Geographic Variation for the Composition of Parrotsh in the South China Sea

Based on the key ecological processes of parrotsh in coral reefs, we compiled species presence-absence data across 51 sites in the South China Sea to identify the distribution and composition of parrotsh and explore the relationship between species distribution and environmental factors, and 50 species (the Pacic: 57 species) of parrotsh were record. Nansha islands had the highest abundance with 41 parrotsh species. Nestedness analysis indicated parrotsh community had statistically signicant nested patterns in the South China Sea and Nansha islands was the topmost site of nested matrix rank. Scleractinian coral species richness and Log(reef area) both had a signicant effect on sites nested matrix rank (P < 0.05), which supports habitat nestedness hypothesis in the South China Sea. Scrapers were the most important functional group composition while the browser had a greater contribution on species nested matrix rank. Linear regression model showed parrotsh species richness increased with increasing longitude, scleractinian coral species richness and reef area. Variations in the parrotsh species richness in longitude was related to distance from the biodiversity hotspot in the Indo-Australian Archipelago. Parrotsh was mainly distributed in the range of 26-29 ℃ , which was almost the same as the optimum temperature for coral growth. Nansha islands should be as biodiversity conservation priority areas, which could provide important reference signicance for conservation efforts of parrotsh in degraded coral reefs habitats, especially in the context of increasing natural variability and anthropogenic disturbance.


Introduction
Parrot sh are recognized as a distinct family, the Scaridae, closely related to the Labridae(Sabetian 2010; Bonaldo et al. 2014). They are protogynous hermaphrodites, undergoing a sex change from female to the terminal male phase (Choat and Robertson 1975), and tending to have different colours and habits among each phase (juvenile, female, male) (Siebeck 2018). At present, 100 recognized parrot sh species belonging to 10 genera (Bolbometopon (1 spp.), Calotomus (5 spp.), Cetoscarus (2 spp.), Chlorurus (18 spp.), Cryptotomus (1 spp.), Hipposcarus (2 spp.), Leptoscarus (1 spp.), Nicholsina (3 spp.), Scarus (52 spp.) and Sparisoma (15 spp.)) in two subfamilies (Scarinae and Sparisomatinae) have been described worldwide (Kulbicki et al. 2018). Genera Sparisoma and Cryptotomus are restricted to the Atlantic, Nicholsina is found in both the Atlantic and Eastern Paci c, ve genera are unique to the Indo-Paci c (Bolbometopon, Cetoscarus, Calotomus, Hipposcarus, and Chlorurus), and the genus Scarus is found in all oceans (Kulbicki et al. 2018). Although the geographic distributions of most parrot sh were known (Bonaldo et al. 2014 Edwards et al. 2014). For example, parrot sh account for the largest proportion of sh biomass (36.8%) caught from coral reef in Polynesia (Pratchett et al. 2011). In terms of ecological function, parrot sh are considered herbivores. One of the most powerful demonstrations of the functional importance of parrot sh (and other herbivorous reef sh) is the large-scale sh exclusion experiment conducted by Hughes et al (Hughes et al. 2007), which showed that the removal of herbivores after mass coral bleaching severely eroded the reef's ability to recover and regenerate. They can help to mediate the competition between corals and macroalgae and enhancing the resilience of coral reef ecosystems following anthropogenic or natural disturbance (Adam et al. 2015). By exerting top-down control on algal communities in a cropped state can provide more space resources for corals and promote the attachment and recruitment of coral larvae, whcih is a vital ecological process (Bellwood et al. 2012;Thurber et al. 2012;Adam et al. 2015;Roos et al. 2016). Compared to other herbivorous sh, parrot sh have specialized feeding morphology that can remove the calcareous surface layers of the reef as they graze and get nutritional resources that are largely unavailable to other shes. Coupled with abundance, their unique interactions (i.e., grazing, erosion, coral predation, production, reworking and transport of sediments) makes parrot sh an integral part of coral reefs (Bonaldo et al. 2014).
Despite their importance to reef ecosystems, parrot sh has still failed to ward off the threat of arti cial factors (Bellwood et al. 2012;Choat et al. 2012;Heenan et al. 2016). Over-exploitation and habitat degradation were considered to be important man-made reasons for the decline of reef sh stocks (Hawkins and Roberts 2004;Hamilton et al. 2017;Suciyono et al. 2019). For example, Bolbometopon muricatum and Scarus guacamaia were classi ed by the International Union for Conservation of Nature (IUCN) as "vulnerable" (VU) and "near threatened" (NT), respectively. Over shing can lead to signi cant declines in sh populations and a tendency to miniaturize individuals, which is detrimental to parrot sh's ecological functions (Hawkins and Roberts 2004;Bellwood et al. 2012). Habitat complexity also plays a key role in reef sh community construction, with reduced complexity leading to a decrease in reef sh richness and diversity (Bellwood et al. 2006;Emslie et al. 2014;). It could lead to local extinction in extreme circumstances (Emslie et al. 2014). And a full understanding of parrot sh composition and distribution patterns and the formation and driving factors of species diversity are necessary and essential steps, if we want to effectively protect parrot sh resources and coral reef ). The geographical distribution pattern of species diversity is one of the main topics in biogeography (Losos and Ricklefs 2009). Biogeographers believed that the distribution pattern of species richness at a large regional scale can be determined by a variety of factors, such as available habitat, latitude and longitude, temperature, connectivity, evolutionary history, dispersal and colonization capacity, etc (Bellwood and Hughes 2001;Mora et al. 2003;Mcclanahan et al. 2011;Parravicini et al. 2013). There are two main gradients in the global distributions of coral reef sh. The rst major distribution gradient is the distance from the center of biodiversity, represented by the Indo-Australian Islands, commonly known as the Coral Triangle (Allen 2008). The second major distribution gradient is the latitudinal gradient, where a decline in species diversity is a common feature of many biota (Choat 1991). Based on most work on the distribution characteristics of parrot sh diversity (Choat et  The South China Sea lies in the tropical zone of the western Paci c Ocean bordered by nine coastal states, with a surface area of 3.5 million square kilometers (Wang et al. 2012). It is one of the world's richest marine biodiversity hotspots, with abundant and diverse marine resources. Existing research reports indicate that a preliminary assessment of the South China Sea biological diversity contains more than 8,600 species of plants and animals (Ng and Tan 2000). Fish alone contribute 3,365 species (Randall and Lim 2000). At the same time, the South China Sea is an important transfer station for reef shes to spread from the coral triangle to high latitude in China (Gao et al. 2014). The resources of the South China Sea where sh is the major protein source for coastal communities, and where contribute to the economic livelihood of neighboring countries (Nguyễn 2004). However, the progress of science technology, the increase of human demands and growing coastal populations have signi cantly increased the pressure on reef sh stocks (Cinner and Mcclanahan 2006).
Due to the unique importance of parrot sh in reef systems and the lack of research in the South China Sea, investigating the species composition of parrot sh and their relationship with environmental factors in various regions can explore the spatial distribution characteristics and the most suitable living environment for parrot sh. The purpose of this article is a) to investigate parrot sh species composition and spatial distribution patterns in the South China Sea; b) to explore the relationship between parrot sh species richness and environmental factors.

Materials
Study sites. The South China Sea(Randall and Lim 2000) is a semi-enclosed sea that is part of the Paci c Ocean (bordered by Brunei Darussalam, Cambodia, China, Indonesia, Malaysia, Philippines, Singapore, Thailand, and Vietnam and contains numerous small islands (Nguyễn 2004).To obtain a comprehensive dataset about the distribution patterns of parrot sh in the South China Sea, we collected data from 51 sites, including Tioman island in Malaysia, Natuna islands and Anambas islands, Redang island, Nansha islands, Taiping island, Subi reef, Zhongye island, Brunei Darussalam, EI Nido in Philippines, the Vietnam coastal areas (including Con Dao, An Thoi, Cu Lao Cau bay, Nha trang, etc), Cambodia, Koh Tao in Thailand, Xisha islands, Qilianyu, Hainan island, Dongsha islands, Weizhou island, Daya bay, Minjiang river estuary, Jiulong river estuary, Pearl river estuary, Hongkong, Taiwan islands (subdivided into the southern, northern, eastern and western of Taiwan), Kenting National Park, Lanyu, Green island, Ryukyu and South Penghu National Park. All sites were between 99.84 °E and 121.73 °E, and between 2.78 °N and 26.06 °N.
Data collection. Collecting information on the composition and distribution of parrot sh in the South China Sea was through published works, regional checklists, monographs on speci c families, scienti c reports, and databases to obtain species records of parrot sh (i.e., presence/absence data). In addition, unpublished data from our team were used only in the compilation of species records for Xisha islands and Qilianyu. In the search process of scienti c reports, key words were mainly reef sh, parrot sh, distribution, South China Sea and the place names mentioned above. It also searched by country or region in the Fishbase and through the Taiwan sh database (http:// shdb.sinica.edu.tw), from which mainly inquired information about the distribution of parrot sh in Taiwan islands and its surrounding islands. The full data set and detailed list of synonyms were available as a supplementary see Fishbase (https:// shbase.cn/summary/FamilySummary.php?ID=364).
According to jaw morphology, foraging activity and extent of substratum excavation, parrot sh were commonly classi ed into three main functional groups: browsers, scrapers and excavators (Bonaldo et  The environmental factors in this article include geographical location (i.e., latitude and longitude), scleractinian coral species richness, reef area, and sea surface temperature. First of all, latitude and longitude were mostly from wikipedia (http://en.wikipedia.org/). We also consolidated species records of scleractinian coral and reef area from literature, reports and books. Extensive search was conducted using key words such as coral reefs, reef-building corals, marine reserves, area and place names of various research sites in the retrieval process. At the same time, using Reefbase (http://www.reefbase.org/main.aspx) was used to supplement. But reef area of some sites (such as Green island, Lanyu, Hongkong) were unable to access via online data. The sea surface temperature were mainly obtained through the following websites: National Oceanic and Atmospheric Administration (http://www.noaa.gov/), Weather-stats (https://weather-stats.com/seamap), World sea water temperatures (https://seatemperature.info/). Nestedness analysis. Based on the collected parrot sh data, a nested model was used to explore the distribution pattern of parrot sh in the South China Sea. Because nestedness is not a stable universal structure, it is closely related to the study object (such as category, island habitat type, matrix size, etc.) (Chen and Wang 2004). Firstly, sites with the paucity of published data or not conform to islands habitat types were removed from our analysis, such as eastern Taiwan, southern Taiwan, northern Taiwan, Cambodia, Brunei Darussalam, etc. Finally, 24 sites were eventually selected for nestedness analysis. The same sites were true for the following analysis. At rst, a binary code "1/0" was used to show presence/absence of species at various sites. The temperature of the matrix is the disorder degree of the matrix system, which can re ect the deviation degree of the analyzed matrix from the completely nested matrix (Zhang et al. 2008). The lower temperature of the matrix, the higher nestedness degree of the matrix. Thus T ranges from 0 for a completely nested matrix to 100 for one that is completely disordered (Boecklen 1997;Wright et al. 1998). Species nestedness is currently calculated with the nestedness temperature T. We based on the calculation of matrix temperature (matrix temperature) of BINMATNEST (binary matrix nestedness temperature calculator) software to quantify nestedness. "BINMATNEST" will arrange input matrix to maximal packing that the occurrence of speices are as much as possible in the top left corner of the matrix, and calculate the nestedness temperature. At the same time, the null model of the software will randomly generate 1,000 matrices for the signi cance test of the input matrix. BINMATNEST creates three null models to test the signi cance of the results, among which null modal 3 has been proved to effectively control the in uence of passive sampling(Moore and Swihart 2007; Rodríguez-Gironés and Santamaría 2010). The sequence of sites was calculated by BINMATNEST and the rank of species was sort according to occurrence frequency, maximum body length and morphological characteristics (the ratio of body length and body depth from Fishbase), which were called species nested matrix rank. First of all, in order of occurrence frequency, the species with high frequency was ordered from the top, when the occurrence frequency of species were the same, the maximum body length was used for further ranking, with larger maximum body length rst. When the maximum body length was still the same, the species with the largest ratio was priority ordering according to the ratio of body length and body depth. The information of maximum body length and the ratio of body length and body depth were both obtained from Fishbase.
Statistical analyses. Paired sample t-test was used to test whether there was a signi cant difference in the number of the three functional groups in each site. The effect of environment factors (latitude, longitude, sea surface temperature, Scleractinian coral species richness, reef area) and species life-history traits on forming a nested pattern were evaluated by Spearman's rank correlation analysis (Schouten et al. 2007;Li et al. 2013). which was conducted between the nested matrix rank of site and environment factors as well as nested matrix rank of species and the maximum body length. According to the nested matrix rank of sites, we divided all sites into two groups and used independent samples t-test to compare whether there was a signi cant difference between the means values (scraper, excavator, browser, scraper/total, excavator/total, browser/total) of the two groups.
We applied a basic linear models to data from all sites to quantify the relationship between species richness and environmental factors, parrot sh species richness was taken as dependent variables, and environmental factors (scleractinian coral species richness, reef area, sea surface temperature, latitude and longitude) were taken as independent variables. The above data calculation and analyses were performed in IBM SPSS Statistics 26 software. In all analyses involving signi cance tests, we followed the common view that P < 0.05 means statistically signi cant differences, P < 0.01 means strongly signi cant differences and P > 0.05 means non-signi cant differences.
R was used to draw the map of study region and the distribution diagram of parrot sh species richness.
Origin 2018 was used to perform linear regressions or nonlinear tting of parrot sh species richness with respect to environment factors.

Results
Species composition. A total of 50 species across 7 genera were recorded at 51 sites in the South China Sea (see Tab S1). Genus Scarus, Chlorurus and Calotomus have 28, 13 and 3 species of parrot sh respectively. Followed by genus Cetoscarus and Hipposcarus, there were both 2 species of parrot sh. Genus Bolbometopon and Leptoscarus both had only 1 species of parrot sh. Distribution characteristics of parrot sh species richness in the South China Sea was shown in Fig. 1. Parrot sh species richness were abundant in Nansha islands, Taiwan islands and Nha Trang. Among them, Nansha islands had the highest number of parrot sh with 41 species, followed by Taiwan islands with 38 species, and the two sites had 31 species in common. Co To in Vietnam and Minjiang River Estuary in China both had the lowest abundance, with only 2 species of parrot sh. The coastal sits had relatively few parrot sh species richness, such as Koh Tao, Redang island and Con Dao, while Nha trang had more abundant parrot sh species richness (33 species). In Taiwan islands, the southern region had the most abundant species of parrot sh, with 36 species. Compared with the whole Taiwan islands, Southern Taiwan was lacking of Scarus scaber and Scarus ferrugineus, among which Scarus scaber was recorded in the northwest of Taiwan, while Scarus ferrugineus was recorded in Penghu islands. Scarus ghobban are the most widely distributed species, with 47 sites, followed by Chlorurus sordidus (38 sites) and Scarus niger (37 sites).Chlorurus perspicillatus, Chlorurus strongylocephalus, Chlorurus troschelii and Hipposcarus harid all were found in a single site.
Composition of functional groups. Three functional groups of parrot sh (30 scrapers, 4 browsers and 16 excavators) were found in the South China Sea (see Tab S1). Scrapers were the most extensive distribution and browsers were the most restricted (Table 1). In addition, paired sample t-test showed that there was a signi cant difference in the number of scrapers and excavators (t 50 = 11.500, P =0.00 < 0.01) as well as excavators and browsers (t 50 = 9.46, P =0.00 < 0.01). "0"represents that the functional group was not collected and it did not mean that the functional group did not exist; Zhongye Island and EI Nido both had 2 unde ned species and South Penghu National Park had 1 unde ned species in published book or literature.
Nestedness of parrot sh assemblages. The maximally ranked species-habitat nested matrix of parrot sh was showed in see Tab S2. The results showed that the distribution of parrot sh presented nested structure in the South China Sea (P<0.001,T=13.21℃). The top three in the site nested rank were Nansha islands, Nha Trang and Xisha islands. And the topmost island (Nansha islands) was judged to be the most hospitable island (see Tab S3). Similarly, the topmost species (Scarus ghobban) was most common and prevalent, which makes it the most resistant to extinction or most prone to colonization (see Tab S4).
Spearman rank correlation analysis was conducted between the nested matrix rank of sites and environment factors, and also between the nested matrix rank of species and maximum body length. The results showed that scleractinian coral species richness, longitude, and log(Reef area) all had signi cant effect on site nested matrix rank (P < 0.05). Latitude and sea surface temperature maximum both had no signi cant effect on site nested matrix rank, and maximum body length re ecting swimming ability also had no signi cant effect on species nested matrix rank. (P > 0.05) ( Table 2). The distribution characteristics of functional groups. To compare whether functional group composition differs between islands with higher species richness and those with lower species richness, we divided the 41 study sites into two groups in order. Group 1 was the site nested rank 1-20 and group 2 was the site 21-41 (see Tab S5). The Independent sample t-test showed that three functional groups and the ratio of browser to total species of parrot sh were signi cantly different between group 1 and group 2, while the scraper/total species of parrot sh and excavator/total species of parrot sh were not signi cant difference. For more details please see Table 3. Compared with scraper and excavator, browser had a greater contribution on the nested matrix rank of site and was an important reason for the difference. Patterns of parrot sh species richness. Linear regression results showed that longitude, scleractinian coral species richness and reef area could explain the variation of parrot sh species richness to a certain extent (P < 0.05, Fig. 2a, c, d). Parrot sh species richness increased with increasing longitude In terms of coral reefs, Parrot sh species richness also increased with the increase of scleractinian coral species and reef area, and the tting degree of the curve was relatively high, being R 2 =0.44 and R 2 =0.34, respectively.
Parrot sh species richness decreased with the increase of latitude (R 1 2 =0.04, P = 0.253 > 0.05, R 2 2 =0.01, P =0.848 > 0.05, Fig. 2b), but this trend was not signi cant, as was the trend in temperature (R 2 =0.01, P = 0.619 > 0.05, Fig. 2e). The gure shows that parrot sh were mainly distributed in the range of 26-29℃ in the South China Sea We found that the Kaiser-Meyer-Olkin measure of sampling adequacy (KMO) was 0.542 < 0.6, but the Bartlett's spherical test was P < 0.05, which could indicate that the factors were suitable for further factor analysis. According to the principle of eigenvalue ≥ 1, the results showed that the 5 factors (longitude, latitude, sea surface temperature, scleractinian coral species richness and reef area) were consolidated into 2 principal components ( Table 4). The cumulative variance contribution value of two components accounted for 70.379%. According to the composition matrix, the rst principal component was taken to represent geographical location (i.e., latitude and longitude) and sea surface temperature, while the second principal component was mainly related to biological factors, such as scleractinian coral species richness (Table 5).  Log(reef area) was the most signi cant associated with nested matrix rank in our study, which could be habitat nestedness of parrot sh. Many scraping and excavating parrot sh have also been recorded to feed from the surface of live scleractinian corals (Bonaldo et al. 2014). And at the global scale, coral reef area was also regarded as the key variables in reef sh richness patterns across the Indo-Paci c (Parravicini et al. 2014). Larger reef area could provide more available resource such as food and shelter for sh, and more sh species were found in these reef. Browsering parrot sh feed mainly on macroalgae, however, limited space in coral reef was not conducive to the growth of macroalgae, which indirectly lead to insu cient food sources for browsering parrot sh (Bonaldo et al. 2014). We also showed that browser had declined signi cantly in relatively small reef area, and even did not exist in some sites, such as taiping island, tioman island and redang island. In addition, life-history traits, such as body size, were likely to affect the capacity of new colonizers to survive and establish reproductive populations (Luiz et al. 2013).
Speci c physiological limitation may fundamentally determine the distribution range of species and large body had the potential to expand their ranges (Davenport and Sayer 1993;Luiz et al. 2012). But the maximum body length re ecting the locomotion of sh had no signi cant correlation with nestedness, which was similar to the results of Kulbicki's study that geographical range was not related to maximum body size among parrot sh (Kulbicki et al. 2015). Therefore, when developing strategies to protect parrot sh resources and species diversity, we should give priority to islands or archipelagos with larger reef area and less human disturbance, such as Nansha islands and Xisha islands in the South China Sea.
In terms of spatial variation, we found that parrot sh species richness increased along longitude and the most abundant parrot sh species was in Nansha islands, which had something to do with the shorter distances to the Indo-Australian Archipelago marine biodiversity hotspots (Siqueira et al. 2021). This result supported the global rst major distribution gradient of coral reef sh mentioned in the introdution. Species richness declines nearly uniformly with increasing distance from the mid-domain of the Indo-Paci c (Bellwood et al. 2012). In additon, Nansha islands had a large reef area and low degree of human disturbance, which could also be the main reasons for the higher parrot sh speceis richness. Latitudinally, the decline of diversity with latitude was a general feature of many biota and could be easily observed in coral reef sh (Choat 1991 . Parrot sh were no exception and it included a pelagic larval phase(Ishihara and Tachihara 2011). The stochastic forces of wind and currents which largely drived the passive dispersal of these larvae would be more likely to bringing a given larvae close enough to a potential home (Musburger 2012).
Sea surface temperatures, habitat size, isolation, and evolutionary history were also in uenced the global distributions of parrot sh ). Our results showed that sites with more scleractinian coral species and larger reef areas helped support more parrot sh species. But when reef area reached a certain size, parrot sh species richness would not uctuate greatly even as the reef continued to increase in size.
For example, the reef area of Nansha islands (26, 059 km 2 ) was much larger than Philippines (11,852 km 2 ),, but parrot sh species richness was about the same as Nansha islands, with a total of 40 species ( In other words not all parrot sh species would be represented on a given reef, with some species saturation at the highest regional diversity (Kulbicki et al. 2018). Studies have shown that sea surface temperature had a key indirect role on reef sh richness and had a direct effect on corals (Parravicini et al. 2014), Most of coral live in above 18 ℃, and the optimum growth temperature is between 25 ℃ and 29 ℃(Wang and Zhao). It could be seen that the temperature of parrot sh distribution basically overlapped with the optimum temperature for coral growth. The results also suggested that coral reef played a signi cant role in parrot sh distribution pattern. Therefore, for some sites with smaller reef area, particularly nearshore islands, if human activity continues to damage coral reef or no protective measures were taken, it was easy to accelerate the degradation of coral reef, which was not conducive to the survival of parrot sh and changed the distribution pattern of parrot sh community. Figure 1 Distribution characteristics of parrot sh species richness in the South China Sea. Relationship between parrot sh species richness and environmental factors.Each point represents the the parrot sh species richness at that location. Based on the results of the scatter plot, the anomaly (Nansha islands) was deleted in the tting analysis of longitude, latitude and sea surface temperature.. Since Taiwan islands are affected by the Kuroshio, we separate the islands and reefs near Taiwan (2) from other sites (1) to construct a species -latitude curve.