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Organic-walled dinoflagellate cysts and benthic foraminifera in coastalsediments of the last century from the Gulf of Tehuantepec, South PacificCoast of Mexico
L.F. Vásquez-Bedoya a, T. Radi b, A.C. Ruiz-Fernández c,⁎, A. de Vernal b, M.L. Machain-Castillo d,J.F. Kielt b, C. Hillaire-Marcel b
a Universidad Nacional Autónoma de México, Posgrado en Ciencias del Mar y Limnología. Calz. Joel Montes Camarena s/n, 82040, Mazatlán, Sin., Mexicob Centre de Recherche en Géochimie et Géodynamique (GEOTOP), Université du Québec à Montréal, Case postale 8888, Succursale Centre-ville Montréal, Qc,Canada H3C 3P8c Universidad Nacional Autónoma de México, Instituto de Ciencias del Mar y Limnología, Calz. Joel Montes Camarena s/n, 82040 Mazatlán, Sin., Méxicod Universidad Nacional Autónoma de México, Instituto de Ciencias del Mar y Limnología, Circuito Ciudad Universitaria s/n, 04510 México D. F., México
Article history:Received 1 September 2007Received in revised form 10 March 2008Accepted 12 March 2008
Qualitative and quantitative analysis of recent organic-walled dinoflagellate cysts (dinocysts) wasperformed on surface sediment samples and a core from the continental shelf of the Gulf ofTehuantepec, Mexico, in order to document the spatial distribution of dinocyst assemblages inrelation to upwelling and primary productivity, and to assess the environmental history of the lastcentury. The analyses of surface sediment samples show a close relation between dinocystassemblages and productivity on a regional scale. Polysphaeridium zoharyi and heterotrophic taxa(notablyBrigantedinium spp.) dominate in the high productivity zone,whereas Spiniferites delicatusand other phototrophic taxa are more abundant in the lower productivity zone. Sediment in aneighteen cm long gravity core (dated using 210Pb and 137Cs) provided a record of the last century atannual to decadal resolution, thus yielding a unique opportunity to examine variations in dinocystassemblages associated with environmental changes. Cyst concentrations in the core rangebetween 477 and 2300 cysts g−1, giving cyst fluxes between 68 and 494 cysts cm−2 yr−1. Twenty-three phototrophic and heterotrophic cyst taxawere identified. Brigantedinium spp., P. zoharyi andBitectatodinium spongium are dominant, and are associated with the seasonal upwelling thatcharacterizes the area. Cysts of potentially toxic species such as P. zoharyi (the cyst of Pyrodiniumbahamense var. compressum and/orbahamense) occur throughout the core.Despite slight variationsin relative abundances of the taxa in the assemblages, there is no evidence for eutrophicationfollowing industrial development of the adjacent coastal zone. Core sampleswere also analyzed forbenthic foraminiferal content in order to determine possible effects of high, upwelling-inducedproductivity on bottomwater oxygenation. The benthic foraminiferal assemblages are dominatedbyHanzawaia concentrica (over 50%), with less abundantUvigerina excellens, Cancris spp., Planulinaornata, Quinqueloculina lamarckiana, Epistominella sandiegoensis, Nonionella basispinata, Cassidulinamodeloensis and Textularia foliacea. The benthic foraminiferal assemblages are characteristic ofoxygen concentrations above 1 ml l−1, indicating that possible changes in productivity did notsignificantly affect bottomwater oxygen concentrations over the last 100 years.
Keywords:Dinoflagellate cysts210Pb137CsBenthic foraminiferaPacific coastEutrophicationUpwellingGulf of Tehuantepec
z-Fernández).
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1. Introduction
Dinoflagellates are important primary producers, and cons-titute a major part of the marine eukaryotic phytoplankton,together with diatoms and coccolithophorids. During their life
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cycle and following sexual reproduction, many dinoflagellatespecies have a non-motile stage, during which the cell isprotected within a calcareous or organic-walled cyst. The ger-mination of these cysts can provide the inoculum for bloomoutbreaks (Dale, 1983; Rengefors, 1998). Dinoflagellate cystshave a high preservation potential and can rest in/on the sedi-ments for decades (Belmonte et al., 1995). Due to this char-acteristic, cysts constitute a reservoir of potential biodiversity,but can also be useful indicators of productivity, eutrophicationand pollution in recent marine environments (Harland, 1983;Nehring, 1995; Sætre et al., 1997; Dale et al., 1999; Pospelovaet al., 2002, 2005; Radi et al., 2007).
About half of all dinoflagellate taxa are phototrophic,acquiring energy by photosynthesis. Commonly, the limitingfactor on phototrophic phytoplankton productivity is theavailability of nutrients such as phosphorus and nitrogen(Anderson and Lindquist, 1985). In general, dinoflagellatesproduce their blooms later in the season than diatoms, whichhave the ability to reproduce much more rapidly than dino-flagellates. Many dinoflagellate species are heterotrophic ormixotrophic, feeding on other organisms such as diatoms, oron dissolved organic substances (e.g., Gaines and Elbraechter,1987). Phototrophic dinoflagellates appear to take advantageof ocean environments with low nutrient levels, especially inthe tropics and during the late summer in more temperateregions, whereas heterotrophic dinoflagellates depend onfood availability (e.g., Taylor and Pollingher, 1987; Gaines andElbraechter, 1987). Dinoflagellates often occur in the moststable environments and appear well-suited to take advan-tage of stratified water conditions, with little turbulence(Gibson and Thomas, 1995; Gibson, 2000). During the 1980s,harmful algal blooms (HABs) of toxin-producing dinoflagel-late species (red tides) were reported frequently in the Gulf ofTehuantepec (Cortés-Altamirano et al., 1996).
Benthic foraminifera have been widely used as indicatorsof changes in bottom water oxygenation (Sen Gupta andMachain-Castillo, 1993; Bernhard et al., 1997; Bernhard andSen Gupta, 1999). On the continental shelf of the Gulf ofTehuantepec, two main assemblages occur, related to bathy-metry and the concentration of dissolved oxygen in the bottomwaters: (1) an assemblage dominated by Hanzawaia nitidulaand Cassidulina sp. A, on the middle shelf at water depthsbetween 100 and 150m and oxygen concentrations from 0.3 to0.5 ml l−1; and (2) an assemblage dominated by Bolivina spp.and Epistominella bradyana in sediments of the outer shelf atwater depths greater than 150 m and dissolved oxygenconcentrations of less than 0.3 ml l−1 (Pérez-Cruz andMachain-Castillo, 1990). Living (rose bengal stained) popula-tions of benthic foraminifers on the inner shelf of the gulf arecharacterized by up to 50% of Hanzawaia concentrica, atdissolved oxygen concentrations above 1 ml l−1 (Machain-Castillo et al., 2006). Changes in benthic foraminiferal assem-blages over the last deglaciationmay reflect changes in bottomwater oxygen concentration, related in part to changes inupwelling activity (Machain-Catillo et al., 2001).
This paper documents the spatial distribution of dinocystsin surface sediments of the Gulf of Tehuantepec and thetemporal distribution of dinocyst assemblages in a 210Pb-dated sediment core. The purpose is to reconstruct possiblechanges in sea-surface conditions and productivity related tourbanization and industrialization along the coasts. In
addition, benthic foraminiferal assemblages were analyzedin order to document possible variations in bottom wateroxygenation.
2. Study area
The Gulf of Tehuantepec is located in the Eastern TropicalPacific, between 14°30′ and 16°12′ N and between 92°00′ and96°00′ W, with an average water depth of approximately250 m and a maximum water depth of around 1000 m. Itrepresents the southern oceanic boundary of the MexicanExclusive Economic Zone (Fig. 1). The regional climate iswarm tropical with a mean annual air temperature of 27 °Cand little seasonal variability (García, 1981). Several rivers(Tehuantepec, Juchitán, Espíritu Santo, Ostuta, Huehuetan,Coatán, Cahuacan and Suchiate) discharge in the Gulf.
This area is influenced by intense, wind-induced upwel-ling which triggers high primary productivity in the order of350 gC m−2 yr−1 (cf. Antoine et al., 1996). It supports a widevariety of commercial fisheries from the coastline to the openocean, including shrimp and tuna. This productivity is notuniform temporally and geographically. The high NE–SWatmospheric pressure gradient along the Sierra Madre (Kirbyet al., 1997) generates a regional atmospheric circulation in-fluenced by the Isthmus of Tehuantepec, and characterized bystrong north-easterly winds (“Tehuanos”) during the winter(Boumaggard et al., 1998). As a consequence, higher winter(December to May) upwelling activity occurs in the northernpart of the Gulf of Tehuantepec (Trasvina et al., 1995; Lluch-Cota, 2002) than in the southwestern zone.
As many other high-productivity upwelling systems, theGulf of Tehuantepec is characterized by an oxygen minimumzone with dissolved oxygen contents close to zero between200 to 800 m (Cline and Richards, 1972), and concentrationsb0.5 ml l−1 below 75–100 m water depth (Pérez-Cruz andMachain-Castillo, 1990). The surface water layer is character-ized by a salinity of about 34 psu. Sea-surface temperaturesrange from 17 to 22 °C in the winter and can reach as much as30 °C in summer (Monreal-Gómez and Salas de León, 1998).Coring site Tehua II-21 (66.7 m water depth), located in thecentral part of the Gulf of Tehuantepec (cf. Fig.1), is marked byan average sea surface salinity of 33.8 psu and by averagewinter and summer sea surface temperatures of 25.8±1.8 °Cand 29.6±0.4 °C (cf. compilation from the data available atNODC, 2001). The primary productivity estimate fromsatellite observations is 340±55 gC m−2 yr−1 (cf. Antoine etal., 1996). Measured dissolved oxygen content in bottomwater at the coring site is 1.5 ml l−1.
The Isthmus of Tehuantepec constitutes the narroweststrip of Mexican territory, stretching 220 kmbetween the Gulfof Mexico to the North in Veracruz and the Pacific Ocean tothe South in Oaxaca. During the last few decades, the area hasexperienced important industrial development. Between the1960s and 1970s, Mexico adopted a strategy to createindustrial centers at the littoral zone of undeveloped regionsand near the border with the United States. Particularly at theTehuantepec Isthmus, the development programs focused onthe creation of two industrial poles (the harbors Coat-zacoalcos in Veracruz and Salina Cruz in Oaxaca) related tothe oil industry. According to the Secretariat of Energy ofMexico, Salina Cruz processes 315,000 barrels of oil per day,
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which is the largest volume of crude oil processed among thesix refineries in Mexico. Salina Cruz is the main supplier of oilproducts in the Pacific zone (Secretaría de Energía, México;
Fig. 1. The sampling area in the Gulf of Tehuantepec, showing meanwind pattern (ar66.7 mwater depth. The dots show the location of surface sediment samples used toKielt, 2007).
http://normateca.energia.gob.mx/wb2/SenerNva). The envir-onmental impact from these industrial activities and theirassociatedpopulation growthhas beenpoorly studied, although
rows). Core TEHUA II-21 (star) was collected at 15°59.987′ N, 94°48.469′W, atestablish a modern dinocyst database in the Gulf of Tehuantepec (cf. Table 1;
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hydrocarbon and heavy metal pollution has been reported incoastal water bodies connected to the Gulf of Tehuantepec(González-Macías et al., 2007).
3. Materials and methods
3.1. Sampling
The studied samples include twenty nine surface sedi-ment samples and one sediment core (41 sections). Thesurface sediment samples (0–1 cm) were collected with aReineck-type box corer during the TEHUA-II oceanographiccruise in May 2003 (Table 1). Gravity core TEHUA II-21,18 cm long, was collected at 15°59.987′ N and 94°48.469′W, water depth ~66.7 m, using a Reineck-type corer, andsub-sampled using a plastic tube (7 cm i.d.) on board of O/VEl Puma, during the TEHUA II oceanographic cruise inOctober 2004 (Fig. 1). No laminations or evidence of biotur-bation were observed in the core. Sediments were sampledat 0.3 cm intervals down to 10 cm, then at 1 cm intervals atgreater depths and stored frozen (−20 °C). Wet sedimentsamples were collected for palynological analyses and keptin a cool room (4 °C). The samples for geochemical andradioisotope analysis (210Pb, 137Cs) were freeze-dried. Sedi-ments were ground to powder with a porcelain mortarand stored in polyethylene bags. Results of all analyses arereferred to dry sediment weights in grams. Bottom waterwas sampled with a Niskin bottle in a rosette sampler. Weused the method of Winkler (Carrit and Carpentier, 1966)for the calculation of dissolved oxygen concentration.
Table 1Location of surface sediment samples used in the modern dinocyst database, water dand primary productivity in the upper water mass (cf. Antoine et al., 1996)
Sites Laboratory number Longitude Latitude Water depth (m)
The sediment chronology was determined from 210Pb and137Csmeasurements.137Cswasmeasured byγ-ray spectrometry(663 keV) in an HPGe well-detector; and 210Pb activity wasmeasured through its daughter isotope 210Po, with 209Po addedas an internal yield tracer. Both radionuclideswere deposited onAg discs and their activities were determined by alpha counting(Hamilton and Smith, 1986). The 210Pb analysis were made atthe Laboratory of Geochemistry and Geochronology of theInstitute of Marine Science and Limnology, the UniversidadNacional Autónoma de México; and 137Cs measurements weremade at the Geochemistry and Geodynamics Research Centre(GEOTOP) of the University du Québec à Montréal.
3.3. Geochemical analyses
Particle size analysis was performed by standard sieve andpipette methods (Galehouse, 1971). The total carbon (TC) andtotal nitrogen (TN) contents of an aliquot (5 to 10mg) of dried,crushed and homogenized sediment were determined witha Carlo Erba™ NC 2500 elemental analyzer. Total inorganiccarbon (TIC) was analyzed independently using a UIC Coulo-metrics coulometer following acidification of the samples andCO2 extraction. Total organic carbon (TOC) was obtained bydifference (i.e., TC minus TIC). Precision, as determined fromreplicate measurements of organic analytical standard substan-ces (Acetanilide, Atropine, Cyclohexanone-2, 4-Dinitrophenyl-Hydrazone andUrea), is estimated at ±0.1% for TOC and ±0.3% forTN contents. The analytical reproducibility was 5%.
epth, concentration of dinocysts in surface sediment samples (cf. Kielt, 2007),
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Sediment sampleswereacidifiedwith1NHCl, dried, crushed,and homogenized before isotopic analysis of the organic carbon(OC). The isotopic composition of C and N was measured with aGV Instruments IsoPrime™mass spectrometer coupled to a CarloErba™ elemental analyzer inline. Isotopic data are reported inδ values (‰) with reference to V-PDB (Coplen-Tyler, 1995) andatmospheric N2 (Mariotti, 1983) respectively, following the usualcorrections (e.g., Craig, 1957). Overall analytical uncertainties(±1σ), as determined from routine replicatemeasurements usingstandards, were better than ±0.1‰ for both C and N isotopes. Allanalyses were made at the GEOTOP.
3.4. Palynological analyses
Surface sediment samples (5 cm3) and core sedimentsamples (5 g) were treated following de Vernal et al. (1999).The sediment was sieved through 106 and 10 μmmesh sievesto eliminate clay and fine silts (b10 μm) and coarse grained(N106 μm) particles. The 10–106 μm size fraction was treatedsequentially with hydrochloric acid (HCl 10%) and hydro-fluoric acid (HF 49%) to dissolve carbonate and silicate phases,respectively. The residues were mounted on a glass slides andcovered with a cover-slide for optical microscopic analysis at400x to 1000x magnification. The concentration of palyno-morphs was estimated based on the marker grain method(Matthews, 1969), which consists of the addition of a knownnumber of exotic grains (Lycopodium spores) to each sample,thus allowing the evaluation of absolute concentrations fromthe relative counts of the marker grains and palynomorphs.
All palynomorphs (dinocysts, total pollen, spores, etc.) werecounted (more than 300 palynomorphs for each sample), withspecial attention to dinocysts. An average of 236 dinocysts wascounted and identified in each sample for the calculation of taxa
Table 2List of dinocyst taxa recorded in surface sediments and core TEHUA II-21
Surface sediment dinoflagellate cysts D
Phototrophic taxa PBitectatodinium spongium (Zonneveld 1997) Zonneveld and Jurkschat 1999 BLingulodinium machaerophorum (Deflandre and Cookson 1955) Wall 1967 LNematosphaeropsis labyrinthus (Ostenfeld 1903) Reid 1974 NOperculodinium centrocarpum (Deflandre and Cookson 1955) Wall 1967 OCyst of Pentapharsodinium dalei Indelicato and Loeblich 1986 CPolysphaeridium zoharyi (Rossignol 1962) Bujak et al., 1980 PSpiniferites delicatus Reid 1974 SSpiniferites mirabilis (Rossignol 1964) Sarjeant 1970 SSpiniferites ramosus (Ehrenberg 1838) Mantell 1854 T
Heterotrophic taxa HBrigantedinium simplex Wall 1965 ex Lentin and Williams 1993 BBrigantedinium cariacoense (Wall 1967) Lentin and Williams 1993 BCyst of Polykrikos schwartziii Bütschli 1873 CCyst of Polykrikos cf. kofoidii Chatton 1914 CEchinidinium aculeatum Zonneveld 1997 CEchinidinium granulatum Zonneveld 1997 ESelenopemphix nephroides Benedek 1972 emend. Benedek and Sarjeant 1981 ESelenopemphix quanta (Bradford 1975) Matsuoka 1985 EStelladinium Bradford 1975 EStelladinium stellatum (Wall and Dale 1968) Reid 1977 LQuinquecuspis concreta (Reid 1977) Harland 1977 SVotadinium spinosum Reid 1977 S
SQV
percentages and concentrations. The dinocysts fluxes werecalculated multiplying the accumulation rate (g cm−2 yr −1) bythe dinocyst concentration (cysts g−1). In order to assess eutro-phication in the area (Matsuoka, 1999), the phototrophic/hete-rotrophic ratio was calculated as follows: the species identifiedwere separated according to their trophic behaviour (Table 2)and the total concentration of the phototrophic taxa was di-vided by the total concentration of heterotrophs.
The taxonomical nomenclature follows Rochon et al. (1999),Head et al. (2001) and Pospelova and Head (2002). The assem-blages included cysts of Polykrikos kofoidii, described byMorey-Grains and Ruse (1980), Matsuoka (1987) and Matsuoka andCho (2000). They also included Polysphaeridium zoharyi as des-cribed by Matsuoka (1989) and Tuberculodinium vancampoe asdescribed by Rossignol (1964) and Wall (1967). The originaldescriptions by Zonneveld (1997), Zonneveld and Jurkschat(1999) and Head (2002) were used to identify Echinidiniumspecies and Bitectatodinium spongium. The specimens belong-ing to the Protoperidiniales were grouped into ‘Protoperidi-nioid’ due to the difficulty of identification at species or genuslevel because of bad orientation or folding. Similarly, Brigante-dinium spp. includes specimens of Brigantedinium simplex andBrigantedinium cariacoense and unidentified Brigantediniumspecies. Rare specimens of the Operculodinium centrocarpumshort processes form (de Vernal et al., 2001)were observed andgrouped with O. centrocarpum.
3.5. Benthic foraminiferal analysis
Benthic foraminiferswere picked from the coarse (N106 μm)fraction. Samples were split into an aliquot of approximately300 specimens, which has been shown to be representative(e.g., Phleger, 1954). For species determination we used the
owncore dinoflagellate cysts
hototrophic taxaitectatodinium spongium (Zonneveld 1997) Zonneveld and Jurkschat 1999ingulodinium machaerophorum (Deflandre and Cookson 1955) Wall 1967ematosphaeropsis labyrinthus (Ostenfeld 1903) Reid 1974perculodinium centrocarpum (Deflandre and Cookson 1955) Wall 1967yst of Pentapharsodinium dalei Indelicato and Loeblich 1986olysphaeridium zoharyi (Rossignol 1962) Bujak et al., 1980piniferites delicatus Reid 1974piniferites mirabilis (Rossignol 1964) Sarjeant 1970uberculodinium vancampoae (Rossignol 1962) Wall 1967
eterotrophic taxarigantedinium simplex Wall 1965 ex Lentin and Williams 1993rigantedinium cariacoense (Wall 1967) Lentin and Williams 1993yst of Polykrikos cf. kofoidii Chatton 1914yst of Protoperidinium americanum (Gran and Braarud 1935) Balech 1974yst of Protoperidinium stellatum (Wall and Dale 1968) Reid 1977chinidinium aculeatum Zonneveld 1997chinidinium delicatum Zonneveld 1997chinidinium granulatum Zonneveld 1997chinidinium transparantum Zonneveld 1997ejeunecysta sp. Artzner and Dörhöfer 1978 emend. Lentin and Williams 1976elenopemphix nephroides Benedek 1972 emend. Benedek and Sarjeant 1981elenopemphix quanta (Bradford 1975) Matsuoka 1985telladinium stellatum (Wall and Dale 1968) Reid 1977uinquecuspis concreta (Reid 1977) Harland 1977otadinium calvum Reid 1977
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specialized literature (see Table 1). Their relative and absoluteabundances were used to calculate Shannon, Equitability andSimpson indexes.
3.6. Statistical data analyses
Principal component analysis (PCA) was performed usingCANOCO forWindows 4.0 (cf. ter Braak and Smilauer,1998) ona dinocyst data set including 24 taxa and 29 samples (Fig. 1).PCA is commonly used to analyze field datasets of many in-dependent variables in order to reduce the number of va-riables (species) by creating factors that may be related toparticular environmental conditions. PCA also allows the de-termination of clusters of inter-related variables (species withcomparable ecological affinities) within the data set. Thefactor loadings are the result of the input provided by indi-vidual variables. The variables that most strongly load on aparticular factor can be used to assign the physical meaning ofthat factor (Szefer and Kaliszan, 1993). Q-mode factor analysiswas used with the down-core dataset of relative abundancesof 22 species of benthic foraminifera (those constituting morethan 1% of the assemblages and present in at least 3 sam-ples) and 12 selected samples, using STATISTICA'99 software(StatSoft, 1999). Dinocyst data of the core were used forquantitative reconstruction of primary productivity based onthe modern analog method and using the modern dinocystdatabase of Radi and de Vernal (2008-this issue).
4. Results and discussion
4.1. Radioisotope dating
The activities of 210Pb in the TEHUA II-21 core show resultsconsistent with the exponential decay law (Fig. 2). Numericalages were calculated using the Constant Rate of Supply (CRS)model (Appleby and Oldfield, 1992), and the sediment core wasdated down to 13 cm depth, corresponding to a time span of~100 years, the limit of using 210Pb data. Accretion and sediment
Fig. 2. 137Cs and 210Pb activities (Bq kg−1) in core TEHUA II-21.
mass accumulation rates vary from0.03 to 0.21 cmyr−1 and from0.05 to 0.29 g cm−2 yr−1, respectively. Themost important incre-ments were recorded between the surface and 6.15 cm depth(i.e. 1960s–present). A single maximum of 137Cs (1.70 Bq kg−1)was found at 6.75 cm depth (Fig. 2). This isotope was producedduring maximum atmospheric nuclear weapons testing (1963),thus dating the 6.75 cm depth level to that age, in agreementwith the 210Pb-derived ages. The 137Cs-derived accretion rate(0.16 cm yr−1) is similar to the average accretion rate obtainedfrom the 210Pb chronology for the same range of depths (0.16±0.04 cm yr−1; between surface and 6.75 cm depth).
4.2. Geochemical data
All samples have a high sand content (76–89%, Fig. 3a) andlow silt (8–20%, Fig. 3b) and clay (1–9%, Fig. 3c) contents, sug-gesting a high-energy coastal environment. Strong currentsmay lead to re-suspension and/or systematic transport of cystsaway from the location of production. However, trap studies inhigh productivity areas have provided evidence that verticalsedimentation of dinocysts is very rapid, so that lateral trans-port might be limited (e.g., Zonneveld and Brummer, 2000).
Sediments have high TIC contents (8.9 to 15.5%; Fig. 3d),predominantly foraminiferal tests andmollusc shells. The TOCcontent varies from 0.4 to 0.8% (Fig. 3e), with peak values at 4and 10 cm depth. The TOC flux data show a general increasingtrend, with values higher than 1 mg cm−2 yr−1 in the upper-most 4 cm (Fig. 3g). Two TOC flux peaks are recorded at 1.95–2.25 and at 3.15–3.45 cm depth, possibly resulted from thecombination of higher productivity and higher coastal input tothe area. The TN content (Fig. 3f) shows a relatively homo-geneous profile, with values ranging from 0.6 to 0.8 mg g−1.
The atomic TOC/TN ratio shows moderate variations withdepth (Fig. 3i), generally oscillating between 8 and 10, typicalmarine values (Giordani and Angliolini, 1983). Between 3 and4 cm depth, the TOC/TN values increase up to 14, coincidingwith the peak of the TOC flux mentioned above.
The δ13C values range from −21.5 to −20.8‰ (Fig. 3j) anddecrease slightly toward the top of the core. Such δ13C dataare typical of marine sources (e.g., Meyers, 1994). The de-creasing trend towards the surface may be explained as asubtle change in organic matter composition due to enhancedcontribution of terrestrial TOC. However, the trend could bealso attributed to the oceanic 13C Suess effect, the recentdecline in 13C/12C ratio of oceanic dissolved inorganic carbon(DIC) due to addition of relatively 13C depleted CO2 from fossilfuel burning (e.g., Keeling, 1989). No data about δ13C in totalDIC in the Gulf of Tehuantepec waters are available. We con-clude that the decrease in δ13C towards the top of the coredoes not necessarily indicate a significant change in the sourceof organic matter.
The δ15N values, ranging from 6.9 to 8.0‰ (Fig. 3k) alsoindicate a TOC input dominated by marine production (e.g.,Meyers, 1994). A shift towards higher values is observed from~4.0 cm depth (ca. 1985 AD) to the surface. It could be relatedto an increased input of nitrogen from heavy 15N sources, suchas eroded soils, fertilizers or waste water (e.g., Talbot, 2001;Church et al., 2006).
The increased sedimentation rates, organic carbon fluxes,TOC/TN ratios and δ15N, as well as the slightly lower values ofδ13C in the most recent sediments of the TEHUA II-21 core
Fig. 3. Sand, silt, and clay size fractions, calcium carbonate (CaCO3), total organic carbon (TOC) and total nitrogen (TN) content, expressed as percentage of dryweight, total organic carbonmass accumulation rate in gC cm−2 yr−1,TOC/TN ratio, δ15N, δ13C of TOC as a function of depth and age in the TEHUA II-21 core.
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Fig. 4. Summary diagram of dinocyst assemblages in surface sediment samples of the Gulf of Tehuantepec (see Fig. 1 and Table 1 for location). The modern productivity (cf. Antoine et al., 1996) and scores of axes 1 and 2 ofprincipal component analysis (PCA) are shown to the right. For geographical location of PCA scores, see Fig. 5.
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may reflect higher coastal sediment transport resulting fromincreasing soil erosion promoted by humanpopulation growth,land use changes and industrial development that have takenplace in the adjacent coastal area of the Gulf of Tehuantepecsince late 1930s. Such land use changes include the dredging ofthe Salina Cruz port in 1938, the construction of three damsbetween 1949 and 1961, the construction of the Transitsmicahighway between 1950 and 1953, a cement factory and the oilrefinery of Salina Cruz during the 1970s.
Fig. 5. (a) Ordination of the taxa along PCA axes 1 and 2; (b) geographical distribution oBraak and Smilauer,1998). Positive PC-1 values correspond to assemblage zone1 (northw
4.3. Dinocyst assemblages
4.3.1. Surface sedimentsDinocyst populations are characterized by abundant hete-
rotrophic taxa (mostly Brigantedinium spp. and Echinidiniumspp.; Fig. 4). There also are more heterotrophic species thanphototrophic ones (cf. Table 2). The distribution of hetero-trophic dinoflagellates is in part controlled by the availabi-lity of prey (diatoms and other dinoflagellates, for example),
f the scores of PC-1, based on a PCA donewith CANOCO for Windows 4.0 (cf. terest zone), negative values correspond to assemblage zone2 (southeastern zone).
Fig. 6. Relationship between PC-1 scores and a) the percentages of dinocystheterotrophic taxa, b) annual productivity and c) winter productivity.
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whereas the distribution of the phototrophic species is insteadcontrolled by the availability of light, competition with theblooming diatom populations and the availability of dissolvednutrients (e.g., Taylor and Pollingher, 1987; Gaines andElbraechter, 1987). The relationship between primary produc-tivity or nutrient concentrations and dinocyst assemblages hasbeen documented in upwelling areas, where dinocyst assem-blages are generally characterized by dominance of hetero-trophic taxa due to the high food availability (Lewis et al., 1990;Zonneveld et al., 2001; Dale et al., 2002; Radi and de Vernal,2004). The cyst assemblages in the Gulf of Tehuantepec thusappear typical of upwelling regions. The PCA analysis, alongwith the taxa percentages, allowed the identification of twoassemblage zones,which differ in geographical location (Fig. 4).The first one is characterized by high concentrations of upto 4000 cysts cm−3 (Table 1), with dominant Brigantediniumspp. and P. zoharyi, accompanied by Quinquecuspis concreta,Selenopemphix quanta, Echinidinium spp. and other heterotro-phic protoperidiniale taxa. This assemblage zone is restricted tothe northern part of the Gulf, where winter upwelling occursand productivity ranges between 246 and 368 gCm−2 yr−1. Thesecondassemblage occurs in the southernpart of theGulf and ischaracterized by lower cyst concentrations (b2000 cysts cm−3;Table 1) with dominant phototrophic taxa, in particular Spi-niferites delicatus, B. spongium and Spiniferites spp. In thisarea, primary productivity is lower, ranging between 129 and218 gC m−2 yr−1.
The relation between dinocyst assemblages and produc-tivity is illustrated by the results of the principal componentanalysis (PCA; Figs. 5 and 6). The productivity gradient is wellcaptured in the dinocyst assemblages, with a strong ordinationof heterotrophic taxa together with P. zoharyi on the negativeside of PC-1 which explains 46.8% of the total variance (Fig. 5).PC-1 is significantly correlated with winter and annualproductivity and percentage of heterotrophic taxa (Fig. 6). Incontrastwith some other upwelling regions, however (Radi andde Vernal, 2004; Radi et al., 2007), there is no significant cor-relation between the percentage of heterotrophic taxa andproductivity. This can be explained by the occurrence of thephototrophic taxon P. zoharyi, which is dominant in the highproductivity zone of the Gulf of Tehuantepec.
4.3.2. Down-core recordCyst concentration in the TEHUA II-21 core varies from 477
to 2296 cysts g−1 (Fig. 7), which is low in comparison to valuesobserved in the coastal zone of North America (e.g., Mudieet al., 2002; Kumar and Patterson, 2002; Thibodeau et al.,2006; Radi et al., 2007) and Europe (e.g., Dale et al., 1999;Harland et al., 2004). From the bottom to the top of the core,dinocyst concentration decreases slightly, but the cyst fluxesrange between 68 and 300 cysts cm−2 yr−1, with a maximumof 500 cysts cm−2 yr−1 at about 8 cm depth (ca. 1950 AD). Thetotal pollen profile shows peak values between 6.5 and 8.5 cmdepth (between 1948 and 1962), decreases toward the top ofthe core. The dinocyst/total pollen ratio (Fig. 7) shows peaksin the early 1960s, possibly because of a reduction in theterrigenous supply, as a consequence of the river impound-ments in the area between 1949 and 1961.
Downcore dinocyst assemblages are relatively diverse(Table 2), with a total of 23 taxa identified (Fig. 8), similarto that in the surface sediment samples from the Gulf of
Tehuantepec. Two taxa are dominant: Brigantedinium spp.(29–69%) and P. zoharyi (~1–36%). Heterotrophic protoper-idiniale and gymnodiniale taxa are dominant in the numberof species and in relative abundance. The heterotrophic taxainclude Brigantedinium spp., Q. concreta, S. quanta and Echini-dinium spp. (Echinidinium delicatum, Echinidinium granulatum
Fig. 7. Dinocyst concentration (cysts g−1) and flux (cysts cm−2 yr−1), phototrophic vs. heterotrophic dinocyst abundances, dinocyst vs. pollen ratio (i.e., marine vs. terrestrial palynomorph ratio) and reconstructed annualprimary productivity from dinocyst assemblages using themodern analoguemethod. The error of reconstruction of annual productivity is about ±34.16 gCm−2 yr−1 (see Radi and de Vernal, 2008-this issue). Vertical scale as inFig. 3.
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Fig. 8. Dinocyst taxa percentages in the TEHUA II-21 sediment core. Vertical scale as in Fig. 3.
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Table 3List of benthic foraminifer species recorded in core TEHUA II-21
Bolivina interjuncta Cushman var. bicostata (Cushman, 1937)=Bolivina costata d'Orbigny var. bicostata (Cushman, 1926)Bulimina marginata (d'Orbigny, 1826)Brizalina acutula (Bandy)=Bolivina advena Cushman var. acutula(Bandy, 1953)Cancris auriculus (Fichtel and Moll)=Nautilus auricula(Fichtel and Moll, 1798)Cancris panamensis (Natland, 1938)Cassidulina modeloensis (Rankin, 1934)Cassidulina tortuosa (Cushman and Hughes, 1925)Cibicides mckannai (Galloway and Wissler, 1927)Epistominella bradyana (Cushman)=Pulvinulinella bradyana(Cushman, 1927)Epistominella sandiegoensis (Uchio, 1960)Fursenkoina pontoni (Cushman)=Virgulina pontoni (Cushman, 1932)Hanzawaia concentrica (Cushman)=Cibicides concentricus(Cushman, 1918)Nonionella basispinata (Cushman and Moyer)=Nonion pizarrensevar. basispinatum (Cushman and Moyer, 1930)Planulina ornata (d'Orbigny)=Truncatulina ornata (d'Orbigny, 1839)Quinqueloculina lamarckiana (d'Orbigny, 1839)Quinqueloculina sp. 1Rectobolivina pacifica (Cushman and McCulloch)=Bifarina pacifica(Cushman and McCulloch, 1942)Spiroloculina planulata (Lamarck)=Miliolites planulata (Lamarck, 1805)Textularia foliacea (Heron-Allen and Earland, 1915)Trifarina bella (Phleger and Parker)=Angulogerina bella(Phleger and Parker, 1951)Uvigerina excellens (Todd, 1948)Uvigerina hootsi (Rankin, 1934)
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and Echinidinium aculeatum). Common phototrophic gonyau-lacale taxa include P. zoharyi, B. spongium, O. centrocarpum, S.delicatus and Spiniferites mirabilis.
Among the dinocyst species, some are thermophilic: B.spongium, S. mirabilis, and P. zoharyi. Among the assemblages,three harmful algal bloom (HAB) cyst types were recorded inlow and variable concentrations throughout the core: P. zoharyi(cyst of Pyrodinium bahamense), which can cause ParalyticShellfish Poisoning (PSP), as well as O. centrocarpum (cyst ofProtoceratium reticulatum) and Lingulodiniummachaerophorum(cyst of Lingulodinium polyedrum) which can produce yesso-toxin (YTX; Draisci et al., 1999; Satake et al., 1997).
Inorder to reconstruct hydrographic conditions andproduc-tivity for the duration of sedimentation of the core, we used themodern analogue method applied to the database of de Vernalet al. (2005) and Radi and de Vernal (2008-this issue), to whichsamples were added from the Gulf of Tehuantepec and thecoastal margins of Mexico in the tropical Pacific (Kielt, 2007).Modern analogs for the fossil samples come fromnearby sites inthe Gulf of Tehuantepec or along the Mexican margins.
The productivity was estimated by using the dataset ofAntoine et al. (1996) as a reference for the modern produc-tivity (see Radi anddeVernal, 2008-this issue, for details aboutthe method and the respective data sets). The reconstructionsreveal a high productivity (N300 gC m−2 yr−1) throughout thesequence, with minor fluctuations (Fig. 7). Maximum valuesbetween 8 and 2 cm correspond to an interval from ca.1950 to1995. This interval is characterized by a maximum abundanceof P. zoharyi, which reflects high productivity according to thedistribution of assemblages in surface sediment samples fromthe Gulf of Tehuantepec. There is no evidence for a signi-ficant increase in productivity during the last decade (1990s),althoughfluctuations in relative taxon abundances (Fig. 8) andin the autotrophic vs. heterotrophic ratio might relate tochanges in the nutrient availability.
4.4. Foraminiferal assemblages
Fifty three species of benthic foraminifers were found in thesediment core (Table 3),mostofwhich are rare anddonot occurcontinuously in the core samples. Only 22 species constitutemore than 1% of the total population in any particular sample(Fig. 9). The assemblages are dominated by H. concentrica,constituting 43 to 57% of the population. Other important butless common species (2 to 8%) are Uvigerina excellens, Cancrisspp., Planulina ornata, Quinqueloculina lamarckiana, Epistomi-nella sandiegoensis, Nonionella basispinata, Cassidulina mode-loensis and Textularia foliacea. The assemblages are ratheruniform throughout the core and similar to those characterizingthe modern shelf of the Gulf of Tehuantepec, at bottom wateroxygen concentrations above 1 ml l−1 (Machain-Castillo et al.,2006), although someof the species (U. excellens,N. basispinata)can be found in high productivity and oxygen minimum envi-ronments (Pérez-Cruz and Machain-Castillo, 1990; Sen Guptaand Machain-Castillo, 1993).
Benthic foraminiferal abundance and diversity are closelyrelated to primary productivity and upwelling in the centralpart of the Gulf of Tehuantepec (Machain-Castillo et al., 2007).We calculated several diversity indices by taking into accountnot only the species richness (number of species present) butalso the distribution of specimens over species. We used the
relative abundance data to calculate Simpson's index (Simpson,1949), which characterizes species diversity (the proportion ofgiven species relative to the total number of species), Shannon'sindexwhich accounts for both relative abundance and evennessof the species (Shannon,1948), and the Equitability index,whichillustrates species distribution (Pielou,1966). None of the indicesshow significant variations through the core (Fig. 9 and Table 4).The results of Q-mode factor analysis also indicate no significantchange in the assemblages throughout time represented in thecore (Table 4). This implies that bottom water oxygen concen-tration did not vary enough to influence the benthic forami-niferal assemblages, and supports the hypothesis of a relativelyuniform productivity at decadal to centennial scale on the innershelf of the Gulf of Tehuantepec.
4.5. Industrial development and environmental impact
The phototroph/heterotroph dinocyst ratio shows twomainfeatures: high variability and no general trend before the 1950s(Fig. 7), and a significant decrease afterwards. Dominance ofheterotrophic taxa combined with a low concentration of di-nocysts, or with increased fluxes of dinocysts, have been pre-viously interpreted as indicating anthropogenic stress relatedto industrial pollution (Sætre et al., 1997) and eutrophication(Matsuoka, 1999). Sætre et al. (1997) also argued that theincrease in heterotrophic taxa reflected food availability (e.g.diatoms), which leads to an increase in abundance of hetero-trophic dinoflagellates, or reduced lightpenetration in thewatercolumn that discriminates against phototrophic taxa. Reducedlight penetration could be caused by eutrophication (higherconcentration of photosynthesizers in the water column), butalso by an increase in the amount of suspended solids in the
Fig. 9. Benthic foraminiferal taxa percentages in the TEHUA II-21 sediment core. The Simpson, Shannon Wiener and Equitability diversity indexes are shown to the right. Vertical scale as in Fig. 3.
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Table 4Simpson, ShannonWiener and Equitability indexes fordown-core foraminiferalassemblages and Factor 1 (98.77% of the total variance) scores obtained byQ-mode factor analysis carried out upon foraminiferal assemblages
Depth(cm)
Diversity indexes Factor analysis
Simpson Shannon Wiener Equitability Factor 1 (98.7%)
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water column. The latter causes an increase in sediment accu-mulation rates, as observed in the present study. The slightincrease in relative abundance of Brigantedinium spp. and S.quanta (Fig. 8) might also indicate a subtle change towardsnutrient-enrichment, as observed in the Adriatic Sea (Justicet al.,1987; Sangiorgi and Donders, 2004). In our core, however,there is no convincing evidence of an increase in nutrients, withthe exception of aminor increase inTOC between the late 1930sand the early 1990s (Fig. 3).
No evidence of eutrophication or pollution was observedin the other environmental proxy records. Nonetheless, it isclear that important changes have occurred since the onsetof the industrialization of the coastal zone of the Gulf ofTehuantepec, starting from late 1930s. The most conspicuouschanges in core TEHUA II-21 are related to a higher sedimentssupply, as shown by increasing 210Pb-derived sediment accu-mulation rates, which could be explained on the basis ofhigher coastal erosion promoted by land uses changes.
5. Conclusions
This study shows that productivity, largely linked to sea-sonal upwelling, is the major parameter controlling the com-position of dinocyst assemblages in the Gulf of Tehuantepec.Geochemical andmicropaleontological records in core TEHUAII-21 show little evidence for major changes in primary pro-ductivity over the last 100 years. Dinocyst assemblages andfluxes, inferred productivity and benthic foraminiferal assem-blages all indicate a continuously high productivity related toupwelling during the last century, without clear indication ofa recent increase in surface production leading to eutrophica-tion and decreased oxygen concentration in bottom waters.Indications for a higher input of terrestrial OM over the lastdecades are found in the record of isotopic composition oforganic carbon (δ13C), and a shift towards an increased conti-nental contribution related to human activities is providedby the record of the isotopic composition of nitrogen (δ15N).The enhanced nutrient supply from the coastal zone of theIsthmus of Tehuantepec resulting from urbanization and in-dustrialization starting in the late 1930s had little effect onthe regional productivity, probably because upwelling leadsto continuous mixing from deep to surface water, attenuating
the impact of anthropogenic forcing. Anthropogenic forcingmay have led to an increased in sediment accumulation rates,however, thus a reduction in cyst concentration and a shifttoward more heterotrophic species.
Acknowledgements
This research was partially funded by grant 45841-F fromthe National Council of Science and Technology from Mexico(CONACyT). The scholarships for LFVB were provided byUNAM-Dirección General de Estudios de Postgrado and theLaboratory of Micropaleontology at (GEOTOP). Mobilitysupport to ACRF was provided by the UNAM-CIC InternationalAcademic Exchange Program, the Geochemistry and Geody-namics Research Centre GEOTOP and the bilateral Mexico-Quebec program for Scientific and Technological Cooperation2007–2009 (Ministère des Relations Internationales du Qué-bec-Secretaría de Relaciones Exteriores deMéxico). Thanks aredue to M. Henry, M.C. Ramírez-Jáuregui, G. Ramírez-Reséndiz,H. Bojórquez-Leyva, L.H. Pérez-Bernal, V.Montes-Montes andG.González-Chávez for their technical assistance; as well to thecrew of O/V El Puma for their help in the field. Analytical workwas supported by infrastructure grants to GEOTOPby the FondsQuébécois de Recherche sur la Nature et les Technologies(FQRNT). The authors gratefully acknowledge the constructivereviews of Francesca Sangiorgi andMarit-Solveig Seidenkrantz.
Appendix A. Supplementary data
Supplementarydata associatedwith this article canbe found,in the online version, at doi:10.1016/j.marmicro.2008.03.002.
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