Mouth and Gut morphology of fish in relation to feeding ecology and trophic groups in Wachapreague, USA.
Casey De-Geir; School of Ocean Science, Bangor University, Anglesey, LL59 5RH
1. Abstract:
Previous studies have shown feeding ecology and trophic groups to be related to gut and mouth morphology of a variety of different fish species. In Wachapreague, Chesapeake Bay 19 fish species have been collected and analysed over 4 years (2012-2016) to see if mouth and gut morphology exhibit patterns similar patterns to previous studies. Each collected specimen measurements of total length, weight, vertical and horizontal mouth opening and gut length were taken. These specimens were then categorised into trophic groups from their trophic levels; omnivores (OV), omnivores with preference for animal matter (OA), carnivores with preference for fish and decapods (CD) and carnivores with preference to fish and cephalopods (CC). From measurements made, we calculated relative mouth area (RMA), relative gut length (RGL), and Zihler’s intestinal length weight index (ILW). There was an insignificant relationship between RMA and ILW. Gut lengths increased with the lowering trophic level groups, as OV species exhibit larger gut lengths to take in optimum amounts of nutrients from low quality food supply. However, RMA did not exhibit expected patterns and shown an insignificant relationship with trophic groups due to high variance in the data, due to life stages not being taken into account as part of the study.
2. Introduction
Feeding ecology varies widely amongst different species of fish due to the high diversity of preferable food sources. Fish morphology in particular mouth morphology (Karachle and Stergiou, 2011) is understood to be highly variable between species due to their preferred food source (Moyle and Cech, 2003). Examples include vertebrates which have adapted mouth shapes for suction feeding. Suction is created by expanding the mouth cavity in order to create low pressure inside, causing water and the prey to flow into the vertebrate’s mouth (Alfaro et al, 2001). Suspension feeders have also developed mechanisms for capturing food that can be highly diluted within their water masses (Gili and coma, 1998) by using rows of comb-like gill rakers. Food articles are concentrated between rakers in the oral cavity and high velocity cross flows transport the food particles towards the oesophagus, working as a filtration system. It has been found fish development is dependent on how much energy they need to consume in order to sustain themselves, this results in developing mouth structures during throughout their life stages. Mouth morphology changes in accordance to preferred prey items, therefore it is possible that the morphology of the gut may also adapt in accordance to the mouth for better digestion (Karachle and Stergiou, 2011).
The gut length of herbivorous fish is larger than that of an omnivore species, and omnivores have a larger gut than that of a carnivorous species (Kapoor et al, 1975). Shorter gut lengths tend to be associated with fish species that’s preferable diet consist of animal matter (Labropoulou and Eleftheriou, 1997) Animal matter is a food of high quality due (e.g. other fish) to high numbers of nutrients however slow digestion rates, this shorter gut enables efficiency of digestion and high nutrient absorption. Longer guts allow the food to spend more time in the digestive tract allowing optimum nutrient absorption for lower quality prey items e.g. plant material and exoskeletons (Wootton, 1998). Studies suggest gut morphology changes as it has been used to for the categorization of fish trophic levels in relation to feeding (Al-Hussaini, 1947; De Groot, 1971; Zihler, 1982). A study by Stergiou and Karpouzi (2002) used 146 Mediterranean fish species for the basis of a trophic level study, in this study 4 trophic groups were classified: Pure Herbivore with preference to vegetation (2.1 – 2.9), Herbivore with preference to animal material (2.9-3.7) and carnivores split into two groups, carnivores with preference for fish/decapods (3.7-4.0) and carnivores with preference for fish/cephalopods (4.0-4.5). This classification is an important contributing factor when reporting results of fish mouth and gut morphology.
As it is understood, a large proportion of the literature based on fish morphology in relation to feeding ecology focuses on fresh water fish (Hugueny and Pouilly, 1999; Kramer and Bryant, 1995). This shows that literature concentrating on marine species is scarce. Chesapeake Bay is the largest estuary found in the United States. It is a complex ecosystem that plays host to many marine and fresh water habitats. These habitats such as salt marshes and sea grass meadows provide food, shelter, nurseries and support a vast amount of fish species, as well as many other organisms. By studying the fish within this ecosystem, a better understanding could be gained of how the diversity of marine species found here, and what their morphologies and trophic groups tell us about complex food web this ecosystem supports.
This report will investigate whether mouth morphology and gut length is related to feeding ecology and whether morphological patterns are related between trophic groups.
3. Materials and methods:
The study site that was used consisted of two locations in the Eastern Shore peninsula in the state of Virginia, USA. This area consists of coastlines along the Atlantic Ocean and Chesapeake Bay, the majority of organisms were caught and collected on the Atlantic side of the peninsula in and around the marsh area of Wachapreague. The two locations were fished at using two techniques; Otter trawl and Seine Netting. The locations using these techniques are as follows: otter trawling in the salt marsh creeks and bayside, and seine netting on the barrier islands. The otter trawls were taken off the back of a boat using a net with the diameter size of 4.9m from otter board to otter board. 1.5 cm square mesh size in the cod end. The otter trawl was cast out from the stern of the boat and towed behind for approximately 5 minutes at 3-4 knots, after this period the trawl was pulled into the boat and the catches were sorted into several salt water filled buckets. The required sample size was collected for each species from the net and put into buckets, caught fish that were not required for the samples were returned back to the water.
The second technique used was seine netting which took place on the barrier islands. The net had a 3mm delta style mesh, and was 7.7 m long attached between two poles. The nets were deployed off the beaches. The seine nets were positioned parallel to the beach with both poles being held by a group of people in waist height deep water so the net was suspended in the water column. With the poles keeping contact with the sediment, they were pushed until the net was horizontal to the shore line in the shallows trapping the fish. This was done as a group split into two, half of the group walked the net into the shore and the other half positioned in an arc in front of the net. The fish were scared into the net using a ‘clapping’ technique hitting the water with hands. Once the seine net was horizontal to the shoreline, it was dragged up on to the beach so captured fish could be collected and sorted. The fish that were not needed in the samples were returned.
A number of individuals from each species caught were taken back from the fishing sites to the Virginia Institute of Marine Science laboratory (VIMS). Upon returning to the lab, every specimen was identified and each trophic level was taken using the fishbase database (www.fishbase.org.). The species were then classified into trophic groups based on trophic levels taken from fishbase, using Stergiou and Karpouzi (2002). The species found were abbreviated as following:
OV – Omnivores
OA – Omnivores with preference for animal matter
CD – Carnivores with preference for fish and decapods
CC – Carnivores with preference to fish and cephalopods
Table 1: 19 total fish species caught over 4 years (2012-2016) using otter trawls and seine nets in Wachapreague, Virginia, USA. The trophic levels were taken from fishbase (www.fishbase.org). Trophic groups taken from Stergiou and Karpouzi (2002).
Species
Common name
n
Trophic Level
Atlantic Menhaden
Brevoortia tyrannus
53
OV
Atlantic Silverside
Menidia menidia
34
OA
Bay Anchovy
Anchoa mitchilli
50
OA
Black Drum
Pogonias cromis
6
CD
Black Sea Bass
Centropristus striata
2
CD
Bluefish
Pomotomus saltatrix
6
CC
Mummichog
Fundulus heteroclitus
10
OA
Northern Kingfish
Menticirrhus saxatilis
4
OA
Pinfish
Lagodon rhomboides
45
OA
Sheeps Head Minnow
Cyprinodon variegatus
16
OV
Silver Perch
Baidiella chrysura
84
OA
Silver Seatrout
Cynoscion nothus
5
CD
Southern King Fish
Menticirrhus americanus
3
OV
Spot
Leiostomus xanthurus
82
CD
Striped Bass
Morone saxatilis
12
CC
Striped Killifish
Fundulus majalis
29
OA
Striped Mullet
Mugli cephalus
17
OV
Summer flounder
Paralichthys dentatus
13
CC
Weakfish
Cynoscian regalis
24
CD
To begin measurements, the total length of each individual fish from the caudal fin to the snout and the weight of the fish was measured. The horizontal mouth opening (HMO) and vertical mouth opening (VMO) were then gently measured in millimetres using Vernier callipers to avoid natural over extension. From this, mouth area (MA) was calculated using the following equation: MA = π*(HMO/2) x (VMO/2). From this the relative mouth area was taken using the following equation: RMA = MA/TL2.
In order to measure gut length (GL) the individual fish were dissected cutting closely from the anal fin to mouth, with another cut vertically to access to organal cavity. The gastrointestinal tract was then removed and gently uncoiled and placed in a straight line for measurement (cm). Relative gut length was then calculated using the following equation: RGL = GL/TL. Lastly, Zihler’s index of intestinal length weight (ILW) was calculated as measurement of gut length in relation to body volume and gut weight (Zihler, 1981). This was calculated in the following equation: ILW=GL (mm)/[10×3√W(g)].
4. Results:
Figure 1. The relationship between average relative mouth area (RMA) and Zilher’s Intestine Length-Weight index (ILW) of the 19 total fish species caught over 4 years (2012-2016) in Wachapreague, Virginia (Regression: R2 = 0.0739, F = 1.2776, P-value = 0.330).
There is a no significant relationship between RMA and ILW of all 19 species as determined by regression, R2 = 0.0739, F = 1.2776, P-value = > 0.05. There is a negative correlation shown between RMA and ILW for all 19 fish species. The general trend that can be seen is as RMA increases, ILW increases. However slight trend can be seen amongst some of the data, as ILW increases, RMA decreases. The majority of the fish species had an ILW of less that 5, however RMA shows more variation amongst species, as the majority had an RMA between 0 and 0.017. There are also outliers that can be seen that don’t fit the trend, and variation amongst all year.
Figure 2. Average Relative gut length (RGL) of the 19 total fish species caught over 4 years (2012-2016) in relation to their trophic groups.
Table 2. Results of a One-Way ANOVA statistical test analysing the relationship of relative gut length between 4 trophic groups.
Source
df
Mean Square
F
Between Groups
17
23.912
27.452
.000
Within Groups
477
.871
There are statistically significant differences between RGL and the 4 trophic groups as determined by One-Way ANOVA, F = 27.452, MS = 23. 912, P < 0.05. As can be seen clearly, OV species have the highest RGL however have the highest amount of variability of all 4 trophic groups. CC have the lowest RGL with the second highest amount of variability, closely followed by CD and OA.
Figure 3. Average Relative Mouth Area (RMA) of the 19 total fish species caught over 4 years (2012-2016) in relation to their trophic groups.
Table 3. Results of a One-Way ANOVA statistical test analysing the relationship of average relative mouth area between 4 trophic groups.
Source
df
Mean Square
F
Between Groups
17
.003
.560
.921
Within Groups
477
.006
There were no statistically significant differences between RMA and the 4 trophic groups as determined by One-Way ANOVA, F = .560, MS = .003, P > 0.05. OA species have the highest RMA of all 4 trophic groups with the second highest amount of variability. CC have the lowest RMA with lowest amount of variability. High variability amongst all 4 species.
Figure 4. Average Intestinal Length Weight Index (ILW) of the 19 total fish species caught over 4 years (2012-2016) in relation to their trophic groups.
Table 4. Results of a One-Way ANOVA statistical test analysing the relationship of Average Intestinal Length Weight Index between 4 trophic groups.
Source
df
Mean Square
F
Between Groups
17
473.24
28.326
.000
Within Groups
477
16.707
There are statistically significant differences between Zilher’s index, ILW and the 4 trophic groups as determined by One-Way ANOVA, F = 28.326, MS = 473.24, P < 0.05. OV species have the highest ILW approx. 3 times larger than OA species, however has the highest variability.
5. Discussion:
The relationship between average relative mouth area and Zilher’s Intestine Legnth-Weight index (ILW) was insignificant. There is some species amongst years that didn’t fit the trend affecting the overall results. Firstly, this could be due to locations the fishing took place, for example seine netting needs to be done manually in shallow water to make it manageable, which may have resulted in juvenile fish species being taken and measured lowering the overall data for relative mouth area (RMA) and Intestine Length-Weight index (ILW). This is not an accurate representation of mature fish species found in Chesapeake Bay. For future studies mature adults could be fished more accurately from each area to gain more of an insight into mature populations, fishing in deeper water to avoid juvenile nurseries, giving the data set less variability as well as more samples taken from each environment to add to the overall data set. Over fishing may have also been a contributing factor as it may have caused a decline in mature fish (Pauly et al, 1998).
There was a significant relationship found between relative gut length (RGL) and trophic group (TG). Omnivores with preference to vegetation had the largest RGL. A study by Hofer and Schiemer (1981) suggests that many species of omnivorous fish possess a long, coiled digestive tract which aids the digestion of plants, and that the length of the intestine is important for efficiency of reabsorption. To add to this, there is a higher intensity of proteolytic digestion in herbivorous fish, as the exposure to proteolytic enzymes rises with increasing gut length. The lower quality food items the omnivores consume relates directly to the long gut length shown in the data. The gut length these animals have adapted allows plant material to spend more time in the digestive tract, increasing overall nutrient intake (Wootton, 1998; Pennisi, 2005). This allows for maximum utilisation of the nutrients available to them. Carnivores with preference for fish and cephalopods (CC) had the smallest gut of all 4 trophic groups, followed by carnivores with preference for fish and decapods (CD). As it is widely understood, animal matter takes a longer period of time to digest due to the higher quality of food sources they consume.
There was a non-significant relationship found between relative mouth area (RMA) and trophic group (TG). Omnivores had largest relative mouth area (RMA) of all four trophic groups, which rejects the findings of Karachle and Stergiou (2003). OA group included the Bay anchovy Anchoa mitchilli, this species is a small pelagic filter feeder which has a large RMA to body size ratio (Karachle and Stergiou, 2011). Relative mouth area (RMA) in OA species was larger than in OV species, this could be that the OA species have larger RMA to accommodate the potentially larger food items such as Gastropods and Crustaceans (Stergiou and Karpouzi, 2002). CC had the smallest RMA of all 4 trophic groups, again this could be largely due to the sites fished at, shallow water areas host nurseries for juvenile fish species. Included in this carnivorous group was the Striped Seabass Morone saxatilis, which primarily consumes copepod Eurytemora affini from larval stages to early adult life (Chesney, 1989). Eventually, M.saxatilis develops into early adult life stages and feeds on animal matter with a main preferable diet of fish, a study conducted by Manooch (1973) shown the species most frequently eaten by M.saxatilis was Atlantic Menhaden in Albemarle Sound, North Carolina. According to a study MA increase is directly related to growth increase, developing structural changes in order to meet their increased energetic demands (Karachle and Stergiou, 2011). This could show that in order to gain an accurate representation of carnivorous fish relative mouth area in Chesapeake Bay, more samples must be taken in order to test the hypothesis, as the carnivorous species caught during the experiment may have been juveniles. In future studies, adult specimens of each species would need to be tested. There was a significant result between Zilher’s Intestine Legnth-Weight index (ILW) and Trophic group (TG). ILW is a measurement of gut morphology in relation to weight of gut and body volume of fish, which is a more accurate representation of the digestion of fish considering more than one factor. The more herbivorous species from the omnivore grouping OV presented the largest gut length of all four groups, these findings from the analysis support the literature on these studies (Wootton, 1998; Pennisi, 2005).
There are clear patterns of fish morphology in relation to feeding ecology, with carnivorous species exhibiting shorter gut length and the more herbivorous species possess longest gut length the increased efficiency of digestion, and maximum extraction of prey items supporting the hypothesis. These strong relationships are also exhibited between Zilher’s Intestine Legnth-Weight index and Trophic group, this is a better representation of the fish species caught as it includes more than one factor in its determination such as gut weight, and body volume and is more reliable amongst a varied amount of fish species and data.
Due to problems experienced during the data analysis, the found mouth area of fish species was not the expected outcome of the results. However, there was one component this study did not take into account which was life stages. As previously mentioned, methods in this study including fishing locations need to be reassessed in order to avoid juvenile nurseries. Due to the nature of the habitats found in Chesapeake Bay, there is a lot of potential fish nursing grounds due to the shelter and foraging opportunities these ecosystems host. By changing locations or choosing deeper waters to fish in as part of this study, the juveniles will be missed and this will avoid fish which have yet to undergo ontogenetic shift in feeding ecology being caught and analysed. However, one thing that may also need to be considered is a new fishing technique which may be needed in order to achieve this, replacing seine netting as it would be a lot more physically challenging in deep suspended water. For future studies, life stages need to be considered better for each specimen, causing less variation in results. Another method could be undertaken were a number of samples from each age class of each fish species could be caught and tested. Examining growth could be determined by the removal of otoliths from the fish’s head, this will provide a comparison in the study and a better understanding of the entirety of the fish populations found in the diverse ecosystems of Wachapreague.
Conclusion
To conclude, morphological features such as mouth area and gut length is related to feeding ecology, however more investigation must be done in order to test and determine whether morphologic patterns are related between groups, and when mouth morphology is used to show relationships between trophic groupings, life stages must also be considered when doing so.
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