Introduction

Remote coral reefs are relatively unaffected by local human-based disturbances and are more influenced by global environmental factors, acting as natural laboratories (Freeman et al. 2012). The variability of coral reef community structure reflects the influence of environmental and biological factors, such as surface currents, seawater temperature (SWT), irradiance, water chemistry, and wave energy, but are also subject to parasitism, predation, and competition interactions (Grigg 2006; Lough and Cooper 2011; Boissin et al. 2019). Global reports indicate partial to total mortality of the dominant reef-building coral genera Porites and Pocillopora for the Pacific region (Hughes et al. 2017a, b, 2018; Eakin et al. 2019), including the Eastern Tropical Pacific (ETP) (Reyes-Bonilla and Calderón-Aguilera 1993; Reyes-Bonilla et al. 2002). Most observations of coral mortality have been mainly attributed to the El Niño Southern Oscillation (ENSO), high storm activity, and long-period swells (Robertson and Allen 1996; Wang and Fiedler 2006; Romero-Torres et al. 2020). Yet, coral community compositions in remote reefs locations and their natural threats (e.g., diseases, bleaching and hurricane events) that may jeopardize the reef’s health status have scarcely been studied (Glynn et al. 1996; Freeman et al. 2012; Glynn et al. 2017).

Clipperton Island constitutes an isolated, uninhabited coral atoll located at the Western Edge of the ETP region (Robertson and Allen 1996). Due to its geographic location, it has been proposed as an important “stepping stone” for the dispersion of fish and propagules of other marine species between Pacific regions (Glynn et al. 1996; Robertson and Allen 1996; Glynn and Ault 2000; Crane et al. 2018; Romero-Torres et al. 2018). In this context, few recent data on the current benthic coral coverage and community status are available for Clipperton Island (Glynn et al. 1996; Jost and Andréfouët 2006; Friedlander et al. 2019). Hence, the documentation of the structure and composition of key reef-building species provides critical baseline data to identify potential effects of local stressors affecting the ecosystem (Hughes et al. 2018). While regular monitoring efforts may not be possible due to the remoteness and poor accessibility of reef locations such as Clipperton Island, periodic monitoring of coral assemblages may help provide relevant insights to identify potential threats to coral reef functionality (Perry and Alvarez-Filip 2018).

The present study assessed morpho-functional benthic community composition (i.e., reef-building species, non-reef building species, space-competitive algae and non-organic structures), as well as the proportion of reef-building coral colonies that displayed potential signs of compromised health, specifically a pink-spotted phenotype. Of note, this phenotype may be indicative of penetration activity of different invertebrates, including but not limited to the parasitic trematode Podocotyloides stenometra, bivalves, or polychaetes (Tribollet and Golubic 2011) or reflect a response to increased sedimentation (Martínez-Castillo et al. 2020). As pink-spotted phenotypes of Porites attributed to trematodiasis have recently been reported the most common disease in the Hawaiian Archipelago, occurring on over 60% of reefs in the region (Couch et al. 2014; Aeby 2015), we here provide a first assessment of pink spot incidence on the isolated and remote shallow reefs of Clipperton Island to serve as a baseline for further monitoring efforts.

Materials and methods

Study area and data collection

The remote Clipperton Atoll in the tropical northeastern Pacific is situated 1100 km from the nearest continental coast (Fig. 1a) (Pitman et al. 2006; Robertson and Allen 1996). The island is of volcanic origin, and due to its 10 km2 extension and enclosed eutrophic inner lagoon considered an almost-atoll (Jost and Andréfouët 2006). The coral reef is composed by a 3.7 km2 well-developed fringing reef that is irregularly segmented by spurs and groves, reef terraces and seaward slopes dominated by massive Porites and branching Pocillopora corals in shallower waters (1–15 m), and massive Porites, Pavona and Leptoseris corals in deeper waters (20–70 m) (Wellington et al. 1995; Glynn et al. 1996). Yet, episodic ENSO events have influenced the seascape of the Clipperton area, for instance intense swells and hurricanes occur during the tropical storm season from May to October (Wang and Fiedler 2006; Zhao and Raga 2015).

Fig. 1
Fig. 1
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Description of the study area and sites and coral phenotype. a Location of remote Clipperton Island in the Eastern Tropical Pacific and b detailed map of the study area. Maps adapted from van Soest et al. (2011). c–f Representative observations of massive Porites corals in the study area exhibiting a pink-spotted phenotype. Close-up (c) and overview (d–f) of Porites colonies. Side lengths of quadrat in (d) 0.25 m, and 0.5 m (c, e, f). White arrows show pink-spotted areas on affected colonies

Benthic coral reef surveys were performed during a scientific sampling campaign as part of the Tara Pacific Expedition at Clipperton Island in August 2018. Four different study sites were selected for each representative reef location around the atoll: North, South, East, and West of Clipperton Island’s shallow reef zones (10–13 m water depth) (Fig. 1b). Benthic assessments were conducted by SCUBA using the line intercept point (LIP) technique along three transects of 20 m length parallel to the shoreline. The LIP surveys used a weight suspended technique recording benthic data at 50 cm intervals along the transect line (120 data points) for each site. The following benthic categories of morpho-functional groups were recorded: Corals: Pocillopora, Porites, Pavona, Leptoseris; algae: macroalgae, crustose coralline algae (CCA); rubble (encompassing small not recently dead corals), rock, sand, and turf algae. Total live coral cover was calculated from the percentage sum product of all Pocillopora (branching), Porites (massive), Pavona (massive), Leptoseris (encrusting) corals for each site. In addition, the proportion of the pink-spotted coral phenotype which may suggest tissue penetration by or infection with a range of invertebrates, including but not limited to the trematode Podocotyloides stenometra, or increased sedimentation rates (Fig. 1c–f) (Aeby 2003) was recorded along with coral cover. The incidence of the pink-spotted coral phenotype was recorded, i.e., all colonies displaying pink spots, regardless of whether abundance of pink spots was low (few spots) or heavy (high densities of pink spots, affecting > 50% of the colony).

As explanatory environmental variable, annual SWT from monthly data of the last decade (2008–2018) were acquired from satellite images of 4 km2 grid resolution (https://oceancolor.gsfc.nasa.gov), using type AquaModis® at level 3, and analyzed with Wam_Statitist® ver. 6.33 software. To identify the intensity of thermal–stress, ENSO events were defined as 3 consecutive overlapping 3-month periods (above the + 0.5 °C anomaly for warm “El Niño” and below the − 0.5 °C for cold “La Niña” phases), the Ocean Niño Index 3.4 region was used (https://ggweather.com/enso/oni.htm/). We also recognized and categorized tropical cyclones that influenced the Clipperton area, using data from the National Hurricane Center, NOAA (https://www.nhc.noaa.gov/data/) during the past decade.

Data analysis

Multiple permutational analyses of variance (PERMANOVA) and their respective post-hoc tests based on Euclidean matrices were used to evaluate differences in benthic morpho-functional group coverage and reef benthic composition (Shannon diversity, H’). Statistical significance was tested with unrestricted permutations (10,000) of raw data. For live coral cover, we performed one-way PERMANOVA to test differences between reef zones (North, West, South, and East). Contributions to the average dissimilarities in coral species, were calculated with similarity percentages analysis (SIMPER) using a 65% cutoff of the accumulated contribution of dissimilarity. Principal coordinate analysis (PCoA) was performed to determine coral composition resemblances at genus level among reef zones based on PERMANOVA’s yields. All PERMANOVAs, SIMPER and PCoA analysis were conducted in PRIMER v.6 with PERMANOVA + extension.

Results

Total live coral cover across the four sites surveyed averaged 66 ± 7.7% (range ~ 54–85%), with statistically significant differences between reef zones (PERMANOVA; F = 3.6931, P < 0.001) were evident for the North and the South reefs, with the highest live coral cover compared with the West and East reefs of the atoll (Fig. 2a and Table 1). No significant differences were found for diversity of benthic assemblages (Shannon diversity, H’) between reef zones (PERMANOVA; F = 0.71818, P = 0.604). At the same time, differences in benthic community composition were evident. Specifically, Pavona and Leptoseris were the coral species that contribute the most to the dissimilarity (14–33%) of benthic assemblages over all reef zones (Fig. 2 and Table 2). The benthic community was dominated by Porites at all four reef sites (around  ~ 45% of cover across all sites), followed by Pocillopora (~ 15% of cover across all sites). Rubble, algae, other life coral, rock, and CCA each individually contributed 5–10% of total benthic cover. Recently dead corals contributed ~ 5% to total benthic cover, and were dominated by dead branching Pocillopora (Table 1). The PCoA results showed that live coral cover on the North reef was dominated mainly by the massive corals Porites and Pavona (~ 80%), and at the rest of the sites, coral cover was dominated by Porites and Pocillopora (~ 60%) (Fig. 2b).

Fig. 2
Fig. 2
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Characterization of benthic communities in the four reef zones off Clipperton Island. a Percentage cover of benthic morpho-functional groups (solid colors) and the proportion of corals displaying a pink-spotted phenotype (grid areas) for each reef zone. b Ordination plot (PCoA; % of total variation explained) of benthic communities and the relationship with coral species. CCA Crustose coralline algae, PS pink-spotted phenotype

Table 1 Benthic cover proportion (mean ± SD of total) of each morpho-functional group, including proportion of pink-spotted corals (potentially reflecting prevalence of trematode infections) for all Clipperton Island reef zones
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Table 2 SIMPER results at coral genera level
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The pink spotted coral phenotype was prevalent at all sites, with an average of 26 and 31% (range 21–38 and 0–66%) prevalence in Porites and other massive corals (Pavona and Leptoseris), respectively (Fig. 2a). No other discolorations suggesting other disease-like phenotypes were observed. While pink spots occasionally matched the presence of small vermetid snails growing in the coral, this was only observed for a minuscule proportion of pink spots observed (estimated < 5% of total observations). Pink-spotted Porites were frequent along transects at all four sites, while other coral genera presenting with pink spots were observed only at the north and south reefs of the atoll (Fig. 2a, Table 1). Abundance of pink spots was heavy in an estimated more than 50% of the surveyed massive coral colonies, including large specimens (> 1 m diameter). Despite the high proportion of coral presenting with the pink-spotted phenotype, highest proportion of dead coral was noted mainly for branching corals and minimal in massive corals with signs of recent macroalgae and coralline algae overgrowth.

Enviromental data analysis showed a mean annual SWT of 28.40 ± 0.80 °C, where the 2015–2016 period had the highest values of monthly SWT and corresponded with the strongest 2015–2016 El Niño warm event over the past 10 years (Fig. 3 and Table 3). In addition, Clipperton Island was affected by ENSO events, cyclones, and a total of 10 hurricanes and 6 tropical storms (in some cases three events per year) (Table 3).

Fig. 3
Fig. 3
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Monthly seawater temperature (mean + SD) from 2008 to 2018 on Clipperton Island. Gray shades represent ENSO periods (La Niña = 2010–2011; El Niño = 2014–2015, 2015–2016), warm and cold phases. Colored shades indicate tropical cyclones that influenced the Clipperton area, yellow = tropical storm, green = Hurricane 1, and purple = Hurricane 2 at Saffir–Simpson scale

Table 3 Historical data of tropical cyclones at Saffir–Simpson scale, maximum wind speed (Wind), annual seawater temperature (SWT), and the intensity of ENSO periods (based on Oni index 3.4) from 2008 to 2018 at Clipperton Island
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Discussion

The benthic reef community composition of Clipperton Island is dominated by reef-building corals, and exhibits a higher live coral cover (in particular of the genera Porites and Pocillopora, exceeding > 60%) compared with other localities along the ETP (Cabral-Tena et al. 2018; Romero-Torres et al. 2020; Cruz-Garcia et al. 2020). This high coral cover suggests overall fair health of this unique coral reef (Wellington et al. 1995; Glynn and Ault 2000; Jost and Andréfouët 2006; Romero-Torres et al. 2020). Yet, high proportions of live corals on Clipperton reefs presented with a pink-spotted phenotype. Of note, such phenotypes can be caused by a penetration by or infection with a range of marine invertebrates, including but not limited to the parasitic trematode Podocotyloides stenometra (Aeby 1992), or by increased sedimentation rates (Tortolero-Langarica et al. 2022a). This observation is possibly related to the combined effects of previous heatwaves, and local inputs of guano-derived nutrients discharged into the reefs during cyclone events (Table 3 and Fig. 3). These results demonstrate that even highly remote reefs supporting high coral cover can be subjected to local threats, including but not limited to putative disease-like phenotypes, which may be related to natural disturbances, such as thermal stress and tropical cyclones.

Our data show that live coral cover of the benthic reef community of Clipperton Island exhibits a similar range of proportion (10–100%) compared to what was reported two decades earlier (Glynn et al. 1996), and characterized by the dominance of only four reef-building coral genera (Porites, Pocillopora, Pavona, and Leptoseris). In addition, coral cover appears to have remained relatively stable, or potentially has rapidly recovered from mass coral mortality events previously reported for the ETP region compared with those coastal reefs steadily influenced by local human-based stressors (Glynn 2000; Hughes et al. 2017a, b, 2018; Eakin et al. 2019; Romero-Torres et al. 2020; Cruz-García et al. 2020; Martínez-Castillo et al. 2020). The composition of benthic morpho-functional groups remains homogeneous around the entire atoll, yet differences in coral community composition between reef zones are apparent, evidencing steady changes in composition from branching to massive corals mainly in the shallow reef community (Fig. 2) (Cabral-Tena et al. 2018; Romero-Torres et al. 2020). This observation may be due to differential exposure to wave energy. The Southern and Eastern reef zones in particular are more protected and may act as shelter areas for branching coral species (i.e., Pocillopora), in contrast to North-Western zones, which are more fragmented in shallow depths, where massive resistant species (i.e., Porites and Pavona) dominate (Figs. 1, 2).

Clipperton Island coral assemblages are remarkably different to coastal ETP reefs due to its prevalence and high abundance of stress-tolerant massive corals over branching corals even on shallow reefs (Glynn et al. 2009, 2015, 2018; Romero-Torres et al. 2020; Tortolero-Langarica et al. 2022b). This feature may be related to the long-term cycle of loss and recovery of coral cover of Pocilloporidae after heat events (i.e., El Niño ENSO 1982–83, 1997–98, and 2015–16; Romero-Torres et al. 2020). These results may suggest that coral diversity (dominated by massive forms) may be able to uphold reef formation and maintain the major geomorphological features characteristic of an atoll similar to other remote and oceanic coral reef locations (i.e., Cocos, Galapagos, and Rapa Nui), in the ETP (Hueerkamp et al. 2001; Glynn et al. 2009; Wieters et al. 2014; Glynn et al. 2015, 2018; Tortolero-Langarica et al. 2022b). Yet, coral assemblages shifting from fast-complex-growth to low-simpler-growth could alter and constrain certain ecological traits, such as rugosity and carbonate production, which will in turn inevitably affect ecosystem functionality (Glynn et al. 1996; Perry and Alvarez-Filip 2018; Cabral-Tena et al. 2018).

A high prevalence of dead and partially dead Porites and Pocillopora at greater depth (18–20 m) previously reported by Glynn et al. (1996) was not apparent in this study, but coral mortality and extreme fragmentation of Pocillopora were evident (personal observation by the authors). This observation may be due to mechanical impacts of severe storms and hurricanes (Table 3 and Fig. 3) that frequently disturb the reef frames of branching corals in the shallower reef areas of Clipperton (Hutchings 1986; Zhao and Raga 2015). The intensive and increasingly frequent storm events (i.e., tropical cyclones, and ENSO) is known to benefit other benthic reef groups (e.g., macroalgae, CCA, and massive corals) less prone to fragmentation, and which compete for available open spaces to settle on the substrate (Sheppard et al. 2009).

For massive corals, partial mortality could potentially be related to the prevalence and high incidence of the pink-spotted phenotype in Porites and tissue lesions on corals off Clipperton Island (Fig. 2). While the (a)biotic cause(s) of the pink-spotted coral phenotype observed on Clipperton Island reefs will still need to be determined using suitable (histological and/or molecular) techniques (Work et al. 2014; Martin et al. 2018), pink-spotted phenotypes which were attributed to P. stenometra infection have previously been observed in Porites throughout the Pacific, ranging from reefs off Hawaii to Guam, Papua New Guinea, Australia, and French Polynesia (Aeby 2003; Martin et al. 2018). Previous studies have reported that such infection can have a negative effect on coral calcification rate, reducing growth rates up to 50%, and increasing bioerosion and space-competition, eventually resulting in coral mortality (Aeby 1992; Trillobet and Golubic 2011). Of note, Porites corals only constitute intermediate hosts of infection with P. stenometra. The final hosts are corallivorous fish, such as butterfly fish, which preferentially feed on swollen, trematode-infected coral polyps, which yield a greater biomass of coral tissues per bite compared to non-infected polyps (Aeby 1992, 2002; Martin et al. 2018). Assuming that the pink-spotted coral phenotype at Clipperton Island reefs can in part be attributed to P. stenometra infection, several potential factors might explain its high prevalence. First, the corallivorous butterfly fish exhibit a low diversity and abundance on Clipperton Island reefs (Robertson and Allen 1996), potentially resulting in relatively low levels of top-down control of potentially trematode-infected coral polyps by feeding. Second, the life cycle of the parasite P. stenometra relies on the presence of multiple hosts during its life cycle, specifically fish, mollusks, and corals. The presence of corallivorous butterfly fish in particular has been linked to coral reef ecosystem health (Hourigan et al. 1988). Consequently, high levels of Porites trematodiasis (with concomitant low levels of other disease-like phenotypes) have previously been linked to healthy coral reef ecosystems (Aeby et al. 2011). Finally, parasite infection–acquisition could potentially be related to the interchange of eutrophic water produced by the phosphate-rich sediments of meromictic enclosed lagoon waters and guano-derived nutrients, which are commonly discharged into the reefs during intense storms and hurricanes (Bourrouilh-LeJan et al. 1985; Jost and Andréfouët 2006). Periodic nutrient enrichment can result in phytoplankton blooms, which correlate with increased growth of pelagic marine invertebrate larvae, such as that of the crown-of-thorn starfish Acanthaster planci (Birkeland 1982; Brodie et al. 2005). Such nutrient enrichment could hence also favor the growth of invertebrate larvae which penetrate and infect coral tissues. On the Northern and Eastern reefs off Clipperton Island, which are closer to the inner lagoon entrances (narrowest carbonate barrier) of the atoll, run-off of nutrient-rich waters from the enclosed lagoon coincide with the observation of higher proportions of pink-spotted coral colonies (Fig. 2). However, the definite cause(s) of the pink-spotted coral phenotype off Clipperton Island still remains to be established.

This study demonstrates that remote shallow oceanic Clipperton Island reefs sustain high live coral cover but may be subject to disease-like conditions, specifically a pink-spotted phenotype which may suggest a high prevalence of invertebrates penetrating and infecting the live coral tissue, including but not limited to parasitic trematodes or natural disturbances, such as sedimentation, thermal stress and storm events. Considering the pronounced effects of such stressors that may slowly erode the fitness of the reef community (as reflected in reduced coral growth and accretion of the reef framework, and/or reduced coral cover). Furthermore, interacting effects of thermal stress and local stressors of corals should be investigated further for a better understanding of long-term dynamics of remote reef systems, natural species resilience and their potential implications (causes and consequences) in the maintenance of the Clipperton benthic coral reef community. Finally, we highlight the importance of establishing regional long-term coral reef monitoring data based on the live coral cover, structure and composition of corals species and other biological and ecological indicators (e.g., calcification, carbonate production, erosion and structural complexity) to inform conservation and management strategies to reduce reef stressors, and to protect the endemism, dispersion function, and natural refuge of coral reef biodiversity that Clipperton provides to the ETP region.