Download diversity, utilization of resources, and adaptive radiation in shallow

DIVERSITY,
UTILIZATION
OF RESOURCES, AND
ADAPTIVE
RADIATION
IN SHALLOW-WATER
MARINE
INVERTEBRATES
OF TROPICAL
OCEANIC ISLANDS
Alan J. Kohn2
Department
of Zoology,
University
of Washington,
Scattlc
98105
AHSTRACT
Important
features of the inshore marine benthic invertebrate
fauna of tropical islands
are very high species diversity
and the gcomorphological
role of reef-building
and sediment-gcncrating
animals in contributing
the structural framework
of habitats.
The former
is due to the adaptive radiation and pcrsistcnt co-occurrence
of large numbers of species
in a number of genera, particularly
of molluscs, echinoderms, and crustaceans.
Among the
molluscs, epifaunal
gastropod genera contribute
importantly
to the high species diversity.
On tropical Indo-West
Pacific island shores and coral reefs, 80% of prosobranch
gastropods belong to genera having more than three sympatric
species; in diverse temperate
faunas the corresponding
figure is 20%.
Features of the environment
and of the animals tending to promote both speciation and
high faunal diversity
are listed:
environmental
heterogeneity
and ecological and behavioral specialization
are the most approachable.
In a reprcscntative
gastropod genus (Co?zus)
with available quantitative
ecological data, topographically
complex, climatically
equable
subtidal coral reefs support more species, lower population
density, and animals of larger
size than do intertidal
marine benches that are topographically
uniform but subject to
more severe weather conditions.
Recurrent group analysis shows strong affinity
among six
common species on reefs and three on benches spanning most of the longitudinal
extent
of the Indo-West
Pacific region, demonstrating
wide species distribution
and constancy
of spccics composition
in these habitat types.
Degree of specialization
and overlap in resource utilization
by co-occurring
congeneric
speciesare discussed with reference to the theory of limiting similarity.
Conus species arc
demonstrated
to specialize more to different
prey species than to substrate type. A more
that co-occurring,
ecologically
similar predator species tend to adopt
general hypothesis,
this strategy, while detritus feeders are more likely to specialize to microhabitat
than food
type,
is only partially
supported by the limited data available on other benthic invertebrate taxa.
INTRODUCTION
Like tropical wet forests among terresthe coral reefs surtrial environments,
rounding tropical oceanic islands are small
portions of the marine realm with very
high faunal diversity.
Despite this common feature, viewed as wholes these two
l Supported
by National
Science Foundation
Grant GB-17735.
Fieldwork
supported
by National Science Foundation
Grant Cl7465
as part
of U.S. Program in Biology, International
Indian
Portions of this paper were
Ocean Expedition.
presented at the Association for Tropical
Biology
Symposium on Adaptive
Aspects of Insular Evolution, 1969.
2 I thank Margaret Lloyd and Natalie Melcnrck
for technical assistance, Dr. J. Felsenstcin for aid
with the community
matrix analyses, and Drs. R.
T. Paine and G. II. Orians for discussion and
criticism of the manuscript.
LIMNOLOGY
AND
OCEANOGRAPHY
community types differ strikingly in habitat structure and ecosys tern organization,
aside from the obvious contrasts in physicochemical
properties of fluid medium
and solid substratum.
In the wet forest, massive primary producer organisms, characterized
by low
production : biolmass ratios and high biomass : unit of energy flow ratios provide
the habitat structure of the community,
enhancing spatial complexity and ameliorating the effects of fluctuating
external
physical factors. Both aspects may be prerequisites for high biotic diversity.
On
the coral reef, the primary producers are
mainly small and inconspicuous algae, with
high productivity : biomass and low biomass : unit of energy flow ratios, and habitat structural
complexity
results mainly
332
MARCH
1971,
V. 16(2)
DIVERSITY
OF
TROPICAI
from elaboration of calcareous cxoskeletons by secondary producers, molluscs and
cchinodcrms as well as the corals.
Few have attempted to document the
occurrence of high faunal diversity
in
these assemblages, and no satisfactory
evaluation exists of tic factors that gcnerate and maintain it. In this paper, I
attempt to quantify some aspects of this
diversity and to apply some recent contributions to the theory of the ecological
niche to evaluate thlc importance of certain factors that can lead to incrcascd
Except in broad outline
faunal diversity.
the community is too complex to be acccssiblc as a who,le. At the prcscnt time
it is more profitable to examine picccs of
it in detail, and it is of considerable interest to examine taxa containing numerous co-occurring similar species, bccausc
they contribute importantly
to faunal diversity and bccausc their spccics are
likely to have similar environmental
rcquircments.
I limit most of the detailed
consideration to one prominent group of
invcrtcbratcs
of tropical inshore marine
habitats, but available information
from
other taxa is summarized and evaluated.
The . research to bc discussed has attempted mainly to apply data from the
study of natural populations to two qucstions: How similar in utilization
of resources arc co-occurring,
taxonomically
similar species in assemblages of varying
diversity?
And how do the numbers of
such species compare with the maximum
that could thcorctically
coexist in stable
rcsourcc-limited
populations?
NATURE
OF
TROPICAL
INVERTEBRATE
MARINE
DIVERSITY
A general increase in numbers of marinc
invertebrate species from Arctic to tropical regions was attributed until recently to
diffcrcnces in the cpifauna, animals living
on or associated with rocks and other hard
substrates; infaunal invertebrates inhabiting sand and mud bottoms were thought
not to have pronounced latitudinal
diversity gradients (Thorson 1952, 1957). More
MARINE
333
INVERTEBRATES
TABLE 1. Proportions
of marine gastropod and
bivalve
molluscs in temperate
and tropical
regions. (Data from Kay 1967, and other sources
available from author)
Teinpcratc
Friday IIarbor, Washington
Woods IIole, Massachusetts
Plymouth, England
Mean
Tropical
continental
islands
Philippines
Krusadai, India
New South Wales
Okinawa
Mean
Tropical
oceanic
Maldives
Hawaii
Seychelles
Ellicc
Kermadec
Society
Mean
57
59
63
43
41
37
60
40
63
E
79
37
38
29
21
69
31
77
82
82
82
86
87
23
18
18
18
14
13
83
17
islands
rcccntly
Sanders (1968) reported pronounced increases in diversity with dccreasing latitude in the bivalve and polychaete assemblages of soft estuarine and
marinc oozes (see also Bakus 1969).
Bccausc I have obtained detailed comparativc ecological information
for one
family of largely cpifaunal prosobranch
gastropod molluscs, ‘and because this order
is an important contributor
to increased
faunal diversity in the tropics (Thorson
1952), I chose this group as an example
for particular
emphasis. Table 1 shows
that the ratio of species of inshore, shallow-water
gastropods and bivalves, the
two largest molluscan classes, is about
60 : 40 in temperate and boreal regions
but is skewed strongly toward the primarily epifaunal gastropods throughout
the
tropics (Kay 1967). Moreover, as Kay
pointed out the bivalve families with the
largest number of species in such habitats
in the tropics are primarily epifaunal.
334
ALAN
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S=250
G=xs=2.5
FIG. 1. The number of genera containing
gastropod molluscs in different
regions.
(Data
“,:?$=4.2
different
numbers of sympatric
from various sources available
The relative contribution to diversity by
genera also rcvcals a pattern of geographic
variation. In temperate regions, the number of co-occurring species in a genus or
family is usually low even in the most
diverse faunas ( Fig. 1) . Contras tingly, a
number of primarily tropical families and
genera have undergone remarkable adaptive radiations, so that they arc character-
species of prosobranch
from author.)
ized by large numbers of co-occurring
species. For example, at Woods Hole
( Massachusetts),
Friday Harbo,r (Washington ) , and Plymouth ( England ) , where
large marine laboratories were sited to
take advantage of the rich marine biota,
80% of all species of prosobranch gastropods belong to genera having three or
fcwcr sympatric species, while in the Indo-
DIVERSlTY
OF
TROPICAL
West Pacific tropics, 80% of species belong
to genera having more than three sympatric species (Fig. 2). The same phcnomenon characterizes other invertebrate
taxa. In the coral family Acroporidae, for
example, 54 species of Acroporn and 30
of Montipora occur in the Marshall Islands (Wells 1954). In tropical Indo-West
Pacific Crustacea, “there are about 100
endemic gcncra, among them many with
large numbers of species” (Ekman 1953,
p, 14). To some extent this reflects the
degree of splitting in our classification systcm; in any cast it also reflects phenetic
similarity.
Although
the extant species
asscmblagcs presumably result fro’m radiations relatively recent in geologic time,
some of the genera involved are known
to have had similarly large numbers of
co-occurring species as far back as the
mid-Tertiary
(Hall 1964; see also Stehli
et al. 1969).
What factors have influenced
these
strikingly
different
patterns of adaptive
radiation
in marine invertcbratc
taxa?
And what can the comparative ecology of
such groups tell us of patterns of tropical
insular evolution?
One might expect the following features
of the environment to promote speciation
and high faunal diversity. This hypothesis
could be tested by correlation of divcrsity with gradients of the cnvironmcntal
variables.
1. Stability of the tropical oceanic environment
in ecological
and probably
evolutionary
or geological time; equable
physical
conditions
of insolation,
tcmpcrature, salinity, etc. without
climatic
cxtrcmes.
2. Isolation of appropriate habitats for
shallow-water cpifauna; restrictioa to narrow bathymetric
and horizontal
bands
along the edges of oceanic islands, This
is especially true of the Indo-West Pacific
region, where suitable habitats comprise
an infinitesimal
fraction
of a biogeographic region covering a fourth of the
world ocean,
3. Complexity of environments; a prio’ri
we cxpcct the most heterogeneous habitats
MARINE
INVERTEBRATES
percent of species of prosFIG. 2. Cumulative
to genera
ohranch gastropod molluscs belonging
containing
varying numbers of sympatric
species
in different
regions characterized
by marine faunas of high diversity.
(Data from various sources
available from author. )
to support the largest numbers of species.
Since the coral reef structure is entirely
biogenic, a positive feedback is possible
bctwccn biotic diversity and topographic
hetcrogencity of reef structure.
4. Vulcanism and subsidence, resulting
in changing dispersion patterns of islands
an d archipelagoes in geologic time, contributes to providing new cand changing
habitats for colonization and to isolating
populations,
a requisite for geographic
speciation.
5. Surfnce currents of the ocean, including the persistent gyres and equatorial
countercurrent in the Pacific and the semiannual shift of current direction
>90”
with the monsoon in the Indian Ocean,
provide transport for pelagic propagules.
Traits of animals expected to promote
both speciation and high faunal diversity
include:
I. Pelagic distributive larval stage in the
lift history, with
II. Large numbers of propagules or larvae, and
III. Long-hued Zarvae that feed during
dispersal.
IV. Extentlecl breeding season; larvae
may bc released subject to varying current
patterns.
336
ALAN
V. Abundance of predators, which keep
prey populations
below densities that
would lead to competitive exclusion.
VI. Specialization of the ecological and
behavioral
characteristics
of the species
prcscn t.
Taken together, this combination of factors
permits Indo-West Pacific species particularly to extend their ranges over a vast
region, and to form distinct geographic
populations occupying new adaptive zones
in rcsponsc to local selective pressures,
with the potential for speciation given
extrinsic isolating mechanisms,
Factors (3) and (VI)
are most approachable quantitatively
as dimensions of
ecological niches, and I have emphasized
them in my studies of the comparative
ecology of Conus, a primarily
tropical
prosobranch gastropod genus of several
hundred species. Large numbers of spctics (up to 24) co-occur on coral reefs
in the tropical Indo-West Pacific; assemblages of fcwcr sp&es, including
some
single-species populations
( Kohn 1966))
provide comparisons,
The group has a
number of attributes that are advantageous for comparative ecological study,
enumcratcd elsewhere (Kohn lQ68). Here
I ask how do the ecological characteristics
of Conus species vary (from specialized
to generalized in utilization
of resources )
in assemblages varying in diversity. I have
used this comparative approach, and the
advances in theory of the ecological niche
due to MacArthur and Levins (1964, 1967),
Lcvins ( 1968)) and MacArthur
( 1969) to
relate species diversity, resource utilization and habitat complexity in one perhaps exemplary taxoccne” of invertebrates
of inshore marine habitats of tropical
islands.
The model of expected ecological characteristics of Conus in two distinct habitat
types (Table 2) is partly a priori, insofar
as it is based on factors (3) and (VI)
above and rcccnt hypothcscs of adaptive
3 In this paper the terms taxocene and assemblage are used as defined by Hutchinson
( 1067 >.
J.
KOIIN
TABLE
Conus
bawd
-
Expected
ecological
characteristics
of
populations
in different
habitat
types,
on expected
selective
pressures
of the
environments
2.
-___
Habitat
type:
HzLbitat
Habitat
topography:
climate:
--
------
Intertidal
marine
bench
(type II)
Snbtidal
coral reef
Uniform
Severe
Expected adaptive strategy
with respect to:
Species diversity
low
high
Population
high
low
Body
density
size
small
large
Ecological niche breadth
with respect to
resource utilization
narrow
wide
Ecological niche breadth
with respect to
climatic variables
wide
narrow
strategies in environments
of varying
patchiness (MacArthur
and Pianka. 1966;
Emlen 1966), and partly a posteriori, insofar as it is based on analyses of natural
populations
of Conus studied to date
( Kohn 1959, 1968).
Selection of the two habitat types indicated (Table 2; see also Kohn 1967) for
comparison is based oln the facts that
1) both occur commonly throughout the
tropical Indo-West Pacific region, the arca
of study; 2) both support Conus populations dcnsc enough to warrant quantitative
analysis; and 3) they illustrate contrasting
environmental
conditions.
Intertidal
marine benches (type II habitats) are topographically
rather uniform smooth platforms subject to desiccation and wetting
by rain at low tide and heavy wave action
at high tide; climatic conditions are thus
variable and often severe. In contrast, subtidal coral reef platforms (type III habitats ) are topographically
more complex,
with patches of different substrate types,
but arc always submerged; their “climate”
is thus more equable and benign. Intermediate and other habitat types support
Conus but these will be treated in more
detail clscwherc.
DIVERSITY
OF
TROPICAL
MARINE
337
INVERTEBRATES
C. frigidus (8,6), C. flavidus (93). The
first six species listed form a recurrent
group. Members of recurrent groups are
Species composition of the Conus asfrcqucnt components of each other’s envibenches an d
semblages of intertidal
ronmcnt; they can be considered as groups
subtidal
coral reefs is quite constant
whose interspecific relationships are likely
throughout the Indo-West Pacific tropics.
to bc of particular intcrcst. The size of the
Most species are widely distributed,
and groups indicates the degree of trans-Indodistribution
restricted
endemism-species
West Pacific homogeneity of species comto one archipelago-is
low. Nine benches
position. Since all species of the sm,aller
in five geographic regions have been ccn- bench group belong to the karger reef
suscd, mainly by counting all individuals
group, some interhabitat homogeneity also
found in transects of quadrats across the occurs. Thcsc groupings are based on
bench; 17 species were found, of which
prescncc or absence of species only; they
5-9 occur on any one bench (Kohn 1967).
do not consider relative abundance. When
The nine most frcqucntly
occurring spc- relative abundance as well as spccics comtics, with the number of occurrences by position is considered in a measure of simibenches and regions respectively (maxima
larity ( R. of Horn 1966)) the polpulations
= 9,s) indicated in parenthcscs are: C. of bench stations and of reef stations are
sponsalis (9,5), C. ehraeus (8,5), C. chulseen to be more similar to each other (9
daeus, ( 8,4), C. lividus ( 6,s) , C. miliaris
bench censuses : mean R. = 0.54; 19 reef
( 4,4), C. catus ( 5,3), C. coronatius ( 4,3),
censnses : mean R. = 0.41) than bench
C. r&us (5,2), C. ftuauidus ($2). The first
populations are to reef populations
( 171
three species listed form a recurrent group,
comparisons : mean R. = 0.32). All of the
the largest group within which all pairs of means differ significantly
( t tests : p <
species show affinity according to the cri0.005 ) .
terion of Fager and McGowan (1963). On
Until this point I have used the simplest
19 subtidal reefs censuscd, 58 spccics oc- index-number
of species-as the measure
currcd; 9-24 occur on any one reef (Kohn
of spccics diversity; in most cases it was
1967), although substrate complexity and the only available datum. However, if all
low population
density gcncrally
made individuals in a population or sample have
quantitative
sampling unfeasible. The 12 been identified and counted, it is desirable
most frequently
occurring species, with
to USC “information
content,” or the unthe number of occurrences by reefs and certainty regarding the species identity of
regions rcspcctivcly
(maxim,a 19, 9) indiany randomly selected individual
(Pielou
catcd in parenthcscs are: C. lividus (l&9),
1966a). The value of this index increases
C. ehraeus (17,9), C. rat&s (17,9), C. &sboth with increasing numbers of species
tans (12,9), C. chaldaeus (12,8), C. sponand increasing equitability
or cvcnncss of
salis ( ll,S), C. miles ( 12,7), C. leopardus
their proportions.
(9,6), C. milinris (9,6), C. imperidis (8,6),
In Table 3, both measures are used to
CONUS POPULATIONS:
DENSITY,
TAULE 3.
subtidul
DIVERSITY,
AND
SIZE
Species tliva~&zj of Corms assembluges of intwtidal
marine benches (habitat type II) and
coral rcwfs (habjtat type III) in the Indo-West
Pacific tropics.
(Data from Kohn 1967)
No. of
assemblages
studied
Intertidal
marine
benches ( type II )
Subtidal coral
reefs (type III )
Mean
sample
size
No.
of co-occurring
Mean
9
221
7.5
191
110
13.7
species
Range
Species
Mean
diversity
(H”)
Range
5-9
1.2
0.4-l .7
9-24
2.1
1.6-2.7
338
ALAN
J.
KOHN
compare species diversity of Conus assemblages in the two major habitat types
throughout the Indo-West Pacific tropics
and to provide a partial basis for the
predicted directions of species diversity
given in Table 2. Species diversity
is
measured bY
‘x
i I.O2
9
9
2 .95-
.90!
0
I
I
2
1 1 I I 1 I 1 1 1 ’ 1 ’ 1 ’
IO
4
6
8
12
14
16
Number of collections
FIG. 3. Cumulative
values of Cmu.s species
diversity
II” plotted
against number of collections, A. Data for two subtidal fringing reefs in
Hawaii.
Upper curve, Maili:
H” = 1.90; mean
H” after last 4 samples, 1.90; 95% confidence
limits for population
diversity are 1.86 < II’,,, <
2.03. The 10 collections
were made 1954-1968
and include
299 individuals
of nine species.
Lower curve, Diamond
Head:
H” = 1.87; mean
H” after last 3 samples, 1.85; 95% confidence
limits are 1.82 < II’,,, < 1.87. The 16 collections
were made 1954-1956 and include 187 individuals of 10 species (Kahn 19,59). B. Data for
an intertidal
bench, Kahuku, Oahu:
H” = 1.32;
mean H” after last 6 samples, 1.34; 95% confidence limits
are 1.31 < H’,,,a < 1.36. The 16
collections
were made 1954-1968
and include
525 individuals
of eight species. Leveling
off of
the curves to the right as more collections
are
added indicates that little further change in diversity would be expected if sample size were
further enlarged and permits computation
of the
variance and confidence limits of II’,,,, in asscmblages that cannot bc sampled randomly
(Pielou
1966b ) .
where s = the number of species, iVi = the
number of individuals
of the it11 species,
and N = the total number of individuals
in the sample. Since the number of species in the population is unknown, H” is
the “maximum likelihood estimator of the
unknown populatioa diversity H”’ ( Piclou
1966a,
p. 464).
However,
it can be
shown by applying the method of Pielou
(1966b) to repeatedly sampled populations
that H” is likely to be a close estimator
of H’ for Conus. In cumulative graphs of
H” vs. number of samples (Fig. 3), the
curves tend to level off after 7-11 collecindividuals),
inditions ( about 150450
cating that in samples added thereafter
any reduction of diversity due to addition
of common species is balanced by additional rare species that increase diversity.
Thus further enlargement of samples of
this size is unlikely
to alter diversity
values.
Diversity and density can both bc estimated more reliably in bench ( type II)
than in reef ( type III) habitats, because
benches have homomgencous substrates and
they arc lacking topographic features with
a vertical component. Representative valucs of density (Table 4)) drawn from the
most reliable estimates in published and
unpubhshcd work, indicate that densities
in type II habitats are characteristically
several times those in type III habitats.
Why this is so remains obscure. It is possibly due to the more homogeneous or less
patchy nature of type II substrate or prey
populations or both to reduced predation
in a harsher environment, or to the relative advantage of small body size, but
DIVERSITY
TABLE
4.
OF
TROPICAL
MABINE
Population
density of Conus spp, in intertidal
bench (type II) and subtidal
habitats (selected for geographic dispersion and large areas censused)
Total
arca
censused
(m2)
Hawaii:
Kahuku, Oahu
Hawaii:
Nanakuli,
Oahu
IIawaii:
Milolii,
Kauai
Marshall Is. : Parry Is., Eniwetok
Marshall Is.: Uliga Is., Majuro
Maldive Is. : Funidu Is., North Ma16
Seychelles Is. : Police Pt., Mah6
567
307
74
325
75
37
19
Type III
Kekcpa Is., Oahu
Hawaii:
Hawaii:
Kapaa, Kauai
Heron Is., Australia
Maldive Is. : Male Is., North Male
Maldivc
Is. : Gan Is., Addu
Chagos Is. : Ilc du Coin, Peros Banhos
Similan Is., Thailand:
Goh Huyong
Butang Is., Thailand:
Pulos Ta Ngah
Mcntawei
Is.. Indonesia:
Pulo Bai
56
669
5,000
167”
780”
613”
892”
697”
1,338”
* Estimated
339
INVERTEBMTES
from
duration
of
No. of
co-occurring
species
Density
( No./m2)
Reference
0.24
0.44
0.59
0.77
8.61
1.00
1.18
5
4
2
9
13
8
15
12
18
0.23
0.02
0.03
0.12
0.11
0.10
0.04
0.03
0.04
reef (type III)
Kohn
( 1959 )
Kahn, unpublished
Kohn, unpublished
Kohn ( 1968 )
Kahn, unpublished
Kahn, unpublished
Kohn ( 1959 >
Frank ( 1969 )
Kohn
I
( 1968 >
Kohn and Nybakken,
in prep.
census.
other hypotheses could bc advanced and
none has been tested ( Kohn 1968).
The conical shell and long narrow foot
of Conus do not adapt the animal well to
withstand heavy waves or strong currents.
These, togcthcr with the stronger effect of
wave action on the substrate in intertidal
than subtidal habitats, and lack of shelter
on a topographically
simple and unifo’rm
substrate, probably select for small body
size in populations
of bench habitats
(Kohn 1968). 0 ccurrcnce on subtidal reefs
of larger individuals of the same species,
and of large individuals of species absent
from benches, both contribute to the displacement of cumulative
size-frcqucncy
distributions
(Fig. 4) in all areas for
which comparative data are at hand. In
all casts, the differences are significant at
the 0.001 level ( Kolmogorov-Smirnov
onctailed two-sample test; Siegel 1956).
How generalized ( or specialized ) arc
the co-occurring species in their USC of
resources, particularly in habitats of types
II and III that vary in diversity of spccics
assemblages ? The measure of gencralization or “niche breadth” ( B ) used is
where Ni is the number of individuals of
species i in the sample and Niw is the
number
of these using resource unit 72
(Levins 1968). B ranges from 1 to h, the
number of resource units. It is biased in
that it assumes all resources to be equally
available; this could not bc determined
but is unlikely.
The reciprocal is a convenient index of specialization
for the
resource under consideration.
Subtidal coral reefs are patchy environments; Kohn (1968) dcscribcd 9 substrate
types cxploitcd by Conus as microhabitats.
A similar analysis gives 6 types cxploitcd
on benches. Table 5A indicates that Conus species representing a broad range of
breadth of microhabitat
type utilization
occur in reef habitats. The most specializcd spccics (C. pulicarius, C. arenatus)
occupy only or mainly one substrate type
(patches of sand); the most gencralizcd
spccics have values of B more than half
the maximum possible value, i.e., if all
340
ALAN
Shell
J.
length
KOIIN
(mm)
4. Cumulative
shell length-frequency
distributions
of Conus species on intertidal
benches
subtidal coral reefs in several parts of the Indo-West
Pacific tropics.
A. Seychelles; B. Maldivc
Chagos Islands; C. Hawaii.
In all cases, P < 0.001 (Kolmogorov-Smirnov
test: Siegel 1956).
FIG.
and
and
DIVERSITY
OF
TROPICAL
MnRINE
341
INVERTEBRATES
Pacific Coaus species in two niche dimensions, substrate type
5. Niche breadth of Indo-West
and prey species composition
of diet, in two habitat types, subticlal coral reefs and intertidal benches.
Data from more than one locale were combined to give mean values of B and B/B,,,,
except where
reef and bench samples of the same species from the same locale are compared.
Locales:
H, Hawaii;
I, Indonesia and west Thailand (other than S); M, Maldives;
S, Sanding Is., Indonesia.
Ranges of B
and B/B,,,
values are given beneath means
TABLE
Benches
Reefs
Corms
Sample
species
Locale
size
sponsalis
lividus
II
II, M, I
61
231
f lavidus
rattus
II
130
72
miliaris
M, S
ebraeus
I-1, M, S
153
chaldaeus
imperialis
coronatus
M
H
I, s
13
17
223
frigidus
M, S
95
musicus
pennaceus
M
II, I
71
152
aristophanes
catus
abbreviatus
distans
arenatus
M
S
II
H
M, 1
14
20
70
13
36
pulicarius
II
12
B
A.
H, M, 1
Microhabitat:
*
5.02
+
4.77
3.82-5.58
4.69
*
4.62
3.51-5.32
4.04
3.164.92
*
3.90
3.03469
*
3.76
2.75
2.60
1.24-3.95
2.44
1.58-3.29
2.39
2.05
1.28-2.81
2.00
2.00
1.98
1.94
*
1.26
1.11-1.41
1.00
69
Range of B,,,,
M
H
S
I-1, M, S
pennaceus
H, I
f lavidus
abbreviatus
vexillum
rattus
rattus
f rigidus
1-I
11
II
H
M
M, S
substrate
0.55
0.48
0.38-0.62
0.52
0.45
0.39-0.56
0.45
0.35-0.55
0.43
0.34-0.52
0.42
0.31
0.22
0.14-0.30
0.27
0.18-0.37
0.27
0.21
0.10-0.31
0.22
0.22
0.22
0.22
0.12
0.09-0.16
0.11
40
24
64
136
81
102
42
19
35
12
67
B
B Al,x
type
*
0.36
211
2.16
I-1
45
2.79
II
96
3.65
*
0.61
II
29
3.55
*
0.59
II
96
2.55
II
9-13
B.
musicus
sponsahs
coronatus
lividus
Locdo
S mnple
size
Food: prey species composition
0.35
6.62
II
*
0.31
6.41
0.28
5.38
0.25
*
4.89
2.24-6.80
0.11-0.36
0.30
4.50
4.05-4.95
0.29-0.31
0.21
4.39
1-I
0.15
3.25
0.10
2.00
II
0.13
*
2.79
0.05
1.00
0.09
1.70
1.22-2.19
0.06-0.12
0.47
0.43
6
142
5.78
81
4.72
0.36
26
2.16
0.17
*
0.44
-
342
ALAN
TABI,E
J.
5.
KOIIN
Continued
-----___
-_--
Reefs
Corms
species
Sample
size
Locale
miliaris
ebraeus
ebraeus
ebraeus
chaldaeus
chaldaeus
distans
imperialis
M
H
M
S
M
S
H
H
Range
of B,,,,
Benches
B
30
38
39
122
31
14
13
11
1.49
1.63
1.30
1.41
1.71
1.15
1.17
1.00
B~%,,x
0.08
0.08
0.07
0.07
0.09
0.06
0.06
0.05
*
*
*
*
*
*
13-21
c(’
h
recurrent
group
of
most
A
Bmn,x
M
I-1
M
27
122
31
1.00
1.12
1.07
*
+
0.17
0.09
0.18
H
53
1.34
*
0.10
B mnx=h
N lh
of
Sample
size
6-13
B=
* Member
Locale
frequently
Nl
occurring
substrate types were utilized equally. On
benches, the range of B is narrower. The
values are generally lower than those of
the dominant
( recurrent)
reef species;
when all spccics arc considered, the bctwcen-habitat
difference is not significant
( Mann-Whitney
U-test: P = 0.4). Holwever, the significantly
higher B/B,,?( values (P < 0.02) indicate that bench species
as a group are more generalized with
respect to their USC of available substrate
types.
In one geographic region, the species
most abundant in and characteristic
of
bench habitats were more specialized
predators than those characteristic of reef
habitats (Kohn 1968). As in the case of
substrate type utilization,
the dcgrec of
food specialization
ranges broadly when
data for more species and regions are considered (Table 5B).
Since the type II environment is more
homogeneous, reducing environmental
resistance to movement, and appropriate
food items are more acccssiblc (and their
population densities are probably greater:
Kohn and Lloyd, in prep.), food specialization is expcctcd as the more efficient
feeding strategy (MacArthur
and Pianka
1966; Emlen 1966). The fact that five of
’
>
species.
the six species represented in both parts
of Table 5B are more specialized predators on benches than reefs in the same
locale provides additional evidence in support of this hypothesis from other regions
and species. However, the values for
dominant ( recurrent ) species are spread
throughout the column, and the difference
in food niche breadth between habitats is
likcwisc not significant (P = 0.2). As in
the case of microhabitat type, bench spcties as a whole arc more generalized
with respect to their USC of the total array
of prey species exploited in the habitat
(P = 0.04).
In general, the species considered arc
more specialized as predators than with
respect to microhabitat.
With few exccptions the highest values of B for food Care
less than I/ the maximum value based on
consumption in equal proportions of all
prey species represented more than once
in diets, Such values of B for food are also
biased upward compared to substrate values, since all substrate resource units present are used to some extent by some
species. This is not true of potential food
resources, since all but one species listed
in Table 5 prey only or mainly on polychaetc annclids, and somlc polychaetes oc-
DIVERSITY
OF
TROPICAL
cur abundantly and are not catcn at all
by Conus ( Kohn and Lloyd, in prep. ) .
ECOLOGICAL
CO-OCCURRING
SIMILARITY
OF
SPECIXS
How similar ecologically arc co-occurring, taxonomically
similar species in assemblages of varying diversity? And how
many species that similar could theoretically persist in a resource-limited
assemblage? Considering
the latter question
first, the current status of theory of the
ecological niche may be traced to the
introduction
of the concept of dimcnsionality of the niche by Hutchinson
( 1958,
1965) and to his early concern with limitation of diversity and how different potentially
competing species must bc to
coexist ( Hutchinson 1959). Subsequently,
MacArthur
and Lcvins (1967) derived a
theoretical criterion for the maximal similarity that three species may have and
continue to coexist, based on the Voltcrra
equations. Levins ( 1968) proposed substituting values of niche overlap for cy, the
competition
coefficient
in the Voltcrra
equations, and proposed the “community
matrix” as a way to calculate the thcorctical maximum number of similar species
that could co-occur, given the limiting
resource set and all values of a.
Because the theory assumes a number
of conditions unlikely
to be realized or
difficult
to determine in nature, tests of
predictions deduced from it have little real
value at the present time. The assumptions include those of the Voltcrra cquations, that only carrying capacity, intrinsic
rate of natural increase, number initially
present, and effect of the numbers of the
other species present affect the rate of
population size change of a species, and
that its responses to these factors arc
instantaneous.
In addition, use of the formula of Levins
( 1968) for calculating a assumes that 1)
the niche dimensions considered are those
that serve to separate species (Levins
1968); 2) overlap in resource utilization
is equivalent to competition; 3) usable resources are equally available and rapidly
- -
MARINE
INVERTEBRATES
343
renewed; 4) spccics abundances arc identical or differcnccs are unimportant;
and
5) additional spccics considcrcd for entrance into the community matrix have
the same mean values of cx and the same
covariance of aii and ajt as those aheady
prcscnt. In the only applications of data
from natural populations to this theory to
date, where the utilization of resources by
three or more species can bc measured
an d arrayed, the predicted limiting similarity is not cxcecded (Orians and IIorn
1969; Pianka. 1969)) or is slightly exceeded
(4 spccics present, 3 predicted:
Culver
1970)) when 2-3 niche dimensions (microhabitat, foosd, time of activity)
arc included in the analyses.
In the following analysis of real situations the dimensions used are assumed
to meet the criteria listed above; the descriptive-correlative
approach used dots
not permit an indcpcndcnt determination.
Howcvcr, I have selected as dimensions
food
resources that could be used up:
an d microhabitat
space. Morcovcr, there
is no independent cvidcncc that any of
the assumptions of the model are met.
The “test” of the theory thus takes on the
character of a “this is what would happen
iY game or simulation.
However, it is
just possible that tropical marine invertebrate genera having several to many cooccurring spccics, like tropical forest Drosophila perhaps ( Lcvins 1968)) approach
the assumed conditions more closely than
other taxocencs that could be considered.
The simplest comparison of overlap of
Conus spccics with rcspcct to resources
would bc utilization
of the two majo’r
habitat types-reefs
vs. benches. However, this comparison would be meaningless, because to test the theory the numbcr of distinct resources must equal or
cxcecd the number of species in the assemblage; Lcvins ( 1968) gives proof of
this theorem,
TO compare the dcgrec of subdivision
of
microhabitat and food resources with the
theoretical limiting similarity, I computed
overlap values for all polssible species pairs
in assemblages from all geographic regions
344
TABLE
from
ALAN
J.
KOHN
6.
Observed numbers of co-occurring
species of Corms and their overlap statistics derived
a matrices compared with maximum ,numbers predicted for species packing, based on the community matrix of Levins (1968)
-Overlap
from
Region
Ihbitnt
A.
Hawaii
IIawaii
Maldive Is.
Indonesia and Thailand
Sanding Is., Indonesia
Microhabitat:
Reefs
Benches
Reefs
Reds
Rt?d
B.
IIawaii
Hawaii
Maldives
Sanding
Hawaii
IIawaii
Hawaii
Maldive
Sanding
Mean
Occu.pation
Is.
Is., Indonesia
Food:
Reefs
Benches
Reefs
Reefs
Is.
Is., Indonesia
C. Microhabitat
Reefs vs. benches
Reefs
Benches
Reefs
Reef
Covariance
of substrate types
0.63
0.014
0.79
0.007
0.50
0.050
0.32
0.067
0.34
0.086
Species composition
0.18
0.41
0.12
0.15
studied from data such as those shown in
Fig. 1 and Tables 3 and 4 of my earlier
report (Kohn 1968). Thcsc and all succeeding overlap (a) measurements rcfcrred to (Table 6) wcrc made according
to the method of Levins ( 196$).
When overlap with respect to microhabitat (occupation of different substrate
types ) is considered ( Table 6A), the numbers of species actually present in most
cases considerably exceed the maximum
numbers for species packing in the community matrix (Levins 1968)) if the latter
are calculated from observed overlap values and their means and covariances. The
predicted values would bc increased if
across
differences
in local distribution
benches (Ko,hn 1959; Kohn and Orians
1962; Kohn and Nybakkcn, in prep.) and
diffcrenccs in depth on reefs (Kohn 1968)
had been considered in the analysis. Calculations based on overlap with respect
to food (species composition of diet in
nature) ( Table 6B ) give predicted maximum numbers of species that match or
are slightly lower than the numbers ob-
statistics
N matrix
x food
0.14
0.05
0.20
0.07
0.002
No. of
species
observed
(in annlysis)
10
6
9
10
6
of diet
0.048
0.028
0.047
0.071
0.031
0.006
0.040
0.014,
<O.OOl
No. of
species
predicted
for packing
7
7
8
6
10
10
6
8
6
>E
8
21
>34
served. Combining the two niche dimensions (for each species pair the overall a
is the product of the individual
ones:
Lcvins 1968) Table 6C gives predicted
maximum numbers that in all cases equal
or exceed obscrvcd numbers.
If all assumptions of the theory were
met, this would indicate that subdivision
of microhabitat
alone is insufficient
to
separate species, subdivision of the food
resource alone is, or is nearly, sufficient,
but that the two resources taken together
provide adcquatc niche dimensionality
so
that the co-occurring species can subdivide them adequately to accommodate the
numbers of species present and avoid comThe assumptions arc
petitive exclusion.
not met. Thus the data show only that cooccurring Conus species spccializc more
to different foods than to substrate types,
and the former specialization is likely to
be somewhat more important in avoiding
potential interspecific
competition among
adults.
In addition to the difficulties
mentioned
above as inherent in applying the commu-
DIVERSITY
OF
TROPICAL
nity matrix model to real situations, two
problems specific to these analyses should
be indicated here. First, I assume that I
have identified the units of resources (food
according to prey spccics; microhabitat
according to substrate patch types : see
Kohn 1968) appropriately
as far as the
animals’ responses to them are concerned.
Secondly, the analysis in Table 6C suggests that some of the species present
could be more generalized predators (or
microhabitat
occupiers ) , or more species
could co-occur. In fact, more spccics do
co-occur (Kohn 1959, 1967, 1968) but
they are rarer and the samples studied
were too small to include in the analyses.
The generally lower overlap values for
food than for microhabitat (Table 6) suggest a more general hypothesis:
that cooccurring
predatory invertebrates
might
tend to adopt a strategy of apportioning
resources by specializing more on different prey spccics rather than subdividing
habitats distinctly.
On the other hand,
co-occurring congcncrs that feed less selectively,
especially those ca tine; mainly
particulate organic detritus, might spccializc more to different microhabitat
patch
types, while apparently overlapping more
with respect to the nature of their food.
One would expect suspension- and dcposit-feeding animals to be less efficient than
predators at specializing
to food type,
because in the former the nature of the
feeding mechanisms and the size of the
food particles require the animal to ingest
or at least contact the particles before it
can evaluate their desirability.
Since additional energy must bc expended in handling inedible material, one might expect
sclcctive particulate feeding to bc a succcssful strategy only if food abundance
were extremely prcdictablc.
It is more
efficient for a predator, o,r an herbivore
feeding on large plants (relative to its
body size), to respond only to appropriate
food items.
How specialized to microhabitat
and
food type are other predatory tropical marinc invertebrates?
The gastrolpod M&a
Zitterata, which co-occurs with Conus spc-
MARINE
INVERTEBRATES
345
ties on the intertidal
benches discussed
above, probably preys cxchrsively on a
worms, not
few spccics of sipunculan
catcn at all by Conus ( Kahn 1970) s In
IIastuZa, a genus of toxoglossan gastropods
in a family closely related to the Co,nidac,
two species co-occurring in the same zone
on surf-swept beaches in Hawaii, where
Corms is absent, are specialized predators
Howon diffcrcnt
spionid polychaetes.
cvcr, a third species occurring higher on
the beach than these, and a fourth occurring lower, are equally specialized prcdators on different spionids (Miller
1970).
In the related genus Terebra, two COoccurring spccics in patches of sand on
reefs specialize on different prey worms
( Miller 1970); one of the prey species is
also eaten by the co-occurring but uncommon Conus pdicarius,
which also eats
cchiuroids (Kohn 1959). On subtidal sandflats, however, four species of Terebra, also
specialized predators on different
polychaotcs and cnteropneusts, occupy generally distinct microhabitat patches ( Miller
1970). Like the Conus species discussed
above, these predators are pursuers of
large food items rather than searchers for
small items that cannot afford to bypass
many. Food specialization is therefore an
especially advantageous strategy for them
( MacArthur
and Levins 1964)) and scvera1 similar species, often of different
sizes, tend to co-occur (Fig, 3 and Kohn
1959, 1968; Miller 1970),
As to detritus feeders, Mr. M. A. Chartack is currently investigating
seven spetics of the brittle-star
genus Ophiocom
co-occurring on Marshall Island reefs. The
four commonest species appear to bc nonselective dc tritus feeders, although some
differcnccs in feeding method and particle
size prcfcrencc were noted, However, they
feed in diffcrcnt microhabitats and in laboratory experiments they show active prefcrcncc for the type of substrate occupied
in nature.
The limited data available thus offer
only modest suppo,rt to the hypothesis that
co-occurring predatory congeners are more
likely to spccializc to different prey spc-
346
ALAN
tics than to microhabitats, while animals
feeding on small particles are more likely
to spccializc to type o,f substrate pa,tch.
DISCUSSION
AND
CONCLUSIONS
My thesis here is that the comparative
ecological approach to groups of co-occurring, similar spccics can generate data
pertinent to hypotheses relating species
diversity, resource utilization,
and habitat
complexity and can thus help to elucidate
patterns of adaptive radiation
and the
organization of at least subunits or componen ts of communities.
Assemblages of inshore marine invcrtebrates of tropical islands in the Indo-West
Pacific region share a number of common
features. Faunal diversity is high and has
a typical taxonomic pattern of a high
average number of species per genus, because several to many genera have many
(5-30 or more) sympatric species. The
species composition of taxocen.cs and their
population density are similar in similar
habitats throughout the region. This similarity of faunal composition (Ekman 1953)
is due in large part to the common, effective dispersal mechanism of long-lived,
pelagic, planktotrophic
larvae, which renders distance less important than is the
case with
other dispersal mcchca.nisms
( IMacArthur and Wilson 1967). Strand
plants of tropical islands provide evidence
of the same phenomenon (Whitehead and
Jones 1969). The absence of species with
such dispersal mechanisms suggests an
unfavorable habitat rather than lack of immigration,
Marine invertebrate taxa such
as gammarid amphipods that lack larval
stages and whose assumed primary dispersal mechanism is rafting on detached
vegetation and debris have fewer co-occurring species per genus and a higher
degree of endemism on tropical Indo-West
Pacific islands ( Barnard 1970).
In the gastropod genus Conus, assemblagcs varying widely in species diversity
occur along the shores of tropical IndoWest Pacific oceanic islands. Marc species
co-occur, but at lower populatio,n densities,
in tonoeranhicallv
comnlex but climati-
J.
KOIIN
tally equable subtidal coral reef habitats
than in topographically
simple, climatically more scverc intertidal
bench habitats, where physical factors and restrictions
of foot and shell form also select for small
body size. As a group, Conus expands ecologically to exploit the wider range of
microhabitats
and prey species available
on reefs compared to benches. All species
occurring on benches also occur on reefs,
probably because only reefs provide suitable oviposition sites (Kohn 1959). Adults
on benches arc thus probably derived from
larvae produced on reefs. Species occurring in both habitat types are more generalized with regard to both prey ‘and
substrate type utilization
on reefs, although they must tolerate a greater amplitude of fluctuation
of climatic variables
(wave action, temperature, desiccation) on
benches. Reef species that do not occur
on benches range broadly fro,m relatively
gcneralizcd to very specialized in microhabitat and food utilization (Tables 2 and 6).
The assumptions of the theory of limiting similarity of co-occurring species arc
not met in the natural populations that I
have studied. However, there have been
few applications
of data to this recent
theoretical
advance (Orians and Horn
1969; Pianka 1969; Culver 1970) and none
dealing with assemblages of marine invertebrates. Moreover, genera of predatory
benthic invertebrates
with many co-occurring species, such as Conus, m.ay approach the assumed conditions relatively
closely, compared with other assemblages
of organisms.
Co-occurring
species of Corms overlap
more with respect to microhabitat (utilization of substrate type) than in utilization
of prey species (Table 6)) suggesting that
differences in prey taxa are not due only
to foraging
in different
microhabitats,
Comparison of observed numbers of spcties with numbers expected by the theory
of limiting similarity to persist in a community of competing species (the community matrix of Levins 1968) indicates that,
as analyzed, subdivision of the two resources, food and substrate type, would
TXCVERSITY
OF
TROT.‘ICAL
accommodate the numbers of spccics prcscnt if the assumptions of the theory wcrc
met. This result is csscntially similar to
those of Orians and Horn - (1969) for
blackbirds, Pianka ( 1969) for dcscrt liza1.ds,1 and Culver (1970) for cave crustaccans, although the limited applicability
of all of these data to the theory, as discussed in the previous section, must bc
strcsscd.
Although high spccics diversity makes
studying tropical marinc invertcbratc taxoccncs difficult because large samples arc
rcquircd whcrc the information
content
per individual is high, the availability of a
set of assemblages varying in diversity,
and of a set of species ranging from spccialized to gencralizcd in their ecological
characteristics, enhances the value of the
comparative approach, particularly
when
the stronger inferential method of manipulation experiments is technically difficult,
The dcscriptivc comparative ecolo,gical
studies discussed hcrc indicate that habitat hctcrogencity
and ccolo8gical spccialization are correlated with the high spccics
diversity of assemblages of some genera
of marinc invcrtcbratcs inhabiting tropical
island shorts and coral reefs, and may
thcrcforc bc important determinants of diversity. This approach also helps to distinguish attributes of cvolvcd rcsponscs to
environmental
variables that arc gcncral
and may be considered principles from
those that are special adaptations characteristic only of particular taxa. It would
now seem fcasiblc to obtain stronecr infcrcnccs by manipulating
populatioL
in naturc, and to evaluate the role of certain
other features of tho environment and of
the animals that arc likely to influcncc spcties diversity and population size, such as
the distribution,
availability
and rate of
utilization of suitable resources, predation,
and perhaps recruitment
success. Study
of these aspects of the ecology of tropical
inshore marine invcrtcbratcs would clearly
help to elucidate the structure and functioning
of the complex ecosystems to
which they belong.
MARINE
1NVERTERRATES
347
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Gammnriclcn
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Cutvm,
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JIOltN, 11. s. 1966. Measurement
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