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Increases in temperature associated with global climate change are predicted to elicit drastic changes, especially to marine and freshwater ecosystems. Even small changes in water temperature (1-2. °C) may alter rates of biological activity, with concomitant effects to communities and ecosystems. The biological erosion of marine habitats and structures is a rarely considered yet important activity that is likely to be influenced by changing ocean temperatures. We conducted an experiment to test how seawater temperature affects erosion by a non-native crustacean (Sphaeroma quoianum). Aquaria were maintained at one of thirteen temperatures (7.5. °C-25.2. °C). In each aquarium, twenty isopods were encaged with an expanded polystyrene foam block (800. ml) and left to burrow. Polystyrene floats under docks are often damaged by isopods in the field. After two months, isopods created the longest burrows in the moderate seawater temperatures (13.8. °C-18.3. °C); these temperatures were 1.1-5.6. °C higher than the mean ambient temperatures whence they came. Shorter burrows were observed for the coldest (7.5. °C) and warmest seawater treatments (25.2. °C). These results indicate that increasing seawater temperatures can exacerbate the bioerosive effects of non-native S. quoianum until a threshold, after which the impacts diminish. Because ocean temperatures are predicted to increase 1.5-2.6. °C in the next 90. years, our data suggest erosion by this non-native crustacean will increase 14.7-37.6% in Coos Bay/South Slough, Oregon (where isopods were collected). However, other invaded bays on the Pacific coast of North America may also experience mean increases of biological erosion of 6.6-29.8%. Since biological activity is tightly coupled with temperature in many species, we hypothesize that the biological erosion rates of other erosive species will also increase with rising water temperatures affecting marine habitats, communities, and structures.
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Small increases in temperature exacerbate the erosive effects
of a non-native burrowing crustacean
Timothy M. Davidson
a,
, Catherine E. de Rivera
a,1
, James T. Carlton
b
a
Department of Environmental Science and Management, Portland State University (ESM), PO Box 751, Portland, OR 97207, United States
b
The Maritime Studies Program, Williams College-Mystic Seaport, PO Box 6000, 75 Greenmanville Avenue, Mystic, CT 06355, United States
abstractarticle info
Article history:
Received 2 January 2013
Received in revised form 7 May 2013
Accepted 13 May 2013
Available online 4 June 2013
Keywords:
Bioerosion
Burrowing isopod
Climate change
Ecosystem engineering
Invasive species
Temperature effects
Increases in temperature associated with global climate change are predicted to elicit drastic changes, espe-
cially to marine and freshwater ecosystems. Even small changes in water temperature (12 °C) may alter
rates of biological activity, with concomitant effects to communities and ecosystems. The biological erosion
of marine habitats and structures is a rarely considered yet important activity that is likely to be inuenced
by changing ocean temperatures. We conducted an experiment to test how seawater temperature affects
erosion by a non-native crustacean (Sphaeroma quoianum). Aquaria were maintained at one of thirteen
temperatures (7.5 °C25.2 °C). In each aquarium, twenty isopods were encaged with an expanded polystyrene
foam block (800 ml) and left to burrow. Polystyrene oats underdocks are often damaged by isopodsin the eld.
After two months, isopods created the longest burrows in the moderate seawater temperatures (13.8 °C
18.3 °C); these temperatures were 1.15.6 °C higher than the mean ambient temperatures whence they came.
Shorter burrows were observed for the coldest (7.5 °C) and warmest seawater treatments (25.2 °C). These
results indicate that increasing seawater temperatures can exacerbate the bioerosive effects of non-native
S. quoianum until a threshold, after which the impacts diminish. Because ocean temperatures are predicted to
increase 1.52.6 °C in the next 90 years, our data suggest erosion by this non-native crustacean will increase
14.737.6% in Coos Bay/South Slough, Oregon (where isopods were collected). However, other invaded bays
on the Pacic coast of North America may also experience mean increases of biological erosion of 6.629.8%.
Since biological activity is tightly coupled with temperature in many species, we hypothesize that the biological
erosion rates of other erosive species will also increase with rising water temperatures affecting marine habitats,
communities, and structures.
© 2013 Elsevier B.V. All rights reserved.
1. Introduction
Increasing temperatures associated with global climate change
have the potential to greatly alter marine, freshwater, and terrestrial
ecosystems (Burgmer et al., 2007; Nicholls et al., 2007; Walther et al.,
2002; Woodward et al., 2010). The effects are diverse, including altering
species distributions and local biodiversity (Burgmer et al., 2007; Sorte
et al., 2010a;Walther et al., 2002), facilitating the invasion of non-native
species (Sorte et al., 2010b; Stachowicz et al., 2002), changing phenol-
ogies (Edwards and Richardson, 2004; Winder and Schindler, 2004),
and threatening stenothermal taxa (Hoegh Goldberg et al., 2007).
Changing temperatures can also have more subtle effects by altering
the rate of biological activities, such as feeding, development, reproduc-
tion, and growth (Cossins and Bowler, 1987; Kishi et al., 2005; Sanford,
1999). Altering temperatures, hence the rate of many biological activi-
ties, may elicit substantial community and ecosystem changes (Kishi
et al., 2005; Kordas et al., 2011; Petchey et al., 1999; Walther, 2010).
Such effects are strong in marine ecosystems where temperature
changes of a few degrees (3 °C) can alter the effect of keystone predators
and trophic dynamics (Sanford, 1999).
The removal or breakdown of consolidated substrata through
burrowing, boring, or bioerosion (biological erosion) is a less often
considered, yet important biological activity that is likely to be
inuenced by changing water temperatures. Since biological erosion
can be substantial in some marine environments and exceed erosion
by physical or chemical processes (Neumann, 1966), increases in the
rates of biological erosion ma y fundamentally alter the physical structure
of ecosystems. When bioeroders and borers occur in high densities or
erode at high rates, they can alter the heterogeneity of ecosystems,
including saltmarshes (Davidson and de Rivera, 2010; Escapa et al.,
2007; Talley et al., 2001), freshwater marshes and river banks (Dutton
and Conroy, 1998), forests (Feller and McKee, 1999; Hogg et al., 2002),
Journal of Experimental Marine Biology and Ecology 446 (2013) 115121
Corresponding author at: Smithsonian Tropical Research Institute, Apartado Postal
0843-03092, Balboa, Ancon, República de Panamá. Tel.: + 507 212 8830; fax: + 507
212 8790.
E-mail addresses: DavidsonT@si.edu (T.M. Davidson), derivera@pdx.edu
(C.E. de Rivera), James.T.Carlton@williams.edu (J.T. Carlton).
1
Tel.: +507 503 725 9076; fax: + 507 503 725 3834.
0022-0981/$ see front matter © 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.jembe.2013.05.008
Contents lists available at SciVerse ScienceDirect
Journal of Experimental Marine Biology and Ecology
journal homepage: www.elsevier.com/locate/jembe
and coral reefs (Hutchings, 1986). For example, burrowing crabs
facilitate the development of tidal channels (Escapa et al., 2007)in
saltmarshes and increase erosion in stream banks (Dutton and
Conroy, 1998). Boring insects can alter the canopy and morphology of
terrestrial and mangrove forests (Feller and McKee, 1999; Hogg et al.,
2002). Bioerosion by herbivorous sh, urchins, and mollusks can also
create scrapes, pits, and depressions in coral reefs (Hutchings, 1986).
In addition, the erosive effects of some species appear to increase in
higher seawater temperatures such as limnoriid isopods (Borges et al.,
2009; Eltringham, 1965), shipworms (Needler and Needler, 1940), and
parrotsh (Smith, 2008). However, ne-scale empirical evidence of the
effects of temperature on the rates of these important erosive activities
is limited.
Burrowing sphaeromatid isopods are estuarine bioeroders distrib-
uted throughout tropical and temperate regions. These crustaceans
use their mandibles to remove small bits of substrata, which are
not intentionally consumed (Rotramel, 1975). Sphaeroma quoianum
(H. Milne-Edwards, 1840), a burrowing isopod native to Australia
and New Zealand, has invaded at least 15 estuaries on the Pacic
coast of NorthAmerica (Davidson, 2008). Dense colonies of this burrower
inhabit and damage marsh banks, wood, friable rock, and expanded
polystyrene foam oats (hereafter: polystyrene) used in oating
docks (Davidson, 2008). Burrowing in polystyrene and the subsequent
breakage of these oats also have an economic effect. Moreover, by
degrading oats into a ne plastic dust, these burrowers exacerbate plas-
tic pollution in oceans (J. Carlton, A. Chang, and E. Wells unpublished, as
cited in Carlton and Ruiz, 2005; Davidson, 2012). Because empirical
evidence of the effect of temperature on erosive activities is limited,
our objective was to quantify how biological erosion may be affected
by changing ocean temperatures. We used S. quoianum as a model
bioeroder to infer how changingocean temperature may affect biological
erosion in marine environments.
We hypothesized that the relationship between temperature and
biological erosion would be parabolic in shape, following general
Q10 predictions. Hence, we expected that the peak of the parabola
would represent the maximum boring rates (longest, most voluminous
burrows). Since the rate atwhich S. quoianum creates plastic particles is
dependent on the erosion process, we also hypothesized that the num-
ber of plastic particles created by S. quoianum will be similarly related
to water temperature. Finally, using the temperature-specicratesof
biological erosion and extensive records of seawater temperature, we
examined how biological erosion rates may increase with future
increases in ocean temperature.
2. Materials and methods
2.1. Lab experiment
We examined the effect of water temperature on biological erosion
rates and plastic pollution by exposing isopods to thirteen water
temperatures in the laboratory. Each closed, aerated saltwater aquarium
(37.85 l) was maintained at one of thirteen temperatures, ranging from
7.5 °C to 25.2 °C, using aquarium chillers and heaters. These tempera-
tures were selected to exceed the mean water t emperatures experienced
by non-native populations near or at their known southernmost distri-
bution (San Diego Bay, CA: 20.6 °C, National Oceanic and Atmospheric
Administration, 2011; San Quintin Bay, Baja California: 17.3 °C, Alvarez
Borrego and Alvarez Borrego, 1982) and northernmost distribution
(Yaquina Bay, Oregon: 11.4 °C, Davidson, 2008; NOAA, 2011).
The water temperatures in the aquaria were changed to the experi-
mental levels slowly over four hours to help the isopods acclimate.
Temperatures were maintained within 0.8 °C of the selected treatment
temperatures. Air pumps were added to provide an adequate supply of
dissolvedoxygen in each tank and salinity was maintained at 30. Water
conditioner (Kordon AmQuel+ instant water detoxier) was added
prior to the experiment and after one month in response to regular
monitoring for nitrates, nitrites, ammonium, and ammonia. The water
conditioner was added to eliminate potentially toxic nitrogen com-
pounds, chlorines, and other chemicals that might otherwise have af-
fected the health of the experimental organisms.
In each aquarium, twenty isopods were caged with a polystyrene
block (800 cm
3
) with one exposed side (100 cm
2
). Polystyrene oats
are often burrowed and damaged by isopods in the eld (Davidson,
2012). While the substratum is articial, the burrowing process in
polystyrene is identical to the burrowing process in natural substrata
(such as marsh banks, decayed wood, and friable rocks; Davidson, per
obs). Thus the results of this experiment are also applicable to natural
substrata. The isopods used in the experiment were collected from
Coos Bay, Oregon in late January 2010. We used non-ovigerous
adult isopods between 7 and 12 mm in length. We divided isopods
into four relative size categories to ensure that all treatments received
isopods of similar size. We created fteen small holes (4 mm deep ×
6.35 mm wide) on the surface of the polystyrene block to prompt
isopod burrowing and left the isopods to burrow for 62 days. Previous
experiments revealed that these small holes greatly decreased the
time it took for isopods to initiate burrowing. We did not include
the holes we made in our measurements if isopods did not burrow
into them. Animals were fed Spray-Dried Marine Phytoplankton (ESV
Aquarium Products, Inc.; Hicksville, NY) every two days. Experimental
blocks were examined three times during the experiment (after
1 month, 1.5 months, and 2 months) to remove any dead isopods
(without replacement) or molts and to note the location of the isopods
(inside or outside of burrows).
At the end of the experiment, we removed all isopods, measured
the total length of burrows created by isopods and calculated the
total volume excavated per block. Burrow length and width measure-
ments were used to estimate the volume of a burrow. To correct for
the vermiform shape of a burrow, we calculated the volume of a
cylinder plus the volume of one-half a sphere (to represent the
tapered end of a vermiform burrow; Davidson and de Rivera, 2012).
We also recorded survivorship, growth (number of molts), and repro-
duction (number of juvenile isopods) at the end of the experiment.
The mean percentages of isopods that were inside of their burrows
(burrow use) were calculated based on the locations of isopods
during the three observations (described above). Juveniles were not
included in our measurements of survivorship. Because we could not
determine when each of the isopods died, the per capita estimates of
biological erosion were based on the average of the original number
of isopods (20) and number of surviving isopods at the end of the
experiment.
Plastic particles were collected by discharging aquarium water
through a 63 μm sieve. We could not detect, using dissecting and light
microscopes, smaller plastic particles in the water discharged through
the sieve. We collected all plastic particles from each aquarium, soaked
them in 2% hydrogen peroxide to remove organic material (isopod
feces), and then poured the solution onto a gridded paper lter
(1 cm
2
grid). Hydrogen peroxide did not appear to affect the plastic
particles in preliminary tests. We agitated the plastic particle solution
to help distribute the particles evenly across the gridded lter and
then counted the number of squares with plasticparticles. We estimated
the number of particles per paper lter by photographing, with a digital
microscope camera, ve random subsamples (1 cm
2
squares) per lter,
then counting thenumber of particles in eachsquare using ImageJ 1.43u
image analysis software. The total number of particles per lter was es-
timated by multiplying the mean number of particles per 1 cm
2
by the
total number of 1 cm
2
squares on the lter that were occupied by plastic
particles. Expanded polystyrene foam is resistant to temperature
changes; the maximum permissible operating temperature of foam is
75 °C and it degrades at temperatures exceeding 90 °C (Goodier,
1961); therefore, our experimental temperatures did not substantially
alter the morphology or properties of the experimental substrata or
particles.
116 T.M. Davidson et al. / Journal of Experimental Marine Biology and Ecology 446 (2013) 115121
2.2. Statistical analysis
We used quadratic regressions in R (version 2.7.2) to examine the
relationships between water temperature and each dependent variable
(burrow length, burrow volume, and the number of plastic particles
created per isopod). The relationships between temperature and
burrow use (percentage of isopods inside burrows), molting frequency
(number of molts found), survivorship, and reproduction (number of
juveniles) at the end of the experiment were also examined. We select-
ed the quadratic model based on the best t of different models (linear,
asymptotic, and quadratic) through visual evaluation of scatter plots
and by the comparison of Akaike information criterion values. Data
were either log-transformed (burrow length and plastic particle data)
or square-root transformed (burrow volume, burrow use, and molt
data) to meet the assumptions of normality, equalvariances of residuals,
and to reduce the inuence of outliers.
2.3. Predictions
To explore the extent of changes to biological erosion rates due to
predicted ocean temperature increases in Coos Bay/South Slough and
other estuaries on the Pacic coast, we calculated the mean ocean
temperatures (20002010) obtained from the stations of the National
Estuarine Research Reserve (NERR) System-Wide Monitoring Program
(SWMP; NOAA, 2011; ESM 1) and predicted increases in ocean temper-
ature by the end of the 21st century from Meehl et al. (2007).Wecalcu-
lated the estimated biological erosion rates in each of the SWMP stations
using the mean ocean temperatures at each respective station under dif-
ferent climate change scenarios (B1 Scenario, +1.5 °C; and A2 Scenario,
+2.6 °C; Meehl et al., 2007) using the relationship between burrow
volume and temperature obtained from the lab experiment.
3. Results
3.1. Lab experiment
The isopods created the longest and most voluminous burrows
and the most plastic particles in the moderate seawater temperatures
after two months (13.8 °C18.3 °C, Fig. 1). Shorter burrow lengths,
lower volumes, and fewer plastic particles were observed for the
coldest and warmest seawater treatments. The mean number of plastic
particles created in the two months by an adult isopod varied from a
minimum of 79 (7.5 °C) to a maximum of 4387 (13.8 °C).
Similar relationships between water temperature and burrow use
and molting frequency were also found (Fig. 2). Fewer isopods (37%)
were found inside of their burrows in the coldest water temperature
while most (89.5100%) of the isopods were present inside of burrows
in the moderate water temperatures (13.818.3 °C). Molting occurred
lessofteninthecolder(b15 °C) than the higher (>15 °C) tempera-
tures. We did not detect a signicant relationship between water
temperature and either survivorship or reproduction with quadratic
regressions (P>0.05, Fig. 3). However, temperature was associated
with whether or not reproduction occurred (logistic regression, z =
2.01, P=0.044).
3.2. Predictions
Based on the mean ocean temperature of Coos Bay/South Slough
(the source of the lab isopods), temperature increases of only 1.5
2.6 °C may increase the erosive effects of isopods by 14.7 to 22.7%
(under the IPCC B1 scenario, +1.5 °C, best case scenario, Table 1)and
23.4 to 37.6% (+2.6 °C, under the A2 scenario). Similarly, increases in
ocean temperature may also increase the erosive impact of non-native
S. quoianum in other estuaries including Elkhorn Slough and San
Francisco Bay (6.69.3% and 8.3312.3%, for the B1 and A2 scenarios,
respectively; Table 1), while in other estuaries (San Diego Bay) the
erosive impact may diminish. The biological erosion rates inother estu-
aries not yet invaded by S. quoianum are predicted to increase (Padilla
Bay, WA) or exhibit variable responses (Tijuana Estuary, CA) with
increasing ocean temperatures given further range expansion.
4. Discussion
4.1. Effects of temperature on biological erosion and the creation of plastic
particles
Seawater temperature had a strong effect on the rate of biological
erosion and other biological activities of the non-native isopod
Fig. 1. Effects of water temperature on the length and volume of burrows and number
of plastic particles created by individuals of Sphaeroma quoianum. The second axis on
the right presents untransformed data. Values presented are per isopod.
Fig. 2. Effects of temperature on burrow use andthe molting frequency (per isopod) of indi-
viduals of Sphaeroma quoianum. The second axis on the right presents untransformed data.
117T.M. Davidson et al. / Journal of Experimental Marine Biology and Ecology 446 (2013) 115121
S. quoianum. The isopods in tanks at the moderate seawater tempera-
tures exhibited higher rates of biological erosion, including longer and
more voluminous burrows. These temperatures were 1.15.6 °C higher
than the mean ambient temperatures of the estuary whence the iso-
pods came (12.7 °C, Coos Bay/South Slough Estuary). As hypothesized,
these relationships were inverse parabolic in shape; the erosive effects
of S. quoianum peaked at 18.3 °C and decreased when exposed to either
warmer or colder temperatures. These results were consistent with
both laboratory and eld experiments examining the effects of temper-
ature on bioerosion by numerous taxa. Numerous bioeroders and
borers exhibited changes in biological erosion when exposed to chang-
ing temperatures, including wood-boring gribbles (Borges et al., 2009;
Eltringham, 1965), boring mollusks (Needler and Needler, 1940;
Norman, 1977), bioeroding sponges (Siegrist et al., 1992), parrotsh
(Smith, 2008), and sipunculans and polychaetes (Siegrist et al., 1992;
Table 2).
Changes in biological erosion rates associated with changing ocean
temperature may have myriad ecological and economic implications
in the marine environment because high rates of bioerosion and boring
can fundamentally change the nature of a habitat and damage marine
structures (Table 2). For example, burrowingby crustaceans accelerated
lateral erosion in saltmarsh habitats (Davidson and de Rivera, 2010)and
stream banks (Dutton and Conroy, 1998) and converted marsh and
stream banks into undercut ledges and slumps. Coral reefs in many
areas of the Eastern Pacic and Caribbean were degraded by bioeroding
urchins (Hutchings, 1986); these effects are especially detrimental in
these coral reef habitats where thermal stressors may interact with
coral bioeroders to facilitate degradation of the reef structure (Rützler,
2002). Furthermore, marine and terrestrial wood-borers destroyed
human structures and damaged forests causing millions of dollars in
damage (Aukema et al., 2011; Miller, 1926). Conversely, reducing the
rates of bioerosion (e.g. reduction in the numbers of bioeroders) may
also have implications for habitats including coral and sand beaches
that require regular bioerosion for maintenance and for coral reefs
Fig. 3. Effects of temperature on survivorship and the reproduction (# of juveniles per
isopod) of individuals of Sphaeroma quoianum.
Table 1
Mean water temperatures (20002010) in the Pacic coast National Estuarine Research Reserve System-Wide Monitoring Program stations, predicted temperatures under B1
(best-case) and A2 scenarios (Meehl et al., 2007), and the predicted change in biological erosion associated with those water temperatures based on temperature-specic boring
rates of S. quoianum.
NERR site Mean water
temperature (°C)
a
B1 scenario
(+1.5 °C)
b
Predicted change in
biological erosion (%)
c
A2 scenario
(+2.6 °C)
b
Predicted change in
biological erosion (%)
Padilla Bay, WA
d
11.52 13.02 24.01 14.12 39.93
Gong Surface 10.73 12.23 28.67 13.33 48.30
Ploeg Channel 11.35 12.85 24.95 13.95 41.61
Joe Leary Estuary 12.82 14.32 17.93 15.42 29.11
Joe Leary Slough 12.08 13.58 21.20 14.68 34.91
Bayview Channel 10.60 12.10 29.53 13.20 49.86
Coos Bay/South Slough, OR 12.72 14.22 18.34 15.32 29.84
Charleston Bridge 11.77 13.27 22.71 14.37 37.61
Valino Island 12.43 13.93 19.59 15.03 32.05
Sengstacken Arm 13.68 15.18 14.66 16.28 23.35
Winchester Arm 13.00 14.50 17.20 15.60 27.83
San Francisco Bay, CA 16.41 17.91 6.60 19.01 9.30
First Mallard 16.73 18.23 5.81 19.33 7.92
Second Mallard 16.75 18.25 5.76 19.35 7.85
Gallinas Creek 16.51 18.01 6.35 19.11 8.86
China Camp 15.66 17.16 8.56 18.26 12.70
Elkhorn Slough, CA 15.75 17.25 8.33 18.35 12.29
Azevedo Pond 16.56 18.06 6.22 19.16 8.63
North Marsh 16.87 18.37 5.45 19.47 7.31
South Marsh 15.69 17.19 8.48 18.29 12.55
Vierra Mouth 13.85 15.35 14.07 16.45 22.32
San Diego Bay, CA 20.56 22.06 2.79 23.16 6.81
Pond Eleven 20.81 22.31 3.32 23.41 7.72
South Bay 20.31 21.81 2.24 22.91 5.89
Tijuana Estuary, CA
d
18.29 20.42 0.76 21.52 0.77
Tidal Linkage 21.79 23.29 5.46 24.39 11.34
Oneonta Slough 18.17 19.67 2.42 20.77 2.09
Boca Rio 17.13 18.63 4.83 19.73 6.23
River Channel 18.94 20.44 0.71 21.54 0.84
Model Marsh 18.56 20.06 1.56 21.16 0.61
a
Mean water temperatures are calculated from the mean temperature of all system-wide monitoring stations between 2000 and 2010. See ESM 1 for details.
b
The B1 scenario depicts climate change under a shift towards global sustainability, clean and resource efcient technology, and a service and information economy. The A2 scenario
depictsclimate change undera continuouslyincreasing population, regionalism, slow economicgrowth and slow technologicalchange (Meehl et a l., 2007). These predictions of uppersea
surface temperature increase by year 2100 are based on consensus expert opinion of the Intergovernmental Panel on Climate Change.
c
Predicted changes in biological erosion were calculated from the relationships between burrow volume and temperature as presented in Fig. 1.
d
Populations of S. quoianum have not yet beenfound in Padilla Bay,WA or Tijuana Estuary,CA (Davidson, unpublished surveys;J. Crooks, per comm.), but the proximity of these baysto
highly invaded bays suggests that invasions may occur in the future. All other estuaries listed here harbor populations of S. quoianum (Davidson, 2008).
118 T.M. Davidson et al. / Journal of Experimental Marine Biology and Ecology 446 (2013) 115121
where small scale bioerosion facilitates coral settlement (reviewed by
Hutchings, 1986).
In addition to affecting rates of bioerosion, changing water temper-
atures also affected the amount of plastic pollution that was created by
this non-native burrower. The boring process of S. quoianum produced
thousands of minute plastic particles during the two-month experi-
ment. These particles were irregular in shape with an equivalent circu-
lar diameter of around 250 μm(Davidson, 2012). We found that an
individual isopod could create as few as 79 particles at 7.5 °C (coldest
temperature treatment) to a maximum of 4387 at 13.8 °C. However,
these values are likely underestimating the potential effects since not
all isopods created a burrow. When plastic particles are calculated per
burrow, the values increase to 89 and 4630 particles per burrow
(Davidson, 2012). These results reveal that small incremental changes
in water temperature greatly increased the rate of plastic pollution
created between these temperatures. When extrapolating these values
to the mean density of isopods in oats, the plastic pollution created
from isopods exceeded several hundred million (Davidson, 2012).
Numerous taxa and trophic levels consume microplastic similar in size
to these particles (Graham and Thompson, 2009; Thompson et al.,
2004). Once ingested, microplastics may have a physical effect by inter-
fering with digestion or causing ulcers (as with birds, Pettit et al., 1981)
or potentially have a toxic effect since microplastics can absorb toxins
from adjacent waters (Mato et al., 2001; Teuten et al., 2007). Thus
there could be a variety of ecological implications for the release of
these minute plastic particles by the activities of S. quoianum and other
boring isopods (reviewed by Davidson, 2012).
Other biological activities such as burrow use and molting frequency
exhibited a similar relationship to temperature. Differences in burrow
use and molting frequency between temperature treatments are likely
responsible for the differences in the amount of biological erosion
and plastic pollution. Low burrow usage implies that isopods are not
burrowing often and perhaps experiencing stressful conditions. Isopods
may also be abandoning their burrows in an attempt to seek less stress-
ful conditions. Since not all isopods in an experimental temperature
treatment responded the same way, these data also reveal that theindi-
vidual response to changes in water temperature varies. Future studies
should investigate what factors may inuence the use and abandon-
ment of burrows and what drives this individual variation in response.
Molting frequency (e.g. growth rate) was also affected by temperature.
Higher temperatures caused more molting. Thus, as the isopods grow in
size, they would also have toconduct more burrow maintenance (their
burrow widths closely match their body widths) and hence would
burrow more. Increases in individual growth rates may also lead to
demographic changes if isopods exposed to higher temperatures
matured faster and experienced shorter generation times. Changes in
demography may lead to additional erosive effects as higher population
growth rates would lead to more biological erosion per unit time. Addi-
tional studies investigating how the demography of bioeroders is affected
by temperature would also help reveal how a changing climate may
affect the process of biological erosion.
4.2. Predicted changes in biological erosion rates under climate change
Our experiment predicted that small increases in seawater temper-
ature (+1.52.6 °C) could cause relatively large increases in biological
erosion rate (14.722.7%) in a non-native crustacean from Coos Bay/
South Slough estuary, Oregon. Assuming that our lab data can be accu-
rately applied to eld populations, we predict that ocean temperature
conditions will increase the erosive impact of non-native S. quoianum
in Coos Bay/South Slough. These results are also relevant to populations
of boring isopods in several other invaded areas on the Paciccoastof
North America that appear to be susceptible to increases in bioerosion
intensity with changing seawater temperatures.
By further extrapolating our results to other stations and estuaries
in the NERR system, we predicted that ocean temperature conditions
will increase the erosive impact of non-native S. quoianum in three of
the four estuaries in the NERR system that this isopod has already
invaded (Table 1). Populations of S. quoianum in Elkhorn Slough, San
Francisco Bay, and Coos Bay/South Slough (and other invaded estuaries
experiencing similar ocean conditions) will likely increase their erosive
impact withincreasing ocean temperatures, assuming that those popu-
lations would exhibit a similar response to temperature as Coos Bay
populations. Since burrowing isopods also bore into numerous natural
substrata in a similar fashion as polystyrene (Davidson, per. obs,
Davidson and de Rivera, 2012), the results of this experiment may
apply to numerous other habitats, structures, and substrata such as
saltmarsh banks, friable rock terraces and riprap, and wooden structures.
Burrowing by isopods facilitates erosion of saltmarsh banks (Davidson
and de Rivera, 2010; Talley et al., 2001) and damages marine structures
and facilities (Cragg et al., 1999; Davidson, 2012), thus increases in
bioerosion with increasing seawater temperatures may result in
increased erosion of saltmarshes and damage to marine habitats and
structures. Similarly, the plastic pollution associated with this biological
erosion would also increase.
Furthermore, as water temperatures warm and become more hospi-
table, subsequent invasion may occur of estuaries that do not yet harbor
populations of S. quoianum (e.g., Padilla Bay, WA). Such patterns have
been observed previously in fouling communities (Stachowicz et al.,
2002). Increasing winter ocean temperatures facilitated the invasion
of non-native tunicates on the east coast of the US (Stachowicz et al.,
2002).
In addition, warming is expected to be greater in high latitude areas
in the northern hemisphere and not asextreme in lower latitude waters
(Meehl et al., 2007). Hence, already warm bays may not experience
substantial decreases in biological erosion even as high latitude bays
experience large increases in biological erosion due to warming. This
spatial variability in warming (and other interacting factors) makes
predicting the specic responses of populations to increasing ocean
temperatures difcult. These challenges are further accentuated by
temporal and ne-scale spatial variability of temperature (such as the
yearly and seasonal variation we observed within estuaries, ESM 1)
as well as differing physiological responses of individuals within
Table 2
Selected studies examining the effects of experimental and observational increases in water temperature on bioerosion and boring.
Taxon Region Substratum Hypothesized effects of increased temperature Reference
Wood-boring shipworms Atlantic USA & Canada,
Sweden
Wood Increased damage to wooden structures Needler and Needler (1940);
Norman (1977)
Wood-boring isopods England Wood Increased damage to wooden structures Eltringham (1965);
Borges et al. (2009)
Boring isopods Pacic USA Polystyrene oats Increased damage to oating docks & facilities This study
Parrotsh Pacic Panama Coral Altered coral structure Smith (2008)
Sipunculans, polychaetes, clionid
sponges
Guam Coral Altered coral structure Siegrist et al. (1992)
Littorine snails New South Wales,
Australia
Sandstone Altered morphology of sandstone platforms & tidepools
a
Petraitis (1992)
a
Physical weathering of rock from the feeding actions of littorine snails increases bioerosion rates and deepens tidepools (North, 1954).
119T.M. Davidson et al. / Journal of Experimental Marine Biology and Ecology 446 (2013) 115121
populations. Thus, while our predictions using decadal means may be
informative, future studies should examine how biological erosion
may vary on ner temporal and spatial scales. Furthermore, extreme
values may be more important than means in determining the effects
of temperature on populations (Gaines and Denny, 1993; Stachowicz
et al., 2002). For instance, extreme temperatures may cause mortality
of a local population of isopods and thus reduce biological erosion
rates. Future studies should examine how biological erosion and other
biological activities are affected by increasing variation and extremes
of water temperatures.
This experiment and our corresponding approximate predictions
reveal the general response that small incremental differences in
water temperature have on the biological erosion rates of a non-native
boring crustacean. Thus, the relative change in biological erosion occur-
ring from changes in temperature, while here predicted for specic
places, is ecologically relevant to a broader geography and suite of
species. While the response of biota to temperature changes may be
stronger in some marine systems (where temperatures are relatively
more stable), these results are also relevant in freshwater systems and
perhaps terrestrial ecosystems (for example, with burrowing earth-
worms, Perreault and Whalen, 2006). In addition, such effects may
vary between eurytolerant taxa found often in temperate regions
and with stenothermal taxa (such as those found in polar and tropical
regions). In stenothermal taxa, we hypothesize that small changes in
temperature may initially affect erosion rates, but persistent or larger
changes in temperature may exceed the physiological tolerances of
the organisms resulting in reduced survivorship, hence a reduction in
bioerosion rate. Since many other bioeroders and borers exhibit similar
responses to increases in temperature (see previous examples), we pre-
dict that other bioeroders and borers will increase biological erosion
rates when subjected to warm temperatures associated with climate
change. Consequently, warming, via its inuence on rates of boring,
burrowing, and bioerosion, may lead to the alteration of the physical
structure of marine and aquatic habitats and exacerbate damage to
human-made structures.
Supplementary data to this article can be found online at http://
dx.doi.org/10.1016/j.jembe.2013.05.008.
Acknowledgments
We are grateful to Anne Phillip, Dereck Guba, and Justin Ashby for
their assistance during the experiment. Heejun Chang, Linda Mantel,
Yangdong Pan, Gregory Ruiz, StevenRumrill, and Mark Sytsma provided
helpful advice and comments. We thank Elise Granek for her advice and
for allowing the use of equipment. We also thank the anonymous
reviewersfortheircommentsonthismanuscript.Thisresearchwas
conducted in the National Estuarine Research Reserve System under an
award from the Estuarine Reserves Division, Ofce of Ocean and Coastal
Resource Management, National Ocean Service, National Oceanic and
Atmospheric Administration.[ST]
References
Alvarez Borrego, J., Alvarez Borrego, S., 1982. Temporal and spatial variability of
temperature in two coastal lagoons. CalCOFI Report, 23, pp. 188197.
Aukema, J.E., Leung, B., Kovacs, K., Chivers, C., Britton, K.O., Frankel, S.J., Haight, R.G.,
Holmes, T.P., Liebhold, A.M., McCullough, D.G., Von Holle, B., 2011. Economic
impacts of non native forest insects in the continental United States. PLoS One 6,
e24587.
Borges, L.M.S., Cragg, S.M., Busch, S., 2009. A laboratory assay for measuring feeding
and mortality of the marine wood borer Limnoria under forced feeding conditions:
a basis for a standard test method. Int. Biodeterior. Biodegrad. 63, 289296.
Burgmer, T., Hillebrand, H., Pfenninger, M., 2007. Effects of climate driven temperature
changes on the diversity of freshwater macroinvertebrates. Oecologia 151, 93100.
Carlton, J.T., Ruiz, G.M., 2005. The magnitude and consequences of bioinvasions in
marine ecosystems: implications for conservation biology. In: Norse, E.A., Crowder,
L.B. (Eds.), Marine Conservation Biology: The Science of Maintaining the Sea's
Biodiversity. Island Press, pp. 123148.
Cossins, A.R., Bowler, K., 1987. Temperature Biology of Animals. Chapman and Hill.
Cragg, S.M., Pitman, A.J., Henderson, S.M., 1999. Developments in the understanding of
the biology of marine wood boring crustaceans and in methods of controlling
them. Int. Biodeterior. Biodegrad. 43, 197205.
Davidson, T.M., 2008. Prevalence and distribution of the introduced burrowing isopod,
Sphaeroma quoianum in the intertidal zone of a temperate northeast Pacic estuary
(Isopoda, Flabellifera). Crustaceana 81, 155167.
Davidson, T.M., 2012. Boring crustaceans damage polystyrene oats under docks
polluting marine waters with microplastic. Mar. Pollut. Bull. 64, 18211827.
Davidson, T.M., de Rivera, C.E., 2010. Accelerated erosion of saltmarshes infested by the
non native burrowing crustacean Sphaeroma quoianum. Mar. Ecol. Prog. Ser. 419,
129136.
Davidson, T.M., de Rivera, C.E., 2012. Per capita effects and burrow morphology of
a burrowing isopod (Sphaeroma quoianum) in different estuarine substrata. J.
Crust. Biol. 32, 2530.
Dutton, C., Conroy, C., 1998. Effects of Burrowing Chinese Mitten Crabs (Eriocheir
sinensis) on the Thames Tideway. Environment Agency.
Edwards, M., Richardson, A.J., 2004. Impact of climate change on marine pelagic
phenology and trophic mismatch. Nature 430, 881884.
Eltringham, S.K., 1965. The effect of temperature upon the boring activity and survival
of Limnoria (Isopoda). J. Appl. Ecol. 2, 149157.
Escapa, M., Minkoff, D.R., Perillo, G.M.E., Iribarne, O., 2007. Direct and indirect effects of
burrowing crab Chasmagnathus granulatus activities on erosion of southwest
Atlantic Sarcocornia dominated marshes. Limnol. Oceanogr. 52, 23402349.
Feller, I.C., McKee, K.L., 1999. Small gap creation in Belizean mangrove forests by a
wood boring insect. Biotropica 31, 607617.
Gaines, S.D., Denny, M.W., 1993. The largest, smallest, highest, lowest, longest, and
shortest: extremes in ecology. Ecology 74, 16771692.
Goodier, K., 1961. Making and using an expanded plastic. New Sci. 240, 706707.
Graham, E.R., Thompson, J.T., 2009. Deposit and suspension feeding sea cucumbers
(Echinodermata) ingest plastic fragments. J. Exp. Mar. Biol. Ecol. 368, 2229.
Hoegh Goldberg, O., Mumby, P.J., Hooten, A.J., Steneck, R.S., Greeneld, P., Gomez, E.,
Harvell, C.D., Sale, P.F., Edwards, A.J., Caldeira, K., Knowlton, N., Eakin, C.M., Iglesias
Prieto, R., Muthiga, N., Bradbury, R.H., Dubi, A., Hatziolos, M.E., 2007. Coral reefs
under rapid climate change and ocean acidication. Science 318, 17371742.
Hogg, E.H., Brandt, J.P., Kochtubajda, B., 2002. Growth and dieback of aspen forests in
northwestern Alberta, Canada, in relation to climate and insects. Can. J. For. Res.
32, 823832.
Hutchings, P.A., 1986. Biological destruction of coral reefs. A review. Coral Reefs 4,
239252.
Kishi, D., Murakami, M., Nakano, S., Maekawa, K., 2005. Water temperature determines
strength of top down control in a stream food web. Freshwater Biol. 50, 13151322.
Kordas, R.L., Harley, C.D.G., O'Connor, M.I., 2011. Community ecology in a warming
world: the inuence of temperature on interspecic interactions. J. Exp. Mar.
Biol. Ecol. 400, 218226.
Mato, Y., Isobe, T., Takada, H., Kanehiro, H., Ohtake, C., Kaminuma, T., 2001. Plastic resin
pellets as a transport medium for toxic chemicals in the marine environment.
Environ. Sci. Technol. 35, 308324.
Meehl, G.A., Stocker, T.F., Collins, W.D., Friedlingstein, P., Gaye, A.T., Gregory, J.M., Kitoh,
A., Knutti, R., Murphy, J.M., Noda, A., Raper, S.C.B., Watterson, I.G., Weaver, A.J.,
Zhao, Z.C., 2007. Global climate projections. Climate change 2007: the physical
science basis. In: Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt,
K.B., Tignor, M., Miller, H.L. (Eds.), Contribution of Working Group I to the Fourth
Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge
University Press, pp. 747845.
Miller, R.C., 1926. Ecological relations of marine wood boring organisms in San Francisco
Bay. Ecology 7, 247254.
National Oceanic and Atmospheric Administration, 2011. National Estuarine Research
Reserve System Wide Monitoring Program. Centralized Data Management Ofce,
Baruch Marine Field Lab, University of South Carolina (http://cdmo.baruch.sc.
edu, accessed 13 Sept 2011).
Needler, A.W.H., Needler, A.B., 1940. Growth of shipworms (Teredo navalis) in Malpeque
Bay. J. Fish. Res. Board Can. 5, 810.
Neumann, C., 1966. Observations on coastal erosion in Bermuda and measurements of
the boring rate of the sponge, Cliona lampa. Limnol. Oceanogr. 11, 92108.
Nicholls, R.J., Wong, P.P., Burkett, V.R., Codignotto, J.O., Hay, J.E., McLean, R.F.,
Ragoonaden, S., Woodroffe, C.D., 2007. Coastal systems and low lying areas. Climate
change 2007: impacts, adaptation and vulnerability. In: Parry, M.L., Canziani, O.F.,
Palutikof, J.F., van der Linden, P.J., Hanson, C.E. (Eds.), Contribution of Working
Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate
Change. Cambridge University Press, pp. 315356.
NOAA, 2011. National Oceanographic Data Center. Coastal Temperature Guide. Long
Term Monthly Mean Water Temperatures for the North Pacic Coast. http://
www.nodc.noaa.gov/dsdt/cwtg/npac.html (accessed 13 Sept 2011).
Norman, E., 1977. The geographical distribution and the growth of the wood boring
mollusks Teredo navalis L., Psiloteredo megotara (Hanley) and Xylophaga dorsalis
(Turton) on the Swedish west coast. Ophelia 16, 233250.
North, W.J. , 1954. Size distribution, erosive activities,and gross metabolic efciency of the
marine intertidal snails, Littorina planaxis and L. scutulata. Biol. Bull. 106, 185197.
Perreault, J.M., Whalen, J.K., 2006. Earthworm burrowing in laboratory microcosms as
inuenced by soil temperature and moisture. Pedobiologia 50, 397403.
Petchey, O.L., Mcphearson, P.T., Casey, T.M., Morin, P.J., 1999. Environmental warming
alters food web structure and ecosystem function. Nature 402, 6972.
Petraitis, P.S., 1992. Effects of body size and water temperature on grazing rates of four
intertidal gastropods. Aust. J. Ecol. 17, 409414.
Pettit, T.N., Grant, G.S., Whittow, G.C., 1981. Ingestions of plastics by Laysan albatross.
Auk 98, 839840.
120 T.M. Davidson et al. / Journal of Experimental Marine Biology and Ecology 446 (2013) 115121
Rotramel, G., 1975. Filter feeding by the marine boring isopod Sphaeroma quoyanum H.
Milne Edwards, 1840 (Isopoda: Sphaeromatidae). Crustaceana 28, 710.
Rützler, K., 2002. Impact of crustose clionid sponges on Caribbean reef corals. Acta
Geol. Hisp. 37, 6172.
Sanford, E., 1999. Regulation of keystone predation by small changes in ocean tempera-
ture. Science 283, 20952097.
Siegrist, H.G., Bowman, R.G., Randall, R.H., Stifel, P.B., 1992. Diagenetic effects related to
hot water efuent in a modem reef on Guam. Pac. Sci. 46, 379.
Smith, T.B., 2008. Temperature effects on herbivory for an Indo Pacic parrotsh in
Panamá: implications for coralalgal competition. Coral Reefs 27, 397405.
Sorte, C.J.B., Williams, S.L., Carlton, J.T., 2010a. Marinerange shiftsand speciesintroductions:
comparative spread rates and community impacts. Glob. Ecol. Biogeogr 19, 303316.
Sorte, C.J.B., Williams, S.L., Zerebecki, R.A., 2010b. Ocean warming increases threat of
invasive species in a marine fouling community. Ecology 91, 21982204.
Stachowicz, J.J., Terwin, J.R., Whitlatch, R.B., Osman, R.W., 2002. Linking climate change
and biological invasions: ocean warming facilitates non indigenous species invasion.
PNAS 99, 1549715500.
Talley, T.S., Crooks, J.A., Levin, L.A., 2001. Habitat utilization and alteration by the
burrowing isopod, Sphaeroma quoyanum, in California salt marshes. Mar. Biol.
138, 561573.
Teuten, E.L., Rowland, S.J., Galloway, T.S., Thompson, R.C., 2007. Potential for plastics to
transport hydrophobic contaminants. Environ. Sci. Technol. 41, 77597764.
Thompson, R.C., Olsen, Y., Mitchell, R.P., Davis, A., Rowland, S.J., John, A.W.G.,
McGonigle, D., Russell, A., 2004. Lost at sea, where is all the plastic? Science 304,
838.
Walther, G.-R., 2010. Community and ecosystem responses to recent climate change.
Phil. Trans. R. Soc. B 365, 20192024.
Walther, G.R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J.C., Fromentin,
J.M., Hoegh-Guldberg, O., Bairlein, F., 2002. Ecological responses to recent climate
change. Nature 416, 389395.
Winder, M., Schindler, D.E., 2004. Climate change uncouples trophic interactions in an
aquatic ecosystem. Ecology 85, 21002106.
Woodward, G., Perkins, D.M., Brown, L.E., 2010. Climate change and freshwater ecosystems:
impacts across multiple levels of organization. Phil. Trans. R. Soc. B 12 (365), 20932106.
121T.M. Davidson et al. / Journal of Experimental Marine Biology and Ecology 446 (2013) 115121
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