Origin of double and multiple tests in benthic foraminifera: observations in laboratory cultures
Introduction
Since the beginning of this century, multiple tests have often been reported in the literature as `twin tests' or `Siamese twin tests' in Recent benthic foraminifera (Rhumbler, 1911; Earland, 1934; Buchner, 1940) and planktonic foraminifera (Earland, 1933, Earland, 1934, Earland, 1936; Boltovskoy, 1966; Boltovskoy and Boltovskoy, 1970; Boltovskoy and Wright, 1976), but their origin is often considered as obscure (Boltovskoy, 1982).
Various hypotheses are proposed to explain the formation of abnormal tests including twin tests: salinity stress (Ayala-Castañares and Segura, 1968; Zaninetti, 1982; Almogi-Labin et al., 1992), accumulation of organic matter (Caralp, 1989), or more recently, pollution (Sharifi et al., 1991; Yanko et al., 1994; review in Yanko et al., 1998; review in Geslin et al., 1999). As a result, abnormal tests are considered as bioindicators of environmental stress. However, these hypotheses are rarely controlled by laboratory experiments, though these observations on laboratory cultures are essential before using morphological abnormalities as environment or paleoenvironment indicators. Moreover, different types of morphological abnormalities can be observed, and twin tests might have a special significance. With a view to use them as bioindicators, it is necessary to understand the mechanism of their formation during ontogeny.
The first purpose of this work is to present the morphological diversity of double tests, primarily from the observation of a few species capable of reproducing in laboratory cultures, but also from the observation of some specimens of the same species collected in natural environments. The second purpose is to explain how various double tests develop, from the observation of many juvenile forms in our laboratory cultures. Finally, the influence of a few environmental parameters on double tests formation will be discussed. The conditions in which such malformations occur in various environments are not, however, the primary subject of this paper. A statistical analysis of malformed individuals either in natural environments or in laboratory cultures, is thus not given here.
In foraminifers which reproduce by gamontogamy (union or pairing of two or more gamonts with the subsequent production of gametes and their fusion), two or more gamonts may join together by their umbilical sides and form a gamontocyst or `nuptial chamber' which fully surrounds both joined tests (Lee et al., 1991). Such grouping of two gamont tests is only temporary and will also not be studied here.
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Material and methods
Specimens of Bolivina sp. collected in Rangiroa (Tuamotu archipelago, French Polynesia; Table 1) and kept in the Laboratory of Zoology of the University of Geneva (Switzerland) were transferred into cultures in the Angers laboratory in November 1996.
Between April 1997 and April 1998, various samples of sediments were collected in Bourgneuf Bay and at Pornic (Loire-Atlantique, France; Table 1), and in the rocky intertidal zone of Ker Châlon beach in front of the LEBIM (Laboratoire d'Etude des
Results
Laboratory cultures enabled the observation of many normal juveniles of Ammonia tepida (Plate I, 1 and 2) and Elphidium crispum (Plate I, 3) born by schizogony (asexual reproduction or multiple fission). Cultures of Ammonia tepida in hypersaline conditions (salinity = 50‰) provided more than hundred abnormal juvenile tests. In such conditions of salinity, nearly half of the 12 to 24 young of a brood showed some abnormalities very early in their ontogenetic development. About half of these
Discussion
This study is the first report of detailed observations of embryonic and juvenile stages of benthic foraminifera with abnormalities. It enables a better understanding of the formation of double or multiple tests. The comparison between our results and those of Röttger and Spindler (1976) concerning abnormalities in the early ontogenetic development of Heterostegina depressa, also enables us to put forward hypotheses on the future development of some juvenile tests of Ammonia tepida described in
Conclusions
Double tests of foraminifers are not always Siamese twin tests. They can result from one juvenile which undergoes early ontogenetic perturbations leading to the formation of second or third additional chambers. Other cases are due to a true twinning and probably result mostly from embryo or juvenile joining. Environmental conditions seem to influence the formation of double tests. They probably act at the cellular level by slowing down some metabolic processes essential to a normal ontogenetic
Acknowledgements
The authors dedicate this work to the memory of E. Boltovskoy. We ask R. Röttger to accept this work as a mark of gratitude for his numerous works which partially suggested our interpretation. We thank J. Pawlowski for his enthusiastic instruction on the culture of foraminifera, as well as F. Redois and E. Geslin for specimens collected in natural environments, E. Goubert for numerous helpful scientific discussions and M. Baslé for his warm welcome into his Laboratory of Histology and
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