Simultaneous polyphenism and cryptic species in an intertidal limpet from New Zealand

Abstract

The small intertidal limpets known under the name Notoacmea helmsi occupy a wide variety of habitats in New Zealand and exhibit a variety of shell forms. Phylogenetic analyses of DNA sequences from two genes, mitochondrial COI and nuclear ITS1, reveal that this taxon comprises at least five morphologically cryptic species, with at least one of these species, N. scapha, consisting of individuals with two obviously different shell types. One of these forms is an ecophenotypic response to living on eelgrass (Zostera) fronds. Unlike its extinct relative, Lottia alveus, N. scapha is not restricted to this substrate, but individuals living elsewhere are larger and have a different shell shape. Although there is significant overlap in shell form among the different cryptic species, there is some habitat differentiation, with two species predominantly found on exposed shores and three confined to mudflats. One species exhibits distinctive light-avoiding behaviour, the first known case in which behaviour can be used to separate cryptic species in molluscs.

Introduction

The ability to correctly identify individuals as belonging to one species or another is a basic requirement of biological research. The consequences of mistaken assignments can be profound, confusing our understanding of basic biological processes as well as misinforming decisions in applied fields such as conservation and invasive species control. Even in apparently well-known groups, systematic identification error can arise from invalid taxonomy due, in turn, to two distinct phenomena—polyphenism and cryptic species. Polyphenisms can lead to individuals of a single biological species being identified as members of two or more species, whereas the real number of species can be underestimated if several cryptic species are present.

Perhaps the best known example of polyphenism affecting conservation decisions is the case of the Dusky Seaside Sparrow, Ammodramus nigrescens. Only after significant sums of money were spent on failed preservation efforts, was it realized that genetic differences between it and populations of the Seaside Sparrow, A. maritimus, from the Atlantic coast were minimal (Avise and Nelson, 1989). Its status had been reduced to a subspecies of A. maritimus before its final extinction in 1987, but even this level of distinction is now considered exaggerated. As Avise and Nelson (1989) put it, “a faulty taxonomy has resulted in well-intentioned but misdirected efforts in endangered species management.”

The reverse result—confusing two or more biological species as one—can arise in the presence of unsuspected cryptic species and can have equally important implications. The introduction of the invasive Zebra Mussel, Dreissena polymorpha, to the Great Lakes region of North America has led to major economic damage, but the various control programmes were complicated by the unsuspected presence of a second, cryptic species, D. bugensis (Spidle et al., 1994). In another case, the conservation status of various populations of the New Zealand endemic Tuatara (Sphenodon), the only living genus of the reptilian order Rhynchocephalia, has been compromised by neglected taxonomic issues (Daugherty et al., 1990, Hay et al., 2003).

One of the more poignant examples of the consequences of species identification error is the first known extinction of a marine invertebrate in historical times, that of the Eelgrass Limpet, Lottia alveus (Carlton et al., 1991). This mollusc, which was previously abundant on the blades of the eelgrass, Zostera marina, on the North American coast between Labrador and New York, disappeared unnoticed in the early 1930s when eelgrass populations were devastated by disease. Its extinction went unrecognized for almost 60 years in large part because most taxonomists of the time considered it to be an ecotype of what is now known as Lottia testudinalis, which lives on nearby rocky shores (Carlton et al., 1991, Nakano and Ozawa, 2004, Nakano and Ozawa, 2007).

Eelgrass beds have drastically declined in several parts of the world on a number of occasions in the 20th Century. Although these populations have usually recovered, the case of Lottia alveus shows that the complete associated eelgrass community need not return. Another lottiid limpet, Notoacmea scapha, endemic to New Zealand, has also been described as being restricted to living on eelgrass, the Australasian species, Z. capricorni. This narrow habitat preference has led to N. scapha being listed as a threatened species by the New Zealand Department of Conservation (Hitchmough, 2002; see also http://www.doc.govt.nz). As in North America, New Zealand Zostera populations have occasionally disappeared over wide parts of the country (Armiger, 1964). And like L. alveus, N. scapha has often been considered an ecotype of a related species, a congener found on hard substrates, N. helmsi (Oliver, 1926, Powell, 1979). Here, we examine shell and radular morphology in conjunction with mitochondrial and nuclear gene DNA sequence to elucidate the species status of N. scapha. To our surprise, we discover that both polyphenism and cryptic species are present in the N. scapha–N. helmsi complex: no limpet species in New Zealand is restricted to living on Zostera but five previously unrecognized species, which are all but indistinguishable morphologically, occur over a wide range of habitats.