Halacarid mites (Acari: Halacaridae) associated with a North Atlantic subtidal population of the kelp Laminaria ochroleuca

Halacarid mites (Acari: Halacaridae) associated with a North Atlantic subtidal population of the kelp Laminaria ochroleuca
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   PLEASE SCROLL DOWN FOR ARTICLE This article was downloaded by: [Harvard University]  On: 1 April 2010  Access details: Access Details: [subscription number 918547555]  Publisher Taylor & Francis  Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK Journal of Natural History Publication details, including instructions for authors and subscription information: Halacarid mites Acari: Halacaridae) associated with a North Atlanticsubtidal population of the kelp aminaria ochroleuca Ana Riesgo a ; Rocío Pérez-Portela a ;Nina Larissa Arroyo aa  Departamento de Biología Animal I, Universidad Complutense de Madrid, SpainOnline publication date: 10 March 2010 To cite this Article  Riesgo, Ana , Pérez-Portela, Rocío andLarissa Arroyo, Nina(2010) 'Halacarid mites (Acari: Halacaridae)associated with a North Atlantic subtidal population of the kelp Laminaria ochroleuca  ', Journal of Natural History, 44:11, 651 — 667 To link to this Article: DOI: 10.1080/00222930903528222 URL: Full terms and conditions of use: article may be used for research, teaching and private study purposes. Any substantial orsystematic reproduction, re-distribution, re-selling, loan or sub-licensing, systematic supply ordistribution in any form to anyone is expressly forbidden.The publisher does not give any warranty express or implied or make any representation that the contentswill be complete or accurate or up to date. The accuracy of any instructions, formulae and drug dosesshould be independently verified with primary sources. The publisher shall not be liable for any loss,actions, claims, proceedings, demand or costs or damages whatsoever or howsoever caused arising directlyor indirectly in connection with or arising out of the use of this material.  Journal of Natural History Vol. 44, Nos. 11–12, March 2010, 651–667 ISSN 0022-2933 print/ISSN 1464-5262 online© 2010 Taylor & FrancisDOI: 10.1080/00222930903528222 TNAH0022-29331464-5262Journal of Natural History, Vol. 1, No. 1, Dec 2009: pp. 0–0Journal of Natural History Halacarid mites (Acari: Halacaridae) associated with a North Atlantic subtidal population of the kelp Laminaria ochroleuca Journal of Natural History A. Riesgo  et al. Ana Riesgo*, Rocío Pérez-Portela and Nina Larissa Arroyo Departamento de Biología Animal I, Universidad Complutense de Madrid, 28040, Spain(Received 9 February 2009; final version received 1 December 2009) We characterised the mite fauna associated with a subtidal population of Lami-naria ochroleuca  in the Cantabrian Sea during a 4-year study. We found 2780individuals belonging to 35 species. The mite assemblage comprised both northAtlantic and Mediterranean species, as usually reported from the Lusitanianregion. The most abundant and diverse subfamily was Copidognathinae, followedby Halacarinae and Lohmannellinae. The greatest abundance of mites wasdetected on kelp holdfasts, not only strictly phytal mites were found but also inter-stitial mites or those associated with other macrofauna. Such a distribution couldbe explained by the high diversity and heterogeneity of microhabitats provided byholdfasts. Mite abundance fluctuated during the 4years of the study. However,the lowest abundance was detected during the last year of sampling. During thatyear, the studied algal population suffered a severe decay leaving only degenerat-ing holdfasts attached to the substrate, which could explain the decrease in mitenumbers. Keywords: Acari; Halacaridae; macroalgae; phytal fauna; Lusitanian region Introduction Halacarid mites (Halacaridae: Acarina: Arachnida) are common inhabitants of manymarine benthic habitats, with a distribution ranging from the upper littoral (Bückinget al. 1998; Mercer et al. 2000) to a depth of almost 7000m (Jankovskaja 1978).Halacarids cannot swim, and planktonic forms are not known (Bartsch 1989), sothey are mainly found in interstitial waters, sandy deposits and flocculent ooze at thesediment surface (Somerfield 1991; Bartsch 1989, 1993; Somerfield and Jeal 1995;Chatterjee and De Troch 2000). They have also been frequently reported to be associ-ated with sessile bryozoans, hydroids or barnacles (André 1946; Bartsch 1991), andmacrophytic algae (André 1946; Bartsch 1978; Pugh and King 1985; Somerfield 1988;Somerfield and Jeal 1995). Their latitudinal distribution ranges from polar to tropicalregions, mites being found in almost all examined geographical marine provinces(Bartsch 2006).The north-eastern Atlantic is among the areas where the halacarid fauna is betterknown, with the highest number of species reported – 147 described species that accountfor 14% of all described halacarid mites (Bartsch 2004). Even so, several regions withinthis zone, such as the Iberian Peninsula, have not been properly investigated. To ourknowledge, only two studies have mentioned free-living Halacaridae from Iberianwaters (Viets 1937; Giere 1979), yet neither mentioned sub-tidal phytal fauna. *Corresponding author. Email:  D o w nl o ad ed  B y : [ H a r v a rd  U ni v e r si t y]  A t : 16 :47 1  A p ril 2010  652 A. Riesgo et al.Several authors have examined the halacarid fauna associated with macroalgae inmany parts of the world: e.g. North, Black, Aral, Red and Mediterranean Seas,north-eastern and north-western Atlantic, Caribbean and Antarctica (Bartsch 1972,1974, 1979, 2004; Pugh and King 1985; Somerfield 1988, 1991; Somerfield and Jeal1995, 1996), and concur that the halacarid distribution is highly dependent on the dif-ferent microenvironments provided by the plants (e.g. Somerfield and Jeal 1996;Gemboldt 2002; Bartsch 2003). Indeed, while some sub-families within Halacaridae,particularly Rhombognathinae, are abundant on fucoids and other flat algalfronds(Hagerman 1966; Bartsch 1996), others appear to be more reliant on themicrohabitat protection provided by the stipes and holdfasts of the algae (Pugh andKing 1985; Somerfield 1988, 1991; Somerfield and Jeal 1995, 1996). Like other inver-tebrates with limited dispersal ability (Sánchez-Jérez et al. 1999), mites are strictlybenthic inhabitants that move mainly by crawling and demonstrate no, or only small-scale, migratory behaviour (Pugh and King 1986). Hence, their dispersal capabilitiesare very limited, while their algal substrata may determine their distribution anddiversity (Russell et al. 2005).In the present study, we analyse the halacarid assemblage associated with asubtidal bed of the kelp Laminaria ochroleuca  De la Pylaie 1824 over a 4-year study atMouro Island (Santander, Cantabrian Sea). The kelp L. ochroleuca  is distributedalong the Cantabrian coast from the western margin in Galicia (Estaca de Bares:43 ° 44 ′ N, 7 ° 51 ′ W) to the eastern margin in the Basque coast (Hondarribia:43 ° 17 ′ 06 ″  N, 2 ° 21 ′ 02 ″  W) (Izquierdo et al. 1993). Populations of L. ochroleuca  in thisarea have suffered periodic declines, presumably as a result of severe storm events,which also cause laminarians to decline in other regions of the world (North et al.1990). To our knowledge, no study has analysed the influence of algal density fluctu-ations on the, often poorly described, associated fauna. While the frond and stipe of  L. ochroleuca  are flat, smooth and simple, its intricate holdfast represents a complexstructure which both traps sediments and is colonised by other smaller algae andinvertebrates (Moore 1973; Arroyo et al. 2004, 2006). The different microhabitatsprovided by L. ochroleuca  are likely to affect acarine distribution with different spe-cies showing discrete associations with frond, stipe or holdfast. We investigated thehalacarid spatial distribution on fronds and holdfasts of L. ochroleuca , and in thesubstrate below the plants, and compared this acarofauna with that described fromother worldwide phytal habitats. Furthermore, we compared halacarid diversityassociated with frond, holdfast and surrounding substrate, and also among the4years of study. A laminarian decay event occurred in the area during the last year of sampling so we also investigated whether it affected the mite abundance, diversityand distribution patterning. Material and methods Sampling and sample processing  The study was conducted from 1996 to 1999 on a kelp bed of L. ochroleuca  developedaround the shelf of Mouro Island (43 ° 28 ′ 24 ″  N, 3 ° 45 ′ 22 ″  W; Bay of Santander,northern Spain, Cantabrian Sea) (Figure 1). During the study, the population of  L.ochroleuca  suffered a severe decline which initially affected only the fronds butended in substantial mortality. A detailed description of both the sub-littoral  D o w nl o ad ed  B y : [ H a r v a rd  U ni v e r si t y]  A t : 16 :47 1  A p ril 2010  Journal of Natural History 653environment surrounding the island and of the kelp bed, as well as fluctuations in theabundance of L. ochroleuca  are found elsewhere (see Arroyo et al. 2004).Samples comprised whole laminarians that were obtained by scuba-diving.Sampling sites were selected at random within the Laminaria  population, and theirpositions were identified using a portable Magellan global positioning system. We Figure 1.Location of Mouro Island in the Bay of Santander. Inset shows location of MouroIsland in the Iberian Peninsula (arrow) along with south-western Europe. The three geographicprovinces confluent in the Iberian Peninsula are also shown: boreal Atlantic (BA), Mediterra-nean (M) and the subtropical–boreal transition zone (BA-ST).  D o w nl o ad ed  B y : [ H a r v a rd  U ni v e r si t y]  A t : 16 :47 1  A p ril 2010  654 A. Riesgo et al.sampled during July–August 1996, May 1997, July–August 1998 and May–June1999. Between-year variability in sampling date was the result of weather conditionsbecause underwater work was conducted in a high-risk diving zone. Ten sampleswere collected during both 1996 and 1997, but because the progressive dieback of  L.ochroleuca  resulted in substantial plant mortality, only eight samples werecollected in 1998, and six in 1999. Plant samples consisted of fronds and holdfasts of  L. ochroleuca  collected from randomly marked 0.5  × 0.5-m quadrats. The frond(considered as lamina and stipe) was covered with a plastic zip-bag and then cut fromthe holdfast. Lamina and stipe were collected, stored and analysed together becauseof their similarities in surface structure, which was flat and smooth, and not hard andencrusted like those of Laminaria hyperborea . Unfortunately, during 1999, no frondswere collected because most of them were severely damaged or simply did not exist.For all samples, the holdfast was then detached from the underlying substrate with apaint-scraper and stored in another bag. Separate storage of both fractions ensuresminimal faunal loss and mixing during sampling. After holdfast removal, we scrapeda 0.25 ×  0.25-m area of hard benthos within randomly selected quadrats each year tocollect potential meiofaunal substratum, including sediment veneer, Mesophyllum crusts, soft algal canopy and biofilm. Further details about quadrat location can befound in Arroyo et al. (2004). At the end of the 4-year sampling, we had 34 frondsamples, 34 holdfast samples and 17 substrate samples ( n  = 85).In the laboratory, each sample (which in the case of holdfasts included not only Laminaria  tissue and associated fauna, but also sediment retained among the intri-cate cavities) was wet-weighed, and then frozen until subsequent faunal extraction.Macrofaunal organisms were first removed under a binocular microscope before theremaining sample was sieved through 1-mm and 62- µ m meshes, which retainedmeiofauna. Meiofauna was preserved in 4% buffered formalin and stained with rose-bengal until taxonomic study (see Arroyo et al. 2004 for details).Halacarid mites were counted and sorted using forceps under a stereo-microscope, cleared out in 70% lactic acid and mounted in modified Hoyer’s fluidslides for further identification. They were identified using a light microscope (10 × and 40 × ), using the keys of André (1946) and Green and MacQuitty (1987), and theavailable literature on halacarid taxonomy. Data analysis Only adults were considered in the statistical analyses because species identificationof juveniles was not possible for the genus Copidognathus  other than Copidognathusremipes.  Nevertheless, juvenile taxonomic composition and abundance is shown inTable 1.To explore the variability on mite diversity among microhabitats (frond, holdfastand substrate) and year samples (1996, 1997, 1998 and 1999), different diversity indi-ces were derived. Selected indices were: species richness indices [S: total species andd:species richness (Margalef)], evenness index (J ′ : Pielou´s evenness) and averagespecies diversity indices (H ′ : Shannon–Wiener index and 1-Lambda ′ : Simpson index).Samples without individuals were discarded. For comparisons of microhabitat, weused samples from all the fractions and the 4years of study ( n  = 61) and the wholespecies assemblage (with juveniles) was considered. For comparisons among annual  D o w nl o ad ed  B y : [ H a r v a rd  U ni v e r si t y]  A t : 16 :47 1  A p ril 2010
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