Research Article |
Corresponding author: Marina Monti-Birkenmeier ( mmonti@inogs.it ) Academic editor: Maria Grazia Mazzocchi
© 2019 Marina Monti-Birkenmeier, Tommaso Diociaiuti, Serena Fonda Umani.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Monti-Birkenmeier M, Diociaiuti T, Umani SF (2019) Long-term changes in abundance and diversity of tintinnids in the Gulf of Trieste (Northern Adriatic Sea). In: Mazzocchi MG, Capotondi L, Freppaz M, Lugliè A, Campanaro A (Eds) Italian Long-Term Ecological Research for understanding ecosystem diversity and functioning. Case studies from aquatic, terrestrial and transitional domains. Nature Conservation 34: 373-395. https://doi.org/10.3897/natureconservation..29841
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Abundance and composition of the planktonic tintinnid ciliates were studied in the Gulf of Trieste (Northern Adriatic Sea, NE Mediterranean Sea) from July 1998 to July 2016. Tintinnids were collected biweekly-monthly from the LTER station C1 (200 m offshore, 17.5 m depth) at four depths (surface, 5 m, 10 m and 15 m). The maximum tintinnid abundance reached 4476 ind. L-1 at surface in February 2016. The tintinnid community comprised a maximum of 35 species and was dominated by the genera Stenosemella, Tintinnopsis, Codonellopsis, Salpingella and Eutintinnus. The most abundant species were Stenosemella nivalis, Tintinnopsis nana, Codonellopsis schabi, Salpingella rotundata and Eutintinnus apertus. We found a species-specific correlation with the abiotic factors considered, i.e., temperature and salinity. Temperature was positively correlated with S. rotundata and E. apertus and negatively with S. nivalis. Salinity was negatively correlated with the majority of the detected species. Agglutinated species presented winter maxima while hyaline species showed higher abundance in summer-autumn. Some key species were present over the whole period studied. Significant differences within the water column were not seen in the species composition, but were seen in the relative abundances of the same species at different depths. Stenosemella nivalis, S. ventricosa and Tintinnopsis beroidea can be considered as keystone species in the area and their possible loss can be seen as a signal of changes in the structure of the entire planktonic system.
Tintinnids, Adriatic Sea, LTER
Tintinnid ciliates represent a fraction of microzooplankton (broadly heterotrophic planktonic organisms spanning 20 μm to 200 μm). They have a key position in the plankton food web as major consumers of picoplankton and nanoplankton and serve as prey for metazoans (
Tintinnids are the most investigated component of microzooplankton communities in the Mediterranean Sea where the west-to-east increase in species richness and in taxonomic diversity has been well documented (
The Gulf of Trieste is the most northern part of the Adriatic Sea, with a surface area of about 600 km2 and a maximum depth around 23 m (Malej and Malačič 1995). The main freshwater input in the Gulf is through the Isonzo River and the hydrodynamics is driven by a wind regime characterised by strong wind events, by the interaction with the Adriatic circulation and by seasonal shifts from stratification to mixing (
Biological factors, such as primarily prey abundance and predator presence, influence tintinnid behavior and ecophysiology (
In this paper, we analysed the long-term development of tintinnids collected in the Gulf of Trieste over a period of 18 years. The tintinnid assemblages were studied in terms of abundance and diversity along the water column and in relation of temperature and salinity. The main goal of this study was to identify the main patterns of temporal variability of the whole tintinnid community and its main components, and the possible key species.
Sampling was carried out in the Gulf of Trieste aboard different boats from July 1998 to July 2016 at the LTER station C1 (https://deims.org/96969205-cfdf-41d8-979f-ff881ea8dc8b). The sampling station is located 200 m offshore at 45°42'3"N, 13°42'36"E (bottom depth 17.5 m) (Figure
In the laboratory, the samples were allowed to settle for 3 days, after which the initial 2 L volume was reduced to 200 mL by siphoning through a glass tube made specifically for this purpose, under a fume hood. The reduced samples were stored in dark glass bottles and subsamples (50 mL) were analysed using inverted microscopes (Leitz and Leica DMI 3000B) at x 200 magnification following the Utermhöhl method (
Tintinnids were determined according to the classifications by
Statistical analysis was carried out using the PRIMER-7 software package (
The total tintinnid abundance ranged from 0 to 4476 ind. L-1 (February 2016) and the median values ranged from 22 ind. L-1 (surface) to 26 ind. L-1 (bottom) from July 1998 to July 2016. Tintinnid abundance integrated along the water column showed a high peak at the beginning of the series (775 ind. L-1 in October 1998) and decreased afterwards remaining < 250 ind. L-1 from March 2000 to April 2007 (Figure
The average seasonal pattern of tintinnid abundance in the integrated water column showed the lowest median values from January to April, and the highest ones from September to November (Figure
The pair-wise test of PERMANOVA revealed significant differences (p-perm < 0.05) among the different sampled layers, with the exception of 5 m and 10 m depths that showed the highest similarity (Table
Long-term fluctuations of total tintinnid abundance (ind. L-1) integrated within the water column (0–15 m) from July 1998 to July 2016 in the Gulf of Trieste.
Box plots of monthly averaged abundance of tintinnids (ind. L-1) integrated within the 0–15 m water column. The black lines represent the median, the white rectangles represent the dispersion of the data (25–75%), and the black bars show the non-outlier range.
Monthly averaged abundance (ind. L-1) of agglutinated (black) and hyaline (dashed) tintinnids integrated within the 0–15 m water column from July 1998 to July 2016.
Long-term fluctuations of total tintinnid abundance (ind. L-1) at different depths (surface, 5 m, 10 m and 15 m) from July 1998 to July 2016 in the Gulf of Trieste.
During the present study, tintinnids belonging to 19 genera and 35 species were recorded. Twenty of these were open sea species and 15 were estuarine-neritic species. The species list shows the frequency of occurrence and maximum abundance of each taxon (Table
Occurrence (number of samples in which the species was present), frequency, maximum abundance (ind. L-1) and distribution of each tintinnid taxon recorded in the Gulf of Trieste between 1998 and 2016 (total number of samples = 1000). C, common (20–100%); QC, quite common (8–20%); QR, quite rare (3–8%); R, rare (1–3%); RR, very rare (<1%), following the classification of
Occurences | Frequencies | Max abundance | Neritic or Open sea | |
Acanthostomella conicoides | 39 | QR | 60 | OSS |
Amphorides cfr. amphora | 3 | RR | 4 | OSS |
Amphorides laackmanni | 9 | RR | 28 | OSS |
Amphorides quadrilineata | 19 | R | 20 | OSS |
Amphorides quadrilineata var. minor | 4 | RR | 20 | OSS |
Amphorellopsis acuta | 66 | QR | 66 | OSS |
Amphorellopsis sp. | 2 | RR | 2 | OSS |
Codonella sp. | 19 | R | 160 | OSS |
Codonellopsis schabi | 126 | QC | 444 | NES |
Codonellopsis sp. | 34 | QR | 35 | NES |
Dadayiella ganymedes | 4 | RR | 8 | OSS |
Dadayiella sp. | 1 | RR | 2 | OSS |
Dictyocysta elegans | 50 | QR | 28 | OSS |
Dictyocysta lepida | 9 | RR | 12 | OSS |
Eutintinnus apertus | 95 | QC | 604 | OSS |
Eutintinnus fraknoi | 100 | QC | 208 | OSS |
Eutintinnus lusus-undae | 68 | QR | 380 | OSS |
Eutintinnus stramentus | 16 | R | 28 | OSS |
Eutintinnus tubulosus | 96 | QC | 650 | OSS |
Eutintinnus sp. | 17 | R | 208 | OSS |
Favella adriatica | 4 | RR | 4 | NES |
Favella sp. | 6 | RR | 24 | NES |
Helicostomella subulata | 67 | QR | 972 | NES |
Leprotintinnus nordqvisti | 11 | R | 10 | NES |
Metacylis joergenseni | 39 | QR | 48 | NES |
Metacylis sp. | 79 | QR | 512 | NES |
Protorhabdonella curta | 2 | RR | 10 | OSS |
Protorhabdonella sp. | 7 | RR | 4 | OSS |
Rhabdonella spiralis | 2 | RR | 6 | OSS |
Salpingella decurtata | 149 | QC | 156 | OSS |
Salpingella rotundata | 194 | QC | 1280 | OSS |
Salpingella sp. | 98 | QC | 120 | OSS |
Steenstrupiella steenstrupii | 16 | R | 24 | OSS |
Steenstrupiella sp. | 1 | RR | 2 | OSS |
Stenosemella nivalis | 429 | C | 4476 | NES |
Stenosemella ventricosa | 212 | C | 360 | NES |
Tintinnopsis angulata | 5 | RR | 38 | NES |
Tintinnopsis beroidea | 122 | QC | 208 | NES |
Tintinnopsis campanula | 63 | QR | 32 | NES |
Tintinnopsis compressa | 42 | QR | 324 | NES |
Tintinnopsis cylindrica | 46 | QR | 46 | NES |
Tintinnopsis nana | 196 | QC | 254 | NES |
Tintinnopsis parvula | 71 | QR | 72 | NES |
Tintinnopsis radix | 88 | QC | 48 | NES |
Tintinnopsis spp. | 115 | QC | 900 | NES |
Undella subcaudata var. acuta | 8 | RR | 32 | OSS |
Choreotrichida unid. | 180 | QC | 670 |
The number of tintinnid species detected in each year from 1998 to 2016 varied between 13 (2006) and 24 (2008) (Table
Occurrence of each tintinnid species recorded in the studied period (1998-2016) in the Gulf of Trieste. Black squares indicate that the species was present at least once in the corresponding year. White squares indicate the absence of the species in those years.
1998 | 1999 | 2000 | 2001 | 2002 | 2003 | 2004 | 2005 | 2006 | 2007 | 2008 | 2009 | 2010 | 2011 | 2012 | 2013 | 2014 | 2015 | 2016 | |
Stenosemella nivalis | |||||||||||||||||||
Stenosemella ventricosa | |||||||||||||||||||
Tintinnopsis beroidea | |||||||||||||||||||
Salpingella rotundata | |||||||||||||||||||
Eutintinnus tubulosus | |||||||||||||||||||
Tintinnopsis campanula | |||||||||||||||||||
Tintinnopsis nana | |||||||||||||||||||
Eutintinnus fraknoi | |||||||||||||||||||
Salpingella decurtata | |||||||||||||||||||
Codonellopsis schabi | |||||||||||||||||||
Eutintinnus apertus | |||||||||||||||||||
Eutintinnus lusus-undae | |||||||||||||||||||
Helicostomella subulata | |||||||||||||||||||
Tintinnopsis cylindrica | |||||||||||||||||||
Dictyocysta elegans | |||||||||||||||||||
Tintinnopsis compressa | |||||||||||||||||||
Tintinnopsis parvula | |||||||||||||||||||
Tintinnopsis radix | |||||||||||||||||||
Metacylis joergenseni | |||||||||||||||||||
Amphorellopsis acuta | |||||||||||||||||||
Steenstrupiella steenstrupii | |||||||||||||||||||
Acanthostomella conicoides | |||||||||||||||||||
Amphorides laackmanni | |||||||||||||||||||
Undella subcaudata var. acuta | |||||||||||||||||||
Amphorides quadrilineata | |||||||||||||||||||
Dadayiella ganymedes | |||||||||||||||||||
Eutintinnus stramentus | |||||||||||||||||||
Leprotintinnus nordqvisti | |||||||||||||||||||
Tintinnopsis angulata | |||||||||||||||||||
Amphorides cfr. amphora | |||||||||||||||||||
Favella adriatica | |||||||||||||||||||
Protorhabdonella curta | |||||||||||||||||||
Rhabdonella spiralis | |||||||||||||||||||
Dictyocysta lepida | |||||||||||||||||||
Number of detected species | 20 | 18 | 14 | 19 | 18 | 18 | 19 | 17 | 13 | 22 | 24 | 18 | 21 | 18 | 17 | 19 | 19 | 22 | 16 |
Considering the vertical distribution of the key species, the light differences detected among layers were due to the different abundances of the most representative species (S. nivalis, S. rotundata, S. ventricosa, T. nana, C. schabi and Salpingella decurtata) regardless the stratification of the water column. Stenosemella nivalis was absent at surface only in 1998 while S. ventricosa and T. beroidea were absent in many occasions at different depths (Suppl. material
The number of tintinnid species was lower during winter time, started to increase in spring and reached the maximum in summer-autumn. The specie richness was always < 12 from January to April, while it was > 25 from August to November (Figure
Seasonal patterns of tintinnid species richness (N species, left axis) and diversity index (Shannon Index + stdev, right axis) in the period from July 1998 to July 2016.
The pair-wise test showed a significant difference (p-perm < 0.05) in the community composition during the year. A significant pattern in composition similarity was detected and the highest similarity values were detected between contiguous months (Suppl. material
The most representative species showed different abundance trends. Stenosemella nivalis reached the maximum average abundance (109 ± 537 ind. L-1) in February while S. ventricosa in November (22 ± 65 ind. L-1); both species presented the lowest values in August (< 2 ind. L-1). The most common Tintinnopsis species showed the maxima in autumn. In particular, the data of the abundances integrated in the water column for T. nana, reached the average maximum value of 23 ± 43 ind. L-1 in October, followed by 11 ± 25 ind. L-1 in November. Codonellopsis schabi was present only from September to January reaching the maximum in November (16 ± 51 ind. L-1) (Suppl. material
The results of IndVal test are synthesized in Table
List of tintinnid taxa and significant IndVal for each season; taxa are ordered by season and decreasing IndVal values. aut=autumn; spr=spring; sum=summer; win=winter.
Season | IndVal | p-value | |
Codonellopsis schabi | aut | 0.4307 | 0.001 |
Tintinnopsis nana | aut | 0.3280 | 0.001 |
Stenosemella ventricosa | aut | 0.2200 | 0.001 |
Tintinnopsis spp. | aut | 0.2008 | 0.001 |
Tintinnopsis radix | aut | 0.1933 | 0.001 |
Tintinnopsis beroidea | aut | 0.1572 | 0.001 |
Dictyocysta elegans | aut | 0.1410 | 0.001 |
Codonellopsis sp. | aut | 0.1092 | 0.001 |
Tintinnopsis campanula | aut | 0.1024 | 0.001 |
Salpingella decurtata | aut | 0.0839 | 0.01 |
Tintinnopsis parvula | aut | 0.0796 | 0.001 |
Amphorides quadrilineata | aut | 0.0410 | 0.002 |
Amphorides laackmanni | aut | 0.0319 | 0.001 |
Leprotintinnus nordqvisti | aut | 0.0262 | 0.002 |
Eutintinnus tubulosus | spr | 0.0912 | 0.008 |
Helicostomella subulata | spr | 0.0642 | 0.024 |
Tintinnopsis compressa | spr | 0.0623 | 0.002 |
Tintinnopsis cylindrica | spr | 0.0413 | 0.003 |
Acanthostomella conicoides | spr | 0.0361 | 0.022 |
Codonella sp. | spr | 0.0273 | 0.012 |
Tintinnopsis angulata | spr | 0.0150 | 0.029 |
Salpingella rotundata | sum | 0.3105 | 0.001 |
Eutintinnus apertus | sum | 0.1823 | 0.001 |
Metacylis sp. | sum | 0.1076 | 0.001 |
Metacylis joergenseni | sum | 0.1065 | 0.001 |
Eutintinnus fraknoi | sum | 0.1020 | 0.001 |
Eutintinnus lusus-undae | sum | 0.1006 | 0.001 |
Amphorellopsis acuta | sum | 0.1002 | 0.001 |
Salpingella sp. | sum | 0.0860 | 0.001 |
Undella subcaudata var. acuta | sum | 0.0162 | 0.04 |
Favella sp. | sum | 0.0132 | 0.044 |
Stenosemella nivalis | win | 0.2882 | 0.001 |
The tintinnid seasonal trend was strictly related to temperature and salinity values (PERMANOVA: pseudo-f = 1.1158 p < 0.05 for temperature and pseudo-f = 1.1531 p < 0.01 for salinity). The dbRDA plot highlighted the distribution of the samples on the base of the similarity in tintinnid composition and the two abiotic variables taken into consideration (Figure
dbRDA (distance bases Redundancy Analysis) plot on the base of similarity in tintinnid composition constrained by temperature and salinity with axis significances (A). The colours represent samples collected in different seasons (blue=summer, red=autumn, green=winter, violet=spring). In the bubble plots (B–E), the bubble scale reports the relationship between bubble diameters and abundance measured for the most representative species: B Stenosemella nivalis C Salpingella rotundata D Eutintinnus tubulosus E Codonellopsis schabi.
This study revealed that, in the Gulf of Trieste, tintinnid abundance integrated within the water column decreased remarkably after the beginning of the year 2000, followed by a continuous but slow recovery starting from the year 2007. This pattern matched that of phytoplankton biomass observed in the same area during the period 2001–2007, characterised by the reduction of river runoff, increase of surface salinity and decreasing concentration of nitrate and silicate (
The total tintinnid abundances were similar to those recorded in the same area by previous studies but higher to the rest of the Adriatic Sea. In the period 1986–1990, at the same station, but only for the surface, the tintinnid abundance reached a maximum value of about 1000 ind. L-1 (
The total tintinnid abundance, integrated within the water column, showed relevant inter-annual fluctuations characterised by autumn maxima and, only in few cases, summer peaks. All the maxima, both in summer and in autumn, were due to blooms of S. nivalis and other few species. The isolated abundance peaks of some neritic species, such as S. nivalis, might be explained by the seasonal recruitment from cysts, as consequence of particular environmental conditions (
The seasonal pattern registered in this study differed between agglutinated and hyaline species. Tintinnids build the lorica according to the material available in the water column and the two lorica types, in general, correspond to different habitats: agglutinated lorica to coastal environments and hyaline lorica to open waters. In our time series, the open sea species were more numerous (27) than the neritic ones (20). The former were more abundant in summer, in agreement with the worldwide pattern of hyaline loricae dominating the communities in summer and agglutinated loricae in winter (
At station C1, we found the four most widely distributed and reported species in the world: A. quadrilineata, D. ganymedes, S. steenstrupii and E. apertus (
In our study, tintinnids were represented by 19 genera and 35 species. This number of taxa agreed with other studies within the same area.
Generally, the lowest species richness and diversity in the Mediterranean tintinnid assemblages is recorded in summer months, reflecting the seasonal minimum of primary production (
In our study, the differences in the vertical distribution of tintinnid composition were not significant, as reported for similar depths by
The seasonal pattern of tintinnid species can be strictly related to temperature and salinity. Tintinnid diversity appeared to be positively linked to salinity at a coastal station in the Ionian Sea (
This paper presented the characteristics of tintinnid assemblages along an 18-year period at a coastal site of the Gulf of Trieste that belongs to the Italian LTER (Long Term Ecological Research) network. Our long-term study has highlighted clear seasonal patterns and large interannual fluctuations of diversity and abundance. Three species appeared to be as keystone species for their persistent occurrence and relevant abundance and can be used to monitor the long-term evolution of the whole microzooplankton community in the Gulf of Trieste. The lack of significant differences among the community composition and relative abundance between 5 and 10 meter depths may suggest to reduce the sampling effort to the surface and bottom depths to monitor the tintinnid assemblages in this shallow marine area.
The site Gulf of Trieste is part of the Long Term Ecological Research national and international networks (LTER-Italy, LTER-Europe, ILTER). This study was carried out under the auspices of INTERREG II and III (Italy–Slovenia) and Ecomadr projects funded by EU and Friuli Venezia Giulia Region. We are grateful to the former LBM technical staff and to the OGS colleagues for field sampling and hydrological data. We would like to thank also all the students and researchers working on the analyses over the years. We are particularly grateful to Dr Elaine Fileman and another anonymous reviewer for their helpful comments and valuable suggestions.
Table S1. Result of pair-wise test on factor year
Data type: statistical data
Explanation note: The years: 1999–2000; 1999–2001; 2003–2005; 2005–2006; 2008–2010; 2012–2014, did not show significant difference
Table S2. Occurrence for each tintinnid species recorded in the studied period (1998–2016) in the Gulf of Trieste at each sampling depth (A, surface; B, 5 m; C, 10 m; D, 15 m)
Data type: occurence
Explanation note: Black squares indicate that the species was present at least once in the corresponding year. White squares indicate the absence of the species in those years.
Table S3. Result of pair-wise test on factor month
Data type: statistical data
Explanation note: The months: Dec-Jan; Dec-Feb; Jan-Feb; Jan-Mar; Feb-Mar, did not show significant differences.
Figure S4. Abundance trend of the most representative agglutinated species: S. nivalis, S. ventricosa, T. nana, C. schabi and hyaline species: S. rotundata, S. decurtata, E. fraknoi, E. apertus
Data type: abundance
Table S5. Sperman’s correlation values with temperature and salinity for each tintinnid taxon detected in the studied period
Data type: statistical data
Explanation note: in red the significative correlation p< 0.05