Environmental and intraspecific dimorphism effects on the stable isotope composition of deep-sea benthic foraminifera from the Southern Gulf of California, Mexico

Marine Micropaleontology 71 (2009) 80–95

Contents lists available at ScienceDirect

Marine Micropaleontology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / m a r m i c r o

Environmental and intraspecific dimorphism effects on the stable isotope composition of deep-sea benthic foraminifera from the Southern Gulf of California, Mexico Francisca Staines-Urías ⁎,1, Robert G. Douglas Department of Earth Sciences, University of Southern California, Los Angeles, CA 90089-0740, USA

a r t i c l e

i n f o

Article history: Received 10 September 2008 Received in revised form 23 January 2009 Accepted 25 January 2009 Keywords: benthic foraminifera dimorphism microhabitat isotopic composition Gulf of California

a b s t r a c t We studied the influence of microhabitat, organic matter flux, and metabolism on the stable oxygen and carbon isotope composition of live (Rose Bengal stained) and dead (empty tests) dimorphic generations (microspheric/sexual and megalospheric/asexual) of deep-sea benthic foraminifera from the southern Gulf of California. Despite the range of environmental conditions that exists between the investigated sites, the distribution and live abundance of dimorphic generations of Bolivina subadvena Cushman and B. argentea Cushman were similar: in every site, each dimorphic generation displayed the same relative depth distribution. Maximum abundance of megalospheric B. argentea was observed between 0 and 2 mm, whereas the microspheric generation of this species is most abundant at depths between 1 and 3 mm. For B. subadvena, megalospheric individuals concentrated at the organic-rich boundary layer (0–1 mm), while individuals of the microspheric generation were most abundant deeper in the sediment (4 and 6 mm). Different specific responses to carbon rain variability were indicate by the variation in the proportions of dimorphic generation and by the consistently lighter δ13C and δ18O values observed in B. subadvena compared to B. argentea. Indicating that B. subadvena populations are being maintain, largely, through asexual reproduction (megalospheric generation), which requires high metabolic rates that account for a larger incorporation of metabolic CO2 into their tests. The comparison of isotopic measurements from three size classes (125, 150 and 250 µm) in dimorphic generations of B. subadvena showed that isotopic fractionation related to ontogeny is small compared to the variation due to dimorphism, illustrating the potential use of the isotopic signals of these two species in the reconstruction of past organic matter fluxes, if the species life strategies are considered. © 2009 Elsevier B.V. All rights reserved.

1. Introduction Our knowledge of the natural variability of the oceans and its control by external forcing and internal dynamics is limited. Differences between past and present conditions are unclear, and future changes are difficult to predict. Reconstruction of paleoceanographic records is an important step toward understanding long-term ocean variability, including present conditions, and provides a reference point for speculation about subsequent changes through natural variability or anthropogenic influences. Isotopic analyses of foraminiferal carbonate provide much of the available evidence concerning past oceanographic conditions. Carbon isotopes from benthic foraminifera carbonate tests have been used as

⁎ Corresponding author. E-mail address: [email protected] (F. Staines-Urías). 1 Present address: CEREGE, CNRS, Europôle Méditérrannéen de l'Arbois, Avenue Louis PHILIBERT, BP80, 13545 Aix en Provence Cedex 04, France. 0377-8398/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.marmicro.2009.01.007

proxies of paleoproductivity and water masses characteristics (e.g. Rathburn et al., 1997; Schmiedl and Mackensen, 1997; Berelson and Stott, 2003; Holsten et al., 2004; Curry and Oppo, 2005). The stable oxygen isotope composition of deep-sea benthic foraminifera has been use to estimate fluctuations of global ice volume and benthic δ18O curves have been used to reconstruct past sea level changes (e.g. Rohling and Cooke, 1999; Waelbroeck et al., 2002; Wade and Pälike, 2004). Yet, the value of any foraminiferal species as a proxy relies on the assumption that the test reflects the environmental conditions in which the animals grew, and that shell mineralogy and geochemistry are reliable recorders of benthic chemistry. Multi-species measurements and the study of recent foraminifera revealed that the stable isotope composition of the test calcite of most species exhibits strong deviations from the calcite precipitated in equilibrium with the ambient bottom water. This disequilibrium is attributed to vital effects, such as incorporation of metabolic CO2 and kinetic effects dependent on the metabolism and calcification rate of the organism. Furthermore, there is evidence indicating that in benthic foraminifera shell biomineralization can occur by two different pathways (1) via direct seawater supply to the calcification space by

F. Staines-Urías, R.G. Douglas / Marine Micropaleontology 71 (2009) 80–95

vacuolization or (2) by various transcellular transport mechanisms that involve specific cell membranes, to produce two distinctive calcite types (Bentov and Erez, 2005; Toyofuku et al., 2008). Considering that, independently of the precipitation pathway, carbon interacts with various metabolic products associated with shell formation, δ13C values of foraminifera are generally more negative than δ13C values in equilibrium with the surrounding water (McCorkle et al., 1990; Spero and Lea, 1996). Thus, researchers had concluded that the stable isotope geochemistry of foraminifera is a reasonably good recorder of environmental conditions, but that reproducible offsets from predicted equilibrium are the rule rather than the exception (Wefer and Berger, 1991; Corliss et al., 2002; Schmiedl et al., 2004). In addition, the shells of many benthic foraminifera species manifest different degrees of morphologic variations, from minor phenotypic differences to significant variations in shell morphology. These morphotypes reflect differences in life cycles and consequently in metabolic processes that, ultimately, affect the degree of isotopic fractionation of individuals within a species. In foraminifera, life cycles may differ from one species to another with respect to gamete morphology, mode of fertilization, test dimorphism, and the pattern of sexual and asexual generations (Goldstein, 1999). Additionally, those taxa that are most abundant within a single contemporaneous assemblage may employ quite different reproductive strategies, depending on the prevailing environmental conditions (Goldstein, 2002). In the absence of evidence to the contrary, most investigators assume that morphovariants respond in the same way to the physical environment, and do not differ significantly in shell mineralogy or geochemistry. In order to minimize any possible effects of morphological variation, analyses are usually based on randomly selected groups of shells. All available evidence shows that the interpretation of carbon isotopes in benthic foraminifera tests in relation to chemical properties of bottom and interstitial waters requires an exhaustive knowledge of the ecology of the investigated taxa (microhabitat, population dynamics, reproductive patterns, food preferences) and understanding of geochemical processes affecting the carbonate and stable isotope chemistry of interstitial waters. The complexity of the factors influencing the stable isotope composition of deep-sea benthic foraminifera demonstrates the necessity of isotopic studies on living benthic foraminifera in relation to their biology and microhabitat. A few studies have documented changes in community structure among shallow and deep infaunal species that are found in low oxygen environments (Gooday et al., 2000; Bernhard, 2003; Ernest et al., 2005). Efforts are also being made to determine the influence of carbon input variability in community structure and specific depths distributions (Rathburn et al., 2001; Fontanier et al., 2003, 2005). However, relatively few studies have attempted to document how biogeochemical variability such as changes in carbon oxidation is incorporated into foraminiferal shell chemistry (Fillipsson et al., 2004; Holsten et al., 2004; Schmiedl et al., 2004) and even fewer studies have attempted to determine the effects of sexual dimorphism on test composition (Nigam and Sarkar, 1993; Douglas and Staines-Urías, 2007). In the present study, we concentrate on the stable oxygen and carbon isotope signatures of two common species of benthic foraminifera that exhibit sexual dimorphism and occur in dysoxic to anoxic marine sediments from the Gulf of California: Bolivina subadvena Cushman: Smith, 1963 and B. argentea Cushman: Cushman and McCulloch, 1942. We will compare the δ18O and δ13C of these species with physico-chemical properties (temperature, TCO2 profiles) of bottom and pore water, in an effort to determine whether dimorphic sexual generations of these species respond similarly to biogeochemical variability and to understand the factors that influence the incorporation of 12C and 13C into the calcium carbonate tests of the aforementioned species. Species of the genus Bolivina have been commonly used as environmental indicators in the Gulf of California and the adjacent Pacific Ocean margin. (Sen Gupta and Machain-Castillo, 1993; Gooday,

81

1994; Berelson and Stott, 2003; Holsten et al., 2004; Douglas and StainesUrías, 2007). Particularly, due to their sensitivity to oxygen and organic carbon concentrations, broad distribution, and high abundance, B. subadvena and B. argentea offer potential as paleoceanographic proxies in researching two important problems — ocean ventilation and organic carbon cycling in marine sediments. In the Gulf of California, as in many other upwelling areas, primary productivity and particle fluxes to the sea floor vary seasonally. The quantity of organic carbon exported from the surface waters and the amount of biogenic material subsequently buried may be both, spatially and temporally variable (Thunell et al., 1996; Thunell, 1998; Pike and Kemp, 1999). This affects bottom water chemistry and benthic biological activity (Thunell, 1998; Gooday and Hughes, 2002; Berelson et al., 2005; Fontanier et al., 2005). Furthermore, there is a growing body of evidence indicating that marine productivity along continental margins and particularly within major upwelling regions have undergone significant variability in the past (Stott et al., 2000; Berelson and Stott, 2003). Because there have been varying interpretations of the carbon isotopic records that accompanied this environmental variability, a better understanding of the factors controlling the geochemistry of foraminifera carbonate will improve the reliability of paleoceanographic reconstructions based on the isotopic composition of benthic foraminifera shells. 2. Dimorphism in benthic foraminifera As for many other marine organisms, foraminifera exhibit two kinds of reproductive modes, i.e. dimorphism. The typical foraminiferal life cycle is characterized by an alternation of sexual and asexual generations (Goldstein, 1999). The sexual generation (gamonts) reproduces by gametogenesis, and pairs of gametes fuse to form the asexual generation (agamonts), which in turn reproduces by division of the parental cell to form either agamonts or gamonts (Boltovskoy and Wright, 1976; Goldstein, 1997). However, among other protists groups, the life cycle of the foraminifera is one of the more variables. For example, the alternation of generations may be obligatory (the typical life cycle) or facultative (this life cycle includes one sexual and two or more asexual generations that may or not present trimorphism; Goldstein, 1999). Furthermore, autogamy (self fertilization) occurs in some foraminifera taxa (Arnold, 1955; Grell, 1954, 1957), including a number of Bolivina species (Sliter, 1970). This mode of fertilization is very difficult to distinguish from the classic asexual reproduction. Although, it has been reported that in autogamic species the size of the offspring may vary depending if the specimen was produce sexually (smaller) or by multiple fission (larger) (Arnold, 1955). Both, B. subadvena and B. argentea exhibit a typical reproductive dimorphism, what led us to suppose that, for both species, the life cycle corresponds to a heterophasic alternation of sexual and asexual generations. In these species, alternate sexual generations are characterized by distinctive morphotypes defined not by the size of the individual but by the difference in the size of the initial chamber or proloculus. Because the sexual generation develops from gametes that are typically 1–4 μm, the proloculus is microspheric. In the asexual generation, division creates a relatively large — megalospheric — proloculus. However, the adult shell of the asexual generation typically has fewer chambers and/or is smaller than adults of the sexual generation (Smith, 1963). In this genus, microspheric and megalospheric generations are usually easy to distinguish because the proloculus is visible (Lutze, 1964). In the Gulf of California, megalospheric (asexual) forms of B. subadvena typically have an oval to slightly compressed cross-section, are smaller and have fewer chambers than microspheric (sexual) forms. The microspheric generation has larger and more elongated tests, with morphovariants ranging from prolate/spheroidal to compressed. In B. argentea, a compressed shape and sharp margins are common to both dimorphic generations. The megalospheric

82

F. Staines-Urías, R.G. Douglas / Marine Micropaleontology 71 (2009) 80–95

Table 1 Distinctive characteristics of dimorphic generation (sexual and asexual) of Bolivina subadvena and Bolivina argentea

Reproductive mode Mg/Ca rates Growing rate Proculus size Life strategy

Preferred habitat

Microspheric

Megalospheric

Sexual Low Slow Small Steady population numbers, tolerance to low oxygen concentration Infaunal Deeper in the sediment

Asexual High Fast Large Blooms during eutrophic periods, opportunistic, short live Epifaunal Near water sediment nterface

specimens are generally smaller and present fewer chambers than microspheric forms. However, the difference in the size between generations is not as conspicuous as in B. subadvena morphotypes. Morphotypic characteristics and distinctive reproductive mode are summarized in Table 1. Previous studies have proved that ratios of dimorphic forms (microspheric/megalospheric) are a useful tool in determining environmental variability (Boltovskoy and Wright, 1976; Nigam, 2005). Published observations based on field samples and laboratory experiments, have indicated an inverse relation between microspheric/megalospheric ratios, and temperature (Nigam and Caron, 2000) and salinity (Nigam 1986; Nigam and Khare, 1995). However, isotopic variation between morphotypes has hardly been explored and only few studies have investigated isotopic composition differences in dimorphic species as a paleooceanographic tool. In a previous study, observations on Rotalidium annectens dead specimens, from the west coast of India, indicated that there is a relation between proloculus size — as a measure of dimorphism — and changes in temperature and salinity (Nigam and Sarkar, 1993). In this study, the authors recognized a significant inverse relation between temperature and salinity, and proloculus size. However, when the isotopic composition (δ18O and δ13C) of each specimen was evaluated against proloculus size, no consistent relation was observed. In the Gulf of California, a study of the isotopic composition of benthic foraminifera found that randomly selected shells of the same species, same morphotype, and from the same sediment sample, had values within 0.15‰ of each other. However, differences in excess of 0.2‰ were detected between microspheric and megalospheric specimens (Douglas and Staines-Urías, 2007). Using B. subadvena as a target species, these authors observed that similarly to the isotopic composition, shell Mg/Ca ratios vary between morphotypes, suggesting different life strategies. The megalospheric generation, which has higher Mg/Ca ratios, appears to be opportunist, blooming in response to organic carbon input. Their response to phytodetritus pulses is similar to that of abyssal benthic foraminifera (Gooday, 1988). Other benthic species that concentrate in the topmost sediment, just below the sediment surface, exhibit similar behavior. In these species, the population declines as soon as the phytodetritus supply from the surface decreases. Population numbers then remain low, increasing only when food becomes available again (Gooday, 1996; Gooday and Rathburn, 1999). Seasonal responses imply that individuals grow rapidly to exploit pulses of phytodetritus to the seafloor during the eutrophic season. In the megalospheric morphotype of B. subadvena, rapid shell growth probably accounts for high Mg uptake and high Mg/Ca ratios (Douglas and Staines-Urías, 2007). Microspheric B. subadvena, which have lower Mg/Ca ratios than megalospheric specimens, appear to grow more slowly and under less optimal conditions, and survive for longer periods. Similar growth strategies have been observed in species from other locations that exhibit seasonal patterns with maximum abundances during the oligotrophic season (Fontanier et al., 2005). These species tend to

prefer infaunal habitats and have relatively high tolerance to low oxygen concentrations (Jorissen et al., 1995; Schmiedl et al., 2004). As phytodetritus deposited during the eutrophic season degrades, these species migrate closer to the sediment surface to feed and reproduce (Linke, 1992; Gooday and Rathburn, 1999; Corliss et al., 2002). Intermittent and slow shell growth may explain the low Mg/Ca ratios in microspheric forms of B. subadvena. Because the microspheric shell is secreted over a relatively long period, its composition represents an average record of bottom conditions over multiple seasons or years (Douglas and Staines-Urías, 2007). In this paper we produce further evidence to support the hypothesis that dimorphic generations of B. subadvena and B. argentea differ in ecology and life habits, resulting in differences in the isotopic signal recorded by each morphotype. 3. Environmental settings The samples used for this investigation were collected from the southern region of the Gulf of California. The Gulf of California is a unique example of a marginal sea where the global atmospheric signal is amplified and modified by regional effects. Due to a well developed oxygen minimum zone (OMZ), the Gulf is also one of the classic locations for annually accumulating laminated (varved) sediments. One well-known characteristic of the Gulf is its high primary productivity, which is climatically driven (Thunell et al., 1996; Thunell, 1998). Wind-created upwelling produces Ekman transport that advects nutrient-rich deep waters to the surface, supporting high primary production. This high primary productivity, in association with moderate rates of deep thermohaline ventilation, creates an OMZ between − 300 and − 800 m (Fernández-Barajas et al., 1994). Laminated sediments are observed in areas where bottom oxygen concentration is b9 µM (0.2 mL L− 1), roughly the trace of the OMZ where it impinges on the slope (Calvert, 1966). In the Gulf, dry and cool winter conditions persist as the East Pacific High and the Inter-Tropical Convergence Zone (ITCZ) retreat towards the Equator. A stable pressure gradient exists and northwesterly surface winds are polarized along the Gulf axis (Pares-Sierra et al., 2003; Jiménez et al., 2005). Northwesterly winds generate coastal upwelling along the eastern side of the Gulf, supporting high primary productivity along this margin. During summer, when the East Pacific High and the ITCZ move northward, the wind field changes, northwesterly winds diminish, and winds crossing the Gulf alternate with intermittent surges that transport moisture northward along the Gulf (Bordoni et al., 2004). Upwelling ceases and primary productivity diminishes. Along the Gulf, the biological response to climate forcing is evident, with important regional differences. It is in the southern region where mid-latitude and tropical influences are better expressed, and local processes, such as internal waves mixing or the permanent upwelling exiting along the Midriff Islands, are least prominent. Because this region is relatively deep, tidal mixing is not very important, and seasonal variability in SST and primary production are clearly associated with climate forcing (Santamaría-del-Ángel et al., 1994). Previous research has revealed an east–west asymmetry in the sedimentary record of the southern Gulf associated with the asymmetry in oceanographic conditions (Van Andel, 1964; Baba et al., 1991; Bernal et al., 2001; Douglas et al., 2002, 2007; Barron et al., 2005). Along each margin, the differences in surface and intermediate water circulation affect the rates of carbon input to the seabed, influencing the amount of dissolved oxygen in bottom waters, creating laminated sediments that are not uniform, but differed in appearance, thickness and composition (Douglas et al., 2002; González-Yajimovich et al., 2005). The locations for this investigation were selected to evaluate these differences. The selected locations are similar in terms of bottom

F. Staines-Urías, R.G. Douglas / Marine Micropaleontology 71 (2009) 80–95

83

Fig. 1. Map of the Gulf of California showing simplified bathymetry (meters), locations of the investigated sites (squares), location of water collection site (circle), and Alfonso and Pescadero Basins location and bathymetry (insets).

water temperature and salinity but differ in terms of organic matter flux and oxygen concentration (Fig. 1, Table 2). Two stations were located on the eastern side of the Gulf, in the Pescadero Basin slope (stations 26 and 27). This basin is located at the entrance of the Gulf, beneath major upwelling plumes. Its position and depth (a maximum of −3000 m) allow free exchange with the waters of the Pacific (Castro et al., 2000). In this area, inputs of fresh organic material are enhanced from October through April, during the upwelling season. The accumulation and decomposition of organic matter reduces oxygen levels (b0.2 µM) and limits oxygen penetration in the sediment (Berelson et al., 2005). A third station was located on the western side, in Alfonso Basin (station 15). This basin is a relatively small closed depression, with a maximum depth of − 400 m and an effective sill depth of about −320 m (Nava-Sánchez et al., 2001). Here primary production is lower and mostly sustained by upwelled water transported from the eastern side by across-Gulf eddies (Pegau et al., 2002). Low-oxygen intermediate water enters the basin and below −200 m, water become suboxic to anoxic (b0.5 µm) (González-Yajimovich et al., 2005). As mentioned before, Pescadero and Alfonso Basin are two locations with contrasting primary productivity settings that produce observable differences in the amount or organic matter reaching the

bottom of each basin. Such differences have been investigated in various occasions (Berelson et al., 2005; Prokopenko et al., 2006). In particular, it has been proposed that high organic content and rapid accumulation rates are the determining factors for the preservation of the original δ15N composition of the sedimentary organic nitrogen (Altabet et al., 1999; Pride et al., 1999). Since, ammonium is a major metabolic product of organic matter decomposition and its δ15N reflects the isotopic composition of decomposing organic nitrogen (plus a small fractionation due to diagenetic processes), the differences in the organic carbon input between Alfonso and Pescadero Basins can be investigated by examining downcore differences in the δ15N of pore water (Hartnett and Devol, 2003). Prokopenko et al. (2006) determined that, in both basins, pore water ammonium was enriched in 15N isotopes, indicating decomposition of organic matter. However, pore water ammonium in the sediments at Pescadero was much lighter (closer to the average δ15N value of the organic matter raining to the sea floor, 8.5‰) than in Alfonso. In Pescadero, surface pore water δ15N values were around 13–14‰ whereas Alfonso exhibited δ15N surface values of 21%. Such results indicate that in Pescadero Basin sedimentation rates and related organic carbon rain must be considerable higher than in Alfonso, facilitating a better preservation of the original isotopic composition of the organic nitrogen.

84

F. Staines-Urías, R.G. Douglas / Marine Micropaleontology 71 (2009) 80–95

Table 2 Location, water depths, oceanographic, geochemical, biological, and sedimentological parameters displaying environmental differences between sites in Alfonso (station 15) and Pescadero (stations 26 and 27) Basins Parameter Station ID Latitude (N) Longitude (W) Water depth Temperature Salinity Oxygen Average total benthic foraminifera [0–1 cm] Total CO2 (TCO2) [0–5 mm] Total organic carbon (TOC) [0–1 cm] Organic carbon MARs Total MARs [0–1 cm] Terrigenous sediment MARs [0–1 cm] Total CaCO3 [0–1 cm] CaCO3 MARs [0–1 cm] Grain size [0–1 cm]

Unit

m °C psu μM specimens gr− 1 mM wt.% mg cm− 2 year− 1 mg cm− 2 year− 1 mg cm− 2 year− 1 wt.% mg cm− 2 year− 1 μm

Alfonso Basin

Pescadero Basin Slope

15 24°16′70″ 110°36′06″ 415 9.1 34.62 0.5 704 2.35 5.61 0.55 12.54 7.65 15.11 1.89 9.602 (median 25.504 (mean)

26 24°16′70″ 108°11′67″ 600 6.7 34.54 0 1019 2.40 3.97 0.68 20.55 15.51 5.5 1.13 5.000 (median) 7.680 (mean)

Data sourcea 27 24°38′18″ 108°10′70″ 500 7.4 34.52 0.2 2259 2.38 – – – – – – –

This This This ⁎ This ⁎ ⁎⁎ ⁎⁎ ⁎⁎

study study study study

⁎⁎ ⁎⁎ ⁎⁎

MARs = Mass Accumulation Rates. a Following data sources have been used: (⁎) Berelson et al. (2005), (⁎⁎) Gonzalez-Yajimovich (2004).

Furthermore, Berelson et al. (2005) observed that the interaction of biologic and oceanographic processes produces contrasting profiles of dissolved TCO2 in the uppermost section (top centimeters) of the sediment within each basin (Fig. 2). 4. Methods Laminated sediments were obtained, using a multicore device, during November 2001 (NH01-CALMEX cruise). Immediately after a core was retrieved, sediment was extruded from the multicore tube and sampled every 1 mm. The estimated error for the depth horizon assigned to each sample — calculated by dividing the total length of the multicore by the number of samples — was approximately ±1 mm. In order to differentiate between benthic foraminifera that were live vs. dead at the time of collection, all samples were preserved in buffered ethanol with Rose Bengal stain (Murray and Bowser, 2000). In anoxic sediment, the degradation of protoplasm may take a considerable period of time (Bernhard, 1988; Corliss and Emerson, 1990), so some dead specimens may be stained. To avoid the inclusion

of such uncertain specimens, only foraminifera in which all but the last chamber, were strongly stained were counted as live. All samples were labeled and wet-preserved (Sperling et al., 2002). This wet preservation method allows a more accurate recognition of stained cytoplasm, which shrinks when dried. In the laboratory, sediment samples were wet-sieved through a 63 µm screen. B. subadvena and B. argentea specimens were counted in the sediment size fraction N63 µm. Specimens were divided into microspheric and megalospheric morphologies, representing different dimorphic generations. For each station a second multicore was used to calculate dry bulk densities in order to transform volumetric-based abundances into abundance per gram of dried sediment. Isotopic analyses of oxygen (δ18O) and carbon (δ13C) were conducted on live and dead specimens. The analyzed samples weighed between 40 and 70 µg, which was 5 to 12 specimens per sample. The specimens used for isotopic measurements were selected within a narrower size range (125–180 µm) than the range used for faunal analysis (N63 µm). After selection, shells were cleaned and prepared according to a procedure first developed by Boyle (1995) and modified to manage

Fig. 2. (A) Pore water TCO2 gradients from Alfonso Basin (station 15) and Pescadero Basin (stations 26 and 27) data from Berelson et al. (2005). (B) Pore water δ13CTCO2 gradients corresponding to the TCO2 profiles presented in panel (A) predicted using Eq. (1) (see Section 4).

F. Staines-Urías, R.G. Douglas / Marine Micropaleontology 71 (2009) 80–95

85

Fig. 3. Live (Rose Bengal stained) abundance profiles (no. specimens g− 1) of benthic foraminifera Bolivina subadvena (closed squares) and Bolivina argentea (open circles) at the three investigated sites. Symbol size indicate different morphotypes (large = megalospheric, small = microspheric). Note difference in scale for station 27.

small samples (less than 100 µg, Douglas and Staines-Urías, 2007). This treatment, originally developed for trace metal analysis, improves the repeatability and accuracy of isotopic measurements (L. Stott personal communication) as shown by preliminary isotopic analyses of foraminiferal carbonate duplicates, carried out in the Mass Spectrometer facility at USC-Department of Earth Sciences, as complement to a previous interlaboratory calibration (Rosenthal et al., 2004). Isotope analyses were carried out using a VG Prism stable isotope ratio mass spectrometer (IRMS), equipped with an automated common acid carbonate system. Samples were reacted in 100% phosphoric acid at 90 °C. Resulting CO2 gas was then analyzed on the IRMS. Oxygen and carbon isotopic data are reported in delta notation relative to PDB standard, Vienna. The long-term standard reproducibility for δ13C is ±0.1‰, based on replicate measurements of a reference standard. In each station, a third multicore was employed to determine TCO2 in pore water (Berelson et al., 2005). Multicores' pore water was sampled by whole-core squeezing (Bender et al., 1987). For each core, a plug was inserted into the bottom and a piston inserted into the top. The piston was pushed down, and the water expressed through a hole in the piston was collected through a filter into sample bottles and syringes (Berelson et al., 1989). The travel of the piston, the sediment porosity, and the volume of water expressed, are measures of where each sample split is located with respect to the sediment depth. The uncertainty in the calculated depth is related to the assignment of the water–sediment interface (depth = 0). The water–sediment interface was visually determined where the piston touched the sediment surface. The approximate uncertainty in depth assignment was ±2 mm. Previous research has revealed that the δ13C of pore water TCO2 can be modeled using a simple isotope mass balance that combines CO2, derived from marine photosynthate organic carbon oxidation (−17‰ to −21‰), with bottom water TCO2, and its δ13C (Stott et al., 2000; Berelson and Stott, 2003; Holsten et al., 2004). This combination can be presented as:

h
i

 13 13 13 ðTCO2bw Þ · δ Cbw + δ Corg TCO2pw − TCO2bw = TCO2pw δ Cpw

ð1Þ

Where (bw) indicates bottom water value and (pw) refers to a pore water value at a chosen sediment depth. For this simplified calculation it is assume that the CO2 added to the pore water profile is derived only from the oxidation of photosynthate carbon with a specific carbon isotopic composition. This calculation does not account for any interaction between discrete sediment depth horizons (e.g. diffusion, any reaction process that affect the overall shape of the pore water profile). Bottom water δ13C values were not measured in any of the selected stations. To estimate pore water δ13C TCO2 values (Fig. 2), we used a bottom water δ13C TCO2 value of − 0.338‰, measured at 500 m depth in a nearby station (Fig. 1). 5. Results 5.1. Microhabitat preferences of living foraminifera Many factors have been proposed to explain the benthic foraminiferal microhabitat, the most important ones being food availability, oxygen concentration, ecosystem stability, competition, and predation. A first step to establish if dimorphic generations differ in their response to environmental variability is to determine if dimorphic generations of the same species have different microhabitat preferences. Furthermore, because the δ13C signals reflect the chemical properties of the microhabitat in which the foraminifera calcified, the evaluation of any species as a potential paleoceanographic proxy requires determining its preferred microhabitat. The vertical distribution of live specimens from the selected foraminiferal species shows the occupation of various microhabitats below the water–sediment interface. Based on counts in the Alfonso and Pescadero Basins, it appears that the dimorphic generations of each species exhibit preference for different microhabitats (Fig. 3). B. subadvena was abundant in all samples. Together, the dimorphic generations of this species constitute up to 89% of the total living benthic foraminifer assemblage. The maximum abundance of megalospheric B. subadvena was observed between 0 and 1 mm, indicating that this generation inhabits the organic-rich boundary layer (fluff layer) at the water–sediment interface. Individuals of the microspheric generation were concentrated deeper in the sediment, between 4 and 7 mm.

86

F. Staines-Urías, R.G. Douglas / Marine Micropaleontology 71 (2009) 80–95

Table 3 Average and standard deviation δ13C and δ18O values, and number of samples analyzed, of live and dead benthic foraminifera from sites 15, 26 and 27 Bolivina subadvena

Bolivina argentea

Megalospheric δ13C

δ18O

Microspheric No. of samples

[‰ VPDB] Live Station 26 Average Std. dev. Station 27 Average Std. dev. Station 15 Average Std. dev. Dead Station 26 Average Std. dev. Station 27 Average Std. dev. Station 15 Average Std. dev.

δ13C

δ18O

Megalospheric No. of samples

[‰ VPDB]

δ13C

δ18O

Microspheric No. of samples

[‰ VPDB]

δ13C

δ18O

No. of samples

[‰ VPDB]

− 1.571 0.122

1.748 0.057

6

− 1.335 0.005

2.021 0.135

4

− 0.538 0.122

1.933 0.159

2

− 0.344 0.010

2.150 0.071

3

− 1.537 0.156

1.841 0.147

5

− 1.506 0.039

1.982 0.120

5

− 0.687 0.028

1.866 0.393

3

− 0.566 0.054

2.045 0.095

4

− 0.925 0.097

1.777 0.024

8

− 0.740 0.084

1.969 0.087

6

– –

– –

–

– –

– _

–

− 1.487 0.149

1.951 0.159

6

− 1.362 0.072

1.908 0.159

3

− 0.488 –

2.175 –

1

− 0.487 0.257

2.450 0.270

3

− 1.844 –

1.755 –

1

− 1.410 0.107

1.846 0.196

2

− 0.655 0.123

2.184 0.088

5

− 0.443 0.099

2.250 0.087

5

− 0.808 0.122

1.586 0.155

6

− 0.752 0.088

1.708 0.112

6

– –

– –

–

– –

– –

–

In Alfonso Basin (station 15) B. argentea was absent, no live or dead specimens were observed in samples from this location. In Pescadero basin (stations 26 and 27), megalospheric B. argentea were most abundant within the top millimeter, near the water–sediment interface, and the microspheric generation of this species was observed to be most abundant between 1 and 3 mm depth. The depth of maximum live abundance of each morphotype varies by 1 mm between sites, which is equivalent to the uncertainty

of the sampling. Megalospheric B. subadvena and megalospheric B. argentea show preference for a shallow microhabitat. Microspheric B. argentea appears to distribute itself in the sediment at an intermediate depth (2–3 mm), and microspheric B. subadvena was persistently observed deeper in the sediments, between 4 and 7 mm. It appears that, despite the range of environmental conditions that exists between sites (e.g. sediment accumulation rates, oxygen concentration, carbon rain rates, etc.) and the slight inter-basin

Fig. 4. Mean δ18O signatures of live (Rose Bengal stained) and dead Bolivina subadvena and Bolivina argentea respect of water temperature and depth in each station.

F. Staines-Urías, R.G. Douglas / Marine Micropaleontology 71 (2009) 80–95

87

Fig. 5. Measure δ18O of benthic foraminifera in Pescadero (stations 26 and 27) and Alfonso (station 15) Basins. Top panels show live megalospheric Bolivina argentea (close circles), microspheric Bolivina argentea (open circle), megalospheric Bolivina subadvena (close squares), and microspheric Bolivina subadvena (open squares). Bottom panels similar to top panels but for dead specimens.

difference in the depth of maximum abundance, each generation displays the same relative depth distribution in each location, i.e. shallow, intermediate, deep. 5.2. Isotopic composition of live specimens Significant differences were observed in the stable oxygen and carbon isotope composition between species and between dimorphic generations. The total range of δ18O values is between 1.586‰ and 2.450‰ (Table 3). By comparing the δ18O values of each morphotype in each station, we observed a systematic trend of increasing δ18O values with increasing water depth as a direct result of temperature decrease (Fig. 4). The δ18O of the taxa here investigated do not vary systematically in relation to sediment depth. Although, δ18O species-specific and some morphotype-specific differences were detected, the different microhabitat preferences of the species investigated do not seem to induce any systematic impact on the stable oxygen isotopes in their tests. In general, B. argentea exhibited higher δ18O values compared to B. subadvena, and within each taxon, megalospheric forms showed lighter oxygen composition than their microspheric counterparts (Fig. 5).

The total range of δ13C values is between − 1.844‰ and −0.344‰ (Table 3). In general, B. subadvena isotopic values were lower than those of B. argentea. Within each species, megalospheric individuals displayed more negative δ13C values than microspheric specimens (Fig. 6). As observed in the δ18O values, δ13C values of megalospheric forms display higher variability compared to those of microspheric forms. 5.3. Isotopic composition of dead specimens Ranges and mean values were similar to those of live specimens at the same depth interval (Figs. 5 and 6). However, the scatter (i.e. standard deviation) in the δ13C and δ18O values is slightly larger than the observed in the live specimens (Table 3). The interbasin difference in the δ13C values was considerably greater and more persistent than the interbasin difference in δ18O values. The trend of increasing δ18O with increasing water depth, observed in live individuals, is also noticeable in dead specimens (Fig. 4). In planktic foraminifera, ontogenic trends toward higher δ18O and δ13C values with increasing test size, suggesting elevated metabolism in juveniles (Spero and Lea, 1996), further complicate the use of stable isotopes in paleoceanography. Remarkably, deep-sea foraminifera

88

F. Staines-Urías, R.G. Douglas / Marine Micropaleontology 71 (2009) 80–95

Fig. 6. Measure δ13c of benthic foraminifera in Pescadero (stations 26 and 27) and Alfonso (station 15) Basins. Top panels show live megalospheric Bolivina argentea (close circles), microspheric Bolivina argentea (open circles), megalospheric Bolivina subadvena (close squares), and microspheric Bolivina subadvena (open squares). Bottom panels similar to top panels but for dead specimens.

seem to lack a significant change in their stable isotope composition with size (Vincent et al., 1981; Dunbar and Wefer, 1984; Grossman, 1987; Wefer and Berger, 1980; Corliss et al., 2002). To estimate the magnitude of the ontogenic effect in the stable isotope composition of B. subadvena, we evaluated the relationship between test size and isotope composition in three size fractions (125–150, 150–250, and N250 µm) of dead specimens of each dimorphic generation. The samples were obtained from the Alfonso Basin where both morphotypes were abundant and exhibited large size ranges. Ontogenic trends were not estimated in B. argentea or in live specimens of B. subadvena, because in all samples live individuals presented small size ranges that didn't allow us to separate specimens into size categories. Results indicate that megalospheric shells exhibit the lower variation in isotope composition with size (Fig. 7, Table 4). The mean δ13C value for the three size fractions of megalospheric B. subadvena was −0.912‰, with a maximum difference of 0.041‰ between the overall average and the average of the most different size class. The overall average δ18O value was 1.559‰, with a maximum difference of 0.086‰ for the most different size class. Microspheric specimens exhibited greater isotopic variability. The δ13C average was −0.634‰, with a maximum difference of 0.096‰ between the average and the most different fraction. In this

morphotype the average value for the δ18O values was 1.354‰, with a maximum difference of 0.121‰. 6. Discussion 6.1. Reproductive dimorphism and differences in shell composition We noticed that compared to the microspheric individuals, the megalospheric specimens exhibit larger deviations from the calculated δ13C of pore water TCO2 (Fig. 8). Although differences between foraminiferal δ13C and pore water δ13C dissolved inorganic carbon (DIC = TCO2) were observed in megalospheric B. argentea, the δ13C signal of this morphotype is comparable to that of pore water at shallow sediment depths, in accordance with its habitat preferences. However, megalospheric B. subadvena δ13C values are substantially lower than expected considering its preference for a shallow habitat. This inconsistency will be analyzed in length in the following paragraphs. In both species, δ13C values of microspheric individuals are consistent with the calculated pore water δ13CDIC values for their preferred microhabitat. Sediment microhabitat is responsible for most of the variability observed in the δ13C signal of infaunal benthic foraminifera (e.g. Rathburn et al., 1996; Mackensen et al., 2000; Holsten et al., 2004;

F. Staines-Urías, R.G. Douglas / Marine Micropaleontology 71 (2009) 80–95

Fig. 7. Stable oxygen and carbon isotope signals of dead specimens of Bolivina subadvena megalospheric (open circles) and microspheric (close circles) dimorphic generations from Alfonso Basin. Samples were selected from a composite of the topmost 3 mm of multicore15. Symbol sizes indicate different size classes.

Schmiedl et al., 2004). The depletion of 13C in pore water TCO2 is mirrored by the decrease of δ13C values with increasing average living depth, and species-specific or generation-specific variations from the expected equilibrium due to isotopic fractionation during calcification, as those observed in megalospheric B. subadvena specimens, are frequently attributed to vital effects. Kinetic fractionation during hydration and hydroxilation of CO2 has been reported as an important factor causing depletion of 18O and 13 C in many biogenic carbonates. This process can be recognized by a significant covariation of δ18O and δ13C values, and is particularly strong at high precipitation rates (McConnaughey et al., 1997; McConnaughey, 2003). Our data show no significant correlation between the δ18O and δ13C values suggesting that other factors than a simple kinetic fractionation during CO2 uptake, are responsible for the anomalous light δ13C values observed in the megalospheric forms (Fig. 9). Accordingly, most studies maintain that vital effects in foraminifera are predominantly caused by incorporation of isotopically light metabolic CO2 into the test carbonate. It has been suggested that the magnitude of this vital effect is proportional to the amount of metabolic CO2 in the internal CO2 pool of each organism (McConnaughey et al., 1997). If so, this vital effect should increase in early life stages and/or during the feeding/growing season, when metabolic rates are higher. Therefore, more negative δ13C and δ18O values would be expected in juvenile specimens and opportunistic species/ generations. Deep-sea foraminiferal faunas respond to seasonal signals. Several studies show that epifaunal deep-sea foraminiferal taxa are capable of taking rapid advantage of seasonal phytodetritus deposition at the sea floor and exhibit a density increase close to the water–sediment interface during eutrophic episodes (e.g. Jorissen et al., 1992; Ohga and Kitazato, 1997; Gooday and Rathburn, 1999; Filipsson et al., 2004; Fontanier et al., 2006). Such reactive behavior has also been observed in laboratory experiments, where reproductive foraminifera responses followed artificial food enrichment in the sediment (Heinz et al., 2001; Ernst et al., 2005). Phytoplankton detritus, which consist of easily hydrolysable organic matter, could sustain the high metabolic activities attributed to the most opportunistic foraminiferal taxa (Gooday and Rathburn, 1999; Gooday and Hughes, 2002; Fontanier et al., 2005).

89

The analysis of carbon stable isotope composition of several benthic foraminifera species showed that the strongest depletion of 13 C is observed in tests of epi- to very shallow infaunal species that are characterized by opportunistic behavior (Ohga and Kitazato, 1997; Schmiedl et al., 2004; Fontanier et al., 2005). The comparison of the δ13C signals of megalospheric B. argentea and megalospheric B. subadvena provides insight into the magnitude of the vital effect on δ13C values. Both, morphotypes inhabit the uppermost section of the sediment and exhibited δ13C values lighter than those of pore water TCO2. However, despite sharing microhabitat preferences, the actual depletion of the δ13C signal with respect to δ13CDIC of pore water is different for each species. The two morphotypes exhibit an average difference of 0.941‰ between their mean δ13C values. The δ13C signal of megalospheric B. argentea is only slightly more negative than the expected value. In contrast, δ13C values of megalospheric B. subadvena specimens exhibit larger offsets from the calculated δ13C value of pore water TCO2 near the water–sediment interface (Fig. 8). In this case microhabitat effects do not explain the observed specific variation in foraminiferal δ13C values, and differences in life cycle between species must be considered. If incorporation of metabolic CO2 is considered as the major factor explaining the vital effect in foraminifera δ13C values, the δ18O values should also exhibit lighter values in opportunistic generations. However, it is expected that the δ13C values should reveal stronger depletion than the concomitant δ18O values. This observation has been attributed to a larger reservoir of oxygen in the ambient water and a smaller reservoir of carbon (bottom water TCO2) which interacts with metabolic CO2 during calcification (Grossman, 1987). When comparing both species, we observed that megalospheric forms have lighter δ18O values than the microspheric ones. It was also noticed that megalospheric B. subadvena exhibit lighter δ18O values than the other morphotypes, in accordance with its reactive behavior (Fig. 5). At the three investigated sites, microspheric forms showed δ13C values closer to those of pore water TCO2. It appears that microspheric

Table 4 Isotopic measurements for size classes of dead specimens of Bolivina subadvena dimorphic generations from Alfonso Basin (station 15) Size class [μm]

Bolivina subadvena Megalospheric δ13C

Microspheric δ18O

[‰ VPDB] N250

150–250

125–150

Average All classes N 250 150–250 125–150 Standard deviation All classes N 250 150–250 125–150

δ13C

δ18O

[‰ VPDB]

− 0.878 − 0.863 – − 0.977 − 1.032 − 0.964 − 0.864 − 0.858 − 1.032 − 0.893 − 0.858 − 0.919 − 0.852 − 0.893 − 0.885 − 0.919

1.477 1.469 – 1.556 1.597 1.594 1.670 1.605 1.597 1.526 1.605 1.542 1.562 1.526 1.513 1.542

− 0.497 − 0.503 − 0.613 − 0.701 − 0.706 – – – – – − 0.728 − 0.689 – – – –

1.261 1.456 1.005 1.464 1.489 – – – – – 1.471 1.345 – – – –

− 0.912 − 0.871 − 0.946 − 0.888

1.559 1.473 1.592 1.548

− 0.634 − 0.538 − 0.704 − 0.709

1.356 1.241 1.477 1.408

0.061 0.011 0.075 0.075

0.054 0.006 0.045 0.045

0.098 0.065 0.004 0.027

0.176 0.226 0.018 0.089

90

F. Staines-Urías, R.G. Douglas / Marine Micropaleontology 71 (2009) 80–95

Fig. 8. Predicted pore water δ13CTCO2 (close triangles) values in the upper cm of the sediment from indicated stations. Average measured δ13C of dimorphic generations of benthic foraminifera Bolivina subadvena (megalospheric = close square, microspheric = open square) and Bolivina argentea (megalospheric = close circle, microspheric = open circle). Vertical error bars indicate the estimated uncertainty in the depth range of maximum abundance, horizontal error bars indicate δ13C values standard deviation.

specimens have lower metabolic rates, favoring calcite precipitation closer to equilibrium with the water. We observed that microspheric forms preferred intermediate and deeper microhabitats. Previous studies have shown that infaunal species, that feed on more degraded organic matter and often live under anoxic conditions, have longer life cycles, commonly exceeding two years (Ohga and Kitazato, 1997; Fontanier et al., 2005). Studies on the seasonal and interannual variability of benthic foraminifera abundance suggest that phytodetritus deposition provokes a rapid reproductive response of the more opportunistic taxa living in the uppermost sediments but that intermediate and deep infaunal populations, associated with deeper redox fronts in the sediment, are much more stable through time and less affected by phytodetritus changes (Gooday and Rathburn, 1999; Fontanier et al., 2003, 2005). The advantage of living in the anoxic part of the sediment

is the lower level of competition because few organisms are able to live there. On the other hand, infaunal species must tolerate anoxia, particularly in oxygen-deprived environments. It is generally accepted that foraminifera are aerobes, however, field investigations and laboratory experiments suggest that foraminifera may be facultative anaerobes. (e.g. Bernhard, 1989, 1993; Sen Gupta and MachainCastillo, 1993; Geslin et al., 2004). These studies confirmed that several species of deep-sea benthic foraminifera are able to live under anoxic conditions, and calcified within anoxic horizons. Exactly how long these species may survive in an anoxic environment without dysoxic or oxic layers in a close range is not clear, however. As proposed by previous investigations (Douglas and StainesUrías, 2007), the isotopic differences between B. subadvena morphotypes support a model of different life strategies between generations. The asexual megalospheric generation exhibits an opportunistic

Fig. 9. Stable oxygen and carbon isotope signals of live specimens of megalospheric Bolivina subadvena (close squares), microspheric Bolivina subadvena (open squares), megalospheric Bolivina argentea (close circles), and microspheric Bolivina argentea (open circles) in Pescadero and Alfonso Basins.

F. Staines-Urías, R.G. Douglas / Marine Micropaleontology 71 (2009) 80–95

response to phytodetritus pulses during the upwelling season. These individuals appear to grow rapidly and be short-lived. In contrast, sexual microspheric individuals appear to survive for longer periods, growing deeper in the sediment column where available organic carbon is relatively low. In addition, the faunal analysis revealed that sexual (microspheric) individuals dominate B. argentea population but that in live populations of B. subadvena, megalospheric (asexual) individuals always outnumber the microspheric ones (Fig. 3). The specific variation in the proportions of the dimorphic generations reflects differences in reproduction effects (e.g. number of offspring produced, timing and frequency of reproduction) and is a clear indication of differences in the life cycle of each species. Rapid increments in density of asexual individuals are associated with an opportunistic response to changes in environmental conditions (Jorissen et al., 1995; Gooday and Rathburn, 1999). We observed that in all the multicores the organicrich layer overlaying the sediments contained a high density of very small (b125 µm) live megalospheric specimens of B. subadvena. In these samples megalospheric B. subadvena individuals composed 70 to 85% of the total benthic foraminifera population. The samples, collected in late November, represent the beginning of the eutrophic season, which in the southern Gulf of California — due to its direct exchange with the Pacific Ocean — occurs earlier than in the central and northern regions (Douglas et al., 2007). At this time, rapid pulses of phytodetritus to the sea floor follow the breakdown of the thermocline at the onset of the northwesterly winds (Pike and Kemp, 1999). However, compare to regions along the eastern margin of the Gulf (Pescadero and Carmen Basins; Gonzalez-Yajimovich, 2004; Berelson et al., 2005) or in Guaymas Basin (Central Gulf of California; Thunell, 1998) organic carbon fluxes are much lower in Alfonso Basin (Silverberg et al., 2007). Further confirmation for the seasonality of organic matter fluxes in the area was provided by a 3-year sediment trap study (AguirreBahena, 2007). This study showed that in La Paz Bay (western Gulf), higher sediment fluxes occurred during fall, starting in October and until the end of December, despite the fact that November and December are the months when the water column density gradient is the largest (well established picnocline). Aguirre-Bahena (2007) explained such contradiction by showing that larger sized organic aggregates are most abundant during these months, and because of their size, these aggregates reach the bottom regardless of a strong picnocline. The organic aggregates (rich in plankton debris) serve as a food source and might trigger an asexual reproductive reaction in B. subadvena. Similar B. subadvena abundance patterns had been reported in other locations within the Gulf of California (Douglas and StainesUrías, 2007), indicating a rapid increase in the abundance of megalospheric specimens of this species in response to increase in food availability. The sudden increase in the abundance of megalospheric B. subadvena juveniles implies higher reproductive and growing rates, requiring higher metabolic rates, which probably account for a larger incorporation of metabolic CO2 into the test of these specimens, explaining the more negative δ13C values. This vital effect also explains why megalospheric B. argentea yields consistently lighter δ13C values than the microspheric morphotype of this species. Additional evidence support this argument: it is in Alfonso Basin, the location with lower organic carbon input and smaller TCO2 gradients, where both generations of B. subadvena exhibit their lowest abundances (pointing to lower reproductive rates) and it's also in this location where the δ13C of megalospheric B. subadvena showed the lowest offset respect to the isotopic composition of pore water (pointing to smaller metabolic effects in its isotopic composition). These results imply different responses to carbon rain variability in B. subadvena compare to B. argentea, and between dimorphic generations of each species, explaining the larger vital effect observed in the δ13C signal of megalospheric B. subadvena.

91

Most important, our results indicate that both intrageneric and intraspecific differences can be significant and, consequently, aggregating different species or different morphotypes should be avoided in stable isotope studies. 6.2. Ontogenic influences on stable isotope composition of test carbonate Size-related variations in stable isotope composition have been shown to be important in planktic foraminifera species. In the most common planktic foraminifera small forms tend to be light, both in oxygen and carbon, and mature forms tend to be heavier (Berger et al., 1978). Strong disequilibrium in δ13C occurs in early life stages with high metabolic activity; δ13C values of later stages approach equilibrium (Oppo and Fairbanks, 1989). In laboratory experiments, for example, Globigerina bulloides exhibited an ontogenic increase of 0.8‰ in δ18O and 2.6‰ in δ13C between juvenile and adult specimens, which was attributed to decreasing metabolic rates (Spero and Lea, 1996). In contrast, differences in isotopic composition of different size fractions of microspheric and megalospheric B. subadvena observed in the present study indicated that ontogenic changes in deep-sea benthic foraminifera are less consistent and lower in magnitude. Altogether, the results suggest that in benthic species that exhibit strong dimorphism, such as B. argentea and B. subadvena, the isotopic fractionation related to ontogeny is small compared to the difference in δ18O and δ13C between dimorphic generations, indicating that isotope composition may be more strongly affected by generational differences in life strategy than by ontogenesis. Suggesting that for benthic species, morphotypic differences — rather than life stage — must be consider when evaluating its potential as a paleoceanographic proxy. 6.3. Pore water influence Live individuals of B. subadvena and B. argentea were found over a range of sediment depths. The abundance data suggests that specific morphotypes may migrate over small depth ranges during their life cycle. However, the δ13C values of each morphotype were relatively constant with depth. It has been suggested that the lack of vertical δ13C variation within a given species can be explain by either (1) calcification in a relative small depth range compared to the depth range suggested by their live distribution, (2) calcification in association with animal burrows creating microenvironments with similar biological and geochemical characteristics at different sediment depths or (3) moving and calcification within the whole microhabitat range resulting in averaging of downcore gradients. The low abundance to complete absence of macrofauna in anoxic basins, such as Alfonso and Pescadero, excludes the possibility of microenvironments associated with burrows. Experimental results indicate that deep-sea benthic foraminifera migrate in response to environmental changes (e.g. food supply, oxygen concentration) (Geslin et al., 2004). It appears that benthic foraminifera are able to actively migrate to their favorite microhabitat to maintain their relative position in the sediment column (Moodley et al., 1998; Ernst et al., 2005). This ability permits benthic forams to calcify in a relatively small sub-zone compared to the total habitat range they can occupy (Chandler et al., 1996; Schmiedl et al., 2004). In our study, maximum specific abundances occur in consistent narrow depth ranges, indicating a narrower range of preferred depths at which most calcification should occur. This explains the vertical homogeneity in δ13C values and also the agreement between isotopic values of live and dead specimens, found at the same depth interval, which is a prerequisite for the use of fossil specimens in paleoclimate reconstructions (Figs. 5 and 6). Pore water δ13C values were not measured in any of the stations in this study. Therefore, it is not possible to compare those values with the values predicted by Eq. (1). However, previous investigations, conducted on laminated sediments from suboxic to anoxic basins

92

F. Staines-Urías, R.G. Douglas / Marine Micropaleontology 71 (2009) 80–95

along the California margin (Santa Barbara, Santa Monica, and Soledad basins) and Mexico northwestern continental slope (Mazatlan and San Blas Basins) corroborate that the primary influence on pore water δ13C values in these basins is the oxidation of photosynthate carbon and the flux of TCO2 through the sediments (Stott et al., 2000; Berelson and Stott, 2003; Holsten et al., 2004). These investigations showed a good agreement between measured pore water δ13CDIC values and those estimated from the reaction diffusion model. Therefore, we expect similar influences on the δ13C signal of pore water in Alfonso and Pescadero Basins allowing us to use the pore water δ13CDIC values calculated with Eq. (1). The depth of primary calcification for each morphotype was estimated by matching the foraminiferal δ13C value to that of pore water δ13CDIC. Based on this, megalospheric B. argentea consistently calcifies within the upper millimeter of sediment, in good agreement with its preference for a shallow habitat. The abundance pattern of microspheric B. argentea indicates a primary depth habitat at an intermediate depth between 1 and 3 mm. This is comparable to 0.5 mm depth that is predicted from its δ13C value. The greatest numbers of microspheric B. subadvena are observed between 4 and 6 mm, except in Alfonso basin where maximum abundance is recorded between 6 and 7 mm. The average depth of calcification for this morphotype based on its δ13C value is 3.2 mm. The benthic foraminifera δ13C values from the investigated sites do match the pore water values calculated from Eq. (1). Small discrepancies between foraminiferal and the modeled pore water δ13C in Alfonso and Pescadero are within 0.1‰ to 0.3‰, which reflect the degree of uncertainty in the model and in the calculation of the depth horizon for each pore water sample. The only exception is megalospheric B. subadvena that presents large discrepancies (up to 1‰) between the estimated calcification depth and the observed average living depth. This morphotype occurs between 0 and 1 mm depth, but its predicted calcification depth, base on its δ13C value, is 3.5 mm. As explained before (see 6.1), we believe that the unusually light δ13C values of this morphotype, compared to the estimated pore water δ13C value in the upper millimeter, are due to high incorporation of metabolic CO2 into its test carbonate, a product of the high metabolic rates that characterized its opportunistic behavior. Similar effects in the isotopic composition of opportunistic, low-oxygentolerant benthic foraminifera species were reported by Filipsson et al. (2004) after monitoring the seasonal variability in the abundance and isotopic composition of live foraminifera in the Baltic Sea. In this study, following the seasonal phytodetritus input, a rapid increase in abundance occurred whereas δ13C values of foraminiferal carbonate decreased. The close correspondence between the isotopic value of benthic foraminifera and the pore water at the depth of the species maximum live abundance implies that the δ13C of fossil megalospheric and microspheric B. argentea, and microspheric B. subadvena can provide a good estimate of the pore water δ13C gradient within dysoxic basins. However, because of the large influence of vital effects on the δ13C signal of megalospheric B. subadvena specimens, we don't recommend the use of this morphotype in this type of reconstruction. 6.4. Influence of carbon oxidation rates on the δ13C of benthic foraminifera The δ13CDIC value of pore water is controlled by a combination of the bottom water δ13CDIC value and the amount of 12C-enriched carbon added to the pore water by the decomposition of organic matter in the surface sediment (McCorkle et al., 1990; Berelson and Stott, 2003; Holsten et al., 2004). Thus, a decrease in the organic matter flux to the sea bed should cause a decrease in the intensity of organic matter degradation on and within the sediment, and consequently should produce a decrease in the TCO2 fluxes, that are presumably dominated by the oxidation of organic carbon. This should result in larger pore water δ13CDIC gradients below the water–

sediment interface in eutrophic environments and much less marked δ13CDIC gradients in more oligotrophic settings. In the Alfonso Basin calculated organic carbon mass accumulation rates are lower (0.55 mg cm− 2 year− 1) than in the Pescadero Basin (0.68 mg cm− 2 year− 1), in correspondence with the pore water TCO2 profiles and the lower carbon oxidation rates predicted from the pore water δ13CDIC profiles (Fig. 2) and in good agreement with measured differences in the δ15N composition of pore water ammonium (Prokopenko et al., 2006). After comparing the pore water δ13C TCO2 profiles from the three investigated sites, we noticed that the pore water δ13CDIC profile in the Alfonso Basin presented a lower gradient than both stations in the Pescadero Basin. The calculated pore water δ13C TOC2 gradients between basins (stations: 15 = −1.964‰ cm− 1; 26 = − 2.932‰ cm− 1; 27 = −3.582‰ cm− 1) showed that at − 1 cm depth the carbon isotopic composition of the pore water TCO2 in Alfonso Basin is, in average, 1.134‰ less negative than in Pescadero Basin, We interpreted this difference as the result of lower organic carbon rain in Alfonso than in Pescadero, consequence of the upwelling asymmetry existing across the Gulf. It was also noticed that the pore water δ13CDIC profile of station 26 presents a steeper slope than the profile of station 27. This distinction between stations was interpreted to be a consequence of the difference in depth between them, resulting in lower organic carbon oxidation in station 26 than in station 27. A difference in depth is particularly important at the beginning of the eutrophic season, when phytodetritus pulses begin traveling through the water column from the surface to the seabed. Then, small differences in depth might produce important variations in the time that such pulses reach the bottom, varying the system's reaction time and the interval in which the benthic community responds to the increase in food availability (Rice et al., 1994).Differences in organic carbon input also explain why the Alfonso Basin exhibits the lower total foraminifera abundance and why the highest abundances — almost twice more foraminifera per gram of sediment — were observed in station 27. Although, oxygen differences can be invoked to explain change in abundance, experimental results indicate that anoxia leads to a decrease in foraminiferal numbers, contrary to what we observed in Alfonso and Pescadero (Alve and Bernhard, 1995; Ernst et al., 2005). Furthermore, individuals of the Bolivina genus show not significant change in abundance related to changes in oxygen concentration but a positive response (increase in numbers) and an active migration towards the water– surface interface in response to high doses of organic matter (Ernst et al., 2005), In laminated sediments, where the flux of CO2 is controlled by diffusion, higher rates of carbon oxidation enhance the δ13C gradient below the water–sediment interface, increasing the δ13C gradient between the epifaunal and infaunal foraminifera species that incorporate the pore water isotopic composition into their calcite. Such foraminifer species can be used to reconstruct a history of carbon oxidation changes within a basin. This approach has been applied to reconstruct organic carbon oxidation rates in Santa Monica Basin using B. argentea (epifaunal) and Buliminella tenuata (infaunal) (Berelson and Stott, 2003). The analysis of live specimens of B. argentea, B. subadvena, and B. tenuata in dysoxic and anoxic basins along the California Borderland Province (Holsten et al., 2004) proved that this methodology can be extended to other basins with different sedimentary characteristics and different TCO2 gradients. Furthermore, the recognition of specific dimorphic differences will help improve these reconstructions. As an example, Holsten et al., 2004 observed that living specimens of B. argentea from the east Mexican margin at the entrance of the Gulf of California yielded δ13C values that were considerable lighter than those of pore water. These authors also mention that samples of this species collected from this location in other times didn't show such difference. This discrepancy can be easily explained if we considered that the conflicting samples were collected during the regional

F. Staines-Urías, R.G. Douglas / Marine Micropaleontology 71 (2009) 80–95

eutrophic season and that, giving the ecological behavior of this species, at the moment of collection B. argentea populations must be dominated by megalospheric individuals that, as mention before, tend to incorporate more metabolic CO2 and consequently to have a lighter δ13C composition. In general, our results support the applicability of the difference between megalospheric B. argentea and microspheric B. subadvena as a proxy for changes in carbon oxidation in the Gulf of California. However, further studies are necessary to validate statistically the applicability of this methodology. 7. Conclusions This study, using live (Rose Bengal stained) epi- and infaunal benthic foraminifera from two basins in the southern Gulf of California, shows that the isotopic composition of the selected species is influenced by a variety of vital effects, interstitial (pore) water geochemistry, and organic matter fluxes. Significant differences in microhabitat preferences and stable oxygen and carbon isotope composition were detected between species and between dimorphic generations of each species. Faunal (specific variation in the proportions of dimorphic generations) and isotopic (consistently lighter stable oxygen and carbon values) analyses indicate different responses to carbon rain variability in B. subadvena compared to B. argentea. In B. subadvena, populations are being maintained largely through asexual reproduction. The asexual (megalospheric) generation exhibits an opportunist behavior, reacting suddenly to increments in organic carbon availability. Their reactivity requires high metabolic rates, which account for a larger incorporation of metabolic CO2 into their test and explains the lighter δ13C and δ18O values consistently observed in this individuals. In contrast, B. argentea populations are dominated by sexual (microspheric) specimens. Dimorphic generations of this species exhibit similar abundances. In this species, megalospheric specimens appear to be a more conservative recorder of the benthic chemistry than in B. subadvena. In both species microspheric individuals show δ13C values consistent with those of pore water TCO2. The comparison of measurements from three size classes (125, 150 and 250 µm) in dimorphic generations of B. subadvena showed that isotopic fractionation related to ontogeny is small, compared to the difference in δ18O and δ13C between dimorphic generations, suggesting that in benthic species that exhibit strong dimorphism the isotope composition may be more strongly affected by generational differences than by ontogenesis. The depth distribution patterns and δ13C of megalospheric B. argentea, microspheric B. argentea, and microspheric B. subadvena, reflect the specific sedimentary microenvironments in which they live. The distinct but uniform δ13C values recorded by each of these three morphotypes suggest a narrow range of depths for test calcification with little variation between sites. The foraminiferal δ13C values are similar to the δ13C of pore water TCO2 at the corresponding depth horizon of specific maximum abundance. The δ13C signal of epifaunal megalospheric B. argentea reflects pore water isotopic composition at the top most sediment. Microspheric B. argentea is representative of pore water at an average depth of 0.5 mm sediment depth, in good agreement with is observed living maximum abundance. The δ13C values of microspheric B. subadvena are similar to the δ13C of pore water TCO2 at an average depth of 3.2 mm, which coincides with the depth were most living specimens live. Due to the larger influence of vital effects on the δ13C signal of megalospheric B. subadvena we don't recommend the use of this particular morthotype in paleoceanographic reconstructions. Both species offer considerable potential as environmental proxies but, because dimorphic generations are responding somewhat differently to environmental changes, their use needs to consider their reproductive life strategies in interpreting the isotopic geochem-

93

istry of their shells. These differences, when understood, expand their usefulness as recorders of benthic chemistry. Acknowledgments This study was supported by the National Science Foundation International Program (United States–Mexico) grant INT-0304933 to Dr. Robert G. Douglas and by the University of Southern California, Department of Earth Science Research Funding. Fellowship support to the first author was generously provided by Consejo Nacional de Ciencia y Tecnologia (CONACyT). We gratefully acknowledge the captain and crew of the R/V New Horizon during the 2001-CALMEX Cruise to the Gulf of California for their assistance in collecting the sediment cores. I. Schimmelpfennig kindly help with all German to English translations. We are also thankful to W. Berelson, for his suggestions and comments on an earlier draft of the manuscript. Thanks to M. Castillo-Machain and an anonymous reviewer for their helpful and constructive comments. References Aguirre-Bahena, F., 2007. Cambios temporales en los componentes y los flujos de la materia en hundimiento en Cuenca Bahía de La Paz, durante el periodo 2002–2005 (Time-changes in the components and fluxes of sinking matter in La Paz Bay Basin, during 2002–2005), Doctoral Dissertation, CICIMAR-IPN, Mexico. Altabet, M.A., Pilskaln, C., Thunell, C., Pride, C., Sigman, D., Chavez, F., Francois, R., 1999. The nitrogen isotope biogeochemistry of sinking particles from the margin of the Eastern Tropical Pacific. Deep-Sea Research I 46, 655–679. Alve, E., Bernhard, J., 1995. Vertical migratory response of benthic foraminifera to controlled oxygen concentrations in an experimental mesocosm. Marine Ecology Progress Series 116, 137–151. Arnold, M., 1955. Life history and cytology of the foraminiferan Allogromia laticollaris. Zoology 61, 167–252. Baba, J., Peterson, C.D., Schrader, H.J., 1991. Modern fine-grained sediments in the Gulf of California. In: Dauphin, J.P., Simoneit, B.R.T. (Eds.), The Gulf and Peninsular Province of the Californias. AAPG Memoir, vol. 47, pp. 569–587. Barron, J.A., Bukry, D., Dean, W.E., 2005. Paleoceanographic history of the Guaymas Basin, Gulf of California, during the past 15,000 years based on diatoms, silicoflagellates, and biogenic sediments. Marine Micropaleontology 56, 81–102. Bender, M., Martin, W., Hess, J., Sayles, F., Ball, L., Lambert, C., 1987. A whole-core squeezer for interstitial pore-water sampling. Limnology and Oceanography 32, 1214–1225. Bentov, S., Erez, J., 2005. Impact of biomineralization processes on the Mg content of foraminiferal shells: a biological perspective. Geology 33, 841–844. doi:10.1130/ G21800.1. Berelson, W.M., Stott, L.D., 2003. Productivity and organic carbon rain to the California margin seafloor: modern and paleoceanographic perspectives. Paleoceanography 18, 2–1 2–15. Berelson, W.M., Hammond, D.E., Giordani, P., 1989. Effect of sea floor disturbance on benthic flux measurements in the continental margin off Southern California. Catalina Basin, Giornale di Geologia 51, 143–150. Berelson, W.M., Prokopenko, M., Graham, A., Sansone, F.J., McManus, J., Bernhard, J.M., 2005. Variable scales of anaerobic diagenesis in continental margin sediments: enhanced organic carbon remineralization at the sulfate–methane interface. Geochimica et Cosmochimica Acta 54, 4611–4629. Berger, W.H., Killingley, J.S., Vincent, E., 1978. Stable isotopes in deep-sea carbonates, Box Core ERDC-92, West Equatorial Pacific. Oceanologica Acta 1, 203–216. Bernal, G., Ripa, P., Herguera, J.C., 2001. Oceanographic and climatic variability in the Lower Gulf of California: links with the tropics and North Pacific. Ciencias Marinas 27, 595–617. Bernhard, J.M., 1988. Postmortem vital staining in benthic foraminifera: duration and importance in population and distributional studies. Journal of Foraminiferal Research 18, 143–146. Bernhard, J.M., 1989. The distribution of benthic foraminifera with respect to oxygen concentration and organic carbon levels in shallow-water Antarctic sediments. Limnology and Oceanography 34, 1131–1141. Bernhard, J.M., 1993. Experimental and field evidence of Antarctic foraminiferal tolerance to anoxia and hydrogen sulfide. Marine Micropaleontology 20, 203–213. Bernhard, J.M., 2003. Potential symbionts in bathyal foraminifera. Science 299, 861–865. Boltovskoy, E., Wright, R., 1976. Recent foraminifera, in Dr. W. Junk B. V (Ed.), The Hague, 515 pp, Netherlands. Bordoni, S., Stevens, B., Ciesielski, P.E., Johnson, R.H., McNoldy, B.D., 2004. The low-level circulation of the North American Monsoon as revealed by QuikSCAT. Geophysical Research Letters 31 (L10109 1-4). Boyle, E.A., 1995. Limits on benthic foraminiferal chemical analyses as precise measures of environmental properties. Journal of Foraminiferal Research 25, 4–13. Calvert, S.E., 1966. Accumulation of diatomaceous silica in the sediments of the Gulf of California. Geological Society of America Bulletin 77, 569–596.

94

F. Staines-Urías, R.G. Douglas / Marine Micropaleontology 71 (2009) 80–95

Castro, R., Mascarenhas, A.S., Durazo, R., Collins, C., 2000. Seasonal variation of temperature and salinity at the entrance to the Gulf of California. Ciencias Marinas 26, 561–583. Chandler, G.T., Williams, D.F., Spero, H.J., Xiaodong, G., 1996. Sediment microhabitats and stable isotope disequilibria phenomenon in microcosm cultured benthic foraminiferal calcite. Limnology and Oceanography 41, 680–688. Corliss, B.H., Emerson, S., 1990. Distribution of Rose Bengal stained deep-sea benthic foraminifera from the Nova Scotian continental margin and Gulf of Maine. Deep Sea Research 37, 381–400. Corliss, B.H., McCorkle, D.C., Higdon, D.M., 2002. Seasonal changes of the carbon isotopic composition of deep-sea benthic foraminifera. Paleoceanography 17 10.1029/ 2001PA000664. Curry, W.B., Oppo, D.W., 2005. Glacial water mass geometry and the distribution of δ13C of CO2 in the Western Atlantic Ocean. Paleoceanography 20, PA1017. doi:10.1029/ 2004PA001021. Douglas, R.G., Staines-Urías, F., 2007. Dimorphism, shell Mg/Ca ratios and stable isotope content in species of Bolivina (benthic foraminifera) in the Gulf of California, Mexico. Journal of Foraminiferal Research 37. Douglas, R.G., Gorsline, D., Grippo, A., Granados, I., Gonzalez-Yajimovich, O., 2002. Holocene ocean–climate variations in Alfonso Basin, Gulf of California, Mexico. In: West, G.J., Bualoe, L.D. (Eds.), Proceedings of the Eighteenth PACLIM Workshop Technical Report 68, pp. 7–20. California, USA. Douglas, R.G., Gonzalez-Yajimovich, O., Ledesma-Vazquez, J., Staines-Urías, F., 2007. Climate forcing, primary production and Holocene biogenic sediments in the Gulf of California. Quaternary Science Research 26, 115–129. Dunbar, R.B., Wefer, G., 1984. Stable isotope fractionation in benthic foraminifera from the Peruvian continental margin. Marine Geology 59, 215–225. Ernst, S., Bours, R., Duijnstee, I., van der Zwaan, B., 2005. Experimental effects of an organic matter pulse and oxygen depletion on a benthic foraminiferal shelf community. Journal of Foraminiferal Research 35, 177–197. Fernández-Barajas, M.E., Monreal-Gómez, M.A., Molina-Cruz, A., 1994. Estructura termohalina y flujo geostrófico en el Golfo de California durante 1992. Ciencias Marinas 20, 267–286. Filipsson, H.L., Nordberg, K., Gustafsson, M., 2004. Seasonal study of δ18O and δ13C in living (stained) benthic foraminifera from two Swedish fjords. Marine Micropaleontology 53, 159–172. Fontanier, C., Jorissen, F.J., David, C., Anschutz, P., Carbonel, P., Chaillou, G., Lafon, V., 2003. Seasonal and inter-annual variability of benthic foraminiferal faunas at 550 m depth in the Bay of Biscay. Deep-Sea Research I 50, 457–494. Fontanier, C., Anschutz, P., Grémare, A., Griveaud, C., Jorissen, F.J., Chaillou, G., 2005. Live foraminiferal faunas from a 2800 m deep lower canyon station from the Bay of Biscay: faunal response to focusing of refractory organic matter. Deep-Sea Research Part I: Oceanographic Research Papers 52, 1189–1227. Fontanier, C., Mackensen, A., Jorissen, F.J., Anschutz, P., Licari, L., Griveaud, C., 2006. Stable oxygen and carbon isotopes of live benthic foraminifera from the Bay of Biscay: microhabitat impact and seasonal variability. Marine Micropaleontology 58, 159–183. Geslin, E., Heinz, P., Hemleben, Ch., Jorissen, F.J., 2004. Migratory response of deep-sea benthic foraminifera to variable oxygen conditions: laboratory investigations. Marine Micropaleontology 53, 227–243. Goldstein, S.T., 1997. Gametogenesis and the antiquity of reproductive pattern in the Foraminiferida. Journal of Foraminiferal Research 27, 319–328. Goldstein, S.T., 1999. Foraminifera: a biological review. In: Sen Gupta, B.K. (Ed.), Modern Foraminifera. Kluwer Academic Publishers, Dordrecht, pp. 37–55. Goldstein, S.T., 2002. Foraminiferal reproductive strategies and dimorphism: a test of ecological adaptations and taxonomic constraints, GSA Annual Meeting Abstracts. González-Yajimovich, O. 2004 Holocene Sedimentation in the Southern Gulf of California and climatic implications. Doctoral Dissertation, University of Southern California, USA, 211pp. González-Yajimovich, O., Douglas, R.G., Gorsline, D.S., 2005. The preserved carbonate record in Holocene sediments of the Alfonso and Pescadero basins, Gulf of California, Mexico,. Proceedings of the Geologists' Association 116, 315–330. Gooday, A.J., 1988. A response by benthic foraminifera to the deposition of phytodetritus in the deep sea. Nature 332, 70–85. Gooday, A.J., 1994. The biology of deep-sea foraminifera, a review of some advances and their applications in paleoceanography. Palaios 9, 14–31. Gooday, A.J., 1996. Epifaunal and shallow infaunal foraminiferal communities at three abyssal NE Atlantic sites subject to differing phytodetritus input regimes. Deep-Sea Research 43, 1395–1421. Gooday, A.J., Hughes, J.A., 2002. Foraminifera associated with phytodetritus deposits at a bathyal site in the northern Rockall Trough (NE Atlantic): seasonal contrasts and a comparison of stained and dead assemblages. Marine Micropaleontology 46, 83–110. Gooday, A.J., Rathburn, A.E., 1999. Temporal variability in living deep-sea benthic foraminifera: a review. Earth-Science Reviews 46, 187–212. Gooday, A.J., Bernhard, J.M., Levin, L.A., Suhr, S.B., 2000. Foraminifera in the Arabian Sea oxygen minimum zone and other oxygen-deficient settings: taxonomic composition, diversity, and relation to metazoan faunas. Deep-Sea Research II 47, 25–54. Grell, K.G., 1954. Der Generationswechsel der polythalamen Foraminifere Rotaliella heterokaryotica, (Generational changes in the heterokaryotic foraminifera Rotaliella). Archiv fuÉr Protistenkunde 100, 268–286. Grell, K.G., 1957. Untersuchungen über die Fortpflanzung und Sexualität der Foraminiferen. I. Rotaliella roscoffensis (Reproduction and sexuality study of the foraminifera Rotaliella roscoffensis). Archiv fuÉr Protistenkunde 102, 147–164. Grossman, E.L., 1987. Stable isotopes in modern benthic foraminifera, a study of vital effect. Journal of Foraminiferal Research 17, 48–61.

Hartnett, H.E., Devol, A.H., 2003. Role of a strong oxygen-deficient zone in the preservation and degradation of organic matter: a carbon budget for the continental margins of northwest Mexico and Washington State. Geochimica e Cosmochimica Acta 67, 247–264. Heinz, P., Schmiedl, G., Kitazato, H., Hemleben, Ch., 2001. Response of deep-sea benthic foraminifera from the Mediterranean Sea to simulated phytoplankton pulses under laboratory conditions. Journal of Foraminiferal Research 31, 210–227. Holsten, J., Stott, L., Berelson, W., 2004. Reconstructing benthic carbon oxidation rates using δ13C of benthic foraminifers. Marine Micropaleontology 53, 117–132. Jiménez, A., Marinone, S.G., Parés-Sierra, A., 2005. Effect of the spatial and temporal variability of winds on the circulation in the Gulf of California. Ciencias Marinas 31, 357–368. Jorissen, F.J., Barmawidjaja, D.M., Puskaric, S., Van Der Zwaan, G.J., 1992. Vertical distribution of benthic foraminifera in the northern Adriatic Sea: the relation with the organic flux. Marine Micropaleontology 19, 131–146. Jorissen, F.J., De Stigter, H.C., Widmark, J.G.V., 1995. A conceptual model explaining benthic foraminiferal microhabitats. Marine Micropaleontology 26, 3–15. Linke, P., 1992. Metabolic adaptations of deep-sea benthic foraminifera to seasonally varying food input. Marine Ecology Progresses Series 81, 51–63. Lutze, G.F., 1964. Statistical investigations on the variability of Bolivina argentea Cushman. Contributions to the Cushman Foundation foraminifera Research 15, 105–116. Mackensen, A., Schmidt, D.N., Schumacher, S., Radke, J., 2000. Microhabitat preferences and stable carbon isotopes of endobenthic foraminifera: clue to quantitative reconstruction of oceanic new production? Micropaleontology 40, 233–258. McConnaughey, T., 2003. Sub-equilibrium oxygen-18 and carbon-13. levels in biological carbonates: carbonate and kinetic models. Coral Reefs 22, 316–327. McConnaughey, T.A., Burdett, J., Whelan, J.F., Paull, C.K., 1997. Carbon isotopes in biological carbonates: respiration and photosynthesis. Geochimica and Cosmochimica Acta 61, 611–622. McCorkle, D.C., Keigwin, L.D., Corliss, B.H., Emerson, S.R., 1990. The influence of microhabitats on the carbon isotopic composition of deep sea benthic foraminifera. Paleoceanography 5, 161–185. Moodley, L., Schaub, B.E.M., vanderZwaan, G.J., Herman, P.M.J., 1998. Tolerance of benthic foraminifera (Protista: Sarcodina) to hydrogen sulphide. Marine ecology progress series 169, 77–86. Murray, J.W., Bowser, S.S., 2000. Mortality, protoplasm decay rate, and reliability of staining techniques to recognize ‘living’ foraminifera: a review. Journal of Foraminiferal Research 30, 66–70. Nava-Sánchez, E.H., Gorsline, D.S., Molina-Cruz, A., 2001. The Baja California peninsula borderland: structural and sedimentological characteristics. Sedimentary Geology 144, 63–82. Nigam, R., 1986. Dimorphic forms of Recent foraminifera: an additional tool in paleoclimatic studies. Palaeogeography, Palaeoclimatology, and Palaeoecology 53, 239–244. Nigam, R., 2005. Addressing environmental issues through foraminifera — case study from the Arabian Sea. Journal of the Paleontological Society of India 50, 25–36. Nigam, R., Caron, D.A., 2000. Does temperature affect dimorphic reproduction in benthic foraminifera? A culture experiment on Rosalina leei. Current Science 79, 105–106. Nigam, R., Khare, N., 1995. Significance of correspondence between river discharge and proloculus size of benthic foraminifera in paleomonsoonal reconstructions. GeoMarine Letters 15, 45–50. Nigam, R., Sarkar, A., 1993. Mean proloculus size, δ13C and δ18O variations in recent benthic foraminifera from the West Coast of India and their climatic implications. Indian Journal Of Earth Sciences 20, 1–6. Ohga, T., Kitazato, H., 1997. Seasonal changes in bathyal foraminiferal populations in response to the flux of organic matter (Sagami Bay, Japan). Terra Nova 9, 33–37. Oppo, D.W., Fairbanks, R.G., 1989. Carbon isotope composition of tropical surface water during the past 22000 years. Paleoceanography 4, 333–351. Pares-Sierra, A., Mascarenhas, A., Marinone, S.G., Castro, R., 2003. Temporal and spatial variation of the surface winds in the Gulf of California. Geophysical Research Letters 30, 6. Pegau, W.S., Boss, E., Martínez, A., 2002. Ocean color observations of eddies during the summer in the Gulf of California. Geophysical Research Letters 29, 9.1–9.3. Pike, J., Kemp, A.E.S., 1999. Diatom mats in Gulf of California sediments: implications for the paleoenvironmental interpretation of laminated sediments and silica burial. Geology 27, 311–314. Pride, C., Thunell, R., Sigman, D., Keigwin, L., Altabet, M., Tappa, E., 1999. Nitrogen isotopic variations in the Gulf of California since the last deglaciation: response to global climate change. Paleoceanography 14, 397–409. Prokopenko, M., Hammond, D.E., Berelson, W.M., Bernhard, J.M., Stott, L., Douglas, R., 2006. Nitrogen cycling in the sediments of Santa Barbara basin and Eastern Subtropical North Pacific: nitrogen isotopes, diagenesis and possible chemosymbiosis between two lithotrophs (Thioploca and Anammox)—riding on a glider. Earth and Planetary Science Letters 242, 186–204. Rathburn, A.E., Corliss, B.H., Tappa, K.D., Lohmann, K.C., 1996. Comparisons of the ecology and stable isotopic compositions of living (stained) deep-sea benthic foraminifera from the Sulu and South China Seas. Deep Sea Research I 43, 1617–1646. Rathburn, A.E., Pichon, J.J., Ayress, M.A., De Deckker, P., 1997. Microfossil and stableisotope evidence for changes in Late Holocene palaeoproductivity and palaeoceanographic conditions in the Prydz Bay region of Antarctica. Palaeogeography, Palaeoclimatology, Palaeoecology 131, 485–510. Rathburn, A.E., Perez, M.E., Lange, C., 2001. Benthic–pelagic coupling in the Southern California Bight: relationships between sinking organic material: diatoms and benthic foraminifera. Marine Micropaleontology 43, 261–271.

F. Staines-Urías, R.G. Douglas / Marine Micropaleontology 71 (2009) 80–95 Rice, A.L., Thurston, M.H., Bett, B.J., 1994. The IOSDL DEEP SEAS program: introduction and photographic evidence for the presence and absence of a seasonal input of phytodetritus at contrasting abyssal sites in the northeastern Atlantic. Deep-Sea Research 41, 1305–1320. Rohling, E.J., Cooke, S., 1999. Stable oxygen and carbon isotope ratios in foraminiferal carbonate, chapter 14. In: Sen Gupta, B.K. (Ed.), Modern Foraminifera. Kluwer Academic, Dordrecht, The Netherlands, pp. 239–258. Rosenthal, Y., Perron-Cashman, S., Lear, C.H., Bard, E., Barker, S., Billups, K., Bryan, M., Delaney, M.L., deMenocal, P.B., Dwyer, G.S., Elderfield, H., German, C.R., Greaves, M., Lea, D.W., Marchitto, T.M., Pak, D.K., Paradis, G.L., Russell, A.D., Schneider, R.R., Scheiderich, K., Stott, L., Tachikawa, K., Tappa, E., Thunell, R., Wara, M., Weldeab, S., Wilson, P.A., 2004. Interlaboratory comparison study of Mg/Ca and Sr/Ca measurements in planktonic foraminifera for paleoceanographic research. Geochemistry, Geophysics, Geosystems 4 2003GC000650. Santamaría-del-Ángel, E., Álvarez-Borrego, S., Müller-Karger, F.E., 1994. Gulf of California biogeographic regions based on coastal zone color scanner imagery. Journal of Geophysical Research 99, 7411–7421. Schmiedl, G., Mackensen, A., Pfeilsticker, M., Hemleben, C., 2004. Environmental and biological effects on the stable isotope composition of recent deep-sea benthic foraminifera from the western Mediterranean Sea. Marine Micropaleontology 51, 129–152. Schmiedl, G., Mackensen, A., 1997. Late Quaternary paleoproductivity and deep water circulation in the eastern South Atlantic Ocean: evidence from benthic foraminifera. Palaeogeography, Palaeoclimatology, Palaeoecology 130, 43–80. Sen Gupta, B.K., Machain-Castillo, M.L., 1993. Benthic foraminifera in oxygen-poor habitats. Marine Micropaleontology 20, 183–201. Silverberg, N., Aguirre Bahena, F., Cortés-Martínez, M., Urcádiz-Cázare, F., 2007. Flujos verticales de carbono orgánico e inorgánico particulado en Cuenca Alfonso, Bahía de La Paz, y comparación con otros ambientes en el norte de México. In: Hernández de la Torre, B., Gaxiola Castro, G. (Eds.), Carbono en Ecosistemas Acuaticos de Mexico. INE, Mexico, pp. 414–425. Sliter, W.V., 1970. Bolivina doniezi Cushman and Wickenden in clone culture. Contributions from the Cushman Foundation for Foraminiferal Research 21, 87–99.

95

Smith, P.B., 1963. Quantitative and qualitative analysis of the family Bolivinidae. U. S. Geological Survey Professional Paper 429-A, 1–39. Sperling, M., Weldeab, S., Schmiedl, G., 2002. Drying of samples may alter foraminiferal isotopic ratios and faunistic composition. Micropaleontology 48, 87–91. Spero, H.J., Lea, D.W., 1996. Experimental determination of intraspecific stable isotope variability in Globigerina bulloides: implications for paleoceanographic reconstructions. Marine Micropaleontology 28, 231–246. Stott, L.D., Berelson, W., Douglas, R., Gorsline, D., 2000. Increased dissolved oxygen in Pacific intermediate waters due to lower rates of carbon oxidation in sediments. Nature 407, 367–370. Thunell, R., 1998. Seasonal and annual variability in particle fluxes in the Gulf of California: a response to climate forcing. Deep-Sea Research 45, 2131–2155. Thunell, R., Pride, C., Ziveri, P., Muller-Karger, F., Sancetta, C., Murray, D., 1996. Plankton response to physical forcing in the Gulf of California. Journal of Plankton Research 18, 2017–2026. Toyofuku, T., de Nooijer, J.L., Nomaki, H., Oguri, K., Kitazato, H., 2008. Calcification pathways in shallow benthic foraminifera: miliolids vs hyaline species. proceedings of The Micropaleontological Society (Foraminifera and Nannofossil Groups), Spring Meeting, Germany. Van Andel, T.H., 1964. Recent marine sediments of the Gulf of California. In: van Andel, T.H., Shor, G.G. (Eds.), Marine Geology of the Gulf of California. AAPG Memories, pp. 216–310. Vincent, E., Killingley, J.S., Berger, W.H., 1981. Stable isotope composition of benthic foraminifera from the equatorial Pacific. Nature 289, 639–643. Wade, B.S., Pälike, H., 2004. Oligocene climate dynamics. Paleoceanography 19, 1–16. Waelbroeck, C., Duplessy, J.C., McManus, J.F., Lambeck, K., Balbon, E., Labracherie, M., 2002. Sea-level and deep water temperature changes derived from benthic foraminifera isotopic records. Quaternary Science Reviews 21, 295–305. Wefer, G., Berger, W.H., 1980. Stable isotopes in benthic foraminifera: seasonal variation in large tropical species. Science 209, 803–805. Wefer, G., Berger, W.H., 1991. Isotope paleontology: growth and composition of extant calcareous species. Marine Geology 100, 207–248.