Historical marine ecology using non-traditional data sources reveals the impact of local and global processes over half a century

doi:10.21203/rs.3.rs-4715597/v1

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Historical marine ecology using non-traditional data sources reveals the impact of local and global processes over half a century

https://doi.org/10.21203/rs.3.rs-4715597/v1

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Human impacts on earth span centuries, yet scientific studies cover a fraction of this time. Historical records and citizen scientist data are a useful resource for the long-term studies needed to understand and respond to pressures on nature, yet their quality and validity have been challenged.

To explore how such non-traditional sources can be used to understand historical ecological change, we studied a site (Shiprock) with long-term citizen science activity in the Sydney, Australia region. We analysed approximately 6000 taxonomic records and reports revealing substantial ecological changes between 1965 and 2020, including the local disappearance of some fish and invertebrate species and declines in the abundance of many taxa including kelp. We found indications of potential range extensions more frequently from the north than the south, consistent with patterns expected from the global processes of climate change.

We compared the relative advantages and limitations of the two main citizen science data collection modes: structured surveys and opportunistic presence records. Structured surveys provided broadly scientifically useful ecological information including species richness, populations, community structure and temporal change. Opportunistic data had the potential to provide long-term retrospective community information and species presence, but were limited in the ability to provide species absence, biomass, populations, community structure and coverage of remote areas.

Our study allowed the development of scientifically- and managerially-relevant insights encompassing foundation, threatened, protected and invasive species, community shifts and the impacts of local and global processes over historical timescales.

Citizen science

climate change

marine protected areas

invasive species

Humans have impacted ecosystems for far longer than we have effectively monitored them (Cushing, 1988; Jackson et al. 2001). Historical ecology studies provide a potential solution to this gap, allowing us to retrospectively understand ecosystem changes that pre-date formal scientific studies (Balée 2006; McClenachan et al. 2012) and inform conservation and sustainability decision-making (Scarborough et al. 2022). Marine historical ecology emerged in the late 20th century and has been used to study timescales from years to centuries and spatial scales from single sites to thousands of km² (Beller et al. 2020; Thurstan 2022).

Understanding historical changes in marine ecosystems requires consideration of novel data sets and the application of diverse social and life science methodologies (Balée 2006). Novel or non-traditional historical data sets can include popular media articles, artworks, museum collections and opportunistic samples (Thurstan et al. 2015, Blasi et al, 2023). Here we define “non-traditional” data sources as any data that fall outside the traditional scientific method, in which data collection is systematically designed to address a hypothesis or research question (Bryman 2015). In the context of this study, these data include historical articles, SCUBA diver logs, citizen scientist surveys and photographs.

With the current degradation of the marine environment under the combined effects of multiple pressures (Brook et al. 2008), it is critical to consider such non-traditional data sets to understand impacts and inform management (McClenachan et al. 2012; Beller et al. 2020). Local records kept by individuals and groups, including through structured citizen science activities, can increase the spatial and temporal scale of studies to span continents and decades, and provide access to locations and times that may be out of reach of traditional scientific research (Dickinson et al. 2010). They are also an important source for coupled systems research, such as is required to understand social-ecological systems (Lepczyk et al. 2009; Scarborough et al. 2022).

The usefulness of non-traditional citizen science data sources has been challenged (Aceves-Bueno et al. 2017); however, the demands of biodiversity research in the future require us to maximise the value derived from these data (Theobald et al. 2015; Callaghan et al. 2021). Whilst the quality of citizen science data can vary depending on individual knowledge, methods and program design, they can reach levels that meet or exceed the quality of data collected by professional researchers (Edgar & Stuart-Smith 2009; Dickinson et al. 2010, Callaghan et al. 2020). It is important, therefore, to consider the limitations and biases of non-traditional data (as indeed it is with traditional scientific method data) in their interpretation and application (Specht & Lewandowski 2018; Callaghan et al. 2019).

Whilst many human impacts result in ecosystem degradation, human-nature interactions are not always negative (Lerner 1993). Environmental stewardship or “active earth-keeping” provides a pathway to sustainable futures, and includes advocacy, restoration, protection and monitoring by citizen scientists (Turnbull et al. 2020). Environmental stewardship of frequented locations can opportunistically provide valuable information, including non-traditional data sources spanning decades (Thurstan et al. 2015). Institutions may also undertake local stewardship actions, such as the design and gazettal of Marine Protected Areas (MPAs). Today, however, many MPAs are not producing the intended social or ecological outcomes (Turnbull et al. 2021). It is essential, therefore, to monitor the results of protection over decadal timescales, something that can also be facilitated through citizen science (Edgar et al. 2023).

Shiprock is an iconic location of high social and ecological value in the southern suburbs of Sydney, Australia. This unique marine community was first documented by some of Sydney’s earliest SCUBA diver citizen scientists - members of the Underwater Research Group of NSW (URG) - in 1965 (Lawler 1998). Since then, Shiprock has been the focus of ongoing efforts to discover, document and conserve its abundant marine life. Early write-ups of Shiprock describe the sense of wonder, discovery, desire to document and ultimately the need to conserve the site that developed over decades (for example, https://www.urgdiveclub.org.au/copy-of-bulletin-archive-1965-1969 accessed 8/6/22). These efforts featured collaboration with scientists at the Australian Museum, particularly in describing species taken as samples from the site:

“Another tropical species of sea urchin belonging to the same family as two caught in late January was collected last week end (6th March)... These were identified by Miss E. Pope of the Australian Museum, as colour variations of ‘Temnopleurus alexandri’.” (URG Bulletin March 1966, C. Lawler).

URG commenced a series of structured surveys around that time, including multiple biodiversity surveys using two transects perpendicular to shore – “A” and “B” – that ran from the shallows to the bottom of the wall, and an environmental survey in November 1966 (Lawler 1998). These surveys were ultimately written up by club member Clarrie Lawler in the journal Wetlands (Lawler 1998).

Shiprock was declared a no-take (sanctuary zone) Aquatic Reserve in 1982 (https://www.dpi.nsw.gov.au/fishing/marine-protected-areas/aquatic-reserves/shiprock-aquatic-reserve accessed 8/6/22). The Reserve is small, spanning 250 m of shoreline and around 2 ha, but it encompasses the central feature wall and nearby rock outcrops. Access to the dive site remained limited due to the steep ravine and rock ledges on the way down from the road until the owners of the property bordering the access track left a generous bequest for the local Council to build stairs in 2004 (URG Bulletin September 2012).

In recent years, citizen science at Shiprock continued in the form of structured surveys through the Reef Life Survey (RLS) program (www.reeflifesurvey.comaccessed7/6/22), and ongoing unstructured documentation through opportunistic photographs published on iNaturalist (https://www.inaturalist.org/home accessed 9/6/22). In 2017, at the instigation of the authors of this paper, the original perpendicular transect surveys were repeated in a collaborative project with URG members. The availability of parallel unstructured opportunistic data and structured survey data, at a single site which effectively provided a standardised spatial scale, allowed a unique basis for our study spanning 50 years.

Our research explores three broad questions:

What can be concluded from the comparison of Shiprock historical and recent data, regarding ecological diversity and change, spanning the last half century?

How can these conclusions be interpreted in the context of the potential local and global drivers of change?

How do the two main citizen science data collection modes at Shiprock (structured surveys vs unstructured opportunistic observations) compare in their strengths and limitations?

Nestled on the northern developed shore of Port Hacking (southern Sydney, Australia), 4 km upstream from the estuary mouth, Shiprock has been a focal point for recreation and stewardship for over half a century. The northern shore of Port Hacking is largely urbanised, whilst the southern shore is largely undeveloped due to the declaration of the world’s second oldest National Park in 1879 – the Royal National Park. The upper reaches of the estuary are bounded by the Royal National Park on both sides.

The Port Hacking estuary has a history of human impacts including fishing and bait collection, dredging, shell grit mining, catchment modification and urban runoff (Meehan & West, 2002; McKinley et al, 2011) however recent studies have found it to be relatively pristine with only slight to moderate pollution impacts (Birch et al, 2021; Alyazichi et al, 2020). Fishing pressure is moderate, with an annual recreational fisher daytime effort approximately 1/3 that of the nearby Port Jackson estuary (Sydney Harbour) (Steffe & Murphy 2011). Natural impacts from strong tidal flows, storms, progradation of the tidal delta and sand migration are also ongoing (Meehan & West 2002).

Shiprock is sheltered from waves and experiences tidal flushing twice daily. Situated on a tight bend in the river, the site is characterised by a vertical underwater wall over 10 m high at its north-eastern end, tapering to a series of ledges 100 m to the south-west. The site also has several small rocky outcrops, numerous overhangs and ledges, and two small caves. High tidal flushing with waters relatively free of urban runoff has allowed the establishment of a highly diverse marine community at Shiprock, founded on rich and abundant sessile invertebrates and algae.

The initial historical data for our study were sourced from The subtidal flora and fauna at Shiprock, Port Hacking, NSW during 1965-70 (Lawler 1998). Discussions with C. Lawler and other URG members then provided a large volume of Shiprock species records in diver logs, newsletters (“The Bulletin”), and survey notes from the 1960s. These included extensive graphical data in the form of hand-drawn pictures of species and habitats (e.g., Figs. 1, 2 and 3). Selected pictures are reproduced here; further historic pictures and prose can be found at https://www.urgdiveclub.org.au/ (accessed 5/6/22).

More recent data were collected from three sources; (i) Reef Life Surveys, (ii) repeats of the original 1960s perpendicular transect surveys, and (iii) the iNaturalist citizen science website.

The Bulletin and dive log extracts

We extracted all references to species at Shiprock from Bulletins and dive logs from 1965 to 2013. These were tabulated and included metadata for date, article, diver, species common name, species scientific name, relative abundance category and descriptive information such as habitat. Abundance categories were: presence, absence, one, few (2–10), many (11–100) and abundant (101+).

Scientific names were checked, verified and updated where necessary using WoRMS (www.marinespecies.org, accessed 9/6/22) and Fishes of Australia (https://fishesofaustralia.net.au/accessed9/6/22). Species names required considerable interpretation and translation. Organisms were historically described by a blend of common and scientific names; for example “Telesto” referred to the soft coral Telesto smithii which is abundant at Shiprock, now most likely Carijoa sp. (https://www.inaturalist.org/observations/8199698 accessed 10/6/22) and possibly invasive (Concepcion et al. 2010). “Sea pens” most likely referred to Cavernularia sp., an octocoral which is common in the sand around Sydney but which may still be undescribed (https://www.inaturalist.org/observations/7015860 accessed 1/6/22), in the family Veretillidae. Charonia rubicunda was a marine gastropod, now C. lampas, and Ritterella was a compound ascidian, most likely R. tokioka (Fig. 2).

Reef Life Surveys (RLS)

RLS is a global program that gathers underwater visual census data using highly trained volunteers (Edgar & Stuart-Smith 2014). At the start of our study, an RLS site had already been established at Shiprock, with surveys conducted in 2010, 2015 and early 2017 at depths between 8 and 10 m. A further 3 surveys were conducted by RLS volunteers (including author J. Turnbull) during our study, in 2018, 2019 and 2020. RLS transects run along a constant depth contour parallel to shore, not down from the shallows as in the perpendicular surveys, and avoid sand under the RLS method (Edgar & Stuart-Smith 2014).

Perpendicular transect surveys:

C. Lawler (1998) reported using surveys along two transects, A and B, running perpendicular to shore and down the Shiprock depth gradient (Fig. 3). The A transect ran from 1 m to 16 m depth over a distance of 46 m, and the B transect ran from 1 m to 14 m depth over a distance of 23 m. Species identifications for Lawler (1998) were confirmed in collaboration with the Australian Museum, often via physical samples collected from Shiprock (C. Lawler, personal communication).

We replicated the original perpendicular transect methods by adapting RLS methods to vertical, rather than along-contour transects. These comprised fish blocks 5 m wide on either side of the transect tape, invertebrate and cryptic fish blocks 1 m wide on either side of the tape, and photo quadrats perpendicular to the substrate every 1–2 m, heading down the historical transect lines instead of across the wall face.

A total of 21 perpendicular transect surveys were conducted by scientists and volunteers between 2017 and 2019 (n = 12 by the authors of this paper; and n = 9 by URG + RLS surveyors), spanning all four seasons in most years. We captured a total of 856 photo quadrats of sufficient quality to enable the classification of sessile organisms during these surveys. Photo quadrats were classified as top (above the vertical wall lip), vertical wall, or bottom (beyond the base of the wall, on transect A only). These were annotated in Coralnet (Beijbom 2012) with random placement of 25 annotation points, using CATAMI classification to the morphotaxa level (Althaus et al. 2013).

iNaturalist

iNaturalist (www.inaturalist.org) is a global citizen science platform hosted by the California Academy of Sciences and National Geographic Society (Mesaglio & Callaghan 2021). On 1 October 2017, we created the Revisiting Shiprock project on iNaturalist to encourage citizen scientists to upload their sightings at Shiprock. The project was open to members of the public, with a simple description of “Marine species found at Shiprock, Port Hacking, Sydney, Australia” and a single rule that sightings must be from Shiprock, as denoted by a pin placed on the map. Almost 3 years later, on 21 Sept 2020, we extracted all research-grade records from iNaturalist, downloading 2358 records with metadata including date of observation, date uploaded, user, place, species and common name.

Analysis

We classified all fish and mobile invertebrates at the species level, where possible. We analysed sessile invertebrates and most algae at the morphotaxa level due to difficulties in identification without physical samples, the taking of which is highly restricted in the Shiprock sanctuary zone. Our primary analysis focused on the changing presence of species, due to shortage of specific quantitative abundance data and formal sampling structure in the historic records. Availability of categorical abundance data (such as a single sighting, few, many etc) did allow some comparison of relative abundances over time. Species were excluded from our analysis if they were: (i) unable to be identified under a contemporary scientific name, (ii) difficult to distinguish visually from other species, (iii) highly cryptic and so unlikely to be noticed, or (iv) commonplace and therefore unlikely to be noted in Bulletins, dive logs or the 1998 paper.

These exclusions are detailed in Supplementary Table S1.

To identify species that have either increased or decreased over the study period we used a Chi-square test and a “losers” vs “winners” categorisation that we considered appropriate given the limitations of our data. This approach has been applied in prior studies of pressures on marine systems (for example Smith et al. 2021; Castro et al. 2021). We categorised losers as species which were recorded prior to the 1980s, i.e. including species found in the 1960s perpendicular surveys or 1960s and ‘70s Bulletins and dive logs, but not recorded since. The 1980s were chosen as the delineator in our study as this period corresponds with a gap in the historical record at Shiprock and is approximately halfway in our historical timeline. Conveniently, it is also the period in which the Shiprock Aquatic Reserve was established. We categorised winners as species which were recorded after 1980, i.e. in the 1990s and 2000s dive logs, 2010–2020 Reef Life surveys, 2017-19 perpendicular surveys or 2017–2020 iNaturalist sightings, but with no corresponding records prior to the 1980s.

We chose selected statistical analyses where these were viable given the historical data limitations. These included Chi-square tests of winners and losers, multivariate analysis of the community at Shiprock over the decades, and univariate analysis of the data from perpendicular surveys in the 1960s and 2010s which we considered methodologically comparable. Multivariate analysis was conducted in PRIMER 7 (Clarke & Gorley, 2015) using non-metric multi-dimensional scaling plots based on Bray-Curtis similarity matrices of abundance data. These data were not pre-treated with a transformation as our abundance scale of 0–4 already represented an approximation of a log transformation. Blank data in the periods of the 1970s, 1990s and 2000s were treated as missing, rather than zeros, due to the lack of absence data in these periods.

Univariate analysis was conducted in R (R Core Team, 2022) using the LME4 package (version 1.1–33) for mixed-effects modelling and DHARMa (version 0.4.6) for verification of model assumptions. We investigated the interaction between period and range, and period and fished status, as predictors for species abundance, with a random effect of species, and the Poisson distribution. Range was determined from species’ distributions on www.reeflifesurvey.com, and fished status was set to “yes” for species listed in the NSW Saltwater Fishing Guide (https://www.dpi.nsw.gov.au/fishing/recreational/fishing-rules-and-regs/saltwater-recreational-fishing-guide, accessed 10/6/22)

To compare the two modes of citizen science data collection – structured surveys vs unstructured opportunistic sightings – we analysed the rate at which these methods identified species over time, and the types of ecological information which could be derived from them. We compared the cumulative rate of species identification for structured surveys (RLS and perpendicular transects) to that of opportunistic searching by untrained divers (iNaturalist) spanning the four contemporary years 2017–2020. We then compared the abundance and frequency of reporting of the most abundant and frequently-reported species, in order to explore population and community perspectives. During this analysis we also noted any patterns observed in the data, for example differing proportions of particular species.

In total, 339 taxa were described in the historical and contemporary records. The number of records and species were higher in the contemporary period (1990–2020), due in part to the higher sampling effort including the new online source, iNaturalist (Table 1). After corrections and exclusions, these consolidated into 321 taxa, 135 in the historical period and 267 in the contemporary period (Supplementary Table S1).

Table 1

Taxa records by period and data source.
Data source	Source type	Start year	End year	Samples	No of records	No of species
Historical period: 1965–1979
Original URG perpendicular surveys	Structured	1965	1969	Unknown	141*	131 **
URG Bulletins (monthly)	Unstructured	1965	1977	18 Bulletins	165	36 **
URG dive logs (up to weekly)	Unstructured	1965	1974	89 logs	585	108 **
1980s – no data; gazettal of Aquatic Reserve
Contemporary period: 1990–2020
Reef Life Surveys	Structured	2010	2020	6 surveys	500	118
Repeat perpendicular surveys (URG and authors)	Structured	2017	2019	21 surveys	1389	147
URG dive logs	Unstructured	1990	2013	55 logs	857	35**
iNaturalist	Unstructured	1998 ***	2020	Unspecified	2358	224 ****
*number of mentions in the 1998 article; the number of survey records behind these is unknown
**predominantly species, with some genera
*** records started being added in 2016, but were backdated by users as far as 1998 based on old photos
**** contains 28 sessile species (RLS and perpendicular surveys species count is for mobile animals only)

Non-metric multi-dimensional scaling analysis revealed separation in the ecological community at Shiprock over the decades, from the historical (pre-1980s) to contemporary (post-1980s) periods (Fig. 4).

Mobile animals

A total of 273 mobile fish and invertebrate species (i.e. excluding sessile invertebrates) were identified with sufficient confidence to allow comparison of historical data to contemporary records, with approximately twice as many fish (183 spp.) as invertebrates (90 spp.) (Table 2). 64 species were excluded as overly common, cryptic or difficult to distinguish visually (Supplementary table S1). Of the remaining 209 species, 34% were recorded in both historical and contemporary periods, 11% were losers and 55% were winners.

Table 2

Mobile animal winners, losers and exclusions
	Recorded both pre- and post 1980s	Loser (pre-1980s only)	Winner (post-1980s only)	Common (exclude)	Cryptic (exclude)	Difficult to distinguish (exclude)	Total
Fish	44	7	88	7	21	16	183
Mobile invertebrate	28	16	26	7	9	4	90
Total	72	23	114	14	30	20	273

Significantly more loser species were invertebrates (X² = 13.43, p < 0.001) whilst significantly more winner species were fishes (X² = 5.84, p < 0.015) (Supplementary table S1). Our analysis of perpendicular surveys revealed a significant increase in abundances of mobile animals with a northern range from the 1960s to the 2010s (Est. = 1.23, p = 0.001) alongside a significant decrease in abundances of animals with a southern range and both north + south range (Est. = -1.92, p = 0.003 and Est. = -1.48, p < 0.001 respectively), (Fig. 5). Whilst there was an observable increase in fished species’ abundances and decrease in non-fished species’ abundances from the 1960s to the 2010s, this result was not significant (p > 0.05) (Fig. 5).

Table 3

Mobile animal species identified in the 1960s and 2010s perpendicular surveys, categorised by range (north of Sydney, South of Sydney or both) and fished status. Ranges based on distributions on www.reeflifesurvey.com, and fished status = Yes for species listed in the NSW Recreational Saltwater Fishing Guide.
	1960s			2010s
	Fish	Invertebrates	Total	Fish	Invertebrates	Total
Range
North	8	1	9	29	0	29
North + South	38	33	71	52	26	78
South	1	4	5	3	1	4
Fished status
No	36	31	67	61	22	83
Yes	11	7	18	23	5	28
Total	47	38	85	84	27	111

Sessile biota

The 1960s account of Shiprock described abundant Sargassum and Ecklonia along the top of the wall, accompanied by a “multitude of animals” including molluscs, urchins, ascidians and bryozoans (Lawler 1998). The wall was inhabited by “hosts of encrusting invertebrates” including ascidians, bryozoans, hydroids, worms, sponges and soft and hard corals. At the base of the wall were layers of bivalves, a wide diversity of gastropods and urchins. The sandy bottom was inhabited by sea stars, urchins and sea pens.

Today, the section of Shiprock above the wall is primarily sand, shell and rock with substantial stands of Sargassum sp., some Ecklonia radiata and a small number of invertebrates (Fig. 6). The vertical wall is dominated by turfing and epiphytic algae and mostly sponges (encrusting, finger and massive), with a range of corals, bryozoans and ascidians. The section below the wall is primarily sand, shell, rock and turfing algae with a smaller number of encrusting invertebrates.

Algae

We categorised one species of algae as a loser (Ecklonia radiata, kelp) and one winner (Caulerpa taxifolia).

Ecklonia radiata was recorded in the 1960s surveys as “forming an almost unbroken frieze along the top edge of the submarine cliff” and as “dense growths” in the shallows. Many kelp were recorded in dive logs in the 1960s and ‘70s, and noted as being eaten by sea urchins in the January 1969 Bulletin. These historical observations contrast with our contemporary ones, where we observed no unbroken frieze or dense growth, and just 14.8% coverage of E. radiata at the top of the wall.

Sargassum now occupies three times the area (44.8%) and algal turf more than double the area (33.5%) of kelp. Sargassum was noted in the 1960s as abundant, and algal turf is unlikely to have been noted by divers, so we did not categorise either of these as winners. Caulerpa taxifolia on the other hand is a notable invasive species that was first recorded in a dive log in January 2009.

Scientific names

Our analysis of scientific names revealed substantial changes between the historical and contemporary periods. Of the 114 species identified in the 1998 Wetlands article (17 of the total of 131 taxa were genera or multiple species), one quarter (29 species) had different or unknown scientific names today (Supplementary Table S2).

Species identification effectiveness

Overall, we found a similar rate of species identification between structured and opportunistic sampling modes over four years. Structured sampling surveys found more species in the first two years, but on completion of the structured surveys, new species continued to be recorded in iNaturalist, exceeding the structured survey tally (Fig. 7).

Structured surveys reported abundances and, due to the standardised survey area, densities, whilst such information could not be derived from the opportunistic sampling data. Fish biomass data could also be calculated from the structured data using fish size classes and the allometric growth equation (Froese 2017). Opportunistic data included all the top 20 species in the Shiprock marine community, but in very different proportions to the structured surveys (Fig. 8). We observed that the more frequently reported species were generally large, colourful and easy to photograph (Supplementary Table S3):

Using a combination of traditional and non-traditional data sources, we found substantial change in the marine community over half a century. Despite the serendipitous nature of much of our data, we detected evidence of major long-term human impacts and stewardship through citizen science over timescales exceeding more traditional scientific studies. Substantial changes, elaborated and discussed below, include declines in the foundation species Ecklonia radiata; arrival of the invasive species Caulerpa taxifolia; arrival of significantly more northern, tropical species than southern species; declines in some mobile invertebrates; local extirpation of a depleted species Argyrosomus japonicus; and arrival of several previously-fished species including the now-protected black cod Epinephelus daemelii (Fig. 9).

Climate change

The clearest indication of the impacts of climate change at Shiprock is in the disproportionate arrival of tropical species from the north. Tropicalisation of marine communities has been documented in numerous studies along the east coast of Australia and worldwide (Vergés et al. 2016; Vergés et al. 2019). Whilst large-scale change cannot be generalised from a single site, it is instructive that Shiprock provides evidence of this global change process in the non-traditional data record. Closely observed sites like Shiprock can function as long-term sentinels of change (Micheli et al. 2020), informing the design of broader studies that can provide more generalisable conclusions.

Several northern arrivals have the potential for substantial ecological impacts. The black rabbitfish Siganus fuscescens is a schooling herbivore that can impact the health of kelp forests (Gajdzik et al. 2021) and may become invasive in the future. The congeneric S. rivulatus, for example, is considered invasive in other jurisdictions (Pickholtz et al. 2018) and, together with other rabbitfish species, can severely deplete macroalgae biomass over large areas (Vergés et al. 2014). Surgeonfishes (Acanthurus spp.) can increase herbivory pressure through schooling (Basford et al. 2015), and large-bodied predators from the Epinephelus genus (gropers) can impact communities both through predation and habitat engineering (Stallings 2008; Ellis 2019).

Declines in kelp at Shiprock may also be related to direct impacts of climate change. Kelp declines related to warmer, nutrient-poor tropical waters have been documented in multiple jurisdictions (Smale 2020). Such losses can have flow-on effects through the loss of the ecosystem services that kelp provides, such as shelter, habitat, nutrient cycling and productivity (Steneck et al. 2013). Loss of kelp may then provide space for fast-growing, opportunistic species such as turfing algae and invasive species (Filbee-Dexter et al. 2016).

Invasive species

Surprisingly few invasive species were detected at Shiprock, possibly due in part to the restriction of our study to CATAMI categories for sessile species and lack of awareness of invasive species by citizen scientists. Many invasive species are cryptic, unremarkable and uncharismatic (https://www.dpi.nsw.gov.au/fishing/aquatic-biosecurity/pests-diseases/marine-pests accessed 8/6/22).

The invasive colonial ascidian Didemnum vexillum and fanworm Sabella spallanzanii have both been recorded in iNaturalist in the estuary but not at Shiprock (www.inaturalist.orgaccessed8/6/22). An encrusting colonial ascidian most likely to be D. vexillum was found to be abundant at Shiprock by the authors over the course of this study (e.g. https://flic.kr/p/2acViVS accessed 8/6/22).

The Pacific oyster Magellana gigas had a single sighting at Shiprock in 2020. No other declared marine invasives were recorded in our study except the alga Caulerpa taxifolia. C. taxifolia was salient among divers as its invasive status was promoted in 2002 and URG began monitoring it in nearby Sydney Harbour at that time (https://www.urgdiveclub.org.au/post/north-harbour-aquatic-reserve-project-summary accessed 6/6/22). There are multiple records of C. taxifolia in Port Hacking, including two at Shiprock in 2011 and 2018 (www.inaturalist.orgaccessed9/6/22).

Whilst opportunistic data collection has been found to be useful for monitoring invasive species (Crall et al. 2010), our study highlights that care must be taken to manage biases arising from (lack of) awareness and detectability of species.

Over-exploitation and Marine Protected Areas

Whilst Shiprock is a very small Aquatic Reserve, small MPAs can be effective for some species if they are no-take (sanctuary zone), well-located and supported by the local community (Turnbull et al. 2018). We found an observable but non-significant increase in fished species’ abundance between the historical and contemporary periods, and there was a wide range of fished species which were not recorded at Shiprock before MPA gazettal in the 1980s but which were now regularly reported, sometimes in substantial numbers. Many winners such as yellow-fin bream Acanthopagrus australis and snapper Pagrus auratus were recorded on our transects, together with morwong, leatherjackets, drummer, trevally and tarwhine. Fished invertebrates were also recorded for the first time since the 1980s including octopus, blue swimmer crabs and cuttlefish.

Mulloway (A. japonicus) have not been recorded in recent times, despite having been recorded at Shiprock in the 1960s. Once widely distributed in subtropical and temperate Australian shallow waters (https://www.dpi.nsw.gov.au/__data/assets/pdf_file/0005/1329611/stock-status-summary-2021-mulloway.pdf accessed 7/6/22), mulloway have been the subject of widescale commercial and recreational fishing, with commercial landings declining over the last 50 years to arrive at today’s depleted stock status. The Shiprock Aquatic Reserve does not appear to have been sufficient to restore local mulloway populations, most likely due to the small size of the reserve being inadequate to offer effective protection for this wide-ranging species (Moffitt, Botsford et al. 2009).

The Shiprock MPA may also have protected aquaria-targeted species (Madrigal-Mora, Hannes Eisele et al. 2022), including colourful fishes such as Canthigaster callisterna, Chromis hypsilepis, Dendrochirus brachypterus, Mecaenichthys immaculatus, Thalassoma lunare, Abudefduf spp., Acanthurus spp. and Chaetodon spp. listed as winners in our study.

Multiple stressors

Most of our loser species were invertebrates, particularly molluscs. Mobile invertebrates in Australia’s cool latitudes are particularly vulnerable as warming waters from the north squeeze populations against deep ocean barriers in the south, putting over 30% of species at high risk of extinction (Edgar et al. 2023). Nine of our twelve mollusc losers rely on calcium carbonate shells – the cowries, whelks and bivalves – resulting in a possible additional threat from climate change through ocean acidification (Parker et al. 2013).

In addition to global climate change pressures, the bivalves Ostrea angasi and Pecten fumatus have been impacted by local human exploitation (Flood et al. 2012; Cook et al. 2021). Ostrea angasi is endemic to Australia’s southern waters but has experienced declines in many locations. It is the subject of recent restoration programs (Pereira et al. 2019), but restoration can be challenging as multiple stressors are at play. In addition to climate change and over-exploitation, habitat loss, sedimentation and nutrient inflows have contributed to population reductions in this socially-valuable species (Cook et al. 2021).

These additional stressors may also be at play in other results in our study. Whilst fishing pressure is moderate in Port Hacking (Steffe & Murphy 2011), even small levels of exploitation can impact on populations, and the small size of the Shiprock reserve may limit its effectiveness (Edgar et al, 2014b; Turnbull et al, 2018). The majority of the shoreline and catchment in Port Hacking is undeveloped and pollution levels are reported to be low, but pollutants are higher in concentration in northern embayments and so may also be impacting on the community at Shiprock (Birch et al, 2021; Alyazichi et al, 2020).

Threatened, vulnerable and protected species

Several threatened, vulnerable and protected species were recorded at Shiprock (https://www.dpi.nsw.gov.au/fishing/species-protection/what-current accessed 9/6/22). The charismatic blue groper Achoerodus viridis is protected from spearfishing in NSW (https://www.marineconservation.org.au/bluegroper/accessed8/6/22) and has increased in numbers over the period of our study. White’s seahorse Hippocampus whitei was first recorded in 1965 (Lawler 1998) then not again for over 30 years until being photographed in 1998, 2004 and 2008 (www.inaturalist.org). Another seahorse, H. abdominalis, and the ornate ghost pipefish Solenostomus paradoxus have not been recorded since the 1960s. Whilst H. whitei is specifically listed as endangered under Australia’s EPBC Act (http://www.environment.gov.au/cgi-bin/sprat/public/publicspecies.pl?taxon_id=66240 accessed 9/6/22), these latter two species fall under more generalised protection from take, trade or movement under Part 13 of the EPBC Act (https://www.legislation.gov.au/Details/C2021C00182 accessed 8/6/22).

Black cod (Epinephelus daemelii) were only recorded at Shiprock after the establishment of the Aquatic Reserve, in 1999 and again in 2003 URG diver logs, and subsequently in recent years on RLS and iNaturalist. Black cod are listed as Near Threatened on the IUCN Red List and Vulnerable in NSW after declines due to overfishing dating back over a century (Francis et al. 2015). Slow-growing, long-lived and a target for spear-fishers, this species has been protected in NSW since 1983 but has been slow to recover (Harasti & Malcolm 2013).

Sampling and technology change

Our conclusions must be considered in light of the historical and structural limitations of the data collection methods and technologies employed. Early data collection at Shiprock required hand-written notes, drawings, memory and physical sample collection. Underwater cameras were not widely available nor affordable. Illustrating this, the first species photograph featured in iNaturalist was taken in March 1998, digitised and uploaded in 2020 (https://www.inaturalist.org/observations/44451492 accessed 9/6/22) There were no photographs in iNaturalist that had been backdated to our historical time period (prior to 1980s). Over the 58 years of our study there was an observable increase in the ease and volume of data collection, ranging from several species able to be recorded by hand or collected on a dive in the 1960s, to 24–36 photographs that could be taken on a single roll of film, to hundreds of photographs taken per dive with a modern digital camera.

The publication process has also accelerated in efficiency over that time, and contemporary online technologies provide a novel layer of personal motivation and reinforcement (Jennett et al. 2016). Historical data were either rarely published, for example in personal dive logs and collections, or required extensive manual effort in hand drawing, colouring, stencilling and physical printing and distribution as in the early URG Bulletins. It is probable therefore that many species may have been present at Shiprock without ever appearing in the historical record.

Structured vs unstructured data collection

Whilst it is difficult to compare structured surveys to unstructured opportunistic sampling due to the wide variation in sampling effort, our study standardises the spatial scale to a single site and provides a basis for temporal comparison by using parallel structured and unstructured projects. The structured project involved trained professional and citizen scientists conducting surveys over standardised areas, and the unstructured project involved initiating an online effort for anyone with an underwater camera to record species in the same time and space. Despite the divergent methods, the rate at which these two projects identified species was surprisingly similar (Fig. 7).

The strongest correlation in the data sets was between the abundances recorded in the two structured methods, perpendicular surveys and RLS (Fig. 8). Frequency of sightings (ie presence on a survey) was correlated between structured methods, but only weakly correlated between iNaturalist and perpendicular surveys. Even though the data sets aren’t directly comparable, we found a weak negative correlation between the frequency of sighting (as a possible proxy for abundance of a species) and abundance in the perpendicular surveys. This appeared to be due to the most abundant, but non-charismatic species such as T. taeniatus, S. lineolata, T. novozelandiae and A. strigatus being infrequently noticed and recorded in iNaturalist (Supplementary Table S3).

The potential application of structured and opportunistic data sets therefore varied substantially. Whilst structured surveys provided reliable information beyond a list of species, such as densities, species absence, community structure and change over time, unstructured sightings provided primarily species presence. Structured surveys can also be designed to target inconvenient or inaccessible times and places (Callaghan et al, 2020) particularly if part of a broader program such as Reef Life Survey. As opportunistic records represented no systematic search in either time or space, there were no reliable absence records, and sighting frequencies were widely divergent from structured survey abundances and densities.

As part of our analysis we observed that colourful, photogenic and charismatic species were frequently reported in iNaturalist despite comprising a small proportion of individuals on a standardised transect (eg in the case of S. jacksoniensis, less than 1%). Other studies have noted this bias (Roberts et al. 2022). Whilst modelling may be used to attempt to compensate for the limitations of unstructured data such as by mimicking randomness in absence and hypothesising factors such as detectability and observer effort (Brown & Williams 2019), such models require their own set of assumptions. Such assumptions do not consider observer-driven variations in sampling effort, for example a diver focusing on photographing gobies for a period, which then gives a false signal of change in the opportunistic data record.

There were also notable differences between RLS and perpendicular surveys. RLS places transects along a depth contour on hard substrate, avoiding sand, and at Shiprock the chosen RLS depths were between 6 and 10 m. Perpendicular surveys ran down from the water surface to the deepest point on the site, spanning sand and rubble both above and below the wall and incorporating very shallow areas. Sand- and sub-surface-dwelling fish were therefore more abundant on perpendicular transects, for example G. subfasciatus and A. vaigiensis juveniles respectively. Fish which prefer structured habitat were more abundant on RLS transects, for example T. taeniatus and O. limenus. It is evident that, even with structured survey methods, it is important to understand methodological foci and limitations.

Overall, we found that structured surveys provided broader community, population and temporal change information whilst unstructured sampling provided better recording of rare, threatened and invasive species (Roberts et al. 2022), and the potential for retrospectivity (Table 4).

Table 4

Ecological information available from structured surveys and opportunistic sampling methods
Ecological information	Structured surveys	Opportunistic sampling
Species presence	Yes	Yes
Species absence	Yes	No
Species richness	Yes	Limited (not standardised)
Invasive species distribution	Limited	Yes, if salient
Threatened species distribution	Limited	Yes, if salient
Coverage in remote areas	Yes, if planned	Likely to be low
Abundance	Yes	Limited
Biomass	Yes	No
Population change	Yes	No
Community structure	Yes	No
Potential for retrospectivity	No	Yes

Relevance to management, governance and sustainability

Our study highlights the value and potentially irreplaceable nature of historical ecological information at high stewardship sites such as Shiprock. Such sites represent an opportunity for managers to discover indicators of change spanning retrospective timescales which are impossible in newly designed forward-looking studies.

Both structured and unstructured data have limitations. For example loser species may be detected in unstructured, opportunistic data, particularly if they are explicitly searched for in a current project, but winners cannot be conclusively determined without historical structured searches that reliably detect absences. Frequency of opportunistic observation is not a suitable proxy for abundance, and biomass, population and community structural information can at best be modelled using assumptions. Structured surveys are superior for broad-scope, reliable community change information however such data are less abundant and so are of very high value where they do exist. Merged data sets incorporating structured and unstructured data therefore provide the most comprehensive insights.

Our study shows that a single site such as Shiprock can be a sentinel for change including detecting declines in foundation species, community shifts relating to global factors such as climate change, and local winner and loser species. This depends, however, on an active, engaged local community that takes on the challenge of monitoring and conserving the site. Management actions that encourage such local stewardship can therefore have wide-ranging benefits for the long-term sustainability of the social-ecological system.

Competing Interests

J.T. is on the Advisory Committee of Reef Life Survey

Funding

for this research was provided by the University of NSW and the University of Sydney, an Australian Government Research Training Program (RTP) Scholarship awarded to J. Turnbull and ARC SRIEAS Grant SR200100005, Securing Antarctica’s Environmental Future.

Author Contribution

All authors contributed to the design of the study.J.T., A.V. and G.C. collected dataJ.T., D.B. and G.C. analysed dataJ.T. wrote the manuscript with contributions from G.C., D.B. and A.V.All authors reviewed the manuscript

Acknowledgement

The authors would like to express our deep gratitude to Clarrie Lawler, who passed away during our study, and to his family particularly Denise Lawler who remains a member of URG today. We would also like to thank Professor Emma L. Johnston for her steady support and insight; Dr Sonia Graham, Lana Kajlich, Mathilde Chevalier and Steve Samois who contributed to components of this study including design, data collection and annotation; and Jordana Costa for the summary infographic. Finally we would like to thank all of the volunteers at RLS, URG and on iNaturalist who provided data essential to the success of our study.

Data Availability

Data are provided within the supplementary information

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Competing interest reported. J.T. is on the Advisory Committee of Reef Life Survey

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Historical marine ecology using non-traditional data sources reveals the impact of local and global processes over half a century

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Abstract

Figures

Introduction

Method

The Bulletin and dive log extracts

Reef Life Surveys (RLS)

Perpendicular transect surveys:

iNaturalist

Analysis

Results

Mobile animals

Sessile biota

Algae

Scientific names

Species identification effectiveness

Discussion

Climate change

Invasive species

Over-exploitation and Marine Protected Areas

Multiple stressors

Threatened, vulnerable and protected species

Sampling and technology change

Structured vs unstructured data collection

Relevance to management, governance and sustainability

Declarations

Competing Interests

Funding

Author Contribution

Acknowledgement

Data Availability

References

Additional Declarations

Supplementary Files

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