Earth-Science Reviews 46 Ž1999. 167–185 www.elsevier.comrlocaterearscirev Colonization of new habitats by benthic foraminifera: a review Elisabeth Alve ) Department of Geology, UniÕersity of Oslo, P.O. Box 1047 Blindern, N-0316 Oslo, Norway Abstract Colonization of new habitats, which have been established as a result of a catastrophic disturbance of the environment, is one of the characteristic repetitive events throughout the Phanerozoic. In recent years, much attention has been paid to investigations focusing on biological recovery of benthic habitats severely disturbed by human activity. In order to improve our environmental and stratigraphical interpretations of such events, we need a more thorough understanding of the processes involved in colonization by one of the most abundant and useful fossil groups, the benthic foraminifera. The present review focuses on processes governing benthic foraminiferal dispersion and colonization patterns in modern environments. For benthic foraminifera, the only active dispersal mechanism is through self-locomotion on or within the sediment and this is considered to be efficient over short distances only. Several passive dispersal methods have been suggested but two seem to be of more general importance. These are dispersal through release and transport of embryonic juveniles and passive suspension and transport of various growth stages. Both are probably important for most benthic foraminifera but the former is likely to be the main mechanism for attached, tubular and larger foraminifera, which are not easily entrained at a later life stage. The latter seems to be a more important dispersion mechanism for benthic foraminifera than previously realized. The colonization rate of soft-bottom substrates is closely related to the hydraulic regime in, and the transit time from, the source area inhabited by species capable of colonizing the new habitat Žas long as food and other environmental characteristics are not limiting factors.. The transit time depends on the speed of the transporting medium and the distance from the source area. There seems to be two end-processes which can operate during the colonization, depending on whether physically induced or biological processes are allowed to dominate. They are characterized by different colonization patterns. In high energy environments Žbottom current velocities often ) 20 cmrs., a short transit time may cause the major components of the nearest ambient seafloor assemblages to colonize the new habitat within days. In this case the colonization is simply through a physical transfer of parts of the source community to the new habitat, allowing no time for pioneer, opportunistic assemblages to develop. In low energy environments Žbottom current velocities generally - 10 cmrs., the transit time is long for most species. Here, colonization follows the classic metazoan successional pattern with an initial, high abundance pioneer assemblage strongly dominated by small opportunists followed by development of assemblages with increasing numbers of specialized species and recovery can take from one to several years. Initial lack of food Že.g., volcanic ash. or ‘hostile’ substrate properties Že.g., recently reoxygenated or severely contaminated sediments. may delay colonization by months or even years. Small, infaunal species Žboth calcareous and agglutinated. are among the first and most successful colonizers of soft bottom habitats from shallow waters to the deep sea. Throchospiral ) Fax: q47-22-85-42-15; E-mail: elisabeth.alve@geologi.uio.no 0012-8252r99r$ - see front matter q 1999 Elsevier Science B.V. All rights reserved. PII: S 0 0 1 2 - 8 2 5 2 Ž 9 9 . 0 0 0 1 6 - 1 168 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185 agglutinated taxa are among the most abundant colonizers on deep sea hard substrates. q 1999 Elsevier Science B.V. All rights reserved. Keywords: benthic foraminifera; meiofauna; dispersal; colonization; succession; recovery 1. Introduction Environmental disturbances have various degrees of destructive impacts on benthic communities and severe, large-scale disturbances can lead to defaunation of existing sediments or establishment of new, unoccupied habitats. Habitat disturbance or destruction may also cause species extinction and this is most likely to happen in areas with high numbers of rarely occurring endemic taxa ŽCulver and Buzas, 1998.. The initial faunal recovery processes and subsequent succession following major disturbances are referred to as colonization ŽLevin and DiBacco, 1995. and this is the topic considered in the present paper, focusing on benthic foraminifera. Small-scale disturbances Že.g., fishes stirring up the sea bottom, animal tracks, faecal casts. of already occupied habitats are not included. However, several aspects of the colonization processes following large-scale disturbances also have implications for our understanding of the dynamics and recovery patterns of small-scale disturbances and are therefore of general interest and applicability. In the marine environment, severe disturbance causing an appearance of new habitats ready for colonization by benthic organisms is generally due to one of the following three causes: Ž1. Sudden depositional events such as turbidity current deposits Že.g., flysch. and other mass-flow deposits which typically occur along continental margins and in fjords, deposition of submarine volcanic ash layers, and anthropogenic dumping activity. Ž2. Sudden exposure of new azoic sea floor which may be due to Ža. natural or human induced erosion such as areas where the surface sediments have been ‘stripped’ off during mass-flow transport, Žb. benthic storms Ži.e., strong currents., Žc. icebergs ploughing into the sea bottom, or Žd. in more recent years, anthropogenic dredging in coastal areas or possible deep sea manganese nodule mining. Ž3. Exposure of new azoic sea floor due to an environmental change such as retreating ice fronts and oxygenation following anoxic events Že.g., sapropels and reoxygenation following organic matter pollution abatement., whereas marine transgressions probably operate too slowly to provide a lag between exposure and colonization. In the marine geological record of sudden depositional events there will be a succession from Ža. a pre-disturbance deposit to Žb. a disturbance deposit followed by Žc. the post-disturbance deposit. Units a and c may contain in situ fossils whereas unit b will either be unfossiliferous Že.g., volcanic ash layer. or contain transported fossils Že.g., turbidites, although they may contain post disturbance, infaunal taxa which utilize organic matter in the turbidite layer ŽRathburn and Corliss, 1994... The marine geological record of sudden exposure of new azoic sea floor may be represented by disturbance deposits without fossils Že.g., as a result of anoxia or ice in contact with the sea floor. followed by post-disturbance deposits Žwith fossils.. However, events such as benthic storms, and dredging may not leave a disturbance deposit but simply erode into older fossiliferous deposits Žin which nothing is currently living. upon which new deposits Žwith fossils. subsequently accumulate Ži.e., create an hiatus.. From a geological point of view, important paleoenvironmental information can be obtained by high resolution studies of sediments deposited just before, during, and after the disturbance event Že.g., Rohling et al., 1997. but detailed paleoenvironmental interpretations can only be achieved through analyses of the fossil assemblages. In many cases, benthic foraminifera represent the best fossil group for study because they are usually the most abundant benthic organisms preserved. While the present review focuses on biological observations of short-term Žin a geological perspective. colonization processes in modern environments, geological investigations are the only which can provide more complete information about long- E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185 term processes. However, in order to perform detailed interpretations, it is necessary to establish whether the sedimentary sequence is complete Ži.e., without hiatus. and whether the benthic community recorded just after the event is redeposited or in situ. In the latter case, valuable paleoenvironmental information can be obtained only if we know how to recognize and interpret foraminiferal colonization patterns and this has to be based on a thorough understanding of foraminiferal biology. Marginal basins, such as the Mediterranean Sea, which have undergone alternation between oxic and anoxic conditions leading to sapropels Že.g., Rohling et al., 1997; Schmiedl et al., 1998 and references therein. present additional problems of scale compared with the observations of modern processes. Questions which might be posed include the following. Ø What is the source area of the colonizing species? Are they from oxic refuges within the basin or are they introduced from the adjacent open ocean? If the latter is the case, was the post-sapropel circulation the same as the present-day anti-estuarine circulation in the Mediterranean; this would present a major problem for transport of foraminifera. Ø How rapidly does recolonization take place in such previously hostile habitats? Is it diachronous or near instantaneous on a geological timescale? Ø How long does it take for the colonizing assemblages to reach comparable diversity and equatability levels to those of the pre-sapropel assemblages after re-establishment of well oxygenated conditions? These are questions that future studies of sapropels might address in the light of the data from modern environments reviewed in this paper. In addition to these more traditional geological applications, analyses of both live and dead benthic foraminiferal assemblages have been shown to have a good potential for studying anthropogenically induced disturbance and recovery effects in marginal marine environments Žreviewed in Alve, 1995a; for discussion of environmental change using benthic foraminifera as proxies, see also Murray, in press.. Consequently, detailed information concerning the dynamics of benthic foraminiferal dispersal, colonization, and recolonization patterns is also important from an environmental management point of 169 view, for interpreting and understanding the ecological implications of, and recovery from, anthropogenically induced environmental stress Že.g., Ellison et al., 1986.. This concerns both short-term biological monitoring evaluating impacts of physical and chemical disturbance and environmental stratigraphy investigations ŽAlve, in press. recording impacts over a longer time period Že.g., back to pre-industrial times.. There are numerous studies of benthic metazoan colonization patterns both in lacustrine and marine environments. The question arises: do benthic foraminifera, being protists, follow the same patterns of dispersal, colonization, and subsequent succession as metazoans? At present, there is only limited understanding of the processes and biological dynamics of benthic foraminiferal dispersal and colonization patterns, and most publications so far have primarily focused on the speed of colonization rather than on the processes involved Že.g., see active vs. passive distinction below.. This review addresses the principal environmental and biological processes which seem to control dispersal and colonization of modern foraminiferal assemblages in newly established, azoic habitats in comparison with what is known of the patterns for marine benthic metazoan invertebrates. 2. Dispersion The dispersal phase of macrobenthic life histories in the marine environment commonly occurs through passive spreading of planktonic larval stages advected by currents Že.g., Grassle, 1978. and recolonization studies have shown that pelagic larval recruitment can account for 70–90% of all individuals, especially of polychaetes and molluscs ŽMcCall, 1977; Santos and Simon, 1980; Diaz-Castaneda et al., 1993.. However, movement by adults and juveniles through the water column have also been reported Že.g., Chandler and Fleeger, 1983; Kern and Bell, 1984.. In contrast to the macrofauna, most meiofaunal taxa lack pelagic larvae and they are known to enter the water column either passively through entrainment, or actively through swimming Žfor review, see Palmer, 1988a; Thistle et al., 1995.. Since benthic foraminifera do not have swimming 170 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185 abilities, active entry to the water column is not possible. Consequently, for most motile benthic foraminifera, there are theoretically four different ways of dispersion Žthree passive, one active.: Ž1. release to the water column of gametes, zygotes, or of embryonic agamonts or gamonts following sexual and asexual reproduction, respectively; Ž2. adaption to a meroplanktonic juvenile life stage with subsequent passive spread by currents; Ž3. self locomotion along the sea floor; or Ž4. through passive Žphysically or biologically induced. entrainment into the water column and subsequent transport of different growth stages. For attached species, the former two are most likely. Shallow water taxa may also be transported by floating objects or larger marine animals Žfor discussion, see Myers, 1936., by birds, and by human activity ŽLessard, 1980; Witte, 1994; McGann and Sloan, 1996.. 2.1. Release of propogules following reproduction Dispersal of foraminifera can involve the release of flagellate gametes to the seawater or the production of amoeboid gametes ŽGrell, 1967.. Of the foraminifera for which aspects of reproduction has been studied, the majority have a life cycle in which gametogenesis produces numerous biflagellated, free-swimming gametes that are released directly into the surrounding seawater ŽGoldstein, 1997.. However, gametes probably do not live long enough Žhours to one or a few days?. to represent a primary dispersal mechanism, and the farther they travel, the lower the density of gametes and likelihood of fertilization ŽS.T. Goldstein, pers. commun., 1998.. Also, in some species Že.g., Spirillina ÕiÕipara, Patellina corrugata., the haploid gametes are confined at all times within an attached cyst implying that dispersal cannot be accomplished in the gamete phase of their life-cycle ŽMyers, 1936.. On the other hand, distributional and seasonal reproduction studies of the shallow water species Trochammina hadai suggest that the sexual generation is more efficiently dispersed than the asexual generation because the gametes are released to and advected by the bottom water ŽKitazato and Matsushita, 1996.. Some shallow water species which live in close association with algae have adapted to the seasonally fluctuating intensity of turbulent coastal zones by alternating the different stages of their life cycles between the sediments and epiphytally on algae ŽErskian and Lipps, 1987. or alternate between intertidal and subtidal habitats ŽWalker, 1976.. Both involve passive dispersion of adult individuals as well as of embryonic juveniles. Some living larger foraminifera can withstand very high current velocities of 3–4 mrs ŽSeverin and Lipps, 1989., suggesting that they are not easily entrained. This is probably due to a combination of their large test size and ability to cling to the substrate with their pseudopodia. Additionally, the fact that larger foraminifera recolonize reef habitats following defaunation caused by for instance a cyclone ŽCollen, 1996., suggests that they re-enter these habitats as embryonic juveniles following reproduction in adjacent areas. This mechanism probably also plays an important role in the dispersal of many attached taxa since they are not easily entrained but still have shown to be among the most successful colonizers of hard substrates Žsee Section 4.. It seems that dispersal by gametes may be efficient over small distances Žmeters to hundreds of meters., whereas zygotes and embryonic juveniles, which probably have a density comparable to seawater and therefore are easily transported, are more prone to disperse over larger distances. The first few chambers of juvenile benthic foraminifera are often thin and transparent and capable of increasing their flotation by extending numerous filose pseudopodia, so there is no reason why they should not remain pelagic for days or possibly weeks ŽMyers, 1936.. However, more studies are needed, both for epifaunal and particularly for infaunal species which probably reproduce within the sediments Ži.e., no immediate release of embryonic offspring to the water column; e.g., Frankel, 1972., before further conclusions concerning the importance of this mode of dispersal can be drawn. 2.2. Meroplanktonic life stage Occurrences of living benthic foraminifera in the water column has led several authors to suggest that some species have a meroplanktonic Ži.e., temporary planktonic. stage in their life cycle we.g., BoliÕina Õaughani ŽLidz, 1966.; Brizalina lowmani ŽHueni et al., 1978.; various tide-pool species ŽWalker, 1976.x. To the authors knowledge, a meroplanktonic life E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185 stage has so far been proved in five genera only ŽTretomphalus, Tretomphaloides, Millettiana, Cymbaloporetta, and Rosalina. which build a float chamber for use during their planktonic stage ŽLoeblich and Tappan, 1987; Ruckert-Hilbig, 1983.. This ¨ is most probably an efficient dispersal method but whether or not it is an adaptive strategy in species other than those with a float chamber is left to be proved. Consequently, until more information is available, no conclusions can be drawn concerning the more general importance of this mode of dispersion. 2.3. Self locomotion In most environments, self locomotion along the sea floor is probably a less efficient and very slow process because foraminifera Žthose investigated so far. move with a speed of - 1 mm per hour Žtypically deep-sea and bathyal species, e.g., Weinberg, 1991; Hemleben and Kitazato, 1995; Bornmalm et al., 1997. up to a few millimeters per hour Žsome shallow water species, e.g., Kitazato, 1988; Wetmore, 1988. and because their movements are known to be random Že.g., Jepps, 1942; Murray, 1963., implying that they do not actively track a new habitat. However, tank experiments have indicated that colonization of new habitats through self locomotion may occur over small distances of some tens of centimeters within 7 days ŽSchafer and Young, 1977.. Consequently, due to the random and relatively slow movement, this method is probably most applicable to active colonization of small-scale disturbed patches. 2.4. PassiÕe entrainment and transport of growth stages It is commonly known that once in suspension, sediment particles can be carried for long distances even at low velocities Žrelative to the velocities needed to entrain them. and their physical behaviour is mainly a function of the settling velocity. It is reasonable to assume that the same holds true for benthic foraminiferal tests and consequently, one of the most important factors for dispersal of foraminifera of various growth stages is the critical shear velocities required to entrain Žsuspend. the 171 foraminifera in the source area, as well as the survival time of the entrained individuals. Compared to other marine, major meiofaunal groups Žcopepods and nematodes., living benthic foraminifera seem to be the least easily suspended ŽSherman and Coull, 1980.. This is not surprising, since copepods are agile swimmers and nematodes lack clinging appendages Že.g., Palmer and Molloy, 1986.. As pointed out by Severin and Lipps Ž1989., a living foraminiferan can use its pseudopodia to anchor itself to the substrate, whereas entrainment of a dead test is simply a function of the size, shape, and density of the test in relation to the bottom current velocity. Furthermore, in shallow water habitats where wave action and turbulence impose a physical stress on the organisms living there, different adaptive strategies Žattachment, avoidance, test robustness. are developed by the benthic foraminifera to withstand transport Žsee discussion in Palmer and Molloy, 1986; Erskian and Lipps, 1987.. Despite all this, living benthic foraminifera have been reported to occur abundantly in the water column and, as discussed in Section 3, several studies have shown that appearance of diverse, abundant assemblages on new substrate can happen so quickly that settlement of various growth stages, rather than settlement Žand subsequent growth. of recently produced offspring, is more likely to have been the major mechanism. There is hardly any information on what bottom current velocities are needed to entrain motile living benthic foraminifera, but some information exists concerning dead tests. Flume experiments have shown that the mean traction velocities for dead tests of common, free living, small Žnominal diameter 0.32–0.52 mm. species such as Quinqueloculina cf. Q. Õulgaris, Islandiella subglobosa, Bulimina aculeata, and UÕigerina peregrina are as low as 5.1, 5.4, 6.6, and 9.2 cmrs, respectively ŽKontrovitz et al., 1978.. Consequently, bottom currents of at least 10–15 cmrs are probably needed to entrain living, adult benthic foraminifera as long as their pseudopodia are active and ‘clinging’ to particles outside the test. On the other hand, foraminifera associated with fluffy sediments, e.g., phytodetritus Žwhich is resuspended by bottom currents exceeding about 7 cmrs Žat 1 m altitude; Lampitt, 1985.. are probably more easily entrained and thereby have a higher dispersion potential. Flume studies indicate that benthic 172 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185 foraminifera suspended in bottom flows of about 4–9 cmrs can passively be transported into fiddler crab burrows ŽDePatra and Levin, 1989.. In addition to physically induced entrainment, biological disturbance Že.g., fiddler crabs, fish, flushing of burrows by infaunal macrobenthos. can also suspend benthic foraminifera. For example, passive transport of foraminifera and other meiofauna has been shown to be doubled due to fish activities ŽPalmer, 1988b.. Due to the fact that suspension transport of both dead and living benthic foraminifera has important implications for the taphonomic aspect of palaeoecological interpretations, comments will be given on transport of dead tests as well as on living individuals. 2.4.1. Suspension transport of dead indiÕiduals Storms have been shown to play an important role in the suspension transport of benthic foraminifera because there are several records of benthic foraminifera in plankton samples taken during or after such events but in several cases the majority of individuals recorded are dead. For example, plankton samples Žnet opening 76 mm. collected from the sea surface and 10 m below the surface after a period of storms in the English Channel had a ‘high content’ of dead benthic foraminifera, but only very thinwalled types, showing a pronounced size sorting Žmajority 150–200 mm in length or diameter according to shape. were recorded ŽMurray, 1965.. Based on the presence of only scattered live Žstained. individuals Ž) 76 mm. of benthic foraminifera in surface water Ž40 m below the surface. samples and samples from 5 m above the sea floor, the Western Approaches and the Western English Channel, Murray et al. Ž1982. concluded that, even though dead tests were abundant, suspension transport is not a widespread means of dispersal of live benthic foraminifera in that area. Suspension and transport of ‘probably dead’ benthic foraminifera has also been reported from the North Sea where Leptohalysis scottii Žas Reophax . occurs regularly during winter and spring in plankton tows Žmesh size 270 mm. collected at 10 m water depth ŽJohn, 1987.. Myers Ž1936. noted that ‘‘it is not uncommon to find even adult Foraminifera in plankton taken from the waters of the littoral zone’’. During a 16-month survey of sediment traps, suspended at 125 m water depth on a mooring in 400 m of water on the eastern side of the USA, Brunner and Biscaye Ž1997. recorded average fluxes of 155 benthic testsrm2 per day from the shelf to the slope during relatively calm spring and summer periods, whereas fluxes of 29,000 and 50,000 testsrm2 per day were found in connection with a winter storm. The transported benthic taxa were typical of the continental shelf in that area and they ranged in size from about 30 to 845 mm, with a median size of 81–98 mm. Only a few living individuals were present in the whole data set ŽBrunner, pers. comm., 1998.. Overall, this shows that transport of benthic foraminiferal tests by water currents may be substantial. 2.4.2. Suspension transport of liÕing indiÕiduals In the above mentioned records, nearly all the transported benthic foraminiferal tests were dead. Considering the fact that in most marine environments, the densities of dead tests are generally one to several orders of magnitude higher than those of living individuals Že.g., Scott and Medioli, 1980; Alve and Murray, 1997., it is not surprising that they are also more common in the water column following resuspension of surface sediments. However, living individuals, representing various growth stages, have also been reported from the water column. For example, Arnold Ž1964. collected some of the individuals Ž Spiroloculina hyalina. used in his culture studies ‘by a plankton net towed obliquely from the surface to a depth of 140 ft’ in an area off La Jolla where the water depth ranged from 120 to 160 ft. Lidz Ž1966. found living individuals of BoliÕina Õaughani in plankton tows Ž62 mm mesh. down to 15 m below the sea surface 0.5–3.5 km offshore of California and also mentioned unpublished records of living species of both BoliÕina and BoliÕinita in plankton tows from the ‘deep ocean water’ in the Catalina Basin Ž) 50 km offshore.. Living individuals of 12 benthic species were recorded in plankton tows Ž72 mm mesh. collected from the surface water just off Bodega Head, California, in water depths to about 25 m ŽLoose, 1970.. The assemblage composition was the same as that living in the intertidal community of the area but the size range of the specimens was somewhat smaller Ž250–500 mm diameter.. No quantitative abundance data were available, but due to the fact that a fair E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185 number of living individuals were found even though ‘the conditions under which the tows were made probably represent a near minimum for energy and turbulence’, it was inferred that ‘great numbers of foraminifera could be transported’ during storms and high energy conditions. Furthermore, in the Gulf of Mexico, living individuals of Brizalina lowmani Ž) 400 individualsrm3 . were recorded in plankton tows collected at 0–25 m water depth from the coast and up to several tens of kilometer offshore ŽHueni et al., 1978.. In a colonization experiment performed in relatively shallow water Ž11–19 m. in the western Baltic Sea, elevated colonization platforms Ž1.5–5.0 m above the sea floor. were used to prevent active locomotion of the foraminifera up and into the colonization trays ŽWefer and Richter, 1976.. Samples were collected monthly and the first recorded living individuals were of intermediate size Žabout 200 mm., i.e., no juveniles and no adults, implying that the primary dispersion of the foraminifera was through suspension and lateral transport of individuals of intermediate growth stages. Both calcareous and agglutinated forms were present but Elphidium excaÕatum was by far the most abundant, and live individuals of E. excaÕatum Žsize: 125–200 mm. were also recorded in the water at that site. A nice example showing that even big Žnearly 1 mm in diameter. taxa can be suspended, transported into a new habitat, and continue to live there, was shown in a colonization experiment carried out in Sagami Bay, off Japan, at 1445 m water depth ŽKitazato, 1995.. The sediment in this particular colonization box consisted of artificial substrate made of silt-sized glass beads. After 1 year of colonization, a large individual of AlÕeolophragmium adÕena with glass beads incorporated into the five last chambers Žout of 11 chambers in the last whorl. was recorded showing that it was alive and in its adult form when it was transported into the colonization box. Another part of the same experiment included colonization in two boxes with defaunated ambient sea floor mud. One was open, whereas the other was covered with a plankton net Ž90 mm mesh. to exclude larger individuals from colonizing. Both shallow and deep infaunal taxa colonized the open box, whereas no stained foraminifera were found in the box covered by the plankton net. Kitazato concluded that the 173 individuals probably had not entered the colonization boxes as either zygotes or juveniles but had been suspended and transported into the new habitat in connection with benthic storms or possibly through bioerosion by deep-sea fish. However, the possibility that the plankton net had been clogged by sediment and thereby decreased the efficient mesh size, cannot be excluded. The cited examples have shown that suspension transport of individuals up to several hundred microns is not uncommon and that the transported living individuals often represent the dominant species inhabiting the sediments in the source areas. We shall return to this point in the discussion of colonization patterns. The processes which lead to colonization Ždispersion, transport, settling. operate all the time in marine environments and normally they contribute to the changing pattern of species distributions and variability in their abundance through time. However, the difference between ‘normal’ conditions and colonization of azoic Žempty space. sediment is that in the former the introduced individuals have to compete with the pre-existing fauna whereas in the latter this does not apply, at least in the initial stage. 3. Colonization of soft bottom substrates Characteristic features of the dominant, metazoan early colonizers include high reproduction capacity and short life cycles Žr-strategistss opportunists. enabling efficient colonization Že.g., Koskenniemi, 1994.. The following specialization stage is characterized by species with lower invasion ability, they tend to have longer life cycles, and habitat selection mechanisms are increasingly important to determine the faunal distribution ŽK-strategistss equilibrium species.. Some species occur later in the environmental development due to initial lack of suitable habitats and the impact of the species’ dispersion ability on the community structure decreases dramatically as more specialized species are introduced ŽKoskenniemi, 1994.. The importance of species dispersal ability at the beginning and the increasing role of the habitat Žand species interactions. later in the succession has been shown for terrestrial invertebrates Že.g., Huhta, 1971. as well as for macrozoobenthos Že.g., Koskenniemi, 1994.. 174 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185 For benthic foraminifera, the current state of knowledge is to a larger extent based on experiments than on field observations. Recent studies Že.g., Smith, 1985; Kukert and Smith, 1992; Snelgrove et al., 1995. have shown that several meio- and macrofaunal colonization experiments have been fraught with artifacts due to hydrodynamic effects and the isolation of the experimental substrate from the ambient sediment by the sides and floor of the trays. However, the present review has not attempted to evaluate possible artifacts concerning the design of the cited experiments. Several of the colonization experiments dealing with benthic foraminifera have focused primarily on ecological aspects rather than the colonization process proper. In these studies, information about the colonization patterns has been obtained as a spin-off and quantitative faunal data of the experimental and ambient Ži.e., nearby in situ. assemblages are not always available. In several cases, purely sand-sized particles Ži.e., no mud. have been used in some of the colonization trays, whereas other trays have contained ambient sea floor sediments which have been defaunated, mostly by freezing. Some of the pure sand experiments will be discussed together with studies of sediments with characteristics beyond the ‘normal’ marine range ŽSection 3.2. because the well-established positive correlation between mud and organic matter implies that pure sand represents an extremely nutrient deficient habitat and, as such, is not representative of most marine environments Žfor macrofaunal responses to colonization in enriched versus unenriched sediments, see, e.g., Snelgrove et al., 1996.. The same applies to recently deposited volcanic ash layers. Studies concerning anthropogenic dump sites and colonization following anoxic events are also discussed in Section 3.2 because they initially represent chemically hostile habitats. 3.1. Azoic ‘normal’ marine sediment Experimental studies in coastal shallow water areas have shown that the initiation of colonization and even establishment of assemblages with densities and a faunal composition comparable to that of the surrounding ambient benthic assemblages may occur in only a few days to weeks. For example, Schafer Ž1976. reported that re-establishment of the major species occurred in colonization frames only 2 days after emplacement at 13 m water depth in Nova Scotia. In addition to the colonization of the surrounding sea floor species, a strongly increasing absolute abundance of living Ammonia beccarii and Elphidium spp., which are characteristic infaunal species of the more shallow areas, occurred a few days later, just after a hurricane had passed. There was no increase of the typical infaunal ambient species, Eggerella adÕena, following this event. The increase in only the shallower water species was directly attributed to disturbance effects caused by the hurricane. At 65 m on the shelf off New Jersey, Ellison and Peck Ž1983. found that defaunated ambient sediments Žmoderately well-sorted, medium–fine sand. were completely colonized 10 weeks after emplacement, and the faunal composition was comparable with that after 43 weeks. In the same way as for the shallow water studies, the colonization occurred in proportions similar to that of the surrounding ambient fauna. There was no particular difference in the faunal composition or density between the 0–1, 1–2, and 2–3 cm levels in the sediments, and it was inferred that colonization on and into the sediment proceeded nearly simultaneously. A similar pattern was recorded after 6 weeks in a colonization experiment Žopen mud-filled box. conducted at 125 m water depth off Florida ŽBuzas et al., 1989.. The cited examples show that in shallow water coastal and inner shelf areas, the assemblage composition and faunal density may rapidly Žwithin days to weeks. approach those of the ambient, surrounding sea floor. In these instances, the major operating mechanism seems to be simply a physical transfer of parts of the surrounding sea floor assemblages into the colonization trays, leaving no time for opportunistic, pioneer species to flourish. This nearly instantaneous dispersal mechanism probably has important implications for maintenance of the homogeneity of faunal compositions in such areas. But what mechanisms operate in calm, physically less disturbed areas Že.g., fjords and the deep sea.? Colonization experiments have recently been carried out at 55–63 m water depth in different, well oxygenated, parts of the Oslo Fjord, Norway, to test macro- and meiofaunal responses to various concen- E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185 Fig. 1. Numerical density Žmean values and SD for replicates. of live Žstained. benthic foraminifera in ambient seabed sediments and colonization boxes Žsurface 0–5 cm. from three stations in the Oslo Fjord, Norway. trations of heavy metals ŽAlve and Olsgard, in press; unpublished data.. As a spin-off from these experiments, information has also been obtained concerning colonization patterns of benthic foraminifera Ž) 63 mm fraction.. Bottom current velocities in these areas are generally around 2 cmrs but higher values can occur, particularly in connection with deepwater renewals ŽEyvind Aas, pers. comm., 1998.. Data presented here represent analyses of three replicate cores Žsurface 0–5 cm. collected from colonization boxes Žcore diameter 57 mm. and three from the adjacent sea floor Žcore diameter 69 mm. at each of three different stations. The colonization devices consisted of 1.5 = 1.5 m aluminium frames, each containing 16 propene plastic boxes Ž29 = 32 = 13 cm height.. The three Žof the 16. boxes, from each frame, which were sampled for the foraminiferal analyses presented here were filled Žto 2 cm below the brim. with frozen, defaunated, ambient sediments Žthe other boxes had ambient or contaminated sediments and will not be discussed here.. The frames were left on the sea floor to colonize for 6 Žareas B and C. and 7.5 Žarea 1. months. This experimental design isolates the colonization sediments from the surrounding sediments. It therefore represents a closer analog to larger scale disturbances followed by colonization of azoic sediments than if there had been an 175 open connection to the surrounding sediments. This would have facilitated direct invasion by neighbouring, free living organisms. At two sites Žareas B and C., the numerical density was significantly lower in the colonization boxes compared to the ambient sea floor assemblages, whereas the difference was not significant at the third site Žarea 1; Fig. 1.. Furthermore, the number of species was significantly lower and Stainforthia fusiformis was 23–40% more abundant in the colonization boxes compared to the ambient fauna ŽFigs. 2 and 3.. This shows that the small, infaunal, opportunistic S. fusiformis was the most successful colonizer and that 6–7.5 months were not enough, in this low energy environment, for recovery of the community structures to ambient levels. Consequently, it seems that different dispersal and colonization patterns operate in high and low energy environments, and that only the latter opens for opportunistic, pioneer species to flourish. In area C, living tubular foraminifera, primarily Rhabdammina, were abundant Žreplicates: 5.6, 10.4, and 15.5 stained tubesr10 cm2 . on the ambient sea floor, whereas no living tubular individuals were present in the colonization boxes indicating that tubular taxa are late immigrants. Their large size and heavy tests must Fig. 2. Number of live Žstained. species Žmean values and SD for replicates. of benthic foraminifera in ambient seabed sediments and colonization boxes Žsurface 0–5 cm. from three stations in the Oslo Fjord, Norway. 176 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185 Fig. 3. Relative abundance Žmean values and SD for replicates. of live Žstained. Stainforthia fusiformis in ambient seabed sediments and colonization boxes Žsurface 0–5 cm. from three stations in the Oslo Fjord, Norway. require a very high shear velocity, compared to most benthic foraminifera, in order to get suspended so they probably disperse at a very early life stage. Their absence in the colonization boxes may indicate that they have a slow turnover rate and either had not reproduced or at least not successfully settled into the boxes. An even more delayed colonization and recovery pattern was recorded in the Baltic Sea experiment ŽWefer and Richter, 1976. where living individuals were found only occasionally during the first 8 months, and the faunal density did not approach that of the surrounding environment until 13 months after installation. It was speculated that this delay might have been due to an absence of strong water movements. Compared to what was recorded in the open coastal shallow water and shelf studies, the colonization in these comparably tranquil, partly landlocked areas, showed a pronounced time lag with recovery times of more than 8 months. The strong dominance of one opportunistic species in the low energy, as opposed to the high energy environments, probably represent the low equatability, low species diversity, and high abundance pioneer assemblages characteristic of metazoan invertebrate colonization. In the deep sea, benthic macrofauna has been shown to have a much slower colonization rate compared to shallow water habitats Že.g., Grassle and Morse-Porteous, 1987, and references therein.. However, more recent investigations suggest that some events in the deep sea may occur more quickly than once thought, particularly in response to different kinds of food enrichment Že.g., Snelgrove et al., 1994, 1996.. For benthic foraminifera, it is difficult to make generalizations like this because their colonization rates seem to a large extent to depend on the hydraulic regime in the source area and on the speed of the transporting medium but there is some evidence that foraminifera colonize more rapidly than macrofaunal invertebrates. In a colonization experiment perfomed in the Panama Basin at 3900 m, Kaminski et al. Ž1988. reported that, if the tubular Dendrophrya arborescens is excluded from the calculations, 9 months may be sufficient time for an agglutinated foraminiferal fauna Ž) 297 mm. to recover to background levels of abundance and diversity after a disturbance Žthe macrofauna did not recover.. The absence of tubular forms in the Panama Basin colonization trays is in good agreement with the above mentioned findings in Oslo Fjord, Norway. In Sagami Bay, Japan, most species of the ambient community recolonized defaunated ambient mud after 1 year but here the assemblage sizes were about 50 times smaller in the culture bottles compared to those of the surrounding sea floor ŽKitazato, 1995.. 3.2. Azoic sediments with characteristics beyond the ‘normal’ marine range In addition to the recruitment rate of individuals to the new substrate, the environmental characteristics of the new habitat Že.g., nutrient flux, geochemical composition. plays an important role for the faunal recovery and development. Examples are instances where there is an initial lack of food, such as habitats emerging following volcanic ash deposition, and initially geochemically hostile sediments, such as those emerging following dumping of polluted sediments or reoxygenation of previously anoxic areas. E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185 3.2.1. Initial lack of food Colonization following the 1991 eruption of Mt. Pinatubo on the Philippines, which caused a 2–6 cm thick ash layer to be deposited in the South China Sea Žcovering an area of at least 36,000 km2 ., has been shown to take many years ŽHess and Kuhnt, 1996, 1997. and is still not complete. Investigations 3 and 5 years after the eruption showed that the benthic foraminiferal community was still far from recovery to background levels. However, the sediment prior to eruption was hemipelagic mud while after the eruption it was volcanic ash so it should not be expected that the post-eruption assemblage would be the same. After 3 years, the recolonization fauna observed in the top centimeter of ash was composed entirely of infaunal forms, such as two species of Reophax and one miliolid. Tubular forms, which had been abundant before the eruption, were not present. Five years after the eruption, the species diversity had increased compared to 1994 Ž3 years. and the first epifaunal saccorhizids and rhizamminids ŽFig. 4. were recorded ŽHess and Kuhnt, 1997.. Textularia sp. was rarely present in the pre-eruption sediments 177 but made up a large portion of the dead assemblage above the ash after 3 years. It was speculated that this skinny Textularia and Reophax dentaliniformis, which showed the largest abundances in the dead surface assemblages, represented the pioneer stage of a colonization succession and that they had been outcompeted by later immigrants. Two species of Reophax were the most successful colonizers here, as was also the case in the Panama Basin experiment ŽKaminski et al., 1988.. Surface samples Žnon-quantitative data. collected during five austral summers following the 1970 volcanic eruption Žeruptions also in 1967 and 1969. on Deception Island, Antarctica, also showed a slow recovery of the benthic foraminiferal assemblages ŽFinger and Lipps, 1981.. The assemblages recorded in the caldera in 1972 were sparse, by 1973 the fauna had undergone substantial enrichment and in 1974– 1976 the samples were rich in foraminifera, suggesting that there was a considerable progressive, but slow, repopulation of the devastated benthos. Some of the field experiments which have involved colonization of pure sand or glass beads seem Fig. 4. Individuals of Rhizammina colonizing the areas ŽSouth China Sea. affected by the ashfall of the 1991 Mt Pinatubo volcanic eruption. Photo taken by Michael Kaminski in June, 1998, during the RrV Sonne Cruise 132, station 11. Width of pictures 8 cm. 178 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185 to illustrate that initially nutrient-deficient sediments show a slowly recovering faunal development. In a colonization experiment Žsand from a sand pit., conducted during 6 weeks at 1 m water depth in the Indian River, Florida, weekly sampling showed that the densities of all taxa were significantly lower after one and two weeks but that the densities ‘stabilized’ after 3 weeks and the colonization occurred in the same rank order as the ambient fauna ŽBuzas, 1993.. It is not know whether or not reproduction occurred in the colonizing sediments. This colonization pattern resembles that described previously ŽSection 3.1. for high energy environemts with a physical transfer of parts of the surrounding sea floor assemblages into the new habitat, i.e., no primarily biologically driven succession would be expected but rather a successive introduction of whichever speciesrindividuals were available for transport during the investigation period. A similar faunal development was seen in the colonization of uncovered sand-filled boxes in the Florida Ž125 m. experiment ŽBuzas et al., 1989.. At greater depths ŽSagami Bay, 1445 m., in boxes with artificial substrates Žsilt-sized glass beads., the densities of living individuals were only one to two thirds of that of the open defaunated ambient mud boxes after 1 year and the number of species was accordingly lower whereas the diversity ŽShannon Wiener index. was comparable ŽKitazato, 1995.. Stained individuals were recorded only in the fluffy surface 5–10 mm which had been deposited since the emplacement. 3.2.2. Geochemically ‘hostile’ sediments The best way of establishing the rate of environmental recovery following disturbance is to monitor the faunal development. In some instances, the predisturbed assemblage may colonize after some time and to what degree this happens can be checked through comparison with the fossil assemblages preserved in the pre-disturbed deposits. In other instances, the environmental characteristics of the habitat at the site have changed to such a degree that the pre-disturbed assemblages are not the best adapted any more. Alternatively, according to the ‘species pool hypothesis’ of Buzas and Culver Ž1994., moreor-less random subgroups of species will establish themselves in the new habitat. Either way, the rate of colonization will, to some extent, depend on the geochemical characteristics of the new area. Following initiation of sewage treatment in the Gota ¨ River estuary, Sweden, it took about 1 year before the benthic foraminifera exhibited its first colonizers and even into the second year only Ammonia beccarii and three allogromiid species were recorded, whereas nematodes and larval forms of macroinvertebrates were present already during the initial phase of the recovery process ŽCato et al., 1980.. A faster colonization was recorded at an offshore dump site used for disposal of dredge spoil rich in organic material, Chaleur Bay, Canada, where Eggerella adÕena and Ammotium cassis had repopulated most of the substrate after 1 month ŽSchafer, 1982.. Two years later, all localities were repopulated, and the number of species and the standing crop had increased from 13 to 37 and 3 to 27 individualsrcm3 , respectively. In the geological record, there are numerous examples where colonization has occurred on substrates which were previously anoxic. Such habitats have completely different chemical and physical properties compared to well-oxygenated sediments and this probably has an impact on the colonization patterns. For example, in Drammensfjord, Norway, it took more than 1 year to colonize sediments which had experienced over 5 years of anoxia ŽAlve, 1995b.. The opportunistic species Stainforthia fusiformis was by far the most abundant and successful colonizer of the previously anoxic habitats both there and in Frierfjord, Norway ŽAlve, 1994.. On the other hand, only sparse living individuals of Bulimina marginata, which is considered to be a species tolerant of low oxygen Že.g., Rohling et al., 1993., were present during the initial colonization phase. The fact that B. marginata made up 45% of the stained assemblage at this site 4 years later ŽBernhard and Alve, 1996. shows that faunal recovery after prolonged anoxia may take several years. Furthermore, it suggests that B. marginata is a slower colonizer of previously anoxic sediments than S. fusiformis. 3.3. Discussion of colonization patterns One of the fundamental aspects to consider for understanding the processes controlling the coloniza- E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185 tion pattern is the post-settlement responses by the recruiting individuals. How do they respond when introduced into a new habitat? If the settling environment is suitable for the species maintenance, do all introduced species start reproducing soon after they have settled, or do they wait until the season of the year when most individuals normally reproduce? The reproduction patterns in benthic foraminifera are very complex and even though the life cycle is known for about 50 species ŽLee et al., 1991., there is still a poor understanding of how often they reproduce and what actually triggers reproduction. Many seasonal studies suggest that reproduction occurs once or a few times a year Že.g., Lutze and Wefer, 1980; Erskian and Lipps, 1987; Cearreta, 1988; Kitazato and Matsushita, 1996.. Wefer Ž1976. suggested that Elphidium excaÕatum had a growth period of about 3 months between each reproductive cycle. Boltovskoy and Lena Ž1969. suggested that the life cycle of small species probably is as short as 1 month, but extremely rapid reproduction rates, just a few hours after the gamonts leave the reproductive cyst, have been reported in very small taxa ŽPawlowski and Lee, 1992.. Most seasonal studies show that, even for species which seem to go through one or several reproduction peaks per year, at least some juveniles are present throughout the year, indicating that they reproduce continuously Že.g., Nonion depressulus, Murray, 1983; Ammonia beccarii, Basson and Murray, 1995; Stainforthia fusiformis, as Fursenkoina fusiformis, Murray, 1992.. Most seasonal studies are from shallow water areas but even though less is known about reproduction rates in deep-sea species Žsee Corliss and Silva, 1993., there are indications that a similar pattern also applies to them. Some deep-sea species have been documented to increase their abundance within a period of 1–2 months, as a response to increased fluxes of phytodetritus Že.g., Gooday, 1988; Gooday and Lambshead, 1989., whereas most of the metazoan meiofauna seem to fail to exploit and utilize phytodetritus as rapidly as the foraminifera ŽGooday et al., 1996.. On the other hand, small individuals of common phytodetritus-exploiting species Že.g., Epistominella exigua. Ždifficult to say for rarer species. are also present between the phytodetritus deposition events ŽA.J. Gooday, pers. commun., 1998.. This implies that even 179 though there are certain times of the year when reproduction is particularly intense, small individuals will always be available for transport and, theoretically, the individuals should also be able to continue to reproduce in the new habitat, whether or not they are introduced during their most reproductive phase. Reproductive activity is generally thought to be closely related to food availability. Different species have their peak densities at different times of the year and this may be a strategy for temporal partitioning of food resources where those resources are limited ŽCorliss and Silva, 1993.. Such partitioning is not required in eutrophic areas where the abundance of food is not a limiting factor. For example, nutrient conditions were not considered to be one of the controlling factors of reproduction for Trochammina hadai as the phytoplankton production Ži.e., nutrient availability. was high throughout the year ŽKitazato and Matsushita, 1996.. However, even in eutrophic areas, reproduction may be seasonal if the food supply is seasonal Žfor examples and discussion, see Gooday and Rathburn, 1999 - this volume.. The species composition established in the new area depends on the species pool in the source areaŽs., the type and availability of food, and the species’ ability to survive and reproduce in the new habitat. It has been pointed out by several authors that many benthic invertebrate larvae actively select their site of settlement, i.e., habitat selection Že.g., Thorson, 1966; Butman, 1987; Woodin, 1991. and larvae of polychaetes with sedentary adult stages seem to be particularly good in discriminating between different substrates ŽGray, 1971.. Similar selective behaviour was suggested for Glabratella ornatissima ŽErskian and Lipps, 1987. but it is not clear whether or not this applies to other species. Pioneer macrobenthic colonizers are often typically epifaunal or shallow infaunal, whereas infaunal groups which mix and aerate the sediments to greater depths, colonize at a later stage ŽMcCall, 1977; Rhoads et al., 1977.. For benthic foraminifera, Schafer and Young Ž1977. suggested that free living species with an epibenthic life style had a higher susceptibility for redistribution than infaunal forms. In this connection, it must be kept in mind that, particularly in areas with variable inputs of liable organic material, the vertical microhabitat position of sediment-dwelling foraminifera is dynamic and do 180 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185 not always show a consistent species specific depth partitioning within the sediments Že.g., Linke and Lutze, 1993; Jorissen et al., 1995.. However, in shallow water habitats, species which are common both within and below the surface 1–2 cm of sediment such as Ammonia beccarii Že.g., Goldstein and Harben, 1993., Elphidium excaÕatum Že.g., Corliss and Van Weering, 1993., and Fursenkoina fusiformis Že.g., Alve and Bernhard, 1995., have been shown to be among the first colonizers in defaunated sediments Žsee above mentioned case studies.. At a bathyal site Ž1445 m., Kitazato Ž1995. recorded that deep infaunal taxa were among the few species which colonized his open, ambient sediment-filled culture bottles. And finally, in the deep sea, infaunal taxa such as skinny species of Textularia and some Reophax species have been shown to be among the first and most successful colonizers Žsee Section 3.2.1.. Consequently, typically infaunal rather than epifaunal species seem to be among the first colonizers in environments ranging from shallow water to the deep sea. It seems that whether or not benthic foraminifera follow the classic metazoan successional colonization pattern to a great extent depends on the intensity of the hydraulic regime in and the transit time Žwhich in turn depends on current speed and transport distance. from the source area as well as on the environmental characteristics Že.g., food availability. of the new habitat ŽFig. 5.. In high energy environ- ments, passive suspension and transport of various growth stages dominate. Here the intensity of the hydraulic regime in the source area is responsible for which size fractions are thrown into suspension. This, together with the transit time, controls whether only the most easily suspended individuals or a more representative and numerically larger fraction of the source assemblage will be recruited. In areas with frequent recruitment of most faunal elements of different growth stages, there is no time for opportunists to flourish and the recovery happens within only a few days to weeks simply by a physical transfer of parts of the surrounding sea floor assemblages into the new habitat Ži.e., the colonization pattern is controlled by physical factors.. An exception may be if the new habitat is eutrophic and thereby probably cause enrichment opportunists, rather than the introduced assemblages, to flourish. On the other hand, in low energy environments with limited or only occasional recruitment Že.g., partly enclosed basins., recovery may take more than one year. When food and the physico-chemical properties of the new habitat are not limiting factors, opportunists Že.g., Fursenkoina fusiformis. which are particularly suited for rapid exploitation of new habitats will dominate during the initial colonization phase Ži.e., the colonization pattern is primarily controlled by biological factors.. The same colonization pattern seems to apply when the transit is slow due to long distance Žhundreds to thousands of kilometers. trans- Fig. 5. Generalized outline of dispersion of growth stages and colonization patterns of benthic foraminifera on soft-bottom substrates. The ‘transit time’ depends on the speed of the transporting medium and on the distance to source area. E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185 port over nutrient deficient areas Že.g., subsequent to ash deposition.. We do not know how long the foraminifera can survive in transit but the dispersal and colonization may occur via stepping-stones such as whale falls, as suggested to be the case for hydrothermal vent and cold seep organisms ŽSmith et al., 1989; Feldman et al., 1998. or other organically enriched patches on the sea floor Žfor benthic foraminiferal patterns associated with such patches, see Gooday and Rathburn, 1999 - this volume.. 4. Colonization of hard substrates Colonization studies of hard substrates show that foraminifera are one of the most successful colonizing groups. For instance, Abyssotherma pacifica was the dominant taxon of all the organisms on one of two recruitment plate arrays placed near a hydrothermal vent at 2600 m depth Ži.e., above CCD. in the East Pacific for more than 3 years ŽVan Dover et al., 1988 Žas Foraminifera sp. 1.; Bronnimann et al., ¨ 1989.. Here, it made up ) 25% of the total living meio- and macrofauna Ži.e., 19 testsr10 cm2 . whereas a relative abundance of only 3% was recorded on the other, indicating a patchy colonization pattern. However, the colonization of this species must have taken more than 3–4 weeks, as it was not recorded on arrays deployed for 23–26 days. Additionally, A. pacifica Žas ‘brown foraminifers’ but species name confirmed by L.S. Mullineaux, pers. comm., 1998. was one of the two far most numerically abundant species Žthe other was a ciliate. of all taxa recorded on basalt colonization plates deployed for 3 years in hydrothermal vent communities at 2505 m water depth, East Pacific Rise, with no temperature anomaly ŽMullineaux et al., 1998.. This shows that trochospiral agglutinated foraminifera like A. pacifica can be significant components of the benthic community that colonizes hard substrates in deep-sea hydrothermal vent environments. Manganese nodules represent a very common hard substratum in the abyssal deep sea ŽMullineaux, 1988., and recolonization is an important topic when considering manganese nodule mining. How long would recovery take following disturbance? After 7 weeks of colonization at 1240 m water depth, the 181 abundance was higher on arrays exposed to low current flow Žvelocities often - 5 cmrs. compared to those exposed to higher flow Žvelocities up to tens of centimeter per second., whereas no difference was recorded after 2 years. These results show that boundary layer flows affect both settlement and post-settlement processes in this abyssal environment. Agglutinated foraminifera Žprimarily Trochammina sp.. were the most abundant of all the colonizing organisms both after 7 weeks and 2 years which is in accordance with the naturally occurring epifaunal assemblages on manganese nodules and crusts. The fact that these attached foraminifera were abundant on the manganese nodules after only 7 weeks indicates that embryonic juvenilesŽ?. were available in high numbers soon after deployment. Whether this high availability is a commonly occurring phenomenon or not is left for future studies to investigate. 5. Conclusions Our present state of knowledge concerning benthic foraminiferal dispersal and colonization of new habitats is based on both experimental and field observations. Dispersal through self locomotion and release of gametes to the water masses may be significant over short distances and the presence of a meroplanktonic life stage has been reported for a few taxa only. Consequently, these methods are not considered to be of general importance for colonization following large-scale disturbance. On the other hand, dispersal through release of embryonic juveniles is considered to be an important mechanism, and it is probably the main mechanism for attached, tubular and larger foraminifera, which are not easily entrained at a later life stage. Finally, passive suspension and lateral transport of various growth stages seems to be a more important dispersion mechanism for benthic foraminifera than has generally been appreciated. This realization has an impact on our understanding of the mode and rate of colonization of new soft bottom habitats, which seems to be closely related to the hydraulic regime in, and the transit time from, the source area inhabited by species capable of colonizing the new habitat. The transit time depends on 182 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185 the speed of the transporting medium and the distance from the source area. It is suggested that the speed and pattern of colonization of soft bottom sediments are controlled by to which extent physical or biological factors are allowed to dominate. If high energy conditions Žbottom current velocities ) about 20 cmrs. dominate in the source area and the transit time for most species which are likely to inhabit the new environment is short Žhours to days., colonization may happen within days and ‘stabilization’ within days to weeks Ždifferent from metazoan pathway.. The process will simply be a physical transfer of parts of the source community to the new habitat, leaving no time for development of an opportunistic pioneer assemblage. However, an exception is probably if the new habitat is highly eutrophic. If the source area is dominated by weak bottom water currents Ž- 10 cmrs., entrainment is rare and the transit time is long Žweeks to months., allowing primarily embryos and small individuals to be transported. This leads to an initial establishment of a pioneer assemblage strongly dominated by one or a few opportunistic species Žsimilar to metazoan pathway., and recovery can take from one to several years. The same colonization pattern seems to apply when the transit is slow due to long distance Žhundreds to thousands of kilometers. transport over nutrient deficient areas Že.g., subsequent to ash deposition.. We do not know how long they can survive in transit but the dispersal and colonization may occur via stepping-stones Žbeneficial temporary habitats connected to organically enriched patches like whale carcasses.. The environmental properties of the new habitat also have important impacts on the colonization pattern. Recovery may be delayed for months or even years due to initial lack of food Že.g., volcanic ash. or ‘hostile’ substrate properties Že.g., recently reoxygenated or severely contaminated sediments.. In these instances, the duration of the time lag depends on the deposition rate of metabolizable organic matter and on how quickly the sediment chemistry recovers to an inhabitable level, respectively. Except for this delay, recovery seems to depend on the hydraulic regime and transit time in the same way as in more ‘normal’ marine settings. Infaunal, small species are among the first and most successful colonizers in new habitats from shal- low water to the deep sea. In the deep sea, trochospiral agglutinated taxa are among the most abundant colonizers on hard substrates. There is still a large gap in our knowledge of the processes governing benthic foraminiferal dispersal and colonization patterns. Considering the important implications a closer understanding of these processes have for paleoenvironmental interpretations, biostratigraphic correlations, and for evaluating the recovery rates following environmental disturbance, this calls for intensified research. Only through a combination of well-planned experiments and field observations following unplanned natural ‘experiments’ such as volcanic eruptions, anoxic events, or mass-flow deposits, can we obtain a better understanding of the dynamics of benthic foraminiferal colonization patterns. Acknowledgements I am very grateful to the organizing committee for inviting me to present this paper at the ‘Cor Drooger Symposium’, to Mike Kaminski for allowing me to use one of his photos, and to John Murray, Andy Gooday, Bert van der Zwaan, and the reviewers Ahuva Almogi-Labin and Frans Jorissen for constructive comments on the manuscript. References Alve, E., 1994. Opportunistic features of the foraminifer Stainforthia fusiformis ŽWilliamson.: evidence from Frierfjord, Norway. J. Micropalaeontol. 13, 24. Alve, E., 1995a. Benthic foraminiferal responses to estuarine pollution: a review. J. Foramin. Res. 25, 190–203. Alve, E., 1995b. 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