Life cycle, nymphal feeding and secondary production of Dinocras cephalotes (Plecoptera) in a Mediterranean river

Abstract

Some aspects of the life history of a population of Dinocras cephalotes inhabiting a Mediterranean river in Southern Spain were studied over a year (2012–2013). The life cycle of this population seems to be semivoltine, of approximately two years of duration, and with an asynchronous egg hatching period. The comparison of these data with those of an unpublished study carried out in the same population almost a decade before (2004–2005) shows the existence of no differences between years. The nymphal feeding study revealed that the main prey of these organisms are Chironomidae, Psychomyiidae and Baetidae, but some of them, usually the smallest, also had non-animal matter in their guts, mainly detritus, coarse particulate organic matter and algae. So, an onthogenetic shift in feeding was detected. This feeding confirms broadly what was already reported in previous studies in the same and other populations. Finally, and for the first time for this species, the secondary production was estimated. Due to differences in hatching, and so development, among nymphs, annual secondary production was calculated both assuming a CPI of 20 months and a CPI of 14 months. In both cases this value was relatively high, 2854.46 and 4077.80 mg DW m–2 year–1, respectively. These results were compared with those of other predators, and particularly with a stonefly predator with a similar life cycle and from a nearby temporal river.

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Life cycle, nymphal feeding and secondary
production of Dinocras cephalotes (Plecoptera) in
a Mediterranean river
José Manuel Tierno de Figueroa, Manuel Jesús López-Rodríguez, Ignacio
Peralta-Maraver & Romolo Fochetti
To cite this article: José Manuel Tierno de Figueroa, Manuel Jesús López-Rodríguez, Ignacio
Peralta-Maraver & Romolo Fochetti (2015) Life cycle, nymphal feeding and secondary
production of Dinocras cephalotes (Plecoptera) in a Mediterranean river, Annales de la Société
entomologique de France (N.S.), 51:3, 259-265
To link to this article: http://dx.doi.org/10.1080/00379271.2015.1059995
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Life cycle, nymphal feeding and secondary production of Dinocras cephalotes (Plecoptera) in a
Mediterranean river
José Manuel Tierno de Figueroa
a
*, Manuel Jesús López-Rodríguez
b
, Ignacio Peralta-Maraver
a
& Romolo Fochetti
c
a
Departamento de Zoología, Universidad de Granada, Campus Fuentenueva s/n, 18071, Granada, Spain;
b
Departamento de Ecología,
Universidad de Granada, Campus Fuentenueva s/n, 18071, Granada, Spain;
c
Dipartimento Innovazione sistemi Biologici, Agroalimentari
e Forestali, Università della Tuscia, Via S. Camillo de Lellis, 01100, Viterbo, Italy
(Accepté le 19 février 2015)
Summary. Some aspects of the life history of a population of Dinocras cephalotes inhabiting a Mediterranean river in
Southern Spain were studied over a year (2012–2013). The life cycle of this population seems to be semivoltine, of
approximately two years of duration, and with an asynchronous egg hatching period. The comparison of these data with
those of an unpublished study carried out in the same population almost a decade before (2004–2005) shows the existence
of no differences between years. The nymphal feeding study revealed that the main prey of these organisms are
Chironomidae, Psychomyiidae and Baetidae, but some of them, usually the smallest, also had non-animal matter in their
guts, mainly detritus, coarse particulate organic matter and algae. So, an onthogenetic shift in feeding was detected. This
feeding confirms broadly what was already reported in previous studies in the same and other populations. Finally, and for
the first time for this species, the secondary production was estimated. Due to differences in hatching, and so development,
among nymphs, annual secondary production was calculated both assuming a CPI of 20 months and a CPI of 14 months. In
both cases this value was relatively high, 2854.46 and 4077.80 mg DW m
–2
year
–1
, respectively. These results were
compared with those of other predators, and particularly with a stonefly predator with a similar life cycle and from a nearby
temporal river.
Résumé. Cycle de vie, régime alimentaire de la nymphe et production secondaire de Dinocras cephalotes (Plecoptera)
dans une rivière méditerranéenne. Certains aspects de l’historie naturelle d’une population de Dinocras cephalotes
d’une rivière méditerranéenne du sud de l’Espagne ont été étudiés durant un an (2012–2013). Le cycle de vie de cette
population semble être semivoltine, avec une durée d’approximativement deux ans, et avec une période asynchrone
d’éclosion. La comparaison de ces données avec celle d’autre étude non publiée accomplies dans la même population
près d’une décennie plus tôt (2004–2005) ne montre pas de différence entre ces années. L’étude du régime alimentaire des
nymphes révèle que leurs proies principales sont des Chironomidae, Psychomyidae et des Baetidae. Toutefois certaines de
ces nymphes, en général les plus petites, avaient aussi de la matière non-animale dans leur tube digestif, surtout des détritus,
des parcelles organiques grossières et des algues. On a donc observé un changement ontogénique d’alimentation. Ce régime
alimentaire confirme largement ce qui était déjà constaté lors d’études antérieures sur cette population et d’autres. Enfin, et
pour la première fois pour cette espèce, on a pu estimer la production secondaire. En raison des différences d’éclosion, et
donc de développement des nymphes, la production secondaire annuelle a été calculée en adoptant un CPI de 20 ou de 14
mois. Dans les deux cas, cette valeur a été relativement haute, soit 2854.46 et 4077.80 mg DW m
–2
year
–1
respectivement.
Ces résultats ont été comparés avec ceux d’autres prédagteurs et particulièrement avec une perle de cycle de vie identique et
d’une rivière temporaire voisine.
Keywords: life history; Perlidae; Southern Spain; stonefly
The stoneflyDinocras cephalotes (Curtis 1827) is the
most widely distributed European Perlidae, found from
Southern Spain (Cádiz) and Southern Italy (Sicily)
(Sánchez-Ortega et al. 2003; Fochetti & Tierno de
Figueroa 2008) to Northern Fennoscandian (Lillehammer
1974; Erkinaro & Erkinaro 2003).
Considering its ecological requirements regarding
egg development, D. cephalotes has always been con-
sidered and reported as a warm stenotherm species
(Elliott 1989;Zwick1996a; Sand & Brittain 2001).
However, other factors seem to be important in shaping
its autoecology: for instance, in Spain its altitudinal
rangespansfrom40to2800maslandinItalyfrom
60 to 1650 m asl (Tierno de Figueroa, Sánchez-Ortega,
et al. 2003; Fochetti & Tierno de Figueroa 2008).
Together with the above-reported wide latitudinal dis-
tribution, from 36° to 70° N, its broad altitudinal range
makes D. cephalotes more euryecious than previously
thought. That is why Graf et al. (2009) reported it as
eurythermous.
*Corresponding author. Email: jmtdef@ugr.es
Annales de la Société entomologique de France (N.S.), 2015
Vol. 51, No. 3, 259–265, http://dx.doi.org/10.1080/00379271.2015.1059995
© 2015 Société entomologique de France
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Besides its wide latitudinal and altitudinal distribution
and its relatively euryecious character, D. cephalotes is an
important ecological element of the European rivers for
some other reasons: it is a top predator within the macro-
invertebrate communities, its large size (mature nymphs
can reach more than 3 cm) and relative high abundance
make it an important prey for carnivorous fishes such as
the brown trout, and adults constitute a respectable
resource for terrestrial predators such as spiders or birds.
Hence, many studies have been conducted to understand
the biology of this species.
One of the most studied aspects of the biology of D.
cephalotes throughout its geographical range is its life
cycle (Hynes 1941; Brinck 1949; Frutiger 1987; Huru
1987; Frutiger & Imhof 1991; Sánchez-Ortega & Alba-
Tercedor 1991; Sand & Brittain 2001; Iannilli et al. 2002).
Life cycle length seems to vary from two to six years. This
variability is mainly due to environmental factors (princi-
pally water temperature) but also to the difficulty in prop-
erly inferring its real duration: it is sometimes difficult to
distinguish different cohorts because of the sexual
dimorphism in size (Sand & Brittain 2001). In addition,
the demonstrated existence of plurimodal hatching of D.
cephalotes eggs (Zwick 1996b) contributes to blurring the
understanding of the real length of its life cycle.
Nymphal feeding habits have been also well studied
(Malmqvist & Sjöström 1980; Berthélemy & Lahoud
1981;Lillehammer1988;Lucyetal.1990;Elliott2000,
2003;Boetal.2007,2008; Gallo et al. 2010; López-
Rodríguez et al. 2012) because of the important role of
nymphs as top-predator within the lotic macroinvertebrate
food web, as previously noted. It turns out that D. cephalotes
behaves as a more generalist predator and it is able to
assimilate a wider trophic resource spectrum than other
Perlids with which it coexists. This could be one of the
reasons why this species has a wider global distribution.
On the other side, the knowledge of the secondary
production of D. cephalotes is so far inexistent, despite
being an important parameter to evaluate the ecological
role of a species in its biocoenosis (Benke 1993).
In the present work, we study the life cycle, nymphal
feeding and secondary production of a D. cephalotes
population inhabiting a Mediterranean river in Southern
Spain. We compare the results of this one-year study with
our own unpublished data on the life cycle of this same
population from a study carried out almost a decade ago.
We also compare our nymphal feeding results with those
previously published for this species in the same river, and
those of the secondary production analysis with data of
other stonefly predator from a nearby area.
Material and methods
Nymphs of D. cephalotes were collected in Castril River (Sierra
de Castril, Granada, South Iberian Peninsula; 37°52′37.6″N, 2°
45′26.1″W; 1040 m asl; Figure 1). Castril River is a tributary of
the Guadalquivir River, and exhibits a limestone substrate com-
posed by cobbles and gravel.
Nymphs were collected with a Surber sampler (area = 0.1 m
2
,
250 µm mesh size). We took six samples during each sampling
event for the secondary production calculation as well as addi-
tional samples to have a higher number of nymphs for the life
cycle and feeding studies; they were preserved in 70% ethanol and
brought to the laboratory. Samplings were carried out monthly
from V.2012 to V.2013. All the macroinvertebrates present in the
samples were also preserved in 70% ethanol, brought to the
laboratory and identified to characterize the community
(Table 1). For the comparison of the life cycle of Dinocras
cephalotes, we used nymphs collected monthly in the same site
from VII.2004 to VII.2005.
Water temperature was hourly recorded by a datalogger
(iBCod, Eclo, 0.01°C accuracy; Eclo, Portugal) placed in the
riverbed during the whole sampling period. The water at our
sampling station was characterized (during the study period) by
very constant mean daily temperatures, ranging only from 8 to
16°C (Figure 2).
Conductivity and pH were measured monthly with a multi-
parametric probe (VWR Symphony, VWR International Eurolab
S.L., Llinars del Vallès, Barcelona, Spain), and discharge (m
3
s
–1
)
was also monthly measured with a propeller meter (Global Water
Mod. FP101, Global Water Instrumentation, Gold River, CA,
USA) in situ during each sampling event. Conductivity ranged
from 209.10 to 243.00 µS cm
–1
(mean = 220.38, SD = 11.20, n=
13), pH ranged from 8.44 to 8.87 (mean = 8.69, SD = 0.12, n=
13) and discharge ranged from 0.41 to 4.51 m
3
s
–1
(mean = 1.71,
SD = 1.48, n= 13).
To describe the life cycle we measured, during the days
following each sampling event, the pronotum width of every
collected specimen with the micrometer of a binocular micro-
scope (10×). We distributed nymphs in 0.5 mm length size
classes and represented the life cycle by means of size–frequency
graphs with the FiSAT II software (version 1.2.0, www.fao.org/fi/
statist/fisoft/fisat/index.htm).
We used the size–frequency method to evaluate secondary
production because nymphs of different size classes were present
at the same time (Hynes & Coleman 1968; Hamilton 1969;
Benke 1979,1993; Benke & Huryn 2006). We applied a
Figure 1. Map of the Iberian Peninsula showing the study area.
260 J.M. Tierno de Figueroa et al.
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correction for the cohort production interval (CPI = mean devel-
opment time from hatching to final size; Benke 1979). We
calculated the annual secondary production assuming a CPI
equal to the minimum nymphal development period and also
assuming a CPI equal to the maximum nymphal development
period recorded in the studied population. We estimated nymphal
biomass with the equation:
DM ¼aXb
;(1)
or, in natural logarithmic form:
Ln DMðÞ¼Ln aðÞþbLn XðÞ (2)
where DM = individual dry mass, X = pronotum width, a =
constant, and b = slope of the regression.
To construct the regression line, we measured 30 ethanol-
preserved specimens, dried them at 60°C for 24 h, and placed
them in a desiccator for 1 h. We weighed the dried specimens to
the nearest 0.01 mg with a Sartorius Weighing Technology
GmbH model MSE 125P-000-DA microbalance (Sartorius
Weighing Technology, Gottingen, Germany).
Thirty nymphs of each sampling date, when possible, were
processed to assess food consumption by means of two types of
gut content analyses. For small individuals (< 15 mm total
length), the contents of the alimentary canal were analyzed
following the transparency method proposed by Bello and
Cabrera (1999) and widely employed in stonefly feeding studies
(e.g. Tierno de Figueroa, Sezzi, et al. 2003; López-Rodríguez
et al. 2009): each nymph was singularly placed in a vial with
Herwitgs’liquid for 24 h at 65°C, and afterwards, cleared indi-
viduals were placed in Herwitgs’liquid on a glass slide with a
cover slip. For large nymphs (> 15 mm total length), guts were
dissected and placed in Herwitgs’liquid on a glass slide with a
cover slip, and afterwards analyzed. As previously observed, no
differences resulted using both methods (Bo et al. 2008).
Identifiable animal gut content items were sorted to the lower
possible taxonomical level. For the remaining contents, five
categories were used: (1) detritus, (2) CPOM (coarse particulate
organic matter), (3) diatoms, (4) fungi, and (5) animal matter
(unidentifiable animal remains > 1 mm). For all the categories,
we estimated in percentage the area that they occupied in the
guts.
Statistical analyses were performed using R (R Core Team
2014). For each category of gut content, mean, standard devia-
tion and maximum-minimum were calculated. We also studied
the correlation between size of the nymphs (measured as prono-
tum width) and percentage of the different gut contents by means
of a Spearman R test.
Results
We collected 330 nymphs of D. cephalotes in 2004–2005
and 346 nymphs in 2012–2013. In both years, the life
cycle was semivoltine with a total duration of two years,
and so with nymphs of different cohorts coexisting at the
same time (Figure 3a,b). Egg hatching was asynchronous,
with small nymphs present in several months, so this
hampers the exact estimation of nymphal development
duration. Nymphal growth was slower in colder months,
with nymphs of the biggest sizes recorded since January
(in 2005) and November (in 2013), some of them even
with black wingpads. Emergence took place at the end of
April and, mainly, in May in both cases.
A total of 269 nymphs collected all through the year
were used for the gut content analyses. Of them, 77 had the
gut empty, while 192 had some kind of food in their guts
(Table 2). The quantity of food inside the guts was highly
variable, ranging from 5% to 100%. The nymphs behaved
mainly as predators, feeding on different macroinvertebrate
prey, but also included a lower quantity of detritus, CPOM
and algae in their diets. Fungi and pollen grains were the
scarcest items in the guts. Percentage prey significantly
increased as the size of D. cephalotes nymphs increased,
indicating that the biggest nymphs were more carnivorous
Table 1. Macroinvertebrate taxa collected during the study
period (2012–2013).
Taxa
Oligochaeta Lumbricidae
Lumbriculidae
Hirudinea
Ephemeroptera Baetidae Baetis sp.
Ephemerellidae Serratella sp.
Ephemeridae Ephemera sp.
Caenidae Caenis sp.
Heptageniidae Epeorus sp.
Ecdyonurus sp.
Rithrogena sp.
Plecoptera Perlidae Perla sp.
Dinocras sp.
Leuctridae Leuctra sp.
Odonata Gomphidae Onychogomphus sp.
Tricoptera Brachycentridae Micrasema sp.
Lepidostomatidae Lasiocephala sp.
Sericostomatidae Sericostoma sp.
Gyrinidae Orectochilus sp.
Psychomyiidae Metalype sp.
Hydropsychidae Hydropsyche sp.
Philopotamidae
Rhyacophilidae Rhyacophila sp.
Coleoptera Elmidae Esolus sp.
Limnius sp.
Elmis sp.
Gyrinidae Gyrinus sp.
Dryopidae Helichus sp.
Dytiscidae
Spercheidae Spercheus sp.
Diptera Chironomidae Orthocladiinae
Prodiamesinae
Tanytarsini
Tanypodinae
Limonidae
Ceratopogonidae
Tabanidae
Simuliidae Simuliini
Empididae Clinocerinae
Stratiomyidae
Athericidae
Annales de la Société entomologique de France (N.S.) 261
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Figure 3. Life cycle of D. cephalotes in the study area in (a) 2004–2005 and (b) 2012–2013.
Figure 2. Mean daily temperatures during the study period in the Castril River.
262 J.M. Tierno de Figueroa et al.
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than the smallest, which ingested significantly more detritus,
CPOM, algae and pollen (Table 2).
Regarding the ingested prey, Chironomidae (including
Prodiamesinae, Tanypodinae and Tanytarsini), Metalype
sp. (Psychomyiidae) and Baetis sp. (Baetidae) were the
most important items in the nymphal diet of D.
cephalotes. In general, the percentage of bigger prey
(mainly Ephemeroptera, Plecoptera and Trichoptera) in
the gut content increased as size of the nymphs increased.
Thus, % Baetidae, % Sericostoma sp. (Sericostomatidae),
%Metalype sp. (Psychomyiidae), % Hydropsyche
sp. (Hydropsychidae) and % Limoniidae significantly
increased as the size of D. cephalotes increased, while %
Chironomidae decreased in the same situation.
In the studied population, dry weight (DW) of D.
cephalotes was related to pronotum width (X) by the
following equation:
Ln DW ¼1:57 þ3:12 Ln X
ðr2¼0:94;F1;28 ¼465:73;p<0:05Þ(3)
The total biomass of the population was 744.90 mg m
–2
,
and the cohort production/biomass ratio was 6.39. We
calculated the annual secondary production both assuming
a CPI of 20 months and a CPI of 14 months. In the first
case, the annual secondary production was 2 854.46
mg DW m
–2
year
–1
and the annual production/biomass
rate (P/B rate) was 3.83 year
–1
. In the second case, the
annual secondary production was 4 077.80 mg DW m
–2
year
–1
and the annual P/B rate was 5.47 year
–1
.
Discussion
The life history of the studied population was similar in
both studied periods, 2004–2005 and 2013–2014. In the
study area, D. cephalotes behaves as a semivoltine species
in contrast to what was reported by some other studies:
e.g. Hynes (1941), Frutiger and Imhof (1991), Sánchez-
Ortega and Alba-Tercedor (1991) and Iannilli et al. (2002)
reported a life cycle of three years in the English Lake
District, in a Prealpine Swiss river, in Sierra Nevada
(Spain) and in an Appenninic river (Italy), respectively;
Huru (1987) reported a life cycle of four to five years in
Northern Norway, and Sand and Brittain (2001), also in
Norway, reported a life cycle of five to six years.
Nevertheless, our results coincide with the two year life
cycle for D. cephalotes under a temperature similar to that
of our study area suggested by Frutiger (1987). Moreover,
the asynchronic egg hatching previously known for this
Table 2. Gut contents of Dinocras cephalotes nymphs in the Castril River, and results of the Spearman correlation test
(R) between pronotum width and percentage of each item.
Items (%) Mean SD Max Min R
Detritus 7.29 19.66 100 0 –0.56*
CPOM 3.70 10.64 100 0 –0.42*
Algae 2.63 10.46 70 0 –0.40*
Fungi 0,18 1.94 25 0 –0.01
Pollen 0.26 1.51 10 0 –0.25*
Prey 85.94 36.69 100 0 0.53*
Baetis sp. (Baetidae) 17.55 32.50 100 0 0.33*
Serratella sp. (Ephemerellidae) 1.20 8.57 100 0 0.02
Epeorus sp. (Heptageniidae) 0.10 1.44 20 0 0.11
Ephemeroptera undet. 2.92 16.21 100 0 –0.01
Leuctra sp. (Leuctridae) 0.21 2.04 20 0 0.07
Perla sp./Dinocras sp. (Perlidae) 0.68 7.52 100 0 0.12
Plecoptera undet. 0.99 8.66 100 0 0.05
Micrasema sp. (Brachycentridae) 0.16 1.61 20 0 0.14
Sericostoma sp. (Sericostomatidae) 0.63 7.35 100 0 0.17*
Metalype sp. (Psychomyiidae) 18.07 33.90 100 0 0.41*
Hydropsyche sp. (Hydropsychidae) 1.25 8.89 100 0 0.18*
Trichoptera undet. 1.25 10.36 100 0 0.01
Elmidae undet. 0.36 3.60 40 0 0.02
Prodiamesinae (Chironomidae) 11.69 28.72 100 0 –0.14*
Tanypodinae (Chironomidae) 1.35 10.30 100 0 –0.06
Tanytarsini, Chironominae (Chironomidae) 0.86 7.89 100 0 –0.08
Chironomidae undet. 5.52 20.51 100 0 –0.18*
Simuliidae 0.36 3.30 40 0 –0.05
Limoniidae 1.98 11.72 100 0 0.21*
Ceratopogonidae 0.63 7.35 100 0 0.11
Prey undet. 18.18 35.25 100 0 –0.00
*Significant at p< 0.05.
Annales de la Société entomologique de France (N.S.) 263
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species (Zwick 1996a,1996b), and also indirectly
observed in our study from the almost continuous exis-
tence of small nymphs, means that the nymphal develop-
ment period could be different among individuals, as
reported by Sánchez-Ortega and Alba-Tercedor (1991).
The studied population shows a slower growth in the
colder period (winter), especially during the second year
of the life cycle, with mature nymphs even from
November in 2012, as noted by other authors (e.g.
Sánchez-Ortega & Alba-Tercedor 1991). This could be
due to the development of gonads and wingpads during
the final instars (Frutiger 1996; Sand & Brittain 2001).
Throughout its distribution area, D. cephalotes is
mainly considered a predator species, feeding principally
on Chironomidae, Baetidae and some families of
Trichoptera, and showing an onthogenetic shift in diet
(metaphoetesis) from more detritivorous toward more pre-
daceous habits (e.g. Berthélemy & Lahoud 1981;
Lillehammer 1988; Lucy et al. 1990; Elliott 2003;Bo
et al. 2007). In our study, this species presented a similar
pattern, with Chironomidae, Psychomyiidae and Baetidae
as the most important prey. Despite the wide trophic
spectrum showed by this species, the comparison with
previous results in the same river shows that the main
prey remain the same in different years (Bo et al. 2008;
López-Rodríguez et al. 2012).
Regarding secondary production of this species, to our
knowledge, there is no available information throughout its
distribution area, despite the importance of this parameter
in understanding the fitness of populations (Benke 1993). A
large difference exists between annual secondary produc-
tion of this population considering a CPI of 20 or a CPI of
14 months. As mentioned before, there is an asynchronous
egg hatching period in this species leading to differences in
the development period among nymphs of the population,
and this is shown by the different values of production.
Thus, and taking into account that the emergence period is
concentrated mainly in May, some nymphs would grow
faster than others (those from eggs hatching in April in
comparison with those hatching in October), and so they
would produce more biomass per unit of area and time and
they would have a higher annual P/B rate, but always within
the most frequent interval reported by other authors (Waters
1977; Benke 1993). The annual P/B rates found in the
population of D. cephalotes are comparable to those of
other freshwater organisms with similar duration of the
development period (see Huryn & Wallace 2000). On the
other hand, the cohort P/B ratio is close to 5, which is the
most frequent value for this parameter in aquatic insects
(Benke & Huryn 2006).
If we compare our results with those of the other pre-
dator stonefly with semivoltine life cycle in nearby regions
(Guadalgenus franzi [Aubert 1963] in López-Rodríguez
et al. 20090 we observe that D. cephalotes has a greater
annual secondary production, even when we consider a CPI
of 20 months, probably due to its higher size at maturity.
Nonetheless, the annual P/B of G. franzi is, overall, higher,
probably due to the fact it inhabits a temporal stream and so
growth is faster and concentrated in the months when the
stream has water. In a broader sense, annual secondary
production of this population is higher than usually reported
for predators, but the annual P/B is within the range of the
most frequent values (Benke 1993).
Acknowledgements
The authors want to thank Carlos Marfil Daza for his help in the
field.
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