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Genetic similarity between Boccardia proboscidea from Western North America and cultured abalone, Haliotis midae, in South Africa

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Genetic similarity between Boccardia proboscidea from Western North America and cultured abalone, Haliotis midae, in South Africa

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South African cultured abalone, Haliotis midae, are commonly infested by the non-indigenous spionid polychaete, Boccardia proboscidea. This annelid species occurs naturally along the west coast of North America and around Japan, but has also been introduced in Hawaiʻi, Australia, New Zealand and perhaps the Iberian Peninsula. Reportedly, worms were inadvertently transported to South Africa on Haliotis rufescens imported from California in the late 1980s. To test this hypothesis, populations from six abalone farms on the west, south and east coasts of South Africa were compared with populations from California (Alamitos Bay and La Jolla), Washington State (False Bay Harbour) and British Colombia (Vancouver Island). Sequence data of 16S rRNA and cytochrome b (Cyt b) mitochondrial genes show a genetic similarity between worms from South Africa and the west coast of North America with identical haplotypes for each gene found among these populations. The data also indicate that worms were spread among farms in South Africa primarily through the transport of infested abalone.
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Genetic similarity between Boccardia proboscidea from Western North America and
cultured abalone, Haliotis midae, in South Africa
Carol A. Simon
a,
, Daniel J. Thornhill
b,c
, Fernanda Oyarzun
d,e
, Kenneth M. Halanych
b
a
Department of Zoology and Entomology, Rhodes University, Grahamstown 6140, South Africa
b
Department of Biological Sciences, Auburn University, 101 Rouse Life Sciences Building, Auburn University, Auburn, AL 36849, USA
c
Department of Biology, Bowdoin College, 6500 College Station Rd., Brunswick, ME 04011, USA
d
Friday Harbor Laboratories, University of Washington, Seattle, Box 351800, Seattle, WA 98195-1800, USA
e
Department of Biology, University of Washington, Seattle, Box 351800, Seattle, WA 98195-1800, USA
abstractarticle info
Article history:
Received 12 February 2009
Received in revised form 26 May 2009
Accepted 26 May 2009
Keywords:
Commercial shellsh
Invasive species
Mariculture
Shell-boring pest
South African cultured abalone, Haliotis midae, are commonly infested by the non-indigenous spionid
polychaete, Boccardia proboscidea. This annelid species occurs naturally along the west coast of North
America and around Japan, but has also been introduced in Hawai i, Australia, New Zealand and perhaps the
Iberian Peninsula. Reportedly, worms were inadvertently transported to South Africa on Haliotis rufescens
imported from California in the late 1980s. To test this hypothesis, populations from six abalone farms on the
west, south and east coasts of South Africa were compared with populations from California (Alamitos Bay
and La Jolla), Washington State (False Bay Harbour) and British Colombia (Vancouver Island). Sequence data
of 16S rRNA and cytochrome b(Cyt b) mitochondrial genes show a genetic similarity between worms from
South Africa and the west coast of North America with identical haplotypes for each gene found among these
populations. The data also indicate that worms were spread among farms in South Africa primarily through
the transport of infested abalone.
© 2009 Elsevier B.V. All rights reserved.
1. Introduction
Recently, increased attention has been paid to infestations of non-
indigenous species such as shell-boring polychaetes on commercially
harvested molluscs (Kuris and Culver, 1999; Bailey-Brock, 20 00; Read
and Handley, 2004; Bertrán et al., 2005; Radashevsky and Olivares,
2005; Vargas et al., 2005; Moreno et al., 2006; Sato-Okoshi et al.,
2008). These annelid worms may reduce the esh condition of
cultured molluscs through delayed growth rates and increased
mortality, thereby increasing production costs (e.g., Martin and
Britayev, 1998; Lleonart, 2001; Simon et al., 2006). Furthermore,
animal transportation for aquaculture is considered a leading vector
for introduction of non-indigenous marine species, including poly-
chaetes, which are inadvertently transferred with their hosts (Naylor
et al., 2001). Thus, putative origins of some non-indigenous species
may be inferred based on the origin of imported aquaculture stocks
(Bailey-Brock and Ringwood, 1982; Kuris and Culver, 1999; Bailey-
Brock, 2000; Radashevsky and Olivares, 2005; Moreno et al., 2006).
However, when a non-indigenous pest living on cultured species does
not infest economically important shellsh in its native range,
establishing its putative origin becomes more problematic. In such
instances, vectors of transportation other than the importation of
organisms for aquaculture, such as ballast water (Carlton and Geller,
1993; Carlton, 1996), must also be considered.
South Africa, the second largest supplier of cultured abalone in the
world, with just less than 850 MT exported in 2008 (Troell et al., 2006;
Wayne Barnes, Abalone Farmers Association of Southern Africa, pers.
comm.). Increased infestation of abalone by spionid polychaetes has
negatively impacted some farms. In one instance, approximately
500,000 abalone were culled at a single farm due to spionid
infestations (R. Clark, Wild Coast Abalone, pers. comm.). The cultured
abalone, Haliotis midae Linnaeus 1758, in South Africa are infested by a
number of spionids, including indigenous Dipolydora capensis (Day
1955) and Polydora hoplura Claparède 1870, and by non-indigenous
Boccardia proboscidea Hartman 1940 which were rst reported in
South Africa in 2004 (Simon et al., 2006; Simon and Booth, 2007). To
date, B. proboscidea has not been detected in naturally occurring
shellsh in South Africa (Simon et al., in press).
The known native range of B. proboscidea includes Japan and the
western coast of North America, from British Columbia to southern
California, with unconrmed records extending the distribution even
further south (Hartman, 1940; Woodwick, 1963; Fauchald, 1977;
Petch, 1995; Sato-Okoshi, 2000; F. X. Oyarzun et al., unpublished data).
In its native range, B. proboscidea occupies a wide ecological niche
burrowing into soft rock and in crevices, among encrusting algae and
Aquaculture 294 (2009) 1824
Corresponding author. Current address: Department of Botany and Zoology,
Stellenbosch University, Matieland, Private Bag X01, Stellenbosch 7602, South Africa.
Tel.: +27 21 808 3068 ; fax: +27 21 808 2405.
E-mail addresses: csimon@sun.ac.za (C.A. Simon), thornhill.dan@gmail.com
(D.J. Thornhill), foyarzun@u.washington.edu (F. Oyarzun), ken@auburn.edu
(K.M. Halanych).
0044-8486/$ see front matter © 20 09 Elsevier B.V. All rights reserved.
doi:10.1016/j.aquaculture.2009.05.022
Contents lists available at ScienceDirect
Aquaculture
journal homepage: www.elsevier.com/locate/aqua-online
in muddy and sandy sediments (Hartman, 1940; Woodwick, 1963;
Gibson et al., 1999). Although it occurs on gastropod shells and mud
deposits in the crevices of Crassostrea gigas Thunberg 1793 shells, B.
proboscidea has never been recorded on abalone shells in its natural
range (Woodwick, 1963; Blake and Evans, 1973; Martin and Britayev,
1998; Sato-Okoshi, 2000). B. proboscidea has been introduced to
Hawai i with cultured oysters (Bailey-Brock, 2000) and to Australia via
either ballast water or mariculture (where it has now spread into
natural environments and cultured molluscs; Blake and Kudenov,
1978; Lleonart, 2001; Hewitt et al., 2004; Sato-Okoshi et al., 2008). It
has also been recorded on abalone in New Zealand (Read, 2004) and
living amongst Zostera, calcareous algae, Mytilus and in rock crevices
on the Iberian Peninsula (Martínez et al., 2006).
Over the last 70 years, South African aquaculturists have imported
several bivalve and gastropod species that could have served as vectors
for B. proboscidea, from Europe, California and Chile (Robinson et al.,
2005). For example, the abalone, Haliotis rufescens Swainson 1822, was
imported to Saldanha Bay from California in the 1980s; however, all
individuals died within a month and were never re-imported (Grifths
et al.,1992). Additionally, since the 1970s, the bulk of the oyster industry
has been maintained by spat of C. gigas imported regularly from Chile,
the United Kingdom and France (Grifths et al., 1992; Robinson et al.,
2005). Based solely on the history of molluscan imports to South Africa
and the known distribution of B. proboscidea, it is impossible to
determine the source or vector of transportation of the South African
B. proboscidea population. As a result, alternative approaches are
required to address this question.
In this study, we utilized a molecular approach based on 16S rRNA
and cytochrome b(Cyt b) mitochondrial gene sequence data to infer the
source population of non-indigenous B. proboscidea infesting farmed H.
midae in South Africa. The west coast of the United States was
hypothesized to be the source population of B. proboscidea,asitwas
the source of the abalone suspected to have introduced this infestation.
Previous studies have successfully used molecular techniques to
establish the (presumed) origin of non-indigenous species, including
spionids (Bastrop et al., 1998; Bastrop and Blank, 2006) and molluscs
(Dupont et al., 2003; Martel et al., 2004; McGlashan et al., 2008).
Therefore, patterns of evolutionary relatedness based on Bayesian and
coalescent analyses may elucidate whether infesting B. proboscidea in
South Africa originated on the west coast of the US.
2. Methods and materials
2.1. Data collection
B. proboscidea was collected from infested abalone from South
African farms near Saldanha Bay on the west coast (Jakobsbaai Sea
Products [Pty] Ltd), in Walker Bay on the south coast (Abagold [Pty]
Fig. 1. Localities of collection sites of Boccardia proboscidea and the major harbours in South Africa with the ow direction of the predominant currents indicated. Localiti es included:
JB (Jakobsbaai Sea Products [Pty] Ltd), Ab (Abagold [Pty] Ltd), AF (Atlantic Fishing), RB (Roman Bay Sea Farm [Pty] Ltd), IJ (Irvin and Johnson Ltd), and HH (Wild Coast Abalone [Pty]
Ltd at Haga Haga).
19C.A. Simon et al. / Aquaculture 294 (2009) 1824
Ltd, Atlantic Fishing, Roman Bay Sea Farm [Pty] Ltd, and Irvin and
Johnson Ltd), and north of Haga Haga on the east coast (Wild Coast
Abalone [Pty] Ltd) (Fig. 1; see Table 1 for the codes that will be used
throughout the paper) of South Africa from March to April 2007 and
preserved in 70% ethanol. DNA was extracted using a Qiagen DNeasy®
Tissue Kit according to the manufacturer's instructions. An approxi-
mately 376 bp fragment of the cytochrome b(Cyt b) mitochondrial
gene (Table 1) was amplied using the primers of Boore and Brown
(2000):Cyt b424F(5-GGW TAY GTW YTW CCW TGR GGW CAR AT-
3) and Cyt b876R(5-GCRT AWG CRA AWA RRA ART AYC TC-3),
with the cycling conditions: initial denaturation 94 °C, 3 min; 40
cycles of 94 °C, 30 s, annealing 45 °C, 30 s, extension 72 °C,1 min; nal
extension 72 °C, 7 min. An approximately 439 bp fragment of the 16S
rRNA mitochondrial gene (Table 1) was amplied using the primers of
Palumbi et al. (1991):16SarL(5-CGC CTG TTT ATC AAA AAC AT-3)
and 16SbrH(5-CCG GTC GAA CTC AGA TCA GCT-3), with the cycling
conditions: initial denaturation 94 °C, 3 min; 40 cycles of 94 °C, 30 s,
annealing 48 °C, 30 s, extension 72 °C, 1 min; nal extension 72 °C,
7 min. All PCR products were veried by 1× sodium borate (SB) agarose
gel electrophoresis. 16S PCR products were gel-puried using the
QIAquick® PCR Purication Kit, while Cyt bPCR products were puried
with the MontagePCR Filter Units (Millipore). Puried PCR products
were bidirectionally sequenced using Genome LabQuick Start Mix
(Beckman Coulter) on a Beckman CEQ 8000 using the same primers as
for PCR, with one exception: Cyt b876Rwas replaced by Cyt bBP 876R
(5-RAA WAR RAA GTA TCA YTC AGG-3). Sequences were edited in
Sequencher v4.6 (Gene Codes Corporation, Ann Arbor, Michigan). The
Cyt bsequences were translated using the Drosophila mitochondrial
code in McClade v4.06 (Maddison and Maddison, 2003) to ensure that
stop codons were not present. All sequences were deposited in GenBank
(Accession nos. FJ434476FJ434482, FJ434486; Table 2).
Available sequence data for B. proboscidea from the western coast
of North America included free-living samples from the intertidal of
Vancouver Island (Accession nos. FJ434483FJ434485 and FJ434487
FJ434489), California and Washington State (Accession nos.
FJ972541FJ972569, see Appendix A). Initial data collection revealed
that Cyt bsequences were more variable than 16S, and therefore more
informative to investigate the putative source population. Therefore,
subsequent data collection efforts emphasized collecting Cyt b, rather
than 16S, sequence data.
2.2. Data analysis
Sequence data from South Africa was compared to North American
data to determine whether haplotypes were shared between regions.
Sequences were aligned using Clustal W (Thompson et al., 1994)in
Bioedit (Hall, 1999). Sequence data were not concatenated as 16S data
of the South African samples possessed no variation and thus provides
limited information about the South African samples. Thus, analyses
herein focused on Cyt b. Alignments are provided in TreeBase (www.
TreeBase.org).
To further explore the relationship between B. proboscidea
populations, phylogenetic relationships among haplotypes were
estimated using Bayesian inference in MrBayes v3.1 (Ronquist et al.,
2005). Based on the availability of sequence data, Marenzallaria
neglecta Sikorski and Bick, 2004 (GenBank Accession no. DQ309261)
was selected as the outgroup for Cyt banalyses, while Dipolydora
giardi (Mesnil, 1896) (GenBank Accession no. DQ779632) was
selected for 16S analyses. The HKY + Γmodel of substitution, as
suggested by a hierarchical Likelihood Ratio Test (hLRT) in MrMo-
deltest v2.2 (Nylander, 2004), was implemented for Cyt bsequence
data. Two sets of four chains (3 hot, 1 cold) were run simultaneously to
1.0 × 10
6
generations and sampled every 100 generations. In initial
analysis using M. neglecta as an outgroup, the rst 1000 burn-in
generations were discarded. Burn-in values were based on the
convergence of likelihood scores in the chains. None of the nodes
was well-supported. Further analysis, using only the unique haplo-
types, was run for 2 × 10
6
generations and sampled every 100
generations without selection of an outgroup. The rst 305 burn-in
generations were discarded. Phylogenetic relationships were also
estimated from 16S sequence data via Bayesian analysis implementing
the K80+ I model of substitution suggested by hLRT in MrModeltest
v2.2 (Nylander, 2004). Two sets of four chains (3 hot, 1 cold) were run
simultaneously to 2× 10
6
generations and sampled every 100
generations, with the rst 450 burn-in generations being discarded.
In all cases, 50% majority-rule consensus trees were computed.
Finally, haplotype networks representing intraspecic relation-
ships were constructed in TCS v1.21 (Clement et al., 2000) with gaps
treated as missing data with other options set to their default values.
Connectivity levels were examined at 92%95% for Cyt bsequence
data and at 95% for 16S. Reticulations between haplotypes were
resolved following Crandall et al. (1994).
3. Results
Forty-eight individuals from South Africa were sequenced for Cyt b
(376 bp) and 26 for 16S (439 bp) resulting in seven Cyt bhaplotypes
but only one 16S haplotype (Table 2). For Cyt bthere was a single
haplotype that represented 40 individuals (haplotype 1), and four
haplotypes (n=6) that each differed from this haplotype by a single
nucleotide substitution (Table 2;Fig. 2). The Cyt bgene had ve (1.3%)
variable characters, of which two (0.5%) were parsimony informative.
The percentage GC content was 47.8% for Cyt band 44.9% for 16S.
With the inclusion of sequences from North American sites, there
were 111 and 50 sequences for Cyt band 16S genes, respectively. In
this expanded dataset, the Cyt bgene had 37 (9.8%) variable
characters, of which 19 (5.1%) were parsimony informative, whereas
GC content was 47.5%. For the 16S gene, there were eleven (2.5%)
variable characters, of which three (0.7%) were parsimony informa-
tive, and GC content was 44.8%. All characters could be aligned
Table 2
Distribution of South African haplotypes, with respective accession numbers, at the six
farms sampled.
Haplotype
names
Population (farm) Total
West coast South coast East coast
Accession number
JB Ab AF RB IJ HH
Cytochrome b
1 FJ434476 6 8 8 7 7 4 40
2 FJ434477 1 1
3 FJ434478 1 1 2
4 FJ434479 1 1
5 FJ434480 1 1
6 FJ434481 1 1 2
7 FJ434482 1 1
16S
A FJ434486 8 2 1 7 6 2 26
Table 1
Collection locations and number of individuals sequenced per sampling site.
Locality Code Number of 16S
replicates
Number of Cyt b
replicates
West coast
Jakobsbaai Sea Products [Pty] Ltd JB 8 6
South coast
Abagold [Pty] Ltd Ab 2 10
Atlantic Fishing AF 1 10
Roman Bay Sea Farm [Pty] Ltd RB 7 10
Irvin and Johnson Ltd IJ 6 8
East coast
Wild Coast Abalone [Pty] Ltd HH 2 4
Total 26 48
20 C.A. Simon et al. / Aquaculture 294 (2009) 1824
unambiguously for both genes. The maximum uncorrected genetic
distances between haplotypes were p=0.01258 and p= 0.04740 for
16 S and Cyt b, respectively.
3.1. Phylogenetic analyses
Bayesian analysis of Cyt bwith M. neglecta as the outgroup
produced a clade which included all samples from South Africa,
Washington (False Bay Harbour), Canada (Vancouver Island), and
three samples from California (Alamitos Bay). Most of the Californian
samples were outside of this clade. However, support for these groups
was poor, with posterior probabilities of 0.50 and 0.64 for the
geographically mixed and California clades, respectively (data not
shown). When reanalysed with only the 32 unique haplotypes (and
excluding the outgroup due to its extreme branch length), nodal
support increased to a posterior probability value of 1.00 (Fig. 2).
Bayesian analysis of 16S data (including 14 unique haplotypes and
outgroup) produced a tree with no resolution (data not shown). This
difference in resolution between 16S and Cyt bmitochondrial genes
has been previously observed in marine invertebrates (e.g. Wilson
et al., 2007; Hunter and Halanych, 2008), with 16S being consistently
less variable than Cyt b. The patterns observed here highlight the
importance of selecting the appropriate gene for the question being
addressed in intraspecic genetic studies.
3.2. Coalescent analyses
Consistent with relationships inferred from the Cyt bhaplotype-only
Bayesian analysis, coalescent analysis of Cyt bby TCS at a 95%
connectivity level generated two haplotype networks with a total of
29 haplotypes. When the connectivity level was reduced to 92%, the two
networks fused into a single haplotype network. For the sake of clarity,
hereinwe focus on results using only the 95% connectivelylevel. The two
resulting networks, designated Networks 1 and 2 (Fig. 3a and b),
corresponded to the mixed clade and California grouping generated by
the Bayesian analysis. In Network 1, a single haplotype was common to
South Africa (n=40), Vancouver Island (n=5), Washington (n=3),
and Alamitos Bay (California, n=2) (Fig. 3a). This network also
included six Cyt bhaplotypes (1 or 2 individuals per haplotype) unique
to South Africa (Fig. 3a). Populations at Abagold [Pty] Ltd (Ab) and
Roman Bay Sea Farm [Pty] Ltd (RB) each had two unique haplotypes,
while one haplotype each was shared by populations at Atlantic Fishing
(AF), RB, and Irvin and Johnson Ltd (IJ), respectively (Tab le 2). Three
more haplotypes represented specimens from California (Alamitos Bay),
Vancouver Island, and Washington State (Fig. 3). Network 2 comprised
19 haplotypes composed exclusively of individuals from southern
California (Alamitos Bay and La Jolla; Fig. 3b).
As mentioned previously, sequence diversity of 16S ribosomal
mtDNA was low compared to that of Cyt bmtDNA. Parsimony network
analysis of all sequences resulted in a single network with 10 haplotypes
(Fig. 3c). The South African haplotype was common to both California
(Alamitos Bay) and Washington State. The difference in the number of
haplotypes generated by Bayesian and parsimony network analysis is a
consequence of missing data at the sequence ends and the way in which
these data are treated by the different analyses (Joly et al. 2007).
4. Discussion
Molecular analyses of two mitochondrial genes suggest that B.
proboscidea infestations on South African abalone farms were
genetically similar to worms from the west coast of North America.
Identical 16S and Cyt bhaplotypes were found in both South Africa
and the North American west coast, indicating a common genetic
history between these geographically disparate locations.
Fig. 2. Bayesian inference phylogeny of unique Boccardia proboscidea Cyt bmtDNA haplotypes. The tree was rooted using the outgroup Marenzallaria neglecta in analyses including all
sampled individuals. Posterior probabilities were obtained from analyses that included only ingroup taxa, as the number of substitutions along the outgroup branch appeared to have
saturated a number of informative nucleotide positions. Nodal support values (0.5) indicated as a posterior probability next to the relevant nodes. Haplotype names correspond to
the results presented in Table 2 for South African samples and Appendix A for American samples. Names including lower case letters indicate that that haplotype has data missing
relative to the primary haplotype and are considered a single haplotype in the parsimony analysis (see Fig. 3).
21C.A. Simon et al. / Aquaculture 294 (2009) 1824
4.1. Putative origin of infestation
The most common Cyt bhaplotype observed in South Africa is
widespread across the North American Pacic coast. This haplotype
may, however, also occur in other unsampled B. proboscidea
populations. Although B. proboscidea is native to Japan (Sato-Okoshi,
2000), to the best of our knowledge, South Africa does not import live
Japanese shellsh. Furthermore 16S data show that Vancouver Island
samples are distinct from more southern samples in North America
suggesting that Japanese samples are also likely to be distinct. While
conrmed reports of these worms occurring in aquaculture stocks in
either Europe or Chile (Ruellet, 2004; Moreno et al., 2006)are
lacking, there are unconrmed reports of this worm occurring in
claybeds in the intertidal of Harwich (Essex, England, T. Worsfold,
pers. comm.) and among Sabellaria alveolata tubes in Clarach
(Ceregidon, Central Wales, V. Cole, pers. comm.). These reports are
of particular interest as oyster spat imported to South African farms
were sourced from suppliers situated close by (A. Antonin, Striker
Oyster Fishing Company, pers. comm.). Thus, until these reports are
conrmed and other populations are more comprehensively
sampled, we cannot denitely rule out alternative origins for the
South African populations. For instance, it is possible that the South
African B. proboscidea populations are a secondary introduction from
either European or Chilean aquaculture stocks that were originally
Fig. 3. (a) and (b) TCS networks of B. proboscidea based on Cyt bmtDNA haplotypes using the 95% connectivity level. Networks 1 and 2 correspond with the mixed clade and
Californian group of haplotypes, respectively (see Fig. 2). (c) TCS networks of B. proboscidea based on 16S rRNA data using the 95% connectivity level. Sampled haplotypes are
indicated by shaded circles; missing or unsampled haplotypes are indicated by black dots. Each branch indicates a single mutational difference. Circle size is proportional to observed
haplotype frequency. Haplotypes are shaded according to the geographic region from which the sample was collected (see legend). Haplotype names correspond to the results
presented in Table 2 for South African samples and Appendix A for American samples.
22 C.A. Simon et al. / Aquaculture 294 (2009) 1824
infected by North American shellsh, but where infestation has gone
undetected. However, given the notable genetic variation observed
among the natural western North American populations, it seems
unlikely that Chilean or European populations would have a genetic
signature similar to those of central California if they are in fact native
populations.
4.2. Current biogeography of haplotypes on South Africa
Populations from farms on the west and east coasts of South Africa
were each represented only by the common Cyt bhaplotype while
those from the farms in the Walker Bay area were represented by two
to four haplotypes. This difference in genetic diversity between farms
may be an artefact of uneven sampling. There were only four and six
samples from Wild Coast Abalone [Pty] Ltd (HH) and Jakobsbaai Sea
Products [Pty] Ltd (JB), respectively, compared to eight or ten from the
other four farms. Alternatively, if this diversity is real, the populations
in the South coast area may 1) be the oldest, 2) have been subjected to
more than one introduction, 3) have had the greatest haplotype
diversity at the time of introduction, or 4) have experienced fewer
population bottlenecks since introduction. Of course, several of these
factors could have worked in concert to produce the current
biogeography.
The genetic similarity between farms suggests that worms are
ultimately derived from the same source. These animals have
planktotrophic larvae that could potentially be released through the
seawater system and serve as a vector for dispersal to other farms.
However, B. proboscidea has not yet been detected in the surrounding
natural environment (Simon, et al., in press). A more plausible
explanation for genetically similar infestations on multiple farms is
that the worms have been spread primarily through the movement of
abalone between farms (cf., Dupont et al., 2003; McGlashan et al.,
2008).
4.3. Possible vectors of transportation
There has been a signicant increase in the incidence of marine
biological invasions as the number of human-mediated vectors,
particularly shipping ballast water and aquaculture, has increased
(e.g., Carlton and Geller, 1993; Carlton, 1996; Naylor et al., 2001). H.
rufescens, which occurs in overlapping distribution ranges with B.
proboscidea (Woodwick, 1963), were imported on a single occasion to
Saldanha Bay from California (Grifths et al., 1992). Although B.
proboscidea has not been recorded on H. rufescens, it has been
recorded on other gastropods and sediment (Woodwick, 1963) which
may have been inadvertently transported with the abalone. By
contrast, South African aquaculturists regularly import the spat of C.
gigas, a known host of B. proboscidea (Bailey-Brock, 2000; Sato-
Okoshi, 2000), from Chile, the United Kingdom and France (Robinson
et al., 2005). While this polychaete has not been recorded from Chile
or France (Ruellet, 2004; Moreno et al., 2006) there are unconrmed
records of this species from the United Kingdom (see above). Spat
larger than 25 mm have been imported to South Africa from the
United Kingdom where they would have been exposed to the natural
environment before transport; such spat are also large enough to host
spionid larvae or juveniles (A. Antonin, Striker Oyster Fishing
Company, pers. comm.). Imported oyster spat may therefore have
been an alternative or additional vector for the introduction of this
species.
5. Conclusions: implications for mariculturists
Several studies (e.g., Kuris and Culver, 1999; Dupont et al., 20 03;
Martel et al., 2004; Moreno et al., 2006; McGlashan et al., 2008;this
study) have raised important issues concerning the management
and movement of aquaculture stocks and their pests. These include
the infestation of naturally occurring molluscs by non-indigenous
species that escape from aquaculture facilities, the spread of non-
indigenous species among farms and the negative economic impact
that they have on cultured shellsh. Simply inspecting molluscs for
epibionts before or immediately after moving between facilities
(both international and local) might not be enough. For example,
many molluscs are infested by non-problematic spirorbid worms
which build calcium tubes on the surface of the shell. Empty
spirorbid burrows often provide a refuge for Polydora-type larvae
(Lleonart, 2001; C. A. Simon pers. obs.). These larvae would easily be
missed during a perfunctory inspection for epibionts and may
therefore go undetected during a limited quarantine period. Regular
and intensive examination of mollusc stocks is imperative to detect
the presence of potentially problematic organisms. These considera-
tions are especially important when stocks are transported around
the world.
Acknowledgements
This work was funded by the National Research Foundation and
Marine and Coastal Management of South Africa (Frontier Program
for Mariculture). All authors contributed to the generation and
analyses of data and the preparation of the manuscript. Special
thanks are due to A.R. Mahon for supplying us with North American
B. proboscidea sequences and T. MacDonald, A. Mouton, and abalone
farmers for supplying the worms. Helpful discussions and comments
on the manuscript were provided by A.R. Mahon, S.R. Santos, G.
Zardi, B. Jansen van Vuuren and M.H. Villet. USA National Science
Foundation funds are gratefully acknowledged (EAR-0120646, OCE-
0425060). This work is AU Marine Biology Program contribution
#53.
Appendix A
Haplotype names and accession numbers of sequences of North
American samples provided by A. Mahon (haplotypes 810; C, E and F)
and F. Oyarzun. Localities: Al, Ca = Alamitos Bay, California; Lj, Ca = La
Jolla, California; FBH, Wa = False Bay Harbour, Washington; Wl, Va =
Witty's Lagoon, Vancouver Island, Canada.
Cytochrome b16S
Haplotype
name
Locality Accession
number
Haplotype
name
Locality Accession
number
1 Al, Ca; FBH,
Wa
FJ972548 A Al, Ca; FBH,
Wa
FJ972541
8 WL, Va;
FBH, Wa
FJ434483;
FJ972549
B Al, Ca FJ972542
9 WL, Va;
FBH, Wa
FJ434484;
FJ972550
C WL, Va FJ434487
10 WL, Va FJ434485 D Al, Ca FJ972543
11 Al, Ca; Lj, Ca FJ972551 E WL, Va FJ434488
12 Lj, Ca FJ972552 F WL, Va FJ434489
13 Al, Ca FJ972553 G FBH, Wa FJ972544
14 Al, Ca FJ972554 H FBH, Wa FJ972545
15 Al, Ca FJ972555 J Al, Ca FJ972546
16 Lj, Ca FJ972556 K Lj, Ca FJ972547
17 Al, Ca FJ972557
18 Al, Ca FJ972558
19 Al, Ca FJ972559
20 Al, Ca FJ972560
21 Al, Ca FJ972561
22 Lj, Ca FJ972562
23 Lj, Ca FJ972563
24 Al, Ca FJ972564
25 Al, Ca; Lj, Ca FJ972565
26 Al, Ca FJ972566
27 Lj, Ca FJ972567
28 Lj, Ca FJ972568
29 Lj, Ca FJ972569
23C.A. Simon et al. / Aquaculture 294 (2009) 1824
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24 C.A. Simon et al. / Aquaculture 294 (2009) 1824
... B. proboscidea has become a pest to abalone farms in South Africa since 2004 when it was first observed burrowing into cultured abalone (Simon et al., 2009). The introduced B. proboscidea presumably originated from the North American Pacific Coast where it is found in the wild benthos (Hartman, 1940(Hartman, , 1941Jaubet et al., 2018;Simon et al., 2009), although the species is now widely distributed throughout the world (Canada, Australia, New Zealand, Argentina, South Africa, Asia, and Europe) (Radashevsky et al., 2019). ...
... B. proboscidea has become a pest to abalone farms in South Africa since 2004 when it was first observed burrowing into cultured abalone (Simon et al., 2009). The introduced B. proboscidea presumably originated from the North American Pacific Coast where it is found in the wild benthos (Hartman, 1940(Hartman, , 1941Jaubet et al., 2018;Simon et al., 2009), although the species is now widely distributed throughout the world (Canada, Australia, New Zealand, Argentina, South Africa, Asia, and Europe) (Radashevsky et al., 2019). The presumed origins of introduced mud worms are, however, often based on circumstantial evidence such as documented movement of shellfish stock and the first described locations of mud worm infestations. ...
... Researchers are increasingly using molecular markers to compare the genetic structure of introduced mud worms to those in other regions (e.g., comparing mtDNA sequences) (Rice et al., 2018;Simon et al., 2009;Williams, 2015). These genetic tools, which Martinelli et al. (2020) leveraged to identify the Washington State Polydora spp. in 2017, will be essential to establish the possible origin(s) of the newly identified Washington mud worms. ...
Article
In 2017, Polydora websteri, a shell‐boring spionid polychaete worm and cosmopolitan invader, was identified for the first time in Washington State. Shell‐boring Polydora spp. and related shell‐boring spionid polychaetes (e.g., Dipolydora spp., Boccardia spp.), colloquially known as mud worms or mud blister worms, live in burrows within the shells of calcareous marine invertebrates, reducing the host's shell integrity, growth, survivorship and market value. Mud worms have a long history of impacting shellfish aquaculture industries worldwide by devaluing products destined for the half‐shell market and requiring burdensome treatments and interventions to manage against infestation. Here, we explore the risks of mud worms to the historically unaffected aquaculture industry in Washington State. This mini‐review is intended to inform shellfish stakeholders by synthesizing the information needed for immediate action in Washington State. We review the recent documentation of Polydora spp. in Washington State, discuss their history as pest species globally, summarize mud worm life history, and discuss effective control strategies developed in other infested regions. Finally, we review existing regulations that could be leveraged by stakeholders to avoid introduction of mud worms into uninfested areas of Washington State.
... Boccardia proboscidea Hartman, 1940 was originally described from northern California (see Radashevsky & Harris, 2010;Fauchald et al., 2011;Figs 1, 2A) and later widely reported from the Pacific coast of North America, from British Columbia, Canada, south to southern California, USA (Hartman, 1940(Hartman, , 1941(Hartman, , 1944(Hartman, , 1954Berkeley & Berkeley, 1950, 1952Hartman & Reish, 1950;Woodwick, 1963Woodwick, , 1977Reish, 1971;Light, 1977Light, , 1978Hobson & Banse, 1981;Dorsey et al., 1983;, and also in Japan (Imajima & Hartman, 1964;Sato-Okoshi, 2000;Abe et al., 2019a, b), Korea (Paik, 1975(Paik, , 1989, and China (Yang & Sun, 1988;Sun, 1994;Zhou et al., 2010). It is considered as an introduced species in Australia, Tasmania and New Zealand (Pollard & Hutchings, 1990;Jones, 1991;Hewitt et al., 2004;Read, 2004;Sliwa et al., 2009), Hawaii (Bailey-Brock, 2000, South Africa (Simon & Booth, 2007;Simon et al., 2009Simon et al., , 2010aMead et al., 2011), Europe (Martínez et al., 2006;Hatton & Pierce, 2013;Kerckhof & Faasse, 2014;López & Richter, 2017;Spilmont et al., 2018), and Argentina (Diez et al., 2011;Jaubet et al., 2011;Radashevsky, 2011;Jaubet et al., 2013Jaubet et al., , 2015Jaubet et al., , 2018. Simon et al. (2009) reported the first sequence data of two mitochondrial genes (16S rDNA and cytochrome b, Cyt b) for B. proboscidea and showed a genetic similarity between worms from South Africa and the Pacific coast of North America. ...
... It is considered as an introduced species in Australia, Tasmania and New Zealand (Pollard & Hutchings, 1990;Jones, 1991;Hewitt et al., 2004;Read, 2004;Sliwa et al., 2009), Hawaii (Bailey-Brock, 2000, South Africa (Simon & Booth, 2007;Simon et al., 2009Simon et al., , 2010aMead et al., 2011), Europe (Martínez et al., 2006;Hatton & Pierce, 2013;Kerckhof & Faasse, 2014;López & Richter, 2017;Spilmont et al., 2018), and Argentina (Diez et al., 2011;Jaubet et al., 2011;Radashevsky, 2011;Jaubet et al., 2013Jaubet et al., , 2015Jaubet et al., , 2018. Simon et al. (2009) reported the first sequence data of two mitochondrial genes (16S rDNA and cytochrome b, Cyt b) for B. proboscidea and showed a genetic similarity between worms from South Africa and the Pacific coast of North America. reviewed the records of the species and sampled in search of worms along the Pacific coast of North and Central America. ...
... Green circles and a question mark -specimens sequenced in the present study (see Table 1). Blue circles -specimens from South Africa, Pacific Canada, and the USA sequenced by Simon et al. (2009Simon et al. ( , 2019, and Pacific USA sequenced by . Yellow circles -adults identified based on the morphology only (see Table S1). ...
Article
Full-text available
The spionid polychaete Boccardia proboscidea Hartman, 1940 is a tube-dweller and shell/stone-borer widely occurring in temperate waters across the world and considered invasive in many areas. It was originally described from California, USA, and later reported from Pacific Canada, the Asian Pacific, Australia, New Zealand, Argentina, South Africa, and northern Europe. The Bayesian inference analysis of sequence data of three gene fragments (836 bp in total) of the mitochondrial 16S rDNA, nuclear 28S rDNA, and Histone 3 has shown that individuals from the Pacific coasts of Canada and the USA, Argentina, Australia, South Africa, the United Kingdom, and Mediterranean France were genetically very similar (maximal average p-distance value, 0.49%, was between 16S rDNA sequences). We consider these individuals to be conspecific and report the earliest records of B. proboscidea from the UK and a possible first Mediterranean record in the Gulf of Lion. The high 16S haplotype diversity of B. proboscidea detected in the north-eastern Pacific suggests a native distribution for the species in the northern Pacific and subsequent introductions through human activities to other parts of the world. The histories of these introductions are reviewed and the hypotheses about times and places of introductions are updated.
... Moreno et al. 2006). This is particularly problematic in South Africa where the oyster industry relies on the movement of stock between nursery and grow-out facilities which may be in different biogeographical regions (Haupt et al. 2010b;Williams et al. 2016; see also Simon et al. 2009). For example, it was demonstrated that Boccardia proboscidea Hartman, 1940, Polydora hoplura Claparède, 1870 and Polydora neocaeca Radashevsky & Williams, 1999 were spread among farms in South Africa that are separated by two or more biogeographic breaks (Fig. 1) by the movement of infested abalone and oysters (Simon et al. 2009;Williams et al. 2016;Malan et al. 2020). ...
... This is particularly problematic in South Africa where the oyster industry relies on the movement of stock between nursery and grow-out facilities which may be in different biogeographical regions (Haupt et al. 2010b;Williams et al. 2016; see also Simon et al. 2009). For example, it was demonstrated that Boccardia proboscidea Hartman, 1940, Polydora hoplura Claparède, 1870 and Polydora neocaeca Radashevsky & Williams, 1999 were spread among farms in South Africa that are separated by two or more biogeographic breaks (Fig. 1) by the movement of infested abalone and oysters (Simon et al. 2009;Williams et al. 2016;Malan et al. 2020). Once established on farms, introduced worms may spread further when they escape from the farms, infest indigenous molluscs and disperse via the movement of larvae (Moreno et al. 2006;Williams et al. 2016). ...
Article
Polychaete worms of the Polydora-complex (commonly referred to as polydorins) include some of the most common pests of cultured molluscs. Modern culture of molluscs, particularly oysters, is associated with large-scale movement of stock which facilitates movement of polydorins either as “hitchhikers” on the transported molluscs or in the packaging. In 2009, a species identified as Polydora cf. ciliata Johnston, 1838 was reported from oysters in a culture facility in Port Elizabeth, South Africa. Since then, more specimens of this species were recorded on farmed oysters from Namibia, Kleinzee and Paternoster on the west coast of South Africa, but tentatively reidentified as Polydora cf. websteri Hartman in Loosanoff and Engle, 1943 based on morphology and limited genetic evidence. The main aim of this study is therefore to clarify the identity of these specimens by integrating morphological and genetic (mitochondrial COI, Cyt b and nuclear 18S rRNA) evidence. Specimens from South Africa match the morphology of the lectotype of P. websteri and are morphologically and genetically very similar to P. websteri from Australia, China, Japan, and the east, gulf and west coasts of the USA. This confirms the presence of P. websteri in South Africa, making this the second most widespread polydorin pest of aquaculture known. Understanding the full distribution range of the species will help to better understand its global route of invasion and consequently assist with preventing or at least minimising further spread. Polydora websteri increases the number of polydorin pests in South Africa to seven.
... For example, ten shell-boring polychaete worm species are known to infect shells of cultured molluscs, mainly oysters and abalone, along the South African coastline (Simon and Sato-Okoshi 2015). Two of these parasites are invasive in South Africa, namely Polydora hoplura and Boccardia proboscidia (Simon et al. 2006(Simon et al. , 2009David and Simon 2014). The former was detected in the 1950s, while B. proboscidia was first recorded in 2004 (Simon et al. 2006(Simon et al. , 2009. ...
... Two of these parasites are invasive in South Africa, namely Polydora hoplura and Boccardia proboscidia (Simon et al. 2006(Simon et al. , 2009David and Simon 2014). The former was detected in the 1950s, while B. proboscidia was first recorded in 2004 (Simon et al. 2006(Simon et al. , 2009. The ability of females of these two polychaetes to produce multiple larval types (poecilogonous), and to survive and reproduce across a wide range of temperatures and substrates, all contribute to their invasion success in South Africa (David and Simon 2014). ...
Chapter
Full-text available
Ecological interactions, especially those that are beneficial (i.e. mutualism) or detrimental (i.e. parasitism), play important roles during the establishment and spread of alien species. This chapter explores the role of these interactions during biological invasions in South Africa, covering a wide range of taxonomic groups and interaction types. We first discuss the different ways in which interactions can be reassembled following the introduction of alien species, and how these depend on the eco-evolutionary experience of the alien species. We then discuss documented examples of parasitism and mutualism associated with invasions in South Africa and how these relate to various ecological and evolutionary hypotheses aimed at explaining species invasiveness. Selected examples of how invasive species impact on native species interactions are provided. A diverse array of biotic interactions (e.g. pollination, fish and mollusc parasitism, plant-soil mutualistic bacteria, seed dispersal) have been studied for various invasive species in South Africa. Surprisingly, only a few of these studies explicitly tested any of the major hypotheses that invoke biotic interactions and are commonly tested in invasion ecology. We argue that many invasions in South Africa are promising candidates for testing hypotheses related to species interactions and invasiveness.
... Furthermore, Mito & Uesugi (2004) showed that out of the 620 million live animals imported into Japan in 2003, 90% were classified as worms for fishing bait, suggesting a great scope for spread of worms via this vector. The global trade of molluscs such as oysters, mussels and abalone is considered one of the most important vectors of alien species (Ruesink et al., 2005) including shell-boring worms such as Boccardia proboscidea (Simon et al., 2009;Simon & Sato-Okoshi, 2015). Worms may also be spread unintentionally when fouling polychaetes such as Ficopomatus enigmaticus, Hydroides elegans and Sabella spallanzanii travel the world on ship hulls (Vitousek et al., 1997;Kocak et al., 1999;Hayes et al., 2005). ...
Article
This systematic review analysed scientific publications to identify relevant research about the impact of alien polychaete species around the world, using the PRISMA (Preferred Reporting Items for Systematic reviews and Meta-Analysis) guide. The criterion for inclusion was studies published in English, with the key terms (e.g. ‘impact’, ‘alien species’, ‘polychaetes’) in the title, abstract and keywords. The literature search was conducted in Scopus and Web of Science from April to December 2020. The search resulted in 150 papers that included information about impact of alien polychaete species. Of these studies, 98% were published in the last 25 years, reporting on the impact of 40 species in 18 regions of the world. Sixty-one per cent of the research was conducted in the Baltic Sea, South-west Atlantic and Mediterranean Sea. The most frequent type of study was field surveys (46%) and the most studied system was open coast areas (36%). The species with the highest number of publications about their impacts were Ficopomatus enigmaticus , Marenzelleria viridis , Sabella spallanzanii and Boccardia proboscidea . Based on evidence of their most severe documented impacts in their introduced ranges, the impact mechanisms (IMos) of the alien polychaete species were strongly related to their biology and lifestyles. We found that species that build conspicuous reefs and tube-dwellers mainly showed physical and structural impact on ecosystems; shell-borers, mainly parasitism and infauna species, showed mainly chemical, physical and structural impacts on ecosystems. Some recommendations for the study of alien polychaete species are discussed.
... There are limited studies investigating the shell infestation of abalone species infested by Polydora species, Phoronids (unsegmented worms) and sponges. However, these studies are often aimed at the distribution of native or invasive species [13][14][15][16] . Surprisingly, no studies on the effects of shell infestation by common organisms such as polychaetes and poriferans have been undertaken for Haliotis iris (Gmelin 1791), despite their commercially and culturally importance. ...
Poster
Full-text available
The endemic New Zealand blackfoot abalone, Haliotis iris (Gmelin 1791), has high cultural and economic importance, being considered a treasured species by Māori and supporting significant commercial and recreational fisheries. Pāua are a slow-growing species, taking three or more years to reach maturity, and five to seven years to reach legal harvest size, and experience high predation and mortality at smaller sizes. Infestation by polychaetes, sponges and other invertebrates as well epibionts on the shell can negatively affect growth, survival and ultimately the market value of pāua. Understanding the role that shell borer and epibionts play in pāua survival and development is essential for the management of this valuable species and fishery. The 2016 Kaikōura earthquake presented additional challenges for the fishery, resulting in mass-mortality of pāua and an ongoing closure to all commercial and recreational harvest. In this context, it is particularly important to assess survival, reproduction and growth of the recovering populations. With the here presented primary morphological and taxonomical studies we assess the extent and diversity of epibiont infestation in pāua along the affected coastline. We examined 100 shells of >110 mm shell length for all epibiota and potential parasites. The identification of species living in and on H. iris shells is a first step in evaluating the impact of shell infestation on growth, survival and reproduction. From these preliminary studies, we can continue to explore the effect of particular species on ontogeny and growth of pāua. Our findings will likely be relevant to other commercial New Zealand shellfish, such as oysters, and to other international abalone fisheries.
... The negative effects of shell-boring polychaetes on commercial molluscs include decreased growth (resulting in smaller sizes at maturity) and poor tissue condition, both of which result in commercial losses for farmers and decreased profitability of farms (Nel, 1996;McDiarmid et al., 2004;Simon and Booth, 2007;Read, 2010;Williams et al., 2016). For example, in South Africa, a single farm was forced to cull 500,000 highly prized abalone (Haliotis midae) as a result of polydorid infestation (Simon et al., 2009). In the wild, heavy infestation by shell borers can significantly weaken the structural integrity of the calcareous matrix, leading to increased mortalities, which in turn may threaten valuable oyster reef habitats that help enhance biodiversity and water quality in critical hotspots (David, 2020). ...
Article
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Anthropogenic climate change is considered to be one of the greatest threats facing marine biodiversity. The vast majority of experimental work investigating the effects of climate change stressors on marine organisms has fo-cused on calcifying organisms, such as corals and molluscs, where cross-generational phenotypic changes can be easily quantified. Bivalves in particular have been the subject of numerous climate change studies, in part because of their economic value in the aquaculture industry and their important roles as ecosystem engineers. However, there has been little to no work investigating the effects of these stressors on the symbionts associated with these bivalves, specifically, their shell-boring polychaete parasites. This is important to understand because climate change may shift the synergistic relationship between parasite and host based on the individual responses of each. If such a shift favors proliferation of the polychaete, it may very well facilitate extinction of host bi-valve populations. In this review I will (i) provide an overview of research completed thus far on the effects of climate change stressors on shell-boring polychaetes, (ii) discuss the technical challenges of studying these parasites in the laboratory , and (iii) propose a standardized framework for carrying out future in vitro and in vivo climate change experiments on shell-boring polychaetes.
... Biofouling on ships is a common dispersal vector for many marine species (Floerl & Coutts, 2009), but the aquaculture industry remains a primary candidate for nontarget species dispersal through hitchhiking. Examples of polychaetes that overcame biogeographic barriers by humanmediated transport in mollusk aquaculture are common (Naylor et al., 2001;Simon et al., 2009;Williams et al., 2016). Mussel seed transport to Northern Brittany and the Bay of Mont-Saint-Michel originated from the Bay of Biscay in 1954 and 1965, respectively, and continues to this day (Goulletquer & Le Moine, 2002). ...
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Aim Evolutionary history of natural populations can be confounded by human intervention such as the case of decorator worm species Diopatra (Onuphidae), which have a history of being transported through anthropogenic activities. Because they build tubes and act as ecosystem engineers, they can have a large impact on the overall ecosystem in which they occur. One conspicuous member, Diopatra biscayensis, which was only described in 2012, has a fragmented distribution that includes the Bay of Biscay and the Normanno-Breton Gulf in the English Channel. This study explores the origin of these worms in the Normanno-Breton region, which has been debated to either be the result of a historic range contraction from a relic continuous population or a more recent introduction. Location Northeastern Atlantic, the Bay of Biscay, and the Normanno-Breton Gulf. Methods We utilized a RAD-tag-based SNP approach to create a reduced genomic data set to recover fine-scale population structure and infer which hypothesis best describes the D. biscayensis biogeographic distribution. The reduced genomic data set was used to calculate standard genetic diversities and genetic differentiation statistics, and utilized various clustering analyses, including PCAs, DAPC, and admixture. Results Clustering analyses were consistent with D. biscayensis as a single population spanning the Bay of Biscay to the Normanno-Breton Gulf in the English Channel, although unexpected genetic substructure was recovered from Arcachon Bay, in the middle of its geographic range. Consistent with a hypothesized introduction, the isolated Sainte-Anne locality in the Normanno-Breton Gulf was recovered to be a subset of the diversity found in the rest of the Bay of Biscay. Main conclusions These results are congruent with previous simulations that did not support connectivity from the Bay of Biscay to the Normanno-Breton Gulf by natural dispersal. These genomic findings, with support from previous climatic studies, further support the hypothesis that D. biscayensis phylogeographic connectivity is the result of introductions, likely through the regions’ rich shellfish aquaculture, and not of a historically held range contraction.
... This pattern may be a result of a widely distributed species showing fairly large intraspecific divergences among sampling sites, but the shared haplotype between Japan and South Africa may also indicate recent translocations. In addition, it is also possible that P. neocaeca represents a diverse population in a smaller native geographic range from where multiple independent translocations originated (see Simon et al. 2009;Radashevsky et al. 2019) but are not currently reflected in our sampling. ...
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