Spatial variability in benthic assemblage composition in shallow and upper mesophotic coral ecosystems in the Philippines

Marine Environmental Research 150 (2019) 104772

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Spatial variability in benthic assemblage composition in shallow and upper mesophotic coral ecosystems in the Philippines

T

Edwin E. Dumalagan Jr.a, Patrick C. Cabaitana, , Tom C.L. Bridgeb,c, Kevin Thomas Goa, Timothy Joseph R. Quimpoa, Ronald Dionnie D. Olavidesa, Jeffrey C. Munara, Cesar L. Villanoya, Fernando P. Siringana ⁎

a

The Marine Science Institute, College of Science, University of the Philippines, Diliman, Quezon City, 1101, Philippines Biodiversity and Geosciences Program, Museum of Tropical Queensland, Queensland Museum Network, 70-102 Flinders St, Townsville, QLD, 4810, Australia c Australian Research Council Centre of Excellence for Coral Reef Studies, James Cook University, 101 Angus Smith Drive, Townsville, QLD, 4811, Australia b

ARTICLE INFO

ABSTRACT

Keywords: Benthic assemblage Coral diversity Reef conditions Reef health

Mesophotic coral ecosystems (MCEs) have received increasing attention in recent years in recognition of their unique biodiversity and also their potential importance as refuges from disturbance events. However, knowledge of the composition of MCEs and how they vary in space is lacking in many regions, particularly the Coral Triangle biodiversity hotspot. Here, we compared the benthic components and coral genera composition between shallow-water reefs (SWRs, 8–13 m depth) and upper MCEs (30–40 m) in four locations in the Philippines that are exposed to differing environmental conditions. Coral cover, abundance, and generic diversity were lower in MCEs than SWRs at three of the four locations. Benthic composition and coral generic composition also varied significantly among locations for both shallow and deep sites. Differences in benthic composition among sites was due primarily to variation in hard corals, macroalgae, sand and silt, while variation in coral assemblage was due to differences in abundance of encrusting Porites, branching Acropora, branching Seriatopora. Our results showed that the composition of MCE communities varied significantly from adjacent shallow reefs, but also among MCEs in differing geographic locations. Furthermore, our results suggest disturbances affecting shallow-water reefs, particularly sedimentation, also negatively impact MCEs, and that depth therefore provides no potential refuge from these disturbances. We recommend that conservation of MCEs consider spatial variability in community composition among sites, and urge further research to better understand the spatial variation in the composition of MCE communities in the Philippines.

1. Introduction Coral reef degradation is accelerating in many parts of the world due to the increasing frequency and intensity of disturbances operating over a range of spatial and temporal scales (Hughes et al., 2003). For example, nearshore reefs are increasingly exposed to higher levels of turbidity due to deforestation and land-use (Quinn and Stroud, 2002; Browne et al., 2015), while even remote oceanic reefs far from direct anthropogenic impacts are threatened by global climate change (Hughes et al., 2017, 2018). However, reefs often exhibit considerable spatial variability in their response to disturbance at smaller scales (Nystrom and Folke, 2001; Roche et al., 2018); for example, the effects of warm-water bleaching events and strong currents caused by storms may attenuate with depth (Abesamis et al., 2017; Muir et al., 2017; Baird et al., 2018; Rocha et al., 2018; Crosbie et al., 2019; Pinheiro et al., 2019a). Consequently, predicting coral reef futures requires ⁎

quantifying variability in the composition of coral reef communities across spatial scales. Historically, most coral reef research has focussed on shallow water reefs (SWR; < 30 m), spanning reef flat to fore reef habitats (Ferrario et al., 2014; Roberts et al., 2015; Heyns et al., 2016). In contrast, benthic and coral assemblages on deeper reefs have received less scientific attention, but advances in diving technology and robotics have led to an increase in awareness of the spatial extent, biodiversity and ecology of mesophotic coral ecosystems (MCEs). MCEs are generally regarded as occurring in depths greater than 30–40 m (Hinderstein et al., 2010; Laverick et al., 2017) and receiving photosynthetically active radiation of < 10% of surface irradiance (Lesser et al., 2009). In addition to their higher than expected biodiversity, MCEs have attracted interest as potential refuges for coral reef biodiversity under the assumption that deeper reefs are less vulnerable to some disturbances (e.g., warm-water bleaching and tropical storms) (Bongaerts and Smith, 2019). However,

Corresponding author. E-mail address: [email protected] (P.C. Cabaitan).

https://doi.org/10.1016/j.marenvres.2019.104772 Received 28 May 2019; Received in revised form 12 July 2019; Accepted 14 August 2019 Available online 15 August 2019 0141-1136/ © 2019 Elsevier Ltd. All rights reserved.

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there are still considerable gaps in MCE research, particularly in the biodiverse Indo-Pacific and Coral Triangle. Within the Coral Triangle, the Philippines is considered the ‘center of the center’ for biodiversity (Veron et al., 2009). However, most studies in the region have been confined to SWRs (Licuanan et al., 2017, 2019), with MCE research still in its infancy (Cabaitan et al., 2019). Many SWRs in the Philippines support low coral cover (Licuanan et al., 2019) attributable to chronic anthropogenic and recurrent natural disturbances such as destructive fishing and storm damage, respectively (Magdaong et al., 2014; Anticamara and Go, 2017). Moreover, most studies on MCEs have focused on comparing species assemblages between SWRs and MCEs at one geographic location (e.g., Abesamis et al., 2017; Nacroda et al., 2017; Quimpo et al., 2018a), while a few have attempted to compare MCEs across geographic regions (Quimpo et al., 2018b, 2019). In addition, most studies of Philippine MCEs have focused on fish species assemblages (Quimpo et al., 2018b), therefore the influence of location and depth on benthic community composition remains poorly known. The aim of this study was to examine variability in the benthic community composition and coral assemblages between SWRs (8–13 m) and MCEs (30–40 m) at four geographic locations exposed to distinct environmental conditions in the Philippines. Specifically, we examined how location and depth influenced (1) benthic cover, and (2) coral assemblages (i.e., generic richness and abundance). This study provides baseline information on coral genera distribution and biodiversity on MCEs in the Philippines.

2.2. Sampling design The sampling sites in each of the four study locations were selected based on depth and presence of complex habitat (i.e., hard-bottom reefs) identified using a side scan sonar (Flores et al., 2019). Assessments of reef benthos and coral assemblages were conducted in both shallow (8–13 m) and mesophotic (30–40 m) depths at each of the four study locations using phototransects. The number of transects varied among locations due to logistical constraints (e.g., limited bottom time due to open circuit SCUBA diving): Calaguas had two transects in each depth, Apo Reef had nine MCE and eight SWR transects, Patnanungan had four MCE and three SWR, and Abra de Ilog had 2 MCE and five SWR transects. Transect tapes, 25 m in length, were laid parallel to the shore at each of the two depths. A camera mounted to a 1-m high steel fabricated monopod was used to record the benthic assemblages along the transects. Pictures of the substrates underneath the transect tape were taken every alternate meter, resulting in 13 photoquadrats from each transect. The 13 photoquadrats from each transect were used as replicates (per site and per depth) in the analysis. A total of 441 photoquadrats were recorded from October 2015 to April 2017 from the MCEs and SWRs of the four study locations. Images of the benthos were analyzed using the Coral Point Count with Excel extensions (CPCe v.3.4; Kohler and Gill, 2006) software. To quantify benthic composition, twenty-five sampling points were overlaid on each image in uniform 5 × 5 grid. Benthos intercepted by the points were recorded and grouped into one of eight benthic categories: live hard corals; consolidated bare substrate that was not covered by corals or other organisms (hereafter referred to as bare substrate); other biota such as gorgonians, soft corals, and sponges; macroalgae; turf algae; and abiotic components that were composed of sand and silt. To quantify coral density and generic richness per quadrat, all live hard corals inside a 1 × 1 m quadrat in every picture were counted and identified to genus based on Richards (2018). Since corals were identified based only on photos, corals could not be identified to species as it entails collection of samples and examination of skeletal structures of the corals in the laboratory. Valid names of corals were based on the World List of Scleractinia (Hoeksema and Cairns, 2019). In addition to taxonomic identity, the morphology of each colony was categorized into six categories: branching (CB), massive (CM), sub-massive (CSM), encrusting (CE), foliose (CF), and solitary (CMR).

2. Methods 2.1. Study locations The study was conducted at four locations (Apo Reef, Calaguas, Abra de Ilog, and Patnanungan) in the Philippines (Fig. 1) that differed in environmental conditions due to monsoonal variations (Aliño and Gomez, 1994) and reef geomorphology (Ross and Hogdson, 1981; Rovere et al., 2015). Apo Reef and Abra de Ilog are situated on the western Philippines near Mindoro Island, whereas Calaguas and Patnanungan are located on the Pacific Seaboard in the eastern Philippines. Apo Reef and Calaguas are located ~30 km off the coasts of Sablayan and Vinzons, respectively. Apo Reef is a pseudo-atoll with an island and fringing reefs and is considered the biggest contiguous coral reef system in the Philippines (Weeks et al., 2010). In contrast, Abra de Ilog and Patnanugnan are situated within ~200 m of the coast and close to population centers, and are therefore influenced by terrestrial runoff. All locations are exposed to the northeast monsoon from November to February, which causes strong winds and waves. However, mean current velocity was higher in Calaguas and Patnanungan (1.138 m-1) than in Apo Reef and Abra de Ilog (0.0949 m-1) (Assis et al., 2017). Underwater visibility was ~5 m in Abra de Ilog while ~15 m in Apo Reef, Patnanungan and Calaguas. Mean temperature (~31.41 °C) and chlorophyll concentration (0.153) were comparable among the four study locations. Reef geomorphology in Apo is diverse, and includes walls, pinnace reefs and terrace slopes in mesophotic depths (Electronic supplementary material 1). The waters surrounding Apo Reef are a marine protected area (MPA) administered as the Apo Reef Natural Park, under the National Integrated Protected Area System (NIPAS Act 7586). Abra de Ilog is located along the Verde Island Passage, a biodiversity hotspot (Carpenter and Springer, 2005). The study sites was situated between river systems, and was therefore exposed to high levels of siltation. Reef mounds are common in Abra de Ilog in both SWRs and MCEs (Electronic supplementary material 1). At Calaguas, forereefs are common at SWRs and MCEs, with the study location having three MPAs and is a popular tourist destination. Patnanungan has fringing reefs that are heavily impacted by human activities such as fishing and mariculture. Similar to Apo Reef, reef geomorphology at Patnanungan is diverse, with walls, pinnacles and terraces common. Shallow forereefs were common at shallow depths at all four sites.

2.3. Statistical analysis Spatial variability in benthic and coral assemblage composition between depths and among locations was examined using multivariate techniques in the program PRIMER (Plymouth Routines In Multivariate Ecological Research) (Clarke and Gorley, 2006). Permutational multivariate analysis of variance (PERMANOVA) based on a Bray-Curtis dissimilarity matrix was used to test the differences in benthic and coral assemblage composition between depths (SWRs and MCEs) and among locations (four locations). Principal coordinate analysis (PCO) was then used to visually explore differences in benthic and coral assemblage composition. Vectors were fitted onto the ordination plots to indicate the variables that best explained the relationships among locations and depths. Similarity percentage (SIMPER) analyses were also used to identify the benthos and corals that contributed to the dissimilarities between depths and locations. General Linear Models (GLM), using the program Statistica, were used to examine the differences in percentage cover of the different benthos and coral genera, and generic richness and density of corals among locations and between depths. Significant results in GLMs were further tested with Tukey's HSD post hoc test to see which locations had significant differences between depths. 3. Results A total of 5008 coral colonies representing 87 genera and 21 families were recorded across all locations (Electronic supplementary material 2). Of the 87 coral genera, 67 were observed in MCEs, 66 in SWRs, and 46 were recorded in both MCEs and SWRs. Despite no 2

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Fig. 1. Map of the Philippines showing the study locations (green circles) of Apo Reef, Calaguas, Abra de Ilog and Patnanungan. Closed blue circles represent mesophotic coral ecosystem (MCE) sampling sites and open blue circles are shallow water reef (SWR) sampling sites. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

difference in the total number of genera recorded in shallow and deep reefs, generic richness was higher in SWRs than in MCEs in all locations except for Calaguas. Porites, Acropora, Dipsastrea and Favites were the most common taxa across all depths (see also Electronic supplementary material 4). Acropora was the most abundant coral in the SWRs, while MCEs were dominated by Porites.

between depths (Table 1a; Fig. 2). PCO and PERMANOVA analyses indicated that differences in benthic assemblage composition between MCE and SWR were greater at Apo Reef and Abra de Ilog than at Calaguas and Patnanungan (Fig. 3; Table 1). Vectors indicated that sites at Apo Reef and Calaguas were associated with live corals and bare substrate, while algae and silt characterized Patnanungan and Abra de Ilog, respectively (Fig. 3). Pair-wise comparisons showed that the benthic assemblage composition also differed between locations within each depth (Table 1b). The difference in benthic assemblage composition was more apparent between Apo Reef and Abra de Ilog and

3.1. Benthic assemblage composition Benthic assemblage composition varied among locations and 3

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Table 1 PERMANOVA results of benthic assemblage composition in response to depth, location and the interaction between the two variables. a) Main effects and interaction Depth Location Location x Depth

F 34.451 98.002 5.0541

p 0.001 0.001 0.001

F 2.753 7.228 9.255 6.460 4.556 6.172 F 3.629 5.406 12.433 4.063 7.036 8.417

p 0.001 0.001 0.001 0.001 0.001 0.001 p 0.001 0.001 0.001 0.001 0.001 0.001

F 22.459 5.4971 20.341 4.484

p 0.001 0.009 0.001 0.016

b) Between locations per depth MCE Apo Reef vs Calaguas Apo reef vs Abra de Ilog Apo reef vs Patnanungan Calaguas vs Abra de Ilog Calaguas vs Patnanungan Abra de Ilog vs Patnanungan SWR Apo Reef vs Calaguas Apo Reef vs Abra de Ilog Apo Reef vs Patnanungan Calaguas vs Abra de Ilog Calaguas vs Patnanungan Abra de Ilog vs Patnanungan

Fig. 3. Principal Coordinates Analysis (PCO) for fourth-root transformed benthic assemblage composition using Bray-Curtis dissimilarity, with vectors showing the direction and strength of change of the coverage of different benthic categories on shallow water reefs (SWR) and mesophotic coral ecosystems (MCE) at four sampling sites: Apo Reef, Calaguas, Abra de Ilog, and Patnanungan. Abiotic refers to sand and silt.

c) Between depths per location Apo Reef Calaguas Abra de Ilog Patnanungan

bare substrate (Fig. 4b), with significantly higher cover in SWRs than MCEs only at Abra de Ilog. Abiotic components were highest in Abra de Ilog, especially in the MCE (Fig. 4c). Other biota such as sponge and soft corals were rare at most locations (Fig. 4d). Macroalgae and turf algae were highest at Patnanungan (Fig. 4e and f).

Patnanungan (between reef locations with high and low coral cover, respectively), than between Apo Reef and Calaguas (both had high coral cover). Interestingly, there were also differences in benthic composition between locations that had low coral (i.e., Abra de Ilog and Patnanungan; Table 1b). Differences in benthic composition between depths were evident at Apo Reef and Abra de Ilog (Table 1c). Hard corals, bare substrate, abiotic components, other biota, macroalgae and turf algae contributed to the differences in assemblage composition between locations and depths (Electronic supplementary material 3). Percentage cover of hard corals were higher in both MCEs and SWRs of Apo Reef and Calaguas than of Abra de Ilog and Patnanungan (Fig. 4a). All locations had high cover of consolidated

3.2. Coral assemblage composition Encrusting Porites were associated with MCEs and massive Porites, branching Porites and branching Acropora were characteristic of SWRs (Fig. 5). PERMANOVA pair-wise comparisons revealed that coral assemblage composition differed between locations at MCEs and SWRs (Table 2b). Coral assemblage composition was also different between depths at each of the four study locations (Table 2c), but the difference between depths were greater at Apo Reef and Calaguas (Fig. 5). High variability in coral assemblage composition was also observed between transects, particularly in Apo Reef.

Fig. 2. Representative photos of the SWRs and MCEs of the study locations showing the variability in benthic assemblage composition.

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Fig. 4. Percent cover (mean ± standard error of the means) of a) live hard corals, b) bare substrate, c) abiotic component, d) other biota such as gorgonians, soft corals and sponges, e) macroalgae and f) turf algae in shallow water reefs (SWR) and mesophotic coral ecosystems (MCE) for Apo Reef, Calaguas, Abra de Ilog and Patnanungan. Asterisks represent significant difference between SWR and MCE using a Tukey's HSD post-hoc test.

Encrusting Porites, massive Porites, branching Acropora, branching Seriatopora, and massive Favites contributed to the variability in coral assemblage composition among locations at both MCEs and SWRs, and between depths at each location (Electronic supplementary material 4). Encrusting Porites, branching Acropora, and branching Seriatopora were consistently more abundant in MCEs and SWRs in Apo Reef than in Abra de Ilog and Patnanungan. The aforementioned coral genera were also abundant in Calaguas. The differences in the abundance of encrusting Porites, branching Seriatopora and branching Acropora contributed to the variation in the coral assemblages between MCEs and SWRs in Apo Reef and Calaguas. At the low coral cover reefs of Abra de Ilog and Patnanungan, differences in coral assemblages were attributed to the differences in abundance of encrusting Porites, massive Porites, and massive Favites.

post hoc test: p < 0.05). Richness was higher in MCEs than in SWRs in Calaguas, but was not statistically significant. Density of corals between depths varied among location (Table 3; Fig. 6b): total coral densities was higher in Apo Reef and Calaguas than in Abra de Ilog and Patnanungan. Coral density was significantly lower in MCEs than in SWRs only in Apo Reef (Tukey's HSD post hoc test: p < 0.05) and did not vary between depths at the other three locations. The most abundant corals across all study locations were tabulate and branching Acropora; Merulinidae; massive, submassive, branching and encrusting Porites; and foliose Montipora (Fig. 7; Table 3). Branching and tabulate Acropora were abundant in SWRs of Apo Reef and Calaguas. Merulinidae (mainly composed of Dipasatrea, Favites and Goniastrea) were recorded in all locations except MCEs at Abra de Ilog (Fig. 7b). Merulinidae abundance was higher in Calaguas, with density higher at SWRs than MCEs. Massive and submassive Porites abundance was highest at Apo Reef (Fig. 7c), with SWRs consistently having higher abundance than MCEs across all locations. Branching Porites were only observed in Apo Reef and were more abundant in SWRs than in MCEs (Fig. 7d). Encrusting Porites were abundant in the MCEs of Apo Reef and Calaguas (Fig. 7e), but were also recorded at the other two locations. Foliose Motipora was abundant in the MCEs of Apo Reef and Calaguas (Fig. 7f).

3.3. Coral generic richness and abundance Coral generic richness was variable between depths at Apo Reef and Abra de Ilog, but not at Calaguas and Patnanungan (Table 3; Tukey's HSD post hoc test: p < 0.05). Calaguas had the highest generic richness, followed by Apo Reef (Fig. 6a). Richness was significantly higher in SWR than in MCE only in Apo Reef and Abra de Ilog (Tukey's HSD 5

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Table 3 GLM analysis results of a) percentage cover of different benthos, b) abundance of different coral genera, and c) overall coral abundance and richness in response to location, depth, and the interaction between the two variables. a) Percentage cover of different benthos

Location Depth Location X Depth

Location Depth Location X Depth

Live Hard F 48.362 11.282 3.396

Coral p < 0.001 < 0.001 0.018

Bare substrate F p 32.072 < 0.001 16.273 < 0.001 9.465 < 0.001

Abiotic components F p 62.373 < 0.001 55.318 < 0.001 4.622 0.003

Macroalgae F 259.1510 68.296 54.839

p < 0.001 < 0.001 < 0.001

Turf Algae F p 40.749 < 0.001 23.090 < 0.001 21.425 < 0.001

Acropora ACT/CB F p 27.853 < 0.001 11.403 < 0.001 3.896 0.009

Merulinidae F p 17.118 < 0.001 32.990 < 0.001 1.955 < 0.120

Porites CM/CSM F p 7.497 < 0.001 79.726 < 0.001 4.432 0.004

Porites CB F 20.444 10.427 19.029

Porites CF F 6.974 11.692 7.097

Porites CE F p 24.704 < 0.001 54.623 < 0.001 15.449 < 0.001

Other biota F p 14.126 < 0.001 0.586 0.444 1.355 0.256

b) Abundance of different coral genera

Fig. 5. Principal Coordinates Analysis (PCO) for fourth-root transformed coral assemblage composition using Bray-Curtis dissimilarity, with vectors showing the direction and strength of change of the coverage of different coral genera on shallow water reefs (SWR) and mesophotic coral ecosystems (MCE) at four sampling sites: Apo Reef, Calaguas, Abra de Ilog, and Patnanungan.

Location Depth Location X Depth

Table 2 PERMANOVA results of coral assemblage composition in response to depth, location and the interaction between the two variables.

Location Depth Location X Depth

a) Interaction across sites and depths Depth Location Location x Depth

F 29.031 10.457 7.2264

p 0.001 0.001 0.001

F 3.131 1.796 4.272 2.405 3.798 1.731 F 2.981 3.787 3.452 2.537 2.208 1.821

p 0.001 0.006 0.001 0.001 0.001 0.016 p 0.001 0.001 0.001 0.001 0.001 0.001

Location Depth Location X Depth

F 54.975 12.335 6.435 11.920

p 0.001 0.001 0.001 0.001

Abundance F p 47.860 < 0.001 4.212 0.041 4.693 0.003

Richness F 68.292 12.653 9.520

p < 0.001 < 0.001 < 0.001

because they show that MCEs cannot be considered to be homogeneous, but that their benthic communities vary considerably depending on geological setting and environmental characteristics (Ross and Hogdson, 1981; Aliño and Gomez, 1994; Rovere et al., 2015). Importantly, our results also suggest that MCEs may be as strongly influenced by factors such as sedimentation as shallow-water reefs, resulting in depauperate MCE communities at sites with high sedimentation rates. In contrast, MCEs at well-protected sites with good water quality such as Apo Reef were also in good condition and supported a high diversity of benthic taxa. Taken together, these results suggest that although benthic communities associated with MCEs in the Philippines exhibit considerable spatial variability, broad-scale environmental factors influencing shallow reefs may provide a good indication of the communities on adjacent MCEs. Higher coral cover in SWRs was largely due to fast-growing branching Acropora as well as massive Porites, both of which common coral taxa in many shallow water reefs (Wilkinson, 1998; Sheppard, 1999; Raymundo et al., 2005). On the other hand, Acropora was rarer on MCEs, where coral communities where dominated by encrusting Porites and merulinids. The high abundance of foliose, encrusting and submassive taxa at the expense of Acropora on MCEs is consistent with observations of MCEs elsewhere (Done, 1982; Wilkinson, 1998; Sheppard, 1999; Raymundo et al., 2005; Forsman et al., 2009; Hoeksema et al., 2016). Hard corals with encrusting and foliose growth forms would enable them to efficiently harbour limited light irradiance essential for zooxanthellae photosynthesis (Kahng et al., 2014, 2017), which suggests that the variability in the coral assemblage composition is likely driven by the exponential decrease in light irradiance with

c) Between depth per site Apo Reef Calaguas Abra de Ilog Patnanungan

p < 0.001 < 0.001 < 0.001

c) Overall coral abundance and richness

b) Between sites per depth MCE Apo Reef vs Calaguas Apo Reef vs Abra de Ilog Apo Reef vs Patnanungan Calaguas vs Abra de Ilog Calaguas vs Patnanungan Abra de Ilog vs Patnanungan SWR Apo Reef vs Calaguas Apo Ree vs Abra de Ilog Apo Reef vs Patnanungan Calaguas vs Abra de Ilog Calaguas vs Patnanungan Abra de Ilog vs Patnanungan

p < 0.001 0.001 < 0.001

4. Discussion MCEs in three of the four locations supported lower coral cover, abundance, and generic diversity than SWRs, a similar pattern to many other MCEs globally (e.g., Lesser et al., 2009 but see Muir et al., 2018). However, overall community composition was more similar between shallow and deep sites at the same location than among MCEs at different locations. These results suggest that location-specific factors (e.g., geomorphology, oceanographic conditions or disturbance regime such as exposure to sedimentation) are more important determinants of benthic communities than depth per se. These findings are important 6

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Fig. 6. a) Coral generic richness (mean ± standard error of the means) and b) coral abundance (mean ± standard error of the means) in shallow water reefs (SWR) and mesophotic coral ecosystems (MCE) for Apo Reef, Calaguas, Abra de Ilog and Patnanungan. Asterisks represent significant difference between SWR and MCE using a Tukey's HSD post-hoc test.

increasing depth (Hoegh-Guldberg, 1999; Smith et al., 2004). Benthic assemblage composition on SWRs and MCEs spatially vary in the scale of 100s of meters, 10s of kilometres, and 100s of kilometres (Cornell and Karlson, 2000; Smith et al., 2010; Bridge et al., 2011a, 2011b, 2012; Keith et al., 2013), a pattern we also found in the Philippines. Our sites are spread across two of the five marine biogeographic regions in the Philippines identified by Aliño and Gomez (1994). Apo Reef and Abra de Ilog are located within the South China Sea bioregion and separated by 110 km, whereas Calaguas and Patnanungan are located in the Northern Philippine Sea facing the Pacific Ocean and separated by ~100 km. Results indicated apparent differences in benthic assemblage composition between study locations situated in a similar biogeographic region, which were also observed in some of the benthic communities in the Great Barrier Reef and Florida Reef Tract (Murdoch and Aronson, 1999; Bridge et al., 2011a, 2012, 2012b). Fish communities at the same sites exhibit similar variability in assemblage composition among study locations (Quimpo et al., 2018b), which suggests that factors influencing the variability in assemblage composition in MCEs operate at the scale of locations, i.e., 100s of kilometers (Bridge et al., 2011a, 2011b, 2012). The observed variability among locations combined with the taxa characteristic of each location provides insight into the prevailing environmental conditions influencing benthic community composition. Apo Reef and Calaguas had higher coral cover at both shallow and mesophotic depths than Abra de Ilog and Patnanungan. Apo Reef and

Calaguas are located in MPAs, which may contribute to the higher coral cover observed at these study locations through mediating negative impacts such as fishing. Apo is one of the best-managed MPAs in the Philippines (Cabral et al., 2014; Quimpo et al., 2018a), while in Calaguas many fishers have shifted from fishing to ecotourism activities (unpublished data). Increases in coral cover following removal of fishing effort was also observed in Hawaiian MCEs (Richmond and Stevens, 2014), and may also benefit reefs in the Philippines. In contrast, Abra de Ilog had the highest percentage cover of sediment and silt, likely because of its proximity to river systems. Sedimentation negatively impacts benthic organisms both directly via smothering, but also indirectly through decreasing light irradiance and inhibiting coral recruitment (Erftemeijer et al., 2012.; Browne et al., 2015). Given that MCEs are already light-limited (Kahng et al., 2014), is likely that areas subjected to terrestrial runoff are likely to be depauperate in benthic fauna. Patnanungan is less exposed to sediment but a high abundance of macroalgae and turf algae which negatively impact coral recruitment and growth (Clements et al., 2018; Johns et al., 2018). The high abundance of macroalgae may be due to nearby fish mariculture sites that use commercial fish feeds with high nutrient content known to enhance algal growth (McCook, 1999; San Diego-McGlone et al., 2008). Together, these highlight that stressors such as sedimentation and eutrophication can have detrimental impacts to MCEs as well as shallow reefs, but also highlights that local management actions that mediate these stressors are likely to benefit MCEs as well as SWRs. 7

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Fig. 7. Abundance (mean ± standard error of the means) of a) Acropora ACT and Acropora CB, b) Merulinidae, c) Porites CM and Porites CSM, d) Porites CB, e) Porites CE, and f) Montipora CF in shallow water reefs (SWR) and mesophotic coral ecosystems (MCE) for Apo Reef, Calaguas, Abra de Ilog and Patnanungan. Asterisks represent significant difference between SWR and MCE using a Tukey's HSD post-hoc test. ACT is Acropora coral tabulate, CM is massive corals, CSM is submassive coral, CB is branching corals, CE in encrusting coral, and CF is foliose coral.

Information on the variability in benthic and coral assemblage composition was obtained using photoquadrats, which limited the taxonomic resolution of coral identifications to genus. Despite the coarse taxonomic resolution, benthic and coral assemblage composition were distinct in each of the locations and depths. Benthic surveys with higher taxonomic resolution identifying corals to species level would likely result in greater differences in composition between shallow and deep sites. Nonetheless, our results suggest that despite examining four very different habitat types, there is consistently limited overlap in benthic community composition between SWRs and MCEs. In addition, the deepest sites examined in our study were at 40 m depth, and it is likely that examining deeper sites would result in even greater differences between SWRs and MCEs. Despite the relatively low overlap in species composition, it is likely that a subset of species do occur in both shallow and mesophotic depths. To better understand connectivity between deep and shallow reefs, future studies should examine vital population processes (e.g., recruitment, growth, mortality) of coral species common between SWRs and MCEs in different regions. Our results suggest that a generalization on the pattern of coral cover, abundance and diversity between SWRs and MCEs could not be made as not all MCEs contained lower coral

cover, abundance, and genera diversity than their SWR counterparts. Also, MCEs in the Philippines appear vulnerable to some of the same stressors as SWRs, particularly sedimentation (Rocha et al., 2018), and therefore are not necessarily protected from disturbances. Expanding marine protected areas could improve protection and conservation covering many species found exclusively in MCEs (Pinheiro et al., 2019b), but only where MPAs can mediate the impacts of stressors. Therefore, expanding MPAs where the main threat seems to be terrestrial runoff would likely have minimal benefit. Acknowledgements We are grateful to the Apo Reef Protected Area Management Board of the Department of Environment and Natural Resources (DENR PAMB) for allowing us to conduct the fieldwork. We thank the Municipal Government of Sablayan, A. Vallejo of Sablayan Tourism Office, F. Magno of DENR-PAMB, Mark Tolentino and Frederico Sabban for their assistance in the field surveys; Ma. Angelique Doctor for preparing the map; and Ian de Guzman for improving the resolution of the figures. This work was funded by the Department of Science and Technology - Philippine Council for Agriculture, Aquatic and Natural 8

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Resources Research and Development (DOST PCAARRD) through its Geo-Physical Coral Mapping (GCM) Project, which was awarded to F.P.S.

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