HomeMy WebLinkAboutEstuarine_Coastal and Shelf Science submitted by Sarah Oktay_201405230907063335Local extirpations and regional declines of endemic upper beach
invertebrates in southern California
D.M. Hubbard
*, J.E. Dugan, N.K. Schooler, S.M. Viola
Marine Science Institute, University of California, 4400 Marine Sciences Bldg., Santa Barbara, CA 93106, USA
article info
Article history:
Received 21 January 2013
Accepted 20 June 2013
Available online xxx
Keywords:
coastal armoring
erosion
beach management
indicator species
intertidal environment
range limit
abstract
Along the world’s highly valued and populous coastlines, the upper intertidal zones of sandy beach eco-
systems and the biodiversity that these zones support are increasingly threatened by impacts of human
activities, coastal development, erosion, and climate change. The upper zones of beaches typically support
invertebrates with restricted distributions and dispersal, making them particularly vulnerable to habitat loss
and fragmentation. We hypothesized that disproportionate loss or degradation of these zones in the last
century has resulted in declines of upper shore macroinvertebrates in southern California. We identified a
suite of potentially vulnerable endemic upper beach invertebrates with direct development, low dispersal
and late reproduction. Based on the availability of printed sources and museum specimens, we investigated
historical changes in distribution and abundance of two intertidal isopod species (Tylos punctatus,Alloniscus
perconvexus) in southern California. Populations of these isopods have been extirpated at numerous his-
torically occupied sites:T. punctatus from 16 sites (57% decrease), and A. perconvexus from 14 sites (64%
decrease). During the same period, we found evidence of only five colonization events. In addition, the
northern range limit of the southern species,T. punctatus, moved south by 31 km (8% of range on California
mainland) since 1971. Abundances of T. punctatus have declined on the mainland coast; only three recently
sampled populations had abundances >7000 individuals m
1.ForA. perconvexus populations, abundances
>100 individuals m
1now appear to be limited to the northern part of the study area. Our results show that
numerous local extirpations of isopod populations have resulted in regional declines and in greatly reduced
population connectivity in several major littoral cells of southern California. Two of the six major littoral
cells (Santa Barbara and Zuma) in the area currently support 74% of the remaining isopod populations.
These isopods persist primarily on relatively remote, ungroomed, unarmored beaches with restricted
vehicle access and minimal management activity. These predominantly narrow, bluff-backed beaches also
support species-rich upper beach assemblages, suggesting these isopods can be useful indicators of
biodiversity. The high extirpation rates of isopod populations on the southern California mainland over the
last century provide a compelling example of the vulnerability of upper beach invertebrates to coastal
urbanization. Climate change and sea level rise will exert further pressures on upper beach zones and biota
in southern California and globally. In the absence of rapid implementation of effective conservation stra-
tegies, our results suggest many upper intertidal invertebrate species are at risk.
2013 Elsevier Ltd. All rights reserved.
1. Introduction
Habitat loss, degradation and fragmentation are broadly
recognized as major threats to biodiversity and to the survival of
vulnerable species and populations (e.g.Wilcove et al.,1998; Fahrig,
2003; Henle et al., 2004; Ewers and Didham, 2006). Coastal
development, human activities and management practices have
been shown to significantly impact sandy beach habitats affecting
ecosystem community structure and biodiversity. On urbanized
coasts, beach ecosystems are challenged by a broad range of
stressors including shoreline development, contaminants, human
activities and management practices, such as grooming, nourish-
ment and coastal armoring (Defeo et al., 2009). Placement of
coastal armoring structures has been shown to reduce the overall
width of beaches over large stretches of coastline (Orme et al.,
2011). Shoreline retreat and erosion coupled with coastal armor-
ing causes a disproportionate reduction of upper beach habitat
relative to wet and saturated lower beach habitats which can
eliminate wrack-associated and other macroinvertebrates (Dugan
and Hubbard, 2006; Dugan et al., 2008; Jaramillo et al., 2012).
Beach filling or nourishment projects can result in complete mor-
tality of sandy intertidal biota (e.g.Peterson and Bishop, 2005;
Schlacher et al., 2012). The widespread practice of beach
*Corresponding author.
E-mail address:hubbard@lifesci.ucsb.edu (D.M. Hubbard).
Contents lists available at SciVerse ScienceDirect
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journal homepage: www.elsevier.com/locate/ecss
0272-7714/$e see front matter 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.ecss.2013.06.017
Estuarine, Coastal and Shelf Science xxx (2013) 1e9
Please cite this article in press as: Hubbard, D.M., et al., Local extirpations and regional declines of endemic upper beach invertebrates in
southern California, Estuarine, Coastal and Shelf Science (2013), http://dx.doi.org/10.1016/j.ecss.2013.06.017
grooming or raking also directly impacts wrack-associated and
upper beach invertebrates (Llewellyn and Shackley, 1996; Dugan
et al., 2003) as well as coastal strand and dune biota (Dugan and
Hubbard, 2010).
As sea level rises, shoreline erosion accelerates, and human
populations expand on coasts, the ecological consequences of all
three of these intensifying pressures on beach ecosystems become
increasingly apparent. The recognition of the impacts of these
growing pressures and habitat losses on beach-dependent plants,
and vertebrate species, including sea turtles, pinnipeds, birds, and
fish, have generated special status designations and major conser-
vation efforts (e.g.Oli et al., 2001; Donlan et al., 2003; Garcia et al.,
2003; Maschinski and Wright, 2006). Less well recognized are the
disappearances ofonceabundantintertidal invertebratefaunafrom
many beachesalong urbanized coastlines (e.g.Nagano,1980). These
losses have the potential to alter the biodiversity and function of
beach ecosystems on regional scales along developed coasts
(Dugan et al., 2008; Defeo et al., 2009; Dugan and Hubbard, 2010).
For some coastal ecosystems, individual populations of organ-
isms, even those in marginal and fragmented habitats (sinks), can
persist through the influx of planktonic propagules and larvae
produced by source populations. A subset of intertidal species may
be more vulnerable to disturbances; these species include taxa that
do not have planktonic larval stages and have low adult dispersal,
(such as oniscoidean isopods, talitrid amphipods and flightless in-
sects). On sandy beaches, a high proportion of intertidal inverte-
brate species can be direct developing taxa, lacking planktonic
larval stages (e.g.>50% in California;Grantham et al., 2003).Brown
(2000)recognized this issue and made a strong case for the
vulnerability of these upper beach species, highlighting the African
isopod,Tylos granulatus, as an example. A list of upper beach in-
vertebrates that appear to exemplify these vulnerabilities in the
southern California region appears in Table 1.
As local scale losses of intertidal species accumulate on urban
coasts, the resulting regional scale declines and fragmentation of
remaining populations of these species need to be documented and
recognized along with the implications for reduced biodiversity
and ecosystem integrity and function. In this study we identified a
suite of species that may be particularly vulnerable to the dispro-
portionate loss and degradation of upper beach habitats in the last
century in southern California (Table 1). Using published literature,
unpublished dissertations,theses and reports, museum recordsand
field surveys, we investigated changes in the distribution and
abundance of selected upper beach invertebrate species over time.
2. Methods
2.1. Study area
Our study area spanned the southern California mainland coast
between Point Conception and the Mexican border (approximately
450 km). The area contains six major littoral cells (Orme et al., 2011,
Fig. 1) and spans five coastal counties. The study area is highly
populated and includes the major population centers of the
metropolitan Los Angeles area (18.1 million people) and the greater
San Diego area (>3 million people). Development of the coast,
including expansion of harbors, contributed several hundred
million cubic meters of sediment (ranging in size from fines to
cobbles) to the coast between 1920 and 1950. Individual projects,
such as improvements at San Diego harbor between 1936 and 1946
placed as much as 30.6 million m
3 of sediment on the shoreline. As
the surplus of sediments added to the coast from big projects faded
in recent decades, the severe reduction of natural sand supply has
become apparent as beaches have narrowed, coastal erosion
accelerated (Griggs et al., 2005) and textural changes have become
apparent (Kuhn and Shepard,1984). The annual sediment deficit in
southern California due to dams trapping sand in reservoirs has
been estimated to be 1.02 million m
3 y 1 for more than 50 years
(Griggs et al., 2005). For almost a century, responses to sand-
starved beaches and coastal erosion in southern California have
included extensive coastal armoring and beach nourishment pro-
jects (Orme et al., 2011). More than 120 km (27%) of the wave
exposed southern California mainland coast is armored (Griggs
et al., 2005). Management of southern California beaches includes
other elements such as beach raking or grooming, berm building,
driving and dredge disposal (Defeo et al., 2009). Mechanical beach
grooming is particularly widespread affecting approximately
161 km (45%) of the beaches on the southern California mainland
(Dugan et al., 2003).
2.2. Study organisms
After evaluating the availability of information on distributions
of potentially vulnerable species (Table 1) over time in the study
area, we focused on two species of intertidal oniscoidean isopods
inhabiting the upper zones of beaches on the Pacific coast of North
America. The tylid isopod Tylos punctatus (Oniscoidea, Tylidae) is a
beach endemic species that was described in 1909 based on a
specimencollected in San Diego,California, USA. The distribution of
T.punctatus extends from its current northern range limit in the
study area near Carpinteria, California, USA to central Baja Califor-
nia, Mexico.T. puncatus is also reported to occur on the shores of
the Sea of Cortez, Gulf of California, Mexico. However, both Lee
(2013)and Hamner et al. (1969)have suggested that Pacific coast
populations are deeply divergent or a separate species from the
lineage found in the Gulf of California. The distribution of the
alloniscid isopod,Alloniscus perconvexus, (Oniscoidea, Alloniscidae)
another beach endemic species extends along the coast both north
and south of the study area from British Columbia, Canada to Baja
California, Mexico.Alloniscus perconvexus was described by Dana in
1854 based on a specimen collected in California.
These two beach isopod species are typical peracarid crusta-
ceans with low fecundity that brood their young and have low
dispersal rates. Theyapparently have very similar ecological niches,
playing a significant role in kelp wrack consumption and process-
ing (Hayes, 1969). However, no studies have made direct compar-
isons of their distribution, behavior or feeding in field settings.
These isopods are prey for shorebirds and fish. Although tolerant of
immersion in salt water, these species of oniscoidean isopods have
no planktonic or swimming life stages (Brusca, 1966). Inhabiting
upper intertidal and supralittoral zones of open coast sandy bea-
ches, these and other sandy beach oniscoidean isopod species
burrow in the sand near the high tide line during the day emerging
at night to feed on wave cast macroalgal wrack and carrion
(Ricketts et al., 1992; Brown and Odendaal, 1994; Carlton, 2007).
Hayes (1969)reported that giant kelp,Macrocystis pyrifera, was the
Table 1
Upper intertidal and coastal strand invertebrate species that appear to be vulnerable
to declines in abundance or reduced distributions on southern California beaches.
#adults capable of flight, *Coastal strand zone.
Species Taxon Common name (family)
Tylos punctatus Isopoda Isopod (Tylidae)
Alloniscus perconvexus Isopoda Isopod (Alloniscidae)
Megalorchestia spp. Amphipoda Beachhoppers (Talitridae)
Dychirius marinus Coleoptera Beetle (Carabidae)
Cincindela spp.# Coleoptera Tiger beetle (Cincindelidae)
Thinopinus pictus Coleoptera Pictured rove beetle (Staphylindae)
Hadrotes crassus Coleoptera Rove beetle (Staphylindae)
Coelus globosus*Coleoptera Globose dune beetle (Tenebrionidae)
Endeodes spp.Coleoptera Soft-winged flower beetle (Melyridae)
D.M. Hubbard et al. / Estuarine, Coastal and Shelf Science xxx (2013) 1e92
Please cite this article in press as: Hubbard, D.M., et al., Local extirpations and regional declines of endemic upper beach invertebrates in
southern California, Estuarine, Coastal and Shelf Science (2013), http://dx.doi.org/10.1016/j.ecss.2013.06.017
preferred food of Tylos punctatus. Burrowing behavior in intertidal
oniscoidean isopods is sensitive to sediment texture and moisture
levels (Holanov and Hendrickson, 1980; de Villiers and Brown,
2012; Viola et al., 2013). Seasonal patterns in surface activity have
been reported for T. punctatus. Between March and November, this
species actively foraged on the beach surface at night, while in the
winter surface activity was reduced, withanimals remaining buried
in the sand or under wrack (Hamner et al., 1968, 1969). Maximum
body lengths attained are 13 mm for T. punctatus (Hayes,1969) and
16 mm for Alloniscus perconvexus. For T. punctatus, annual growth
rate estimates ranged from 0.5 to 4 mm with a mean of 2 mm and
males reached larger sizes than females (Hayes,1969). These isopod
species are relatively long-lived with late reproduction and low
fecundity. For T. punctatus,Hamner et al. (1969)reported that few
females reproduced before their third year producing one brood
(mean of 13.6 young) per summer and most died soon after.
2.3. Data sources
We compiled historical and recent data on the distribution and
abundance of Tylos punctatus and Alloniscus perconvexus, from
museum records, published papers, theses, dissertations, books,
technical reports and new field surveys. We obtained location in-
formation for a total of 118 beach sites, including sites where the
two isopod species had been reported and sites where intertidal
macroinvertebrate communities had been surveyed. Our data also
included records from 37 additional sites on the California Channel
Islands obtained from avarietyof sources (Hewatt,1946; US Bureau
of Land Management, 1979; Straughan, 1982; Garthwaite et al.,
1985; Dugan et al., 1995).
The data we compiled were classified into three major time
periods, early (1913e1955), middle (1969e1982) and recent
(1996e2012). Most of the early records (1913e1955) of the distri-
butions of Tylos punctatus and Alloniscus perconvexus provided only
general location information, such as the name of the nearest city
(Searle,1905; Stafford,1912,1913; Thompson and Thompson,1919;
Johnson and Snook, 1927; Smithsonian National Museum of
Natural History, 2012). The records from 1969 to 2012 generally
provided more detailed location information including beach
segment (although some of these have changed over time), and
local landmarks. The records from this period often included den-
sity estimates. Published studies, reports, data archives and
museum specimens associated with the majority of these later
records came from:Hamner et al. (1969)three sites,Clark (1969)
six sites,Hayes (1969, 1970; 1974; 1977)26 sites,Craig (1973)
three sites,Patterson (1974)nine sites,Parr et al., 1978 one site,
Straughan (1982)26 sites, and Dugan et al. (1995, 2000, 2003 and
unpublished) 77 sites.
2.4. Field surveys
To investigate the distribution and persistence of the study
species in the region, we re-surveyed 20 sites that had supported
one or more of these upper beach isopod species in the past. Our
surveys were conducted between 2010 and 2011 using a variety of
sampling methods. For surveys focused solely on upper beach taxa,
we sampled three shore normal transects at each site during
daylight hours, taking thirty 10 cm cores to 20 cm depth, from the
highest (seasonal maximum) wrack line to the lower (seaward)
limit of the talitrid amphipod zone on each transect. Cores were
sieved through 1.0e1.5 mm mesh bags to retain animals, placed in
Fig. 1.Map of the southern California study area showing coastal counties and major littoral cells (separated by dotted lines, after Orme, 2011). Sites where changes in population
status were found are indicated for Tylos punctatus (triangles) and Alloniscus perconvexus (circles) on the mainland coast. For both species, closed symbols indicate extirpations
evident between early and middle period records and open symbols indicate those between the middle and recent records. Symbols with striped shading indicate colonization
events (middle to late, or within the late period).
D.M. Hubbard et al. / Estuarine, Coastal and Shelf Science xxx (2013) 1e9 3
Please cite this article in press as: Hubbard, D.M., et al., Local extirpations and regional declines of endemic upper beach invertebrates in
southern California, Estuarine, Coastal and Shelf Science (2013), http://dx.doi.org/10.1016/j.ecss.2013.06.017
labeled plastic bags then frozen and sorted in the laboratory. For
intertidal community biodiversity surveys, three shore normal
transects were also sampled and core size and depth and sieve size
were the same as described above. Community biodiversity survey
methods are described in detail in Dugan et al. (2003)and Schooler
et al., 2013. In all surveys, densities were expressed as number of
individuals per meter of shoreline based on the intervals between
cores. The lower limit for detecting populations of isopods with
these methods and the zone widths encountered would be at a
density of approximately 20 individuals m
1 of shoreline. At four of
the 20 sites, we did not conduct quantitative surveys, but visually
searched for surface burrows and excavated sand near and under
wrack that was located at and above the high tide line.
3. Results
3.1. Early records
Our earliest records of these two endemic upper beach isopod
species are more than 100 years old (e.g.Alloniscus perconvexus at
Santa Barbara in 1876;Searle, 1905), however, we were not able to
confirm how commonly these isopods were encountered on bea-
ches in the study area prior to initial coastal urbanization in the
1920’s and the intensive development in the 1950’s following
World War II. Since the first quantitative intertidal surveys of
southern California beaches conducted in the 1970’s, these isopods
have been reported at only a small proportion (25%) of the beach
sites surveyed. However, the earliest (40 years ago) of these
quantitative surveys were conducted following the onset of major
urban development and widespread beach grooming along the
southern California coastline.
3.2. Extirpations
Our recent surveys indicated that populations of these isopod
species are no longer present at the majority of the beaches they
historically occupied along approximately 450 km of shoreline on
the southern California mainland. Overall, our analysis found
populations of upper beach isopods have been extirpated at nine of
the 12 (75%) sites where they were reported in the early period
(before 1955) (Fig. 1). These extirpations are clustered along the
metropolitan Los Angeles coast. Populations of Tylos punctatus
appear to have been eliminated from 16 of the 28 sites where they
were reported in the early and middle periods for an estimated
extirpation rate of 57% in less than 100 years (Fig.1). The estimated
extirpation rate for Alloniscus perconvexus in the study is compa-
rable at 64%, based on the elimination of populations from 14 of 22
sites where they were reported in the early and middle periods
(Fig.1).T. punctatus abundance has declined dramatically in recent
years at a site where it was first reported in 2002 (Broad Beach,
Zuma littoral cell). South of the study area, there is little informa-
tion on the distribution or densities of these species, but the
extirpation of one documented population of T. punctatus at
Hamner et al.’s (1968, 1969)study site, Estero Punta Banda, Baja
California, Mexico, located 100 km south of the US/Mexico border
was noted by Hayes and Hamner (pers. comm.).
3.3. Current distribution
We were able to currently document the presence of pop-
ulations of one or both of these isopod species atonly29 sites in our
southern California mainland study area (Fig. 2a, b). These records
include only 12 of the 31 sites where populations of isopods had
been reported in the early and middle periods (five not re-
sampled). Twenty of the sites that now support at least one of
these isopods were not surveyed before 1996. On the mainland we
confirmed the presence of Tylos punctatus at 17 sites, and Alloniscus
perconvexus at 25 sites, and both species occurred at 13 of these
sites. These totals do not include five sites with older records of
these species that we were not able to visit. Populations of one or
both of these species areknownto occuron a numberof beaches on
the California Channel Islands (Fig. 2a, b) but only three of these
sites have been recently visited to confirm status of the pop-
ulations. The majority of the remaining populations of these iso-
pods (74%) are now concentrated in the two northern littoral cells
(Santa Barbara and Zuma cells) in our study area. Several of the
major littoral cells in the study area currently support only a few
populations each (Santa Monica cell: one population of each spe-
cies at a single site, San Pedro cell: four populations at two sites,
Oceansidecell:five populationsatthree sites, SilverStrandcell: one
population)(Fig. 2a, b). Of the 29 beach sites that currently support
extant populations on the mainland,16 are backed bycoastal bluffs,
seven are backed by vegetated coastal dunes, and six are backed by
manmade structures (four by rock revetments).
3.4. Coastal impacts
Information on specific causes of extirpations of Tylos punctatus
and Alloniscus perconvexus from individual beaches in southern
California is limited, although both coastal erosion and manage-
ment have strongly affected their upper beach habitat. There are
some clear examples of large-scale beach habitat destruction, such
as the development of the ports of Los Angeles (San Pedro) and
LongBeach (Fig. 3), which eliminated beach habitatand atleast two
populations of T.punctatus (e.g.Johnson and Snook, 1927). Wide-
spread mechanical beach grooming initiated in the 1960’s, which
severely alters upper beach habitat, coincides with a large gap in
the moderndistributionof T. punctatus and A. perconvexus along the
urban Los Angeles coast in the central portion of our study area
(Fig.1). Most recently, a population ofT.punctatuswas present at an
estimated abundance 713 m
-1 of shoreline in a 2002 survey at
Broad Beach near Malibu (Zuma littoral cell) but was not detected
in quantitative sampling in 2010 (although wefound one individual
in wrack) after the installation of intertidal coastal armoring (rock
and geotextile revetment) (Fig. 4).
3.5. Gaps in distributions
The maximum gaps between populations are currently much
larger in size (>100 km) than the gaps between all reported lo-
calities for each of these species (about 30 km) in the study area
(Figs. 1 and 2). Importantly, a gap of 107 km of coastline now
separates the cluster of the remaining 12 northernmost mainland
populations of Tylos punctatus from the southern populations
(Fig. 2a). Similarly, a gap of 107 km is present between the 21
northern populations of Alloniscus perconvexus and the four
remaining southern populations on the mainland (Fig. 2b). This
major gap in distributions of both isopod species encompasses the
entire Santa Monica littoral cell and all but the southern end of the
San Pedro littoral cell.
Currently most of the isopod populations that are separated
from other conspecific populations by 10 km or less are clustered in
small stretches of the study coast. All eleven gaps of less than ten
km for Alloniscus perconvexus populations occur across a 113 km
stretch of coast in the Santa Barbara and Zuma littoral cells (25% of
the study area), with ten of the gaps in a 51 km distance at the
northern end (11%). For Tylos punctatus, six of the nine gaps less
than ten km occur in the vicinity of its northern range limit at
Rincon County Park, Santa Barbara littoral cell and along the Zuma
littoral cell (69 km, 15% of the study area).
D.M. Hubbard et al. / Estuarine, Coastal and Shelf Science xxx (2013) 1e94
Please cite this article in press as: Hubbard, D.M., et al., Local extirpations and regional declines of endemic upper beach invertebrates in
southern California, Estuarine, Coastal and Shelf Science (2013), http://dx.doi.org/10.1016/j.ecss.2013.06.017
3.6. Population persistence
There are no data available to document year-to-year dynamics
of populations of these isopod species over the decades at any site
in California. However, museum specimens of Tylos punctatus
collected at Torrey Pines in 1925, and observations from 1965 to
1966 (Hayes, 1969) combined with the current existence of a
population appear to indicate 87 years of persistence at that site.
Populations were also documented over a period of 89 years in
Santa Barbara (1876,1899 and 1965,Smithsonian National Museum
of Natural History, 2012; Searle, 1905; Hamner et al., 1969). There
may be one example of longer duration from Laguna based on a
Fig. 2.Current confirmed distributions and abundance (where reported) of populations of (a)Tylos punctatus, and (b)Alloniscus perconvexus on the southern California mainland
coast since 1996 and on the California Channel Islands (since 1977). The size of the gray circles indicates the relative abundance of populations at the sites. Small squares indicate the
lack of information on abundance.
D.M. Hubbard et al. / Estuarine, Coastal and Shelf Science xxx (2013) 1e9 5
Please cite this article in press as: Hubbard, D.M., et al., Local extirpations and regional declines of endemic upper beach invertebrates in
southern California, Estuarine, Coastal and Shelf Science (2013), http://dx.doi.org/10.1016/j.ecss.2013.06.017
collection of T. punctatus made there in 1913, but we were not able
to determine the exact location of the original collection. Pop-
ulations of both species appear to have persisted continuously on
the beaches of the California Channel Islands (Fig. 2) with inter-
mittent reports of both species occurring at Christy Beach on Santa
Cruz Island for over 73 years starting with a report by Hewatt
(1946), observations by Straughan in the 1970’s(Straughan, 1982),
and our recent observations through 2012. However, overall our
analysis found populations of at least one species of upper beach
isopods remained at only two of the eleven (27%) of the sites
identified on the mainland coast before 1950 (Torrey Pines and
perhaps Laguna for which the early location was not specified).
From the middle period to the present, there are six other sites
with records of populations of these isopods spanning at least four
decades: Silver Strand State Beach (San Diego County)first sur-
veyed by Clark (1969), Horse Pastures [now called Crystal Cove
State Park, Orange County], Little Dume [actually Big Dume Cove,
Los Angeles County], Hope Ranch (Santa Barbara County) starting
with surveys by Patterson (1974), Arco [now called Haskell’s, Santa
Barbara County] and Isla Vista (Santa Barbara County)first sur-
veyed by Craig (1973). The estimated persistence of populations
first identified by surveys between 1969 and 1971 was six out of 18
(33%). For populations at sites first surveyed between 1996 and
1999, 10 out of 11 populations (91%) were detected in 2010 and
2011. The exception to this was the dramatic decline of Tylos
punctatus populations at Broad Beach (Zuma littoral cell)(see
above).
3.7. Range limits
The reported northern range limits for the southern isopod
species,Tylos punctatus, all fell within the Santa Barbaralittoral cell.
Hamner (1969)reported the northern range limit of T. punctatus on
beaches near the Santa Barbara wharf, which have been groomed
regularly since that report. In 1971,T. punctatus was collected eight
km further west at Hope Ranch by Patterson (1974), a record
verified by specimens archived at the Santa Barbara Museum of
Natural History. We re-surveyed the Hope Ranch site and ten other
sites with suitable upper beach habitat within 25 km (five east and
five west) between 1996 and 2010 without detecting T. punctatus.It
should be noted that Alloniscus perconvexus was present at a subset
of those sites, including Hope Ranch. The northernmost mainland
population of T. punctatus found in our current surveys was at
Rincon County Park in the Santa Barbara littoral cell. This result
indicates that the northern range limit of T.punctatus shifted
southward by 31 km between 1971 and 1996 (a shift equivalent to
8% of the California mainland range).
Fig. 3.Example of historical loss of beach habitat. The coastline of San Pedro and Long
Beach, California: (a) shortly after statehood in 1859, and (b) the same coastline decades
after port development (2007). The area includes at least two sites, San Pedro and Long
Beach and approximately 7 km of beach that formerly supported populations of Tylos
punctatus. Photographs courtesy of Google Earth and http://www.caltsheets.org/
Fig. 4.Example of recent alteration of beach habitat. The coastline at Broad Beach, Los
Angeles County in: (a) 2002 when Tylos puntatus abundance was estimated to be
714 m
-1 of shoreline, and (b) 2010 when Tylos puntatus was not detected in quanti-
tative sampling. The dry sand zone, coastal strand vegetation and connection between
the dunes and the intertidal zone visible in the earlier photograph are not evident in
2010. Photographs courtesy of the California Coastal Records Project.
D.M. Hubbard et al. / Estuarine, Coastal and Shelf Science xxx (2013) 1e96
Please cite this article in press as: Hubbard, D.M., et al., Local extirpations and regional declines of endemic upper beach invertebrates in
southern California, Estuarine, Coastal and Shelf Science (2013), http://dx.doi.org/10.1016/j.ecss.2013.06.017
3.8. Colonizations
Colonization or recovery events appear to be very limited for
these species in the study area (Fig.1). We found onlyfive instances
that were consistent with colonization of formerly unpopulated
sites (but which might have been associated with populations
below the detection limits of earlier surveys) in the records for
these isopods. There are only three sites where populations are
known to have colonized and persisted; all of which are located
within a few kilometers of sites that have apparently supported
persistent populations. In the San Diego area,Hayes (1969)found
neither isopod species in his surveys at Scripps Beach or Ocean
Beach.Hayes (1969)transplanted more than 1000 Tylos punctatus
to Scripps Beach in 1967.Straughan (1982)reported T. punctatus at
both Scripps Beach and Ocean Beach a few years later. We subse-
quentlycollected a few T. punctatus at the Scripps Beach site in 2011
but not in 2009 or 2010. Grooming resumed at that site in 2012,
despite its status as a marine reserve. Populations of both isopod
species have been documented for decades at Black’s Beach located
approximately one km to the north of Scripps Beach. At Ocean
Beach, however, neither isopod was detected in our surveys in 2009
or 2010. At the south end of the Santa Barbara littoral cell, during
years of heavy off-road vehicle use at Ormond Beach,Straughan
(1982)found no upper beach isopods present in multiple surveys
(1971e1978). In 1996, more than a decade after vehicles were
excluded from that site, we surveyed her site once and found
T. punctatus.In2009e2011, both species of isopod were present in
our surveys. Again, nearby populations of both species were pre-
sent on beaches at Mugu Naval Air Station located immediately to
the south. Lastly, on a beach on the University of California main
campus in Santa Barbara,Alloniscus perconvexus was not detected
in our quantitative surveys between 1996 and 2001. Our 2011
survey and subsequent observations indicate it recolonized this
beach, which is located w3 km downcoast from a population of
these isopods at Isla Vista. This recovery may be associated with
sand dynamics that resulted in widening of these bluff-backed
beaches in recent years (Barnard et al., 2012).
3.9. Population abundance
Estimated abundances of endemic upper beach isopods surveyed
in southern California reported in this and previous studies ranged
over three orders of magnitude from 21 to 31,000 individuals m
1 of
shoreline. Population abundance information is not available for the
early periods and the earliest abundance estimates we could find
were made in 1967 (San Diego).
For Tylos punctatus the highest abundance estimate ever re-
portedwas 31,000 individuals m
1 of shoreline at Carlsbad Beach in
the Oceanside littoral cell in the late 1960s (Hayes,1969). However,
T. punctatus was not detected in our surveysat that location in 2010,
2011 or 2012 after sandy upper beach habitat had been converted
to cobble by erosion. The highest abundance of T. punctatus recor-
ded in recent years was observed on Santa Cruz Island
(>20,000 individuals m
1 in 2011) (Fig. 2a). For the mainland coast,
the highest values of abundance of T. punctatus recorded in recent
years were <10,000 individuals m
1 (Fig. 2a). Peak abundance es-
timates ranging from 7000 to 9000 m
-1 were found at three sites
between 1996 and 2010, which were located in three different
littoral cells (Santa Barbara, Zuma and Oceanside) (Fig. 2a).
Recent peak estimates for population abundance of Alloniscus per-
convexus were higher than those obtained for Tylos punctatus on the
mainland coast, reaching maximum values of 20,920 individuals m
1
at Oil Piers and 11,075 individuals m
1 at Deer Creek, both in the Santa
Barbaralittoralcellin2010(Fig. 2b). Importantly, in the four major
southern littoral cells, population abundance of A. perconvexus did not
exceed 100 individuals m
1 at any site (Fig. 2b). All of the populations
with abundances >100 individuals m
1 of this species were found at
sites in the two northern littoral cells (Santa Barbara and Zuma)
(Fig. 2b).
Where these two isopod species co-occurred in earlier and our
surveys, an inverse relationship in abundancewas apparent (Fig. 5).
Differences in the mean abundance between the two species
increased significantly as the mean abundance of Tylos punctatus
increased. This relationship was significant for all surveys con-
ducted between 1969 and 2011 (r ¼0.870,n ¼19,p <0.001), and
also for the surveys conducted between 1996 and 2011 (r ¼0.773,
n ¼18,p <0.001). Although this result is consistent with compe-
tition between the two species, we could not adequately evaluate
potential mechanisms underlying this pattern due to a lack of
supporting experimental or observational data and the fragmen-
tation and restricted distribution of populations of both species in
the region.
4. Discussion
The high extirpation rates of populations of upper beach isopods
on the mainland coast of southern California over the last century
found by our analyses provide a compelling example of the
vulnerability of upper beach biota to habitat loss and alteration
associated with coastal development and beach management
practices. Our study also identified major gaps in distributions and
declines in abundance of two invertebrate species endemic to the
upper intertidal zones of sandy beaches. Our results for two species
of beach isopods on the southern California mainland strongly
support Brown’s (2000)predictions concerning the vulnerability of
populations of upper beach invertebrates, particularly those with
low dispersal abilities and low reproductive rates. They also sup-
port our hypothesis that a disproportionate loss and alteration of
upper intertidal zones of beaches in the study area due to devel-
opment, armoring, grooming and other factors has been associated
with declines in the diversity and distribution of upper intertidal
macroinvertebrates.
Endemic upper beach isopods may be sensitive indicators of
beach ecosystem conditions because of their life history attributes,
limited dispersal and habitat requirements (Brown, 2000). The
extensive loss of populations of both isopod species across the
southern California mainland coast is probably associated with
widespread anthropogenic stressors detailed in the study area
description, many of which disproportionately affect upper inter-
tidal habitats. For example, the majority of the 161 km of groomed
beaches are located in the Santa Monica and San Pedro littoral cells
where a major gap in isopod distributions now exists, despite the
Fig. 5.Abundance of Tylos punctatus (x-axis) and Alloniscus perconvexus (y-axis) at 18
sites where they co-occurred in samples between 1996 and 2011.
D.M. Hubbard et al. / Estuarine, Coastal and Shelf Science xxx (2013) 1e9 7
Please cite this article in press as: Hubbard, D.M., et al., Local extirpations and regional declines of endemic upper beach invertebrates in
southern California, Estuarine, Coastal and Shelf Science (2013), http://dx.doi.org/10.1016/j.ecss.2013.06.017
relatively wide sandy beaches (Orme et al., 2011). Although early
recordsarelimited for southernCalifornia, weconsider itlikelythat
populations of other species of invertebrates of the upper intertidal
beach with narrow habitat preferences and/or low dispersal abili-
ties (Table 1) have suffered comparable declines and fragmentation
of their distributions (e.g.Nagano, 1980 for tiger beetles).
Most of the currently known populations of these isopods occur
on unarmored beaches that lack routine beach grooming and have
limited vehicle access and minimal management manipulations
associated with recreation. These include areas requiring more
effort (hikes, stairs) for visitors or vehicles to access, a military base,
and California State Parks with high levels of resource protection.
The isolated but relatively undisturbed and lightly visited beaches
of the California Channel Islands appear to support persistent
populations of both species (Garthwaite et al.,1985) attesting tothe
abilityof small populationsof these species toremainviable. Onthe
mainland coast, many of the remaining populations of isopods
occur on narrow bluff-backed pocket beaches that retain sufficient
sand volumes and suitable upper beach habitat. These narrow
beaches also support species-rich assemblages of upper beach in-
vertebrates, suggesting these isopods may be useful as indicators of
biodiversity. Populations of isopods are also present on some bea-
ches backed by artificial rock revetments that are presently above
the reach of regular tidal influence.
Due to the strong influence of sediment transport and dynamics
associated with littoral cells (e.g.Griggs et al., 2005), we expect
connectivity will be much greater among populations of upper
beach biotawithin littoralcells than acrosslittoralcells. The 100 km
gapsnowpresentintherangesofthetwoisopods(Fig.1)ondensely
populated urban coast in the vicinity of metropolitan Los Angeles
(SantaMonicaandSanPedrolittoralcells)suggestthatdistributions
of these animals are now severely fragmented. The largest gaps
between all documented historic populations were roughly 30 km
onthe mainlandcoastfor bothspecies.Thehistoricgapswerelikely
smaller than 30 km if undocumented populations were present in
the study area. The large gaps and small number of adjacent popu-
lation pairs has resulted in reduced potential for connectivity be-
tween the northern and southern populations remaining in our
study area and within the Santa Monica and San Pedro littoral cells.
Beaches with high potential for connectivity or colonization from
knownpopulations(e.g.within10km)arenowmostlylimitedtothe
Santa Barbara and Zuma littoral cells. However, the low number of
colonization and re-colonization events we were able to document
inourdatasetdoesnotaugurwellfornaturalrecoveryofisopodson
mainland beaches, particularly in the four southern littoral cells.
Habitat fragmentation and connectivity of populations of these
and other upper beach species will be further affected by sea-level
rise associated with climate change. As sea level rises, the narrow
bluff-backed beaches where most of these populations persist in
the study area will have little potential for retreat. Only a small
fraction (<10%) of the 450 km of southern California coast will have
the potential to provide suitable upper beach habitat under a sce-
nario of 140 cm of sea-level rise by 2100 (Revell et al., 2011; NOAA,
2012). Most of the potential for shoreline retreat and restoration in
the region under this scenario appears to be in the eastern Santa
Barbara littoral cell, where as much as 12 km of relatively unde-
veloped shoreline might be able to accommodate retreat geo-
morphically if the economic and political elements of conservation
planning are achieved. Successful conservation strategies for
coastal endemic species such as these isopods and those in Table 1
will likelyrequire assisted migration, transplantation of species and
associated communities to new sites, and restoration of degraded
areas capable of accommodating sea-level rise.
Urbanized coastal southern California has been recognized as a
hotspot of endangerment and extinction for terrestrial flora and
fauna (e.g.Dobson et al.,1997). Biota of the upper beach and coastal
strand zones of this region appear to fit this pattern. Based on our
results, we suggest that populations of two beach endemic isopods,
Tylos punctatus and Alloniscus perconvexus,arenowfragmented and
declining across much of their historically occupied southern Cal-
ifornia range. Our estimates for the extirpation rates of these iso-
pods seem to be lower in the most recent period than in earlier
decades. However, there are far fewer extant populations and two
recent examples, including the armoring of one site (2006) and the
resumption of grooming at a designated marine reserve (2012),
suggest that the current coastal management framework is not
sufficient to protect the remaining populations of these isopods.
Given the prospects for continued population losses posed by hu-
man activities, coastal erosion, sea-level rise and climate change,
these two beach isopods could be considered imperiled species on
the southern California coastline.
Acknowledgments
We are very grateful to M. Clark, R. Garthwaite, W. Hamner, W.
Hayes, F.G. Hochberg, D. Pryor, D. Straughan, and S. Taiti for gener-
ouslysharingtheirrecords,expertiseandlong-termperspectiveson
the study animals and area. We would also like to thank L. Hurtado,
R. Wetzer, and J. Wright for their expert assistance. We gratefully
acknowledge our crew of student field and laboratory assistants for
their willing and cheerful help with field surveys and sample pro-
cessing. We thank California State Parks for permission to conduct
field surveys at numerous state beaches in the study area. We also
thank the University of California Natural Reserve System for
providing research access tothe Scripps Coastal Reserve, Santa Cruz
Island Natural Reserve and Coal Oil Point Natural Reserve for field
surveys.ThisresearchwassupportedbyfundingfromtheCalifornia
Sea Grant Program (Project R/ENV 210, including a Sea Grant
Traineeship to N. Schooler and Project R/MPA-24 through the Cali-
fornia Ocean Protection Council), the UCSB Coastal Fund, and the
Santa Barbara Coastal Long Term Ecological Research project (Na-
tional Science Foundation award no. OCE-0620276).
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