Variations in the dietary compositions of morphologically diverse

syngnathid fishes

Alan J. Kendricka,b & Glenn A. HyndescaCentre for Fish and Fisheries Research, School of Biological Sciences and Biotechnology,Murdoch University, Murdoch, Western Australia, 6150, AustraliabPresent address: Marine Conservation Branch, Department of Conservation and Land Management, 47Henry St, Fremantle, Western Australia, 6150, Australia (e-mail: alanke@calm.wa.gov.au)cCentre for Ecosystem Management, School of Natural Sciences, Edith Cowan University, Joondalup,Western Australia, 6027, Australia

Received 6 January 2003 Accepted 17 July 2004

Key words: pipefish, seahorse, seadragon, trophic ecology, habitat

Synopsis

We examined the diets of 12 morphologically diverse syngnathid species in shallow seagrass-dominatedmarine waters of south-western Australia to determine whether they differed among species that varied inbody form, size and snout morphology, and in particular whether species with long snouts ingested moremobile prey. Although all species consume mainly small crustaceans, the dietary compositions of thesespecies often vary markedly. We suggest that these differences are related to factors that influence both theirforaging capabilities and/or locations. Those species with long snouts (e.g. the common seadragon Phyl-lopteryx taeniolatus and long-snouted pipefish Vanacampus poecilolaemus) consume far more relativelymobile prey than species with short snouts. Species with short snouts (e.g. the pug-nosed pipefish Pugnasocurtirostris and Macleay’s crested pipefish Histiogamphelus cristatus) mainly consume slow moving prey.Spotted pipefish, Stigmatopora argus, and wide-bodied pipefish, Stigmatopora nigra, restrict their diets toplanktonic copepods, probably because their small gape size limits their ability to feed on alternative largerprey. Both the short-snouted seahorse, Hippocampus breviceps, and West Australian seahorse, Hippo-campus subelongatus, ingest mainly slow-moving prey, even though the latter species possesses a moderatelylong snout. This may reflect the fact that seahorses are weak swimmers that anchor themselves to vege-tation or the substrate with a strongly prehensile tail and rarely venture into open water to pursue mobileprey. In contrast, the relatively large P. taeniolatus, which resides above, rather than within, the macrophytecanopy, consumes mysids, which aggregate in open water above the seabed. Those pipefishes with char-acters that imply relatively enhanced mobility, such as well developed caudal fins and non-prehensile tails,are trophically diverse, suggesting that they are able to feed either on the sediment or phytal surfaces or inthe water column.

Introduction

Fishes of the family Syngnathidae are typicallysmall and cryptic and are usually associated withvegetated or other complex epibenthic habitats(Lourie et al. 1999, Kuiter 2000). These highlyspecialised fishes are characterised by limited

mobility due to the small size of their fins and theoccurrence on their bodies of semi-rigid dermalplates that restrict flexibility. Furthermore, somespecies, such as Hippocampus spp. and Stigmato-pora spp. do not possess caudal fins. Being inca-pable of rapidly pursuing or ‘lunging’ at prey,syngnathids utilise a ‘sit and wait’ or saltatory (i.e.

Environmental Biology of Fishes (2005) 72: 415–427 � Springer 2005

‘stop and go’) ambush foraging strategy (Howard& Koehn 1985, James & Heck 1994, Flynn & Ritz1999). Prey, which typically comprise small crus-taceans (Ryer & Orth 1987, Tipton & Bell 1988,Teixeira & Musick 1995), are then captured with arapid vertical ‘flick’ of the head that places themouth close to the target, while the buccal cavity issimultaneously expanded to create an inhalantcurrent (Bergert & Wainwright 1997). As syng-nathids have no teeth, these prey are swallowedintact. Unlike most other teleosts that employ jawprotrusion to assist the process of suction feeding(Muller & Osse 1984, Gerking 1994), the jaws ofsyngnathids are fused such that the small mouth islocated at the end of a tubular snout (Branch1966), the length of which varies markedlybetween species.It could be expected that a long snout would

increase both the distance from which a syngnat-hid can initiate an attack and the speed at which itsmouth prescribes an arc towards the prey, pro-vided that the inertial mass of the larger snout isminimised (Muller & Osse 1984, Flynn & Ritz1999). Hence, syngnathids with long snouts shouldbe able to attack prey from a greater distance andwith greater speed than those with short snoutsand, for this reason, could be expected to moresuccessfully catch relatively fast moving prey. Al-though this hypothesis has gained support fromdietary studies of some pipefish (Franzoi et al.1993, Campolmi et al. 1996), syngnathid speciesalso vary widely in size, body form (i.e. pipefish,pipehorse, seadragon or seahorse) and in thepresence or absence of fins (Dawson 1985, Lourieet al. 1999). The syngnathid body forms can bedistinguished primarily by the angle of the headrelative to the body. The most divergent forms arethe pipefish, in which the head is in line with thehorizontally orientated body, and the seahorses,among which the head is positioned approximatelyperpendicular to the vertically orientated body.Specialisations in the body shape and feedingstructure of teleosts can be related to the habitatsthat they occupy and the prey types that theyconsume (Keast & Webb 1966, Wainwright &Richard 1995, Fulton et al. 2001). Such factorscould therefore be expected to influence the loca-tions in which syngnathids forage and, hence, thelikelihood that they would encounter particularprey types. For instance, Howard & Koehn (1985)

suggested that relatively mobile pipefish species,which are characterised by well-formed fins andnon-prehensile tails, would be trophically diverseas they could forage on the sediment or in thephytal canopy. In contrast, those species with areduced or absent caudal fin and a prehensile tailwould attach themselves to vegetation and feedmostly on planktonic prey.

Our initial aim was to determine the diets of 12syngnathid species that vary widely in body form,size and snout morphology. Emphasis has beenplaced on testing the hypothesis that syngnathidswith long snouts would ingest higher volumes ofrelatively mobile prey. We then compared dietaryand morphological data to ascertain how varia-tions in body morphology, and hence mobility,might also contribute to differences in the foraginglocations and dietary compositions of these spe-cies.

Materials and methods

Study locality and sampling regime

We conducted the study in shallow marine watersadjacent to the Port of Fremantle in south-westernAustralia (32�3.2¢S, 115�44.0¢E), which supportextensive areas of the seagrasses Amphibolis grif-fithii, Posidonia sinuosa and Posidonia coriacea(Hyndes et al. 2003). Syngnathid fishes were col-lected during 1997 and 1998 in both the day andnight using large and small beam trawls. The smalltrawl was 1.0 m wide and 0.5 m high with 2.5 mmmesh in the body and 1.0 mm mesh in the cod-end,whereas the large trawl was 2.5 m wide and 1.5 mhigh with 25 mm mesh in the body and 10 mmmesh in the cod-end.

Biotic measurements and data analyses

As spotted pipefish Stigmatopora argus andwide-bodied pipefish Stigmatopora nigra wereabundant in the study area, at least 100 individualsof each of these species were randomly selectedfrom the trawl samples, along with all availableindividuals of 10 less abundant syngnathid species.Because of the rarity of some of these species, suchas tiger pipefish Filicampus tigris and smoothpipefish Lissocampus caudalis, fish that were

416

collected during both the day and night were usedin this study. Although syngnathids are visualfeeders (Howard & Koehn 1985, James & Heck1994) and could thus be expected to feed diur-nally, most fish that were collected at night inthis study were caught prior to midnight andtheir guts usually contained some intact preyitems. The standard length (SL) of all fish, ex-cept for Hippocampus spp. and Stigmatoporaspp. was measured to the nearest 1 mm. Theheight (HT), i.e. the vertical distance from thetip of the coronet to the tip of the tail (Lourieet al. 1999), of Hippocampus spp. and the snout-vent length (SVL) of Stigmatopora spp. wererecorded. As the tails of Stigmatopora spp. werefrequently mutilated, the linear relationship be-tween the SVL and SL of undamaged individualswas used to estimate the SL of damaged fish(Kendrick & Hyndes 2003).The anterior half of the undifferentiated ali-

mentary tract, which was designated as the gut(Ryer & Orth 1987), was dissected from each fishand stored in 70% ethanol. Guts were examinedunder a dissecting microscope. We recorded gutfullness on a scale of 0 (i.e. completely empty) to10 (i.e. fully distended) and identified dietaryitems to the lowest possible taxon before poolingthem into broader taxonomic groups to formdietary categories. The identification of gastro-pod egg capsules remains tentative (S. Slack-Smith, Western Australian Museum, pers.comm.). Calanoid and cyclopoid copepods andmysids, which inhabit the water column and re-main in constant motion (Ritz 2000), were des-ignated as relatively mobile prey, together withfish, decapod larvae and Lucifer sp. Less mobileprey categories were typically phytal and/orbenthic crawling grazers (e.g. gammarid and ca-prellid amphipods) (Barnes 1974, Main 1987,Ryer 1988, Klumpp et al. 1989, Jernakoff et al.1996), weakly or passively planktonic (e.g. indi-vidual eggs) or sedentary (e.g. bivalves and eggcapsules). Digested matter and unidentifiablecrustacean fragments were excluded from analy-ses, whereas non-dietary material (i.e. sedimentand vegetation fragments) was included in Ta-ble 1, but was excluded from analyses thereafter.The percent frequency of occurrence (%F ) ofeach dietary category and the relative contribu-tion of each category by volume (%V ) were

calculated for each species using the pointsmethod, which accounts for gut fullness (Hyslop1980). Volumetric data were used for subsequentanalyses, as this best represents the relative sig-nificance of each prey category (Platell et al.1998, Platell & Potter 1999).Data were square-root transformed and a simi-

larity matrix was constructed using the Bray–Curtissimilarity coefficient (Field et al. 1982, Clarke1993), and multivariate analyses were carried outusing PRIMER (Clarke & Warwick 1994). To en-sure parity of representation, analyses were under-taken on 20 randomly-selected samples from eachadequately abundant species (i.e. all except F. tigris,L. caudalis and western crested pipefish Mitotich-thys meraculus). Multidimensional scaling (MDS),multivariate dispersion (MVDISP) and one-wayanalysis of similarities (ANOSIM), applied to thesimilarity matrix, were used to compare dietarycompositions among syngnathid species. Due tomultiple pair-wise tests (n ¼ 36) for ANOSIM, sig-nificance levels were adjusted using the Bonferroniprocedure (Quinn & Keough 2002) to minimise thelikelihood of a Type I Error. The high sensitivity ofANOSIM means that pair-wise R-statistic values,which range from 0 (i.e. similarities within and be-tween species are the same) to 1 (i.e. replicateswithina species aremore similar to each other than those ofother species), additionally represent an importantcomparative tool (Clarke 1993, Hyndes et al. 1997).Dietary richness and evenness were measured

by the number of prey categories in each sampleand Simpson’s index of diversity (1)k), respec-tively. Simpson’s index, k ¼ Rpi

2 where pi is theproportion of prey category i in a gut sample,represents the probability that two randomlyselected units of volume would be from the sameprey category (Hayek & Buzas 1997). Headlength (HL) (i.e. the tip of the lower jaw to therear margin of the operculum) and snout length(SnL) (i.e. the tip of the lower jaw to the inneranterior margin of the bony orbit) were mea-sured to 0.1 mm on a sample of fish from eachspecies whose size range corresponded to thoseused for dietary analyses. Gape was designatedas the average of the height and width of thefully open mouth, while the ratio SnL/HL wasused to determine the proportion of the headlength of each species that was represented by itssnout.

417

Table

1.Frequency

ofoccurrence

(%F)andcontributionbyvolume(%

V)ofthedifferentmajortaxaanddietary

categories

tothecompositionoftheoveralldiets

of12

syngnathid

species.

Majortaxaand

dietary

categories

Phyllopteryx

taeniolatus

Vanacampus

poecilolaem

us

Stigmatopora

argus

Stigmatopora

nigra

Hippocampus

breviceps

Histiogamphelus

cristatus

%F

%V

%F

%V

%F

%V

%F

%V

%F

%V

%F

%V

Foraminiferans

3.5

<0.1

4.5

0.1

0.6

<0.1

23.9

1.0

6.9

<0.1

Polychaetes

1.5

0.4

Pycnogonids

4.5

0.6

1.7

0.3

Crustaceans

96.6

95.3

98.5

95.8

100

99.6

100

99.9

100

91.1

98.3

89.2

Cladocerans*

3.6

<0.1

1.4

<0.1

Calanoid

copepods*

10.3

0.8

4.5

0.3

99.4

68.0

100

69.5

10.5

0.6

5.2

3.9

Cyclopoid

copepods*

96.4

21.5

96.5

21.4

4.5

0.6

3.5

0.4

Harpacticoid

copepods

3.5

<0.1

10.5

3.5

88.5

8.0

84.7

6.7

52.2

7.5

20.7

1.2

Ostracods

3.5

0.1

1.5

<0.1

12.1

0.2

15.3

0.5

22.4

0.7

1.7

<0.1

Cumaceans

2.4

0.1

2.8

0.1

Tanaids

2.4

<0.1

3.0

1.5

Mysids*

89.7

80.8

88.1

67.8

2.4

<0.1

3.5

0.3

4.5

1.2

41.4

14.7

Isopodlarvae

28.5

0.1

16.7

0.1

Isopods

1.5

0.1

29.9

3.9

Valviferanisopods

5.2

0.6

Gammaridamphipods

3.5

<0.1

10.5

2.1

24.8

1.4

20.8

1.1

95.5

61.4

87.9

45.6

Caprellid

amphipods

0.7

<0.1

44.8

13.5

60.3

21.8

Decapodlarvae*

1.8

0.1

1.4

0.1

1.5

0.2

Lucifersp.*

13.8

5.8

1.8

0.1

0.7

<0.1

Caridshrimps

27.6

7.8

32.8

22.0

2.4

0.1

0.7

0.1

6.9

1.0

Crabs

Molluscs

6.1

6.9

25.4

2.3

3.5

1.3

Polyplacophorans

Gastropodeggcap.

14.9

1.1

Gastropods

2.4

<0.1

3.5

<0.1

6.0

1.2

3.5

1.3

Bivalves

3.6

<0.1

4.2

<0.1

4.5

<0.1

Chordates

6.9

0.7

Fish*

6.9

0.7

Other

1.5

0.4

12.7

0.3

0.7

1.5

Individualeggs

1.5

0.4

12.7

0.3

0.7

<0.1

Gelatinouseggmass

1.5

<0.1

Non-dietary

item

s51.7

4.0

26.9

3.6

4.8

22.9

0.1

41.8

4.5

75.9

9.1

Vegetation

6.9

2.0

6.0

1.2

2.4

<0.1

0.7

<0.1

17.9

1.6

15.5

1.4

Sedim

ent

44.8

2.0

22.4

2.4

2.4

<0.1

22.2

0.1

31.3

2.9

72.4

7.7

Number

ofguts

33

86

165

144

82

69

%containingitem

s87.9

(29)

77.9

(67)

100(165)

100(144)

81.7

(67)

84.1

(58)

418

Foraminiferans

23.1

0.4

20.5

0.3

18.2

<0.1

10.0

<0.1

Polychaetes

3.9

1.7

2.6

0.4

Pycnogonids

Crustaceans

100

79.0

97.4

91.3

100

92.0

100

91.1

100

97.0

100

92.9

Cladocerans*

Calanoid

copepods*

7.7

0.3

25.6

2.3

75.0

13.1

Cyclopoid

copepods*

19.2

1.8

12.8

0.2

Harpacticoid

copepods

69.2

12.5

92.3

25.3

4.5

<0.1

87.5

47.1

10.0

0.1

Ostracods

19.2

0.5

25.6

1.0

75.0

1.5

10.0

0.1

Cumaceans

Tanaids

3.9

0.6

15.4

2.7

Mysids*

26.9

7.3

10.3

2.8

40.9

20.6

100

80.0

70.0

5.4

Isopodlarvae

2.6

<0.1

Isopods

30.8

3.0

20.5

2.6

Valviferanisopods

Gammaridamphipods

100

45.2

79.5

41.9

72.7

27.5

37.5

7.6

87.5

35.3

100

68.2

Caprellid

amphipods

19.2

3.0

38.5

9.2

36.4

13.6

6.3

3.5

70.0

14.3

Decapodlarvae*

3.9

2.5

Lucifersp.*

Caridshrimps

3.9

2.3

15.4

2.9

45.5

25.8

20.0

4.4

Crabs

2.6

0.4

13.6

4.5

10.0

0.4

Molluscs

7.7

2.2

33.3

2.1

27.3

0.9

12.5

0.4

Polyplacophorans

2.6

0.3

Gastropodeggcap.

7.7

2.0

28.2

1.7

Gastropods

18.2

0.9

12.5

0.4

Bivalves

3.9

0.2

2.6

0.1

9.1

<0.1

Chordates

Fish*

Other In

dividualeggs

Gelatinouseggmass

Non-dietary

item

s84.6

16.7

71.8

5.9

54.5

7.1

62.5

8.9

25.0

2.6

90.0

7.1

Vegetation

38.5

5.2

12.8

0.3

31.8

2.7

20.0

1.4

Sedim

ent

73.1

11.5

69.2

5.6

36.4

4.4

62.5

8.9

25.0

2.6

80.0

5.7

Number

ofguts

32

46

27

19

812

%containingitem

s81.3

(26)

84.8

(39)

81.5

(22)

84.2

(16)

100(8)

83.3

(10)

*–Relativelymobileprey.

419

Results

Dietary compositions

Small crustaceans dominated the diets of all 12syngnathid species (Table 1). ANOSIM of data re-presenting the dietary samples for nine of thesespecies showed that there was a significant differ-ence in the dietary composition among species(P<0.001, Global R = 0.651). Samples from S.argus and S. nigra formed a discrete group on theright of the MDS plot (Figure 1, group A) and ex-hibited low levels of dispersion (i.e. 0.61 and 0.66,respectively). Pair-wise tests indicated that, whilethe dietary compositions ofS. argus andS. nigra didnot differ significantly from each other, they diddiffer from those of all other species (Table 2). Theunique compositions of the diets of these species isemphasised by the consistently high R-statisticvalues associated with pair-wise comparisons of

S. argus and S. nigra and all other species (i.e.‡0.86). The diets of these two species similarlycomprised ca. 70%calanoid, ca. 21%cyclopoid andca. 7% harpacticoid copepods (Table 1). The twoformer prey types were present in 96–100%of theS.argus and S. nigra guts, while the latter prey typeoccurred in 85–89% of the samples. The guts ofthese species contained little non-dietarymaterial inthe form of vegetation or sediment.The dietary samples of the common seadragon

Phyllopteryx taeniolatus and long-snouted pipe-fish Vanacampus poecilolaemus formed a mostlydiscrete group at the bottom of the MDS plotand also exhibited relatively low levels of dis-persion (i.e. 0.82 and 0.63, respectively) (Fig-ure 1, group b). ANOSIM showed that, whilethe dietary compositions of these species werenot significantly different from each other, theydiffered significantly from each of the otherseven species (Table 2). The diets of P. taeniol-atus and V. poecilolaemus comprised ca. 80 and68% mysids, respectively, and these preyoccurred in >88% of these samples (Table 1).Although carid shrimps and Lucifer sp. alsocontributed >5% to the dietary volumes of thesespecies, the %F of these prey did not exceed33%. Non-dietary items, comprising vegetationfragments and sediment, never exceeded 4% ofthe gut volumes of these species.Among the remaining species, ANOSIM

showed that the diets of the short-snouted sea-horse Hippocampus breviceps, Macleay’s crestedpipefish Histiogamphelus cristatus and the PortPhillip pipefish Vanacampus phillipi were not sig-nificantly different (Table 2). While the dietarycompositions of the West Australian seahorseHippocampus subelongatus and H. cristatus did notdiffer significantly, low R-statistic values indicatethat differences between the diets of the formerspecies and H. breviceps (R ¼ 0.307) and V. phillipi(R ¼ 0.294) were not great. Similarly, the diets ofthe pug-nosed pipefish Pugnaso curtirostris andV. phillipi were not significantly different, whiledifferences in the diet of the former species andH. cristatus (R ¼ 0.203) and, especially, H. brevi-ceps (R ¼ 0.147) were small. The diets of H. su-belongatus and P. curtirostris were the mostdissimilar (R ¼ 0.440) of these five species, amongwhich dispersion ranged from 1.10 (H. cristatus) to1.51 (H. subelongatus) (Figure 1). Gammarid

Figure 1. Two dimensional MDS ordination plot and disper-

sion determined using volumetric dietary data from each of nine

syngnathid species (n ¼ 20). Group A represents most samples

from Stigmatopora argus and Stigmatopora nigra, while group

B represents samples from Phyllopteryx taeniolatus and Vana-

campus poecilolaemus.

420

amphipods were the main prey of all these species,contributing 28–61% to their dietary volumes andoccurring in ‡73% of the guts (Table 1). Otherprey categories that contributed >5% to the dietsof these species were harpacticoid copepods,mysids, caprellid amphipods and carid shrimps,while the contribution of non-dietary items, com-prising vegetation fragments and sediment, rangedfrom 4.5 (H. breviceps) to 16.7% (V. phillipi).Data for the three least abundant species (M.

meraculus, L. caudalis and F. tigris) were not in-cluded in multivariate analyses due to sample sizesof fish containing prey being <17. Like the dietsof P. taeniolatus and V. poecilolaemus, that of M.meraculus was dominated by mysids, in terms ofboth frequency of occurrence and volume (Ta-ble 1). In comparison, L. caudalis consumed highvolumes of harpacticoid copepods and gammaridamphipods, while the diet of F. tigris was domi-nated by gammarid and caprellid amphipods.

Dietary breadths

Mitotichthys meraculus, P. taeniolatus and V. poe-cilolaemus exhibited similar dietary richness andeveness (i.e. 1.4–1.6 and 0.14–0.15, respectively),which were notably lower than those of all otherspecies (Figure 2). Among the other syngnathid

Table

2.R-statistic

values

andsignificance

forpair-w

isecomparisonsusingAnalysisofSim

ilarity

(ANOSIM

)ofdietary

compositionsofninerelativelyabundantsyngnathid

species.

P.taeniolatus

V.poecilolaem

us

S.argus

S.nigra

H.breviceps

H.cristatus

V.phillipi

P.curtirostris

V.poecilolaem

us

0.000ns

S.argus

0.897*

0.950*

S.nigra

0.899*

0.950*

0.050ns

H.breviceps

0.874*

0.907*

0.958*

0.955*

H.cristatus

0.667*

0.349*

0.961*

0.957*

0.083ns

V.phillipi

0.808*

0.835*

0.956*

0.951*

0.005ns

0.072ns

P.curtirostris

0.858*

0.884*

0.869*

0.862*

0.147*

0.203*

0.043ns

H.subelongatus

0.431*

0.457*

0.864*

0.860*

0.307*

0.171ns

0.294*

0.440*

Significance

acceptedatp<

0.0014[ns–notsignificant.

*–significant].

Figure 2. Mean dietary richness (+1 se) and evenness (+1 se)

of 12 syngnathid species with sample sizes above the columns.

421

species, dietary richness ranged from 2.1 (H. sube-longatus) to 3.8 (P. curtirostris), while the evenessranged from 0.35 (H. subelongatus) to 0.47 (P.curtirostris).

Snout length as a proportion of head length and thedietary content of relatively mobile prey

The mean snout length as a proportion of headlength of M. meraculus, P. taeniolatus, S.argus, S.nigra andV. poecilolaemus ranged from 0.53 to 0.70and the diets of these species all comprised >70%relatively mobile prey (Figure 3). The diets of theremaining seven species, among which snout lengthas a proportion of head length ranged from 0.34 (L.caudalis) to 0.53 (H. subelongatus), each containedvolumes of £20% of relatively mobile prey.

Mean gape, size range and body morphology

The mean gape sizes of the 12 syngnathid speciesranged from 0.5 (S. nigra) to 1.8 mm (P. taeniolatus)(Table 3). Phyllopteryx taeniolatus and F. tigris,

which both attained lengths of ‡300 mm SL, werethe largest syngnathids, while H. breviceps and L.caudalis (ca. 80–90 mmSLorHT)were the smallest.Nine species conformed to the elongate pipefishbody form, while H. breviceps and H. subelongatuswere seahorses and P. taeniolatus was the only sea-dragon. Of the five species that lacked caudal fins(i.e.H. breviceps,H. subelongatus, P. taeniolatus, S.argus andS. nigra) onlyP. taeniolatus did not have aprehensile tail, while among the pipefishwith caudalfins, only L. caudalis possessed a prehensile tail(Gomon et al. 1994, Lourie et al. 1999, Kuiter2000).

Discussion

All of the syngnathid species that we examined inthis study fed mainly on small crustaceans, whichconcurs with the compositions of diets of thisfamily in other studies (Brook 1977, Livingston1982, Bell & Harmelin-Vivien 1983, Huh & Kitting1985, Ryer & Orth 1987, Tipton & Bell 1988,Bennet & Branch 1990, Franzoi et al. 1993, Mottaet al. 1995, Teixeira & Musick 1995, Woods 2002).Syngnathids in general exhibit a high degree oftrophic specialisation compared to many otherepibenthic or demersal marine teleosts (e.g. Hyn-des et al. 1997, Platell et al. 1998, Platell & Potter1999). However, we have demonstrated that a highdegree of trophic specialisation also occursbetween different syngnathid species, and it isprobable that these differences can be explained, atleast in part, by differences in their snout mor-phologies and feeding behaviours. Those syng-nathids that consume mainly relatively mobileprey, which undergo rapid and constant motion,are characterised by long snouts. The mysidParamesopodopsis rufa, for example, swims atspeeds of 26 mm s)1, while calanoid copepodsgenerally move at up to 20 mm s)1, but may ex-ceed 50 mm s)1 (Mauchline 1998, Ritz 2000). Incontrast, syngnathid species that feed on relativelyslow moving prey possess short snouts. Whilethese slower prey, including harpacticoid copepodsand gammarid amphipods, are capable of rapidescape behaviour (Singarajah 1969, Main 1987,Mauchline 1980, 1998, Titleman 2001), theimmobile or saltatory foraging behaviour ofsyngnathids would enable them to ambush prey

Figure 3. Mean dietary volume of relatively mobile prey

(±1se) in the diets of 12 syngnathid species of varying snout

length as a proportion of head length (±1 se).

422

while minimizing the chances of eliciting this re-sponse (Ritz et al. 1997). Thus, these prey wouldbe captured as they ‘crawl’ or ‘walk’ on the sedi-ment and/or phytal surfaces (Hicks & Coull 1983,

Main 1987, Ryer 1988). These conclusions aresupported by previously published syngnathiddiets, although comparisons are constrained bydifferences in dietary analyses. Species with long

Table 3. Mean gape (±1 se) and sample size of 12 syngnathid species ranked by their maximum standard length (SL) or height (HT).

The body form and presence or absence of a caudal fin and prehensile tail are also provided for each species.

Species Mean gape Size range Body Caudal Prehensile

±1 se (mm) (SL or HT*) (mm) form fin tail

Filicampus tigris 1.5 ± 0.0 (12) 259–333 pipefish yes no

Phyllopteryx taeniolatus 1.8 ± 0.2 (16) 87–300 seadragon no no

Stigmatopora argus 0.6 ± 0.1 (31) 35–278 pipefish no yes

Mitotichthys meraculus 1.1 ± 0.1 (15) 96–269 pipefish yes no

Vanacampus poecilolaemus 1.1 ± 0.1 (28) 36–260 pipefish yes no

Histiogamphelus cristatus 1.2 ± 0.1 (21) 19–209 pipefish yes no

Hippocampus subelongatus 1.7 ± 0.1 (18) 46–180* seahorse no yes

Pugnaso curtirostris 0.9 ± 0.1 (17) 31–168 pipefish yes no

Vanacampus phillipi 0.8 ± 0.1 (16) 36–165 pipefish yes no

Stigmatopora nigra 0.5 ± 0.1 (16) 36–143 pipefish no yes

Lissocampus caudalis 0.6 ± 0.0 (8) 56–89 pipefish yes yes

Hippocampus breviceps 0.9 ± 0.1 (13) 34–79* seahorse no yes

Table 4. The body form, snout length as a proportion of head length and major prey for each of 14 syngnathid species.

Species Body form Mean and range of snout length as

proportion of head length

Major prey

Syngnathus typhle pipefish 0.63 (0.53–0.71)9,12 mysids, fish1,6

Syngnathus louisianae pipefish (0.56–0.67)4 shrimp, mysids, amphipods4

Syngnathus taenionotus pipefish 0.59 (0.56–0.63)9,12 mysids, decapod zoae, calanoid

copepods8

Mitotichthys semistriatus pipefish (0.53–0.63)7 calanoid copepods, gammarid am-

phipods10

Syngnathus floridae pipefish (0.53–0.63)4 shrimp, mysids, amphipods3,4,13,17

Syngnathus acus pipefish 0.55 (0.43–0.59)7,12 carid shrimp, amphipods, isopods,

copepods1,2

Syngnathus fuscus pipefish 0.48 (0.42–0.59)12 gammarid and caprellid amphipods,

isopods, calanoid copepods16,17

Syngnathus scovelli pipefish (0.40–0.59)4 amphipods3,4,11,15

Syngnathus abaster pipefish 0.45 (0.40–0.53)9,12 harpacticoid copepods, amphipods,

polychaetes6,8

Hippocampus whitei seahorse 0.44 (0.37–0.50)14 amphipods5

Hippocampus abdominalis seahorse 0.38 (0.31–0.45)14 carid shrimps, amphipods, mysids19

Micrognathus crinigerus pipefish (0.30–0.44)4 amphipods, copepods4

Urocampus carinirostris pipefish (0.28–0.36)7 calanoid, cyclopoid, harpacticoid

copepods10

Hippocampus zosterae seahorse (0.23–0.24)14 harpacticoid copepods18

1–Bell & Harmelin–Vivien (1983); 2–Bennet & Branch (1990); 3–Brook (1977); 4–Brown, (1972); A comparative life history study

of four species of pipefishes (Family Syngnathidae) in Florida. PhD thesis, The University of Florida, Florida. 5–Burchmore et al.

(1984); 6–Campolmi et al. (1996); 7–Dawson (1985); 8–Franzoi et al. (1993); 9–Piero Franzoi, pers. comm; 10–Howard & Koehn

(1985); 11–Huh & Kitting (1985); 12–Sara LeCroy, pers. comm; 13–Livingston (1982); 14–Lourie et al. (1999); 15–Motta et al.

(1995); 16–Ryer & Orth (1987); 17–Teixeira & Musick (1995); 18–Tipton & Bell (1988); 19–Woods (2002).

423

snouts (ca. >0.5 of the head length) tend to con-sume relatively mobile prey, while species withshort snouts feed more commonly on less mobileprey, such as amphipods, harpacticoid copepodsand polychaetes (Table 4).Among those syngnathids with long snouts that

fed on relatively mobile prey, the consumptionprimarily of mysids by M. meraculus, P. taeniola-tus and V. poecilolaemus and copepods by S. argusand S. nigra probably reflects differences in theirgapes, which ranged from 1.1–1.8 and 0.5–0.6 mm,respectively. The mysids ingested by the formerspecies were up to 12 mm long and 1 mm wide,whereas the copepod prey of the latter two speciesdid not exceed 1.0 and 0.4 mm in length and width(A. Kendrick, unpublished data). Thus, S. argusand S. nigra would only be able to ingest thesmallest mysids. That the former and larger threespecies consume very few calanoid or cyclopoidcopepods is likely to reflect the energetic ineffi-ciency of capturing numerous small prey (Werner& Hall 1974).Differences in snout length and gape do not fully

explain the variability in the diets of the 12 syng-nathid species that we studied. The body form ofspecies (i.e. seahorse, pipehorse, seadragon orpipefish) and the presence or absence of fins willalso influence where syngnathids forage and,hence, their likelihood of encountering andingesting certain prey types. It is notable that theseahorse H. subelongatus consumed little relativelymobile prey despite having a very similar snoutlength to the pipefish M. meraculus, which fed al-most exclusively on mysids. We suggest that therelatively restricted swimming ability of seahorsesalso influences their diet. With swimming capa-bilities more suited to maneuverability than speed,and with a strongly prehensile tail (Hale 1996,Consi et al. 2001), the seahorse body form isadapted to inhabiting relatively complex habitatsand these fishes rarely venture into open waterwhen feeding (Flynn & Ritz 1999). Hence, theconsumption of epibenthic prey by H. subelonga-tus is likely to reflect such sedentary behaviour,despite this relatively large seahorse possessing amoderately long snout and a relatively large gape.Supporting this assertion, the smaller H. brevicepsingested minor volumes of prey (e.g. egg massesand capsules) that would have been plucked di-rectly from seagrass leaves and/or the sediment.

Similarly, the seahorses Hippocampus whitei,Hippocampus zosterae and Hippocampus abdomi-nalis consume mainly epibenthic invertebrates(Burchmore et al. 1984, Tipton & Bell 1988,Woods 2002).Differing markedly in body form from seahorses

and pipefish, the seadragon P. taeniolatus wasamong the largest syngnathids examined in thisstudy.While this species lacks a caudal fin, the tail isnot prehensile. Instead the complex dermalappendages of this species, and the leafy seadragonPhycodurus eques, mimic drifting algae, which al-lows them to cryptically reside above, rather thanwithin, themacrophyte canopy (Gomon et al. 1994,Groves 1998, Kuiter 2000). This enables P. taeni-olatus to occupy a different foraging habitat tomany other syngnathids and places it in the prox-imity of prey, such asmysids, that aggregate in openwater above the seabed (Mauchline 1980, Flynn &Ritz 1999).All other species examined in this study con-

formed to the very elongate pipefish body form,which can be separated into those with reduced orabsent caudal fins and weakly prehensile tails (i.e.L. caudalis, S. argus and S. nigra) and those withwell developed caudal fins and non-prehensile tails(i.e. F. tigris, H. cristatus, M. meraculus, P. curti-rostris, V. phillipi and V. poecilolaemus). Thecharacters of the former group imply relativelyimmobile foraging habits compared to the greatermobility of the latter group (Howard & Koehn1985). We suggest that the focus on planktoniccopepods by both S. argus and S. nigra reflectstheir ability to grasp leaves in the seagrass canopywith their tails, a conclusion that is supported byother studies (Burchmore et al. 1984, Howard &Koehn 1985, Steffe et al. 1989, Edgar & Shaw1995, Jenkins & Sutherland 1997). Lissocampuscaudalis also grasps vegetation with its tail (Go-mon et al. 1994, Kuiter 2000) and has a similargape to S. argus and S. nigra, but has a relativelyshort snout. Although sample sizes were small, webelieve that the short snout of L. caudalis influ-ences its consumption of mostly slower-moving,small epibenthic prey.The major prey of pipefish with well developed

caudal fins were either gammarid amphipods (i.e.F. tigris, H. cristatus, P. curtirostris and V. philli-pi) or mysids (i.e. M. meraculus and V. poecilo-laemus). The additional ingestion of harpacticoid

424

copepods and caprellid amphipods by the formerfour species, together with the consistent presencein their guts of sediment, suggests that they foragemainly on the sediment and phytal surfaces. Sim-ilarly, Edgar & Shaw (1995) found that V. phillipiate mainly benthic crustaceans, while Howard &Koehn (1985) noted that this species lay horizon-tally on the sediment of aquaria in preference toinhabiting the vegetative canopy. In contrast, M.meraculus forages on mysids in open water abovethe substrate, where, as noted above, these preyaggregate. We suggest that M. meraculus orien-tates within the phytal canopy like its morpho-logically similar congener M. semistriatus andswims clear of the vegetation when pursuing prey(Howard & Koehn 1985). While also mainlyingesting mysids, V. poecilolaemus frequently alsoconsumed carid shrimps that live on the sedimentand leaves (Edgar 2000) within the dense P. sinu-osa meadows that this species mainly inhabits inthe study area (Kendrick & Hyndes 2003). Al-though the dark brown colour of this pipefishwould enable it to be camouflaged among thedetritus beneath the seagrass canopy, it must alsocommonly move out of the seagrass canopy tocapture mysids.We conclude that the diets of syngnathid fishes

are related to factors that influence both theirforaging capabilities (e.g. snout length and gapesize) and/or locations (e.g. body form and mobil-ity). Although previous studies have highlightedthese factors individually (Howard & Koehn 1985,Franzoi et al. 1993, Campolmi et al. 1996), wehave shown that these factors should not be con-sidered in isolation with regard to syngnathidtrophic ecology. This result also agrees withbroader studies that have associated patterns ofteleost dietary composition with functional mor-phology (Wainwright 1988, Wainwright & Rich-ard 1995), although few have examined theserelationships within such highly specialised groupsof fishes (Ferry-Graham et al. 2001).

Acknowledgements

Thanks are extended to Steve Letch and the crewof Maritime Image, and to Lachlan MacArthurand Emily Stewart for their help in the field. AnneBrearley, George Kendrick, Margaret Platell and

Shirley Slack-Smith kindly identified dietarymaterial. Unpublished morphological data forsome syngnathid species were generously providedby Sara LeCroy and Piero Franzoi, who, togetherwith Ian Potter and Margaret Platell providedhelpful discussion and comment on the manu-script. Statistical advice provided by Bob Clarke isgreatly appreciated. This work was carried outwhile the senior author was the recipient of aMurdoch University Research Scholarship.Funding was provided by Cockburn Cement Ltdand the Natural Heritage Trust.

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