Spatial and temporal variation in natural enemy assemblages on Maryland native plant species

Habitat manipulation is a branch of conservation biological control in which vegetation complexity and diversity are increased in managed landscapes to provide food and other resources for arthropod natural enemies. This is often achieved by maintaining noncrop plant material such as flowering strips and beetle banks that provide natural enemies with nectar and pollen, alternative prey, shelter from disturbance, and overwintering sites. In most cases, plant material used in habitat manipulation programs is not native to the area in which it is planted. Using native plant species in conservation biological control could serve a dual function of suppressing pest arthropod outbreaks and promoting other valuable ecosystem services associated with native plant communities. We evaluated 10 plant species native to Maryland for their attractiveness to foliar and ground-dwelling natural enemies. Plants that showed particular promise were Monarda punctata, Pycnanthemum tenuifolium, and Eupatorium hyssopifolium, which generally harbored the greatest abundance of foliar predators and parasitoids, although abundance varied over time. Among ground-dwelling natural enemies, total predator and parasitoid abundance differed between plant species, but carabid and spider abundance did not. Matching certain plant species and their allied natural enemies with specific pest complexes may be enhanced by identifying the composition of natural enemy assemblages at different times of year and in both foliar and ground habitat strata.     

Springtime coupling between ice algal and phytoplankton assemblages in southeastern Hudson Bay,Canadian Arctic

Microalgal assemblages from the bottom ice, the ice-water interface and the water column were systematically sampled from April to June 1986, in southeastern Hudson Bay (Canadian Arctic). The taxonomic similarity between samples from the three environments was assessed using a clustering procedure. There were two groups that comprised samples from both the ice-water interface and the water column, while five other groups were made of samples originating from a single environment. Taxonomic compositions of the two mixed groups suggest two types of connexion between the ice-water interface and the water column, i.e. before the phytoplankton bloom, there was seeding of the water column by ice algae and, during ice melt, interfacial algae contributed to the water column communities that were otherwise typically phytoplankton. Overall, the phytoplankton community underwent a succession from pennate to centric diatoms. Sinking rates of algae from the ice-water interface were estimated using settling columns (SETCOL). The sinking rates increased seasonally (0.4–2.7 m d^–1), which enhanced accessibility of ice-algal cells to the pelagic grazers. Ice algae contributed to water column production as they became accessible to the pelagic grazers, and also by seeding the water column before the phytoplankton bloom.Contribution to the programs of GIROQ (Groupe interuniversitaire de recherches océanographiques du Québec) and of the Maurice Lamontagne Institute (Department of Fisheries and Oceans)     

Regional and seasonal variability of zooplankton collected using sediment traps in the southeastern Beaufort Sea, Canadian Arctic

Time-series sediment traps were deployed at six mooring sites in the southeastern Beaufort Sea from October 2003 to August 2004 during the cruise of the Canadian research vessel Amundsen within the framework of the Canadian Arctic Shelf Exchange Study (CASES). Trap-collected zooplankton (TCZ) at around 200 m water depth was dominated by copepods accounting for 74–93% of the total abundance throughout the year with increase in abundance at all sites during the fall. Seven distinct TCZ groups were identified through cluster analysis. Two marked seasonal shifts in TCZ composition from late fall to early winter and from spring to early summer were revealed at five sites at 200 m depth. The zooplankton was dominated by Oncaea spp., pteropods, and copepod nauplii in the late fall cluster and in the winter cluster, and by copepod nauplii in the summer cluster. A significant change in water temperature, salinity, and sea ice concentration was observed only with the spring–summer shift. The cluster analysis also revealed that TCZ composition at 200 m at a station located in the Cape Bathurst Polynya was markedly different from those at other sites through the study period by being characterized by the dominance of various copepodite stages of Metridia longa. This was probably due to a less prolonged period of sea ice cover, which provides favorable food conditions for the zooplankton community.     

Spatial and temporal variation of phytoplankton in two subtropical Brazilian reservoirs

The purpose of this study was to verify the longitudinal distribution of phytoplankton biomass in two subtropical Brazilian reservoirs in the State of Paraná and investigate intervening factors on changes in phytoplankton biomass according to functional groups. In the Capivari and Segredo reservoirs, samples were obtained every 3 months during 2002, along a longitudinal axis (fluvial, transition, and lacustrine zones) at different depths. One hundred and eighteen taxa were identified, with Chlorophyceae as the most specious group. During the study period, both reservoirs had mostly low biomass values (less than 1 mm³ l⁻¹). The short retention time of these reservoirs constituted the principal limiting factor to phytoplankton development. Biomass values above 1 mm³ l⁻¹ were observed in the Capivari fluvial zone in March and in the Segredo lacustrine zone in December, with dominance by Microcystis aeruginosa Kütz (L_M) and Anabaena circinalis Rab. (H₁), respectively. Vertical and horizontal gradients of analyzed abiotic variables and phytoplankton biomass were observed. Considering the phytoplankton biomass values, both reservoirs were oligotrophic for the duration of the study. The Canonical Correspondence Analysis (CCA) evidenced temporal and spatial gradients of phytoplankton biomass; nevertheless, it did not follow the classic model proposed for deep reservoirs, since higher biomass was registered in the lacustrine zone during some months and in fluvial zones during other months. Distinct functional groups of phytoplankton characterized both studied reservoirs. Capivari Reservoir was best characterized by L_M and Y groups, indicative of its greater water column stability and higher phosphorus concentration, whereas Segredo Reservoir was principally characterized by the MP functional group, indicative of its greater mixing zone extension and higher nitrate concentration. The obtained results also evidenced the influence of morphometric conditions and watershed purposes as important structuring factors of phytoplankton biomass in these reservoirs. Handling editor: L. Naselli-Flores     

Spatial and temporal variation in community composition and photosynthetic characteristics of phytoplankton in the upper Westerschelde estuary (Belgium,SW Netherlands)

Community composition, biomass and primary production of phytoplankton were studied in the east- ernmost section of the Westerschelde estuary in 1984. Photosynthetic characteristics were compared with distribution of some dominant phytoplankton species along a salinity gradient from 5 to 22 Spring phytoplankton, with Cyclotella meneghiniana (freshwater) and Skeletonema costatum (marine) as the dominant species grew faster than summer phytoplankton. In summer, biomass achieved its maximum, due to the riverine Scenedesmus species and the marine diatoms Thalassiosira levanderi and Ditylum brightwellii, as dominants. Growth conditions were more favourable to phytoplankton communities above 15%, than below this salinity. The data were compared with previous studies (1972) of species composition in the area.     

Trophic variability of Arctic fishes in the Canadian Beaufort Sea: a fatty acids and stable isotopes approach

Trophic ecology of most demersal Arctic fishes remains one of the major knowledge gaps for understanding food web dynamics and connectivity among ecosystems. In this study, fatty acids (FA) and stable isotopes (SI) were used to study the feeding ecology of seven species (n = 106) of the most abundant benthic fishes (eelpouts, sculpins and agonids) in the Canadian Beaufort Sea from shallow (20–75 m), slope (200–350 m) and deep (500–1000 m) habitats. Both FA and SI results revealed among- and within-species variability in diet composition. Correspondence analysis of FA signatures identified high within-species variability in diet, resulting in high overlap among species. Calanus-derived FA were present in all species (Calanus markers up to 13 % of total FA) and were particularly important in Ribbed Sculpin, Adolf’s and Longear Eelpout collected in deep habitats, suggesting a strong contribution of pelagic-derived FA to benthic fish communities. Incorporation of this signal in the benthos may result from either direct consumption of deep overwintering copepods (i.e., off-bottom feeding) or through detrital accumulation in benthic invertebrate prey. Mean SI values differed among species and indicated that a large range of trophic positions (δ¹⁵N varied from 14.09 to 17.71 ‰ for Canadian Eelpout and Adolf’s Eelpout, respectively) and carbon dietary sources are preyed upon (δ¹³C range from ?21.13 to ?23.85 ‰ for Longear Eelpout and Ribbed Sculpin, respectively). SI analyses suggested that most species examined were low- to mid-trophic generalist benthic carnivores, with the exception of Ribbed Sculpin, which was a low-trophic pelagic predator.     

Contribution of benthic microalgae to the temporal variation in phytoplankton assemblages in a macrotidal system

Suspended marine benthic microalgae in the water column reflect the close relationship between the benthic and pelagic components of coastal ecosystems. In this study, a 12‐year phytoplankton time‐series was used to investigate the contribution of benthic microalgae to the pelagic system at a site along the French‐Atlantic coast. Furthermore, all taxa identified were allocated into different growth forms in order to study their seasonal patterns. The highest contribution of benthic microalgae was observed during the winter period, reaching up to 60% of the carbon biomass in the water column. The haptobenthic growth form showed the highest contribution in terms of biomass, dominant in the fall‐winter period when the turbidity and the river flow were high. The epipelic growth form did not follow any seasonal pattern. The epiphytic diatom Licmophora was most commonly found during summer. As benthic microalgae were found in the water column throughout the year, the temporal variation detected in the structure of pelagic assemblages in a macrotidal ecosystem was partly derived from the differentiated contribution of several benthic growth forms.     

Spatial variability of the photosynthetic parameters and biomass of the Gulf of California phytoplankton

Spatial variability of the central Gulf of California (CGC) phytoplankton biomass and photosynthetic parameters in relation to physical forcing was studied. Sampling was carried out in November, and the surface TC range was 20-27.5°C. Strong tidal mixing in the midrift islands regions injects relatively cool, nutrient-rich waters to the euphotic zone. Some of this water is transported via jets and cool filaments throughout the Gulf. In general, chlorophyll a (Chl) of small phytoplankton (<8 m) (up to >2.5 mg m^-3) was higher than that of large phytoplankton. Highest values of phytoplankton assimilation numbers (P^Bm) [3.17 mg C (mg Chla)^-1 h^-1], and photosynthetic efficiency ^B) [0.23 mg C (mg Chl a)^-1 h^-1 (W m^-2)^-1] were determined for the large phytoplankton cells (>8 m). Our hypothesis that P^Bm values increase from cooler to warmer waters is not supported by the data. We found a 27-fold spatial difference of Chl, compared with a 10-fold difference of P^Bm and a 6-fold difference of ^B. Thus, in our study area, the major source of variability for primary productivity (PP) comes from Chl, and not from P^Bm and ^B. Therefore, we propose that it is possible to estimate late-fall PP for the CGC using average photosynthetic parameters. Average values for P^Bm and ^B of total phytoplankton were 0.72 mg c (mg Chl a)^-1 h^-1 and 0.12 mg C (mg Chl a^-1 h^-1, (W m^-2)^-1, with standard errors of 0.07 and 0.03, respectively.      

Spatial and temporal variability in ringed seal (Pusa hispida) stable isotopes in the Beaufort Sea

Arctic ecosystem dynamics are shifting in response to warming temperatures and sea ice loss. Such ecosystems may be monitored by examining the diet of upper trophic level species, which varies with prey availability. To assess interannual variation in the Beaufort Sea ecosystem, we examined spatial and temporal trends in ringed seal (Pusa hispida) δ¹³C and δ¹⁵N in claw growth layers grown from 1964 to 2011. Stable isotopes were correlated with climate indices, environmental conditions, seal population productivity, and geographic location. Sex and age did not influence stable isotopes. Enriched ¹³C was linked to cyclonic circulation regimes, seal productivity, and westward sampling locations. Higher δ¹⁵N was linked to lower sea surface temperatures, a higher percentage of pups in the subsistence harvest, and sample locations that were eastward and further from shore. From the 1960s to 2000s, ringed seal niche width expanded, suggesting a diversification of diet due to expansion of prey and/or seal space use. Overall, trends in ringed seal stable isotopes indicate changes within the Beaufort Sea ecosystem affected by water temperatures and circulation regimes. We suggest that continued monitoring of upper trophic level species will yield insights into changing ecosystem structure with climate change.     

九龙江河口浮游植物的时空变动及主要影响因素

于2009年春（5月）、夏（8月）、秋（11月）在九龙江河口水域进行了水文、化学和生物的生态完全示范区综合外业调查,研究了九龙江河口浮游植物的种类组成、密度分布、季节变化、空间差异及主要影响因素,并结合前期资料分析了年际变动。结果表明,九龙江河口的浮游植物共记录7个门类75属134种。主体是硅藻,绿藻次之,甲藻和蓝藻较少,黄藻检出率高,裸藻和金藻零星检出。种类组成的空间差异大,绿藻在河口内区淡水水域比硅藻更占优势, 中肋骨条藻（Skeletonema costatum）、短角弯角藻（Eucampia zodiacus）、圆筛藻（Coscinodiscus spp.）、颗粒直链藻（Melosira granulata）、微小小环藻（Cyclotella. caspia）是河口区咸淡水水域及近海区的主要种类。浮球藻（Planktosphneria gelotinosa）、栅藻（Scenedesmus spp.）、盘星藻（Pediastrim spp.）、小席藻（Phormidium tenus）是河口内区淡水水域的主要种类。根据浮游植物的生态类型及其生境特征大致可分为三大类群。浮游植物密度夏季最高,平均为358.68103cells/L,密集中心的季节变化明显,密度分布由优势类群的密度分布决定。中肋骨条藻和短角弯角藻的数量庞大,导致优势种突出,多样性降低,种间分布不均匀,群落结构简单化。与史料比对,种类组成因淡水藻类的列入而更丰富,密度年际降低,中肋骨条藻仍是第一优势种,但优势度有较大降幅,优势类群有重大年际变化,细胞个体较小的种类占优。盐度和营养盐对浮游植物的分布及密度变化造成极大的时空差异,存在线性、复合线性、多项回归等复杂的相关关系。     

Optical gradients and phytoplankton production in the Mackenzie River and the coastal Beaufort Sea

We sampled a 300-km transect along the Mackenzie River and its associated coastal shelf system (western Canadian Arctic) in July–August of 2004 to evaluate the gradients in optical, phytoplankton and photosynthetic characteristics. The attenuation of photosynthetically available radiation (PAR) was best explained by coloured dissolved organic matter (CDOM) and turbidity (non-algal particles), while UV attenuation correlated most strongly with CDOM. Bacillariophyceae and Chlorophyceae dominated in the river, and shifted to Cryptophyceae and Prasinophyceae in the estuarine transition zone. In the coastal shelf waters, picoplanktonic cells dominated the surface autotrophic communities while both large and small cells occurred in the deep chlorophyll maximum. High PAR attenuation reduced the integral primary production rate in the river, while at an offshore marine site, 55% of integral production was at or below the pycnocline, under low PAR. Climate change is likely to increase the sediment and CDOM loading to these waters, which would exacerbate light limitation of photosynthesis throughout the system.     

Spatial and temporal variation in species composition of dung beetle assemblages in southern Ireland

Abstract. 1. This study attempts to identify the main community characteristics that contribute to variability in dung beetle assemblage composition and structure across a range of spatial and temporal scales.
2. Dung beetle assemblages ( Aphodius , Sphaeridium, and Geotrupes species) were monitored by dung-baited pitfall trapping at 10-day intervals during the seasonally active period at eleven sites in southern Ireland. Three of the sites were monitored over at least 2 years between 1991 and 1996.
3. Although the species composition of the above taxonomic groups was comparable among sites and years, relative abundances of component species varied considerably. Detrended correspondence analysis ordinations indicated a similar level of variability in dung beetle assemblage structure among years, and among sites ≈1–180 km apart.
4. Processes that may contribute to spatio-temporal variability in dung beetle assemblages are discussed, and strategies for future research are suggested.     

Spatial and temporal variation in mercury contamination of seabirds in the North Sea

Once the moult patterns have been taken into account, feather methylmercury levels can be used to accurately measure the mercury burdens of seabirds. We used body feathers from live seabirds and from museum collections to examine geographical and temporal patterns of mercury contamination in the North Sea. This approach identifies an increase in mercury concentrations in seabirds of the German North Sea coast during the last 100 years, especially high levels during the 1940s, and reduced contamination in the last few years. Comparisons among populations suggest that some increases in mercury levels are predominantly due to local pollution inputs, as on the German coast, while in other areas deposition from jet stream circulation of global contamination may be the major contributor. Mercury levels are far higher in seabirds from the German North Sea coast than in populations from the north and west North Sea or from most areas of the North Atlantic. We advocate the use of museum collections of birds for studies of long-term changes in levels of mercury contamination.     

Distribution, diversity and biomass of summer zooplankton from the coastal Canadian Beaufort Sea

Composition, abundance, biomass and distribution of zooplankton in the coastal Canadian Beaufort Sea were studied in the summer of 2005 and 2006. Data were collected from two cross-shelf transects (11 stations in each). Sampling was conducted with vertical hauls using a conical net of 153-μm mesh size. Our results revealed that there are three ecological zones, Intense Plume, Diffuse Plume and oceanic, which are primarily shaped by the highly variable Mackenzie River plume. The Intense Plume Grouping was located at stations influenced greatly by the Mackenzie River, where Podon leuckarti, Pseudocalanus spp., Copepoda nauplii and Limnocalanus macrurus were most abundant. The Diffuse Plume Grouping, that was located in the transitional zone between the river plume and the ocean, had the highest diversity. This grouping was characterised by high abundance of Copepoda nauplii, Polychaeta larvae, Pseudocalanus and L. macrurus. The Oceanic Grouping, located farthest from shore beyond the 85-m depth contour, was mainly inhabited by marine taxa—Calanus glacialis, C. hyperboreus, Triconia (Oncea) borealis and Microcalanus spp.—and had the greatest overall zooplankton abundance and biomass of all groupings.     

Spatial and temporal dynamics of the steady-state phytoplankton assemblages in a temperate shallow hypertrophic lake (Lake Manyas,Turkey)

Spatial and temporal dynamics of phytoplankton biomass and species composition in the shallow hypertrophic Lake Manyas, Turkey, were studied biweekly from January 2003 to December 2004 to determine steady-state phases in phytoplankton assemblages. Steady-state phases were defined when one, two or three coexisting species contributed to at least 80% of the standing biomass for at least 2 weeks and during that time the total biomass did not change significantly. Ten steady-state phases were identified throughout the study peiod. During those periods, Achnanthes microcephala (Kützing) Cleve twice dominated the phytoplankton biomass alone and contributed to more than 50% of the total biomass in seven phases. Microcystis aeruginosa (Kützing) Kützing, Anabaena spiroides Klebahn, Cyclotella stylorum Brightwell, Pediastrum boryanum (Turpin) Meneghini and Phacus pusillus Lemmermann were also represented once in steady-state phytoplankton assemblages. A. microcephala was dominant usually during cold periods of the year, while M. aeruginosa and A. spiroides were usually dominant in warm seasons. The total number of species showed a clear decrease during steady-state phases at all stations. All stations were significantly different in terms of the measured physical and chemical parameters (P < 0.05) and phytoplankton biomass (F = 117, P < 0.05).     

Spatial and temporal variation of fish assemblages in a subtropical small stream of the Huangshan Mountain

Spatial and temporal variation of fish assemblages were investigated seasonally from May 2007 to February 2008 across 11 study sites in a subtropical small stream, the Puxi Stream, of the Huangshan Mountain. Along the longitudinal gradient from headwater to downstream, fish species richness and abundance increased gradually, but then decreased significantly at the lower reaches. The highest species richness and abundance were observed in August and the lowest in February. Based on analysis of similarities (...     

Elemental composition, total lipid content, and lipid class proportions in zooplankton from the benthic boundary layer of the Beaufort Sea shelf (Canadian Arctic)

Biochemical analyses such as lipid class and elemental composition can inform us about a species’ role in community energetics and nutrient cycling. The accumulation of lipid-rich energy stores affects the elemental composition and stoichiometry of animal tissues, and this relationship is especially relevant to zooplankton at higher latitudes due to increased seasonal lipid storage. However, due to sampling difficulties, the elemental composition and energy storage capabilities of polar, benthic boundary layer zooplankton are poorly known. We determined elemental and lipid class compositions for 26 taxa of benthic boundary layer zooplankton from the Beaufort Sea shelf. Elemental composition as a percentage of dry weight ranged 21–56% for carbon (C), 4–11% for nitrogen (N), and 0.1–1.1% for phosphorus (P) across all taxa. C concentration and C:N were positively correlated with the storage lipids triacylglycerols (TG) and wax esters/steryl esters (WE/SE) and negatively correlated with membrane lipids (phospholipids and sterols). Most taxa had high levels of storage lipids, generally TG. High levels of WE/SE were found in the copepod Calanus hyperboreus (>90% of total lipid) and the chaetognath Eukrohnia hamata (72%). In contrast, the chaetognath Parasagitta elegans had only minor proportions of both TG and WE/SE. The high levels of storage lipids in most taxa indicate that feeding behavior of benthic boundary layer zooplankton on the Beaufort Sea shelf is tightly linked with seasonal pulses of epipelagic production. This is the first report on the biochemical composition of most of the amphipod and mysid taxa presented here.     

Vertical distribution of sympagic meiofauna in sea ice in the Canadian Beaufort Sea

This is the first study to determine vertical distribution patterns of sympagic meiofauna, including metazoans, protozoans and eggs >20 μm, in the Amundsen Gulf (southeastern Beaufort Sea, Arctic). Full sea-ice cores were sampled from mid of March to end of May 2008 (Circumpolar Flaw Lead system study). Investigations were performed on first-year ice from three pack- and three fast-ice stations. Additionally, 5-cm bottom-ice sections were sampled at 13 pack-ice and 5 fast-ice stations. The metazoan community was composed of nematodes, rotifers, copepods, copepod nauplii, platyhelminthes and a few rare taxa such as mollusks, cnidarians and nemerteans. High numbers of eggs, between 50 and 2,188 eggs L⁻¹, particularly of nematodes and copepods, were present in the ice. Investigations revealed also eggs of the pelagic species Calanus hyperboreus and Sagitta spp. within the ice, so that further research is needed to clarify whether more organisms than expected might use this habitat as a reproduction ground. Many different morphotypes of protozoans were observed in the samples, especially ciliates of the order Euplotida. The highest abundance was always found in the lowermost 5 cm of the ice cores, nevertheless sympagic meiofauna was not restricted to that part of the ice. Integrated meiofauna abundance ranged between 41 and 4,738 × 10² Ind. m⁻² and was highest in the fast ice in early May. Differences between pack and fast ice in terms of integrated meiofauna communities and vertical distribution were not significant, while the analysis of the bottom-ice sections indicated both a temporal development and ice-type-specific differences.     

Spatial and temporal variations in phytoplankton biomass and primary productivity in the Southwest Atlantic and the Scotia Sea

Summary Two cruises of the ARA/Islas Orcadas (late winter/early spring 1978 and late summer/early fall 1979) provided data which show that temporal variability of phytoplankton biomass and productivity in the oceanic wates of the Southwest Atlantic and Scotia Sea is insignificant when compared to the influence of geographical variability. Two bloom stations sampled during the late winter/early spring cruise had chlorophyll a concentrations and productivity values an order of magnitude higher than waters sampled from the same locations the following late summer/early fall. However, a comparison of 10 paired stations from the two cruises indicated no seasonal trend, as measured values of chlorophyll a and productivity from the first cruise were randomly larger or smaller than values measured during the second cruise. Consideration of individual stations from both seasons suggests the need to re-examine widely held notions regarding the effect of the Polar Front Zone and the island-mass effect on phytoplankton abundance and productivity. Higher-than-expected standing stock and productivity values at some open-ocean stations and at some stations within the Polar Front Zone indicate that looking for specific factors which promote localized enhancement or impoverishment of phytoplankton would be more useful than continuing with attempts to generalize Antarctic productivity data into broad seasonal or geographical patterns.In memory of Mary Alice McWhinnie (1922–1980)     

Spatial distribution of phytoplankton productivity in the Amundsen Sea, Antarctica

To date, no direct measurements of primary production were taken in the Amundsen Sea, which is one of the highest primary productivity regions in the Antarctic. Phytoplankton carbon and nitrogen uptake experiments were conducted at 16 selected stations using a ¹³C–¹⁵N dual isotope tracer technique. We found no statistically significant depletions of major inorganic nutrients (nitrate?+?nitrite, ammonium, and silicate) although the concentrations of these nutrients were markedly reduced in the surface layer of the polynya stations where large celled phytoplankton (>20?μm) predominated (ca. 64?%). The average chl-a concentration was significantly higher at polynya stations than at non-polynya stations (p?<?0.01). Average daily carbon and nitrogen uptake rates by phytoplankton at polynya stations were 2.2?g?C?m^?2?day^?1 (SD?=?±1.4?g?C?m^?2?day^?1) and 0.9?g?N?m^?2?day^?1 (SD?=?±0.2?g?N?m^?2?day^?1), respectively, about 5–10 times higher than those at non-polynya stations. These ranges are as high as those in the Ross Sea, which has the highest productivity among polynyas in the Antarctic Ocean. The unique productivity patterns in the Amundsen Sea are likely due to differences in iron limitation, phytoplankton productivity, the timing of phytoplankton growing season, or a combination of these factors.