Dictyotales, Phaeophyceae) Species from the Canary Islands1
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J. Phycol. 46, 1075–1087 (2010) Ó 2010 Phycological Society of America DOI: 10.1111/j.1529-8817.2010.00912.x NICHE PARTITIONING AND THE COEXISTENCE OF TWO CRYPTIC DICTYOTA (DICTYOTALES, PHAEOPHYCEAE) SPECIES FROM THE CANARY ISLANDS1 Ana Tronholm,2 Marta Sanso´n, Julio Afonso-Carrillo Departamento de Biologı´a Vegetal (Bota´nica), Universidad de La Laguna, 38271 La Laguna, Canary Islands, Spain Heroen Verbruggen, and Olivier De Clerck Research Group Phycology and Centre for Molecular Phylogenetics and Evolution, Biology Department, Ghent University, Krijgslaan 281 S8, 9000 Ghent, Belgium Coexistence in a homogeneous environment The advent of DNA sequencing two decades ago requires species to specialize in distinct niches. has considerably altered our ideas about algal spe- Sympatry of cryptic species is of special interest to cies-level diversity. A plethora of studies has revealed both ecologists and evolutionary biologists because cryptic or sibling species within morphologically the mechanisms that facilitate their persistent coexis- defined species, falsifying the assumption that speci- tence are obscure. In this study, we report on two ation events always coincide with any noticeable sympatric Dictyota species, D. dichotoma (Huds.) morphological differentiation. As aptly stated by J. V. Lamour. and the newly described species Saunders and Lemkuhl (2005), species do not D. cymatophila sp. nov., from the Canary Islands. evolve specifically to render their identification Gene sequence data (rbcL, psbA, nad1, cox1, cox3, easier for scientists. In many cases, the respective and LSU rDNA) demonstrate that D. dichotoma and cryptic species are confined to discrete nonoverlap- D. cymatophila do not represent sister species. ping geographic regions. However, cryptic species Rather, D. cymatophila and D. dichotoma have con- are also shown to occur in close sympatry. Studies verged on a nearly identical morphology, only to be on mangrove algae reveal that individuals of distinguished with detailed morphometric observa- Bostrychia, conforming to a single morphospecies tions. Both species co-occur in eulittoral pools but belonging to separate noninterbreeding genea- and the shallow subtidal in Tenerife. Even though logical lineages, may grow completely intermingled D. cymatophila was more dominant in wave-exposed (Zuccarello and West 2003). places and D. dichotoma in less exposed areas, the The coexistence of species that are morphologi- spatial distribution of both species overlapped in cally identical challenges community ecological intermediate habitats. The species display radically theories that predict that two organisms competing different phenologies. D. dichotoma reached its for the same resource cannot stably coexist if other highest density in winter and early spring and ecological factors are constant (Gause 1932). So, disappeared nearly completely in autumn, while how similar can species be before they can no D. cymatophila dominated the study site from July until longer coexist? According to Gause’s law of compet- November. The timing of gamete release also differs itive exclusion, one of the species will outcompete between both species, D. dichotoma releasing gametes the other, leading to local extinction or an evolu- twice every lunar cycle, while the release of gametes tionary or behavioral shift toward a different ecolog- in D. cymatophila occurred roughly every other day. ical niche. The resulting partitioning of niches can occur in several ways: classical resource partitioning Key index words: Canary Islands; cryptic species; and temporal and spatial niche partitioning Dictyota cymatophila; Dictyota dichotoma; niche (Chesson 2000, Amarasekare 2003, Noda 2009). partitioning; phenology; reproductive ecology Competitive coexistence is best studied in animal Abbreviations: AIC, Akaike information criterion; communities, where coexisting species mostly exhi- ANOSIM, analyses of similarity; BI, Bayesian bit differences in diet and foraging patterns. It is inference; BIC, Bayesian information criterion; now widely accepted that plants also compete for GTR, general time reversible; ML, maximum natural resources (Silvertown 2004). However, niche likelihood; nMDS, nonmetric multidimensional differences among plants and algae have not been scaling; SIMPER, similarity percentage analyses characterized in the same amount of detail as in animal systems. The high species richness encoun- tered in plant communities combined with an apparent lack of niche differences between the com- 1Received 30 November 2009. Accepted 20 July 2010. posing species has led certain authors to challenge 2Author for correspondence: e-mail [email protected]. the classical theories based on the Lotka–Volterra 1075 1076 ANA TRONHOLM ET AL. competition model. In its most extreme form, the this study was to investigate the possibility that mul- unified neutral theory, the importance of niche dif- tiple species are present using analyses of DNA ferences between competing species is discarded sequence data sets. Following the observation of two altogether (Hubbell 2001, Volkov et al. 2003). distinct genetic entities (see Results), we set out to Algae have long served as model systems to study (i) evaluate whether morphological differences exist competitive coexistence in rocky coastal habitats using a morphometric and multivariate approach; (Dayton 1971, Connell 1972, Noda 2009). Several (ii) investigate potential niche differentiation by studies have indicated that the response of sympat- studying fine-scale distribution patterns, phenology, ric species to environmental gradients and grazers and gamete release periodicity; and (iii) make differs and that this facilitates coexistence. Differ- appropriate taxonomic changes. The obtained ences are obvious in cases where the co-occurring results can serve to study the generality of Gause’s species are either morphologically or ecologically law for rocky shore algae. dissimilar (Littler and Littler 1980). In the case of cryptic or pseudocryptic species (i.e., species that can be identified by means of key morphological MATERIALS AND METHODS characters, which are established after detailed com- Sampling, density estimation, and specimen preservation. Specimens parisons of morphological and nonmorphological were collected at Punta del Hidalgo, a rocky shore in the north features; Sa´ez and Lozano 2005), however, it is all of Tenerife, Canary Islands (28°35¢ N, 16°20¢ W). The Dictyota but clear whether genetic differentiation necessarily population was monitored on a monthly basis from April 2003 to March 2004 (see Tronholm et al. 2008), from three different coincides with ecological differentiation. habitats (semiexposed eulittoral pools, semiexposed shallow In this study, we address coexistence and poten- sublittoral, and exposed lower eulittoral), and genotyped using tial niche differentiation in the brown algal genus partial psbA sequences. Total density and the respective propor- Dictyota. Dictyota species are very common in inter- tions of the different life-cycle phases were estimated in situ tidal and shallow subtidal habitats along rocky coasts counting all specimens from a eulittoral area of about 100 m2. worldwide. Although present in cold-temperate Sporophytes and male and female gametophytes were distin- waters, the genus reaches its highest diversity in guished by the distinctive pattern of arrangement of sporangia, antheridial sori, and oogonial sori, respectively (see Fig. 7). tropical and warm-temperate environments where For morphometric analyses and descriptive purposes, a multiple species often coexist and reach high densi- minimum of 10 individuals were randomly collected each ties (Herren et al. 2006, Sotka and Hay 2009). Iden- month and preserved in a 4% formalin ⁄ seawater solution. tification of Dictyota species is generally considered For molecular analyses, specimens were collected from the difficult due to high levels of morphological plastic- study site as well as other localities in the Canary Islands and ity combined with the absence of clear diagnostic dried in silica gel (see Table S1 in the supplementary material). All liquid-preserved and voucher specimens are characters separating many species (Schnetter et al. deposited in TFC (Departamento de Biologı´a Vegetal, 1987, De Clerck and Coppejans 1999, De Clerck Universidad de La Laguna, Canary Islands, Spain). Silica 2003, Tronholm et al. 2008). Gene sequence data samples and DNA extracts are preserved at Ghent University have greatly aided species delineation and resulted (Ghent, Belgium). in the detection of multiple cryptic entities in Morphological analyses. For morphometric examination and Dictyota (Lee and Bae 2002, Hoshina et al. 2004, descriptive purposes, 119 randomly collected specimens from different seasons and life-cycle phases were studied. The 33 Hwang et al. 2005, Tronholm et al. 2008). vegetative and reproductive characters used in this study are Recent fieldwork and morphological examination listed in Table 1. The branching angle was measured in the of D. dichotoma populations raised the suspicion that apical and median-proximal parts of the thallus. The length pseudocryptic diversity may be present on the and width of cortical and medullary cells were measured in Canary Islands’ rocky shores. The principal goal of surface view at a branch situated well below the apex, while Table 1. Quantitative variables used in the morphometric analysis. Vegetative characters Reproductive characters Thallus length (cm) Sporangia Male