Dietary variation and food selection by mayfly grazers in a subtropical mountain stream
© Chuang et al.; licensee Springer. 2014
Received: 10 April 2014
Accepted: 13 August 2014
Published: 2 September 2014
The classification of functional feeding groups of aquatic insects is often misleading in tropical/subtropical streams because their feeding habits are assumed to be the same as their temperate counterparts according to the mouthpart structure and foraging behavior. This study aimed to examine the diets and preferences of mayfly grazers (Baetis spp. and Rhithrogena ampla) in a subtropical mountain stream in the dry and wet seasons.
In the stream, epilithic algal communities on insect-excluded bricks (as a grazer-excluded control) were dominated by small adnate diatoms, most likely due to the high current velocity. Both grazers preferred understory and small adnate diatoms, Achnanthes spp. and Achnanthidium pyrenaicum, in both seasons. However, the stalked diatoms Gomphonema spp. were preferred only by Baetis, but not by Rhithrogena, in the dry season when the current velocity became relatively slower. The results of pairwise tests further showed that the algal compositions on the insect-excluded bricks coincided with the diets of both grazers in the wet season but were distinct from those on the bricks in the dry season. Seasonal variations in the algal compositions of the diets of Rhithrogena and on the insect-excluded bricks were apparent, but not in the diets of Baetis.
The algal physiognomy was most likely attributed to the impact of the high current velocity in the stream. Our results suggest that the diet preference by mayfly grazers in the stream is potentially influenced by algal availability.
Herbivory is an important factor regulating the biomass and community structure of benthic algae in streams (Feminella and Hawkins ; Steinman ). Although algal biomass can be effectively reduced by herbivores in a neotropical stream (Barbee ), research on the functional feeding mode of grazers in tropical and subtropical streams is still limited. Not only can they limit algal biomass, but they can also alter the physiognomy and community structure of algae, exerting strong indirect effects within food webs and on nutrient cycling (Holomuzki et al. ). Stream food webs rely primarily on two food sources: autochthonous primary production within the stream and allochthonous organic matter transferred to the stream as leaf litter, woody debris, and dissolved organic carbon. Autochthonous algae may be more important than allochthonous organic matters to stream consumers in tropical forested headwater streams (March and Pringle ). An open forest canopy can lead to autochthonous algae becoming the dominant food source for herbivores in rainforest streams (Brito et al. ) and tropical Asia (Salas and Dudgeon ; Mantel et al. ; Yam and Dudgeon ; Lin et al. ). Autochthonous algae are the main energy source in some shaded tropical headwater streams (Mantel et al. ; Lau et al. ; ; Li and Dudgeon ). However, few studies have examined the diets of aquatic insects in tropical/subtropical streams (Boyero et al. ).
Aquatic insects have been shown to influence the community structure of benthic algae in temperate streams by food selection (Hill and Knight ; Feminella and Resh ; Feminella and Hawkins ; Peterson et al. ). A mat of benthic algae generally consists of a variety of algal physiognomic forms (Wellnitz and Ward ; Holomuzki and Biggs ). Algae in the upper layer of the mat or the overstory are expected to be easily accessible to most aquatic insects, whereas prostrate forms in the understory can only be ingested by aquatic insects possessing mouthparts specialized for detaching these algae from the substratum (Steinman ). The mouthpart structure and foraging behavior of aquatic insects vary among different taxa. They most likely select food on the basis of algal size or growth form (Tall et al. ).
In tropical and subtropical streams, benthic fauna such as aquatic insects have been identified as an obvious knowledge gap requiring further studies (Boyero et al. ). This knowledge gap constrains the ability to understand grazer community in general. Consequently, the feeding habits of aquatic insects in such streams are often assigned to functional feeding groups according to the mouthpart structure and foraging behavior for the North American stream fauna (Merritt et al. ). However, such classification of functional feeding groups is most likely misleading for various insect taxa (Boyero et al. ). Several studies have investigated the effects of mayfly grazers on algae in temperate streams or in laboratory channels (Kohler ; Wallace and Gurtz ; Lamberti et al. ). However, relatively little attention has been paid to the feeding behavior and diet of mayfly grazers in the tropical and subtropical streams.
The Chichiawan Stream (24° 23′ N, 121° 18′ E) is a headwater stream of central Taiwan at an elevation of 1,770 to 2,100 m. The tropical/subtropical monsoon climate in Taiwan is characterized by abundant rainfall in the summer and a dry period in the winter (Yu and Lin ). The stream is characterized by short, straight, and steep channels and is often influenced by fluctuations in precipitation and typhoons. The Chichiawan Stream is the last refuge for the critically endangered Formosan salmon (Oncorhynchus formosanus). Due to the Formosan salmon's critically endangered status (Chung et al. ), there is an urgent need to identify the energy sources supporting the stream food web. Lin et al. () identified mayfly grazers as an important food source for the Formosan salmon in the stream. Nevertheless, the diet of mayfly grazers in the Chichiawan Stream is still unclear. Our objectives are (1) to identify algal compositions in the gut contents of two dominant mayfly grazers (families Baetidae and Heptageniidae) in this subtropical mountain stream, (2) to determine whether there is a seasonal variation in the diet of these grazers, and (3) to assess the degree of food selectivity by these grazers by comparing the algal composition of their gut contents with the algal composition of bricks in the stream where grazing by aquatic insects was excluded.
Physico-chemical variables in the Chichiawan Stream in the dry and wet seasons
Chl a concentration on insect-excluded bricks (mg m−2)
0.4 to 14.4
4.3 to 49.9
Chl a concentration on grazed cobbles (mg m−2)
1.9 to 53.5
6.1 to 182.7
Conductivity (μS cm−1)
287.0 ± 11.0
222.5 ± 1.5
Current velocity (m s−1)
0.87 ± 0.10
1.10 ± 0.05
Discharge (m3 s−1)
1.84 to 2.30
2.58 to 2.96
Chung et al. ()
Dissolved inorganic nitrogen (DIN, mg L−1)
1.81 ± 1.61
1.57 ± 0.85
Lin et al. ()
Cobbles (26%), boulders (21%)
Lin et al. ()
Total phosphorus (TP, mg L−1)
0.03 ± 0.02
0.02 ± 0.02
Lin et al. ()
Water temperature (°C)
9.1 ± 0.4
18.8 ± 0.8
Aquatic insects are the dominant herbivores in the Chichiawan Stream. Only a small number of other herbivores, including tadpoles (Bufo bankorensis and Rana sauteri), snails (Hippeutis sp. and Lymnaea sp.), and fish (Varicorhinus barbatulus and Crossostoma lacustre), are normally observed in the stream (Lin et al. ). Aquatic insects living in the stream are dominated by algivorous grazers and filter feeders (Kuo and Chiu ). Two dominant taxa of grazers (Lin et al. ), the Baetidae mayfly (Baetis spp.) and the Heptageniidae mayfly (Rhithrogena ampla), were collected for examination of their gut contents in this study.
Mayfly samples were collected from randomly selected cobbles in riffles of the midstream of the Chichiawan Stream using a hand net, as riffles constituted >80% of the stream area (Yeh ). To reveal seasonal variations, cobbles with a diameter of approximately 20 cm were collected during the dry season of January and February and during the wet season of June and early July 2005. Only two cobbles were processed each day of each season because mayflies were collected during their feeding time (during the daytime between 1600 and 1800 hours) to minimize the percentage of empty guts (Yu ). The procedure was repeated for 6 days in the dry season and 5 days in the wet season. The sampling was completed before the annual typhoon season (July to October) because the high discharge levels have been shown to remarkably reduce aquatic insect populations (Chiu et al. ) and algal biomass (Tsai et al. ) in the stream. In total, 12 and 10 cobbles were collected during the dry and wet seasons, respectively.
The mayflies living on each cobble were carefully removed with forceps and placed in a squirt bottle filled with 75% ethanol. Prior to gut removal, the total body length and head capsule width of the mayflies were recorded. The entire gut was removed under a stereomicroscope. The entire gut content was fixed in Lugol's solution for algal taxa identification. After removal of aquatic insects, the epilithic algal samples on the cobbles were also collected for further analyses.
For collecting epilithic algal samples, a frame made of steel was used to define an algal patch sampling area of 12.5 cm2. Four algal patches were scraped off a surface area on each brick or cobble of 50 cm2 with a toothbrush. The scraped algae were washed off from the toothbrush and the brick or cobble with filtered stream water, and the algae/water mixture was poured into a 100-mL graduated sample bottle. The sample bottles were transferred to a refrigerator on ice and stored in the dark until the samples were processed. In the laboratory, the algal samples were centrifuged for 10 min to concentrate them to 5 mL. A 3-mL subsample was filtered using a GF/F glass fiber filter (Whatman, GE Healthcare UK Limited, Buckinghamshire, UK), and chlorophyll a (Chl a) was extracted from the filter using a solution of 90% acetone (Lobban et al. ). The other 2-mL subsample was fixed in Lugol's solution for taxa identification.
Epilithic algal compositions were identified and counted using a light microscope of differential interference contrast (Zeiss Axioplan 2, Göttingen, Germany). Filamentous algae such as Oscillatoria and Cladophora were counted in every cell using a hemocytometer. Diatom samples were further treated with H2SO4 and KNO3 (Sabater et al. ) and mounted with Naphrax. At least 500 diatom valves were counted per sample. Identification was carried out according to Patrick and Reimer (), Patrick and Reimer (), Round et al. (), Vyverman (), Yamagishi (), Round and Bukhtiyarova (), and Krammer and Lange-Bertalot (). The relative abundance (%) of algal cells was calculated for analysis of the algal composition.
A two-tailed Student's t test was used to compare epilithic Chl a concentrations between the insect-excluded bricks and grazed cobbles and to compare head capsule width of mayflies between the wet and dry season. Epilithic algal species were categorized into five physiognomic groups, including adnate, stalked, erect, motile, and filamentous, using a modified version of the methods of Wellnitz and Ward () and Holomuzki and Biggs (). To assess seasonal changes in the diets of the mayflies, variations in the algal compositions of their gut contents were examined using multivariate analyses in PRIMER v6 (Clarke and Gorley , PRIMER-E Ltd, Plymouth, UK). Empty guts were excluded from this analysis. Dissimilarity coefficients of untransformed cell numbers of algal communities on the insect-excluded bricks and in the gut contents were computed using Gower's distance, which takes into account the joint absence of food items in the samples. The dissimilarity matrix was first classified by hierarchical agglomerative clustering using the unweighted pair group mean arithmetic (UPGMA) linking method and was then ordinated using the non-metric multidimensional scaling (MDS) techniques. Using season and mayfly taxon as two grouping variables, we assessed the dispersion of algal composition within each group in ordination space using permutational multivariate analysis of variance (PERMANOVA). A one-way PERMANOVA analysis of Gower's distance was used to determine the seasonal effect on algal compositions of the insect-excluded bricks, and a two-way PERMANOVA was used to determine the interactive effect of season and mayfly taxon on algal compositions in the gut contents and pooled samples of insect-excluded bricks and gut contents. Effects were considered to be significant at the 0.05 probability level by comparing the observed statistic to its 9999 permutations distribution in the absence of differences. In cases of a restricted number of possible permutations in pairwise tests, p values were obtained from Monte Carlo samplings (Anderson and Robinson ). Similarity of percentages (SIMPER) was employed to reveal which algal species contributed most to the dissimilarities between the groups for each season or the most common algal species in replicate samples for each group. All the multivariate analyses were performed using the PRIMER v6 with PERMANOVA + add-on software package (Anderson et al. ).
where r i is the relative abundance of algal species i in the gut content and p i is the relative abundance of algal species i in the source sample. The index returns a proportion coefficient from 0 to 1, with values exceeding 1/n indicating a preference for algal species i and values less than 1/n indicating an avoidance of algal species i, where n is the total number of algal species included in the analysis. In this study, only the most 20 common algal species (each contributes >2% to the similarity by using the SIMPER analysis) in replicate samples on the insect-excluded bricks were included for the analysis in each season (i.e., n = 20, 1/n = 0.05).
Results of the multivariate permutational analysis
Gut contents of mayflies
Season × Treatment
Insect-excluded bricks + gut contents of mayflies
Season × treatment
Seasonal variations in the algal composition were further determined using the SIMPER analysis (Figure 3b). Approximately, 11% of the variations between the dry and wet seasons were caused by Cocconeis placentula var. euglypta, which was more abundant during the wet season. A. pyrenaicum (10.6%) and Gomphonema spp. (9.6%) were also significant contributors to the variation and were also more abundant during the wet season.
Comparison of caged bricks with grazed cobbles
SIMPER analysis of contribution of species
Achnanthidium minutissimum (Kützing) Czarnecki
Achnanthidium pyrenaicum (Hustedt) H. Kobayasi
Cocconeis placentula var. euglypta
Diatoma vulgaris Bory de Saint-Vincent
Planothidium lanceolatum (Brébisson ex Kützing) Lange-Bertalot
Gut contents of mayflies
In total, 11 and 19 individuals of Baetis and Rhithrogena were examined for their gut contents and their head capsule widths (mean ± standard deviation) were 0.99 ± 0.19 and 2.74 ± 0.67 mm, respectively. No significant difference in head capsule width was detected between the wet and dry seasons for both mayflies (Student's t test, p = 0.84 for Baetis and p = 0.96 for Rhithrogena). However, the algal composition of the gut contents of both mayflies between the two seasons was significantly distinct (Table 2). Algal compositions between the gut contents of two mayflies also significantly differed. The composition of the gut contents of Rhithrogena was more variable than that of Baetis (Figure 2).
Pooled analysis of insect-excluded bricks and gut contents of mayflies
Pair-wise tests of the effects of season and treatment
Groups within level ‘wet season’
Rhithrogena vs. Baetis
Rhithrogena vs. control
Baetis vs. control
Groups within level ‘dry season’
Rhithrogena vs. Baetis
Rhithrogena vs. control
Baetis vs. control
Groups within level ‘treatment’
Dry vs. wet (Rhithrogena)
Dry vs. wet (Baetis)
Dry vs. wet (control)
Gut contents of mayflies
In temperate streams, while Baetis was categorized as collectors-gatherers and facultative scrapers, Rhithrogena was assigned as scrapers and facultative collectors-gatherers (Merritt et al. ). Such classifications were mainly based on examination of the mouthpart structure and foraging behavior for mayflies, rather than on the gut contents. Consequently, both mayflies in different taxa were considered to feed on the same food sources: detritus and diatoms (Merritt et al. ). Our results of gut content analysis demonstrate that both mayflies preferred understory and small adnate diatoms, Achnanthes spp. and A. pyrenaicum in the Chichiawan Stream. We also discovered that the preference of diatom species by Baetis and Rhithrogena was different; stalked diatoms Gomphonema spp. were preferred by Baetis, but not by Rhithrogena, in the dry season. In the wet season, however, when the current velocity became relatively faster, the distinctness in preference by Baetis and Rhithrogena decreased.
In the dry season, diatoms in the gut contents of Baetis and Rhithrogena show some distinctness, except for the most dominant Achnanthidium/Achnanthes-type diatoms. Interestingly, only 8 species of 52 taxa of diatoms in this study were dominant in the gut contents, and they were mainly small diatoms. These small cells are monoraphid heterovalves, except the stalked Gomphonema (asymmetrical biraphid). Baetis preferred the stalked Gomphonema, but not Rhithrogena. Different types of grazers occupied different feeding niches in relation to the key growth forms in the benthic algal mat (Steinman ). Scraping and gathering grazers feed on stalked or short filament algal species (e.g., genus Gomphonema) and tend to feed on the mid-layers of algal communities. Rasping and scraping grazers feed on prostrate and adnate algal species such as genus Cocconeis and small Achnanthidium/Achnanthes species. In general, the biovolume of Gomphonema was greater than that of small Achnanthidium/Achnanthes-type diatoms. The preference for Gomphonema by Baetis in the dry season might not be caused by the size or characteristics of the mouthpart but instead be a result of the hydrological condition in the stream. Baetis has a fusiform body and prefers a near-bed current velocity of <80 cm s−1, whereas Rhithrogena has a flattened body and prefers a current velocity of >80 cm s−1 (S.F. Yu, personal observation). High velocity scoured off the stalked or large-sized algae, especially the overstory and mid-layer algal species. Therefore, Baetis had more opportunity to feed on larger diatom species than Rhithrogena. A similar study conducted in northeastern Taiwan also indicated that Rhithrogena preferred riffles with faster current velocity, though not so fast as that in the Chichiawan Stream (Yang ).
Seasonal variation in algal composition
The difference in diatom composition on the insect-excluded bricks in the Chichiawan Stream between the dry and wet seasons was contributed mostly from genera Cocconeis, which adnates to the understory of algal mat or to the surface of filamentous algae and was more abundant in the wet season. However, such diatoms were not the preferred species for the dominant mayfly grazers in the stream. Two possible explanations must be considered for why Rhithrogena and Baetis did not prefer Cocconeis spp. in the stream. First, genus Cocconeis was attached directly via the raphid valve by mucilage, but Achnanthidium and Achnanthes were attached to rock using a mucilage stalk secreted from the end of the raphid valve. Therefore, the short-stalked Achnanthidium and Achnanthes were relatively easier for mayfly to graze than the prostrate and tightly attached Cocconeis. The second reason might be that Cocconeis usually attach tightly to the surface of filamentous green algae, such as Cladophora and Spirogyra. However, filamentous algae are usually difficult for grazing insects to harvest or digest (Lamberti and Resh ). Overgrowth of the filaments of Cladophora interfered with the feeding of Rhithrogena that requires a relatively flat substrate free of obstructions to the movements of the maxillary palps (McShaffrey and McCafferty ). Moreover, small and stalked Achnanthidium/Achnanthes-type diatoms with monoraphid were always attaching to the rocks in the rapid riffles with less filamentous algae, and they became the most important food source for Baetis and Rhithrogena in the stream.
Regardless of dry or wet season or changing flow regime, the two mayfly grazers preferred small adnate diatoms species in the Chichiawan Stream. The Chesson's α values were much higher for adnate diatoms, Achnanthes spp. and A. pyrenaicum, than the values for the other species, indicating that they were the most preferred diatom species for mayfly grazers, Baetis and Rhithrogena, in both seasons. These small adnate diatom species were also the most abundant algal species in the Chichiawan Stream (Yu and Lin ) and were usually found in riffles with high current velocity (Su et al. ).
Food selectivity by mayflies
The algal grazer Baetidae was observed using its gouge-shaped mandibular tips (Arens ). Stalked, erect, and filamentous growth forms of algae are often vulnerable to most herbivores, whereas prostrate forms are vulnerable only to raspers and scrapers (Holomuzki et al. ). Wellnitz and Ward () indicated that adnate forms of algae such as Achnanthes are most vulnerable to the gouging mouthparts of Baetid mayflies. Nearly all mayflies of the family Heptageniidae can use their two-segmented strongly modified labial palps, with scrubbing brushes similar to maxillary palps, as algal scrapers (Arens ). These might be the reasons that understory algae rather than overstory algae were preferred by the dominant mayfly grazers in the Chichiawan Stream.
Our findings are contrary to the general impression that overstory algae are more vulnerable than understory algae to grazing insects. Steinman () indicated that 37 out of 43 previous studies (or 86%) show that grazers in streams have a preference for overstory diatoms. However, these studies usually focus on the functional feeding group of gathering-collector. Relatively little attention has been paid to the feeding behavior and the gut content of Heptageniid Rhithrogena species with a scraping brush on the maxillary palp (e.g., McShaffrey and McCafferty ). Wellnitz and Ward () reported that a grazer, Ecdyonurus venosus (Heptageniidae), uses a brushing mouthpart and other grazers, Baetis spp. (Baetidae), use mandibles and maxilla to scrape and gather periphyton. Research on the gut contents of Baetis and Rhithrogena in tropical and subtropical streams is still rare (Yang ). Our results demonstrate that Baetis and Rhithrogena preferentially feed on understory algae, which were mainly adnate form or Achnanthes-type algae, in the Chichiawan Stream.
The preference of small adnate diatoms species by the dominant mayfly grazers in the Chichiawan Stream year-round is most likely a result of the high current velocity on algal physiognomy in the stream. The current velocity of the stream is the main factor affecting epilithic algal biomass and compositions in this subtropical mountain stream (Tsai et al. ), which can regulate the levels of subsidy and stress experienced by periphyton by simultaneously regulating nutrient uptake rates and shear forces (Biggs et al. ). Continental islands in the tropics/subtropics of the western Pacific are characterized by mountainous watersheds, high precipitation, and high water runoff; therefore, many mountain streams on these islands, including the Chichiawan Stream, have relatively short, straight, and steep channels in comparatively small and narrow watersheds (Smith et al. ). The current velocity in the Chichiawan Stream remained fast (>0.60 m s−1) year-round. The high gradient (130 m km−1) and flow environments in the stream caused the diatom communities to shift toward more adnate forms in the stream, such as the tightly adherent diatoms Achnanthes, Achnanthidium, and Cocconeis. Our results suggest that the preference by mayfly grazers in the stream is potentially influenced by algal availability.
Although a previous study found that the density of Achnanthidium species decreased with increasing grazer density (Yu and Lin ), mayflies did not actually prefer the similar adnate form of A. minutissimum, which were the smallest-sized diatoms in the Achnanthidium species complex in the Chichiawan stream. A. minutissimum can colonize rapidly in this stream after flushing floods (Lin and Lin ). Grazers can maintain the early successional nature of algal communities under conditions of high current velocity (Poff and Ward ). Small-celled unicellular algae have a low biomass, short cell cycle, and rapid growth rate. Such conditions favor organisms that follow an opportunistic or r-selection strategy (Sigee ). Therefore, while Achnanthes spp. and other Achnanthidium species were preferentially grazed by the dominant mayflies, the small-sized A. minutissimum can grow on the lowest layer of algal mats.
The two dominant mayfly grazers preferred understory and small adnate diatoms species in the Chichiawan Stream in the dry and wet seasons. The algal physiognomy was most likely attributed to the impact of the high current velocity in the stream. The preference by the mayfly grazers in the stream is potentially influenced by algal availability.
This study was financially supported by the Shei-Pa National Park Headquarters, Miaoli County, Taiwan.
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