Introduction

Zooplanktivorous fish play a major role in the ecology of the reef and are the most abundant functional group in many coral reefs (Williams and Hatcher 1983; Rilov and Benayahu 1998; Rossier and Kulbicki 2000). Yet, data regarding their bathymetric distribution patterns (as well as of other taxa) is lacking beyond 30 m (Lesser 2004).

Analyses of spatial distributions and population dynamics of members of ecological guilds that rely solely on total abundance, as oppose to size structure, may well fail to detect major interspecific interactions (Robertson 1998). Studies of the bathymetric range of adult, juveniles and new recruits of coral reef fish species generally show that the young inhabit either shallower depths than the adults (Rosland and Giske 1994; Zeller and Pauly 2001; Letourneur et al. 2003; Methven et al. 2003; Sassa et al. 2004; Koczaja et al. 2005) or share the same depths (Bean et al. 2002).

The 10 species of Angelfish of the genus Genicanthus (Swainson 1839) are often seen in deep reefs and although they are not common above 20 m (Randall 1975), G. caudovittatus, G. lamarck and G. semicinctus occasionally occur at 10 m depth. The zooplanktivorous G. caudovittatus is reported to reach depths of 60–70 m (Khalaf and Disi 1997; Allen et al. 1998; Froese and Pauly 2006), yet different studies reported a variety of shallow depth preferences, potentially biased by incomplete sampling of the deeper reefs. For example, in Eilat (northern Gulf of Aqaba; Red Sea), Rilov and Benayahu (2000) found that G. caudovittatus (Günther, 1860) are abundant at depths of ca. 20 m (their deepest transects), while Brokovich (2001) found that they are rare in shallow reefs (depths of up to 15 m). This same species was reported in Aqaba (10 km east of Eilat) as abundant at 12 m and rare at 6 m (Khalaf and Kochzius 2002) (their deepest studied depth was 12 m). Unfortunately, in all of the above studies, quantitative data of deep populations (>30 m) was not available, nor was data regarding bathymetrical distribution of the juveniles. The goal of this study was to describe the depth distribution of different size classes of G. caudovittatus and to examine whether depth partitioning trends in this species coincide with other, deep and shallow, diurnal zooplankters. We also examined possible interspecific interactions with other functional groups.

Methods

We used advanced technical diving techniques (TRIMIX SCUBA diving, by EB and SE) to quantitatively examine the fish community in the Red Sea near Eilat between 5 and 65 m. At each of 3 sites, where possible, (Dekel beach, Japanese Gardens and the Interuniversity Institute) we completed a visual census of fishes in 3–6 replicates of 50 m2 (25 × 2 m) at each of 5 different depths (total number of transects in parentheses): 5 m (7 transects), 10 m (6 transects), 30 m (10 transects), 45–50 m (12 transects) and 60–65 m (7 transects). Sample sizes deferred due to the absent of a reef at some locations and depths and also due to technical difficulties in reaching some sites as oppose to others. We recorded fish abundance underwater on a plastic slate. We only recorded fish that passed in front of the diver but a whole school was counted if one of its fish crossed the transect (Bortone et al. 1986). We estimated the total lengths (TL) of all fishes in the transect to the nearest centimeter (Bell et al. 1985; Rossier and Kulbicki 2000). We assigned species to functional groups according to their diet using data from the primary literature (Randall 1983; Debelius 1993, 1998; Randall 1995; Khalaf and Disi 1997) and Fishbase (Froese and Pauly 2006). For G. caudovittatus we defined juveniles as ≤60 mm TL, adults as larger than 60 mm TL. Juvenile size was defined following Randall’s (1975) publication of a photo of a juvenile of ca. 55 mm TL. In addition to G. caudovittatus, we surveyed 25 other diurnal zooplanktivore species. Thirteen species (incl. G. caudovittatus) had sufficient data for meaningful analyses of the depth partitioning between different size classes. These were: a – Amblyglyphidodon flavilatus; b – Chromis dimidiata; c – C. pembae; d – C. viridis; e – Cirrhilabrus blatteus; f – C. rubriventralis; g – Dascyllus aruanus; h – D. marginatus; i – D. trimaculatus; j – Genicanthus caudovittatus; k – Paracheilinus octotaenia; l – Pomacentrus trichourus; m – Pseudanthias squamipinnis. As a possible factor in determining zooplanktivores distribution, we also analyzed piscivores abundance and compared with the above species. One diver (EB) recorded all fish data. Adult and juveniles depth preferences were decided according to the maximal abundance for the species. In cases where there was no clear peak, we averaged the depth range of the species.

Results

Twelve species out of the 13 studied conform to the known trend of juveniles occupying the same or shallower depth as the adults. In contrast, G. caudovittatus demonstrate an opposite trend (Fig. 1). We find the highest densities of adults around 30 m, (mean TL of all G. caudovittatus at this depth ± SD: 138 ± 42, N = 55) while juveniles predominate deeper reefs: we find more than 80% of the small juveniles between 60–65 m (mean TL of all fish at this depth ± SD: 40 ± 3 mm, N = 63); we find mid-size fish between 45–50 m (mean TL of all fish at this depth ± SD: 56 ± 26 mm, N = 24) (Fig. 2). These differences in average G. caudovittatus size per depth are statistically significant (one way ANOVA, P < 0.001). Examining the other 12 species recorded, we find large variances in abundance caused by the tendency of some species to school. Zooplanktivorous fishes, in general, appear to peak (though not significantly) at the same depth of the peak in the abundance of juveniles G. caudovittatus (65 m differ from 30 m in G. caudovittatus, post hoc tests to one way ANOVA, P < 0.05; Fig. 3). However, piscivorous fishes were significantly less abundant in the deeper habitats (post hoc to one way ANOVA, P < 0.05; Fig. 3).

Fig. 1
figure 1

The maximum depth of occurrence for the adults and juveniles of 13 species of diurnal zooplanktivores. The diagonal is the line of equality. Letters represent the different species: a – Amblyglyphidodon flavilatus; b – Chromis dimidiata; c – C. pembae; d – C. viridis; e – Cirrhilabrus blatteus; f – C. rubriventralis; g – Dascyllus aruanus; h – D. marginatus; i – D. trimaculatus; j – Genicanthus caudovittatus; k – Paracheilinus octotaenia; l – Pomacentrus trichourus; m – Pseudanthias squamipinnis

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Fig. 2
figure 2

Size class distribution of G. caudovittatus. Error bars not included, see text for details

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Fig. 3
figure 3

Relative average abundance (relative to maximum abundance in each group) of juveniles G. caudovittatus, and other diurnal zooplanktivores and piscivores (of all sizes)

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Discussion

Population size structure has received little attention in studies of mechanisms that structure reef fish assemblages (Robertson 1998). Here we examine the size distribution of G. caudovittatus along the depth gradient with relation to other zooplanktivore species and possible predators. Several studies have suggested that young fish inhabit the same or shallower depths as adults [see Introduction and also Green (1996) and a review by Jones (1988)]. In this study we show an opposite trend for one species, G. caudovittatus, in which juveniles occupied deeper waters than the adults. This oddity raises interesting questions regarding juvenile–adult depth partitioning in zooplanktivorous fish. Size-dependent differences in bathymetric distribution can be influenced by different habitat needs, intra-specific competition (including territoriality by the adults), interspecific competition with other zooplanktivores, predation and/or hydrodynamic processes which determine larval bathymetric distribution. Although this study did not directly test any of these possibilities, we speculate as to the cause of the observed size variation with depth. We here raise several hypotheses as to why the young individuals of the zebra angelfish appear in deeper waters than adults, which should be further examined.

Because adults and young G. caudovittatus differ greatly in size, it is very likely that they have different diets and shelter needs which reduce intra-specific competition (Jones 1988; Fishelson and Sharon 1997; McCormick 1998; Robertson 1998). Furthermore, if juveniles of this species do not compete with the adults over territory or mates, which is likely, habitat segregation by sexual maturity may not seem a necessity. The abundance of zooplanktivorous fishes, seems to peak at the same depth of juveniles G. caudovittatus, or at least does not change with depth. As a consequence inter-specific competition would probably not lead the juveniles to go deeper. Piscivorous fishes, on the other hand, were found to be significantly less abundant in the deeper habitats suggesting that deep reefs may be offering juvenile G. caudovittatus a refuge from predation. Whether predation indeed drives G. caudovittatus juveniles deeper, and the reasons why juveniles of this species, as oppose to all others, are able to use the deep reef should be further studied.

This study demonstrates that the deep reefs may serve as nursery grounds for G. caudovittatus. So far nursery grounds were mainly reported in areas distant from the reef such as shallow waters, gravel regions and sea-grass (Beck et al. 2001; Gullstrom et al. 2002; Dorenbosch et al. 2004; Mumby et al. 2004). The finding of a deep nursery ground further stress the importance of deep coral reef research for understanding the ecological patterns and processes defining the reef community structure. These findings also suggest that when conservation decisions and plans are made, the deep reef should be included for enabling sustainable persistence of some reef fishes.