Revista Chilena de Historia Natural 79: 263-278, 2006 Native and non-indigenous boring polychaetes in Chile: a threat to native and commercial mollusc species Poliquetos perforadores nativos y no indígenas en Chile: una amenaza para moluscos nativos y comerciales RODRIGO A. MORENO*, PAULA E. NEILL & NICOLÁS ROZBACZYLO Departamento de Ecología and Center for Advanced Studies in Ecology & Biodiversity (CASEB), Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Casilla 114-D, Santiago 6513677, Chile; * e-mail for corresponding author: [email protected]ABSTRACT Boring polychaetes infesting the shells of aquacultured molluscs affect host fitness and cause serious economic problems for the aquaculture industry. In Chile, knowledge of the native and non-indigenous polychaete fauna associated with mollusc hosts is limited, in spite of the fact that numerous native and non- indigenous mollusc species are actively harvested. We present the first complete list of boring polychaete species present in Chile, with a review of the information regarding each species’ status as a native or non- indigenous species (NIS), together with information on native and introduced ranges, affected host species, likely vectors of introduction and donor areas. We recorded a total of nine boring polychaetes present along the Chilean coast including native and NIS. Within the NIS category we provide the first published report of the Sabellid Terebrasabella heterouncinata in South America. Boring polychaetes utilized both native and introduced host species. The finding of polychaete species which utilized multiple native and NIS hosts, indicates a potential risk for spread between aquaculture facilities and the natural environment. Our analysis suggests that aquaculture activities are probably the primary introduction vector for boring polychaete species to Chile and that this region does not differ in the magnitude of introduced boring polychaetes relative to other regions of the world. We discuss current laws and management regarding polychaete infestations and make recommendations for future management in Chile, which should contemplate a rational compromise between the socio-economic needs of the country and plans to protect and preserve the nation’s biodiversity. Key words: Bioinvasions, legislation, management, NIS, Southeastern Pacific. RESUMEN La colonización de especies de poliquetos perforadores sobre conchas de moluscos de cultivos puede afectar la adecuación biológica del hospedador y causar serios problemas económicos para la industria acuícola. En Chile, el conocimiento de la fauna de poliquetos perforadores nativos y no indígenas asociados con moluscos hospedadores es limitado, a pesar del gran número de moluscos nativos y no indígenas que son activamente cultivados. Se presenta el primer listado completo de poliquetos perforadores en Chile, con información sobre el estatus de cada especie como nativa o especie no indígena (ENI), rangos nativos e introducidos, las especies hospedadores afectadas, los probables vectores de introducción y áreas donantes. Se registró un total de nueve especies de poliquetos perforadores en Chile, incluyendo especies nativas y ENI. Dentro de la categoría ENI se registra por primera vez a Terebrasabella heterouncinata en Sudamérica. Los poliquetos perforadores infestan especies nativas e introducidas. El hallazgo de poliquetos que utilizan múltiples hospedadores nativos y ENI, indica un potencial riesgo de diseminación entre centros de cultivos y el ambiente natural. Nuestro análisis sugiere que las actividades acuícolas son probablemente el principal vector de introducción de especies de poliquetos perforadores en Chile, no difiriendo en orden de magnitud con respecto a otras regiones del mundo. Se discute la actual legislación y planes de manejo sobre infestaciones de poliquetos perforadores y se realizan recomendaciones para el futuro manejo en Chile, la que debería contemplar un compromiso racional entre las necesidades socioeconómicas del país y planes de protección y preservación de la biodiversidad de la nación. Palabras clave: Bioinvasiones, legislación, manejo, ENI, Pacífico suroriental.
Transcript
263BORING POLYCHAETES OF CHILE Revista Chilena de Historia Natural79: 263-278, 2006
Native and non-indigenous boring polychaetes in Chile:a threat to native and commercial mollusc species
Poliquetos perforadores nativos y no indígenas en Chile:una amenaza para moluscos nativos y comerciales
RODRIGO A. MORENO*, PAULA E. NEILL & NICOLÁS ROZBACZYLO
Departamento de Ecología and Center for Advanced Studies in Ecology & Biodiversity (CASEB), Facultad de CienciasBiológicas, Pontificia Universidad Católica de Chile, Casilla 114-D, Santiago 6513677, Chile;
Boring polychaetes infesting the shells of aquacultured molluscs affect host fitness and cause seriouseconomic problems for the aquaculture industry. In Chile, knowledge of the native and non-indigenouspolychaete fauna associated with mollusc hosts is limited, in spite of the fact that numerous native and non-indigenous mollusc species are actively harvested. We present the first complete list of boring polychaetespecies present in Chile, with a review of the information regarding each species’ status as a native or non-indigenous species (NIS), together with information on native and introduced ranges, affected host species,likely vectors of introduction and donor areas. We recorded a total of nine boring polychaetes present alongthe Chilean coast including native and NIS. Within the NIS category we provide the first published reportof the Sabellid Terebrasabella heterouncinata in South America. Boring polychaetes utilized both nativeand introduced host species. The finding of polychaete species which utilized multiple native and NIShosts, indicates a potential risk for spread between aquaculture facilities and the natural environment. Ouranalysis suggests that aquaculture activities are probably the primary introduction vector for boringpolychaete species to Chile and that this region does not differ in the magnitude of introduced boringpolychaetes relative to other regions of the world. We discuss current laws and management regardingpolychaete infestations and make recommendations for future management in Chile, which shouldcontemplate a rational compromise between the socio-economic needs of the country and plans to protectand preserve the nation’s biodiversity.
La colonización de especies de poliquetos perforadores sobre conchas de moluscos de cultivos puede afectarla adecuación biológica del hospedador y causar serios problemas económicos para la industria acuícola. EnChile, el conocimiento de la fauna de poliquetos perforadores nativos y no indígenas asociados con moluscoshospedadores es limitado, a pesar del gran número de moluscos nativos y no indígenas que son activamentecultivados. Se presenta el primer listado completo de poliquetos perforadores en Chile, con información sobreel estatus de cada especie como nativa o especie no indígena (ENI), rangos nativos e introducidos, lasespecies hospedadores afectadas, los probables vectores de introducción y áreas donantes. Se registró un totalde nueve especies de poliquetos perforadores en Chile, incluyendo especies nativas y ENI. Dentro de lacategoría ENI se registra por primera vez a Terebrasabella heterouncinata en Sudamérica. Los poliquetosperforadores infestan especies nativas e introducidas. El hallazgo de poliquetos que utilizan múltipleshospedadores nativos y ENI, indica un potencial riesgo de diseminación entre centros de cultivos y elambiente natural. Nuestro análisis sugiere que las actividades acuícolas son probablemente el principal vectorde introducción de especies de poliquetos perforadores en Chile, no difiriendo en orden de magnitud conrespecto a otras regiones del mundo. Se discute la actual legislación y planes de manejo sobre infestaciones depoliquetos perforadores y se realizan recomendaciones para el futuro manejo en Chile, la que deberíacontemplar un compromiso racional entre las necesidades socioeconómicas del país y planes de protección ypreservación de la biodiversidad de la nación.
Aquacultured organisms are frequently fouled bya diverse array of epibionts, including algae,sponges, bryozoans, barnacles, molluscs,ascidians and polychaetes (e.g. Corriero &Pronzato 1987, Martin & Britayev 1998, López etal. 2000, Giacobbe 2002, Castilla et al. 2005).When marine species are introduced to newareas–often for aquaculture purposes–theirassociated epibionts can also be accidentallyintroduced (Naylor et al. 2001). This phenomenonpresents a risk to the biodiversity of the recipientcommunities through species interactionsbetween the non-indigenous assemblage and therecipient community (e.g. Naylor et al. 2001). Forexample, the non-indigenous epibionts mayacquire new hosts in the recipient communities(e.g. Kuris and Culver 1999, Culver & Kuris2004) or, conversely, organisms from therecipient community may learn to consume orotherwise utilize the introduced species (e.g.Magoulick & Lewis 2002). Either of thesescenarios could lead to changes in populationdynamics and community structure (e.g. Grosholzet al. 2000, Ross et al. 2003).
Boring polychaetes frequently infest theshells of aquacultured mollusc species. Thesepolychaetes can cause severe damage to themollusc shells, affecting the fitness of theirhosts (Blake & Evans 1973, Handley &Berquist 1997, Cáceres-Martínez et al. 1998,Martin & Britayev 1998, Read 2004,McDiarmid et al. 2004) and often causingfinancial loss to aquaculturists. At least threefamilies of boring polychaetes have beenreported in the literature: Spionidae, Sabellidaeand Cirratulidae. In particular, boringpolychaetes of the spionid genera such asBoccardia, Dipolydora, Polydora and thesabellid Terebrasabella heterouncinataFitzhugh and Rouse cause serious economicproblems for the aquaculture industry at aglobal level (see Evans 1969, Kuris & Culver1999, Lleonart et al. 2003a, 2003b, Cárdenas &Cañete 2004, Read 2004, Radashevsky &Olivares 2005). The specific effects of boringpolychaete species on their hosts have beenwell-studied for several commerciallyimportant molluscs both in their native andintroduced ranges (e.g. oysters, scallops,mussels, abalone; Kent 1979, Basilio et al.1995, Cáceres-Martínez et al. 1998, Kuris &
Culver 1999, McDiarmid et al. 2004, Vargas etal. 2005), however there are few availablestudies of boring polychaetes on species thatare not of economic importance.
In Chile, information regarding infestationsof native and non-indigenous boringpolychaetes on native and exotic molluscs ofcommercial importance is available,particularly for Spionidae polychaetes (seeRozbaczylo et al. 1980, Rozbaczylo et al. 1994,Basilio et al. 1995, Sato-Okoshi & Takatsuka2001, Cárdenas & Cañete 2004, Radashevsky& Olivares 2005, Bertrán et al. 2005) andCirratulidae polychaetes of the genusDodecaceria (see Carrasco 1977, Rozbaczylo& Carrasco 1996). Nevertheless, Chilecontinues to lag behind other countries (e.g.Australia, New Zealand, USA) in thedevelopment of plans to prevent and managepolychaete invasions both to aquaculturefacilities and natural environments. As Chilebecomes an important global provider ofseveral non-indigenous aquaculture products(e.g. salmon, abalone) it is vital to begin riskassessment and to implement appropriatemanagement strategies to protect naturalecosystems while continuing to look after thesocioeconomic interests of the country.
The purpose of this work is twofold: (1) toprovide the most current listing of marineboring polychaete species present in Chile,reviewing information regarding each species’status as a native or non-indigenous species,together with information on native andintroduced ranges, affected host species, andlikely vectors of introduction and donor areasand (2) to discuss current laws andmanagement regarding polychaete infestationsand make recommendations for futuremanagement in Chile.
Database and selection criteria
The database compiled for this study consistsin an exhaustive bibliographic review of boringpolychaete species on calcareous substratesrecorded along the Chilean coast, from thenorthern geopolitical boundary in Arica (18º20’S) to the southern tip of the continent at CapeHorn (56º S). We reviewed the list ofpolychaetes of Chile compiled by Rozbaczylo(1985; and posterior publications) and technicalreports from aquaculture facilities; in addition
265BORING POLYCHAETES OF CHILE
we conducted personal interviews with marinebiologists, and experts in aquaculture andbiosecurity from governmental and privateentities1 (see Appendices I and II). Using thesesources we compiled a list of all of the boringpolychaete species recorded in Chile. Wecategorized each of the selected speciesaccording to its geographic distribution as: (1)Native species (i.e. species with an historicrange of distribution in Chile or Peru2 and (2)Non-indigenous species (NIS; i.e. species witha recent record in Chile, present outside of theirnative or historic range of distribution or theirnatural range of dispersal3; such speciestypically present a notorious, biogeographicallyincongruous range of distribution). For amarine boring polychaete to be included in theNIS category it had to conform to at least oneof the following operational criteria based onOrensanz et al. (2002) and Castilla et al.(2005): (1) species whose non-native status inChile was well-documented in scientificpublications, written governmental reports,and/or based on the professional experience ofthe authors; (2) species with a notorious,incongruent range of distribution, including asingle report or discontinuous range withinChile, (3) species with an extremely widegeographical distribution, includingcosmopolitan species, (4) species documentedas NIS in other regions, (5) species that wereabundant in the vicinity of presumed centers ofintroductions (e.g. ports, aquaculture facilities),but rare or absent from other studied areas.
In Appendix III we provide a detailedidentification of the three new records ofboring polychaetes species recorded in thisstudy. The identification of these species wasmade following keys by Gravier (1908),Fauchald (1977), Rozbaczylo (1980) andFitzhugh & Rouse (1999). We used astereomicroscope and a scanning microscope toexamine the diagnostic characters for eachspecies. In addition, we compiled a list of thehost species in Chile affected by each of theboring polychaete species in the database, withinformation on the status of each host as Nativeor Non-Indigenous to the Chilean coast andwhether or not the host species is of economicimportance. Finally, for each of the non-indigenous polychaete species we compiledinformation on their native and introducedranges, and utilized this information, togetherwith data on affected host species, to proposepotential vectors and pathways of introductionto Chile. While precise introduction vectorsand pathways are not known with certainty, weutilize indirect evidence (i.e. published reportsof pathways used by congeneric or biologicallysimilar species introduced to other marinesystems around the world) or direct evidence ofthe presence of marine NIS utilizing specificvectors in Chile (e.g. specimens present on theshells of introduced mollusc species) followingCastilla and Neill (in press).
MARINE BORING POLYCHAETES IN CHILE
Current knowledge of boring polychaetes inChile
This is the first complete review of native andnon-indigenous boring polychaetes present onthe southeastern Pacific coast of Chile, togetherwith information on the affected hosts and thepossible vectors and donor areas of NISpolychaetes to the Chilean coast. We recordeda total of nine boring polychaete speciespresent along the Chilean coast, belonging tothe families Spionidae, Cirratulidae andSabellidae. Three of these species wereclassified as native species (Table 1) and sixspecies were classified as NIS (Tables 1 and 2).The geographical distributions of boringpolychaete species recorded on the Chileancoast are presented in Table 3. Within the NIS
1 Given current controversy regarding legislat ionrestricting aquaculture activities we are not able to providethe names of the experts that we interviewed in ourpublished work. Instead we have provided the name of theresearcher who conducted the interview. Additionalinformation regarding specific interview questions and theprofessional profile of the experts we interviewed areavailable in Appendices I and II.2 We included the coast of Peru in our definition so as notto increase the number of NIS on the list by adhering tostrict political boundaries. Therefore, if a species has anhistoric range in Peru as well as reports in Chile we havereported it as native to Chile. Note that using this broadergeographic range may result in the inclusion of speciesthat have undergone southward range extensions to Chile(such as those associated with ENSO phenomena).3 For this database we considered NIS to be those boringpolychaete species present beyond the southeastern Pacificcoasts of Chile or Peru, with a “recent” record in Chile;there was generally additional evidence of the non-nativestatus of such species, such as a lack of records in theearly literature or reported association with an introducedaquaculture species.
266 MORENO ET AL.
category we emphasize the first publishedreport of the sabellid fan worm, Terebrasabellaheterouncinata in South America, whichcorresponds to specimens found infestingHaliotis rufescens in an abalone aquaculturefacility of southern Chile (R.A. Moreno,personal interview).
Chile exhibits the same order of magnitudeof introduced boring polychaetes relative toother regions of the world: 12 NIS polychaetesin New Zealand (see Cranfield et al. 1998,Handley 2000, Read 2004); seven in California,USA (see Blake and Evans 1973, Boyd et al.2002); and seven in Australia (see McEnnulty
1: Sato-Okoshi & Takatsuka (2001); 2: Vargas et al. (2005); 3: Carrasco (1977); 4: Rozbaczylo & Carrasco (1996); 5:Hernández et al. (2001); 6: Rozbaczylo et al. (1994); 7: Blake (1983); 8: Rozbaczylo et al. (1980); 9: Bertrán et al. (2005);10: Basilio et al. (1995); 11: Radashevsky & Olivares (2005); 12: Kuris & Culver (1999)* This species is considered to be “native to Chile”, however within the country it has been trasplanted to culture facilitieslocated outside of the native range
TABLE 1
List of boring polychaete taxa recorded on the Chilean coast, with information on the status of eachpolychaete as Native or Non-Indigenous species (NIS). In addition we list the host species that are
affected by each boring polychaete, and we indicate whether affected hosts are Native or Non-Indigenous species in Chile, and whether the host is of direct economic importance ($)
Lista de taxa de poliquetos perforadores registrados en la costa del Pacífico suroriental de Chile, con información sobre elestatus de cada especie de poliqueto como Nativo o No indígena. Además se incluye una lista de las especies hospedadorasafectadas por cada poliqueto perforador, y se indica el estatus de los hospedadores como especies Nativas o No indígenas
et al. 2001, Hayes et al. 2005). Members of thefamily Spionidae were the most frequent boringpolychaete species observed in Chile (onenative and five introduced species). Thisfinding coincides with reports from otheraquaculture centers on the Pacific coast whereSpionidae are the most frequently reportedboring polychaete species (e.g. Eastern Pacificcoast: USA, Baja California, México; Blake &Evans 1973, Cáceres-Martínez & Tinoco-Orta2001, northwestern Pacific coast: Japan; Sato-Okoshi 1999; and the southwestern Pacificcoast: Australia; Lleonart et al. 2003a, 2003b,McDiarmid et al. 2004).
In Chile only three of the Spionidae species(Dipolydora huelma, Polydora rickettsi and P.uncinata) have been studied in terms of theireffects on economically important introducedmollusc species (e.g. Haliotis spp.). All ofthese polychaetes have been found in land-based abalone aquaculture facili t ies. Insouthern Chile D. huelma and P. rickettsi arereported to infest Haliotis rufescens abalonefarms. Infestation prevalence variesconsiderably according to the polychaetespecies (i.e. D. huelma has been reported toinfest over 88 % of mature abalone, while P.rickettsi infested approximately 24 % of matureabalone), whether specimens are immature ormature (i .e. mature specimens are moreinfested) and locality (Vargas et al. 2005). Innorthern Chile P. uncinata had notably highlevels of infestation prevalence, being found onup to 98.8 % of medium to large sized Haliotisdiscus hannai (Radashevsky & Olivares 2005).While these high prevalences of boringpolychaetes in aquaculture facilities suggestimportant consequences for aquaculturists,none of these studies report on economic lossassociated with polychaete infestations.
The two other families of boringpolychaetes found in Chile were represented byfewer species (two species belonging toCirratulidae and one species of Sabellidae). Thetwo Cirratulidae species (Dodecaceriachoromyticola and D. cf. opulens) were foundinfesting native and exotic hosts of economicimportance on the Chilean coast. However, theeconomic effects of the infestation byDodecaceria in culture centers on the Chileancoast are largely unknown, which is of concernespecially considering that Dodecaceria is areported pest in scallop cultures (Placopecten
magellanicus) in New England (Blake 1969,Martin & Britayev 1998). Furthermore, thediscovery of one Sabellidae species(Terebrasabella heterouncinata) infesting redabalone (Haliotis rufescens) in Puerto Montt,southern Chile (Table 2) represents the firstpublished record of this species in SouthAmerica (R.A. Moreno, personal interview).This species has been widely documented as amarine pest in abalone culture centers inCalifornia, USA, where numerous studies havebeen conducted in attempts to control and/oreradicate this pest (Culver et al. 1997, Kuris &Culver 1999, Culver & Kuris 2000). Given themagnitude of damage caused by T.heterouncinata in aquaculture facilities on thenortheastern Pacific coast, this polychaeteconstitutes a serious threat for aquacultureactivities on the Chilean coast. At present thispolychaete has only been observed in a closedcircuit land-based culture system and all knownhosts containing specimens were placed inquarantine and later eliminated (R.A. Moreno,personal interview).
Affected host species
The boring polychaete species utilized a totalof 19 different host species, consisting in 15mollusc species, three crustaceans and onecalcareous encrusting alga. This l istingincluded six native hosts with no commercialvalue, 10 native hosts with commercial value,and three NIS hosts introduced for aquaculturepurposes (Table 1). We found evidence ofnative boring polychaete species infesting bothnative and non-indigenous hosts, as well as thecontrary case of non-indigenous polychaetesinfesting native and non-indigenous hosts.Three of the polychaete species presented hostspecificity: the non-indigenous polychaetesPolydora uncinata and Terebrasabellaheterouncinata bored into introducedaquaculture species (i.e. Haliotis spp.), whilethe native Dodecaceria choromyticola infestedeconomically important native molluscs. Atpresent the two non-indigenous polychaetes arereported to present high host-specificity(Polydora uncinata and Terebrasabellaheterouncinata), and are found only in land-based abalone aquaculture systems. Currentlythere is no available information regarding thepotential introduction of this species to the
268 MORENO ET AL.
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o (4
2º29
’S),
Ya l
dad
Bay
(43
º07’
S),
Chi
loé
Isla
nd (
43º0
0’S
)
Coq
uim
bo (
29º5
5’S
)
Pue
rto
Mon
tt (
41º3
0’S
)
NIS
bor
ing
poly
chae
tesp
ecie
s
Dip
olyd
ora
giar
di
Boc
card
ia t
ricu
spa
Pol
y dor
a bi
occ i
pita
lis
Pol
y dor
a ri
c ke t
tsi
Pol
y dor
a un
c ina
ta
Te r
e bra
sabe
lla
hete
roun
c ina
ta
1: B
lake
& K
uden
ov (
1978
); 2
: B
lake
(19
83);
3:
Sa t
o-O
kosh
i &
Tak
a tsu
ka (
2001
); 4
: C
a rra
sco
(197
7);
5: R
ozba
c zyl
o e t
al.
(19
94);
6:
Roz
bac z
ylo
e t a
l. (
1980
); 7
: B
a sil
io e
t a l
. (1
995)
;8:
Be r
trá n
et
a l.
(200
5);
9: V
a rga
s e t
al.
(20
05);
10:
Sa t
o-O
kosh
i (1
998)
; 11
: R
a da s
hevs
ky &
Oli
vare
s (2
005)
; 12
: K
uris
& C
ulve
r (1
999)
; 13
: C
ulve
r &
Kur
is (
2000
)
269BORING POLYCHAETES OF CHILE
natural environment from the land-basedsystems (e.g. escape via effluent tubes).Furthermore, recent Chilean legislation nowallows for the abalone hosts of these twospecies to be cultivated in open and semi-enclosed circuits in nearshore waters on thenorthern and southern coasts of Chile(FONDEF 1999, 2001, 2003, PYME 2005, seealso discussion), which could constitute apotential risk to native host populations(Naylor et al. 2001). The other six species wereobserved to utilize multiple host species (Table1). The finding that some native polychaetesalso utilize introduced aquaculture species iscause for concern, since the high densities ofavailable NIS hosts could support higherabundances of boring polychaete populations,which could subsequently increase the load ofpolychaetes on their native hosts. Likewise, thefinding that several non-indigenous polychaetesutilize multiple hosts (including both nativeand introduced hosts) also constitutes a seriousthreat to native organisms which are affectedby this load of new ‘parasites’ lacking acommon evolutionary history (Sax & Brown2000).
Vectors and pathways of boring polychaeteintroductions to Chile
Aquaculture activities are likely the primaryvector of introduction of exotic boringpolychaetes to Chile (Table 2), probablyinvolving long-distance transfers ofpolychaetes on molluscs from aquaculturefacilities on other continents. This hypothesis issupported by the observations that fourpolychaete NIS are present in aquaculturecenters and are reported to infest at least oneexotic host species in Chile (Tables 1 and 2).For at least two polychaete species the datasuggest that following their introduction withaquacultured species (e.g. Crassostrea gigas,Haliotis spp.) the polychaete taxa were able todisperse locally to nearby populations of nativehost species. These native hosts may promotefurther dispersal of the introduced polychaeteswithin the natural environment.
We identified a variety of possible donorareas, including the North Pacific Ocean (botheast and west coasts), the Central Pacific (eastcoast), the South Pacific (east coast and westcoast), the North Atlantic (east coast) and the
TABLE 3
Global geographical distribution of boring polychaete species recorded on the Chilean coast
Distribución geográfica global de las especies de poliquetos perforadores registrados en la costa de Chile
Boring polychaete species Geographical distribution
Boccardia tricuspa (Hartman, 1939) California, east coast of Mexico, Ecuador, Galapagos Islands(Hartman 1968, Blake 1983); Chile: Las Cruces (Rozbaczylo etal. 1994) to Puerto Montt (Sato-Okoshi & Takatsuka 2001)
Dipolydora giardi (Mesnil, 1896) Cosmopolitan on calcareous substrates (Sato-Okoshi &Takatsuka 2001); Ecuador (Blake 1983); Chile: Montemar;Puerto Montt (Sato-Okoshi & Takatsuka 2001), Juan FernándezArchipelago, Robinson Crusoe Island (Blake 1983)
Dipolydora huelma Sato-Okoshi & Takatsuka, 2001 Chile: Seno Reloncaví (Sato-Okoshi & Takatsuka 2001); PuertoMontt, Castro-Chiloé (Vargas et al. 2005)
Terebrasabella heterouncinata Fitzhugh & Rouse, 1999 South Africa; California, Baja California, Mexico (Kuris &Culver 1999); Chile: Puerto Montt
270 MORENO ET AL.
South Atlantic (east coast). Five of the six NISlikely arrived from the northern hemisphere(Table 2). On the southeastern Pacific coast ofChile there was no clear pattern regarding areasof introduction. Non-indigenous polychaetespecies were observed in at least 20 differentsites in northern, central and southern Chile,ranging from Arica (20º 54’ S) to Yaldad Bay(43º 07’ S) (Table 2). The NIS polychaetes, P.uncinata and T. heterouncinata were recordedonly in land-based aquaculture systems, whilethe native D. huelma was recorded in bothland-based aquaculture systems and naturalenvironments. The native Dodecaceriachoromyticola was observed only in sea-basedaquaculture systems and the NIS polychaetesD. giardi, and P. rickettsi were observed inboth sea-based aquaculture systems and naturalenvironments. Finally, two of the NIS, B.tricuspa and P. bioccipitalis, were recordedonly in natural environments in the intertidaland shallow subtidal zones of the Chileancoast. The lack of a clear pattern in theintroduced ranges of polychaete NIS withinChile may be a product of incompleteinformation regarding boring polychaeteinfestations on native hosts that are not ofeconomic importance. Nevertheless, it isimportant to highlight that secondary pathwaysof dispersal from the source site may exist (e.g.the transfer of boring polychaetes on shellfishor aquaculture equipment moved betweenfacilities). Evaluating potential vectors andintroduction pathways of boring polychaetes isa fundamental part of the risk assessmentprocess (e.g. Ruiz & Carlton 2003).
CURRENT LAWS AND MANAGEMENT AND
RECOMMENDATIONS FOR FUTURE MANAGEMENT
Legislation and management of boringpolychaetes in Chile
It is important to highlight that although Chilehas legislation regarding exotic speciesintroductions to marine environments (TheFishery and Aquaculture Law, “Ley General dePesca y Acuicultura” 1989), the main emphasisof these regulations has been on protecting thenation’s natural resources. While writtenenvironmental law (Law 18.892) stipulates thataquaculturists must assure conditions that
guarantee the protection of “biodiversity”(PYME 2005), in practice law-enforcers onlyeffectively monitor effects on the“biodiversity” of native species of economicimportance (e.g. Concholepas concholepas,Fissurella spp.).
Current legislation is focused on preventingthe introduction and dispersal of non-targetmarine species associated with aquacultureactivities (The Fishery and Aquaculture Law,“Ley General de Pesca y Acuicultura” 1989).For example, together with approving andfinancing projects to cultivate exotic abalone(Haliotis spp.) in sea cages along the Chileancoast, the government has also passed legislationwhich specifies that the abalone can only befarmed in areas devoid of hard substrates, andthat concessions must strictly adhere toprograms of environmental vigilance regardingthe protection, control and eradication of“diseases” that present significant risks tohydrobiological species (Resolutions No 319/01and 320/01 of Ministerio de Economía, Fomentoy Reconstrucción, hereafter MEFR). However,many aquaculturists remain doubtful regardingwhether it is possible to find adequate areas foraquaculture which comply with all of themeasures of protection (e.g. areas devoid of hardsubstrates) (P.E. Neill, personal interview).
In addition, the government has providedfunding to an institution (i.e. Fundación Chile)in charge of developing techniques for theprevention and control of infectious and non-infectious diseases in abalone, with specificreference to boring polychaetes (FONDEF2001). Measures of polychaete prevention andcontrol include quarantine of infested abalone,eradication of polychaetes via dessication,exposure to freshwater, chemicals or wax (R.A.Moreno, personal interview).
In 2003 the National Fisheries Service(Servicio Nacional de Pesca, hereafterSERNAPESCA) established the ActiveVigilance Program (“Programa de VigilanciaActiva”, Resolution No 1809/03) to monitorabalone and oyster aquaculture centers in Chilefor high risk diseases. This monitoring programcan also be extended to other aquaculturefacili t ies and natural populations ofeconomically important mollusc species ifsolicited. This program consists in semi-annualmonitoring (fall and spring-summer) in andnear aquaculture centers for the presence of
271BORING POLYCHAETES OF CHILE
specific high risk “diseases” in mollusc species.The monitoring is conducted by governmentauthorized (SERNAPESCA) diagnosticlaboratories who aim to identify sanitary risksassociated with the aquacultured species asspecified by a government ministry (i.e.MEFR), which dictates legislation on theProtection, Control and Eradication of HighRisk Diseases to Hydrobiological Species(Resolution No 319/01). A subgroup of thisministry (Subsecretaria de Pesca) emits twolists of high risk disease organisms whichshould be evaluated (for more details see theAquatic Animal Health Code, OIE 2005).Nevertheless, under current sanitary legislation(Resolution No 1623/05 MEFR), manypolychaetes and other epi- or endo-biontswhich are known to be present in aquaculturefacilities are not considered “disease” agents, inspite of the damage that they cause toeconomically important mollusc species (e.g.“polydoriasis”, Lleonart et al. 2003a, 2003b).At present SERNAPESCA is working toimprove regulations to include the control oforganisms that damage aquaculture facilities,but which have not yet been included on thehigh risk diseases lists (R.A. Moreno, personalinterview).
The Chilean government has expressed itscommitment to protecting native biodiversity bysigning several international agreements (Camus2005), including the International Convention onthe Trade of Threatened Species of Wild Faunaand Flora (CITES, Supreme Decree No 141/75),which makes references to preventing theintroduction of non-indigenous species thatthreaten ecosystems, habitats or species, andcontrolling or eradicating NIS which have beenintroduced. While in theory Chilean legislationaims to protect aquatic resources againstunwanted invaders, such as non-indigenousboring polychaetes, whether or not theseregulations are enforced or even feasibleremains to be seen. The current socio-economicconcerns of the country place strong pressure onlaw makers and enforcers which may hinder theapplication of measures to protect biodiversity inthe field. For example, aquaculturists arecurrently lobbying to assuage proposedlegislation to permit abalone farming in moremarine areas (P.E. Neill, personal interview).
Worms settling onto and boring into shellscause myriad problems for aquaculturists (e.g.
spoiled shell shape and quality, internal shellblisters, serious reduction in shell strength,damaged adductor muscles, energy wasted onshell repair, reduced flesh condition andincreased vulnerability to serious pathogens,massive mortalities and resulting economicloss; Dunphy and Wells 2001, Lleonart et al.2003a, 2003b, McDiarmid et al. 2004, Read2004, Simon et al. 2004). Therefore, legislationto prevent, control and/or eradicate NISpolychaetes should provide long-term mutualbenefits to both the nation’s economy (e.g.aquaculture) as well as to the nation’s nativebiodiversity. Nevertheless, social aspects ofaquaculture in Chile, such as the need to obtainshort-term profits-especially for small-scaleaquaculturists-make the effectiveimplementation of legislation and subsequentcompliance with regulations a complex issue.
Future recommendations
Given the geographic layout of Chile(possessing over 4,200 km of coastline over 38degrees of latitude, Camus 2001) this countryhas been touted as an ideal region for marineaquaculture; the same attribute, however,makes this region a prime target for non-indigenous species introductions. Given thatexotic species introductions is a topic of globalconcern, and the fact that at least 6 NIS boringpolychaete species are present on the Chileancoast, interacting with at least 14 native andnon-indigenous hosts, it is important forresearchers, managers and aquaculturists todevelop strategies to prevent futureintroductions and to control or eradicate NISthat have already been introduced. Researchersneed to generate baseline studies regarding thepresence/absence of boring polychaetes innatural environments as well as determine theprevalence and ecological effects of non-indigenous polychaetes on their hosts.
A difficult task which must be broached inChile is the need to develop a long-term planwhich represents a rational compromisebetween the socio-economic plans for thecountry and plans to protect and preserve thenation’s biodiversity (Arroyo 2003, Camus2005). To ensure marine biosecurity in Chile itis fundamental to implement preventivemeasures, including periodic monitoring ofnative populations in the vicinity of both land-
272 MORENO ET AL.
based and sea-based aquaculture facilities todetect and control the possible escape of non-target species, implementation of treatmentsystems for water discharged from aquaculturefacilities into the ocean (e.g. mechanicalmethods, electrochemical treatments, UVradiation, chlorine treatment) development ofcertification protocols to assess the cleanlinessof introduced aquaculture species andaquaculture equipment and the establishment ofactive vigilance programs to assure thatinfested organisms and equipment are notmoved between facilities within the country(see Campalans 2005). Researchers shoulddevelop a document for aquaculturists and thegeneral public, which educates about the risksof non-indigenous species introductions andprovides an efficient plan-of-action to followwhenever an NIS is discovered. In addition topenalties for organizations that do not complywith laws regarding species introductions,proactive legislation should also beimplemented to restrict the arrival of NIS toChile. Specific areas of focus should beidentifying and controlling vectors ofintroduction and primary donor areas, andbeing alert to the arrival of species that arereported as pests in other regions of the world.
ACKNOWLEDGEMENTS
We thank Fernanda Oyarzún (University ofWashington, Seattle, USA) for helping us withthe literature on boring polychaetes fromCalifornia, USA. We acknowledge thecooperation of Fabián Avilés (Aquagestión-Fundación Chile), Servicio Nacional de Pescaand Subsecretaría de Pesca, Valparaíso, Chile,and six anonymous experts who shared dataand information in confidential interviews. Thephotographs of Terebrasabella heterouncinataand Dodecaceria cf. opulens were graciouslyprovided by Fabián Avilés (Aquagestión-Fundación Chile). We are grateful to Dr.Patricio A. Camus and two anonymousreviewers for their valuable recommendationsto improve this manuscript. Significantfinancial support was provided by Dr. FabiánJaksic through FONDAP grant No 1501-0001 toCASEB (Cross-Cutting Tearn on Bioinvasions).R.A. Moreno is supported by the EU-projectCENSOR “Climate variability and El Niño
Southern Oscillation: Impacts for naturalresources and management”, contract 511071 tothe Alfred Weneger Institute for Polar andMarine Research (AWI), Bremerhaven,Germany. This is CENSOR publication 0024.P.E. Neill is supported by a CONICYT DoctoralFellowship, CONICYT Thesis Project support(No AT-4040050), IDEA WILD grant and PEOScholar Award.
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SAX DF & JH BROWN (2000) The paradox of invasion.Global Ecology and Biogeography 9: 363-371.
SERVICIO NACIONAL DE PESCA (1999) Anuarioestadístico de pesca. Ministerio de Economía,Fomento y Reconstrucción, Chile. 291 pp.
SIMON C, H KAISER & PJ BRITZ (2004) Infestation ofthe abalone, Haliotis midae , by the sabellid,Terebrasabella heterouncinata, under intensiveculture conditions, and the influence of infestationon abalone growth. Aquaculture 232: 29-40.
VARGAS L, P QUIJÓN & C BERTRÁN (2005)Polychaete infestation in cultured abalone (Haliotisrufescens Swainson) in southern Chile. AquacultureResearch 36: 721-724.
WOODWICK KH (1961) Polydora rickettsi, a new speciesof spionid polychaeten from lower California.Pacific Science 15: 78-81.
Associate Editor: Patricio CamusReceived October 13, 2005; accepted March 9, 2006
275BORING POLYCHAETES OF CHILE
APPENDIX 1
Questions asked during interviews of professional specialists in marine biosecurity in Chile withrespect to legislation and the management of pests and high risk infectious diseases provoked by
boring polychaetes in aquacultured species
Preguntas realizadas a profesionales especialistas en bioseguridad marina en Chile, en relación a legislación y el manejo deplagas y enfermedades infecciosas de alto riesgo provocadas por poliquetos perforadores en especies de cultivos
APPENDIX 2
Profile of the professionals who were interviewed during our study. We indicate the professionaltitle and/or academic degree, institutional affiliation and area of speciality regarding marine
biosecurity in Chile
Perfil profesional de los encuestados donde se indica el título profesional y/o grado académico, afiliación institucional yáreas de especialización en materias de bioseguridad marina en Chile
Academic degree Institution Function
Ph.D. in Biology Subsecretary of Fisheries (SUBPESCA) Biosecurity, laws
Veterinarian National Fisheries Service (SERNAPESCA) Pest management in aquaculture
Marine Biologist Aqua-Gestión Fundación Chile Pest management in aquaculture
Aquaculture Engineer Private aquaculture business Pest management in aquaculture
• How does Chile rank among developedcountries such as Australia, New Zealandand the USA in terms of preventativemeasures regarding marine biosecurity?
• Are the governmental institutions that are incharge of legislating marine biosecurityissues, such as the National FisheriesService (Servicio Nacional de Pesca;SERNAPESCA) and the Subsecretary ofFisheries (Subsecretaría de Pesca;SUBPESCA), currently working to developand/or perfect new regulations such as thecontrol and management of pests that causeeconomic damage to aquaculturebusinesses? What kind of monitoringprograms are currently in existence?
• Are private aquaculture businesses along theChilean coast developing plans to lobby thecurrent legislation allowing an increase inthe number of aquaculture centres forspecies of economic importance? Which
particular issues are currently of concern toaquaculturists?
• Are the governmental entities in charge ofprotecting, controlling and eradicating highrisk infectious diseases in aquaculturecurrently creating documentation and/or aplan of action to incorporate polydoriasis asa high risk disease in Chile?
• Do the specimens of red abalone (Haliotisrufescens) that were infested with the boringpolychaete Terebrasabella heterouncinatacome from reproductive stocks importedfrom aquaculture centers in California,USA?
• What sanitary procedure was followed forspecimens of Haliotis rufescens infestedwith T. heterouncinata?
• Were the specimens of Haliotis rufescensinfested with T. heterouncinata located in aclosed, land-based culture system on in thesea?
276 MORENO ET AL.
APPENDIX 3
Diagnosis of boring polychaete species recorded in this study infesting native and introducedmollusc hosts of economic importance on the Chilean coast
Diagnosis de las especies de poliquetos perforadores registradas en este estudio hospedando en moluscos nativos eintroducidos de importancia económica en la costa de Chile
Fig. 1: Detail of the shell of a red abalone (Haliotisrufescens) from Puerto Montt, Chile, on which thebranchial crowns of Terebrasabellaheterouncinata can be observed (Photo: F. Avilés).Detalle de una concha de abalón rojo Haliotis rufescens dePuerto Montt, Chile en que asoman las coronas branquialesde Terebrasabella heterouncinata (Foto: F. Avilés).
Fig. 2: Lateral view of a complete specimen ofTerebrasabella heterouncinata which was extrac-ted from a shell of the red abalone Haliotis rufes-cens from Puerto Montt, Chile (Photo: F. Avilés).Vista lateral de un ejemplar completo de Terebrasabellaheterouncinata extraído de una concha del abalón rojo Ha-liotis rufescens de Puerto Montt, Chile (Foto: F. Avilés).
Diagnosis: we examined the externalmorphology of a total of seven specimens,which were obtained by decalcifying shells ofthe red abalone, Haliotis rufescens Swainson,from Puerto Montt, Chile (Fig. 1). The presenceof a skeleton in the branchial crown, fusion ofthe mid-dorsal margens of the branchial lobesand the presence of companion setae on thethoracic neuropodia indicate that the specimensbelong to the subfamily Sabellinae (according toFitzhugh & Rouse 1999), within the familySabellidae (according to keys by Fauchald 1977and Rozbaczylo 1980). From the consistency inthe observed characteristics for the sevenspecimens and the description by Fitzhugh &Rouse (1999), we were able to identify all of thespecimens as belonging to the speciesTerebrasabella heterouncinata. The specimenswere 1-1.5 mm long. The branchial crown hadtwo pairs of radioles. The anterior half of thebody was thinner, and the posterior half wasslightly expanded and sac-like (Fig. 2). Eachindividual had 8 thoracic segments and onlythree abdominal segments. Thoracic neuropodialuncini present in setigers 2-8 were of two types:those in setigers 2-6 were acicular, with adistinct main fang surmounted by a series ofsmaller teeth, while the uncini in setigers 7-8were avicular, the main fang was absent and allteeth were uniform in size, in a narrow,elongate, rasp-shaped arrangement. Companionsetae were present in the neuropods of setigers2-6 and absent in setigers 7-8. Abdominalnotopodial uncini in setigers 9-11 were acicular,with the distinct main fang surmounted by aseries of smaller teeth.
Remarks: this species has been recordedliving in galleries of the shells of variousgenera and species of marine gastropods inSouth Africa, including the abalone Haliotismidae, and in California there are records in thered abalone Haliotis rufescens.
277BORING POLYCHAETES OF CHILE
Fig. 3: A piece of shell from the red abaloneHaliotis rufescens from Puerto Montt, Chilewhich has been bored into by a specimen ofDodecaceria cf. opulens (Photo: F. Avilés).Trozo de concha de abalón rojo Haliotis rufescens de Puer-to Montt, Chile perforado por un ejemplar de Dodecaceriacf. opulens (Foto: F. Avilés).
Dodecaceria cf. opulens Gravier, 1908
Diagnosis: we examined the externalmorphology of three specimens extracted fromgalleries that were dug into the shell of the redabalone Haliotis rufescens (Fig. 3) from PuertoMontt, Chile. The color of the fixed specimenswas brownish-orange and green; individualsmeasured between 30 to 60 mm in length and 2mm wide, with up to 120 setigers (Fig. 4). Theprostomium is blunt, and forms a hood over themouth. The buccal segment is long and blunt,but with two stout grooved palps at its junctionwith setiger one. In the peristomium andsecond segment there are two pairs of branchialfilaments; from the third to the eleventhsegment there is only one pair of branchialfilaments; with those of the first two segmentsbeing very short. The first setiger is uniramouswith simple capillaries. The second setiger isbiramous and bears notopodial and neuropodialsetae. The setae of the first 10 setigers aresimple capillaries with a serrated edge.Beginning at setiger 11 there are stout,notopodial and neuropodial spoon-shapedhooks. The neuropodial hooks are the mostrobust.
Remarks: in this study we record, for thefirst time, the presence of Dodecaceria cf.opulens in the shell of red abalone (Haliotisrufescens) from Puerto Montt, Chile. Earlier,Rozbaczylo & Carrasco (1996) mention thepresence of this species in the shells of thegastropod molluscs Fissurella maxima andConcholepas concholepas, as well as in thebivalve Aulacomya ater. Hernández et al.(2001) recorded this species in the shell of thebarnacle Austromegabalanus psittacus inConcepción, Chile.
Polydora bioccipitalis Blake & Woodwick, 1971
Diagnosis: we examined the externalmorphology of two specimens taken from amud-blister in the shell of the clam Muliniaedulis (King & Broderip). These specimenswere compared with specimens extracted fromthe shell of Mesodesma donacium (Lamarck)that were deposited in the Collection of Floraand Fauna “Professor Patricio Sánchez Reyes”(SSUC), of the Pontificia Universidad Católicade Chile in Santiago. The specimens were 18mm long, with up to 110 setigers. This species
Fig. 4: Lateral view of a complete specimen ofDodecaceria cf. opulens extracted from a shellof the red abalone Haliotis rufescens fromPuerto Montt, Chile (Photo: F. Avilés).Vista lateral de un ejemplar completo de Dodecaceria cf.opulens extraído de una concha de abalón rojo Haliotisrufescens de Puerto Montt, Chile (Foto: F. Avilés).
278 MORENO ET AL.
is easily recognized by the followingcombination of characters: the prostomium isdeeply notched on the anterior margin, with acaruncle that extends up to setigers 10-14,approximately; with two nuchal tentacles in arow located at the level of the first setiger andbetween the palps, immediately following thetwo pairs of eyes. Notosetae are absent onsetiger one. Bidentate hooded hooks are presenton the neuropodia beginning at setiger 10. Thebranchiae are long, blunt and wide, and beginon setiger seven, continuing to near theposterior end of the body. Setiger 5 is largerthan other setigers and includes a curved row of8 to 10 heavy spines alternating with pennoned
companion setae. The heavy spines are falcateand have three accessory structures. Thepygidium is disclike, with a dorsal gap.
Remarks: in this study we recorded thisspecies, for the first time, on the paleal sinus ofa specimen of the clam Mulinia edulis (King &Broderip), collected in the locality of PlayaSanto Domingo, south of the port of SanAntonio, Chile. Earlier, Rozbaczylo et al.(1980) recorded this species in the shell of livespecimens of the bivalve Mesodesma donaciumin Playa Morrillos. Blake (1983) recorded thisspecies in Playa El Aguila, approximately 100km south of Iquique, Chile in shells of liveMesodesma donacium.
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