- Email: [email protected]
Evidence for the decline and possible extinction of a marine parasite species caused by intensive fishing
Fisheries Research xxx (xxxx) xxx–xxx
Contents lists available at ScienceDirect
Fisheries Research journal homepage: www.elsevier.com/locate/fishres
Short communication
Evidence for the decline and possible extinction of a marine parasite species caused by intensive fishing ⁎
Ken MacKenziea, , Campbell Pertb a b
School of Biological Sciences (Zoology), The University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, Scotland, UK Marine Scotland Marine Laboratory, 375 Victoria Road, Aberdeen AB11 9DB, Scotland, UK
A R T I C L E I N F O
A B S T R A C T
Handled by B. Morales-Nin
The first good evidence of the role of intensive commercial fishing in the decline and possible extinction of a marine parasite is presented. The larva of Stichocotyle nephropis Cunningham, 1887 (Aspidogastrea: Digenea) was described in 1887 from the outside of the intestine of the decapod crustacean Nephrops norvegicus (L., 1758) in the North Sea. Similar larvae were found outside the intestine of the American lobster Homarus americanus (Milne-Edwards, 1837) caught off New England in 1895. The adult form was first found in 1898 in the bile ducts of the thornback ray Raja clavata (L., 1758) from the North Sea, then in the barndoor skate Dipturus laevis (Mitchill, 1818) caught off Nantucket. There have been few records of its occurrence since then, with the last records from the northeast and northwest Atlantic published in 1972 and 1986 respectively, despite the recent attempts reported herein to find larvae and adult parasites. Both the elasmobranch final hosts are listed as “near threatened” or “ endangered” and the latest evidence on their population sizes suggests that they may have been fished to below the thresholds required for successful transmission of the parasite.
Keywords: Stichocotyle nephropis Parasite extinction Intensive fishing
1. Introduction The negative effects of parasites on commercial fisheries are fairly well documented. There are reports of marine parasites causing mass mortalities of commercially important fish species (Yamamoto et al., 1984), and there are reports of loss of fish biomass due to parasitic infections through loss of condition (Brooker et al., 2007) or reduced fecundity (Pinto, 1956). Parasites can also cause spoilage of fish products through the presence of highly visible macroparasites in the product (Burt, 1994), or by changes in texture caused by enzymes released by microparasites rendering the product unmarketable (Moran et al., 1999). The converse relationship – the effects of fisheries on parasites – is less well documented. It has been hypothesised that commercial fishing could drive fish populations below the threshold density for transmission of some of their parasites (Dobson and May, 1987). This may be regarded as a desirable outcome for fisheries affected by parasites that cause mortalities, decrease condition or cause spoilage, but it could have serious ecological implications. The latter were addressed by Wood et al. (2010), who argued that the removal of fish from the oceans over a long period of time may be driving a long-term global decline in fish parasites. These authors argued that parasites are a critical and influential part of biodiversity and that their loss could
⁎
substantially alter ecosystem function. They referred to an example of a freshwater fish parasite probably rendered locally extinct through being entirely “fished out” of its host population in some Canadian lakes (Black, 1983), but they were unable to find a similar example in the marine environment due to lack of empirical data. This has remained the situation until now, but herein we present evidence of the decline and possible extinction of a marine parasite species hastened by intensive fishing of its definitive hosts. 2. The parasite and its historical records Stichocotyle nephropis Cunningham, 1887 is a member of the Aspidogastrea, a sub-class of the class Digenea. Its larval stage was found and described by Cunningham (1887) encysted on the outside of the intestine of the decapod crustacean Nephrops norvegicus (L., 1758) in the North Sea. The adult form was found later by Odhner (1898) from the bile ducts of the thornback ray Raja clavata (L., 1758) caught in the eastern North Sea. On the other side of the Atlantic, Nickerson (1895) reported and described S. nephropis larvae from 1 to 2% of more than 500 American lobsters Homarus americanus (Milne-Edwards, 1837) caught off New England. The final host in the northwest Atlantic was not identified until much later, when Linton (1940) reported a single adult worm from an unnamed infection site in a barndoor skate Dipturus
Corresponding author. E-mail address: [email protected] (K. MacKenzie).
http://dx.doi.org/10.1016/j.fishres.2017.10.014 Received 5 June 2017; Received in revised form 12 October 2017; Accepted 20 October 2017 0165-7836/ © 2017 Elsevier B.V. All rights reserved.
Please cite this article as: MacKenzie, K., Fisheries Research (2017), http://dx.doi.org/10.1016/j.fishres.2017.10.014
Fisheries Research xxx (xxxx) xxx–xxx
K. MacKenzie, C. Pert
the thornback ray. Radujkovic and Raibaut (1989) carried out complete parasitological examinations of 11 specimens from the Adriatic Sea but did not report S. nephropis. Similarly, Rocha et al. (2013) examined the gills and viscera, including the livers, of 29 specimens from the northwest Atlantic coast of Portugal without a mention of S. nephropis. In Scottish waters, thornback rays were found to be active predators on N. norvegicus, their remains being found in the stomach contents of almost 52% of rays examined (Thomas, 1965). Nephrops norvegicus is distributed from Iceland and north Norway south to Portugal. It is not common in the Mediterranean, except for the Adriatic. Its distribution is very patchy and discontinuous due to its preference for a particular type of sediment (Bell et al., 2006). Most parasitological studies on N. nephropis have focused on a pathogenic dinoflagellate of the genus Hematodinium (see Stentiford and Neil, 2011), with the only reports of infections with S. nephropis coming from British (mainly Scottish) coastal waters. In the period 2000–2002 catches from the North Sea, west of Scotland and the Irish Sea accounted for about 35% of the total catch of N. norvegicus (Bell et al., 2006). The Scottish fishery is now the second most valuable fishery in Scotland with total landings in 2014 of over 20,000 t worth £73 million. The health of most stocks is generally considered to be stable (Marine Scotland Science, 2016).
laevis (Mitchill, 1818) caught off Nantucket. Linton (1940) also reported larvae from the rectum of lobsters, but gave no infection data. Montrieul (1954) reported S. nephropis from lobsters caught off Nova Scotia and New Brunswick, but provided no infection data, while Boghen (1978) found no S. nephropis in a sample of 233 lobsters caught off New Brunswick. The final record – that of Brattey and Campbell (1986) – was of one infected lobster in a sample of 885 caught in Canadian Atlantic waters in the period 1980–1982. In the same year, Van Engel et al. (1986) examined the intestines and rectums of 218 lobsters caught off southern New England from August 1975 to March 1977; none was infected with S. nephropis. We have found no further reports of adults from barndoor skate or any other skate in the northwest Atlantic. There is a similar dearth of records from the northeast Atlantic until the publication of two surveys of the occurrence and distribution of S. nephropis larvae in N. norvegicus from British waters by MacKenzie (1963) and Symonds (1972). Whereas Cunningham (1887) had reported S. nephropis infecting 25–33% of N. norvegicus from the Firth of Forth on the east coast of Scotland, neither MacKenzie (1963) or Symonds (1972) found any infected N. norvegicus in the northeastern North Sea. Both surveys were carried out during the period 1962–1964 and recorded S. nephropis from northwest Scotland south to the Bristol Channel and Celtic Sea, with the highest prevalences of up to 48% in large host individuals from northwest Scotland. The only report of adult S. nephropis from thornback ray since that of Odhner (1898) was that of MacKenzie (1963), who found it in one of 14 thornback rays caught off the west coast of Scotland. The present status of S. nephropis was first brought to our attention when the senior author received a request in 2001 from staff of the Natural History Museum in London for specimens of S. nephropis for genetic analysis. About 20 specimens of large N. norvegicus were collected from an area off the west coast of Scotland where the highest prevalence of infection had previously been recorded. None was infected. Since then the senior author has examined several hundred N. norvegicus from areas where it was previously common and none has been infected. Efforts by staff of the Natural History Museum to obtain specimens from various sources on both sides of the Atlantic have similarly failed to find a single specimen of this parasite (Dr T. Littlewood, pers. comm.). In 2012 the present authors decided to carry out another search for S. nephropis in Scottish waters. A total of 1247 N. norvegicus from the west of Scotland and 120 from the Moray Firth on the east coast were examined for S. nephropis, but none was found to be infected. Then in 2014 we examined the livers of 32 thornback rays caught off the west of Scotland for the adult parasite; again none was infected.
3.2. Northwest Atlantic The barndoor skate is distributed from the Grand banks and southern Gulf of St. Lawrence south to North Carolina (Froese and Pauly, 2016). Casey and Myers (1998) reported that long-term research surveys on the continental shelf between the Grand Banks of Newfoundland and southern New England revealed the barndoor skate as being “…close to extinction”. Forty-five years earlier, research surveys off southern Newfoundland had recorded this skate in 10% of their tows, but none had been caught in the past 20 years. Roberts et al. (1998) also considered the barndoor skate to be “…threatened with extinction by intensive trawling.” However, a more recent study by Gedamke et al. (2005) has suggested that the barndoor skate may be more resilient to overfishing than previously believed. There have been few studies of the parasites infecting barndoor skate, apart from those referred to in the previous section. Schmitt et al. (2015) investigated the diet of barndoor skate in the Gulf of Maine. They found that they fed on a variety of crustaceans and teleost fish, with the latter becoming more prominent in larger skate. The barndoor skate is listed as “Endangered” in the IUCN Redlist 2016 (IUCN, 2016). The American lobster has a distribution similar to that of the barndoor skate – from Labrador south to North Carolina (Cobb and Castro, 2006). The most recent surveys of the parasites infecting American lobsters were carried out by Brattey and Campbell (1986) and Van Engel et al. (1986), with only the former reporting S. nephropis. Reported landings of American lobster are currently at or near historically high levels, with record high stock abundance and recruitment (Cobb and Castro, 2006; McMahan et al., 2016).
3. The host species: distributions, current status and diet 3.1. Northeast Atlantic The thornback ray is distributed in the Northeast Atlantic from Iceland and North Norway south to Morocco and Namibia, including the Mediterranean and Black Seas (Froese and Pauly, 2016). No fishery has specifically targeted this species, but it is readily caught as a bycatch. In British waters the most notable decline in abundance of the more common species of ray in the latter half of the 20th century was that for R. clavata (see Dulvey et al., 2000). Rogers and Ellis (2000) compared catch data from research surveys in British coastal waters from the periods 1901–1907 and 1989–1997 and reported that all rays of intermediate body size showed marked declines in relative abundance, but especially Raja brachyura and thornback ray. In the Irish Sea thornback ray showed by far the greatest decrease in abundance of any fish species. In the North Sea there has been a 50% decrease in catches of thornback rays since the 1950s and the remaining population is now centred in the Thames estuary in the southern North Sea (Wiegand et al., 2011). The IUCN Redlist 2016 (IUCN, 2016) lists the thornback ray as “Near threatened”. There have been few parasitological studies of
4. Discussion The evidence presented above shows a marked decline in the occurrence of S. nephropis on both sides of the North Atlantic over the past century. Such a decline is indicative of a reduced rate of transmission between the hosts of the different stages in the parasite’s life cycle, which is usually the result of a decrease in the population density of at least one of its main host species. If the density of a host population falls below the threshold level necessary for successful transmission, the result may be a complete failure of transmission and local extinction of the parasite (Dobson and May, 1987; Wood et al., 2014). Climate change in recent decades must also be considered as a possible factor in the decline of S. nephropis. Many of the effects of climate change on parasites will be indirect, mediated through effects on the distribution 2
Fisheries Research xxx (xxxx) xxx–xxx
K. MacKenzie, C. Pert
Black, G.A., 1983. Taxonomy of a swimbladder nematode, Cystidicola stigmatura (Leidy), and evidence of its decline in the Great Lakes. Can. J. Fish. Aquat. Sci. 40, 643–647. Boghen, A.D., 1978. A parasitological survey of the American lobster Homarus americanus from Northumberland Strait, Southern Gulf of St. Lawrence. Can. J. Zool. 56, 2460–2462. Brattey, J., Campbell, A., 1986. A survey of parasites of the American lobster, Homarus americanus (Crustacea Decapoda), from the Canadian Maritimes. Can. J. Zool. 64, 1998–2003. Brooker, A.J., Shinn, A.P., Bron, J.E., 2007. A review of the biology of the parasitic copepod Lernaeocera branchialis (L. 1767) (Copepoda: Pennellidae). Adv. Parasitol. 65, 297–341. Burt, M.D.B., 1994. The sealworm situation. Parasitic and Infectious Diseases. Academic Press, Inc, New York, pp. 347–362. Casey, J.M., Myers, R.A., 1998. Near extinction of a large, widely-distributed fish. Science 281, 690–691. Cobb, J.S., Castro, K.M., 2006. Homarus species. In: Phillips, Bruce F. (Ed.), Lobsters: Biology, Management, Aquaculture and Fisheries. Wiley-Blackwell, Oxford, pp. 310–339. Cunningham, J.T., 1887. On Stichocotyle nephropis. A new trematode. Trans. R. Soc. Edinb. 32, 273. Dobson, A.P., May, R.M., 1987. The effects of parasites on fish populations – theoretical aspects. Int. J. Parasitol. 17, 363–370. Dulvey, N.K., Metcalfe, J.D., Glanville, J., Pawson, M.G., Reynolds, J.D., 2000. Fishery stability, local extinctions and shifts in community structure in skates. Conserv. Biol. 14, 283–293. Froese, R., Pauly, D. (Eds.), 2016. FishBase. World Wide Web Electronic Publication. www. fishbase.org.version10/2016. Gedamke, T., DuPaul, W., Musick, J.A., 2005. Observations on the life history of the barndoor skate, Dipturus laevis, on Georges Bank (Western North Atlantic). J. Northw. Atl. Fish. Sci. 35, 67–78. IUCN, 2016. IUCN Red List of Threatened Species. Version 2016.1. Linton, E., 1940. Trematodes from fishes mainly from the Woods Hole region, Massachusetts. Proc. U. S. Natl. Mus. 88, 1–172. MacKenzie, K., 1963. Stichocotyle nephropis Cunningham, 1887 (Trematoda) in Scottish waters. Ann. Mag. Nat. Hist. Ser. 13 6, 505. Marcogliese, D.J., 2001. Implications of climate change for parasitism of animals in the aquatic environment. Can. J. Zool. 79, 1331–1352. Marine Scotland Science, 2016. Fish and Shellfish Stocks 2016 Edition. Available: http://www. gov.scot/Resource/0050/00500638.pdf. (Accessed 27 March 2017). McMahan, M.D., Cowan, D.F., Chen, Y., Sherwood, G.D., Grabowski, J.H., 2016. Growth of juvenile American lobster Homarus americanus in a changing environment. Mar. Ecol. Progr. Ser. 557, 177–187. Montrieul, P., 1954. Parasitological investigations. Rapp. Ann. Stat. Biol. Mar., 1953, Appendice V. Département des Pêches, Québéc, pp. 69–73 Contr. No. 50. Moran, J.D.W., Whitaker, D.J., Kent, M.L., 1999. A review of the myxosporean genus Kudoa Meglitsch, 1947, and its impact on the international aquaculture industry and commercial fisheries. Aquaculture 172, 163–196. Nickerson, W.S., 1895. On Stichocotyle nephropis Cunningham, a parasite of the American lobster. Zool. J. Anat. 8, 447–480. Odhner, T., 1898. Ueber die geschlechtsreife Form von Stichocotyle nephropis Cunningham. Zool. Anz. 21, 509–513. Pinto, J.S., 1956. Parasitic castration in males of Sardina pilchardus (Walb.) due to testicular infestation by the coccidian Eimeria sardinae (Thélohan). Rev. Fac. Cienc. Univ. Lisboa Serie C 5, 209–214. Radujkovic, B.M., Raibaut, A., 1989. Faune des parasites de poisons marins de côtes du Montenegro. Acta Adriatica 30, 5–12. Roberts, C.M., Hawkins, J.P., Chapman, N., Clarke, V., Morris, A.V., Miller, R., Richards, A., 1998. The threatened status of marine species. A Report to the World Conservation Union (IUCN), Species Survival Commission, and Center for Marine Conservation, Washington, D.C. 10 pp. Rocha, S., Casal, G., Al-Quraishy. Azevedo, C., 2013. Morphological and molecular characterization of a new myxozoan species (Myxosporea) infecting the gall bladder of Raja clavata (Chondrichthyes), from the Portuguese Atlantic coast. J. Parasitol. 99, 307–317. Rogers, S.I., Ellis, J.R., 2000. Changes in the demersal fish assemblages of British coastal waters during the 20th century. ICES J. Mar. Sci. 57, 866–881. Schmitt, J.D., Gedamke, T., DuPaul, W.D., Musick, J.A., 2015. Ontogenic and sex-specific shifts in the feeding habits of the barndoor skate. Mar. Coast. Fish.: Dyn. Manag. Ecosyst. Sci. 7, 409–418. Stentiford, G.D., Neil, D.M., 2011. Diseases of Nephrops and Metanephrops: a review. J. Invert. Pathol. 106, 92–109. Symonds, D., 1972. Infestation of Nephrops norvegicus (L.) by Stichocotyle nephropis Cunningham in British waters. J. Nat. Hist. 6, 423–426. Thomas, H.J., 1965. The white fish communities associated with Nephrops norvegicus (L.) and the by-catch of white fish in the Norway lobster fishery, together with notes on Norway lobster predators. Rapp. Proc. Verb. Réun. Cons. Perm. Int. Explor. Mer 156, 155–160. Van Engel, W.A., Harris Jr., R.E., Zwerner, D.E., 1986. Occurrence of some parasites and a commensal in the American lobster, Homarus americanus, from the Mid-Atlantic Bight. Fish. Bull. 84, 197–200. Walker, P.A., Heessen, H.J.L., 1996. Long-term changes in ray populations in the North Sea. ICES J. Mar. Sci. 53, 1085–1093. Wiegand, J., Hunter, E., Dulvy, N.K., 2011. Are spatial closures better than size limits for halting the decline of the North Sea thornback ray, Raja clavata? Mar. Freshw. Res. 62, 722–733. Wood, C.L., Lafferty, K., Micheli, F., 2010. Fishing out marine parasites?: Impacts of fishing on rates of parasitism in the ocean. Ecol. Lett. 13, 761–775. Wood, C.L., Sandin, S.A., Zgliczynski, B., Guerra, A.S., Micheli, F., 2014. Fishing drives decline in fish parasite diversity and has variable effects on parasite abundance. Ecology 95, 1929–1946. Yamamoto, K., Takagi, S., Matsuoka, S., 1984. Mass mortality of the Japanese anchovy (Engraulis japonica) caused by a gill monogenean Pseudanthocotyloides sp. (Mazocreidae) in the Sea of Iyo (“Iyo-nada”), Ehime Prefecture. Fish Pathol. 9, 119–123.
and abundance of their hosts (Marcogliese, 2001). These effects are likely to be felt more at the edges of the geographical distributions than in the core areas. Increasing sea temperatures in the Northeast Atlantic in recent years have already pushed the distribution of N. norvegicus further north, with individuals being caught in trawls around the Lofoten Islands, off northwest Norway (personal observations), where they had never been seen before. On both sides of the North Atlantic, the findings of both larval and adult stages of S. nephropis were from well within the core areas of their hosts’ distributions. The populations of the only known hosts of the larval stage of S. nephropis – Nephrops norvegicus and the American lobster – appear to be stable, but this is clearly not the case for the two known hosts of the adult stage, both of which have shown drastic decreases in population density over the past century. It is possible, of course, that as yet undiscovered populations of S. nephropis still exist, but the evidence strongly suggests that S. nephropis is now locally extinct in the core part of its known former geographical distribution. Its distribution in the Northeast Atlantic is likely to have been shrinking prior to the surveys of the early 1960s, because by then it seemed to have disappeared from its type locality in the North Sea. Landings of all ray species from the North Sea decreased significantly during the 1930s (Walker and Heessen, 1996), suggesting that ray populations were already decreasing at that time. The main population of thornback rays is now located in the southwestern part of the North Sea while the main population of N. norvegicus is in the northern North Sea. This disconnection would seriously reduce the parasite’s chances of successful transmission. The evidence thus suggests that overfishing of its final host species has at least hastened the decline and possibly led to the extinction of S. nephropis. We are not the first to suggest this: Stentiford and Neil (2011) commented “Whether evidence for reduced prevalence of S. nephropis in N. norvegicus may act as a surrogate for data pertaining to reductions in stock abundance of elasmobranchs such as R. clavata requires further assessment…” The parasites identified as S. nephropis on opposite sides of the North Atlantic are separated by most of the width of that ocean. The distributions of the intermediate and final hosts of each are limited to their own side of the Atlantic and none of them occurs in the intervening area, so it is likely that the two parasites were similar but separate species. Stichocotyle nephropis is the sole member of its genus and family. If it has become extinct, then we will have lost a unique species that has left very few records of its existence. We know virtually nothing of its biology and we have no idea what effects it may have had on the health and behaviour of any of its hosts. This is the first good evidence from the marine environment of a parasite species possibly rendered extinct by intensive fishing. Wood et al. (2014) concluded that trophically transmitted parasites appear to be sensitive to fishing impacts and might be at risk of local extirpation in fished environments. The narrow host specificity of S. nephropis to final host species that are particularly vulnerable to intensive fishing probably hastened its decline and possible extinction. Acknowledgements The authors thank Adrian Weetman and his staff for collecting samples during a research cruise aboard FRV “Scotia”. We are also grateful to Dr Tim Littlewood for his contribution in the form of a personal communication. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. References Bell, M.C., Redant, R., Tuck, I., 2006. Nephrops species. In: Phillips, Bruce F. (Ed.), Lobsters: Biology, Management, Aquaculture and Fisheries. Wiley-Blackwell, Oxford, pp. 42–461.
3
Contents lists available at ScienceDirect
Fisheries Research journal homepage: www.elsevier.com/locate/fishres
Short communication
Evidence for the decline and possible extinction of a marine parasite species caused by intensive fishing ⁎
Ken MacKenziea, , Campbell Pertb a b
School of Biological Sciences (Zoology), The University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, Scotland, UK Marine Scotland Marine Laboratory, 375 Victoria Road, Aberdeen AB11 9DB, Scotland, UK
A R T I C L E I N F O
A B S T R A C T
Handled by B. Morales-Nin
The first good evidence of the role of intensive commercial fishing in the decline and possible extinction of a marine parasite is presented. The larva of Stichocotyle nephropis Cunningham, 1887 (Aspidogastrea: Digenea) was described in 1887 from the outside of the intestine of the decapod crustacean Nephrops norvegicus (L., 1758) in the North Sea. Similar larvae were found outside the intestine of the American lobster Homarus americanus (Milne-Edwards, 1837) caught off New England in 1895. The adult form was first found in 1898 in the bile ducts of the thornback ray Raja clavata (L., 1758) from the North Sea, then in the barndoor skate Dipturus laevis (Mitchill, 1818) caught off Nantucket. There have been few records of its occurrence since then, with the last records from the northeast and northwest Atlantic published in 1972 and 1986 respectively, despite the recent attempts reported herein to find larvae and adult parasites. Both the elasmobranch final hosts are listed as “near threatened” or “ endangered” and the latest evidence on their population sizes suggests that they may have been fished to below the thresholds required for successful transmission of the parasite.
Keywords: Stichocotyle nephropis Parasite extinction Intensive fishing
1. Introduction The negative effects of parasites on commercial fisheries are fairly well documented. There are reports of marine parasites causing mass mortalities of commercially important fish species (Yamamoto et al., 1984), and there are reports of loss of fish biomass due to parasitic infections through loss of condition (Brooker et al., 2007) or reduced fecundity (Pinto, 1956). Parasites can also cause spoilage of fish products through the presence of highly visible macroparasites in the product (Burt, 1994), or by changes in texture caused by enzymes released by microparasites rendering the product unmarketable (Moran et al., 1999). The converse relationship – the effects of fisheries on parasites – is less well documented. It has been hypothesised that commercial fishing could drive fish populations below the threshold density for transmission of some of their parasites (Dobson and May, 1987). This may be regarded as a desirable outcome for fisheries affected by parasites that cause mortalities, decrease condition or cause spoilage, but it could have serious ecological implications. The latter were addressed by Wood et al. (2010), who argued that the removal of fish from the oceans over a long period of time may be driving a long-term global decline in fish parasites. These authors argued that parasites are a critical and influential part of biodiversity and that their loss could
⁎
substantially alter ecosystem function. They referred to an example of a freshwater fish parasite probably rendered locally extinct through being entirely “fished out” of its host population in some Canadian lakes (Black, 1983), but they were unable to find a similar example in the marine environment due to lack of empirical data. This has remained the situation until now, but herein we present evidence of the decline and possible extinction of a marine parasite species hastened by intensive fishing of its definitive hosts. 2. The parasite and its historical records Stichocotyle nephropis Cunningham, 1887 is a member of the Aspidogastrea, a sub-class of the class Digenea. Its larval stage was found and described by Cunningham (1887) encysted on the outside of the intestine of the decapod crustacean Nephrops norvegicus (L., 1758) in the North Sea. The adult form was found later by Odhner (1898) from the bile ducts of the thornback ray Raja clavata (L., 1758) caught in the eastern North Sea. On the other side of the Atlantic, Nickerson (1895) reported and described S. nephropis larvae from 1 to 2% of more than 500 American lobsters Homarus americanus (Milne-Edwards, 1837) caught off New England. The final host in the northwest Atlantic was not identified until much later, when Linton (1940) reported a single adult worm from an unnamed infection site in a barndoor skate Dipturus
Corresponding author. E-mail address: [email protected] (K. MacKenzie).
http://dx.doi.org/10.1016/j.fishres.2017.10.014 Received 5 June 2017; Received in revised form 12 October 2017; Accepted 20 October 2017 0165-7836/ © 2017 Elsevier B.V. All rights reserved.
Please cite this article as: MacKenzie, K., Fisheries Research (2017), http://dx.doi.org/10.1016/j.fishres.2017.10.014
Fisheries Research xxx (xxxx) xxx–xxx
K. MacKenzie, C. Pert
the thornback ray. Radujkovic and Raibaut (1989) carried out complete parasitological examinations of 11 specimens from the Adriatic Sea but did not report S. nephropis. Similarly, Rocha et al. (2013) examined the gills and viscera, including the livers, of 29 specimens from the northwest Atlantic coast of Portugal without a mention of S. nephropis. In Scottish waters, thornback rays were found to be active predators on N. norvegicus, their remains being found in the stomach contents of almost 52% of rays examined (Thomas, 1965). Nephrops norvegicus is distributed from Iceland and north Norway south to Portugal. It is not common in the Mediterranean, except for the Adriatic. Its distribution is very patchy and discontinuous due to its preference for a particular type of sediment (Bell et al., 2006). Most parasitological studies on N. nephropis have focused on a pathogenic dinoflagellate of the genus Hematodinium (see Stentiford and Neil, 2011), with the only reports of infections with S. nephropis coming from British (mainly Scottish) coastal waters. In the period 2000–2002 catches from the North Sea, west of Scotland and the Irish Sea accounted for about 35% of the total catch of N. norvegicus (Bell et al., 2006). The Scottish fishery is now the second most valuable fishery in Scotland with total landings in 2014 of over 20,000 t worth £73 million. The health of most stocks is generally considered to be stable (Marine Scotland Science, 2016).
laevis (Mitchill, 1818) caught off Nantucket. Linton (1940) also reported larvae from the rectum of lobsters, but gave no infection data. Montrieul (1954) reported S. nephropis from lobsters caught off Nova Scotia and New Brunswick, but provided no infection data, while Boghen (1978) found no S. nephropis in a sample of 233 lobsters caught off New Brunswick. The final record – that of Brattey and Campbell (1986) – was of one infected lobster in a sample of 885 caught in Canadian Atlantic waters in the period 1980–1982. In the same year, Van Engel et al. (1986) examined the intestines and rectums of 218 lobsters caught off southern New England from August 1975 to March 1977; none was infected with S. nephropis. We have found no further reports of adults from barndoor skate or any other skate in the northwest Atlantic. There is a similar dearth of records from the northeast Atlantic until the publication of two surveys of the occurrence and distribution of S. nephropis larvae in N. norvegicus from British waters by MacKenzie (1963) and Symonds (1972). Whereas Cunningham (1887) had reported S. nephropis infecting 25–33% of N. norvegicus from the Firth of Forth on the east coast of Scotland, neither MacKenzie (1963) or Symonds (1972) found any infected N. norvegicus in the northeastern North Sea. Both surveys were carried out during the period 1962–1964 and recorded S. nephropis from northwest Scotland south to the Bristol Channel and Celtic Sea, with the highest prevalences of up to 48% in large host individuals from northwest Scotland. The only report of adult S. nephropis from thornback ray since that of Odhner (1898) was that of MacKenzie (1963), who found it in one of 14 thornback rays caught off the west coast of Scotland. The present status of S. nephropis was first brought to our attention when the senior author received a request in 2001 from staff of the Natural History Museum in London for specimens of S. nephropis for genetic analysis. About 20 specimens of large N. norvegicus were collected from an area off the west coast of Scotland where the highest prevalence of infection had previously been recorded. None was infected. Since then the senior author has examined several hundred N. norvegicus from areas where it was previously common and none has been infected. Efforts by staff of the Natural History Museum to obtain specimens from various sources on both sides of the Atlantic have similarly failed to find a single specimen of this parasite (Dr T. Littlewood, pers. comm.). In 2012 the present authors decided to carry out another search for S. nephropis in Scottish waters. A total of 1247 N. norvegicus from the west of Scotland and 120 from the Moray Firth on the east coast were examined for S. nephropis, but none was found to be infected. Then in 2014 we examined the livers of 32 thornback rays caught off the west of Scotland for the adult parasite; again none was infected.
3.2. Northwest Atlantic The barndoor skate is distributed from the Grand banks and southern Gulf of St. Lawrence south to North Carolina (Froese and Pauly, 2016). Casey and Myers (1998) reported that long-term research surveys on the continental shelf between the Grand Banks of Newfoundland and southern New England revealed the barndoor skate as being “…close to extinction”. Forty-five years earlier, research surveys off southern Newfoundland had recorded this skate in 10% of their tows, but none had been caught in the past 20 years. Roberts et al. (1998) also considered the barndoor skate to be “…threatened with extinction by intensive trawling.” However, a more recent study by Gedamke et al. (2005) has suggested that the barndoor skate may be more resilient to overfishing than previously believed. There have been few studies of the parasites infecting barndoor skate, apart from those referred to in the previous section. Schmitt et al. (2015) investigated the diet of barndoor skate in the Gulf of Maine. They found that they fed on a variety of crustaceans and teleost fish, with the latter becoming more prominent in larger skate. The barndoor skate is listed as “Endangered” in the IUCN Redlist 2016 (IUCN, 2016). The American lobster has a distribution similar to that of the barndoor skate – from Labrador south to North Carolina (Cobb and Castro, 2006). The most recent surveys of the parasites infecting American lobsters were carried out by Brattey and Campbell (1986) and Van Engel et al. (1986), with only the former reporting S. nephropis. Reported landings of American lobster are currently at or near historically high levels, with record high stock abundance and recruitment (Cobb and Castro, 2006; McMahan et al., 2016).
3. The host species: distributions, current status and diet 3.1. Northeast Atlantic The thornback ray is distributed in the Northeast Atlantic from Iceland and North Norway south to Morocco and Namibia, including the Mediterranean and Black Seas (Froese and Pauly, 2016). No fishery has specifically targeted this species, but it is readily caught as a bycatch. In British waters the most notable decline in abundance of the more common species of ray in the latter half of the 20th century was that for R. clavata (see Dulvey et al., 2000). Rogers and Ellis (2000) compared catch data from research surveys in British coastal waters from the periods 1901–1907 and 1989–1997 and reported that all rays of intermediate body size showed marked declines in relative abundance, but especially Raja brachyura and thornback ray. In the Irish Sea thornback ray showed by far the greatest decrease in abundance of any fish species. In the North Sea there has been a 50% decrease in catches of thornback rays since the 1950s and the remaining population is now centred in the Thames estuary in the southern North Sea (Wiegand et al., 2011). The IUCN Redlist 2016 (IUCN, 2016) lists the thornback ray as “Near threatened”. There have been few parasitological studies of
4. Discussion The evidence presented above shows a marked decline in the occurrence of S. nephropis on both sides of the North Atlantic over the past century. Such a decline is indicative of a reduced rate of transmission between the hosts of the different stages in the parasite’s life cycle, which is usually the result of a decrease in the population density of at least one of its main host species. If the density of a host population falls below the threshold level necessary for successful transmission, the result may be a complete failure of transmission and local extinction of the parasite (Dobson and May, 1987; Wood et al., 2014). Climate change in recent decades must also be considered as a possible factor in the decline of S. nephropis. Many of the effects of climate change on parasites will be indirect, mediated through effects on the distribution 2
Fisheries Research xxx (xxxx) xxx–xxx
K. MacKenzie, C. Pert
Black, G.A., 1983. Taxonomy of a swimbladder nematode, Cystidicola stigmatura (Leidy), and evidence of its decline in the Great Lakes. Can. J. Fish. Aquat. Sci. 40, 643–647. Boghen, A.D., 1978. A parasitological survey of the American lobster Homarus americanus from Northumberland Strait, Southern Gulf of St. Lawrence. Can. J. Zool. 56, 2460–2462. Brattey, J., Campbell, A., 1986. A survey of parasites of the American lobster, Homarus americanus (Crustacea Decapoda), from the Canadian Maritimes. Can. J. Zool. 64, 1998–2003. Brooker, A.J., Shinn, A.P., Bron, J.E., 2007. A review of the biology of the parasitic copepod Lernaeocera branchialis (L. 1767) (Copepoda: Pennellidae). Adv. Parasitol. 65, 297–341. Burt, M.D.B., 1994. The sealworm situation. Parasitic and Infectious Diseases. Academic Press, Inc, New York, pp. 347–362. Casey, J.M., Myers, R.A., 1998. Near extinction of a large, widely-distributed fish. Science 281, 690–691. Cobb, J.S., Castro, K.M., 2006. Homarus species. In: Phillips, Bruce F. (Ed.), Lobsters: Biology, Management, Aquaculture and Fisheries. Wiley-Blackwell, Oxford, pp. 310–339. Cunningham, J.T., 1887. On Stichocotyle nephropis. A new trematode. Trans. R. Soc. Edinb. 32, 273. Dobson, A.P., May, R.M., 1987. The effects of parasites on fish populations – theoretical aspects. Int. J. Parasitol. 17, 363–370. Dulvey, N.K., Metcalfe, J.D., Glanville, J., Pawson, M.G., Reynolds, J.D., 2000. Fishery stability, local extinctions and shifts in community structure in skates. Conserv. Biol. 14, 283–293. Froese, R., Pauly, D. (Eds.), 2016. FishBase. World Wide Web Electronic Publication. www. fishbase.org.version10/2016. Gedamke, T., DuPaul, W., Musick, J.A., 2005. Observations on the life history of the barndoor skate, Dipturus laevis, on Georges Bank (Western North Atlantic). J. Northw. Atl. Fish. Sci. 35, 67–78. IUCN, 2016. IUCN Red List of Threatened Species. Version 2016.1. Linton, E., 1940. Trematodes from fishes mainly from the Woods Hole region, Massachusetts. Proc. U. S. Natl. Mus. 88, 1–172. MacKenzie, K., 1963. Stichocotyle nephropis Cunningham, 1887 (Trematoda) in Scottish waters. Ann. Mag. Nat. Hist. Ser. 13 6, 505. Marcogliese, D.J., 2001. Implications of climate change for parasitism of animals in the aquatic environment. Can. J. Zool. 79, 1331–1352. Marine Scotland Science, 2016. Fish and Shellfish Stocks 2016 Edition. Available: http://www. gov.scot/Resource/0050/00500638.pdf. (Accessed 27 March 2017). McMahan, M.D., Cowan, D.F., Chen, Y., Sherwood, G.D., Grabowski, J.H., 2016. Growth of juvenile American lobster Homarus americanus in a changing environment. Mar. Ecol. Progr. Ser. 557, 177–187. Montrieul, P., 1954. Parasitological investigations. Rapp. Ann. Stat. Biol. Mar., 1953, Appendice V. Département des Pêches, Québéc, pp. 69–73 Contr. No. 50. Moran, J.D.W., Whitaker, D.J., Kent, M.L., 1999. A review of the myxosporean genus Kudoa Meglitsch, 1947, and its impact on the international aquaculture industry and commercial fisheries. Aquaculture 172, 163–196. Nickerson, W.S., 1895. On Stichocotyle nephropis Cunningham, a parasite of the American lobster. Zool. J. Anat. 8, 447–480. Odhner, T., 1898. Ueber die geschlechtsreife Form von Stichocotyle nephropis Cunningham. Zool. Anz. 21, 509–513. Pinto, J.S., 1956. Parasitic castration in males of Sardina pilchardus (Walb.) due to testicular infestation by the coccidian Eimeria sardinae (Thélohan). Rev. Fac. Cienc. Univ. Lisboa Serie C 5, 209–214. Radujkovic, B.M., Raibaut, A., 1989. Faune des parasites de poisons marins de côtes du Montenegro. Acta Adriatica 30, 5–12. Roberts, C.M., Hawkins, J.P., Chapman, N., Clarke, V., Morris, A.V., Miller, R., Richards, A., 1998. The threatened status of marine species. A Report to the World Conservation Union (IUCN), Species Survival Commission, and Center for Marine Conservation, Washington, D.C. 10 pp. Rocha, S., Casal, G., Al-Quraishy. Azevedo, C., 2013. Morphological and molecular characterization of a new myxozoan species (Myxosporea) infecting the gall bladder of Raja clavata (Chondrichthyes), from the Portuguese Atlantic coast. J. Parasitol. 99, 307–317. Rogers, S.I., Ellis, J.R., 2000. Changes in the demersal fish assemblages of British coastal waters during the 20th century. ICES J. Mar. Sci. 57, 866–881. Schmitt, J.D., Gedamke, T., DuPaul, W.D., Musick, J.A., 2015. Ontogenic and sex-specific shifts in the feeding habits of the barndoor skate. Mar. Coast. Fish.: Dyn. Manag. Ecosyst. Sci. 7, 409–418. Stentiford, G.D., Neil, D.M., 2011. Diseases of Nephrops and Metanephrops: a review. J. Invert. Pathol. 106, 92–109. Symonds, D., 1972. Infestation of Nephrops norvegicus (L.) by Stichocotyle nephropis Cunningham in British waters. J. Nat. Hist. 6, 423–426. Thomas, H.J., 1965. The white fish communities associated with Nephrops norvegicus (L.) and the by-catch of white fish in the Norway lobster fishery, together with notes on Norway lobster predators. Rapp. Proc. Verb. Réun. Cons. Perm. Int. Explor. Mer 156, 155–160. Van Engel, W.A., Harris Jr., R.E., Zwerner, D.E., 1986. Occurrence of some parasites and a commensal in the American lobster, Homarus americanus, from the Mid-Atlantic Bight. Fish. Bull. 84, 197–200. Walker, P.A., Heessen, H.J.L., 1996. Long-term changes in ray populations in the North Sea. ICES J. Mar. Sci. 53, 1085–1093. Wiegand, J., Hunter, E., Dulvy, N.K., 2011. Are spatial closures better than size limits for halting the decline of the North Sea thornback ray, Raja clavata? Mar. Freshw. Res. 62, 722–733. Wood, C.L., Lafferty, K., Micheli, F., 2010. Fishing out marine parasites?: Impacts of fishing on rates of parasitism in the ocean. Ecol. Lett. 13, 761–775. Wood, C.L., Sandin, S.A., Zgliczynski, B., Guerra, A.S., Micheli, F., 2014. Fishing drives decline in fish parasite diversity and has variable effects on parasite abundance. Ecology 95, 1929–1946. Yamamoto, K., Takagi, S., Matsuoka, S., 1984. Mass mortality of the Japanese anchovy (Engraulis japonica) caused by a gill monogenean Pseudanthocotyloides sp. (Mazocreidae) in the Sea of Iyo (“Iyo-nada”), Ehime Prefecture. Fish Pathol. 9, 119–123.
and abundance of their hosts (Marcogliese, 2001). These effects are likely to be felt more at the edges of the geographical distributions than in the core areas. Increasing sea temperatures in the Northeast Atlantic in recent years have already pushed the distribution of N. norvegicus further north, with individuals being caught in trawls around the Lofoten Islands, off northwest Norway (personal observations), where they had never been seen before. On both sides of the North Atlantic, the findings of both larval and adult stages of S. nephropis were from well within the core areas of their hosts’ distributions. The populations of the only known hosts of the larval stage of S. nephropis – Nephrops norvegicus and the American lobster – appear to be stable, but this is clearly not the case for the two known hosts of the adult stage, both of which have shown drastic decreases in population density over the past century. It is possible, of course, that as yet undiscovered populations of S. nephropis still exist, but the evidence strongly suggests that S. nephropis is now locally extinct in the core part of its known former geographical distribution. Its distribution in the Northeast Atlantic is likely to have been shrinking prior to the surveys of the early 1960s, because by then it seemed to have disappeared from its type locality in the North Sea. Landings of all ray species from the North Sea decreased significantly during the 1930s (Walker and Heessen, 1996), suggesting that ray populations were already decreasing at that time. The main population of thornback rays is now located in the southwestern part of the North Sea while the main population of N. norvegicus is in the northern North Sea. This disconnection would seriously reduce the parasite’s chances of successful transmission. The evidence thus suggests that overfishing of its final host species has at least hastened the decline and possibly led to the extinction of S. nephropis. We are not the first to suggest this: Stentiford and Neil (2011) commented “Whether evidence for reduced prevalence of S. nephropis in N. norvegicus may act as a surrogate for data pertaining to reductions in stock abundance of elasmobranchs such as R. clavata requires further assessment…” The parasites identified as S. nephropis on opposite sides of the North Atlantic are separated by most of the width of that ocean. The distributions of the intermediate and final hosts of each are limited to their own side of the Atlantic and none of them occurs in the intervening area, so it is likely that the two parasites were similar but separate species. Stichocotyle nephropis is the sole member of its genus and family. If it has become extinct, then we will have lost a unique species that has left very few records of its existence. We know virtually nothing of its biology and we have no idea what effects it may have had on the health and behaviour of any of its hosts. This is the first good evidence from the marine environment of a parasite species possibly rendered extinct by intensive fishing. Wood et al. (2014) concluded that trophically transmitted parasites appear to be sensitive to fishing impacts and might be at risk of local extirpation in fished environments. The narrow host specificity of S. nephropis to final host species that are particularly vulnerable to intensive fishing probably hastened its decline and possible extinction. Acknowledgements The authors thank Adrian Weetman and his staff for collecting samples during a research cruise aboard FRV “Scotia”. We are also grateful to Dr Tim Littlewood for his contribution in the form of a personal communication. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. References Bell, M.C., Redant, R., Tuck, I., 2006. Nephrops species. In: Phillips, Bruce F. (Ed.), Lobsters: Biology, Management, Aquaculture and Fisheries. Wiley-Blackwell, Oxford, pp. 42–461.
3