Closer to the rear edge:

ecology and genetic diversity down the core-edge gradient

of a marine macroalga
,2 R. JACINTO,2 C. A. MONTEIRO,2
G. I. ZARDI,1 K. R. NICASTRO,2, E. A. SERRAO
1

AND

G. A. PEARSON2

Department of Zoology and Entomology, Rhodes University, Grahamstown 6140 South Africa
2
CCMAR (Centre of Marine Sciences), Campus Gambelas, 8005-139 Faro, Portugal

Citation: Zardi, G. I., K. R. Nicastro, E. A. Serrao, R. Jacinto, C. A. Monteiro, and G. A. Pearson. 2015. Closer to the rear
edge: ecology and genetic diversity down the core-edge gradient of a marine macroalga. Ecosphere 6(2):23. http://dx.doi.
org/10.1890/ES14-00460.1

Abstract. A fundamental goal in ecology is to understand distribution and abundance of species.

Peripheral populations inhabiting the trailing-edge of a species distribution may carry considerable
ecological and evolutionary value yet being most threatened under predicted climate change scenarios.
However, the nature of species distributional limits and the ecological and genetic implications of living at
low latitude rear edges remain unclear. The assumption that population abundance declines towards range
edges, where environmental selective pressure increases, is the basis of a wide range of ecological and
evolutionary predictions. Empirical data have provided contrasting evidence about the consequences of
living at low latitude distributional limits, raising concerns regarding their generality and highlighting the
need for combined multidisciplinary tests. Here, we provide a long-term, comprehensive evaluation of
latitudinal patterns in genetic diversity, demographic, morphological and life history traits in the marine
macroalga Fucus guiryi.
The center to edge transition was mirrored by increasing water and air temperature gradients, with sea
surface temperature of coldest months being the most relevant influence on F. guiryi traits. Overall, we
identified a strong correlation between ecological data, collected over one year at bimonthly intervals, and
distance to the range center. We found decreasing population and individual size towards distributional
margins. Similarly, reproductive capacity, threshold size for reproduction, density of reproductive
population and recruitment rates showed a core to edge reduction. Temporal variability of individual
reproductive effort and recruitment rates did not conform to the general pattern. In contrast, population
genetic data did not show a core-edge gradient, as gene diversity and allelic richness were not significantly
lower at edge populations, contradicting predictions of higher drift and bottlenecks for smaller edge
populations.
The contrasting support provided by genetic and ecological data highlights the need to combine multiple
and cross-disciplinary evidence for a comprehensive understanding of ecological and evolutionary
mechanisms linked to species ranges.
Key words: allelic richness; distributional limits; Fucus spp.; peripheral populations.
Received 24 November 2014; accepted 5 December 2014; published 12 February 2015. Corresponding Editor: D. P. C.
Peters.
Copyright: 2015 Zardi et al. This is an open-access article distributed under the terms of the Creative Commons
Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the
original author and source are credited. http://creativecommons.org/licenses/by/3.0/
E-mail: katynicastro@gmail.com

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ZARDI ET AL.

2006, Eckert et al. 2008). Abundance patterns,

and demographic parameters in general, appear
to be driven by interacting fluctuations of several
environmental factors and are more variable than
originally thought (e.g., Gaston 2009, Viejo et al.
2010). Relative to the core, southern edge
populations of many species show lower intrapopulation genetic diversity and increased interpopulation genetic divergence due to habitat
fragmentation, increased random genetic drift,
bottleneck effects, and reduced gene flow (Arnaud-Haond et al. 2006, Provan and Maggs 2011,
Assis et al. 2013). However, there is increasing
doubt as to the generality of this correlation
(reviewed in Eckert et al. 2008). Population
demography and diversity can be asymmetrical
at low latitudes as rear-edge populations might
inhabit former refugial areas, and thus contain
intrinsically greater genetic diversity, not just
within- but also between-edge populations (Diekmann and Serrao 2012, Assis et al. 2013). These
contrast with leading edges resulting from
expansions carrying founder effects (e.g., postglacial recolonizations; Marko et al. 2010).
The lack of convincing evidence and the
contrasting genetic predictions emphasize the
need to combine information about geographical
distributions of abundance with similarly scaled
demographic and population genetic data. Overlaying datasets for several parameters may
provide novel, broader insights into the complex
patterns of species distribution and allow reevaluation and refinement of current macroecological and evolutionary hypotheses (Abeli
et al. 2013). Furthermore, another major drawback to detecting biogeographic patterns has
been the scarcity of medium/long-term data
series directed to address macroecology of
population dynamics. Few studies have highlighted the critical importance of long-term,
sustained observations of biota for large scale
ecology studies (e.g., Lima et al. 2007a, Wethey et
al. 2011, Mieszkowska et al. 2014a, Mieszkowska
et al. 2014b). Seasonal studies carried out on
several consecutive sampling dates have provided stronger support for biogeographic hypotheses relative to snapshot sampling schemes (i.e.,
one sampling date per year, Defeo et al. 2001,
Lesica and McCune 2004, Abeli et al. 2012).
Additionally, although several studies have
quantified variation in trait means rather than

INTRODUCTION
Characterization of species geographic ranges
and their borders is fundamental in ecology,
evolution and conservation biology. The study of
geographic ranges is experiencing renewed interest prompted by current habitat and global
climate changes and their profound influence on
distributional patterns of a wide variety of taxa
(e.g., Chen et al. 2011, Nicastro et al. 2013,
Freeman and Class Freeman 2014). Research has
mainly targeted high latitude limits of species
distributions also favoured by the relatively
easier access to sampling sites and funding
availability. On the other hand, populations
residing at the low-latitude margin of species
distribution ranges or trailing edges have only
recently started to receive deserved attention
(e.g., Hampe and Petit 2005, Araujo et al. 2011,
Lepais et al. 2013, Ferreira et al. 2014).
The general assumption is that population
abundance, reproductive output and recruitment
decline towards rear edges where conditions are
expected to be less favorable (Castro et al. 2004,
Hampe 2005, Viejo et al. 2010). This straightforward view is based on the idea that within the
realized niche of a species, rapid and/or steady
changes in abiotic and biotic conditions affect
individual performance, and thus population
size. These ecological and demographic premises
have been used to predict how genetic diversity
varies among populations across the geographical range of species. Much of the research
focused in contrasting central vs. low latitude
peripheral populations is prompted by the
interest in understanding whether marginal
populations have reduced genetic diversity
translating into reduced fitness and lower adaptive capacity relative to larger central populations
(Pearson et al. 2009, Hampe and Jump 2011,
Lepais et al. 2013).
The benign center view of species distribution
is supported by abundant empirical evidence
across a wide range of taxa and habitats (Jump
and Woodward 2003, Guo et al. 2005, Angert
2006, Fenberg and Rivadeneira 2011, Langlois et
al. 2012). However recent reviews and metaanalyses of experimental studies have raised
concerns regarding the generality of this hypothesis showing support by 39% of the reviewed
studies (Sagarin and Gaines 2002, Sagarin et al.
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measuring the variance, geographical trends in

either demographic or neutral genetic parameters
are rarely subjected to statistical testing and few
studies have assessed geographical or temporal
variability in the amount of phenotypic or
genetic variation.
In this study, we move beyond earlier studies,
focused either on specific traits or on once-off
measurements, to provide a multi-trait comprehensive assessment of ecological assumptions of
species distribution, and related population
genetic implications, using demographic, morphological, life history, and genetic diversity
information of a dominant intertidal macroalga.
We focused on the Atlantic Iberian coastline
because it is characterized by a strong latitudinal
gradient in air and sea water temperature
throughout the whole year (e.g., Lima et al.
2007a, Assis et al. 2013, Nicastro et al. 2013) and
marks the geographic limit of many marine
species (e.g., Perez-Ruzafa et al. 1993, Boaventura
et al. 2002, Lima et al. 2007b, Diekmann and
Serrao 2012). We selected the ecosystem-building
brown macroalga Fucus guiryi as model species.
First, we determined its current distributional
range and endpoints along the Iberian Peninsula.
Second, we assessed whether individual and
population traits, recorded along a gradient from
core to rear edge of this species and averaged
across one year of measurements, showed a
gradual decline with distance to the center. Third,
we tested the prediction that gene diversity and
allelic richness were highest at the center of the
range and declined towards the southern range
limit. Finally, we assessed whether the environmental gradient from core to margin is correlated
to all measured biotic variables.

female (oogonia) gametangia. Sperm and eggs

are released from antheridia and oogonia respectively after expulsion from the receptacle, and
fertilization is external. There are no planktonic
stages, zygote attachment develops during 412
h post-fertilization.
Only the continuous distributional range sustained by steady environmental gradients along
Iberian shores was considered for the calculation
of location Range Indexes and all the measurements (see Results). Other relatively restricted
populations separated by hundreds to thousands
of kilometers (to the north and the south of
Iberia), sustained by discontinuous environmental conditions, were not included. The species can
also be found in isolated pockets of cold
upwelling in Morocco (K. R. Nicastro and G. I.
Zardi, personal observation) and after a major gap
along western France it reappears again in
Brittany and the British islands ( personal observation). Further investigation is needed to understand whether these populations are selfsustained and which environmental conditions
allow their persistence.

Determination of the geographical center

of a continuous range
Extensive field surveys were carried out
during low spring tides between 2011 and 2013
on rocky intertidal shores along the Atlantic
North African, Iberian and French coastlines.
Locations were visited at least twice, covering
winter and summer months; two observers
performed searches lasting approximately 60
min across all microhabitats present. To avoid
micro- and meso-scale variations, all locations
had a similar orientation towards incoming
waves, with no obstructing structures and lay
on open stretches of exposed coast. Mean wave
action does not differ greatly along the north and
west coast of Portugal, which is exposed to the
prevailing northwest oceanic swell. On the south
coast, wave conditions are less severe because it
is not exposed to the North Atlantic swell (Costa
1994, Boaventura et al. 2002, Marquet et al. 2013).
To standardize the position of each experimental locations within the species range, a Range
Index (RI) was calculated as in (Sagarin and
Gaines 2002): RI 2(L  S)/R; where L is the
position (i.e., the distance in km) of a location
relative to the range limit, S is the mid-point of

METHODS
Model species and study area
Fucus guiryi is a canopy-forming, intertidal
rocky shore, hermaphrodite macroalga, recently
described by Zardi et al. (2011). Fucus spp. are
dominant bioengineers along northern hemisphere shores and can influence coastal species
richness by modifying habitats, increasing spatial
complexity and facilitating the presence of other
species (Seed and OConnor 1981). Reproductive
tissue (receptacles) develops at the apices and
contains conceptacles with male (antheridia) and
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at bimonthly intervals over a one year period

(January to December 2012). At each sampling
date and location, four independent 30 cm 3 30
cm quadrats were haphazardly chosen at the
middle of the vertical range of the species. All the
algae inside each quadrat were counted. For each
individual we determined length, maximum
circumference (measured with a tape around
the widest part of the frond), and number of
receptacles of all intact individuals (i.e., with no
visible breakage, as might happen a result of
hydrodynamic force or grazing). A subsample of
algae was carried back to the laboratory for
further processing.
Population density and density of the reproductive population were estimated as the density
of the algae within the vertical range of the
species (i.e., number of algae or of reproductive
algae per quadrat) standardized to the locations
mean percentage cover. This was estimated as the
average species cover at the location, assessed on
two different sampling occasions as the proportion of (vertical) transects covered by the species
(as in Murray et al. 2006). For this, a baseline tape
was laid out along the upper edge of the
intertidal zone, parallel to the shore. A pointintercept transect was then surveyed perpendicular to the horizontal tape at each 5-m interval,
for a total of five transects per site and a total of
100 equidistant sampling points per transect.
Individual biomass per quadrat was calculated
as the average dry weight of five haphazardly
chosen adult individuals per quadrat.
Individual number of mature oogonia (IMO)
was calculated as follows: IMO C 3 MO; where
C is the average number of conceptacles counted
in three to five receptacles and MO is the average
number of mature oogonia counted under a
compound microscope from three sectioned
conceptacles. Mature oogonia were defined as
those in which cleavage furrows were evident
(Pearson et al. 1998). To estimate individual
reproductive effort, IMO was subsequently averaged across five haphazardly chosen reproductive individuals per quadrat and standardized to
the average number of receptacles per reproductive individual counted in each quadrat.
Recruitment rates were monitored using circular fiberglass collecting disks of 5.6 cm2 in area
made from food-grade isophthalmic fiberglass
resin as described in Ladah et al. (2003). Two to

Fig. 1. Map of the study area. Names of population

sampled are reported while site codes and range
indexes are given in brackets. Bar represents 100 km.

the species range (km) and R is the extent of the

range (km). The Ruler tool in Google Earth was
used to calculate distances between coastal
locations (from a height of 5 km and keeping a
distance of 1 km from the coastline).Values of RI
can vary from 1 to 1; close to zero they indicate
the center of the species distributional range
while values close to 1 or 1 indicate distributional edges. RI provides a continuous measure
of peripherality that allows appropriate statistical
tests and avoids the subjectivity of categorical
approaches and approximate definition of range
limits.

Demographic, life-history and morphological

variables
Six locations were chosen to uniformly and
equally represent locations across RI, i.e., two
between RI 0 and RI 0.1, two between RI 0.5
and 0.6 and two between RI 0.8 and R 0.9
(Fig. 1).
To estimate demographic, morphological and
life-history parameters, sampling was performed
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five disks per patch (30 cm 3 30 cm under algae,

n 4) were fastened with a nut to the rocky
substratum and replaced every two months. Any
attached individual that had reached a postsettlement size/stage was considered a recruit.
The number of recruits per disk area was counted
with a dissecting microscope and averaged
values were calculated for each patch.
For each location and each sampling interval,
the following demographic, life-history and
morphological variables were calculated: individual length, individual bushiness (i.e., maximum circumference-to-length ratio), individual
biomass, population density, minimum length of
a reproductive individual, maximum individual
reproductive effort, density of the reproductive
population, recruitment rates.

from the National Aeronautics and Space Administration (NASA) Goddard Earth Sciences
(GES) Data and Information Services Center
(DISC). Four annual environmental predictors
were selected based on the biological significance
to Fucus spp. along this stretch of coast (e.g.,
Nicastro et al. 2013, Zardi et al. 2013, Assis et al.
2014) and averaged across the years: SST of the
hottest and coldest month and air temperature of
the hottest and coldest month.

Data analyses
To test the null hypothesis of no relationship
between each variable and RI, a series of
univariate linear regressions using RI as a
predictor were run for each locations annual
mean of the demographic, life-history and
morphological variables. Additionally, temporal
variations of individual reproductive effort and
of recruitment rates were calculated as the
coefficient of variation between sampling dates.
To test the prediction that HE and A dropped
towards the edge, univariate linear regressions
were implemented between each of these genetic
diversity measures and RI.
To test the prediction of the presence of an
environmental gradient from center to edge, RI
was correlated with each environmental variable
using a series of Spearman rank correlations.
To test the null hypothesis of no relationship
between environmental variables and all biotic
variables, a series of univariate linear regressions
using as a predictor were run for each locations
annual mean of all demographic, life-history and
morphological variables and also for each locations genetic diversity measures.
For each univariate linear regression, homogeneity (visual examination of the plot) and
normality (Shapiro-Wilks test) of the residuals
was verified prior to testing and variables were
log-transformed if needed. When the above
assumptions were not met even after transformation, a Spearman rank correlation was calculated instead.
Finally, to test the null hypothesis of no
differences between sampling intervals, a series
of one-way ANOVAs using sampling intervals (n
6) as fixed factor. When the assumption of
homogeneity of variance was not met, data were
either log- or square root-transformed. In the
event of a significant main effect of sampling

Genetic diversity
At each location, vegetative apices from 48
individuals were sampled every meter at a fixed
vertical height within the species patches. Tissue
was stored in silica drying crystals for genetic
analyses. DNA was isolated from 510 mg of
dried tissue with a CTAB method (Hoarau et al.
2007) but modified using a silica filter plate
(Milipore MultiScreen HTS, FB Cat number
MSFBN6B10) instead of silica fines. Six microsatellite loci were amplified as in Zardi et al. (2013)
for the following loci: L20, L58, L38, L94, L78 and
F26II. Fragment length was analyzed on an
automated DNA sequencer ABI PRISM 3130
(Applied Biosystems) using both GeneScan 350
ROX (L20, L38, L58, L78, L94) and GeneScan 500
LIZ (F26II) standards. PEAK SCANNER v. 1.0
software (Applied Biosystems) was used to
estimate allele length.
For each location separately, expected heterozygosities (HE ) were estimated using GENETIX
version 4.05 (Belkhir et al. 1996-2004) while
was assessed using StandArich
allelic richness (A)
(http://www.ccmar.ualg.pt/maree/software.php?
softsarich) and adjusted by estimating the allelic
richness (Rs) using the rarefaction process to
account for differences in sample size.

Environmental variables
To estimate environmental parameters at each
location, monthly averaged Sea Surface Temperature (SST) and air temperature datasets between
January 2010 and September 2014 were retrieved
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ZARDI ET AL.

interval, a post hoc test (Student-Newman-Keuls)

was applied.
All statistical analyses were conducted using
IBM SPSS 20 software.

ductive output (Fig. 6A) differed between

locations: at the beginning of summer (May/
June) in northern localities and central FL, at the
start of autumn in central ER (September/
October) and in mid-late summer at the southern
marginal sites AR and CS (July/August).
Overall, the predicted negative relationships
were found between all variables and distance to
the center of the range, measured as RI (Figs. 2
and 3), except for individual bushiness, which
increased significantly towards peripheral populations (Fig. 2B). Although minimum size of a
reproductive individual was not significantly
associated with RI (Fig. 3A), it did show a sharp
decline after the two most northern locations.
Also, temporal variability of reproductive effort
and recruitment rates lacked of any correlation
with RI (Fig. 4).

RESULTS
Determination of the geographical center
of a continuous range
In Iberia, Fucus guiryi is currently continuously
distributed from La Franca (Spain; 43823 0 3800 N,
4834 0 24 00 W) to near Albufeira (Portugal;
378053 0 2100 N, 8811 0 3300 W). Within this region, it
displays two boundaries, a northeastern edge in
the warm areas of the Bay of Biscay and the other
in Southern Portugal, with a distributional center
in NW Iberia (North Portugal-Galicia). South of
southern Portugal, cold upwelled waters sustain
restricted F. guiryi populations within isolated
areas (western Alboran Sea and Morocco). Along
the N Spain coastline, the distribution is not
limited by the absence of rocky substratum.
Rocky shores typify this stretch of coast (over
500 km) where the species has suitable (substratum) habitat but along which it was not found.
Moreover, further north of the warm waters of
the Bay of Biscay, species presence has been
reported (but as F. spiralis var. platycarpus)
(Batters 1902) at both sides of the English
Channel and as far north as the Scottish Orkney
islands. However, these areas are not part of the
Iberian continuous coastal distribution and are
separated by hundreds to thousands of km
where the species is not present and thus were
not part of the continuous environmental gradient used as model in the present study.

Genetic diversity
A total of 35 different alleles were found in the
six sampled populations. Population allelic rich
ness standardized to the smallest sample size (A)
and gene diversity HE ranged from 3.86 to 1.54
and from 0.506 to 0.056, respectively. Because
contrasting A and HE values were recorded for
populations at RI close to zero (A 3.86 and HE
0.506 for VC; A 1.78 and HE 0.124 for AM), no
significant p-values for either correlation with RI
were recorded (Fig. 5).

Environmental variables
Hottest months were always in August or
September while the coldest from December to
February (Fig. 6). Sea surface temperature (SST)
of the coldest month was the most relevant
environmental variables affecting F. guiryi (Tables 1A, 2A, 3A in Appendix). In contrast, SST of
the hottest month was significantly correlated to
bushiness, population density and density of the
reproductive population only. None of the
environmental variables were significantly related to genetic diversity.
All environmental variables were significantly
positively correlated with RI, thus increasing
towards the edge of the continuous species
distribution. Environmental conditions that are
patchily distributed conspicuously violate one
of the abundant center hypothesis assumptions
(Brown 1984). Our study area extends along well
defined temperature gradients (e.g., Lima et al.

Demographic, life-history and morphological

variables
Range indexes for the locations examined over
one year varied between 0.003 and 0.874 (Fig.
1). All measured variables fluctuated throughout
the sampling period (see figures in Appendix). In
most locations, variables showed an effect of
sampling intervals. P-values and post-hoc results
are depicted in figures. For population density in
VN and AR, for maximum individual reproductive effort in FL and recruitment rates in FL, main
effect was only slightly significant while SNK did
not indicate any significant comparison. Moreover, the timing of maximum individual reprov www.esajournals.org

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Fig. 2. Morphological and demographic variables. Univariate regressions or Spearman rank correlations using
range index as a predictor. Mean values of response variables used are: (A) individual length; (B) individual
bushiness; (C) individual biomass; (D) population density. All p-values are significant.

2006, Benali et al. 2012, Nicastro et al. 2013) as

confirmed by the correlation results, thus meeting the fundamental assumption that environmental similarity is a continuously decreasing
function of the distance between sites (Brown
1984).

override larger scale latitudinal gradients (Helmuth et al. 2002). Relevant environmental variables considered here are significantly correlated
to Range Index. In our study, the linear relationship between F. guiryi demography/life history
and range index reflects, and is potentially
sustained by, a broad cold- to warm-temperate
environmental cline. Interestingly, winter SSTs are
the most significant variables that influence
morphological, demographic and reproductionrelated variables, while summer SSTs are the least
relevant environmental variables affecting the
species. Latitudinal gradients in air and sea
temperatures, which are intensified by upwelling
events that dominate north-western Iberia during
summer periods (Arstegui et al. 2006), have been
reported as the cause of species distributional

DISCUSSION
Demographic, life-history and morphological
variables
The expected pattern of strong decline of
demographic and life history traits towards the
margin of species distribution relies on the
presence of a strong environmental cline. Often,
however, empirical results will not display this
trend because the effects of local abiotic factors
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Fig. 3. Reproduction-related variables. Univariate regressions or Spearman rank correlations using range index
as a predictor. Response variables used are: (A) minimum length of a reproductive individual; (B) maximum
individual reproductive effort; (C) (mean) density of the reproductive population; (D) (mean) recruitment rates.

patterns. In particular, the western Iberian coastline studied here represents latitudinal clines in
abundance and distributional edge limits for
many coastal species (Boaventura et al. 2002,
Lima et al. 2006, Pereira et al. 2006, Assis et al.
2013).
Mirroring the sharp latitudinal environmental
gradient, we observed a substantial latitudinal
cline in population density, individual morphology and size (length, bushiness and biomass).
Stunted specimens with a compact, bushy
appearance (short and wide) developed towards
marginal locations. In general, body size greatly
affects thermoregulation through its effects on
energy and water requirements allowing higher
resistance and resilience to environmental condiv www.esajournals.org

tions (Walters and Hassall 2006, Gardner et al.

2011). Alternatively, smaller body size could
simply reflect non-adaptive variation triggered
by the direct and/or indirect effect of more
stressful conditions and marginal sites (Meiri
2011); e.g., a negative effect of heat stress proteins
production on growth rate (Tomanek 2010).
Previous studies have reported dwarf morphotypes in other Fucus spp. inhabiting fringe
habitats (F. serratus, Viejo et al. 2010; F. gardneri,
Wright et al. 2004; F. vesiculosus, Taylor and Hay
1984). In these species, bushy morphology is
often related to reduced elongation accompanied
by an increase in the rate of dichotomy, i.e., the
more slowly the plants elongate, the faster they
bifurcate (Knight and Parke 1950). Intraspecific
8

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Fig. 4. Temporal variation of reproduction-related

variables. Univariate regressions or Spearman rank
correlations using range index as a predictor. Mean
values of response variables used are: (A) temporal
variability of individual reproductive effort; (B) temporal variability of recruitment rates.

Fig. 5. Genetic diversity. Spearman rank correlations

using range index as a predictor. Variables used are:
(A) expected heterozygosity (HE ); (B) allelic richness
All p-values are non-significant.
(A).

shorter and wider individuals, layering and

clumping of ramified thalli significantly reduces
surface area and allows more water to be
retained between ramifications (e.g., Plumaria
elegans, Fucus spp., Sargassum muticum and
Pelvetia fastigiata; Norton 1991).
Low reproductive success is probably one of
the most common demographic effects setting
range limits. Indeed, there is much evidence for
partial or total failure of reproduction at range
limits, particularly among plants and it has been
suggested that this may be a more significant
limitation than subsequent offspring mortality
rates (Gaston 2009). Changes in reproduction and

phenotypic shifts can be the results of divergent

selection pressures across environments, typifying plastic phenotypic variations or genetically
distinct ecotypes or both (e.g., Torres-Dowdall et
al. 2012, Zardi et al. 2013). Regardless of what
triggers phenotypic divergence, morphological
variations in seaweeds allows algae to maximize
fitness in a wide variety of habitats. Specifically,
bushy morphology decreases the damage suffered due to desiccation or herbivory and
accordingly, intertidal distribution of compact
morphotypes is correlated with the intensity of
desiccation stress (e.g., Taylor and Hay 1984). In
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Fig. 6. Regressions between environmental and biotic variables. (A) Summary of the regressions using
environmental variables as predictors. Significant p-values are depicted with an asterisk (*). Latitude-time
Hovmoller diagram with (B) monthly averaged SSTs (C) monthly averaged near surface air temperatures. For
complete statistical results see Tables 1A, 2A, 3A in the Appendix.

zel et al. 2006). In fucoid seaweeds, reproductive

patterns can be altered under variable stressful
and unpredictable environmental situations such
as higher hydrodynamic and grazing stress
(Russell 1979), moderate abiotic stress (Dethier
et al. 2005), or at range edges (for some species
but not others; Araujo et al. 2011). Contrasting
studies also report no differences in reproductive
output when subjected to spatial and temporal
berg and Pavia
environmental variability (A
1997).
We observed a strong north to south reduction
in the size of reproductive populations, individual reproductive effort and recruitment rates.
Typically, changes in reproduction are interpreted in the context of niche-based theory where
individual performance is ranked from survival
to growth to reproduction. With increasing
proximity to range margins, harsher conditions
and declines in the availability and/or accessibility of resources trigger an ordered response at the
immediate expense of reproduction and in
favour of maintenance (growth and survival;

recruitment at range edges have been observed in

a wide variety of ecosystems and taxa; these
includes several, distinct variables such as
numbers of offspring (e.g., Hassall et al. 2006),
fertility (e.g., Garca et al. 2000, Viejo et al. 2010),
reductions in length of the reproductive season
(e.g., Gaston 2003), levels of sexual reproduction
(e.g., Kawecki 2008, Beatty and Provan 2011),
levels and timing of reproductive maturation
(e.g., Lester et al. 2007) and number of reproductive individuals (Granado-Yela et al. 2013).
Phenological events regulate the ability to capture resources and define the extent of growth
and reproduction, thus playing a crucial role in
reproductive success and survival of the individuals (Chuine 2010). There is evidence that
phenology is a significant determinant of fitness
and a key adaptive trait in shaping species
abundance and distributional ranges (e.g., Vitasse et al. 2014, Zhang et al. 2014). Importantly,
phenology is largely affected by environmental
fluctuations and several studies have reported
recent climate-induced phenological shifts (Menv www.esajournals.org

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ZARDI ET AL.

Townsend et al. 2008). However, variability of

resource allocation can also be considered in the
context of non-hierarchical life-history strategies
where the trade-off between life-history traits
varies depending on local conditions and interaction of several environmental determinants
(Zardi et al. 2007, Nicastro et al. 2010). In this
view, regardless of the position within the species
range, relative reproductive allocation is generally expected to increase in environments where
risk of adult mortality and environmental heterogeneity are high and chances of survival to the
next reproductive event are scarce (Stearns and
Koella 1986, Siems and Sikes 1998).
Not only the investment in reproduction is
correlated with distance to center, but also the
size of reproductive individual is changing with
range index. In the context of life-history strategies, theory predicts that increased adult mortality under stressful conditions promotes smaller
size at maturity (Olsen et al. 2004). Our results
confirm this life-history prediction; although,
reduction of minimum size for reproduction
exhibited a non-significant relationship with
distance to center, it dropped abruptly south of
the two northernmost locations (VC and AM).
Similar patterns have been observed for F.
serratus; in this species, lower reproductive
investment and smaller size at maturity are
related to low physiological response when
facing harsher environmental conditions (e.g.,
high water and air temperature, low humidity) at
the periphery of the species distribution
(Martnez et al. 2012). The adaptive significance
of size-dependent reproductive patterns still
remains poorly understood. However, this study
suggests that smaller size at maturity in peripheral individuals does not necessarily compensate
for extensive reductions in reproductive effort
and size of reproductive population; indeed
recruitment rates and overall adults abundance
showed a strong negative correlation with
distance from the center despite of size of
individuals at the marginal habitat.
Overall, our annual study captured wide
temporal fluctuations in all demographic, morphological and life history parameters (see
Appendix figures). Population traits and dynamics are often characterized by large temporal
fluctuations (Williams et al. 2003, Guo et al. 2005)
and patterns revealed by only one snapshot
v www.esajournals.org

sample may disagree with average annual

patterns (e.g., Defeo and Cardoso 2004, Nicastro
et al. 2010). In particular, timing and intensity of
gamete maturation and release can be extremely
variable. Reproductive events each year or in
different areas across the species range often do
not coincide (e.g., Zardi et al. 2007, Nicastro et al.
2010). In particular, greater reproductive variability has been observed in populations at the
range edge, which is expected when such edges
match limits of the ecological niche (e.g., Angert
2009). Seasonal sampling covering the entire
reproductive period will capture reproduction
maxima and allow large scale comparisons to be
made with confidence despite possible temporal
shifts along the range. In our study, maximum
individual reproductive effort and recruitment
rate showed conspicuous temporal variability,
however, it was not significantly associated with
distance from the range center. Temporal variability in recruitment rates was particularly low
in central populations where receptacles are
present throughout the year, probably guaranteeing a continued presence of new recruits. In
contrast, in southern populations, reproductive
fronds are mostly shed over several months
(between reproductive peaks; K. R. Nicastro and
G. I. Zardi, personal observation) leading to
relatively greater temporal variability in recruitment.

Genetic diversity
Our population-genetic data did not display
the expected core-edge prediction: contrasting
levels of A were recorded at RI close to zero and
no significant regression with geographic distance or environmental variables was noted for
either A or HE. Inter-specific hybridization with
neighboring taxa is the most likely explanation
for the pattern reported here, as explained below.
Several species of Fucus co-inhabit the intertidal and shallow subtidal zone along northern
European shorelines (Luning 1990) and hybridization is known to occur between species that
partially overlap in the intertidal zonation (e.g.,
Billard et al. 2005). In particular, in VC, several
Fucus spp. (F. spiralis, F. guiryi, F. vesiculosus, F.
serratus) coexist and show extensive hybridization (Zardi et al. 2011). However, at the second
most northern site (AM, less than 10 km from
VC), gaps of several meters separate the F. guiry
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February 2015 v Volume 6(2) v Article 23

ZARDI ET AL.

canopy from smaller patches of the only other

Fucus spp. present (F. serratus; personal observation). Southwards, F. guiry occurs in allopatry and
no other Fucus spp. are present. Thus, different
levels of hybridization across the species range
might be blurring the native patterns of genetic
diversity for this species at the most central sites
of our study range. Putative secondary contact of
two F. guiryi lineages from different refugial
populations, could also contribute to an increase
of genetic variability in VC area. Northern
Portugal has been suggested to be a past refugial
area for several marine species and admixture
through secondary contact in some sites cannot
be excluded. However, this scenario seems
unlikely given that the closest population (AM)
has very different gene diversity and allelic
richness but is located less than 10 km away.
Additionally, there is no evidence for the
existence of distinct lineages of F. guiryi, because
the different alleles found in our core populations
of this species are not private and are also found
in the sympatric species, supporting introgression rather than ancient divergence as the origin
of such alleles (Zardi et al. 2011).
Genetic characterization of edge populations of
several other marine species along this same
coastline have revealed contrasting patterns.
Similarly to our findings, southern edge populations of the seagrass Zostera marina have lower
genetic diversity compared to those inhabiting the
center of the species distribution. However, when
the southern edge was considered as a whole
rather than per population, no geographic patterns in genetic diversity were observed (Diekmann and Serrao 2012). In contrast, genetic
diversity of the kelp Saccorhiza polyschides is
significantly correlated with latitude; with an
unexpected increase towards the southern edge
despite recent bottlenecks and much lower densities, suggesting that diversity prior to recent
extinctions/recolonizations might have been even
higher than current levels (Assis et al. 2013). High
levels of genetic diversity have also been observed
in southern peripheral populations of F. ceranoides
(with a consistent decline towards higher latitudes) highlighting their refugial status throughout past glacial conditions (Neiva et al. 2012).
These apparent population-genetic discrepancies may arise as a result of complex biogeographic history and/or introgression events and,
v www.esajournals.org

as suggested here, of inter-specific hybridization

phenomena. The general hypothesis of lower
genetic diversity at margins may lose its predictive power when applied to genetic datasets that
solely contemplate gradients of contemporary
environmental conditions.

Conclusions
Coupling population dynamics with genetic
diversity is a significant step forward towards a
comprehensive understating of effects of peripherality at rear edges and ultimately, the potential
for shifts in species southern margins as a
response to climatic changes.
As we have shown, empirical testing should
consider the complexity of biotic and abiotic
factors, including their spatio-temporal variability, that define a species range. In particular, we
stress the importance of long-term sampling
(rather than once-offs) along the geographic
range of the organisms of interest (rather than
center vs. southern edge), especially in regions of
strong environmental clines, to account for
temporal shifts and seasonal and non-climatic,
site specific fluctuations of demographic, morphological and life history traits.
Finally, population-genetic core-edge predictions should deal more exhaustively with the
intrinsic complexity of the genetic pattern by
evaluating also past influences such as levels of
inter-specific hybridization, which may be critical
in sustaining species genetic diversity.

ACKNOWLEDGMENTS
This work was financed by FCT (Foundation for
Science and Technology, Portugal) through projects
PTDC/MAR/110251/2009, EXCL/AAG-GLO/0661/2012
and supported by an award from the South Africa
Research Chairs Initiative (SARChI) of the Department
of Science and Technology. K. R. Nicastro was funded
by FCT postdoctoral grant SFRH/BPD/45544/2008.
Enviormental data used were acquired as part of the
activities of NASAs Science Mission Directorate, and
are archived and distributed by the Goddard Earth
Sciences (GES) Data and Information Services Center
(DISC). G. I. Zardi and K. R. Nicastro contributed
equally to this work.

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SUPPLEMENTAL MATERIAL
APPENDIX
Table A1. Regressions between environmental and morphological/demographic variables. Univariate regressions
(R2) or Spearman rank (Rho) correlations using environmental variables as predictors.
SST
Hottest month
Variable

Rho

Individual length
Individual bushiness
Individual biomass
Population density

0.755
0.914
0.724

0.894

Air temperature
Coldest month

Rho

0.08
,0.05
0.104
,0.01

0.959
0.923
0.965

0.671

Hottest month
P

Rho

,0.01
.0.01
,0.01
,0.05

0.912
0.912
0.971

Coldest month

Rho
0.928
0.928

0.81

,0.05
,0.05
,0.001
,0.05

R2

0.96
0.655

,0.01
,0.01
,0.01
0.051

Log-transformed.

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Table A2. Regressions between environmental and reproduction-related variables. Univariate regressions (R2) or
Spearman rank (Rho) correlations using environmental variables as predictors.
SST
Hottest month
Variable
Minimum length of a
reproductive individual
Maximum individual
reproductive effort
Density of the reproductive
population
Recruitment rates

Rho

Air temperature
Coldest month

Rho

0.754

0.083 0.958

0.712

0.112
0.875 ,0.01

0.656

Hottest month
P

Rho

Rho

,0.01 0.964

0.14

0.638

0.906 ,0.01 0.736

0.096

R2

,0.05 0.853

P
0.173

0.914 ,0.01

0.703 ,0.05 0.696

0.445 0.142

0.156 0.886

Coldest month

0.165
0.827 ,0.05

,0.05

Table A3. Regressions between environmental and genetic diversity. Univariate regressions (R2) or Spearman
rank (Rho) correlations using environmental variables as predictors.
SST
Hottest month
Variable

Rho

Expected heterozygosity (HE )

Allelic richness

0.532
0.528

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Air temperature
Coldest month

Rho

0.277
0.282

0.651
0.675

17

P
0.162
0.141

Hottest month
Rho
0.493

Coldest month

Rho

0.32

0.242
0.321

0.145
0.221

R2

P
0.784
0.674

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Fig. A1. Individual length. Bimonthly measurements of mean individual length, n 4 quadrats, at: (A) VC; (B)
AM; (C) ER; (D) FL; (E) AR; (F) CS. Codes correspond to locations in Fig. 1 while ANOVAs p-values and post
hoc results for each location are depicted.

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Fig. A2. Individual bushiness. Bimonthly measurements of mean individual bushiness, n 4 quadrats, at: (A)
VC; (B) AM; (C) ER; (D) FL; (E) AR; (F) CS. Codes correspond to locations in Fig. 1 while ANOVAs p-values and
post hoc results for each location are depicted.

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Fig. A3. Individual biomass. Bimonthly measurements of mean individual biomass, n 4 quadrats, at: (A) VC;
(B) AM; (C) ER; (D) FL; (E) AR; (F) CS. Codes correspond to locations in Fig. 1 while ANOVAs p-values and post
hoc results for each location are depicted.

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Fig. A4. Population density. Bimonthly measurements of population density, n 4 quadrats, at: (A) VC; (B)
AM; (C) ER; (D) FL; (E) AR; (F) CS. Codes correspond to locations in Fig. 1 while ANOVAs p-values and post
hoc results for each location are depicted.

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Fig. A5. Minimum length of a reproductive individual. Bimonthly measurements of minimum length of a
reproductive individual, n 4 quadrats, at: (A) VC; (B) AM; (C) ER; (D) FL; (E) AR; (F) CS. Codes correspond to
locations in Fig. 1 while ANOVAs p-values and post hoc results for each location are depicted.

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Fig. A6. Maximum individual reproductive effort. Bimonthly measurements of maximum individual
reproductive effort, n 4 quadrats, at: (A) VC; (B) AM; (C) ER; (D) FL; (E) AR; (F) CS. Codes correspond to
locations in Fig. 1 while ANOVAs p-values and post hoc results for each location are depicted.

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Fig. A7. Density of the reproductive population. Bimonthly measurements of the density of the reproductive
population, n 4 quadrats, at: (A) VC; (B) AM; (C) ER; (D) FL; (E) AR; (F) CS. Codes correspond to locations in
Fig. 1 while ANOVAs p-values and post hoc results for each location are depicted.

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Fig. A8. Recruitment rates. Bimonthly measurements of recruitment rates, n 4 quadrats, at: (A) VC; (B) AM;
(C) ER; (D) FL; (E) AR; (F) CS. Codes correspond to locations in Fig. 1 while ANOVAs p-values and post hoc
results for each location are depicted.

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