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Effects of two polychaete worms, Nereis diversicolor and Arenicola marina, on aerobic and anaerobic decomposition in a sandy marine sediment

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The effects of 2 polychaete species, Nereis diversicolor and Arenicola marina, on benthic metabolism and decomposition processes in organic-poor (0.06 % POC), sandy sediment were experimentally investigated. Sediment O-2 uptake and COP release were stimulated by 80 to 90 % and 260 to 270 % for N. diversicolor and A. marina, respectively, from basal rates of approximately 30 mmol m(-2) d(-1). These enhancements in benthic fluxes were due to both increased solute exchange due to macrofauna irrigation and increases in total benthic metabolism. Although the latter was enhanced by 10 to 35 % and 115 to 123 % by N, diversicolor and A, marina, respectively, both species inhibited anaerobic decomposition as indicated by 66 and 42 % lower sulfate reduction rates. Benthic fluxes and basal rates of benthic metabolism (without macrofauna) were 2 to 3 times higher in sediments enriched with organic matter compared to unamended sediments. Similarly, sulfate reduction rates were 3 times higher in enriched sediments. Total benthic metabolism in enriched sediments was stimulated by N. diversicolor to a similar extent (+ 27 to 34 %) as in unamended sediments, whereas A. marina stimulated total benthic metabolism to a slightly lesser extent (+43 to 55%) in enriched sediments than in unamended sediments. N. diversicolor had little effect on sulfate reduction (-4 %) in enriched sediments, while A, marina reduced sulfate reduction by 85 % in enriched sediments. Porewater profiles reflected the balance between stimulating effects on sediment decomposition processes and removal of porewater solutes by benthic macrofauna. Porewater and sediment profiles of reduced S compounds also showed the effects of these polychaetes on sedimentary S cycling, i.e, lower anaerobic decomposition and increased reoxidation of reduced compounds. Both species affected sediment element cycles, stimulating C cycling and favoring more oxidized species and processes in S cycling. Furthermore, both species affected the fate and distribution of the metabolites produced from decomposition by enhancing the exchange of solutes across the sediment-water interface and porewater flushing. In general, the biogeochemical impact of A. marina was greater than that of N. diversicolor.
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... Density and size structure determine the magnitude of the activities that drive the organization of the assemblage; reduction in either reduces the impact of the ecosystem engineers. The lugworm Arenicola marina is an important ecosystem engineer on the Atlantic Coast of Europe (Cadee, 1976, Beukema anddeVlas 1979;Reise, 1987;Banta et al., 1999;. It is a boreal species, common in upwelling regions of Portugal and Spain and further north from France into the North Sea and beyond the Arctic Circle. ...
... Fecal deposition occurs approximately every 20-40 min (Wells, 1945) impacting surficial species. The primary effect of A. marina is not however its deposition of feces, but rather its advective forcing of porewater and thus the creation of transient oxic sediment volumes at depth within the sediment, potentially increasing rates of remineralization of organics and increasing availability of nutrients such as ammonium, nitrate, carbon dioxide, and silicate at the sediment surface (Banta et al., 1999;Kristensen et al., 2014). The hydraulic activities cause dramatic temporal alterations in the availability of electron acceptors at depth within the sediment . ...
... The hydraulic activities cause dramatic temporal alterations in the availability of electron acceptors at depth within the sediment . These activities result in fertilization of microphytobenthos of surficial sediments (Chennu et al., 2015), significant alterations of porewater gradients (Hüttel, 1990;Banta et al., 1999;Papaspyrou et al., 2007;Volkenborn et al., 2019), increase in aerobic reduction of organic matter (Banta et al., 1999;Papaspyrou et al., 2007), and alteration of the composition of the sedimentary assemblage with tube-building forms and seagrasses in particular being negatively affected (Reise, 1985;Flach, 1992;Philippart, 1994;Valdemarsen et al., 2011). At densities of ~40 m − 2 or greater the spheres of influence of arenicolids overlap creating a bed of interacting forces that drives the biogeochemical nature of the system as well as the species composition (Wethey et al., 2008;Volkenborn et al., 2010). ...
Article
In asking how ecosystems will change with the forces of climate change, one approach is to identify the biotic forcing functions and focus on the ecologically dominant species, because as those species are affected, results will cascade through the system altering components such as biological diversity. Given the status of A. marina as an important ecosystem driver, it is of interest to ask how increasing temperatures will impact its distribution. The literature strongly suggests that the period during which it is most susceptible is late summer when the metabolic load of gametes is maximal and sediment temperatures at burrow depth during low tide are likely to exceed 25 °C. We used the probability of occurrence of fatal heat waves that penetrate to animal burrow depth as a primary factor in our modeling of past, present and future climates and the distribution of A. marina. Modeled sediment temperatures were validated against in situ temperature logger data and then used to develop the relationship between August SST and the occurrence of fatal heat waves to enable use of SST data directly. Modeled thermal gradients corresponded well to high resolution remotely sensed temperatures along the French and Iberian coasts and to distribution shifts in A. marina, known both from the literature and field surveys done by the authors in 2005–2014. Model hindcasts suggest that published occurrences of A. marina within the Mediterranean after 1860 except within the Gulf of Lions are unlikely. Given the known sensitivity of A. marina to anaerobiosis during heat waves, particularly when ripe, the forecasts based on CMIP6 25 km scale ocean models all predict the complete disappearance of A. marina from the Mediterranean and restriction to the upwelling zone on the western margin of Iberia and to the Atlantic coast of Europe north of 45°N with the suggestion of more limited populations in the English Channel and perhaps into the Wadden Sea. These biogeographic shifts will likely cause fundamental changes in ecosystem function along the coasts of Iberia, France, UK, and perhaps into Belgium and the Netherlands.
... The downward pumping of water into burrows results in the injection of water into the surrounding sediment, especially at the depth of the feeding pocket for animals living in I-or J-shaped burrows . This drives the advective transport of pore-water upward along the path of least resistance, often along the feeding funnel, out of the sediment (Banta et al., 1999;Rijken, 1979). Macrobenthic organisms that portray this type of behavior in sandy advective sediment often represent important species in coastal and estuary 125 environments, such as the lugworm Arenicola marina, common along the European coast, and the bamboo worm Clymenella torquata, mainly found in the Northwest Atlantic. ...
... Overlying water O2 concentrations in all experiments remained close to saturation with values at the chamber outflow lines of 228.8 ± 3.5 M (mean and sd of control core without sediment), 217.5 ± 17.9 M (non-irrigated core) and 199.4 ± 12.7 M (irrigated cores) in the summer experiment and 292.4 ± 8.3 M (control core), 290.7 ± 7.7 M (non-irrigated core) and 294.6 ± 9.2 M (irrigated cores) in the winter experiment. In all experiments, the highest Fed flux values were observed for the first two days after the experiment onset, likely due to higher carbon turnover rates following disturbance and the initial 230 transient phase of the experiments (Banta et al., 1999). These initial values are not considered in the following discussion as https://doi.org/10.5194/bg-2022-247 ...
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Multiple investigators have suggested that the benthic flux of dissolved iron (Fed) from continental shelf sediments represents an important source of this micronutrient to ocean waters. The magnitude, biogeochemical controls, and seasonal dynamics of Fed fluxes to date, however, have mostly been studied for muddy cohesive sediments dominated by molecular diffusion. Data from these studies have been included in global biogeochemical models to determine the contribution of this Fe source to the ocean. Fed fluxes from sandy advective sediments have received little consideration, although these sediments cover 50–60 % of the continental shelves. Sandy permeable deposits function as dynamic catalytic filters characterized by the rapid exchange of solutes and infiltration of particles —including labile Corg and reactive metal oxides— and high biogeochemical reaction rates. In this article, we discuss how the fundamentally different modes of solute and particle transport in sands affect the sedimentary Fe cycle and Fed flux. We present a case study in which we simulate bioirrigation in sands in summer and winter. In our experiments, Fed fluxes from non-irrigated sediments under diffusive conditions did not exceed 6 and 13 μmol Fe m-2 d-1 in winter and summer, respectively. Fluxes from irrigated cores reached values of 150 μmol Fe m-2 d-1 (winter) and 115 μmol Fe m-2 d-1 (summer). The results indicate that the pumping activity of the benthic macrofauna plays a key role in controlling the extent of the benthic Fed flux from permeable sediments, and that both biogenic and physical advection enhance fluxes. We argue that bioturbated sandy advective sediments constitute an important benthic Fe source to coastal waters and advocate for a more differentiated treatment of sediment type (muddy diffusive vs. sandy advective) and macrofaunal activity -reflecting different functional groups of the macrobenthos- in global biogeochemical Fe models. A better understanding of the benthic Fe cycle in sandy advective sediments is particularly important to help predict how anthropogenic effects such as changes in the deposition patterns of Corg and metals, the expansion of oxygen minimum zones, and changes in benthic biodiversity will affect the tightly coupled benthic-pelagic ecosystem along continental shelves.
... Continuous observation of Abra ovata showed that this bivalve's behavioural activity is linked to sediment-mixing intensity (Maire et al. 2007a). Depending on their behavioural traits, bioturbating species can induce various changes in the benthic compartment such as the microbial community structure (Banta et al. 1999, Marinelli et al. 2002, Papaspyrou et al. 2006 and in the biogeochemical reactions occurring in the sedimentary column (Gutiérrez & Jones 2006). Trait-based approaches therefore allow the description of different functional groups of macrofauna species, such as gallery-diffusors, biodiffusors, regenerators and upward-and downward-conveyors (François et al. 1997). ...
Thesis
The aim of this PhD is to describe the role of benthic foraminifera in bioturbation processes focusing on particulate fluxes at the sediment-water interface. Specifically, the objectives are fourfold: (i) characterising the motion behaviour of key benthic foraminiferal species inhabiting intertidal mudflats from the Eastern English Channel at the sediment water interface to further classify them into functional groups of bioturbation, (ii) quantifying surface sediment reworking rates of the above-mentioned species, (iii) understanding how biotic and abiotic parameters may drive the mode and the intensity of surface sediment reworking of the dominant species Haynesina germanica, and (iv) further describing the vertical burrowing dynamics and the biogenic structures built by Haynesina germanica to quantify its bioturbation rates. To do so, the following parameters are described: the travelled distance, the velocity, the vertical position, the activity level and the tortuosity of the path. The motion-behaviour is described for the following species: Haynesina germanica, Cribroelphidium williamsoni, Quinqueloculina seminulum, Ammonia tepida and Miliammina fusca. Although they are all classified in the functional group of biodiffusors, these species differ in their preferential vertical position within the sediment. Specifically, C. williamsoni is an epifaunal-biodiffusor, Q. seminulum, M. fusca and H. germanica are gallery-biodiffusors while A. tepida is a surficial biodiffusor. This therefore means that the mode of sediment reworking is species-specific in benthic foraminifera. Its intensity is mediated by specific traits as well as biotic and abiotic factors. Indeed, travelled distance, velocity, activity level and tortuosity of the path would vary between and within species. As a consequence, the rate and the mode of sediment reworking are species-, individual- and functional group-dependant. Specifically, the surface area of the test, the species density, the temperature and the organic matter concentration are key parameters that control the bioturbation activity of H. germanica. The present work highlights the role of benthic foraminifera in sediment reworking processes taking place at the sediment-water interface and in the sediment column. It opens new perspectives on the understanding of the ecology of foraminifera and their putative non-negligible role in bioturbation processes in intertidal ecosystems.
... More importantly, polychaetes can be exposed to low oxygen and high sulfide environments [20]. Through its remediation, anaerobic decomposition and sulfate reduction rate in sediments are suppressed [21]. In coastal sediments, half or more of the anaerobic decomposition is usually carried out by anaerobic microbes, so polychaete bioturbation must have a large impact on the microbial communities. ...
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Polychaetes are important benthic macrofauna that lives in sediments, usually in intertidal flats with high organic content and high sulfide. It has been suggested that polychaete bioturbation could perform environmental remediation. During the process, the microbial community plays important roles. Here, we used high-throughput sequencing technology to study the bioturbation effects on the bacterial community in the polychaete (Perinereis aibuhitensis) burrows at different tidal positions in intertidal flat. The results showed that the bacterial communities were dramatically influenced by the polychaete bioturbation. The ACE, Chao, and Shannon indices of the polychaete burrows increased in summer. Dominant phyla in the polychaete burrows were Proteobacteria, Campilobacterota, Desulfobacterota, Chloroflexi, and Bacteroidota, and the dominant bacterial families were Sulfurvaceae, Flavobacteriaceae, Rhodobacteraceae, Woeseiaceae, Desulfobulbaceae, and Sulfurimonadaceae. Results of linear discriminant analysis effect size (LEfSe) showed that groups that include organic matter degraders, such as Bacteroidota, Flavobacteriaceae, Rhodobacteraceae, Woeseiaceae, and groups that include sulfur oxidizers, such as Campilobacterota, Sulfurovaceae, Rhodobacteraceae, Desulfobulbaceae, and Sulfurimonadaceae, were significantly increased due to the polychaete bioturbation. The polychaete bioturbation reduced the complexity of the bacterial co-occurrence network while increased its modularity and homogeneity. The polychaete bioturbation also changed the functional groups, which significantly enhanced in functional groups of aerobic nitrite oxidation, nitration, dark thiosulfate oxidation, dark sulfur oxidation, and dark sulfite oxidation, while nitrogen respiration and nitrate respiration decreased. These results provide insight into the impact of bacterial communities under the intertidal polychaete bioturbation.
... The worm has adaptations to survive by anaerobic metabolism for extended periods of anoxia when ventilation is prevented (Sch€ ottler, 1979;Wohlgemuth et al., 2000;Welker et al., 2013). When the burrows are ventilated during inundation, oxygen and other electron acceptors, such as SO 4 À , are rapidly transported to deep subsurface sediment and metabolites, such as H 2 S, are flushed out of the sediment (Banta et al., 1999). Burrows with 2-3 mm oxidized walls may then extent to at least 10-20 cm depth driving SO 4 2À penetration substantially deeper . ...
Book
Carbon Mineralization in Coastal Wetlands fills the current knowledge gap in carbon mineralization, providing a balanced view of the carbon dynamics of coastal wetlands. This book provides a holistic treatment of carbon mineralization, from the contributions of litter/root decomposition pathways to carbon mineralization and the processes and sources of greenhouse gas production. This book compares carbon mineralization in coastal wetlands and highlights differences in carbon dynamics. As studies on blue carbon have strongly emphasized the storage potential of coastal wetlands, this book serves as an ideal resource on the topics discussed.
... Thus, burrow lines serve as their connection to the surface. Additionally, bioturbation by marine benthic macrofauna is noted to influence ecological processes (Montserrat et al., 2008;Kristensen et al., 2012;Wendelboe et al., 2013) by altering microbially mediated redox pathways (Nielsen et al., 2003;Quintana et al., 2015) resulting to organic matter degradation (Aller, 1994;Quintana et al., 2013), and facilitate the exchange of O 2 , CO 2 , and nutrients between sediment and overlying water (Banta et al., 1999;Michaud et al., 2006;Kristensen et al., 2014). However, in the study, the early juveniles created narrow or small burrow lines which can be easily filled or closed by the erosion and deposition of fine sediment particles. ...
Article
Polychaete aquaculture has progressed in some countries to meet the high demand of fish bait and aquaculture industries. However, knowledge on the aquaculture requirements of polychaetes in the grow-out is still scarce. The present study aimed to determine the optimal feeding rate (FR) and sediment depth (SD) for the grow-out culture of mud polychaete Marphysa iloiloensis from early juvenile to adult stage. The effects of two FRs (50 and 100 g m⁻²) with three different levels of SD (2, 3, and 5 cm) on M. iloiloensis survival, growth performance, and biomass were evaluated. The study was performed in a 2 × 3 factorial experiment using completely randomized design with four replicates per treatment that lasted 120 days. Early juveniles (30 days old) were stocked in glass tanks at 1000 individuals m⁻² and grown for 120 days (herein refer as ‘adult’, with musculature and capable of reproduction). Regardless of FR, M. iloiloensis had the highest survival of 45 ± 2% in 5 cm SD but statistically comparable to 3 cm SD (34 ± 5%), while survival was significantly lowest in 7 cm SD (26 ± 3%). The levels of nitrite (NO2) and total ammonia nitrogen (TAN) was significantly higher in the rearing water of 100 g m⁻² FR than in 50 g m⁻² FR. Higher FR resulted to poor water quality and appeared to contribute to the low M. iloiloensis survival in 100 g m⁻² FR. Growth performance was similar among treatments. There was a significant interaction between FR and SD on M. iloiloensis biomass (p < 0.05). In 50 g m⁻² FR, no difference was observed in the different levels of SD while in 100 g m⁻² FR, biomass was significantly higher in 5 cm SD than in 7 cm SD (p < 0.05). M. iloiloensis biomass in 50 g m⁻² FR was higher compared to 100 g m⁻² FR, regardless of the SD. Overall, the culture of M. iloiloensis using 50 g m⁻² FR in 3–5 cm SD showed the best survival and biomass. Based on these findings, it is recommended that the grow-out culture of M. iloiloensis from early juvenile to adult should follow the 50 g m⁻² FR and should be done in tanks with 3–5 cm SD to improve production.
... In addition to physical disturbance, Arenicola spp. particle reworking affects the biogeochemistry of the sediment in terms of sulfur dynamics (Nielsen et al., 2003), organic matter recycling (Kristensen, 2001;Wendelboe et al., 2013), total aerobic and anaerobic metabolisms (Banta et al., 1999), and promotes excessive growth of epiphytes, reducing photosynthesis and growth of seagrass leaves (Govers et al., 2014). ...
Article
Seagrass meadows provide important and valuable ecosystem services. They are affected by several natural and human-induced stressors, but a combination of natural recovery and management actions have recently inverted the worldwide reduction. The main objectives of this study were to provide science-based knowledge on ecology and restoration, framed on environmental-related policies. By coupling the general guidelines with practical experience, obtained from sequential in situ experiments carried out for several months in a show-case study area, this study provides guidelines useful for restoration practitioners. A decision-making approach is proposed to answer the following questions: 1) What is the best Zostera noltei transplanting method? 2) What is the best technique to reduce the bioturbation activity of Arenicola spp.?, 3) Do bioturbation reduction techniques affect the survival rate of Z. noltei transplants?, and finally, 4) What are the key steps to maximize the success of a Z. noltei transplant and increase the species’ resilience? Having a Portuguese coastal lagoon as show-case (Mira Channel, Ria de Aveiro), different transplant and restoration methodologies were tested (i.e. metal frames, nails, bamboo sticks, shoots inserted unanchored into the sediment, and intact units of sediment with seagrasses, named as SODs) to assure low environmental impact on donor meadows, high survival rate of transplanted shoots and the recovery of fragmented or lost meadows. Moreover, to potentially reverse a degraded Arenicola spp. colonized seagrass habitat, different types of natural membranes were tested. Results showed that the best transplanting method is the use of SODs as the self-facilitation process of Z. noltei is enhanced, while being the least invasive for the donor population. The use of a natural membrane can significantly decrease the bioturbation stress caused by Arenicola spp., with jute membrane being the best option, given its cost-handling-benefit trade-offs. Enhancing the success of seagrass restoration requires the implementation of effective measures by environmental restoration practitioners. We defined a three-step process to improve the resilience of Z. noltei. This stepwise approach consists on 1) Characterization of the donor population, 2) Identification of the constraints and implementation of measures to prevent them, and 3) Scale-up the restoration plan. The application of this stepwise approach in intertidal coastal and estuarine systems management will, therefore, facilitate the success of Z. noltei restoration plans.
... It has been shown that H. diversicolor is able to modify the conditions of the sediment environment and influence the behavior of other species or communities (e.g., Witte and De Wilde, 1979;Reise, 1981;Ó lafsson and Persson, 1986;Jensen and André, 1993;Emmerson, 2000;Gillet and Torresani, 2003;Paramor and Hughes, 2004;Wenzhöfer and Glud, 2004;Papaspyrou et al., 2006;Cuny et al., 2007;Pischedda et al., 2011;Engelsen et al., 2010;Godbold et al., 2011;Stauffert et al., 2013;Taylor and Cunliffe, 2015). Sediment reworking and ventilation by H. diversicolor may also partly control the fate of organic matter or pollutants (e.g.; Gilbert et al., 1994;Gilbert et al., 1997;Christensen et al., 2002;Banta and Andersen, 2003;Kristensen and Mikkelsen, 2003;Fernandes et al., 2006a;Burlinson and Lawrence, 2007;Tang and Kristensen, 2007;Cardoso et al., 2008;Bonnard et al., 2009;Mayor et al., 2009;Stomperudhaugen et al., 2009;Mouneyrac et al., 2010;Buffet et al., 2011;Buffet et al., 2013;Sun et al., 2018), sedimentary biogeochemical cycling (e.g.; Clavero et al., 1994;Gilbert et al., 1995;Banta et al., 1999;Ferro et al., 2003;Kristensen et al., 2011;Pischedda et al., 2012;Martinez-Garcia et al., 2015;Valdemarsen et al., 2018), and physical properties of the seabed (e.g.; Fernandes et al., 2006b;Fernandes et al., 2009;Widdows et al., 2009). However, the magnitude of influence, like that of many species, can depend on environmental history and context (e.g. ...
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Chapter
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The present review gives a short presentation of current knowledge with main emphasis on recent advances in the understanding of the lugworm Arenicola marina's irrigation pump, food energy requirements and feeding biology as related to bioturbation, nutrient fluxes and other secondary effects on the environment. The lugworm uses little energy (< 5% of total metabolic output) to pump water through its burrow into the sediment, but it is unlikely that the worm significantly enhances its nutritional intake by filter feeding as it does not filter sufficient water to gain enough nutritional benefit. While A. marina is found in a wide range of habitats, its mode of life sets limits on the types of sediments it can inhabit. It is critical for the lugworm to be able to pump water into the feeding pocket to adequately ventilate its burrow and to loosen and feed on sediment particles. There appears to be ample food in most sediments to support the nutritional needs of A. marina. These food sources may be dead organic matter and living organisms such as bacteria, microalgae, micro- and meiofauna, but there seems to be an unnecessary dichotomy between microbial and detrital food sources in the ongoing discussion of deposit feeder nutrition. Several food sources are probably utilised by A. marina, the balance being shifted depending on what is available in a given environment. A. marina is a good example of a 'ecosystem engineer' as it profoundly affects both the structure and chemical nature of as well as processes occurring within the sediment. As such A. marina plays an important role in affecting both energetics and material fluxes at the sediment-water interface of the habitats in which it lives.
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The following methods of measurement of sediment parameters are discussed: 1) rate of diffusional exchange of reactants and products across the sediment-water interface; 2) the concentration profiles of these reactants and profiles in the sediment, and 3) profiles and integrated rates of reactions in the sediment. The effect of increasing organic loading (6.2, 37.2 and 62.0 mmol C m-2d-1), with organic matter distributed in three ways: close to the sediment surface, a linear gradient downwards, or evenly mixed throughout the sediment. -from Authors
Article
A number of sediment incubations were set up to reproduce some of the conditions used by Kristensen and Blackburn [1] and to make a comparison with their results. There were three types of microcosm: aerobic (OX), anaerobic (AN) and aerobic with Nephtys (NOX). In addition to other measurements, dissolved organic nitrogen (DON) pools and fluxes, were measured. The sediment in this experiment contained more particulate organic matter (POM). Nephtys (NOX) had the same effect as Nereis in increasing the rate of mineralization of POC and PON, compared with the OX-cores (2.1 and 2.6 times, respectively). Again, the AN-cores had a higher mineralization rate (loss of POM) than that of the OX-cores, but in addition, mineralization in NOX-cores was not significantly different from AN-cores. It was thus confirmed that anoxic mineralization could be as high, or higher, than the oxic process. Both the temporal patterns of O2-and and CO2-fluxes and their magnitudes were very similar to those reported earlier. This contrasts with the higher loss of POM in the present experiment. However, the loss of C in DOC (associated with the measured DON) can account for the extra POM loss. The pore-water profiles of σCO2 and NH4+ were similar to those in the earlier report, and the fluxes of σCO2, O2, NH4+ and NO3- followed the same temporal pattern.