AMER. ZOOL., 23:411-425 (1983)
Feeding Strategies in Marine Snakes: An Analysis of
Evolutionary, Morphological, Behavioral and
Ecological Relationships1
HAROLD K. VORIS 2 AND HELEN H. VORIS
Division of Amphibians and Reptiles, Field Museum of Natural History,
Roosevelt Road and Lake Shore Drive, Chicago, Illinois 60605
SYNOPSIS. Analysis of 1,063 stomach contents from 39 species of sea snakes indicates
that about one-third of the shallow, warm, marine, Indo-Australian fish families are preyed
upon by sea snakes. Families of eels and gobies are taken by the greatest numbers of snake
species. Most species of sea snakes feed on fish families whose members are relatively
sedentary, dwelling along the bottom, within burrows or reef crevices. With one exception,
a fish egg-eating specialization found uniquely in the Aipysurus-Emydocephalus lineage, the
dietary habits of sea snakes cannot be categorized according to the snakes' three phylogenetic lineages. Eels, mullet-like, rabbitfish-like and goby-like fish forms are taken by all
three lineages. Two or three snake species are generalists, and numerous ones specialize
on eels, goby-like fish or catfish. There are differences among sea snake species in the
relationship between snake neck girth and the maximum diameter of the prey; in the
relationships of both snake gape measurements and fang length, to the type of prey taken;
and in the relationship of snake shape and body proportions to the prey selected. Several
modes of feeding have been observed among sea snakes: feeding in nooks and crannies
in the bottom or in reefs, cruising near the bottom, and feeding in drift lines. Analysis
of percent digestion of stomach contents and projections backward to the times of prey
capture provides evidence for feeding periodicity. The greatest amount of diet overlap
is for two species of sea snakes which do not both occur at the same locality. Where species
do co-occur, diet overlap index values are lower. The numbers of species present as well
as their relative abundances vary among localities as does the relative importance of
generalists, eel-eaters, egg-eaters and other specialized feeders.
can be incorporated into studies on feedThe purpose of this report on sea snake ing, in order to approach broader quesfeeding is twofold: to review and synthesize tions. For example, with appropriate field
the published data on sea snake diets; and data we can begin to understand not only
to present an analysis of existing diet data, what sea snakes prey on, but how often,
focusing on the interrelationships of mor- and under what conditions. Integrating this
phology, behavior and ecology of sea snakes information with data on functional morphology and behavior, we can begin to
and their prey.
With the exception of a few species, our understand competition and mechanisms
knowledge of sea snake diets is generally of resource partitioning, and we can begin
sketchy and often limited to identification to bring to bear theoretical constructs such
of prey items. While more basic diet data as the optimal foraging theory (Schoener,
are needed, particularly for species for 1971) on our understanding of how sea
which little is known of dietary habits, one snakes have evolved and are adapted to
goal of the subsequent analyses is to gen- their present environment.
erate awareness of how other types of data
INTRODUCTION
SEA SNAKE DIET DATA
A summary of the existing records of
identifiable
stomach contents for 39 species
1
From the Symposium on Adaptive Radiation Within
is presented in Appendix A.
of
sea
snakes
a Highly Specialized System' The Diversity of Feeding Mechanisms of Snakes presented at the Annual Meeting of The 1,063 stomach contents represent at
the American Society of Zoologists, 27-30 December least 56 fish families as well as several other
1981, at Dallas, Texas.
kinds of items. These data were derived
2
Temporary Address: Systematic Biology Pro- from: Denburgh and Thompson, 1908;
gram, Division of Environmental Biology, National
Science Foundation, 1800 G Street, N.W., Washing- Wall, 1921; Smith, 1926, 1935; Volsae,
1939; Klawe, 1964; Minton, 1966; Visser,
ton, D.C. 20550.
411
412
HAROLD K. VORIS AND HELEN H. VORIS
1967; Voris, 1972; McDowell, 1974; Kropach, 1975; Limpus, 1975; McCosker,
1975; Pernetta, 1977; Glodek and Voris,
1982; and Voris, unpublished data. Generally only one identifiable stomach content was observed per snake specimen, with
Pelamis platurus being the notable exception. Klawe (1964) reported 137 stomach
contents from 22 P. platurus specimens, and
Kropach (1975) reported that small fish
were found "in large numbers" within large
Pelamis. Also several Emydocephalus annulatus and E. ijimae were found with stomachs very full offish eggs, suggesting visits
to several nests (Voris, 1966).
Stomach content identifications were as
precise as their conditions would allow.
Sometimes species identifications were
possible, or distinct types within a family
or genus could be distinguished even if
species names could not be applied. Stomach content data were included in the subsequent analysis if they were identified to
at least family. Those with more precise
identifications were used as a guide for the
assignment of prey families into categories
described later. This approach maximized
the size of the data set without sacrificing
a meaningful level of analysis.
In the shallow, warm Indo-Australian
waters forming the center of sea snake
species distribution, there are approximately 160 families offish (Springer, personal communication, 1981). The number
of stomach contents recorded for each of
the 56 fish families that sea snakes have
been documented to eat, is given in Appendix B. In descending order, the number of
sea snake species preying on each family
(some species prey on more than one family) is given below:
Gobiidae (9), Moringuidae (8), Ophichthidae (8), Congridae (6), Clupeidae (5),
Muraenidae (5), Plotosidae (5), Trypauchenidae (5), Engraulidae (4), Gobioididae
(4), Labridae (4), Acanthuridae (3), Carangidae (3), Eleotridae (3), Lutjanidae (3),
Pomacentridae (3), Tetraodontidae (3),
Xenocongridae (3), Apogonidae (2), Ariidae (2), Atherinidae (2), Blenniidae (2),
Callionymidae (2), Fistulariidae (2), Leiognathidae (2), Mugilidae (2), Polynemidae
(2), Scaridae (2), Scorpaenidae (2), Sciaen-
idae (2), Serranidae (2) and Synodontidae
(2). The remaining 24 fish families listed
in Appendix B are each taken by one sea
snake species; in addition five snake species
eat fish eggs and four also take other items
such as invertebrates. Clearly, the families
of gobies (Gobiidae) and eels (Moringuidae, Ophichthidae, Congridae and
Muraenidae) play a central role in sea snake
diets.
Although there are probably more than
56 fish families preyed upon by sea snakes,
it is possible to begin to understand the
relationships among sea snakes and their
prey by examining this particular subset of
fish in more detail with an emphasis on
those aspects which seem most likely to be
important to ophidian predators.
PREY CHARACTERISTICS
Because sea snakes, like other snakes,
swallow their prey whole,fishsize and shape
are likely to be important. Using the specific items eaten within each fish family as
a guide, and information about fish families provided by Nelson (1976) and Herald
(1961), the fish families and other items
eaten by sea snakes have each been assigned
to one of 12 body form categories depicted
in Figure 1. There is a progression toward
increasing diameter and decreasing length
from body forms one to four; and an
increase in the degree of lateral or vertical
flattening proceeding from form five to
form eight. Forms nine and ten are each
characterized by distinctive features which
alter their effective body forms, such as the
ability to inflate, or the presence of spines,
respectively. Fish eggs, a diet item distinct
from other prey forms is designated as form
11, and the occasional invertebrates taken
by sea snakes are grouped in category 12.
The body form category for each fish family is given in Appendix B. The number of
sea snake species feeding on each type of
body form, as well as the number of fish
families in each form category are presented in Figure 2. In close parallel with
the results of the previous analysis according to fish family, eels and goby-like fish
are taken by the greatest numbers of sea
snake species, followed by mullet-like and
awl-like fish.
413
MARINE SNAKE DIET ANALYSIS
0
1.
3.
C
EELS
5.
MULLET-LIKE
9.
6.
RABBITFISH-LIKE
10.
SPINOUS
11.
FISH EGGS
12.
INVERTEBRATES
AWL-LIKE
7.
4.
PUFFER-LIKE
SURGEONFISH-LIKE
GOBY-LIKE
8.
FLATFISH
FIG. 1. The twelve prey body form categories used in this study. Line drawings of fishes are adapted from
Nelson (1976).
Although many aspects of fish behavior
undoubtedly affect predator-prey interactions, the differential mobility of snakes and
fish in the aquatic medium is clearly important. A behavioral distinction related to this
can be made between those fish which are
generally free-swimming (pelagic) and
those which are more benthic and usually
sit or hover. The designation for each fish
family as consisting of fish that are primarily "sitters" or "swimmers" was reached
by consulting literature sources (Nelson,
1976 and Herald, 1961), and is given in
Appendix B. A comparison of the number
of fish families in each category with the
number of sea snake species feeding in each,
reveals that although only 20 fish families
were considered predominantly "sitters,"
they were fed on by 34 species of sea snakes.
Although 36 fish families were considered
"swimmers," only 14 sea snake species
preyed on them.
Closely related to these behavior categories are the habitats in which they occur.
Six habitats have been defined. These are
depicted in Figure 3, together with the
number of fish families occurring in each
and the number of sea snake species feeding on them. The habitat classifications for
each of the 56 fish families fed on by sea
snakes are given in Appendix B.
Examination of the habitat categories
suggests certain relationships among them.
Habitat one, burrows in the bottom, is most
closely related to habitat two, nooks, crannies or crevices in a reef. Habitats three
and four are adjacent to habitats one and
two respectively, that is, near the bottom
and near the reef surface. Habitats five and
six are both open water environments, with
the distinction that habitat six is near the
surface, e.g., in drift lines.
Habitats three, four and five contain the
greatest numbers of fish families, 18, 10
and 12 respectively, totalling 40 out of 56
fish families (Fig. 3). However, the greatest
numbers of sea snake species feed on families in habitats one, two and three, sug-
414
HAROLD K. VORIS AND HELEN H. VORIS
c/)
LLJ
o
1X1
Q_
CO
LU
CO
LU
CD
5 -
4
5
6
7
8
9
FISH SHAPE CATEGORIES
10
11
12
Fie. 2. The number of sea snake species feeding on fish belonging to families assigned to each body form
category. The number of fish families assigned to each category is given within each bar. The total number
offish families preyed on by sea snakes was 56.
gesting that prey living in burrows, crevices or along the bottom are particularly
important in the diet of sea snakes.
Another prey characteristic, the degree
of scalation, is probably important with
respect to the ability of the fang to penetrate the surface of the prey. However since
a range of scalation conditions often existed
within a fish family, it was not informative
to examine the distribution of sea snake
species feeding on prey with different
degrees of scalation at the family level.
The fish characteristics described above,
body form, behavior, habitat and scalation,
are clearly not independent of one another.
Burrowing types and bottom dwellers, for
example, tend to be elongated and naked,
or have very fine scales. They are found in
habitats one and two, where they sit or
hover in the proximity of burrows or crevices. The relationships among fish characteristics are given in the upper portion
of Figure 4. In the subsequent discussion
that addresses the relationships between
snake characteristics and primarily fish
body forms, the body form has been used
as in index to the set of characteristics associated with each, as given in Figure 4.
SEA SNAKE DIET IN A PHYLOGENETIC
CONTEXT
A phytogeny of the sea snakes has been
presented elsewhere (Voris, 1977). That
study and others (McDowell, 1972) indicate that three groups of sea snakes have
had independent origins among the Flap-
415
MARINE SNAKE DIET ANALYSIS
HABITATS
SEA SNAKE
SPECIES FEEDING
EC
LU
00
HABITAT 1 HABITAT 2 HABITAT 3 HABITAT 4
HABITAT 5 HABITAT 6
FIG. 3. The number offish families assigned to each of six habitat categories (see inset) and the number of
sea snake species feeding on fish belonging to families assigned to each habitat.
idae. These three lineages are depicted in
the vertical axis of Figure 4, omitting those
species for which there are fewer than five
identifiable stomach contents. The numbers and proportion of stomach contents
in each body form category are presented
for each of the 22 sea snake species in the
body of the figure.
It may be seen that with only a few exceptions, sea snake prey are not partitioned
according to the snake lineages. For example, eels are taken by all three lineages, and
are a primary food source for species in
two of the lineages, Laticauda colubrina in
species in two of the lineages. Within the
Aipysurus and Emydocephalus lineage, there
is a unique feeding specialization on fish
eggsIt is also apparent from Figure 4, that
many marine snakes tend to be specialists.
The egg-eating and eel-eating specialists
have already been mentioned. For some
sea snake species the degree of specialization is extreme; they eat only a few species
within one or two families (Glodek and
Voris, 1982). Not only are the goby-like
fishes eaten by at least 1 1 sea snake species,
there are three species, Ephalophis greyi,
one, and Microcephalophisgracilis, Hydrophis
melanosoma, H. melanocephalus, H. fascialus
Thallasophina viperina and Astrotia stokesii
which might be specializing on them,
and H. brookii in another. Mullet-like fish although more data are needed to docu(form five) and rabbitfish-like prey (form ment this. Large numbers of stomach consix) are also taken by species in all three tent records for Enhsdrina schislosa clearly
lineages. Along with the goby-like fish, they indicate that it specializes on sea catfish.
provide a significant portion of the diet for
There are a few species that tend to be
416
HAROLD K. VORIS AND HELEN H. VORIS
0-20%
21-40%
_
417
MARINE SNAKE DIET ANALYSIS
generalists. Lapemis hardwickii is the best
example, taking a total of 31 fish families
(Appendix A) from all body form categories except one. Aipysurus laei'is, another
generalist, takes 12 fish families, fish eggs
and invertebrates, a total of five body forms
of prey. Pelamis platurus also appears to be
a generalist, eating 21 fish families from
six body form categories. However, feeding in the drift lines as it does, it encounters
primarily the larval forms of 18 of the 21
families it has been reported to eat (Tyler,
Johnson, personal communication, 1981)
suggesting that it is specializing to some
degree on an age or size class rather than
being a true generalist. Standard length
measurements of P. platurus stomach contents generally fall between 0.5 and 7.0 cm,
and seem to support this view (Klawe, 1964;
Kropach, 1975), as do observations by
Paulson (1967). He reported that the
regurgitated food of P. platurus specimens
was composed entirely of small surface-living epipelagic fishes, "including the young
of some of the big game species, such as
tunas and billfishes."
SIZE AND SHAPE RELATIONSHIPS AMONG
SEA SNAKES AND THEIR PREY
In addition to categorizing fish and other
sea snake prey into the body forms
described earlier, it is also possible to identify four body types among the sea snakes,
with intermediate forms among them.
Measurements of the girth at the neck,
girth at two-thirds the snout-vent (SV)
length, and of the SV length, made in the
field on freshly killed specimens (except for
Ephalophis greyi for which preserved specimens were measured) as described in
Lemen and Voris (1981), provided the basis
of defining these body types, which are
depicted in Figure 5. The predominant
prey for each of the 16 species figured are
indicated by symbols. Representatives of
the short, stocky body type, E. greyi and
Aipysurus eydouxii, feed on gobies and fish
k EPH CHE
AlP EYD
A
HP HAR #
1YD OHNO
50
60
70
80
SNOUT-VENT LENGTH (cm)
90
I
110
120
O< 5 ITEMS
Fic. 5. Mean SV length and girth ratio (neck girth/
girth at 2/s SV length) values for 16 sea snake species.
The line drawings depict the four major marine snake
body types and their approximate positions relative
to the axes. Sample sizes for each species were: A.
peromi (4), A. eydouxn (20), E. schistosa (20), E. greyi (8),
H. brookn (34), H. caerulescens (20), H cyanoanctus (8),
H.fasaatus (20), H. melanosoma (25), H. ornatus (5), H.
spiralis (2), H. torquatus (8), L. hardwickn (20), L. colubrina (5), M. graalis (5), T. viperina (20). T h e predominant diet of each species is indicated by one of
five symbols.
eggs respectively. Long snakes with a rather
uniform girth, a second body type, are represented by Hyclrophis spiralis and H. cyan-
ocinctus. The only two stomach content records for H. spiralis are eels, while H.
cyanocinctus has been documented to take
eels and other elongated fish forms. In the
area of the figure representing the third
body type, moderate length and girth, there
are the eel specialists, Laticauda colubrina
and H. melanosoma; as well as H. torquatus
and H. caerulescens, both of whom take
elongated fish forms.
Fic. 4. The phylogenetic relationships of 22 sea snake species for which there are at least five identifiable
stomach contents each, are given in the vertical axis. The 12 body form categories and associated characteristics
of sea snake prey are given in the horizontal axis. For each sea snake species, the number and proportion of
stomach contents in each body form category is given in the body of the table.
418
HAROLD K. VORIS AND HELEN H. VORIS
Three sea snake species, Microcephalophis bone to the width of the parietal bone (skull
gracihs, Hydrophis fasciatus and H. brookii, width) has been used as an index of gape.
previously documented to specialize on eels, Details of skull measurements have been
have been termed microcephalic because described earlier (Voris, 1977). Gape index
their anterior bodies are extremely small determinations are shown for 14 species of
in actual terms (neck girths are only about sea snakes in Figure 6 in relation to the SV
2 cm) as well as relative to their posterior length and relative girth data presented in
girths. These represent a fourth body type. Figure 5. The gape relationships of the
It is interesting that Enhydrina schistosa, the three microcephalic eel-eating species indicatfish specialist, exhibits the same ratio of cate that as the relative girth decreases from
neck girth to body girth as H. brookii, Hydrophis brookii to H. fasciatus to Microcealthough in actual measurements the for- phalophis gracilis, the gape increases, sugmer is larger and longer. The size rela- gesting a possible compensatory adaptationships among E. schistosa and its catfish tion allowing the taking of similar prey
prey have been studied and reported on in items. Comparison of H. brookii with Enhydetail elsewhere (Voris and Moffett, 1981). drina schistosa, two species with similar relOne aspect of that study was an analysis of ative girth relationships, shows a major difthe relationship between the maximum ference in gape. That of E. schistosa, the
neck diameters of 94 E. schistosa, and the catfish specialist, is much larger than that
maximum diameters of their catfish prey. of H. brookii, an eel-eater. E. schistosa's gape
The results indicated that the largest cat- is in fact the largest of all the sea snake
fish eaten were approximately twice the species in the figure.
snakes' neck diameters.
Three species with similar, rather uniUsing the same methods of measure- form girth relationships (0.62), but varying
ment and calculation for snake neck diam- SV lengths, have very different gape indices
eter and prey diameter described in the and diets. Aipysurus eydouxii, the shortest,
study cited above, comparative data were specializes on fish eggs, and has the smallest
obtained for three additional species of gape. Hydrophis cyanocinctus, the longest,
snakes. In each case the maximum diam- eats eels and elongated fishes and has an
eters of the largest prey were much less intermediate gape. Lapemis hardwickii is
than twice the diameters of the snakes' intermediate in SV length, but has the largnecks. For the microcephalic eel specialist, est gape of the three species, and the most
Hydrophis fasciatus (n = 25), the maximum generalized diet, taking all body forms
prey diameters approached 1.5 times the except fish eggs.
snakes' neck diameters. A similar ratio was
Fang size is probably another important
observed for the generalist, Lapemis hard- factor in sea snake-prey relationships. Mean
wickii (n = 27). The moderate to long, uni- adult fang length data for 33 sea snake
form girth eel-eater, H. melanosoma (n = species have been published previously
10), took prey with maximum diameters (Voris, 1972), and data for a few additional
only about equal to its neck diameter. These species have been obtained. If the mean
data suggest that there are differences, not fang length measurements are substituted
only in actual prey sizes, but in the inges- for the gape index shown in Figure 6,
tion ratios, i.e., size relationships between somewhat similar relationships may be
sea snake species and their prey.
observed among the seven sea snake species
Neck girth or diameter is of course not discussed above. That is, among the three
the only factor determining the size and microcephalic species, Microcephalophis
type of prey taken by sea snakes. The gape gracilis has the largest fang (1.3 mm) and
resulting from the sea snakes' distendable Hydrophis brookii the shortest (1.0 mm), with
jaw is also an important component of the H. fasciatus (1.1 mm) somewhat intermematrix of variables determining prey taken. diate between the two. Enhydrina schistosa,
Gape itself is a function of both skeletal the catfish specialist, has a much longer
structure and tissue flexibility. In this anal- mean fang length (2.6 mm) than H. brookii
\ sis the ratio of the length of the quadrate to which it is similar in relative girth.
MARINE SNAKE DIET ANALYSIS
419
Among the three species with similar, relatively uniform girths, Aipysurus eydouxii,
the shortest, eats fish eggs and has a very
short fang (1.0 mm). Hyclrophis cxanocinctus,
the longest of the three, eats eels and elongated fish, and has an intermediate length
[Hydori
fang (2.0 mm). Lapemis hardwickii, the gen|Lai col
eralist, is intermediate in SV length and
has a fang similar in length to E. schislosa
(2.7 mm). The longest fangs occur in two
V T T
species not shown in Figure 6, the generalist Aipysurus laevis (4.2 mm) and Astrotia
-A
V
50
64
78
92
106
120
stokesii (3.6 mm) which feeds on goby-like
SNOUT-VENT LENGTH (cm)
fish; the shortest fang belongs to another
egg-eater, Emydocephalus annulatus (0.6 FIG. 6. Mean values of SV length, relative girth (girth
at neck/girth at 2/s SV length) and gape index (quadmm).
SEA SNAKE FEEDING BEHAVIOR
rate bone length/parietal bone width) for 14 sea snake
species. The sample sizes are given in the heading of
Figure 5, except for the gape index data which were
obtained from measurements made on 2-6 skulls per
species.
Our knowledge of sea snake feeding
behavior is based on two types of data;
direct observations made in the field or
laboratory, and inferences from certain
indirect information.
wole et ai, 1978); Hyclrophis major swallowField observations of what has been ing an eel, tail-first (Heatwole et ai, 1978);
interpreted to be foraging behavior have and Pelamis platurus feeding on fish in drift
been made for Acalyptophis peronii lines (Klauber, 1935; Paulson, 1967; Dun(McCosker, 1975; Heatwole et ai, 1978), son, 1975; Kropach, 1975). Field obserAipysurus apraefrontahs (Heatwole et ai, vations of Microcephalophis gracilis with its
1978), A. duboisii (McCosker, 1975; Heat- head poked into burrows in the sand, have
wo\eelal., 1978), ,4. lams (Heatwole, 1975; been interpreted by MacLeish (1972),
Limpus, 1975: Heatwole et ai, 1978), Heatwole (1975), and Heatwole et ai (1978)
Astrotia stokesii (Heatwole, 1975; Heatwole to mean that M. gracilis feeds on fish eggs.
et ai, 1978), Emydocephalus annulatus However the stomach contents of the par(Heatwole, 1975: McCosker, 1975; Heat- ticular snake specimen observed were not
wole et ai, 1978), H. elegans (Limpus, analyzed to verify this. The existing stom1975), H. major (Heatwole et ai, 1978), H. ach content data for M. gracilis (8 eels,
melanocephalus (McCosker, 1975: Minton Appendix A) suggest that it is more likely
and Heatwole, 1975), Laticauda colubnna that the above observed snake was in the
(Pernetta, 1977), Microcephalophis gracilis process of trapping an eel in its burrow.
(Heatwole, 1975: Heatwole et ai, 1978), P. The previous analysis of fang length, docplaturus (Dunson, 1975: Kropach, 1975), umenting that M. gracilis has the longest
and an unidentified microcephalic species fang of the three microcephalic species,
longer than that of the known egg-eaters,
(Mahadevan and Nayar, 1965).
Observations of actual interactions with further supports this interpretation.
prey are less common: only a few species
Observations of sea snakes feeding in the
have been observed in a post-foraging laboratory have been recorded in detail for
feeding stage in their natural habitats: Laticauda laticaudata eating eels (Klemmer,
Aipysurus duboisii, with a freshly caught fish 1962, 1967), L. semifasciata trapping and
(Heatwole et ai, 1978): A laevis attempting eating fish in nooks and crannies (Pickwell,
to swallow a live fish, and feeding on freshly 1972), E. schistosa eating catfish and puffkilled ones planted in its path by the exper- fish (Voris et ai, 1978), and L. colubrina
imenters (Heatwole et ai, 1978): Astrotia eating eels (Radcliffe and Chiszar, 1980).
stokesii attempting to swallow a fish (Heat- A few other species have also been observed
420
HAROLD K. VORIS AND HELEN H. VORIS
100
100
- 75
- 50
- 25
0000
0600
1200
NOON
1800
0000
0600
1200
NOON
1800
0000
HOUR
FIG. 7. For 56 E. schistosa specimens, the hour of capture is plotted against the percent digestion of the
stomach contents of each snake. Points representing stomach contents of snakes captured in the early morning
hours have been projected forward (horizontal lines) to 0700 hr, the approximate time digestion was terminated. The stippled regions indicate night. The diagonal lines project backwards to the times of estimated
prey capture by each snake, at an angle reflecting a digestion rate of 2.77 percent per hour over 36 hr, as
determined experimentally in the laboratory.
feeding in captivity: Pelamisplaturus (Shaw,
1962; Klawe, 1964; Pickwell, 1972; Dunson, 1975; Kropach, 1975) and Hydrophis
melanosoma (Voris et al., 1978).
Much information about sea snake feeding behavior has been inferred from various types of indirect data. Most commonly, analysis of stomach contents has
allowed researchers to infer where sea
snakes have been feeding based on knowledge of the habits and habitats of the identified prey (see earlier references). Observations of the prey orientation in the
stomach have led to the conclusion that
most sea snakes take their prey head first,
with occasional exceptions by eel-eaters;
Hydrophis major was observed eating an eel
tail-first by Heatwole etal. (1978); Pernetta
(1977) found one eel to be eaten tail-first
by Laticauda colubrina; and McCosker
(1975) found that eight out of 48 eels taken
by H. melanocephalus had been ingested tailfirst. Frequency of encountering stomach
contents among different species of sea
snakes has been mentioned bv McCosker
(1975) who pointed out that nearly one out
of every three Emydocephalus annulatus
specimens contained fish eggs in contrast
to the rarity of prey items in other captured
snakes. This type of information may suggest some differences in feeding frequencies among different sea snake species.
Detailed field records of the time, location and conditions {e.g., turbidity, salinity,
currents, weather, tides) of snake capture,
along with representative fish collections
from the same site, provide useful data from
which inferences can be made about where
snakes are foraging, under what conditions, and what prey are potentially available to them. Klawe (1964) for example,
found for Pelamis platurus that "a comparison of [fish] collections with the fish
ingested by the snakes proved that the most
abundant fish at a locality contribute the
most heavily to the diet of the snakes."
Interpretation of the role vision in Enh\drina schistosa feeding behavior by Voris et
al. (1978) made use of detailed records of
field conditions.
421
MARINE SNAKE DIET ANALYSIS
The state of digestion of stomach contents together with information on rates of
digestion, prey habits, and time and conditions of snake capture can be used to indicate when and under what conditions
snakes have fed. McCosker (1975) used this
type of data to suggest that Lapemis hardwickii fed diurnally on a specimen of Priacanthus cruentatus, that Aipysurus duboisii
feeds crepuscularly, and that A. laevis feeds
during periods of prey inactivity, whether
nocturnal or diurnal.
In the present study, the percent digestion of the stomach contents (all catfish)
was determined for each of 56 Enhydrina
schistosa collected at stake nets in the mouth
of the Muar River at Muar, Malaysia during the two spring tides of each lunar month
over a ten-month period (Fig. 7) (details of
collection method, site and conditions published earlier, Voris and Glodek, 1980). In
Figure 7 the hours of snake capture are
plotted within a single 24-hr period, and
the times of the snakes' respective prey
captures are estimated using backward
projections based on digestion rates determined from laboratory experiments. In the
figure there are certain gaps or windows
in the times of prey capture, namely from
about 0200 to 0600 hr, and 1200 to 1800
hr. These are obviously neither exclusively
nocturnal nor diurnal periods, but rather,
are those times during which the ebbing
tides coincided with the river discharge,
making them periods with the strongest
currents and maximum turbidity. These
data suggest that E. schistosa's feeding is not
restricted to either diurnal or nocturnal
conditions (a point corroborated by laboratory observations, Voris el ai, 1978), but
that feeding is inhibited during periods of
strong currents. Since the stake nets were
only operated during the strongest, i.e.,
spring, tidal cycles of each lunar month, it
is not possible to say from these data how
the weaker neap tidal conditions might
affect the feeding behavior of E. schistosa.
However this preliminary analysis suggests
some interesting possibilities for further
directions in feeding behavior studies, and
the potentially powerful effect of integrating field data with various other related
types of information.
Ae
A eydouxii
A granulatus
E schrstosa
H. brookii
H caerulescens
H fascisms
H melanosoma
. hardwickn
\r
H b
Ag
H c
H 1
Hm
•A
•
•
• •• •
••
• A
•A
••
••
\
•
\\
• A
\
DIET OVERLAP
•A
\
•
\
Do
•
21-30
COOCCURRENCE
4 MUAR
•
SUNGAI BULOH
•
PARIT BOTAK
A ENOAU
FIG. 8. Diet overlap (Schoener, 1968) and co-occurrence data for eight species of marine snakes collected
at four localities in the Straits of Malacca and the
South Cina Sea.
DIET AND COMMUNITY COMPOSITION
Sea snake collections made at four localities in the coastal waters of Malaysia over
a ten-month period in 1975, have enabled
us to evaluate the relationships among sea
snake species and their prey at particular
localities, for the first time. Details of collecting methods and sampling periods have
been published previously (Jeffries and
Voris, 1979; Glodek and Voris, 1982).
For eight marine snake species (including the non-venomous file snake, Acrochordus granulatus, not a true sea snake but
often collected in the same localities as
other sea snakes), each represented by 1 1
or more stomach contents identifiable to
the level of species or distinct type, diet
overlap has been estimated using the
Schoener index (Glodek and Voris, 1982).
These data, which are presented in Figure
8, indicate that there is very little diet overlap among these eight species, with the
highest level being only 21-30.
When locality data are superimposed on
the diet overlap data, it may be seen that
diets overlap even less between co-occurring species. For example, Hydrophis
melanosoma and H. brookii are both present
at Muar, however their diet overlap is only
1 1-20. Hydrophis caerulescens and H.fascia-
tus occur together at both Sungai Buloh
and Parit Botak, however their diet overlap is even lower, 0-10. Lapemis hardwtckii
is found at three localities, co-occurring
with five of the other seven snake species.
Its maximum diet overlap is with Acrochordus granulatus, with which it co-occurs at
422
HAROLD K. VORIS AND HELEN H. VORIS
70
EELS &
ELONGATED
FISH
MUAR
n = 968
BOTAK
n = 499
SNAKE SPECIES
FIG. 9. Comparison of diets in the context of the relative abundance of the more common species of marine
snakes at each of four Malaysian localities. Species representing less than two percent of the sample are not
shown.
Sungai Buloh and Parit Botak, at a level of
only 11-20.
Looking at each of the four localities
mentioned above, in terms of feeding roles
represented, an even more complex picture emerges. In Figure 9 the relative frequencies of snake species are presented for
each of the four localities, omitting those
species making up less than two percent of
the sample at each locality. It may be seen
that there are differences among the localities not onl\ in the number of snake species
present, but in the feeding roles filled by
the dominant and subdominant species.
At Sungai Buloh there is a single dominant species that is a generalist, and two
subdominants, one of which eats goby-like
fish; the other eats eel-like fish. Eel specialists play a minor role. At Muar there is
a single dominant species, a catfish specialist; the main subdominants eat eels,
elongated fish and gobies. At Parit Botak
there are three dominant species, an eeleater, a generalist and an egg-eater. The
MARINE SNAKE DIET ANALYSIS
423
major subdominant eats elongated fish. At gists G. S. Glodek, R. K. Johnson, J. C.
Mersing there are two dominant species, a Tyler, and V. G. Springer who provided
generalist and a goby-eater, with a number advice and assistance on prey species. We
of subdominants including an egg-eater, appreciate the efforts of S. A. Brunner on
and a goby-like and elongated fish eater, skeleton preparations and P. Gritis for help
with catfish and eel specialists being less with data collection. We are grateful for
permission to use in our figures numerous
common.
It is particularly interesting to note that line drawings from Fishes of the World by J.
the actual snake species composition is very S. Nelson.
similar at Sungai Buloh and Parit Botak:
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the five species found at Sungai Buloh all
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ippine Islands, with a note on the palatine teeth
species is different at the two localities and
in the proteroglypha. Proc. Calif. Acad. Sci. Series
the relative importance of various feeding
4, 3:41-48.
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CONCLUSIONS
We have made a beginning in the understanding of sea snake feeding at several
levels. There are trends for the group as
a whole: families of eels and gobies are
taken by the greatest numbers of sea snake
species; most sea snake species feed on fish
families whose members are relatively sedentary, dwelling along the bottom, within
burrows in the bottom or reef crevices;
most prey are scaleless or have fine scales.
Among species of marine snakes we have
documented differences in diet, feeding
behavior, and size and shape inter-relationships with prey. At the community
level, there is a complex merger of these
aspects of sea snake feeding. There are differences among sea snake assemblages with
respect to their species composition, the
relative frequencies of the various species
present, the number of dominant and subdominant species, and their feeding role
structures. We have yet to understand at
even a single locality, the factors that determine sea snake community composition and
the relative importance of feeding roles.
ACKNOWLEDGMENTS
We wish to thank the many individuals
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Klawe, W. L. 1964. Food of the black-and-yellow sea
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HAROLD K. VORIS AND HELEN H. VORIS
Mahadevan, S. and K. N. Nayar. 1965. Underwater
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APPENDIX A
Summary of stomach content data from
literature sources for 39 species of sea
snakes. Totals are given in parentheses.
Acalyptophis peronii: Gobiidae 7; Trypauchenidae 3; (10).
Aipysurus apraefrontalis: Anguilliformes 2;
(2).
Aipysurus duboisii: Acanthuridae 1; Blenniidae 1; Muraenidae 1; Scaridae 1; (4).
Aipysurus eydouxii: Fish eggs 41; Cuttlefish/
squid 1; (42).
Aipysurus foliosquama: Clinidae 1; Eleotridae 2; Labridae 4; Anguilliformes 1; (8).
Aipysurus fuscus: Gobiidae 3; Labridae 4;
Fish eggs 1;(8).
Aipysurus laevis: Acanthuridae 6; Apogonidae 31; Carangidae 1; Clupeidae 1;
Engraulidae 1; Labridae 2; Lutjanidae
7; Pempheridae 14; Pomacentridae 2:
Scaridae 4; Scorpaenidae 2; Serranidae
2; Fish eggs 1; Crabs 4; Shrimp 4; Pelecypod 1; (83).
Astrotia stokesii: Batrachoididae 8; Opisthognathidae 1; (9).
Emydocephalus annulatus: Fish eggs 24; (24).
Emydocephalus ijimae: Fish eggs 2; (2).
Enhydrina schistosa: Ariidae 130: Engraulidae 2; Harpadontidae 1; Leiognathidae
3; Plotosidae 21; Sciaenidae 1; Tetraodontidae 11: Anguilliformes 1; Shrimp
2; (172).
Ephalophis greyi: Gobiidae 9: (9).
Hydrophis belcheri: Moringuidae 1: Anguilliformes 1; (2).
Hydrophis brookii: Gobiidae 2; Moringuidae
17; Ophichthidae 1; Anguilliformes 9;
(29).
Hydrophis caerulescens: Gobiodidae 5; Moringuidae 1; Trypauchenidae 8; (14).
Hydrophis cyanocinctus: Congridae 1; Gobiidae 1; Gobioididae 3; Anguilliformes 1;
(6).
Hydrophis elegans: Muraenidae 1; Ophichthidae 2: Plotosidae 1: Sillaginidae 1;
(5).
MARINE SNAKE DIET ANALYSIS
425
Hydrophis fasciatus: Moringuidae 19:
Polynemidae 83; Pomacentridae 8;
Muraenidae 1: Ophichthidae 6: TryScombridae 5: Serranidae 11; Sphyraepauchenidae 2: Xenocongridae 55;
nidae 1; Stromateidae 1: TetraodontiAnguilliformes 5: (88).
dae 1: (235).
Hydrophis inornatus: Atherinidae 1: Thalassophina viperina: Callionymidae 6;
'Gobioididae 1: (2).
Platycephalidae 1; Anguilliformes 1: (8).
H\drophis kingi: Anguilliformes 1; (1).
Thalassophis anomalus: Congridae 1: (1).
Hydrophis lapemoides: Gobiidae 1; OphAPPENDIX B
ichthidae 1; Anguilliformes 1: (3).
Hydroplus major: Carapidae 1: Plotosidae 1: Summary of stomach contents data from
'(2).
literature sources for 39 species of sea
Hydroplus melanocephalus: Congridae 3; snakes, distributed according to fish family
Moringuidae 2: Ophichthidae 39; (44). (or other type of item). Following the numHydrophis melanosoma: Congridae 5; Mo- ber of contents from each family are the
ringuidae 9; Muraenidae 38; Anguilli- body form code 1-12 (see Fig. 1); the
behavior code (1 = "sitter"; 2 = "swimformes 17; (69).
Hydrophis nigrocinctus: Congridae 1; (1). mer"); and the habitat code 1-6 (see Fig.
Hydrophis obscurus: Triacanthidae 1; (1). 3), in order.
Hydrophis ornatus: Gobiidae 1: Plotosidae
Acanthuridae (11) 7-2-4; Apogonidae (39)
i;(2).
6-2-4; Ariidae (131) 10-2-3; Atherinidae
Hydroplus spirahs: Ophichthidae 2; (2).
(5) 5-2-5; Batrachoididae (8) 4-1-3; BlenHydrophis torquatus: Gobioididae 4; Platy- niidae (3) 4-1-1; Callionymidae (1 1) 4-1-3;
cephalidae 1: Trypauchenidae 1; (6).
Carangidae (24) 7-2-5; Carapidae (1) 2-1Kerilia jerdom: Ophichthidae 2; (2).
1; Chaetodontidae (1) 7-2-4; Clinidae (1)
Kolpophis annandalei: Clupeidae 1; (1).
4-1-1; Clupeidae(15) 5-2-5; Congridae(14)
Lapemis hardwickii: Apogonidae 8; Ariidae 1-1-2; Coryphaenidae (11) 6-2-6; Cyno1; Callionymidae 5: Carangidae 7; Clu- glossidae (1) 8-1-3; Eleotridae (21) 4-1-3;
peidae 11: Cynoglossidae 1; Eleotridae Engraulidae (18) 5-2-5; Fistulariidae (3) 218; Engraulidae 7; Fistulariidae 1; Gobi- 2-4; Gobiidae (26) 4-1-3; Gobioididae (13)
idae 1; Labridae 1: Leiognathidae 6; 2-1-1; Harpadontidae (1) 5-2-5: KyphosiLutjanidae 3; Moringuidae 2; Mugilidae dae (1) 6-2-6; Labridae (11) 5-2-4; Leio2; Nemipteridae 1; Platycephalidae 3; gnathidae (9) 7-2-5; Lutjanidae (11) 6-2-5:
Plotosidae 1; Polynemidae 1; Priacan- Moringuidae (52) 1-1-1; Mugilidae (31) 5thidae 1; Sciaenidae 10; Scorpaenidae 2; 2-5; Mullidae (44) 5-2-3; Muraenidae (47)
Siganidae 8; Soleidae 1: Synodontidae 1; 1-1-2; Nemipteridae (1) 6-2-5; Nomeidae
Tetraodontidae 1; Trichiuridae 6: Try- (1) 6-2-4; Ophichthidae (60) 1-1-1; Opispauchenidae 12; Xenocongridae 2; thognathidae (1) 4-1-1; Pempheridae (14)
Gobioidei 4; Anguilliformes 2; Cuttle- 6-2-5; Platycephalidae (5) 4-1-3: Plotosidae
fish/squid 8; Amphipod 1; (139).
(25) 3-2-3; Polynemidae (84) 6-2-5; PomaLapemis curtus: Clupeidae 1; Gobiidae 1; centridae (11) 6-2-4; Priacanthidae (1) 6Sparidae 1; (3).
2-3: Scaridae (5) 6-2-4; Sciaenidae (11) 6Laticauda colubnna: Congridae 3: Morin- 2-3; Scombridae (5) 5-2-6; Scorpaenidae (4)
guidae 1; Muraenidae 6: Pomacentridae 6-1-3: Serranidae (13) 6-2-3: Siganidae (8)
1; Synodontidae 1; Anguilliformes 3: 6-2-4; Sillaginidae (1) 5-2-5; Soleidae (1) 8(15).
1-3; Sparidae (1) 7-2-3; Sphyraenidae (1)
Laticauda sclustorhynchus: Eleotridae 1: (1). 5-2-6; Stromateidae (1) 6-2-6; SynodontiMicrocephaloplus gracilis: Ophichthidae 7; dae (2) 5-1-3; Tetraodontidae (13) 9-2-4;
Xenocongridae 1; (8).
Triacanthidae (1) 7-2-3; Trichiuridae (6)
Pelamis platurus: Acanthuridae 4; Ather- 2-2-3; Trypauchenidae (26) 3-1-1; Xenoinidae 4; Blenniidae 2; Carangidae 16; congridae (58) 1-1-2: Anguilliformes (45)
Chaetodontidae 1; Clupeidae 1; Cory- 1; Gobioidei (4) 4; Fish Eggs (69) 11; Crabs
phaenidae 11; Engraulidae 8; Fistulari- (4) 12: Shrimp (6) 12; Cuttlefish/squid (9)
idae 2; Kyphosidae 1; Lutjanidae 1; 12; Amphipod (1) 12; Pelecypod (1) 12.
Mugilidae 29; Mullidae 44; Nomeidae 1;