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Effect of habitat characteristics on the distribution and abundance of damselfish within a Red Sea reef

Article in Environmental Biology of · December 2013 DOI: 10.1007/s10641-013-0212-9

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Effect of habitat characteristics on the distribution and abundance of damselfish within a Red Sea reef

Lauren E. Nadler & Deborah C. McNeill & Magdy A. Alwany & David M. Bailey

Received: 17 April 2013 /Accepted: 27 November 2013 # Springer Science+Business Media Dordrecht 2013

Abstract For reef fish with an obligate relationship in patchy reef habitats than in continuous sections of the to their habitat, like Pomacentrid damselfish, choosing a reef, probably because average coral colony size was suitable home amongst the reef structure is key to sur- greater in patchy reef type. Fish group size increased vival. A surprisingly small number of studies have ex- significantly with coral colony volume and with larger amined patterns in adult damselfish distributions com- branch spacing. Multi- groups of fish commonly pared to other ontogenetic phases. The aim of this study occurred and were increasingly likely with reduced was to determine which reef and coral colony character- branching density and increased coral size. istics explained adult damselfish distribution patterns in a Red Sea reef. The characteristics investigated were reef Keywords Coral reefs . spp . Chromis spp . type (continuous or patchy), coral species (seven species spp . Gulf of Aqaba of Acropora), and coral morphology (coral size and branching density). The focal damselfish species were Dascyllus aruanus, D. marginatus, Chromis viridis,and Introduction C. flavaxilla. Occupancy (presence or absence of resident damselfish), group size and fish species richness were not For fish with an obligate relationship to their significantly different between the seven Acropora spe- habitat, choosing an appropriate home amongst the reef cies. However, within each coral species, damselfish structure is key to avoiding predation, maximizing were more likely to occupy larger coral colonies than growth rate and finding mates (Booth and Wellington smaller coral colonies. Occupancy rates were also higher 1998; Martinez and Marschall 1999; Coker et al. 2009). Many Pomacentrid damselfish species exhibit strong site fidelity to a single coral colony, rarely venturing L. E. Nadler (*) : D. C. McNeill : D. M. Bailey Institute of Biodiversity, Health and Comparative more than one meter away (Sale 1971; Sackley and Medicine, University of Glasgow, University Avenue, Kaufman 1996). Spatial distribution and abundance of Glasgow G12 8QQ, UK damselfish species are known to result from both larval e-mail: [email protected] recruitment (e.g. Booth and Wellington 1998; Booth M. A. Alwany 2002;Ben-Tzvietal.2008) and subsequent post- Department of Marine Science, Faculty of Science, Suez settlement movement during other ontogenetic phases Canal University, 41522 Ismailia, Egypt (e.g. Frederick 1997; Simpson et al. 2008; Coker et al. 2012); yet, surprisingly few studies have examined dis- Present Address: L. E. Nadler tribution patterns in adult damselfish compared to the School of Marine and Tropical Biology, James Cook larval and juvenile developmental stages (Bay et al. University, Townsville, QLD 4811, Australia 2001;Belmakeretal.2009; Ben-Tzvi et al. 2009). Environ Biol Fish

Damselfish group size represents a trade-off between This study aims to describe adult damselfish distri- survival and growth rate. Larger group sizes decrease bution patterns in a Red Sea reef in the southern Gulf of individuals’ chances of predation (Sackley and Kaufman Aqaba. Though the Red Sea is known as a coral reef 1996) but increase competition for food (Kent et al. 2006). biodiversity hotspot with unique attributes such as var- These groups can be composed of one or more species, iable conditions and prevalent endemism, there are far even when food and energy requirements overlap fewer ecological studies in this region than other well- (Shpigel 1982; Shpigel and Fishelson 1986). However, known systems such as those in the Great Barrier Reef the habitat characteristics that promote larger group sizes and Caribbean (Berumen et al. 2013). The objective of and higher species abundance are still unclear. Sale this work was to fill knowledge gaps on which reef (1972a) found that increased coral size helped to mitigate types and coral morphologies promote adult damselfish agonistic interactions in damselfish groups, indicating that residency within seven Acropora spp. certain habitat morphologies may facilitate co-habitation. Previous studies have qualitatively examined the effect of branching morphology on damselfish occupancy and Material and methods found that the proportion of inhabited was higher in coral species with a less dense morphology (Booth 1992; Study site Bergman et al. 2000; Nanami and Nishihira 2005; Holbrook et al. 2000, 2008; Noonan et al. 2012). How- This study was implemented in Dahab, Egypt, in the Gulf ever, no quantitative comparisons between branch density of Aqaba (~28.49° N, 34.50° E) between May and July and damselfish group size have been performed. 2011 (Fig. 1). The Gulf of Aqaba is 180 km long and varies Though damselfish species have been found to asso- from 6 to 26 km wide. It is connected to the rest of the Red ciate with particular branching coral species, studies to Sea at the Straits of Tiran (Monismith and Genin 2004). date have examined these damselfish preferences in Two adjacent sites were sampled: Suleiman Reef and terms of confamilial groups of coral species that often the Islands. Suleiman Reef is a 200 m wide reef flat, exhibit highy divergent morphologies (e.g. Sale 1972a; dropping off at the reef crest into a continuous reef slope Fishelson et al. 1974; Shpigel and Fishelson 1986;Kent that reaches a sandy bottom at approximately 11–12 m et al. 2006). Whether closely related, congeneric coral deep. Seaward of the reef slope, there are a number of species would lead to similar adult damselfish-coral patch reefs surrounded by sand, at 12–15 m depth. species associations is still unclear. Bonin’s(2012)stud- The Islands site is more complex. Seaward of the ies of recently settled juveniles showed some damselfish fringing reef are the Islands themselves: two areas of species associating almost exclusively with a single reef that emerge at low water. The Islands are joined to Acropora spp. while others exhibited little preference. the fringing reef by large subtidal coral boulders be- Whether any species-specific coral preferences would tween which are sandy “pools”. Two pools within the carry over to the adult stage is unknown, as juveniles Islands site were surveyed. The first pool drops off at the have previously been shown to have more specialized reef crest into a continuous reef slope that reaches a habitat requirements than adults (Wilson et al. 2008). sandy bottom at approximately 9–11 m deep. Within Isolated (patchy) reef habitats are frequently found the sandy-bottomed pool, there are a number of patch exhibiting higher reef fish diversity, abundance, and reefs surrounded by sand at 11–13 m depth. The second stability than continuous reef habitats (Ault and Johnson pool has a similar topography to the first but is shallower 1998a; Nanami and Nishihira 2001, 2003; Belmaker with the continuous reef slope reaching 6–7 m deep and et al. 2009). This trend has been attributed to differences patch reefs found around the sandy bottom at 6–8m. in physical characteristics, limits on post-settlement movement due to increased predation pressure, or vari- Study species ation in larval supply (Ault and Johnson 1998a, b; Nanami and Nishihira 2001; Belmaker et al. 2011). Seven Acropora spp. were included in the surveys: However, none of these studies have investigated if, in A. gemmifera, A. samoensis, A. secale, A. valida, A. addition to different pressures, patchy reef habitats pos- eurystoma, A. digitifera, and A. selago. Four site- sibly contain coral colonies with ideal morphological attached Pomacentrid damselfish species, all of which characteristics. seek shelter within branching coral colonies, were studied. Environ Biol Fish

Fig. 1 The Gulf of Aqaba in the northern Red Sea. Dahab, on the transect location, except T6 where only two transects were exam- Sinai Peninsula, is indicated. Inset shows location of the two ined due to topographical constraints (images attained from Goo- sample sites (the Islands and Suleiman Reef) and the transect gle Earth; large image: image © 2011 GeoEye, image © 2011 locations in each (T1-T6). Each transect was 50 m long. Three DigitalGlobe, © Cnes/Spot Image, © 2010 Google; inset image: transects at different depths and reef types were assessed at each image © 2012 DigitalGlobe, © 2010 Google)

These were: the Dascyllus aruanus, continuous reef ended at 6–7 m depth. In total, six the Red Sea dascyllus D. marginatus, the blue-green transects in the patchy reef (7–13 m) and 11 transects chromis Chromis viridis, and the Arabian chromis in the continuous reef (5–10 m) were conducted. C. flavaxilla. No other damselfish species were found All Acropora spp. colonies ≥20 cm diameter ((width inhabiting these Acropora spp. in the study area. Initial + length)/2) were counted and the presence or absence surveys indicated a lower coral colony size limit of of each damselfish spp. was noted. From here on, “oc- occupancy; therefore, only corals with a diameter cupancy” will be used to describe the presence of dam- ≥20 cm were included in the analysis. Only adult selfish (of any number ≥1) within a coral colony. Occu- damselfish were present at the time of surveying, as pancy data was collected in order to ascertain a general confirmed by the size and coloration of individuals overview of the prevalence of resident damselfish in found (Lieske and Myers 2004). The yearly recruitment corals within our study sites and where these damselfish pulses began shortly after surveys were concluded in were most commonly found. July (L.E. Nadler, pers. obs.). Surveys of coral colony characteristics Surveys of coral occupancy by fish A total of 181 Acropora spp. colonies (66 with resident A total of 17 belt transects (50 m×2 m) were surveyed at damselfish and 115 without) were selected randomly for six locations (T1–T6) within the two study sites, the further analyses, using both belt transects and timed Islands and Suleiman Reef (Fig. 1). At each location, swims. Timed swims were conducted by completing three transects were conducted: two on continuous reef, ten fin kicks and measuring the first coral colony en- at approximately 5 m and 10 m depth, and one on the countered that was occupied by damselfish. This meth- patchy reef below the continuous reef wall (patchy reef od was used in addition to belt transects in order to was generally only 4 to 5 m in width below the reef wall increase the sample size of coral colonies inhabited by making only one belt transect in this section of reef damselfish (as each transect contained at least twice as feasible). At the sixth location, only two transects were many uninhabited coral colonies as compared to occu- possible (one patchy and one continuous) as the pied coral colonies). Environ Biol Fish

A variety of traits of each coral colony were measured was analyzed using a binomial error structure and logit and/or recorded, including: 1) Acropora coral species; 2) transformation. In order to account for the nesting of each habitat type (continuous or patchy); 3) size characteristics transect within a particular location (T1–T6, Fig. 1), gen- (length, width, and height); and 4) branching features eral linear mixed-effects models (GLMM) in the “lme4” (average branch diameter and spacing). Size characteristics package (Bates and Maechler 2011)inRwereused,with (including length, width, and height) were measured using transect nested within location included as a random a tape (± 5 mm). Six branches per colony were measured effect. These models were confirmed using the likelihood for diameter and spacing using calipers (± 0.5 mm). All ratio test (LRT). Morphological differences (coral size branch measurements were taken at 10 mm from the and branching density) between occupied and unoccu- branch tip. In addition, the number and species of damsel- pied corals of individual Acropora spp. were explored fish inhabiting each coral colony were recorded. using LMs in the four most common Acropora spp.

Statistical analysis Group size

Analyses were performed in the statistical software R ver- A Wilcoxon signed rank test was performed to deter- sion 2.15.0 (R Development Core Team 2012). Additional mine if group size (the number of fish found inhabiting a packages “bbmle” (Bolker and R Development Core Team single coral) varied significantly between Chromis and 2012), “MASS” (Venables and Ripley 2002), and “lme4” Dascyllus damselfish species. Measures of fish group (Bates and Maechler 2011) were used. Primer 6 (Clarke size were then analyzed in terms of reef characteristics 1993) was used to investigate coral colony composition. (reef type and species of the host coral) and coral mor- phology (coral volume and branching density). Analy- Spatial and inter-species variation in coral assemblage ses of total group size (total number of fish per group of and colony characteristics all damselfish species) and group size of each individual damselfish species were performed using negative bino- In order to determine if Acropora spp. assemblages mial regression (NBR) as confirmed by the LRT, in varied by reef type, one-way analysis of similarity order to account for overdispersion in this count data. (ANOSIM) was performed using Primer 6 (Clarke As outliers were found in the total group size, all anal- 1993). Data on the counts of the study Acropora spp. yses were performed both with and without these out- within each transect were square root transformed and liers included to determine if they were exerting undue analyzed using the Bray-Curtis coefficient of similarity. influence on the significance of the statistics. As no Linear models (LM) were used to determine the differences were found in the significance of the analy- morphological differences in coral colonies (coral vol- ses, these outliers were included in all further analyses ume, branch diameter, and branching spacing) between and no additional action was taken on them. the reef types and the seven Acropora spp. Using Tukey post hoc comparisons, pair-wise differences between the Fish density Acropora spp. were determined. Overall coral size was determined by coral volume, as a function of length, Fish density was calculated by dividing damselfish group width and height, using the following formulas: size by coral volume (number of damselfish per 1 cm3 of coral). This data exhibited a normal distribution and was ¼ = ∏ 2 Coral Volume 1 3 r h therefore analyzed using generalized linear models with a r radius = ((length + width)/2)/2 Gaussian distribution. Differences in damselfish density h height were examined in terms of reef characteristics (reef type and species of the host coral) and coral morphology (coral volume and branching density). Occupancy Species richness As occupancy was a binary response variable (presence versus absence of damselfish), variation in coral occu- Species richness (total number of damselfish species pancy (in terms of reef type and species of the host coral) found co-habitating) was analyzed using Poisson Environ Biol Fish regression (PR) as confirmed by the LRT, as no There was no significant inter-species variation in overdispersion was found in this dataset. Trends in this coral volume (LM: F6,174=1.501, p=0.339), but signif- species richness measure were assessed through reef char- icant morphological differences were found in average acteristics (reef type and species of the host coral) and coral branch diameter (LM: F6,174=26.42, p<0.0001) and morphology (coral volume and branching density). average branch spacing (LM: F6,171=21.99, p< 0.0001) (Fig. 2). Results of pairwise Tukey post hoc comparisons are detailed in Table 1. Results Occupancy Spatial and inter-species variation in coral assemblage and colony characteristics Seventeen transects were analyzed, containing 441 col- onies of the focal Acropora spp., of which only 13.4 % Transects contained 11 to 35 Acropora spp. coral colo- were occupied by damselfish (Table 2). No significant nies (average number of corals transect−1 ± SE: 25.94± Acropora spp. preference was exhibited, as overall oc- 2 2.51). No significant differences in species composition cupancy (GLMM: χ 13=4.91,p=0.267) and occupancy of transects were found between continuous and patchy in terms of individual damselfish spp. (GLMM: 2 reef (one-way ANOSIM: global R=0.091, p=0.391). D. aruanus: χ 13=4.41, p=0.558; D. marginatus: 2 2 However, coral morphology varied significantly be- χ 13=3.38, p=0.848; C. viridis: χ 13=6.266, p=0.919; 2 tween the different reef types. Coral size (in terms of C. flavaxillia: χ 13=0.86,p=0.863) was not significant- colony volume) was significantly larger in patchy reef ly different between Acropora spp.

(LM: F1,179=8.55, p=0.004). Branch diameter (average Occupancy was significantly higher in patchy reef 2 branch diameter ± SE: 0.86 cm±0.01 cm) was signifi- (GLMM: χ 1=13.06, p=0.002) (Table 2). Considering 2 cantly larger in continuous reef (LM: F1,179=27.64, p< individual damselfish spp., D. aruanus (GLMM: χ 1= 2 0.0001), though no significant differences in branch 11.88, p=0.001) and D. marginatus (GLMM: χ 1= spacing (average branch spacing ± SE: 1.18 cm± 9.46, p=0.002) were significantly more likely to inhabit 2 0.01 cm) were found between reef types (LM: F1,176= patchy reef corals whereas C. flavaxilla (GLMM: χ 1= 1.43, p=0.234). 6.44, p=0.008) was found exclusively in coral colonies

Fig. 2 Variation in average branch diameter (a) and average branch spacing (b) in the seven Acropora spp. (error bars indicate standard error) Environ Biol Fish

Table 1 Statistics on the pairwise morphological differences be- average branch diameter and italics represent differences in terms tween the study Acropora spp. (as calculated using Tukey post hoc of average branch spacing comparisons), with bold representing differences in terms of

A. valida A. samoensis A. secale A. eurystoma A. gemmifera A. selago A. digitifera

A. valida <0.001 <0.001 0.006 <0.001 0.109 0.869 A. samoensis <0.001 0.558 <0.001 0.999 <0.001 < 0.001 A. secale <0.001 0.027 0.094 0.895 <0.001 0.001 A. eurystoma 0.037 <0.001 0.414 0.066 <0.001 0.088 A. gemmifera 0.019 0.822 0.999 0.721 <0.001 0.001 A. selago 0.368 <0.001 <0.001 0.008 0.002 0.988 A. digitifera 0.999 0.001 0.089 0.589 0.156 0.942

in continuous reef (Fig. 3). C. viridis did not exhibit a Group size significant preference for either reef type (GLMM: 2 χ 1=0.63, p=0.433). Though the Chromis spp. exhibited a higher maximum In the four most prevalent Acropora spp., occu- and mean group size than the Dascyllus spp. (Fig. 4), no pancy of corals (in the subset of colonies that significant differences between the species’ group sizes (in were measured for morphological characteristics) terms of the number of fish found living together on a was found to be significantly higher in larger single coral colony) were found (Wilcoxon signed-ranks corals than smaller corals (Table 3). Average test: Z=−1.24, n=181, p=0.213). Group size was not branch spacing was not found to be a significant significantly higher in any specific Acropora spp. (NBR: factor influencing occupancy in any of the Acropora total group size: LRT6,174=9.31, p=0.111; D. aruanus spp. examined, though a trend towards higher occupan- group size: LRT7,175=6.32, p=0.503; C. viridis group size: cy in corals with larger branch spacing was indicated in LRT6,174=5.88, p=0.389), except for a trend in groups of A. secale (Table 3). Occupancy in A. samoensis was D. marginatus (NBR: LRT6,174=13.21, p=0.073) and in significantly higher in corals with smaller branch diam- C. flavaxilla (NBR: LRT6,174=24.32, p=0.0005). eters, though branch diameter was not significant in the Reef type did not exert a significant effect on overall other Acropora spp. (Table 3). damselfish group size (NBR: LRT1,179=0.10, p=0.821)

Table 2 Summary of the varia- tion in damselfish occupancy Variable Category Total Occupied Percentage found in the transects (the pro- occupied portion of Acropora spp. coral colonies inhabited by damselfish) All 441 59 13.37 % Acropora spp. A. valida 184 26 14.13 % A. samoensis 92 15 16.30 % A. secale 74 6 8.11 % A. eurystoma 52 11 21.15 % A. selago 18 0 0 % A. digitifera 13 0 0 % A. gemmifera 8 1 12.50 % Reef type Patchy 120 36 30.00 % Continuous 321 23 7.17 % Environ Biol Fish

Fig. 3 Variation in transect occupancy by reef type in the four focal damselfish species or C. viridis group size (NBR: LRT1,179=0.43, p= higher branch diameter in the largest third of corals 0.258). The number of fish in groups of D. aruanus (NBR: LRT1,176=3.201, p =0.042). Only (NBR: LRT2,180=19.25, p<0.0001) and D. marginatus D. marginatus exhibited a significant relationship with (NBR: LRT1,173=8.63, p=0.008) was significantly average branch diameter, with the size of these groups higher in patchy reef, while C. flavaxilla (NBR: decreasing with increasing average branch diameter

LRT1,179=82.62, p<0.0001) was exclusively found in (NBR: LRT1,175=10.80, p=0.001). continuous reef. Total fish group size increased significantly with

Total fish group size depended on an interaction increasing coral volume (NBR: LRT1,176=44.45, between coral size and branch diameter; the number of p<0.0001). Group size also increased significantly with fish in a group decreased with increasing branch diam- coral volume in groups of D. marginatus (NBR: eter in the smallest 2/3 of corals and increased with LRT1,176=23.31, p =0.0002), C. viridis (NBR:

Table 3 Variation in occupancy in the subset of Acropora corals measured for morphological characteristics, for the four most prevalent Acropora spp. found (statistics were calculated using a linear model)

A.valida A. samoensis A. secale A. eurystoma (n=64) (n=42) (n=31) (n=27)

Coral size

df 1,62 1,40 1,29 1,25 F 11.89 11.51 27.79 12.39 P-value 0.001 0.002 < 0.001 0.002 Branch diameter

df 1,62 1,40 1,29 1,25 F 1.398 6.661 0.702 0.069 P-value 0.242 0.014 0.409 0.795 Branch spacing

df 1,61 1,40 1,29 1,24 F 0.549 1.173 4.058 0.114 P-value 0.462 0.285 0.053 0.739 Environ Biol Fish

50

40

30

20 Damselfish Group Size 10

0

Chromis flavaxilla Chromis viridis Dascyllus marginatus Dascyllus aruanus All Species Damselfish Spp.

Fig. 4 Variation in damselfish group size in Chromis flavaxilla n=66) (each box plot illustrates the minimum, quartiles, median, (n=12), C. viridis (n=20), Dascyllus marginatus (n=20), and maximum for each damselfish species. Points above each D. aruanus (n=37), and total group size (including all species, boxplot illustrate outliers in that dataset)

LRT1,176=32.40, p<0.0001), and C. flavaxilla (NBR: a trend indicated in the density of D. marginatus LRT1,176=8.04, p<0.0001). However, coral size did not (LRT1,174=1.82, p=0.070). No reef type effect was have a significant effect on D. aruanus group size found for total damselfish density (LRT1,174=1.09, (NBR: LRT1,179=2.29, p=0.107). p=0.296) or C. viridis density (LRT1,174=1.23, All measures of fish group size exhibited a sig- p=0.254). nificant relationship with average branch spacing, Fish density increased significantly with coral vol- except in C. flavaxilla groups (NBR: LRT1,174= ume in terms of total damselfish density (GLM: 0.67, p>0.05). As branch spacing increased, total LRT1,176=13.68, p=0.0009) and C. viridis density damselfish (NBR: LRT1,174=14.14, p<0.0001), (GLM: LRT1,176=32.45, p<0.0001), with a trend again D. marginatus (NBR: LRT1,174=11.90, p<0.0001) indicated for D. marginatus density (LRT1,176=6.85,p= and C. viridis (NBR: LRT1,174=3.91, p=0.003) 0.063). No coral volume effect was found on D. aruanus groups increased in size. D. aruanus (NBR: (GLM: LRT1,176=0.17, p=0.549) or C. flavaxilla LRT1,174=11.21, p<0.0001) exhibited the opposite (GLM: LRT1,176=0.57, p=0.497) density. trend, decreasing in group size with increased branch Higher damselfish density was found with in- spacing. creased branch spacing in all four species of dam-

selfish (GLM: D. aruanus density: LRT1,176=0.59, p Fish density <0.0001; D. marginatus density: LRT1,176=7.00, p= 0.005; C. viridis density: LRT1,176=4.61, p<0.0001; Damselfish density (mean total damselfish density ± C. flavaxilla density: LRT1,176=3.54, p<0.0001), SE: 4.43×10−4 fish cm3−1±6.88×10−5) was not sig- though no total damselfish density effect was detect- nificantly correlated with Acropora spp. (GLM: total ed (GLM: LRT1,176=3.32, p=0.103). Branch diame- damselfish density: LRT1,174=0.71, p =0.661; ter had no significant effect on any measure of fish D. aruanus density: LRT1,176=1.89, p=0.190; density (GLM: total damselfish density: LRT1,176= D. marginatus density: LRT1,174=1.45, p=0.227; 0.03, p=0.185; D. aruanus density: LRT1,176=1.82, C. viridis density: LRT1,174=0.90, p =0.581; p=0.173; C. viridis density: LRT1,176=0.13, p= C. flavaxilla density: LRT1,176=0.32, p=0.794). A 0.731; C. flavaxilla density: LRT1,176=0.79, p= significant reef type effect was found with 0.368), except in D. marginatus (GLM: LRT1,176= D. aruanus (GLM: LRT1,176=22.67, p<0.0001) and 0.27, p=0.009), in which density decreased signifi- C. flavaxilla (LRT1,174=5.18, p=0.019) density, with cantly as average branch diameter increased. Environ Biol Fish

Species richness While coral size was an important colony character- istic for abundance, branching density was more signif- Damselfish species richness within the damselfish icant in determining damselfish group size. Previous groups did not vary between the Acropora spp. exam- work focusing on habitat selection in D. aruanus found ined (PR: LRT6,174=8.82,p=0.363) but was significant- that group size increased in response to both increased ly higher in patchy reef (PR: LRT1,179=9.70, p=0.006), coral size and branch spacing (Sale 1972b;Holbrook with increasing coral size (PR: LRT1,179=28.704, p= et al. 2000). Yet, in this study, group size did not vary 0.0005) and with increasing branch spacing (PR: with coral volume and actually decreased with increas-

LRT1,174=1.99, p<0.0001). As average branch diame- ing branch spacing. This trend could indicate that the ter increased, group species richness decreased (PR: abundance of suitable habitat exceeded the demand in

LRT1,175=6.14, p=0.002). our study sites. In addition, smaller branching spacing may represent optimal habitat for adult D. aruanus in terms of competition for resources and predator defense. Discussion To the best of our knowledge, no prior work has analyzed variation in damselfish group size in terms of The aim of this study was to determine adult damselfish a quantitative measure of branching morphology, with species distribution in the Gulf of Aqaba in response to previous studies examining trends in terms of categori- reef type (patchy versus continuous), coral species and cal variables. Branch spacing affects the available hab- coral morphology characteristics. In line with previous itable space within a coral colony, therefore potentially studies of reef types that showed isolated reef patches had influencing factors such as group size and resource higher species richness and abundance than continuous competition. Colony branching morphology directly in- reef habitats (Sale 1972b, 1991; Ault and Johnson 1998a; fluences the hydrodynamics of the coral, by altering Holbrook et al. 2000; Booth 2002;NanamiandNishihira how much flow can penetrate the inner branching struc- 2002, 2003;Belmakeretal.2009), damselfish occupan- ture of the organism (Chang et al. 2009). Maintenance cy in this study was significantly higher in the patchy of tight branch spacing with depth may aid in efficient reef. Variation between reef types was related to differ- filter feeding and nutrient retention (Lowe et al. 2005; ences in coral morphology rather than Acropora spp. Reidenbach et al. 2006;Holbrooketal.2008), but assemblage, with significantly larger coral colonies excessively dense configurations can result in decreased found in patchy than continuous reef. These results indi- flow or stagnant water in the center of the branching cate that damselfish distribution is likely in large part structure (Chamberlain and Graus 1975). dictated by the presence of corals of a sufficient size. A positive relationship has been shown to exist be- The effect of increasing coral size on damselfish tween resident damselfish and their coral hosts through abundance has previously been explored (e.g. Sale input of nutrients (Pinnegar and Polunin 2006; 1972a, b; Nanami and Nishihira 2005;Noonanetal. Holbrook et al. 2008), increased aeration (Goldshmid 2012). Holbrook et al. (2000) described a minimum et al. 2004), and protection from predators (Weber and coral size, below which no damselfish occupancy oc- Woodhead 1970; Liberman et al. 1995). As a result, curred. Similarly, these results indicated that group size coral skeletal growth significantly increases in compar- increased significantly with coral size in D. marginatus, ison to colonies that lack fish (Liberman et al. 1995; C. viridis and C. flavaxilla, and that occupancy had a Holbrook et al. 2008, 2011). In a potential feedback lower coral size limit. Sale (1972b) used group size as an loop, larger colonies may then support larger groups of indirect indicator of limited habitat availability. There- fish (Holbrook et al. 2011). fore, optimal habitat for these three species may have As previous studies have found that increased flow been limited in our study sites, while ideal habitat con- can lead to thicker coral branches (Griffith and ditions for D. aruanus could have been below carrying Newberry 2008; Mass and Genin 2008), resident dam- capacity. Yet, a study undertaken in the northern Gulf of selfish could hypothetically induce morphological Aqaba showed no significant correlation between group changes in their host coral colony through the increased size of D. marginatus and coral size (Kent et al. 2006), flow they create while swimming in their sleep indicating that, within the Red Sea, habitat preference (Goldshmid et al. 2004). However, these results did may vary geographically. not find a strong correlation between the presence or Environ Biol Fish abundance of damselfish and branch diameter, which reduced occupancy to zero no matter how ideal the could indicate that the flow that resident fish induce is morphology of a coral colony, likely as a result of not high enough to stimulate a plastic response in predation on newly settled damselfish recruits branching morphology. (Belmaker et al. 2009;Holbrooketal.2011). Increased group size may negatively impact on the Microhabitat structure may influence damselfish spe- fitness of individual fish due to increased competition cies richness (Ormond et al. 1996), abundance for resources. Kent et al. (2006) analyzed the stomach (Shulman 1984; Tolimieri 1998) and survivorship contents of small versus large groups of D. marginatus in (Shulman 1984). Hixon and Beets (1989, 1993) de- Eilat (northern Gulf of Aqaba) to show that small groups scribed the importance of refuges close to body size in consumed double the amount of food as large groups. increasing survivorship of prey species, likely due to the Competition is therefore likely to play a defining role in many larger predators that these refuges would inevita- the distribution and abundance of damselfish. Nemeth bly exclude (Nemeth 1998). However, smaller crevices (2007) observed that despite equal settlement of Stegastes also lead to reduced flow, which reduces available oxy- partitus recruits to back and fore reefs, higher abundance gen (therefore increasing the chance of hypoxic condi- of adults was found on the fore reef due to competition for tions), which is essential when large numbers of fish are space and food on the back reef. This competition likely taking refuge (Goldshmid et al. 2004). Little work has had a negative effect on growth rates, extending the period been done to examine the impact of habitat characteris- of time juveniles were vulnerable to predation. tics on damselfish species richness, which increased Spatial variation in damselfish distribution between significantly in patchy reef in this study. This trend reef types may be linked to differences in mortality rates indicates that, as in damselfish occupancy, coral size (Booth 2002). Predation pressure has been shown to be likely plays a larger role in determining the suitability lower in continuous than patchy reef (Nanami and of a coral colony for co-habitation of multiple damsel- Nishihira 2001; Belmaker et al. 2009), reducing the risk fish species than branching density (which did not vary associated with post-settlement dispersal (Ault and between the reef types), with larger coral volume en- Johnson 1998a;Ben-Tzvietal.2009). However, this abling multi-species use via habitat partitioning. theory has primarily been assessed in sites where only To date, no ecological studies have been published on one reef type was available (Nanami and Nishihira C. flavaxilla. Within this study site, C. flavaxilla exclu- 2001, 2002, 2003;Belmakeretal.2009). Both sively inhabited the continuous reef, often inhabiting Suleiman Reef and The Islands contain a mixture of coralcolonieswithoradjacenttogroupsofC. viridis, continuous and patchy reef at very small spatial scales, suggesting similar requirements to their more well- enabling movement between the two. studied congener. A recent study (Wyatt et al. 2012) Inter and intra-specific aggressive behavior may in- indicated that dietary preferences in C. viridis can vary fluence distribution, resulting in species or life-stage significantly depending on which section of the reef partitioning (Robertson 1996;Nemeth2007; Ben-Tzvi they live on. Therefore, the niche overlap between et al. 2009). Bay et al. (2001) found that although C. viridis and C. flavaxilla may depend on where they juveniles of a range of damselfish species exhibited are found in a reef system. Mixed-species shoaling has overlapping distributions across reef zones, this trend been shown to facilitate foraging opportunities in other was lost in the adult life stage, likely due to interspecies species (Pereira et al. 2013), which may aggression instigated as a result of competition for the be the driver of co-habitation in this case. same resources. Intra-specific aggression is also com- This study is the first to examine coral species prefer- mon, with a number of studies on Dascyllus spp. in ences in adult damselfish within the Acropora genera. particular illustrating the prevalence of adult aggression Individual damselfish spp. were not found to associate towards juveniles; this behavior often leads to juvenile with any particular Acropora spp. despite significant mor- D. aruanus settling in corals adjacent to adult groups phological differences in their branching features. There- until sufficient size is reached (Sale 1972b; Booth 1995; fore, these findings could suggest that adult damselfish Ben-Tzvi et al. 2009). Predators can also have a strong lose the coral species-specialisation that has been found in influence on distribution; recent studies indicate that the recruits, as other factors like morphological characteristics presence of predators like the dottyback Pseudochromis of the individual coral colony become more important for olivaceus or the arc-eye hawkfish Paracirrhites arcatus survival (Wilson et al. 2008;Bonin2012). Environ Biol Fish

To the best of our knowledge, no previous publica- Bay LK, Jones GP, McCormick MI (2001) Habitat selection and tions have examined damselfish occupancy in A. selago aggression as determinants of spatial segregation among damselfish on a coral reef. Coral Reefs 20:289–298 and A. digitifera. Both species remained uninhabited Belmaker J, Ziv Y, Shashar N (2009) Habitat patchiness and throughout these surveys. Although low in abundance, predation modify the distribution of a coral-dwelling dam- their morphology was not significantly different from selfish. Mar Biol 156:447–454 the more abundant A. valida, which was regularly found Belmaker J, Ziv Y,Shashar N (2011) The influence of connectivity on richness and temporal variation of reef fishes. Landsc Ecol inhabited. Occupied A. selago were observed in other 26:587–597 Gulf of Aqaba sites. In those instances, it was larger Ben-Tzvi O, Abelson A, Polak O, Kiflawi M (2008) Habitat (>1 m diameter), with a plate-like growth forms (L.E. selection and the colonization of new territories by Chromis – Nadler, pers. obs). viridis. J Fish Biol 73:1005 1018 Ben-Tzvi O, Kiflawi M, Polak O, Abelson A (2009) The effect of By analyzing damselfish occupancy, group size and adult aggression on habitat selection by settlers of two coral- species richness, this study illustrated how different reef dwelling damselfishes. PLoS One 4:e5511 characteristics and coral morphological traits affect spa- Bergman KC, Ohman MC, Svensson S (2000) Influence of habitat tial distribution of adults. While occupancy peaked in structure on Pomacentrus sulfureus, a western Indian Ocean reef fish. Environ Biol Fish 59:243–252 patchy reef due to its predominance of larger corals, Berumen ML, Hoey AS, Bass WH, Bouwmeester J, Catania D, group size varied mostly independently of reef type. Cochran JEM, Khalil MT, Miyake S, Mughal MR, Spaet This was most likely due to the importance of loose JLY,Saenz-Agudelo P (2013) The status of coral reef ecology – branching morphology in supporting larger group sizes. research in the Red Sea. Coral Reefs 32:737 748 Bolker B, R Development Core Team (2012) bbmle: Tools for Group species diversity was dependent on both coral general maximum likelihood estimation. URL http://CRAN. size and branching morphology, though the increased R-project.org/package=bbmle. Accessed 5 April 2012 diversity found in patchy reef indicates that coral size Bonin MC (2012) Specializing on vulnerable habitat: Acropora may be the stronger determinant. No preference for selectivity among damselfish recruits and the risk of bleaching-induced habitat loss. Coral Reefs 31:287–297 specific Acropora spp. was found in any of the damsel- Booth DJ (1992) Larval settlement patterns and preferences by fish group characteristics despite significant morpholog- domino damselfish Dascyllus albisella Gill. J Exp Mar Biol ical differences. This study provides essential informa- Ecol 155:85–104 tion on the habitat distributions of damselfish species in Booth DJ (1995) Juvenile groups in a coral-reef damselfish: density-dependent effects on individual fitness and popula- a sparsely-studied area of the Red Sea, fills a knowledge tion demography. Ecology 76:91–106 gap on the ecology of coral reef fish in this poorly Booth DJ (2002) Distribution changes after settlement in six understood biodiversity hotspot (Berumen et al. 2013) species of damselfish () in One Tree Island and reinforces the need for further work in this area. lagoon, Great Barrier Reef. Mar Ecol Prog Ser 226:157–164 Booth DJ, Wellington G (1998) Settlement preferences in coral- reef fishes: effects on patterns of adult and juvenile distribu- Acknowledgments We thank K. Dunlop, M. Dirnwoeber, R. tions, individual fitness and population structure. Aust J Ecol Nager, D. Haydon, and the staff at the Dahab Marine Research 23:274–279 Center and DiveIn Center (in particular K. Jentsch, A. Tischer, H. Chamberlain JA, Graus RR (1975) Water flow and hydromechan- Lange, T. von Arx, M. Gold, Ibraham, and Salem) for their generous ical adaptations of branched reef corals. Bull Mar Sci 25: assistance. Funding for this study was provided by the University of 112–125 Glasgow, Glasgow Natural History Society, Royal Geographical Chang S, Elkins C, Alley M, Eaton J, Monismith S (2009) Flow Society (with IBG), and the Gilchrist Trust. 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J Exp Ault TR, Johnson CR (1998b) Relationships between habitat and MarBiolEcol414–415:62–68 recruitment of three species of damselfish (Pomacentridae) at Fishelson L, Popper D, Avidor A (1974) Biosociology and ecol- Heron Reef, Great Barrier Reef. J Exp Mar Biol Ecol 223: ogy of pomacentrid fishes around the Sinai peninsula (north- 145–166 ern Red Sea). J Fish Biol 6:119–133 Bates D, Maechler M (2011) lme4: Linear mixed effects models Frederick JL (1997) Post-settlement movement of coral reef fishes using S4 classes. http://cran.r-project.org/web/packages/lme4/ and bias in survival estimates. Mar Ecol Prog Ser 150:65–74 Environ Biol Fish

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