www.sciencemag.

org/cgi/content/full/1122039/DC1

Supporting Online Material for

Scaling of Connectivity in Marine Populations
R. K. Cowen,* C. B. Paris, A. Srinivasan

To whom correspondence should be addressed. Marine Biology and Fisheries,

Rosenstiel School of Marine and Atmospheric Science, University of Miami, 4600
Rickenbacker Causeway, Miami, FL 33149, USA. E-mail: rcowen@rsmas.miami.edu

Published 15 December 2005 on Science Express

DOI: 10.1126/science.1122039

This PDF file includes

Materials and Methods
Fig. S1
Table S1
References

Cowen, Paris and Srinivasan

Supporting Online Material
www.sciencemag.org
Material and Methods
Figure S1
Table S1
References

Materials and Methods

Model Description
An individual dispersal event from any given spawning effort defines one of many
possible outcomes given the inherent variation in ocean circulation (both spatially and
temporally) and available recruitment habitat. Therefore, in order to define the true
dispersal kernel (defined as the probability of successful recruitment in x,y space),
multiple dispersal events were evaluated to encompass the full range of possibilities and
frequency of occurrence. To achieve this, we examined dispersal originating from 260
separate locations corresponding to the wider Caribbean coral reef habitat (see below)
every 30 days over a 5-yr period, resulting in a total of ca. 60 temporal replications.
When the spatial distribution and amplitude of successful settlers are accumulated from
each release site, a connectivity matrix can be built representing the dispersal outcome
from each source location. (Note that the sampling frequency, i.e. every 30 d, exceeds the
minimum time [10 d] required to eliminate correlation in flow among dates).

Cowen, Paris and Srinivasan

To quantify the effective geographical distances and connectivity among coral reef fish
populations in the wider Caribbean region, we used a combination of models. First, a GIS
environment was used to model a set of reef areas within the study region, which are
linked through complex and diverse oceanographic regimes. Second, since the currents
represent a functional connection among reefs and contribute to the probability of
successful dispersal of larvae (or connectivity), we used a circulation model to depict
varying currents in time and space within the study area. Third, daily output from the
circulation model was used offline in a Lagrangian biological model that tracks
individual virtual larvae (i.e., pelagic dispersive phase of coral reef fishes) with a range of
passive to active behaviors. Virtual larvae were tracked within the modeled environment
(i.e., including currents and coral reef habitat) until they settled on suitable habitat.
Larval Dispersal Model
Spawning Sites and Settlement Habitat The domain of the study site is bounded by
5oN-35oN latitude and 90oW-55oW longitude, and consists of a heterogeneous landscape
of coral reefs with complex water flow. Using GIS, the coral reef habitat was represented
by a series of 260 contiguous or distant areas that were mapped in vector format (i.e.
polygons) and were the basis for the coral reef map for the region. These polygons,
identified via remote sensing imagery at multiple scales, were standardized to 500 m
resolution (S1) and buffered with a 9 km sensory zone (S2) for use in the analysis,
matching both the spatial resolution of the ocean model and the extent of the retention
zone in vertically migrating coral reef fish larvae (S3). They differ widely in biotic (e.g.,
coral cover and threat levels) and abiotic characteristics (e.g., geomorphology, orientation
in the current), but they are all similar in area (ca. 50 km X 9 km or 450 km2). These reef

Cowen, Paris and Srinivasan

polygons were defined in the model as nodes (Ni), each representing a habitat patch i =
1,,n (where n = 260) and located by spatial centroid (lat, lon) and described by its size
(Si). For this modeling experiment all Si where equal.
Ocean Circulation Model The Miami Isopycnal Coordinate Ocean Model (MICOM) is
an isopycnic vertical coordinate ocean model with a coastal extent of 20 m. MICOM was
developed using the theoretical foundation set forth in references (S4- S6). The Atlantic
model has very high equatorial resolution and latitudinal resolution of 1/12 or ~ 8 km for
each variable at mid-latitudes. MICOM uses bottom topography from a digital terrain
data set with 5' latitude-longitude resolution (ETOPO5) and a coastal boundary set at the
20-m isobath with 16 coordinate surfaces in the vertical. For more information about
MICOM, see the RSMAS web page

(http://oceanmodeling.rsmas.miami.edu/ micom/).

The source code is also available from this web page.

In the present connectivity study, velocity fields from MICOM years 1979-1983 (forced
by true daily winds of the European Center for Medium-Range Weather Forecasts,
ECMWF) were coupled to a particle-tracking code to perform Caribbean-wide
simulations of larval dispersal, encompassing coral reef species spawning and settlement
sites. Extrapolating velocities from the ocean model boundary to the shoreline, without
modifying velocities in the interior, supplied a diffusive coastal boundary to the existing
velocity field and simulates transport into shallow areas where most of the reef polygons
are located (i.e. beyond the 20 m bathymetry) within the 5N-35N and 55W-90W
domain.
ParticleTracking Code - An offline Lagrangian code module was developed to track the
trajectory of individual particles (larvae) within the fluid as a function of time. The

Cowen, Paris and Srinivasan

particles were released within the ocean domain and then moved along the underlying
model-generated velocity fields by a fourth order Runge-Kutta integration of the
Ordinary Differential Equation (S7). Mesoscale to small scale turbulences modify the low
frequency mean flow in the region. Therefore, at each time step a random displacement
selected from a Gaussian distribution through a Markov process was added to the
particles to parameterize the effects of the physical processes occurring at length scales
smaller than the resolution of the ocean model (S8, S9), resulting in a diffusivity
coefficient of ca. 105 cm2s-1. Additional functionality includes the automatic tracking of
particles (larvae) from user selected spawning locations. The particles are essentially
independent of each other and therefore the model was a good candidate for parallel
computation. The parallel implementation of this model used a master-slave paradigm in
which the master process reads in the number of particles and distributes a set of these
particles to the slave unit. Each slave unit accesses the velocity data from the data files
independently and moves the particles for a specified time interval and, when finished,
requests more work from the master. A beta version of the parallel offline code has been
successfully run on a 20-Processor LINUX Cluster linked by Ethernet at the University
of Miami. Each workstation is equipped with 2 AMD-Athlon processors, 1GB of main
memory, and 30 GB of storage. The cluster was used for efficient simulations of larval
transport, primarily in dedicated mode (1 process per processor). The code exhibits a
nearly linear scalability and is suitable for high throughput computations.
Larval behavior (i.e. onset of active behavior), sensory capabilities within 9 km of the
settlement habitat (i.e. leading to recruitment to reefs located within the sensory zone,
SZ) and complex species-specific reproductive strategies (spawning schedules, site

Cowen, Paris and Srinivasan

selection, and pelagic larval durations, PLDs) were introduced as parameters or
incorporated within the tracking algorithm to control the virtual larval trajectories (S10,
S11). Specifically, during ontogeny, flexion of the larval notochord allows for formation
of the caudal fin and increased swimming ability (S12). Therefore, the timing of
notochord flexion represented a benchmark for the onset of active behavior in the model.
We note here that the retention mechanism is modeled following empirical data obtained
for damselfishes from observations near Barbados, where surface currents can reach 120
cm/s and have an average speed of 15 cm/s (S3). Nonetheless, data show that on average,
retention occurs at nearly 100% after the onset of vertical migration, which occurs at the
flexion stage (5-8 day for the bicolour damselfish). Here we used 15 d as the start of the
retention mechanism, which is conservative and probably underestimates self-recruitment
for most short- and medium lived species (i.e. gobies, and damselfishes). When we lower
this value to 5 d, it corresponds to the observations for damselfishes. Sensitivity analysis
on the onset of active behavior of the virtual larvae in the model was therefore performed
for day 5, 15, and 30. In this modeling scenario, an active virtual larva, among an
ensemble of larvae released at a spawning event, is retained for the remainder of the
larval duration before recruiting successfully if its trajectory, which is subjected to the
underlying velocity field (i.e. deterministic velocity) and to random displacement (i.e.
turbulent velocity), intercepts a SZ located in the diffusive coastal boundary. Otherwise,
it continued its trajectory until the end of the PLD or until it intercepts a SZ. Mortality at
the end of the transport scenario occurred at 100% for simulated larvae that are outside
SZ at the end of PLD. In contrast, passive virtual larvae could only recruit within the SZ
at the end of the PLD.

Cowen, Paris and Srinivasan

Simulations of Spawning Events From each of the 260 nodes, a spawning event
comprised of 1000 particles/modeled species was released on a monthly basis for 5 years,
simulating lunar cyclic production (ca. 16 10

particles/species). Successful larval

recruitment was measured by the number of larvae reaching a suitable habitat (i.e. reef
polygon) at the end of a selected larval period or PLD (range = 15-45 d) with a series of
active larval behavior scenarios (i.e. onset of larval behavior ranging from 5 to 30 d; note
that virtual larvae are typically advected out of their source node within a maximum of 12 days after release). Successful recruitment was thus calculated as the percent of
surviving virtual larvae, scaled by natural mortality occurring during the larval pelagic
period, which typically ranges between 0.1-0.5 d-1 (S13). Some definitions: successful
recruitment refers strictly to supply of larvae to settlement habitat and does not include
post-settlement processes; local recruitment refers to self-recruitment within the same
node (i.e. within 50 km of the release location); subsidy recruitment designates import of
larvae from areas outside of the release node, while total recruitment represents both
recruitment from within the release node (local recruitment) and outside the release node
(subsidy recruitment).
Model Output and Data Analysis The results of dispersal simulations were output in
two types of files: animation files and polygon files. The animation files (i.e., coordinates
at time steps) serve to plot particle trajectories, while polygon files (i.e., source node Ni
and time at arrival node Nj) were used to plot the probability distribution of particles or
dispersal kernels, to build transition matrices of source/receiving sites, and to map
connectivity using Graph Theory (S14). Connections between nodes were represented by
several types of matrices:

Cowen, Paris and Srinivasan

The distance matrix D = dij represents the functional distances between patches ij
measured as the minimum distance centroid-to-centroid.

The dispersal probability matrix P = pij represents the probability that an

individual in node i will disperse to node j.

The adjacency matrix (or edge) A = aij is a binary matrix in which each element is
defined as aij = 1 if node i and j are connected, otherwise aij = 0. The diagonal of
A is set to zero (i.e., no self loop) and A is generated from P by choosing a
threshold probability to define adjacency.

The expected flux from node i to node j is:

Fij = Si/Stot * pij , where Si = size of i
Stot = Si
pij = pij /pi or proportion of probability of dispersal
Validation Model validation has been accomplished on several levels. First,
comparisons of Atlantic inflow to the Caribbean Sea between observations of velocity
and transport (S15) and MICOM in the Florida Straits (NW region) and the Yucatan
Channel (SW region) agree well, as well as mean total transport from MICOM model
years 1979-1984 (S16). In addition, MICOM mean simulated surface velocities (i.e.
mixed layer) in this region do not statistically differ from observations of in situ surface
drifters (see Fig. 4d, in reference [S17]). Second, the Lagrangian scheme and the
biological components of the coupled model have been validated at various scales by
comparison of (1) predicted passive trajectories and their variance with oceanic floats
released off Barbados (see Fig. 12, in reference [S9]) and in the Intra-American Seas
region (IAS, http://www.iaslinks.org/ias-rto.html, see Fig. 4, in reference [S18]), (2)

Cowen, Paris and Srinivasan

predicted active (i.e. ontogenetic vertical migration) virtual larval trajectories and
observed larval patches (see Fig. 6, in reference [S3]), and (3) the estimated recruitment
levels generated by active larval behavior with those observed at Barbados (see Fig. 6, in
reference [S10]).
Demographically-Relevant Recruitment - Estimates of demographically-relevant
recruitment is a balance between the adult mortality rates, the spawning potential (i.e., the
number of females in the population times the mean reproductive output of each female),
and larval survival (which is related to larval mortality rate and larval duration).
Populations of species with low adult mortality rates (e.g. long-lived species such as
grouper and snapper) require much lower annual recruitment rates than short-lived
species. The proportion of the population that is composed of sexually mature females
can range from 0.5 - 0.15, generally being lower for long-lived species due to delay of
onset of sexual maturity. However, individual spawning output is generally higher for
longer lived species because of the larger size attained. At the same time, many smaller
species increase their annual reproductive output by spawning frequently during the year
as compared to some large species such as grouper, which are known to spawn only
during a narrow window of time each year (S19, S20). Finally, the number of surviving
larvae resulting in potential settlers is driven by larval mortality rates and the larval stage
duration. Three separate examples are shown in Table S1 for species differing in adult
mortality (and consequently, longevity), spawning output and total larval mortality.
Using these variables, a range of proportions of successful settlers (i.e. settling larvae that
survived the pelagic phase) required to sustain a constant population size was estimated.

Cowen, Paris and Srinivasan

Figure S1 Probability density function standardized by settlement levels (i.e.
proportion of surviving virtual larvae) given the probability of dispersal (i.e. dispersal
kernels) for coral reef fish larvae with a 30-d PLD and onset of behavior at 15 d as a
function of the spawning site (i.e. from the source node (Ni): Dispersal kernels (solid
lines) and cumulative recruitment (dotted line) (A) averaged (n = 260) over the entire
Caribbean region ( prob. dist.(Nij) /Ni ), (B) averaged over sub-regions of the
Bahamas Bank, (C) averaged over sub-regions of the Greater Antilles, and (D) averaged
for Haiti. A vertical line dropped at the intersection of the cumulative curve with a
specific recruitment level (e.g. 0.1 = level required to sustain long-lived species such as
snapper and groupers), provides an estimate of minimum dispersal distance required.

Cowen, Paris and Srinivasan

Table S1. Overview of calculations for estimating demographically relevant settlement rates for a range of life histories. A range of
adult mortality rates are utilized to calculate age structures and longevity of adults, which then were matched to common species as
examples. The following parameters were taken from the literature for the chosen example species (S21-S26), or best estimates were
made when specific values were not available: Age at first maturity, fecundity, number of spawning events per year, larval duration,
and larval mortality rate. Based on the number of eggs produced per year, and the ensuing typical larval mortality, the resulting
proportion of surviving larvae needed to settle to replenish the population is estimated as the number of required settlers divided by
number of potential settlers surviving larval stage (AE).
Species

Annual
Mortality
Rate

Longevity

Required
Settlers*

Age at
50%
Maturity

Number
of
Females

Fecundity

Spawning
Events per
Year

Eggs
Produced
per Year

BCD
1,552,500,0
00
42,000,000
47,250,000

Snapper

0.2

~ 15 yr

239

4-5

230

75,000

90

Damselfish
Goby

0.9
2.0

~ 4-5 yr
~ 1-2 yr

1460
6400

1-2
1

350
1890

2500
500

56
100

Pelagic
Larval
Duration

Larval
Mortality
Rate

Number of
Surviving
Larvae

45

0.3

2128

Proportion of
Surviving
Larvae
Required to
Settle/yr
A/E
0.11

30
30

0.3
0.3

5200
5831

0.28
1.097

Exponent (Z) of annual mortality in exponential population growth model Nt = N0e(b-Z)t

* Number of new Age 0 settlers required to maintain a standard sized population (N=1000) of Age 1+ fish, assuming the same annual
mortality rate. In fact, mortality may be expected to be higher during the first year on the reef, which would require even higher
proportion of available settlers to settle, i.e. this number is a conservative estimate for evaluating population connectivity. No densitydependent mortality is accommodated in this simplification.

Numbers of adults in each population that is female was estimated based on age of maturity for comparable species (i.e. those listed
in the table), a simple age distribution based on the modeled mortality rates, and the assumption of a 1:1 male:female ratio of mature
adults.

Gobies mature at ca. age 5 month, therefore the number of mature females exceeds the number of Age 1+ individuals in the standard
population.

10

Cowen, Paris and Srinivasan

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