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A comparative study of the solitary ascidian communities at two distinct marine environments in Southeast Queensland


Emer Cunningham 2020

Abstract
Sessile marine communities are a product of their environments. Environmental factors largely dictate the development of these communities, which are thus predicted to change under the growing effects of human activity. The solitary ascidian communities at two sites in Southeast Queensland were characterised and compared to investigate whether their different environments yielded different communities. The percent cover, community structure, and species composition of solitary ascidians at Dunwich, North Stradbroke Island and Manly, Queensland were determined from year-long Autonomous Reef Monitoring Systems (ARMS) data. Although sites had very similar solitary ascidian cover, the observed differences in overall structure and species composition at Dunwich and Manly appear to reflect their environments. High human influence at Manly notably facilitated high invasive ascidian presence. The results of this study demonstrate that anthropogenic activity can negatively impact sessile marine communities, and suggest that further invasions and disturbances should be prevented.

Introduction
A variety of factors influence the development of sessile marine communities. Firstly, most sessile marine invertebrates have a planktonic larval stage in their biphasic life cycles, where they exist in the water column before finding an appropriate surface to settle on (Pawlik 1992). Larval settlement is a key process in invertebrate community development, and this process occurs in response to environmental and biotic conditions (Jackson 1983; Pawlik 1992). Conditions that encourage larval settlement can be species-specific, but widely include local environmental factors such as temperature, salinity, water currents, and light availability (Pawlik 1992; Hoegh-Guldberg and Pearse 1995). Once larvae have settled, biotic processes such as competition and disturbance can further characterise and change sessile marine communities (Jackson 1983). Competition for space is common in sessile marine communities, since the largely non-motile organisms require sufficient space to survive and will interfere with other organisms to claim it (Jackson 1983; Keough 1984). Disturbances also alter the composition of sessile marine communities; the effects of temperature, human activity, and weather events have been recorded across global marine communities (Dayton 1971; Addessi 1994; Johnson et al. 2011). Ultimately, sessile marine communities are a product of their environment, which largely dictates the development of such communities.

Under the growing effects of anthropogenic activity, the development of sessile marine communities and their resulting adult communities are expected to change (Johnson et al. 2011; Agius 2016). For example, larval settlement is largely impacted by temperature (Hoegh-Guldberg and Pearse 1995). Human-driven climate change can thus pose threats to community formation, because although slight temperature increases can enhance larval development, larger increases will reduce larval settlement success (Munday et al. 2009). Altered biotic processes will further change sessile marine community composition (Lenihan et al. 2018). In recent decades, non-native invertebrate species have been dispersed to new areas through human activity and now pose threats to native communities (David et al. 2010; Pineda et al. 2011). For example, non-native larvae can be transported in ships’ ballast water, and invasive, biofouling species can travel large distances on the undersides of boats (David et al. 2010; Pineda et al. 2011). These introduced species are often good competitors that can tolerate environmental variability, which gives them a competitive edge over native biodiversity (Pineda et al. 2012a).

Thus, it is imperative to study marine ecosystems that are under threat from anthropogenic stressors. The changing ecology of sessile marine communities should be characterised in order to evaluate their current health, and to predict and mitigate future impacts of human activity.

For this study, sessile marine communities in Southeast Queensland were studied in light of their different environments. Specifically, solitary ascidian communities were characterised. These communities were assumed to be representative of their wider sessile marine community and to thus exhibit typical responses to their respective environments. Ascidian ecology has been widely studied under human activity and climate change; a number of trends have been observed in ascidian communities as a result of environmental change.

For example, invasive and biofouling ascidian species are becoming increasingly prolific and widespread due to anthropogenic influence (David et al. 2010; Pineda et al. 2011). As discussed, non-native invertebrates can be human-dispersed to new areas (Pineda et al. 2011). We are becoming increasingly aware that this process has helped spread ascidian species (Zhan et al. 2015). Their dispersal by boats has led to a global growth in invasive ascidian presence, and has turned docks and marinas into focal points for invasions (Simkanin et al. 2012). Ascidians are often overlooked as biofoulers, but they can be among the most problematic (Aldred and Clare 2013; Zhan et al. 2015). For example, Blum et al. (2007) found that the presence of a non-native solitary ascidian species (Ciona intestinalis (Linneaus, 1767)) greatly changed the native sessile marine community, by reducing species diversity and altering community assembly processes (Blum et al. 2007). Such changes to solitary ascidian communities are further facilitated by environmental variability; fluctuations in temperature, salinity, and pollutants can reduce larval settlement and survival (Thiyagarajan and Qian 2003; Rimondino et al. 2015). These trends have been observed in nature and in aquaculture, to the detriment of aquaculture productivity as well as native biodiversity (Blum et al. 2007; Ramsay et al. 2009; Simkanin et al. 2012).

Such trends are expected to be seen in this investigation’s ascidian communities, but to differing extents across two different environments. The two study sites are located within Southeast Queensland: a jetty at Dunwich, North Stradbroke Island, and a boat harbour at Manly, Queensland. It is hypothesised that the solitary ascidian communities at Dunwich and Manly will be different, because they will be products of their different environments. Dunwich is isolated from mainland Queensland and protected from high human activity, and as such, its marine communities will host a diversity of native species. Manly boat harbour is under constant human influence and experiences fluctuations in salinity, temperature, and pollution levels; the communities at Manly will thus feature a high number of invasive, biofouling species that settle and colonise space efficiently.

These differences will be tested by comparing the percent cover, community structure, and species composition of the solitary ascidian communities at Dunwich and Manly. Firstly, it is predicted that Manly will have a higher percent cover of solitary ascidians than at Dunwich, due to a higher recruitment of invasive, biofouling species. Secondly, the community structure at Dunwich is expected to be more diverse and even than at Manly, since Dunwich will host a diversity of native species while Manly will be dominated by invasive species. Lastly, the species composition at Manly is predicted to show a higher proportion of tolerant invasive and widespread species, whereas Dunwich will feature more native species with Australian ranges.

Materials and Methods
Sessile marine community sampling

Sessile marine communities were sampled using Autonomous Reef Monitoring Systems (ARMS). ARMS consisted of nine settlement plates, each with a top and bottom surface with dimensions of 25x25cm. Thus, each ARMS had 18 available plate surfaces for invertebrate settlement. In March and April 2019, ARMS were deployed at two sites in Southeast Queensland where they remained for one year to allow local marine invertebrates to settle and form communities. A total of six ARMS were deployed: three at Dunwich, North Stradbroke and three at Manly, Queensland (Figure 1).

Dunwich is a small town located on the leeward side of North Stradbroke Island, within Moreton Bay. Three ARMS were deployed at One Mile Jetty (27°29'35"S, 153°24'11"E) on 26 March 2019, where they hung upside-down from pontoons at a constant water depth. This jetty sees frequent human activity, as it serves as a ferry terminal connecting North Stradbroke to mainland Queensland. However, Dunwich remains separated from mainland Queensland in protected area, so may have a more consistent environment due to comparably less human influence than at Manly.

Manly is a bayside suburb situated east of Brisbane city. The other three ARMS were deployed in Manly boat harbour (27°27'19"S, 153°11'24"E) on 2 April 2019, again hanging upside-down from pontoons. This boat harbour is highly used, so human movement directly disturbs this environment. Other sources of anthropogenic activity increase the environmental variability; Manly boat harbour experiences high fluctuations in temperature, salinity, and pollution levels due to human activity. Further, the harbour’s boats can aid the dispersal of various ascidians, especially biofouling or invasive species.

Data collection

ARMS were taken to the University of Queensland in late March and early April 2020 where each plate was photographed in a laboratory. A total of 106 plate surfaces were extensively analysed to characterise their solitary ascidian communities (n=18 plate surfaces per ARMS, except Manly ARMS 2, where n=16 due to missing photographs for one plate). 

Plate photographs were analysed in ImageJ. Firstly, the number of solitary ascidians on each plate was recorded. The plate photographs were calibrated to reflect the true plate dimensions (25x25cm), and the area of plate cover by each individual (cm2) was calculated. Area measurements were then converted to percentage cover of the total plate.

Individual ascidians were identified to species level. The invasive status and distribution of each species was then researched. Species were categorised as either native or invasive to Moreton Bay using primary literature. As such, some species could be classified based on behaviour as well as distribution; for example, cryptogenic and cosmopolitan species such as Styela plicata (Lesueur, 1823) and Ascidia sydneiensis (Stimpson, 1855) were classified as invasive due to their wide ranges and high biofouling and competitive ability (Kott 1985). Species were further categorised by distribution using occurrence data from the Global Biodiversity Information Facility (GBIF) as: Australian, Indo-Pacific (including Indo-Pacific ranges that extended to more temperate latitudes), Pantropical, or Global (for species whose ranges extended notably beyond tropical latitudes).

Data analysis

Percent cover

All analyses were conducted in RStudio. A Welch two-sample t-test was performed to test for differences in mean solitary ascidian plate cover between Dunwich and Manly. The percent cover of solitary ascidians for all plates was graphed as boxplots for each site to visualise any site differences. An Analysis of Variance (ANOVA) was conducted to further test for differences in mean percent cover between all six ARMS.

Community structure

Solitary ascidian communities were summarised across ARMS and sites. The abundance and species richness of each ARMS was noted, and summed to find site totals. Shannon’s diversity index (H’) and Pielou’s evenness was calculated for each ARMS, and the mean of these indices was calculated for each site.

To further explore the overall structure of the solitary ascidian communities, a non-metric multi-dimensional scaling (nMDS) analysis was run on ARMS plate-level species relative abundance data, using the vegan package in RStudio. The Bray-Curtis dissimilarity of each plate’s solitary ascidian community was visualised in an nMDS ordination to identify site differences and possible within-site variation. Site differences were quantified by an Analysis of Similarities (ANOSIM).

Species composition

The invasiveness and distributions of solitary ascidians at each site were visualised in stacked column graphs, depicted the proportions of all ascidian individuals within defined categories. These graphs were created in RStudio using the ggplot2 package.

The effect of invasive species at Manly was further studied. A linear regression analysis was run to test for changes in solitary ascidian plate cover (%) as a result of invasive ascidian presence across all Manly ARMS plate surfaces. An ANOVA was performed on the linear model, and the relationship was plotted in RStudio.
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Figure 1

Results
Percent cover

A very similar percent plate cover of solitary ascidians was observed between sites. Visually, the percent cover across the ARMS plates at each site followed a similar distribution (Figure 2). The average plate cover differed by only 0.02% between Dunwich (mean=7.74%) and Manly (mean=7.72%). A Welch two-sample t-test confirmed that solitary ascidian cover did not significantly differ between sites (t=0.012, df=103.78, P=0.990). Plate cover was further analysed across all six ARMS. Even on this finer scale, no significant differences in plate cover were observed (F5,100=4.13, P=0.839).

Community structure
Dunwich generally hosted fewer individual solitary ascidians but was slightly more species rich than Manly (Table 1). However, on average the overall community at Manly had higher diversity and evenness (H’=1.092, J’=0.609) than at Dunwich (H’=0.885, J’=0.440), (Table 1: noted as "Figure 6").

A visual representation of solitary ascidian community structure showed a clear distinction between sites (Figure 3). The species relative abundances of Dunwich plates were evidently different from those in Manly, and this difference was significant (ANOSIM: R=0.946, P=0.001). Four key species contributed significantly (P=0.001) to the observed difference in site communities: Ascidia empheres and Phallusia julinea primarily distinguished the Dunwich community while Styela plicata and Ascidia sydneiensis defined the Manly community (Figure 3). 

Species composition

No invasive solitary ascidian species were found at Dunwich (Figure 4A). However, the distributions of the species at Dunwich were not strictly Australian – rather, 85.21% of ascidians had wider Indo-Pacific distributions, and the remainder were Pantropical (Figure 4B). A high proportion (80.65%) of solitary ascidians at Manly were members of invasive species (Figure 4A). As such, many ascidians had Pantropical ranges, and some individuals were Globally distributed (Figure 4B). Species with solely Australian distributions were only found at Manly (Figure 4B). 

On the Manly ARMS plates, an increase in the proportion of invasive ascidians led to an increase in overall solitary ascidian plate cover (Figure 5). For the plates with no invasive ascidians, ascidian cover was consistently less than 5% (Figure 5). Despite variation in plate cover at higher proportions of invasive ascidians, the overall increase in plate cover with invasive ascidian presence at Manly was significant (F1,50=11.46, P=0.001).
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Figure 2
3
Figure 3
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Figure 4
5
Figure 5
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Figure 6

Discussion
This comparative study provisionally supports the hypothesis that Dunwich and Manly would have different solitary ascidian communities due to their different environments. Despite inhabiting similar plate cover, the community structure and species composition of solitary ascidians at Dunwich and Manly appear to reflect the level of human activity and variability that their respective environments face.

Solitary ascidians occupied a very similar proportion of ARMS plate space at Dunwich and Manly, which was not expected. It was instead predicted that the Manly ARMS would have greater ascidian coverage due to a high presence of competitive, biofouling ascidians species. Such species were indeed found in Manly, but their presence did not significantly increase Manly’s overall solitary ascidian plate cover when compared to Dunwich at both a site and ARMS level. This result did not account for taxa other than solitary ascidians; further study into which other organisms successfully claimed space at both sites show more consistent trends with previous studies (for example, Ramsay et al. 2009). Despite occupying a similar amount of space, the solitary ascidian communities at Dunwich and Manly were differentiated by their overall community structure and species composition.

Community structure differed between Dunwich and Manly, albeit not as expected. A slightly higher species richness was observed at Dunwich, but the Manly ascidian community was comparably more abundant, diverse, and even. Looking at the relative species abundances for each site, Dunwich was clearly dominated by Ascidia empheres (Sluiter, 1895), a species that is native to the east Australian coast and parts of Indonesia (Kott 1985). Manly was alternatively most abundant in two key species, Styela plicata (Lesueur, 1823) and Ascidia sydneiensis (Stimpson, 1855), which are both invasive species (Kott 1985). Thus, the high relative abundance of A. empheres on the Dunwich ARMS may have reduced this site’s Pielou’s evenness and Shannon’s diversity indices when compared to Manly.

These most abundant species were found only at their respective site, and significantly characterised the site communities. Only two ascidian species were found at both sites: Ascidia gemmata (Sluiter, 1895) and Cnemidocarpa areolata (Heller, 1878), which both have Indo-Pacific ranges that extend into more temperate latitudes (Kott 1985). As with their overall structures, the solitary ascidian communities of Dunwich and Manly had distinct species compositions that appear to be products of their environments.

As expected, the species assemblages at Manly featured a high proportion of invasive ascidian species. Invasive species were absent from Dunwich, which was instead populated by native species like A. empheres and Phallusia julinea (Sluiter, 1915) (Kott 1985). A majority of the species found at One Mile Jetty had Indo-Pacific distributions, and the remainder had pantropical ranges (Kott 1985). It was predicted that species would be largely restricted to Australian waters. However, Indo-Pacific ranges were noted by Kott (1985) to dominate among native Australian ascidians, based on Australia’s bridging position between tropical and temperate waters (Kott 1985). The sole presence of native species and their mainly Indo-Pacific ranges thus implies a correlation between Dunwich’s local environment and species composition; protected areas that are isolated from high human activity may better facilitate the development of native sessile marine communities. This trend is especially evident when compared to Manly. 

Manly was comprised of 85.21% invasive solitary ascidians. As a result, the species at Manly had a variety of distributions; some ascidians had native Australian ranges, others had been introduced globally, and most were pantropically distributed. This variability in species distributions implies that the sessile marine community at Manly formed through the settlement of larvae from many different origins (Pineda et al. 2011). Further, the ascidian larvae that settled and developed successfully often belonged to robust species. The most abundant species at Manly (Styela plicata and Ascidia sydneiensis) are known to be tolerant of environmental variability, which characterises Manly boat harbour (Pineda et al. 2012b; Astudillo et al. 2016). For example, S. plicata can survive within a range of salinities and temperatures, and this robustness has contributed to its successful worldwide introduction and persistence (Pineda et al. 2012b). 

Also, an increase in plate cover was seen to be driven by high invasive ascidian presence at Manly. Invasive ascidians such as S. plicata and A. sydneiensis thus outcompeted both native ascidian species and other organisms in the Manly ecosystem for ARMS plate space, as expected (Agius 2007). This further shows that Manly’s human-influenced environment allows non-native species to successfully invade and outcompete native biodiversity.

Future research could enhance these qualitative comparisons by quantifying environmental factors (such as temperature variability), which could be used to more confidently compare site communities. Also, the communities that were sampled in this study were representative of one year’s development. It could be interesting to monitor ARMS periodically throughout the year to gain insight into the successional development of these sessile marine communities, considering how temporal variability is common (Astudillo et al. 2016; Casso 2017). Comparisons between sites could also be complemented by comparisons between years to reduce such effects of temporal variability and meaningfully observe environmental and ecological changes over time.

Ultimately, the results of this comparative study show differences in the solitary ascidian communities of Dunwich and Manly that are representative of their different environments. Despite the relative proximity of One Mile Jetty and Manly boat harbour, their solitary ascidian communities differ in overall structure and species composition. As human activity and anthropogenic climate change continue to threaten marine ecosystems, it is increasingly important to prevent further invasions and disturbances. Future studies should continue to investigate how environmental conditions can shape community composition, with the important aim of mitigating the growing effects of human activity.

Acknowledgements
Thank you to Sandie and Bernie Degnan for their advice through this research project. I would also like to thank those involved in deploying and retrieving the Dunwich and Manly ARMS.

References

Addessi L (1994) Human Disturbance and Long-Term Changes on a Rocky Intertidal Community. Ecol Appl 4:786-797.

Agius BP (2007) Spatial and temporal effects of pre-seeding plates with invasive ascidians: Growth, recruitment and community composition. J Exp Mar Biol Ecol 342:30-39.

Aldred N, Clare AS (2014) Mini-review: Impact and dynamics of surface fouling by solitary and compound ascidians. Biofouling 30:259-270.

Astudillo JC, Leung KMY, Bonebrake TC (2016) Seasonal heterogeneity provides a niche opportunity for ascidian invasion in subtropical marine communities. Mar Environ Res 122:1-10.

Blum JC, Chang AL, Lilijesthrom M, Schenk ME, Steinberg MK, Ruiz GR (2006) The non-native solitary ascidian Ciona intestinalis (L.) depresses species richness. J Exp Mar Biol Ecol 342:5-14.

Casso M, Navarro M, Ordonez V, Fernandez-Tejedor M, Pascual M, Turon X (2018) Seasonal patterns of settlement and growth of introduced and native ascidians in bivalve cultures in the Ebro Delta (NE Iberian Peninsula). Reg Stud Mar Sci 23:12-22.

David GK, Marshall DJ, Riginos C (2010) Latitudinal variability in spatial genetic structure in the invasive ascidian, Styela plicata. Mar Biol 157:1955-1965.

Davies P (2011) Wild guide to Moreton Bay and adjacent coasts. Queensland Museum, South Brisbane.

Dayton PK (1971) Competition, Disturbance, and Community Organization: The Provision and Subsequent Utilization of Space in a Rocky Intertidal Community. Ecol Monogr 41:351-389.

Hoegh-Guldberg O, Pearse JS (1995) Temperature, Food Availability, and the Development of Marine Invertebrate Larvae. Am Zool 35:415-425.

Jackson JBC (1983) Biological determinants of present and past sessile animal distributions. In: Tevesz MJS, McCall PL (eds) Biotic Interactions in Recent and Fossil Benthic Communities. Springer Science+Business Media, New York, pp 39-120.

Johnson CR, Banks SC, Barrett NS (2011) Climate change cascades: Shifts in oceanography, species’ ranges and subtidal marine community dynamics in eastern Tasmania. J Exp Mar Biol Ecol 400:17-32.

Keough MJ (1984) Effects of Patch Size on the Abundance of Sessile Marine Invertebrates. Ecology 65:423-437.

Kott, P (1985) The Australian Ascidiacea: Part I, Phlebobranchia and Stolidobranchia. Mem Qd Mus 23:1-440.

Lenihan HS, Peterson CH, Miller RJ, Kayal M, Potoski M (2018) Biotic disturbance mitigates effects of multiple stressors in a marine benthic community. Ecosphere 9:e02314.

Pawlik JR (1992) Chemical ecology of the settlement of benthic marine invertebrates. Oceanogr Mar Biol Annu Rev 30:273-335.

Pineda MC, Lopez-Legentil S, Turon X (2011) The whereabouts of an ancient wanderer: global phylogeography of the solitary ascidian Styela plicata. PLoS One 6:e25495.

Pineda MC, McQuaid CD, Turon X, Lopez-Legentil S, Ordonez V, Rius M (2012a) Tough Adults, Frail Babies: An Analysis of Stress Sensitivity across Early Life-History Stages of Widely Introduced Marine Invertebrates. PLoS One 7:e46672.

Pineda MC, Turon X, Lopez-Legentil S (2012b) Stress levels over time in the introduced ascidian Styela plicata: the effects of temperature and salinity variations on hsp70 gene expression. Cell Stress Chaperon 12:435-444.

Ramsay A, Davidson J, Bourque D, Stryhn H (2009) Recruitment patterns and population development of the invasive ascidian Ciona intestinalis in Prince Edward Island, Canada. Aquat Invasions 4:169-176.

Rimondino C, Torre L, Sahade R, Tatian M (2015) Sessile macro-epibiotic community of solitary ascidians, ecosystem engineers in soft substrates of Potter Cove, Antarctica. Polar Res 34:24338.

Simkanin C, Davidson IC, Dower JF, Jamieson G, Therriault TW (2012) Anthropogenic structures and the infiltration of natural benthos by invasive ascidians. Mar Ecol 33:499-511.

Thiyagarajan V, Qian PY (2003) Effect of temperature, salinity and delayed attachment on development of the solitary ascidian Styela plicata (Lesueur). J Exp Mar Biol Ecol 290:133-146.