BIOLOGICAL

CONSERVATION

Biological Conservation 126 (2005) 297–305

www.elsevier.com/locate/biocon

Review

Coral reefs: Conserving the evolutionary sources

John C. Briggs *

Georgia Museum of Natural History, University of Georgia, Athens, GA 30602, United States

Received 26 June 2004; received in revised form 6 May 2005; accepted 3 June 2005
Available online 28 July 2005

Abstract

The current worldwide degradation of coral reefs constitutes an international problem that calls for immediate attention. A mul-
titude of conservation hotspots scattered over the circumtropical seas have been identified, but there has been no general agreement
as to how to attack the problem. The major difficulty seems to be the lack of a priority system. Are some reefs more important than
others? If so, where are they located and what needs to be done? Some reefs are located in areas where the biodiversity (species,
genera, families) is exceptionally high and where there is evidence of past and present evolutionary production. These areas are
called centres of origin and one is located in the Indo-Pacific Ocean and the other in the Atlantic. The Indo-Pacific centre, located
in the East Indies Triangle, is considered to be the primary tropical center due to its broad geographic influence. The Atlantic centre,
located in the southern Caribbean Sea, is considered a secondary centre because its influence is restricted to the tropical Atlantic.
These centres, although occupying relatively small geographic areas, are evidently the source of dominant species that have played
the major role in assembling coral reef communities across each ocean. The existence of the two centres permits one to realize that,
in the coral reef environment, there is a geographical separation between process and pattern. Recognition of the separation will
allow significant improvements in conservation planning. The evolutionary process in the centres must be protected in order to
maintain the outlying diversity patterns.
Ó 2005 Elsevier Ltd. All rights reserved.

Keywords: Reef conservation; Marine diversity; Centres of origin; Indo-West Pacific; Caribbean Sea

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 298
2. The East Indies centre . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 298
3. The Caribbean centre . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 300
4. Evolutionary influence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 301
5. Conservation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 301
6. Marine reserves . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 302
7. Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 303
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 303
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 303

*
Present address: 82-651 Sky View Lane, Indio, CA 92201, United
States.
E-mail address: clingfish@earthlink.net.

0006-3207/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biocon.2005.06.018
298 J.C. Briggs / Biological Conservation 126 (2005) 297–305
1. Introduction
We need a conservation strategy to protect the evolu-
tionary process that is responsible for the creation of high
diversity (Bowen, 1999). When one attempts to separate
process from pattern, it becomes necessary to consider
evolution within its biogeographic context. Aside from
their esthetic and commercial value, the highest diversity
centres are important because they have an evolutionary
function. Palaeontological investigations, representing
extended periods of geological time, indicate that success-
ful new species, genera, and families are most often
produced in high diversity, tropical settings (Jablonski
and Bottjer, 1990a,b), i.e., ‘‘diversity begets diversity.’’
At the present time, the highest marine diversity is
found among the coral reefs in a relatively small region
of the tropical Indo-West Pacific Ocean (IWP). This
region, called the East Indies Triangle (Fig. 1), extends
from the northern Philippines to the Malay Peninsula
and eastward to just beyond New Guinea (Briggs,
1995). A diversity centre for the Atlantic Ocean may be
found among the coral reefs in the southern part of the
Caribbean Sea (Fig. 2). When the two diversity centres
are considered from a functional standpoint, it becomes
possible to separate process from pattern and to take a
new approach to the problem of coral reef conservation.
2. The East Indies centre
The concentration of diversity in the East Indies
Triangle has been recognized by biologists for more
Fig. 1. Location of the East Indies Centre of Origin.
Fig. 2. Location of the Southern Caribbean Centre of Origin.
than 60 years (Ekman, 1935) and three principal expla-
nations for its existence have been published. Of the
three theories, the most popular has been the accumula-
tion hypothesis. This theory proposed that many of the
species in the Triangle had arisen in peripheral areas and
had been transported inward by ocean currents or
tectonic means. The second theory proposed that the
diversity center was formed by an overlap of the Indian
Ocean and western Pacific faunas. The third theory
proposed that the Triangle represented a centre of
evolutionary origin that produced dominant species
capable of spreading throughout the IWP and beyond.
The considerable increase in knowledge that has
taken place, especially over the past 10 years, now
makes it possible to propose answers to the questions
of the significance and origin of the East Indies diversity
centre. Within the IWP, it has been possible to identify
six coincidental biogeographic patterns that are critical
for the centre of origin hypothesis (Briggs, 1999a). The
first and most well known is that of species diversity.
Extending from the Triangle in any direction, there is
a decreasing gradient in the number of species. Within
some clades, there also appears to be a similar gradient
for genera. The second pattern is that of the geological
age of certain genera and species in which age increases
with distance from the East Indies. The third pattern is
that of dispersal tracks. By determining the evolutionary
relationships within certain families, some authors have
inferred historical routes of dispersal outward from the
East Indies. The fourth pattern is that of phylogenetic
relationship in which the species of the East Indies reefs
tend to be more advanced (apomorphic) compared to
their peripheral or deep-water relatives. Pattern five is
that created by extinctions. The drama of extinction
often makes its debut in the East Indies, gradually
 J.C. Briggs / Biological Conservation 126 (2005) 297–305
spreads outward, and plays itself out among relict pop-
ulations far from their centre of origin. Pattern six takes
the form of a decreasing gradient of genetic diversity (as
determined by molecular studies) that extends from the
diversity centre eastward across the Pacific.
The foregoing six biogeographic patterns, when con-
sidered together, appear to provide strong support for
the presence of a centre of origin. In comparison, the
idea that the high diversity of the East Indies is caused
by an overlap of the Pacific and Indian Ocean faunas
(Woodland, 1983) is not viable. The fauna of the Indian
Ocean immediately west of the East Indies is virtually
the same as that immediately to the east (Allen and
Adrim, 2003). Although about 52 closely related fish
species are separated by the Malay Peninsula (Randall,
1998), that number is so small compared to the total fish
fauna (3000+ species) that it is insignificant. In order for
an overlap to notably enhance diversity, the two faunas
would have to be significantly different.
The accumulation theory was originally proposed by
Ladd (1960), who described many Tertiary molluscan
fossils from atolls in the Central and Western Pacific
representing species that no longer lived in those areas.
When he found that some of the old species he described
were still living in the higher diversity centre, he thought
that the original faunistic centre was located in the
islands of the Central Pacific and that prevailing winds
and currents had carried species into the Indo-Malayan
area. The Tertiary species that Ladd found were later
determined to be geographical relicts that once had very
broad or circumtropical distributions. In regard to a few
such species, the East Indies can be considered a last
refuge (Vermeij, 1978). The accumulation theory has
continued to be supported (Santini and Winterbottom,
2002; Bellwood and Wainwright, 2002), but fossil and
contemporary biogeographic evidence is lacking (Briggs,
2004).
Results are now available from two broad-scale
analyses of the coral reefs that extend across the Indian
and Pacific oceans. The first (Connolly et al., 2003) ana-
lyzed the ranges of 727 hermatypic coral species and
1766 reef-associated fish species. The results indicated
that the latitudinal range midpoints clustered very close
to the equator, thus illustrating a ‘‘mid-domain’’ effect
(Colwell and Lees, 2000). In contrast, it was found that
the longitudinal range midpoints clustered directly over
the East Indies, a location far to the west of the
midpoint of the Indo-Pacific Ocean. In searching for
an answer to the longitudinal anomaly, Connolly et al.
decided upon a ‘‘gyre effect’’ by which westward flowing
currents would drive the biodiversity patterns. This may
be considered an application of the accumulation
theory.
The second analysis (Mora et al., 2003) was entirely
devoted to reef fishes. Distributional data for 1970
species from 70 locations were examined. When the
299
ranges of the individual species were plotted, the latitu-
dinal and longitudinal patterns proved to be similar to
those found by the first research group, but the reason
given for the longitudinal anomaly was much different.
Mora et al. pointed out that the unimodal, longitudinal
cluster of midpoints in the East Indies would not be
compatible with either the overlap or the accumulation
hypothesis. With an overlap, one would expect a
bimodal longitudinal curve, and an accumulation from
elsewhere should shift the curve toward the source with
a tail extending that direction.
Mora et al. (op. cit.) also found that the mean pelagic
larval duration, in the two families for which sufficient
information was available, was negatively correlated
with distance from the East Indies. Considering that
the species richness in the two families was also nega-
tively correlated with distance, it was concluded that
the decline in species richness, as one moved away from
the East Indies, was probably due to dispersal limita-
tions. Another significant finding was that 86% of the
species in reef communities across the Indo-Pacific were
also present in the East Indies. They concluded that
speciation in and dispersal from the East Indies played
the major role in assembling communities throughout
the Indian and Pacific oceans.
In addition to the two broad-scale surveys, a detailed
study of the coral reef fishes of the Indonesia has been
published (Allen and Adrim, 2003). Indonesian waters,
as defined by the authors, include the inner part of the
East Indies Triangle south of the Philippines. This work
recorded a total of 2057 species. If the area were to be
expanded to include the remainder of the Triangle, the
species diversity would likely exceed 3000. The number
of coral reef fishes that exist in the entire Indo-Pacific
has been estimated by Allen and Adrim (op. cit.) to be
3764. This means that more than three fourths of the
reef species in the Indo-Pacific, a region that stretches
across two thirds of the globe, also occur within the East
Indies, an area that represents a small fraction of the
whole. Some 97 species were considered to be endemics.
A significant finding was that the endemics tended to be
clustered in four different regions of the Triangle. This
suggests the possibility that the four regions may repre-
sent local areas of evolutionary origin. If so, they would
deserve special attention in conservation planning.
More recently, a general biodiversity study, involving
distributional data for 2983 species within the East
Indies vicinity, has been published (Carpenter and
Springer, in press). This information for this study was
derived from the 1998–2001 FAO Species Identification
Guide for Fishery Purposes (Carpenter and Niem, 1998–
2001). Consequently, the data pertained to a broad mix
(marine plants, invertebrates, vertebrates) of the larger,
commercially important species but omitted the smaller
species of less economic value. Included in the database
were 2047 fish species from coral reefs as well as other
300 J.C. Briggs / Biological Conservation 126 (2005) 297–305
habitats. Despite the bias toward the commercial
species, the authors concluded that there was a higher
concentration of species per unit area in the Philippines
than anywhere in Indonesia. However, both the Philip-
pines and Indonesia are located within the East Indies
Triangle (Fig. 1) so a biogeographic distinction between
the two areas does not appear to be justified.
The East Indies centre became established in its pres-
ent location about 10 million years ago and palaeonto-
logical data have helped to reveal its previous history.
The earliest cowries (Cypraeidae) were found to occur
in the Paleocene of Pakistan and India (Kay, 1990).
The earliest coral reef fish assemblage has been found
in the Eocene rocks of Monte Bolca in Italy (Bellwood,
1996). Reef corals were not well developed in the East
Indies until the early Miocene (Wilson and Rosen,
1998). In the Tethys Sea, the area of greatest molluscan
diversity extended from Europe and North Africa to
India (Piccoli et al., 1987). Beginning in the mid-Eocene,
there was a substantial increase in the molluscan diver-
sity of Java. By the late Miocene, the diversity centre
in the East Indies was evidently well established.
It seems clear that the late Mesozoic and early
Tertiary location of the tropical centre of origin was in
that part of the Tethys Sea that extended from Europe
and North Africa to India. Two important events were
probably responsible for the eastward migration of the
centre. First, in the mid-Eocene the global temperature
began to decline. Second, the early Miocene collision
between Africa and Eurasia eliminated the Tethys and
established the Mediterranean. The tropical biota that
was trapped in the Mediterranean gradually disappeared
as the climate got colder. A contributing factor was
probably the continuing fusion of India to Asia, with
the formation of the Arabian Sea and the Bay of Bengal.
The northern parts of these two seas, with mud and sand
bottoms, do not support coral reef communities.
It is important to realize that the influence of the East
Indies Centre extends far beyond the IWP. Two princi-
pal barriers separate the IWP from the other tropical
shelf regions. They are the deep-water East Pacific
Barrier that lies between Polynesia and the New World,
and the Old World Land Barrier comprising Africa and
Eurasia. A variety of IWP species have crossed the for-
mer to become established in the Eastern Pacific (EP).
These include 80 fishes (Robertson et al., 2004) and 61
gastropod molluscs (Emerson, 1991). Conversely, there
have been few successful migrations in the opposite
direction. Twenty-two shore fishes have apparently
migrated westward, but 12 of them do not extend past
Hawaii. None of the molluscan lineages has been able
to invade the IWP from other tropical regions (Vermeij,
2004). About 95% of the EP coral species are recent
immigrants from the IWP (Robertson et al., op. cit.).
This predominant eastward invasion has occurred
despite the fact that the north equatorial current has
been shown to carry larval stages from the EP towards
the IWP (Scheltema, 1988). Similarly, the other bound-
aries of the IWP appear to function essentially as
one-way filters. Some tropical shore species have been
able to migrate westward around the Cape of Good
Hope to colonize the Atlantic, but there seems to have
been little traffic from the Atlantic to the IWP. Since
the opening of the Suez Canal in 1869, more than 200
species of IWP organisms have established themselves
in the Mediterranean, but less than a dozen have taken
the reverse course (Por, 1978). When the biota of the
other three tropical regions is examined (EP, Western
Atlantic, Eastern Atlantic), the relationship to the
IWP seems obvious. Most of the families and a large
fraction of the genera are shared among all four. Many
of the families and the older genera certainly predate the
rise of the East Indies centre some 10 million years ago.
The beginnings of such older taxa probably took place
in the diversity centre of the Tethys Sea.
3. The Caribbean centre
Although the subaerial rise of the Isthmus of Panama
did not form a complete marine barrier until the late
Pliocene, there are indications that the reef fauna of
the Caribbean began to separate from that of the
Indo-Pacific in the late Miocene, about 7 million years
ago (Muss et al., 2000). During the intervening time, a
new evolutionary relationship became established within
the Atlantic. A diversity centre developed within the
southern part of the Caribbean Sea, but its present spe-
cies richness is far less than that of the East Indies. For
example, the latter probably supports about 3000 fish
species compared to about 700 in the Caribbean (Rocha,
2003). Similarly, there are about 450 hermatypic coral
species in the East Indies compared about 50 in the
Caribbean (Veron, 1995).
The shelf fauna of the Eastern Atlantic (EA) tropics
is separated from that of the Caribbean by the deep-
water mid-Atlantic Barrier. The overall species diversity
of the EA is only about one third that of the Caribbean
(Briggs, 1985). Recent research (Joyeux et al., 2003) has
revealed the presence of 92 trans-Atlantic species of reef
fishes, the great majority of them belonging to well-
developed Caribbean genera. Circumstantial evidence
indicates an eastward migration, with only four species
apparently having traveled in the opposite direction.
Works on several groups of West African invertebrates
appear to indicate the same kinds of relationships
(Briggs, 1974). Within the Western Atlantic (WA),
Caribbean species have apparently been penetrating to
the north into Florida and Bermuda and southward into
Brazilian waters (Rocha, 2003). These are indications
that the Caribbean has been operating as a centre of
origin. The entire tropical portion of the WA has been
 J.C. Briggs / Biological Conservation 126 (2005) 297–305
referred to as a centre of origin (Briggs, 2003) but this
designation is better restricted to the southern part of
the Caribbean.
4. Evolutionary influence
The influence of a centre of origin depends on the
occurrence of successful speciation within a very
competitive environment. A review of speciation modes
in the IWP indicated that all three types (allopatric,
parapatric, sympatric) have apparently been active
(Briggs, 1999b). Aside from the mode, the success of
the speciation process is probably dependent on the size
of the population involved and its geographic location.
It has been proposed that the centrifugal speciation
model (Brown, 1957) is applicable to centres of origin
(Briggs, 2000). It predicts that ultimately successful
species are produced by large, central populations. In
contrast, the peripatric theory (Mayr, 1954) would have
the successful species arise from small peripheral popu-
lations. Genetic variation appears to be driven mainly
by population size (Kimura and Ohta, 1971) and small
populations may undergo additional losses through
genetic drift. The greater the genetic diversity, the
greater the adaptive potential. There is a highly signifi-
cant correlation between heterozygosity and population
fitness (Reed and Frankham, 2003).
As many systematic works have demonstrated
(Helfman et al., 1997), widespread geographic patterns
consisting of a mosaic of closely related species or
subspecies, are often traceable to the previous existence
of a broadly distributed ancestral species. The presence
of such a mosaic, with its evidence of many allopatric
(often vicariant) speciation events, has led many investi-
gators to conclude that this mode of speciation has been
predominant. It probably is in terms of the total number
of speciation events, yet these accidental byproducts of
genetic divergence (Coyne and Orr, 2004) are evidently
not successful in producing species that will continue
to spread and establish phyletic lines. It is the formation
of the ancestral species by natural selection in its centre
of origin that is the event of primary evolutionary
significance.
It is important to note that elements of the tropical
biotas have been able to extend their ranges by means
of latitudinal dispersal. Fish families in high latitudes
are generally older than those of the tropics. Tropical
bivalve faunas are significantly younger than non-tropical
ones (Flessa and Jablonski, 1996). The steep latitudinal
gradients of the youngest bivalve clades provided addi-
tional evidence that the tropics have served as a major
source of evolutionary diversification (Crame, 2000).
As a result, the tropics may be seen as a species pool
supplying taxa to the higher latitude regions. In view
of the information now available about the East Indies,
301
it seems that most successful tropical origins have been
taking place in that centre. This view is substantiated
by fossil evidence of patterns of increasing age, in corals
and other groups, that extend outward from the East
Indies (Briggs, 1999a).
5. Conservation
The East Indies is the primary centre of origin in the
marine environment. It is evidently the source of a series
of successful species that have spread across the entire
Pacific and Indian oceans, and often to other tropical
regions and into higher latitudes. Also, there appears
to be good evidence for the recognition of a secondary
centre of origin in the southern part of the Caribbean
Sea. As long as these centres maintain their diversities,
natural selection will supply species that are increasingly
better adapted and more competitive. It is the continu-
ous dispersal of species from the centres that apparently
permits peripheral habitats to maintain their diversity.
The evolutionary process, as it responds to changes in
the physical and biological environment, functions most
efficiently in centres of origin where populations possess
relatively high levels of genetic variation. If such a centre
is damaged to the extent that its operation is compro-
mised, the evolutionary process will be less responsive
to changes in the environment. If this happens, the inev-
itable outcome will be a further erosion of the present
species diversity.
Perhaps even more important, the presence of an
operating centre of origin means that well adapted spe-
cies will be available to augment ecosystem recovery. In
regard to coral reefs, many of which are severely affected
by overfishing and other causes, a natural recovery is
possible. In cases where the cause can be removed, the
damage can eventually be repaired by the recruitment
of individuals (and species) from elsewhere. Nearly all
reef fish species possess pelagic larval stages and,
although dispersal by currents is important, many can
actively seek places to settle (Leis and McCormick,
2002), but coral larvae are generally less mobile. In gen-
eral, damage to a peripheral pattern is repairable as long
as the evolutionary process at the source is protected and
there is no barrier to prevent gene flow. If the source is
compromised, the damage is likely to be permanent. A
conservation emphasis on source should not mean a
neglect of the pattern. Many outlying reefs are unique
in terms of their species endemism, local diversity, and
ecosystem structure. But there must be a priority system,
for every coral reef cannot be equally protected.
A total of 97 fish species have been identified as ende-
mic in Indonesia, an area that occupies the inner part of
the East Indies Triangle (Allen and Adrim, 2003). Mora
et al. (2003) identified 90 such species and considered
them to be neo-endemics that were recently derived
302 J.C. Briggs / Biological Conservation 126 (2005) 297–305
and had yet to expand their ranges. If true, this conclu-
sion would mean that these, and the other short-ranged
neo-endemics belonging to the many invertebrate
groups, represent the evolutionary future of the Indo-
Pacific. As they spread out, they will replace many of
todayÕs common, widely distributed species. Future hu-
man generations will be able to appreciate these new
species and their descendants provided we protect signif-
icant portions of the East Indies.
Although the East Indies Triangle is small compared
to the vast extent of the IWP, it covers an impressive
geographic area including all of the Philippines, the lower
Malay Peninsula, and the large islands of Borneo,
Sulawesi, Sumatra, Java, and New Guinea. It also in-
cludes thousands of small islands that lie in the interven-
ing areas. Much of Malaysia and the Philippines
support dense human populations and all of their coral
reefs have been degraded, many severely so. Aside from
the reef structures, overfishing is evident in many areas
so artisanal and commercial fisheries are no longer pro-
ductive. Without additional protection, the damaged
reefs and overfished populations will not recover.
In contrast, the Caribbean Centre occupies a much
smaller geographic area and its species diversity is much
lower. Nevertheless, coal reefs under the influence of this
centre, extend from Bermuda south to about Rio de
Janeiro, and eastward to the offshore islands of the EA.
In the southern Caribbean there are many short-ranged
species that are probably neo-endemics with significance
for the future of the entire tropical Atlantic. Although reef
deterioration is circumtropical, and many of the causes
are common to most areas, it is evident that the most
severe damage has occurred in the WA. During the past
30 years, the average hard coral cover in the Caribbean
Basin has been reduced by 80% (Gardner et al., 2003).
While some of the decline appears to be due to the detri-
mental effects of bioerosion caused by increased nutrients
(Hallock et al., 1993), the major cause appears to be overf-
ishing (Pandolfi et al., 2005). Overfishing of the large
herbivorous and carnivorous vertebrates reduces the pop-
ulation control on smaller species. When some smaller
species become too crowded, they are vulnerable to
disease. In the mid 1980s, more than 99% of the Diadema
antillarum populations were eliminated by an infectious
disease. The removal of this important herbivore allowed
many of the reefs to be overwhelmed by algae to the extent
that they have not been able to recover. In addition, the
lower population sizes of the WA coral species, and
probable lower genetic diversity, suggest that they are less
resilient to detrimental influences.
6. Marine reserves
In many parts of the world, Marine Reserves or
Marine Protected Areas have been established long
enough to permit evaluations of their effectiveness. A
recent study has shown that not only are such reserves
beneficial but they can produce almost immediate
results. A total of 112 assessments conducted in 80
reserves indicated increases in individual organism size,
biomass, and species diversity (Halpern and Warner,
2002). But, the most remarkable result of this study
was the indication that these increases reached their
mean levels in 1–3 years, and that the increased levels
were consistent for up to 40 years. In some situations,
a longer recovery time may be required. An assessment
carried out in the Philippines suggested that populations
of large predatory reef fishes may require 15–40 years
for full recovery (Russ and Alcala, 2004). Considering
such results, the case for marine reserves appears to be
well supported, but the question of their placement
involves political and social considerations as well as
biological justification.
There are many publications devoted to the selection,
design, objectives, and management of marine reserves.
It has been argued that there are two divergent stances
concerning optimal management (Jones, 2001). The
‘‘top down’’ approach is characterized as being govern-
ment-led and science-based with an emphasis on preser-
vation. The ‘‘bottom up’’ stance involves the human
community with science guidance and an emphasis on
multiple use. In some Philippine reserves, the latter
approach appears to be working quite well (White and
Vogt, 2000). The ultimate decision to use one or the
other, or to adopt a middle-ground approach, will prob-
ably depend on the distribution of human as well as
marine populations.
Conservation priorities for biodiversity hotspots
found on tropical reefs in various parts of the world
have been popular (Roberts et al., 2002). Hotspots were
chosen using two primary criteria, species diversity and
endemism. However, these two criteria do not correlate
well (Hughes et al., 2002; Briggs, 2002). Almost all reef
areas that harbor relatively large numbers of endemics
are located on the fringes of the tropics, and many of
them are confined to small oceanic islands. Typically,
these are places with low species diversity but with a
high percentage of endemics. Studies of historic patterns
of extinction and replacement suggest that the endemic
species found in such places are phylogenetic relicts or
are derived from relictual lineages that have speciated
in isolation (Briggs, 1999c). Certainly, many such
endemics represent important parts of our biological
heritage and ought to be conserved, but do they rate a
high priority? In any case, they usually exist in small
populations with poor prospects for long-term
persistence.
Recently, there have appeared several articles by
authoritative biologists and conservationists on the
coral reef crisis. The most important were written by
Pandolfi et al. (2005) who decried the terrible condition
 J.C. Briggs / Biological Conservation 126 (2005) 297–305
of the US coral reefs, Bellwood et al. (2004) who urged a
reassessment of current management practices, Pandolfi
et al. (2003) who urged the adoption of a common goal
to reverse the reef degradation, and Hughes et al. (2003)
who were concerned with the resilience of the reefs under
human and climatic change impacts. The concern about
resilience is important, for resilience depends on the
ability of populations to adapt to change. Such adaptive
potential is determined by the level of genetic variation,
and that variation is apparently highest in the centres of
origin. Previous authors have not recognized that process
and pattern are geographically separated, so this phenom-
enon had not been considered from a conservation
viewpoint. The establishment of marine reserves or ‘‘No
Take Areas’’ are commonly recommended and are
supported by most of the recent literature.
Political realities will require the willingness of the
individual nations to recognize the need and to cooper-
ate in the designation of reserves of sufficient size to
conserve the evolutionary process. The Australian gov-
ernment was able to exert its influence in order to have
the Great Barrier Reef (GBR) recognized as the first
marine World Heritage Site. That designation has been
most helpful in achieving conservation status for parts
of that reef (about 33% is now fully protected). Yet, as
marvelous as the GBR is, its diversity does not match
that of the East Indies. The GBR represents part of
the pattern, most of which is the product of the evolu-
tionary process in the East Indies. Additional biological
survey work will need to be done in order to select
reserve locations within the East Indies Triangle and
in the Caribbean, but the need for action is immediate
and should not be made to wait upon years of survey
work. The various reserves should have a collective
effect so that the species are represented by populations
large enough to retain a high level of genetic diversity.
At present, the greatest species diversity in reef fishes
appears to be in the vicinity of the island of Flores in
Indonesia (Allen and Adrim, 2003). Reef-coral diversity
appears to be high throughout the East Indies Triangle
(Veron, 1995).
Considering that most families of tropical marine
organisms are represented by more species in the East
Indies than anywhere else in the world, and that many
of them are still poorly known in a taxonomic sense, it
would be practical to choose an indicator group to rep-
resent overall diversity in a prospective reserve site. The
same course of action would seem to be indicated for the
Caribbean. Perhaps the group with the greatest hetero-
geneity would provide the best model (Beger et al.,
2003). But so far, it is the research on the fishes that
has provided most of our information about evolution
and distribution in the tropical seas. Invertebrate groups
such as the nematodes, annelids, arthropods, and mol-
luscs are more speciose than the fishes but, in general,
they are less well known. In the final analysis, it is the
303
welfare of the ecosystem that is of conservation concern,
not that of its individual components.
7. Conclusions
The continuing degradation of coral reefs has become
an agonizing reality to biologists, conservationists, and to
those of the general public who value them for their
beauty and diversity of animal life. Many reefs have
already devolved into piles of rubble that only support
seaweed. In recent years, much research has been devoted
to the identification and characterization of conservation
hotspots that need immediate attention. The result in the
marine environment has been the identification of numer-
ous hotspots scattered over the world ocean, mainly in
the tropics. Certainly, it has been worthwhile to call atten-
tion to all those places but the lack of a priority system
presents a quandary. If it can be assumed that we want
to protect the places of highest diversity and also the pro-
cess that produces diversity, the choices become obvious.
The East Indies possesses the greatest species, generic,
and family diversity and it also functions as the oceanic
worldÕs primary centre of evolutionary radiation. The
Caribbean Sea evidently contains a secondary evolution-
ary centre. The hotspots that are located peripheral to
these centres represent more of the pattern and less of
the process. This is not a suggestion that we ignore the
pattern but, in terms of priority, it should be secondary.
If we first concentrate on the process, benefits to the pat-
tern should follow. To set aside significant portions of the
centres as reserves or marine parks will be a huge under-
taking and will require unprecedented international
cooperation, but this is an important first priority. If
marine biologists from many nations can agree upon this
conservation procedure, it will be an important first step.
Neither centre has been completely neglected. Several
organizations have projects in both areas but none of
them approach the broad-scale effort that is mandated.
Conservation organizations and governments must be
persuaded that the present diversity and evolutionary
future of the marine world is at stake.
Acknowledgements
I thank B.W. Bowen, C.C. Lindsey, J.S. Nelson, and
J.C. Ogden for their helpful comments on the manu-
script. I am indebted to the University of Georgia for
continued facility support.
References
Allen, G.R., Adrim, M., 2003. Coral reef fishes of Indonesia.
Zoological Studies 42, 1–72.
304 J.C. Briggs / Biological Conservation 126 (2005) 297–305
Beger, M., Jones, G.P., Mundy, P.L., 2003. The conservation of coral
reef biodiversity: a comparison of reserve selection procedures.
Biological Conservation 111, 53–62.
Bellwood, D.R., 1996. The Eocene fishes of Monte Bolca: the earliest
coral reef fish assemblage. Coral Reefs 15, 11–19.
Bellwood, D.R., Wainwright, P.C., 2002. The history and biogeogra-
phy of fishes on coral reefs. In: Sale, P.F. (Ed.), Coral Reef Fishes.
Academic Press, San Diego, pp. 5–32.
Bellwood, D.R., Hughes, T.P., Folke, C., Nystrom, M., 2004.
Confronting the coral reef crisis. Nature 429, 827–833.
Bowen, B.W., 1999. Preserving genes, species, or ecosystems. healing
the fractured foundations of conservation policy. Molecular
Ecology 8, S5–S10.
Briggs, J.C., 1974. Marine Zoogeography. McGraw-Hill, New York.
Briggs, J.C., 1985. Species richness among the tropical shelf regions.
Biologiya Morya 6, 3–11 (in Russian).
Briggs, J.C., 1995. Global Biogeography. Elsevier, Amsterdam.
Briggs, J.C., 1999a. Coincident biogeographic patterns: Indo-West
Pacific Ocean. Evolution 53, 326–335.
Briggs, J.C., 1999b. Modes of speciation: Indo-West Pacific. Bulletin of
Marine Science 65, 645–656.
Briggs, J.C., 1999c. Extinction and replacement in the Indo-West
Pacific Ocean. Journal of Biogeography 26, 277–283.
Briggs, J.C., 2000. Centrifugal speciation and centres of origin. Journal
of Biogeography 27, 1183–1188.
Briggs, J.C., 2002. Letter to the editor re: Roberts et al., 2002. Science
296, 1026.
Briggs, J.C., 2003. Marine centres of origin as evolutionary engines.
Journal of Biogeography 30, 1–18.
Briggs, J.C., 2004. Older species: a rejuvenation on coral reefs? Journal
of Biogeography 31, 525–530.
Brown Jr., W.L., 1957. Centrifugal speciation. Quarterly Review of
Biology 32, 247–277.
Carpenter, K.E., Niem, V.H., 1998–2001. FAO Species Identification
Guide for Fishery Purposes. The Living Marine Resources of the
Western Central Pacific, 6 vols. FAO, Rome.
Carpenter, K.E., Springer, V.G., 2005. The center of marine shorefish
biodiversity: the Philippine Islands. Environmental Biology of
Fishes (in press).
Connolly, S.R., Bellwood, D.R., Hughes, T.P., 2003. Indo-Pacific
biodiversity of coral reefs: deviations from a mid-domain model.
Ecology 84, 2178–2190.
Colwell, R.K., Lees, D.C., 2000. The mid-domain effect: geometric
constraints on the geography of species richness. Trends in Ecology
and Evolution 15, 70–76.
Coyne, J.A., Orr, H.A., 2004. Speciation. Sinauer Associates, Sunder-
land, MA.
Crame, J.A., 2000. Diversity gradients in the marine realm: evidence
from the composition of recent bivalve faunas. Paleobiology 26,
188–214.
Ekman, S., 1935. Tiergeographie des Meeres. Akademische Verlagsg-
eschellschaft, Leipzig, Germany.
Emerson, W.K., 1991. First records for Cymatium mundum (Gould) in
the Eastern Pacific Ocean, with comments on the zoogeography of
tropical trans-Pacific tonnacean and non-tonnacean prosobranch
gastropods with Indo-Pacific faunal affinities in west American
waters. Nautilus 105, 62–80.
Flessa, D.W., Jablonski, D., 1996. Geography of evolutionary
turnover. In: Jablonski, D., Erwin, D.H., Lipps, J. (Eds.),
Evolutionary Paleobiology. University of Chicago Press, Chicago,
pp. 367–379.
Gardner, T.A. et al., 2003. Long-term region-wide declines in Carib-
bean corals. Science 301, 958–960.
Hallock, P., Mullerkarger, J.C., Hallas, J.C., 1993. Coral-reef decline.
Research and Exploration 9, 358–378.
Halpern, B.S., Warner, R.R., 2002. Marine reserves have rapid and
lasting effects. Ecology Letters 5, 361–366.
Helfman, G.S., Collette, B.B., Facey, D.E., 1997. The Diversity of
Fishes. Blackwell Science, Oxford.
Hughes, T.P., Bellwood, D.R., Connolly, S.R., 2002. Biodiversity
hotspots, centres of endemicity, and conservation of coral reefs.
Ecology Letters 5, 775–784.
Hughes, T.P. et al., 2003. Climate change, human impacts, and the
resiliance of coral reefs. Science 301, 929–933.
Jablonski, D., Bottjer, D.J., 1990a. The ecology of evolutionary
innovation: the fossil record. In: Nitecki, M.H. (Ed.), Evolutionary
Innovations. University of Chicago Press, Chicago, pp. 253–288.
Jablonski, D., Bottjer, D.J., 1990b. Onshore-offshore trends in marine
invertebrate evolution. In: Ross, R.M., Allmon, W.D. (Eds.),
Causes of Evolution. University of Chicago Press, Chicago, pp. 21–
75.
Jones, P.J.S., 2001. Marine protected areas: issues, divergencies, and
the search for the middle ground. Reviews in Fish Biology and
Fisheries 11, 197–216.
Joyeux, J.-C., Floeter, S.R., Ferreira, C.E.L., Gasparini, J.L., 2003.
Solving the South Atlantic puzzle requires more data, not more
speculation. Journal of Biogeography 30, 1461–1463.
Kay, E.A., 1990. Cypraeidae of the Indo-Pacific: fossil history and
biogeography. Bulletin of Marine Science 47, 23–34.
Kimura, M., Ohta, T., 1971. Theoretical Aspects of Population
Genetics. Princeton University Press, Princeton.
Ladd, H.S., 1960. Origin of the Pacific island molluscan fauna.
American Journal of Science 258-A, 137–150.
Leis, J.M., McCormick, M.I., 2002. The biology, behavior, and
ecology of the pelagic, larval stage of coral reef fishes. In: Sale, P.F.
(Ed.), Coral Reef Fishes. Academic Press, New York, pp. 171–199.
Mayr, E., 1954. Change of genetic environment and evolution. In:
Huxley, J., Hardy, A.C., Ford, E.B. (Eds.), Evolution as a Process.
Allen and Unwin, London, pp. 157–180.
Mora, C., Chittaro, P.M., Sale, P.F., Kritzer, J.P., Ludsin, S.A., 2003.
Patterns and processes in reef fish diversity. Nature 421, 933–936.
Muss, A., Robertson, D.R., Stepien, C.A., Wirtz, P., Bowen, B.W.,
2000. Phylogeography of Ophioblennius: the role of ocean currents
and geography in reef fish evolution. Evolution 55, 561–572.
Pandolfi, J.M et al., 2003. Global trajectories of the long-term decline
of coral reef ecosystems. Science 301, 955–958.
Pandolfi, J.M. et al., 2005. Are US coral reefs on the slippery slope to
slime? Science 307, 1725–1726.
Piccoli, G., Sartori, S., Franchino, A., 1987. Benthic molluscs of
shallow Tethys and their destiny. In: McKenzie, K. (Ed.), Shallow
Tethys 2, Proceedings International Symposium on Shallow Tethys
2. A.A. Balkema, Rotterdam, pp. 333–373.
Por, F.D., 1978. Lessepsian Migration. Springer, Berlin.
Randall, J.E., 1998. Zoogeography of shore fishes of the Indo-Pacific
region. Zoological Studies 37, 227–268.
Reed, D.H., Frankham, R., 2003. Correlation between fitness and
genetic diversity. Conservation Biology 17, 230–237.
Roberts, C.M. et al., 2002. Marine biodiversity hotspots and conser-
vation priorities for tropical reefs. Science 295, 1280–1284.
Robertson, D.R., Grove, J.S., McCosker, J.E., 2004. Tropical trans-
pacific shore fishes. Pacific Science 58, 507–565.
Rocha, L.A., 2003. Patterns of distribution and processes of speciation
in Brazilian reef fishes. Journal of Biogeography 30, 1161–1171.
Russ, G.R., Alcala, J.C., 2004. Marine reserves: long-term protection
is required for full recovery of predatory fish populations.
Oecologia 138, 622–627.
Santini, F., Winterbottom, R., 2002. Historical biogeography of Indo-
western Pacific coral reef biota: is the Indonesian region a centre of
origin. Journal of Biogeography 29, 189–205.
Scheltema, R.S., 1988. Initial evidence for the transport of teleplanic
larvae of benthic invertebrates across the east Pacific barrier.
Biological Bulletin 174, 1445–1452.
Vermeij, G.J., 1978. Biogeography and Adaptation. Harvard Univer-
sity Press, Cambridge.
 J.C. Briggs / Biological Conservation 126 (2005) 297–305 305

Vermeij, G.J., 2004. Nature: An Economic History. Princeton
University Press, Princeton.
Veron, J.E.N., 1995. Corals in Space and Time. University of South
Wales, Sydney.
White, A.T., Vogt, H.P., 2000. Philippine coral reefs under threat:
lessons learned after 25 years of community based conservation.
Marine Pollution Bulletin 40, 537–550.
Wilson, M.E.J., Rosen, B.R., 1998. Implication of paucity of corals in
the Paleogene of SE Asia: plate tectonics or centre of origin. In:
Hall, R., Holloway, J.D. (Eds.), Biogeography and Geological
Evolution of SE Asia. Backhuys, Leiden, pp. 165–195.
Woodland, D.J., 1983. Zoogeography of the Siganidae (Pisces): an
interpretation of distribution and richness patterns. Bulletin of
Marine Science 33, 713–717.