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Selectively Harvested Owl Limpet, Lottia Gigantea Phillip B

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Selectively Harvested Owl Limpet, Lottia Gigantea Phillip B Marine Ecology. ISSN 0173-9565 ORIGINAL ARTICLE Genetic diversity and population structure of the size- selectively harvested owl limpet, Lottia gigantea Phillip B. Fenberg1, Michael E. Hellberg2, Lynne Mullen3 & Kaustuv Roy4 1 Department of Palaeontology, The Natural History Museum, London, UK 2 Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, USA 3 Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA 4 Section of Ecology, Behavior, and Evolution, University of California, San Diego, La Jolla, CA, USA Keywords Abstract Lottia gigantea; microsatellites; size-selective harvesting. Size-selective harvesting can elicit a genetic response in target species through changes in population genetic subdivision, genetic diversity and selective Correspondence regimes. While harvest-induced genetic change has been documented in some P.B. Fenberg, Department of Palaeontology, commercially important species through the use of historic samples, many The Natural History Museum, Cromwell Road, commonly harvested species, such as coastal molluscs, lack historic samples London SW7 5BD, UK. and information on potential harvest induced genetic change. In this study, we E-mail: [email protected], [email protected] have genotyped six microsatellite markers from populations across much of the California mainland range of the size-selectively harvested owl limpet (Lottia Accepted: 2 May 2010 gigantea) to explore the genetic structure and diversity of this species. We found no significant genetic structure or differences in genetic diversity among doi:10.1111/j.1439-0485.2010.00386.x populations of L. gigantea. Our results suggest high gene flow among popula- tions and that differences in life history, demography, and body size previously observed between protected and exploited populations is largely due to pheno- typic plasticity. From a conservation perspective, if proper actions are taken to curb harvesting, then exploited populations should be able to return to their pre-impact state given sufficient time. 2008). However, for the vast majority of affected species, Problem we do not know whether observed changes have a genetic Size-selective harvesting is one of the most widespread basis, represent phenotypic plasticity, or result from a anthropogenic impacts on marine species. The loss of lar- combination of both (Kuparinen & Merila 2007; Allen- ger (older) individuals due to such harvesting has numer- dorf et al. 2008; Fenberg & Roy 2008). ous cascading effects on the biology of affected species The most powerful way to detect harvest-induced and populations, including changes in life history, genetic changes is to analyze samples collected over an demography, reproductive output, and even ecological extended period of time as a species is exploited (Colt- interactions (Fenberg & Roy 2008). Size-selective harvest- man et al. 2003; Kuparinen & Merila 2007; Allendorf ing has been shown to elicit rapid microevolutionary et al. 2008). This approach has produced mixed results responses in some wild populations (Coltman et al. 2003; for harvested fish species, with some such studies showing Grift et al. 2003; Olsen et al. 2004; Kuparinen & Merila a change in genetic diversity or structure over time 2007; Nussle et al. 2009) and intense harvest-induced (Smith et al. 1991; Hauser et al. 2002; Heath et al. 2002; mortality (regardless of selectivity) over multiple genera- Hutchinson et al. 2003) while others reveal no significant tions should result in genetic changes (Allendorf et al. trends (Nielsen et al. 1999; Ruzzante et al. 2001; Chevolot Marine Ecology (2010) 1–10 ª 2010 Blackwell Verlag GmbH 1 Genetic diversity and population structure Fenberg, Hellberg, Mullen & Roy et al. 2008). Such historical analyses are, however, not California (26.1 °N) to northern California (39.4 °N). possible for the majority of harvested species due to the Individuals undergo a single spawning event in the winter lack of archived samples from the past. months, typically in January or February (Daly 1975). A comparison of genetic variation between populations Larvae are pelagic and although the exact larval duration of a target species from well-protected marine reserves of this species remains unknown, laboratory studies of with those from exploited areas is a valuable alternative to other Northeastern Pacific Lottia species (Lottia digitalis detecting harvest-induced genetic change when historic and Lottia asmi) suggest that metamorphic competence samples are not available. However, a prerequisite for such (at 13 °C) occurs around 5 days after fertilization (Kay & studies is the proper establishment of population genetic Emlet 2002). However, even with a short pelagic phase, substructure of the target species (Coltman et al. 2003; larvae within the north-flowing coastal Davidson Current Allendorf et al. 2008). Comparisons between protected during the winter could potentially be transported long and exploited populations of a panmictic species will pro- distances, upwards of 350 km (Glickman 1999; Gruenthal vide little evidence of harvest-induced genetic change with- et al. 2007). The potential for high rates of dispersal out historical data. On the other hand, if genetic between L. gigantea populations is thus substantial. On differences exist, then comparisons of protected and the other hand, there are physical and biological reasons exploited sites can provide information about an intended to think that local retention of larvae is also possible. For function of protection, the preservation of intraspecific example, rocky intertidal habitats in the middle portion genetic diversity (Trexler & Travis 2000). For example, of the geographic range of L. gigantea (Southern Califor- allelic richness for a harvested fish species (Diplodus sar- nia) are often separated by long stretches of unsuitable gus) is significantly higher at protected areas compared sandy habitats and provincial and phylogeographic with non-protected areas (Perez-Ruzafa et al. 2006). Inter- boundaries (e.g. Point Conception and Monterey Bay), as estingly, depleted populations of the Tasmanian black-lip well as topographical headlands, which can also limit abalone (Haliotis rubra) have higher levels of genetic diver- larval dispersal (Burton 1998; Dawson 2001; Wares et al. sity than do healthy populations (Miller et al. 2009). This 2001; Banks et al. 2007). Perhaps more importantly, is hypothesized to be due to a higher ratio of migrants to human exploitation of this species has the potential to self-recruiting larvae at depleted populations relative to affect the genetic makeup of local populations. healthy populations (Miller et al. 2009). Thus information Decades of size-selective harvesting have reduced the about patterns of gene flow and population connectivities body sizes of most California mainland populations of of harvested species is necessary for better understanding L. gigantea, with the exception of those living in well pro- the long-term consequences of harvest-induced mortality. tected reserves and along isolated stretches of coastline Intertidal and subtidal species of molluscs represent a (Pombo & Escofet 1996; Lindberg et al. 1998; Roy et al. large portion of species currently known to be affected by 2003; Sagarin et al. 2007). Exploited and protected popu- size-selective harvesting (Fenberg & Roy 2008). Humans lations of this species differ in several ways. On average, have exploited coastal molluscs (clams, limpets, abalone, individuals of L. gigantea from protected populations are and other gastropods) as a food source since prehistoric larger, grow faster, change sex at a larger size (L. gigantea times (Jerardino et al. 1992; Siegfried 1994; Mannino & is a protandric hermaphrodite), are less abundant, and Thomas 2002), and for many species subsistence harvesting have different ecological interactions with the surround- in the past has given way to widespread commercial har- ing community compared with those from exploited pop- vesting. However, there is a general lack of data on the ulations (Pombo & Escofet 1996; Lindberg et al. 1998; effects of harvesting (commercial, recreational or subsis- Roy et al. 2003; Sagarin et al. 2007; Fenberg 2008). tence) on the genetic population structures of shallow- Besides humans, American black oystercatchers (Haema- water molluscan species. Even along the coast of California, topus bachmani) also eat L. gigantea, yet they do not hunt where many species of molluscs are routinely harvested for the large individuals, are sensitive to human encroach- (Murray et al. 1999), information about genetic structure is ment, and do not regularly occur at sites frequented by only available for a few species (Gruenthal et al. 2007; humans (Lindberg et al. 1998). Addison et al. 2008; Gruenthal & Burton 2008). Exploited populations have significantly lower biomass In this study, we examine the genetic diversity and and total reproductive output compared to protected areas population structure of one of the most widely exploited (Fenberg 2008). Such reductions in reproductive output molluscs in California, the owl limpet Lottia gigantea. Lot- can decrease the number of migrants among local popula- tia gigantea is an intertidal gastropod that can reach a tions and potentially result in a loss of genetic variation maximum length greater than 100 mm, making it the (Allendorf et al. 2008). The primary goal of this study largest patellogastropod (limpet) in North America. The is to quantify patterns
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