TEMPORAL VARIABILITY AND SPATIAL DIVERSITY OF SMALL PELAGIC FISH
BIOMASS IN THE NORTHERN ADRIATIC SEA
M. Azzalia, A. De Felicea, I. Leonoria and M. Lunaa
a
Istituto di Scienze Marine (ISMAR-CNR), Largo Fiera della Pesca, 60125 Ancona, Italy
ABSTRACT
Small pelagic fish aggregate, forming distributions of abundance on a wide variety of space and
time scale. This phenomenon is of great ecological and biological importance and has relevant
effects on fishery. The major difficulty for understanding fish variability is the lack of sufficient
data on biomass variability over both temporal and spatial scales expecially over long periods. In
the Adriatic Sea distributions of abundance of small pelagic fish were acoustically estimated for
more than two decades on a time scale of one year and on spatial scale from aggregations (tenths of
metres) to the whole North Adriatic Sea (hundreds of kilometres).
The aim of this paper is to provide a conceptual framework and mathematical tools for study this variety,
using acoustic data.
Keywords: Temporal variability, Spatial diversity, Small pelagic fish, North Adriatic Sea,
Acoustics
Contact author: Massimo Azzali; Address: ISMAR-CNR, Largo Fiera della Pesca, 60125 Ancona
(Italy); Fax: +39 071 55313; E-mail: m.azzali@ismar.cnr.it
INTRODUCTION
It is evident that small pelagic fish aggregate on a wide variety of space and time scales. The purpose of this
paper is to provide a conceptual framework and mathematical tools for study this variety. The framework
which will be used is the spatial-temporal scale of biomass distribution, composition and structure. Although
the geographical distribution of small pelagic fish biomass appears to occur on a continuum of space scales,
we have attempted to break the continuum into categories of patterns, at increasing spatial resolution. Space
scales of patterns used for studying the Adriatic Sea are categorised in macro, meso, coarse, and fine scales
(Table 1). The whole Adriatic Sea is defined as a macro-scale. It is characterised by highs and lows of
species abundance, throughout areas where differences in species compositional structure is low. The
division of the Adriatic Sea into northern and southern sections, called meso-scales, is due to a variety of
causes of both biological and physical origins. From the biological point of view, North Adriatic differs from
South Adriatic for the presence of sprat population, and for a mean abundance of the other small pelagic fish
35% higher than South Adriatic. This may be due, in part, to the fresh and rich of nutrient water plume,
resulting from the outflow of Po, the major river of Adriatic and in part to the particular bottom topography
and geology of North Adriatic. North Adriatic is the object of this paper. It was sampled acoustically for
more than two decades (1976-2001). Measures for assessing diversity of patterns in North Adriatic are based
on the segmentation of the total pelagic biomass in three overlapping hierarchy of space scales. At mesoscale, the spatial distribution of the pelagic biomass is examined as a whole and then resolved per species or
group of species, without taking into account any spatial pattern of the single species. At coarse scale, the
map of the pelagic biomass is divided into two predominant categories of spatial patterns. Areas that have a
biomass density at least 2 times higher than the average density in the entire North Adriatic are placed in one
category. They are called “hot spots”. The complement of these areas, that form the rest of the region, are
placed in the other category. At fine scale, the pelagic biomass is resolved to the level of forms of
aggregation: in accumulation, in school and in disperse forms. All these patterns are variable in space, as
well in time. The temporal variability is assessed for each pattern (species, spatial patterns, forms of
aggregations) in the total period of observation (1976-2001). The diversity in space and variability in time of
the small pelagic fish patterns will be analysed by entropy (MacArthur, 1955) and moment theory (Glasbey
and Horgan, 1995).
Table 1. Categories of scales of patterns in the Adriatic sea
NAME
(observation period)
The Adriatic Sea
(1987-2001)
South Adriatic
(1987-2001)
SPACE SCALE
Area
DOMINANT PATTERNS
Macro-scale
≈37900(nm2) Pelagic biomass
Sampled Area ≈13800(nm2) Pelagic species/group of species
Area
Meso-scale
≈16000(nm2) Pelagic biomass
Sampled Area ≈6100 (nm2) Pelagic species/group of species
Spatial Diversity and
temporal Variability of
pelagic biomass:
1) as a whole
2) per species
Spatial Diversity and
temporal Variability of
≈320.7 (t/nm2)
1) hot spots
≈45.3 (t/nm2) 2) complementary area
Spatial Diversity and
≈ 0.005 (kg/m2) temporal Variability of :
1) Layers
≈ 48.6(kg/m2) 2) Schools
<0.005 (kg/m2) 3) Disperse forms
Meso-scale
Area
≈21900(nm2) Pelagic biomass as a whole and per
species (anchovies; sardines; sprats;
Sampled Area ≈7600 (nm2) other pelagic species).
North Adriatic
(1976-2001)
What we look for
"hot spots"
Coarse-scale
≈700 (nm2) "hot spots"
2
Complem. area ≈6900 (nm ) Complem. area
Fine-scale
Layers
≈1398 (nm2 ) layers
Schools
≈1.3 (nm2)
Disperse forms variable
Schools
Disperse forms
MATERIALS AND METHODS
Data on the pelagic biomass of small pelagic fish in North Adriatic were collected from 1976 to 2001 using
the standard echo integration method (MacLennan and Simmonds, 1992). In this period 22 echo surveys
were carried out. The interval between two consecutive acoustic surveys was generally one year, the season
of the surveys autumn, with few gaps or shifts inevitable over a so long time period. Measures assessing
different components of North Adriatic diversity were obtained using a Sw package called GFRDBS (Azzali,
2002). This package processes the data in a geographical context, converting Lat&Lon into X&Y
coordinates. The North Adriatic sampled acoustically is contained in a grid of 100x180 nm. The smallest unit
of information or pixel in X, Y map is one square nautical mile (nm2). The set of the pixels provides the
spatial distribution or map of the pelagic biomass. Diversity measures of biomass distribution in North
Adriatic are based on the allocation of the pixels in the three different sets of patterns. They are:
1.
set of pelagic species patterns. The total pelagic biomass B(t) 
Bi (t) , found in the entire sampled

area during the period of observation t, is resolved in four group of species, sardines (i=1), anchovies (i=2),
sprats (i=3), other pelagic species (i=4). The segmentation of the biomass per species describes the mesoscale structure of the pelagic biomass. It appears to have a persistence of few years with cycles of many
years.
2.
set of biomass density patterns. The pixels (X,Y) of the map of the pelagic biomass found in period of
observation t are allocated in two categories according to the range of biomass density in which a pixel lies.
Pixels with density values at least 2 times higher than the average density in the entire investigated area are
placed in the high density category (“hot spots”) and the rest of pixels in the low density category. Thus the
total pelagic biomass B(t) 
Bi (t) was divided in two corresponding categories: the category i=1

containing the biomass found in the hot spots and the category i=2 containing the biomass found in the
remaining areas. It may be assumed that hot spots are for fish the “best” places to live. Here small pelagic
fish find abundance of food and develop fundamental ecological interactions. The geographical position, the
dimensions (mean total extension ≈ 695.8 nm2 , mean density ≈ 320 t/nm2 in North Adriatic) and number
(mean = 7, in North Adriatic) of the hot spots united with their complementary area (mean extension ≈
6883.3 nm2 , mean density ≈ 45 t/nm2) form the coarse scale of the pelagic biomass. The coarse-scale
structure appears to have lifetime of several months with approximately seasonal cycles.
3.
set of aggregation form patterns. The total pelagic biomass B(t) 
Bi (t) observed in the survey t is

divided in three types aggregations: layers (i=1), schools (i=2) and other forms (i=3). The layers in North
Adriatic may be dozens of miles long (in total the mean extension of layers is ≈ 1398 nm2 , mean number of
layer 13.5) and are formed by mixed species and size of small pelagic fish at low density (≈ 5.05 g/ m2).
They are characterized by strong interactions between fish and plankton. The layer structure can persist for
weeks or even months. The schooled distributions of fish in North Adriatic have in total a mean extension of
1.3 nm2. It is on this scale that individual interactions between fish of the same species and similar size
occur. The densities within schools are particularly high (mean density ≈ 48.6 kg/ m2, mean number of
school ≈ 2617.3). The schooled distribution has cyclic day-night changing; however the cyclic structure can
persist stably in the same area for several weeks or months with seasonal cycles. The other forms of
aggregations have irregular and unstable shape and density very low (< 5.05 g/m2).
For diversity we intend how much biomass was found distributed in each pattern of a set during a survey.
We use the quantity (MacArtur, 1955; Okubo, 1980; Pahl-Wostl, 1995):
(1) D m t   a m
p

i 1
Bi t 
p
log
Bi t 
p
 B t   B t 
i 1
i
i 1
p
;  Bi t   Bt 
am ≥ D m ≥ 0
i 1
i
as a measure of diversity of the pelagic biomass distribution. Where:

Dm(t) is the diversity index for the pattern set m (m=1 species patterns; m=2 biomass density patterns;
m=3 aggregation form patterns) at the period of survey t;

Bi(t) is the biomass of all fish present in the pattern i (i=1..p) during the period of survey t;

p is the number of partitioning of the pelagic biomass: (p=4 pelagic biomass resolved per species;
p=2 pelagic biomass resolved per levels of density and p=3 pelagic biomass resolved per aggregation forms);

am is a positive constant of normalization (am = 100/log(p)). It renders the diversity measure Dm
ranging from 0 to 100, independently of the number of the segmentations chosen (p). The diversity is defined
high if 100 > Dm > 80, average if 80 ≥ Dm > 50 and low if 50 ≥ Dm >0.
The quantity Dm has the following properties that substantiate it as a reasonable measure of diversity. If all
animals belong to one pattern (i =1, say) of the set m, then Dm = -log1 = 0, corresponding to the state of
minimum diversity. If all the patterns of the set m contain the same quantity of biomass, then Dm has a
maximum value (Dm = am log(p) = 100). This is the most diverse status.
Although Dm measures the patchiness diversity taking into account the biomass distribution in the sampled
area, it does not specify the spatial dispersion of patchiness. We use the centre of gravity, the moments of
inertia and the dispersion ellipse as a measure of how dispersed from its centroid the pelagic biomass (as a
whole or per hot spots) is (Glasbey and Horgan, 1995).
We define variability the degree to which the biomass of a pattern varies over the entire period of
observation (1976-2001). The observations are done at the time t = t1, t2,..,t22 at interval around one year.
Persistence, the complementary concept of variability, is how long the biomass within a pattern lasts before
it is changed to a new value. Patterns that exhibit little variability, or high persistence may be said stable.
Variability (or persistence) is assessed for nine kinds of pattern. They are:

five patterns at meso-scale level: the pelagic biomass as a whole (pattern n=1) and per species
(patterns: n=2, anchovies; n=3, sardines; n=4, sprats; n=5, other pelagic species);

one pattern at coarse-scale level: the hot spots (pattern n=6);

two patterns at fine-scale level: layers (pattern n=7) and schools (pattern n=8).
In calculating the temporal variability of the above patterns from 1976 to 2001 one has to take into account
the absolute temporal extension (τ) of each pattern relative to the time necessary to complete a survey (< one
month) and in relation to the interval between two consecutive surveys (about one year). We assume that τ
>> one month, for all the patterns. The patterns at meso-scale level (biomass, pelagic species) have cycles
generally longer than the interval between surveys. The patterns at coarse and fine-scale have seasonal
lifetime and cycles, therefore their variability may be assessed by surveys that are carried out in the same
season at interval of one year.
We use the complementary quantities:

 

 B t (n )   B t (n ) 
(2) Pn  a T  
log 
 ; (3) Vn  a T logT  Pn  t=1,2,..,T
t   B t (n ) 
  B t (n ) 
 t
  t

as a measure of persistence (2) or variability (3) of a pattern relative to the total period of observation (19762001). Where:

t is the progressive number of the surveys carried out from 1976 to 2001 (t=1, 2, ,T);

Bt(n) is the pelagic biomass found in the pattern n (n=1..9) during the survey t. If the pattern n
doesn’t occupy the entire sampled area, the biomass has to be given a weight in proportion to the spatial
extension of the pattern under consideration relative to the total sampled area.

aT is a positive constant of normalization (aT = 100/log(T)). It renders the persistence (variability)
measure Pn (Vn) ranging from 0 to 100 (100 to 0), independently of the number of the surveys (T) carried out
in the total period of observation.
The proprieties that justify the use of Pn (Vn) as reasonable measure of persistence (variability) in pattern are:
(1) if the pattern n contains exactly the same level of biomass in all the surveys (t = 1, 2,..,T), then Pn = 100
(Vn, = 0), corresponding to the state of maximum persistence (minimum variability); (2) if the biomass
within the pattern n is found only during one survey (t=1, say), then Pn = 0 (Vn, = 100) corresponding to the
state of minimum persistence (maximum variability).
The formulas (2) and (3) are applied not only to the acoustic data, but also to anchovies and sardines catches
derived from ISTAT bulletins to compare the variability of the biomass at sea with that of catches.
RESULTS AND DISCUSSION
The measures of diversity and variability derived from information and moment theory were applied to a
conceptual framework that partitions the pelagic biomass into categories of patterns, assessed acoustically in
North Adriatic from 1976 to 2001. In this period important changes occurred in the composition and
abundance of pelagic biomass (Azzali et al., 2002). The population of anchovies, the most valued of the
pelagic species in the Adriatic Sea, collapsed in the period 1984-1990. Its recovery began around 1996 and
continued until 2001. In the general opinion this was the most important event occurred in the Adriatic Sea
during the last three decades. In the 1998 began the progressive decline of the sardine population and in the
1996 the fall of sprats that in 1998 -2000 arrived close to extinction. However this biologically dramatic
phenomenon passed almost unnoticed, because sardines are low quoted in the market and sprats have no
quotation at all. The total pelagic biomass fluctuated almost regularly in the period 1976-2001 with cycles
ranging from 3 to 5 years.
Contrasting with the general opinion, the period 1996-2001 appears to have more ecological significance
than the anchovy collapse period. Year-to-year measures of species diversity indicate that during the
anchovy collapse the pelagic species heterogeneity in North Adriatic was rather well preserved, while in the
recent decrease of sardines and sprats stocks the species diversity fell to the minimum value respect to the
entire period of observation (1976-2001). Species diversity index (D1) was estimated from average to low in
the period 1986-1990 (D1 ranging between 72 and 52), but from low to very low in the period 1996-2001 (D1
ranging between 47 and 37). In the other years under examination the species diversity index in North
Adriatic ranged between high values (> 80) and average values (> 70).
The biomass contained in hot spots relative to that contained in the complementary area seems rather
irrespective of the substantial changes in abundance of the pelagic species. The diversity index D2 remained
high (> 80) in the two critical periods (1984-1990 and 1996-2001) and ranged between 76.5 (year 1977) and
99.9 (year 1998) during the entire period of observation. The hot spots contain the main portion of the
“catchable” biomass, therefore the catchability of pelagic species may remain high even when the abundance
of some species decreases.
The minima of the index of aggregation form diversity (D3) were found one year before the beginning of
anchovy collapse (D3 = 28.9 in the year 1983) and just at the beginning of sardines decline (D3 = 42.2 in the
year 1998). However from an examination of the two diversity indices it appears that 93% of pelagic
biomass was found in disperse forms in the 1983 survey, while in the 1998 survey 85% of pelagic biomass
was aggregated in schools. These data give the impression that the environmental background that caused the
collapse of anchovy differs from that involved in the decline of sardines and sprats. The first event was
probably caused by a general unfavourable habitat and because of it all pelagic fish remained in separate
disperse forms. In the 1998 the habitat appeared particularly favourable only to anchovies, that formed dense
and numerous schools.
Measures of temporal variability relative to the period 1976-2001 indicate that generally North Adriatic is a
stable system. In a scale from 0 (minimum variability) to 100 (maximum variability), the pelagic biomass as
a whole has a variability 3, sardines 8.5, anchovies 9 and sprats 18.3. Measures of the variability of anchovy
and sardine catches in the same area and period resulted about 2 times lower than that of their respective
biomass. The variability of the biomass distributed in hot spots was estimated around 10, and the variability
of the biomass contained in both the layers and schools was estimated around 18.
No evident relationship between diversity and stability was found within the spatial and temporal scales
chosen. In fact while the diversity of the distribution of biomass over the pelagic species was subjected to
highs (D > 80) and lows (D < 40), the stability of the single species calculated for the entire period remained
in average high (P >80 or V<20).
Finally a traditional statistical study was applied to the parameters of the ellipse of dispersion of
pelagic biomass to identify which of them present the highest variations; the results are reported in
Table 2.
Table 2. Values of CV (%) for the parameters of the ellipse of dispersion
North Adriatic: 1976-2001
Parameters of the ellipse of dispersion for total pelagic biomass
Centroid X
Centroid Y
Ellipse major axis (nm)
Ellipse minor axis (nm)
Inclination angle (°)
Area of ellipse of dispersion (nm 2)
Mean value
36.94
72.8
44.78
15.7
101.12
2233.49
Standard deviation
4.76
17.32
7.14
2.08
5.36
525.34
CV (%)
12.89
23.79
15.96
13.27
5.3
23.5
Parameters of the ellipse of dispersion for high density biomass
Centroid X
Centroid Y
Ellipse major axis (nm)
Ellipse minor axis (nm)
Inclination angle (°)
Area of ellipse of dispersion (nm 2)
Mean value
37.73
60.39
35.72
12.69
101.42
1465.96
Standard deviation
7.34
25.65
9.71
2.87
18.3
627.85
CV (%)
19.44
42.47
27.18
22.62
18.05
42.8
The parameters that seems to have a greater variability are the ordinate of the ellipse’s centre of
gravity and the area of the ellipse; other parameters show similar Coefficient of Variation (CV)
values; these results are similar for total pelagic biomass ellipse and high density biomass ellipse,
even if variability for the last one is higher than the first one.
CONCLUSIONS
We have stressed the importance to process acoustic data in function of patterns and their spatial and time
scales. For this we have used a conceptual framework based on an overlapping hierarchy of patterns ranging
from thousands of square nautical miles to hundreds of square meters. Diversity in the distribution of
biomass over sets of patterns and biomass variability of each single pattern have been measured using
functions derived from information theory. The results seem to indicate that:

The ecological significances of the two dramatic events that occurred in the Adriatic Sea (collapse of
anchovies 1984-’90; fall of sprats and decline of sardines 1996/1998-2001) are contrasting: the species
diversity index remained rather high during the collapse of anchovy stock but was minimized by the fall of
sprats and sardines. Also the physical and biological origins of the two events appear to be different.

Variability measures over all the patterns are generally low (i.e North Adriatic appears as a stable
ecosystem), but variability indices increase at increasing of the resolution of the ecosystem structure (from
pelagic biomass to pelagic species and forms of aggregation).

No evident relationship between diversity and variability indices was found. However both indices
depend critically on the spatial and temporal scales of observation chosen.
Many aspects of these results should be completed and validated by information on the ecology of the
individual species and on the dynamic of their pattern in function of physical parameters. However it seems
evident that acoustic studies centred on patterns can provide useful information on the knowledge of the
structure of an ecosystem.
ACKNOWLEDGEMENTS
This research was supported by MIPAF and EU (only for the period 1993-1996). We would like to thank the
crew of the R/V “S. Lo Bianco”, “Thetys”, “G. Dallaporta” that worked on this research in the period
considered in this article.
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