hume et al. (2013)

Journal of Fish Biology (2013)

doi:10.1111/jfb.12075, available online at wileyonlinelibrary.com

BRIEF COMMUNICATION

Evidence of a recent decline in river lamprey Lampetrafluviatilis parasitism of a nationally rare whitefish

Coregonus lavaretus: is there a diamond in the ruffeGymnocephalus cernuus?

J. B. Hume*†, C. E. Adams*‡, C. W. Bean§ and P. S. Maitland‖*Institute of Biodiversity, Animal Health & Comparative Medicine, College of Medical,

Veterinary & Life Sciences, University of Glasgow, Graham Kerr Building, Glasgow G128QQ, U.K., ‡Scottish Centre for Ecology & the Natural Environment, Rowardennan, Loch

Lomond, G63 0AW, U.K., §Scottish Natural Heritage, Caspian House, Mariner Court,Clydebank, G81 2NR, U.K.and ‖Fish Conservation Centre, Gladshot, Haddington

EH41 4NR, U.K.

(Received 30 October 2012, Accepted 22 January 2013)

Lamprey-induced scarring of the nationally rare Coregonus lavaretus , a known host of a freshwater-resident population of European river lamprey Lampetra fluviatilis , was found to have declinedprecipitously since the establishment of several non-native fishes in Loch Lomond. Evidence pre-sented in this study points to the possibility that L. fluviatilis in this lake may have altered its trophicecology in response to the negative impact that non-native species, in particular ruffe Gymnocephaluscernuus , have had on their favoured host. © 2013 The Authors

Journal of Fish Biology © 2013 The Fisheries Society of the British Isles

Key words: foraging; Loch Lomond; non-native; powan; Scotland; resident.

Lampreys (Petromyzontiformes) are an enigmatic group of fishes that express arange of specialized foraging strategies prior to sexual maturation. These include:parasitic or predacious modes of feeding on actinopterygians in marine or freshwaterenvironments, where the blood and body tissues of hosts are removed (Renaud et al .,2009); carrion feeding and scavenging (Holcík, 1986; Kan & Bond, 1981); or inmany species, the absence of a postlarval feeding phase (Hardisty & Potter, 1971).Some large European lake systems contain populations of Lampetra fluviatilis (L.1758) known to feed exclusively within the lake, including Lakes Onega and Ladogain the Russian Federation (Berg, 1948), several lakes in Finland (Valovirta, 1950;Tuunainen et al ., 1980), Lough Neagh, Northern Ireland (Goodwin et al ., 2006) andLoch Lomond, Scotland (Maitland, 1980).

†Author to whom correspondence should be addressed. Tel.: +44 (0)141 330 6637; email: [email protected]

1© 2013 The AuthorsJournal of Fish Biology © 2013 The Fisheries Society of the British Isles

2 J . B . H U M E E T A L .

These populations remain mostly uncharacterized, to a large extent because ofinherent difficulties in observing adult petromyzontids foraging under natural con-ditions and a reliance on the observation of prey that have survived attacks bypetromyzontids. This methodology does not lend itself to clearly defined descrip-tions of petromyzontid foraging ecology as it reveals hardly any information abouthost mortality or petromyzontid behaviour and there must necessarily be some inter-polation of sparse or incidental data. Yet scarring data from surviving hosts remaina critical source of information, particularly in a conservation context (DFO, 2010).Many freshwater-resident petromyzontid species are also endemic (Taylor et al .,2012) and with the notable exception of sea lamprey Petromyzon marinus L. 1758in the Laurentian Great Lakes most of these populations are drastically understudied.

Loch Lomond is the largest area of fresh water in the U.K. (71 km2) and containsthe greatest number of fish species of any lake in Scotland (Winfield et al ., 2010).Fifteen species are native, including populations of the nationally rare whitefishCoregonus lavaretus (L. 1758) (known locally as powan). This study refers to themore common C. lavaretus , in preference to Coregonus clupeoides Lacepede 1803for Loch Lomond coregonids, as suggested by Kottelat & Freyhof (2007). Recentwork has shown these fish to be indistinguishable from other putatively identified‘species’ of C. lavaretus in the U.K. (Etheridge et al ., 2012). Loch Lomond alsosupports a freshwater-resident European river lamprey L. fluviatilis (L. 1758) popula-tion, and both L. fluviatilis and C. lavaretus currently experience substantial nationaland international conservation protection. Since 1970 a further six non-native specieshave been recorded (Adams, 1994; Etheridge & Adams, 2008), the most perniciousbeing the deliberate introduction of ruffe Gymnocephalus cernuus (L. 1758) to thelake prior to 1982 (Maitland et al ., 1983). This event marked a clear watershedin the ecology of the Loch Lomond system, particularly its effect on the trophicinteractions between piscivorous species and C. lavaretus .

Gymnocephalus cernuus are thought to have a deleterious effect on the C. lavare-tus population as they are a major predator of their ova (Adams & Tippett, 1991;Etheridge et al ., 2011). Prior to the introduction of G. cernuus , C. lavaretus were afavoured prey item for several predatory species including otters Lutra lutra (McCaf-ferty, 2005), grey herons Ardea cinerea (Adams & Mitchell, 1995), cormorantsPhalacrocorax carbo (Adams et al ., 1994) and pike Esox lucius L. 1758 (Adams,1991), all of which subsequently altered their trophic ecology to feed heavily onG. cernuus as the population increased exponentially through the 1980s (Maitland& East, 1989). One additional species that was known to utilize C. lavaretus as akey prey item in the past is L. fluviatilis (Maitland, 1980). This parasitic lamprey istypically anadromous, feeding within estuaries before returning to rivers in order tospawn (Maitland et al ., 1984), but in Loch Lomond the population comprises twocomponents, one of which retains anadromous tendencies while the other remainswithin the lake to feed (Maitland et al ., 1994; Adams et al ., 2008).

Casual observation suggested that the number of C. lavaretus exhibiting evidenceof L. fluviatilis feeding, collected from the lake during routine monitoring and otherscientific studies in recent years, was remarkably low compared with past experi-ence. Given the significant increase in scientific and conservation interest of bothC. lavaretus (Etheridge et al ., 2010a ,b, 2011, 2012a ,b) and L. fluviatilis popula-tions of Loch Lomond (Adams et al ., 2008; Hume et al ., 2013) it was deemed anappropriate time to re-examine the C. lavaretus population for L. fluviatilis-induced

© 2013 The AuthorsJournal of Fish Biology © 2013 The Fisheries Society of the British Isles, Journal of Fish Biology 2013, doi:10.1111/jfb.12075

L A K E F O R AG I N G I N L A M P E T R A F L U V I AT I L I S 3

feeding scars (Maitland, 1980). Here evidence is presented that suggests a changein trophic interactions between L. fluviatilis and C. lavaretus that has occurred sincethe introduction of non-native fish species to Loch Lomond, by comparing the pro-portion of C. lavaretus that were historically parasitized (pre-1980) to the proportionparasitized in 2010.

Coregonus lavaretus were collected in gillnets set overnight from December 2009to February 2010 as part of a separate study and examined for L. fluviatilis-inducedscars; that is types A and B, stage IV marks sensu Ebener et al . (2006). Scars appearas roughly circular patches of scale-less skin, sometimes with a shallow depression,and are easily recognized and distinguished from damage caused by nets or birds.Depth and location of nets varied widely throughout the study period and knot-to-knot mesh of nets deployed ranged from 25 to 38 mm. The presence or absence ofL. fluviatilis-induced scars, and their frequency on individuals where present, wasrecorded for each C. lavaretus specimen along with fork length (LF) (±1 mm). Amixed collection of several other fish species during the study period was similarlyexamined for L. fluviatilis-induced scars. The 2010 results on the frequency of L.fluviatilis-induced scars on C. lavaretus in the lake were compared to historicaldata for the period 1951–1979 (Maitland, 1980). In the historical data set, onlyC. lavaretus known to be collected between December and February were includedand data from these years were combined (1951–1979) so that comparisons couldbe made with the single 2010 data set.

The proportion of C. lavaretus in Loch Lomond bearing scars in 2010 was sig-nificantly lower than during the period 1951–1979 (χ2 = 3·84, d.f. = 1, P < 0·001)(Table I). The frequency of scarred C. lavaretus in the period 1951–1979 rangedfrom 26 to 43% (mean 36·6%), while in 2010 only 6% of C. lavaretus exhibitedL. fluviatilis-induced scars. The incidence of multiple scars was also lower in 2010,where two scars were the maximum observed on an individual, compared with up toeight scars in 1951–1979. The mean LF of C. lavaretus collected in 2010 was, how-ever, significantly greater than that of 1951–1979, both for unscarred (t-test = −7·75,d.f. = 341, P < 0·05) and scarred individuals (t =−6·37, d.f. = 21, P < 0·05) (Fig. 1).Scarring was not randomly distributed amongst C. lavaretus size classes, but wasmost frequently recorded from individuals of 250–350 mm LF (Fig. 2). Across bothsampling periods, 90·9% (n = 379) of C. lavaretus within this size range were scarredat least once and no specimens outside this size range were scarred three or moretimes. Individuals <250 mm LF were scarred at low frequencies (7%, n = 30), and nospecimen <210 mm LF bore scars, although fish as small as 150 mm were examined.

Five other fish species were collected during sampling in 2010: roach Rutilusrutilus (L. 1758) (n = 443), E. lucius (n = 4), perch Perca fluviatilis L. 1758 (n = 39),G. cernuus (n = 1) and brown trout Salmo trutta L. 1758 (n = 24). Only R. rutilusexhibited L. fluviatilis-induced scars (2·3%, n = 10) and those individuals had a simi-lar mean LF (224, range 202–248 mm), compared with unscarred specimens (n = 129,mean 228, range 183–290 mm).

It is apparent that C. lavaretus were historically an important constituent of thediet of L. fluviatilis in Loch Lomond (Maitland, 1980) and that presently the evidencefor continued parasitism of the C. lavaretus population has declined drastically. Asingle major event (i.e. the introduction of G. cernuus by 1982) has occurred inLoch Lomond since the collection of the historical data and four hypotheses, notnecessarily mutually exclusive, could explain the apparent differences between the


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Table I. Frequency of historical (1951–1979) and recent (2010) Lampetra fluviatilis-inducedscars recorded from Coregonus lavaretus collected in Loch Lomond. The proportion of fishscarred during each time period, as well as the number of scars recorded from individual fish,

is indicated

Number of scarsSampleperiod

Number ofC. lavaretus

examined % Scarred 1 2 3 4 5 6 7 8

1951–1979 1079 36·6 183 98 54 33 13 6 5 32010 364 6 18 4 0 0 0 0 0 0

historical and recent data sets. An explanation of their relevance to interpretingthe foraging ecology of L. fluviatilis , and ways in which to address any remainingknowledge gaps follows. (1) A decline in the L. fluviatilis population size. If thenumber of L. fluviatilis entering the lake to feed each year has declined since 1979this might explain why fewer parasitized C. lavaretus were subsequently collected in2010, compared with the historical data. No quantitative data exist on the numbersof adult L. fluviatilis between 1951 and 1979, making comparisons impossible. Yet

50 (a) (b)

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Fig. 1. Fork length (LF) frequency distribution of all Coregonus lavaretus collected from Loch Lomond duringboth (a), (b) historical (1951–1979) and (c), (d) recent (2010) periods, with and without the presence ofLampetra fluviatilis-induced scars. Coregonus lavaretus were measured to ±1 mm. , the mean LF foreach of the four categories.



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Fig. 2. Fork length (LF) frequency distribution of all Coregonus lavaretus collected from Loch Lomond exhibit-ing one or more Lampetra fluviatilis-induced scars, during both historical (1951–1979) and recent (2010)periods combined (n = 417). Coregonus lavaretus were measured to ±1 mm. , the delineation of LF

classes <250, 250–350 and >350 mm.

the sporadic data that are available suggest that adult L. fluviatilis numbers haveat least remained stable since 1983 (Hume, 2011). (2) An increase in C. lavaretuspopulation size. Similarly, if the number of C. lavaretus available to L. fluviatiliseach year has increased since 1979 this could result in the reduced probability ofcapturing C. lavaretus specimens in 2010 that had been parasitized. Recent evidencefrom hydroacoustic surveys suggests that the C. lavaretus population is in decline(Winfield et al ., 2008), probably the result of increased ova predation by G. cer-nuus (Etheridge et al ., 2011). Such a situation might be expected to result in similaror greater proportions of scarred C. lavaretus in recent years, if the L. fluviatilispopulation size has remained stable. This is difficult to separate from the possibil-ity that L. fluviatilis may find it more difficult to detect a less abundant host. Anexperimental design featuring choice chambers containing diffuse v . concentrated C.lavaretus holding water could be used as means of testing the relative importanceof olfaction in the ability of a parasitic-phase L. fluviatilis to detect potential hostsand orient towards them (Kleerekoper & Mogensen, 1963). (3) Higher C. lavaretusmortality rate. If, as has been suggested by Winfield et al . (2008), the populationof C. lavaretus now comprises mainly individuals 40–99 mm LF, then it is possi-ble L. fluviatilis continue to parasitize C. lavaretus but they are not surviving tobe counted as scarred individuals in the population. Maitland (1980) suggested C.


6 J . B . H U M E E T A L .

lavaretus <250 mm were rarely parasitized, possibly as the result of a pelagic life-history strategy, and certainly very few individuals <250 mm were recorded withscars either historically or recently. Examining the frequency of scars on individualscannot provide estimations of mortality in the population, but can suggest that asubstantial proportion of C. lavaretus have survived to be counted (Schneider et al .,1996). Therefore, an experimental approach utilizing C. lavaretus of different sizeclasses (e.g . <250 mm, 250–350 mm, >350 mm) and exposing them to L. fluviatilisparasitism in a controlled environment (Farmer & Beamish, 1973) could provide datanecessary in forming any robust conclusions about the effect of L. fluviatilis para-sitism on its host. (4) Host switching by L. fluviatilis could have altered its feedingpreferences to alternative hosts and certainly S. trutta and R. rutilus were histori-cally parasitized in Loch Lomond (Maitland, 1980). The mixed species collection of2010, however, found that the proportion of R. rutilus scarred by L. fluviatilis hasalso declined in comparison to the 1951–1979 period (5–2·3%) and S. trutta werenot found to be scarred at all. Elsewhere, freshwater-resident L. fluviatilis in LoughNeagh switch from feeding on native to non-native hosts throughout the year andthe latter now contribute a significant proportion of their diet (Inger et al ., 2010).In Loch Lomond, G. cernuus is numerically the most abundant non-native species(Adams, 1994), yet there is no evidence L. fluviatilis have begun to parasitize themsince their colonization was first detected in 1982. It is possible, however, that G.cernuus experiences greater mortality (Kitchell, 1990) due to their smaller body sizecompared to C. lavaretus [100–150 mm v . 150–400 mm; Maitland (2000)], and aretherefore unlikely to be collected while bearing a L. fluviatilis-induced scar. Certainlyother predatory species altered their trophic ecology in Loch Lomond to exploit theestablishment of G. cernuus , and some lamprey species are known to utilize verysmall hosts (Cochran & Jenkins, 1994). Although a large-scale survey of all fishspecies bearing fresh wounds in Loch Lomond during the summer feeding periodof L. fluviatilis would be most likely to yield critical data, ethically and logisticallythis would be very difficult to justify. Alternatively, either a targeted examinationof the G. cernuus population during the summer trophic period of L. fluviatilis or acaptive feeding experiment utilizing both C. lavaretus and G. cernuus hosts withinaquaria could establish the relative rates of mortality in these species as a result ofL. fluviatilis feeding.

Drawing these four hypotheses together and teasing apart the effects each mayhave on the other is not simple, and the results of future studies outlined above willbe likely to shed more light on a complex situation. Although it is not possible toconclusively explain these data with any one hypothesis, a combination of these maybe used to infer some key points about the trophic ecology of L. fluviatilis in LochLomond, and elsewhere, and how it has changed in response to the introduction ofnon-native species.

Prior to the introduction of G. cernuus to the lake, C. lavaretus was abundant inLoch Lomond and utilized by a variety of species including L. fluviatilis . Coregonuslavaretus of 250–350 mm LF were, in particular, heavily parasitized by the L. flu-viatilis population, and many exhibited multiple scars within this size range. As C.lavaretus appear to undergo a change in habit from pelagic to at least partly ben-thic foraging at c. 250 mm LF (Maitland, 1980; Etheridge et al ., 2010a ,b), it seemslikely that at this point C. lavaretus become vulnerable to L. fluviatilis . Coregonuslavaretus <250 mm are probably not exposed to foraging L. fluviatilis and so are



rarely scarred. Coregonus lavaretus >350 mm that have already ‘passed through’ thestage of L. fluviatilis-vulnerability, probably suffer increased rates of mortality dueto repeated attacks, and do not survive to be counted as scarred, as explained by thelack of evidence for increasing scar numbers on larger individuals.

As G. cernuus also forage benthically there exists the possibility that L. fluviatilissearching for a suitable host (i.e. C. lavaretus 250–350 mm LF) will encounter G.cernuus in high numbers, yet parasitized G. cernuus are not surviving to be countedas scarred given their small body size in comparison to C. lavaretus . This couldalso explain the reduced incidence of multiple scars on C. lavaretus of suitable sizein 2010, as L. fluviatilis in the lake are no longer prioritizing formerly abundantC. lavaretus hosts but feeding heavily on the now abundant G. cernuus . At present,this appears to be the most parsimonious explanation for evidence of a changein L. fluviatilis and C. lavaretus trophic interactions, and suggests that L. fluviatilispopulations may be adaptable in their foraging ecology (Inger et al ., 2010). Althoughundoubtedly of conservation concern, curiously the establishment of G. cernuus inLoch Lomond may act to secure the long-term stability of its endemic species.

We thank several anonymous referees for helping to improve an early draft of thismanuscript, and special thanks to M. Docker for insightful comments and discussion. Thanksalso to everyone involved in collecting powan during the difficult winter spawning season,including support staff at the Scottish Centre for Ecology & the Natural Environment.

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