algae-dominated ecosystems have been observed in reef ecosystems worldwide and are predicted to become more frequent in many regions [8,17,23].
Ascidians are sessile filter feeders belonging to the phylum Chordata, are found in both solitary and colonial form, are highly fecund reproducing both sexually and asexually, and are associated with high growth and maturation rates [24,25]. As such, ascidians can thrive across different ecosystems and are able to invade new regions. On coral reefs, ascidians have been found growing over both dead and living hard corals, macroalgae, rocks, shells, and loose sediment [24,26]. In addition to their adaptability, ascidians are tolerant to extreme environmental conditions, including varying salinity, temperature, light availability, and pollution levels [25,27,28]. Colonial ascidians colonise both natural and artificial structures [29] and can outcompete local species to become dominant members of the benthic community [30,31,32]. Ascidians have also been shown to out-compete corals [26,33,34,35,36], can erode the corals’ calcium carbonate skeleton [37] and cause tissue mortality through toxin and chemical secretion [38]. Therefore, where present or increasing in coral reef habitats, ascidian populations can pose a risk to coral health and coral cover on the reef.
Notably, a recent study conducted on Lizard Island found that following the 2016 and 2017 mass bleaching events, Didemnum cf. molle populations (a native ascidian) rapidly increased in coral reef habitats following extensive bleaching-induced coral mortality [12]. Similarly, Shenkar et al. [39] reported that the ascidian Botryllus eilatensis underwent seasonal expansion on reefs in the Red Sea with mean cover increasing to 27% under favourable seasonal conditions. The authors also reported rapid overgrowth of corals by the colonial ascidians during increases in nutrient concentrations. In 1996, Bak et al. [35] studying Trididemnum solidum in the Caribbean also reported an expansion of ascidians and a 900% increase in density over 15 years, resulting in overgrowth of corals. Finally, population outbreaks of Diplosoma species have been reported in American Samoa [34], Fiji [36], and in Indonesia on degraded reefs [26]. Overall ascidian populations are understudied on coral reefs and there is a lack of understanding of the role ascidians play on subtropical reefs.
For subtropical coral reefs, endemism is often high, with many sub-tropical regions hosting isolated and genetically distinct populations that are at high risk of extinction and local extinction under climate change [40,41] Research also indicates that many subtropical coral reefs are undergoing rapid changes to community structure due to the coupling of climate change and local disturbances such as eutrophication, sedimentation, and overfishing [19,42,43,44,45]. However, studies have hypothesised that subtropical regions have the capacity to act as a climate refuge for both local and invading tropical species [43,46]. Therefore, understanding the population structure and response of organisms across the diversity of subtropical coral reef ecosystems is imperative in predicting and managing the impact of environmental changes on a local scale in these regions.
Norfolk Island Marine Park (−29°01′58.18″ S 167°57′15.81″ E, Figure 1A) is situated in the South Pacific approximately 1400 km to the east of Australia. The remote subtropical fringing and coastal reefs of Norfolk Island are to-date understudied and species records for the reef communities are limited. Recent work has indicated that inshore reef sites at Norfolk Island face anthropogenic stressors including global increases in sea surface temperatures leading to a coral bleaching event in 2020 [47], in addition to local stressors from land-based pollution as reported in 2022–2023 linked to severe storms from La Niña [47,48,49,50]. Local stressors from land-based pollution were linked to a severe outbreak of coral disease during the 2020 to 2023 period, where up to 60% of the coral population in the lagoon was impacted by disease in December 2020 and April 2021 [48]. Importantly, the persistence of disease continues up until April 2023 [51] (pers. observations of authors). Here, we aim to assess benthic cover, substrate, and species interactions of ascidian taxa at Norfolk Island’s inshore reefs following the disturbance events of 2020 to 2022, including 1, 2- and 3-years post-bleaching (2020) and 3 years pulse land-based pollution and run-off linked to severe rain events [47,48,51]. In doing so, this study documents the occurrence and ecology of ascidian populations at three reef sites with differing environmental stressors in the lagoonal coral reefs of Norfolk Island.

2. Materials and Methods

This study was conducted at Norfolk Island (hereafter NFI) (29.0408° S, 167.9547° E) located 1400 km east of the East Coast of mainland Australia (Figure 1A,B). Three sites in the south of NFI were investigated: Slaughter Bay (hereafter SB) and Emily Bay (hereafter EB) which form part of the lagoonal reef system, and Cemetery Bay (hereafter CB), a wave-exposed fringing platform reef east of the lagoon (Figure 1C). All reef sites are situated next to the Kingston and Arthur Vale Historic Area (KAVHA) catchment, which serves as the primary catchment area for surface and sub-surface waters from the island. A seasonal creek flows from the KAVHA catchment into EB (Figure 1C), and it has been shown as a source of land-based pollution to the lagoonal reef particularly during high rainfall events where the creek flows directly into Emily Bay. The creek is expected to be one of the sources of nutrient inputs into the lagoon. A golf course is adjacent to the CB reef. Reef sites vary in the level of exposure to waves and flushing. CB experiences regular high wave exposure and flushing during high tide, while EB and SB are lagoonal reefs with outer reef protection from wave action (Figure 1).
Surveys were conducted at three time points: April 2021, April 2022, and April 2023 (Figure 1D). At each time point, replicate 10 m transects were completed at each site where 0.25 m2 (0.5 m × 0.5 m) quadrats were photographed every meter. The number of replicate transects varied at each site as a response to the reef area, where 23 transects were laid in SB, 15 transects in EB, and 5 transects in CB. CB represents a significantly smaller reef area (~4500 m2) compared to the larger SB/EB lagoon. Photoquadrats (n = 10/transect over three timepoints = 1290 total) were manually cropped to the size of the quadrats and uploaded onto CoralNet (www.coralnet.ucsd.edu, accessed on 17 December 2023), a web-based tool developed to analyse benthic communities on coral reefs using semi-automated annotation of the images, where all annotations are checked by the authors prior to further analysis [52]. In total, 100 points were generated and uniformly (10 rows × 10 columns) projected onto each image and the substrate directly beneath each point was manually identified to train the program’s semi-automated classifier followed by manually confirming each annotated point. Each point was categorized as one of these broad benthic categories: Hard coral, macroalgae, ascidians, turf, cyanobacteria, other benthic invertebrates, hard substrate, soft substrate consisting of sand and sediment, and an “all other” category for unidentifiable benthos (see Table S1 in the Supplementary Material for detailed classifications). Ascidian cover is likely to be a conservative estimate as this method of examining the photoquadrats can undercount rare benthic categories, whilst also leading to more cryptic ascidian growth (e.g., in crevices or under hangs) not being visible [12]. Reliable species identification includes both morphological and molecular approaches [53]. The frequency of occurrence of ascidians was calculated by dividing the number of transects containing ascidians by the total number of transects and multiplying it by 100 to get the percentage. Therefore, the higher the frequency of occurrence the more widespread ascidians may occur across a site. The mean cover of each benthic category was calculated per site at each timepoint by calculating the mean cover per replicate transect.
Ascidian interactions with substrate type and other benthic organisms were visually assessed in each photoquadrat from all three sites and three timepoints where ascidians were recorded. Such interactions occur when ascidians are adjacent to, bordered by, or growing on top of other benthos or substrates. Where multiple and/or large ascidian colonies were evident in a photoquadrat, it can become difficult to distinguish distinct colonies (Figure S1A in the Supplementary Material). Here, ascidian clusters that were attached to the same substrate and interacting with the same benthic organisms were counted as a single ascidian unit (hereafter referred to as ascidian units) (Figure S1B in the Supplementary Material). As such, records of colonial ascidian here reflect the number of estimated distinct ascidian colonies without reference to colony size. The primary colonial interaction for each ascidian unit was also recorded as the preferred substrate and/or interaction (as per [35]). Ascidian units in the current study were observed by two apparent interaction types. Firstly, ascidian units were observed growing on top of bare rock, turf or sand, sediment, and benthic organisms. Secondly, ascidian units were found to be bordered by different substrate types and organisms. Recording interactions therefore includes documenting both the organisms and structure the colonies are bordered by/interacting with (hereby called interactions) and the substrate they are growing on (hereby called substrate). Only the primary interacting organism was recorded and determined by its coverage of at least 70% of the colony’s border, based on visual estimation.
All analyses and statistics were performed using R version 4.0.3 [54]. Data was processed and analysed using the tidyverse [55], readxl [56], RColorBrewer [57], and openxlsx packages [58]. A correlation matrix using the corrplot package [59] was computed to investigate potential associations between ascidians and other benthic organisms and substrate within the dataset. A hurdle model, which accommodates zero-inflated data, was fitted to examine the influence of site and timepoint on mean ascidian percent cover, using the package glmmTMB [60]. Percent cover was scaled to the interval [0, 1] by division by 100. The formula used for the hurdle model was: Ascidian cover ~ Time point * Site + (1|Transect_ID) using the beta family. Model assumptions were tested using the Dharma package [61]. Subsequently, a likelihood ratio test (LRT) was performed to evaluate the significance of the interaction between timepoint and site. In the post hoc analysis, estimated marginal means were obtained for all combinations of time points and sites using the emmeans package [62], allowing for the calculation of significant differences in ascidian percent cover changes between time points. A diagonal matrix was constructed to represent the pairwise comparisons between time points and sites. Contrasts were set up to examine variations in the rate of change within sites over time and between different sites across years. To control for multiple tests, a multivariate t-distribution adjustment was applied.
All of the data, code, plots and tables are available and can be accessed on this GitHub Repository: https://github.com/seckha/NFI_benthic_communtiy/tree/main/3%20TP%20Analysis (accessed on 25 June 2024).

3. Results

3.1. Ascidian Morphotype Identification

Two morphotypes of ascidians were observed at the 3 lagoonal coral reef sites of Norfolk Island. The most frequent morphotype observed is consistent with the Diplosoma spp. (Figure 2A–C; Ashley Coutts pers. comm., 16 August 2022) belonging to the family Didemnidae. In 2023 a single observation was made of a bright green Diplosoma spp. (Figure 2D), (Ashley Coutts pers. comm., 16 August 2022) [63].

3.2. Benthic Cover

Benthic surveys covered 57.5 m2 in SB, 37.5 m2 in EB, and 12.5 m2 in CB (0.25 m2 covered per quadrat × 10 quadrats per transect).
In April 2021, Diplosoma spp. colonies were found on 7 of 23 transects in SB, on 3 of 15 transects in EB, and on 3 of 5 transects in CB (Table 1). In April 2022, Diplosoma spp. colonies were found on 9 of 23 transects in SB, 7 of 15 transects in EB, and 2 of 5 transects in CB (Table 1). In April 2023, Diplosoma spp. colonies were found on 6 of 23 transects in SB, on 2 of 15 transects in EB, and on 3 of 5 transects in CB (Table 1). As such, frequency of occurrence demonstrated that CB had the highest frequency in April 2021 and 2023 with Diplosoma spp. being present on 60% of the transects, indicating that the Diplosoma spp. colonies are more widespread in CB than at any other sites to those time points (Table 1), as SB and EB had lower frequencies in April 2021 (30%, 20%) and April 2023 (26%, 13%). In April 2022, EB had the highest frequency of occurrence of Diplosoma spp. colonies with 47%, while they occurred at 39% in SB and 40% in CB.
Mean cover values for each benthic category are represented over all three time points representing the overall benthic cover for each site in the study period (Figure 3, Table 2). Mean cover values for each benthic category at each time point can be found in Supplementary Materials Figure S2 and Table S2.
Average hard coral cover at across all time points was 25 ± 3.09% in SB, 30.2 ± 4.67% in EB, and 37.5 ± 7.23% in CB (Table 2). Other broad benthic categories that covered the reef included macroalgae, turf, cyanobacteria, sand and sediment, hard substrate, and other invertebrates (Table 2). Mean sand and sediment cover was 28.1 ± 2.22% in SB, 29.8 ± 3.41% in EB, and 32.3 ± 7.59% in CB (Table 2). Mean ascidians made up 0.2 ± 0.06% of cover in SB, 0.1 ± 0.07% in EB, and 1.7 ± 1.08% in CB (Table 2). All other invertebrates covered 0.5 ± 0.05% in SB, 0.7 ± 0.09% in EB, and 0.6 ± 0.05% in CB (Table 2).
Investigation of correlations between ascidian cover and cover of other benthic organisms along with substrate variables such as sand and sediment, revealed very weak associations (−0.1 ≥ r ≤ 0.1; Supplementary Material Figure S3). Given the limited strength of these correlations, further exploration of relationships was not pursued.

3.3. Ascidian Cover over Time

Ascidian cover varied significantly between reef sites and time points (Likelihood Ratio Test (LRT): χ2 = 19.422, df = 12, p-value ≤ 0.001; Figure 4, Table 3). At SB mean ascidian cover did not change over time (p = 0.985; Table S3) where mean cover was found to be 0.1 ± 0.05% in 2021, 0.2 ± 0.09% in 2022, and 0.3 ± 0.22% in 2023 (Figure 4A; Table S2). At EB, mean ascidian cover did not change over time (p = 1; Table S3), where mean cover was 0.1 ± 0.07% in 2021, 0.3 ± 0.12% in 2022 and 0 ± 0.02% in 2023 (Figure 4B; Table S2). At CB, mean ascidian cover increased from 1.2 ± 0.88% in April 2021 to 3.8 ± 1.68% in April 2023 (Figure 4C; Table S2), representing a 3.2-fold increase within two years. There was a significant decrease in ascidian cover at CB in April 2022 compared to April 2021, where cover was measured at 0.1 ± 0.12% (Figure 4; Table S2) (p = 0.03; Table S3). Overall, there was a significant change measured in ascidian cover from 2022 to 2023 in CB compared to this same time frame in SB (p = 0.005; Table S3) and EB (p = 0.009; Table S3).

3.4. Ascidian Substrate and Species Interactions

Percentage of Diplosoma spp. units occupying each substrate type and their interactions with other benthic organisms and substrates are represented for all three timepoints for each site (Table S4 for substrate types, Table S5 for interactions). In total, 90 photoquadrats (April 2021: 25 photoquadrats; April 2022: 34 photoquadrats; April 2023: 31 photoquadrats) containing 113 ascidian units were assessed for the substrate type they were growing on (Figure 5A) and for their interactions with other benthic organisms and other media including sand and sediment, and hard substrate (Figure 5B).
Diplosoma spp. were found growing on and interacting with a range of substrates and organisms including cyanobacteria, hard coral, macroalgae, turf, sand and sediment, and hard substrate consisting of bare rock, dead coral, and coral rubble (Figure 5A,C–H). Loose substrate consisting of sand and sediment was the predominant substrate in all sites, with 71.74% of ascidians growing on it in SB, 44.4% in EB, and 61.3% in CB (Table S4). In contrast, sand and sediment only bordered 21.7% of ascidians in SB, 22.22% in EB and 9.7% in CB (Table S5). Ascidians were found on hard substrate at two sites, with 4.4% in SB, none in EB, and 3.23% in CB (Table S4). A total of 2.17% of ascidians were observed as interacting with hard substrate in SB (Table S5). Macroalgae functioned as substrate for 6.5% of ascidians in SB, 11.1% in EB, and 6.5% in CB (Table S4). More frequently, ascidians were bordered by macroalgae with 17.4% in SB, 11.11% in EB, and 19.4% in CB (Table S5). Turf was a substrate for 13.04% of ascidians in SB, and 22.2% in EB, however, it was not the predominant substrate in CB as only 6.5% of ascidians were growing on turf (Table S4). Ascidians were found to more frequently interact with turf than grow on it, with 39.4% in SB, 30.4% in EB, and 45.2% in CB (Table S5). Cyanobacteria, consisting of mostly red cyanobacteria, was found to be an unlikely substrate in SB and CB, where 4.4% of ascidians and 3.2%, respectively, were found to use cyanobacteria as a substrate. In EB, 16.7% of ascidians were found to be growing on cyanobacteria (Table S4). Ascidians at every site underwent interactions with cyanobacteria (17.4% in SB, 30.6% in EB, 19.4% in CB; Table S5). Ascidians were observed as growing on hard coral in EB and CB, where 5.6% and 3.3% units were recorded (Table S4). No ascidians were recorded as growing on hard coral in SB (Table S4). Ascidians at every site underwent interactions with hard coral (2.2% in SB, 5.6% in EB, 6.5% in CB; Table S5).

4. Discussion

There are substantial knowledge gaps regarding the populations and function of subtropical reef ecosystems globally. This study aims to assess cover and interactions of ascidian taxa on the inshore coral reefs of Norfolk Marine Park, a remote and understudied subtropical coral reef ecosystem. Ascidian benthic cover and interactions were assessed in April 2021, April 2022, and April 2023. During this time, there were multiple disturbance events recorded at reef sites of Norfolk Island [47,48,51]. We find that Norfolk Island inshore reefs host species of ascidian Diplosoma spp. with two morphotypes present: light-blue and a single occurrence of a brightly green-coloured morphotype. The green morphotype is potentially host to photosynthetic algae Prochloron sp. (Ashley Coutts pers. comm., 16 August 2022) [63].
Mean ascidian cover ranged from 0–4.46%, with the lowest recorded cover measured at EB in April 2023 (0%), and the highest cover with a mean of 3.8% measured at CB in April 2023, a reef site more exposed to the ocean compared to the lagoon (EB and SB) [48]. Where populations of ascidians seem to be low (<1%) and stable in lagoonal reefs EB and SB over time, we find that there is a 3.2-fold increase in ascidian cover in CB within two years. This finding is comparable to the expansion of Diplosoma virens following the 2016 and 2017 mass bleaching events in Lizard Island, where ascidian cover increased from 0.6 ± 0.2% before the bleaching events to 4.6 ± 0.8% after the bleaching events [12]. Expansion of ascidians can occur in response to a variety of environmental factors and understanding the drivers of ascidian populations may aid in understanding the role and risk of ascidians at Norfolk Islands inshore coral reefs.
Eutrophic conditions have been shown to facilitate ascidian population expansion [39,64,65] Shenkar et al. [39] found that Bortyllus eilatensis cover in the Red Sea was highest during spring, which can be explained by vertical mixing that brings up nutrients into the water column during winter. Furthermore, nutrients due to anthropogenic activities in Israel created favourable conditions for B. eilatensis to thrive [39,66]. Previous research has indicated that there are variable signals of terrestrial pollution at Cemetery Bay, with values of dissolved inorganic nitrogen measured in April 2021 possibly attributable to an adjacent golf course [49]. The increase in ascidian populations measured in this study one year later at Cemetery Bay could indicate a delayed response to nutrients present at this site. Although the study by Page, Ainsworth et al. (2023) also found signals of terrestrial pollution in EB and SB, the larger reef area and volume of water compared to CB may offset the effects of pollution through dilution [49].
Ascidian cover has also been documented to vary seasonally and year-to-year in response to reproduction, growth, and mortality [24]. In the Mediterranean, where environmental parameters fluctuate seasonally, much like in subtropical environments [67,68], several ascidian taxa have been found to exhibit a seasonal growth cycle and for the investigated taxa, summer conditions were reported as least favourable [69]. However, the impact of seasonal variation on ascidian cover remains uncertain and requires further study both seasonally at Norfolk Island and across subtropical reefs where a comparatively higher proportion of macroalgae and other benthic invertebrate taxa exist in contrast to tropical reefs [70,71,72,73].
This study also reports that Diplosoma spp. interacts with different substrate types and benthic organisms on the inshore reefs of Norfolk Marine Park where ascidians were found to have the highest cover on loose substrate (comprised of sand and sediment) compared to hard substrate and other invertebrates. Specifically, Diplosoma spp. were found to grow predominantly on sand and sediment at all three sites. Additionally, interactions between ascidians and turf were prevalent in SB and CB. Notably, no ascidians were found to be growing on hard corals in SB, while 5.6% of colonies were found growing on corals in EB and 19.4% in CB. Similarly, SB had the lowest ascidian-hard coral interactions with 2.2% of colonies interacting with corals, compared to 5.6% in EB, and 6.5% in CB. These findings contrast with other studies which find ascidians in interaction with corals. For example, Trididemnum solidum occurring in Curaçao preferred hard substrates such as coral and rocks with thin algal turfs compared to loose substrate such as coral rubble and sand [35]. T. solidum was also found growing on coral in a different study [74], however only a very small fraction of coral colonies (<1%) was involved in interactions with the ascidian. Rodríguez-Martínez et al. (2012) hypothesised that a disease event resulting in high partial mortality of corals might have facilitated the establishment of ascidian colonies, which might imply a preference for settlement of T. solidum on dead coral. A severe disease event in Norfolk Island has been recorded from December 2020–April 2023 resulting in up to 60% of corals being impacted by disease [48,51], although the potential for Diplosoma spp. to increase over time following this ongoing event needs to be assessed in future studies.
In this study, Diplosoma spp. was also found to occur across all habitat types within the reef, similar to the observations of D. virens in Fiji [75], which highlights the potential for any population expansions at Norfolk to contribute to changes in benthic cover across the reef ecosystem. Ryland et al. [75] found that D. virens was associated preferentially with the calcareous macroalgae Halimeda and was otherwise primarily found around a coral debris–sand mixture consisting of coral clumps and accumulated rubble. As Diplosoma spp. were found growing on various benthic organisms in the current study, it is likely that these organisms can occupy open and available space through coral mortality [12,26,35], or other stochastic events such as a storm event that can fragment and transport ascidian colonies to new areas [12,34]. In conclusion, this investigation into interactions of ascidians with other benthic organisms and substrates highlights their adaptability to environmental variation.
The insights gained from this study underscore the need for ongoing monitoring of benthic cover, including ascidian cover and/or density and abundance, and their interactions with other members of the reef benthos over time. Continued monitoring is key for detecting any potential phase shifts in the ecosystem. Additionally, a comprehensive understanding can be gained by monitoring and quantifying the environmental and biological factors in ascidian expansion, such as measuring nutrient levels, water quality, and fish biomass.

Limitations of the Study

This study presents the ecological dynamics of ascidian populations at subtropical reef locations. While these findings provide valuable insights, several limitations must be acknowledged. Firstly, accurate taxonomic identifications of ascidian species are made by coupled morphological and molecular approaches [53] and were not applied in the current study. As such, species identification is presumed based on expert advice. Future work should look to provide a more in-depth analysis of species present at subtropical reef sites. The survey methodology, with semi-fixed quadrats in SB and EB, and more randomly distributed quadrats in CB, introduces a potential source of variation in benthic cover estimates across different time points. Additionally, the quantification method of benthic cover conducted using CoralNet (www.coralnet.ucsd.edu, accessed on 17 December 2023) and 100 uniformly placed points is likely to underestimate the presence and cover of ascidians, as colonies can be quite small and are rarer on the reef compared to other benthic organisms such as hard corals, macroalgae, and turf. Our study was also limited to analysing populations at one timepoint each year and future studies could look to explore seasonal variation in ascidian populations. Despite these limitations, this study contributes to our understanding of the ecology of ascidians in subtropical reefs, specifically on Norfolk Island. It underscores the importance of careful consideration of survey and quantification methods, and interaction assessments to achieve a comprehensive understanding of the dynamics and ecology of ascidians on subtropical reefs, and worldwide.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d16070384/s1, Table S1: Specifically identified taxa and groups classified in CoralNet and included in the broad benthic categories used for data analysis; Figure S1: Substrate preference and interaction methodology; Figure S2: Percent cover-based frequency distribution of the benthic categories ascidians, cyanobacteria, hard coral, hard substrate, macroalgae, other benthic invertebrates, sand and sediment, turf, and all other present at each site in April 2021, April 2022, and April 2023; Table S2: Mean percent cover and standard error (SE) for all the benthic categories identified in the ecological surveys in all sites at all three time points (TP); Table S3: Odds ratios, standard errors (SE) z-ratios, p-values, and asymptotic lower (LCL) and upper (UCL) confidence limits for contrasts assessing changes in ascidian percent cover across sites and time points; Table S4: Percentage of ascidians that covered each substrate type at each site (CB = Cemetery Bay; EB = Emily Bay; SB = Slaughter Bay) averaged over three time points; Table S5: Percentage of ascidians that interacted with/were bordered by different benthic organisms at each site (CB = Cemetery Bay; EB = Emily Bay; SB = Slaughter Bay) averaged over three time points; Figure S3: Correlation matrix illustrating the pairwise relationships between various benthic groups.

Author Contributions

Conceptualization, T.D.A., C.E.P. and W.L.; methodology, C.E.P. and S.E.; formal analysis, C.E.P. and S.E.; resources, T.D.A. and W.L.; data curation C.E.P. and S.E.; writing—original draft preparation, S.E.; writing—review and editing, T.D.A., C.E.P., W.L. and S.E.; visualization, C.E.P. and S.E.; supervision, C.E.P., T.D.A. and W.L.; funding acquisition, T.D.A. and W.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Parks Australia to establish and undertake an LTMP from 2020–2023.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

All of the data, code, plots and tables are available and can be accessed on this GitHub Repository: https://github.com/seckha/NFI_benthic_communtiy/tree/main/3%20TP%20Analysis (accessed 27 June 2024).

Acknowledgments

Parks Australia provided funding, support, and communication throughout the completion of this study and the associated long-term monitoring program established on the reef in 2020. We also thank community members of Norfolk Island who assisted with this work. Fieldwork was also undertaken by Sophie Vuleta and members of the NFI LTMP. Thank you to Maeve McGillycuddy for her help in shaping and refining the statistical analysis of this study. This study was funded Scientia Fellowship awarded to T.D.A.

Conflicts of Interest

The authors declare no conflicts of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

References

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Figure 1. (A) Location of Norfolk Island 1400 km east of the Australian East Coast. (B) Map of Norfolk Island and location of the 3 study sites (red box). (C) Slaughter, Emily, and Cemetery Bay are located in the south of Norfolk Island. The KAVHA catchment creek flows directly into the lagoon at Emily Bay. (D) Timeline of the bleaching event in March 2020 [47], followed by benthic surveys in April 2021, April 2022, and April 2023. Disease was prevalent from December 2020 until April 2023 [48]. Red line: Austral summer, blue line: Austral winter. Picture credits: (A) Google Maps, 2023, (B,C) Google Earth, 2023.
Figure 1. (A) Location of Norfolk Island 1400 km east of the Australian East Coast. (B) Map of Norfolk Island and location of the 3 study sites (red box). (C) Slaughter, Emily, and Cemetery Bay are located in the south of Norfolk Island. The KAVHA catchment creek flows directly into the lagoon at Emily Bay. (D) Timeline of the bleaching event in March 2020 [47], followed by benthic surveys in April 2021, April 2022, and April 2023. Disease was prevalent from December 2020 until April 2023 [48]. Red line: Austral summer, blue line: Austral winter. Picture credits: (A) Google Maps, 2023, (B,C) Google Earth, 2023.
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Figure 2. Images of ascidian colonies observed at Norfolk Island. (A–C) Colonial ascidian suspected to be Diplosoma spp. (D) Colonial ascidian suspected to be Diplosoma spp. containing photosynthetic algae. Photo credits: (A–C) Charlotte Page, (D) Ashley Coutts, Biofouling Solutions Pty Ltd., used with permission.
Figure 2. Images of ascidian colonies observed at Norfolk Island. (A–C) Colonial ascidian suspected to be Diplosoma spp. (D) Colonial ascidian suspected to be Diplosoma spp. containing photosynthetic algae. Photo credits: (A–C) Charlotte Page, (D) Ashley Coutts, Biofouling Solutions Pty Ltd., used with permission.
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Figure 3. Benthic categories ascidians, cyanobacteria, hard coral, hard substrate, macroalgae, other benthic invertebrates, sand and sediment, turf, and all other. (A) Mean percent cover-based frequency distribution of the benthic categories present at each site (SB = Slaughter Bay; EB = Emily Bay; CB = Cemetery Bay) averaged over April 2021, 2022, and 2023. Each bar represents the relative proportion for each benthic category, calculated based on its mean percent cover value. See mean percent cover values in Table 2. (B) Ascidians. (C) Red cyanobacteria in the “cyanobacteria” category. (D) Hard coral. (E) Dead coral in the “hard substrate” category. (F) Macroalgae. (G) Anemone belonging to the “other benthic invertebrates” category. (H) Sand in the “sand and sediment” category. (I) Green turf belonging to the “turf” category. Photo credits: Norfolk Island, Charlotte Page, used with permission.
Figure 3. Benthic categories ascidians, cyanobacteria, hard coral, hard substrate, macroalgae, other benthic invertebrates, sand and sediment, turf, and all other. (A) Mean percent cover-based frequency distribution of the benthic categories present at each site (SB = Slaughter Bay; EB = Emily Bay; CB = Cemetery Bay) averaged over April 2021, 2022, and 2023. Each bar represents the relative proportion for each benthic category, calculated based on its mean percent cover value. See mean percent cover values in Table 2. (B) Ascidians. (C) Red cyanobacteria in the “cyanobacteria” category. (D) Hard coral. (E) Dead coral in the “hard substrate” category. (F) Macroalgae. (G) Anemone belonging to the “other benthic invertebrates” category. (H) Sand in the “sand and sediment” category. (I) Green turf belonging to the “turf” category. Photo credits: Norfolk Island, Charlotte Page, used with permission.
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Figure 4. Box plots showing percent cover of Diplosoma spp. at (A) Slaughter Bay, (B) Emily Bay, (C) Cemetery Bay over three time points in April 2021, 2022, and 2023. The box represents the interquartile range (IQR; 25th to 75th percentile), with the black line indicating the median. Whiskers extend to 1.5 × IQR from the quartiles, and points beyond are outliers.
Figure 4. Box plots showing percent cover of Diplosoma spp. at (A) Slaughter Bay, (B) Emily Bay, (C) Cemetery Bay over three time points in April 2021, 2022, and 2023. The box represents the interquartile range (IQR; 25th to 75th percentile), with the black line indicating the median. Whiskers extend to 1.5 × IQR from the quartiles, and points beyond are outliers.
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Figure 5. Percentage-based frequency distribution of (A) substrate Diplosoma spp. were found growing on and (B) interactions Diplosoma spp. had with cyanobacteria, hard coral, hard substrate, macroalgae, sand and sediment, and/or turf averaged the sites (SB = Slaughter Bay; EB = Emily Bay; CB = Cemetery Bay) over April 2021, 2022, and 2023. Diplosoma spp. growing (C) on coral, (D) in between a bed of macroalgae and turf, (E) on sand and interacting with turf, macroalgae, and coral, (F) on coral and interacting with red cyanobacteria, (G) on sediment and interacting with macroalgae, (H) on sand and interacting with turf and red cyanobacteria. Photo credits: Norfolk Island, Charlotte Page and Sophie Vuleta, used with permission.
Figure 5. Percentage-based frequency distribution of (A) substrate Diplosoma spp. were found growing on and (B) interactions Diplosoma spp. had with cyanobacteria, hard coral, hard substrate, macroalgae, sand and sediment, and/or turf averaged the sites (SB = Slaughter Bay; EB = Emily Bay; CB = Cemetery Bay) over April 2021, 2022, and 2023. Diplosoma spp. growing (C) on coral, (D) in between a bed of macroalgae and turf, (E) on sand and interacting with turf, macroalgae, and coral, (F) on coral and interacting with red cyanobacteria, (G) on sediment and interacting with macroalgae, (H) on sand and interacting with turf and red cyanobacteria. Photo credits: Norfolk Island, Charlotte Page and Sophie Vuleta, used with permission.
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Table 1. Frequency of occurrence of Diplosoma spp. at each site and time point. Rounded to two decimal points.
Table 1. Frequency of occurrence of Diplosoma spp. at each site and time point. Rounded to two decimal points.
SiteApril 2021April 2022April 2023
Slaughter Bay30%39%26%
Emily Bay20%47%13%
Cemetery Bay60%40%60%
Table 2. Mean percent cover and standard error (SE) for all the benthic categories identified in the benthic surveys in all sites (SB = Slaughter Bay; EB = Emily Bay; CB = Cemetery Bay) averaged over all time points. Mean percent cover rounded to one decimal point and SE to two decimal points.
Table 2. Mean percent cover and standard error (SE) for all the benthic categories identified in the benthic surveys in all sites (SB = Slaughter Bay; EB = Emily Bay; CB = Cemetery Bay) averaged over all time points. Mean percent cover rounded to one decimal point and SE to two decimal points.
SiteCategoryMean Cover (%)SE
SBAll other0.00.00
Ascidians0.20.06
Cyanobacteria13.32.66
Hard coral25.03.09
Hard substrate0.80.24
Macroalgae23.72.03
Other benthic invertebrates0.50.05
Sand and sediment28.12.22
Turf8.30.72
EBAll other0.00.00
Ascidians0.10.07
Cyanobacteria17.13.19
Hard coral30.24.67
Hard substrate0.80.10
Macroalgae16.11.23
Other benthic invertebrates0.70.09
Sand and sediment29.83.41
Turf5.11.42
CBAll other0.00.00
Ascidians1.71.08
Cyanobacteria7.83.91
Hard coral37.57.23
Hard substrate0.90.18
Macroalgae12.22.92
Other benthic invertebrates0.60.05
Sand and sediment32.37.59
Turf7.10.05
Table 3. Comparison of Model 1 (including an interaction term between time point and site) against Model 2 (null hypothesis without interaction) using a Likelihood Ratio Test. Models were fitted using a hurdle model with beta family distribution. p-values indicate the significance of the interaction effect.
Table 3. Comparison of Model 1 (including an interaction term between time point and site) against Model 2 (null hypothesis without interaction) using a Likelihood Ratio Test. Models were fitted using a hurdle model with beta family distribution. p-values indicate the significance of the interaction effect.
ModelDFAICBIClogLikDevianceChisqChi DFp Value
Model 28−134.91−112.0375.454−150.91
Model 112−146.33−112.0185.165−170.3319.4224<0.001
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Eckhardt, S.; Ainsworth, T.D.; Leggat, W.; Page, C.E. Colonial Ascidian Populations at Inshore Coral Reefs of Norfolk Island, South Pacific. Diversity 2024, 16, 384. https://doi.org/10.3390/d16070384

AMA Style

Eckhardt S, Ainsworth TD, Leggat W, Page CE. Colonial Ascidian Populations at Inshore Coral Reefs of Norfolk Island, South Pacific. Diversity. 2024; 16(7):384. https://doi.org/10.3390/d16070384

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Eckhardt, Shannon, Tracy D. Ainsworth, William Leggat, and Charlotte E. Page. 2024. "Colonial Ascidian Populations at Inshore Coral Reefs of Norfolk Island, South Pacific" Diversity 16, no. 7: 384. https://doi.org/10.3390/d16070384

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