Haematophagous feeding stage of the

anadromous sea lamprey Petromyzon

marinus: low host selectivity and wide range

of habitats

Sergio Silva1,2,*; Mário J. Araújo3; Miguel Bao4; Gonzalo Mucientes5,6 & Fernando Cobo1,2 1Department of Zoology and Physical Anthropology, Faculty of Biology, University of Santiago de Compostela, Lope Gómez de Marzoa

s/n, 15782 Santiago de Compostela, Spain. 2 Hydrobiology Station “Encoro do Con”, Castroagudín s/n, 36617 Vilagarcía de Arousa, Pontevedra, Spain. 3CIMAR-LA/CIIMAR Interdisciplinary Centre of Marine and Environmental Research, Rua dos Bragas, 289, 4050-123 Porto, Portugal 4 ECOBIOMAR, Instituto de Investigaciones Marinas (CSIC), Eduardo Cabello 6, E-36208 Vigo, Spain 5 Grupo de Ecología Pesquera, Instituto de Investigaciones Marinas (CSIC), Eduardo Cabello 6, E-36208 Vigo, Spain. 6 CIBIO – Universidade de Porto, Centro de Investigação em Biodiversidade e Recursos Genéticos, Campus Agrário de Vairão, 4485-668

Vairão, Portugal.

York, May - 2014

Life cycle

Metamorphosis (4-10 months without feeding: critical stage)

Larval stage

Downstream migration (Little information available)

Haematophagous stage (Information restricted to occasional

captures of lampreys or host at sea)

Upstream migration

Reproduction

Freshwater

Sea?

Freshwater

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Issues

1. Downstream migration and onset of the haematophagous feeding

2. Duration of the hematophagous life stage (mark recapture program)

3. Host species and distribution during the haematophagous life stage

© CEMMA

© G. Mucientes© M.J. Araújo © G. Mucientes

© EHEC © EHEC © EHEC © EHEC

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1. Downstream migration and onset of the haematophagous feeding

Silva et al. (2013). Hydrobiologia 700: 277-286

Silva et al. (2013). Journal of Fish Biology 82: 1739-1745

Permanent trap

Visual records

Trammel nets

Seine and hand nets

Monthly distribution of the percentage (mean ± standard error) of postmetamorphic

lampreys captured in a permanent trap (40 km away from the mouth) during their

downstream migration (1997-2010). N = 6839 individuals.

October to May

Unimodal pattern

Silva et al. (2013). Hydrobiologia 700: 277-286

Downstream migration

Our results suggest that 10-30% of postmetamorphics start

feeding in the river before migrating to the sea.

Host species:

Salmo salar Linnaeus, 1758

Alosa fallax (Lacépède, 1803)

Salmo trutta Linnaeus, 1758 (resident and anadromous form)

Pseudochondrostoma duriense (Coelho, 1985)

Silva et al. (2013). Hydrobiologia 700: 277-286

Silva et al. (2013). Journal of Fish Biology 82: 1739-1745

Silva et al. (in press). Limnetica

Feeding in the river

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Large numbers of lampreys were observed feeding in the estuary and nearest coast for several

months (November to May), where they found high abundances of hosts, mainly mullets.

Feeding in the estuary

Silva et al. (2013) . Hydrobiologia 70: 277-286

Mugilidae is a cosmopolitan family which is

typical of coastal areas, with species all over

the world. They might be a key element in the

diet of anadromous populations of sea

lamprey.

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Capture of individuals Hand and seine nets

Trammel nets: bad idea

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Box plots (maximum and minimum values, lower and upper quartiles, and median) of the total length,

weight, and condition factor for transformers captured in September 2010 (grey box), postmetamorphic

lampreys captured monthly during their downstream migration between 1997 and 2010 (white boxes) and

captured feeding in the estuary (hatched boxes)

Silva et al. (2013) . Hydrobiologia 700: 277-286

River-estuary comparison

2. Duration of the hematophagous feeding stage

Silva et al. (2013). Aquatic Biolology 18: 59-62

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Mark-recapture program

Individually numbered T-bar anchor tags (FLOY)

More than 3000 postmetamorphic lampreys tagged (2010-2012)

Marked in the estuary, recaptured lamprey was caught 13.5 moths after tagging

Date TL (mm) W (g) Δ TL (%) Δ W (%)

Tagged

postmetamorphic 01/02/2011 218 20

Adult recaptured 26/03/2012 895 1218 311 5990

FIRST RECAPTURE

Silva et al. (2013). Aquatic Biolology 18: 59-62

© EHEC © EHEC

Silva et al. (2013). Aquatic Biolology 18: 59-62

End of metamorphosis: October-November

Spawning: May - June

Postmetamorphic phase: 1.5 years (18-20 months)

Haematophagous feeding period for this lamprey : 10-14 months

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Postmetamorphic phase:

1.5 years (18-20 months)

Haematophagous feeding period for this

lamprey : 10-14 months (≈1 year)

3. New host species and marine distribution

Sources:

• Inland and coastal commercial fisheries

• Inland and marine sport fishing

• Offshore surveys (scientific expeditions and mark-recapture campaigns)

• Stranded individuals (CEMMA and CEPESMA)

• Personal communications from other researchers (Richard Sabatié and John Hume)

Silva et al. (2014). Hydrobiologia. Online first

Attacks from fresh and brackish waters to

coastal areas and open sea (up to 800 km

from the nearest coast).

New records on 23 host species of

chondrichthyans, osteichthyans, and

cetaceans (13 orders and 21 different

families). Nineteen species described for

the first time as hosts of P. marinus. © Rodrigo López

Alosa alosa (a), Liza ramada (b), Scomber scombrus (c), Trachurus trachurus (d), Merluccius

merluccius (e) and Sebastes mentella (f) attacked by Petromyzon marinus

Silva et al. (2014). Hydrobiologia. Online first

© R Sabatié

© R Sabatié

© Xulio Valeiras

© M Bao

© G Mucientes

© MJ Araújo

Pierced (indicative of active feeding) (a) and non-pierced (b) wounds caused by Petromyzon marinus on

Mesoplodon bidens. Pierced (c) and non-pierced (d) wounds caused by P. marinus on Balaenoptera

acutorostrata

Silva et al. (2014). Hydrobiologia. Online first

© CEMMA

© CEMMA© CEMMA

© CEMMA

Silva et al. (2014). Hydrobiologia. Online first.

Combination of new records and existing literature-based records

•A total of 54 confirmed host species.

•They belong to diverse taxonomic groups and exhibit different morphological,

physiological and ecological patterns.

•Low degree of host selection (the main selection factor seems to be the host size with

larger individuals or species being preferred)

•Wide range of habitats during haematophagous stage (from fresh and brackish waters to

open sea).

•Freshwater feeding by early postmetamorphic sea lampreys as a widespread behaviour

in anadromous populations of P. marinus in their native range.

•Marine distribution of P. marinus mainly related to coastal areas with part of the

population widely dispersed in offshore areas.

•So, high plasticity during the haematophagous stage related to habitats and host

species.

Acknowledgements

The authors thank the staff of the Hydrobiology Station “Encoro do Con” (USC), the staff of Ximonde

Permanent Trap (Xunta de Galicia), Dr. Carlos Antunes (CIIMAR-UP), Dr. John B. Hume (University of

Glasgow), Dr. Richard Sabatié (ENSAR-FR), Dr. Rodrigo López (PAISASIGMO), Rafael Bañon (UTPB-

Xunta de Galicia), Manuel E. Garci (IIM-CSIC), CEMMA, CEPESMA, scientific crew of Vizconde de Eza

Oceanographic Vessel, commercial vessels “Ameal” and “Amel”, Skipper A. Blanco (“Casca”, Bueu),

Skipper P. Castro (MERAK, Galicia), João Araújo and Napoleão Rodrigues (fishermen of River Minho),

Vasco Presa (fisherman of V. P. Âncora) and Xulio Valeiras (IEO) for their important collaboration. The

authors are also grateful to Dr. Martyn C. Lucas (University of Durham) for his valuable comments. This

study has been partially supported by the project 10PXIB2111059PR of Xunta de Galicia and the project

MIGRANET of the Interreg IV B SUDOE (South-West Europe) Territorial Cooperation Programme

(SOE2/P2/E288).