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Exploring the role of macroalgal traits on the feeding behaviour of a generalist herbivore in Malaysian waters

  • Lim Wai Yin

    Lim Wai Yin received her Bachelor’s degree in applied biology, majoring in marine and aquatic systems, from the Science University of Malaysia in 2016, and has recently joined the Master’s degree program in the field of marine sciences in Universiti Malaya. Prior to her graduate study, she had been managing the aquatic life’s culturing environment in an aquaculture farm. Her recent research focuses on studying chemical ecology of autotroph-herbivore interactions in tropical marine ecosystems.

         , Lim Phaik Eem

    Professor Lim Phaik Eem is the Deputy Director and Head of the Marine Biotechnology Research Unit at the Institute of Ocean and Earth Sciences, Universiti Malaya. She is an internationally renowned phycologist in the South-East Asian region, where she has actively worked on the taxonomy and conducted phylogenetic studies of seaweeds since the 1990s. She has published more than 100 refereed journal articles and several book chapters.

         , Affendi Yang Amri

    Affendi Yang Amri is a research officer at the Institute of Ocean and Earth Sciences, Universiti Malaya. He is ta scientific advisor for Reef Check Malaysia which is an NGO that monitors coral reefs using citizen science volunteers and works closely with the Federal Marine Parks of Malaysia. His present research interests are studying the local mass coral bleaching phenomena and ecological connectivity between adjacent coral reef, seagrass and mangrove habitats.

         , Song Sze Looi

    Dr. Song Sze Looi obtained her PhD from the University of Malaya in 2013. She is currently an assistant professor at the Xiamen University Malaysia. To date, she has published more than 30 articles with approximately 300 citations. She has extensive experience in biotechnology, genetic, and genomic research.

         and Acga Cheng

    Dr. Acga Cheng is a senior lecturer at Universiti Malaya. She received her PhD from the National University of Malaysia in 2013. Her main research interests include climate-resilient agriculture and biodiversity conservation. She is a Fellow of the Higher Education Academy (UK), and has recently completed the USDA Borlaug Fellowship Program at Louisiana State University (US).

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Published/Copyright: August 18, 2020
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Botanica Marina
From the journal Botanica Marina Volume 63 Issue 5

Abstract

With the potential adverse effects of climate change, it is essential to enhance the understanding of marine ecosystem dynamics, which can be driven by the co-evolutionary interaction between autotrophs and herbivores. This study looked into the autotroph-herbivore interactions in Malaysian waters, mainly to determine if autotroph nutritional quality significantly influences herbivore consumption rates. We documented the relative consumption rate of a generalist herbivore (Chanos chanos Forsskål) obtained from the Straits of Malacca through multiple feeding trials using 12 macroalgal species collected from different coastal areas of the Straits of Malacca, the Straits of Johor, and the South China Sea. The herbivore fed selectively on the tested macroalgal species, with the most and least consumed species having the lowest and highest total nitrogen content, respectively. Besides total nitrogen content, the least consumed species also had the highest total phenolic content. Interestingly, we observed that the herbivore generally preferred to consume filamentous macroalgae, especially those collected from the South China Sea. Overall, our findings demonstrated that the feeding behaviour of a generalist herbivore could be influenced by the nutritional quality of the autotrophs, which may depend directly or indirectly on other factors such as autotroph morphology and geography.

Keywords: autotroph-herbivore interaction; generalist herbivore; macroalgal nutritional quality; relative consumption rate

1 Introduction

The marine biome covers approximately three-fourths of the biosphere, providing essential ecosystem services such as habitats for species and carbon sequestration (Townsend et al. 2018). Being the largest biome, it accounts for nearly 90% of the world’s water supply and plays a significant role in preserving millions of existing marine species (Moosdorf and Oehler 2017). Anthropogenic activity has been one of the main drivers of global warming, influencing both temperatures and rainfall distribution globally (Abram et al. 2014Abram et al., 2014; Asmida et al., 2017; Bagarinao, 1991). The shift in weather patterns due to climate change can also lead to significant ecosystem changes, which are mostly negative. Ocean warming, for instance, has been reported to cause a shift to dominance by invasive species and facilitate their invasions, and consequently affecting the structure and function of ecosystems worldwide (Laffoley and Baxter 2016), including coastal and marine ecosystems in Malaysia (Bishop et al. 2017).

Species interactions take place in nature regularly, and one of the most dominant interactions is between autotrophs and herbivores. The autotroph-herbivore interactions in both terrestrial and aquatic biomes have thus far displayed a dynamic evolutionary history, whereby the autotrophs have evolved intricate defence mechanisms to reduce the impact of herbivory. Likewise, the herbivores have evolved countermeasures to outwit these mechanisms (Burkepile and Parker 2017; de Vries et al. 2017; Poore et al. 2012). In the case of marine ecosystems, several studies demonstrated that autotroph characteristics largely influence the consumption patterns of herbivorous fish (Mantyka and Bellwood 2007; Schwartz et al. 2016; Van Alstyne et al. 2009). According to Elger and Lemoine (2005), autotroph palatability depends primarily on autotroph characteristics and their interactions. Nutritional quality of autotrophs such as their levels of nitrogen was found to correlate with the consumption rates of generalist herbivores in native communities (Chan et al. 2012; Elger and Lemoine 2005; Van Alstyne et al. 2009).

To date, the value of autotroph nutritional quality and geography (especially in terms of novelty) in predicting herbivore consumption have not been widely explored, especially for aquatic communities (Clements et al. 2009; Grutters et al. 2017). Several studies on aquatic ecosystems showed that the dynamic interactions between autotroph-herbivore could prevent or reduce the detrimental effects of the presence of invasive autotroph species (Grutters et al. 2017; Parker et al. 2006). Nonetheless, the consumption rate of generalist herbivores whether to consume native or non-native autotrophs has been inferred to lie beyond the evolutionary novelty theory which consists of two dominant hypotheses: (1) enemy release hypothesis which posits that herbivores are maladapted to consume non-native autotrophs; and (2) biotic resistance hypothesis which posits that non-native autotrophs are maladapted to fend off herbivores (Grutters et al. 2017; Maron and Vila 2001; Parker et al. 2006).

Although the autotroph-herbivore synergies have been previously discussed for both terrestrial and aquatic environments in different parts of the world, many studies have reported contradictory findings and conclusions on the effects of nutritional quality and novelty of autotrophs and herbivore feeding patterns (Cronin et al. 2002; Grutters et al. 2017; Raubenheimer et al. 2009; Wong et al. 2010). To the best of our knowledge, the critical characteristics in marine autotrophs such as their nutritional qualities (Behmer and Joern 2008) and geography (Lamarre et al. 2012) that attract or deter herbivores have not been well-addressed in Malaysia. Hence, the current study delved into the value of major nutritional qualities of macroalgae, and their relationships with geography and other possible factors in determining the feeding behaviours of a generalist herbivore. Macroalgae were used as autotrophs in this study because they represent a distinguished group of photosynthetic organisms in the marine biome and are known to have strong interaction with marine herbivores. The overall outcome of this study can help manage the local coastal and marine biodiversity in a changing climate.

2 Materials and methods

2.1 Study organisms

Generalist herbivory is considered the dominant form of autotroph consumption (Dudgeon et al. 2006; Gregory 1983; Vilà et al. 2009). Milkfish (Chanos chanos Forsskål), which is relatively abundant in the tropical waters of the Indian Ocean, was used as an herbivore in this study due mainly to its generalist tendencies (Bagarinao 1991, 1999). Nevertheless, milkfish have yet to be found in some tropical estuaries such as Ponggol (Singapore) and Kretam (North Borneo) (Bagarinao 1991). In the present study, milkfish fingerlings were used instead of adults because they have a higher metabolic rate, which allows them better access to quality feeding patches (Gotceitas and Godin 1992; Millidine et al. 2009). The fingerlings were collected from the northern part of the West Coast of Peninsular Malaysia (06o09′20ʺN, 100o34′11ʺE). They were then transferred and placed in specialized design fibreglass tanks (i.e. artificial seawater systems) in a glasshouse in Rimba Ilmu, University of Malaya (Supplementary Figure S1). These tanks were equipped with a mechanical filtration system with appropriate water quality levels of >5 mg l−1 dissolved oxygen, 30 salinity, 7–8 pH, and 19–20 °C temperature (Sumagaysay-Chavoso and San Diego-McGlone 2003). All these water parameters were monitored at least twice a week using a YSI-Pro Plus multiprobe (YSI Incorporated, Ohio, USA) and a salinity refractometer (Spartan Refractometers, Japan) (Sumagaysay-Chavoso 1998). Protein skimmer was added in the tanks daily to remove the excess organic nutrients and wastes from water. During an acclimation period of 14 days, the fingerlings were only fed with Malaysian sea lettuce (Ulva reticulata Forsskål) once a day and fish food pellets once a week.

The 12 marine macroalgal species used in this study consist of those commonly found near Malaysian waters, collected along the coastal areas of the Straits of Malacca, the Straits of Johor, and the South China Sea (Table 1; Figure 1). The geographical origin of all tested macroalgal species was documented based on previous literature (Asmida et al., 2017; Lee et al. 2014; Muta Harah et al. 2014; Phang et al. 2010Abram et al., 2014; Asmida et al., 2017; Lee et al., 2014; Muta Harah et al., 2014; Phang et al., 2010). We worked with multiple macroalgal species from six different sampling locations to help ensure that our results would be general. Samples were collected in intertidal and subtidal zones at low tide between September 2017 and April 2019. Only healthy-looking samples with minimal epiphytes were collected from the sampling sites. The samples were cleaned and kept in fibreglass tanks in Rimba Ilmu until the feeding trials were conducted.

Table 1:

Sampling areas and coordinates and morpho-functional groups of tested macroalgae.

Macroalgal speciesCoastal areaCoordinate of sampling siteMorpho-functional group
Dictyota ciliolate KützingSOM02°30′60ʺN, 101°47′60ʺECorticated foliosea
Gracilaria firma Chang et XiaSOM02°48′49ʺN, 101°30′06ʺECorticated tereteb
Gracilaria salicornia (C. Agardh) DawsonSOM02°48′49ʺN, 101°30′06ʺECorticated teretec
Padina gymnospora (Kützing) SonderSOJ01°18′60ʺN, 103°36′60ʺECorticated foliosed
Ulva reticulata ForsskålSOJ01°18′60ʺN, 103°36’60ʺEFoliosee
Amphiroa fragilissima (Linnaeus) LamourouxSOJ01°18′60ʺN, 103°36′60ʺENon-calcifiedf
Ceratodictyon spongiosum ZanardiniSOJ01°18′60ʺN, 103°36′60ʺEFilamentousg
Cladophora sericea (Hudson) KützingSOJ01°18′60ʺN, 103°36′60ʺEFilamentousa
Acanthophora muscoides (Linnaeus) Bory de Saint-VincentSCS05°48′00ʺN, 102°37′10ʺECorticatedh
Chaetomorpha antennina (Bory de Saint-Vincent) KützingSCS05°48′00ʺN, 102°37′10ʺEFilamentousg
Cladophora prolifera (Roth) KützingSCS04°24′60ʺN, 103°26′6ʺEFilamentousg
Valoniopsis pachynema (G. Martens) BørgesenSCS04°24′60ʺN, 103°26′60ʺEFilamentouse

  1. SOM: Straits of Malacca, SOJ: Straits of Johor, SCS: South China Sea.

  2. aBenvenuto et al. 2003.

  3. bBeach et al. 2006.

  4. cSousa-Dias and Melo 2008.

  5. dCladeira et al. 2017.

  6. eSidik et al. 2001.

  7. fWilliams et al. 2008.

  8. gBalata et al. 2011.

  9. hPadilla and Allen 2000.

Figure 1: Distribution and collection site of juvenile milkfish and sampling sites of macroalgae in Malaysia.
Figure 1:

Distribution and collection site of juvenile milkfish and sampling sites of macroalgae in Malaysia.

Marine macroalgae occur in a variety of size, shape, toughness, and degree of calcification, and classified into different functional form groups based on their specific morphology, growth form and ecological characteristics (Diaz-Pulido and McCook 2003; Hanley et al. 2007; Padilla and Allen 2000). The macroalgal species evaluated in this study were categorized into several functional groups based on previous literature (Table 1). Based on Morrison and Hay (2011), some autotroph-herbivore pairs in the present study may be classified as evolutionary novel to each other because they occurred on three territorial waters (i.e. the Straits of Malacca, the Straits of Johor, and the South China Sea) (Figure 1). This can be applied to the pairings of milkfish with macroalgal species collected from coastal areas of the Straits of Johor and the South China Sea, given that milkfish were obtained from the Straits of Malacca and have not been found in some tropical estuaries as mentioned in the previous section (Bagarinao 1991).

2.2 Feeding trials

We employed the no-choice feeding trial because this approach provides the flexibility to determine compensatory feeding in herbivores (Duarte et al. 2010; Elger and Barrat-Segretain 2002; Grutters et al. 2017). Based on established protocols, 48 h no-choice feeding trials were conducted for all macroalgal species in triplicate (Burlakova et al. 2009; Elger et al. 2002). All the juvenile milkfish were starved for 48 h prior to the feeding trials. Three fishes with almost the same body weight (1.4 ± 0.5 g) were grouped and placed into each fibreglass tank. Then, each group of fish was randomly fed a standardized amount of fresh fragments of each macroalgal species (FWalgae:initial) that had been blotted dry. After 48 h, the three fishes from each treatment were dried to obtain their body dry mass, which was used to express the consumption standardized for fish mass (DWfish). The remaining macroalgal fragments from each treatment were then dried in an oven at 60 °C for at least 72 h before reweighing (DWalgae:final).

To calculate the relative consumption rate (RCR), the mean of initial fresh-to-final dry mass ratio of the controls were used to calculate the DWalgae:initial from FWalgae:initial. The linear relationship was assessed for each macroalgal species separately using six controls. Following Elger and Barrat-Segretain (2004), the RCR (mg g−1 day−1) was calculated as follows: RCR = DWalgae:initial−DWalgae:final/DWfish/timeday

2.3 Autotroph nutrient analysis

Previous studies reported the correlation between autotrophs characteristics such as nitrogen and phosphorus content to herbivore consumption rates (Cronin et al. 2002; Dorenbosch and Bakker 2011). Hence, five critical nutritional components of macroalgae, including total dry matter, nitrogen, phosphorus, carbon and phenolic contents, were evaluated in this study. Fresh fragments (n = 5) of each macroalgal species were weighed and dried at 60 °C for at least 48 h or until constant weight to obtain their total dry matter content (Elger and Willby 2003). The dried material samples were finely ground and was used to determine the total nitrogen, phosphorus, carbon, and phenolic content. Each analysis was performed in triplicate, with the average value used as the datum for each variable.

2.4 Estimation of nitrogen, phosphorus and carbon contents

A modified Nessler’s reagent spectrophotometry method was used to analyse the total nitrogen content (Makino and Osmond 1991). Ammonium sulphate ((NH4)2SO4) was used as the standard compound. The Nessler’s reagent was prepared by mixing 10 g of Mercury (II) iodine with 7 g of potassium iodine (KI) and 50.0 ml of 20% sodium hydroxide (NaOH). Concentrated sulphuric acid (H2SO4) and saturated potassium were used to digest 0.1 g of sample. After digestion, 0.5 ml aliquot of the digested solution was poured into a 10.0 ml test tube and added with 7.0 ml of Nessler’s reagent, 0.1 ml of 50% concentrated H2SO4, 0.1 ml of saturated potassium persulphate and 2.3 ml of distilled water. Using the UV Mini-1240 spectrophotometer (Shimadzu, Kyoto, Japan), the absorbance of the samples along with a reagent blank was measured at 480 nm. A calibration curve of (NH4)2SO4 was plotted and used to determine the nitrogen content.

The total phosphorus content was determined using the vanado-molybdate method with minor modifications (Legiret et al. 2013). Digestion was performed with diacid mixture (3 nitric acid:1 perchloric acid) using 0.5 g of dried sample. The volume was made up to 50.0 ml with distilled water. Then, 10.0 ml of digested solution were mixed with 10.0 ml of ammonium molybdate solution. Distilled water was added to the mixed solution until a total volume of 50.0 ml was obtained. The change in colour due to different level of acidity was measured at 420 nm on a UV Mini-1240 spectrophotometer (Shimadzu, Kyoto, Japan) against a phosphorus solution calibration curve. To determine the total carbon content, dry combustion analysis was performed using the CHN628 Series Elemental Determinator according to the manufacturer’s protocol (LECO, Michigan, USA). The instrument automatically determines carbon, hydrogen, and nitrogen by oxidizing the samples and the combustion products (i.e. combination of gases) were then separated and determined via a thermal conductivity detector. In the combustion chamber, oxidation process was carried out in the presence of catalyst at the nominal temperature of 950 °C in a stream of pure oxygen (99.99%).

2.5 Estimation of total phenolic content

The modified Folin-Ciocalteu method was used to determine the total phenolic content, with gallic acid as the standard compound (Blainski et al. 2013). A 0.25 ml aliquot of sample extract (1.0 mgml−1 of ethanol) was mixed with 1.25 ml of Folin-Ciocalteu reagent. After 5 min of incubation at room temperature, 1.00 ml of 7.5% sodium carbonate solution was added and the mixture was mixed thoroughly. Sample was incubated at room temperature for 2 h before obtaining the absorbance value at 760 nm using the UV Mini-1240 spectrophotometer (Shimadzu, Kyoto, Japan). The concentration of total phenolic, which expressed as µg g−1 gallic acid equivalents of the sample dry weight, was obtained from gallic acid calibration curve.

2.6 Statistical analysis

All data sets obtained were subject to descriptive statistics. The normality of the distributions was tested using Shapiro-Wilk Test. One-way analysis of variance (ANOVA) was carried out to compare means between two or more variables, followed by the Tukey’s honestly significant difference (HSD) post hoc test (Poore and Steinberg 1999). Linear regression was performed to evaluate the relationships among studied variables. All possible two-way interactions (macroalgal nutrient, morphology, and novelty) were analysed using a linear mixed-effects model, with macroalgae as the random intercept. All analyses were performed using SPSS Statistics Software Version 25 (SPSS Inc., Chicago, USA) and the significance level for the P-value was set at 0.05.

3 Results

3.1 Herbivore consumption rates

The present study looked into the effects of critical autotroph nutritional quality and its relationships with other factors (biogeographical and morphological) on the consumption rates of a generalist herbivore. The results from our no-choice feeding trials showed that the herbivore preferred to feed on certain species of macroalgae (Table 2; Figure 2). Valoniopsis pachynema and Cladophora prolifera were the two most preferred species, having significantly higher RCR (P < 0.05) than other species. Both the species were collected from the coastal areas of the South China Sea (Figure 2). The least consumed species was Padina gymnospora, with a significantly lower RCR than all tested species (Table 2). This species was collected from Tanjung Balau Beach near the Straits of Johor, which is situated north of Singapore (Figure 1).

Table 2:

Relative consumption rate (RCR) and important nutritional components of macroalgae.

Macroalgal speciesRelative consumption rate (mg g−1 day)Total dry matter (%)Total nitrogen content (%)Total phosphorus content (%)Total carbon content (%)Total phenolic content (µg g−1)
Acanthophora muscoides37.34 ± 2.76bc29.74 ± 0.48e0.86 ± 0.10g0.04 ± 0.00g6.29 ± 0.00jND
Amphiroa fragilissima29.32 ± 3.14bc59.21 ± 0.81a2.36 ± 0.04e0.12 ± 0.00d14.30 ± 0.00fND
Ceratodictyon spongiosum39.80 ± 0.65bc7.82 ± 0.07i6.66 ± 0.04b0.06 ± 0.00f11.20 ± 0.00b691.80 ± 0.85b
Chaetomorpha antennina46.85 ± 4.39bc19.33 ± 0.90fg1.91 ± 0.05ef0.18 ± 0.00c19.25 ± 0.00c231.90 ± 0.99c
Cladophora prolifera78.20 ± 7.31a47.89 ± 1.87b2.44 ± 0.19de0.10 ± 0.01e12.40 ± 0.01gND
Cladophora sericea50.02 ± 8.72b16.25 ± 0.58gh1.63 ± 0.03f0.19 ± 0.00bc17.10 ± 0.00e191.60 ± 1.13d
Dictyota ciliolata27.49 ± 2.11c21.92 ± 0.79f4.62 ± 0.22c0.09 ± 0.00e26.05 ± 0.00a9.70 ± 0.14f
Gracilaria firma34.67 ± 3.48bc16.91 ± 0.03g2.99 ± 0.05d0.23 ± 0.00a25.31 ± 0.00bND
Gracilaria salicornia39.13 ± 0.05bc12.53 ± 0.11h2.94 ± 0.11d0.19 ± 0.00b19.22 ± 0.00dND
Padina gymnospora1.74 ± 0.81d31.53 ± 0.55de7.55 ± 0.09a0.13 ± 0.00d9.40 ± 0.00i1261.80 ± 0.06a
Ulva reticulata29.37 ± 3.61bc40.98 ± 0.06c6.60 ± 0.12b0.13 ± 0.00d25.30 ± 0.00bND
Valoniopsis pachynema94.04 ± 6.04a34.62 ± 0.76d0.69 ± 0.04g0.04 ± 0.00g5.90 ± 0.00k17.40 ± 0.05e

  1. Means (±SD) followed by the same letter within columns do not differ significantly between treatments (P > 0.05, Tukey HSD test). ND, not detected (<5 µg g−1).

Figure 2: Relative consumption rate (RCR; mg g−1 day−1) of juvenile milkfish (Chanos chanos Forsskål) on tested macroalgae collected from three territorial waters of Malaysia. Error bars represent standard deviation.
Figure 2:

Relative consumption rate (RCR; mg g−1 day−1) of juvenile milkfish (Chanos chanos Forsskål) on tested macroalgae collected from three territorial waters of Malaysia. Error bars represent standard deviation.

Based on the results of RCR, all the filamentous macroalgae were consumed in higher amounts than other functional form groups of macroalgae. Two of the filamentous species (V. pachynema and C. prolifera) were among the most consumed species by the generalist herbivore (Tables 1 and 2). On the other hand, the most heavily calcified macroalga (Amphiroa fragilissima), which expected to have the least RCR due to calcification in their thalli, was consumed within the intermediate range by herbivore in this study (Tables 1 and 2).

3.2 Compositional analysis

Table 2 also shows the mean values of five autotroph nutritional characteristics evaluated in this study. The total dry matter content in A. fragilissima (59.21%) was higher (P < 0.05) than all other species. The highest total nitrogen content was found in the least consumed species P. gymnospora (7.55%), whereas the most consumed species V. pachynema recorded the lowest mean (0.69%). V. pachynema also recorded the lowest total phosphorus (0.04%) and carbon content (5.90%). Similar to V. pachynema, Acanthophora muscoides recorded significantly lower total phosphorus content (0.04%) than other tested species. Besides total nitrogen content, the least consumed species P. gymnospora also recorded the highest total phenolic content (1261.80 µg g−1). The total phenolic content for six species were not detected in the present study (Table 2), indicating that these species had total phenolic content lower than 5 µg g−1 and this is not uncommon in phycological research (Figueroa et al. 2014; Jerez-Martel et al. 2017; Machu et al. 2015).

A linear mixed-effects model with macroalgae as the random intercept was constructed to identify the parameters (macroalgal nutrient, morphology, and novelty) that best explained the RCR of the generalist herbivore (Table 3). Among these parameters, the macroalgal morphology recorded the highest F-value (F = 20.7) (Table 3), indicating that this factor could play the most significant role in influencing the herbivore consumption rates in our study. Among the five tested nutritional characteristics, the total phenolic content showed the strongest correlation with the RCR of the generalist herbivore (F = 13.1), followed by total carbon (F = 5.0) and nitrogen (F = 3.3) contents (Table 3). In our regression analysis, the total nitrogen demonstrated the strongest relationship with the RCR of the generalist herbivore, showing a negative correlation with RCR (R2 = 0.414) (Supplementary Figure S2). This was observed when the least consumed macroalgae (P. gymnospora) in this study recorded the highest total nitrogen content (Table 2).

Table 3:

Results of mixed-effect linear model fit by reduced maximum likelihood for testing nutritional factors best related to herbivore consumption rates, with species as random intercept.

Fixed effectsFNumerator d.f.Denominator d.f.P-value
Intercept14.5112.700.002
Total dry matter content0.03112.320.872
Total carbon content5.0115.750.040
Total nitrogen content3.3118.540.086
Total phosphorus content1.3117.440.278
Total phenolic content13.1116.100.002
Morphology20.7112.160.001
Evolutionary novelty1.9112.970.195

  1. Bold values indicate statistical significance (P < 0.05).

4 Discussion

The interactions between autotroph and herbivore have been previously discussed for both terrestrial and aquatic environments; however, many studies have reported conflicting findings and conclusions on the effects of autotroph nutritional quality and geography on herbivore feeding patterns (Cronin et al. 2002; Grutters et al. 2017; Raubenheimer et al. 2009; Wong et al. 2010). With the potential adverse effects of climate change, coupled with the increasing human impacts on marine environments, it is essential to enhance the understanding of the marine ecosystem dynamics, which can be driven by the co-evolutionary interaction between autotrophs and herbivores. In Malaysia, anthropogenic activities near the coastal areas such as fishing and trade have been reported as one of the major threats to marine ecosystems (Islam and Jorgensen 2018). It is evident that the coastal ecosystems are getting more vulnerable to both point source and non-point source pollution, which may lead to environmental degradation (Bakke et al. 2013; Islam and Jorgensen 2018). Hence, the current study was carried out to predict the consumption rates of a generalist herbivore based mainly on the nutritional characteristics of macroalgae found along the coastal areas in Malaysia, and to deduce if other factors such as macroalgal morphology and novelty also play a role in determining the herbivore feeding behaviours.

The characteristics of the tested macroalgae in this study, especially their total nitrogen content, were found to influence the RCR of the generalist herbivore (Table 2). The highest and lowest total nitrogen content was found in the least (P. gymnospora) and most (V. pachynema) consumed macroalgal species, respectively. This is further supported by our regression analysis, which revealed a strong negative correlation between the RCR and the total nitrogen content of macroalgae (Supplementary Figure S2). Interestingly, V. pachynema also recorded the lowest total phosphorus and carbon contents. These results may be explained by compensatory feeding, which is regarded as an adaptive strategy that allows herbivores to enhance nutrient intake from low quality autotrophs (Cruz-Rivera and Hay 2001). This strategy has been reported in several studies, where herbivores were observed to graze more on autotrophs with lower nutritional quality to maintain their growth and development (Cruz-Rivera and Hay 2001; Duarte et al. 2014). It is important to note that compensatory feeding is necessary for generalist herbivores to maintain their populations during seasonal changes or periods when high-quality foods are unavailable, especially when generalists are less constrained that specialist in their selection of foods that have noticeable nutritional disparity (Cruz-Rivera and Hay 2000).

Based on our linear mixed-effects model, the RCR of the herbivore was also found to be influenced largely by the total phenolic content of macroalgae (Table 3), indicating that the generalist herbivore preferred to consume macroalgae with low phenolic compounds. Previous studies have demonstrated that the presence of substantial amounts of phenolic compounds in autotrophs may play a role in anti-herbivore defence (Qiu and Kwong 2009; Vergés et al. 2007). In general, marine autotrophs have a lower total phenolic content than most terrestrial autotrophs, although it is considered an important characteristic that may involve in defending aquatic autotrophs against pathogens and herbivores (Smolders et al. 2000). This can be supported by several observations conducted previously on some generalist herbivores, including freshwater fish Scardinius erythrophthalmus (Linnaeus) and Ctenopharyngodon idella (Cuvier and Valenciennes) (Dorenbosch and Bakker 2011) and snail species Pomacea canaliculate (Lamarck) and Lymnaea stagnalis (Linnaeus) (Grutters et al. 2017; Qiu and Kwong 2009). On the contrary, the total dry matter, carbon, and phosphorus contents did not exhibit a significant correlation with RCR in the present study. Similar results were obtained in some earlier studies, which highlighted that nutritional characteristics of autotrophs alone could merely provide an accurate prediction on herbivore feeding behaviour (Paz et al. 2019; Pillans et al. 2004; Tomas et al. 2011).

It is worth noting that the linear model also showed that the macroalgal morphology may play a role in determining the herbivore feeding behaviour. The two most consumed species (V. pachynema and C. prolifera) are both filamentous macroalgae, and each of the other three tested filamentous macroalgae (Ceratodictyon spongiosum, C. antennia, and Cladophora sericea) recorded an RCR of at least 43 mg g−1 day−1 (Table 2). This may be because filamentous macroalgae have low thallus toughness and are easy to ingest. Thallus toughness has been reported as one of the primary morphological properties that could affect the feeding rates of herbivores marine invertebrate grazing herbivores, such as abalone, sea snails and amphipods (Goecker and Kåll 2003; McShane et al., 1994; Pennings et al., 2000). Nevertheless, the articulated calcareous species A. fragilissima with tough thallus was not the least consumed macroalgae in this study. This result is in line with several previous studies where some marine herbivorous fish species were relatively insensitive to autotrophs toughness (Mantyka and Bellwood, 2007).

In terms of geography, it was observed that the generalist herbivore in this study generally consumed higher amount of macroalgae collected from the South China Sea, including the two most consumed species, V. pachynema and C. prolifera (Figures 1 and 2). The herbivore was collected from the Straits of Malacca, which is one of the busiest straits in the world (Islam and Jorgensen 2018). One the other hand, the least consumed species P. gymnospora was collected from the Straits of Johor, which is located close to Ponggol estuary in Singapore where juvenile milkfish was reported not to be found (Bagarinao, 1999). Although milkfish has a wide geographical distribution, it has not been observed in several tropical estuaries in Singapore and North Borneo, which are close to the Straits of Johor and the South China Sea, respectively (Bagarinao, 1991, 1994). Presuming that macroalgae collected from the Straits of Malacca were native to the herbivore and those collected from the Straits of Johor and the South China Sea were non-native, our results are in line with some earlier reports, whereby certain herbivores preferentially consumed invasive autotrophs although both native and invasive autotrophs contained similar nutritional values (Parker and Hay 2005; Parker et al. 2012; Strong et al. 2009). However, it is important to mention that the macroalgal novelty recorded a low F-value (F = 1.9) (Table 3) in the present study, indicating that this factor had the least influence on herbivore consumption rates.

Based on the results of this study, we infer that the feeding behaviour of the generalist herbivore are largely determined by the nutritional characteristics and morphology of macroalgae, and possibly their novelty (Tables 2 and 3). Our results are consistent with a recent study conducted by Grutters et al. (2017), which utilized freshwater species as the study system. We believe that our findings lead to further insights into the dynamics that occur between marine autotrophs and herbivores based on important autotroph characteristics, including total nitrogen and phosphorus contents. Intensive research should be carried out to test the major hypotheses in invasion biology such as biotic resistance and enemy release hypotheses to ensure that the current ecosystems continue to have the ability to resist disturbances to their dynamics. We suggest future research to include appropriate autogenic controls to achieve more meaningful results. Additionally, we recommend the incorporation of geographic variation in future studies that aim to develop theories of ecology.

Corresponding author: Acga Cheng, Functional Omics and Bioprocess Development Laboratory, Institute of Biological Sciences, Faculty of Science, University of Malaya, Kuala Lumpur, Malaysia, E-mail:

Funding source: Universiti Malaya

Award Identifier / Grant number: RU003F-2017

About the authors

Lim Wai Yin

Lim Wai Yin received her Bachelor’s degree in applied biology, majoring in marine and aquatic systems, from the Science University of Malaysia in 2016, and has recently joined the Master’s degree program in the field of marine sciences in Universiti Malaya. Prior to her graduate study, she had been managing the aquatic life’s culturing environment in an aquaculture farm. Her recent research focuses on studying chemical ecology of autotroph-herbivore interactions in tropical marine ecosystems.

Lim Phaik Eem

Professor Lim Phaik Eem is the Deputy Director and Head of the Marine Biotechnology Research Unit at the Institute of Ocean and Earth Sciences, Universiti Malaya. She is an internationally renowned phycologist in the South-East Asian region, where she has actively worked on the taxonomy and conducted phylogenetic studies of seaweeds since the 1990s. She has published more than 100 refereed journal articles and several book chapters.

Affendi Yang Amri

Affendi Yang Amri is a research officer at the Institute of Ocean and Earth Sciences, Universiti Malaya. He is ta scientific advisor for Reef Check Malaysia which is an NGO that monitors coral reefs using citizen science volunteers and works closely with the Federal Marine Parks of Malaysia. His present research interests are studying the local mass coral bleaching phenomena and ecological connectivity between adjacent coral reef, seagrass and mangrove habitats.

Song Sze Looi

Dr. Song Sze Looi obtained her PhD from the University of Malaya in 2013. She is currently an assistant professor at the Xiamen University Malaysia. To date, she has published more than 30 articles with approximately 300 citations. She has extensive experience in biotechnology, genetic, and genomic research.

Acga Cheng

Dr. Acga Cheng is a senior lecturer at Universiti Malaya. She received her PhD from the National University of Malaysia in 2013. Her main research interests include climate-resilient agriculture and biodiversity conservation. She is a Fellow of the Higher Education Academy (UK), and has recently completed the USDA Borlaug Fellowship Program at Louisiana State University (US).

  1. Author contribution: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: This research was supported by the University of Malaya under Research University Grant (grant number: RU003F-2017)

  3. Conflict of interest statement: The authors declare no conflicts of interest regarding this article.

References

Abram, N.J., Mulvaney, R., Vimeux, F., Phipps, S.J., Turner, J., and England, M.H. (2014). Evolution of the southern annular mode during the past millennium. Nat. Clim. Change 4: 564, https://doi.org/10.1038/nclimate2235.Search in Google Scholar

Asmida, I., Akmal, A.B.N., Ahmad, I., and Diyana, M.S. (2017). Biodiversity of macroalgae in Blue Lagoon, the Straits of Malacca, Malaysia and some aspects of changes in species composition. Sains Malays. 46: 1–7, https://doi.org/10.17576/jsm-2017-4601-01.Search in Google Scholar

Bagarinao, T. (1991). Biology of milkfish (Chanos chanos Forsskal). Aquaculture Department: Southeast Asian Fisheries Development Cente.Search in Google Scholar

Bagarinao, T. (1994). Systematics, distribution, genetics and life history of milkfish, Chanos chanos. Environ. Biol. Fish. 39: 23–41, https://doi.org/10.1007/bf00004752.Search in Google Scholar

Bagarinao, T. (1999). Ecology and farming of milkfish. Aquaculture Department: Southeast Asian Fisheries Development Center.Search in Google Scholar

Bakke, T., Klungsøyr, J., and Sanni, S. (2013). Environmental impacts of produced water and drilling waste discharges from the Norwegian offshore petroleum industry. Mar. Environ. Res. 92: 154–169, https://doi.org/10.1016/j.marenvres.2013.09.012.Search in Google Scholar

Balata, D., Piazzi, L., and Rindi, F. (2011). Testing a new classification of morphological functional groups of marine macroalgae for the detection of responses to stress. Marine Biol. 158: 2459–2469, https://doi.org/10.1007/s00227-011-1747-y.Search in Google Scholar

Beach, K.S., Borgeas, H.B., and Smith, C.M. (2006). Ecophysiological implications of the measurement of transmittance and reflectance of tropical macroalgae. Phycologia 45: 450–457, https://doi.org/10.2216/05-30.1.Search in Google Scholar

Behmer, S.T. and Joern, A. (2008). Coexisting generalist herbivores occupy unique nutritional feeding niches. Proc. Natl. Acad. Sci. Unit. States Am. 105: 1977–1982, https://doi.org/10.1073/pnas.0711870105.Search in Google Scholar

Benvenuto, C., Sartoni, G., and Gherardi, F. (2003). Foraging behaviour of the hermit crab Clibanarius erythropus in a Mediterranean shore. J. Mar. Biol. Assoc. U. K. 83: 457–461, https://doi.org/10.1017/s0025315403007331h.Search in Google Scholar

Bishop, M.J., Mayer-Pinto, M., Airoldi, L., Firth, L.B., Morris, R.L., Loke, L.H.L., Hawkins, S.J., Naylor, L.A., Coleman, R.A., Chee, S.Y., , (2017). Effects of ocean sprawl on ecological connectivity: impacts and solutions. J. Exp. Mar. Biol. Ecol. 492: 7–30, https://doi.org/10.1016/j.jembe.2017.01.021.Search in Google Scholar

Blainski, A., Lopes, G., and de Mello, J. (2013). Application and analysis of the Folin–Ciocalteu method for the determination of the total phenolic content from Limonium brasiliense L. Molecules 18: 6852–6865, https://doi.org/10.3390/molecules18066852.Search in Google Scholar

Burkepile, D.E. and Parker, J.D. (2017). Recent advances in plant-herbivore interactions. F1000Research 6, https://doi.org/10.12688/f1000research.10313.1.Search in Google Scholar

Burlakova, L.E., Karatayev, A.Y., Padilla, D.K., Cartwright, L.D., and Hollas, D.N. (2009). Wetland restoration and invasive species: apple snail (Pomacea insularum) feeding on native and invasive aquatic plants. Restor. Ecol. 17: 433–440, https://doi.org/10.1111/j.1526-100x.2008.00429.x.Search in Google Scholar

Caldeira, A.Q., De Paula, J.C., Reis, R.P., and Giordano, R.G. (2017). Structural and functional losses in macroalgal assemblages in a southeastern Brazilian bay over more than a decade. Ecol. Indicat. 75: 242–248, https://doi.org/10.1016/j.ecolind.2016.12.029.Search in Google Scholar

Chan, A.Y., Lubarsky, K., Judy, K.N., and Fong, P. (2012). Nutrient addition increases consumption rates of tropical algae with different initial palatabilities. Mar. Ecol. Prog. Ser. 465: 25–31, https://doi.org/10.3354/meps09946.Search in Google Scholar

Clements, K.D., Raubenheimer, D., and Choat, J.H. (2009). Nutritional ecology of marine herbivorous fishes: 10 years on. Funct. Ecol. 23: 79–92, https://doi.org/10.1111/j.1365-2435.2008.01524.x.Search in Google Scholar

Cronin, G., Lodge, D.M., Hay, M.E., Miller, M., Hill, A.M., Horvath, T., Bolser, R.C., Lindquist, N., and Wahl, M. (2002). Crayfish feeding preferences for freshwater macrophytes: the influence of plant structure and chemistry. J. Crustac Biol. 22: 708–718, 10.1651/0278-0372(2002)022[0708:cfpffm]2.0.co;2.10.1163/20021975-99990285Search in Google Scholar

Cruz-Rivera, E. and Hay, M.E. (2000). Can quantity replace quality? Food choice, compensatory feeding, and fitness of marine mesograzers. Ecology 81: 201–219, https://doi.org/10.1890/0012-9658(2000)081[0201:cqrqfc]2.0.co;2.10.1890/0012-9658(2000)081[0201:CQRQFC]2.0.CO;2Search in Google Scholar

Cruz-Rivera, E. and Hay, M.E. (2001). Macroalgal traits and the feeding and fitness of an herbivorous amphipod: the roles of selectivity, mixing, and compensation. Mar. Ecol. Prog. Ser. 218: 249–266, https://doi.org/10.3354/meps218249.Search in Google Scholar

de Vries, J., Evers, J.B., and Poelman, E.H. (2017). Dynamic plant–plant–herbivore interactions govern plant growth–defence integration. Trends Plant Sci. 22: 329–337, https://doi.org/10.1016/j.tplants.2016.12.006.Search in Google Scholar

Diaz-Pulido, G. and McCook, L.J. (2003). Relative roles of herbivory and nutrients in the recruitment of coral-reef seaweeds. Ecology 84: 2026–2033, https://doi.org/10.1890/01-3127.Search in Google Scholar

Dorenbosch, M. and Bakker, E.S. (2011). Herbivory in omnivorous fishes: effect of plant secondary metabolites and prey stoichiometry. Freshw. Biol. 56: 1783–1797, https://doi.org/10.1111/j.1365-2427.2011.02618.x.Search in Google Scholar

Duarte, C., Navarro, J.M., Acuna, K., and Gomez, I. (2010). Feeding preferences of the sandhopper Orchestoidea tuberculata: the importance of algal traits. Hydrobiologia 651: 291–303, https://doi.org/10.1007/s10750-010-0309-5.Search in Google Scholar

Duarte, C., Acuña, K., Navarro, J.M., Gómez, I., Jaramillo, E., and Quijón, P. (2014). Variable feeding behavior in Orchestoidea tuberculata (Nicolet 1849): exploring the relative importance of macroalgal traits. J. Sea Res. 87: 1–7, https://doi.org/10.1016/j.seares.2013.12.003.Search in Google Scholar

Dudgeon, D., Arthington, A.H., Gessner, M.O., Kawabata, Z.I., Knowler, D.J., Lévêque, C., Naiman, R.J., Prieur-Richard, A.H., Soto, D., Stiassny, M.L., , (2006). Freshwater biodiversity: importance, threats, status and conservation challenges. Biol. Rev. 81: 163–182, https://doi.org/10.1017/s1464793105006950.Search in Google Scholar

Elger, A. and Lemoine, D. (2005). Determinants of macrophyte palatability to the pond snail Lymnaea stagnalis. Freshw. Biol. 50: 86–95, https://doi.org/10.1111/j.1365-2427.2004.01308.x.Search in Google Scholar

Elger, A. and Barrat-Segretain, M.H. (2002). Use of the pond snail Lymnaea stagnalis (L.) in laboratory experiments for evaluating macrophyte palatability. Arch. Hydrobiol. 153: 669–683, https://doi.org/10.1127/archiv-hydrobiol/153/2002/669.Search in Google Scholar

Elger, A. and Barrat-Segretain, M.H. (2004). Plant palatability cn be inferred from a single date feeding trial. Funct. Ecol. 18: 483–488, https://doi.org/10.1111/j.0269-8463.2004.00846.x.Search in Google Scholar

Elger, A. and Willby, N.J. (2003). Leaf dry matter content as an integrative expression of plant palatability: the case of freshwater macrophytes. Funct. Ecol. 17: 58–65, https://doi.org/10.1046/j.1365-2435.2003.00700.x.Search in Google Scholar

Elger, A., Barrat-Segretain, M.H., and Amoros, C. (2002). Plant palatability and disturbance level in aquatic habitats: an experimental approach using the snail Lymnaea stagnalis (L.) Freshw. Biol. 47: 931–940, https://doi.org/10.1046/j.1365-2427.2002.00820.x.Search in Google Scholar

Figueroa, F.L., Barufi, J.B., Malta, E., Conde-Álvarez, R., Nitschke, U., Arenas, F., Mata, M., Connan, S., Abreu, M.H., Marquardt, R., , (2014). Short-term effects of increasing CO2, nitrate and temperature on three Mediterranean macroalgae: biochemical composition. Aquat. Biol. 22: 177–193, https://doi.org/10.3354/ab00610.Search in Google Scholar

Goecker, M.E. and Kåll, S.E. (2003). Grazing preferences of marine isopods and amphipods on three prominent algal species of the Baltic Sea. J. Sea Res. 50: 309–314, https://doi.org/10.1016/j.seares.2003.04.003.Search in Google Scholar

Gotceitas, V. and Godin, J.G.J. (1992). Effects of location of food delivery and social status on foraging-site selection by juvenile Atlantic salmon. Environ. Biol. Fish. 35: 291–300, https://doi.org/10.1007/bf00001896.Search in Google Scholar

Gregory, S.V. (1983). Plant-herbivore interactions in stream systems. In: Barnes, J.R. and M.G.W. (Eds.). Stream ecology. Plenum Press, New York, pp. 157–189.10.1007/978-1-4613-3775-1_8Search in Google Scholar

Grutters, B.M.C., Roijendijk, Y.O.A., Verberk, W.C.E.P., and Bakker, E.S. (2017). Plant traits and plant biogeography control the biotic resistance provided by generalist herbivores. Funct. Ecol. 31: 1184–1192, https://doi.org/10.1111/1365-2435.12835.Search in Google Scholar

Hanley, M.E., Lamont, B.B., Fairbanks, M.M., and Rafferty, C.M. (2007). Plant structural traits and their role in anti-herbivore defence. Perspect. Plant Ecol. Evol. Systemat. 8: 157–178, https://doi.org/10.1016/j.ppees.2007.01.001.Search in Google Scholar

Islam, M.N. and Jorgensen, S.E. (2018). Environmental management of marine ecosystems. CRC Press.10.1201/9781315153933Search in Google Scholar

Jerez-Martel, I., García-Poza, S., Rodríguez-Martel, G., Rico, M., Afonso-Olivares, C., and Gómez-Pinchetti, J.L. (2017). Phenolic profile and antioxidant activity of crude extracts from microalgae and cyanobacteria strains. J. Food Qual. 2017, https://doi.org/10.1155/2017/2924508.Search in Google Scholar

Laffoley, D.D.A. and Baxter, J.M. (2016). Explaining ocean warming: causes, scale, effects and consequences. International Union for Conservation of Nature and Natural Resources (IUCN), Gland, Switzerland, p. 451.10.2305/IUCN.CH.2016.08.enSearch in Google Scholar

Lamarre, G.P.A., Baraloto, C., Fortunel, C., Dávila, N., Mesones, I., Rios, J.G., Ríos, M., Valderrama, E., Pilco, M.V., and Fine, P.V.A. (2012). Herbivory, growth rates, and habitat specialization in tropical tree lineages: implications for Amazonian beta-diversity. Ecology 93: S195–S210, https://doi.org/10.1890/11-0397.1.Search in Google Scholar

Lee, W.A., Namasivayam, P., and Ho, C.I. (2014). Effects of sulfate starvation on agar polysaccharides of Gracilaria species (Gracilariaceae, Rhodophyta) from Morib, Malaysia. J. Appl. Phycol. 26: 1791–1799, https://doi.org/10.1007/s10811-013-0231-0.Search in Google Scholar

Legiret, F.-E., Sieben, V.J., Woodward, E.M.S., Bey, S.K.A.K., Mowlem, M.C., Connelly, D.P., and Achterberg, E.P. (2013). A high performance microfluidic analyser for phosphate measurements in marine waters using the vanadomolybdate method. Talanta 116: 382–387, https://doi.org/10.1016/j.talanta.2013.05.004.Search in Google Scholar

Machu, L., Misurcova, L., Vavra Ambrozova, J., Orsavova, J., Mlcek, J., Sochor, J., and Jurikova, T. (2015). Phenolic content and antioxidant capacity in algal food products. Molecules 20: 1118–1133, https://doi.org/10.3390/molecules20011118.Search in Google Scholar

Makino, A. and Osmond, B. (1991). Effects of nitrogen nutrition on nitrogen partitioning between chloroplasts and mitochondria in pea and wheat. Plant Physiol. 96: 355–362, https://doi.org/10.1104/pp.96.2.355.Search in Google Scholar

Mantyka, C.S. and Bellwood, D.R. (2007). Macroalgal grazing selectivity among herbivorous coral reef fishes. Mar. Ecol. Prog. Ser. 352: 177–185, https://doi.org/10.3354/meps07055.Search in Google Scholar

Maron, J.L. and Vila, M. (2001). When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95: 361–373, https://doi.org/10.1034/j.1600-0706.2001.950301.x.Search in Google Scholar

McShane, P.E., Gorfine, H.K., and Knuckey, I.A. (1994). Factors influencing food selection in the abalone Haliotis rubra (Mollusca: gastropoda). J. Exp. Mar. Biol. Ecol. 176: 27–37, https://doi.org/10.1016/0022-0981(94)90195-3.Search in Google Scholar

Millidine, K.J., Armstrong, J.D., and Metcalfe, N.B. (2009). Juvenile salmon with high standard metabolic rates have higher energy costs but can process meals faster. Proc. Biol. Sci. 276: 2103–2108, https://doi.org/10.1098/rspb.2009.0080.Search in Google Scholar

Moosdorf, N. and Oehler, T. (2017). Societal use of fresh submarine groundwater discharge: an overlooked water resource. Earth Sci. Rev. 171: 338–348, https://doi.org/10.1016/j.earscirev.2017.06.006.Search in Google Scholar

Morrison, W.E. and Hay, M.E. (2011). Herbivore preference for native versus (vs.) exotic plants: generalist herbivores from multiple continents prefer exotic plants that are evolutionarily naïve. PloS One 6: e17227, https://doi.org/10.1371/journal.pone.0017227.Search in Google Scholar

Muta Harah, Z., Japar Sidik, B., Natrah, F.M.I., Emmclan, L.S.H., Wan Hazma, W.N., and Nordiah, B. (2014). Seaweed community of the Merambong shoal, Sungai Pulai estuary, Johore. Malay. Nat. J. 66: 117–131.Search in Google Scholar

Padilla, D.K. and Allen, B.J. (2000). Paradigm lost: reconsidering functional form and group hypotheses in marine ecology. J. Exp. Mar. Biol. Ecol. 250: 207–221, https://doi.org/10.1016/s0022-0981(00)00197-0.Search in Google Scholar

Parker, J.D. and Hay, M.E. (2005). Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol. Lett. 8: 959–967, https://doi.org/10.1111/j.1461-0248.2005.00799.x.Search in Google Scholar

Parker, J.D., Burkepile, D.E., and Hay, M.E. (2006). Opposing effects of native and exotic herbivores on plant invasions. Science 311: 1459–1461, https://doi.org/10.1126/science.1121407.Search in Google Scholar

Parker, J.D., Burkepile, D.E., Lajeunesse, M.J., and Lind, E.M. (2012). Phylogenetic isolation increases plant success despite increasing susceptibility to generalist herbivores. Divers. Distrib. 18: 1–9, https://doi.org/10.1111/j.1472-4642.2011.00806.x.Search in Google Scholar

Paz, L.E., Ferreira, A.C., Simonetti, M.A., and Capítulo, A.R. (2019). Selection of macrophytes by a generalist invertebrate herbivore and potential impacts for stream rehabilitation. Aquat. Bot. 158, https://doi.org/10.1016/j.aquabot.2019.05.006.Search in Google Scholar

Pennings, S.C., Carefoot, T.H., Zimmer, M., Danko, J.P., and Ziegler, A. (2000). Feeding preferences of supralittoral isopods and amphipods. Can. J. Zool. 78: 1918–1929, https://doi.org/10.1139/z00-143.Search in Google Scholar

Phang, S.M., Lim, P.E., and Yeong, H.Y. (2010). Malaysian seaweed resources in the South China sea and their potential economic and ecological applications. J. Sci. Tech. Tropics 6: 87–109, https://doi.org/10.1142/9789812815200_0001.Search in Google Scholar

Pillans, R.D., Franklin, C.E., and Tibbetts, I.R. (2004). Food choice in Siganus fuscescens: influence of macrophyte nutrient content and availability. J. Fish. Biol. 64: 297–30, https://doi.org/10.1111/j.0022-1112.2004.00261.x.Search in Google Scholar

Poore, A.G. and Steinberg, P.D. (1999). Preference–performance relationships and effects of host plant choice in an herbivorous marine amphipod. Ecol. Monogr. 69: 443–464, https://doi.org/10.2307/2657225.Search in Google Scholar

Poore, A.G.B., Campbell, A.H., Coleman, R.A., Edgar, G.J., Jormalainen, V., Reynolds, P.L., Sotka, E.E., Stachowicz, J.J., Taylor, R.B., Vanderklift, M.A., , (2012). Global patterns in the impact of marine herbivores on benthic primary producers. Ecol. Lett. 15: 912–922, https://doi.org/10.1111/j.1461-0248.2012.01804.x.Search in Google Scholar

Qiu, J.W. and Kwong, K.L. (2009). Effects of macrophytes on feeding and life-history traits of the invasive apple snail Pomacea canaliculata. Freshw. Biol. 54: 1720–1730, https://doi.org/10.1111/j.1365-2427.2009.02225.x.Search in Google Scholar

Raubenheimer, D., Simpson, S.J., and Mayntz, D. (2009). Nutrition, ecology and nutritional ecology: toward an integrated framework. Funct. Ecol. 23: 4–16, https://doi.org/10.1111/j.1365-2435.2009.01522.x.Search in Google Scholar

Schwartz, N., Rohde, S., Hiromori, S., and Schupp, P.J. (2016). Understanding the invasion success of Sargassum muticum: herbivore preferences for native and invasive Sargassum spp. Marine Biol. 163: 181, https://doi.org/10.1007/s00227-016-2953-4.Search in Google Scholar

Sidik, B.J., Bandeira, S.O., and Milchakova, N.A. (2001). Methods to measure macroalgal biomass and abundance in seagrass meadows. Global Seagrass Res. Methods: 223–232, https://doi.org/10.1016/b978-044450891-1/50012-8.Search in Google Scholar

Smolders, A.J.P., Vergeer, L.H.T., Van der Velde, G., and Roelofs, J.G.M. (2000). Phenolic contents of submerged, emergent and floating leaves of aquatic and semi-aquatic macrophyte species: why do they differ? Oikos 91: 307–310, https://doi.org/10.1034/j.1600-0706.2000.910211.x.Search in Google Scholar

Sousa-Dias, A. and Melo, R.A. (2008). Long-term abundance patterns of macroalgae in relation to environmental variables in the Tagus Estuary (Portugal). Estuar. Coast Shelf Sci. 76: 21–28, https://doi.org/10.1016/j.ecss.2007.05.039.Search in Google Scholar

Strong, J.A., Maggs, C.A., and Johnson, M.P. (2009). The extent of grazing release from epiphytism for Sargassum muticum (Phaeophyceae) within the invaded range. J. Mar. Biol. Assoc. U. K. 89: 303–314, https://doi.org/10.1017/s0025315408003226.Search in Google Scholar

Sumagaysay-Chavoso, N.S. (1998). Milkfish (Chanos chanos) production and water quality in brackishwater ponds at different feeding levels and frequencies. J. Appl. Ichthyol. 14: 81–85, https://doi.org/10.1111/j.1439-0426.1998.tb00618.x.Search in Google Scholar

Sumagaysay-Chavoso, N.S. and San Diego-McGlone, M.L. (2003). Water quality and holding capacity of intensive and semi-intensive milkfish (Chanos chanos) ponds. Aquaculture 219: 413–429, https://doi.org/10.1016/s0044-8486(02)00576-8.Search in Google Scholar

Tomas, F., Box, A., and Terrados, J. (2011). Effects of invasive seaweeds on feeding preference and performance of a keystone Mediterranean herbivore. Biol. Invasions 13: 1559–1570, https://doi.org/10.1007/s10530-010-9913-6.Search in Google Scholar

Townsend, M., Davies, K., Hanley, N., Hewitt, J.E., Lundquist, C.J., and Lohrer, A.M. (2018). The challenge of implementing the marine ecosystem service concept. Front. Marine Sci. 5: 359, https://doi.org/10.3389/fmars.2018.00359.Search in Google Scholar

Van Alstyne, K.L., Pelletreau, K.N., and Kirby, A. (2009). Nutritional preferences override chemical defenses in determining food choice by a generalist herbivore, Littorina sitkana. J. Exp. Mar. Biol. Ecol. 379: 85–91, https://doi.org/10.1016/j.jembe.2009.08.002.Search in Google Scholar

Vergés, A., Becerro, M.A., Alcoverro, T., and Romero, J. (2007). Experimental evidence of chemical deterrence against multiple herbivores in the seagrass Posidonia oceanica. Mar. Ecol. Prog. Ser. 343: 107–114, https://doi.org/10.3354/meps06885.Search in Google Scholar

Vilà, M., Basnou, C., Pyšek, P., Josefsson, M., Genovesi, P., Gollasch, S., Nentwig, W., Olenin, S., Roques, A., Roy, D., , (2009). How well do we understand the impacts of alien species on ecosystem services? A pan-European, cross-taxa assessment. Front. Ecol. Environ. 8: 135–144.10.1890/080083Search in Google Scholar

Williams, E.A., Craigie, A., Yeates, A., and Degnan, S.M. (2008). Articulated coralline algae of the genus Amphiroa are highly effective natural inducers of settlement in the tropical abalone Haliotis asinina. Biol. Bull. 215: 98–107, https://doi.org/10.2307/25470687.Search in Google Scholar

Wong, P.K., Liang, Y., Liu, N.Y., and Qiu, J.W. (2010). Palatability of macrophytes to the invasive freshwater snail Pomacea canaliculata: differential effects of multiple plant traits. Freshw. Biol. 55: 2023–2031, https://doi.org/10.1111/j.1365-2427.2010.02458.Search in Google Scholar

Supplementary Material

The online version of this article offers supplementary material https://doi.org/10.1515/bot-2020-0029.

Received: 2020-05-04
Accepted: 2020-07-22
Published Online: 2020-08-18
Published in Print: 2020-10-25

© 2020 Lim Wai Yin et al., published by De Gruyter, Berlin/Boston

This work is licensed under the Creative Commons Attribution 4.0 International License.

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  1. Frontmatter
  2. In this issue
  3. Physiology and ecology
  4. Exploring the role of macroalgal traits on the feeding behaviour of a generalist herbivore in Malaysian waters
  5. Mangrove community response to subsidence inflicted sea level change in Car Nicobar Island, India
  6. Seagrass characterization on the southern Pacific coast of Costa Rica: history, vegetation, and environment
  7. Taxonomy/phylogeny and biogeography
  8. The Ulvophyceae (Chlorophyta) of eastern Sorsogon, Philippines, including Halimeda magnicuneata sp. nov. (Bryopsidales)
  9. Reassessment of Tristan da Cunha Gelidium (Gelidiales, Rhodophyta) species
  10. Distribution patterns and biogeography of Sargassum (Fucales, Phaeophyceae) along the coast of Vietnam
  11. A survey of marine fungi on wood in South Australia
  12. Genomics
  13. Comprehensive analysis and identification of heat-responsive genes in Agarophyton vermiculophyllum by RNA-sequencing
  14. Corrigendum
  15. Corrigendum to: The seaweed resources of Israel in the Eastern Mediterranean Sea
https://doi.org/10.1515/bot-2020-0029
Keywords for this article
autotroph-herbivore interaction; generalist herbivore; macroalgal nutritional quality; relative consumption rate
Creative Commons
BY 4.0

Articles in the same Issue

  1. Frontmatter
  2. In this issue
  3. Physiology and ecology
  4. Exploring the role of macroalgal traits on the feeding behaviour of a generalist herbivore in Malaysian waters
  5. Mangrove community response to subsidence inflicted sea level change in Car Nicobar Island, India
  6. Seagrass characterization on the southern Pacific coast of Costa Rica: history, vegetation, and environment
  7. Taxonomy/phylogeny and biogeography
  8. The Ulvophyceae (Chlorophyta) of eastern Sorsogon, Philippines, including Halimeda magnicuneata sp. nov. (Bryopsidales)
  9. Reassessment of Tristan da Cunha Gelidium (Gelidiales, Rhodophyta) species
  10. Distribution patterns and biogeography of Sargassum (Fucales, Phaeophyceae) along the coast of Vietnam
  11. A survey of marine fungi on wood in South Australia
  12. Genomics
  13. Comprehensive analysis and identification of heat-responsive genes in Agarophyton vermiculophyllum by RNA-sequencing
  14. Corrigendum
  15. Corrigendum to: The seaweed resources of Israel in the Eastern Mediterranean Sea
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