CSIRO PUBLISHING
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Marine and Freshwater Research, 2003, 54, 957–965
Diet, feeding behaviour and habitat utilisation of the blue stingray Dasyatis chrysonota (Smith, 1828) in South African waters David A. Ebert A,C and Paul D. Cowley B A Pacific
Shark Research Center, Moss Landing Marine Laboratories, 8272 Moss Landing Road, Moss Landing, CA 95039, USA. B South African Institute for Aquatic Biodiversity, Private Bag 1015, Grahamstown 6140, South Africa. C Corresponding author. Email:
[email protected] Abstract. Analysis of stomach contents for Dasyatis chrysonota revealed that diet varied with size and habitat. The diet of all size classes in the surf zone was comprised primarily of Callianassa spp., Donax spp. and unidentified polychaete species. The medium and large size classes fed primarily on Donax spp., whereas the very large size class fed mainly on Callianassa spp. Polychaetes were of secondary importance as prey for the medium size class. The diet of D. chrysonota in the nearshore zone consisted mainly of Balanoglossus capensis and Callianassa spp. Balanoglossus capensis decreased from an index of relative importance (IRI) of 75.3% for the medium size class to 59.9% for the very large size class, whereas Callianassa spp. increased from 22.8% to 39.4% between the medium and the very large size classes. The offshore zone was the only area in which small size class D. chrysonota were caught. The diet of these small D. chrysonota was primarily polychaetes and amphipods. Polychaetes increased in importance in the medium size class, but declined in each successively larger size class. Conversely, Pterygosquilla armata capensis became the single most important prey item for the very large size class, comprising an IRI of 50.9%. The behaviour pattern used by D. chrysonota to locate and extract prey is described. Extra keywords: benthic communities, predation, size class, stomach contents, surf zone. Introduction The blue stingray Dasyatis chrysonota (Smith, 1828) is a common coastal batoid species found in the waters around southern Africa. This species occurs from KwaZulu-Natal, South Africa on the east coast to central Angola on the west coast of southern Africa (Cowley and Compagno 1993). It is one of the most abundant batoid species along South Africa’s Eastern Cape coast, where it is considered an important predator in the nearshore sandy beach ecosystem (Rossuow 1983). The ecological impact of batoid fish on benthic communities has been investigated in several studies. Smith and Merriner (1985) noted that feeding schools of cownose rays (Rhinoptera bonasus) inflict serious damage to commercial oyster beds and natural eelgrass beds in Chesapeake Bay on the east coast of the US. Van Blaircom (1982) concluded that foraging batoids played an influential role in shaping infaunal communities in a sandy beach ecosystem off La Jolla, California. In the Eastern Cape, South Africa, Rossuow (1983) studied elasmobranchs with a particular emphasis on the ecology of the lesser guitarfish Rhinobatos annulatus and stated that these and other batoids are important predators in the surf zone. Dasyatis chrysonota may also play an important role in the structuring of benthic communities, especially along sandy beaches (Lasiak 1982). However, © CSIRO 2003
the only published information on the feeding habits of this species is anecdotal and indicates that they feed on a variety of benthic invertebrates and small fish (Wallace 1967; Van der Elst 1981; Rossuow 1983; Compagno et al. 1989). Dasyatis chrysonota occupy different habitats throughout their life and although they may feed on a wide variety of prey items, the proportions of the different prey items may vary considerably among different size classes. Gray et al. (1997), for example, found that because large bat rays (Myliobatis californica) were physically more powerful and could dig deeper, they were able to excavate prey items unavailable to smaller conspecifics. Given the possible importance of D. chrysonota on structuring benthic communities along the southern African coast, the lack of knowledge on its feeding habitats is significant. The aims of the present study were to investigate the diet of D. chrysonota and to determine whether D. chrysonota exhibits ontogenetic and dietary changes associated with different habitats. In addition, the feeding behaviour of D. chrysonota is described. Materials and methods Dasyatis chrysonota were collected along the South African coastline (34◦ 40 S, 19◦ 00 E to 33◦ 30 S, 27◦ 50 E) between March 1987 and May 1989 from three distinct habitats with a soft sandy substrate: (1) the surf zone; (2) the nearshore zone; and (3) the offshore zone. The surf zone is characterised by the presence of a swash zone, a trough and a bar, which 10.1071/MF03069
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is made up of unconsolidated materials and marks the breaker zone. The nearshore zone is defined as the area immediately seaward of the outer breaker zone to a depth that corresponds with the modal wave base (Short 1983). The modal wave base, or outer limit of surf circulation cells, is where wave orbital motions begin to interact with the bed sufficiently to initiate sand transport. The depth at which the modal wave base occurs depends on the beach type. For intermediate beach types, this depth can be between 10 and 30 m (Short 1983). The offshore zone is the area extending seaward from the modal wave base that becomes the inner continental shelf with increased distance from shore (Horikawa 1988). Stomach samples were obtained from rock and surf anglers (surf zone), light tackle ski-boat anglers (nearshore zone) and trawling aboard the R. V. Africana (offshore zone). Stomachs were removed as soon as possible after capture and preserved in 10% formalin for subsequent analysis. Prey items were identified to the lowest possible taxa and grouped by phyla. An index of relative importance (IRI), following Pinkas et al. (1971), was used to rank prey items. This index was calculated by summing the numerical and weight percentage values and multiplying the result by the percentage frequency of occurrence: IRI = %F (%N + %W) where %N, %W and %F are the percentage contributions of a prey species in terms of number, weight and frequency of occurrence, respectively, in the stomachs examined. The IRI values were converted to a percentage and are shown graphically following the suggestions of Cortes (1997) to promote consistency and to facilitate comparison between elasmobranch studies. Dietary analyses using percentage IRI were compared by size and habitat to determine whether any changes occur. Four size classes were chosen arbitrarily based on disc width (DW): 60 cm. For discussion purposes, these size classes are referred to as small, medium, large and very large, respectively. The habitats compared were the surf, nearshore and offshore zones, as described above. The proportional food overlap between size classes and habitats was calculated using Horn’s index of overlap (Krebs 1999). The degree of overlap was determined using Langton’s (1982) scale, in which values range between 0 and 0.29 (low), 0.30–0.59 (medium) and ≥0.60 (high). We observed the feeding behaviour of three D. chrysonota kept in captivity in a portable pool at the Rhodes University laboratory in Port Alfred (South Africa). Live sand prawns (Callianassa kraussi) were introduced to the approximately 4000-L porta-pool and allowed to settle in the sand substrate to simulate the natural environment. The food searching and prey seizing behaviours of D. chrysonota were then observed and recorded.
Results A total of 369 stomachs was examined, of which 315 (85.4%) contained prey items. Results from the quantitative stomach contents analysis of all D. chrysonota captured during the study period are listed in Table 1. Overall, unidentified polychaetes, at 59.3%, had the highest %IRI, followed by Callianassa spp. (10.0%), unidentified amphipods (9.6%) and Balanoglossus capensis (9.3%). Surf zone Only 39% of the 100 stomachs examined from the surf zone contained prey. Three of the four D. chrysonota size classes (medium, large and very large) were represented in the surf zone. The dietary importance according to %N, %W and %F of the major prey groups or species is given in Table 2. The
D. A. Ebert and P. D. Cowley
Table 1. Diet according to percentage frequency (%F), number (%N), weight (%W) and index of relative importance (%IRI) of Dasyatis chrysonota for all size classes combined (n = 315) Prey items
%F
%N
%W
%IRI
Nemertea Unidentified spp.
14.9
6.2
1.7
2.3
Sipunculida Unidentified spp.
1.0
0.4
1.3
0.0
Echiurida Ochoetostoma spp. Unidentified spp.
0.6 4.1
0.4 1.4
1.1 1.6
0.0 0.2
61.3
27.2
22.4
59.3
8.3
2.9
1.7
0.7
6.3
3.5
12.9
2.0
19.4
8.0
18.5
10.0
33.3
13.8
1.0
9.6
5.4
0.7
0.4
0.1
1.3
0.1
0.1
0.0
1.3 12.7
0.1 1.7
0.0 0.2
0.0 0.5
0.3 11.1
0.0 2.4
0.0 1.4
0.0 0.8
15.9
3.5
1.1
1.4
0.6 4.1 1.6 1.9 5.7 3.5 5.4
0.2 1.0 0.2 0.2 0.8 1.7 0.9
1.2 1.2 0.7 0.7 1.0 0.4 1.3
0.0 0.2 0.0 0.0 0.2 0.1 0.2
11.4 4.1
1.7 3.0
1.4 5.1
0.7 0.6
0.3
0.0
0.2
0.0
16.8
12.7
15.7
9.3
9.5 1.3 1.0 1.0 0.6 1.6 9.8
2.7 0.6 0.1 0.1 0.0 0.2 1.4
0.9 1.5 0.6 0.5 0.1 0.3 1.6
0.7 0.1 0.0 0.0 0.0 0.0 0.6
Annelida Polychaeta unidentified Arthropoda Crustacea Unidentified spp. Stomatopoda Pteroygosquilla armata capensis Anomura Callianassa spp. Amphipoda Unidentified spp. Isopoda Unidentified spp. Copepoda Unidentified spp. Mysidacea Gastrosaccus psammodytes Unidentified spp. Penaeidae Macropetasma africana Unidentified spp. Caridea Processa spp. Brachyura Goneplax rhomboides Mursia cristimanus Neopilumnoplax spp. Ovalipes punctatus Thaumastoplax spiralis Unidentified larvae Unidentified spp. Mollusca Pelecypoda Donax spp. Unidentified spp. Gastropoda Bullia spp. Chordata Hemichordata Balanoglossus capensis Teleosti Bregmaceros spp. Gobius spp. Gonorhynchus spp. Cynoglossus spp. Gnathophis spp. Engraulis capensis Unidentified spp.
Feeding habits of Dasyatis chrysonota
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Table 2. Diet according to percentage frequency (%F), number (%N), weight (%W) and index of relative importance (%IRI) of surf zone Dasyatis chrysonota Prey items
Disc width (cm) 30–45 (n = 9)
Sipunculida Unidentified spp. Echiurida Ochoetostoma spp. Unidentified spp. Annelida Polychaeta unidentified Arthropoda Stomatopoda Unidentified spp. Anomura Callianassa spp. Amphipoda Unidentified spp. Isopoda Unidentified spp. Mysidacea Gastrosaccus psammodytes Penaeidae Macropetasma africana Brachyura Ovalipes punctatus Thaumastoplax spiralis Unidentified larvae Unidentified spp. Mollusca Pelecypoda Donax spp. Unidentified spp. Gastropoda Bullia spp.
%N
%W
%IRI
0.0
0.0
0.0
0.0
11.1 44.4
1.3 8.3
8.3 6.6
22.2
10.9
11.1
>60 (n = 7)
%N
%W
%IRI
%N
%W
%IRI
4.3
5.3
2.3
0.3
0.0
0.0
0.0
0.0
1.9 12.0
4.3 8.7
9.3 3.3
11.2 5.7
2.0 1.8
0.0 14.3
0.0 12.0
0.0 9.1
0.0 4.5
6.7
7.1
26.1
17.3
23.2
23.9
28.6
4.0
4.1
3.5
1.9
0.7
0.5
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
11.1
3.8
25.5
5.2
13.0
6.7
4.5
3.3
42.9
62.7
66.4
83.1
11.1
0.7
0.2
0.2
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
11.1
0.7
0.2
0.2
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
11.1
0.7
0.2
0.2
13.0
2.0
0.2
0.6
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
14.3
2.7
1.0
0.8
0.0 0.0 11.1 11.1
0.0 0.0 34.6 0.7
0.0 0.0 11.5 0.3
0.0 0.0 9.3 0.2
8.7 8.7 0.0 13.0
2.0 2.7 0.0 3.3
5.0 0.5 0.0 1.0
1.4 0.6 0.0 1.3
14.3 0.0 0.0 14.3
1.3 0.0 0.0 14.7
0.7 0.0 0.0 13.8
0.4 0.0 0.0 6.1
44.4 33.3
32.7 3.9
39.6 4.0
58.4 4.8
30.4 0.0
48.0 0.0
46.4 0.0
64.9 0.0
0.0 14.3
0.0 1.3
0.0 0.8
0.0 0.5
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
14.3
1.3
4.1
1.2
major prey item in both the medium and large size classes was Donax spp., which contributed 63.2% and 64.9% towards the IRI, respectively (Fig. 1). In the medium size class, the other major prey items, in order of importance, were unidentified Echiurida, unidentified Brachyura larvae, unidentified Polychaeta and Callianassa spp., which collectively constituted 35.6% of the IRI. In the large size class, the other major prey items were unidentified Polychaeta (IRI = 23.9%) and, to a lesser extent, unidentified Echiurida, unidentified Brachyura, and Callianassa spp. A marked change in the food composition was observed in the very large size class. The major prey item was Callianassa spp., which contributed 83.1% towards the IRI, whereas unidentified Brachyura, unidentified Echiurida and unidentified Polychaeta collectively only contributed 14.1% (Fig. 1). In contrast with the smaller size classes, Donax spp. was absent in the very large size class. A total of 17 prey items was observed for all size classes combined in the surf zone habitat. The diversity of prey items for surf zone D. chrysonota declined with increasing size. Those in the medium size category had 12 different prey
%F
90
%F
Donax spp. Polychaeta spp. Callianassa spp.
80 70 60 IRI (%)
%F
45–60 (n = 23)
50 40 30 20 10 0 30–45
45–60 Size classes (cm)
>60
Fig. 1. Percentage index of relative importance (IRI) for major prey items in the diet of surf zone Dasyatis chrysonota according to size class.
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D. A. Ebert and P. D. Cowley
Table 3. Diet by percentage frequency (%F), number (%N), weight (%W) and index of relative importance (%IRI) of nearshore zone Dasyatis chrysonota Prey items
Disc width (cm) 30–45 (n = 22) %F
Annelida Polychaeta unidentified Arthropoda Anomura Callianassa spp. Mysidacea Unidentified spp. Penaeidae Unidentified spp. Brachyura Ovalipes punctatus Thaumastoplax spiralis Unidentified spp. Mollusca Pelecypoda Donax spp. Chordata Hemichordata Balanoglossus capensis Teleosti Unidentified spp.
45–60 (n = 42)
>60 (n = 13)
%N
%W
%IRI
%F
%N
%W
%IRI
%F
%N
%W
%IRI
9.1
3.2
2.4
0.4
21.4
11.1
5.0
3.2
15.4
3.1
0.9
0.5
59.1
22.1
30.6
22.6
59.5
25.8
35.9
33.9
69.2
35.2
41.9
39.5
13.6
1.2
0.2
0.1
4.8
0.7
0.1
0.0
0.0
0.0
0.0
0.0
4.5
0.8
0.5
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0 27.2 0.0
0.0 3.6 0.0
0.0 3.3 0.0
0.0 1.4 0.0
4.8 23.8 7.1
0.5 4.9 0.7
1.0 5.1 0.3
0.1 2.2 0.1
7.7 0.0 0.0
0.5 0.0 0.0
2.4 0.0 0.0
0.2 0.0 0.0
4.5
0.4
1.4
0.1
8.1
2.4
0.3
0.0
0.0
0.0
0.0
0.0
81.8
68.3
58.8
75.4
61.9
55.8
50.2
60.5
69.2
61.2
54.8
59.9
4.5
0.4
2.8
0.1
2.4
0.3
1.4
0.0
0.0
0.0
0.0
0.0
items, whereas those in the large and very large size classes had 10 and eight different prey items, respectively.
Callianassa spp. 80
Nearshore zone
Offshore zone The stomachs of 206 specimens were examined and 199 (97%) contained prey items. This zone also included
60 IRI (%)
Prey organisms were present in 77 of 95 (81%) stomachs examined. Three of the four D. chrysonota size classes (medium, large and very large) were represented in the nearshore zone. All prey items are listed in Table 3. The diet of D. chrysonota in the nearshore zone consisted mainly of B. capensis and Callianassa spp., which, as %IRI, collectively comprised 97.9%, 94.4% and 99.3% of the diets for the medium, large and very large size classes, respectively (Fig. 2). Balanoglossus capensis decreased from an IRI of 75.4% for the medium size class to 59.9% for the very large size class. Callianassa spp. increased from 22.6% to an IRI of 39.5% between the medium and very large size class. The percentage IRI contribution for all other dietary items in each size class was relatively insignificant. The diversity of prey items for nearshore zone-caught D. chrysonota was lowest among the three zones sampled, with only 10 different prey items found. The very large size class had the lowest diversity of prey items (four) compared with the medium and large size classes, which had eight and nine, respectively.
Balanoglossus capensis
70
50 40 30 20 10 0 30–45
45–60 Size classes (cm)
>60
Fig. 2. Percentage index of relative importance (IRI) for major prey items in the diet of nearshore zone Dasyatis chrysonota according to size class.
D. chrysonota in the small size class (60 cm >60 cm >60 cm
0.372 0.136 0.264
0.451 0.959 0.209
1.000
0.136 0.022 0.511
0.279 0.107 0.365
0.581 0.983 0.271
0.193 0.028 0.740
Surf Zone >60 cm
Nearshore >60 cm
Offshore >60 cm
1.000 0.568 0.374
1.000 0.201
1.000
(a )
(b )
Fig. 4. The foraging behaviour of Dasyatis chrysonota. (a) Prey searching, initiated by slow swimming near the substrate and (b) the body assumes a convex shape over prey location, followed by expansions and contractions of the orobranchial cavity to draw the prey from its burrow.
Feeding habits of Dasyatis chrysonota
movements. Once a prey item was located, the stingray stopped suddenly and quickly settled upon the substrate. The body then assumed a convex shape over the location of the prey (Fig. 4b) and a rapid continuous expansion and contraction of the orobranchial chamber began. Water and sediments are taken into the mouth during this process, but quickly expelled through the gill slits and occasionally via the spiracles. This created a suction action by pushing water towards the posterior margins of the disc. The raised pelvic fins acted as an outlet region for water and sand sediments from the evacuated depression. Once the prey was drawn from its burrow it was seized by the stingray’s highly protractible jaw and drawn into its mouth. If the prey item escaped, the stingray quickly pounced on it again, seizing it with its mouth and ingesting the prey item. During each observed predation bout, the stingray raised its tail with its serrated spine positioned at an angle of 40◦ –60◦ (Fig. 4b). Once the predation bout was finished, the stingray would lower its tail and settle onto the bottom, conforming to the contour of the substrate. Discussion Quantitative analysis of stomach contents revealed that D. chrysonota feed on a wide variety of benthic epifauna and infauna. The relative importance of certain dominant macrofaunal organisms in the diet from each habitat suggests an opportunistic feeding strategy. Although the primary prey items changed between size classes and habitats, the main prey groups observed were crustaceans, molluscs, polychaetes and hemichordates. Dietary studies on several species of dasyatid rays from the western Atlantic and Gulf of Mexico reveal that crustaceans and molluscs are among the most important prey items (Hess 1961; Struhsaker 1969; Snelson and Williams 1981; Thorson 1983; Gilliam and Sullivan 1993). Bivalve molluscs, although very important to the diet of surf zone D. chrysonota, were relatively unimportant in the other zones studied. Balanoglossus capensis, an abundant hemichorate found in the nearshore zone, was similarly found to be an important dietary item in this habitat, but was non-existent in the diet of D. chrysonota in the other two habitats studied. Teleosts have been found to be important in the diets of D. akajei and D. americana (Gilliam and Sullivan 1993; Taniuchi and Shimizu 1993). Hess (1961) found that D. centroura and D. sayi occasionally fed off the bottom on small teleosts. In contrast, teleosts were relatively unimportant prey items in the diet of D. chrysonota. The diet for all size classes of D. chrysonota in the surf zone was comprised primarily of Callianassa spp., Donax spp. and unidentified polychaete species. Aspects on the ecology for many of these surf zone macrofaunal prey items, especially those occurring in the intertidal region, is discussed by McLachlan (1983). The medium and large size classes of D. chrysonota fed primarily on small Donax spp. (
