The Rise of the Dipteraâ•'Microbial Mat Interactions During the Cenozoic: Consequences for the Sedimentary Record of Saline

doi: 10.1111/ter.12058 The rise of the diptera-microbial mat interactions during the Cenozoic: consequences for the sedimentary record of saline lakes

M. Esther Sanz-Montero,1 Jose-Pedro Calvo,1 M. Angeles Garcıa del Cura,2 Concepcion Ornosa,3 Raimundo Outerelo3 and J. Pablo Rodrıguez-Aranda1 1Departamento de Petrologıa y Geoquımica, Facultad de Geologıa (UCM), C/Jose Antonio Novais, 2, Madrid 28040, Spain; 2Instituto de Geociencias (CSIC-UCM), C/Jose Antonio Novais, 2, Madrid 28040, Spain; 3Departamento de Zoologıa y Antropologıa Fısica, Facultad de Biologıa (UCM), C/Jose Antonio Novais, 2, Madrid 28040, Spain

ABSTRACT Shoreline gypsiferous sediments of an inland lake in central dae hinders significant preservation of microbialites. The Spain furnishes valuable insight into reconstructions of early overwhelming rise of Diptera at the onset of the Cenozoic sedimentary changes related to shore fly–microbial mat inter- resulted in extensive feeding and dwelling activity and con- actions in fossil gypsum precipitating saline lake systems. The tributed to reshape the saline aquatic habitat where microbial association of adult and larval forms of Ephydra (Diptera) mats thrived, thus leading to the formation of specific trace with microbial matgrounds overlying the lake margin results fossils that are illustrative of the existence of microbes in the in the formation of gypsiferous meniscate back-filled burrows paleoenvironment. that provide an analogue for recurring, extensively developed trace fossils that occur in Cenozoic, but not older, lacustrine Terra Nova, 25, 465–471, 2013 gypsum rocks. In this setting, sediment burrowing by ephydri-

that the presence of shallow feeding living in arid zone shallow ephemeral Introduction burrows associated with matgrounds waters with drastic seasonal salinity Although the concept of Phanerozoic has recurred at certain times in fluctuations (Krivosheina, 1986). stromatolite decline by grazing and Earth’s history. Under these extreme conditions, burrowing animals (Garrett,1970; Some invertebrates feed and grow shore flies and their cyanobacteria Awramik, 1971) was considered too well on cyanobacterial substrates food are often the only successful simplistic (Pratt, 1982), it is generally (Monakov, 2011). However, most organisms. Ephydridae not only toler- accepted that the appearance of examples of successful exploitation of ate high salinities, with their optimal three-dimensional trace fossils in cyanobacteria under natural condi- range around 180& (Warren, 2006, Early Cambrian strata testified to a tions come from dipteran larvae (Fo- p. 637), but require certain concentra- behavioural revolution (Seilacher, ote, 1977). Laboratory experiments tions for survival and normal devel- 1999). The rapid evolution of effi- conducted by Krivosheina (2008) con- opment (Herbst, 1999). cient grazing animals constrained firmed the ability of higher Diptera, The appearance of higher Diptera development of benthic mats while dominantly Ephydridae, to feed on took place in the Late Cretaceous bioturbation disrupted buried mats and digest cyanobacteria. Ephydri- (Blagoderov et al., 2002). Through- and closed a taphonomic window of dae, also called shore flies, alkaline or out the Palaeogene, the dominant preservation for soft-bodied organ- brine flies (Foote, 1995), are common structure of Diptera gradually shifted isms (Gehling, 1999). The earliest in aquatic habitats throughout the to the modern one. By the beginning mobile animals are interpreted to world and they often are the sole of the Neogene, dipteran ecological have burrowed microbially bound insect species of the benthic and and taxonomic diversity expanded sediments for food resources (Geh- shoreline portions of inland saline rapidly, which resulted in the appear- ling, 1999; Gingras et al., 2011). This lakes and ponds (Herbst, 1988). ance of the polydominant fauna of interaction was conducive to a Ephydridae are an important food modern type. The ancestors of mod- remarkable increase in the degree of source for wildlife in saltwater pools, ern higher Diptera were adapted for bioturbation of the sediment. Buatois such as it is observed in Mono Lake, life as saprophages in rotting vegeta- and Mangano (2011) have noticed California, where millions of birds are tion (Ferrar, 1987). The adaptative supported almost entirely by ephydr- radiation of higher Diptera, for Correspondence: Dr. M. Esther Sanz- ids (Jehl, 1986; Rubega and Inouye, instance Ephydridae, to different spa- Montero, PhD, Petrologıa y Geoquımica, 1994). Other insects, such as dragon- tial and trophic resources like micro- Facultad de Ciencias Geologicas, Univers- flies and chironomids are also com- bial mats, illustrates some reasons idad Complutense, C/ Jose Antonio Nov- mon inhabitants of modern and for the ample widespread success of ais, 2, Madrid 28040, Spain. Tel.: ancient saline lake environments this type of insects in wetlands (Kei- +34 91 394 49 18; fax: +34 91 544 (Brennan and McLachlan, 1979; per et al., 2002). 25 35; e-mail: [email protected], Gingras et al., 2007; Scott et al., Preservation of organic remains [email protected] 2009). Ephydridae are well adapted to and/or ichnofabrics in sedimentary

© 2013 John Wiley & Sons Ltd 465 The Cenozoic rise of the diptera-microbial mat interactions • M. E. Sanz-Montero et al. Terra Nova, Vol 25, No. 6, 465–471 ...... deposits that accumulated in saline ally, the burrow traces form a very sil saline lake systems. As discussed environments is usually poor (War- dense network within the sediment below, these processes were especially ren, 2006), which makes paleoecolog- and locally exceed 60% of the total significant after the end of the Creta- ical reconstructions more challenging volume of the gypsum strata ceous. (Truc, 1980; Palacios-Fest et al., (Figs 1A and B). The individual bur- 1994). In contrast, strongly burrowed rows are 0.5–5 mm in diameter, and Methods gypsum deposits showing a tangle- up to 5 cm in length (Fig. 1B) within pattern structure occur in several the tangle-pattern fabric. The bur- Fieldwork in Lake El Longar (altitude fossil evaporite lake basins in the rows display typical meniscate infill 683 m amsl) (Fig. 2) was conducted Cenozoic record, especially from the composed of lenticular gypsum, fae- in five campaigns during different sea- Mediterranean region (Truc, 1980; cal pellets and variable amount of sons between 2009 and 2012. Sedi- Ortı and Salvany, 1990; Arribas micrite and/or clay (Figs 1C and D). mentological work and sampling were et al., 1991; Rodrıguez-Aranda and The gypsum meniscate infill appears mainly performed along the eastern Calvo, 1998; Huerta et al., 2010; Dr. to have further aided in their recog- marshy shoreline (Fig. 2). The Ibrahim Gundogan,€ 2012, pers. nition. exposed shoreline varies over the sea- commun.). In the basins, up to 150- This article focuses on microbial sons and it may reach some tens of m-thick sedimentary sequences mats thriving in the inland saline metres in the dry periods. containing burrowed gypsum beds Lake El Longar, central Spain, that Water temperature, salinity and were deposited in shallow, but exten- offers a chance to compare extant lit- pH immediate measurements were sive lakes that covered areas of hun- toral biomats burrowed by Ephydri- taken with a PC300XS Sampler. dreds to thousands of km2. Burrows dae with Cenozoic bioturbated Water samples were collected in occur throughout gypsum beds that gypsum deposits. Thus, this study duplicate directly from the lake. The locally reach up to 1 m in thickness provides for the first time a modern water anions were determined by and show a diffuse, mottled structure analogue for interpreting gypsiferous electrophoresis, the cations by atomic (Fig. 1A). Selective silicification meniscate back-filled burrows. More- absorption and carbonates and bicar- enhancing morphological traces of over, observation from this modern bonates by titration in the Geochem- the burrows is locally recognized environment furnishes valuable istry Laboratory of the Museo (Fig. 1B) (Arribas et al., 1991; Sanz- insight into reconstructions of early Nacional de Ciencias Naturales- Montero et al., 2008; Sanz-Montero sedimentary changes related to shore CSIC (Madrid). and Rodrıguez-Aranda, 2009). Usu- fly–microbial mat interactions in fos- Diptera specimens were studied and images taken using a stereo- scopic binocular microscope. (A) (B) Forty organosedimentary samples comprising mineral and microbial mats were collected by hand and by using a PVC dredging device dug up to 10 cm deep into the shoreline matground. The mineralogy was determined by XRD of powdered specimens on a Philips X-ray diffrac- tion system. For preparation of thin- sections, sediment samples were dehydrated by lyophilization, embed- (D) (C) ded and impregnated with Epofix resin. Optical and fluorescence

SPAIN Madrid Lillo

250 km

Fig. 1 Examples of bioturbated gypsum from the Miocene of the Madrid Basin. Rocks shown in A and D crop out in the vicinity of Lake El Longar, their location ° ′ is arrowed in Fig. 2. B and C bioturbated rocks crop out at Brea de Tajo (40 14 1 km 15″ N, 3°4′32″ W; altitude 725 m amsl) (Rodrıguez-Aranda, 1995). (A) Close-up view of a burrowed gypsum bed characterized by a diffuse, mottled appearance, pen cap for scale = 40 mm long. (B) Hand sample showing silicified gypsum bur- Fig. 2 Location map and satellite view rows with a tangle-pattern fabric, coin for scale, diameter = 23 mm. Photomicro- of Lake El Longar. The main sampling graphs showing meniscate back-filled burrows formed of gypsum (C) and silica area is encircled. The location of Mio- pseudomorphs after lenticular gypsum (D). cene gypsiferous rocks is arrowed.

466 © 2013 John Wiley & Sons Ltd Terra Nova, Vol 25, No. 6, 465–471 M. E. Sanz-Montero et al. • The Cenozoic rise of the diptera-microbial mat interactions ...... examinations of thin sections were physical, chemical and biological in diameter (Fig. 5) encrust the mat performed using an Olympus BX51 processes (Sanz-Montero et al., surface and also occur in the pig- microscope. For high-resolution tex- 2012). From the surface downwards, mented phototroph-dominated layers tural analysis, carbon-coated thin the mat is composed of a green of both green and purple cyanobac- sections and fresh broken surfaces of superficial layer of cyanobacteria teria (Fig. 5A). The gypsum crystals previously air-dried and gold-coated showing two morphologically distinct are embedded in a biofilm complex samples were studied with scanning types of Oscillatoria, minor occur- composed of bacterial cells with sur- electron microscopy provided with rences of Pseudoanabaena, LPP- rounding extracellular polymers and X-ray energy-dispersive spectroscopy. forms (Guerrero and De Wit, 1992), syngenetic mineral phases comprising In addition, two wet, uncoated speci- and local presence of diatoms (Navi- mainly celestite (Fig. 5B), calcite, mens were observed by an environ- cula and Nitzschia), a thin red layer halite, hexahydrite and elemental mental scanning electron microscope. formed by photosynthetic purple sul- sulphur. phur bacteria, and a lowermost cm thick black layer with evidence for Setting Diptera-microbial mat interactions sulphate reduction (Fig. 4). Lake El Longar is an inland, closed Gypsum is the main precipitate Throughout the spring–summer per- lake occupying a Quaternary flat-bot- from the lake brine. Lenticular gyp- iod, the wet shoreline area of the tomed depression in Miocene gypsif- sum crystals reaching up to 500 lm lake is dominated by small erous mudstone located in La Mancha (Central Spain). The lake Table 1 Chemical features of El Longar water. covers an area of 1 km2 and has 5.36 km of perimeter. Lake water (ppm) level can reach a maximum of 30 cm TDS T ° À 2À 2À À 2+ 2+ + + & but usually water depth is below Date ( C) pH Cl SO4 CO3 HCO3 Ca Mg Na K ( ) 20 cm. The main wildlife value of the June 25.2 8.50 10778 14261 0.0 426.83 756 4000 3100 705 34.0 area, mainly during the breeding sea- 2010 son, is with waterfowl species such as October 28.5 7.79 81360 142520 1351.4 701.22 444 33440 38860 5700 304.4 terns and cranes, and also the pres- 2010 ence of threatened steppe birds and March 18.2 7.76 14307 21812 0.0 0.00 674 6800 8300 940 52.9 terrestrial halophilic invertebrates. As 2012 with other lakes, dipteran larvae are a major source of food for waterfowl, shore birds and other animals in Lake El Longar. The marginal vegetation (A) (B) consists of annual and perennial halo- phytic plants (Cirujano, 1980). The local climate is Mediterranean characterized by aridity and continentality, with average temperature of 14.3 °C and average annual rainfall of 360 mm, though with significant seasonal fluctuations. The summer months are very dry, which favours desiccation of the shallower lake areas. The last complete desiccation of the lake happened in summer 2008. (C) (D) Data on the hydrochemistry of the lake water is shown in Table 1. The lake brine is Mg-Na-(Ca)-SO4-Cl type III B (Eugster and Hardie, 1978). The salinity of the water ranges from 34 to 304&. The shoreline area of the lake is covered by a cohesive and tiered microbial mat. The sediment surface displays varied mat-related morphologies including desiccation polygons Fig. 3 Littoral area of Lake El Longar (June 2010). (A) General view of the ben- (Figs 3A and B), pustular, convolute, thic surface which is colonized by microbial mats with polygonal desiccation wrinkle marks, mat chips, curling up, cracks. (B) A high proliferation of Ephydridae flies (black blobs) is just restricted gas domes, etc. The occurrence and to the water’s edge. (C) Close-up view of the flies densely populating the shoreline distribution of the mat surface struc- biomats. (D) Close-up view of microbial mat degradation by grazing Ephydridae. tures are related to a variety of Bar for scale is 15 cm.

© 2013 John Wiley & Sons Ltd 467 The Cenozoic rise of the diptera-microbial mat interactions • M. E. Sanz-Montero et al. Terra Nova, Vol 25, No. 6, 465–471 ...... semi-aquatic flies (Diptera: Ephydri- head is small and withdrawn into the burrows are backfilled by lenticular dae) (Figs 3C and D) and their thorax. The larval respiratory syphon gypsum and pellets. The wall of the aquatic larvae scavenging and feed- and spiracles are fully extended burrow trace is typically delimited by ing on the microbial mats. The Dip- (Fig. 6A), which allow to obtain gypsum (‘burrow-lining’) (Fig. 8) tera move following the progressive atmospheric oxygen, even though probably due to the reinforcement of retreat of the strandline (Fig. 3C) as they may be at least partially sub- the burrow walls by impregnation the brine concentration increases so merged most of the time. The mature with mucus (D’Alessandro and that the upper layer of sediment is larvae pupate, by grasping the ben- Bromley, 1987). As a result, most of burrowed in an area extending at thic mats, with prolegs of the VI and the shore sediment consists of a mix- least 5 m from the water line to the VIII abdominal segments that act as ture of meniscate tubules, cyanobac- back of the shore and around 500 m claws. Pupae skin hardens to form a terial peat, disrupted gypsum and in width along the shoreline. Other case that holds the insect in a non- syngenetic mineral phases, pellets, ground-burrowing organisms inhabit- feeding stage (Fig. 6C). pupae and insect remains including ing the upper part of the shoreline In Lake El Longar both larvae empty cases (Figs 6C and 7). include salt-tolerant beetles, but they and adults of Ephydridae are con- are quite subordinate in number in fined to cyanobacterial mats and feed Discussion and conclusion relation to the extremely abundant on cyanobacteria (Figs 3D and 7A). Ephydridae populations. The vast Burrows produced by feeding of the Gypsiferous meniscate back-filled majority of flies are Ephydra macel- larvae on microbial mats are traces recurrently found in Cenozoic laria (Diptera). The flies develop in a arranged in all directions, this result- lacustrine deposits have distinctive few weeks from egg to larva with ing in an extensive burrowing of the infilling pattern, sizes, morphologies three larval instars that display the uppermost layer of the biomat that and architectures (Fig. 1) consistent same morphology before pupating displays a characteristic tangle pat- with their construction by dipteran and metamorphosing. Larvae are tern (Fig. 7B). The burrow traces are larvae. The first finding of similar translucent-white maggots with eight cylindrical and internally meniscate, burrows produced today by Ephydri- pairs of distinct ventral prolegs, dor- up to 2 cm in length and 3.5 mm in dae in Lake El Longar is noteworthy sal spine patterns and distensible diameter (Figs 7B and 8). Single by two reasons: (i) it allows positive bifurcated syphon (Figs 6A and B), which are typical characters of Ephy- dridae. The larvae are from 1-to-25- mm long, including the respiratory (A) (B) tube. The larvae and pupae remain submerged throughout development. As an adaptation to the microbial mat habitat of the Ephydridae imma- tures, the prolegs bear crochets that assist in grasping the substrate (Ma- this and Simpson, 1981). The larval 100 μm 200 μm

Fig. 5 Thin-section (A) and SEM-BSE (B) photomicrographs of gypsum precipi- tates. (A) Gypsum crystals precipitated within the microbial mat. (B) Micrometer- sized celestite crystals (white minerals) interspersed within lenticular gypsum crystals of different sizes.

(A)r h (C)

p 1 mm

(B)

Fig. 4 Top view showing the laminated 1 mm 500 μm microbial community. The mat is composed of a 1 mm-thick green superficial Fig. 6 Photomicrographs showing features of Ephydridae larvae. (A) and (B) lat- layer (g), a red layer formed by purple eral and ventral, respectively, views showing the typical morphology and adapta- sulphur bacteria (r), and a lowermost tions of a third larval instar to the microbial mat ecosystem: a respiratory black layer (b) several cm in thickness. bifurcated siphon (r), opposite the head (h); eight pairs of prolegs-bearing crochets On the underside of the red layer, oxy- (p), the sixth and eighth pairs that act as claws are arrowed. (C) Ephydridae imma- gen bubbles can be seen. ture (I) and cases (arrowed) embedded in a microbial mat.

(A) (B) (A)

Fig. 7 Burrowed biomat in the shoreline of Lake El Longar. (A) Burrowed sediment surface showing some microbial mat remains with grazed edges (m) associated with Ephydridae larvae and exuviae (some arrowed). (B) Uppermost part of the sediment showing tangle-pattern tubules with gypsum infill (arrowed); coin for scale, diameter = 20 mm. 500 μm identification of the animals that Although pupae and cases have on (B) produced burrowed gypsum deposits occasion been found in Miocene lake during the Cenozoic; and (ii) recogni- deposits (Palmer and Carvalho, 1957; tion of this type of bioturbated gyp- Pierce, 1996; Park and Downing, sum lithofacies can be used as 2001), fossilization of Diptera evidence of former microbial mats in remains is rare because soft tissues the environment. are destroyed by predators, scaveng- In a prior overview on trace fos- ers and microbes. In contrast and sils in Miocene gypsum deposits, according to the documented occur- Rodrıguez-Aranda and Calvo (1998) rences of mm-sized, tangle-pattern 500 μm interpreted the gypsiferous meniscate burrow structures in gypsum deposits back-filled traces as feeding and from Palaeogene and, more com- Fig. 8 Photomicrographs of meniscate dwelling structures produced by sub- monly, from Neogene sedimentary back-filled burrows resulting from feed- aquatic insect larvae that were tenta- sequences in the Mediterranean ing activities of Ephydridae larvae. (A) tively attributed to Chironomidae. region (see references above); the Longitudinal section. The meniscate The interpretation was based on the potential for preservation in the geo- backfill consists of lenticular gypsum similarities in both geometry and logical record of gypsum backfilled, crystals. Note that the burrows are size of the traces compared with meniscate bioturbation fabrics is rel- usually delimited by lineation of gyp- burrow traces made by chironomids atively high. sum lenses (‘burrow-lining’). (B) Trans- versal section of a burrow showing in modern and ancient, fresh to The abundance of burrowers in inner porosity and pellets, likely fecal moderately saline lacustrine environ- the environment, which is the case of in origin (some arrowed). ments (Table 2), whilst recognizing Ephydridae larvae in many saline the lack of modern analogous from lakes, can contribute to increase the gypsum-forming lakes. The present preservation potential of their traces. This may explain the scarcity of study on recent gypsiferous lake The development of large popula- microbial buildups in Cenozoic evap- sediments enables us to re-interpret tions of these insects and the preser- orite rocks that were deposited in the role played by chironomids and vation of their body remains in the lacustrine environments where the to recognize the importance of shoreline deposits of Lake El Longar microbial mats would be expected to Ephydridae as producers of the bio- is envisaged as a good modern ana- have thrived. Stromatolites and turbated gypsum facies. One physio- logue for bioturbated gypsum facies thrombolite, however, develop in hy- logical feature that is considered in fossil evaporite lake systems. persaline settings (Des Marais, 2003; meaningful is that the Ephydridae As with other saline lakes, mainly Petrash et al., 2012) that are charac- larvae possess breathing tubes that from North America (Herbst, 1988; terized by higher rates of organic allow them to connect directly to Schultze-Lam et al., 1996), the graz- production relative to grazing (Stal, the atmosphere. This respiratory ing activity of ephydrids has been 2000). strategy forces the larvae to stay found to have a significant influence The evolution of higher Diptera close to the shore and likely pre- on mat growth in the El Longar from their appearance in the Late vents the formation of complex indi- shoreline (Figs 3D and 7). Thereby, Cretaceous and further expansion vidual tubes such as those exhibited the activity of burrowers prevents the through the Palaeogene and, namely, by chironomidae larvae that in addi- development of microbially induced during the Miocene matches well tion need their tubes to remain open sedimentary structures, thus reducing with the presence and stratigraphic for ventilation purposes (Rasmussen, the preservation of microbialite in distribution of mm-sized gypsum 1996). which mineralization is taking place. back-filled burrows in evaporitic

Table 2 Comparison of the burrow features made by larvae of Ephydra macellaria in Lake El Longar with those of chironomidae larvae in fresh to saline lake environments (data compiled from Paterson and Walker (1974), Hammer (1986), Williams et al. (1990), Gingras et al. (2007), White and Miller (2008) and Brand et al. (2012); note that chironomid larval tubes forming laminar tufa (e.g. Brasier et al., 2011) are described as a particular case of burrowing made by this group of insects.

Size (mm)

Burrows Diameter Length Shape Pattern Infill Walls

Ephydra 1–3.5 3–20 Blindly ending Tangle-pattern Gypsum and pellets macellaria cylindrical tubes meniscate backfill Gypsum-lined Chironomids 1–36–25 Non-blindly ending, Thalassinoides-like Often muddy or sandy, U, J, L, Y-shaped tubes passive infill Silk-lined Organism Chironomid larval 0.5–5 Up to 15 Lenticular to Convolute networks with Empty hollows–spar tubes in laminar tufa hemispherical tubes hemispherical cross-sections cemented Calcite micrite-lined Tufa laminae showing tangle-pattern

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