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Benthic algal community
dynamics on Palmyra Atoll
throughout a decade with two
thermal anomalies
Adi Khen
1
*, Maggie D. Johnson
2
, Michael D. Fox
2
and Jennifer E. Smith
1
1
Center for Marine Biodiversity and Conservation, Scripps Institution of Oceanography, University of
California, San Diego, La Jolla, CA, United States,
2
Biological and Environmental Sciences and
Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
Coral reef algae serve many important ecological functions, from primary
production to nutrient uptake and reef stabilization, but our knowledge of
longer-term effects of thermal stress on algae in situ is limited. While ocean
warming canfacilitate proliferation of algae and potential phase shifts from coral to
macroalgal-dominated states, algal responses may vary by species, genus,
functional group, or type (e.g., calcareous vs. fleshy). We used 11 years of annual
monitoring data (2009-2019) that spans two El Niño-associated heatwaves to
examine benthic algal community dynamics on Palmyra Atoll in the central Pacific
Ocean. We quantified the percent cover of algal taxa via image analysis of
permanent benthic photoquadrats from two habitats on Palmyra: the deeper,
wave-exposed fore reef (10 m depth) and the shallower, wave-sheltered reef
terrace (5 m depth). Each habitat was characterized by distinct algal communities:
predominantly calcareous taxa on the fore reef and predominantly fleshy taxa on
the reef terrace. Patterns in abundance fluctuated over time and/or in response to
thermal anomalies in 2009 and 2015. Fleshy algae generally increased in cover
post-warming, which coincided with large declines of the calcified macroalgae,
Halimeda spp. Long-term monitoring of coral reef algal communities is critical for
understanding their differential responses to thermal stress and can improve
projections of ecosystem functioning in the context of global change.
KEYWORDS
long-term monitoring, seaweed, macroalgae, Halimeda, community composition,
thermal stress, coral reefs, climate change
1 Introduction
Benthic algae are key components of coral reef ecosystems, where they contribute to
primary production and reef building as well as sand, sediment, and carbonate production.
The dominance of one functional group or taxon over another has implications for coral
reef functioning and the ecological services they provide (Woodhead et al., 2019). Although
Frontiers in Marine Science frontiersin.org01
OPEN ACCESS
EDITED BY
Guang Gao,
Xiamen University, China
REVIEWED BY
Jinlin Liu,
Tongji University, China
Robert Steneck,
University of Maine, United States
*CORRESPONDENCE
Adi Khen
akhen@ucsd.edu
RECEIVED 04 December 2024
ACCEPTED 13 January 2025
PUBLISHED 28 January 2025
CITATION
Khen A, Johnson MD, Fox MD and Smith JE
(2025) Benthic algal community dynamics
on Palmyra Atoll throughout a decade
with two thermal anomalies.
Front. Mar. Sci. 12:1539865.
doi: 10.3389/fmars.2025.1539865
COPYRIGHT
© 2025 Khen, Johnson, Fox and Smith. This is
an open-access article distributed under the
terms of the Creative Commons Attribution
License (CC BY). The use, distribution or
reproduction in other forums is permitted,
provided the original author(s) and the
copyright owner(s) are credited and that the
original publication in this journal is cited, in
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practice. No use, distribution or reproduction
is permitted which does not comply with
these terms.
TYPE Original Research
PUBLISHED 28 January 2025
DOI 10.3389/fmars.2025.1539865
many coral reefs across the globe are shifting from coral to algal
dominance (Pandolfiet al., 2003;McManus and Polsenberg, 2004;
Hughes et al., 2010,2017), algae are inherently a natural component
of healthy coral reefs. Despite their functional, morphological, and
taxonomic diversity (Fong and Paul, 2011), reef algae remain
understudied relative to other reef taxa. Aside from some short-
term laboratory studies, little is known about how individual algal
taxa or functional groups respond to a combination of stressors in
nature (Wernberg et al., 2012). Thus, in situ studies integrating
natural environmental conditions with longer-term benthic algal
community dynamics are essential for revealing possible reef
community trajectories in the coming decades.
Algae on coral reefs are often classified into functional groups
(e.g., turf, crustose coralline algae, and macroalgae), based on the
underlying assumption that shared traits correspond to similar
ecological roles, functions, or processes. Algal functional groups
have previously been defined by their susceptibility to herbivory
(Steneck and Watling, 1982), their nutrient uptake, productivity, and
turnover rates (Littler and Littler, 1980;Littler et al., 1983), or their
morphology, internal anatomy (e.g., cortication), thallus structure,
and branching pattern (Steneck and Dethier, 1994;Balata et al.,
2011). However, there is still a potential for variable responses to
environmental conditions within functional groups, particularly
following disturbance events (Phillips et al., 1997). Moreover,
calcareous algal taxa (in which photosynthesis is coupled with the
deposition of calcium carbonate) and non-calcareous (i.e., fleshy)
taxa are differentially affected by environmental stressors (Johnson
et al., 2014). While the functional group approach (when based on
morphological traits) can sometimes predict community assemblage
(Stelling-Wood et al., 2020), these traits may not accurately represent
functional identity (Mauffrey et al., 2020) and individual genus and/
or species variability must be considered (Fong and Fong, 2014;
Ryznar et al., 2021).
Two algal functional groups that are sometimes pooled in reef
benthic studies, yet have distinct ecological roles, are the crustose
coralline algae (CCA) and the algal turfs. CCA are encrusting,
calcifying red algae that stabilize the reef framework and support
structural complexity (Teichert et al., 2020;Littler and Littler, 2013;
Steneck, 1986). They also contribute to carbonate production,
possibly more so than reef-building corals (Cornwall et al., 2023).
By releasing chemical cues that induce settlement in coral larvae
(Harrington et al., 2004), CCA further promote reef growth and
resilience. The ecological contributions of CCA on coral reefs are
threatened by environmental change, as they are sensitive to
thermal stress in both experimental and field settings (Martin and
Gattuso, 2009;Short et al., 2015). “Turf algae”(algal turfs) refers to a
mixed assemblage of largely fleshy filamentous algae, juvenile
macroalgae, and/or cyanobacteria less than 2 cm tall (Adey and
Steneck, 1985). Algal turfs are opportunistic and rapid colonizers of
open space after coral bleaching or disease outbreaks (Diaz-Pulido
and McCook, 2002). They are a main food source for herbivorous
grazers (Carpenter, 1986), but can have negative effects on reefs by
inhibiting coral recruitment (Birrell et al., 2008) or harboring
pathogenic microbes that compromise coral health (Pratte et al.,
2018). Despite occupying much of the benthos on today’s reefs
(Wismer et al., 2009), they are often miscategorized as “bare space”
and, thus, grossly underestimated in surveys of benthic community
coverage. Turfs thrive under conditions that threaten corals,
including nutrient pollution (Smith et al., 2010), warming
(Johnson et al., 2017), ocean acidification (Falkenberg et al.,
2013), and sedimentation (Birrell et al., 2005), which suggests that
their abundance on reefs will continue to increase with the
progression of climate change (Harris et al., 2015;Tebbett and
Bellwood, 2019).
Another distinction lost with the typical categorization of algae
is the presence or absence of a calcium carbonate skeleton (i.e.,
calcification). The relative balance of fleshy to calcareous or reef-
building taxa may be indicative of more degraded vs. “healthier”
coral reefs (Smith et al., 2016), and thus tracking the abundance of
calcareous and fleshy algal taxa is useful for assessing ecosystem
status. Moreover, fleshy and calcareous taxa have different
ecological functions, whether beneficial or detrimental. Fleshy
macroalgae typically grow faster than calcareous macroalgae and
are generally more edible to herbivores. However, fleshy macroalgae
can harm corals directly through abrasion, or indirectly by releasing
toxic allelochemicals (Rasher and Hay, 2010), causing hypoxia and
physiological stress (Barott et al., 2012) by limiting photosynthetic
activity and depleting the corals of energy (Titlyanov et al., 2007).
Calcareous algae are generally more benign competitors with corals
than fleshy algae (Barott et al., 2012; but see: Keats et al., 1997a and
Longo and Hay, 2015, where corals frequently experienced damage
from contact with calcareous algae), although their competitive
ability may be influenced by seasonality (Brown et al., 2020).
Therefore, to holistically evaluate the ecological implications of
stressors such as warming, it is informative to look not only at
variability across individual algal taxa or functional groups, but also
between fleshy and calcareous algae.
For algae and other primary producers, temperature is expected to
increase metabolic and photosynthetic rates until a thermal tolerance
limit is exceeded (Davison, 1991). Calcification in calcareous algae may
initially benefit from warmer temperatures until prolonged exposure
leads to mortality or reduction in productivity, as seen in experimental
studies (Martin and Gattuso, 2009;Page et al., 2021;butsee:Krieger
et al., 2023). In contrast, fleshy algae have been found to respond
positively to thermal stress in field studies (McClanahan et al., 2001;
Burt et al., 2013;Graham et al., 2015). The combined effects of
temperature and other stressors can be synergistic (Ellis et al., 2019)
or antagonistic (Darling et al., 2010). For example, ocean acidification
has been found to cause net negative or species-specificeffectson
tropical calcareous algae while stimulating growth in some fleshy algae
(Johnson et al., 2014), but when combined with warming, effects can be
more complex or interactive (Diaz-Pulido et al., 2012;Kram et al., 2016;
Johnson et al., 2017).
The calcareous macroalgal genus Halimeda is a group of
siphonous green algae that contribute significantly to productivity
and calcification on coral reefs (Hillis-Colinvaux, 1980), and can
cover up to 20% of the benthos (Perry et al., 2020). Halimeda is one
of the most ubiquitous tropical algal genera with representative
species occurring on reefs around the world. Indeed, Halimeda spp.
may contribute more to tropical carbonate budgets than corals
(Rees et al., 2007) due to their fast growth and high turnover rates
(Vroom et al., 2003;Smith et al., 2004). Most species of Halimeda
Khen et al. 10.3389/fmars.2025.1539865
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are holocarpic and as such, when they reproduce they die and their
calcified segments break down into sand (Harney and Fletcher,
2003). Halimeda spp. are synchronous spawners that release all of
their gametes simultaneously, leading to complete adult mortality
(Hay, 1997), although the exact mechanisms that trigger their
reproduction are unknown (Clifton and Clifton, 1999;Clifton,
2013). Considering the high abundance, cosmopolitan
distribution, and ecological significance of Halimeda spp., it is
important to monitor their cover on a consistent basis as well as
before, during, and after thermal anomalies. Few studies have
examined the long-term changes in cover of Halimeda spp. in
situ (but see: Lambo and Ormond, 2006, where Halimeda cover
decreased in Kenya at the time of the 1998 coral bleaching event but
increased drastically by 2004).
Here, we measured benthic algal cover over an 11-year time
series of permanent benthic photoquadrats from two reef habitats
on Palmyra Atoll. Thermal anomalies occurred in both 2009 and
2015 (Williams et al., 2010;Fox et al., 2019), which allowed us to
explore how temperature may influence algal community dynamics.
Our objectives were to (i) describe benthic algal community
composition on the fore reef and reef terrace habitats, (ii)
quantify the abundance of individual algal taxa or functional
groups, (iii) compare fleshy (turf and fleshy macroalgae) vs.
calcareous (CCA and calcareous macroalgae) cover, and (iv)
determine whether benthic algal cover varied over time, with
temperature, and/or by habitat. Additionally, for the major
calcareous macroalgal genus, Halimeda, we measured yearly
changes in benthic cover by habitat and site to validate our
hypothesis that Halimeda spp. may be temperature-sensitive and
negatively affected by warm-water events.
2 Methods
2.1 Study site
Palmyra Atoll (5.89 °N, 162.08 °W), U.S. Minor Outlying Islands, is
located in the Northern Line Islands, central Pacific. Palmyra was
designated as a National Wildlife Refuge in 2001 and this protection
was further expanded in 2009 as part of the PacificRemoteIslands
Marine National Monument. The Atoll was temporarily occupied by
the U.S. military during World War II but is currently uninhabited
aside from a small field research station. Thus, its reefs are considered
quasi-pristine (Sandin et al., 2008)andrelativelyundisturbed from
localized human impacts such as fishing or pollution, yet are still
susceptible to global climate change. Palmyra’s benthic communities
are dominated by reef-builders such as hard corals and CCA, with
remaining surfaces covered by turf algae, macroalgae, soft corals, and
other invertebrates (Braun et al., 2009;Williams et al., 2013;Khen
et al., 2022).
2.2 Data collection
In September 2009, permanent monitoring plots were
established in the two major reef habitats on Palmyra: the wave-
exposed fore reef (FR) at 10 m depth and the wave-sheltered reef
terrace (RT) at 5 m depth, with four sites per habitat and ten
replicate plots (90 cm x 60 cm) per site (Supplementary Figure 1),
for a total surveyed area of 21.6 m
2
at each habitat. Replicate plots
were 5 m apart along a 50 m transect perpendicular to shore,
marked by stainless steel eye bolts in opposing corners that were
secured to the benthos with marine epoxy. At least once a year from
2009 to 2019, usually in the late summer or early fall, plots were
photographed by SCUBA divers with a Canon G-series camera
attached to a PVC frame that maintained a fixed distance from the
substrate. All images were digitized (i.e., manually traced) in Adobe
Photoshop (Creative Cloud) to quantify abundance of algal taxa in
terms of planar areas or percent cover at the functional group level
for CCA and turf, family-level for peyssonnelioids, and genus or
species-level for other macroalgae. Algae were identified visually by
morphology, and taxa were grouped as either calcareous (CCA,
Halimeda spp., Galaxaura rugosa, and Peyssonneliaceae sp.) or
fleshy (Avrainvillea sp., Lobophora sp., Dictyosphaeria spp.,
Caulerpa serrulata, and turf) based on the presence or absence of
biogenic calcium carbonate structures. Palmyra’s thermal history
was obtained from a revised percentile-based method of estimating
Degree Heating Weeks (DHW; Liu et al., 2006) developed by
Mollica et al. (2019), which more accurately captures the degree
of accumulated thermal stress experienced by central equatorial
Pacific reefs than traditional DHW (Fox et al., 2021).
2.3 Statistical analyses
All analyses were conducted in R software version 3.6.3 (R Core
Team, 2018). First, using only annual time points taken during the
late summer or fall (excluding irregular time points to minimize the
effect of seasonal variation), we constructed a non-metric
multidimensional scaling (nMDS, via metaMDS in vegan for R;
Oksanen et al., 2019) ordination plot visualizing the trajectory of
algal community composition through time at each habitat. This
nMDS was based on Bray-Curtis dissimilarity measures for square-
root-transformed algal percent cover data (Anderson, 2001). We
applied a square-root transformation to balance the effect of
disproportionately-abundant taxa. We tested the effects of habitat,
year, and/or their interactionbyconductingathree-way
permutational multivariate analysis of variance (PERMANOVA
with 9999 permutations via adonis in vegan;Anderson, 2001;
Oksanen et al., 2019) on the same Bray-Curtis distance matrix.
We did not include site as a nested factor because not all algal taxa
were present at each site within a habitat. To identify which algal
taxa were the main contributors to differences among habitats, we
ran a SIMPER or “similarity percentages”analysis (via simper in
vegan;Clarke, 1993;Oksanen et al., 2019).
To test whether percent cover of fleshy or calcareous algae
varied by habitat and/or over time (only for consistent annual time
points), we ran two-way analyses of variance (ANOVAs) with
Type-II sum of squares. Assumptions of normality and
homogeneity of variance were checked through visual inspection
of the residuals. We did not incorporate repeated measures and
instead treated years independently because different algal
Khen et al. 10.3389/fmars.2025.1539865
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populations were sampled each year rather than the same
individuals. Post-hoc letter groupings were assigned via Tukey’s
multiple comparisons using multcomp (Hothorn et al., 2008).
Next we explored possible effects of temperature on a single
taxon of interest, Halimeda, through an analysis of covariance
(ANCOVA) with Type-II sum of squares. Habitat was considered
afixed factor and temperature (in terms of percentile-based DHW
values during the week of sampling) was considered a continuous
factor. We also examined the relationship between accumulated
thermal stress and Halimeda cover using Pearson’s correlation. To
further investigate patterns in abundance for this genus, we plotted
its percent cover within each quadrat, by site, over time. Lines were
smoothed by locally-weighted regression (i.e., LOESS in ggplot2;
Wickham, 2016). Finally, we calculated the difference in mean
percent cover of Halimeda by site (with quadrats as replicates)
between consecutive years. Two-tailed t-tests were used to
determine which sites experienced significant changes not
overlapping zero (e.g., an increase or decrease in percent cover
one year later).
3 Results
3.1 Algal community composition in each
habitat over time
The benthic algal community on Palmyra’s fore reef was calcifier-
dominated compared to the fleshy-dominated reef terrace (Figure 1;
Supplementary Figure 1). Certain taxa were only present in either
habitat: G. rugosa on the reef terrace and Avrainvillea sp. on the fore
reef. Across both habitats, the most abundant algal taxa or groups on
Palmyra included CCA (exhibiting a percent cover range of 0 to
87.6% of the benthos within a single quadrat, average = 20.2 ± 17.4%
SD), turf (percent cover = 0 to 88.3%, average = 16.7 ± 17.6%),
and Halimeda (percent cover = 0 to 92.3%, average = 8.4 ± 12.4%).
The least abundant algal genera were Avrainvillea (percent cover = 0
to 1.7%, average = 0 ± 0.1%), Dictyosphaeria (percent cover = 0
to 27.1%, average = 0.4 ± 1.7%), and Caulerpa (percent cover = 0 to
46.6%, average = 0.6 ± 3.3%). Distinct yearly trajectories of algal
community composition were seen in each habitat (Figure 2).
Benthic algal community composition on Palmyra varied
significantly by habitat (p <0.001) and year (p <0.001), with an
interaction indicating that habitats changed differently across years
(p <0.001; Supplementary Table 1). There was more year-to-year
variation in algal community composition on the fore reef
compared to the reef terrace, particularly after the second thermal
anomaly in 2015. However, habitat was a better predictor for algal
community composition than year, explaining 11.6% of the
variation (R
2
= 0.116; Supplementary Table 1) compared to 4.3%.
A SIMPER analysis revealed that the taxa contributing most to
habitat differences were CCA, turf algae, and Halimeda
(Supplementary Table 2). Calcareous algae (particularly CCA,
Halimeda spp., and Peyssonneliaceae sp.) were more abundant on
the fore reef whereas fleshy algae (turf, Lobophora sp., C. serrulata,
and Dictyosphaeria spp.) were more abundant on the reef terrace.
3.2 Cover of individual algal taxa by habitat
and year
Overall, CCA were more abundant on the fore reef than the reef
terrace, covering 25.3 ± 0.8% (mean ± SE) and 15.4 ± 0.8% of the
total benthos, respectively (Figure 3B). In contrast, turf algae were
more abundant on the reef terrace than the fore reef at 21.3 ± 1.0%
and 11.5 ± 0.5% cover, respectively (Figure 3H). Between fall 2014
and fall 2015 on the reef terrace, there was a decline in CCA from
20.0 ± 3.2% to 12.7 ± 2.9% and a concomitant rise in turf algae from
19.6 ± 3.5% to 28.6 ± 3.7%; the increase in turf at the time of the
FIGURE 1
Benthic algal community composition over time on Palmyra from 2009 to 2019 at the (A) Fore Reef and (B) Reef Terrace habitats in terms of relative
proportions of each taxon or functional group.
Khen et al. 10.3389/fmars.2025.1539865
Frontiers in Marine Science frontiersin.org04
second thermal anomaly was seen to a lesser extent on the fore reef.
However, by fall 2017, turf and CCA cover were restored to pre-
disturbance levels in both habitats. Other algal groups were far less
abundant than turf and CCA. Benthic cover of C. serrulata, found
almost exclusively on the reef terrace, was highest in the fall of 2010
and 2019 at 3.6 ± 1.5%, but dropped to undetectable levels in fall
2012, 2014, and 2018 (Figure 3A). Similarly, also on the reef terrace,
Dictyosphaeria spp. (D. cavernosa and D. versluysii) comprised up
to 1.5% total cover but were nearly negligible in the fall of 2014,
2015, 2018, and 2019 (Figure 3C). The reef terrace had 4.3 ± 0.6%
cover of G. rugosa in fall 2019 but was typically around 2.5%
(Figure 3D). There was consistently higher cover of Lobophora sp.
on the reef terrace (5.0 ± 0.5%) compared to the fore reef (1.9 ±
0.2%; Figure 3F). Cover of Peyssonneliaceae sp., found mainly at the
fore reef, was lowest in the fall of 2017 at 1.2 ± 0.3% yet reached up
to 10-15% of the benthos every fall between 2011 and 2014
(Figure 3G). Avrainvillea sp. was not plotted because it occupied
less than 0.01% of the benthos. Halimeda spp. (primarily H. opuntia
with minor coverage by H. taenicola and H. fragilis) were more
abundant on the fore reef, at 14.2 ± 0.8% cover throughout the time
series compared to 4.4 ± 0.3% on the reef terrace (Figure 3E).
3.3 Calcareous vs. fleshy algal trajectories
by habitat
Throughout the time series, the fore reef had higher cover of
calcareous algae than fleshy algae, at 46.5 ± 0.8% (mean ± SE) and
13.4 ± 0.5%, respectively (Figure 4A), whereas the reef terrace had
similar cover of calcareous and fleshy algae, at 22.1 ± 0.8% and 28.0
± 0.9%, respectively (Figure 4B). Percent cover of fleshy algae varied
by habitat (p <0.001) and year (p <0.001) with no significant
interaction (Supplementary Table 3). Percent cover of calcareous
algae also varied by habitat (p <0.001) and year (p = 0.004), with
habitats changing differently over time (p = 0.011). On the reef
terrace, the cover of calcareous algae remained consistent through
time whereas on the fore reef, calcareous algae were replaced by
fleshy algae at the time of the second thermal anomaly in 2015 but
re-stabilized by fall 2017. A similar yet less pronounced response
was observed on the reef terrace.
3.4 Abundance of Halimeda spp. with
respect to temperature
Several months after the first thermal anomaly, Halimeda cover
dropped from 18.8 ± 3.2% (mean ± SE) in fall 2009 to 5.8 ± 0.8% in
spring 2010 on the fore reef and 5.4 ± 1.0% to 2.2 ± 0.4% on the reef
terrace (Figure 3E). By late summer 2010, Halimeda cover had
decreased significantly at four out of eight sites (Supplementary
Table 5) but increased in subsequent years. Between fall 2014 and
fall 2015, Halimeda cover decreased again at all sites; its cover during
the second thermal anomaly was among its lowest throughout the
time series, at 4.5 ± 0.9% on the fore reef and 0.7 ± 0.2% on the reef
terrace. Regardless of the amount of Halimeda within each quadrat or
site, its abundance followed a similar trajectory with sharp declines by
2015, and growth or no change thereafter (Supplementary Figure 2).
Between fall 2016 and fall 2017, Halimeda cover increased
significantly at six out of eight sites by up to 20% (Supplementary
Table 5). Thus, in all cases where significant differences were detected,
FIGURE 2
Non-metric multidimensional scaling (nMDS) based on Bray-Curtis dissimilarity measures of benthic algal community composition by taxon (in terms
of square-root-transformed percent cover data). Lines terminating in an arrowhead represent the yearly trajectory of each habitat (Fore Reef in
orange, Reef Terrace in red) from 2009 to 2019. Asterisks denote thermal anomalies in 2009 and 2015.
Khen et al. 10.3389/fmars.2025.1539865
Frontiers in Marine Science frontiersin.org05
the sites that changed did so in the same direction. There were
significant effects of percentile-based DHW (p = 0.023) and habitat (p
<0.001) on Halimeda cover (Supplementary Table 4). A negative
relationship between Halimeda cover and accumulated thermal
stress was seen (Figure 5), with a linear correlation on the reef
terrace (Pearson’s r = -0.65, p = 0.03) but not on the fore reef
(Pearson’s r = -0.03, p = 0.92).
4 Discussion
As corals suffer widespread declines due to climate change,
there has been a corresponding rise in the abundance of algae on
reefs worldwide (Pandolfiet al., 2003;Hughes et al., 2017;Reverter
et al., 2021). However, “algae”encompass a heterogenous group of
functionally, phylogenetically, morphologically, and taxonomically
distinct taxa (Fong and Paul, 2011). While short-term changes in
macroalgal abundance on coral reefs, including seasonality, have
been well-documented (Aguila Ramı
rez et al., 2003;Ateweberhan
et al., 2006;Lefèvre and Bellwood, 2010), longer-term dynamics of
benthic algae at the community, functional group, or species level
remain poorly characterized. Here, we present results of an 11-year
time series from Palmyra Atoll in the central Pacific Ocean. From
2009 to 2019, the cover of fleshy and calcareous algae was more
stable at the reef terrace but fluctuated at the fore reef. At the time of
the second, more-severe thermal anomaly in 2015, there was a
general decrease in calcareous algae at both habitats accompanied
by an increase in fleshy algae which was restored within two years.
Given Palmyra’s remote location and high level of federal
protection, such data sets can provide baseline information on
coral reef algal communities in the context of global stressors.
Long-term ecological monitoring is necessary for detecting
trends in species abundance and distribution through time. Prior
to this study, the latest comprehensive analysis of Palmyra’s benthic
algal community composition was based on summary data from
surveys conducted sporadically between 2004 to 2008 (Braun et al.,
2009). Before that, knowledge of algal diversity on Palmyra was
limited to early explorers’species lists (Rock, 1916;Dawson et al.,
FIGURE 3
Percent cover (mean ± SE) of (A) Caulerpa serrulata,(B) Crustose Coralline Algae, (C) Dictyosphaeria spp., (D) Galaxaura rugosa,(E) Halimeda spp.,
(F) Lobophora sp., (G) Peyssonneliaceae sp., and (H) Turf Algae, by habitat (Fore Reef in orange, Reef Terrace in red). Dashed vertical lines indicate
thermal anomalies in 2009 and 2015.
Khen et al. 10.3389/fmars.2025.1539865
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1955;Dawson, 1959). In 2008, the most abundant macroalgal
genera on Palmyra were Halimeda,Lobophora,Galaxaura, and
Dictyosphaeria (Braun et al., 2009). This remained consistent
through 2019, although we also identified C. serrulata as a
common macroalgal taxon on the reef terrace (Supplementary
Table 2). Additionally, Braun et al. (2009) mentioned high cover
of the red alga Dichotomaria marginata near a shipwrecked
longliner vessel which was removed in 2013. Dichotomaria was
absent from our analyses, although not all of the same reef habitats
or sites were represented here, and our study involved small-scale
photoquadrats as opposed to large spatial scale surveys. Braun et al.
(2009) found algal communities to be relatively similar across sites
from the reef terrace and fore reef habitats across the atoll, whereas
in the present study, algal communities showed significant
differences by habitat and time, with more overall stability at the
reef terrace. Calcareous algal cover was consistently higher at the
fore reef, although it is worthwhile to note that Palmyra’s reef
terrace is largely occupied (up to 50%) by hard corals (Fox et al.,
2019;Khen et al., 2022,2024). Overall, fleshy algal abundance on
Palmyra (average percent cover = 20.8%) was low in comparison to
FIGURE 5
Percent cover of Halimeda spp. (mean ± SE) by habitat (Fore Reef in orange, Reef Terrace in red) corresponding to the percentile-based Degree
Heating Weeks (DHW) at each observation time point, labeled by year.
FIGURE 4
Percent cover (mean ± SE) of calcareous (in purple) and fleshy algae (in green) on Palmyra at the (A) Fore Reef and (B) Reef Terrace habitats, along
with post-hoc letter groupings for significant (a= 0.01) differences among years. Dashed vertical lines indicate thermal anomalies in 2009 and 2015.
Khen et al. 10.3389/fmars.2025.1539865
Frontiers in Marine Science frontiersin.org07
reefs with local human populations (average percent cover = 59.3%
according to Smith et al., 2016) whereas calcareous algal abundance
(average percent cover = 34.4%) was much higher than that of
inhabited islands (average percent cover = 16.9%; Smith
et al., 2016).
4.1 Environmental drivers of algal
community structure
Ecological succession and community structure can be shaped
by physical forces such as light and sediment transport (Glynn,
1976), irradiance and water motion (Done, 1982), and wave energy
(Dollar, 1982). On Palmyra, local environmental factors likely
contributed to the spatial variability in benthic algal communities
by habitat. The shallower, wave-sheltered reef terrace, which
receives more light, solar irradiance (Hamilton et al., 2014), and
an influx of nutrients and sediments from the nearby lagoon
(Rogers et al., 2017), had a higher relative abundance of turf and
other fleshy algae throughout the study (Figure 1;Supplementary
Figure 1). The fore reef, which is subject to more wave action and
water motion (Williams et al., 2013;Hamilton et al., 2014;Gove
et al., 2015), had a higher relative abundance of calcareous algae.
Calcified crusts such as CCA and peyssonnelioid taxa are resistant
to high wave energy, which may explain their dominance at this
habitat, as has been seen elsewhere in the tropical Pacific(Page-
Albins et al., 2012). Coralline algae can also shed their epithallial
cells to prevent fouling by fleshy organisms and reinforce their
foundation in wave-exposed habitats (Keats et al., 1997b).
Articulated algal morphologies such as Halimeda are more
vulnerable to dislodgement by waves (Steneck and Dethier, 1994),
but nutrients supplied from upwelling and internal tides on the fore
reef (Williams et al., 2018) may have promoted their growth (Smith
et al., 2004). While temperature could be expected to differ by
habitat, our observations were limited to 10 m depth and upwelling-
induced cooling on Palmyra has only been found to occur below 15
m(Fox et al., 2023).
4.2 Role of herbivory in benthic
algal communities
Although we did not quantify herbivore abundance in this
study, given that Palmyra has very high fish biomass (Williams
et al., 2011;Edwards et al., 2014) and that grazing pressure drives
algal succession (Carpenter, 1986;Hixon and Brostoff, 1996),
biological factors such as grazing may have further contributed to
differences in algal community structure. In our photoquadrat time
series, algal turfs often appeared cropped (pers. obs.), indicative of
grazing. Herbivores can help control fleshy algal cover (Littler et al.,
2006;Burkepile and Hay, 2009) and their presence is associated
with higher cover of corals and CCA (Smith et al., 2010). With
herbivores now being used as a restoration tool to reverse coral-
algal phase shifts on degraded reefs (Mumby, 2014;Ladd and
Shantz, 2020), Palmyra exemplifiestheroleofherbivoryin
maintaining a “healthy”calcifier-dominated reef. Palmyra’s reef
system is dominated by top predators and larger-bodied grazers
(e.g., parrotfish and surgeonfish) as opposed to small planktivores
or echinoids (Sandin et al., 2008). Hamilton et al. (2014) found that
Palmyra’s reef terrace had a higher density of herbivorous fish and
higher grazing intensity (in terms of bite rates) than the fore reef.
Most herbivorous fish on Palmyra feed preferentially on algal turfs
(Hamilton et al., 2014), which are more abundant on the reef terrace
(although parrotfish bite scars are also seen frequently on CCA on
the fore reef; see Charendoff et al., 2023), suggesting that habitat-
specific differences in algal and herbivore assemblages
are interrelated.
4.3 Evidence of thermal sensitivity in
Halimeda spp.
Our study also provides observational evidence that the
calcareous macroalgal genus, Halimeda, may be sensitive to
warming. At both habitats on Palmyra, benthic cover of
Halimeda was among its lowest in 2015 (Figure 5), when
percentile-based DHWs reached a value of 7.76 (or a monthly
mean sea surface temperature of 29.8 °C; National Oceanic and
Atmospheric Administration’s Coral Reef Watch). Perhaps if
temperatures on Palmyra had reached a more extreme upper
limit,thiswouldhavehadamoremeasurableimpacton
Halimeda cover across the atoll. It has previously been proposed
that Halimeda growth and calcification could benefit from seawater
temperatures ranging from 24 to 32 °C, but that temperatures above
34 °C will have consequences that may become lethal at 36 °C (Wei
et al., 2020). Other experimental studies have shown that exposure
to elevated temperatures can either inhibit (Sinutok et al., 2011)or
enhance (Campbell et al., 2016) photosynthetic efficiency,
calcification, and growth in Halimeda spp., indicating that results
may be context-dependent or species-specific(Schubert et al.,
2023). Given their role in both primary and calcium carbonate
production on reefs (Rees et al., 2007), and as a preferred food
source to many reef fishes (Mantyka and Bellwood, 2007;Hamilton
et al., 2014), refining the thermal sensitivity limits of Halimeda by
species (while also taking into account accumulated thermal stress)
and identifying the mechanisms behind this observed phenomenon
will be ecologically relevant in the face of global climate change.
5 Conclusion
In conclusion, more species-specific studies on the thermal
tolerance of benthic algae are needed in order to better
understand current and potential impacts of climate change on
coral reefs. Additionally, comparing calcareous vs. fleshy responses
of benthic algae in situ will be useful for assessing ecosystem status
in the context of rising seawater temperatures. Long-term
monitoring in relatively unimpacted locations, such as Palmyra
Atoll, allows us to track baseline algal community dynamics over
time. To strengthen the value and resolution of these ecological data
sets, future efforts should consider larger-scale surveys with higher
sampling frequency. Although Palmyra’sreefshaveremained
Khen et al. 10.3389/fmars.2025.1539865
Frontiers in Marine Science frontiersin.org08
calcifier-dominated as of 2019, successional trajectories from
Palmyra could inform mitigation strategies at more degraded
reefs shifting toward fleshy algal dominance.
Data availability statement
The datasets presented in this study can be found in online
repositories. The names of the repository/repositories and accession
number(s) can be found below: https://github.com/akhen1/
palmyra-algae.
Author contributions
AK: Conceptualization, Data curation, Formal Analysis,
Funding acquisition, Investigation, Visualization, Writing –
original draft, Writing –review & editing, Methodology. MJ:
Conceptualization, Investigation, Methodology, Writing –review
& editing. MF: Conceptualization, Formal Analysis, Investigation,
Methodology, Writing –review & editing. JS: Conceptualization,
Funding acquisition, Investigation, Resources, Supervision, Writing
–review & editing, Methodology, Project administration.
Funding
The author(s) declare that financial support was received for the
research, authorship, and/or publication of this article. AK was
supported by the National Science Foundation Graduate Research
Fellowship (Award No. 1650112) and the Beyster Family Fellowship
in Conservation and Biodiversity. Funding for this work was
generously provided by the Scripps Family Foundation, the Bohn
Family, and the Gordon and Betty Moore Foundation.
Acknowledgments
We thank the staff of The Nature Conservancy, U.S. Fish and
Wildlife Service, and the Palmyra Atoll Research Consortium
(PARC) for their logistical support and access to the refuge. This
publication is PARC contribution #168. We thank Gareth Williams,
Brian Zgliczynski, Clinton Edwards, Amanda Carter, Samantha
Clements, and Stuart Sandin for their assistance with fieldwork. We
thank Karina Arzuyan, Marie Diaz, Sarah Romero, Kyle Conner,
Shelley Hazen, and Kailey Ramsing for their help with
image digitization.
Conflict of interest
The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could be
construed as a potential conflict of interest.
The author(s) declared that they were an editorial board
member of Frontiers, at the time of submission. This had no
impact on the peer review process and the final decision.
Generative AI statement
The author(s) declare that no Generative AI was used in the
creation of this manuscript.
Publisher’s note
All claims expressed in this article are solely those of the authors
and do not necessarily represent those of their affiliated
organizations, or those of the publisher, the editors and the
reviewers. Any product that may be evaluated in this article, or
claim that may be made by its manufacturer, is not guaranteed or
endorsed by the publisher.
Supplementary material
The Supplementary Material for this article can be found online
at: https://www.frontiersin.org/articles/10.3389/fmars.2025.1539865/
full#supplementary-material
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