Sieve Plates and Habitat Adaptation in the Foraminifer Planulina ornatal

Johanna M. Resig2 and Craig R. Glenn 2

Abstract: Planulina ornata (d'Orbigny), a coarsely perforate species of forami­ nifera having a low trochospiral test, was recovered attached to phosphatic hardgrounds from the lower oxygen-minimum zone off Peru. Above the base of individual pores are calcified, perforate sieve plates, the largest so far described. Structure of the pores suggests a possible association with mitochondria and respiratory function. These large pores may facilitate extraction of the severely limited amount of oxygen from the ambient bottom waters at that locale.

IN THE COURSE of investigating foraminifera Jahn (1953) illustrated and described the mi­ encrusting phosphoritic hardgrounds from croporous pore plates and termed them sieve the lower part of the oxygen-minimum zone plates. In some of the studied species, the of the Peru continental slope (Resig and pore plates occur singly at the base of each Glenn 1997), Planulina ornata (d'Orbigny), a pore (Be et al. 1980), but other species have species in which the calcified pore plates and multiple plates, one with each growth lamina their perforations are unusually large, was (LeCalvez 1947, Jahn 1953, Sliter 1974). recovered. Documentation of this occurrence Some pore-sieve plate and micropore diame­ is presented here to supplement the small ters that may be typical offinely and coarsely body of literature on pore microstructure and perforate benthic species and planktonic spe­ function in foraminifera and to lend support cies are as follows: I-j..lm sieve plate, O.I-j..lm to the proposed association of these struc­ micropores in a nonionid (Jahn 1953); 2- to tures with respiratory organelles (Berthold 6-j..lm sieve plate, 0.2- to 0.3-j..lm micropores 1976, Leutenegger and Hansen 1979). in Lamellodiscorbis aguayoi (Arnold 1954b); and An increasing number of perforate fora­ 3.3-j..lm sieve plate, 0.1- to 0.6-j..lm micropores minifera representing various benthic and in Globigerinoides sacculifer (Be et al. 1980). planktonic genera are shown to have their Planulina ornata, in contrast, has 6- to lO-j..lm pores closed offfrom the chambers by organic diameter sieve plates and 0.5- to 1.0-j..lm membranes or plates (Table 1), a condition diameter micropores. These well-defined that may exist for most perforate foraminifera structures are presumably functional within (Boltovskoy and Wright 1976). The plates the species' habitat. are reported to be nonporous in some fora­ minifera such as Ammonia (Banner and Wil­ HABITAT OF Planulina ornata liams 1973), but the majority of those studied are microporous and either calcified or not. Planulina ornata was originally described by d'Orbigny (1839) as Truncatulina ornata from off the Port ofValparaiso, Chile, where it was 1 Partial support of this research was provided by a rare. Its geographic range continues north­ Nation-ai-Science Foundation grant (OCE-9201305) to ward to Alaska (Buzas and Culver 1990). c.R.G. This is University of Hawai'i School of Ocean and Earth Science and Technology Contribution No. Specimens occur free in the sediment and 6005. Manuscript accepted 1 March 2002. are reported to be most frequent on the outer 2 Department of Geology and Geophysics; University continental shelf (Bandy and Arnal 1957 of Hawai'i at Manoa, Honolulu, Hawai'i 96822. [Central America], Bandy 1961 [Gulf of California]) or on the upper continental slope Pacific Science (2003), vol. 57, no. 1:103-110 between 160 and 260 m (Boltovskoy and © 2003 by University ofHawai'i Press Theyer 1970 [Chile]). Their bathymetric All rights reserved range generally extends deeper along the

103 104 PACIFIC SCIENCE· January 2003

TABLE 1 western American margin, to about 1860 m Reported Occurrence of Pore Plates in Foraminifera off Chile (Ingle et al. 1980) or 1200 m off Peru (Resig 1981). Dchio (1960) found Superfarnily/Species Reference protoplasm-bearing tests identified through rose bengal stain from 38 to 946 m and empty Spirillinacea tests from 10 to 1260 m off San Diego, Cali­ Patellina corrugata Berthold (1976) fornia. Specimens are also present in Qua­ Nodosariacea Robulus midwayensis* Hay et aI. (1963) ternary sediment of four cores from the Bolivinacea Peruvian margin taken in water depths be­ Bolivina argentea Leutenegger and tween 307 and 447 m (Resig 1990). In none Hansen (1979) ofthese reports did the species compose more Bolivina cf. excavata Leutenegger and Hansen (1979) than 4% of the benthic foraminiferal as­ Bolivina sp. Sliter (1974) semblages. "Loxostomum" pseudobeyrichi Leutenegger and The extent to which sedimentary speci­ Hansen (1979) mens reflect the life habitat of P. ornata is not Cassidulinacea known. Specimens found free in the sediment Cassidulinoides cornuta Leutenegger and Hansen (1979) may have lived as epi- or infauna; they may Buliminacea have experienced pre- or postmortem dis­ Buliminella tenuata Leutenegger and lodgement or transport. The adherent speci­ Hansen (1979) mens reported here are the only ones so far to Globobulimina pacifica Leutenegger and Hansen (1979) have been collected with certainty in their life Discorbacea positions. Discorbis erecta LeCalvez (1947) Several specimens of P. ornata were recov­ Discorinopsis aguayoi** Arnold (1954a,b) ered from off the coast of Peru at' 11° 59.89' Rosalina floridana Angell (1967) S, 77° 50.91' W in a water depth of 517 m, Planorbulinacea Cibicides cassivellauni Wood and during operations of the Johnson Sea Link Haynes (1957) I submersible (Figure 1). The specimens ad­ Cymbaloporetta squammosa Lynts and hered on their umbilical sides to phosphatic Pfister (1967) crusts (samples 3363 no. 1 and no. 3) that Asterigerinacea Amphistegina madagascariensis*** Hansen (1972) formed in the lowermost portion of the Amphistegina lobifera Leutenegger and impinging Peruvian oxygen-minimum zone, Hansen (1979) under the following oceanographic parame­ Nonionacea ters: O2 = 0.06 ml/liter (2.7 lJ-M), temper­ Nonionella stella Leutenegger and ature 9.7°C, and salinity 34.7%0. Current Hansen (1979) = = Nonionidae (unspecified) Jahn (1953) velocity averaged 7 em/sec. Large encrusting Rotaliacea agglutinated foraminifera were dispersed over Ammonia spp. Banner and the surface of the crusts at a density of ap­ Williams proximately 46 specimens per square centi­ (1973) Nummulitacea meter on 3363 no. 3 (Resig and Glenn 1997), Nummulitidae (unspecified) Jahn (1953) their food presumably drawn from benthic Globigerinacea microbes and phytodetritus settling from the Planktonic species (unspecified) Towe (1971) high-productivity surface waters associated Globigerinoides sacculifer Anderson and with Peruvian upwelling. Of the total fora­ Be (1976) Globorotalia menardii Hemleben et al. minifera occupying the habitat, less than 1% (1977) were adherent forms; the remainder were permanently affixed to the hard phosphatic­ ,.., Lenticulina 11lidwayensis; **, Lo11le/lodiscorbis aguayoi; ***, A11lphistegi1lll lessonii. crust substrate. The bathymetric range exhibited by P. ornata may relate directly to the dissolved oxygen profile off the western Americas, where oxygen depletion begins on the outer Sieve Plates and Habitat of Planulina Resig and Glenn 105

6 8 10 12 14 16 18 20 0 12.0°5 Transect ~ 7cmls 3372'1

200 :I> 23 cmls < Cfl III 0 10 cmls S 3 ~ (') c .r: :: ii. 400 CD GI no data 0 a s.. ;;: '" 11 cmls .,0" == ~ 7cmls

6cmls

100 200 300 Dissolved O2 (flM) 34.5 34.6 34.7 34.8 34.9 35.0 35.1 I ! I ! I I I Salinity (%.)

FIGURE 1. Location of samples 3363 no. 1 and no. 3 containing Planulina ornata at 11" 59.89' S, 77" 50.91' W, water depth 517 m. Oceanographic parameters as well as other samples examined from along a depth traverse are also shown. (After Resig and Glenn 1997.) shelf (Bandy 1961, Ingle et al. 1980, Resig geous epifaunal adaptation for attachment in and Glenn 1997) and where specimens of P. turbulent water and for stability in traveling ornata are most frequent. Bandy (1963) re­ on the surface of the seafloor (Corliss 1985). ported unusually large (1 to 2 mm diameter) The aperture, an equatorial arch at the base specimens of the species from the bottom of of the final chamber (Figure 2A), is sur­ three California Borderland basins with dis­ mounted by a lip and extends beneath an um­ solved oxygen values of 0.2-0.4 ml/liter. bilical folium onto the umbilical side. Large pores are densely and evenly distributed over the chamber surfaces on both sides ofthe test. TEST MORPHOLOGY AND PORE The pores of P. ornata are 6 to 10 11m in MICROSTRUCTURE diameter and are closed by calcified sieve Details of the morphology of Planulina ornata plates in which the rnicropore diameters are are shown in Figure 2A-M. Planulina ornata 0.5 to 1.0 11m (Figure 2D and F). Because has a compressed, keeled, trochospiral test in these sieve plates are formed at the base of which the flat umbilical side is only slightly the pore only when a new chamber is added, less evolute than the spiral side, which is of they are no longer visible in the early cham­ very low convexity (Figure 2A-C). Plano­ bers after new laminae added to the test convex shapes are considered to be advanta- deepen the pore canals (Figure 2G). Some of

Sieve Plates and Habitat of Planulina . Resig and Glenn 107 these sieve plates appear to be in direct and sieve plates (LeCalvez 1947, Jahn 1953), contact with the interior, whereas others are which effectively block the passage of pseu­ covered by the test's organic lining (Figure dopodia (Berthold 1976). In some instances, 2E, H, and M). The absence of the lining however, thin cytoplasmic strands have been may be an artifact of preservation or may seen to penetrate microporous sieve plates provide some contact of the endoplasm with (Febvre-Chevalier 1971, Hansen 1972, An­ the test's exterior. derson and Be 1976, Be et al. 1980), but other Orientation of the test during attachment plates are imperforate (Banner and Williams is with the umbilical side against the hard­ 1973) and impervious to such cytoplasmic ground (Figure 2K). Because the principal interchange. opening of the aperture is peripheral, the . The differences in structure of the pore pseudopodia would still be functional as plates complicate the interpretation of their food gatherers in this position. The umbilical function or functions. Towe (1971) suggested extension of the aperture might allow the an initial stage of chamber calcification in pseudopodia to contribute directly to test at­ which the open or partially closed pores tachment, although light cementation was served an excretory function, and a subse­ also noted (Figure 2J). During attachment, quent stage of closure of the pore with an the pores on the umbilical side appear to be impervious organic lining. Be et al. (1980) sequestered from contact with the overlying noted that the microporous plates penetrated water mass. by rhizopodial strands might function to transport waste in colloidal form from the test interior or for metabolic or oxygen exchange PORE FUNCTION between the exterior and the cytoplasm. Test perforations are not essential to the Leutenegger and Hansen (1979) provided function and well-being of foraminifera; for both cytological and experimental evidence example, two of the principal extant groups, regarding pore function. In fixed sections of those with porcelaneous or agglutinated tests, the cells of benthic foraminifera, they found are mostly without wall perforations. How­ the mitochondria to be abundant and evenly ever, perforations have contributed to the distributed in the cytoplasm of species from a adaptive success of the Rotaliina and their highly oxygenated environment, whereas a numerical superiority in all but a few modem low-oxygen habitat contained species with environments, principally those habitats in fewer mitochondria that were clustered be­ which low pH affects the precipitation of cal­ neath the pore sieve plates. Mitochondria cium carbonate. Although originally consid­ organelles are sites of major oxygen con­ ered as outlets for pseudopodia (Loeblich and sumption as food substances are oxidized and Tappan 1964), pores have been functionally adenosine triphosphate (ATP) is produced reevaluated since the discovery of pore plugs and distributed throughout the cell to drive

FIGURE 2. Planulina ornata (d'Orbigny). A, Edge view of specimen with missing ultimate chamber (wnbilical side to left), foramen indicates equatorial position of lipped aperture. Diameter 0.58 mrn. ]SL 3363 no. 3. B, C, D, F, G, Side views and pore details. B, Umbilical side showing extension of apertute along chamber bases. C, Spiral side. Maximwn diameter 0.62 mrn. D, Enlargement of pores on ultimate chamber ofspiral side showing calcareous sieve plates. Width of field 37 llJIl. F, Enlargement of pores on wnbilical side showing calcareous sieve plates. Width of field 45 llJIl. G, Enlargement of pores on fourth chamber from last of spiral side; sieve plates have disappeared from view as pore canals deepened. Width offield 45 llJIl.]SL 3363 no. 1. E, H, Edge view and wall detail. E, Edge view ofspecimen with broken wall. Diameter 0.46 mrn. H, Enlargement of wall to the right of foramen showing position of sieve plate and organic lining at base of pore. Length offield 35 Ilm. KK71, GC3 (see Resig 1981). I, J, Specimen that had been ce­ mented to the substrate surmounting a spicule. I, Spiral side. J, Umbilical side showing cement over most of surface of attachment. Maximwn diameter 0.70 mrn. ]SL 3363 no. 1. K, L, Light photographs. K, Specimen attached by its wnbilical side to a phosphatic crust. L, Umbilical side of detached specimen. Maximwn diameter 0.76 mrn. ]SL 3363 no. 1. M, Enlargement of pores on interior surface of a wall fragment showing organic membrane over some pores while others remain open to the interior. Width offield 43 llJIl. KK71, GC3. 108 PACIFIC SCIENCE· January 2003

metabolism (Hemleben et al. 1988). Leute­ formis) adapted to a low-oxygen environment. negger and Hansen (1979) suggested that However, chloroplasts present in the cyto­ their positioning beneath the pores leads to plasm of S. fusiform is may have played a role localized oxygen deficiency, which in turn in its metabolism through oxygen production draws in external oxygen through a diffusion and thus affected the disposition of the endo­ gradient. In a confirming experiment, 14COZ plasmic mitochondria in that species. For uptake by symbiont-bearing Amphistegina, now, the possibility that the activity of mi­ they demonstrated a pathway of dissolved tochondria in pseudopodia is more important gases through the pores. than their activity associated with pores Some of the low-oxygen species studied (Bernhard and Sen Gupta 1999) remains un­ by Leutenegger and Hansen (1979) from resolved. 750-m water depth off Southern California In P. ornata the broad test surface area pen­ also occur in muddy substrate of the oxygen­ etrated by unusually large pores in which the minimum zone off Peru (Resig 1981). These sieve plates are perforated by micropores of a include Buliminella tenuata, Globobulimina pa­ size precluding the passage of mitochondria cifica, and "Loxostomum" pseudobeyrichi. These strongly suggests a function related to respi­ species are finely perforate in contrast to the ration in the oxygen-starved environment to coarse perforations in P. ornata, and their which the adherent specimens were bound. elongate tests suggest that they are infaunal. Determination of the distribution of mi­ Globobulimina pacifica does not have an or­ tochondria in this species would clarify the ganic lining that covers the pores, an adapta­ functional morphology of the pore structure. tion that Leutenegger and Hansen attributed Unfortunately, the collection of viable speci­ to low oxygen accommodation. mens of this relatively rare species might In P. ornata, the large pore diameters prove elusive. would provide a large surface for mitochon­ drial positioning, whereas the calcified sieve ACKNOWLEDGMENTS plate in which the micropore diameters are We thank the crew and scientific personnel 0.5 to 1.0 Ilm is a barrier to loss of these of RV Steward Johnson and Johnson Sea Link organelles, which are about 1-2 Ilm in diam­ I Cruise S] 10-92 for their roles in sample and eter (Hemleben et al. 1988). Large pore data collection, as well as two unidentified size, presumably to enhance respiration, also manuscript reviewers for their suggestions. has been reported in other species in low­ oxygen environments when compared with their representatives in well-oxygenated Literature Cited waters (Moodley and Hess 1992, Sen Gupta Anderson, O. R., and A. W. H. Be. 1976. The and Machain-Castillo 1993, Holtzmann ultrastructure of a planktonic foraminifer 2000). The pores on the attachment surface Globigerinoides sacculifer (Brady), and its of P. ornata are presumably sequestered from symbiotic dinoflagellates. J. Foraminiferal this function during test attachment, but Res. 6:1-21. might be in use during dislodgment or free­ Angell, R. W. 1967. The test structure and living mode. composition of the foraminifer Rosalina Although a respiratory function of pores floridana. J. Protozool. 14:299-307. fits our observations on the morphology and Arnold, Z. 1954a. Discorinopsis aguayoi (Ber­ habitat of P. ornata, conflicting results con­ mudez) and Discorinopsis vadescens Cush­ cerning the distribution of mitochondria are man and Bronnimann: A study ofvariation reported by Bernhard and Alve (1996), who in cultures of living foraminifera. Contrib. found them to be concentrated at the pe­ Cushman Found. Foraminiferal Res. 5:4­ riphery of chambers "not clearly associated 13. with pores," along the peripheral septa, and ---. 1954b. A note on foraminiferan principally at the aperture in two shallow­ sieve-plates. Contrib. Cushman Found. water hyaline species, one (Stainforthia fusi- Foraminiferal Res. 5:77. Sieve Plates and Habitat ofPlanulina . Resig and Glenn 109

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