ASYNCHRONOUS CALCIFICATION IN JUVENILE MEGALOSPHERES: AN ONTOGENETIC WINDOW INTO THE LIFE CYCLE AND POLYMORPHISM OF PENEROPLIS

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1 Journal of Foraminiferal Research, v. 39, no. 1, p , January 2009 ASYNCHRONOUS CALCIFICATION IN JUVENILE MEGALOSPHERES: AN ONTOGENETIC WINDOW INTO THE LIFE CYCLE AND POLYMORPHISM OF PENEROPLIS MARTIN R. LANGER 1,3,WALID A. MAKLED 1,STEPHANIE J. PIETSCH 2 AND ANNA WEINMANN 1 ABSTRACT Fully calcified megalospheric juveniles were found to be closely packed within a brood chamber of the larger symbiont-bearing foraminifer Peneroplis sp. (d Orbigny) from Chuuk Island (Micronesia). The juveniles exhibit a notable variation in size of the proloculi and various forms of test deformations. Both the size variation of the megalospheric proloculi and the test deformations are indicative of asynchronous calcification and are a potential source of natural polymorphism in Peneroplis. The results of this study have implications for the interpretation of abnormal shell forms as bioindicators and place constraints on the classic definition of three size classes in Peneroplis. INTRODUCTION Our modern understanding of the life cycle of benthic foraminifera has largely been influenced by the groundbreaking studies of Winter (1907) on Peneroplis pertusus from the Mediterranean Sea. Winter postulated a classic dimorphic life cycle with an alternation of sexual and asexual generations and meticulously illustrated every stage by hand drawings. In the Winter model, the sexual generation produces microspheric diploid agamonts, which in turn lead to megalospheric haploid gamonts by multiple fission (asexual reproduction). Later, the general life-cycle model was modified to include a third asexual generation, the schizont, positioned between the agamontic and the gamontic generations (Rhumbler, 1909; Röttger and others, 1990; Lee and others, 1991; Goldstein, 1999). The modification from the dimorphic to the paratrimorphic life-cycle model was believed to be valid for all larger symbiont-bearing foraminifera (Leutenegger, 1977). In 1993, using light and transmission electron microscopy, Faber and Lee observed that both agamonts and schizonts of Peneroplis pertusus released megalospheric juveniles and, thus, suggested that a paratrimorphic life cycle seems to be applicable to this taxon as well. Their observations were documented by light and high-resolution transmission electron microscopy. While examining benthic foraminifera for biogeographic studies from the Chuuk Island atoll system (Micronesia; Fig. 1), we discovered an adult specimen of Peneroplis sp. in the reproductive stage ready to release juveniles. The adult specimen contained numerous calcified megalospheric juveniles that were seen through the broken apertural face of the parental shell. We examined the parental test in detail 1 Steinman Institut für Geologie, Mineralogie und Paläontologie, Rheinische Friedrich Wilhelms Universität, Nussallee 8, Bonn, Germany. 2 Zoologisches Forschungsmuseum Alexander Koenig, Museumsmeile Bonn, Adenauerallee 160, Bonn, Germany. 3 Correspondence author. martin.langer@uni-bonn.de and the megalospheric juveniles by high-resolution, scanning electron microscopy (SEM). Our observations can be integrated into the life-cycle models of Winter (1907) and Faber and Lee (1993), and they provide new insights into the reproductive biology of the larger symbiont-bearing foraminifer Peneroplis. MATERIALS AND METHODS The sediment sample containing Peneroplis specimens was collected in April 2006 within the Chuuk Lagoon atoll system south of Uman Island (Fig. 1). The Chuuk system is part of the Caroline Island group and a member of the Federated States of Micronesia. The atoll consists of 11 major islands and many smaller islets within a 64-km-wide lagoon surrounded by a protective reef. The sample site is located near the shipwreck of the WW II freighter, the Sankisan Maru, about 500 m off the southern end of Uman Island at a depth of 30 m (7u009 7u219N, 151u859 E; Fig. 1). Sedimentary sample material was collected by scuba diving, dried, and later transported to the laboratory in Bonn, Germany. The juvenile-bearing parental test of Peneroplis sp. was picked from the dried sediment sample material without prior washing. The test was inspected by light microscopy and carefully mounted on stubs for SEM examination. For full documentation, the adult specimen was SEM-photomicrographed at different high-resolution levels and from various observational angles. The parental test was carefully opened up with a picking needle to isolate the juveniles chamber by chamber. All juveniles present within the brood chamber were counted. During the course of investigation, a few megalospheres detached from the SEM stub and could not be measured. RESULTS High-resolution SEM of Peneroplis sp. showed the parental test to contain densely packed juveniles within the largest chamber (Pl. 1, Figs. 1 and 3 5). The juveniles were visible through the partly opened apertural face of the test wall. The opening of the apertural face was not inflicted by the examiners and took place prior to our examination. The rupture on the apertural face of the pre-opened chamber showed sharp, tooth-like, and somewhat irregular breakage fissures in addition to sub-rounded and rather smooth edges (Pl. 1, Figs. 3 5). The parental test was characterized by planispirally arranged, involute chambers, 10 to 11 of which were visible from the exterior (Pl. 1, Fig. 1). Close examination of the test revealed residues and suture lines of another two chambers that had already broken off the test (Pl. 1, Fig. 1; reconstructed Pl. 1, Fig. 2). The largest chamber, which contained the juveniles, thus represents the third-to-last Journal of Foraminiferal Research fora d 24/11/08 16:38:22 8 0

2 ASYNCHRONOUS CALCIFICATION 0 FIGURE 1. Location map showing the sampling site (*) ofpeneroplis sp. within the Chuuk Island atoll lagoon system south of Uman Island, Micronesia. The sample containing Peneroplis sp. originated from a depth of 30 m. chamber. Due to the involute chamber arrangement, the proloculus remained hidden and could not be seen from the exterior by SEM. The test surface of the adult specimen was characterized by a coarsely pitted wall and lacked the characteristic ribs that ornament the lateral chamber walls in other peneroplids. The large pits had circular, oval, or ovate openings and were arranged in single rows perpendicular to the septum and roughly parallel to the periphery of the shell. The pits penetrated the porcelaneous test wall incompletely and to different depths. Similar strongly pitted and nonribbed forms have been discovered by Hottinger and others (1993) from the lower part of the photic zone in the Gulf of Aqaba. Hottinger and others (1993) also pointed out that the systematic position of these very rare varieties has not been resolved yet and considered these forms to represent extreme variants of Peneroplis planatus. Until this issue is resolved, we follow Hottinger and others (1993) but keep this species of Peneroplis in open nomenclature. At least 13 juveniles were densely packed within the preopened third-to-last brood chamber (Pl. 1, Fig. 3). The orientation of the juvenile specimens seemed to be erratic and not arranged in double rows or tetrads. In addition, the apertural openings of the juveniles pointed to different directions. After breaking the brood chamber (Pl. 1, Fig. 8), 40 individual juveniles became visible. We were later able to recover 26 out of 40 juveniles, and we examined, photographed, and measured them separately. All juveniles were fully calcified and revealed the typical form of a megalospheric gamont composed of a proloculus and flexostyle (Pl. 1, Figs. 6 7, 9 13, and 16 18). The tube-like flexostyle was one-half coil in length and had a sub-rounded to subtriangular apertural opening at the end of the tube (Pl. 1, Figs. 6 7). The test of the megalospheric gamonts was subcircular in side view and sub-rounded to sub-carinate in peripheral view (Pl. 1, Figs. 6 7 and 11). The test surface of the megalospheric juveniles showed the proloculus to be densely and regularly pitted (Pl. 1, Fig. 7). In contrast, the surface of the flexostyle, in particular, along the peripheral margin, showed larger, elongate, rhomboid, and slit-like pits mostly arranged parallel to the periphery of the test (Pl. 1, Figs. 7 and 9 11). The size of the juvenile gamonts, measured as the maximum internal diameter (see Pl. 1, Fig. 7), ranged between 18 and 28 mm (n5 26, with a mean of 21.9 mm). Among all juvenile megalospheres recovered from the brood chamber, 7 out of 26 individuals (5 26.9%) showed deformations of the test. The deformations included indentations on the outer test surface; these were seen within the proloculus (Pl. 1, Figs and 13), along the flexostyle (Pl. 1, Figs. 11 and 16), and around the apertural opening on the flexostyle (Pl. 1, Fig. 11). The shape and form of the indentations often resembled imprints of neighboring tests (Pl. 1, Fig. 11). DISCUSSION The life cycle of polythalamous foraminifera has been traditionally considered to consist of a heterophasic alternation between a megalospheric, haploid, uninucleate gamont and a microspheric, diploid, polynucleate agamont (Schaudinn, 1894a, 1894b, 1895a, 1895b, 1903; Lister, 1895, 1903; Winter, 1907; Le Calvez, 1950; Goldstein, 1999). The heterophasic alternation between a sexual and an asexual generation commonly results in a dimorphism of the test (Lister, 1895; Winter, 1907). Observations on the life cycle of the porcelaneous genus Peneroplis date back to the year 1894 when Schaudinn showed that the parental protoplasm undergoes multiple fission and that juveniles develop and calcify within the test of the adult. In 1907, Winter provided a detailed account and meticulously illustrated every stage of the classic dimorphic life cycle of Peneroplis pertusus (16 stages). In his documentation, he showed that in Peneroplis, as in many other classically dimorphic species (Goldstein, 1999), the proloculus of the megalospheric gamont is larger than that of the microspheric agamont (Winter, 1907). Journal of Foraminiferal Research fora d 24/11/08 16:42:17 9

3 0 LANGER AND OTHERS PLATE 1 Scanning electron micrographs of the parental shell and megalospheric juveniles of the benthic foraminifer Peneroplis sp. 1 Side view showing the parental shell containing juveniles within the largest chamber. Note that the last two chambers are broken off, as indicated by remnants of previous chamber walls attached to the marginal surface of the adult test (see arrow). 2 Parental specimen with broken-off chambers reconstructed along the remnants of the lateral chamber lines. 3 Higher magnification of the broken apertural face showing densely packed and fully calcified megalospheric Journal of Foraminiferal Research fora d 24/11/08 16:43:14 10

4 ASYNCHRONOUS CALCIFICATION 0 In 1993, Faber and Lee re-examined the life cycle of Peneroplis planatus from the Gulf of Aqaba (Elat, Egypt). Their observation that both agamonts and schizonts released megalospheric juveniles led them to the assumption that Peneroplis planatus has a paratrimorphic life cycle, which includes a third schizont generation. However, the presence of gamonts has not been shown conclusively and was only implied by the occurrence of microspheric agamonts. To date, a complete paratrimorphic life cycle including agamonts, schizonts, and gamonts has not been documented for Peneroplis. Some authors have suggested that the size of the proloculi in some foraminifera correlates with the presence of three generations (gamonts, agamonts, and schizonts) in a true trimorphic life cycle (Lehmann and others, 2006). Detailed measurements of the diameter of the proloculi of Peneroplis pertusus from the Mediterranean Sea revealed the presence of only two different size classes, where megalospheric proloculi ranged between 38.5 mm and mm (n 5 100), and microspheric proloculi ranged between 15 mm and 26 mm (n 5 50; Winter, 1907). Similarly, Faber and Lee (1993) found two different size classes in the diameter of the proloculi in Peneroplis planatus from the Gulf of Aqaba (n 5 190; microspheric proloculi mm and megalospheric proloculi mm). Natural populations of Peneroplis thus comprise a significant range of variability within the size of the proloculi. Fairly large size ranges were also found in proloculi of other foraminifera. Goldstein and Moodley (1993) noted that in Ammonia beccarii (Linné) forma tepida (Cushman) gamontic proloculi ranged between 27 mm and 48 mm (mean 5 33 mm), which is significantly smaller than those reported by Bradshaw (1957) for agamonts of Streblus beccarii (Linné) forma tepida (Cushman). Similarly, Salami (1976) reported variations in the size of the proloculus in the agglutinated foraminifer Trochammina cf. T. quadriloba (Höglund) and pointed out that it lacks a clear indication of a dimorphism reflected in prolocular size. Winter (1907) also pointed out that only the megalospheric individuals possess the tube-like flexostyle ( Hals des Embryo ) attached to the proloculus; the flexostyle was absent in the microspheric generation. The gamontic juveniles liberated from the parental brood chamber of Peneroplis sp. in this study all displayed the typical form of a megalosphere composed of proloculus and flexostyle. As outlined already, the diameter of the proloculi ranged between 18 mm and 28 mm. The size range in Peneroplis sp. from Chuuk Island is slightly below or at the lower size range of megalospheric juveniles from the Mediterranean and the Gulf of Elat and thus does not support the presence of a third size class representing a potential schizont generation. The comparison, however, concerns peneroplids from different locations. Faber and Lee (1993) observed that the number of juveniles released from the parental test varied with size of the adult and, at least in the laboratory, ranged between 500 and 1500 individuals. In contrast, Schacko (1882) reported 118 juvenile embryos in Peneroplis proteus (d Orbigny), and, later, Winter (1907) depicted only,100 juvenile megalospheric gamonts present within the parental test of Peneroplis pertusus (Forskål). Our specimen from Chuuk Island contained 40 gamontic juveniles within the third to last chamber, but the first two chambers were already broken off the parental test. From the illustrations provided by Winter (1907), it is reasonable to assume that the two missing chambers contained approximately the same or slightly more juveniles than the third chamber. This would add approximately another 70 to 90 megalospheric gamonts to the 40 counted here, resulting in a total of 110 to 130 gamontic megalospheres. The number of juvenile offspring reported by Faber and Lee (1993) thus differs significantly from both Winter s observations and ours. It is not known, however, if this is caused by intraspecific differences in the reproductive biology between Peneroplis pertusus, P. planatus, orpeneroplis sp. As pointed out by Faber and Lee (1993), the number of juveniles released from the parental test varies with size of the parental test, where larger individuals contain larger numbers of offspring than smaller tests. In terms of a potential trimorphic life cycle in Peneroplis, this would result in a general pattern where large agamonts potentially contain larger numbers of megalospheric gamonts than parental schizonts that also produce megalospheric gamonts. The number of juveniles may therefore be indicative of a trimorphic life cycle that otherwise is particularly difficult to detect (Röttger and others, 1990). The small number of juveniles detected in our parental specimen thus argues in favor of schizogony as a potential reproductive mode. According to Lehmann and others (2006), schizogony may be the dominant mode of reproduction at some sites, at least in Trochammina inflata, and might explain the high densities of schizonts in natural populations of Heterostegina depressa (Röttger and others, 1990). MEGALOSPHERIC JUVENILES All juveniles recovered from the brood chamber were found to be fully calcified megalospheres composed of proloculus and an attached flexostyle. The flexostyle r juveniles within the brood chamber. 4, 5 Broken apertural face showing details of the irregular breakage patterns of the parental apertural face and densely packed juveniles. 6 Parental test after the brood chamber was manually broken to liberate calcified juveniles for further examination. 7, 8 Isolated juveniles with non-deformed, regularly calcified megalospheres consisting of prolocular chamber and attached tube-like flexostyle. 9 13, Megalospheric juveniles showing various types of test deformations. Deformations include test impressions on the lateral and peripheral wall of the juveniles. Patterns of test deformations in selected juveniles show that impressed test walls result from dense packaging within the brood chamber ofthe parental test. 17, 18 Dissected megalosphere showing the globular proloculus and with attached tube-like flexostyle. 14, 15 Irregular growth, test abnormalities, and deformations in adult tests of peneroplids from Chuuk Island. The specimen shows a twisted coiling axes deviating from the planispiral plane of coiling in the adult stage (14, see schematic axes) and aberrant coiling in the initial prolocular stage (15, see encircled marking) resulting in a 90u change of axes from a horizontal to a vertical coiling mode. Scale bars: 1, 2, 8, 14, mm; 3, 4, mm; 6, 7, 9 13, mm. Journal of Foraminiferal Research fora d 24/11/08 16:43:51 11

5 0 LANGER AND OTHERS envelops the proloculus in the equatorial plane and is approximately one half-coil in length (Pl. 1, Figs ). High magnifications of a dissected proloculus show that the wall structure of the megalosphere is composed of thin calcite needles typical of a miliolid (Debenay and others, 2000; Pl. 1, Fig. 18). The needles are bundled in fiber-like structures, resulting in a surface meshwork interspersed with pits that do not penetrate the wall of the proloculus or the flexostyle (see Pl. 1, Figs. 3 and 17 18). Descriptions of apparently early perforate growth stages (Winter, 1907; Hofker, 1930, 1951; Loeblich and Tappan, 1987) therefore might be only optical artifacts (Hottinger and others, 1993). Our findings clearly illustrate that the calcification of the megalospheric juveniles takes place within the parental test (Winter, 1907; Faber and Lee, 1993; Schaudinn, 1894a). This contrasts with the observations in Miliolina or Calcituba, where calcification takes place externally (Schaudinn, 1894a; 1895a). Prior to the calcification of the megalospheric juveniles, Winter (1907) observed that pseudopods within the parental test of Peneroplis pertusus dissolve the septa within the last few chambers to increase the room for the brood. The megalospheric juveniles isolated from the brood chamber of the adult test display variations in the size of internal proloculi diameter, ranging from 18 to 28 mm (n 5 26). Figure 3 on Plate 1 shows the megalospheric juveniles densely packed within the limited space of the brood chamber. Seven out of twenty-six megalospheric individuals (26.9%) exhibit various forms of deformation that appear to be inflicted by the neighboring tests as a result of close packaging (Pl. 1, Figs and 16). Abnormalities and test deformations have also been described and illustrated for P. pertusus by Schacko (1883) and Winter (1907). In certain cases where the developing juveniles suffer from extreme space limitations (e.g., within the innermost chambers of the parental test), the megalospheric proloculi may even show dwarfism (Winter, 1907). Both the size variation of the megalospheric proloculi and the test deformations are indicative of asynchronous calcification of juveniles within the parental brood chambers. A prominent example of asynchronous calcification is displayed in a megalospheric juvenile on Plate 1, Figure 11. The indentation visible results from an imprint of a neighboring test and can only be explained by time-shifted development of juveniles within the brood chamber, here described as asynchronous calcification of megalospheric juveniles. Calcification and maturation of juveniles have also been described and illustrated by Winter (1907) in Peneroplis. He considered the deformed abnormalities and variations in size of juvenile megalospheres to be the source of natural polymorphism in Peneroplis. Unlike Peneroplis, where juvenile calcification takes place within the parental test, those foraminifera, which calcify externally (Polystomella [5 Elphidium], Miliola), do not exhibit such a high percentage of polymorphism (Winter, 1907). We therefore conclude that microspheric agamonts produce non-uniform, size-variable, and highly heterogeneous offspring, placing serious constraints on the classic definition of three size classes (trimorphic life cycle) in Peneroplis. In different species of Peneroplis and apparently in Peneroplis sp. from Chuuk Island, the test deformations present in the juvenile megalospheres remained visible in adult test morphology (Winter, 1907; Schacko, 1883; Pl. 1, Figs ). In addition, pronounced test abnormalities (5 malformations) resulting from asexual reproductive processes (schizogony) were also described and illustrated by Geslin and others (2000) for Ammonia tepida (Cushman). High percentages of abnormalities are commonly considered indicative of environmental stress (e.g., pollution; Alve, 1991; Yanko and others, 1999; Geslin and others, 2000; Le Cadre and others, 2003; Le Cadre and Debenay, 2005). In addition, Boltovskoy and others (1991) noted that rapidly changing physical-chemical conditions of the environment can create deformed, aberrant specimens. The high percentage of deformed megalospheric juveniles present in the parental test examined here (26%) indicates that this is a natural phenomenon in populations of Peneroplis (Schacko, 1883; Winter, 1907). This ultimately has consequences for the interpretation of abnormal shell forms as bioindicators of environmental pollution or environmental stress. We acknowledge that our interpretation is based on a fortuitous finding of 40 juvenile megalospheres extracted from a brood chamber of an adult specimen of Peneroplis. Due to the rarity of the species, we were not able to demonstrate here that deformations in the proloculus persist in adults or that the rate of prolocular deformation is similar to that found in the adult population. However, the persistence of deformation has been convincingly demonstrated in other peneroplids from other pristine locations with extensive sampling and observations (Schacko, 1882, 1883; Winter, 1907). Our observations, together with previous studies, indicate that asynchronous calcification of juvenile megalospheres within the spacelimited brood chamber is the key mechanism driving the test deformation that leads to polymorphism in natural populations of Peneroplis. The release of megalospheric juveniles from the parental test was described and illustrated by Winter (1907) to be induced by the pseudopodia of the juveniles partly dissolving the parental test wall. The dissolution ultimately weakens the stability of the parental test and leads to predetermined ruptures and breakage points (Heron-Allen, 1915; Langer and Bell, 1995). In addition, active and vigorous movement of the densely packed juveniles within the brood chamber increases in the brood chamber until it probably exceeds the nominal tensile strength and eventually results in test rupture along the pre-dissolved sites. Test breakage primarily takes place along the sutures, on the apertural face, and along the peripheral test wall of the parental test. In the adult specimen studied here, the broken margins along the opened apertural face exhibited signs of dissolution, test breakage, and rupture (Pl. 1, Figs. 3 5), as described by Winter (1907). The irregular and somewhat erratic arrangement of juveniles within the brood chamber of the studied specimen did not display the sorted arrangement in rows of two or tetrads as described by Faber and Lee (1993) but rather followed the observations of Winter (1907), where juveniles selectively moved toward test openings to ultimately leave the parental test. However, the irregular arrangement of Journal of Foraminiferal Research fora d 24/11/08 16:43:51 12

6 ASYNCHRONOUS CALCIFICATION 0 juveniles as shown in Plate 1 (Figs. 3 5) might result from prior transport, treatment, or preparation for SEM. CONCLUSIONS Our study on megalospheric juveniles present within a brood chamber of Peneroplis leads to the following principal conclusions. 1. Natural populations of Peneroplis sp. produce nonuniform and highly heterogeneous offspring having a significant range of proloculus sizes. This places constraints on the classic definition of three size classes (trimorphic life cycle) in Peneroplis. 2. Significant percentages of megalospheric juveniles present in the parental test of Peneroplis commonly exhibit various forms of test deformation. Juvenile test deformities can be carried through into the adult (Schacko, 1882, 1883; Winter, 1907; this study). Our study indicates that this is a natural phenomenon in populations of Peneroplis, which is suggested here as a representative of those types of foraminifers in which juvenile calcification takes place within the parental test. This ultimately has consequences for the interpretation of abnormal shell forms as bioindicators of environmental pollution or environmental stress. 3. The size variation of the megalospheric proloculi and the test deformations are indicative of asynchronous calcification and are a potential source of natural polymorphism in Peneroplis. ACKNOWLEDGMENTS We gratefully acknowledge the support of Phil Forte, who collected the foraminiferal sample material around Chuuk Island, and Joan Bernhard, for the organization of the sample material, for logistic support, and for comments on the manuscript. We appreciate the information, constructive comments on an earlier version of the manuscript, and the helpful review provided by Susan Goldstein on issues of foraminiferal life cycles. We also acknowledge the stimulating comments provided by three anonymous reviewers and the editorial help of Charlotte Brunner. This study was supported by a grant from the Deutsche Forschungsgemeinschaft awarded to ML (La 884/5-1, 5-2) and by a scholarship from the Egyptian Ministry for High Education to WM. D. Kranz made the drawing of the reconstruction. REFERENCES ALVE, E., 1991, Benthic foraminifera in sediment cores reflecting heavy metal pollution in Sorfjord, western Norway: Journal of Foraminiferal Research, v. 21, no. 1, p BOLTOVSKOY, E., SCOTT, D. B., and MEDIOLI, F. S., 1991, Morphological variations of benthic foraminiferal tests in response to changes in ecological parameters: a review: Journal of Paleontology, v. 65, p BRADSHAW, J. 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