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Keywords:

  • cannibalism;
  • diet;
  • Indian Ocean;
  • longnose lancetfish;
  • pelagic environment

Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. ACKNOWLEDGMENTS
  9. REFERENCES

ABSTRACT:  Conspecific predation among longnose lancetfish Alepisaurus ferox was investigated in four spatio-temporal strata of the western Indian Ocean. The cannibalism level varied from 0 to 45.5% by frequency of occurrence and was negatively related with abundance of non-evasive prey (such as crustaceans Charybdis smithii and Natosquilla investigatoris) and foraging success. Predation by lancetfish is often described as a non-selective process, constrained by local prey availability and by its feeding speed during an attack of prey. Our results show that lancetfish may adapt its opportunistic foraging behavior, feeding on non-conspecific abundant prey such as crustaceans when available, and switching to a high level of conspecific predation in poor waters.


INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. ACKNOWLEDGMENTS
  9. REFERENCES

The longnose lancetfish Alepisaurus ferox is an abundant pelagic predator1,2 inhabiting all tropical waters of the world oceans, extending to sub-Arctic regions in the Pacific and Atlantic oceans. Often recorded as by-catch or even stranded,3–5 this species has no commercial value but represents great interest as biological sampler for studying food chains in pelagic ecosystems. Stomach contents of lancetfish are often well preserved because of their digestive characteristics. Food is stored in the stomach and digestion occurs in the intestine, so prey can be easily identified.6 Lancetfish is also an important link in the pelagic food chain as a predator on micronektonic organisms7 and as prey for tuna and billfish,8–11 which are the targets of pelagic tropical fisheries.

The feeding habits of lancetfish have been investigated in the Atlantic Ocean,12,13 Indian Ocean,7,14–18 and Pacific Ocean.16,19–23 Conspecific prey has been reported in several diet studies,7,12,13,17–20,23,24 but was absent in a number of other investigations.14,15,22 Kubota3 mentioned cannibalism as evidence for opportunistic (i.e. non-selective) predation for this species. However, variability in the occurrence of conspecific prey in the lancetfish diet has been not analyzed yet. In this paper, we investigate changes in conspecific predation by area, season and predator size. Using lancetfish as a biological sampler, the prey composition of the stomach contents allowed us to explore the relationship between conspecific predation, foraging success, occurrence of non-evasive prey in the diet, and productivity of the different areas.

MATERIALS AND METHODS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. ACKNOWLEDGMENTS
  9. REFERENCES

Lancetfish stomachs were collected in the western Indian Ocean during research longline cruises carried out in 1986–1987 and 2001–2003 (Table 1). Fish were caught by tuna longlines deployed in subsurface waters; estimated depth of hooks ranged 50–350 m. All the lancetfish caught were measured to the nearest cm (fork length, FL) and weighed to the nearest 10 g. Stomachs were non-selectively sampled, either preserved in formaldehyde (1986–1987) or stored frozen (2001–2003), and processed in the laboratory. Details of processing are presented in Potier et al.7 In total, 306 stomachs (243 non-empty) were collected (Table 1) and partitioned into four spatio-temporal strata (Fig. 1, Table 1): high seas during the North-easternmonsoon (stratum 1), Seychelles waters during the South-western monsoon (stratum 2), Seychelles waters during the North-eastern monsoon (stratum 3), and Mauritian waters during the spring intermonsoon period (stratum 4). Cannibalism level (CL) was assessed using three quantitative indexes of occurrence and abundance of conspecific prey in the stomachs: (i) frequency of occurrence (CLf = number of stomachs including conspecifics divided by the total number of non-empty stomachs); (ii) percent abundance in number (CLn = total number of conspecifics divided by the total number of prey items); and (iii) the percent abundance in reconstituted weight (CLrw = total reconstituted weight of conspecifics divided by the total reconstituted weight of prey items). Because our goal was to explore the importance of cannibalism in the lancetfish diet by predator size, indexes were computed with the data pooled across all the stomachs collected from each stratum, and for two size classes: ‘small’ (FL < 100 cm) and ‘large’ lancetfish (FL ≥ 100 cm). The 100-cm limit was based on prey composition differences between small and large lancetfish17 and to obtain a balanced number of fish in each size class. The importance of prey groups waspresented as the percentage total Index of Relative Importance26IRI = (N + P) × F, where N is the number in percentage, P is the reconstituted weight in percentage, and F is the frequency of occurrence of each food item in non-empty stomachs.

Table 1.  Sampling data for lancetfish Alepisaurus ferox in the western Indian Ocean
Vessel name, originCruise NoPeriod of samplingSeasonAreaStratumTotal number of stomachs/ non-empty stomachs
  1. EEZ, Exclusive Economic Zone; IRD, Institut de Recherche pour le Développement, France; SFA, Seychelles Fishing Authority, Seychelles; YugNIRO, Southern Scientific Research Institute of Marine Fisheries and Oceanography, Ukraine.

R/V Nikolai Reshetnyak, YugNIRO20Dec. 1986–Jan. 1987North-eastern monsoon (boreal winter)High seas off EEZs of Kenya and Seychelles150/37
21Apr–June 1987Spring intermonsoon periodMauritius EEZ, northern part4108/69
R/V l'Amitié, SFA for IRDAM3November 2001North-eastern monsoon (boreal winter)EEZ of Seychelles358/53
AM4Jan–Feb. 2002
AM5Feb–Mar. 2002
AM7Dec. 2002
AM8Jan. 2003
AM1Aug. 2001South-western monsoon (boreal summer) 290/84
AM2Oct. 2001
AM6July 2002
AM9July 2003
image

Figure 1. Location of stations where lancetfish Alepisaurus ferox were caught during 20th (×) and 21st (inline image) cruises of R/V Nikolai Reshetnyak (North-eastern monsoon and spring intermonsoon, respectively) and during cruises of R/V l'Amitié, North-eastern monsoon (●) and South-western monsoon (◊). Isobaths depths are 200 (bold), 2000 and 4000 m. Dotted lines are approximate position of 200-mile Exclusive Economic Zones (EEZs) of coastal states. 1 nautical mile = 1852 m. Coastline and bathymetry data are from GEBCO.25

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A quantitative index of stomach fullness (ISF) was computed as ISF (%) = SCW/(TW − SCW) × 100, where SCW is the wet weight of the stomach contents and TW is total wet weight of the fish. This index is a good indicator of foraging success for lancetfish because recently consumed prey are not digested but accumulate in the stomach. To subtract the cannibalism effect and estimate relative abundance of non-conspecific prey, we also calculated ISF using the weight of non-conspecific prey only (ISFncp). Stratum effects on ISF and ISFncp were tested using non-parametric Kruskal–Wallis rank sum tests and post-hoc multiple comparison tests. Similar tests were also performed for small and large lancetfish. The percentage of empty stomachs varied greatly by stratum (from 7 to 36%) with two main groups: IRD cruises recovered a low percentage of empty stomachs (7–9%) while a higher proportion were observed in YugNIRO cruises (26–36%, Table 1). This obvious cruise effect has no clear explanation except the difference in longline gear (regular vs monofilament) and in the selection of the samples: total A. ferox catches were sampled during the YugNIRO cruises, whereas random sampling was performed during the IRD cruises. Therefore, we decided to work with non-empty stomachs only.

RESULTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. ACKNOWLEDGMENTS
  9. REFERENCES

The fork lengths of lancetfish ranged 44–176 cm (Fig. 2). Crustaceans were the most important food source in strata 1, 2 and 3 by reconstituted weight, and exhibited very high IRI values (Fig. 3a). In stratum 4, fish prevailed and crustaceans ranked second. The dominant prey species were the swimming crab Charybdis smithii, the juvenile stomatopod Natosquilla investigatoris, conspecific individuals, the barracudina Paralepis elongata, the hatchetfish Sternoptyx diaphana and hammerjaw Omosudis lowei (details in Potier et al.7,18 and Romanov and Zamorov17). Size range, mean and standard deviation of dominant prey species/groups are presented in Table 2.

image

Figure 2. Size-frequency distribution of sampled lancetfish Alepisaurus ferox with non-empty stomachs only in (a) stratum 1, (b) stratum 2, (c) stratum 3 and (d) stratum 4. Black bars are ‘small’ (FL < 100 cm) and gray bars are ‘large’ (FL = 100 cm) fishes; n, sample size.

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image

Figure 3. Cannibalism level (percent abundance in number of conspecifics, CLn) and feeding characteristics of lancetfish Alepisaurus ferox for each stratum. (a) CLn (▪) computed from all lancetfish sizes and principal prey groups (% of IRI), (b) prey availability (shaded bars, ISFncp, index of stomach fullness for non-conspecific prey only) and size-specific CLn and (c) relative abundance (% of IRI) of conspecific (black bars) and non-conspecific (shaded bars) fish prey.

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Table 2.  Size of principal prey species and groups recorded in the stomachs of lancetfish Alepisaurus ferox
Prey animalsSwimming crab (n = 219) CWStomatopod (n = 503) TLSquids (n = 34) MLLancetfish (n = 21) SLOther fish (n = 135) SL
  • range and mean ± standard deviation (SD) (mm).

  • CW, carapace width; ML, mantle length; SL, standard length; TL, total length; n, number of individuals examined for each respective prey species or group.

Range26.0–69.218.7–84.09.8–136.045.0–630.011.0–235.0
Mean ± SD38.4 ± 6.856.7 ± 11.539.8 ± 26.0212.2 ± 168.169.6 ± 57.6

Conspecific predation was recorded in all strata except stratum 1 (Table 3, Fig. 3a). High CL indexes were computed for large lancetfish, while cannibalism among small lancetfish was sporadic (Table 3). For large lancetfish, an increasing trend in the three CL indexes was observed from stratum 1 to stratum 4, with the highest levels observed in stratum 4 (Table 3, Fig. 3a,b): CLf = 45.5%, CLn = 8.6% and CLrw = 40.1%.

Table 3.  Cannibalism levels by size groups of lancetfish Alepisaurus ferox
Size groupCLStrata
1234
  • CLf = number of stomachs including conspecifics divided by the total number of non-empty stomachs; CLn = total number of conspecifics divided by the total number of prey items; and CLrw = percent abundance of conspecifics in reconstituted weight.

  • n, number of individuals examined in each respective stratum from strata 1–4, respectively; small, lancetfish < 100 cm fork length (FL); large, ≥100 cm FL.

Small (n = 14, 21, 21, 36)CLf (frequency of occurrence)09.54.82.8
CLn (% in number)00.40.40.4
CLrw (% in reconstituted weight)015.61.67.3
Large (n = 23, 63, 32, 33)CLf (frequency of occurrence)09.525.045.5
CLn (% in number)00.72.78.6
CLrw (% in reconstituted weight)012.712.740.1

Kruskal–Wallis tests show significant differences in foraging success by stratum both for ISF and ISFncp (P < 0.001 and P < 0.00001, respectively). Pairwise tests show significant differences between strata 1 and 3 (P < 0.01), strata 1 and 4 (P < 0.001), strata 2 and 3 (P < 0.01) and strata 2 and 4 (P < 0.001). Hereafter, we used ISFncp medians to present the foraging success per stratum.

The abundance of non-evasive prey recovered in the lancetfish stomachs such as the crustaceans C. smithii and N. investigatoris (Fig. 3a), and foraging success (ISFncp) were negatively related with CL (Fig. 3b), while predation on conspecifics and on non-conspecific fish prey exhibited the same trend from stratum 1 to stratum 4 (Fig. 3c).

DISCUSSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. ACKNOWLEDGMENTS
  9. REFERENCES

Cannibalism is common and variable among piscivores.27 For lancetfish, previous studies have already reported this special form of predation.7,12,13,17–20,23,24 Cannibalism is often attributed to low food quantity or quality and examples showing a significant contribution to the diet in marine fish (except gadiforms) are few.27–30 Our results show that cannibalism among large lancetfish of the western Indian Ocean can constitute a substantial part of the diet.

The three CL indexes computed for large lancetfish fluctuated with the same increasing trend from strata 1–4, i.e. from the high seas off Kenya and Seychelles (no cannibalism) to Mauritian waters (the highest cannibalism level). In stratum 4, the relative low value of CLn (8.6%) compared to the high values of CLf and CLrw (45.5 and 40%, respectively) is caused by the high number of small crustaceans usually recovered from the stomachs of lancetfish.7,17,18,23 However, CLn reflects a number of successful attacks and can be considered as a good proxy for estimating cannibalism levels. The gradient between strata 1–4 corresponds to a negative relationship between cannibalism and feeding level.

The foraging success of lancetfish measured by a quantitative stomach content index reflects to some extent the abundance and availability of vulnerable prey. Abundant patches of the swimming crab C. smithii have been often recorded in the equatorial pelagic zone of western Indian Ocean from approximately 5–6°S to the Arabian Sea during the South-western monsoon, the autumn intermonsoon period, and the North-eastern monsoon.31–35 Lancetfish actively fed on this prey during the NE monsoon in high seas, and during the SE monsoon in waters around Seychelles (95 and 74% of the IRI, respectively) selecting it from other organisms such as evasive prey or conspecifics (CLn = 0–0.7% and CLf = 0–9.5%). A sharp decrease in crab numbers recovered from the lancetfish stomachs was observed in the Seychelles waters during the NE monsoon (2.7% of IRI). The stomatopod N. investigatoris replaced C. smithii in the lancetfish diet in this stratum, and CLf and CLn increased compared to strata 1 and 2. During the NE monsoon N. investigatoris occurs in very dense and extensive swarms in the surface waters of the western Indian Ocean18,36,37 and these swarms are targeted by several top predators.7,37

The highest cannibalism level was recorded in stratum 4 (Fig. 3), i.e. beyond the south tropical front, which is a natural border between equatorial waters (strata 1–3) and waters of the South Equatorial Current flowing through the Mauritius Exclusive Economic Zone.38 The Mauritian waters are far from the areas of pelagic occurrence of C. smithii33,35 and are known as the poorest waters of the Indian Ocean.38 The simultaneous decreases of the non-evasive prey abundance in the stomachs and of the foraging success were associated with an increase in the prey diversity: 20 prey taxa were recorded in the high seas, 41 and 43 prey taxa in the Seychelles waters during the SW and NE monsoons, respectively, and 62 prey taxa were recorded in Mauritian waters.17,18 This pattern reflects a change in the lancetfish foraging behavior, i.e. from feeding on dense patches of vulnerable prey to opportunistic hunting for any prey, increasingly including conspecifics.

The relative abundance of lancetfish (in terms of longline catch rates) was similar in all strata. Size composition was well balanced between small and large individuals. Smaller conspecifics were recorded in every stratum; therefore, they were available for predation by large individuals. The observed pattern of variability in CL by strata and the relationship between CL and foraging success highlights the opportunistic feeding behavior of this predator.

Overall packing density of crustacean aggregations is low in comparison with epipelagic fish schools (e.g. anchovy).39In situ observations36,37 showed that N. investigatoris aggregate in denser swarms than C. smithii. Concentrations of C.  smithii in the surface patches varied within 0.1–0.2 crabs31,35,40 per m2 and density in the upper surface layer (0–150 m) reached35 0.156 inds/m3. Apparently such aggregation level of crustacean prey is enough to retain their high value for lancetfish.

Lancetfish is an ambush predator41 known to attack large, fast-swimming evasive prey.22,41–43 However, it was shown44–46 that many predatory fish select small prey independently of predator size. The prey value for the predator depends on factors including profitability, probability of capture, handling and satiation level.44,45,47 Smaller prey items have a higher value for fish even though they are less profitable since they are ‘most likely to be successfully captured, do not need to be orientated, and have relatively short handling times’.45 Evasive prey quickly loses its value for a predator with increasing prey abundance since pursuit and handling are costly in time and energy. Such prey is less likely to be selected by fish when the prey deficit threshold is passed.45 The average value of small prey is also less variable to the fish at all levels of satiation.45

Small non-evasive crabs are optimal prey for lancetfish due to their size (Table 2), avoidance behavior (low swimming ability) and post-capture handling (easy to swallow whole), while conspecifics are large and evasive. Although conspecifics are prey of high nutritional quality,27 our data show that they are forced rather than preferred prey for lancetfish.

CONCLUSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. ACKNOWLEDGMENTS
  9. REFERENCES

Our results provide evidence that some pelagic fish can adapt their feeding behavior to the variability in the prey abundance encountered in the field. Cannibalism among lancetfish of the western Indian Ocean appears to be an option for increasing adult survival during periods, or in areas of low prey abundance. However, precise information on the prey composition and on the relative biomasses in the environment is required for thorough study of the potential selection of prey by a top predator.

ACKNOWLEDGMENTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. ACKNOWLEDGMENTS
  9. REFERENCES

This work is a contribution of the Research Unit ‘THETIS’ UR109 of the IRD. We thank Pierre Lopez (IRD) for completing the figures.

REFERENCES

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. ACKNOWLEDGMENTS
  9. REFERENCES
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