Population maintenance among tropical reef fishes: Inferences from small-island endemics

Abstract

To what extent do local populations of tropical reef fishes persist through the recruitment of pelagic larvae to their natal reef? Endemics from small, isolated islands can help answer that question by indicating whether special biological attributes are needed for long-term survival under enforced localization in high-risk situations. Taxonomically and biologically, the endemics from seven such islands are broadly representative of their regional faunas. As natal-site recruitment occurs among reef fishes in much less isolated situations, these characteristics of island endemics indicate that a wide range of reef fishes could have persistent self-sustaining local populations. Because small islands regularly support substantial reef fish faunas, regional systems of small reserves could preserve much of the diversity of these fishes.

Full text

Population maintenance among tropical reef fishes:
Inferences from small-island endemics
D. Ross Robertson*
Smithsonian Tropical Research Institute (Panama´ ), Unit 0948, APO AA 34002-0948
Edited by May R. Berenbaum, University of Illinois, Urbana, IL, and approved February 27, 2001 (received for review August 3, 2000)
To what extent do local populations of tropical reef fishes persist
through the recruitment of pelagic larvae to their natal reef?
Endemics from small, isolated islands can help answer that ques-
tion by indicating whether special biological attributes are needed
for long-term survival under enforced localization in high-risk
situations. Taxonomically and biologically, the endemics from
seven such islands are broadly representative of their regional
faunas. As natal-site recruitment occurs among reef fishes in much
less isolated situations, these characteristics of island endemics
indicate that a wide range of reef fishes could have persistent
self-sustaining local populations. Because small islands regularly
support substantial reef fish faunas, regional systems of small
reserves could preserve much of the diversity of these fishes.
T
he great majority of marine organisms, including tropical reef
fishes, have pelagic larvae, and the prevailing view is that local
populations of such fishes are demographically interlinked by larval
dispersal (1–3). It is important to know whether this view is true, not
only for understanding the population biology and evolution of
these organisms, but also for their management and for reserve
design. Two recent field studies demonstrated substantial levels of
return of reef fish larvae to their natal source (self-recruitment) in
reef systems under low to moderate levels of isolation (4, 5).
Because simulations also indicate that self-recruitment likely is
common among reef fishes at such levels of isolation (6), it probably
occurs much more frequently than previously thought. This article
considers whether local populations of reef fishes in general have
the potential to persist through self-recruitment. To do so, I
examine the general biogeographic and biological characteristics of
the shore fishes endemic to seven of the smallest, most isolated
islands in the tropics: Easter Island (Polynesia); Clipperton, Cocos,
and Malpelo (eastern Pacific); and Ascension, St. Helena, and St.
Paul (central Atlantic) (Table 1). Such endemics represent vital
indicators of whether special biological qualities are required to
survive through evolutionary time in the most localized and risky
(14) situations available. If the island endemics lack special at-
tributes and simply constitute a representative cross section of the
types of reef fishes available regionally, then such fishes in general
should be capable of maintaining persistent, self-sustaining local
populations.
Shore fishes that have survived at the seven islands through
evolutionary time include not only morphologically distinct
endemic species and subspecies but also genetically distinct
populations of species that are classed presently as widespread
nonendemics. The former represent an average of 14.1% of the
seven islands’ shore fish faunas (Table 1). All of the three studies
published to date (15–17) found populations of the latter type at
two of these islands, suggesting that currently recognized levels
of morphology-based endemism probably substantitally under-
estimate the percentage of these island’s shore fish faunas that
are very long-term residents.
Endemics include members of a fifth of the genera and half the
families present in the biogeographic regions containing the
seven islands. Differences in family-level species richness among
the endemic and regional faunas follow the same general pat-
tern: most endemics belong to the families that are regionally
speciose, and none or few belong to regionally species-poor
families (Table 2). The prominent exceptions are moray eels
(Muraenidae), which are regionally species-rich but lack island
endemics. The pelagic larval duration (PLD) of morays is among
the longest known for reef fishes (23), and long distance dispersal
of moray larvae may reduce the likelihood that island popula-
tions remain sufficiently genetically isolated for endemics to
develop. Except for this case, the combined endemic fauna is
broadly representative, in taxonomic terms, of the combined reef
fish fauna of the three regions in which the seven islands occur.
Are the general biological characteristics of endemics represen-
tative of their regional faunas? First, the relative abundances of
species in various major adult-diet categories do not differ in the
endemic and regional faunas (Table 3; G ⫽ 0.38, not significant;
power to detect a small effect ⬎99%). Most endemics, like most
species in the regional faunas, are predators, and endemics are not
disproportionately represented in any particular level of the food
chain. Second, body size of endemics varies considerably (4–60 cm
in length; see refs. 7–13). Among terrestrial animals, insular forms
tend to be average-sized members of their genera (25). A similar
pattern exists among the island endemic fishes: 55.6% of 61
endemics from 40 genera occur in the middle third of their
intrageneric size-frequency distribution; 19.0% occur in the upper
third; and 25.4% occur in the lower third (G ⫽ 6.81; P ⬍ 0.01; the
null expectation is equal abundances of the three types). Although
these results might indicate that large and small members of a genus
tend to be at a disadvantage on such islands, body size is influenced
by many variables that are not necessarily related to facilitating
island living (25, 26). Because longevity broadly correlates positively
with body size among fishes (27), the longevity of endemics likely
varies widely among genera but is near average within most genera.
This aspect of the biology of island endemics in particular needs
further examination, because longevity likely affects vulnerability to
extinction resulting from occasional recruitment failures. Although
many island endemics have broad depth and habitat ranges, each
island maintains one or more endemics that is a habitat specialist
(7–13, 20). Like the vast majority of marine fishes, all of the island
endemics belong to taxa that produce externally fertilized eggs and
have pelagic larvae (1, 28). The ability to maintain self-recruiting
island populations might be affected by whether a passively floating
planktonic egg or a swimming larva leaves the island at the
beginning of the pelagic stage (larval activity might enhance
near-island retention); by the duration of that stage (shorter PLDs
might facilitate retention); and by the form, size, and swimming
capacity of end-stage larvae. The proportions of species that release
pelagic larvae (hatched from demersal eggs) vs. planktonic eggs do
not differ between the endemic and regional faunas (47.7% and
41.7%; n ⫽ 88 and 1,234, respectively; G ⫽ 0.65, not significant;
power to detect a small effect ⬎99%). Reflecting their taxonomic
diversity, larvae of taxa to which island endemics belong have widely
varying forms, end-stage sizes (⬇1–10 cm in length) and swimming
This paper was submitted directly (Track II) to the PNAS office.
Abbreviation: PLD, pelagic larval duration.
*E-mail: ross.robertson@stri.org.
The publication costs of this article were defrayed in part by page charge payment. This
article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C.
§1734 solely to indicate this fact.
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capacities, and life histories (28, 29). The literature contains infor-
mation on the PLDs of genera to which 44 endemics belong (e.g.,
ref. 1 and references therein); 20 of those species belong to taxa that
usually have PLDs ⱕ1 month, and the remainder belong to taxa
with durations of ⬇1–3 months. PLDs of insular endemics in the
eastern Pacific (including species from Clipperton and Cocos) are
not shorter than those of congeners with larger geographic ranges
(30). A similar pattern exists among Hawaiian endemic fishes (31)
and among reef fishes living at isolated small islands vs. conspecifics
in larger, less isolated areas (32, 33). Thus, the capacity to sustain
small, very isolated populations seems unrelated to variation in the
PLD. In summary, the available evidence indicates that island
endemics do not have an unusual set of basic adult and larval
characteristics that might be important for long-term maintenance
of island populations.
How rich are the faunas of these and other small islands? The
shore fish faunas of oceanic islands usually are viewed as being
depauperate, in part because of their limited area (e.g., refs. 11,
19, and 23). Area effects could be responsible for the fact that
each of the seven islands has fewer reef fishes than the region
containing it and the tendency for the larger of those islands to
have more endemics (Table 1). However, any such effects cannot
Table 1. Seven islands: Isolation, habitat area, and endemism among their shore fish faunas
Island Isolation, km
Shallow habitat, km
2
* Shorefish fauna
Now Recent range Endemism, % Total no. species
Ascension 1,300 39 24–39 25.3
†
79
Clipperton 950 4 4–11 8.8 102
Cocos 450 14 14–110 7.6
‡
224
Easter 1,500
§
72 40–72 22.2 126
Malpelo 350 1.2 1.2–17 3.2
‡
220
St. Helena 1,300 37 36–110 22.1
†
86
St. Paul 960 0.2 0.2–2 9.5 42
Data from refs. 7–13.
*Habitat ⬍50 m deep from hydrographic charts (areas include soft bottoms as well as reef); recent range is with
sea levels to 100 m below present.
†
Includes 13 species endemic to both islands.
‡
Includes two species endemic to both islands.
§
1,500 km from Ducie Island to the west and 450 km to tiny Sala y Gomez to the east.
Table 2. Taxonomic characteristics of the endemic reef fish faunas of seven islands vs. those
of regional faunas
Family*
Endemic faunas,
%
Regional faunas, %
Average Range
Group I
Gobiidae 12.4 7.0 5.8–8.9
Labridae 12.4 7.0 5.4–10.1
Pomacentridae 9.0 6.0 4.9–6.6
Serranidae 6.7 9.5 7.8–12.3
Scorpaenidae 6.7 3.3 2.3–4.1
Blenniidae 5.6 3.9 3.1–5.2
Tripterygiidae 5.6 1.5 0.4–2.8
Chaetodontidae 4.5 3.1 0.9–5.2
Chaenopsidae 3.4 2.0 0–4.7
Muraenidae 0 6.0 4.2–8.5
Group II Average Range in averages
9 Families 2.3 Family
⫺1
1.5 Family
⫺1
0.4–3.1 Family
⫺1
13 Families 1.2 Family
⫺1
0.7 Family
⫺1
0.1–3.1 Family
⫺1
Group III Average Range in averages
31 Families 0 Family
⫺1
0.7 Family
⫺1
0.1–3.1 Family
⫺1
Total fauna 88 Species, 66 genera, 1,234 Species, 341 genera,
31 Families 62 Families
Data are from refs. 7–13 and 18–22; www.biobase.org兾cloftep兾; L. Rocha, personal communication for Brazil;
and unpublished observations at all the islands except St. Paul.
*Family groups: Group I, 10 families with the highest average levels of species richness in both the regional faunas
and (except for the Muraenids) the endemic fauna; Group II, 9 families (Apogonidae, Bothidae, Callionymidae,
Gobiesocidae, Holocentridae, Monacanthidae, Pomacanthidae, Sparidae, and Tetraodontidae) and 13 families
(Belonidae, Cirrhitidae, Congridae, Creediidae, Dactyloscopidae, Kuhliidae, Kyphosidae, Mullidae, Ogcocepha-
lidae, Ophichthidae, Paralichthyidae, Scaridae, and Synodontidae) with moderate and low levels of species
richness, respectively, in the endemic and regional faunas; Group III, 31 families lacking island endemics and with
low levels of species richness in regional faunas.
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yet be separated from those of isolation, latitude, island age, and
the size of the regional source fauna. Although analyses are
lacking, the structure of the species-richness兾habitat-area rela-
tionship among reef fishes across the island-to-region scale,
comparison of the relative richness of the faunas of small islands
and much larger parts of the surrounding biogeographic regions
can provide an indication of the faunal capacity of small areas
and the ability of the members of a regional fish fauna to
maintain localized populations. I used comprehensive, island-
wide surveys of the abundance and the occurrence of juveniles
and of adults of varying sizes at Clipperton [1994 (see ref. 11) and
1998] and Cocos [1997 (see ref. 12)] to estimate which members
of an island fauna likely are residents, i.e., have self-sustaining
populations rather than being rare strays. Those surveys and data
from Malpelo (13) indicate that ⱖ80% of the species at these
islands probably are residents. These isolated islands have oce-
anic origins; therefore, their shore fish faunas were derived
entirely by long-distance dispersal, and these islands are inac-
cessible to many species with low dispersal capabilities. However,
despite this limitation and their low habitat diversity, these three
islands, which collectively represent ⬍0.1% of the continental
shelf area with reefs in the tropical eastern Pacific (34), support
one or more resident populations of 42% of the reef fishes
endemic to that biogeographic region. Further, Cocos, Malpelo,
and five other small islands affected to varying degrees by low
habitat diversity, isolation, and latitude have reef fish faunas that
are, on average, approximately two-thirds the size of the faunas
of adjacent areas that are two to three orders of magnitude larger
(Table 4). To assess the sizes of populations of endemics that can
be sustained by small islands, I censused five noncryptic endem-
ics (species readily visible to divers) at Clipperton in 1998 in 110
5-m ⫻ 20-m strip transects at various depths around the island.
Those counts indicate that ⬍4km
2
of shallow habitat supported
between 61 ⫾ 6.0 ⫻ 10
3
and 4.3 ⫾ 0.35 ⫻ 10
6
adults of different
endemics and, hence, that small areas can support large popu-
lations of individual species of reef fishes. This ability extends to
top predators; nonpelagic (as well as pelagic) sharks historically
were abundant around at least three of the seven islands (9, 38)
and currently are common at Cocos (ref. 12 and unpublished
observations). Thus, moderately small islands regularly support
relatively rich reef fish faunas and substantial populations of
individual species.
The seven islands differ greatly in the amounts of shallow
habitat they provide, amounts that have fluctuated considerably
during repeated recent ⬎100-m changes in sea level (ref. 39;
Table 1). These islands are scattered across 26° of latitude and
have differing temperature, wind, and large-scale water current
regimes. Although Ascension, Easter, and St. Helena are dry
islands, the remainder are wet. The climates of these islands
probably also varied historically. The three eastern Pacific
islands are affected directly by environmental stresses that might
be expected to cause extinctions: Clipperton by occasional
hurricanes and Clipperton, Cocos, and Malpelo by El Nin˜o-
related water heating (34). Unlike the situation with corals (34),
major environmental disruptions in the tropical eastern Pacific
produced by recent El Nin˜os apparently have had only limited
permanent effects on reef fishes, including insular endemics (one
possible localized extinction; see ref. 40). Despite a history of
mass shore fish kills caused by low-temperature stress, Bermuda,
an isolated, high-latitude coral reef, maintains a fauna of resi-
dent shore fishes that includes five shallow-water endemics and
is 63% the size of the fauna of the much larger Bahamas (41).
Thus, the risks of localized extinctions posed to reef fishes by
recent levels of such stresses seem to be relatively low, and the
fish faunas of oceanic islands evidently persist under strongly
fluctuating environmental conditions.
The diverse and historically unstable environments of the seven
islands, the abundance of shore fishes that are long-term survivors
at those islands, the diversity of their endemics and the lack of
special general characteristics among them, the large population
sizes of endemics, and the relative richness of small-island reef fish
faunas together indicate that such fishes in general have good
prospects for long-term survival as self-sustaining populations in
areas similar in size to the larger among the seven islands consid-
ered here. Terrestrial biological reserves that are intended to
preserve high levels of diversity are large and interconnected to
maintain low-density populations of organisms such as trees, birds,
and mammals and to take advantage of the fact that species richness
increases with area. Small terrestrial reserves suffer declines in
Table 3. Relative abundances of fishes with different diets in
island endemic and regional faunas
Diet
Species with each diet, %
Endemics Regional faunas
Animals
Mobile 50.0 52.1
Sessile 12.5 11.3
Zooplankton 18.2 15.4
Sessile algae 12.5 14.0
Sessile algae and animals 6.8 7.0
See Table 2 for sample sizes. Diets based on genus and family characteristics
(11, 20, 24).
Table 4. Relative richness of reef fish faunas of small islands vs. those of much larger adjacent
areas
Small island Larger adjacent area
Small island habitat area
Small island fauna, %
of larger area faunakm
2
% of larger adjacent area
Cocos Galapagos ⬇6* ⬇0.9* 79.1
Malpelo Galapagos ⬇0.1* ⬍⬍0.1* 71.5
Gorgona Costa Rica–Ecuador
†
14* ⬍0.1* 57.6
Navassa Four West Caribbean atolls ⬇8 ⬇0.2 80.0
Rose Atoll Four Samoan islands ⬇7 ⬇0.7 67.1
Pitcairn Tuamotu Islands ⬇8 ⬍0.1 66.2
Rapa Tuamotu Islands ⬍10 ⬍0.1 61.6
*Habitat data are from hydrographic charts and ref. 34. * indicates areas of reef rather than total habitat;
remaining areas are of total habitat.
†
Continental coastline. Data for faunas: Cocos, Malpelo, and Gorgona are from refs. 11–13, 35, and 36, and
www.biobase.org兾cloftep兾; Navassa (Eastern Caribbean) are from B. Collette (personal communication); Rose
Atoll are from A. Green (personal communication); Pitcairn and Rapa (South Pacific) are from refs. 10, 18,
and 37.
Robertson PNAS
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diversity when they become isolated by degradation of surrounding
habitat (42). The presumption that management of reef fishes must
be organized at large spatial scales derives from the perception that
their populations demographically are widely interlinked by larval
dispersal (3). However, if local shore fish populations normally are
self-sustaining, the diversity that exists in a small marine reserve
established now likely will remain largely intact. A system of small
reserves dispersed throughout a biogeographic region to include the
geographic ranges of the broadest range of resident species should
thus have a good chance of preserving most of that region’s diversity
of reef fish species, genera, and families for the foreseeable future.
Small reserves cannot provide a solution to resource problems, such
as rapidly diminishing fisheries for shore fishes, and thus cannot
duplicate important functions of large reserves. However, despite
such limitations, small-reserve systems represent an important tool
that can be readily incorporated in regional conservation plans for
preserving diversity per se among reef fishes.
J. Caselle, K. Clifton, J. Earle, M. Lang, and S. Swearer assisted with
fieldwork. This work was financed by National Geographic Society Grant
5831-96 and the Smithsonian Tropical Research Institute and was
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