Elsevier

Biological Conservation

Volume 144, Issue 12, December 2011, Pages 2984-2990
Biological Conservation

Test and application of a non-destructive photo-method investigating the parasitic stage of the threatened mussel Margaritifera margaritifera on its host fish E. Salmo trutta

https://doi.org/10.1016/j.biocon.2011.09.001Get rights and content

Abstract

The objective was to test the application of a novel, non-destructive photo-method estimating the larval encystment of one of the highly threatened unionid mussels, the freshwater pearl mussel (Margaritifera margaritifera) on the gills of its host fish, brown trout (Salmo trutta). There were significant correlations between the encystment intensity based on microscope counts and using the new photo-method for both young-of-the-year and older brown trout just after the encystment in October 2007 and just before larval release from the host fish in June 2008. The mean encystment intensity based on the two methods did not differ from each other for the two age classes of trout when based on comparisons including all individuals. An aquaria experiment showed that there were no differences in survival or growth between fish subjected to the treatments: photo-method and individual marking, photo-method and a control. When applied to encystment in single streams, there were significant correlations between the mean encystment intensity in each stream based on the methods for both trout age classes. Therefore, it may be possible to get reliable estimation of the encystment rates without injuring the mussel or the host fish, which may also be used in restoration and cultivation work. Furthermore, the larvae of M. margaritifera are among the smallest of all the worldwide-distributed, threatened unionid mussel species. The photo-method may therefore also be used for other mussel species with larger larvae, as they are more easily recognized on photos. Therefore, it may now be possible to investigate every life stage of unionid species without using harmful methods at all.

Highlights

► A non-destructive photo-method investigated encystment of a unionid mussel on its host fish. ► The method reliably estimated encystment without injuring mussels or host fish. ► When applied to individual streams, mean encystment intensity was estimated for YOY and older fish. ► The photo-method may be used for other unionid mussel species. ► It may now be possible to investigate every life stage of unionids without using harmful methods.

Introduction

Reliable estimation of population density is fundamental in ecology, since it affects properties such as the estimation of population growth and status of populations (Stewart et al., 2001, Taylor and Pollard, 2008, Jones, 2011). Many methods used to estimate population density involve sampling methods that harm or even kill individuals. For threatened species, such destructive methods may cause substantial losses that are potential threats to these populations (Awruch et al., 2008, Rowcliffe et al., 2008, Österling et al., 2008). Still, estimates of abundance of threatened species are essential to be able to make the right conservation decisions (Rovero and Marshall, 2009, Tugores et al., 2010).

The conservation of threatened species may include investigating which life stage limits a population. For threatened species with a parasitic life-stage on a host, this means that the parasitic life-stage also needs investigation (Bogan, 1993, Hastie and Young, 2001). In this case, destructive methods may not only harm the threatened species, but also its host (Österling et al., 2008). Functioning host populations are however needed to sustain the threatened species (Haag and Warren, 1998, Haag and Warren, 2003, Vaughn and Taylor, 2000). Therefore, the risk of reducing the parasite and the host during this life stage means that it is vital that sampling methods are non-destructive at the parasitic life stage.

Mussels in the order unionoida, one of the most threatened groups in freshwater, are obligate temporary parasites on one or more fish species (Bogan, 1993, Haag and Warren, 1997, Strayer et al., 2004). The parasitic stage is therefore one of the life stages that potentially hinders recruitment of new mussels to the benthic population (Strayer et al., 2004, McNichols et al., 2011). Today, the method commonly used to investigate the parasitic stage is to kill the fish, cut out the gills and count the number of larvae using a microscope (Österling et al., 2008). However, low host fish densities and low encystment intensity on the host fish may make destructive sampling methods inappropriate, motivating the need to develop non-destructive methods to protect both the host fish population and the mussel parasite.

The threatened freshwater pearl mussel (Margaritifera margaritifera) is a gill parasite on brown trout (Salmo trutta) or Atlantic salmon (Salmo salar) (Young and Williams, 1984, Hastie and Young, 2001). The mussels reproduce during summer, whereupon the mussels are gravid for about one month. When the glochidia larvae are ripe, which occur approximately between July and September, larvae are released from the gravid mussels (Hastie and Young, 2003). Upon release, the larvae must encounter and be encapsulated on the gills of a host fish. The larvae then live as parasites until they release from the fish, which occurs approximately between June and July the following year (Hastie and Young, 2001). Young-of-the-year (YOY) fish have been suggested to be important hosts, because they are often numerous and lack a well-developed immune response to the encystment of glochidia larvae (Bauer and Vogel, 1987, Bauer, 1987b). Older fish (one year or older) appear to have a stronger immune response, and the larvae may therefore fall off older fish before completing their parasitic life cycle stage (Bauer, 1987c). Therefore, reliable, non-harmful methods are needed to be developed for comparisons of encystments on YOY fish and older fish.

This investigation tested (1) the reliability of photography as a novel, non-harmful method for measuring the encystment of larvae of M. margaritifera on the gills of its host fish, S. trutta, and (2) the application of the method on YOY and older brown trout populations separately, as the encystment capacity may differ depending on the age of the fish. Specifically, one aim was to investigate if it is possible to get reliable estimates of the encystment intensity just after the larval release in autumn, when the larvae are smallest. If so, the photo-method may be applicable to other mussel species, as the larvae of M. margaritifera are among the smallest of all unionoid larvae and therefore less easy to recognize compared to mussel species with larger larvae. Another aim was to see if it is possible to get reliable estimates of the potential number of mussels that will be released from the fish in early summer and recruit to the benthic population. The third aim was to test if the host fish suffered from the photo-method. Lastly, to test an application of the method, the mean encystment intensity based on the photo-method and microscope counts were compared in several streams.

Section snippets

Materials and methods

The investigation was performed in the Ljungan catchment in central Sweden (68°99´–69°49´N, 14°65´–15°65´E). One stream (Hiån) was electrofished for brown trout in October 2007, which was approximately one month after the last gravid mussel was observed. Only one stream was electrofished since the trout densities are generally low in most of these streams and the local authorities wanted to avoid to disturbing these vulnerable populations. Eighteen streams were electrofished for brown trout in

Results

There were significant correlations between the number of larvae in the spatula area counted on the preserved gills under the microscope and the number of larvae at the spatula area counted on the photograph on the trout from Hiån in October 2007 (Fig. 2a) and on every trout from all streams in June 2008 (Fig. 2b).

Discussion

This investigation showed that a non-destructive method could be used instead of a destructive method when investigating the parasitic stage of a unionid mussel species on its host fish. The photo-method used here measured the encystment of M. margaritifera glochidia larvae on S. trutta gills without injuring the fish, or causing reduced growth of the fish. Therefore, it may be possible to investigate every life-stage of the highly threatened unionoid mussels such as M. margaritifera using

Acknowledgments

I thank Fortums Nordiska Miljöfond for financing this study, H. Söderberg for inspiration, H. Karlsson for field assistance, and B. Arvidsson, L. Greenberg and four anonymous referees for commenting earlier versions of the manuscript. The electro-fishing and all other fish handling was performed under licenses from the Country Administration in Västernorrland and from the Swedish Animal Welfare Agency CFN, Gothenburg (Dnr: A81-07).

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