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Secondary production in a Laminaria hyperborea kelp forest and variation according to wave exposure
Estuarine, Coastal and Shelf Science 95 (2011) 135e144
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Secondary production in a Laminaria hyperborea kelp forest and variation according to wave exposure Kjell M. Norderhaug*, Hartvig Christie Norwegian Institute for Water Research (NIVA), Biodiversity and Eutrophication in Marine Environments, Gaustadaleen 21, NO-0349 Oslo, Norway
a r t i c l e i n f o
a b s t r a c t
Article history: Received 22 November 2010 Accepted 21 August 2011 Available online 29 August 2011
The secondary production of mobile invertebrate fauna in the Laminaria hyperborea (Gunn.) Foslie kelp forest increases with wave exposure level. This faunal group has a key function in transferring kelp carbon to higher levels in the food web. By using a size-frequency method the calculated production was 68 (18) g D.W. m2 yr1 (S.E.) at low, 250 (57) at medium and 308 (64) at high exposure levels. The calculations included 30 macrofauna species, which accounted for 96% of the specimens registered, with Gastropods, amphipods and bivalves being the most abundant taxa. The calculated secondary production is high, but comparable to that previously reported from other macrophyte systems and was 3%, 8% and 8% of the total primary production at low, medium and high exposure levels, respectively. Our results indicate that large quantities of Laminaria kelp are exported from the system, although the production of sessile animals was not taken into account. The most important factor in determining faunal densities and secondary production was probably habitat size but at low exposure levels the percentage of eggcarrying crustacean females and juveniles were lower than at medium and high exposure levels, thereby indicating lower fitness for animals at low exposure stations. Ó 2011 Elsevier Ltd. All rights reserved.
Keywords: secondary production macrofauna kelp forest Laminaria hyperborea
1. Introduction To establish ecosystem production budgets, it is necessary to calculate the production at each trophic level. The production of the level above the primary producers (secondary production) depends on the size of the primary production, how much of the production is transferred to the secondary producers and how much is exported from the system. Theory established from marine pelagic ecosystems suggests a secondary production efficiency of approximately 20% of primary production (Skjoldal, 2004). In several publications, the production of single or a few common marine benthic secondary producers has been presented (e.g. Asmus, 1987; Edgar, 1993; Vetter, 1996; Sejr et al., 2002). However, few attempts have been made to calculate the total benthic secondary production, i.e. the total production of all species of secondary producers, or the production of key faunal groups, though Fredette et al. (1990) calculated the production for 13 species, accounting for 20% of the identified fauna in an eelgrass community, and Brey (1990) analysed 337 datasets, including 138 benthic species. Macrophyte beds are high productive ecosystems and represent habitats which are in rapid decline globally (Nellemann et al., 2009). Thus, their importance for production in the coastal zone * Corresponding author. E-mail address: [email protected] (K.M. Norderhaug). 0272-7714/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2011.08.028
should be given detailed attention. In the NE Atlantic, Kelp Laminaria hyperborea (Gunn.) Foslie forms dense forests in the coastal rocky zone. The estimated annual production in well-developed forests can be as high as 9000 g D.W. m2 (3000 g C m2, Abdullah and Fredriksen, 2004), while along the Norwegian coast these forests cover 5800 km2 (Rinde, 2009). The kelp forests support large numbers of secondary producers inhabiting kelp fronds, epiphytic algae on kelp stipes, kelp holdfasts and on the rock in between the kelps (Christie et al., 2003; Jørgensen and Christie, 2003). Numerous sessile animals (sponges, bryozoans and ascidians) are found on kelp stipes (Norton et al., 1977; Bartsch et al., 2008) and mobile invertebrate fauna are found in high densities on epiphytic algae on the kelp stipes and on kelp holdfasts (Moore, 1973; Norderhaug et al., 2002). More than 100,000 mobile invertebrates per square metre are found on kelp stipes and holdfasts in well-developed kelp forests (Christie et al., 2003). While larger invertebrates and in particular sea urchins Strongylocentrotus droebachiensis (O.F. Müller) are important secondary consumers controlling large barren ground areas on the Norwegian coast, they are scarce inside dense kelp forest (Norderhaug and Christie, 2009). By mainly feeding on kelp detritus (Fredriksen, 2003; Norderhaug et al., 2003; Bartsch et al., 2008) and being the main prey for kelp forest-associated fish (Fredriksen, 2003; Norderhaug et al., 2005; Schaal et al., 2010), the mobile fauna has a key
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function in transferring kelp carbon to higher ecosystem levels. Because of high primary production, secondary production may also be expected to be very high. However, kelp is rigid and contains deterring secondary metabolites (Toth and Pavia, 2002a, b). As a result, most of the kelp standing stock is normally not grazed directly (although sea urchin grazing is an important exception, see Norderhaug and Christie, 2009), but enters the food web in the form of Particulate Organic Matter (POM, Newell et al., 1982; Duggins et al., 1989; Fredriksen, 2003; Norderhaug et al., 2003). By bacterial degradation, the kelp POM increases the food value (Norderhaug et al., 2003), though some primary production is then lost through bacterial respiration and the transfer rate of carbon from primary to secondary producers becomes less efficient. The secondary production is expected to vary considerably according to physical conditions. Wave exposure is probably the single most important factor that affects production in several different ways, both positively and negatively: high wave exposure may increase faunal mobility for species depending on water movement for dispersal (e.g. gastropod rafting, Vahl, 1983). At the same time, high wave exposure is expected to increase the loss of fauna through export from the system (Jørgensen and Christie, 2003; Waage-Nielsen et al., 2003). A significant part of the kelp POM is not consumed inside the kelp forest but instead is lost from the system through export which supports other systems in coastal areas (Vetter, 1995; Bustamante and Branch, 1996). The dependence of secondary producers on kelp material as food decreases with the degree of wave exposure (Schaal et al., 2009). Wave exposure is also of principal importance to habitat size. Kelp density, biomass and size (stipe length and habitat size) as well as the amount of epiphytic algae increases with exposure (Christie et al., 2003). Together with the kelp holdfasts, epiphytic algae comprise the main habitats of the fauna and, during summer and autumn, faunal abundances correlate with habitat size (Norderhaug et al., 2002, 2007). Thus, faunal abundances increase with exposure, and the secondary producers may be limited by habitat size and not by food. The first and primary aim of this study was to test whether the secondary production in a kelp L. hyperborea forest increases with wave exposure level. This was done by calculating the production of the dominating invertebrate species at stations with three levels of wave exposure. The second aim was to test whether the primary production mainly is consumed inside the kelp forest or is lost from the system through export of fragmented kelp. This was assessed by comparing primary production calculations from the same stations (Pedersen pers. comm.) with our calculated secondary production. The third aim was to assess whether differences in the secondary production between stations of different wave exposure level were linked to differences in faunal abundances and habitat size, faunal condition and resource partitioning, and/or loss of fauna from predation and wave surge. This was assessed by comparing faunal abundances, densities and proportions of eggcarrying females and juveniles at stations with different wave exposure level. 2. Methods
Fig. 1. Map of the study area between the islands of Harøy and Sandøy in the Møre archipelago, showing the locations of the nine stations (green: low, yellow: medium and red: high exposure stations) and the predicted level of wave exposure in the area. Wave exposure is modeled according to Isæus (unpublished).
distance to the nearest shore, island or coast) model (Isæus, unpublished), including wind strength and direction (16 directions) averaged over five years (data from the Norwegian Meteorological Institute). Canopy stipes (with epiphytic algae) and holdfasts (i.e. the most important faunal habitats, Christie et al., 2003) were used as sampling units. Three stipes and holdfasts respectively, were randomly sampled at each station and in each season by SCUBA diving and separately enclosed in cotton bags under water. The fauna on each sample was collected by washing with fresh water and sieving (mesh size 250 mm). By the use of this method we collected mobile macrofauna representatively, while sessile animals and meiofauna were not sampled. In the laboratory, the animals were counted and identified according to species or highest possible taxonomic separation, and all species were divided into four to six size classes. The length of a representative number of animals within each size class was measured and dried (60 C for 72 h), and the dry weight (D.W.) of each size class was measured. The lengths and D.W. were then used in production calculations. We used the size-frequency method (Hynes and Coleman, 1968) modified by Hamilton (1969) for calculations of the annual production of each species:
2.1. Experimental design The study was performed in the archipelago along the Møre coast in Norway. Fauna on L. hyperborea kelp was sampled from three replicate stations of three different wave exposure levels (a total of nine stations in a crossed design, see Fig. 1) and from four different seasons (April, June, September and November). Exposure levels (low, medium and high) were predicted from a fetch (i.e. the
P ¼ i
i X qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi Nj Njþ1 Wj Wjþ1 j¼i
Where P is the estimated production, i is the the number of size classes used, Nj is the mean number of individuals in size class j (averaged over seasons) and Wj is the mean dry weight of individuals belonging to size class j.
K.M. Norderhaug, H. Christie / Estuarine, Coastal and Shelf Science 95 (2011) 135e144
Univariate statistical techniques in the SPLUS 7.0 computer package were applied for testing of differences among the studied factors. Differences in faunal abundances, densities per unit habitat and differences in the percentage of egg-carrying females and juveniles were tested by mixed models with wave exposure (three levels) and season (month) as fixed factors and station as a random factor (Pinheiro and Bates, 2000). Differences in the total production were tested by a mixed model with wave exposure level as a fixed factor and station as a random factor. Response data were log transformed. Each test was followed by Tukey’s test for testing pair-wise differences between exposure levels. Table 1 Average density of canopy plants at stations with low, medium and high wave exposure. Habitat size measured as average total Fresh Weight Epiphytic algae per Stipes (EFWS), total EFWM (epiphytic fresh weight m2) in different seasons (sampling months), average EFW m2 throughout the year (across all the sampling seasons), and average HW (holdfast volume ml m2).
Canopy plants (No. m2) EFWS April EFWS June EFWS September EFWS November EFWM April EFWM June EFWM September EFWM November Average EFW m2 HW ml m2
Low
SE
Medium
SE
High
SE
8.9 8.9 23 56 39 79 205 498 347 282 2949
2.7 2.3 6 15 11 6.2 16 41 30 10 75
7.3 21 157 176 108 153 1146 1285 788 843 4449
2.1 7.3 42 22 16 15 88 46 34 35 102
12.3 62 116 134 159 763 1427 1648 1956 1448 7876
0.2 13 30 15 38 2.6 6 3 7.6 21 5.6
3.1. Fauna abundances, densities and secondary production Altogether, 275,887 animals were identified according to species or higher taxa level. The total number of animals per square metre increased significantly with exposure level (Fig. 2, Table 2, Tukey lower-upper bound: Medium-Low: 0.31e0.47 and HighMedium: 0.08e0.24). At most stations, the abundances increased from April to June and peaked in September, while in November the total number of animals decreased. 90000
No. per square meter
80000 70000 60000 50000 40000 30000 20000 10000 0
L1
L2 April
L3 L1
L2 June
L3
L1
L2
L3 L1
September
L2
L3
November
90000 80000
No. per square meter
2.2. Data analysis
3. Results
70000 60000 50000 40000 30000 20000 10000 0
M1 M2 M3 M1 M2 M3 M1 M2 M3 M1 M2 M3 April
June
September
November
90000 80000
No. per square meter
This widely used method is well suited for calculating benthic invertebrate production (Cartes et al., 2001). In cases in which the Cohort Production Interval (CPI, time from hatching to attaining the largest size class, see Vetter, 1996) was known, it was accounted for by multiplying the yearly production by 1/CPI (years). The CPI for each species is listed in Appendix 1. The polychaetes and amphipods in the family Lysianassidae were only identified to genus or family level. In the case of Lysianassidae, the CPI according to common species in the family (Moore and Wong, 1996) and from the same region was used because there are considerable differences in the reproduction history between regions (Skadsheim, 1989; Saint-Marie, 1991). In the case of amphipods this is valid since reproductive patterns for amphipods follow taxonomic lines (Nelson, 1980). Numbers per square metre at each station were calculated using the numbers of animals on stipes and holdfasts multiplied by the average number of canopy kelps per square metre (Table 1). Egg-carrying females and juveniles for species with brood pouch and direct development, i.e. amphipods and isopods, were counted and the percentage of egg-carrying females and juveniles was calculated for each species. These ratios were used as indicators for fitness and differences in resource partitioning between wave exposure levels, assuming that fit animals living in good conditions can allocate more energy into reproduction than less fit animals living in poor conditions (Begon et al., 1990). Fresh weight of epiphytic algae and holdfast volume (according to Jones, 1971) was measured and represented habitat size, The average densities of canopy plants at each station with a low, medium or high degree of wave exposure are shown in Table 1 and were used in calculations of fauna abundances and production per m2. Habitat size is presented from different seasons (sampling months) and as the average habitat size throughout the year (with average densities of canopy plants, data from Pedersen). Average sizes of the sampled holdfasts (ml m2) are also presented.
137
70000 60000 50000 40000 30000 20000 10000 0
H1 H2 H3 H1 H2 H3 H1 H2 H3 H1 H2 H3 April
June
September
November
Fig. 2. The average total number (No. m2 S.E.) of animals at stations with low (L13), medium (M1-3) and high (H1-3) wave exposure levels and from different seasons.
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Table 2 Results from mixed model on differences in the total abundances m2 of all identified mobile fauna and the total secondary production yr1 m2 of the 30 dominating mobile species, with wave exposure as a fixed factor with three levels (low, medium and high), season as a fixed factor with four levels (April, June, September and November) and Station as a random factor.
Fauna abundance Intercept Exposure Season Station Exposure x Season Exposure x Station Season x Station Exposure x Season x Station Secondary production Intercept Exposure Station Exposure x Station
Df
F
P
1 2 3 2 6 4 6 12
12,098 146 49 0.53 4.2 8.7 1.1 1.4
<104 <104 <104 0.59 0.001 <104 0.39 0.19
1 2 2 4
1233 88 1.2 4.0
<104 <104 0.31 0.02
The species specific production was calculated for the 30 most numerous and large species (Table 3). They accounted for 96% of the identified specimens in total and include two polychaete, two isopod, twelve amphipod, three decapod, five gastropod, five bivalve and one echinoderm species/taxa. The total secondary production increased significantly with exposure (Fig. 3, Table 2, Tukey lower-upper bound: Low-Medium: 1.3e0.7 and HighMedium: 0.2e0.7) and was 68 (18 g D.W. m2 yr1 SE) at low, 250 (57) at medium, and 308 (64) at high exposure levels (Fig. 3). The largest contributors to the total production were mussels at low and medium exposure levels, particularly the suspension feeding and burrowing mussel Hiatella arctica (Linnaeus), with biomasses of 1.7 (g D.W. m2 0.26 S.E.), 1.8 (0.38) and 2.6 (0.47) respectively at stations with low, medium and high wave exposure level and production (g D.W. m2 yr1 SE) of 23 (2.1), 39 (2.1) and 40 (4.7) (Table 3). Additionally, the biomass and production of juvenile Modiolus modiolus (Linnaeus) and Mytilus edulis (Linnaeus) was high. At medium and high exposure, gastropods (Lacuna vincta (Montagu) and Rissoa parva (Da Costa)) and amphipods (particularly Jassa falcata (Montagu), but also Apherusa jurinei (MilneEdwards), Ampithoe rubricata (Montagu) and Lembos websteri (Bate)) contributed much. Decapods (Hyas araneus (Linnaeus), Hyppolyte varians (Leach) and Eualus pusiolus (Krøyer)), isopods (Idotea baltica (Pallas) in particular) and brittle stars Ophiopholis acuelata (Linnaeus) also contributed significantly to the total production at medium and highly exposed stations. Idotea granulosa and the amphipod Gammarellus homari (Fabricius) were not found at low exposure stations. Densities of fauna per unit habitat (g fresh weight epiphytic algae and ml holdfast, respectively) were highest during June and/ or September (Fig. 4a, b). The densities on epiphytes and holdfasts were higher at medium and high exposure levels than at low exposure levels (Fig. 4a, b, Table 4, Tukey lower-upper bound: LowMedium: 0.17e0.02 (holdfast fauna), 0.35e0.05 (epiphyte fauna) and High-Medium: 0.13e0.01 (holdfast fauna), 0.29e0.01(epiphyte fauna). In general, there were smaller differences between exposure levels in the densities on the holdfasts than on the epiphytes, but there were significant differences between stations both on epiphytes and holdfasts (Fig. 4a, b). 3.2. Reproduction patterns The proportions of egg-carrying crustacean females were highest in April and June when more than 10% of the total populations were females carrying eggs at medium and high exposure levels (Fig. 5a).
Throughout the year there was higher average proportions of eggcarrying females at medium and high exposure levels than on low exposed levels (Table 5, Tukey lower-upper bound: LowMedium: 0.06e0.01 and High-Medium: 0.01e0.04). The proportions of juveniles were high in June when they comprised more than half the crustacean populations and low during the rest of the year (Fig. 5b). Throughout the year there was significantly higher average proportions of juveniles at high and medium exposure levels compared to low exposed levels (Table 5, Tukey lower-upper bound: Low-Medium: 0.09e0.008 and HighMedium: 0.05e0.04). 4. Discussion The secondary production of mobile macrofauna associated to L. hyperborea kelp forest is high but comparable to that reported from other macrophyte systems (e.g. Fredette et al., 1990). It varied between 68 and 308 D.W. g m2 year1at the stations used in this study. Our study is one of the first from the marine environment to calculate the total production of a faunal group with a key function in transferring primary production to higher ecosystem levels (but see Fredette et al. (1990) and Brey (1990)). Coastal macrophyte communities are among the ecosystems with the highest primary production on the planet (Nellemann et al., 2009). The primary production at the stations investigated was approximately 2300, 3000 and 4000 g dry weight per square metre per year (calculated from Pedersen pers. comm.). Abdullah and Fredriksen (2004) demonstrated that a primary production of 9000 g D.W. m2 yr1 (3000 g C m2 yr1) is not uncommon in kelp forests in Norway, and Christie et al. (2003) found up to 10 times the abundances of fauna per square meter as found in our study, indicating the possibility of a very large secondary production in some NE Atlantic kelp forests. There was a significantly increasing production of mobile macrofauna with exposure from low to medium and high wave exposure level. For that reason, the secondary production of the investigated faunal group was 3%, 8% and 8%, respectively, of the primary production at low, medium and high exposure levels whereas general theory suggests a secondary production of 20% of production efficiency in marine systems (Skjoldal, 2004). Our results suggest that the fauna is probably not food limited, and only a small part of the kelp production is utilized in the kelp forest (Hawkins et al., 1992). Kelp forests represent excess source systems which can provide kelp material to other coastal ecosystems (Vetter, 1995; Bustamante and Branch, 1996). However, sessile animals (Norton et al., 1977; Bartsch et al., 2008) were not taken into account. Although they are less important for transferring kelp primary production to higher levels in the food web than the mobile fauna (Norderhaug et al., 2005; Bartsch et al., 2008), they may contribute significantly to the secondary production. Also, our calculations are conservative and may be underestimated for several reasons. Only fauna from the most important habitats, i.e. holdfasts and epiphytes on kelp stipes (Christie et al., 2003) was sampled, and animals on kelp fronds, understory plants and the sea floor in between plants were not taken into account. Egg production was not included in our calculations. The food quality of kelp is low until it has been degraded by bacteria; as a consequence, some carbon is lost through respiration in the microbial loop before the kelp material is consumed by macrofauna (Norderhaug et al., 2003). Other error sources include the fact that the fauna have a different feeding ecology, and although their main food source is degraded kelp material (Norderhaug et al., 2003; Fredriksen, 2003), some are omnivores, carnivores and detritivores (as discussed by Benke et al., 2001), and to a certain extent we compared animals at different levels in the food web.
Table 3 The average yearly biomass (B, D.W. þ- SE), production (g D.W. per year) and P/B-ratios for the dominating species. Low
Medium
Typosyllis spp. Polynoinae I. baltica I. granulosa Lysinassidae G. homari A. bispinosa A. jurinei D. thea A. rubricata L. websteri C. bonelli J. falcata I.anguipes P. marina C. septentrionalis E. pusiolus H. varians H. araneus A. pellucida M. helicinus L. vincta O. semicostata R. parva B. reticulatum M edulis M. modiolus M. discors T. minuta H. arctica O. acuelata
0.13 (0.05) 1.3 (0.2) 0.09 (0.01) e 0.02 (0.01) e 4 104 4 103 0.14 0.23 0.17 0.06 0.50 0.06 0.01 0.03 0.10 0.14 0.03 104 0.26 0.78 0.10 0.80 0.07 0.15 0.35 0.05 9 104 1.7 1.1
(104) (2 103) (0.04) (0.14) (0.07) (0.02) (0.11) (0.01) (2 103) (0.01) (0.03) (0.09) (0.52) (106) (0.19) (0.23) (0.03) (0.25) (0.02) (0.04) (0.22) (0.01) (104) (0.26) (0.05)
P (S.E.)
P/B (S.E.)
B (S.E.)
0.20 (0.13) 2.4 (1.7) 4 103 (104) e 0.17 (0.1) e 9 104 (5 104) 0.02 (0.01) 0.76 (0.42) 0.20 (0.13) 1.2 (0.17) 0.12 (0.09) 3.2 (1.0) 0.21 (0.06) 0.03 (0.01) 0.13 (0.08) 0.39 (0.07) 4.9 (1.9) 2.2 (0.15) 7 103 (2 105) 1.5 (1.7) 3.9 (0.51) 0.32 (0.09) 2.5 (0.67) 0.42 (0.27) 4.2 (0.23) 3.1 (0.31) 0.25 (0.03) 0.01 (9 104) 23 (2.1) 0.67 (0.07)
1.6 1.8 21 e 10 e 2.3 5.0 5.4 0.84 7.0 2.0 6.4 3.8 2.7 4.2 4.0 35 74 68 5.7 5.0 3.1 3.1 6.4 26 8.8 5.7 10 13 0.58
0.51 2.2 0.78 2 103 0.11 0.02 103 3.0 0.11 0.71 0.88 0.45 6.8 0.21 9 103 0.02 0.29 0.13 0.09 0.03 0.05 7.2 0.08 7.0 0.03 0.92 0.53 0.17 103 1.8 0.48
(0.35) (1.7) (0.03) (3.6) (4.0) (0.13) (0.53) (0.63) (1.2) (0.65) (0.75) (1.2) (0.06) (0.53) (0.36) (2.2) (33) (1.3) (3.0) (2.1) (1.2) (0.46) (0.99) (3.3) (2.1) (0.69) (0.39) (0.27) (0.16)
High P (S.E.) (0.15) (0.7) (0.7) (104) (5 104) (8 103) (3 104) (0.4) (0.02) (0.34) (0.12) (0.02) (1.2) (0.04) (2 103) (7 103) (0.12) (0.11) (0.09) (9 103) (0.05) (1.1) (0.03) (1.1) (0.02) (0.18) (0.12) (0.05) (2 104) (0.38) (1.73)
0.44 3.1 20 0.06 0.49 0.24 4 103 5.6 0.37 1.6 4.2 0.23 29 0.58 0.02 0.06 10 7.1 7.1 1.2 1.4 33 0.16 12 0.12 46 13 1.7 0.03 39 0.17
P/B (S.E.) (0.17) (0.6) (0.4) (5 103) (104) (104) (104) (1.8) (0.46) (1.5) (2.8) (0.27) (2.2) (0.29) (0.04) (0.06) (1.0) (1.5) (0.91) (1.5) (0.82) (10) (0.03) (3.8) (0.24) (2.9) (0.85) (0.19) (3 104) (2.1) (0.86)
0.88 1.4 26 30 4.6 19 3.2 1.9 3.4 2.3 4.8 0.50 4.3 2.7 1.8 2.5 35 53 53 45 26 4.7 2.1 1.8 3.6 49 24 10 22 21 0.35
(0.86) (1.7) (2.1) (1.0) (0.3) (1.9) (0.1) (0.4) (1.2) (0.3) (2.2) (0.54) (0.55) (0.3) (1.0) (0.8) (0.11) (0.24) (0.24) (2.1) (7.2) (1.0) (1.3) (1.0) (3.7) (0.65) (2.1) (0.41) (1.0) (0.14) (0.70)
B (S.E.)
2
3
8
2
0.43 1.5 1.6 103 0.11 0.03 103 3.3 0.30 1.5 1.0 0.42 8.5 0.64 103 0.02 0.01 0.23 0.03 0.04 0.02 14 0.09 7.3 0.02 0.72 0.92 0.11 103 2.6 8.7
(0.05) (0.5) (0.5) (2 104) (0.03) (0.01) (3 104) (0.08) (8 103) (0.20) (0.25) (0.07) (3.2) (0.03) (2 103) (0.01) (0.04) (0.01) (8 103) (6 103) (6 103) (1.8) (0.01) (0.73) (0.01) (0.19) (0.19) (0.02) (5 104) (0.47) (0.61)
P (S.E.)
P/B (S.E.)
0.30 3.1 3.1 0.03 0.77 0.42 0.03 10 1.6 3.2 6.3 0.44 51 2.0 0.02 0.08 0.02 8.9 1.4 1.7 1.8 73 0.27 19 0.10 23 14 0.81 0.02 40 5.9
0.70 2.2 2.1 18 6.9 19 11 3.1 5.1 2.1 6.5 1.1 6.0 3.1 2.0 3.7 1.8 39 53 43 74 5.1 3.0 2.6 5.4 32 15 7.1 16 16 0.68
(0.40) (2.2) (2.2) (0.01) (0.1) (0.4) (0.03) (0.8) (0.06) (0.50) (1.3) (0.23) (8.7) (0.08) (5 103) (1.1) (4 103) (0.21) (0.64) (1.2) (0.76) (4.2) (0.06) (2.1) (0.03) (2.0) (2.2) (0.04) (5 103) (4.7) (1.7)
(0.71) (1.1) (1.1) (2.6) (0.88) (10) (10) (0.90) (0.19) (0.61) (1.5) (0.90) (0.64) (0.11) (0.55) (0.51) (0.71) (0.19) (25) (4.3) (23) (1.4) (0.95) (0.47) (3.1) (4.2) (1.9) (0.48) (0.21) (0.52) (0.28)
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B (S.E.)
139
140
K.M. Norderhaug, H. Christie / Estuarine, Coastal and Shelf Science 95 (2011) 135e144
120 Polychaeta Isopoda
100
Amphipoda
Production
Decapoda Gastropda
80
Bivalvia Ophiuroidea
60
40
20
0
Low
Medium 2
Fig. 3. The average total annual secondary production (g D.W. m
The most likely explanation for increasing secondary production with exposure is that habitat size is of primary importance for faunal densities, and thus for the total secondary production. In accordance with the findings of Christie et al. (2003) and
year S.E.) at stations with low, medium and high exposure.
Norderhaug et al. (2007), habitat size and faunal densities increase with exposure. At all exposure levels, faunal densities peaked in summer during the main reproduction period. A significant divergence from this correlation was most likely attributed to other
b
90 80 70 60 50 40 30 20 10
4 3 2 1 0
0
L1
L2
L3
April
L1
L2
L3
June
L1
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L3
September
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L1
L3
90
6
80 70
5
60 50 40 30 20 10
L3
L1
L2 June
L3
L1
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November
4 3 2 1 0
0
M1 M2 M3 M1 M2 M3 M1 M2 M3 M1 M2 M3
M1 M2 M3 M1 M2 M3 M1 M2 M3 M1 M2 M3 April
June
September
April
November
90
June
September
November
6
80 70 60
No. per ml
No. per g algae
L2 April
November
No. per ml
No. per g algae
6 5
No. per ml
No. per g algae
a
High
50 40 30 20
5 4 3 2 1
10
0
0
H1 H2 H3
H1 H2 H3
H1 H2 H3
H1 H2 H3
April
June
September
November
H1 H2 April
H3
H1 H2 June
H3 H1
H2 H3
September
H1
H2 H3
November
Fig. 4. (a) Densities (S.E.) of fauna per g (fresh weight) algae epiphytic algae at stations with low (L1-3), medium (M1-3) and high (H1-3) wave exposure level and from different season (sampling month). (b) No. (S.E.) of fauna per ml holdfast volume at stations with low (L1-3), medium (M1-3) and high (H1-3) wave exposure level and from different season (sampling month).
K.M. Norderhaug, H. Christie / Estuarine, Coastal and Shelf Science 95 (2011) 135e144 Table 4 Results from mixed model on differences in faunal densities (per unit habitat) on kelp holdfasts and epiphytic algae on the kelp stipe, with wave exposure as fixed factors with three levels (low, medium and high), season as fixed factors with four levels (April, June, September and November) and Station as a random factor. Holdfast fauna
Intercept Exposure Season Station Exposure X Season Exposure X Station Season X Station Exp X Sea X Stat
Epiphyte fauna
Df
F
P
Df
F
P
1 2 3 2 6 4 6 12
116 5.0 14 2.7 10 3.0 2.1 1.5
<104 9 103 <104 0.08 <104 0.02 0.06 0.13
1 2 3 2 6 4 6 12
244 5.1 12 2.4 0.80 5.3 0.56 2.5
<104 0.009 <104 0.10 0.58 9 104 0.76 0.01
differences in the conditions between stations with a different wave exposure level (e.g. habitat quality/morphology, food access). At low exposure levels, the fauna fitness seemed to be lower compared to stations with a higher wave exposure. The secondary production was only 3% of the primary production compared to 8% at medium and high exposure levels, and there significantly lower fitness measured as the percentage of egg-carrying crustacean females and juveniles than at stations with a higher exposure. This
a
141
indicates that the animals could allocate less energy to reproduction at low exposure levels compared to medium or high exposure levels, resulting in lower production. At medium and high exposure levels, there were no significant differences in the utilization of primary production (8% at both exposure levels), faunal densities per unit habitat (chapter 3.1), proportions of egg-carrying females or proportions of juveniles (chapter 3.2). A significant higher secondary production at high compared to medium exposure levels (chapter 3.1) were probably driven by a larger habitat size at high exposure stations (Table 1), and thereby suggesting a density dependent regulation of the secondary production by habitat availability. Significant variations between stations in the faunal densities (Table 4) and production (Table 2) were probably resulting from variation in habitat suitability/morphology (see e.g. Hacker and Steneck, 1990; Norderhaug 2004) that was not taken into account in our study. The epiphytic algae are important as shelter for wave surges (Fincham, 1974; Fenwick, 1976), and a high export of mobile fauna from the kelp forest has been reported by Waage-Nielsen et al. (2003) indicating that wave forces are producing a significant loss of fauna from the system. An increasing production with wave exposure suggests that this loss is more than compensated for by factors linked to fauna fitness and habitat availability. The resilience
0,25
0,7
Prop. juveniles
Prop. egg-carrying females
Prop. egg-carrying females
0,25
Prop. egg-carrying females
b 0,25 0,2 0,15 0,1 0,05
0,6 0,5 0,4 0,3 0,2 0,1
0
0
L1
L2
L3
L1
April
L2
L3
June
L1
L2
L3
September
L1
L2
L3
L1
November
L2
L3
L1
April
L2
L3
June
L1
L2
L3
September
L1
L2
L3
November
Prop. juveniles
0,7
0,2 0,15 0,1 0,05
0,6 0,5 0,4 0,3 0,2 0,1 0
0
M1 M2 M3 M1 M2 M3 M1 M2 M3 M1 M2 M3
M1 M2 M3 M1 M2 M3 M1 M2 M3 M1 M2 M3 April
June
September
April
November
June
September
November
Prop. juveniles
0,7
0,2 0,15 0,1 0,05
0,6 0,5 0,4 0,3 0,2 0,1
0
0
H1
H2 April
H3
H1
H2 June
H3
H1
H2
H3
September
H1
H2
H3
November
H1
H2 April
H3
H1
H2 June
H3
H1
H2
H3
September
H1
H2
H3
November
Fig. 5. (a) The proportions of egg-carrying females (S.E.) of the total crustacean populations (isopods, amphipods and decapods) at low (L1-3), medium (m1-3) and high (H1-3) wave exposure stations and at different seasons (sampling months). (b) The proportions of juveniles (S.E.) of the total crustacean populations (isopods, amphipods and decapods) at low, medium and high exposure stations and at different seasons (sampling months).
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Table 5 Results from mixed model on differences in proportions of egg-carrying crustacean females and proportions of juveniles (among all taxa), with wave exposure as fixed factors with three levels (low, medium and high), season as fixed factors with four levels (April, June, September and November) and Station as a random factor.
Holdfast fauna Intercept Exposure Season Station Exposure X Season Exposure X Station Season X Station Exp X Sea X Stat
Egg-carrying females
Juveniles
Df
F
P
Df
F
P
1 2 3 2 6 4 6 12
29 12 9.5 0.22 1.9 3.4 1.7 1.4
<104 <104 <104 0.80 0.10 0.01 0.14 0.20
1 2 3 2 6 4 6 12
48 5.0 137 0.46 8.8 2.1 0.39 0.93
<104 9 103 <104 0.63 <104 0.09 0.88 0.52
of macrophyte communities against physical stress was shown by Christie and Kraufvelin (2004). They reported that a macroalgaeassociated amphipod community could tolerate a daily loss through export of 1e2% of the population without experience a reduction in the population size. In general, faunal densities on holdfasts were less variable between season, wave exposure and station in comparison to epiphytes (Fig. 4). This is to be expected since fauna living on holdfasts live in a more stable and long lasting environment than fauna living on epiphytes (Norderhaug et al., 2002). The holdfastassociated fauna live close to the sea floor hidden in between the holdfast root-like ramifications, while epiphytic algae on the kelp stipes are more exposed to water movement. The total epiphytic volume is also reduced in winter when most of the epiphytic algae die or are reduced, whereas holdfasts remain throughout the life of the kelp (up to more than 10 years). The abundances, biomass (B), production (P) and P/B-ratios for most species was similar to what has been reported in comparable studies (Asmus, 1987; Fredette et al., 1990; Edgar, 1990; Cartes et al., 2001; Christie et al., 2003), but for some crustaceans and molluscs the P/B-ratio was high, including the isopods in the genus Idotea, the decapods Hyas araneus, Ealus pusiolus and Hippolyte varians, the gastropod Ansates pellucida (Linnaeus) and Margarites helicinus (Fabricius) and the bivalves Mytilus edulis, Modiolus modiolus, Turtonia minuta (Fabricius) and H. arctica (Linnaeus) (Table 3). The main reason for a high P/B-ratio for all these species was very low numbers of the largest size classes. This may result from low
survivorship or emigration. Our study cannot fully explain the mechanisms responsible for the observed patterns but earlier studies may give some information and the explanation may differ between the species. Larger invertebrates such as Idotea, H. araneus, A. pellucida have probably low survivorship because they are among the main prey of numerous kelp forest fish (Norderhaug et al., 2005). A. pellucida is associated to the kelp frond (Christie et al., 2003), exposed to predators and wave surge. The P/B-ratio for M. helicinus increased with wave exposure, indicating a high loss from wave surge at high exposure levels. Large decapods like H. araneus are in addition to being found on kelp stipes, also found on the sea floor between the kelps (own observations). Since no sampling was performed in between the kelps in our study, a high P/B-ratio may reflect that larger individuals live on the sea floor in between kelps. M. edulis in the highly mobile plantigrade stage settles temporarily in the kelp forest in large numbers and probably emigrates from the kelp forest later (Bayne, 1964; Norderhaug et al., 2002). Species with low own-motility like bivalves found in this study, including T. minuta and H. arctica may experience significant loss from predation and wave surge (Fincham, 1974; Fenwick, 1976; Norderhaug et al., 2002, 2005).
5. Conclusions The secondary production is large in NE Atlantic kelp forests. Wave strength is highly important for variation in the secondary production by determining habitat size, general conditions and loss from the system. This study showed that the positive effects from wave exposure exceed the negative ones in determining total secondary production. Our study documented that the kelp forest system is increasingly productive with wave exposure level, and this may contribute in explaining a high kelp forest stability and robustness against environmental perturbations (Johnson and Mann, 1988; Norderhaug and Christie, 2009).
Acknowledgements The authors would like to thank Morten Foldager Pedersen of the University of Roskilde, Denmark, for data on canopy kelp densities and comments to earlier versions of the ms, Guri Sogn Andersen and Stein Fredriksen for data on epiphytic volumes and Trine Bekkby NIVA for running the wave exposure model in the study area.
Appendix 1. Published data on reproduction (P: Pelagic larvae, D: Direct development), recruitment period (1: Peak period springautumn, 2: Estimated for taxa or closely related species), cohort production interval (CPI, years), feeding biology (DF: Deposit feeder, D: Detritus feeder, H: Herbivore, P: Predator, O: Omnivore) and relevant references for the dominating (in terms of abundance and size) kelp associated fauna species.
Species (taxa)
Reproduction
Polychaeta Typosyllis sp. Polynoinae
P
Crustacea Isopoda Idotea baltica (Pallas) Idotea granulosa (Rathke)
D D
Amphipoda Lysianassidae Gammarellus homari (Fabricius) Apherusa bispinosa (Bate)
Recruitment
CPI (yrs)
Feeding biology
Key references in addition to own data
<0.5
DF P/O
Kirkegaard (1992), NIVA database Kirkegaard (1992), NIVA database
Summer JulyeSeptember
0.52 1
H/D H/D
Moore (1973), Fredette et al. (1990), Johnson et al. (2001) Hagerman (1966), Moore (1973), Leiffson (1998)
D D
Year-round1 Year-round1
0.52 <1
D/O
Moore and Wong (1996), Johnson et al. (2001) Moore (1973), Saint-Marie (1991), Galan (2000)
D
Year-round1
D
Hagerman (1966), Moore (1973)
Summer
K.M. Norderhaug, H. Christie / Estuarine, Coastal and Shelf Science 95 (2011) 135e144
143
(continued ) Species (taxa)
Reproduction
Recruitment
Apherusa jurinei (Milne-Edwards) Dexamine thea (Boeck) Ampithoe rubricata (Montagu)
D D D
Year-round1 Year-round1 Summer
Lembos websteri (Bate)
D
Corophium bonnellii (G.O. Sars) Jassa falcata (Montagu)
Feeding biology
Key references in addition to own data
1
D D H/D
Year-round1
0.5
D/O
D D
Year-round1 Year-round1
0.25e0.5 0.2e0.5
D/O D/O
Ischyrocerus anguipes (Krøyer) Phtisica marina (Slabber) Caprella septentrionalis (Krøyer)
D D D
Year-round1
Hagerman (1966), Moore (1973) Moore (1973) Skutch (1926), Moore (1973), Nicotri (1977), Borowsky (1983), Norderhaug et al. (2003) Nelson (1980), Moore (1981), Shillaker and Moore (1987), Saint-Marie (1991) Moore (1981), Shillaker and Moore (1987), Saint-Marie (1991) Nair and Anger (1979), Nelson (1980), Borowsky (1983), Galan (2000), Norderhaug et al. (2003) Moore (1973), Galan (2000), Weslawsky and Legezynska (2002)
Decapoda Eualus pusiolus (Krøyer) Hippolyte varians (Leach)
P P
Hyas araneus (Linnaeus)
P
Gastropoda Ansates pellucida (Linnaeus)
P
May
<1
H
Tooth and Pavia (2002), Fredriksen (2003), Graham and Fretter (1947), MarLIN.ac.uk
Margarites helicinus (Fabricius) Lacuna vincta (Montagu)
P
JanuaryeJune, September (MarlIN)
<1
D/H
Fretter and Manly (1977), Martel and Ghia (1991), Moen and Svensen (2000)
Onoba semicostata (Montagu) Rissoa parva (da Costa)
P
Summer
0.25e0.75
D/H
Wigham (1975), Southgate (1982), Wazren (1996), Norderhaug et al. (2003)
Bivalvia Mytilus edulis (Linnaeus) Modiolus modiolus (Linnaeus) Musculus discors (Linnaeus) Turtonia minuta (Fabricius) Hiatella arctica (Linnaeus)
P P D D P
Spring-autumn Spring-autumn Summer Summer Summer
1e2 5e10 2e5 1
S S S S S
MarLIN.ac.uk Wiborg (1946), MarLIN.ac.uk Martel and Ghia (1991), MarLIN.ac.uk Ockelman (1964) Hagerman (1966), Sejr et al. (2002)
Echinodermata Ophiohpolis acuelata (Linnaeus)
P
AprileJuly
D
Mortensen (1924)
Year-round1
CPI (yrs)
D <1
P/D
Summer (Year-round)
Hagerman (1966), Moore (1973), Moen and Svensen (2000), Galan (2000), Norderhaug et al. (2005)
MarLIN.ac.uk
Bittium reticulatum (da Costa)
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Norderhaug, K.M., Christie, H., Fosså, J.H., Fredriksen, S., 2005. Fish-macrofauna interactions in a kelp (Laminaria hyperborea) forest. Journal of Marine Biological Association UK 85, 1279e1286. Norderhaug, K.M., Christie, H., Fredriksen, S., 2007. Is habitat size an important factor for faunal abundances on kelp (Laminaria hyperborea)? Journal of Sea Research 58, 120e124. Norderhaug, K.M., Christie, H., 2009. Sea urchin grazing and kelp re-vegetation in the NE Atlantic. Marine Biology Research 5, 515e528. Norton, T.A., Hiscock, K., Kitching, J.A., 1977. The ecology of Lough Ine. XX. The Laminaria forest at Carrigathorna. Journal of Ecology 65, 919e941. Ockelman, K.W., 1964. Turtonia minuta (Fabricius) a neotonous venerecean bivalve. Ophelia 1, 121e146. Pinheiro, J.C., Bates, D.M., 2000. Mixed-Effects Models in S and S-PLUS. Springer Verlag, New York, 528 pp. Rinde, E., 2009. Dokumentasjon av modellerte marine Naturtyper i DNs Naturbase. Førstegenerasjonsmodeller til kommunenes startpakker for kartlegging av marine naturtyper 2007. NIVA report, 32 pp. Saint-Marie, B., 1991. A review of the reproductive bionomics of aquatic gammeridean amphipods: variation of life history traits with latitude, depth, salinity and superfamily. Hydrobiologia 223, 189e227. Schaal, G., Riera, P., Leroux, C., 2009. Trophic significance of the kelp Laminaria digitata (Lamour.) for the associated food web: a between-sites comparison. Estuarine. Coastal and Shelf Science 85, 565e572. Schaal, G., Riera, P., Leroux, C., 2010. Trophic ecology in a Northern Brittany (Batz Island, France) kelp (Laminaria digitata) forest, as investigated through stable isotopes and chemical assays. Journal of Sea Research 63, 24e35. Sejr, M.K., Sand, M.K., Jensen, T., Petersen, J.K., Christensen, P.B., Rysgaard, S., 2002. Growth and production of Hiatella arctica (Bivalvia) in a high-Arctic fjord (Young Sound, Northeast Greenland). Marine Ecology Progress Series 244, 163e169. Shillaker, R.O., Moore, P.G., 1987. The feeding habits of the amphipods Lembos websteri Bate and Corophium bonellii Milne Edwards. Journal of Experimental Marine Biology and Ecology 110, 93e112. Skadsheim, A., 1989. Regional variation in amphipod life history: effects of temperature and salinity on breeding. Journal of Experimental Marine Biology and Ecology 127, 25e42. Skjoldal, H.R., 2004. The Norwegian Sea Ecosystem. Tapir Academic Press, Trondheim, 555 pp. Skutch, A.F., 1926. On the habits and ecology of the tube-building amphipod Ampithoe rubricata Montagu. Ecology 7, 481e502. Southgate, T., 1982. Studies on an intertidal population of Rissoa parva (Gastropoda: Prosobranchia) in south-west Ireland. Journal of Natural History 16, 183e194. Toth, G.B., Pavia, H., 2002a. Intraplant habitat and feeding preference of two gastropod herbivores inhabiting the kelp Laminaria hyperborea. Journal of Marine Biological Association UK 82, 243e247. Toth, G.B., Pavia, H., 2002b. Lack of phlorotannin induction in the kelp Laminaria hyperborea in response to grazing by two gastropod herbivores. Marine Biology 140, 403e409. Vetter, E.W., 1995. Detritus-based patches of high secondary production in the nearshore benthos. Marine Ecology Progress Series 120, 251e262. Vetter, E.W., 1996. Secondary production of a Southern California Nebalia (Crustacea: Leptrostraca). Marine Ecology Progress Series 137, 95e101. Vahl, O., 1983. Mucus drifting in the limpet Helcion (¼Patina) pellucida (Prosobranchia, Patellidae). Sarsia 68, 209e211. Waren, A., 1996. Ecology and systematics of the North European species of Rissoa and Pusillina (Prosobranchia: Rissoidae). Journal of Marine Biological Association UK 76, 1013e1059. Weslawsky, J.M., Legezynska, J., 2002. Life cycles of some Arctic amphipods. Polish Polar Research 23, 253e264. Wiborg, F.K., 1946. Undersøkelser over oskellet (Modiolus modiolus (L.)). Fiskeridirektoratets Skrifter 8, 85. Wigham, G.D., 1975. The biology and ecology of Rissoa parva (Da Costa) [Gastropoda: Prosobranchia]. Journal of Marine Biological Association UK 55, 45e67. Waage-Nielsen, E., Christie, H., Rinde, E., 2003. Short-term dispersal of kelp fauna to cleared (kelp harvested) areas. Hydrobiologia 503, 77e91.
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Secondary production in a Laminaria hyperborea kelp forest and variation according to wave exposure Kjell M. Norderhaug*, Hartvig Christie Norwegian Institute for Water Research (NIVA), Biodiversity and Eutrophication in Marine Environments, Gaustadaleen 21, NO-0349 Oslo, Norway
a r t i c l e i n f o
a b s t r a c t
Article history: Received 22 November 2010 Accepted 21 August 2011 Available online 29 August 2011
The secondary production of mobile invertebrate fauna in the Laminaria hyperborea (Gunn.) Foslie kelp forest increases with wave exposure level. This faunal group has a key function in transferring kelp carbon to higher levels in the food web. By using a size-frequency method the calculated production was 68 (18) g D.W. m2 yr1 (S.E.) at low, 250 (57) at medium and 308 (64) at high exposure levels. The calculations included 30 macrofauna species, which accounted for 96% of the specimens registered, with Gastropods, amphipods and bivalves being the most abundant taxa. The calculated secondary production is high, but comparable to that previously reported from other macrophyte systems and was 3%, 8% and 8% of the total primary production at low, medium and high exposure levels, respectively. Our results indicate that large quantities of Laminaria kelp are exported from the system, although the production of sessile animals was not taken into account. The most important factor in determining faunal densities and secondary production was probably habitat size but at low exposure levels the percentage of eggcarrying crustacean females and juveniles were lower than at medium and high exposure levels, thereby indicating lower fitness for animals at low exposure stations. Ó 2011 Elsevier Ltd. All rights reserved.
Keywords: secondary production macrofauna kelp forest Laminaria hyperborea
1. Introduction To establish ecosystem production budgets, it is necessary to calculate the production at each trophic level. The production of the level above the primary producers (secondary production) depends on the size of the primary production, how much of the production is transferred to the secondary producers and how much is exported from the system. Theory established from marine pelagic ecosystems suggests a secondary production efficiency of approximately 20% of primary production (Skjoldal, 2004). In several publications, the production of single or a few common marine benthic secondary producers has been presented (e.g. Asmus, 1987; Edgar, 1993; Vetter, 1996; Sejr et al., 2002). However, few attempts have been made to calculate the total benthic secondary production, i.e. the total production of all species of secondary producers, or the production of key faunal groups, though Fredette et al. (1990) calculated the production for 13 species, accounting for 20% of the identified fauna in an eelgrass community, and Brey (1990) analysed 337 datasets, including 138 benthic species. Macrophyte beds are high productive ecosystems and represent habitats which are in rapid decline globally (Nellemann et al., 2009). Thus, their importance for production in the coastal zone * Corresponding author. E-mail address: [email protected] (K.M. Norderhaug). 0272-7714/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2011.08.028
should be given detailed attention. In the NE Atlantic, Kelp Laminaria hyperborea (Gunn.) Foslie forms dense forests in the coastal rocky zone. The estimated annual production in well-developed forests can be as high as 9000 g D.W. m2 (3000 g C m2, Abdullah and Fredriksen, 2004), while along the Norwegian coast these forests cover 5800 km2 (Rinde, 2009). The kelp forests support large numbers of secondary producers inhabiting kelp fronds, epiphytic algae on kelp stipes, kelp holdfasts and on the rock in between the kelps (Christie et al., 2003; Jørgensen and Christie, 2003). Numerous sessile animals (sponges, bryozoans and ascidians) are found on kelp stipes (Norton et al., 1977; Bartsch et al., 2008) and mobile invertebrate fauna are found in high densities on epiphytic algae on the kelp stipes and on kelp holdfasts (Moore, 1973; Norderhaug et al., 2002). More than 100,000 mobile invertebrates per square metre are found on kelp stipes and holdfasts in well-developed kelp forests (Christie et al., 2003). While larger invertebrates and in particular sea urchins Strongylocentrotus droebachiensis (O.F. Müller) are important secondary consumers controlling large barren ground areas on the Norwegian coast, they are scarce inside dense kelp forest (Norderhaug and Christie, 2009). By mainly feeding on kelp detritus (Fredriksen, 2003; Norderhaug et al., 2003; Bartsch et al., 2008) and being the main prey for kelp forest-associated fish (Fredriksen, 2003; Norderhaug et al., 2005; Schaal et al., 2010), the mobile fauna has a key
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function in transferring kelp carbon to higher ecosystem levels. Because of high primary production, secondary production may also be expected to be very high. However, kelp is rigid and contains deterring secondary metabolites (Toth and Pavia, 2002a, b). As a result, most of the kelp standing stock is normally not grazed directly (although sea urchin grazing is an important exception, see Norderhaug and Christie, 2009), but enters the food web in the form of Particulate Organic Matter (POM, Newell et al., 1982; Duggins et al., 1989; Fredriksen, 2003; Norderhaug et al., 2003). By bacterial degradation, the kelp POM increases the food value (Norderhaug et al., 2003), though some primary production is then lost through bacterial respiration and the transfer rate of carbon from primary to secondary producers becomes less efficient. The secondary production is expected to vary considerably according to physical conditions. Wave exposure is probably the single most important factor that affects production in several different ways, both positively and negatively: high wave exposure may increase faunal mobility for species depending on water movement for dispersal (e.g. gastropod rafting, Vahl, 1983). At the same time, high wave exposure is expected to increase the loss of fauna through export from the system (Jørgensen and Christie, 2003; Waage-Nielsen et al., 2003). A significant part of the kelp POM is not consumed inside the kelp forest but instead is lost from the system through export which supports other systems in coastal areas (Vetter, 1995; Bustamante and Branch, 1996). The dependence of secondary producers on kelp material as food decreases with the degree of wave exposure (Schaal et al., 2009). Wave exposure is also of principal importance to habitat size. Kelp density, biomass and size (stipe length and habitat size) as well as the amount of epiphytic algae increases with exposure (Christie et al., 2003). Together with the kelp holdfasts, epiphytic algae comprise the main habitats of the fauna and, during summer and autumn, faunal abundances correlate with habitat size (Norderhaug et al., 2002, 2007). Thus, faunal abundances increase with exposure, and the secondary producers may be limited by habitat size and not by food. The first and primary aim of this study was to test whether the secondary production in a kelp L. hyperborea forest increases with wave exposure level. This was done by calculating the production of the dominating invertebrate species at stations with three levels of wave exposure. The second aim was to test whether the primary production mainly is consumed inside the kelp forest or is lost from the system through export of fragmented kelp. This was assessed by comparing primary production calculations from the same stations (Pedersen pers. comm.) with our calculated secondary production. The third aim was to assess whether differences in the secondary production between stations of different wave exposure level were linked to differences in faunal abundances and habitat size, faunal condition and resource partitioning, and/or loss of fauna from predation and wave surge. This was assessed by comparing faunal abundances, densities and proportions of eggcarrying females and juveniles at stations with different wave exposure level. 2. Methods
Fig. 1. Map of the study area between the islands of Harøy and Sandøy in the Møre archipelago, showing the locations of the nine stations (green: low, yellow: medium and red: high exposure stations) and the predicted level of wave exposure in the area. Wave exposure is modeled according to Isæus (unpublished).
distance to the nearest shore, island or coast) model (Isæus, unpublished), including wind strength and direction (16 directions) averaged over five years (data from the Norwegian Meteorological Institute). Canopy stipes (with epiphytic algae) and holdfasts (i.e. the most important faunal habitats, Christie et al., 2003) were used as sampling units. Three stipes and holdfasts respectively, were randomly sampled at each station and in each season by SCUBA diving and separately enclosed in cotton bags under water. The fauna on each sample was collected by washing with fresh water and sieving (mesh size 250 mm). By the use of this method we collected mobile macrofauna representatively, while sessile animals and meiofauna were not sampled. In the laboratory, the animals were counted and identified according to species or highest possible taxonomic separation, and all species were divided into four to six size classes. The length of a representative number of animals within each size class was measured and dried (60 C for 72 h), and the dry weight (D.W.) of each size class was measured. The lengths and D.W. were then used in production calculations. We used the size-frequency method (Hynes and Coleman, 1968) modified by Hamilton (1969) for calculations of the annual production of each species:
2.1. Experimental design The study was performed in the archipelago along the Møre coast in Norway. Fauna on L. hyperborea kelp was sampled from three replicate stations of three different wave exposure levels (a total of nine stations in a crossed design, see Fig. 1) and from four different seasons (April, June, September and November). Exposure levels (low, medium and high) were predicted from a fetch (i.e. the
P ¼ i
i X qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi Nj Njþ1 Wj Wjþ1 j¼i
Where P is the estimated production, i is the the number of size classes used, Nj is the mean number of individuals in size class j (averaged over seasons) and Wj is the mean dry weight of individuals belonging to size class j.
K.M. Norderhaug, H. Christie / Estuarine, Coastal and Shelf Science 95 (2011) 135e144
Univariate statistical techniques in the SPLUS 7.0 computer package were applied for testing of differences among the studied factors. Differences in faunal abundances, densities per unit habitat and differences in the percentage of egg-carrying females and juveniles were tested by mixed models with wave exposure (three levels) and season (month) as fixed factors and station as a random factor (Pinheiro and Bates, 2000). Differences in the total production were tested by a mixed model with wave exposure level as a fixed factor and station as a random factor. Response data were log transformed. Each test was followed by Tukey’s test for testing pair-wise differences between exposure levels. Table 1 Average density of canopy plants at stations with low, medium and high wave exposure. Habitat size measured as average total Fresh Weight Epiphytic algae per Stipes (EFWS), total EFWM (epiphytic fresh weight m2) in different seasons (sampling months), average EFW m2 throughout the year (across all the sampling seasons), and average HW (holdfast volume ml m2).
Canopy plants (No. m2) EFWS April EFWS June EFWS September EFWS November EFWM April EFWM June EFWM September EFWM November Average EFW m2 HW ml m2
Low
SE
Medium
SE
High
SE
8.9 8.9 23 56 39 79 205 498 347 282 2949
2.7 2.3 6 15 11 6.2 16 41 30 10 75
7.3 21 157 176 108 153 1146 1285 788 843 4449
2.1 7.3 42 22 16 15 88 46 34 35 102
12.3 62 116 134 159 763 1427 1648 1956 1448 7876
0.2 13 30 15 38 2.6 6 3 7.6 21 5.6
3.1. Fauna abundances, densities and secondary production Altogether, 275,887 animals were identified according to species or higher taxa level. The total number of animals per square metre increased significantly with exposure level (Fig. 2, Table 2, Tukey lower-upper bound: Medium-Low: 0.31e0.47 and HighMedium: 0.08e0.24). At most stations, the abundances increased from April to June and peaked in September, while in November the total number of animals decreased. 90000
No. per square meter
80000 70000 60000 50000 40000 30000 20000 10000 0
L1
L2 April
L3 L1
L2 June
L3
L1
L2
L3 L1
September
L2
L3
November
90000 80000
No. per square meter
2.2. Data analysis
3. Results
70000 60000 50000 40000 30000 20000 10000 0
M1 M2 M3 M1 M2 M3 M1 M2 M3 M1 M2 M3 April
June
September
November
90000 80000
No. per square meter
This widely used method is well suited for calculating benthic invertebrate production (Cartes et al., 2001). In cases in which the Cohort Production Interval (CPI, time from hatching to attaining the largest size class, see Vetter, 1996) was known, it was accounted for by multiplying the yearly production by 1/CPI (years). The CPI for each species is listed in Appendix 1. The polychaetes and amphipods in the family Lysianassidae were only identified to genus or family level. In the case of Lysianassidae, the CPI according to common species in the family (Moore and Wong, 1996) and from the same region was used because there are considerable differences in the reproduction history between regions (Skadsheim, 1989; Saint-Marie, 1991). In the case of amphipods this is valid since reproductive patterns for amphipods follow taxonomic lines (Nelson, 1980). Numbers per square metre at each station were calculated using the numbers of animals on stipes and holdfasts multiplied by the average number of canopy kelps per square metre (Table 1). Egg-carrying females and juveniles for species with brood pouch and direct development, i.e. amphipods and isopods, were counted and the percentage of egg-carrying females and juveniles was calculated for each species. These ratios were used as indicators for fitness and differences in resource partitioning between wave exposure levels, assuming that fit animals living in good conditions can allocate more energy into reproduction than less fit animals living in poor conditions (Begon et al., 1990). Fresh weight of epiphytic algae and holdfast volume (according to Jones, 1971) was measured and represented habitat size, The average densities of canopy plants at each station with a low, medium or high degree of wave exposure are shown in Table 1 and were used in calculations of fauna abundances and production per m2. Habitat size is presented from different seasons (sampling months) and as the average habitat size throughout the year (with average densities of canopy plants, data from Pedersen). Average sizes of the sampled holdfasts (ml m2) are also presented.
137
70000 60000 50000 40000 30000 20000 10000 0
H1 H2 H3 H1 H2 H3 H1 H2 H3 H1 H2 H3 April
June
September
November
Fig. 2. The average total number (No. m2 S.E.) of animals at stations with low (L13), medium (M1-3) and high (H1-3) wave exposure levels and from different seasons.
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Table 2 Results from mixed model on differences in the total abundances m2 of all identified mobile fauna and the total secondary production yr1 m2 of the 30 dominating mobile species, with wave exposure as a fixed factor with three levels (low, medium and high), season as a fixed factor with four levels (April, June, September and November) and Station as a random factor.
Fauna abundance Intercept Exposure Season Station Exposure x Season Exposure x Station Season x Station Exposure x Season x Station Secondary production Intercept Exposure Station Exposure x Station
Df
F
P
1 2 3 2 6 4 6 12
12,098 146 49 0.53 4.2 8.7 1.1 1.4
<104 <104 <104 0.59 0.001 <104 0.39 0.19
1 2 2 4
1233 88 1.2 4.0
<104 <104 0.31 0.02
The species specific production was calculated for the 30 most numerous and large species (Table 3). They accounted for 96% of the identified specimens in total and include two polychaete, two isopod, twelve amphipod, three decapod, five gastropod, five bivalve and one echinoderm species/taxa. The total secondary production increased significantly with exposure (Fig. 3, Table 2, Tukey lower-upper bound: Low-Medium: 1.3e0.7 and HighMedium: 0.2e0.7) and was 68 (18 g D.W. m2 yr1 SE) at low, 250 (57) at medium, and 308 (64) at high exposure levels (Fig. 3). The largest contributors to the total production were mussels at low and medium exposure levels, particularly the suspension feeding and burrowing mussel Hiatella arctica (Linnaeus), with biomasses of 1.7 (g D.W. m2 0.26 S.E.), 1.8 (0.38) and 2.6 (0.47) respectively at stations with low, medium and high wave exposure level and production (g D.W. m2 yr1 SE) of 23 (2.1), 39 (2.1) and 40 (4.7) (Table 3). Additionally, the biomass and production of juvenile Modiolus modiolus (Linnaeus) and Mytilus edulis (Linnaeus) was high. At medium and high exposure, gastropods (Lacuna vincta (Montagu) and Rissoa parva (Da Costa)) and amphipods (particularly Jassa falcata (Montagu), but also Apherusa jurinei (MilneEdwards), Ampithoe rubricata (Montagu) and Lembos websteri (Bate)) contributed much. Decapods (Hyas araneus (Linnaeus), Hyppolyte varians (Leach) and Eualus pusiolus (Krøyer)), isopods (Idotea baltica (Pallas) in particular) and brittle stars Ophiopholis acuelata (Linnaeus) also contributed significantly to the total production at medium and highly exposed stations. Idotea granulosa and the amphipod Gammarellus homari (Fabricius) were not found at low exposure stations. Densities of fauna per unit habitat (g fresh weight epiphytic algae and ml holdfast, respectively) were highest during June and/ or September (Fig. 4a, b). The densities on epiphytes and holdfasts were higher at medium and high exposure levels than at low exposure levels (Fig. 4a, b, Table 4, Tukey lower-upper bound: LowMedium: 0.17e0.02 (holdfast fauna), 0.35e0.05 (epiphyte fauna) and High-Medium: 0.13e0.01 (holdfast fauna), 0.29e0.01(epiphyte fauna). In general, there were smaller differences between exposure levels in the densities on the holdfasts than on the epiphytes, but there were significant differences between stations both on epiphytes and holdfasts (Fig. 4a, b). 3.2. Reproduction patterns The proportions of egg-carrying crustacean females were highest in April and June when more than 10% of the total populations were females carrying eggs at medium and high exposure levels (Fig. 5a).
Throughout the year there was higher average proportions of eggcarrying females at medium and high exposure levels than on low exposed levels (Table 5, Tukey lower-upper bound: LowMedium: 0.06e0.01 and High-Medium: 0.01e0.04). The proportions of juveniles were high in June when they comprised more than half the crustacean populations and low during the rest of the year (Fig. 5b). Throughout the year there was significantly higher average proportions of juveniles at high and medium exposure levels compared to low exposed levels (Table 5, Tukey lower-upper bound: Low-Medium: 0.09e0.008 and HighMedium: 0.05e0.04). 4. Discussion The secondary production of mobile macrofauna associated to L. hyperborea kelp forest is high but comparable to that reported from other macrophyte systems (e.g. Fredette et al., 1990). It varied between 68 and 308 D.W. g m2 year1at the stations used in this study. Our study is one of the first from the marine environment to calculate the total production of a faunal group with a key function in transferring primary production to higher ecosystem levels (but see Fredette et al. (1990) and Brey (1990)). Coastal macrophyte communities are among the ecosystems with the highest primary production on the planet (Nellemann et al., 2009). The primary production at the stations investigated was approximately 2300, 3000 and 4000 g dry weight per square metre per year (calculated from Pedersen pers. comm.). Abdullah and Fredriksen (2004) demonstrated that a primary production of 9000 g D.W. m2 yr1 (3000 g C m2 yr1) is not uncommon in kelp forests in Norway, and Christie et al. (2003) found up to 10 times the abundances of fauna per square meter as found in our study, indicating the possibility of a very large secondary production in some NE Atlantic kelp forests. There was a significantly increasing production of mobile macrofauna with exposure from low to medium and high wave exposure level. For that reason, the secondary production of the investigated faunal group was 3%, 8% and 8%, respectively, of the primary production at low, medium and high exposure levels whereas general theory suggests a secondary production of 20% of production efficiency in marine systems (Skjoldal, 2004). Our results suggest that the fauna is probably not food limited, and only a small part of the kelp production is utilized in the kelp forest (Hawkins et al., 1992). Kelp forests represent excess source systems which can provide kelp material to other coastal ecosystems (Vetter, 1995; Bustamante and Branch, 1996). However, sessile animals (Norton et al., 1977; Bartsch et al., 2008) were not taken into account. Although they are less important for transferring kelp primary production to higher levels in the food web than the mobile fauna (Norderhaug et al., 2005; Bartsch et al., 2008), they may contribute significantly to the secondary production. Also, our calculations are conservative and may be underestimated for several reasons. Only fauna from the most important habitats, i.e. holdfasts and epiphytes on kelp stipes (Christie et al., 2003) was sampled, and animals on kelp fronds, understory plants and the sea floor in between plants were not taken into account. Egg production was not included in our calculations. The food quality of kelp is low until it has been degraded by bacteria; as a consequence, some carbon is lost through respiration in the microbial loop before the kelp material is consumed by macrofauna (Norderhaug et al., 2003). Other error sources include the fact that the fauna have a different feeding ecology, and although their main food source is degraded kelp material (Norderhaug et al., 2003; Fredriksen, 2003), some are omnivores, carnivores and detritivores (as discussed by Benke et al., 2001), and to a certain extent we compared animals at different levels in the food web.
Table 3 The average yearly biomass (B, D.W. þ- SE), production (g D.W. per year) and P/B-ratios for the dominating species. Low
Medium
Typosyllis spp. Polynoinae I. baltica I. granulosa Lysinassidae G. homari A. bispinosa A. jurinei D. thea A. rubricata L. websteri C. bonelli J. falcata I.anguipes P. marina C. septentrionalis E. pusiolus H. varians H. araneus A. pellucida M. helicinus L. vincta O. semicostata R. parva B. reticulatum M edulis M. modiolus M. discors T. minuta H. arctica O. acuelata
0.13 (0.05) 1.3 (0.2) 0.09 (0.01) e 0.02 (0.01) e 4 104 4 103 0.14 0.23 0.17 0.06 0.50 0.06 0.01 0.03 0.10 0.14 0.03 104 0.26 0.78 0.10 0.80 0.07 0.15 0.35 0.05 9 104 1.7 1.1
(104) (2 103) (0.04) (0.14) (0.07) (0.02) (0.11) (0.01) (2 103) (0.01) (0.03) (0.09) (0.52) (106) (0.19) (0.23) (0.03) (0.25) (0.02) (0.04) (0.22) (0.01) (104) (0.26) (0.05)
P (S.E.)
P/B (S.E.)
B (S.E.)
0.20 (0.13) 2.4 (1.7) 4 103 (104) e 0.17 (0.1) e 9 104 (5 104) 0.02 (0.01) 0.76 (0.42) 0.20 (0.13) 1.2 (0.17) 0.12 (0.09) 3.2 (1.0) 0.21 (0.06) 0.03 (0.01) 0.13 (0.08) 0.39 (0.07) 4.9 (1.9) 2.2 (0.15) 7 103 (2 105) 1.5 (1.7) 3.9 (0.51) 0.32 (0.09) 2.5 (0.67) 0.42 (0.27) 4.2 (0.23) 3.1 (0.31) 0.25 (0.03) 0.01 (9 104) 23 (2.1) 0.67 (0.07)
1.6 1.8 21 e 10 e 2.3 5.0 5.4 0.84 7.0 2.0 6.4 3.8 2.7 4.2 4.0 35 74 68 5.7 5.0 3.1 3.1 6.4 26 8.8 5.7 10 13 0.58
0.51 2.2 0.78 2 103 0.11 0.02 103 3.0 0.11 0.71 0.88 0.45 6.8 0.21 9 103 0.02 0.29 0.13 0.09 0.03 0.05 7.2 0.08 7.0 0.03 0.92 0.53 0.17 103 1.8 0.48
(0.35) (1.7) (0.03) (3.6) (4.0) (0.13) (0.53) (0.63) (1.2) (0.65) (0.75) (1.2) (0.06) (0.53) (0.36) (2.2) (33) (1.3) (3.0) (2.1) (1.2) (0.46) (0.99) (3.3) (2.1) (0.69) (0.39) (0.27) (0.16)
High P (S.E.) (0.15) (0.7) (0.7) (104) (5 104) (8 103) (3 104) (0.4) (0.02) (0.34) (0.12) (0.02) (1.2) (0.04) (2 103) (7 103) (0.12) (0.11) (0.09) (9 103) (0.05) (1.1) (0.03) (1.1) (0.02) (0.18) (0.12) (0.05) (2 104) (0.38) (1.73)
0.44 3.1 20 0.06 0.49 0.24 4 103 5.6 0.37 1.6 4.2 0.23 29 0.58 0.02 0.06 10 7.1 7.1 1.2 1.4 33 0.16 12 0.12 46 13 1.7 0.03 39 0.17
P/B (S.E.) (0.17) (0.6) (0.4) (5 103) (104) (104) (104) (1.8) (0.46) (1.5) (2.8) (0.27) (2.2) (0.29) (0.04) (0.06) (1.0) (1.5) (0.91) (1.5) (0.82) (10) (0.03) (3.8) (0.24) (2.9) (0.85) (0.19) (3 104) (2.1) (0.86)
0.88 1.4 26 30 4.6 19 3.2 1.9 3.4 2.3 4.8 0.50 4.3 2.7 1.8 2.5 35 53 53 45 26 4.7 2.1 1.8 3.6 49 24 10 22 21 0.35
(0.86) (1.7) (2.1) (1.0) (0.3) (1.9) (0.1) (0.4) (1.2) (0.3) (2.2) (0.54) (0.55) (0.3) (1.0) (0.8) (0.11) (0.24) (0.24) (2.1) (7.2) (1.0) (1.3) (1.0) (3.7) (0.65) (2.1) (0.41) (1.0) (0.14) (0.70)
B (S.E.)
2
3
8
2
0.43 1.5 1.6 103 0.11 0.03 103 3.3 0.30 1.5 1.0 0.42 8.5 0.64 103 0.02 0.01 0.23 0.03 0.04 0.02 14 0.09 7.3 0.02 0.72 0.92 0.11 103 2.6 8.7
(0.05) (0.5) (0.5) (2 104) (0.03) (0.01) (3 104) (0.08) (8 103) (0.20) (0.25) (0.07) (3.2) (0.03) (2 103) (0.01) (0.04) (0.01) (8 103) (6 103) (6 103) (1.8) (0.01) (0.73) (0.01) (0.19) (0.19) (0.02) (5 104) (0.47) (0.61)
P (S.E.)
P/B (S.E.)
0.30 3.1 3.1 0.03 0.77 0.42 0.03 10 1.6 3.2 6.3 0.44 51 2.0 0.02 0.08 0.02 8.9 1.4 1.7 1.8 73 0.27 19 0.10 23 14 0.81 0.02 40 5.9
0.70 2.2 2.1 18 6.9 19 11 3.1 5.1 2.1 6.5 1.1 6.0 3.1 2.0 3.7 1.8 39 53 43 74 5.1 3.0 2.6 5.4 32 15 7.1 16 16 0.68
(0.40) (2.2) (2.2) (0.01) (0.1) (0.4) (0.03) (0.8) (0.06) (0.50) (1.3) (0.23) (8.7) (0.08) (5 103) (1.1) (4 103) (0.21) (0.64) (1.2) (0.76) (4.2) (0.06) (2.1) (0.03) (2.0) (2.2) (0.04) (5 103) (4.7) (1.7)
(0.71) (1.1) (1.1) (2.6) (0.88) (10) (10) (0.90) (0.19) (0.61) (1.5) (0.90) (0.64) (0.11) (0.55) (0.51) (0.71) (0.19) (25) (4.3) (23) (1.4) (0.95) (0.47) (3.1) (4.2) (1.9) (0.48) (0.21) (0.52) (0.28)
K.M. Norderhaug, H. Christie / Estuarine, Coastal and Shelf Science 95 (2011) 135e144
B (S.E.)
139
140
K.M. Norderhaug, H. Christie / Estuarine, Coastal and Shelf Science 95 (2011) 135e144
120 Polychaeta Isopoda
100
Amphipoda
Production
Decapoda Gastropda
80
Bivalvia Ophiuroidea
60
40
20
0
Low
Medium 2
Fig. 3. The average total annual secondary production (g D.W. m
The most likely explanation for increasing secondary production with exposure is that habitat size is of primary importance for faunal densities, and thus for the total secondary production. In accordance with the findings of Christie et al. (2003) and
year S.E.) at stations with low, medium and high exposure.
Norderhaug et al. (2007), habitat size and faunal densities increase with exposure. At all exposure levels, faunal densities peaked in summer during the main reproduction period. A significant divergence from this correlation was most likely attributed to other
b
90 80 70 60 50 40 30 20 10
4 3 2 1 0
0
L1
L2
L3
April
L1
L2
L3
June
L1
L2
L3
September
L1
L2
L1
L3
90
6
80 70
5
60 50 40 30 20 10
L3
L1
L2 June
L3
L1
L2
L3
September
L1
L2
L3
November
4 3 2 1 0
0
M1 M2 M3 M1 M2 M3 M1 M2 M3 M1 M2 M3
M1 M2 M3 M1 M2 M3 M1 M2 M3 M1 M2 M3 April
June
September
April
November
90
June
September
November
6
80 70 60
No. per ml
No. per g algae
L2 April
November
No. per ml
No. per g algae
6 5
No. per ml
No. per g algae
a
High
50 40 30 20
5 4 3 2 1
10
0
0
H1 H2 H3
H1 H2 H3
H1 H2 H3
H1 H2 H3
April
June
September
November
H1 H2 April
H3
H1 H2 June
H3 H1
H2 H3
September
H1
H2 H3
November
Fig. 4. (a) Densities (S.E.) of fauna per g (fresh weight) algae epiphytic algae at stations with low (L1-3), medium (M1-3) and high (H1-3) wave exposure level and from different season (sampling month). (b) No. (S.E.) of fauna per ml holdfast volume at stations with low (L1-3), medium (M1-3) and high (H1-3) wave exposure level and from different season (sampling month).
K.M. Norderhaug, H. Christie / Estuarine, Coastal and Shelf Science 95 (2011) 135e144 Table 4 Results from mixed model on differences in faunal densities (per unit habitat) on kelp holdfasts and epiphytic algae on the kelp stipe, with wave exposure as fixed factors with three levels (low, medium and high), season as fixed factors with four levels (April, June, September and November) and Station as a random factor. Holdfast fauna
Intercept Exposure Season Station Exposure X Season Exposure X Station Season X Station Exp X Sea X Stat
Epiphyte fauna
Df
F
P
Df
F
P
1 2 3 2 6 4 6 12
116 5.0 14 2.7 10 3.0 2.1 1.5
<104 9 103 <104 0.08 <104 0.02 0.06 0.13
1 2 3 2 6 4 6 12
244 5.1 12 2.4 0.80 5.3 0.56 2.5
<104 0.009 <104 0.10 0.58 9 104 0.76 0.01
differences in the conditions between stations with a different wave exposure level (e.g. habitat quality/morphology, food access). At low exposure levels, the fauna fitness seemed to be lower compared to stations with a higher wave exposure. The secondary production was only 3% of the primary production compared to 8% at medium and high exposure levels, and there significantly lower fitness measured as the percentage of egg-carrying crustacean females and juveniles than at stations with a higher exposure. This
a
141
indicates that the animals could allocate less energy to reproduction at low exposure levels compared to medium or high exposure levels, resulting in lower production. At medium and high exposure levels, there were no significant differences in the utilization of primary production (8% at both exposure levels), faunal densities per unit habitat (chapter 3.1), proportions of egg-carrying females or proportions of juveniles (chapter 3.2). A significant higher secondary production at high compared to medium exposure levels (chapter 3.1) were probably driven by a larger habitat size at high exposure stations (Table 1), and thereby suggesting a density dependent regulation of the secondary production by habitat availability. Significant variations between stations in the faunal densities (Table 4) and production (Table 2) were probably resulting from variation in habitat suitability/morphology (see e.g. Hacker and Steneck, 1990; Norderhaug 2004) that was not taken into account in our study. The epiphytic algae are important as shelter for wave surges (Fincham, 1974; Fenwick, 1976), and a high export of mobile fauna from the kelp forest has been reported by Waage-Nielsen et al. (2003) indicating that wave forces are producing a significant loss of fauna from the system. An increasing production with wave exposure suggests that this loss is more than compensated for by factors linked to fauna fitness and habitat availability. The resilience
0,25
0,7
Prop. juveniles
Prop. egg-carrying females
Prop. egg-carrying females
0,25
Prop. egg-carrying females
b 0,25 0,2 0,15 0,1 0,05
0,6 0,5 0,4 0,3 0,2 0,1
0
0
L1
L2
L3
L1
April
L2
L3
June
L1
L2
L3
September
L1
L2
L3
L1
November
L2
L3
L1
April
L2
L3
June
L1
L2
L3
September
L1
L2
L3
November
Prop. juveniles
0,7
0,2 0,15 0,1 0,05
0,6 0,5 0,4 0,3 0,2 0,1 0
0
M1 M2 M3 M1 M2 M3 M1 M2 M3 M1 M2 M3
M1 M2 M3 M1 M2 M3 M1 M2 M3 M1 M2 M3 April
June
September
April
November
June
September
November
Prop. juveniles
0,7
0,2 0,15 0,1 0,05
0,6 0,5 0,4 0,3 0,2 0,1
0
0
H1
H2 April
H3
H1
H2 June
H3
H1
H2
H3
September
H1
H2
H3
November
H1
H2 April
H3
H1
H2 June
H3
H1
H2
H3
September
H1
H2
H3
November
Fig. 5. (a) The proportions of egg-carrying females (S.E.) of the total crustacean populations (isopods, amphipods and decapods) at low (L1-3), medium (m1-3) and high (H1-3) wave exposure stations and at different seasons (sampling months). (b) The proportions of juveniles (S.E.) of the total crustacean populations (isopods, amphipods and decapods) at low, medium and high exposure stations and at different seasons (sampling months).
142
K.M. Norderhaug, H. Christie / Estuarine, Coastal and Shelf Science 95 (2011) 135e144
Table 5 Results from mixed model on differences in proportions of egg-carrying crustacean females and proportions of juveniles (among all taxa), with wave exposure as fixed factors with three levels (low, medium and high), season as fixed factors with four levels (April, June, September and November) and Station as a random factor.
Holdfast fauna Intercept Exposure Season Station Exposure X Season Exposure X Station Season X Station Exp X Sea X Stat
Egg-carrying females
Juveniles
Df
F
P
Df
F
P
1 2 3 2 6 4 6 12
29 12 9.5 0.22 1.9 3.4 1.7 1.4
<104 <104 <104 0.80 0.10 0.01 0.14 0.20
1 2 3 2 6 4 6 12
48 5.0 137 0.46 8.8 2.1 0.39 0.93
<104 9 103 <104 0.63 <104 0.09 0.88 0.52
of macrophyte communities against physical stress was shown by Christie and Kraufvelin (2004). They reported that a macroalgaeassociated amphipod community could tolerate a daily loss through export of 1e2% of the population without experience a reduction in the population size. In general, faunal densities on holdfasts were less variable between season, wave exposure and station in comparison to epiphytes (Fig. 4). This is to be expected since fauna living on holdfasts live in a more stable and long lasting environment than fauna living on epiphytes (Norderhaug et al., 2002). The holdfastassociated fauna live close to the sea floor hidden in between the holdfast root-like ramifications, while epiphytic algae on the kelp stipes are more exposed to water movement. The total epiphytic volume is also reduced in winter when most of the epiphytic algae die or are reduced, whereas holdfasts remain throughout the life of the kelp (up to more than 10 years). The abundances, biomass (B), production (P) and P/B-ratios for most species was similar to what has been reported in comparable studies (Asmus, 1987; Fredette et al., 1990; Edgar, 1990; Cartes et al., 2001; Christie et al., 2003), but for some crustaceans and molluscs the P/B-ratio was high, including the isopods in the genus Idotea, the decapods Hyas araneus, Ealus pusiolus and Hippolyte varians, the gastropod Ansates pellucida (Linnaeus) and Margarites helicinus (Fabricius) and the bivalves Mytilus edulis, Modiolus modiolus, Turtonia minuta (Fabricius) and H. arctica (Linnaeus) (Table 3). The main reason for a high P/B-ratio for all these species was very low numbers of the largest size classes. This may result from low
survivorship or emigration. Our study cannot fully explain the mechanisms responsible for the observed patterns but earlier studies may give some information and the explanation may differ between the species. Larger invertebrates such as Idotea, H. araneus, A. pellucida have probably low survivorship because they are among the main prey of numerous kelp forest fish (Norderhaug et al., 2005). A. pellucida is associated to the kelp frond (Christie et al., 2003), exposed to predators and wave surge. The P/B-ratio for M. helicinus increased with wave exposure, indicating a high loss from wave surge at high exposure levels. Large decapods like H. araneus are in addition to being found on kelp stipes, also found on the sea floor between the kelps (own observations). Since no sampling was performed in between the kelps in our study, a high P/B-ratio may reflect that larger individuals live on the sea floor in between kelps. M. edulis in the highly mobile plantigrade stage settles temporarily in the kelp forest in large numbers and probably emigrates from the kelp forest later (Bayne, 1964; Norderhaug et al., 2002). Species with low own-motility like bivalves found in this study, including T. minuta and H. arctica may experience significant loss from predation and wave surge (Fincham, 1974; Fenwick, 1976; Norderhaug et al., 2002, 2005).
5. Conclusions The secondary production is large in NE Atlantic kelp forests. Wave strength is highly important for variation in the secondary production by determining habitat size, general conditions and loss from the system. This study showed that the positive effects from wave exposure exceed the negative ones in determining total secondary production. Our study documented that the kelp forest system is increasingly productive with wave exposure level, and this may contribute in explaining a high kelp forest stability and robustness against environmental perturbations (Johnson and Mann, 1988; Norderhaug and Christie, 2009).
Acknowledgements The authors would like to thank Morten Foldager Pedersen of the University of Roskilde, Denmark, for data on canopy kelp densities and comments to earlier versions of the ms, Guri Sogn Andersen and Stein Fredriksen for data on epiphytic volumes and Trine Bekkby NIVA for running the wave exposure model in the study area.
Appendix 1. Published data on reproduction (P: Pelagic larvae, D: Direct development), recruitment period (1: Peak period springautumn, 2: Estimated for taxa or closely related species), cohort production interval (CPI, years), feeding biology (DF: Deposit feeder, D: Detritus feeder, H: Herbivore, P: Predator, O: Omnivore) and relevant references for the dominating (in terms of abundance and size) kelp associated fauna species.
Species (taxa)
Reproduction
Polychaeta Typosyllis sp. Polynoinae
P
Crustacea Isopoda Idotea baltica (Pallas) Idotea granulosa (Rathke)
D D
Amphipoda Lysianassidae Gammarellus homari (Fabricius) Apherusa bispinosa (Bate)
Recruitment
CPI (yrs)
Feeding biology
Key references in addition to own data
<0.5
DF P/O
Kirkegaard (1992), NIVA database Kirkegaard (1992), NIVA database
Summer JulyeSeptember
0.52 1
H/D H/D
Moore (1973), Fredette et al. (1990), Johnson et al. (2001) Hagerman (1966), Moore (1973), Leiffson (1998)
D D
Year-round1 Year-round1
0.52 <1
D/O
Moore and Wong (1996), Johnson et al. (2001) Moore (1973), Saint-Marie (1991), Galan (2000)
D
Year-round1
D
Hagerman (1966), Moore (1973)
Summer
K.M. Norderhaug, H. Christie / Estuarine, Coastal and Shelf Science 95 (2011) 135e144
143
(continued ) Species (taxa)
Reproduction
Recruitment
Apherusa jurinei (Milne-Edwards) Dexamine thea (Boeck) Ampithoe rubricata (Montagu)
D D D
Year-round1 Year-round1 Summer
Lembos websteri (Bate)
D
Corophium bonnellii (G.O. Sars) Jassa falcata (Montagu)
Feeding biology
Key references in addition to own data
1
D D H/D
Year-round1
0.5
D/O
D D
Year-round1 Year-round1
0.25e0.5 0.2e0.5
D/O D/O
Ischyrocerus anguipes (Krøyer) Phtisica marina (Slabber) Caprella septentrionalis (Krøyer)
D D D
Year-round1
Hagerman (1966), Moore (1973) Moore (1973) Skutch (1926), Moore (1973), Nicotri (1977), Borowsky (1983), Norderhaug et al. (2003) Nelson (1980), Moore (1981), Shillaker and Moore (1987), Saint-Marie (1991) Moore (1981), Shillaker and Moore (1987), Saint-Marie (1991) Nair and Anger (1979), Nelson (1980), Borowsky (1983), Galan (2000), Norderhaug et al. (2003) Moore (1973), Galan (2000), Weslawsky and Legezynska (2002)
Decapoda Eualus pusiolus (Krøyer) Hippolyte varians (Leach)
P P
Hyas araneus (Linnaeus)
P
Gastropoda Ansates pellucida (Linnaeus)
P
May
<1
H
Tooth and Pavia (2002), Fredriksen (2003), Graham and Fretter (1947), MarLIN.ac.uk
Margarites helicinus (Fabricius) Lacuna vincta (Montagu)
P
JanuaryeJune, September (MarlIN)
<1
D/H
Fretter and Manly (1977), Martel and Ghia (1991), Moen and Svensen (2000)
Onoba semicostata (Montagu) Rissoa parva (da Costa)
P
Summer
0.25e0.75
D/H
Wigham (1975), Southgate (1982), Wazren (1996), Norderhaug et al. (2003)
Bivalvia Mytilus edulis (Linnaeus) Modiolus modiolus (Linnaeus) Musculus discors (Linnaeus) Turtonia minuta (Fabricius) Hiatella arctica (Linnaeus)
P P D D P
Spring-autumn Spring-autumn Summer Summer Summer
1e2 5e10 2e5 1
S S S S S
MarLIN.ac.uk Wiborg (1946), MarLIN.ac.uk Martel and Ghia (1991), MarLIN.ac.uk Ockelman (1964) Hagerman (1966), Sejr et al. (2002)
Echinodermata Ophiohpolis acuelata (Linnaeus)
P
AprileJuly
D
Mortensen (1924)
Year-round1
CPI (yrs)
D <1
P/D
Summer (Year-round)
Hagerman (1966), Moore (1973), Moen and Svensen (2000), Galan (2000), Norderhaug et al. (2005)
MarLIN.ac.uk
Bittium reticulatum (da Costa)
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