Access to this full-text is provided by Wiley.
Content available from Conservation Letters
This content is subject to copyright. Terms and conditions apply.
Received: 5 February 2018 Revised: 26 August 2018 Accepted: 4 September 2018
DOI: 10.1111/conl.12609
LETTER
Harnessing marine microclimates for climate change adaptation
and marine conservation
C. Brock Woodson1Fiorenza Micheli2Charles Boch2Maha Al-Najjar3
Antonio Espinoza1,4 Arturo Hernandez5Leonardo Vázquez-Vera5Andrea Saenz-Arroyo6
Stephen G. Monismith3Jorge Torre5
1COBIA Lab, University of Georgia, Athens,
Georgia
2Hopkins Marine Station and Center for Ocean
Solutions, Stanford University, Pacific Grove,
California
3EFML, Stanford University, Palo Alto,
California
4Sociedad Cooperativa de Producción Pes-
quera Buzos y Pescadores, Isla Natividad, Baja
California Sur, México
5Comunidad y Biodiversidad, La Paz, Mexico
6Departamento de Conservacion de la Biodi-
versidad, El Colegio de la Frontera Sur, San
Cristobal de las Casas, Mexico
Correspondence
C. Brock Woodson, College of Engineering,
University of Georgia, 708C Boyd GSRC,
200 D.W.Brooks Dr., Athens, GA 30602.
Email: bwoodson@uga.edu
Funding information
Division of Ocean Sciences, Grant/Award
Numbers: 1416837, 1737090; Division of
Environmental Biology,Grant/Award Num-
ber: 1212124
Funding information
NSF, Grant Numbers: CNH-DEB-1212124,
OCE-1416837, OCE-1737090; WaltonFamily
Foundation; Packard Foundation; Marisla and
Sandler Family Foundation
Main Points
-Responses to climate change and large-scale forcing can vary widely at local scales
creating marine microclimates.
-Microclimates are robust even under extreme large-scale forcing events (ENSO,
climate change) potentially creating spatial refuges or ‘safe spaces’ for important
species.
-Small/medium no-take zones, artificial reefs, and other possible spatial manage-
ment can be placed to harness local variability as an adaptation or conservation
measure in the face of climate change.
KEYWORDS
climate forcing, environmental variability, fisheries, local conservation, marine microclimates
Abstract
Climate change is warming, deoxygenating, and acidifying the ocean at an unprecedented rate. However, responses to large-
scale forcing are variable at relatively small spatial scales, creating marine microclimates. Marine microclimates can provide
spatial refuges (safe spaces) or local adaptation that may be harnessed to improve marine conservation and management.
We analyze multiyear data sets within two fishing cooperatives in Baja California, Mexico, to quantify small-scale ocean
variability, describe the degree to which this variability affects the abundance of species, and discuss the potential for marine
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original
work is properly cited.
© 2018 The Authors. Conservation Letters published by Wiley Periodicals, Inc.
Conservation Letters. 2019;12:e12609. wileyonlinelibrary.com/journal/conl 1of9
https://doi.org/10.1111/conl.12609
2of9 WOODSON ET AL.
microclimates to improve conservation and management efforts. We find that variation in ocean conditions and species abun-
dances at scales of a few kilometers is striking and robust to large-scale climate forcing. We posit that incorporation of marine
microclimates into fisheries management and conservation efforts can improve ecosystem sustainability by allowing local
adaptation and maintenance of spatial refuges in the face of climate change.
1INTRODUCTION
Climate change is altering ocean conditions and increas-
ing the frequency and severity of extreme events (Cavole
et al., 2016; Sydeman, Santora, Thompson, Marinovic, &
Lorenzo, 2013; Wang, Gouhier, Menge, & Ganguly, 2015).
Increasing extreme events (hypoxia, heat waves, acidifica-
tion) along with background environmental change portend
a grim fate for marine ecosystems (Breitburg et al., 2018;
Bruno et al., 2018; Hughes et al., 2018). However, climate-
scale variability manifests differently in nearshore regions,
creating marine microclimates that may provide a natural
refuge from large-scale climate effects (Kwiatkowski & Orr,
2018; Safaie et al., 2018). Local alteration of large-scale cli-
mate responses can directly affect important coastal ecosys-
tems (Boch et al., 2018). Marine microclimates may provide
a key avenue for building adaptive capacity and enabling con-
servation in the face of global climate change (Cinner et al.,
2018).
Generally, local management and conservation efforts are
perceived to be futile in the face of larger scale climate
change driven declines in ecosystem health and fisheries
production (Boyce, Lewis, & Worm, 2010; Cheung et al.,
2009; DeCarlo et al., 2017; Lotze & Worm, 2009; Pauly
& Christensen, 1995). However, local oceanographic con-
ditions and ecological outcomes can be dramatically differ-
ent than the general predictions of climate change (O'Leary
et al., 2017). Management should reflect the local manifes-
tation of climate variability instead of responding to ubiqui-
tous global forecasts and perceptions (Prince, 2003). Thus,
it is important to identify marine microclimates so that they
can be incorporated into local conservation and adaptation
efforts.
In order to help understand how global climate variabil-
ity manifests locally in the central Baja California region
of México, we partnered with two fishing cooperatives
and established a long-term collaborative program that
included moorings with sensors for temperature, salinity,
and dissolved oxygen around Isla Natividad (27.85◦N,
–115.17◦W) and at El Rosario (29.86◦N, –115.80◦W) at the
north end of Vizcaino Bay in 2013 (Figure 1). We quantified
the abundance of kelp forest species through annual surveys
at multiple sites to examine spatial and temporal patterns
in ecologically and commercially important species. Here,
we illustrate how local information on ocean environmental
variability reveals the presence of marine microclimates at
scales (a few kilometers) that can enable local conservation
and adaptation efforts in the face of global climate change
(Myers & Worm, 2003; Worm et al., 2009), thereby provid-
ing environmental data for informed local conservation and
management decisions (Prince, 2003).
2METHODS
2.1 Oceanographic data
Mooring sites were established on each side of Isla Natividad
and Isla San Jerónimo (El Rosario) in approximately 15 m
of water (Figure 1). Moorings recorded temperature, salinity,
dissolved oxygen, and currents every 10 min over a 4-year
period from 2013 to 2017. To assess patterns and responses of
the nearshore ecosystems around Isla Natividad to global and
regional scale climate variability, we compiled several large-
scale data sets including satellite-derived sea surface temper-
ature (SST), satellite-derived wind stress, and the Multivari-
ate El Niño Southern Oscillation (ENSO) Index for the years
2006–2016 (Wolter & Timlin, 1998). We used standard time
series techniques to examine differences between our three
sites. Details of the in situ oceanographic monitoring, satellite
and regional data used, and analyses are given in the Supple-
mentary Material.
2.2 Ecological data
Cooperative members, NGOs, and academic scientists per-
form ecological surveys at Isla Natividad following annual
training (Micheli et al., 2012; Fulton et al., in press). The
surveys are visual censuses of replicate 30 ×2 m transects
(60 m2) conducted on SCUBA between depths of 5 and
20 m in three control, fished sites, and two marine reserves
(Figure 1) yearly (2006–2016) between late July and early
August. A range of 11–30 transects are sampled per site every
year (avg. =20.8, total =1,162 transects). Commercially
and ecologically important fish species observed within a
2-m wide by 2-m high window along the 30-m benthic tran-
sect (120 m3) are counted and sized. Numbers of mobile
macroinvertebrates and kelp (numbers of plants and stipes,
within each plant, of the giant kelp, Macrocystis pyrifera
and the southern sea palm, Eisenia arborea) within the
WOODSON ET AL.3of9
FIGURE 1 Fishing concessions and mooring locations in the Baja Vizcaino region. (a) Location of two participating cooperatives and
concessions shown with mooring locations (red circles) and bathymetry (200 and 500 m depth contours). (b) El Rosario and (c) Buzos y Pescadores
(Isla Natividad) with cooperative rights (blue shading) and bathymetry (20, 40, and 100 m depth contours). (d) Inset of Isla Natividad showing
marine protected areas (green shading), mooring locations, survey locations (blue diamonds), and bathymetry (10, 20, and 40 m depth contours)
30 m ×2m belt transect are also enumerated and recorded.
For this analysis, we focus on surveys from two sites, La
Guanera (northeast, Tavg =18.57 ±2.64◦C) and Baben-
cho (southwest, Tavg =15.83 ±1.28◦C). We chose these
sites for several reasons: (a) Babencho is the closest to the
Morro Prieto mooring, (b) the distance between the sites
(2.6 km) is similar to the distance between mooring locations
(2.4 km), and (c) temperature and oxygen variability during
July (the period of reef surveys) at each reef site was com-
parable to the moorings on the respective side of the island
(Punta Prieta, Tavg =19.30 ±2.41◦C; Morro Prieto, Tavg =
16.08 ±0.99◦C).
We obtained mean biomass for algal species from the lit-
erature or web searches (Supporting Information Table 1).
We computed the number and biomass of each fish species
by calculating an average biomass from size (length) estima-
tions from visual census and applying a length–width rela-
tionship obtained from FishBase (Supporting Information
Table 2) (Froese & Pauly, 2017). For invertebrates, we used
an average size derived from the literature (Supporting Infor-
mationTable2).
3RESULTS
High variability in ocean conditions occurs both across and
within fishing concessions (Figure 2). Temperature varia-
tion at sites on the north and south ends of Vizcaino Bay
(Chinatown–Isla San Jeronimo, Morro Prieto–Isla Nativi-
dad) separated by 220 km are more correlated (R2=0.74,
P<0.001; Figure 2) than sites 2.4 km apart (Morro Pri-
eto and Punta Prieta–Isla Natividad; R2=0.49, P<0.001)
after removal of the seasonal signal. Similar to Morro Pri-
eto, Chinatown, although buffered by the much smaller Isla
San Jeronimo (∼1 km across), within the fishing conces-
sion of Ensenada cooperative (El Rosario), is located within
an upwelling center and oceanographic variability is largely
related to regional wind-driven upwelling. Variations in salin-
ity and dissolved oxygen follow similar patterns to tempera-
ture at regional scales.
Mean temperatures across Isla Natividad differ primarily
during the upwelling season in this region (March–July) when
Morro Prieto experiences the colder waters associated with
active upwelling (Figure 2). Consequently, the mean annual
4of9 WOODSON ET AL.
FIGURE 2 Time series of (a) ENSO index, (b) annual upwelling (wind stress) anomaly (grey bars) and upwelling index (blue), (c)
temperature, and (d) dissolved oxygen at ∼15 m depth from El Rosario, and Isla Natividad (Morro Prieto, Punta Prieta)
temperature change at Morro Prieto is around 12.2◦C (12.4–
24.6◦C). In contrast, Punta Prieta, on the other side of the
island (Figure 2), is not strongly affected by wind-driven
upwelling due to the orientation of the coastline relative to
the prevailing wind direction, and sees significantly warmer
waters from Vizcaino Bay. Overall, Punta Prieta exhibits
about 75% of the total annual temperature variability of Morro
Prieto (mean =9.4◦C, range =14.7–24.1◦C). However, daily
average differences across the island can be as much as 6◦C,
with discrete differences as high as 8◦C.
Although Punta Prieta is generally warmer, it does not
warm or cool as much as Morro Prieto, which sees both
lower and higher extremes associated with large-scale forc-
ing reflected in the higher variability at seasonal frequencies
(Figure 3). At synoptic periods (scales of mesoscale variabil-
ity and atmospheric weather patterns), both sites see similar
magnitude in responses based on integrated variance over the
synoptic band (Figure 3; Supporting Information Table 3).
However, over diurnal and tidal band frequencies, the temper-
ature at Punta Prieta is significantly more variable than Morro
Prieto. Focusing on differences in environmental variability
within the Isla Natividad concession, annual mean tempera-
ture differences across the island are not always significant
(Figure 4). For example, in 2013 and 2014, Punta Prieta was
on average 1.5◦C warmer than Morro Prieto for the entire year.
However, in 2015, during a strong ENSO event, the Punta Pri-
eta side of the island was not significantly warmer, and still
maintained high levels of diurnal and tidal variability, which
could manifest as a refuge from extreme conditions (Boch
et al., 2018).
Dissolved oxygen concentrations followed similar patterns
with higher values at Punta Prieta on average during 2013 and
2014, but no significant differences during 2015. Morro Pri-
eto experienced several low oxygen events that lasted for 1–3
days and coincided with bursts of intense upwelling. How-
ever, these events were not observed at Punta Prieta. Punta
Prieta also experiences significant variability at semidiurnal
and diurnal time scales with temperature and dissolved oxy-
gen fluctuations as much as 4◦Cand2mgL
−1, respectively. In
contrast, Morro Prieto has a relatively less variable environ-
ment over time periods of a few days based on integrated vari-
ance over diurnal and semidiurnal bands (Supporting Infor-
mation Table 3).
High local variability in the marine environment exists
across an island that is only 7 km long and averages 1 km
width. The 4-year period of this study also captured an aver-
age, cool year (2014), and two anomalously warm years
(2015–2016). It also captured a significant transition in global
climate anomalies with a transition from cool ENSO con-
ditions to the strongest El Niño (beginning in 2015) event
WOODSON ET AL.5of9
FIGURE 3 Variance spectra of (a) temperature and (b) dissolved
oxygen across Isla Natividad. Variance-preserving and scaled spectra to
show amount of variance (square-root for nonsquared units) in each
period band (seasonal, synoptic weather, diurnal, and semidiurnal/tidal)
since 1997–1998, along with the North Pacific warm blob
(Cavole et al., 2016). During this period, the southeast side
of the island experienced more extreme annual temperatures
with very little short time scale variation (Figures 2 and 3).
That is, this coastal habitat has a relatively constant climate
with long spells of extremely warm or cool waters (similar to
a typical temperate weather pattern with prolonged cold win-
ters and hot summers). In contrast, habitats on the northeast
side of the island experience less extreme annual temperature
variation and high short time scale variability (Figures 2 and
3). On this side of the island, the mean daily temperatures are
more constant throughout the year, but with high diurnal and
tidal variability. This variability may be attributed to inter-
nal waves—waves that travel along density interfaces in flu-
ids that can have immense impacts on nearshore ecosystems
(Woodson, 2018). Internal waves act to bring deep, cooler
waters up into coastal areas such as kelp forest reefs (McPhee-
Shaw et al., 2007). The tidal temperature and oxygen variabil-
ity mediates the extreme temperatures so that organisms are
not exposed to prolonged warm or cool periods, but instead are
exposed to short (up to 6 hr) exposure to moderately warmer
or cooler waters (more akin to a Mediterranean climate where
temperatures are mostly rather pleasant, but highly variable
from day to night).
Observed marine microclimates are coincident with pro-
nounced differences in the reef communities across the island
(Figure 5). Overall, algae, mobile invertebrates, and fishes
are significantly more abundant on the northeast side of the
island compared to the southwest (Figure 5). This pattern
holds in spite of the expected higher nutrient flux associated
with the strong upwelling that occurs on the southwest side
of the island. In addition, patterns of abundance are strikingly
different across the island for most species (Figure 5). Algal
biomass was significantly greater on the northeast side of the
island in 7 out of 11 years (2-sample t-test; n=41 for all years;
P<0.05 in 7/11 years) with the pattern driven primarily by
M. pyrifera (Figure 5). Invertebrate and fish biomass were sig-
nificantly different in only 2 out of 11 years (2-sample t-test;
n=48 for all years; P<0.05 in 2/10 years). However, abalone
and lobster biomass were significantly different in 6 of 10 and
4 out of 10 years, respectively. Similarly, biomass of kelp bass
and sheephead were significantly different in 5 of 11 and 4 of
11 years, respectively. Such differences illustrate the potential
influence of marine microclimates on species abundances at
relatively small spatial scales.
In response to large-scale climate drivers such as ENSO,
temperatures at both sites are positively correlated with the
multivariate ENSO index at a 3-month lag (R2=0.53,
P=0.01 and R2=0.51, P=0.006 for the northeast and south-
west sides, respectively) with overall mean monthly SSTs
statistically similar during strong positive ENSO anomalies.
However, the northeast side of Natividad island maintains
high diurnal and tidal variability, indicating that temperatures
fluctuate between extreme highs and lows every 12–24 hr.
These fluctuations are reflected in the overall depth-averaged,
daily water temperatures that are lower on the northeast side of
the island than on the typically cooler southwest (upwelling)
side of the island. Thus, in response to large-scale forcing
from positive anomalies of ENSO events, sessile invertebrates
on the southwest side of the island may be relatively more sen-
sitive to environmental stressors than those on the northeast
side of the island (Boch et al., 2018). The northeast side of the
island, therefore, may provide a spatial refuge from extreme
warming and low oxygen events even at the scale of this small
island. We observed similar marine microclimates around the
even smaller Isla San Geronimo in the El Rosario cooperative
(Figures 1 and 6), suggesting that marine microclimates may
be a common feature of the coastal ocean.
6of9 WOODSON ET AL.
FIGURE 4 Differences in (a) temperature and (b) dissolved oxygen across Isla Natividad. Positive values (red shading) indicate higher values
on northeast side of island. Black squares indicate mean daily difference with standard deviations
4DISCUSSION
Coastal species often exhibit variation in performance asso-
ciated with large-scale climate variability (Boyce et al., 2010;
Cheung et al., 2009; DeCarlo et al., 2017; Lotze & Worm,
2009; Pauly & Christensen, 1995); however, marine micro-
climates that allow these species to adapt to future condi-
tions (Boch et al., 2018; Safaie et al., 2018) may also exist.
Our results suggest environmental variation at the scale of
kilometers could provide refuges from climate stressors, and
other recent studies have demonstrated similar variation and
reduced coral bleaching at scales as little as 10s of meters
(Safaie et al., 2018). Small-scale variation in environmental
conditions has the potential to provide spatial and temporal
refuges for marine animals, and opportunities for conserva-
tion and adaptation to long-term climate trends.
Many marine species are resilient to short-term heating and
hypoxia exposure, but not to longer period extremes (Kim,
Barry, & Micheli, 2013; Somero et al., 2016). Mobile species,
such as many finfish and lobsters, could thus take advantage
of these microclimates to reduce exposure to harsh condi-
tions. For sessile or sedentary species, such as abalone and
sea urchins, microclimates may determine fine-scale distribu-
tion patterns. Conservation and management plans can har-
ness marine microclimates, particularly for sedentary species.
For example, the northeast coast of Isla Natividad may pro-
vide a refuge from extreme heat waves. By not fishing this
region during strong El Nino conditions, populations may be
more resilient and recover more quickly following large-scale
disturbances.
We can use observed responses of the nearshore environ-
ment to large-scale climate variability such as ENSO to make
predictions about the spatial variability of climate change
within fishing cooperative spatial concessions. For example,
with projections for a +2◦C increase in global atmospheric
temperatures by 2100, we can expect all waters around Isla
Natividad to warm. However, the northeast side of the island
may still experience high short-term variability, based on
our observations. As climate variability increases (e.g., more
intense and frequent ENSO events), we may expect the south-
west side of the island to experience longer, more intense peri-
ods of anomalously cold or warm waters, while the northeast
side will likely only see a gradual warming associated with
general climate trends.
Interestingly, the small-scale variability around the island
also points to differential responses of the ecosystems to
WOODSON ET AL.7of9
FIGURE 5 Time series of (a) all algae, (b) giant kelp (Macrocystis pyrifera), (c) Eisenia arborea, (d) all invertebrates, (e) abalones (Haliotis
spp.), (f) red spiny lobster (Panulirus interruptus), (g) all fishes, (h) kelp and barred sand bass (Paralabrax spp.), and (I) California sheephead
(Semicossyphus pulcher) across Isla Natividad (blue—southwest, red—northeast). Grey squares indicate the annual cumulative wind stress as a
measure of upwelling (nutrient supply). Shading shows 95% confidence intervals and nonoverlap indicates significant differences in abundance
between sites for that year
climate change. Historically, the southwest (upwelling) side
of the island was more productive for abalone. However,
since the recent die-offs (Micheli et al., 2012), abalone are
now more abundant on the northeast side of the island
(Figure 5). We may expect to see small-scale spatial shifts in
ecosystem structure and function that are reflected in changes
in the distribution of catch for commercially important species
(Cavole et al., 2016; Kroeker, Micheli, Gambi, & Martz,
2011; Somero et al., 2016). These changes provide a glim-
mer of hope for conservation efforts where climate change
is often perceived as a problem that acts on scales larger
than those to which these communities can respond (Cinner
et al., 2012; Defeo et al., 2013). In the presence of marine
microclimates, a series of small permanent or rotating no-take
reserves may provide a greater benefit than a few larger per-
manent protected zones. Such reserves could also be species-
specific, allowing communities to harvest particular species
to provide economic stability while ensuring long-term
conservation.
Local variability can also be incorporated in climate adap-
tation and conservation efforts. Cost effective and scalable
coastal oceanographic observing systems providing informa-
tion on local physical variability to local communities are
key to enable them to harness variability for more effec-
tive local management. Moreover, areas that provide con-
sistent refuges from environmental extremes under different
8of9 WOODSON ET AL.
FIGURE 6 Comparison of sites across Isla San Jeronimo in the El Rosario concession. Sites are approximately 1 km apart on opposite sides
of island. (a) Temperature, (b) temperature difference (ΔT), (c) dissolved oxygen, and (d) dissolved oxygen difference (ΔDO)
large-scale oceanographic regimes (Boch et al., 2018; Safaie
et al., 2018) provide opportunities for restoration efforts and
marine protected areas, and for supporting alternatives to wild
capture fisheries for local communities (Cinner et al., 2018)—
for example, by providing suitable conditions for artificial
reefs, enhancement of exploited populations via juvenile out-
plants, and locally-owned mariculture operations. Identify-
ing such refuges has the potential to support local adaptation
to climate change and enhance marine conservation (Cinner
et al., 2018).
Marine microclimates can provide spatial refuges for many
species and are not currently considered in marine conserva-
tion efforts (marine protected area design). Marine protected
areas that incorporate local scale variability can provide
a mechanism for climate adaptation in spite of large-scale
forecasts (Bruno et al., 2018). Harnessing small-scale vari-
ability in environmental conditions could provide a means of
adapting to climate change similar to how microclimates have
been suggested as adaptations in land-based agriculture (Lin,
2007; Smith & Olesen, 2010). Conservation and adaptation to
climate change must be a collaborative effort among fishers,
NGOs, the government, and scientists. Multistakeholder
collaboration facilitates understanding of complex processes
operating at different scales and promotes transparency and
informed decision making, which will ultimately improve
fisheries management and conservation efforts globally.
ACKNOWLEDGMENTS
We would like to thank A. Greenley and the staff of Comu-
nidad y Biodiversidad and ReefCheck of California for their
help with logistics and in the field. This work was sup-
ported by grants from NSF (CNH-DEB-1212124, OCE-
1416837, and OCE-1737090), the Walton Family Foundation,
the Packard Foundation, and the Marisla and Sandler Family
Foundation. We are grateful to CONANP (National Commis-
sion of Natural Protected Areas) and members of the coopera-
tives Buzos y Pescadores and Ensenada, and the Isla Natividad
community for their participation and support.
REFERENCES
Boch, C. A., Micheli, F., AlNajjar, M., Monismith, S. G., Beers, J.
M., Bonilla, J. C., …Woodson, C. B. (2018). Local oceanographic
WOODSON ET AL.9of9
variability influences the performance of juvenile abalone under cli-
mate change. Scientific reports,8, 5501.
Boyce, D. G., Lewis, M. R., & Worm, B. (2010). Global phytoplankton
decline over the past century. Nature,466, 591–596.
Breitburg, D., Levin, L. A., Oschlies, A., Grégoire, M., Chavez, F. P.,
Conley,D.J.,…Isensee, K. (2018). Declining oxygen in the global
ocean and coastal waters. Science,359, eAam7240.
Bruno, J. F., Bates, A. E., Cacciapaglia, C., Pike, E. P., Amstrup, S. C.,
van Hooidonk, R., …Aronson, R. B. (2018). Climate change threat-
ens the world's marine protected areas. Nature Climate Change,1,
499–503.
Cavole, L. M., Demko, A. M., Diner, R. E., Giddings, A., Koester, I.,
Pagniello, C. M., …Franks, P. J. S. (2016). Biological impacts of the
2013–2015 warm-water anomaly in the Northeast Pacific: Winners,
losers, and the future. Oceanography,29, 273–285.
Cheung, W. W. L., Lam, V. W. Y., Sarmiento, J. L., Kearney, K., Wat-
son, R., & Pauly, D. (2009). Projecting global marine biodiversity
impacts under climate change scenarios. Fish and Fis herie s,10, 235–
251.
Cinner, J. E., Adger, W. N., Allison, E. H., Barnes, M. L., Brown, K.,
Cohen, P. J., …Morrison, T. H. (2018). Building adaptive capacity
to climate change in tropical coastal communities. Nature Climate
Change,8, 117.
Cinner, J. E., McClanahan, T. R., Graham, N. A. J., Daw, T. M., Maina,
J.,Stead,S.M.,…Bodin, Ö. (2012). Vulnerability of coastal commu-
nities to key impacts of climate change on coral reef fisheries. Global
Environmental Change,22, 12–20.
DeCarlo, T. M., Cohen, A. L., Wong, G. T., Davis, K. A., Lohmann, P.,
& Soong, K. (2017). Mass coral mortality under local amplification
of 2 C ocean warming. Scientific reports,7, 44586.
Defeo, O., Castrejón, M., Ortega, L., Kuhn, A., Gutiérrez, N., & Castilla,
J. C. (2013). Impacts of climate variability on Latin American small-
scale fisheries. Ecology and Society,18, 30.
Froese, R., & Pauly, D. (2017). FishBase 2017, version (march,
2017). World Wide Web electronic publication Home page at:
http://www.fishbase.org.
Hughes, T. P., Anderson, K. D., Connolly, S. R., Heron, S. F., Kerry,
J. T., Lough, J. M., …Bridge, T. C. (2018). Spatial and temporal
patterns of mass bleaching of corals in the Anthropocene. Science,
359, 80–83.
Kim, T. W., Barry, J. P., & Micheli, F. (2013). The effects of intermit-
tent exposure to low-pH and low-oxygen conditions on survival and
growth of juvenile red abalone. Biogeosciences,10, 7255.
Kroeker, K. J., Micheli, F., Gambi, M. C., & Martz, T. R. (2011). Diver-
gent ecosystem responses within a benthic marine community to
ocean acidification. Proceedings of the National Academy of Sci-
ences,108, 14515–14520.
Kwiatkowski, L., & Orr, J. C. (2018). Diverging seasonal extremes for
ocean acidification during the twenty-first century. Nature Climate
Change,8, 141.
Lin, B. B. (2007). Agroforestry management as an adaptive strategy
against potential microclimate extremes in coffee agriculture. Agri-
cultural and Forest Meteorology,144, 85–94.
Lotze, H. K., & Worm, B. (2009). Historical baselines for large marine
animals. Trends in ecology & evolution,24, 254–262.
McPhee-Shaw, E. E., Siegel, D. A., Washburn, L., Brzezinski, M. A.,
Jones, J. L., Leydecker, A., & Melack, J. (2007). Mechanisms for
nutrient delivery to the inner shelf: Observations from the Santa Bar-
bara Channel. Limnology and Oceanography,52, 1748–1766.
Micheli, F., Saenz-Arroyo, A., Greenley, A., Vazquez, L., Montes,
J. A. E., Rossetto, M., & De Leo, G. A. (2012). Evidence that
marine reserves enhance resilience to climatic impacts. PloS One,7,
e40832.
Myers, R. A., & Worm, B. (2003). Rapid worldwide depletion of preda-
tory fish communities. Nature,423, 280–283.
O'Leary, J. K., Micheli, F., Airoldi, L., Boch, C., De Leo, G., Elahi, R.,
…Wong, J. (2017). The resilience of marine ecosystems to climatic
disturbances. BioScience,67, 208–220.
Pauly, D., & Christensen, V. (1995). Primary production required to sus-
tain global fisheries. Nature,374, 255–257.
Prince, J. D. (2003). The barefoot ecologist goes fishing. Fish an d Fish-
eries,4, 359–371.
Safaie, A., Silbiger, N. J., McClanahan, T. R., Pawlak, G., Barshis, D.
J., Hench, J. L., …Davis, K. A. (2018). High frequency temperature
variability reduces the risk of coral bleaching. Nature Communica-
tions,9, 1671.
Smith, P., & Olesen, J. E. (2010). Synergies between the mitigation of,
and adaptation to, climate change in agriculture. The Journal of Agri-
cultural Science,148, 543–552.
Somero, G. N., Beers, J. M., Chan, F., Hill, T. M., Klinger, T., & Litvin,
S. Y. (2016). What changes in the carbonate system, oxygen, and tem-
perature portend for the northeastern Pacific ocean: A physiological
perspective. BioScience,66, 14–26.
Sydeman, W. J., Santora, J. A., Thompson, S. A., Marinovic, B., &
Lorenzo, E. D. (2013). Increasing variance in North Pacific climate
relates to unprecedented ecosystem variability off California. Global
Change Biology,19, 1662–1675.
Wang, D., Gouhier, T. C., Menge, B. A., & Ganguly, A. R. (2015). Inten-
sification and spatial homogenization of coastal upwelling under cli-
mate change. Nature,518, 390–394.
Wolter, K., & Timlin, M. S. (1998). Measuring the strength of ENSO
events: How does 1997/98 rank? Weather,53, 315–324.
Woodson, C. B. (2018). The fate and impact of internal waves in
nearshore ecosystems. Annual Review of Marine Science,10, 421–
441.
Worm, B., Hilborn, R., Baum, J. K., Branch, T. A., Collie, J. S., Costello,
C., …Zeller, D. (2009). Rebuilding global fisheries. Science,325,
578–585.
SUPPORTING INFORMATION
Additional supporting information may be found online in the
Supporting Information section at the end of the article.
How to cite this article: Woodson CB, Micheli
F, Boch C, et al. Harnessing marine microclimates
for climate change adaptation and marine con-
servation. Conservation Letters. 2019;12:e12609.
https://doi.org/10.1111/conl.12609