Effects of Ocean Acidification Over the Life History of the Barnacle Amphibalanus Amphitrite
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Vol. 385: 179–187, 2009 MARINE ECOLOGY PROGRESS SERIES Published June 18 doi: 10.3354/meps08099 Mar Ecol Prog Ser OPENPEN ACCESSCCESS Effects of ocean acidification over the life history of the barnacle Amphibalanus amphitrite Michelle R. McDonald1, James B. McClintock1,*, Charles D. Amsler1, Dan Rittschof2, Robert A. Angus1, Beatriz Orihuela2, Kay Lutostanski2 1Department of Biology, University of Alabama at Birmingham, Birmingham, Alabama 35294-1170, USA 2Duke University Marine Laboratory, Nicholas School of the Environment, 135 Duke Marine Lab Road, Beaufort, North Carolina 28516-9721, USA ABSTRACT: Increased levels of atmospheric CO2 are anticipated to cause decreased seawater pH. Despite the fact that calcified marine invertebrates are particularly susceptible to acidification, bar- nacles have received little attention. We examined larval condition, cyprid size, cyprid attachment and metamorphosis, juvenile to adult growth, shell calcium carbonate content, and shell resistance to dislodgement and penetration in the barnacle Amphibalanus amphitrite reared from nauplii in either ambient pH 8.2 seawater or under CO2-driven acidification of seawater down to a pH of 7.4. There were no effects of reduced pH on larval condition, cyprid size, cyprid attachment and metamorpho- sis, juvenile to adult growth, or egg production. Nonetheless, barnacles exposed to pH 7.4 seawater displayed a trend of larger basal shell diameters during growth, suggestive of compensatory calcifi- cation. Furthermore, greater force was required to cause shell breakage of adults raised at pH 7.4, indicating that the lower, active growth regions of the wall shells had become more heavily calcified. Ash contents (predominately calcium carbonate) of basal shell plates confirmed that increased calci- fication had occurred in shells of individuals reared at pH 7.4. Despite enhanced calcification, pen- etrometry revealed that the central shell wall plates required significantly less force to penetrate than those of individuals raised at pH 8.2. Thus, dissolution rapidly weakens wall shells as they grow. The ramifications of our observations at the population level are important, as barnacles with weakened wall shells are more vulnerable to predators. KEY WORDS: Ocean acidification . Barnacle . Life history . Larval ecology . Intertidal ecology . Calcification Resale or republication not permitted without written consent of the publisher INTRODUCTION ence shifts in carbonate saturation horizons (Feely et al. 2004, Orr et al. 2005, Fabry et al. 2008). As such, the The current decline in the pH of the world’s oceans combination of lowered seawater pH and the reduced (ocean acidification) is an important consequence of saturation states of calcium carbonate and its poly- surface water interchange with increasing concentra- morphs aragonite and calcite are likely to have nega- tions of anthropogenically generated atmospheric CO2 tive effects on a variety of processes in marine inverte- (Takahashi et al. 1997, Sabine et al. 2004, Caldeira & brates both related and unrelated to calcification. Wickett 2005, Guinotte & Fabry 2008, Riebesell 2008). The impacts of ocean acidification on benthic marine Models predict that by the year 2100, mean seawater invertebrates has been the focus of a number of recent pH levels could decrease from current ambient levels studies (e.g. oysters, Kurihara et al. 2007; mussels, of about 8.1 to 7.7 (IPCC 2007), and by 2300 to levels as Beesley et al. 2008; sea urchins, Kurihara & Shirayama low as 7.3 (Caldeira & Wickett 2003). Given these pre- 2004; brittle stars, Wood et al. 2008, Dupont et al. 2008; dicted declines in pH, global ocean waters will experi- hard corals, Fine & Tchernov 2007). These experimen- *Corresponding author. Email: [email protected] © Inter-Research 2009 · www.int-res.com 180 Mar Ecol Prog Ser 385: 179–187, 2009 tal laboratory studies have revealed that exposure to We selected the barnacle Amphibalanus (=Balanus) CO2-induced acidified seawater disrupts a variety of amphitrite (Pitombo 2004), as it is a dominant fouling calcification-related and unrelated biological processes organism (Rittschof et al. 1984, Rittschof 2001) and is of across a range of life history stages that span from fertil- considerable ecological importance (Henry 1959). ization (Havenhand et al. 2008) and larval development Moreover, its growth and development from naupliar and growth (reviewed by Kurihara 2008) to aspects of to adult stages have been well studied (Costlow & juvenile and adult growth, muscle function, acid-base Bookhout 1958, Pechenik et al. 1993, Anil et al. 1995, balance, immune response, and shell calcification (e.g. Anil & Kurian 1996, Thompson et al. 1998). As a model Kurihara & Shirayama 2004, Kurihara et al. 2007, Miles for antifouling research (Rittschof et al. 1984, 1992, et al. 2007, Beesley et al. 2008, Bibby et al. 2008, Wood Rittschof 2001, Hung et al. 2008), standardized tech- et al. 2008). For example, very early embryos of the oys- niques for its culture are well established (Rittschof et ter Crassostrea gigas exposed to a seawater pH of 7.4 al. 1984, 1992, Anil et al. 1995, Qian et al. 2003). We suffer both delayed development and delayed larval examined the effects of CO2-induced seawater acidifi- shell formation (Kurihara et al. 2007). Development in cation in this common barnacle on aspects of larval the sea urchins Hemicentrotus pulcherrimus and Echi- condition, cyprid size, cyprid attachment and meta- nometra mathaei exposed to seawater pH ranging from morphosis, juvenile to adult growth, the onset of repro- 6.8 to 7.4 is characterized by decreased fertilization, re- ductive maturity (egg production), and aspects of adult duced developmental speed, and smaller larval size shell integrity including the forces required to break (Kurihara & Shirayama 2004). Embryos and larvae of and to penetrate shells, and the levels of ash (predom- the brittle star Ophiothrix fragilis suffer complete mor- inately calcium carbonate) in basal shell plates. tality within 8 d even at a moderately reduced pH of 7.9 We selected an experimental pH level of 7.4 in part (Dupont et al. 2008). Regenerating arms in adult brittle because of its direct comparative value with pH levels stars Amphiura filiformis exposed to pH 6.8 exhibit sig- tested in numerous previous studies of ocean acidifica- nificant muscle wastage (Wood et al. 2008), and growth tion on calcified marine invertebrates (e.g. 23 of 30 ex- of juvenile mussels Mytilus edulis is reduced at pH 6.7 perimental studies cited in Table 1 of Kurihara 2008), (Berge et al. 2006) while adults become immunocom- and also because it represents a pH level that is esti- promised (Bibby et al. 2008). mated to occur in the world’s oceans under current While studies such as those cited above collectively models of anthropogenic CO2 emissions (pH 7.4 is pre- report the effects of ocean acidification on a variety of dicted to occur by approximately 2250; Caldeira & discrete life history stages of marine invertebrates, Wickett 2003). Although acclimation or microevolu- they are primarily short-term studies. Indeed, to our tionary adaptation might be expected to occur among knowledge, no studies to date have examined the marine invertebrates as they encounter seas with de- impacts of chronic exposure to CO2-driven ocean acid- clining pH, a period of several hundred years is ification across all life history stages with the exception arguably a relatively brief period on traditional evo- of the brief 9 d life cycle of the copepod Acartia tsuen- lutionary time scales. Moreover, recently it was dis- sis (Kurihara & Ishimatsu 2008). This gap in our knowl- covered that marine invertebrates such as barnacles, edge is emphasized in a recent paper by Dupont et al. living in coastal regions along the continental shelf (2008) indicating the importance of future studies of western North America (Canada to Mexico), are examining the collective effects of ocean acidification increasingly exposed to seasonally upwelled, corrosive across all life stages of given species. ‘acidified’ seawater (pH 7.6 to 7.7; Feely et al. 2008). Accordingly, here we examined the effects of CO2- Although much of this acidification is due to natural induced ocean acidification over the course of all major respiration processes at intermediate depths below the life history stages, from larval release of the nauplius to photic zone, the continued uptake of anthropogenic reproductive adult, of the common intertidal barnacle CO2 is increasing the areal extent of exposure of Amphibalanus amphitrite. Barnacles are important marine organisms to waters that are undersaturated members of shallow marine ecosystems, and others with respect to polymorphs of calcium carbonate have considered it important to understand the effects (Feely et al. 2008). of ocean acidification on them. For example, one mod- eling study (Wootton et al. 2008) and another experi- mental technique study (Findlay et al. 2008) included MATERIALS AND METHODS barnacles in their analyses. To our knowledge, ours is only the second experimental study to investigate the Larval collection and culture. Naupliar larvae were effects of ocean acidification on barnacles (see Findlay collected from living adult Amphibalanus amphitrite re- et al. 2009), an ecologically important group of benthic moved by mechanical force from wooden pilings of the calcified marine invertebrates. pier at Duke Marine Laboratory along Beaufort Inlet, McDonald et al.: Ocean acidification and barnacle life history 181 North Carolina, USA (34° 43.0’ N; 76° 40.3’ W) in August 1984). Once the naupliar larvae had developed into 2008. Adult barnacles were placed in a 19 l bucket of cyprid larvae, the culture beakers were monitored seawater and broken apart using a hammer. The bucket approximately every 4 h to check for cyprid attach- containing the barnacles was subsequently placed in a ment and metamorphosis. Both nauplii and cyprids dark room, and a fiber optic light was positioned against were sub-sampled from each of the beakers on Days 2, one side of the bucket to attract swimming naupliar lar- 3, 4, and 5 post-naupliar release for later observations vae.