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Butterflyfishes of the Southern Red Sea Zekeria, Zekeria Abdulkerim

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Download date: 26-09-2021 Butterflyfishes of the Southern Red Sea 31

Chapter 4 Resource Partitioning among Four Butterflyfish Species

Z. A. Zekeria, Y. Dawit, S. Ghebremedhin, M. Naser and J. J. Videler Published in Marine and Freshwater Research. 2002,vol. 53, pp.1-6. 32 Chapter 4. Resource Partitioning

Abstract

Feeding habits and territorial behaviour of four sympatric Red Sea butterflyfishes were investigated in the Eritrean coastal waters. Feeding habits were studied by focal animal sampling. Individual bite rates and types of food consumed were recorded. Stomach contents of 125 specimens were analysed in the laboratory. The food items in the stomach were sorted and their volume estimated. The four species showed marked variation in their food preferences and feeding habits. The most abundant butterflyfish Chaetodon larvatus, an obligate corallivore, forms monogamous pairs. Each pair defends a relatively small territory against conspecifics and C. semilarvatus. The latter species also feeds on scleractinian corals but lives solitary or in small aggregations. The third species, Heniochus intermedius, feeds on non-coralline benthic invertebrates (mainly polychaetes); it usually lives in pairs or in aggregations of up to 24 individuals. Both C. semilarvatus and H. intermedius occupy undefended and overlapping home ranges. The least abundant species, C. mesoleucos, forms monogamous pairs, defends a territory and feeds mainly on non-coralline benthic invertebrates (mainly nematodes and polychaetes). The study reveals that the four species co-exist in the same habitat where they partition the food resources. Both C. larvatus and C. semilarvatus feed on scleractinian corals, but partition this food source by feeding at different times. While C. larvatus was observed to feed only during daytime C. semilarvatus feeds by day and night. Butterflyfishes of the Southern Red Sea 33

INTRODUCTION

Fourteen species of butterflyfish are recorded from the Red Sea (Randall 1983). The distribution shows marked variations from north to south (Roberts et al 1992), as well as locally (Bouchon-Navaro & Bouchon, 1989 and Roberts & Ormond, 1987). Only twelve chaetodontid species are found in the southern Red Sea (Kemp 1998), of which four are common on the reefs around Massawa and the islands of the Dahlak archipelago (See chapter 3). The butterflyfish assemblage in the southern Red Sea differs from that in the north (Righton et al 1996). Chaetodon austriacus and C. paucifasciatus dominate the northern reefs and are absent in the south. C. larvatus, the most dominant chaetodontid in the south, has a very low density in the north (Roberts et al 1992).

Butterflyfishes are one of the best-studied fish families on coral reefs (Motta 1989). Their feeding habits have been investigated in the Pacific (Reese 1975, 1981), Japan (Sano 1989), the Red Sea (Ormond 1972, Harmelin-Vivien & Bouchon-Navaro 1982) and in French Polynesia (Harmelin-Vivien & Bouchon-Navaro 1983). Distribution patterns of chaetodontids are documented for the Great Barrier Reef (Fowler 1990a), French Polynesia (Bell et al 1986’ Bouchon-Navaro 1986), the West Indies (Alevizon et al 1985), and the Red Sea (Bouchon-Navaro & Bouchon 1989, Roberts et al 1992).

These studies have shown that a number of chaetodontids co-exist in the same habitat. Many butterflyfish species are known to feed on corals. However, there is little information on how these closely related species co-exist in the same habitat while most of them use similar food resources. Bouchon-Navaro (1986) and Pitts (1991) examined resource partitioning among butterflyfishes in the northern Red Sea and western Atlantic respectively. Results from those studies show partitioning of either food or space resources among co-existing species. In the present work, trophic and spatial partitioning among four chaetodontid fish species in the southern Red Sea was investigated.

MATERIALS AND METHODS

Study area

The study was conducted in the southern Red Sea near Massawa (Fig. 4.1). The fishes used for analysis of stomach contents were collected from the reef east of Sheikh Said Island. Observations on the feeding and ranging behaviour of the fish species were made on Resimedri reef near Massawa, and surveys of the distribution and abundance of the butterflyfishes took place on seventeen reefs around Massawa and in the Dahlak archipelago. Most of the reefs in the study area are of the fringing type and reach a depth of 10 m. The dominant coral genera found in the study area are Porites, Echinopora, Montipora and Stylophora. The coral cover of eastern Sheikh Said and Resimedri reefs is 34 Chapter 4. Resource Partitioning

45% and 57% respectively. These values are relatively high compared with the mean coral cover of 23% found for the seventeen reefs studied (See chapter 3).

Distribution and abundance of fishes

A belt-transect method was used to estimate the abundance of the butterflyfishes (Crosby & Reese 1996) at seventeen sites in the study area (see chapter 3). At each site, three lines, each 100-m long, were laid parallel to the shoreline. Visual census of fishes was conducted by slowly swimming or diving along the line and counting all the butterflyfishes observed within 2.5 m distance on either side of the line. Crosby & Reese (1996) recommended a transect width of 10 m. However, owing to poor visibility and because of the narrowness of many surveyed reefs we reduced the width to 5 m. The fishes were identified to species level and their abundance was recorded on a PVC slate. Data collection took place between 0900 and 1300 hours in March, April and August 2000.

Figure 4.1. Study site. Asterisks indicate locations of surveyed reefs. RM = Resimedri; SS = Sheik Said Island; TW = Twalot Island. The two arrows indicate the observation and the fish collection sites. Butterflyfishes of the Southern Red Sea 35 Collection of fishes

125 fishes belonging to four chaetodontid species were caught in a barrier net while diving and snorkelling. Immediately after capture, fishes were preserved in ice and transferred to a laboratory where lengths and weights were measured. The sampled fish were stored in a deep freezer until dissection. Collection took place at different times of the day from November 1999 to April 2000.

On 14 April 2001, forty-five additional specimens of C. larvatus, C. semilarvatus and H. intermedius were collected to investigate the fullness index of their stomach. Five individuals from each species were captured in the morning (0600–0700 hours), after noon (1200–1300 hours) and in the evening (1800–1900 hours).

Dissection and stomach content analysis

Total length, standard length and body depth were measured to the nearest mm; body mass was measured to the nearest g. After dissection mass of the stomach and length of the intestine were measured. Stomachs were opened under a dissecting microscope, and their contents were spread out in a Petri dish and examined under a microscope. The bottom of the Petri dish was divided into 0.25 mm2 squares. Prey items were classified as turf algae, scleractinian corals (coral polyp, zooxanthellae, nematocyst and coral mucus), nematodes, sedentary polychaetes, errant polychaetes, hydrozoans, crustaceans, ascidiaceans and larvaceans. The volumetric percentage of a given food item was estimated by determining the number of grid squares covered by each food type as a fraction of total number of squares covered by the stomach content (Mol 1995). For the fish collected on 14 April 2001, the gutted mass and the mass of the stomach content were determined.

Field observations

Field observations were carried out while snorkelling or diving on the reef slope at depths varying from 2 to 5 m. Each fish was followed for 15 min, and the number of bites and the type of coral consumed were recorded on a PVC slate. Feeding observations were made for at least three days for each species from January to April 1999. During each day at least three replicate feeding observations were made three times: morning (0600–0800 hours), noon (1130–1300 hours) and evening (1700–1930 hours).

Ranging habits were investigated by following the movement of fishes for 3 h per day and for five days for each fish species. Five individuals from each species were marked by applying subcutaneous injections of Alcian Blue (De Jonge & Videler 1989). The movements of the marked fishes were monitored for two months. Territories were marked with floats. Sizes of the territories were determined by plotting the territories to 36 Chapter 4. Resource Partitioning scale on graph paper. The ranging habit and feeding behaviour for two C. larvatus pairs were monitored during one year.

Data analysis

Several coefficients were calculated to determine the relative importance of prey items in the diet: the mean volumetric percentage (MVP) of a prey is the sum of individual volumetric percentages for the food item divided by the number of specimens examined; the percentage frequency of occurrence (PFO) is the number of stomachs containing a particular prey item as a percentage of the total number of stomachs containing food; and the ranking index (RI) is calculated by multiplying mean volumetric percentage and percentage frequency of occurrence.

Habitat width (H’h) was calculated by use of the Shannon index (H’) as follows:

H ' = ( Pi ln Pi ) h ∑ where Pi represents the relative abundance of a fish species in habitat i.

The evenness of fish distribution (Eh) was determined by use of the Pielou evenness index (E) which was calculated as E = H' /lnN h h

Where N is the total number of habitats in which the fish species was recorded (Pielou 1966).

The same equations were also used to calculate the diet breadth (H’d) and diet distribution (Ed) for the four fish species where Pi represents the proportion by volume of a prey item i, and N is the total number of fishes with stomachs containing food.

Overlap between two species in resource use was calculated on the basis of prey types and habitat use (Sala & Ballesteros 1997). Habitat overlap (T) was determined as:

T = 1 − 0. 5 P − P ∑ x hi y hi where P and P are the proportions of abundance in the habitat hi for all fish species xhi yhi pairs x,y.

Diet overlap (αH) was determined as

α = 1 − 0 .5 Px − Py H ∑ fi fi where P and P are the proportions by volume in the stomachs of the prey item f for all xfi yfi i fish species pairs x, y. Butterflyfishes of the Southern Red Sea 37

The overlap index varies from 0, when the two species use totally different resources, to 1, when they use the resources in the same proportion. An overlap value

(αH) equal to or above 0.60 was considered significant, following Keast (1978).

Stomach fullness index (FI) was the mass of the stomach content as a percentage of the gutted mass of the fish.

RESULTS

Distribution patterns

The four species were widely distributed, with H’h being 2.52 for C. larvatus, 2.41 for C. semilarvatus, 2.26 for C. mesoleucos and 2.47 for H. intermedius. They showed little variation in their distribution on the seventeen reefs, with Eh being 0.09 for C. larvatus, 0.91 for C. semilarvatus, 0.91 for C. mesoleucos and 0.87 for H. intermedius. There was high overlap of habitat between pairs of species among all species (Table 4.1), particularly between C. larvatus and C. semilarvatus (T = 0.71).

Table 4.1. Habitat overlap (T) among four butterflyfish species in the Red Sea

Fish species C. larvatus C. semilarvatus C. mesoleucus H. intermedius

C. larvatus 1.00 0.71 0.54 0.59 C. semilarvatus 1.00 0.53 0.65 C. mesoleucus 1.00 0.58 H. intermedius 1.00

Diet

C. larvatus (H’d 0.24, Ed 0.03) and C. semilarvatus (H’d 0.41, Ed 0.07) mainly ate polyps of scleractinian corals. The mean volumes occupied by this food item were 96.1% and 90.1% of the total food volume respectively (Table 4.2). As a result, the dietary overlap between the two species was very high, αH = 0.94 (Table 4.3). C. semilarvatus

Table 4.3. Diet overlap (αH) among four butterflyfish species in the Red Sea

Fish species C. larvatus C. semilarvatus C. mesoleucus H. intermedius

C. larvatus 1.00 0.94 0.05 0.19 C. semilarvatus 1.00 0.10 0.23 C. mesoleucus 1.00 0.32 H. intermedius 1.00 38 Chapter 4. Resource Partitioning supplemented its diet with errant polychaetes and a small quantity of nematodes. C. mesoleucos (H’d 1.50, Ed 0.19) and H. intermedius (H’d 1.88, Ed 0.17) consumed different types of food with little overlap (αH = 0.48): The diet of C. mesoleucos was composed mainly of unidentified matter, polychaetes, nematodes and scleractinian corals, whereas that of H. intermedius was mainly polychaetes and scleractinian corals, supplemented with larvaceans, crabs and amphipods (Table 4.2).

Table 4.2. Mean volumetric percentage (MPV), percentage frequency of occurrence (PFO) and ranking index (RI) of food items in the diets of four butterflyfish species collected from Red Sea

C. larvatus C. semilarvatus C. mesoleucus H. intermedius

No of fish 30 45 15 25

Size range (cm) 7.93-11.72 10.37-17.41 9.6-1.41 8.3-17.40

Food item MVP PFO RI MVP PFO RI MVP PFO RI MVP PFO RI

Coral 96.1 100.0 9605 90.1 100.0 9008 6.7 26.7 178 24.5 64.0 1571

Polychaet (sed) 0.1 6.7 1 0.0 0.0 0 9.3 100.0 935 37.8 92.0 3480

Polychaet (err) 1.0 13.3 13 4.9 91.1 442 17.7 100.0 1771 4.8 76.0 367

Nematod 0.0 0.0 0 1.9 75.6 142 17.9 100.0 1792 0.0 0.0 0

Copepod 0.2 13.3 3 0.0 0.0 0 0.0 0.0 0 0.0 0.0 0

Amphipod 0.0 0.0 0 0.0 0.0 0 0.0 0.0 0 4.2 48.0 201

Shrimp 0.0 0.0 0 0.0 0.0 0 0.0 0.0 0 0.3 4.0 1

Crab 0.2 10.0 2 0.0 0.0 0 0.0 0.0 0 5.0 60.0 301

Hydrozoa 0.1 3.3 0 0.3 37.8 13 0.0 0.0 0 2.8 28.0 79

Ascidacia 0.0 0.0 0 0.0 0.0 0 1.2 46.7 56 3.5 40.0 142

Larvacea 0.0 0.0 0 0.0 0.0 0 0.0 0.0 0 5.0 16.0 80

Turf Algae 0.8 20.0 15 1.5 42.2 62 0.2 20.0 4 6.1 84.0 509

Others 1.6 20.0 33 1.4 22.2 31 2.0 60.0 120 5.9 80.0 476

Unidentified 0.0 0.0 0 0.0 0.0 0 45.0 100.0 4496 0.0 0.0 0

Feeding habits

The average feeding rate of C. larvatus was 10.5 bites min–1, whereas C. mesoleucos and C. semilarvatus fed at 6.4 and 6.6 bites min–1 respectively. H. intermedius spent most of the daytime hiding below coral and was only occasionally observed feeding at a rate of 1.1 bites min–1. With the exception of C. mesoleucos the species showed significant diurnal variation in feeding rate (P <0.05).

The feeding rate of C. larvatus was low in the morning, increased around noon and decreased during the afternoon (Fig. 4.2). C. larvatus and C. mesoleucos defend Butterflyfishes of the Southern Red Sea 39 territories during the day (see below) and sleep by night in coral crevices within their territories. We have no indication of feeding activity during the night in these two species

The feeding rate of C. semilarvatus increased gradually over the day (Fig. 4.2). The fishes were observed wandering over the reef after sunset. Night conditions made it difficult to observe feeding activities. C. semilarvatus collected at different times of the day showed significant variation in the stomach fullness index (P <0.05): individuals captured early in the morning had more food in their stomachs (mean FI = 1.76) than those investigated later in the day (mean FI = 1.27). This offers circumstantial evidence for nocturnal feeding.

16

14 )

-1 12

10

8

6

4

Feeding rate (bites mn

2

0 6:30 12:00 18:30 Time (hr)

Figure 4.2. Mean (± s.d.) number of bites min-1 in four chaetodontids in the southern Red Sea., g, C. larvatus;▲, C. semilarvatus; ♦, C. mesoleucos;●, H. intermedius.

The feeding rate of H. intermedius was very low throughout the day but increased sharply in the evening just before dusk (Fig. 4.2). H. intermedius was active after sunset. Fishes captured early in the day had more food in their stomach (FI = 0.84) than those collected either at noon or in the evening (FI = 0.48 and 0.50 respectively). These findings, as in C. semilarvatus, offer circumstantial evidence for nocturnal feeding by H. intermedius. The guts of the corallivorous species, C. larvatus and C. semilarvatus, were longer than those of the omnivores (Table 4.4). The relative length of intestine also shows the relation with the feeding habit of these species. C. larvatus had a relatively long gut and the highest feeding rate, whereas H. intermedius had the shortest gut and the lowest feeding rate. Although the observed feeding rate of C. semilarvatus was much lower than that of C. mesoleucos, if our argument of night feeding by C. semilarvatus is correct the 40 Chapter 4. Resource Partitioning total number of bites taken by C. semilarvatus throughout the day and night could be higher than the bites consumed by C. mesoleucos by day only.

Ranging and social behaviour

The spacing behaviour of the chaetodontids was investigated by following movements of marked individuals. C. larvatus lives in heterosexual pairs occupying territories ranging from about 24 m2 to 66 m2. Pairs are monomorphic and swim close to one another; heterosexuality was confirmed by examining the gonads of twenty pairs. The abundance of C. larvatus in most sites was so high that the whole reef was divided into continuous territories. Both pair members participate in defending their territory against conspecific neighbours and occasionally against C. semilarvatus. They mainly use advertisement or display behaviour to chase intruders. More time was spent feeding than patrolling the territory.

Table 4.4. Relative intestine length in four chaetodontids in the Red Sea

Species Name N Fish length (FL) Intestine length (IL) Relative length (RL)

Mean s.d. Mean s.d. RL = IL / FL

C. larvatus 20 10.7 1.1 64.3 18.6 6.0 C. semilarvatus 45 14.0 1.4 96.4 16.4 6.9 C. mesoleucus 6 13.2 0.5 53.6 6.5 4.1 H. intermedius 63 15.2 1.7 57.4 17.4 3.8

C. mesoleucos also lives in heterosexual pairs (confirmed by examining the gonads of twenty pairs) but defends relatively larger territories, ranging from 947 m2 to 966 m2. Defence was directed only against conspecifics. More time was spent patrolling the territory than feeding.

C. semilarvatus and H. intermedius are not territorial. Tagged individuals were not seen again on the reef after their release. C. semilarvatus is solitary or lives in groups of up to 20 individuals and actively wanders over the reef during the day. H. intermedius usually lives in pairs or in groups of up to 24 individuals. Pairs spend most of the daytime hiding below large corals. Both C. semilarvatus and H. intermedius were observed wandering over the reef after sunset.

DISCUSSION

Sano (1989) classified butterflyfish species into three categories based on food diversity. He grouped fishes with H’d values <0.3 as specialists and fishes with values

>1.0 as generalists. The third category, low diversity feeders, has intermediate H’d values. Butterflyfishes of the Southern Red Sea 41

According to this classification, the present study suggests that, in the southern Red Sea, C. larvatus belongs to the specialists, C. semilarvatus to the low diversity feeders and H. intermedius and C. mesoleucos to the generalists. The composition of the stomach contents classifies C. larvatus and C. semilarvatus as corallivores whereas C. mesoleucos and H. intermedius feed mainly on non-coralline benthic invertebrates.

In the northern Red Sea, C. larvatus feeds mainly on scleractinian corals whereas the diet of C. semilarvatus consists almost completely of non-coralline invertebrates (Ormond 1972). According to Harmelin-Vivien & Bouchon-Navaro (1982), H. intermedius in the Gulf of Aqaba is planktivorous, feeding mainly on larvaceans. The observed differences in the feeding habits between the chaetodontid populations of the southern and northern Red Sea could be due to the availability of food. Although coral polyps are abundant in both areas, the presence of competing corallivores may make this food source difficult to exploit for less competent species. Depending on food availability, diets may vary among individuals within sites, among sites and temporally (Roberts & Ormond 1992). Regional variation in feeding behaviour has also been noted for Chaetodon auriga, C. lunula, C. unimaculatus and Forcipiger flavissimus (Harmelin- Vivien & Bouchon-Navaro 1983), for C. kleinii (Sano 1989), for C. miliaris (Ralston 1981) and for C. trifascialis (Irons 1989).

In the Gulf of Aqaba, potential competitors occupy different regions on the reef: C. austriacus and C. trifascialis on the reef flat and C. fasciatus at 5 m depth (Bouchon- Navaro 1986). In the southern Red Sea, however, the two corallivorous species share the same habitat. Lack of space partitioning among the fishes may be due to the nature of the reef in the study area. The reefs in the Gulf of Aqaba extend to depths greater than 30 m while the reefs of the southern Red Sea rarely exceed 10 m (Roberts et al 1992).

C. mesoleucos and H. intermedius seem to partition diverse non-coralline invertebrates while C. larvatus and C. semilarvatus consume scleractinian corals. The observed agonistic behaviour of C. larvatus against C. semilarvatus indicates competition for food resources between these rival species.

The ‘niche compensatory hypothesis’ (Ebeling & Hixon 1991) asserts that co- occurring species showing a high degree of overlap in one niche dimension (e.g. habitat) separate along another dimension (e.g. diet). Taking both distribution and feeding habits into consideration, partitioning of resource use among the four chaetodontid species is evident. C. larvatus and C. semilarvatus show significant feeding overlap but partition the resources temporally. As indicated by the observational feeding studies and by the diurnal variation in the stomach fullness index, C. larvatus feeds mainly during daytime whereas C. semilarvatus seems to concentrate its feeding effort late in the evening and during the night. According to Bemert and Ormond (1981) C. semilarvatus is a nocturnal species. 42 Chapter 4. Resource Partitioning

Schoener (1974) pointed out that habitat separation is far more effective than food separation in preventing species overlap. In the present study, at least at a local scale, food partitioning appears to be more important than habitat partitioning in structuring fish assemblages. However, when the whole Red Sea is taken into consideration, it is likely that habitat partitioning has played an important role in the regional distribution of the butterflyfishes. The butterflyfish assemblage of the northern Red Sea is different from that of the south. For example, C. larvatus dominates the reefs in the south whereas C. austriacus, which is absent in the south, is dominant in the north. These two species exhibit a number of similar characteristics: they are obligate corallivores, live in heterosexual pairs, and defend small territories (Bouchon-Navaro & Bouchon 1989, Righton et al 1998, Roberts et al 1992, Wrathall et al 1992). Since both are generalist obligate coral feeders, C. larvatus and C. austriacus occupy similar niches on the reefs. The similarities in ecological role could be the reason for their dominance in different parts of the Red Sea.

The four chaetodontid species studied here show significant variation in their feeding rates. C. larvatus has a higher feeding rate than the non-coralline invertebrate feeders. The observed feeding rate for C. semilarvatus is low in the morning and increases during the day. Results from feeding observation and fullness index suggest that C. semilarvatus remains active and feeds also by night. Bemert and Ormond (1981) found C. semilarvatus to feed entirely by night. The total number of bites taken during day and night by C. semilarvatus could be much higher than those taken by C. mesoleucos during the day only.

Since coral tissue is poor in nutrients, the fishes take less energy per feeding bite. Coral has high water content and its energy content is relatively low (Tricas 1989). Moreover, corallivorous butterflyfishes have very low absorption efficiencies (Hourigan 1989). The feeding habits of the four fish species are also reflected in the length of their guts. The longest guts occur in microphagous and herbivorous species, and carnivorous fishes have the shortest guts (Kapoor & Smit 1975). Hence, corallivorous species require higher feeding rates (Reese 1991).