Rapid proliferation and impacts of cyanobacterial mats on Galapagos rocky reefs during the 2014-2017 El Niño Southern Oscillation

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DOI: 10.1016/j.jembe.2019.03.007
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Abstract
Cyanobacteria use limiting resources efficiently to take advantage of nutrient pulses, adapt to variable surroundings , and spread; this proliferation is often an indicator of ecosystem stress. We documented the sudden appearance of benthic cyanobacterial mats on a subtidal rocky reef (Roca Cousins, Galapagos Islands) during El Niño in January 2016. At this time, cyanobacteria covered 32.0% of horizontal rock surfaces and 2.6% of rock walls at 6-8 m depth. Monitored photo quadrats and observations indicated that these mats were previously absent from rock walls and horizontal-sloping substrata at this site for 16 years prior to their initial appearance. The cyanobacteria was also observed at 4 other sites in the central Galapagos Islands during 2016-2018. Laboratory experiments testing the effects of temperature (28-31 °C) on cyanobacterial growth and survival indicated that survival was higher at 28 than 31 °C, suggesting that 31 °C may be an upper thermal limit. Over two years in the field, cyanobacterial mats peaked during the warm El Niño (January 2016) and declined during two cold La Niña periods (June 2016, September 2017), ultimately declining to 6.0% cover in January 2018. Regression analysis of the temperature and cyanobacterial percent cover data indicated that temperature explained 56.9% of the variation in cyanobacteria cover in the field over the 2-year period. The cyanobacterial mats may be a consortium of several species as the closest genetic matches confirmed by Sanger sequencing (90-91.5%) were Oscillatoria spongeliae, Merismopedia glauca, and Synechococcus elongatus. Comparison of areas under the cyanobacterial mats to the adjacent uncovered rock substrata suggested that the cyanobacteria had a negative influence on underlying crustose coralline algae (CCA), as the cover of bleached CCA was 1.75 fold higher under the mats while the cover of "healthy" pink-pigmented CCA was 3 fold higher on the uncovered substrata. Short-term field experiments and feeding surveys performed to evaluate predation and to calculate electivity indices indicated that the cyanobacterial mats were avoided by dominant consumers (Eucidaris gala-pagensis, Pentaceraster cumingi, Nidorellia armata, and Prionurus laticlavius). Taken together, these results imply that the novel appearance of cyanobacterial mats in the Galapagos rocky subtidal zone was facilitated by unusually warm temperatures during the 2014-2017 El Niño (28-29 °C) and that the cyanobacteria were regulated by temperature, but not by consumers. Future outbreaks of mat-forming cyanobacteria during El Niño periods may negatively impact the abundance of CCA and have direct and indirect negative effects on other components of marine benthic communities that rely on CCA as either a settlement substratum or food source.
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Journal of Experimental Marine Biology and Ecology
journal homepage: www.elsevier.com/locate/jembe
Rapid proliferation and impacts of cyanobacterial mats on Galapagos rocky
reefs during the 20142017 El Niño Southern Oscillation
Fiona L. Beltram
, Robert W. Lamb, Franz Smith, Jon D. Witman
Brown University, Department of Ecology and Evolutionary Biology, Box GW, Providence, RI 02912, United States
ARTICLE INFO
Keywords:
Cyanobacteria
El Niño
Subtidal reef
Benthic community
Thermal tolerance
Bleaching of crustose coralline algae
ABSTRACT
Cyanobacteria use limiting resources eciently to take advantage of nutrient pulses, adapt to variable sur-
roundings, and spread; this proliferation is often an indicator of ecosystem stress. We documented the sudden
appearance of benthic cyanobacterial mats on a subtidal rocky reef (Roca Cousins, Galapagos Islands) during El
Niño in January 2016. At this time, cyanobacteria covered 32.0% of horizontal rock surfaces and 2.6% of rock
walls at 68 m depth. Monitored photo quadrats and observations indicated that these mats were previously
absent from rock walls and horizontal-sloping substrata at this site for 16 years prior to their initial appearance.
The cyanobacteria was also observed at 4 other sites in the central Galapagos Islands during 20162018.
Laboratory experiments testing the eects of temperature (2831 °C) on cyanobacterial growth and survival
indicated that survival was higher at 28 than 31 °C, suggesting that 31 °C may be an upper thermal limit. Over
two years in the eld, cyanobacterial mats peaked during the warm El Niño (January 2016) and declined during
two cold La Niña periods (June 2016, September 2017), ultimately declining to 6.0% cover in January 2018.
Regression analysis of the temperature and cyanobacterial percent cover data indicated that temperature ex-
plained 56.9% of the variation in cyanobacteria cover in the eld over the 2-year period. The cyanobacterial
mats may be a consortium of several species as the closest genetic matches conrmed by Sanger sequencing
(9091.5%) were Oscillatoria spongeliae, Merismopedia glauca, and Synechococcus elongatus. Comparison of areas
under the cyanobacterial mats to the adjacent uncovered rock substrata suggested that the cyanobacteria had a
negative inuence on underlying crustose coralline algae (CCA), as the cover of bleached CCA was 1.75 fold
higher under the mats while the cover of healthypink-pigmented CCA was 3 fold higher on the uncovered
substrata. Short-term eld experiments and feeding surveys performed to evaluate predation and to calculate
electivity indices indicated that the cyanobacterial mats were avoided by dominant consumers (Eucidaris gala-
pagensis,Pentaceraster cumingi, Nidorellia armata, and Prionurus laticlavius). Taken together, these results imply
that the novel appearance of cyanobacterial mats in the Galapagos rocky subtidal zone was facilitated by
unusually warm temperatures during the 20142017 El Niño (2829 °C) and that the cyanobacteria were
regulated by temperature, but not by consumers. Future outbreaks of mat-forming cyanobacteria during El Niño
periods may negatively impact the abundance of CCA and have direct and indirect negative eects on other
components of marine benthic communities that rely on CCA as either a settlement substratum or food source.
1. Introduction
Under normal conditions, benthic marine cyanobacteria often face
competition from dominant photosynthetic species that inhibit their
spread and success on reefs. However, cyanobacteria are well suited to
colonization of reefs that are experiencing altered or degraded condi-
tions, and can quickly become strong competitors themselves (Ford
et al., 2018). In general, prokaryotes such as cyanobacteria experience
optimal growth at high temperatures (Robarts and Zohary, 1987),
which means that cyanobacteria can tolerate a greater degree of tem-
perature uctuation than many marine organisms. Short generation
times can also favor enhanced adaptive capabilities in variable en-
vironments. Many cyanobacterial species can move within benthic mats
or surface blooms to avoid UV damage while still outcompeting other
benthic organisms for light access (Paerl and Paul, 2012). Others thrive
in nitrogen-decient waters and can switch between nitrogen xation
and other modes of energy acquisition (Paerl and Huisman, 2008).
Accordingly, cyanobacteria may be useful indicators of reef ecosystem
https://doi.org/10.1016/j.jembe.2019.03.007
Received 18 October 2018; Received in revised form 19 February 2019; Accepted 14 March 2019
Corresponding author.
E-mail addresses: ona_beltram@alumni.brown.edu (F.L. Beltram), Robert_Lamb@brown.edu (R.W. Lamb), franzinho@actrix.co.nz (F. Smith),
Jon_Witman@brown.edu (J.D. Witman).
Journal of Experimental Marine Biology and Ecology 514–515 (2019) 18–26
0022-0981/ © 2019 Elsevier B.V. All rights reserved.
T
stress due to changes in temperature, nutrient depletion, coral death, or
increases in solar irradiation (Hallock, 2005;Ford et al., 2018). This
plasticity may also help cyanobacteria thrive in warming marine eco-
systems.
While cyanobacterial blooms are usually a transient sign of recent
ecosystem stress, mat-forming cyanobacteria can quickly dominate
benthic communities by colonizing any available substratum and
overgrowing other organisms (Schroeder et al., 2008;Kelly et al.,
2012). Eventually, this dominance can permanently alter reef eco-
system structure and function by disrupting foundational processes
such as coral recruitment (Titlyanov et al., 2006). As stated by Ford
et al. (2018),reefs dominated by benthic cyanobacterial mats are
likely to produce signicantly less of the ecosystem services associated
with healthy, coral-dominated reefs.
This study documents the novel appearance and ecological impacts
of benthic cyanobacterial mats in shallow rocky subtidal communities
in the central Galapagos Islands (Witman et al., 2010). The mats ap-
peared in January 2016 at the height of the recent, exceptionally strong
El Niño-Southern Oscillation (ENSO) (Wang et al., 2017) at Roca
Cousins (RC, Fig. 1), a pristine oceanic site. Cyanobacterial mats were
recorded for the rst time in 16 years of bi-annual monitoring there and
at 4 other sites (Fig. 1).
Here, we document the appearance of these mats in terms of the
percent of the rocky substrata covered, and use an observational-ex-
perimental approach to address 4 main questions: 1) Will the cyano-
bacterial mats survive in the Galapagos rocky subtidal system beyond
their initial bloom cycle? 2) Is the growth and/or survival of the cya-
nobacteria coincident with the ENSO temperature regime? 3) Is the
extent of cyanobacterial cover regulated through consumption by sea
stars, sea urchins, or sh? And 4) If the cyanobacteria persists, does its
presence negatively impact the underlying benthic community? Finally,
we sought to identify the species of cyanobacteria comprising the mats
using molecular methods.
2. Material and methods
2.1. Mat persistence and eects of temperature
Changes in the percent cover of cyanobacterial mats were quantied
by conducting photo transects in two habitats at Roca Cousins: 1) along
a vertical wall at 68 m depth and 2) across the horizontal substratum
on a terrace at the top of the wall at 56 m depth, both using a quad-
rapod camera framer (Fig. 1,Witman et al., 2010). Photo transects were
2030 m long with photo quadrats taken at random marks (n=1820
Fig. 1. Map of the study area in the central
Galapagos Islands (after Witman et al., 2010). Black
dots indicate sites where benthic communities are
monitored bi-annually. Sites where cyanobacteria
was observed are indicated in red. Note the clus-
tering of observations around the RC site where cy-
anobacterial mats initially appeared. Site abbrevia-
tions as Rocas Cousins]RC, Rocas Beagle = RB, Guy
Fawkes = GF, Baltra = BAL, Pinzon = PIN. Field
experiments were conducted at the Rocas Cousins
(RC) and Baltra (BAL) sites. Temperatures were
measured at all sites at 10-min intervals throughout
the study period. Depths indicated in meters. (For
interpretation of the references to colour in this
gure legend, the reader is referred to the web ver-
sion of this article.)
F.L. Beltram, et al. Journal of Experimental Marine Biology and Ecology 514–515 (2019) 18–26
19
per transect) on the wall and at approximately one meter increments on
the horizontal substratum (n=2530). The photo quadrats were
0.25 m
2
in area (Fig. 2). Transects were conducted biannually on the
vertical wall since 2002 and on the horizontal substratum since January
2016. The percent cover of the cyanobacterial mats was estimated by
overlaying a random 200-dot grid on each 24-megapixel quadrat image
(Fig. 2) using Adobe Photoshop software and counting the number of
dots on the mats corresponding to cyanobacteria using a computer
display. The values for each quadrat were then averaged to obtain a
single percent cover value for each of the available time periods. These
were then regressed against temperature using the following equation:
arcsin square root cyanobacteria cover (y) = 0.5554 + 0.0387×,
where x = mean subtidal temperature on the same days that the pho-
tographs used to obtain percent cover values were taken.
An additional method involving xed quadrats was used to track
changes in the cyanobacteria and benthic communities at Roca Cousins.
This consisted of drilling into the rock to set bolts spaced so that 2
corners of the 0.25 m
2
quadrat frame could be aligned on them, al-
lowing a photo quadrat to be taken in exactly the same area of hor-
izontal rocky substratum. The xed quadrats (n= 4 at 56m, n=3at
1011 m) were photographed at Roca Cousins in January 2017, July
2017, and January 2018. Percent cover of cyanobacteria was obtained
from the quadrat photos (Fig. 2) using the same methods as the photo
transects. Repeated measures ANOVA was performed with quadrat
identity as the between-subjects factor and time as the within-subjects
factor.
We consider the El Niño Southern Oscillation (ENSO) as the time
span from the start of an El Niño to the end of the following La Niña
(Trenberth 1997), as indicated by the Oceanic Niño Index (ONI) for
Pacic region 3.4 (https://www.cpc.ncep.noaa.gov/products/analysis_
monitoring/enso_advisory/). The ENSO studied here began in No-
vember 2014 and continued through January 2017. The El Niño phase
of this ENSO extended from November 2014 June 2016 and is re-
ferred to as the 20142016 El Niño. The 7-month-long La Niña period
began in June 2016 and ended in January 2017. A second La Niña
period, the 20172018 La Niña, began 9 months after the rst one
ended, extending from September 2017 April 2018.
The underwater temperature regime at Roca Cousins was measured
over the 2-year study by deploying HOBO Tidbittemperature loggers
at 6 m depth, set to record at ten-minute intervals. Average subtidal
temperatures on the day that the photo transects were conducted were
used for linear regression analysis of the relationship between tem-
perature and cyanobacteria percent cover at the RC site.
A lab experiment was performed to investigate the optimal tem-
peratures and potentially limiting upper temperatures for the survival
and growth of the cyanobacteria. Samples were collected by removing
45cm
2
pieces from mats at Rocas Cousins and transporting them im-
mediately to the Charles Darwin Research Station (Puerto Ayora,
Galapagos Islands), where the experiment was set up. The experimental
unit was a single piece of the cyanobacterial mat tied to an acrylic plate
and set in a 7.5 L clear plastic bucket. Temperature was controlled by a
25-watt Hydor Theoheater in each bucket. Six temperature treat-
ments were maintained at 1 °C increments from 26 to 31 °C, with 3
replicates of each temperature (18 buckets total). The temperatures
used in these treatments encompassed the maximum temperatures re-
corded at the 5 sites (25.129.7 °C) containing cyanobacterial mats
during the El Niño period (Table 1,Lamb et al., 2018).Treatments were
assigned to buckets at random to eliminate potential eects of en-
vironmental gradients across the experimental space. Each unit was
aerated and the seawater was changed daily throughout the duration of
the 14 - day experiment (July 27 August 6, 2017). The buckets were
placed outdoors, in a location that was shaded enough to mitigate daily
temperature uctuations yet unobstructed enough to allow even access
of moderate levels of ambient light. To quantify changes in the surface
area of the cyanobacteria, samples were photographed daily and the
resulting photographs analyzed for total area using Image J software.
Area values were converted to percent cover, and linear regressions
were t to plots of percent cover over time. A one-way ANOVA was
then performed on the slopes of the linear regressions, grouped by
treatment.
2.2. Eects of consumers on cyanobacterial mats
To test whether predators and herbivores feed on cyanobacteria and
may regulate their abundance, an experiment was conducted at the
Baltra site (Fig. 1) at 10 m depth in July 2017 to manipulate consumer
access to transplanted pieces of cyanobacteria. The procedure consisted
of rst transplanting samples of cyanobacteria onto 10 × 10 cm acrylic
plates. Standardized samples of cyanobacterial mats were retained on
the plates by sections of elastic shnet stockings with wide, 1.5-cm
Fig. 2. (A) shows a photo quadrat (0.25 m
2
area) taken on January 19, 2016
illustrating the high cover of mat forming cyanobacteria (brown areas) during
the 201416 El Niño. Also visible are pink crustose coralline and green Codium
algae. The sea star is Nidorellia armata which was one of the sea stars assessed
for potential feeding on the cyanobacteria. This is one of many photo quadrats
taken with the quadrapod camera system which was used to assess the abun-
dance and distribution of cyanobacteria in transects on horizontal substrata
(Fig. 3) and on rock walls (Fig. 4), and in xed quadrats. (B) provides an ex-
ample of healthypink-pigmented crustose coralline algae, while the arrow in
(C) indicates an area of white, bleached crustose coralline algae. J. Witman
photo credit. (For interpretation of the references to colour in this gure legend,
the reader is referred to the web version of this article.)
Table 1
Maximum temperatures recorded by Onset Tidbittemperature loggers at the 5
study sites where cyanobacterial mats were observed (6 m depth) during the
20142016 El Niño period, as indicated by the Oceanic Nino Index (ONI) for
Pacic region 3.4. NA = data not available.
Site OctoberDecember 2014 JanuaryDecember 2015 JanuaryJune 2016
RC 25.5 °C 29.3 °C 28.6 °C
RB 25.1 °C 29.1 °C 28.6 °C
GF 25.5 °C 29.7 °C 28.7 °C
BAL 25.7 °C 29.6 °C 29.1 °C
PIN NA 29.0 °C 28.3 °C
F.L. Beltram, et al. Journal of Experimental Marine Biology and Ecology 514–515 (2019) 18–26
20
mesh openings. Consumers had access to the cyanobacteria exposed in
the large openings of the mesh. Plates were arranged in replicated pairs
(n= 7), with one plate per pair enclosed in a cage of Aquamesh
(0.22 m
2
area) to exclude predation by sh and invertebrates. The other
plate was not caged, which allowed consumer access. Paired replicates
were situated approximately 3 m apart to ensure independence. The
experiment ran for 7 days (July 25 August 4, 2017). All treatments
were photographed at the beginning and end of the experiment with the
quadrapod camera framer. Changes in surface area were measured from
the photographs using ImageJ (as above) and a Student's t-test was
performed on the resulting data.
To investigate potential predation of cyanobacteria in a more de-
tailed manner, a 2-h experimental assay was conducted at Roca Cousins
in August 2017. In this experiment, pieces of cyanobacterial mats were
collected and axed to acrylic plates that were attached to underlying
lead weights and placed on the natural rock substrata in two groups
spaced approximately 12 m apart (n= 15 replicates per group). Fishnet
stockings were used to retain the transplanted cyanobacteria in the eld
as in the lab experiment (above). A GoPro4 video camera was focused
on each group of cyanobacteria and also on 2 adjacent, comparable
areas of the rock substratum containing natural patches of cyano-
bacteria. The cameras recorded any feeding on the cyanobacteria on the
plates and on the natural substratum while divers were absent. Bites
were recorded for the yellowtail surgeonsh Prionurus laticlavius, ring-
tail damselsh Stegastes beebii, Panamic fanged blenny Ophioblennius
steindachneri, and the wrasse Thalassoma lucasanum. P. laticlavius is a
dominant herbivore on the reef (Quimbayo et al., 2018), descending in
large schools to feed on benthic algae. S. beebii perform a similar
function; additionally, they dene their territories by maintaining
gardensof foliose algae on the substratum. The videos were sub-
divided into fteen-minute replicates, separated by two-minute incre-
ments. The resulting video segments were analyzed using BORIS
software, counting all bites by each sh species on cyanobacteria and
the surrounding substratum. Bite rates were calculated per fteen-
minute segment and averaged by species.
The sea stars Nidorellia armata and Pentaceraster cumingi are major
herbivores on Galapagos reefs (Sonnenholzner et al., 2013). During
August 2017, we assessed potential sea star feeding on cyanobacteria by
stretching two 30-m long transects horizontally across the bottom
(68 m depth) at Roca Cousins in order to photograph quadrats of the
benthic communities at 1 m intervals. Concurrently, each sea star en-
countered within a 1-m swath of the transect was turned over to see if it
was feeding, which was indicated by eversion of the cardiac stomach.
The prey or substratum underneath the sea star was recorded. Using
data on the availability of potential food items in the natural habitat
from the photo quadrats taken along the transects combined with the
sea star feeding data, electivity indices were calculated (Ivlev, 1961) for
all potential food items.
2.3. Ecological impacts
To compare the community structure of the benthos underlying
cyanobacterial mats with reef not covered by cyanobacteria, mats were
removed from seven replicate 0.25 m
2
areas of the horizontal rock
substratum at 46 m depth at Roca Cousins in July 2016. The 4-step
procedure consisted of 1) placing the frame of the quadrapod over an
area covered in cyanobacteria, 2) taking a high-resolution photograph,
3) holding the quadrapod in place on the substratum while all cyano-
bacteria inside the frame was gently scraped owith a gloved nger,
and 4) taking a second photograph. Images were later aligned in ImageJ
to identify percent cover of algae and invertebrates (see Table 3 for
detailed categories) in the area under the cyanobacteria that was ex-
posed after removal. Percent cover values for these areas were de-
termined using a standard-spaced (1.5 × 1.5 cm) grid, as the irregular
shape of the removal areas meant that the 200 random dot grid method
was not dense enough to represent actual community composition.
General percent cover values for all other benthic organisms were ob-
tained using the 200-dot grid method described above. The two sets of
values were compared via Student's t-test, using the average percent
cover of each category (n= 7 removal quadrats).
All statistical analyses were performed using R v. 3.4.2, and in-
cluded the use of ANOVA functions in packages userfriendlyscience and
lawstat.
2.4. Microscopic and genetic evaluation of cyanobacterial mats
Microscopy and genetic methods were used in an eort to identify
the species making up the mats. Samples of the cyanobacterial mats
were prepared for microscopy using a standard wet mount technique.
All microscopy was conducted with a Zeisslight microscope at 40 to
100 X with an attached Olympuscamera.
To obtain genetic data, samples were rst dissected into four dis-
tinct layers (top, middle, bottom, and cross-section). A QIAGENkit
was used for extraction. Each sample was placed into a 1.5-μL
Eppendorf tube, and 500 μL of phosphate-buered saline (PBS) was
added, along with four Zirconia beads and 100 μL glass beads. Samples
were homogenized, then centrifuged. The pellets were re-suspended in
180-μLBuer ATL. The tubes were then incubated at 37 °C for 30 min.
25 μL of proteinase K was added to each tube before incubation at 56 °C
for one hour. Then, 200 μLofBuer AL and 200 μL ethanol were added.
The tubes were vortexed and the samples added to spin columns. These
were centrifuged at 6000 gfor 1 min and ow-through was discarded.
The samples were then washed with 500 μLBuer AW1, centrifuged at
6000 gfor 1 min, washed with 500 μL of AW2, and centrifuged at
20,000 gfor 1 min. The columns were placed in labeled tubes with
50 μL of elution buer, then centrifuged at 6000 gfor 1 min to transfer
the samples. A master mix for PCR was then created using DMSO,
PhusionMaster Mix, water, the template DNA, and forward and re-
verse primers diluted to 10 μM. Cyanobacteria-specic primers
CYA106F and CYA781R were used after Nübel et al. (1997). PCR was
run as follows: 1) an initial denaturing at 95 °C for 5 min, 2) denaturing
at 95 °C for 45 s, 3) annealing at 52 °C for 45 s, 4) extension at 72 °C for
3 min, 5) 35 cycles of Steps 24, and 5) a nal extension at 72 °C for
10 min. After using agarose gel electrophoresis to ensure that the PCR
product was of the expected length, it was cleaned up following the
QIAGEN protocol. Samples were sequenced via the Sanger method by
the University of Rhode Island's Genomics and Sequencing Center. The
resulting sequences were matched to existing genetic information using
the National Center for Biotechnology Information (NCBI)s BLAST tool.
3. Results
Cyanobacterial mats were initially observed at the Roca Cousins site
in January 2016 (Figs. 1, 2) where cyanobacteria covered 32.0% of the
primary substratum (Fig. 3). Mat cover fell to 13% in June, then in-
creased to 26% cover in January 2017. This pattern of cyanobacterial
cover was similar to that of subtidal temperatures measured at the same
site (Fig. 3). At the outset of the cyanobacterial bloom, the maximum
temperature was 28.6 °C (6 m depth) and during the previous
12 months the temperature peaked at 29.3 °C (Table 1). These tem-
peratures are characteristic of a strong El Niño (Lamb et al. 2018, J.
Witman and F. Smith, unpublished data). Temperatures dropped to
15.1 °C during June 2016 as cyanobacteria cover declined during the
cool, La Niña phase of the ENSO cycle (Fig. 3). Divers observed that the
cyanobacteria lost pigment and aked othe substratum during cool
periods in July 2016 and August 2017. Two years after it was initially
observed, cyanobacterial abundance declined to an average of 6% cover
at RC in January 2018 (Fig. 3A).
This relationship was characterized by a signicant positive linear
relationship between subtidal temperature and the percent cover of
cyanobacterial mats over the two year period (Fig. 3C, both variables
measured at RC). Linear regression of daily mean temperature against
F.L. Beltram, et al. Journal of Experimental Marine Biology and Ecology 514–515 (2019) 18–26
21
cyanobacteria percent cover indicated that temperature explained
56.9% of the variation in cyanobacteria cover (Fig. 3C, adjusted
r
2
= 0.569, p= 0.050, cover data arcsin square root transformed).
The photographic time series on the rock wall at Roca Cousins in-
dicated that cyanobacteria was absent from January 2002 until January
2016 (Fig. 4). This conrms that the initial appearance of the mats
occurred at Rocas Cousins during January 2016 of the El Niño period,
when they covered an average of 2.6% of the rock wall habitat. Cya-
nobacteria cover was 12.3 times higher on the horizontal substrata than
in rock wall habitats, but it appeared in both habitats (rock wall, hor-
izontal substrata) at the same time. After the initial appearance at RC,
small patches of cyanobacterial mats were subsequently observed at 4
additional biannually monitored sites across the archipelago (Rocas
Beagle, Guy Fawkes, Baltra, Pinzon, Fig. 1) between January 2016 and
2018, indicating that cyanobacterial mats were more broadly dis-
tributed beyond than the original RC study site. Cyanobacteria do not
appear in the photo quadrats taken on rock walls from Rocas Cousins or
any other of the 11 bi-annually monitored sites (Fig. 1) prior to January
2016 (J. Witman and F. Smith, unpublished data).
The xed quadrat series at 6 m depth, analyzed over three time
periods between July 2016 and January 2018, also demonstrated large
temporal variation in the percent cover of cyanobacteria. Repeated
Fig. 3. Association between the average percent cover of cyanobacterial mats (A) and temperature (B) recorded at 6 m depth at the Rocas Cousins site. Each data
point represents a reading taken by HOBO Tidbitloggers (see Methods). (C) shows a signicant linear regression of temperature and cyanobacteria abundance
where temperature explained 56.9% of the variation in the percent cover of cyanobacteria (cover data arcsin square root transformed, p< 0.05). The regression is
based on data from the 6 sampling periods shown in (A) and (B). Error bars represent standard errors.
Fig. 4. Average percent cover of cyanobacteria on the monitored rock wall (6 m depth), at Roca Cousins from January 2002 to January 2018. n= 594 photo quadrats
(0.25 m
2
area) as in Fig. 2.
Error bars represent standard errors.
F.L. Beltram, et al. Journal of Experimental Marine Biology and Ecology 514–515 (2019) 18–26
22
measures ANOVA indicated a signicant eect of time period on per-
cent cover (F
3,2
= 15.4, p= 0.004).
The lab experiment revealed dierences in the survival of the cya-
nobacteria as a function of temperature (Fig. S1). While the overall
trend was that the transplanted cyanobacterial mats decreased in size
over the course of the 10-day experiment, the treatments at 3031 °C
lost signicantly more area than those 2829 °C. This was indicated by
the one-way ANOVA on the slopes of the regression lines (Fig. S1, F
4,
12
= 3.8753, p= 0.03) followed by Tukey's post-hoc tests (Table 2). A
one-way ANOVA comparing the initial size of the transplanted cyano-
bacterial mats among temperature treatments indicated that there was
no dierence in mat sizes used in the experiment (F
4, 12
= 3.1454,
p= 0.0551, data arc sine transformed). Subsequent Tukey's tests did
not return any signicant dierences in initial mat size among all
pairwise comparisons of temperature treatment groups.
Despite exceptionally abundant herbivorous shes (Quimbayo
et al., 2018) and sea urchins (Witman et al., 2017) in the Galapagos
subtidal, the consumer exclusion experiments indicated that herbivores
do not control the spatial cover of cyanobacterial mats in this en-
vironment. There was no dierence in the average change of cyano-
bacteria surface area between the open (0.026% ± 0.0081%) and
caged (0.035% ±0.019%) treatments (n= 6 per treatment, p= 0.59,
two-sample t-test) after 7 days of excluding sh and sea urchins.
Data from the video-recorded predation assays suggested that the
absence of an eect of consumer exclusion (as above) resulted from a
lack of feeding on the cyanobacterial mats. For example, the videos
revealed that four species of sh, P. laticlavius,S. beebii, O. steindachneri,
and T. lucasanum were actively biting the substrata surrounding the
cyanobacteria throughout the recording period (Table S1). Average bite
rates, however, were 0.5 to 21.5 times higher on the substrata than on
the cyanobacteria transplanted to the plates (Table S1), depending on
the species. The bite rate of the major herbivore P. laticlavius was up to
6.75-fold higher on the substrata than on the transplanted cyano-
bacteria. None of the sh bit the cyanobacteria more than once in any
15-min segment of video (Table S1).
Similarly, electivity analysis of sea star diets revealed negative
electivity values for cyanobacteria (1.0, Table S2), indicating that
Nidorellia armata and Pentaceraster cumingi avoided feeding on the mats.
The only positive electivity values were for Nidorellia armata and
Pentaceraster cumingi feeding on CCA (Table S2), suggesting a pre-
ference for CCA by these sea stars.
Comparison of the areas under the cyanobacterial mat to the normal
rock substratum highlighted several notable dierences in community
composition (Fig. 5,Table 3). For example, there was 3 times more
pink-pigmented CCA outside of the areas covered by cyanobacterial
mats than occurred underneath the mats (Table 3, paired t-test,
p< 0.001). Conversely, the area of bleached crustose coralline algae
was 1.75 times higher under the cyanobacteria (Table 3, paired t-test,
p< 0.043). The cover of eshy encrusting algae Hildenbrandia and
bare rock was also signicantly higher under the cyanobacteria (Fig. 5).
The appearance of the cyanobacteria is a dark brown mat-like lm
over the reef surface (Fig. 2), adhering loosely to the substratum. The
lm is a few millimeters thick, with a clear gelatinous under-layer.
Under a light microscope (100× magnication), it is possible to dis-
tinguish two distinct layers. The top layer is composed of tightly
packed, multicellular non-branching laments (Fig. 6A, B). No notice-
able mucous sheath is visible, and the laments are segmented with
rounded ends. These laments appear lightly pigmented, and give the
mat its brown-green colour. The second layer is far less structured; in
most cases, no discernible patterning is visible. In some samples,
translucent sheets with a honeycomb pattern can be identied. Grains
of sand and other bits of sediment are sometimes embedded within this
lower, gelatinous layer.
The closest conrmed genetic matches from the Sanger sequencing
data were Oscillatoria spongeliae,Merismopedia glauca, and
Synechococcus elongatus. Identity matches ranged between 90.4% and
91.5%. Our sequences also matched partial sequences and uncultured
OTUs in the NCBI database with a high degree of delity. Often, OTUs
have been identied from a sample but have not been successfully
cultured in a laboratory setting, and represent local variations or en-
demic species. Additionally, there may be more than one species
comprising the mat.
4. Discussion
We observed unusual temporal variability in the abundance, growth
and survival of mat-forming cyanobacteria on scales of weeks to years
in the Galapagos rocky subtidal that were clearly associated with
temperature. The rapid proliferation of cyanobacteria at Roca Cousins,
covering one third of the rocky reef in 6 months where it was previously
absent, occurred during the transition from the cold season to the
warmest months of the 20142016 El Niño. Observation of cyano-
bacteria at four additional sites occurred under similar temperature
regimes (Table 1). In other reef ecosystems in the Pacic and Caribbean
bloomsof benthic cyanobacteria typically occur during warm
summer months (Albert et al., 2005;Ford et al., 2018). Among benthic
organisms, cyanobacterial growth rates are nearly unparalleled as
blooms are capable of covering up to 30 km
2
of substratum in three
months (Albert et al., 2005). On the scale of weeks, our results from the
lab experiment indicate that 28 °C water temperatures provide a better
environment for cyanobacteria than either the 30 or 31 °C temperature
treatments. Maximum temperatures at 6 m depth attained the 2829 °C
range at several of the Galapagos sites where cyanobacterial mats oc-
curred during the 20142016 El Niño. Our nding that temperatures
characteristic of El Niño resulted in the least loss of surface area in the
buckets, along with the positive relationship between temperature and
cyanobacteria percent cover in the eld, suggests that the El Niño
thermal regime was benecial to the persistence of the cyanobacteria.
The 3031 °C range may be an upper threshold for the thermal toler-
ance of these mat-forming bacteria. However, further testing of tem-
perature eects with greater replication and a broader range of tem-
perature treatments is needed to identify upper, lower, and optimal
temperatures for cyanobacterial growth and survival.
Temperature, though, is not the only factor that dictates the es-
tablishment and survival of cyanobacteria on reefs (Charpy et al., 2011,
Ford et al., 2018). Temperature changes can covary with other en-
vironmental factors such as nutrient availability. While nitrogen is often
a limiting nutrient, cyanobacteria have been found to be more re-
sponsive to iron and phosphorus limitation. In areas of volcanic sedi-
ment, such as the Galapagos Islands, sudden releases of iron can result
from anoxic events or phytoplankton blooms (Ahern et al., 2003,Schils,
2012). Free ions have been documented to trigger benthic cyano-
bacterial mat growth. Cyanobacteria in algal turf assemblages may act
as a seed population for the expansion of more cyanobacterial mats
(Ford et al., 2018). If such a seed population was present among the
Table 2
Results of Tukey's post-hoc tests following ANOVA test on the slopes of
linear regressions t to changes in percent cover of cyanobacteria (Fig.
S1), grouped by temperature treatments. Signicant dierences in
boldface type.
Temperature (°C) treatment comparison P-value
29 vs 28 0.504
30 vs 28 0.040
31 vs 28 0.030
32 vs 28 0.177
30 vs 29 0.441
31 vs 29 0.342
32 vs 29 0.846
31 vs 30 0.999
32 vs 30 0.992
32 vs 31 0.972
F.L. Beltram, et al. Journal of Experimental Marine Biology and Ecology 514–515 (2019) 18–26
23
Galapagos reef community, the combination of temperature increases
and changes in nutrient availability may have provided the perfect
stormto precipitate the rapid growth observed in January 2016.
Biological and anthropogenic factors may have also contributed to
the unique, rapid expansion of benthic cyanobacterial mats in rocky
subtidal habitats of the central Galapagos. In particular, sea cucumbers
(holothurians) have been shown to reduce the abundance of cyano-
bacteria through their feeding in both lab and eld experiments
(Uthicke, 1999,Michio et al., 2003,Moriarty et al., 1985). This includes
the consumption of a species of Oscillatoria, (a genus identied in the
Galapagos mats), by the holothurian Holothuria atra in Moorea
(Sournia, 1976). While these studies were conducted in soft-substrate
habitats, it is possible that holothurians may play a similar role in re-
ducing cyanobacteria in hard-substrate habitats as well. In the Gala-
pagos Islands, populations of the sea cucumber Stichopus fuscus have
been severely overshed since 2004 (Shepherd et al., 2004;Wolet al.,
2012). This raises the possibility that the recent increase in benthic
cyanobacteria in the central Galapagos may have been at least partly
fostered by the overshing of sea cucumbers.
While there are a number of factors that dier between horizontal
and vertical (rock wall) habitats in the subtidal zone, we suggest that
Macroalgae
Invertebrates
Codium
Bleached CCA
Hildenbrandia
Rock
Pigmented CCA
0 204060
Percent cover (mean +/− SE)
Control
Removal
Fig. 5. Percent cover of benthic organisms and bare
rock underlying cyanobacteria after it was removed
(grey bars, labeled removal) vs on the un-
manipulated rocky substrata where cyanobacteria
didn't occur (clear bars, labeled control) at the RC
site in July 2016. Sample size was seven 0.25 m
2
quadrats. Error bars represent standard errors.
Table 3
Results of Student's t-test comparing the average percent cover of benthic or-
ganisms and bare rock underneath versus outside of areas covered by cyano-
bacterial mats, (n = 7 removal quadrats). Data plotted in Fig. 5. Signicant
dierences in boldface type. CCA = Crustose Coralline Algae.
Category T-value P-value
Pink CCA 11.42033 8.38 × 10
8
Bleached CCA 2.258224 0.04335
Hildenbrandia 3.857338 0.00228
Codium 1.672733 0.120228
Bare Rock 2.63635 0.02172
Invertebrates 0.198657 0.845857
Macroalgae 1.682731 0.118242
Fig. 6. Microscopic structure of the cyanobacteria A. upper layer of the mat, 40× magnication. Note pigmentation, close packing, and orientation of laments. B.
upper layer, 100× magnication. Note multicellular laments. C. Gelatinous underlayer, 100× magnication. Photo credits F. Beltram.
F.L. Beltram, et al. Journal of Experimental Marine Biology and Ecology 514–515 (2019) 18–26
24
higher light levels on horizontal vs. vertical surfaces (Witman and
Cooper, 1983;Miller and Etter, 2008) is a key factor explaining the
greater abundance of the photosynthetic cyanobacterial mats in hor-
izontal rocky habitats at Roca Cousins.
The results of the eld experiments manipulating consumer access
to cyanobacterial mats in and out of cages and the video-recorded
predation assays are consistent with other studies indicating that
benthic cyanobacteria are unpalatable to many species of consumers
(Homan, 1999;Ford et al., 2018). In particular, the cyanobacterial
mats investigated here were largely avoided by two species of sea stars
(N. armata, P. cumingi) and 4 species of sh (P. laticlavius,S. beebii, O.
steindachneri, and T. lucasanum). Cyanobacteria is often avoided be-
cause of its low nutritional value and concentration of toxic secondary
metabolites, which reduce palatability (Thacker et al., 1997;Golubic
et al., 2010;Capper et al., 2016). Once established, the cyanobacteria's
ability to persist in an ecosystem may be due to the fact that major
herbivores do not use it as a signicant source of food. Not all con-
sumers, however, avoid cyanobacteria. Surgeonsh (Ctenochaetus
striatus) in Vanuatu and unicornsh in French Polynesia and New Ca-
ledonia have been observed feeding on blooms of cyanobacteria
(Laurent et al., 2012).
The removal experiment indicates that Hildenbrandia, bare rock, and
bleached coralline algae (CCA) are commonly found under cyano-
bacterial mats at Roca Cousins, and that pigmented CCA is more
common outside of the cyanobacterial mat than under it. The cyano-
bacteria may preferentially recruit to certain substrata, growing in
areas where these are present in greater abundance as Brocke et al.
(2015) demonstrated with settlement patterns of benthic cyano-
bacterial on reefs surrounding Curacao that were dependent on species-
specic substrate preferences. The study by Brocke et al. (2015) in-
volved multiple species of Oscillatoria, which was also identied as a
possible component of the Galapagos cyanobacterial mats. In this study,
the nding of signicantly higher occurrence of bleached CCA beneath
cyanobacterial mats than outside the mats is consistent with the hy-
pothesis that the mats adversely aect CCA, causing it to lose pigment.
It follows that the amount of pink pigmented CCA would be higher
outside the mats which was another result of our cyanobacteria removal
experiment. However, since we were unable to add cyanobacteria to
natural substrates in the eld to denitively show that CCA bleach
when covered by cyanobacteria, we cannot rule out alternate hy-
potheses to cause bleached CCA. One of these is that the bleached CCA
patches were created by sea star (N. armata) feeding that was subse-
quently covered by cyanobacteria. However, this interpretation is less
likely to explain the occurrence of typically small patches of bleached
CCA (Fig. 2C) beneath cyanobacterial mats documented here as N. ar-
mata feeding creates large (tens of square centimeters) areas of
bleached CCA nearly equal to the surface area of the oral side of the sea
star. One scenario for cyanobacteria colonization may involve pre-
ferential settlement and recruitment of cyanobacteria to bleached pat-
ches of CCA due to the lack of other encrusting species in the patches.
This scenario is particularly relevant given the ability of cyanobacteria
to quickly and opportunistically dominate bare space. Similarly, eshy
algae such as Hildenbrandia may also serve as a preferred recruitment
substrate for epiphytic cyanobacteria.
These spatial patterns also provide insight into the potential impacts
of long-term cyanobacterial mat cover on reef-building species such as
corals. Kuner et al. (2006) found that the presence of local macroalgae
and cyanobacteria negatively aected coral recruitment in the Florida
Keys through obstruction of space. Dictyota spp, which makes up about
50% cover on the reefs they studied, had a particularly signicant ne-
gative eect on recruitment. In the Galapagos rocky subtidal, one third
of the substrata was obstructed by lms of the cyanobacterial mats in
January 2016, which could have prevented the recruitment of coral
planulae at this time. Kuner et al. (2006) also found that reduced coral
recruitment success could not be explained solely by spatial competi-
tion, and speculated that allelochemicals associated with the
cyanobacteria also played a role in the coral recruit mortality they
documented. Further molecular analyses are needed to resolve the
species composition of the cyanobacterial mats studied here, and can
provide more detailed information regarding the potential presence of
allelochemical activity. These mats, however, may directly aect coral
recruitment through light obstruction or space pre-emption.
Introduction of cyanobacterial mats to a reef environment can
drastically alter reef community structure and function. Cyanobacteria-
dominated reefs can display simplied food webs with weaker energy
ow from primary producers to higher-level consumers (Ullah et al.,
2018). Thus, the presence of cyanobacteria may accelerate degradation
of already threatened reefs, and destabilize more functional ones. The
appearance of cyanobacterial mats at a relatively pristine oceanic site in
Galapagos suggests that extreme climate events such as El Niño may
foster their development even in the absence of other factors known to
be conducive to cyanobacterial growth, such as habitat degradation and
water pollution (Ford et al., 2018). Since the frequency and magnitude
of El Niño events are predicted to increase with climate change (Cai
et al., 2014), unravelling the primary drivers of cyanobacterial blooms
and their direct and indirect ecological impacts across trophic levels in
the Galapagos subtidal reefs warrants further investigation.
5. Conclusions
This study documents the rapid expansion of cyanobacterial mats at
a subtidal site in the central Galapagos Islands, covering 33% of the
rocky reef. Our ndings suggest that this expansion was facilitated by
unusually warm temperatures during the 20142017 El Niño.
Experimental results from a lab experiment corroborate evidence from
the eld, as temperatures characteristic of El Niño resulted in the least
loss of surface area. While temperature is implicated in the expansion of
cyanobacteria, consumer response to its presence played a signicant
role in its persistence on the reef, especially at Rocas Cousins. The cy-
anobacteria was unpalatable to several herbivorous sh species and
avoided by two species of sea stars, largely freeing it from consumer
pressure. The continued presence of cyanobacterial mats on subtidal
reefs in the Galapagos Islands could have far-reaching impacts on the
overall structure of the benthic community.
Supplementary data to this article can be found online at https://
doi.org/10.1016/j.jembe.2019.03.007.
Funding
This research was funded by grants from the National Science
Foundation (OCE-01450214, OCE-1623867) and the Galapagos
Conservancy to J. Witman, and by scholarships to F. Beltram from
Brown University UTRA and Voss Fellowship Programs.
Acknowledgments
Thanks to our colleagues, especially C. Lupi and A. Perez-Matus for
their help in the eld and laboratory and B. Brown for help with the
molecular analyses. A. Izurierta, M. Romoleaux, H. Jager and the rest of
the staat the Charles Darwin Foundation facilitated our research.
Thanks to the Galapagos National Park, in particular D. Rueda, J.
Suarez, E. Espinoza and D. Lara, for permission to conduct this research
under research permit # PC-06-16. We are indebted to the following
captains of Galapagos research vessels and boats; W. Aguirre of the
Valeska, E. Rosero of the Queen Mabel and N. Ibarra of the Genesis for
transportation to the research sites and for dedicated help at sea. To all
we are grateful. This publication is contribution number XXX of the
Charles Darwin Foundation for the Galapagos Islands.
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