ArticlePDF Available

Abstract and Figures

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.
Content may be subject to copyright.
Small increases in temperature exacerbate the erosive effects
of a non-native burrowing crustacean
Timothy M. Davidson
, Catherine E. de Rivera
, James T. Carlton
Department of Environmental Science and Management, Portland State University (ESM), PO Box 751, Portland, OR 97207, United States
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
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: (T.M. Davidson),
(C.E. de Rivera), (J.T. Carlton).
Tel.: +507 503 725 9076; fax: + 507 503 725 3834.
0022-0981/$ see front matter © 2013 Elsevier B.V. All rights reserved.
Contents lists available at SciVerse ScienceDirect
Journal of Experimental Marine Biology and Ecology
journal homepage:
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
) with one exposed side (100 cm
). 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
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
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
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
by the
total number of 1 cm
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
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
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)
B1 scenario
(+1.5 °C)
Predicted change in
biological erosion (%)
A2 scenario
(+2.6 °C)
Predicted change in
biological erosion (%)
Padilla Bay, WA
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
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
Mean water temperatures are calculated from the mean temperature of all system-wide monitoring stations between 2000 and 2010. See ESM 1 for details.
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.
Predicted changes in biological erosion were calculated from the relationships between burrow volume and temperature as presented in Fig. 1.
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.,
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,
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
Guam Coral Altered coral structure Siegrist et al. (1992)
Littorine snails New South Wales,
Sandstone Altered morphology of sandstone platforms & tidepools
Petraitis (1992)
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://
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
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]
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,
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,
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,
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 (
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:// (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,
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
... Human-induced changes in ocean chemistry [1][2][3][4][5][6][7][8][9], temperature [1,5,9,10], and water quality [3,[11][12][13][14][15][16] are threatening coral reefs [1,11,17]. Predictions of reef response to changing ocean conditions are often based on the response of reef building corals alone [17,18]; however, coral reef bioerosion from borers (e.g., boring bivalves, sponges, and marine worms) and grazers (e.g., parrotfish and urchins) and secondary accretion from crustose coralline algae (CCA) and other encrusting invertebrates are also critical processes for reef sustainability [19]. ...
... Further, how will multiple environmental stressors impact individual reef processes? Many environmental parameters interact to drive patterns in accretion and erosion, including ocean acidity [1][2][3][4][5][6][7][8][9], temperature [1,5,9,10], nutrients [3,[11][12][13][14], and gradients of human influence (e.g., chlorophyll, turbidity, sedimentation) [15,16]. This myriad of drivers complicates the predictions of reef response to climate change. ...
Full-text available
Corals build reefs through accretion of calcium carbonate (CaCO3) skeletons, but net reef growth also depends on bioerosion by grazers and borers and on secondary calcification by crustose coralline algae and other calcifying invertebrates. However, traditional field methods for quantifying secondary accretion and bioerosion confound both processes, do not measure them on the same time-scale, or are restricted to 2D methods. In a prior study, we compared multiple environmental drivers of net erosion using pre- and post-deployment micro-computed tomography scans (μCT; calculated as the % change in volume of experimental CaCO3 blocks) and found a shift from net accretion to net erosion with increasing ocean acidity. Here, we present a novel μCT method and detail a procedure that aligns and digitally subtracts pre- and post-deployment μCT scans and measures the simultaneous response of secondary accretion and bioerosion on blocks exposed to the same environmental variation over the same time-scale. We tested our method on a dataset from a prior study and show that it can be used to uncover information previously unattainable using traditional methods. We demonstrated that secondary accretion and bioerosion are driven by different environmental parameters, bioerosion is more sensitive to ocean acidity than secondary accretion, and net erosion is driven more by changes in bioerosion than secondary accretion.
... Field studies have been indirect or strongly confounded by other environmental variables: Fabricius et al. (2011) showed that the density of externally visible borer orifices in live Porites sp. were higher in closer proximity to CO 2 seeps in Papua New Guinea ). Manzello et al. (2008 compared 3 sites in the eastern tropical Pacific and found that erosion rates were higher at sites with frequent upwelling of water with a low aragonite saturation state (Manzello et al. 2008), but these upwelling sites also had high nutrients and low temperature: temperature and nutrients are both known drivers of bioerosion (Le Grand & Fabricius 2011, Davidson et al. 2013. ...
... Sampling technique. Previous studies have identified nutrient concentration (e.g. Rose & Risk 1985, Holmes 2000, Le Grand & Fabricius 2011, chlorophyll (Le Grand & Fabricius 2011), temperature (Davidson et al. 2013), pH (Tribollet et al. 2009, Wisshak et al. 2012, 2013, Reyes-Nivia et al. 2013, Fang et al. 2013) and depth (Perry 1998, Le Grand & Fabricius 2011, Schmidt & Richter 2013 as possible drivers of the accretionerosion balance. This study compared the effect of these environmental parameters on net accretionerosion using data obtained from discrete water samples (pH, TA, nitrate (NO 3 -), nitrite (NO 2 -), ammonium (NH 4 + ), phosphate (PO 4 3-), and chlorophyll a) and from continuous sensors (temperature and depth) along the transect. ...
Full-text available
Coral reefs persist in an accretion-erosion balance and ocean acidification resulting from anthropogenic CO2 emissions threatens to shift this balance in favor of net reef erosion. Corals and calcifying algae, largely responsible for reef accretion, are vulnerable to environmental changes associated with ocean acidification, but the direct effects of lower pH on reef erosion has received less attention, particularly in the context of known drivers of bioerosion and natural variability. This study examines the balance between reef accretion and erosion along a wellcharacterized natural environmental gradient in Ka¯ne‘ohe Bay, Hawai‘i using experimental blocks of coral skeleton. Comparing before and after micro-computed tomography (μCT) scans to quantify net accretion and erosion, we show that, at the small spatial scale of this study (tens of meters), pH was a better predictor of the accretion-erosion balance than environmental drivers suggested by prior studies, including resource availability, temperature, distance from shore, or depth. In addition, this study highlights the fine-scale variation of pH in coastal systems and the importance of micro habitat variation for reef accretion and erosion processes. We demonstrate significant changes in both the mean and variance of pH on the order of meters, providing a local perspective on global increases in pCO2. Our findings suggest that increases in reef erosion, combined with expected decreases in calcification, will accelerate the shift of coral reefs to an erosiondominated system in a high-CO2 world. This shift will make reefs increasingly susceptible to storm damage and sea-level rise, threatening the maintenance of the ecosystem services that coral reefs provide
... The Sphaeroma found in Hainan, Dongzhaigang, was Sphaeroma terebrans Bate, 1866 (Baratti, Filippelli, and Messana, 2011;Fan et al., 2014), which is a marine, intertidal wood-borer species that is widely distributed across tropical and subtropical areas (Brooks, 2004). Various studies have shown that it can live at a wide range of salinities and temperatures (Davidson, de Rivera, and Carlton, 2013;Heath and Khazaeli, 1985). The S. terebrans habitats often overlap, which means that it is commonly found in mangroves across China, the Philippines, and Kenya (Baratti et al., 2011). ...
... Nutrient loading also weakens coral skeletal structure (Caroselli et al. 2011;Mwachireya et al. 2016;Rice et al. 2019), which could make corals more susceptible to infestation by macroborers in eutrophic reefs. Notably, environmental parameters other than nutrients (e.g., pH, temperature, etc.) also affect patterns of bioeroder densities and bioerosion rates (e.g., Le Grand and Fabricius 2011;Davidson et al. 2013;Silbiger et al. 2014;Enochs et al. 2016;Silbiger et al. 2016Silbiger et al. , 2017. These parameters may covary or interact with nutrients (Manzello et al. 2008;DeCarlo et al. 2015;Prouty et al. 2017;Silbiger et al. 2018) and could contribute to the macroborer patterns in this study. ...
Full-text available
Bioerosion by reef-dwelling organisms influences net carbonate budgets on reefs worldwide. External bioeroders, such as parrotfish and sea urchins, and internal bioeroders, including sponges and lithophagid bivalves, are major contributors to bioerosion on reefs. Despite their importance, few studies have examined how environmental (e.g., nutrients) or biological drivers (e.g., the actions of other bioeroders) may influence bioeroder dynamics on reefs. For example, internal bioeroders could promote external bioerosion by weakening the coral skeletal matrix. Our study investigated: (1) whether nutrient supply influences the dynamics between internal and external bioeroders and (2) how the presence of a boring bivalve, Lithophaga spp., influences parrotfish bioerosion on massive Porites corals. We hypothesized that nutrient supply would be positively correlated with Lithophaga densities on massive Porites colonies, and that as bivalve density increased, the frequency and intensity of parrotfish bioerosion would increase. To test these hypotheses, we analyzed six time points over a 10-yr period from a time series of benthic images and nitrogen content of a dominant macroalga from the fringing reefs around Moorea, French Polynesia. We found Lithophaga densities were positively correlated with nitrogen availability. Further, massive Porites that are more infested with Lithophaga had both a higher probability of being bitten by parrotfish and a higher density of bite scars from parrotfishes. Our findings indicate that increasing nutrient availability may strengthen the relationship between internal and external bioeroders, suggesting that colonies at more eutrophic sites may experience higher bioerosion rates.
... Some species and bioerosion effects are influenced strongly by temperature variability, such as lichens whose thalli expand and contract inside rock in response to freezethaw cycles (Chen et al. 2000). Furthermore, the relationship between temperature and bioerosion is unlikely to be linear, but rather depends on the magnitude of the temperature increase and the physiological tolerances of the taxa, since high temperatures will eventually lead to stressful conditions that depress survivorship and bioerosive activities (Davidson et al. 2013). Such ambiguities reinforce the need for more controlled empirical studies to investigate the long-term effects of temperature on different bioeroder functional groups and comparisons across a broad latitudinal range before general predictions can be made. ...
Full-text available
Bioerosion, the breakdown of hard substrata by organisms, is a fundamental and widespread ecological process that can alter habitat structure, biodiversity and biogeochemical cycling. Bioerosion occurs in all biomes of the world from the ocean floor to arid deserts, and involves a wide diversity of taxa and mechanisms with varying ecological effects. Many abiotic and biotic factors affect bioerosion by acting on the bioeroder, substratum, or both. Bioerosion also has socio-economic impacts when objects of economic or cultural value such as coastal defences or monuments are damaged. We present a unifying definition and advance a conceptual framework for (a) examining the effects of bioerosion on natural systems and human infrastructure and (b) identifying and predicting the impacts of anthropogenic factors (e.g. climate change, eutrophication) on bioerosion. Bioerosion is responding to anthropogenic changes in multiple, complex ways with significant and wide-ranging effects across systems. Emerging data further underscore the importance of bioerosion, and need for mitigating its impacts, especially at the dynamic land–sea boundary. Generalised predictions remain challenging, due to context-dependent effects and nonlinear relationships that are poorly resolved. An integrative and interdisciplinary approach is needed to understand how future changes will alter bioerosion dynamics across biomes and taxa.
... Other sphaeromatids also burrow in soft stone, peat, and even into extruded polystyrene foam Bell 2001, Davidson et al. 2008). Sphaeroma quoianum, for example, has often been reported to excavate galleries in polystyrene floats under docks (Davidson et al. 2013). ...
... There are several mechanisms that could be mediating the increased dissolution rates in the high temperature-pCO 2 treatments. (1) Higher temperatures could increase the metabolism of the bioeroder community, thus increasing borer activity (e.g., Davidson et al., 2013). (2) Because many boring organisms excrete acidic compounds to erode the skeletal structure (Hutchings, 1986), reduced pH in the overlaying water column may reduce the metabolic cost to the organisms, making it easier for eroders to break down the CaCO 3 . ...
Full-text available
Climate change threatens both the accretion and erosion processes that sustain coral reefs. Secondary calcification, bioerosion, and reef dissolution are integral to the structural complexity and long-term persistence of coral reefs, yet these processes have received less research attention than reef accretion by corals. In this study, we use climate scenarios from RCP 8.5 to examine the combined effects of rising ocean acidity and sea surface temperature (SST) on both secondary calcification and dissolution rates of a natural coral rubble community using a flow-through aquarium system. We found that secondary reef calcification and dissolution responded differently to the combined effect of pCO2 and temperature. Calcification had a non-linear response to the combined effect of pCO2 and temperature: the highest calcification rate occurred slightly above ambient conditions and the lowest calcification rate was in the highest temperature–pCO2 condition. In contrast, dissolution increased linearly with temperature–pCO2 . The rubble community switched from net calcification to net dissolution at +271 μatm pCO2 and 0.75 °C above ambient conditions, suggesting that rubble reefs may shift from net calcification to net dissolution before the end of the century. Our results indicate that (i) dissolution may be more sensitive to climate change than calcification and (ii) that calcification and dissolution have different functional responses to climate stressors; this highlights the need to study the effects of climate stressors on both calcification and dissolution to predict future changes in coral reefs.
Full-text available
Dodge-Wan, D. and Nagarajan, R., 2020. Boring of intertidal sandstones by isopod Sphaeroma triste in NW Borneo (Sarawak, Malaysia). Journal of Coastal Research, 36(2), 238–248. Coconut Creek (Florida), ISSN 0749-0208. Sphaeromatid isopods are known for their ability to bore into wood and friable rock and to cause damage to mangrove plant roots, wooden structures, and polystyrene dock floats in the intertidal zone. The ability of isopods to bore extensively into rock and accelerate coastal erosion is less well known and has not been previously reported in Malaysia. This study investigated the presence, the identity, and the erosive effect of rock-boring isopods in sandstones of the NW Borneo coastal region (Sarawak, East Malaysia). A multidisciplinary approach was used, including field and laboratory observations (geological and biological) of rocks and wood. This study revealed that abundant cylindrical borings in soft intertidal rock are created by the boring isopod Sphaeroma triste (S. triste). Bioerosion by this species can result in the direct removal of up to 50% of the exposed surface of the rock and penetrate the rock up to a few centimeters depth. This has a significant but localised impact on coastal erosion, contributing to the development of concavities in the rock, enlargement of joints, deepening of wave cut notches, widening of rock pools, and erosion of fallen blocks and sea-cave walls. There is evidence of modification of the isopods' mandible incisor processes by abrasion during rock boring. Although several Sphaeromatid species are known to bore into soft rocks, this is the first report and comprehensive description of boring into sandstone substrates by S. triste. The S. triste borings are compared with those made by other species reported elsewhere. In terms of neoichnology, the borings belong to deep-tier Trypanites ichnofacies, and fossil equivalents may be useful in palaeogeographic reconstructions of ancient shorelines, although they may have poor preservation potential.
Thousands of marine species have been moved around the globe by human activities, at increasing rates over the past century. Many of these species (here termed “alien”) have taken up residence on mudflats. How are mudflats changing as a consequence of this biological reshuffling? The preceding chapters document mudflats as productive environments with strong species interactions, which both shape and are shaped by the physical environment. The same pattern appears when alien species are added to the system. Attributes of the physical environment play strong roles in determining the success of different alien species on mudflats, while many high-impact alien species create biogenic structure and/or modify sediment stability. Above-ground habitat complexity from alien vegetation or reefs can facilitate both alien and native species, but it can also interfere with infauna and birds that depend on an unimpeded sediment interface or particular grain size. Most mudflat aliens, however, simply add to the diversity and linkages of native communities. The biological changes from invasions are occurring within a context of other global changes, all likely to interact because alien species can be promoted by anthropogenic hard structure and warming temperatures.
Full-text available
The human-mediated introduction of marine non-indigenous species is a centuries-if not millennia-old phenomenon, but was only recently acknowledged as a potent driver of change in the sea. We provide a synopsis of key historical milestones for marine bioinva-sions, including timelines of (a) discovery and understanding of the invasion process, focus-ing on transfer mechanisms and outcomes, (b) methodologies used for detection and monitoring, (c) approaches to ecological impacts research, and (d) management and policy responses. Early (until the mid-1900s) marine bioinvasions were given little attention, and in a number of cases actively and routinely facilitated. Beginning in the second half of the 20 th century, several conspicuous non-indigenous species outbreaks with strong environmental, economic, and public health impacts raised widespread concerns and initiated shifts in public and scientific perceptions. These high-profile invasions led to policy documents and strategies to reduce the introduction and spread of non-indigenous species, although with significant time lags and limited success and focused on only a subset of transfer mechanisms. Integrated, multi-vector management within an ecosystem-based marine management context is urgently needed to address the complex interactions of natural and human pressures that drive invasions in marine ecosystems.
Full-text available
Biostatistics channels ecologists into thinking primarily about the mean and variance of a probability distribution. But many problems of biological interest concern the extremes in a variable (e.g., highest temperature, largest force, longest drought, maximum lifespan) rather than its central tendency. Such extremes are not adequately addressed by standard biostatistics. In these cases an alternative approach--the statistics of extremes--can be of value. In the limit of a large number of measurements, the probability structure of extreme values conforms to a generalized distribution described by three parameters. In practice these parameters are estimated using maximum likelihood techniques. Using this estimate of the probability distribution of extreme values, one can predict the expected time between the imposition of extremes of a given magnitude (a return time) and can place confidence limits on this prediction. Using data regarding sea-surface temperature, wave-induced hydrodynamic forces, wind speeds, and human life-spans we show that accurate long-term predictions can at times be made from a surprisingly small number of measurements if appropriate care is taken in the application of the statistics. For example, accurate long-term prediction of sea-surface temperatures can be derived from short-term data that are anomalous in that they contain the effects of an extreme EL Nino. In the cases of wave-induced forces and wind speeds, the probability distribution of extreme values is similar among years and diverse sites, indicating the possible existence of unifying principles governing these phenomena. Limitations and possible misuse of the method are discussed.
Full-text available
Using field measurements and field experiments, we investigated the effect of a dominant Southwest Atlantic intertidal burrowing crab, Chasmagnathus granulatus, on the inland growth of tidal creeks and creek genesis in salt marshes. By burrowing intensively on marsh sediments, this crab changed sediment physical parameters, such as penetrability, water content, and shear strength, which are related to sediment resistance to erosion. There were positive relationships between crab density and activities occurring in the creek heads and creek growth rates. Field experiments show that the presence and activity of C. granulatus and the presence of their burrows enhance the growth rates of tidal creeks, promoting marsh erosion. When crabs were present, these creeks grew faster than did creeks in which crabs were excluded. Furthermore, the interaction (disturbance and herbivory) between crabs and the dominant halophyte marsh plant, Sarcocornia perennis, generate circular depressions that accumulate standing water (salt pans), which in turn facilitates the creation of new creeks in the marsh surface, which evolve, to a greater extent, into fully functional tidal creeks because of colonization by crabs, which in turn further enhances creek growth rates. These direct and indirect effects of crabs on marsh erosion provide strong evidence of the importance of bioturbation and biological processes to the erosion and geomorphology of marshes.
Full-text available
Trembling aspen (Populus tremuloides Michx.) is the most important deciduous,tree in the Canadian boreal forest, with >1000 Tg of carbon stored in the aboveground biomass of this species. Since the early 1990s, aspen dieback has been noted over parts of the southern boreal forest and aspen parkland in western Canada. In this study, tree-ring analysis and forest health assessments were conducted in 18 aspen stands near Grande Prairie, Alta., to exam - ine causes of reduced growth,and dieback. Defoliation histories were reconstructed based on light-colored (“white”) tree rings and records of past insect outbreaks. The results indicated that several factors contributed to the observed dieback. Defoliation by forest tent caterpillar ( Malacosoma,disstria Hbn.) and drought in the 1960s and 1980s led to reduced growth,and predisposed,some,stands to secondary,damage,by wood-boring insects and fungal pathogens. Thaw‐freeze events during a period (1984‐1993) of unusually light snow,cover in late winter may,have also contrib- uted to the observed dieback. Under global change, the severity of these stressors may increase, which would pose a serious concern for the future health, productivity, and carbon sequestration of aspen forests in the region. Résumé : Avec plus de 1000 Tg de carbone emmagasiné dans la biomasse épigée de cette essence, le peuplier faux-
The two common representatives in Southern California of the nearly world wide genus, Littorina, are L. planaxis and L. scutu!ata. The former generally occurs at higher levels in the intertidal, but the zones of distribution of the two species overlap. L. planaxis may often be found 5 to 10 feet above spring high tide level, but L. scutulata prefers a zone two or three feet on either side of the high tide mark. Published information concerning these two species of snail is scanty in spite of their great abundance and their availability. Their importance to the high intertidal community, however, warrants an extensive study of their ecology, and the present paper describes some of the basic biology of these interest ing animals. SIZE DISTRIBUTION Inspection of colonies of Littorina at different places along the La Jolla shore has revealed that the majority of snails at any given locality fall within certain rather well defined size limits. Lysaght (1941) noted a similar condition in L. neritoides on the Plymouth Brçakwater. In order to gain a more exact picture of size distributions in the present study, three typical Littorina environments were chosen, and height measurements were made of all the periwinkles found within a selected area, representative of the environment.